Swelling and mechanical properties of alginate hydrogels with respect to promotion of neural growth

Tissue Engineering - Part C: Methods

Volumn 20, Issue 5, 2014, Pages 401-411

  Matyash, Marina ^a,b   Despang, Florian ^a   Ikonomidou, Chrysanthy ^c   Gelinsky, Michael ^a  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^c UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALGINATE; CALCIUM; GELATION; IONIC STRENGTH; MECHANICAL STABILITY; NEURONS; SODIUM CHLORIDE; STIFFNESS; STIFFNESS MATRIX; THREE DIMENSIONAL;

ALGINATE HYDROGELS; HIGH IONIC STRENGTH; IONIC CROSS-LINKS; MOLECULAR COMPOSITIONS; NEURAL REGENERATION; NEURITE OUTGROWTH; PHYSIOLOGICAL SALINE; VOLUME STABILITY;

HYDROGELS;

ALGINIC ACID; CALCIUM ALGINATE; CALCIUM ION; SODIUM CHLORIDE; BUFFER; CALCIUM CHLORIDE; GLUCURONIC ACID; HEXURONIC ACID; HYDROGEL; SOLUTION AND SOLUBILITY;

AQUEOUS SOLUTION; ARTICLE; GELATION; HYDROGEL; IN VIVO STUDY; IONIC STRENGTH; NERVE FIBER GROWTH; PH; PRIORITY JOURNAL; THREE DIMENSIONAL IMAGING; YOUNG MODULUS; ANIMAL; BRAIN CORTEX; CELL CULTURE; CELL PROLIFERATION; CYTOLOGY; DRUG EFFECTS; FLOW KINETICS; HUMAN; MECHANICS; METABOLISM; NERVE CELL; NEURITE; PHARMACOLOGY; SOLUTION AND SOLUBILITY; WISTAR RAT;

ALGINATES; ANIMALS; BUFFERS; CALCIUM CHLORIDE; CELL PROLIFERATION; CELLS, CULTURED; CEREBRAL CORTEX; ELASTIC MODULUS; GLUCURONIC ACID; HEXURONIC ACIDS; HUMANS; HYDROGELS; MECHANICAL PHENOMENA; NEURITES; NEURONS; RATS, WISTAR; RHEOLOGY; SODIUM CHLORIDE; SOLUTIONS;

EID: 84899507251     PISSN: 19373384     EISSN: 19373392     Source Type: Journal    
DOI: 10.1089/ten.tec.2013.0252     Document Type: Article

References (65)

1. Straley, K.S., Foo, C.W., and Heilshorn, S.C. Biomaterial design strategies for the treatment of spinal cord injuries. J Neurotrauma 27, 1, 2010.
2. Wang, S., and Cai, L. Polymer gel system for nerve repair and regeneration. In: Kulshrestha, A., ed. Chapter 3 in Biomaterials, ACS Symposium Series. Washington, DC: American Chemical Society, 2010, pp. 43-63.
3. Li, G.N., and Hoffman-Kim, D. Tissue-engineered platforms of axon guidance. Tissue Eng Part B Rev 14, 33, 2008.
4. Subramanian, A., Krishnan, U.M., and Sethuraman, S. Development of biomaterial scaffold for nerve tissue engineering: biomaterial mediated neural regeneration. J Biomed Sci 16, 108, 2009.
5. Haug, A., and Larsen, B. Biosynthesis of alginate: Part II. Polymannuronic acid C-5-epimerase from Azotobacter vinelandii (Lipman). Carbohydr Res 17, 297, 1971.
6. Smidsrød, O., Glover, R.M., and Whittington, S.G. The relative extension of alginates having different chemical composition. Carbohydr Res 27, 107, 1973.
7. Draget, K.I., Smidsrød, O., and Skjåk-Braek, G. Alginates from algae. In: Steinbüchel, A., and Rhee, S.K., eds. Polysaccharides and Polyamides in the Food Industry. Properties, Production, and Patents. Weinheim: WILEY-VCH, 2005, pp. 1-30.
8. Evans, L.R., and Linker, A. Production and characterization of the slime polysaccharide of Pseudomonas aeruginosa. J Bacteriol 116, 915, 1973.
9. Panikkar, R., and Brasch, D.J. Composition and block structure of alginates from New Zealand brown seaweeds. Carbohydr Res 293, 119, 1996.
10. Morris, E., Rees, D., Thom, D., and Boyd, J. Chiroptical and stoichiometric evidence of a specific, primary dimerisation process in alginate gelation. J Carbohydr Res 66, 145, 1978.
11. Grant, G., Morris, E., Rees, D., Smith, P., and Thom, D. Biological interactions between polysaccharides and divalent cations: the egg-box model. FEBS Lett 32, 195, 1973.
12. Jorgensen, T.E., Sletmoen, M., Draget, K.I., and Stokke, B.T. Influence of oligoguluronates on alginate gelation, kinetics, and polymer organization. Biomacromolecules 8, 2388, 2007.
13. Rees, D.A. Polysaccharide shapes and their interactions- some recent advances. Pure Appl Chem 53, 1, 1981.
14. Stokke, B.T., Smidsrød, O., Bruheim, P., and Skjåk-Braek, G. Distribution of uronate residues in alginate chains in relation to alginate gelling properties. Macromolecules 24, 4637, 1991.
15. Netz, R.R., and Andelman, D. Polyelectrolytes in solution and at surfaces. In: Urbakh, M., and Giladi, E., eds. Encyclopedia of Electrochemistry. Weinheim: Wiley-VCH, 2002, pp. 282-322.
16. Dobrynin, A.V., and Rubinstein, M. Theory of polyelectrolytes in solutions and at surfaces. Prog Polym Sci 30, 1049, 2005.
17. LeRoux, M.A., Guilak, F., and Setton, L.A. Compressive and shear properties of alginate gel: effects of sodium ions and alginate concentration. J Biomed Mater Res 47, 46, 1999.
18. Martinsen, A., Skjak-Braek, G., and Smidsrod, O. Alginate as immobilization material: I. Correlation between chemical and physical properties of alginate gel beads. Biotechnol Bioeng 33, 79, 1989.
19. Draget, K.I., Steinsvag, K., Onsoyen, E., and Smidsrod, O. Na- and K-alginate; effect on Ca2 + -gelation. Carbohydr Polym 35, 1, 1998.
20. Kuo, C.K., and Ma, P.X. Maintaining dimensions and mechanical properties of ionically crosslinked alginate hydrogel scaffolds in vitro. J Biomed Mater Res A 84, 899, 2008.
21. Fang, Y., Al-Assaf, S., Phillips, G.O., Nishinari, K., Funami, T., Williams, P.A., and Li, L. Multiple steps and critical behaviors of the binding of calcium to alginate. J Phys Chem B 111, 2456, 2007.
22. Kuo, C.K., and Ma, P.X. Ionically crosslinked alginate hydrogels as scaffolds for tissue engineering: part 1. Structure, gelation rate and mechanical properties. Biomaterials 22, 511, 2001.
23. Kong, H.J., Smith, M.K., and Mooney, D.J. Designing alginate hydrogels to maintain viability of immobilized cells. Biomaterials 24, 4023, 2003.
24. Birdi, G., Bridson, R.H., Smith, A.M., Bohari, S.P., and Grover, L.M. Modification of alginate degradation properties using orthosilicic acid. J Mech Behav Biomed Mater 6, 181, 2012.
25. Jejurikar, A., Seow, T.X., Lawrie, G., Martin, D., Jayakrishnan, A., and Grøndahl, L. Degradable alginate hydrogels crosslinked by the macromolecular crosslinker alginate dialdehyde. J Mater Chem 22, 9751, 2012.
26. Gattas-Asfura, K.M., and Stabler, C.L. Chemoselective crosslinking and functionalization of alginate via Staudinger ligation. Biomacromolecules 10, 3122, 2009.
27. Discher, D.E., Janmey, P., and Wang, Y.L. Tissue cells feel and respond to the stiffness of their substrate. Science 310, 1139, 2005.
28. Levental, I., Georges, P.C., and Janmey, P.A. Soft biological materials and their impact on cell function. Soft Matter 3, 299, 2007.
29. Matyash, M., Despang, F., Mandal, R., Fiore, D., Gelinsky, M., and Ikonomidou, C. Novel soft alginate hydrogel strongly supports neurite growth and protects neurons against oxidative stress. Tissue Eng Part A 18, 55, 2012.
30. Jiang, F. X., Yurke, B., Schloss, R. S., Firestein, B. L., and Langrana, N. A. Effect of dynamic stiffness of the substrates on neurite outgrowth by using a DNA-crosslinked hydrogel. Tissue Eng Part A 16, 1873, 2010.
31. Koch, D., Rosoff, W.J., Jiang, J., Geller, H.M., and Urbach, J.S. Strength in the periphery: growth cone biomechanics and substrate rigidity response in peripheral and central nervous system neurons. Biophys J 102, 452, 2012.
32. Previtera, M.L., Langhammer, C.G., and Firestein, B.L. Effects of substrate stiffness and cell density on primary hippocampal cultures. J Biosci Bioeng 110, 459, 2010.
33. Jiang, F.X., Yurke, B., Firestein, B.L., and Langrana, N.A. Neurite outgrowth on a DNA crosslinked hydrogel with tunable stiffnesses. Ann Biomed Eng 36, 1565, 2008.
34. Engler, A.J., Sen, S., Sweeney, H.L., and Discher, D.E. Matrix elasticity directs stem cell lineage specification. Cell 126, 677, 2006.
35. Leipzig, N.D., and Shoichet, M.S. The effect of substrate stiffness on adult neural stem cell behavior. Biomaterials 30, 6867, 2009.
36. Saha, K., Keung, A.J., Irwin, E.F., Li, Y., Little, L., Schaffer, D.V., and Healy, K.E. Substrate modulus directs neural stem cell behaviour. Biophys J 95, 4426, 2009.
37. Seidlits, S.K., Khaing, Z.Z., Petersen, R.R., Nickels, J.D., Vanscoy, J.E., Shear, J.B., and Schmidt, C.E. The effects of hyaluronic acid hydrogels with tunable mechanical properties on neural progenitor cell differentiation. Biomaterials 31, 3930, 2010.
38. Novikova, L.N., Mosahebi, A., Wiberg, M., Terenghi, G., Kellerth, J.O., and Novikov, L.N. Alginate hydrogel and matrigel as potential cell carriers for neurotransplantation. J Biomed Mater Res A 77, 242, 2006.
39. Dhoot, N.O., Tobias, C.A., Fischer, I., and Wheatley, M.A. Peptide-modified alginate surfaces as a growth permissive substrate for neurite outgrowth. J Biomed Mater Res A 71, 191, 2004.
40. Yamada, Y., Hozumi, K., Katagiri, F., Kikkawa, Y., and Nomizu, M. Biological activity of laminin peptideconjugated alginate and chitosan matrices. Biopolymers 94, 711, 2010.
41. Ohta, M., Suzuki, Y., Chou, H., Ishikawa, N., Suzuki, S., Tanihara, M., Mizushima, Y., Dezawa, M., and Ide, C. Novel heparin/alginate gel combined with basic fibroblast growth factor promotes nerve regeneration in rat sciatic nerve. J Biomed Mater Res A 71, 661, 2004.
42. Suzuki, Y., Tanihara, M., Ohnishi, K., Suzuki, K., Endo, K., and Nishimura, Y. Cat peripheral nerve regeneration across 50 mm gap repaired with a novel nerve guide composed of freeze-dried alginate gel. Neurosci Lett 259, 75, 1999.
43. Suzuki, Y., Kitaura, M., Wu, S., Kataoka, K., Suzuki, K., Endo, K., Nishimura, Y., and Ide, C. Electrophysiological and horseradish peroxidase-tracing studies of nerve regeneration through alginate-filled gap in adult rat spinal cord. Neurosci Lett 318, 121, 2002.
44. Kataoka, K., Suzuki, Y., Kitada, M., Hashimoto, T., Chou, H., Bai, H., Ohta, M., Wu, S., Suzuki, K., and Ide, C. Alginate enhances elongation of early regenerating axons in spinal cord of young rats. Tissue Eng 10, 493, 2004.
45. Prang, P., Muller, R., Eljaouhari, A., Heckmann, K., Kunz, W., Weber, T., Faber, C., Vroemen, M., Bogdahn, U., and Weidner, N. The promotion of oriented axonal regrowth in the injured spinal cord by alginate-based anisotropic capillary hydrogels. Biomaterials 27, 3560, 2006.
46. Pawar, K., Müller, R., Caioni, M., Prang, P., Bogdahn, U., and Kunz, W. Increasing capillary diameter and the incorporation of gelatin enhance axon outgrowth in alginatebased anisotropic hydrogels. Acta Biomater 7, 2826, 2011.
47. Grasdalen, H., Larsen, B., and Smidsrod, O. A P.M.R. study of the composition and sequence of uronate residues in alginates. Carbohydr Res 68, 23, 1979.
48. Ebert, A.D., McMillan, E.L., and Svendsen, C.N. Isolating, expanding and infecting human and rodent fetal neural progenitor cells. Curr Protoc Stem Cell Biol Chapter 2:Unit 2D.2, 2008.
49. Freund, J., and Kalbitzer, H.R. Physiological buffers for NMR spectroscopy. J Biomol NMR 5, 321, 1995.
50. Pirke, K.M., Wisser, H., and Mertin, J. Die Konzentrationen von Natrium, Kalium, Calcium, Magnesium und Chlorid im Liquor cerebrospinalis und ihre Beziehungen zu den Serumkonzentrationen. Clin Chem Lab Med 10, 462, 1972.
51. Draget, K., Ostgaard, K., and Smidsrod, O. Homogeneous alginate gels-a technical approach. Carbohydr Polym 14, 159, 1990.
52. Elkin, B.S., Azeloglu, E.U., Costa, K.D., and Morrison, B. Mechanical heterogeneity of the rat hippocampus measured by atomic force microscope indentation. J Neurotrauma 24, 812, 2007.
53. Green, M.A., Bilston, L.E., and Sinkus, R. In vivo brain viscoelastic properties measured by magnetic resonance elastography. NMR Biomed 21, 755, 2008.
54. Christ, A.F., Franze, K., Gautier, H., Moshayedi, P., Fawcett, J., Franklin, R.J., Karadottir, R.T., and Guck, J. Mechanical difference between white and gray matter in the rat cerebellum measured by scanning force microscopy. J Biomech 43, 2986, 2010.
55. Solon, J., Levental, I., Sengupta, K., Georges, P.C., and Janmey, P.A. Fibroblast adaptation and stiffness matching to soft elastic substrates. Biophys J 93, 4453, 2007.
56. Rhiner, C., and Hengartner, M.O. Sugar antennae for guidance signals: syndecans and glypicans integrate directional cues for navigating neurons. Sci World J 6, 1024, 2006.
57. Frischknecht, R., and Seidenbecher, C.I. The crosstalk of hyaluronan-based extracellular matrix and synapses. Neuron Glia Biol 4, 249, 2008.
58. Purushothaman, A., Sugahara, K., and Faissner, A. Chondroitin sulfate ''wobble motifs'' modulate maintenance and differentiation of neural stem cells and their progeny. J Biol Chem 287, 2935, 2012.
59. Kawada, A., Hiura, N., Shiraiwa, M., Tajima, S., Hiruma, M., Hara, K., Ishibashi, A., and Takahara, H. Stimulation of human keratinocyte growth by alginate oligosaccharides, a possible co-factor for epidermal growth factor in cell culture. FEBS Lett 408, 43, 1997.
60. Kawada, A., Hiura, N., Tajima, S., and Takahara, H. Alginate oligosaccharides stimulate VEGF-mediated growth and migration of human endothelial cells. Arch Dermatol Res 291, 542, 1999.
61. Tajima, S., Inoue, H., Kawada, A., Ishibashi, A., Takahara, H., and Hiura, N. Alginate oligosaccharides modulate cell morphology, cell proliferation and collagen expression in human skin fibroblasts in vitro. Arch Dermatol Res 291, 432, 1999.
62. Yamamoto, Y., Kurachi, M., Yamaguchi, K., and Oda, T. Induction of multiple cytokine secretion from RAW264.7 cells by alginate oligosaccharides. Biosci Biotechnol Biochem 71, 238, 2007.
63. Pasquali, P., Zalcman, A., Murtas, S., Adone, R., Brambilla, G., Marianelli, C., Cagiola, M., and Ciuchini, F. In vitro stimulation of murine peritoneal monocytes induced by alginates. Arch Pharm Res 28, 936, 2005.
64. Silva, G.A., Czeisler, C., Niece, K.L., Beniash, E., Harrington, D.A., Kessler, J.A., and Stupp, S.I. Selective differentiation of neural progenitor cells by high-epitope density nanofibers. Science 303, 1352, 2004.
65. Cai, L., Lu, J., Sheen, V., and Wang, S. Optimal poly(L-lysine) grafting density in hydrogels for promoting neural progenitor cell functions. Biomacromolecules 13, 1663, 2012.