Human Amniotic Membrane: A Versatile Scaffold for Tissue Engineering

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The Human Amniotic Membrane: A Versatile Scaffold for Tissue Engineering Julien H Arrizabalaga, and Matthias U Nollert ACS Biomater. Sci. Eng., Just Accepted Manuscript • DOI: 10.1021/acsbiomaterials.8b00015 • Publication Date (Web): 14 May 2018 Downloaded from http://pubs.acs.org on May 14, 2018

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ACS Biomaterials Science & Engineering

The Human Amniotic Membrane: A Versatile Scaffold for Tissue Engineering Julien H. Arrizabalaga1 and Matthias U. Nollert*,1,2

1

Stephenson School of Biomedical Engineering, University of Oklahoma, Norman, OK, United

States 2

School of Chemical, Biological & Materials Engineering, University of Oklahoma, Norman,

OK, United States *Author to whom correspondence should be addressed to. Email: [email protected]

ACS Paragon Plus Environment

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ABSTRACT The human amniotic membrane (hAM) is a collagen-based extracellular matrix derived from the human placenta. It is a readily-available, inexpensive, and naturally biocompatible material. Over the past decade, the development of tissue engineering and regenerative medicine, along with new decellularization protocols, has recast this simple biomaterial as a tunable matrix for cellularized tissue engineered constructs. Thanks to its biocompatibility, decellularized hAM is now commonly used in a broad range of medical fields. New preparation techniques and composite scaffold strategies have also emerged as ways to tune the properties of this scaffold. The current state of understanding about the hAM as a biomaterial is summarized in this review. We examine the processing techniques available for the hAM, addressing their effect on the mechanical properties, biodegradation, and cellular response of processed scaffolds. The latest in vitro applications, in vivo studies, clinical trials, and commercially-available products based on the hAM are reported, organized by medical field. We also look at the possible alterations to the hAM to tune its properties, either through composite materials incorporating decellularized hAM, chemical crosslinking, or innovative layering and tissue preparation strategies. Overall, this review compiles the current literature about the myriad capabilities of the human amniotic membrane, providing a much-needed update on this biomaterial.

KEYWORDS Human amniotic membrane, tissue engineering, biomaterials, extracellular matrix, regenerative medicine.


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INTRODUCTION Anatomy and Components The human amniotic membrane (hAM), also known as the amnion, is the innermost layer of the fetal membranes. It is loosely attached to the chorionic membrane, or chorion. Together, these fetal membranes form the amniotic sac, which contains the embryo and amniotic fluid during pregnancy. Both membranes are loosely connected via a spongy collagen layer, making them easy to peel and separate from each other.1 The hAM is a translucent and avascular biomaterial with a thickness of 20 to 50µm.1,2 As seen in Figure 01, the hAM consists of an epithelium monolayer in contact with the amniotic fluid, a basement membrane, a compact layer, a fibroblast layer, and then a spongy layer connected to the chorion.3 In a majority of tissue engineering applications, what is mentioned as the hAM actually refers to the basement membrane, decellularized and isolated from its surrounding layers to produce a thin and homogeneous biomaterial. Collagens type III, IV, and V are the major components of the basement membrane, providing structural integrity and mechanical strength to the tissue.4,5 Non collagenous glycoproteins such as laminin, fibronectin, and nidogen are also present.3,6 Amniotic Fluid Epithelium Basement membrane Compact layer Fibroblast layer Spongy layer Chorion

Figure 01: Schematic representation of the structure of the human fetal membranes. The amnion is composed of 5 distinct layers: epithelium, basement membrane, compact layer,


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fibroblast layer, and spongy layer. The chorion (not depicted) consists of a reticular layer, a basement membrane, and an outer trophoblasts layer.

Biological Properties The hAM possesses anti-microbial, anti-fibrosis, and anti-inflammatory properties.7,8 When implanted into the human body it effortlessly adheres to the wound surface, reduces scars, decreases pain, promotes wound healing, and has a low risk of immunogenicity.7,9–12 Another critical property of the hAM for tissue engineering applications is its ability to support cell attachment, proliferation, and differentiation.7,11,12 Various cell lines have been reported to adhere and proliferate on decellularized hAM. Figure 02 presents a specific example of the type of results numerous investigators have obtained, demonstrating that the culture of human mesenchymal stem cells on the hAM does not affect their immunophenotype or differentiation abilities.13 This unique set of biological and biochemical properties combined with its reduced cost and unlimited availability have shaped the hAM into a biomaterial of choice for clinical and tissue engineering applications.


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Figure 02: Characterization of human mesenchymal stem cells derived from bone marrow (BM-dMSC) or from adipose tissue (ASCs) previously seeded on hAM scaffolds. A: Immunophenotype of the cells as determined by flow cytometric analysis. B: Chondrogenic (Alcian Blue staining), osteogenic (Alizarin Red staining), and adipogenic (Oil Red O staining) differentiation of the cells. The culture of both BM-dMSC and ASCs on hAM scaffolds did not affect their immunophenotype or differentiation abilities. Reproduced with permission from ref 13.13 Copyright 2015 Mary Ann Liebert, Inc.

Amniotic Membrane-Derived Cells The hAM has also been reported as a source of 2 populations of stem cells: human amniotic epithelial cells (hAECs) and human amniotic mesenchymal stromal cells (hAMSCs).14,15 hAECs are present on the epithelium monolayer facing the amniotic fluid. hAMSCs are part of the stromal layer found between the basement amniotic membrane and the loose spongy layer connected to the chorion, as depicted in Figure 01. Overall, hAECs and hAMSCs represent valuable sources of multipotent stem cells for tissue engineering and regenerative medicine applications. The possibility of obtaining these cells from the hAM adds even more value to this tissue, which is usually considered to be medical waste. The isolation, characterization, differentiation, and applications of amniotic membrane-derived cells have already been thoroughly reviewed.11,12,16–18 Consequently, the present article will only focus on the prospects offered by the human amniotic membrane.

Historical perspective The hAM was first used for skin reconstruction by Dr. Davis in 1910.19 Subsequently, the hAM was employed for a broad range of applications: surgical dressings, the treatment of burns and ulcers, the reconstruction of the oral cavity, bladder, and vagina.20,21 In the 1940s the first ophthalmic applications of the hAM to treat conjunctival defects and chemical burns were reported.22–24 The initial interest for this biomaterial then faded away, most likely due to more


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stringent regulations regarding tissue transplantations, and the hAM almost disappeared from the literature for about 50 years. The resurgence of the hAM happened in the 1990s when it was reported by Kim et al. as an effective scaffold for ocular surface reconstruction.25,26 New preparation, preservation, and storage techniques were also developed over the same time period, assisting the hAM to gain significance for ophthalmic and dermatologic applications without the worry of disease transmission from fresh unprocessed tissue. In 2001, processed hAM received approval from the United Stated Food and Drug Administration (FDA) for ocular surface reconstruction, increasing its use even further and triggering the development of several commercial hAM derived products.27 Nowadays, the hAM has been widely adopted for burn wound dressing and ocular surface reconstruction. New clinical applications are also currently explored such as nerve wrapping,28–30 reconstruction of the oral cavity,31 flexor tendon repair,32 and the treatment of limbal stem cell deficiency.33

The development of tissue engineering diversified the potential uses of the hAM as a scaffolding material from traditional fields such as ophthalmology and dermatology to new disciplines. Over the last two decades, novel hAM modifications have been incorporating cells and utilizing the hAM as a scaffold to recreate complex 3D structures as opposed to last century uses as an acellular dressing.26 An ideal scaffold for tissue engineering applications is non-immunogenic and supports the attachment and proliferation of cells without affecting their immunophenotype or differentiation abilities. It also has comparable mechanical properties, biodegradation rate permeability, and flexibility to the tissue it intends to replace. Decellularized hAM is a versatile biomaterial that can be used to engineer several types of tissues from the human body.7


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Decellularized hAM is currently being investigated for a broad range of applications such as blood vessel tissue engineering,34 cartilage regeneration,35 and urothelium tissue engineering.36

PRESERVATION AND DECELLULARIZATION TECHNIQUES Tissue Processing and Preservation The hAM can be used two ways, either intact with its epithelium layer or decellularized with its epithelium removed. An intact hAM would simply be detached from the chorion, cut to size, and preserved for upcoming applications. The epithelium monolayer and extracellular matrix would remain untouched. Intact membranes are typically used for wound dressing in clinical applications, while decellularized hAM are ideal scaffolds for tissue engineering constructs. Epithelial cells need to be removed from the hAM in order to not interfere with new cells seeded on the scaffold. The goal of the decellularization process is to remove all epithelial cells and obtain a uniform and smooth basement membrane.37–39 Figure 03 illustrates the removal of the epithelium layer after decellularization.40 Intact hAM for clinical applications are processed, sterilized, and preserved prior to implantation in humans. Tissue processing simply consists of mechanically separating the amnion from the chorion, cutting it into smaller pieces, and flattening it onto nitrocellulose paper. Tissue preservation helps provide a steady supply of scaffolds for clinical applications. Several protocols have been developed for the preservation of intact hAM, including cryopreservation in glycerol, air-drying, freeze-drying, and incubation in trehalose.38,41


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Figure 03: Histological comparison of (A) an intact hAM with (B) a hAM decellularized with 0.1% trypsin-EDTA. The letters, e, b, and s respectively designate the epithelium, basement membrane, and stroma. Adapted with permission from ref 40.40 Copyright 2007 Mary Ann Liebert, Inc.

Decellularization hAM intended for tissue engineering applications are de-epithelialized. Rapid freezing is often used as a preliminary step to introduce ice crystals into the intracellular space and cause cell lysis.42 Enzymatic treatments and chemical treatments are then needed to solubilize the remaining cytoplasmic and nuclear cellular membranes.43 Enzymatic treatments for decellularization include protease digestion, calcium chelating agents, and nucleases.44 Most protocols commonly use EDTA, dispase, trypsin, or thermolysin.38,43,45 Saghizadeh et al. also reported using NaOH to efficiently de-epithelialize the hAM.46 Nucleases such as DNases and RNases are also advantageous for removing nucleotides after an initial cell lysis.44 Finally, sodium dodecyl sulfate is one of the most popular and attractive detergents used for treating the hAM since it yields a complete removal of cellular remnants without damaging the collagen from the tissue.44,47,48


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Gamma irradiation and chemical solutions (peracetic acid and ethanol) are the main techniques used for the sterilization of the hAM.48 Supercritical carbon dioxide has also been described as a preparation technique to obtain a sterile hAM without affecting its composition.49

Commercially Available Products The advances realized these past decades for the stabilization, preservation, and storage of tissues also lead to the development of several commercially available products derived from the hAM.35,50 These products have the advantages of being stable, as well as easily transported and stored. A majority of them consist of either cryopreserved or dehydrated intact hAM and have been recommended for the treatment of ophthalmic and dermal wounds. For instance, BioTissue AmnioGraft (cryopreserved intact hAM on a carrier paper) and IOP Ophthalmics AmbioDisk (dehydrated intact hAM) are both recommended for ophthalmic surgery. MiMedx AmnioFix, also made of dehydrated intact hAM, is endorsed for soft tissue surgery. Detailed information about commercially available hAM products can be found in the review written by Gindraux et al.50

TISSUE MODIFICATIONS Despite its attractive biological and biochemical properties, the hAM has been limited by its mechanical properties and biodegradation rate for some tissue engineering or regenerative medicine applications. To overcome these limitations, alterations to the hAM have been made to


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tune its properties, either through incorporating composite materials, chemical crosslinking, or innovative layering and tissue preparation strategies into the hAM.

Crosslinking Chemical crosslinking of the hAM has been reported to improve its mechanical properties and biodegradation rate without affecting affect the viability, proliferation, and immunophenotype of cells cultured on top of crosslinked hAM.51–57 Figure 04 presents an innovative technique developed by Hariya et al. for the production of transparent and resilient crosslinked hAM tissue laminates.58 Carbodiimide was used for crosslinking and up to 8 layers were assembled to produce a tougher and optically clearer graft for corneal transplantation.

Figure 04: Fabrication of transparent and resilient crosslinked hAM tissue laminates. For the first lamination stage, hAM are repeatedly dried and stacked up to produce a multilayer tissue laminate. Then, tissue constructs are optically clarified after successive carbodiimide crosslinking, washing, drying, and quenching steps. The final laminates contain up to 8 hAM layers and benefit from improved light transmittance and mechanical properties. Reproduced with permission from ref 58.58 Copyright 2016 Elsevier Ltd.

Composites


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New preparation techniques and composite scaffold strategies have also emerged as ways to tune the properties of the hAM. Recent publications describe applications of the hAM for osteochondral tissue engineering by coating it with poly(lactic-co-glycolic acid).59 The hAM was mixed with fibrin to produce a tissue engineered blood vessel and was combined with collagenglycosaminoglycan scaffolds for tendon tissue engineering.60,61 A similar composite material approach was used by Adamowicz et al. who layered denuded hAM with electrospun poly(Llactide-co-ε-caprolactone) (PLCL) for reconstructive urology.62 These composite scaffolds, presented in Figure 05, were successfully implanted in rats and promoted bladder augmentation.62

Figure 05: Scanning electron microscopy images of hAM-PLCL composite scaffolds. A: Cross-section image of the composite scaffold. B: Delaminated composite. Frozen hAM was sandwiched and covered on both sides with two layers of electrospun PLCL. Adapted with permission from ref 62.62 Copyright 2016 Adamowicz et al.

Several more composite and preparation techniques have been used to functionally augment the hAM for tissue regeneration purposes.63 A decellularized hAM was assembled with electrospun silk fibroin to produce a 3D bilayer of artificial skin.64 Denuded hAM was coated with


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poly(ester) urethane on both sides to improve its mechanical strength and produce a biocompatible surgical mesh.65 Another popular preparation method is the combination of several hAM scaffolds to produce multilayer constructs such as the hAM tissue laminates presented in Figure 04. Multilayer constructs have been reported for the fabrication of tissue engineered blood vessels,60,66,67 surgical patches,68 applications in ophthalmology,58,69,70 and oral and maxillofacial surgery.71,72 Skin defects have also been treated with solubilized hAM combined with hyaluronic acid hydrogel.73 Finally, micronized hAM (300 to 600µm microparticles) combined with epidermal stem cells successfully repaired full-thickness skin defects when transplanted in nude mice.74

CLINICAL APPLICATIONS Ophthalmology The hAM is widely used for a variety of ocular surface diseases thanks to its attractive biological properties, transparency, thinness, and composition akin to the one of the conjunctiva.75 The hAM can be applied on the ocular surface either as a temporary dressing or as a permanent graft.27 When used as a temporary biological bandage, the hAM acts as barrier to protect the healing epithelium from the movement of the eyelids. A hAM dressing aims to repel inflammation of the host tissue and reduce scarring.27 A permanent hAM graft transplanted on the ocular surface is used to promote the proliferation of the epithelial cells present on the ocular surface.76 The patient’s cells will grow over the hAM and the scaffold will be integrated into the patient’s tissue. For deep corneal ulcerations or perforations, the hAM can also be stuffed into the defects prior to patching or grafting.77


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Today the hAM is widely used for the management of several ocular ailments of the cornea or the conjuctiva. Applications of the hAM for corneal surface reconstruction include the treatment of chemical burns, bullous keratopathy, persistent epithelial defects, ulcers, and lesions.77 The hAM has been adopted for a variety of conjunctival pathologies including symblepharon, pterygium, chemical burns, and scleral thinning, for the covering and reconstruction of conjunctival lesions, and for the management of Stevens-Johnson syndrome.77–79

The hAM has also been applied to the treatment of limbal stem cell deficiency. Unlike the ophthalmic applications previously described, this recent method uses the hAM to produce a cellularized graft.80–82 Limbal stem cells are critical for the constant maintenance and regeneration of the corneal epithelium. Damage to the limbus would lead to the deficiency of these stem cells, epithelial breakdown, chronic inflammation, corneal conjunctivalization, and a loss of corneal clarity.83 Limbal stem cell deficiency can be treated with the transplantation of limbal epithelial cells expanded ex vivo. Cells can be obtained from a small biopsy of the patient’s other eye if healthy, or from another living individual or a cadaveric donor if both of the patient’s eyes are affected by limbal stem cell deficiency.83 In the case of donor shortages, oral mucosal epithelial cells and bone marrow mesenchymal stem cells could also be used as replacement cell sources to reconstruct the corneal surface.84–87 Decellularized hAM have been successfully used as substrates for the ex vivo expansion of limbal epithelial cells. Transplantation of these cellularized grafts resulted in the repopulation of the corneal epithelium and integration of the hAM with the corneal tissue.77,88,89 Figure 06 illustrates the transplantation process of limbal epithelial cells using the hAM as a carrier membrane.


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Limbal epithelial cells Biopsy Transplantation Healthy donor eye Cell seeding Diseased eye hAM graft

Decellularized hAM

Figure 06: Illustration of the transplantation process of autologous limbal epithelial cells for the treatment of a unilateral limbal stem cell deficiency. A small biopsy (about 2 by 2 mm of tissue) is performed on the patient’s healthy donor eye. Limbal epithelial cells are then isolated and seeded onto a sheet of decellularized hAM. After 2 to 3 weeks of culture, the cellularized hAM graft is transplanted onto the patient’s diseased corneal surface.

Other recent innovations have been finding new ways to attach the hAM to the ocular surface. The hAM is a thin material that is typically attached to the corneal surface with sutures. However, hAM bandages need to be replaced every week and repeated interventions at the diseased corneal surface is not recommended. Possible side effects of sutures also include conjunctival bleeding or scarring.90 The strategies developed for the sutureless fixation of the hAM include the use of fibrin,91,92 chemically defined bioadhesives,93,94 light-initiated bonding with Rose Bengal dye95,96 and medical devices (ProKera and AmnioClip) that use a dual ring system to mount the hAM and apply it like a contact lens.90,97 Dermatology The hAM has been described as an effective therapeutic option for burn wound dressing. Indeed, the hAM presents several advantages for skin applications such as its anti-inflammatory


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properties, antimicrobial effects, low immunogenicity, and good wound adherence. When used to cover burn wounds, the hAM reduced pain and scars, prevented infections, and promoted reepithelialization. 98–100 The hAM has been used to treat both superficial and partial-thickness burns,100 as an overlay for skin autografts,

101,102

and as a dressing for skin graft donor sites.103,104 Besides burn wound

dressing, the hAM proved effective for the treatment of chronic leg ulcers, pressure sores, and for patients with epidermolysis bullosa.105–107 These long-established dermatology applications of the hAM involve using it as an acellular biomaterial, while the most recent studies report using the hAM for the attachment and proliferation of various cell lines. Patients with stable vitiligo were transplanted with autologous melanocytes seeded on a decellularized hAM, resulting in over 90% skin repigmentation.108,109 Skin equivalents were constructed by combining a hAM seeded with fibroblasts and normal keratinocytes.55,110,111 Biological wound dressings were designed to promote tissue regeneration for patients with full-thickness skin defects, by combining the hAM with mesenchymal stem cells.13,74,112

Oral and Maxillofacial Surgery After oral surgery, bone surfaces are often exposed to the oral cavity which can lead to possible infections and scar formation. Thanks to its biological properties, the hAM has been described as an effective scaffold for the reconstruction of the oral cavity.31 Consequently, the hAM has been used for a broad range of applications: treatment of oral mucosa defects after removal or cancerous legions,113 flap surgery,

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oronasal fistula reconstruction in cleft palate surgery,71,72

and temporomandibular joint surgery.115


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Recent tissue engineering approaches involve the fabrication of a myomucosal flap using oral keratinocytes cultured on hAMs,116 and the autologous transplantation of oral mucosal epithelial cell sheets cultured on hAMs for intraoral mucosal defects.117–119 Figure 07 shows that oral mucosal epithelial cells cultured on the hAMs present comparable keratin expression to cells present in the native oral mucosa.118


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Figure 07: Comparison of hAM-cultured oral mucosal epithelial cells with the oral mucosa. A-F: hematoxylin and eosin staining. B-G, C-H, D-I, E-J: Expression of keratins 4, 13, 1, and 10 in green with the cell nuclei stained in red with propidium iodide. Keratin expression was similar between the hAM cultured oral mucosal epithelial cells and the oral mucosa. Reproduced with permission from ref 118.118 Copyright 2015 Amemiya et al.


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Otolaryngology The human amniotic membrane has shown therapeutic promises as a scaffold in otolaryngology. Patches of hyperdry hAM were used as dressing substitutes for fascia grafts of the temporal muscle in canal wall down tympanoplasty.120,121 The hAM grafts were completely epithelialized faster than the classic fascia grafts.

TISSUE ENGINEERING APPLICATIONS The hAM has been investigated as a scaffold for tissue engineering and regenerative medicine applications in a broad range of disciplines. Several of these studies were already reported in previous paragraphs dedicated to tissue modifications of the hAM, along with novel cellularized applications of the hAM in ophthalmology, dermatology, and oral and maxillofacial surgery. Articular cartilage has minimal self-healing capability and often advances to osteoarthritis once damaged.122,123 The hAM has been described as an ideal substrate for the culture of chondrocytes.124–127 Consequently, chondrocytes have been seeded on the HAM in order to obtain a delivery vehicle for cell transplantation that could promote cartilage regeneration in vivo. For instance, Jin et al. seeded rabbit articular chondrocytes on decellularized hAM and used these constructs in vivo to cover rabbit osteochondral defects. After 8 weeks of implantation the defect area was successfully regenerated.40 The hAM has been reported as a potential osteoinductive biomaterial for bone regeneration.128,129 Decellularized hAM helped induce the osteogenic differentiation of human dental apical papilla cells seeded on top of it, opening potential applications for the hAM in bone and tooth tissue engineering.130 Intact hAM simply exposed to osteogenic media also promoted the differentiation of the stem cells contained in the hAM towards osteogenic pathways.131


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In the past years, the hAM has been investigated as a scaffold for tissue engineering of the urinary tract system. The hAM was described as a viable scaffold for the culture of urothelial cells and the reconstruction of damaged urothelium tissue.36,132–134 The hAM has been characterized as blood compatible and as an adequate cell carrier matrix for endothelial and smooth muscle cells.66,135,136 Consequently, several studies have reported rolling the hAM to engineer small diameter blood vessels.34,60,66,67,137 Finally, the hAM has been used as a scaffold for salivary gland regeneration,138 for esophageal wall tissue engineering,139 for the treatment of pelvic floor dysfunction,140 for liver regeneration, 141,142

and as a support of in vitro ovarian follicular culture.143

LIMITATIONS Risk of disease transmission Due to its human origin, the hAM carries a risk of disease transmission from its donor. Consequently, the use of fresh untreated hAM is not recommended. The collection, processing, and transplantation of the hAM have to follow the proper laws and regulations of the country where they would be performed.35 To avoid bacterial contamination, it is recommended to collect hAM tissue after caesarean section under sterile conditions. Typically, serological testing for syphilis, hepatitis, and HIV are performed on the donor at the time of tissue collection.77 Serological screening is repeated 6 months after birth to confirm that there were no false negatives during the first round of testing. In the meantime, the hAM is quarantined until both results are negative. Then, the hAM needs to be processed under aseptic conditions and stored in a sterile environment.77,88


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Donor variation The hAM is a biological human tissue and its composition is affected by intra and inter donor variations.76,144 The fetal sex, gestational age, donor age, health, and diet are all parameters that affect the properties of the hAM. Between donors, the thickness of the hAM varies from 20 to 50µm.1,2 From the same donor, the hAM will also be thinner away from the placenta and thicker closer to the umbilical cord.145 The transparency of the hAM will also change depending on its original location in the amniotic sac.146 One possibility to overcome these donor variations would be the development of pooling and screening methods to sort out different hAMs according to previously defined characteristics.

Effects of decellularization and storage techniques The preservation, decellularization, and sterilization protocols used to process the hAM will affect its mechanical properties, transparency, chemical composition, and cell adhesion properties.38,147–150 Characterizing how a treatment influences the morphology and composition of the hAM helps verify that no undesirable or unwanted property changes were induced. For instance, it is critical to ensure that the cell adhesion properties of the hAM are maintained after processing if the hAM is intended for tissue engineering applications. Standardization of processing techniques helps reduce variability. Standard protocols developed for commercially available hAM products and for tissue banks help produce consistent hAM allografts for clinical applications.50,151–153


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CONCLUSION The hAM is a readily available and inexpensive biomaterial that can efficiently be processed, preserved, and de-epithelialized. Thanks to its unique set of biological properties, the hAM is now a material of choice for several clinical applications in ophthalmology, dermatology, and oral and maxillofacial surgery. The development of standard processing protocols and tissue banks, along with commercially available hAM derived products, will further expand the clinical applications of the hAM. Moreover, decellularized hAM has proven worthwhile for a broad range of tissue engineering applications due to its ability to support cell attachment, proliferation, and differentiation. Modifications of the hAM have been developed to tune its properties, either through composite materials incorporating the hAM, chemical crosslinking, or innovative layering and tissue preparation strategies. Such advantageous techniques have the potential to become increasingly popular for the preparation of hAM based scaffolds for tissue engineering applications. Additionally, the hAM has been identified as a source of human amniotic epithelial cells and human amniotic mesenchymal stromal cells. These two multipotent cell lines are valuable for tissue engineering and regenerative medicine applications. Overall, the hAM is truly a versatile biomaterial and its foreseeable future as a scaffold for tissue engineering applications looks very promising.

SUPPORTING INFORMATION This manuscript is not accompanied by any supporting information for publication.


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AUTHOR INFORMATION Corresponding Author *Author to whom correspondence should be addressed to. Email: [email protected]

ACKNOWLEDGMENTS This work was supported by the Vice President for Research of the University of Oklahoma.

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TABLE OF CONTENTS GRAPHIC

Cellularized hAM graft

Isolation & Processing

Amniotic Fluid Epithelium

Basement membrane

Tissue Engineering applications

Compact layer

Tubular construct

Fibroblast layer Spongy layer

Decellularized hAM

Chorion

Fetal membranes

Cells

Tissue laminate

For Table of Contents Use Only. Manuscript Title: “The Human Amniotic Membrane: A Versatile Scaffold for Tissue Engineering” Authors: Julien H. Arrizabalaga and Matthias U. Nollert


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Human Amniotic Membrane: A Versatile Scaffold for Tissue Engineering

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