Spectroscopic and Physicochemical Characterization of Sulfonated

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Spectroscopic and physicochemical characterization of sulfonated Cladophora cellulose beads Igor Rocha, Yocefu Hattori, Mirna Diniz, Albert Mihranyan, Maria Strømme, and Jonas Lindh Langmuir, Just Accepted Manuscript • DOI: 10.1021/acs.langmuir.8b01704 • Publication Date (Web): 31 Aug 2018 Downloaded from http://pubs.acs.org on September 3, 2018

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Spectroscopic and physicochemical characterization of sulfonated Cladophora cellulose beads Igor Rocha,†‡ Yocefu Hattori,£ Mirna Diniz,† Albert Mihranyan,† Maria Strømme† and Jonas Lindh*† †Nanotechnology and Functional Materials, Department of Engineering Sciences, Uppsala University, Box 534, 75121, Uppsala, Sweden ‡CAPES Foundation, Ministry of Education of Brazil, Brasília - DF 70040-020, Brazil £ Physical Chemistry, Department of Chemistry, Uppsala University, Box 534, 75121, Uppsala, Sweden

Keywords Cladophora nanocellulose, dialdehyde cellulose, Raman spectroscopy, sulfonated beads

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Abstract The work presents a full physicochemical characterization of sulfonated cellulose beads prepared from Cladophora nanocellulose intended for use in biological systems. 2,3-dialdehyde cellulose (DAC) beads were sulfonated and transformation of up to 50% of the aldehyde groups was achieved resulting in highly charged and porous materials compared to the compact surface of the DAC beads. The porosity could be tailored by adjusting the degree of sulfonation and a subsequent reduction of the aldehyde groups to hydroxyl groups maintained the beads structure without considerable alteration of the surface properties. The thermal stability of the DAC beads was significantly increased with the sulfonation and reduction reactions. Raman spectroscopy also showed to be a useful technique for the characterization of sulfonated cellulose materials.

Introduction One of the main features of cellulose materials applied in biotechnology is their biocompatibility,1–3 which is often incorrectly reported as being inherent to cellulose since it comes directly from nature. However, cellulose itself is not always biocompatible and the material does not necessarily behave the same when its size is on a nanoscale dimension.4–6 Nanocellulose is a very versatile material composed of cellulose chains with one or more dimension within the nanometer range.7 It can be obtained from various sources including wood, bacteria and algae such as Cladophora species, which are harvested in coastal areas around the world.8 Cladophora nanocellulose contains unique properties such as a high surface area and high degree of crystallinity.9 Several studies using this material in biomedical applications have been carried out.10–13


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Because of their size, nanocellulose structures can interact with biological systems such as cells and tissues in ways different from those of their macro-sized counterparts; therefore, it is important to understand how the interactions between biomaterials based on nanocellulose and biological structures occur.14–16 From this perspective, characterization of the material surface regarding macro- and nanostructures, charge and physicochemical properties needs to be fully accessed to understand how the chemical groups on the surfaces of cells and tissues can be affected as well as how steric hindrances can modulate the biocompatibility of these nanocellulose materials. Our group has published the synthesis and characterization of a sulfonated cellulose material that can potentially be used as an immunosorbent, along with the first screening of its biocompatibility.17,18 Sulfonate groups are known to have important biological properties such as anticoagulant activity in polysaccharides like heparin.19 In an attempt to better understand the properties of nanocellulose materials, this study focus on the characterization of various beads produced from nanocellulose from Cladophora green algae which were spontaneously formed during a periodate oxidation reaction and subsequently sulfonated to different degrees and reduced without losing their spherical morphology. The materials were characterized with regard to morphology, size, structural changes and chemical properties. The possibility to tune the physiochemical properties and to be able to characterize the formed materials is key to obtain materials suitable for bioapplications. The characterization data and methods presented herein will have a strong impact on the future development of sulfonated cellulose materials for bioapplications as it is of vital importance to determine the physiochemical properties of the materials in order to better understand how different physiochemical properties affects the biological response to the materials.


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2. Materials and Methods 2.1. Chemicals Nanocellulose from Cladophora green algae was provided by FMC Biopolymer, USA. Sodium metaperiodate, sodium bisulfite solution, sodium borohydride, and other chemicals used were of analytical or reagent grade and were used as received. Deionized water was used in all experiments.

2.2. Preparation of Materials Cladophora nanocellulose was oxidized to 2,3-dialdehyde cellulose via reaction with sodium metaperiodate in aqueous acetate buffer according to a procedure developed by Lindh et al. and beads were formed after total oxidation for 240h.20 The sample was named DAC. The aldehyde groups in never-dried DAC beads were sulfonated in an aqueous dispersion with sodium bisulfite for 48h following a procedure by Rocha et al.17 using 0.125, 0.25 and 0.50 equivalents to the aldehyde groups. The resultant respective samples were named SDAC12, SDAC25 and SDAC50. The remaining aldehyde moieties were further reduced to hydroxyl groups with sodium borohydride in water for 24h using stoichiometric amounts and the resultant materials were named RSDAC12, RSDAC25 and RSDAC50. The samples were purified with water and ethanol and left to dry for 24h in a fume hood.

2.3. Characterization 2.3.1. Raman Spectroscopy. The materials were dried under vacuum for 24h before analysis. Raman analyses were performed on an inVia™ confocal Raman microscope (Renishaw, UK) with 6000 times acquisition for 0.1s using a 785 nm beam laser.


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2.3.2. Conductometric titration. This technique was used in order to evaluate the amount of sulfonation. The titrations were performed using a T70 titrator (Mettler Toledo, Switzerland) in 0.01 M dispersions (pH 2.8) previously sonicated and purged with nitrogen gas. The titrant was a 0.05 M NaOH solution.21

2.3.3. Scanning Electron Microscopy (SEM). SEM images were recorded with a Leo 1550 SEM instrument (Zeiss, Germany). Samples were mounted on aluminum stubs using doublesided adhesive carbon tape and sputtered with Au/Pd with a plasma current of 30 mA for 30s.

2.3.4. ζ-Potential Measurements. The electrophoretic mobility of the samples was measured using 0.001%(w/w) dispersions of the modified materials in NaCl(aq.) (10 mM) at pH 6.5 previously ultrasonicated (Vibracell 600 W, 20 kHz, USA) using a universal dip cell, a ZetaSizer Nano instrument and ZetaSizer Properties Software, both from Malvern Instruments, UK.

2.3.5. Speciﬁc Surface Area (SSA) and Pore Size Distribution Analysis. The nitrogen adsorption−desorption experiments were performed at 77 K using a ASAP 2020 gas sorption instrument (Micromeritics, USA). The samples were degassed under vacuum (1 × 10−4 Pa) at 70 °C for 24h prior to analysis. The SSA was calculated using the Brunauer−Emmett−Teller (BET) method22 on the adsorption branch of the isotherm at P/P0 between 0.05 and 0.3. The pore size distribution was calculated using the Barrett−Joyner−Halenda (BJH) method23 based on the desorption branch of the isotherm. Pore volumes were calculated assuming cylindrical geometries of the pores.


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2.3.6. Pycnometry. The true density, σt, was measured using helium pycnometry (AccuPyc 1340, Micromeritics, USA). Samples were dried from EtOH in ambient air and were further dried under reduced pressure prior to analysis.

2.3.7. Laser diffraction. Samples were dispersed in water and sonicated and the particle size was analyzed using a Mastersizer 3000 instrument (Malvern Instruments, UK).

2.3.8. Thermogravimetric analysis (TGA). Samples were analyzed with a TGA/SC 3+ instrument (Mettler Toledo, Switzerland) at a temperature range of 25–800 °C with a temperature increase of 5 °C per minute under nitrogen atmosphere.

3. Results and Discussion Scheme 1 illustrates the modifications made for the production of RSDAC beads. First, nanocellulose from Cladophora green algae was converted to DAC beads by periodate oxidation, a process that drastically changed the fibrillar structure of the material and sharply reduced its degree of crystallinity, as previously reported by Lindh et al.20 In our previous work we suggested that possible reasons for the morphological changes were the opening of the glucose ring leading to more flexible chains and development of inter- and intrafibrillar hemiacetal cross-links.20 The subsequent sulfonation according to the method developed by Zhang et al.,24 using 0.125, 0.25 and 0.5 equivalents of sodium bisulfite to the aldehyde groups produced materials with different surface and physicochemical properties that nevertheless maintained the bead morphology. This material showed a clear anticoagulant effect when compared with unmodified


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Cladophora nanocellulose.18 The total reduction of the remaining aldehyde groups did not drastically modify the structure of the RSDAC beads compared to the SDAC beads but it was necessary for a possible application as an immunosorbent material, as the aldehyde groups are highly prone to reaction with proteins present in biological systems.17

Scheme1. Chemical modifications of Cladophora nanocellulose.17

The SEM images in Figure 1 show the morphology and surface structures of the different materials. The spherical shape acquired during periodate oxidation was preserved through all the subsequent reactions but the porosity of the surface was considerably affected by the modifications, with sulfonation promoting a significant increase in the porosity of the beads, as discussed below. The smooth, compact surfaces observed in Figure 1 (b) and (c) can be attributed to loss of crystallinity and formation of hemiacetal bonds. The porosity of the samples in Figure 1 (d) – (f) is the result of the introduction of sulfonate groups that created surface charges which made the fibers repel each other; there is a clear reduction in the porosity with the reduction of the aldehyde moieties to hydroxyl groups.


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1µm

Figure 1. SEM micrographs of: a) Cladophora nanocellulose, b) DAC, c) RDAC, d) SDAC12, e) SDAC25, f) SDAC50, g) RSDAC12, h) RSDAC25, i) RSDAC50.

In order to observe how sulfonation affected the surface of the beads, which is relevant to their potential interactions with proteins in biological systems, a detailed study was performed. Table 1 shows relevant properties of the materials. Pycnometry analysis showed an increase in the


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specific density from the unmodified nanocellulose with a density of 1.57 g cm-3 to 1.64 g cm-3 for the DAC beads, which can be explained by variations in the packing of the cellulose chains with the loss of crystallinity. The SDAC beads showed slightly lower specific density values, which correlated with the degree of sulfonation, but no significant variation was observed for the RSDAC materials. Alteration of charge can render bioinert materials bioactive, as shown by Hua et al.25 in a study where the response from the studied cell lines varied with the surface charges on membranes produced from Cladophora nanocellulose. The charge properties of the surface of the materials showed a strong relation with the degree of sulfonation, as observed in the ζ-potential and surface-charged groups, and also showed, as expected, that the reduction did not alter the charges derived from the sulfonate groups. Finally, the surface area and total pore volume data obtained in nitrogen adsorption-desorption experiments also exhibited direct proportionality with the degree of sulfonation but no clear effect was observed with the reduction reaction. Interestingly, the surface area decreased almost tenfold with periodate oxidation producing a very smooth surface on more dense beads, when compared to the unmodified nanocellulose, and increased again drastically after sulfonation.


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Table 1. Physicochemical properties of the materials CN

DAC

RDAC SDAC12

SDAC25

SDAC50

RSDAC12

RSDAC25

RSDAC50

Specific density 1.57 ± 1.64 ± 1.68 ± 0.02 0.11 0.05 (g cm-3)

1.60 ± 0.09

1.58 ± 0.05

1.58 ± 0.10

1.61 ± 0.07

1.61 ± 0.04

1.59 ± 0.11

Surfacecharged groups 32 ± 7 31 ± 5 (µmol g−1)

40 ± 4

148 ± 8

240 ± 7

490 ± 7

160 ± 12

255 ± 10

488 ± 9

ζ-potential at pH 6.5 (mV)

-7 ± 2 -10 ± 1 -11 ± 3

-13 ± 2

-18 ± 3

-29 ± 5

-11 ± 2

-19 ± 5

-27 ± 2

Specific surface area (m2 g-1)

95 ± 2 10 ± 1

12 ± 2

56 ± 4

90 ± 3

100 ± 2

50 ± 3

84 ± 2

90 ± 3

Total pore volume (cm3 g−1)

0.44

0.10

0.15

0.21

0.25

0.27

0.12

0.20

0.22

Bead d50 size in aq. suspension (µm)

-

13 ± 8

12 ± 3

14 ± 2

15 ± 2

15 ± 6

15 ± 4

15 ± 3

17 ± 5

The pore size distribution showed an increase in the size of the pores in the sulfonated samples (ranging from 20 to 60 nm) compared to the unmodified Cladophora nanocellulose (8 to 20 nm; Figure 2). The figure inset shows the augmentation of the size of the pores with increased degrees of sulfonation. If the pores in the sulfonated beads are in the mesoporous range and the porosity of the beads can be tailored, protein retention systems based on size exclusion is a potential application for these materials.


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1.0

dV/dlog(w) Pore Volume (cm g )

1.5

Cladopora nanocellulose DAC SDAC12 SDAC25 SDAC50 RSDAC12 RSDAC25 RSDAC50

-1 3 )-1 dV/dlog(w) Pore Volume (cm3 g-1 nm

-1 -1

2.0

3

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3 -1 dV/dlog(w) PorePore Volume (cm g dV/dlog(w) Volume (cmnmg ))

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0.75

0.50

RSDAC25

RSDAC12

RSDAC50

0.25

0.00 10

Pore Width (nm)

0.5

0.0 10

Pore Width (nm)

100

Figure 2. Pore size distribution in the cellulose materials. The inset shows the increase in size of the pores with higher degrees of sulfonation. The thermal profile of the materials was also evaluated by thermogravimetry. The curves presented in Figure 3a show a very marked difference between DAC and the other materials, with an increase in thermal stability with the modifications to the DAC beads. Three main stages of mass loss are described in the literature: physisorbed water molecules are lost at temperatures below 100 °C, O atoms are lost at 300 °C, and degradation of the polymer backbone occurs at higher temperatures.26 The various endothermic events comprising mass loss for the DAC material are shown in Figure 3b as derivative thermogravimetry (DTG), where a single sharp decomposition around 380 °C occurs for the sulfonated beads. This result could be caused by the weaker intermolecular bonds in the DAC material, decreasing its thermal stability.


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There were no significant differences between SDAC and RSDAC materials; the mass of the sulfonated beads was reduced more than that of the DAC material because of decomposition of the sulfonated groups.

100 80 60 40

0.5

b

0.0

-(dm/dT) (mg °C-1)

DAC SDAC25 SDAC50 RSDAC50

a

weight loss (w%)

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

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20

-0.5 -1.0 -1.5 -2.0 -2.5

DAC SDAC25 SDAC50 RSDAC50

-3.0 -3.5

0 100

200

300

400

500

600

700

800

100

200

300

400

500

600

700

800

temperature (°C)

temperature (°C)

Figure 3. Thermogravimetric curves of samples: (a) TGA, (b) DTG. Raman spectroscopy was performed in order to verify the formation of the sulfonated moieties and further reduction of the aldehyde groups to hydroxyl groups. Figure 4 shows Raman shifts in the region between 1200-800 cm-1 caused by characteristic groups of cellulose materials and vibrations of the sulfonate groups. The bands at 1066 and 885 cm-1 correspond to the stretching modes of O=S=O and C–O–S, respectively, confirming the insertion of sulfonated groups onto the material. Additionally, a bathochromic shift was observed for both bands with increasing degrees of sulfonation, as has previously been reported for sulfated cellulose.27


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RSDAC50

SDAC50

Intensity (AU)

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

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SDAC25 1066 cm-1 825 cm-1

DAC

Cladophora nanocellulose

1095 cm-1 1123 cm-1 1152 cm-1

1200

1100

1000

900

800

-1

Raman shift (cm ) Figure 4. Raman spectra of the analyzed samples


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Conclusions Sulfonation and reduction of the DAC beads resulted in preservation of their spherical shape but some physicochemical properties were altered. Raman spectroscopy was shown to be a valuable tool for evaluating the modifications. The mesoporous structure of the SDAC and RSDAC beads could be tailored by varying the degree of sulfonation and the size of the pores makes them promising candidates for protein retention.

ASSOCIATED CONTENT AUTHOR INFORMATION Corresponding Author *[email protected] Author Contributions All authors contributed to the writing of the manuscript and have given approval for the final version.

ACKNOWLEDGMENTS The Bo Rydin Foundation and The Olle Engkvist Byggmästare Foundation are gratefully acknowledged for their financial support. I.R. thanks the Brazilian Ministry of Education and the CAPES agency for financial support.


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Spectroscopic and Physicochemical Characterization of Sulfonated

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