Design and applications of cell-selective surfaces and interfaces

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Design and applications of cell-selective surfaces and interfaces Haolan Zhang, Xiaowen Zheng, Wajiha Ahmed, Yuejun Yao, Jun Bai, Yicheng Chen, and Changyou Gao Biomacromolecules, Just Accepted Manuscript • DOI: 10.1021/acs.biomac.8b00264 • Publication Date (Web): 17 Apr 2018 Downloaded from http://pubs.acs.org on April 18, 2018

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Biomacromolecules

Design and applications of cell-selective surfaces and interfaces Haolan Zhang1, Xiaowen Zheng1, Wajiha Ahmed1, Yuejun Yao1, Jun Bai1, Yicheng Chen2, Changyou Gao1 *

1. MOE Key Laboratory of Macromolecular Synthesis and Functionalization, Department of Polymer Science and Engineering, Zhejiang University, Hangzhou 310027, China

2. Department of Urology, Sir Run-Run Shaw Hospital, College of Medicine, Zhejiang University, Hangzhou 310016, China

* email: [email protected]

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Biomacromolecules 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

ABSTRACT. Tissue regeneration involves versatile kinds of cells. The accumulation and disorganized behaviors of undesired cells impair natural healing process, leading to uncontrolled immune response, restenosis, and/or fibrosis. The cell-selective surfaces and interfaces can have specific and positive effects to the desired types of cells, allowing tissue regeneration with restored structures and functions. This review outlines the importance of surfaces and interfaces of biomaterials with cell-selective properties. The chemical and biological cues including peptides, antibodies and other molecules, physical cues such as topography and elasticity, and physiological cues referring to mainly interactions between cells-cells and cell-chemokines or cytokines are effective modulators to achieve cell-selectivity upon they are applied into the design of biomaterials. The cell-selective biomaterials have also shown their practical significance in tissue regeneration, in particular for endothelialization, nerve regeneration, capture of stem cells, and regeneration of tissues of multiple structures and functions.

Keywords: biomaterials; surfaces; interfaces; cell-selectivity; tissue regeneration

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1. Introduction

Regeneration of tissues is critical to recover the structures and functions of trauma and wound. It is a comprehensive process involving many types of cells at different stages of time, including immune cells such as neutrophils, monocytes, macrophages, dendritic cells and T cells, epithelial cells, endothelial cells, and fibroblasts, etc.1 The regeneration rate and outcomes are determined by the interplay of different types of cells and their synchronized behaviors. The process and performance of healing may be hampered in some circumstance, and are turned into uncontrolled and malignancy such as fibrosis and hyperplasia. Fibrosis, known as the phenomena of overgrowth, hardening, and scarring of various tissues, is destined as the eventual consequence under natural healing conditions of adults’ injuries, leading to disruption of normal tissue architectures and severely impaired organ functions.2 The main reason of fibrosis accounts to the disorganized and excess accumulation of extracellular matrices (mainly collagen) secreted by a patch of cells such as myofibroblasts which are differentiated from fibroblasts. So far two strategies have been adopted to avoid fibrosis and to achieve induced regeneration.1 In the molecular level, chemokines or cytokines are utilized to block undesired signals or over production of extracellular matrices. In the cellular level, adhesion and proliferation of fibroblasts or myofibroblasts are modulated, and those normal tissue-repair cells are captured to accelerate the healing process of trauma. The basic interactions between the implanted biomaterials and organisms such as protein adsorption, cell behaviors and tissue responses are mainly governed by the surfaces and interfaces of biomaterials, and thereby determine the biological performance of tissue 3



regenerative biomaterials. The biomaterials having bioactive surfaces and interfaces can effectively promote adhesion, proliferation and differentiation of cells, and can promote integration between implants and hosts. However, in most cases, initiated immune response is unavoidable, resulting in accumulation of immune cells and fibroblasts, and inflammation and fibrosis. In the case of spinal cord injury, for example, microdevices are often implanted to assist the regeneration of central nerve system.3 However, the implants may cause chronic foreign reaction, leading to recruitment of immune cells and reactive cells including microglia and astrocytes that cover the surface rapidly and form scar or hypertrophy.4 Such consequences cause limited long term functionality or even failure of implantation. By contrast, the implants having cell-selective property can recruit the desired types of cells, which are superior in the regeneration of hierarchical tissues such as full-thickness of blood vessels and osteochondral defects. Engineering cellular environment with biomaterials to accelerate the healing processes has been a long-standing challenge in regenerative medicine. Since cellular activities lie in the extracellular matrix and are extensively influenced by microenvironment, the nature of cell-material interactions is mainly defined by the properties of material surfaces and cell-material interfaces. Therefore, surface modification is a straightforward and convenient way to endow the implanted biomaterials with desired functions without significant change of the bulk properties. This review outlines the importance of surfaces and interfaces of biomaterials with cell-selective properties, which are deemed as key issues in regeneration of specific tissues, and highlights the current designs and methods of fabricating this type of functional surfaces. 4


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Biomacromolecules

2. Design and fabrication of cell-selective surfaces and interfaces

The ordinary biomaterials show no specific interactions with biological systems such as adsorption of proteins and attachment of cells, namely they interact with cells regardless of the cell types. For example, the so called “bioactive materials” can promote the adhesion and proliferation of many types of cells. Although in many cases they are testified by using the target cells and may show very positive effects, they can simultaneously benefit the adhesion and proliferation of other types of cells, even for those undesired ones.5-7 The cell-selective surfaces and interfaces, on the other hand, can offer specific microenvironments with respect to the promotion of target cells over other types of cells in a great extent. The promoted activities of desired cells include attachment, proliferation, migration and differentiation, etc., among which the attachment is the earliest and most important cell event when interacting with biomaterials, and thereby is extensively considered.8, 9 Meanwhile, the undesired types of cells are better repelled. For this purpose, specific interactions such as bioactive molecules, and physical and physiological cues should be incorporated into the biomaterials systems. The bioactive molecules can function as the chemical and biological ligands binding to the target cells in a high specificity, and activate some cellular activities such as directional migration or differentiation.10-13 To avoid the non-specific interactions of proteins and cells and thereby to improve the specificity, the surfaces are usually endowed with the so-called antifouling property by introducing very hydrophilic polymers. The physical cues for enhancing cell-selectivity on surfaces include roughness, topology and stiffness, etc.9, 14, 15 The cells-secreted chemokines and cytokines are the typical physiological cues that strongly promote 5



the migration of particular types of cells to the desired sites, and may further stimulate their differentiation.16-19 Although different types of cues show the positive selection of cells, the cell types and hence the types of tissues to be regenerated are diverse, leading to the universal design of cell-selective surface impossible. Surface modification of existing biomaterials and medical devices needs the “activation” of inert biomaterials surface, allowing specific interactions with proteins and cells, or in most other cases the further immobilization of functional molecules or transformation of physical properties. The methods of surface activation include plasma treatment, electrochemical etching, aminolysis, and alkaline hydrolysis, etc.20-22 Subsequent modifications by surface-initiated atomic transfer radical polymerization (SI-ATRP), click chemistry, and layer-by-layer (LbL) self-assembly etc. can thus be implemented.8,

23, 24

The surface topologies can be created by photolithography,

microcontact printing and electrospinning etc.25-28

2.1 Chemical and biological cues

The cell-selective surfaces implemented by chemical and biological cues include specific binding to target cells and repelling of undesired cells. The ligand molecules can selectively promote the adhesion of target cells, while the hydrophilic or zwitterionic polymers are robust to resist non-specific adhesion of cells. Polymers in the form of brushes or multilayers cannot only play a role in determining the properties of surfaces, but also function as reactive linkers for conjugations of bioactive molecules.29 The ligand molecules include peptides, antibodies and other chemokines that can be recognized by particular types of cells. 6


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Peptides Peptides are chemicals composed of several α-amino acids through amide bonds and possess many important functions in biological process. Cell-selective peptides have selective affinities to certain types of cells, while have no obvious effects to others. Traditionally, the cell-selective peptides are segments of cell-binding domains in cell adhesion proteins or extracellular matrix (ECM). Compared to proteins, peptides have advantages of better stabilities and easier processing.30, 31 Therefore, the cell-selective peptides have been widely utilized for fabrication of cell-selective surfaces. The immobilization of cell-adhesive peptides on biomaterial surface involves the formation of amide bond as a result of reaction between amino group of peptide and surface carboxylic group. 6, 32

To avoid the side reactions in the peptide itself, carboxyl-active esters have been developed

to bind the unprotected peptides, resulting in easier covalent immobilization.33 The strategies to covalently immobilize peptides on biomaterials surface may include activation of carboxyl groups with N-hydroxysuccinimide (NHS), functionalization of peptides with thiol groups to allow Michael addition, azido alkyne click reaction, and photo-induced activation etc.33, 34 Another important concern related to immobilization of peptides is availability of the functional groups on the surface of biomaterials because the synthetic and biodegradable biomaterials have very a few functional groups on their surface. Conjugation of peptides to polymers is a convenient way to obtain the peptides-conjugated polymers, which are easily coated onto many types of biomedical polymers to allow the surface enrichment of cell-selective

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peptides.

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Copolymerization, chemical treatment, plasma treatment, SI-ATRP, γ-irradiation

grafting polymerization can also be used to immobilize peptides.35-39 It is known that Arg-Gly-Asp (RGD) tripeptides can strongly stimulate and promote cell adhesion and growth when they are immobilized onto synthetic biomaterial surfaces.6, 7 However, in the case of blood contacting biomaterials, RGD-modified vascular grafts also lead to platelet deposition and adhesion of other cells, because they have the ability to recognize platelet adhesion receptors αIIbβ3.40, 41 In contrast to RGD, another peptide called cRRE exhibits a lower affinity for αIIbβ3, but a high affinity for the adhesion receptors α5β1 of endothelial cells (ECs) via the interaction between the Trp residue in cRRE and Trp subunit on α5.42 Kato et al. successfully screened 12 selective tripeptides for ECs and smooth muscle cells (SMCs) by a peptide array-based interaction assay of solid bound peptides and anchorage-dependent cells.43, 44 Cys-Ala-Gly (CAG) tripeptide turns out to be the best tripeptide for selection of ECs, and its affinity for SMCs is much lower than RGD. The electrospun polycaprolactone (PCL) fibers blended with CAG peptides significantly enhance the ECs adhesion in vitro44. The rate of ECs adhesion is two-folds of that of SMCs. ECs have a wide spreading morphology covering a large surface area, whereas SMCs appear to be shrunken with a round morphology. Khan et al. used photo-induced thiol-ene click chemistry to functionalize the polycarbonate urethane (PCU) surface by covalently linking CAG peptides. The PCU surface is grafted

with

hydrophilic

poly(ethylene

glycol)

methylmethacrylate

(PEGMA)

and

pentafluorophenyl methacrylate copolymers via SI-ATRP, which is further immobilized with

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cysteine terminated CAG peptides. The modified surface shows selective and rapid growth of ECs with reduced platelet adhesion and activation.8 Arg-Glu-Asp-Val (REDV) is a fibronectin-derived tetrapeptide that has the ability to bind specifically to α4β1 integrin found abundantly on ECs while scarce on SMCs.41 Therefore, REDV can selectively promote the adhesion and proliferation of ECs instead of SMCs, and has been extensively used to enhance the endothelialization on biomaterials.45, 46 For instance, REDV is incorporated

into

hydrophilic

copolymer

brushes

composed

of

N-(2-hydroxypropyl)methacrylamide (HPMA) and eugenyl methacrylate (EgMA) by a thiol-ene click reaction. The modified surface not only promotes competitiveness of ECs adhesion, but also resists platelet adhesion and has antibacterial properties (Figure 1).23 Besides immobilization on surfaces, REDV can also be conjugated to nanoparticles for specific targeting of ECs.47

Figure 1. Schematic of surface grafting of HPMA and EgMA copolymers by ATRP at different monomer ratios; the terminated allyl groups are functionalized with cysteine-terminated CREDV peptides by photo-initiated thiol–ene click chemistry. Reproduced from ref 23 with permission of the Royal Society of Chemistry. http://dx.doi.org/10.1039/c5tb01155h

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Lin et al. immobilized REDV peptides on heparin (HEP) and chitosan (CHI) multilayers, on which REDV-coupled CHI (CHI-REDV) molecules were deposited as the terminating layer. Because the native HEP/CHI presents cell-resistant property, the HEP/CHI with REDV peptide selectively promotes the adhesion of ECs with the minimal attachment of SMCs.24 Besides the abovementioned peptides for cells in blood vessel regenerations, there are various peptides for cells involved in regeneration of other types of tissues such as cells in nerve regeneration, and capture of stem cells, etc.48-50 Cell-selective peptides cannot only be identified by deriving from functional proteins, but also screened out by biotechnologies. For example, high throughput micro array assays and phage display technology are powerful strategies to screen out affinitive peptides with desired binding properties towards multiple types of cells.

51-54

Concerning the diverse types of cells involved in different tissues, further works should be carried out to develop more cell-selective peptides. Moreover, the appropriate immobilization on surfaces is same important as the correct use of cell-selective peptides, so that the density, stability and accessibility can be effectively manipulated. Antibodies Antigens expressed on different types of cells are able to bind specially with related antibodies, which are applicable for cell selectivity. CD34 is reported to be expressed in bone marrow-derived circulating endothelial progenitor cells (EPCs) in humans.55, 56 Melchiorri et al. compared the enhanced endothelialization by loading of vascular endothelial growth factor (VEGF) and immobilizing anti-CD34 antibodies on vascular grafts, respectively. Results show that the anti-CD34 antibody has minimal non-specific adsorption and lower elution rates, 10


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highlighting the advantages of antibodies in early formation of endothelium by maintaining the inner lumen diameter, thus reducing the restenosis.57 In another work, the use of anti-CD34 modified polymer films results in increased number of viable cells after 7 days, and plays a role in cell selection and proliferation. 58, 59 Hydrophobins are produced by filamentous fungi. They are amphiphilic molecules with a molecular weight of 7-15 kDa. The amino acid sequences possess specific hydrophobic and hydrophilic regions. The self-assembly of hydrophobins can convert the surface from hydrophilic to hydrophobic and vice versa. The adhesive properties of hydrophobins can be used to immobilize other proteins without loss of activity. One of the Class II hydrophobins, HFBI, has been proved to be biocompatible, and has been used for surface functionalization of implants with the aim to capture cells for tissue engineering. Platelet endothelial cell adhesion molecule-1 (PECAM1/CD31) is expressed by ECs as a cell marker. Zhang et al. immobilized anti-CD31 antibody on vascular grafts via HFBI bridging.60 Specific binding of human umbilical vein endothelial cells (HUVECs) and ECs adhesion is dramatically enhanced. Another antibody CD133 is also expressed on EPCs surface, and hence anti-CD133 antibody is immobilized on ePTFE vascular graft for in vivo application.55, 56, 61 Antibodies-modified substrates are very powerful for selective capture of stem cells as well. For example, a stent coated with anti-human CD34 antibody molecules is used for capturing EPCs from the blood stream.59 In another work, chitosan membranes are modified with anti-human CD3, anti-human CD29 and anti-human CD105 to selectively capture adipose stem

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cells (ASCs) from adipose tissue. The purity of ASCs is significantly increased when incubating with mixed osteoblast like cells (SaOs-2) and cells separated from liposuction samples for 72 h.62 Other molecules Besides the peptides and antibodies, some other molecules can also interact specifically with cells, and thus are incorporated on surfaces for cell-selectivity.63,

64

Heparin is a typical

anticoagulant, and has binding sites for cell growth factors.65, 66 When immobilized on stainless steel modified with a plasma-polymerized allylamine film via electrostatic force, heparin enhances ECs adhesion and proliferation rather than SMCs.63 Nylon-3 polymers exhibit fascinating biological properties, and show great promise in tissue regeneraiton.67-69 Liu et al. used nylon-3 polymers to study the adhesion and growth of ECs without the use of specific peptide motifs. They selected several Nylon-3 copolymers, in which β-Lactams and DM homopolymers (poly-DM) exhibit poor fibroblasts growth. Fibroblasts and SMCs do not show much growth on the poly-DM polymers-modified surfaces, while ECs exhibit healthy morphology on all the poly-DM modified surfaces. 64 Glycopolymers with hydrocarbon pendent residues have been widely used for specific recognition of hepatic cells due to the recognition between galactose or N-acetylgalactosamine residues of disialylated glycoproteins and hepatic asialoglycoprotein receptor (ASGPR), a transmembrane glycoprotein specifically expressed on hepatocytes.70-72 Polymers consisting of 2-methacryloyloxyethyl

phosphorylcholine

(MPC)

block

and

2-lactobionamidoethyl

methacrylate (LAMA) block were synthesized and immobilized on surfaces. Hepatocytes but not fibroblasts adhere on

the surface due to both antifouling effect of zwitterionic 12


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poly(2-methacryloyloxyethyl phosphorylcholine) (PMPC) and specific recognition between HepG2 cells and LAMA.71 Similarly, selective adhesion of hepatocytes are achieved on a surface of 2-lactobionamidoethyl methacrylate and N-isopropylacrylamide copolymer brushes.73 Combination of bioactive molecules and anti-fouling surfaces Taking endothelialization as an example, it is of great importance to minimize the protein adsorption and to inhibit the platelet adhesion and activation as well as adhesion of smooth muscle cells. One strategy is the functionalization of inner surface of artificial vascular grafts. For this purpose, various strategies have been employed to create hydrophilic surfaces, especially the immobilization of hydrophilic polyethers or zwitterionic moieties. These polymers cannot only resist non-specific adsorption, but also provide reaction sites for bioactive molecules and binding sites for growth factors. The hydrophilicity of artificial vascular grafts can be enhanced by surface-grafting

of

PEG

and

zwitterionic

polymers

such

as

PMPC

poly(3-dimethyl(methacryloyloxyethyl)ammonium propane sulfonate) (poly(DMAPS)) etc.

and 74-79

The adhesion behaviors of cells can be further mediated by responsive polymer brushes.80 The complete covering of the inner surface of blood vessels with a biofunctional and confluent layer of ECs would enhance the long-term applicability of the implants as it would mimic the natural blood vessel tunica intima. Otherwise, the lack of endothelialization would result in a low patency rate. Wei et al. prepared several binary copolymers by using butyl methacrylate (BMA), p-nitrophenyloxycarbonyl poly(ethylene glycol)methacrylate (MEONP)PEGMA via radical polymerization. They coated the PET films with reactive copolymers and then with REDV 13



peptides (Figure 2), aiming at integration of the non-specific resistance and specific adhesion of PEG and REDV peptides, respectively.78 Slight selectivity for ECs over SMCs is achieved by using the binary copolymers. However, the surface modified by the terpolymers shows significant resistance to SMCs adhesion, while can well promote attachment, proliferation and growth of ECs. Similarly, a surface combined of REDV with anti-fouling zwitterionic polymers such as polycarboxybetaine and phosphorylcholine also shows excellent cell selectivity, because the zwitterionic polymers usually exert better resistance to non-specific adhesion of proteins and cells.77

Figure 2. Schematic illustration of different surfaces coated with REDV peptides. Reprinted from ref 78, Copyright (2011), with permission from Elsevier.

In the strategies of cooperating bioactive molecules and anti-fouling polymers, conformational relations are crucial to achieve the good selectivity, because the promotion of adhesion will be hindered if the bioactive molecules are buried in oversized anti-fouling polymers and vice versa. In addition, the molecular chain length and density of grafting should be controlled precisely to coordinate the promotion of adhesion and resistance.

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Biomacromolecules

2.2 Physical cues

As a matrix to offer mechanical support and grafting sites, the substrate itself has a variety of properties that influence cell behaviors. For example, the performance of cell adhesion is distinct on the substrate having same cell-adhesive peptides but different wettability.81 Other physical properties such as modulus, morphological features and thermal features can also dramatically influence cell adhesion, and may promote selective cell adhesion at some cases. For example, fibroblasts, generally considered as tough cells that show good adhesion on various conditions, form spherical aggregation on an RGD-immobilized surface with a low modulus.82 Investigation into the mechanisms of cell sensing on nano-scaled surfaces can provide guidance for fabrication of cell-selective surfaces as well.83, 84 Stiffness is an intrinsic physical property of biomaterials, and has a profound influence on cell adhesion, migration and differentiation.85, 86 Differing from chemical or other physical parameters that affect cell behaviors by direct contact, elasticity of biomaterials takes comprehensive effects ranging from the surface to dozens or even hundreds micrometers away from the surface.87 When cells adhere on a soft thin layer which is coated on a stiff substrate, they will sense the stiffness of both the coated layer and substrate.88, 89 On the protamine sulfate (PrS) and DNA multilayers deposited on a stiff substrate, the number of SMCs decreases much faster than that of ECs along with the increase of layer number. Consequently, the ratio of ECs to SMCs is improved.15 Topological structures including roughness, porosity, nanoscale symmetry and dimension of nanounits play an important role in cell-material interactions.90-92 For example, nanopatterns

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coated with Fn meditate cell attachment and spreading at both early and later stages, while only influence proliferation at a longer time scale.93 Isotropic pillar or groove-patterned surfaces have been widely used to investigate and reveal the mechanisms of different cell behaviors.9, 94, 95 Ding et al. found that 1 µm groove is the most favorable pattern for adhesion and proliferation of ECs, which inhibits the growth of SMCs simultaneously (Figure 3). In addition, the nanopatterns exert outstanding repelling effect of platelet adhesion and activation. 9 These results are important for selective control of cell behaviors by rationally designed surface topography, which is useful to fabricate cell-selective vascular and hemocompatible devices.

Figure 3. Patterned surfaces with 1 µm grooves promote adhesion of ECs instead of SMCs, while with 1 µm pillar topology they inhibit both. Reprinted with permission from ref 9. Copyright 2014 American Chemical Society.

To better understand how nanotopography influences cell behaviors, Csaderova et al. studied the behavior of ECs and fibroblasts on nanopillared PCL surfaces obtained by E-beam

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lithography and hot embossing. The PCL nano pillars inhibit the growth of fibroblasts, while favor the spreading of ECs and promote continuous endothelial lining.14

2.3 Physiological cues

Different from chemical and physical cues that straightforwardly regulate cell-selective properties of substrates, specific physiological microenvironments achieve the selectivity of cells by recruiting desired types of cells via the in situ secreted chemokines and cytokines. It is known that regeneration is a complicated process involving different types of cells, which influence each other by synergistic or antagonistic effect of secreted cytokines through amplification. Therefore, it is possible that the strategies of mediating cell-cell interactions are more effective than the direct regulation of cell-materials interactions.96,

97

In particular, inflammation has a close

relationship with the healing process. Recruited immune cells produce cytokines and chemokines, which are mitogenic and chemotactic for endothelial cells and epithelial cells, and thus can promote vascularization by inducing migration of these cells toward injured sites. However, in chronic inflammation, cytokines and chemokines produced by immune cells can induce epithelial-mesenchymal transition (EMT) and mesenchymal-myofibroblast transition, leading to permanent fibrotic scar.2 For example, when stimulated by different cytokines, monocytes recruited from circulation would be polarized into two main phenotypes, M1 and M2, which have distinct influence on recruiting types and behaviors of cells.16, 17 In fact, at the very initial stage of injury, accumulation of immune cells is inevitable, suggesting the great importance of materials in response to inflammation. 17



There are several cell-related methods to obtain a specific functional surface. One strategy is to significantly affect the directed migration and oriented differentiation of stem cells by cultivating immune cells as a cytokine source on the surface of the materials. For example, M1 macrophages are able to promote the long-distance rostral migration of neural stem/progenitor cells (NS/PCs) in a CXCR4-dependent manner. Moreover, NS/PC-derived neurons integrate into the local circuitry and exhibit an enhanced functionality during the co-transplanting with M2 macrophages. However, it also results in limited cell migration of NS/PC-derived cells.98 The mesenchymal stem cells (MSCs)-capture ability of macrophages was recently investigated after being cultured on two types of PCL films with different topography: electrospun PCL-fiber film and PCL-solid film fabricated by melting the PCL-fiber film. The PCL-fiber recruits more monocytes, and supports the macrophage phenotype transition from M1 to M2, as determined by the ratio of M2/M1 marker (CD163/CCR7)-positive cells and the expression of arginase-1/iNOS. The PCL films implanted in vivo were taken out for Transwell experiment ex vivo, showing that the MSCs substantially migrate toward the PCL-fiber film due to the higher level of stromal-derived factor-1α (SDF-1α) compared to PCL-solid film.99 These results indicate the importance of inherent interactions between immune cells and stem cells. In this regard, the design of biomaterials for tissue regeneration can be extensively widened by integration of surfaces with the ability of capture of specific immune cells, which then may optimize the following cell microenvironments and adaptive cellular interactions, leading to better tissue regeneration.

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Since cell communications are interactive, the paracrine products of MSCs exhibit multifunctions in immunomodulation, anti-scarring and angiogenesis. The various growth factors and chemokines secreted by MSCs cannot only promote vascularization but can also induce polarization of macrophages toward anti-inflammatory phenotypes.18, 19, 100 In order to explore how materials mediate the influence of MSCs on immune cells and angiogenesis-related cells, adipose-derived MSCs (Ad-MSCs) were incubated on the surface of polystyrene microplate (MP) and PCL electrospun fiber matrix with three different patterns, respectively. Significantly higher levels of anti-inflammatory and pro-angiogenic cytokines were detected on the electrospun fiber substrates compared to the microplates. The culture medium from the Ad-MSCs on the fiber matrix not only promotes macrophage recruitment and induced polarization towards anti-inflammatory phenotype, but also results in accelerated regeneration in an excisional wound healing model (Figure 4).25

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Figure 4. Schematic of design to investigate the influence of the fiber morphology and fiber orientation on the paracrine secretion and function of Ad-MSCs. The scaffolds for cell culture include electrospun fibers in random, aligned and a mesh organization, which are designated as REF, AEF and MEF. The cultures on EFs are compared to the Ad-MSCs cultured on polystyrene microplate (MP). Subsequently the culture medium is taken for paracrine production analysis, macrophage and HUVEC culture and wound healing, respectively. Reprinted from ref 25, Copyright (2017), with permission from Elsevier.

FTY720, a synthetic analog of sphingosine-1-phosphate (S1P), can function as agonist of S1P receptors, since S1P signal path is involved in determination of macrophage phenotype and enhances the recruitment of anti-inflammatory immune cells such as M2 macrophages.101, 102 When being implanted in mandibular defects, the ratio of M2 macrophages in PLGA/PCL electrospun nanofibers loaded with FTY720 is improved, leading to significant osseous tissue ingrowth.103 The successful recovery of skeletal muscle injury mainly depends on the supportive cues from innate immune cells in the inflammatory cascade after injury. Moreover, the anti-inflammatory immune cells such as M2 macrophages and non-classical monocytes Ly6Clo are able to control fibrosis formation and restore tissue architectures.104 A further investigation of S1P signaling pathways proves that FTY720 can also selectively recruit Ly6Clo monocytes.

105

The PLGA films blended with FTY720 can accelerate the accumulation of anti-inflammatory phenotype macrophages, and improve the reconstruction of muscle fibers and decrease the formation of fibrotic tissues.105

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3. Target cells for tissue regeneration

3.1 Cells involved in endothelialization

Formation of blood vessels in vivo involves two major processes, vasculogenesis and angiogenesis. Sprouting of capillaries from pre-existing blood vessels occurs during angiogenesis. In vasculogenesis, the de novo assembly of undifferentiated endothelial cells to capillaries in situ should occur. This process starts in the early stages of embryogenesis. First of all, mature endothelial cells are formed by the differentiation of EPCs, and then primitive vessel network is formed by the proliferation of mature ECs in avascular area. In the next step, the more complex capillary network is generated by the morphogenic process of angiogenesis. ECs degrade the surrounding extracellular matrix by releasing matrix metalloproteinases (MMPs). Then the cells start migrating to the newly developed gaps and form new blood vessels. The formation of blood vessels is assisted by different types of adhesion proteins, growth factors, oxygen sensors and junctional molecules, etc.106, 107 The stabilization and maturation of blood vessels is assisted by differentiated pericytes and SMCs, which are involved in the suppression of ECs growth.108 Usually native blood vessels are composed of three layers i.e., tunica intima, tunica media and tunica adventitia. The lining of the vessel lumen is made up of endothelial cells that are the part of tunica intima, while the sub endothelial layer consists of mostly loose connective tissue. The endothelial cells in the inner lining of blood vessels are the physical interface between blood and surrounding tissues. Maintaining the homeostatic thrombotic balance

21



helps in regulation of inflammation and angiogenesis.109, 110 Therefore, selective promotion of ECs activity and suppression of SMCs determine the rate and effect of vascularization. Cardiovascular diseases account for one of the major causes of death worldwide.111 Percutaneous transluminal coronary angioplasty (PTCA) based on the stent implantation has been used to treat cardiovascular diseases, particularly coronary vascular diseases.112, 113 However, in-stent restenosis causes smooth muscle cells to undergo rapid adhesion and proliferation, leading to the narrowing of vessels. Even for the drug eluting stents, long term implantation still leads to a high probability of failure because of the late local endothelium regeneration and late stent thrombotic events.114,

115

It is reported that neointima formation is the results of

injury-induced migration and proliferation of SMCs and delay in re-endothelialization. The vessel endothelium prevents thrombosis and hyperplasia inside the vessel, and thereby maintains the vessel integrity. Therefore, rapid re-endothelialization can be a potential solution to prevent in-stent restenosis (ISR) and late stent thrombosis (LAST).113 Unfortunately, artificial vascular grafts cannot spontaneously promote endothelialization in situ due to low attachment, spreading and growth of endothelial cells.115 Adhesion and proliferation of endothelial cells can be enhanced by immobilization of extracellular matrix molecules or cell-adhesive peptides on material surfaces, but the effects of these strategies are limited because of the competing adhesion of many other cells with ECs in vivo.7, 36, 116 By contrast, a cytocompatible matrix immobilized with ECs-specific ligands can promote ECs adhesion and rapid in situ endothelialization.117 Kuwabara et al. evaluated the endothelialization degree of implanted CAG-containing PCL grafts with a diameter of 0.7 mm 22


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Biomacromolecules

and a length of 7 mm. The degree of endothelialization after implantation for 6 weeks (97.4%) is significantly higher than that of the control group (76.7%).118 To exert selective capture of endothelial cells under physiological simulation, Plouffe et al. studied the role of REDV and Val-Ala-Pro-Gly (VAPG) peptides (selective for SMCs) along with fluid shear stress to achieve selective capture of SMCs and ECs in microfluidic devices. The adhesion of ECs on REDV-modified surfaces is higher than that of SMCs on VAPG-modified surfaces at a lowest shear stress. Moreover, adhesion of non-target (SMCs and fibroblasts) cells on the REDV-coated surfaces is of the same magnitude as that of adhesion of target cells (SMCs) on VAPG-coated surfaces. These observations suggest that SMCs and fibroblasts are able to attach onto the REDV-coated surfaces along with ECs but to a smaller extent. Non-target adhesion of cells on VPAG-coated surfaces is much smaller. Another factor is the relative magnitude of adhesion of target cells and non-target cells. The magnitude difference between target (ECs) and non-target cells (SMCs and fibroblasts) on the REDV-coated surfaces increases below a shear stress of 2.6 dyn/cm2. 45, 119 Besides capturing endothelial cells from circulation, the migration of endothelial cells from surrounding tissues to the injury sites can accelerate regeneration, which has been achieved by a gradient surface in vitro.120 Tyr-Lle-Gly-Ser-Arg (YIGSR) is an active peptide segment derived from β1 chain of laminin, a kind of glycoprotein locating on cell membrane. It can interact with the 67 kDa laminin binding protein (67LR), which is highly expressed on membrane surface of ECs.31 Therefore, YIGSR exerts great potential in supporting attachment, spreading and migration of ECs after being modified on various surfaces.121-125 On the complementary gradient 23



surface of PHEMA and YIGSR, ECs exhibit significant orientation and directional migration towards the increased direction of YIGSR density, while SMCs show random movement without significant change in the mobility rate (Figure 5).

12

The synergetic effect of adhesive peptides

and adhesion-resistant polymers opens new strategies for controlling selected cell migration in tissue regeneration. To simplify the material processing and promote this technique to practical application, methacrylate-modified hyaluronic acid (MAHA) molecules are grafted onto polydopamine-treated PCL films, on which thiol-containing REDV peptides are covalently immobilized in a gradient manner. Preferential migration of ECs but not SMCs is similarly realized. 13

Figure 5. Schematic illustration to show the structure of the complementary density gradient of PHEMA and YIGSR and its influence on the mobility of ECs and SMCs. The direction of increased YIGSR density and decreased PHEMA density is defined as the ‘‘+X’’ direction. Reprinted with permission from ref 12. Copyright 2014 American Chemical Society.

24


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Biomacromolecules

The recruitment of EPCs in circulation is another strategy for re-endothelialization due to their potential of differentiation into ECs.106 Generally the surface receptors of EPCs are similar to ECs.126 The EPCs emerged as potential targets for cell selectivity in blood vessel regeneration and related investigations have been rarely reported. Seeto et al. studied the dynamic adhesion of endothelial colony forming cells (ECFCs), one type of EPCs, on PEG hydrogels grafted with RGD, REDV and YIGSR peptides under circulation condition.127 Blood outgrowth endothelial cells (BOECs), or the so-called late-EPCs, have been found to increase surface endothelialization and vascularization. Another advantage of using BOECs is that the cells can be obtained from peripheral blood. Moreover, the population density of BOECs is larger than that of the mature ECs at the same culture period of time.128, 129 Veleva et al. synthesized bioactive methacrylic acid terpolymers modified with selective HBOECs specific ligands (TPSLEQRTVYAK peptide), and found that HBOECs binding is directly proportional to the peptide concentration bound to the polymers, allowing the specific adhesion of HBOECs and promoting endothelialization.52

3.2 Cells involved in nerve regeneration

Regeneration of peripheral nerves is very important but is also complex. Unlike central nervous system, it has a remarkable ability to regenerate.130, 131 Various synthetic materials have been developed for neural regeneration by mimicking their extracellular matrix.132-136 After nerve injury, axons need to regrow back to their targets and regain functions, otherwise the axon degeneration would hamper nerve tissue regeneration.137 Schwann cells (SCs) together with tissue macrophages and inflammatory cells remodel the environment to make it more conducive 25



Page 26 of 73

for axonal regrowth,138 indicating the importance of directional migration of SCs in periphery nerve regeneration.139 Glycosyltransferase lh3 is essential in the returning process of injured axons to their original synaptic targets, and is expressed largely by Schwann cells to support target-selective regeneration.138, 140 In the peripheral nerve regeneration, SCs wrap around the axons and serve as the substrate for axon growth, meanwhile producing kinds of adhesion molecules and neurotrophins factors for regenerating axons.141 Nevertheless, after injury the fibroblasts migrate into the wound site rapidly and result in scar tissue, thus impedes the migration of Schwann cells and nerve tissue regeneration.142

Neural

cell

adhesion

molecule

(NCAM)-derived

peptides

such

as

Ile-Lys-Val-Ala-Val (IKVAV) and KHIFSDDSSE (KHI) peptides are found to minimize fibroblasts adhesion and promote neuron cell adhesion to obtain neuron-selective substrates.48 For instance, polylysine hydrogels modified with IKVAV peptides can promote neurogenesis.49 A complementary density gradient of poly(3-dimethyl-methacryloyloxyethyl ammonium propane sulfonate) (PDMAPS) and KHI peptide surface can significantly enhance the SCs migration rate and directional movement while reduce the fibroblasts migration (Figure 6).10 Moreover, SCs preferentially migrate to the direction of higher KHI density, whereas fibroblasts have no particular direction.

26


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Biomacromolecules

Figure 6. Schematic of structure of a complementary density gradient of zwitterionic polymer PDMAPS and nerve cell adhesion molecule KHI. SCs present directional and faster migration towards the direction of increasing density of KHI compared to fibroblasts. Reprinted from ref 10, Copyright (2015), with permission from Elsevier.

In contrast with the peripheral nerve regeneration, human neural progenitor cells (hNPCs) are potential for therapy of central nervous disorder. hNPCs could selectively expand on the substrate co-immobilized with EGF and bFGF to overcome the limitation from neuropheres.143 Three-dimensional scaffold of nanofibers formed by self-assembly of amphiphilic peptide molecules can mediate the selective differentiation of NPCs into neurons.144 Stephanopoulos et al. fabricated RGD peptides-DNA conjugates, which can form nanotubes and enhance the differentiation of neural stem cells into neurons rather than astrocytes.145 The responses of brain tissue to various materials implanted with neural electrodes have been widely reported.4,

146

Implanted neuroprosthetic devices often suffer from coverage of scar formed by resident glial cells, limiting the long functional stability. In a recent work, the polyimide-insulated microwires modified with KHI could enhance the material biocompatibility by reducing the glial scar 27



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formation. The recruited astrocytes coat the modified wires within 24 h, whereas 14 days are needed on the control wires. The coated thin layer of astrocytes on the microwires will then reduce the microgial response.147 In another study, a simple one-step sol-gel of organosilica is used to obtain 11 different hybrid thin films with different organic functional groups. The addition of (3-aminopropyl)triethoxysilane thin film is the best to support neuron adhesion and neurite development. The hybrid organosilica also offers selective support to neuronal growth and limitation to astrocyte growth.148 This interaction of cells on selective substrate is similar to the study reported by Krsko and co-workers.149 One important area where multiple cell types must be controlled is the development of engineering approaches to mitigate spinal-cord injury. Trauma to the spinal cord can damage both ascending and descending axons at the site of a lesion. The disability of axonal regeneration is mainly attributed to the glial scar forming at the injury site.150, 151 Thus, an important challenge in regenerative neuroscience is to create an environment that permits axonal regeneration across this glial scar.152, 153 Despite substantial progresses have been made, regeneration of spinal cord continues to be impeded by the presence of glial scar cells including macrophages, meningeal cells, astrocytes and oligodendrocyte progenitor cells, and the inhibitory substances secreted by these cells. Thus, one major goal associated with constructing a bridge is to promote axonal growth while limiting the attachment of other types of cells.154 Micropatterned nanofibers are very effective to guide neurite growth.155, 156 Micropatterns have also been recognized to contribute to cellular responses such as selective attachment157-161 and enhance

the

differentiation

of

potential

cells

into

28


neurons.162,

163

Submicron-sized

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Biomacromolecules

surface-patterned PEG hydrogels are used to mediate adhesion and direct growth of neural cells while preventing the adhesion of astrocytes. A separation of about 2 µm between cell-repulsive PEG hydrogels is enough to guide neurite growth and to inhibit astrocyte adhesion and growth.149 Nanostructure and nano-fluidic transport used by Han et al. selectively enhance survival of neuronal cells.164 Human embryonic stem cells (hESCs) are differentiated into neurons by ridge/groove patterns.165 The hESCs differentiation into neuronal or glial lineage can be also influenced by the combination of topography and biochemical cues.166 Surface morphology acts similar to patterns since neural-like cells could be derived from mesenchymal stem cells.167

3.3 Stem cells

Stem cells have attracted much attention in field of tissue engineering and regenerative medicine owing to their pluripotency, low immunogenicity, and expansion potential.168 Classical tissue engineering needs sufficient number of stem cells before engraftment. However, there are many limitations in the ex vivo expansion of stem cells, including the time-consuming process of expansion, and loss of phenotype.169 Moreover, it has been reported that more than 90% of the transplanted MSCs die after 4 days’ implantation.170 Only a few of them are directly involved in tissue repair. Therefore, in situ tissue regeneration has been a promising approach via recruiting endogenous MSCs to tissue defects and stimulating intrinsic repair potential of the body. However, most biomaterials do not possess the ability to selectively adhere stem cells over other types of cells. For example, collagen consisting of RGD peptide sequences is able to promote the non-selective adhesion of multiple types of cells via the interactions with integrin, osteoclast 29



associated receptor (OSCAR), G-protein coupled receptor (GPR56), leukocyte-associated Ig-like receptor (LAIR-1), and glycoprotein VI (GPVI), which are widely expressed by fibroblasts and immune cells, and thereby activate the signaling cascades to result in fibrosis.171 Therefore, it is of great importance to modify the surface of biomaterials to achieve the specific affinity to stem cells. As aforementioned, the selective properties of biomaterials are generally relied on the specific interactions between the receptors of stem cells and the biomaterial surfaces. CXCR4 is notably expressed on hematopoietic stem cells (HSCs), MSCs and ESCs, and has previously been demonstrated to play an important role in stem cells homing and immobilization in vivo.172, 173 So far chemoattractants, stem-cell specific peptides, stem-cell affinitive topography and cell-related technology have been developed to endow biomaterials with recruitment, capture or directed differentiation of stem cells. Many chemoattractants such as SDF-1α, 174-176 substance P, 177, 178

and VEGF 179, 180 have the ability to recruit and immobilize stem cells onto implants. Some

biomaterials themselves have the ability to control stem cell fate. For example, three-dimensional hyaluronic acid (HA) microenvironments are beneficial for MSC chondrogenesis, and collagen type-II and chondroitin sulfate can facilitate a more chondrogenic phenotype without the use of growth factors.181,182 It is reported that HA macromers can activate MSC chemotaxis up to 4-fold in vitro through CXCR4 and CD44 receptor signaling.183 SDF-1α is a member of CXCL12, which has a specific affinity to CXCR4. The HA hydrogel packaged with SDF-1α has a synergistic effect in the treatment of myocardial infarction (MI). The activity of SDF-1α can be well maintained in the crosslinked HA hydrogel, and can be gradually released within 3 days. 30


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Biomacromolecules

The HA Gel/rSDF-1α system can immobilize significantly more circulating BMSCs, which are homed to the heart through sustained delivery of rSDF-1α and HA.184 Shao et al. identified a peptide sequence (E7, EPLQLKM) with seven amino acids via this technology.50 Compared to the peptide with the same amino acids as E7 but in a scrambled order (M7, MLKPLEQ), E7 shows an efficient specific interaction with MSCs regardless of their species. Moreover, the selectivity of E7 is further demonstrated by co-culturing MSCs, RAW264.7 cells and NIH3T3 cells on E7-modified collagen substrates. A flow model simulating the MSC capture in vivo reveals its good selectivity under a flow circumstance (Figure 7Error! Reference source not found.).185 In addition, E7 modified silk fibroin-gelatin scaffolds appear to be a promising biomaterial for knee cartilage repair.186, 187 Other peptides discovered by the phage display technology and targeted to ESCs, MSCs, and other stem cells are summarized in Table 1.

Figure 7. A surface with selective capture of MSCs (BMSCs) over fibroblasts (NIH3T3 cells) and immune cells (RAW264.7 cells) is developed by conjugating E7 peptides on collagen substrates. Reproduced from ref 185 with permission of the Royal Society of Chemistry. http://dx.doi.org/10.1039/c7tb02812a 31



The selectivity of topography to adhesion and differentiation of stem cells has been widely studied too.165,

188-191

A systematic study has shown that BMSCs on submicro- and

nano-dimensional multi-patterned substrates possess apparently selective migration behaviors. A chip containing 36 differently designed surfaces including squares and grooves varying in feature sizes between 10 and 1000 nm were fabricated, and the grooved patterns could be further subdivided into three groups according to the different ridge to groove ratios. Significant difference exists between the patterns and smooth surface with respect to the cellular affinity. Based on selective migration rather than proliferation, all sizes of squares show strong cell-repelling capacity, and the cell repelling of the nano-grooved patterns depends on the ridge to groove ratios.192 Chen et al. found that the scaffolds having both the radially oriented pore and SDF-1 can most effectively promote the cartilage regeneration, offering a combination between topographies and stem cell-specific molecules for selective homing of MSCs.176 Besides migration, the specific surface pattern controls the adhesion and differentiation of MSCs too.193 On the different patterns of square array, hexagonal array, and disordered square array with dots displaced randomly, human MSCs (hMSCs) show the totally different cell morphology. The nanoscale disorder stimulates differentiation of hMSCs to produce bone mineral in vitro, suggesting that the topography can control the specific differentiation of stem cells.92 It is well known that mechanical properties of biomaterials such as elasticity and stiffness can effectively modulate stem cell fate.194-200 The soft substrates mimicking brains facilitate

32


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Biomacromolecules

neuronal differentiation, stiffer substrates mimicking muscle promote myogenic differentiation, and rigid substrates mimicking collagenous bone improve osteogenic differentiation.194 Detailed and comprehensive work has been done to realize the commitment of MSCs populations in response to the rigidity of three-dimensional microenvironments, with lipogenesis occurring predominantly at 2.5-5 kPa and osteogenesis occurring predominantly at 11-30 kPa.195 Apart from mechanical properties, roughness and porosity are also important issues which should be considered in design of biomaterials.201-203

3.4 Other cells

For knee repair, it is of great importance to regenerate articular cartilage and subchondral bone simultaneously because cartilage defect often extends deeply into the knee joint and reach subchondral bone. Cartilage and subchondral bone have dissimilar components, and thereby combination of two types of scaffolds are required to have an ability to promote the regeneration of cartilage and subchondral bone, respectively. In a difunctional regeneration scaffold for knee repair, a DNA aptamer Apt19S that can selectively recognize and capture pluripotent stem cells is immobilized.204 The scaffold composes of two parts. The upper part for cartilage regeneration is formed by sodium alginate (SA) hydrogel loaded with graphene oxide (GO), and kartogenin (KGN), a cytokine that can promote chondrogenic differentiation of MSCs.205 The bottom part for subchondral bone regeneration is made of 3D GO-based biomineral framework (3D-GBF). After implantation into full-thickness rat osteochondral defect in vivo, endogenous MSCs are recruited selectively from a marrow clot to the defect site. Subsequently, MSCs in the upper part 33



Page 34 of 73

selectively differentiate into chondrocytes due to the induction of KGN, while MSCs in the bottom part specifically differentiate into osteoblasts as a result of induction of GO and high modulus.11 Promotion of migration to injury sites and proper proliferation of hepatic cells is crucial for liver

regeneration.

Galactose-modified

hyperbranched

polymers,

poly(methylene

bisacrylamideaminoethyl piperazine) (LA-HPMA), are immobilized on a surface in a gradient fashion to selectively guide the directional migration of hepatic cells due to strong interaction between galactose and hepatocytes. PEG molecules are grafted onto the same substrate to form a complementary gradient, which function as anti-fouling polymers to resist non-selective cell adhesion. As a result, hepatocytes migrate directionally towards the increased density of LA-HPMA, whereas fibroblasts move randomly (Figure 8).206

Figure 8. Schematic for complementary grafting density gradient of PEG and glycopolymer LA-HPMA, which promote selective adhesion and directional migration of hepatocytes (HepG2) over other types of cells (NIH3T3 cells as a typical example). Reprinted from ref 206, Copyright (2016), with permission from Elsevier.

34


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Biomacromolecules

4 Conclusions and future perspectives

Selective cell promotion is a crucial issue for the organized and programmed regeneration process, and may offer a solution for malignant consequences such as fibrosis and hyperplasia on a cell level. Since the main challenges and target cells change with regeneration sites, the fabrication methods of selective surfaces depend strongly on the specified tissues. For instance, the restenosis occurs in blood vessel and blood-contacting implants, hence the selective enhancement of ECs and inhibition of SMCs is one of the key issues. In nerve regeneration, the key issue lies on avoiding fibrosis, and thereby it is favored to promote the adhesion and proliferation of Schwann cells and nerve progenitor cells while to repel fibroblasts. Selective molecules can also be incorporated into nanoparticles for targeting and cure of inflamed cells. Preferences of cells to surrounding environments are mediated by both chemical and physical cues. Various technologies that can modify surface with molecules and manipulate surface physical properties, and typical cell selective surfaces are summarized in Table 1. The design of cell-selective surface by chemical and biological cues mainly depends on the discovery and incorporation of cell-specific molecules. With the development of molecular biology and high throughput methods such as phage display technology, more and more selective molecules among peptides, antibodies and growth factors will be discovered, broadening the applications to more types of cells. In addition, newly synthesized molecules such as Nylon-3 and KGN can also function as selective cues, expanding the database for making cell-selective surfaces. Recently, some studies have been focused on the combinational effect and comparison 35



of two factors on cell selectivity, although very a few of them may take the synergistic advantages. Combining the specific bioactive molecules with physical characters is another promising strategy to achieve target cell capture through synergistic effects of selectivity. The cell-cell talk expands the understanding of comprehensive cell interactions in the healing process and offers more strategies for cell-selective materials. In particular, the inflammatory signals take a decisive role in the healing process, which may promote myofibroblasts recruitment and fibrosis. Nowadays most solutions are focused on blocking the signaling transduction pathways, whereas a few studies have reported materials-related solutions. In the future, the regeneration outcome as a result of cell selectivity not only lies in recruitment, migration and differentiation of targeted cells, but also depends on the maintenance of cell phenotypes, such as avoiding epithelial mesenchymal transition that usually causes fibrosis. The still bigger challenge is the regeneration of tissues and even organs with multiple types of cells, for example, blood vessels consisting of three layers, and osteochondral defects including both bone and cartilage. The traditional tissue engineering method can partially resolve this puzzle by pre-seeding different kinds of cells in different locations of composite scaffolds. However, the organized regeneration and establishment of hierarchical structures by the in situ method is rarely reported. Taking the natural healing process into consideration, the interplay of the tissue microenvironment with the implants should be paid more attention, for example, the modulation of stem cell differentiation and immune responses by the deliberately designed biomaterials with favorable physical topography and chemical properties. In this way, the biomaterials can better interact and adapt to the local tissue environment, leading to the 36


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Biomacromolecules

regeneration of tissues and organs with complex structures and functions.207 Such a concept is only in its infant stage, and more efforts should be endeavored to explore the intrinsic interactions of biomaterials and host tissues with respect to the time-dependent alterations of tissue microenvironment and structures and properties of implantable biomaterials.

Acknowledgements

This study is financially supported by the National Key Research and Development Program of China (2016YFC1100403), the Natural Science Foundation of China (21434006), the 111 Project of China (B16042), and the Fundamental Research Funds for the Central Universities (2017XZZX001-03B).

Table 1. Typical cell-selective surfaces for tissue regeneration Design of materials

Key molecules used

Functions

Cells involved

Regeneration

Ref

tissues 77

Zwitterionic polycaboxybetaine coating modified with REDV peptide

Polycaboxybetaine, REDV peptide

Adhesion, proliferation, migration

ECs, SMCs

Blood vessels

Coating of REDV modified terpolymer brush and PEG on PET films

REDV peptide, PEGMA, BMA, PET, p-nitrophenyloxycarbonyl, poly(ethylene glycol)methacrylate

Adhesion proliferation

ECs, SMCs

Blood Vessels

78

Chemokines blended PLGA films.

FTY720, PLGA.

Recruitment of non-classical monocytes Ly6Clo

Selectively recruitment of Ly6Clo, accumulation of M2 macrophages.

Skeletal muscle.

105

CAG peptide blended PCL electrospun fibers

PCL, CAG peptide

Adhesion, proliferation

ECs, SMCs

Vascular grafting in vivo

44,

37


118


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Functionalization of Polycarbonate urethane by Covalent linking of CAG peptide and hydrophilic polymer brush

Polycarbonate Urethane, CAG peptide, Hydrophilic PEGMA, pentafluorophenyl methacrylate

Adhesion, proliferation

ECs, platelets

Blood vessels

8

Grafting of REDV on PEG diacrylate hydrogels

REDV peptide, acryloyl-PEG-succinimidyl valerate, PEG diacrylate

Adhesion

ECFCs

Blood vessels

127

Incorporation of REDV into hydrophilic copolymers

REDV peptide, N-(2-hydroxypropyl) methacrylamide (HPMA) and eugenyl methacrylate (EgMA)

Adhesion

ECs, SMCs, platelets

Blood vessels

23

REDV immobilized chitosan on the top layer of multilayers composed of chitosan and heparin

REDV peptide, heparin, chitosan

Adhesion

ECs, SMCs

Blood vessels

24

Fabrication of gradient density PHEMA and complementary gradient of YIGSR peptide

YIGSR peptide, PHEMA

Adhesion, migration,

ECs, SMCs

Blood vessels

12

Deposition of polydopamine on PCL films followed by grafting of methacrylate hyaluronic acid and subsequently gradient grafting of REDV

PCL, Polydopamine, Methacrylate modified hyaluronic acid (MAHA), REDV peptide

Adhesion, migration

ECs, SMCs

Blood vessels

13

Functionalization of polyester with VEGF or anti-CD34 antibody by using heparin.

VEGF, polyester, heparin, anti CD34 Ab

Adhesion, endothelium formation

ECs

Vascular grafting for blood vessels

57

Immobilization of Anti CD31Ab on HBFI coated PCL films

Anti-CD31 Ab. HBFI hydrophobins

Adhesion

ECs

Blood vessels

60

PCL films Anti-CD133 Ab functionalized on multilayer of heparin/collagen modified ePTFE

Anti-CD 133 Ab, heparin, collagen, ePTFE

Adhesion, proliferation, anti-coagulation

ECs

Vascular grafting for blood vessels in vivo

61

Bioactive methacrylic acid terpolymer matrix modified with Phage display selected HBOECs specific ligands

Methacrylic acid terpolymer, HBOECs specific ligand (TPSLEQRTVYAK peptide)

Adhesion, proliferation, endothelialization

HBOECs

Blood vessels

52

Nylon-3 polymer poly-DM modified surfaces

Poly-DM (Nylon-3 polymer)

Adhesion, migration,

ECs, SMCs

Blood vessels

64

38


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Biomacromolecules

proliferation Borosilicate glass coverslips immobilized peptides

RGDS, KHIFSDDSSE, IKVAV, YIGSR and so on

Selective adhesion of astrocytes

Astrocytes, fibroblasts

Central nervous system

48

Bifunctional Hydrogels with different stiffness regimes

polylysine (PL) and IKVAV

Neuronal differentiation and adhesion

embryonic and adult neuronal progenitor cells

Nerve

49

A complementary density gradient

PDMAPS, KHIFSDDSSE peptide

Selective migration of

Schwann cells (SCs), fibroblasts (fibroblasts)

Peripheral nerve regeneration

10

Selectively treat/target microglia cells reduce the pro-inflammatory response

Microglia cells and macrophages

Spinal cord

208

Schwann cells

Minocycline loaded nanoparticles

PCL, minocycline

injury

Anchored growth factors onto Ni ion-bound glass

EGF-His, bFGF-His

Selective expansion of hNPCs in adherent culture

Human neural progenitor cells

Central nervous disorders

143

3D network of nanofibers formed by self-assembly of peptide

IKVAV

Selective differentiation of neural progenitor cells into neurons

Neural progenitor cells, neurons, astrocytes

Spinal cord

144

Polyimide-insulated microwires modified with peptide

KHIFSDDSSE, APTES

Improved biocompatibility through reduced glial scarring

Astrocytes, microglia


147

Hybrid thin film Organosilica Sol−Gel

C8, C18, Vy, SH, NCO, Cl, and Ip hybrid silica samples

Support neuronal growth and limit astrocyte growth

PC12 cells, primary cortical neurons, astrocytes


148

Surface-patterned poly(ethylene glycol) hydrogels

PEG,

Mediated adhesion and directed growth of neural cells

Neurons, astrocytes

Nerve regeneration

149

collagen scaffold

SDF-1

Recruitment

BMSCs

cartilage and subchondral bone

158

PLLA/gelatin mesh scaffold

SP, SDF-1α

Recruitment

MSCs, HSCs

not mentioned

159

Controlled surface morphology and hydrophilicity of PCL

PCL

Selective differentiation of mesenchymal stem cells to

Mesenchymal stem cells, neural cells

Nerve tissue repair

167

39



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neural like cells Nanoscale ridge/groove pattern arrays

PUA, PET

Direct differentiation of human embryonic stem cells into selective neurons

hESCs, neuronal lineage

Nerve injury repair

165

HA

HA, growth factor beta-3 (TGF-b3)

Recruitment, capture

hMSCs

cartilage and subchondral bone

163

chondroitin sulfate, collagen type II

chondroitin sulfate, collagen type II

Differentiation

hBMSCs

cartilage

164

PCL stent

anti-human CD34 antibody

Capture

EPCs

vascularization

89,17 0

Chitosan membranes

anti-human CD3, anti-human CD29, anti-human CD105

Capture, purification

ASCs

not mentioned

171

PCL / collagen

E7 (EPLQLKM)

Capture

mesenchymal stem cell

Osteochondral grafts

50, 185, 187

Bilayer scaffold loaded with aptamer Apt19S. Upper part: SA hydrogel; Bottom part: 3D-GBF

Aptamer Apt19S, sodium alginate, KGN, grapheme oxide.

Capture of MSCs; Differentiation into chondrocytes and osteoblasts

MSCs, chondrocytes, osteoblasts.

Knee

11

References: 1.

Gurtner, G. C.; Werner, S.; Barrandon, Y.; Longaker, M. T. Wound repair and regeneration. Nature 2008,

453, (7193) 314-321 DOI: 10.1038/nature07039

2.

Wynn, T. A. Cellular and molecular mechanisms of fibrosis. J. Pathol. 2008, 214, (2) 199-210 DOI:

10.1002/path.2277

3.

Minev, I. R.; Musienko, P.; Hirsch, A.; Barraud, Q.; Wenger, N.; Moraud, E. M.; Gandar, J.; Capogrosso,

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Design and applications of cell-selective surfaces and interfaces

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