Biodegradable hydrogels composed of oxime crosslinked poly(ethylene glycol), hyaluronic acid and collagen: A tunable platform for soft tissue engineering

Journal of Biomaterials Science, Polymer Edition

Volumn 26, Issue 3, 2015, Pages 143-161

  Hardy, John G ^a,b   Lin, Phillip ^b   Schmidt, Christine E ^a,b  

^a J Crayton Pruitt Family Department of Biomedical Engineering   (United States)

^b The University of Texas at Austin   (United States)

Author keywords

biodegradable; biomaterials; biomimetic mechanical properties; central nervous system; in vitro cell culture; injectable hydrogels; peripheral nervous system; tissue engineering

Indexed keywords

BIOLOGICAL MATERIALS; BIOMATERIALS; BIOMECHANICS; BIOMIMETICS; CELL ADHESION; CELL CULTURE; CELL ENGINEERING; CELLS; COLLAGEN; CROSSLINKING; CYTOLOGY; HYALURONIC ACID; MANGANESE; MECHANICAL PROPERTIES; NEURONS; NEUROPHYSIOLOGY; ORGANIC ACIDS; POLYETHYLENE GLYCOLS; POLYOLS; SCAFFOLDS (BIOLOGY); STEM CELLS; TISSUE; TISSUE ENGINEERING;

BIODEGRADABLE; CENTRAL NERVOUS SYSTEMS; IN-VITRO; INJECTABLE HYDROGELS; PERIPHERAL NERVOUS SYSTEM;

HYDROGELS;

ALDEHYDE; BIOMATERIAL; COLLAGEN TYPE 1; HYALURONIC ACID; MACROGOL; OXIME; COLLAGEN; HYDROGEL; MACROGOL DERIVATIVE;

ARTICLE; BIOCHEMICAL COMPOSITION; BIODEGRADABILITY; CELL CULTURE; CELL VIABILITY; CENTRAL NERVOUS SYSTEM; CLICK CHEMISTRY; CONTROLLED STUDY; CROSS LINKING; CYTOTOXICITY; HUMAN; HUMAN CELL; HYDROGEL; MAMMAL CELL; MESENCHYMAL STEM CELL; MOLECULAR MECHANICS; PERIPHERAL NERVOUS SYSTEM; POLYMERIZATION; SCHWANN CELL; SOFT TISSUE; TISSUE ENGINEERING; ANIMAL; BIODEGRADABLE IMPLANT; CARBON NUCLEAR MAGNETIC RESONANCE; CELL ADHESION; CELL SURVIVAL; CHEMICAL STRUCTURE; CHEMISTRY; DEVICES; DRUG EFFECTS; INFRARED SPECTROSCOPY; MATERIALS TESTING; MESENCHYMAL STROMA CELL; PHYSIOLOGY; PROTON NUCLEAR MAGNETIC RESONANCE; RAT; SCIATIC NERVE; SYNTHESIS; TISSUE SCAFFOLD;

ABSORBABLE IMPLANTS; ANIMALS; CARBON-13 MAGNETIC RESONANCE SPECTROSCOPY; CELL ADHESION; CELL SURVIVAL; COLLAGEN; HUMANS; HYALURONIC ACID; HYDROGELS; MATERIALS TESTING; MESENCHYMAL STROMAL CELLS; MOLECULAR STRUCTURE; OXIMES; POLYETHYLENE GLYCOLS; PROTON MAGNETIC RESONANCE SPECTROSCOPY; RATS; SCHWANN CELLS; SCIATIC NERVE; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; TISSUE ENGINEERING; TISSUE SCAFFOLDS;

EID: 84920439986     PISSN: 09205063     EISSN: 15685624     Source Type: Journal    
DOI: 10.1080/09205063.2014.975393     Document Type: Article

References (95)

1. Slaughter BV, Khurshid SS, Fisher OZ, Khademhosseini A, Peppas NA. Hydrogels in regenerative medicine. Adv. Mater. 2009; 21: 3307-3329.
2. Rahman CV, Saeed A, White LJ, Gould TWA, Kirby GTS, Sawkins MJ, Alexander C, Rose FRAJ, Shakesheff KM. Chemistry of polymer and ceramic-based injectable scaffolds and their applications in regenerative medicine. Chem. Mater. 2012; 24: 781-784.
3. Bae KH, Wang LS, Kurisawa M. Injectable biodegradable hydrogels: progress and challenges. J. Mater. Chem. B. 2013; 1: 5371-5388.
4. Van Tomme SR, Storm G, Hennink WE. In situ gelling hydrogels for pharmaceutical and biomedical applications. Int. J. Pharm. 2008; 355: 1-18.
5. Barner-Kowollik C, Du Prez FE, Espeel P, Hawker CJ, Junkers T, Schlaad H, Van Camp W. "Clicking" polymers or just efficient linking: what is the difference? Angew. Chem. Int. Ed. 2011; 50: 60-62.
6. Iha RK, Wooley KL, Nystrom AM, Burke DJ, Kade MJ, Hawker CJ. Applications of orthogonal "click" chemistries in the synthesis of functional soft materials. Chem. Rev. 2009; 109: 5620-5686.
7. OReilly RK, Joralemon MJ, Hawker CJ, Wooley KL. Preparation of orthogonally-functionalized core Click cross-linked nanoparticles. New J. Chem. 2007; 31: 718-724.
8. Lallana E, Fernandez-Trillo F, Sousa-Herves A, Riguera R, Fernandez-Megia E. Click chemistry with polymers, dendrimers, and hydrogels for drug delivery. Pharm. Res. 2012; 29: 902-921.
9. Vermonden T, Censi R, Hennink WE. Hydrogels for protein delivery. Chem. Rev. 2012; 112: 2853-2888.
10. Malkoch M, Vestberg R, Gupta N, Mespouille L, Dubois P, Mason AF, Hedrick JL, Liao Q, Frank CW, Kingsbury K, Hawker CJ. Synthesis of well-defined hydrogel networks using Click chemistry. Chem. Commun. 2006; 26: 2774-2776.
11. Jiang Y, Chen J, Deng C, Suuronen EJ, Zhong Z. Click hydrogels, microgels and nanogels: emerging platforms for drug delivery and tissue engineering. Biomaterials. 2014; 35: 4969-4985.
12. Lowe AB, Hoyle CE, Bowman NC. Thiol-yne click chemistry: a powerful and versatile methodology for materials synthesis. J. Mater. Chem. 2010; 20: 4745-4750.
13. van Dijk M, Rijkers DTS, Liskamp RMJ, van Noostrum CF, Hennink HE. Synthesis and applications of biomedical and pharmaceutical polymers via click chemistry methodologies. Bioconjugate Chem. 2009; 20: 2001-2016.
14. Nimmo CM, Shoichet MS. Regenerative biomaterials that "click": simple, aqueous-based protocols for hydrogel synthesis, surface immobilization, and 3D patterning. Bioconjugate Chem. 2011; 22: 2199-2209.
15. Alge DL, Azagarsamy MA, Donohue DF, Anseth KS. Synthetically tractable click hydrogels for three-dimensional cell culture formed using tetrazine-norbornene chemistry. Biomacromolecules. 2013; 14: 949-953.
16. Yigit S, Sanyal R, Sanyal A. Fabrication and functionalization of hydrogels through "click" chemistry. Chem. Asian J. 2011; 6: 2648-2659.
17. Ulinuc A, Popa M, Hamaide T, Dobromir M. New approaches in hydrogel synthesis-click chemistry. Cellul. Chem. Technol. 2012; 46: 1-11.
18. Sun J, Tan H. Alginate-based biomaterials for regenerative medicine applications. Materials. 2013; 6: 1285-1309.
19. Elchinger PH, Faugeras PA, Boëns B, Brouillette F, Montplaisir D, Zerrouki R, Lucas R. Polysaccharides: the "click" chemistry impact. Polymers. 2011; 3: 1607-1651.
20. Piluso S, Hiebl B, Gorb SN, Kovalev A, Lendlein A, Neffe AT. Hyaluronic acid-based hydrogels crosslinked by copper-catalyzed azide-Alkyne cycloaddition with tailorable mechanical properties. Int. J. Artif. Organs. 2011; 34: 192-197.
21. Hua X, Li D, Zhou F, Gao C. Biological hydrogel synthesized from hyaluronic acid, gelatin and chondroitin sulfate by click chemistry. Acta Biomater. 2011; 7: 1618-1626.
22. Hachet E, Sereni N, Pignot-Paintrand I, Ravaine R, Szarpak-Jankowska A, Auzély-Velty R. Thiol-ene clickable hyaluronans: from macro-to nanogels. J. Coll. Int. Sci. 2014; 419: 52-55.
23. Li Y, Wang L, Wu J, Ma Y, Wang J, Wang Y, Luo Y. Poly(vinyl alcohol) and hyaluronic acid derived hydrogel: a novel synthesis method using thiol-yne click reaction. Mater. Lett. 2014; 134: 9-12.
24. Gramlich WM, Kim IL, Burdick JA. Synthesis and orthogonal photopatterning of hyaluronic acid hydrogels with thiol-norbornene chemistry. Biomaterials. 2013; 34: 9803-9811.
25. Owen SC, Fisher SA, Tam RY, Nimmo CM, Shoichet MS. Hyaluronic acid click hydrogels emulate the extracellular matrix. Langmuir. 2013; 29: 7393-7400.
26. Yu F, Cao X, Li Y, Zeng L, Yuan B, Chen F. An injectable hyaluronic acid/PEG hydrogel for cartilage tissue engineering formed by integrating enzymatic crosslinking and Diels-Alder "click chemistry". Polym. Chem. 2014; 5: 1082-1090.
27. Jin R, Moreira Teixeira LS, Krouwels A, Dijkstra PJ, van Blitterswijk CA, Karperien M, Feijen J. Synthesis and characterization of hyaluronic acid-poly(ethylene glycol) hydrogels via Michael addition: an injectable biomaterial for cartilage repair. J. Acta Biomater. 2010; 6: 1968-1677.
28. Ganguly T, Kasten BB, Bucar DK, MacGillivray LR, Berkman CE, Benny PD. The hydrazide/hydrazone click reaction as a biomolecule labeling strategy for M(CO) 3 (M = Re, (99m)Tc) radiopharmaceuticals. Chem. Commun. 2011; 47: 12846-12848.
29. Grover GN, Lam J, Nguyen TH, Segura T, Maynard HD. Biocompatible hydrogels by oxime Click chemistry. Biomacromolecules. 2012; 13: 3013-3017.
30. Novoa-Carballal R, Muller AHE. Synthesis of polysaccharide-b-PEG block copolymers by oxime click. Chem. Commun. 2012; 48: 3781-3783.
31. Ulrich S, Boturyn D, Marra A, Renaudet O, Dumy P. Oxime ligation: a chemoselective click-type reaction for accessing multifunctional biomolecular constructs. Chem. Eur. J. 2014; 20: 34-41.
32. Thavarajah R, Mudimbaimannar VK, Elizabeth J, Rao UK, Ranganathan K. Chemical and physical basics of routine formaldehyde fixation. J. Oral Maxillofac. Pathol. 2012; 16: 400-405.
33. Dalle-Donne I, Carini M, Orioli M, Vistoli G, Regazzoni L, Colombo G, Rossi R, Milzani A, Aldini G. Protein carbonylation: 2,4-dinitrophenylhydrazine reacts with both aldehydes/ketones and sulfenic acids. Free Radical Biol. Med. 2009; 46: 1411-1419.
34. Hahne H, Neubert P, Kuhn K, Etienne C, Bomgarden R, Rogers JC, Kuster B. Carbonyl-reactive tandem mass tags for the proteome-wide quantification of N-linked glycans. Anal. Chem. 2012; 84: 3716-3724.
35. Corbett PT, Leclaire J, Vial L, West KR, Wietor JL, Sanders JKM, Otto S. Dynamic combinatorial chemistry. Chem. Rev. 2006; 106: 3652-3711.
36. Lehn JM. From supramolecular chemistry towards constitutional dynamic chemistry and adaptive chemistry. Chem. Soc. Rev. 2007; 36: 151-160.
37. Schmidt CE, Leach JB. Neural tissue engineering: strategies for repair and regeneration. Annu. Rev. Biomed. Eng. 2003; 5: 293-347.
38. Zhong YH, Bellamkonda RV. Biomaterials for the central nervous system. J. R. Soc. Interface. 2008; 5: 957-975.
39. Bellamkonda RV, Pai SB, Renaud P. Materials for neural interfaces. MRS Bull. 2012; 37: 557-561.
40. Webster R, Didier E, Harris P, Siegel N, Stadler J, Tilbury L, Smith D. PEGylated proteins: evaluation of their safety in the absence of definitive metabolism studies. Drug Metab. Dispos. 2007; 35: 9-16.
41. Hudson SP, Langer R, Fink GR, Kohane DS. Injectable in situ cross linking hydrogels for local antifungal therapy. Biomaterials. 2010; 31: 1444-1452.
42. Vercruysse KP, Marecak DM, Marecek JF, Prestwich GD. Synthesis and in vitro degradation of new polyvalent hydrazide cross-linked hydrogels of hyaluronic acid. Bioconjugate Chem. 1997; 8: 686-694.
43. Prestwich GD, Marecak DM, Marecek JF, Vercruysse KP, Ziebell MR. Controlled chemical modification of hyaluronic acid: synthesis, applications, and biodegradation of hydrazide derivatives. J. Controlled Release. 1998; 53: 93-103.
44. Jia XQ, Burdick JA, Kobler J, Clifton RJ, Rosowski JJ, Zeitels SM, Langer R. Structural analysis and mechanical characterization of hyaluronic acid-based doubly cross-linked networks. Macromolecules. 2004; 37: 3239-3248.
45. McKinnon DD, Domaille DW, Cha JN, Anseth KS. Biophysically defined and cytocompatible covalently adaptable networks as viscoelastic 3D cell culture systems. Adv. Mater. 2014; 26: 865-872.
46. Jia X, Yeo Y, Clifton RJ, Jiao T, Kohane DS, Kobler JB, Zeitels SM, Langer R. Hyaluronic acid-based microgels and microgel networks for vocal fold regeneration. Biomacromolecules. 2006; 7: 3336-3344.
47. Jha AK, Hule RA, Jiao T, Teller SS, Clifton RJ, Duncan RL, Pochan DJ, Jia X. Hyaluronic acid-based hydrogels: from a natural polysaccharide to complex networks. Macromolecules. 2009; 42: 537-546.
48. Prestwich GD, Kuo JW. Chemically-modified HA for therapy and regenerative medicine. Curr. Pharm. Biotechnol. 2008; 9: 242-245.
49. Burdick JA, Prestwich GD. Hyaluronic acid hydrogels for biomedical applications. Adv. Healthcare Mater. 2011; 23: H41-H56.
50. Collins MN, Birkinshaw C. Hyaluronic acid based scaffolds for tissue engineering-A review. Carbohydr. Polym. 2013; 92: 1262-1279.
51. Grover GN, Braden RL, Christman KL. Oxime cross-linked injectable hydrogels for catheter delivery. Adv. Mater. 2013; 25: 2937-2942.
52. Lin F, Yu JY, Tang W, Zheng JK, Defante A, Guo K, Wesdemiotis C, Becker ML. Peptide-functionalized oxime hydrogels with tunable mechanical properties and gelation behavior. Biomacromolecules. 2013; 14: 3749-3758.
53. Maheshwari G, Brown G, Lauffenburger DA, Wells A, Griffith LG. Cell adhesion and motility depend on nanoscale RGD clustering. J. Cell Sci. 2000; 113: 1677-1686.
54. Kim JP, Zhang K, Kramer RH, Schall TJ, Woodley DT. Interleukin-1α stimulates keratinocyte migration through an epidermal growth factor/transforming growth factor-α-independent pathway. J. Inv. Dermatol. 1992; 98: 764-770.
55. Cavalcant-Adam EA, Volberg T, Micoulet A, Kessler H, Geiger B, Spatz JP. Cell spreading and focal adhesion dynamics are regulated by spacing of integrin ligands. Biophys. J. 2007; 92: 2964-2974.
56. Selheuber-Unkei C, Erdmann T, Lopez-Garcia M, Kessler H, Schwartz US, Spatz JP. Cell adhesion strength is controlled by intermolecular spacing of adhesion receptors. Biophys. J. 2010; 98: 543-551.
57. Huang J, Grater SV, Corbellini F, Rinck-Jahnke S, Bock E, Kemkemer R, Kessler H, Ding J, Spatz JP. Impact of order and disorder in RGD nanopatterns on cell adhesion. Nano Lett. 2009; 9: 1111-1116.
58. Alvarado-Velez M, Pai SB, Bellamkonda RV. Hydrogels as carriers for stem cell transplantation. IEEE T. Bio-Med. Eng. 2014; 61: 1474-1481.
59. Dooley D, Vidal P, Hendrix S. Immunopharmacological intervention for successful neural stem cell therapy: New perspectives in CNS neurogenesis and repair. Pharmacol. Therapeut. 2014; 141: 21-31.
60. Yang N, Wernig M. Harnessing the stem cell potential: a case for neural stem cell therapy. Nat. Med. 2013; 19: 1580-1581.
61. Kim SU, de Vellis J. Stem cell-based cell therapy in neurological diseases: a review. J. Neurosci. Res. 2009; 87: 2183-2200.
62. Kim SU. Neural stem cell-based gene therapy for brain tumors. Stem Cell Rev. Rep. 2011; 7: 130-140.
63. Rossi F, Cattaneo E. Opinion: neural stem cell therapy for neurological diseases: dreams and reality. Nat. Rev. Neurosci. 2002; 3: 401-409.
64. Ourednik V, Ourednik J, Park KI, Snyder EY. Neural stem cells-A versatile tool for cell replacement and gene therapy in the central nervous system. Clin. Genet. 1999; 56: 267-278.
65. Grade S, Bernardino L, Malva JO. Oligodendrogenesis from neural stem cells: perspectives for remyelinating strategies. Int. J. Dev. Neurosci. 2013; 31: 692-700.
66. Patel AN, Genovese J. Potential clinical applications of adult human mesenchymal stem cell (Prochymal®) therapy. Stem Cells Cloning. 2011; 4: 61-72.
67. Li Y, Liu M, Yan Y, Yang S-H. Neural differentiation from pluripotent stem cells: the role of natural and synthetic extracellular matrix. World J. Stem Cells. 2014; 6: 11-23.
68. Euler de Souza Lucena EE, Guzen FP, Lopes de Paiva Cavalcanti JRL, Galvaõ Barboza CAG, Silva do Nascimento Júnior ES, de Sousa Cavalcante J. Experimental considerations concerning the use of stem cells and tissue engineering for facial nerve regeneration: a systematic review. J. Oral Maxillofac. Surg. 2014; 72: 1001-1012.
69. Xiong Y, Qu C, Mahmood A, Liu Z, Ning R, Li Y, Kaplan DL, Schallert T, Chopp M. Delayed transplantation of human marrow stromal cell-seeded scaffolds increases transcallosal neural fiber length, angiogenesis, and hippocampal neuronal survival and improves functional outcome after traumatic brain injury in rats. Brain Res. 2009; 1263: 183-191.
70. Qu C, Mahmood A, Liu XS, Xiong Y, Wang L, Wu H, Li B, Zhang ZG, Kaplan DL, Chopp M. The treatment of TBI with human marrow stromal cells impregnated into collagen scaffold: functional outcome and gene expression profile. Brain Res. 2011; 1371: 129-139.
71. Schlick TL, Ding ZB, Kovacs EW, Francis MB. Dual-surface modification of the tobacco mosaic virus. J. Am. Chem. Soc. 2005; 127: 3718-3723.
72. Marsano E, Gagliardi S, Ghioni F, Bianchi E. Behaviour of gels based on (hydroxypropyl) cellulose methacrylate. Polymer. 2000; 41: 7691-7698.
73. Flory PJ. Principles of polymer chemistry. Ithaca (NY): Cornell University Press; 1953.
74. Metters AT, Anseth KS, Bowman CN. Fundamental studies of biodegradable hydrogels as cartilage replacement materials. Biomed. Sci. Instrum. 1999; 35: 33-38.
75. Lee Y, Kim DN, Choi D, Lee W, Park J, Koh WG. Preparation of interpenetrating polymer network composed of poly(ethylene glycol) and poly(acrylamide) hydrogels as a support of enzyme immobilization. Polym. Adv. Technol. 2008; 19: 852-858.
76. Collins MN, Birkinshaw C. Investigation of the swelling behavior of crosslinked hyaluronic acid films and hydrogels produced using homogeneous reactions. J. Appl. Polym. Sci. 2008; 109: 923-931.
77. Cleland RL, Wang JL. Ionic polysaccharides. III. Dilute solution properties of hyaluronic acid fractions. Biopolymers. 1970; 9: 799-810.
78. Cleland RL. Ionic polysaccharides. IV. Free-rotation dimensions for disaccharide polymers. Comparison with experiment for hyaluronic acid. Biopolymers. 1970; 9: 811-824.
79. Lowman AM, Peppas NA. Hydrogels. In: Mathiowitz E., editor. Encyclopedia of controlled drug delivery. New York (NY): Wiley; 1999. p. 397-418.
80. de Jong SJ, van Eerdenbrugh B, von Nostrum CF, Kettenes-van den Bosch JJ, Hennink WE. Physically crosslinked dextran hydrogels by stereocomplex formation of lactic acid oligomers: degradation and protein release behavior. J. Controlled Release. 2001; 71: 261-275.
81. Cesaretti M, Luppi E, Maccari F, Volpi N. A 96-well assay for uronic acid carbazole reaction. Carbohydr. Polym. 2003; 54: 59-61.
82. Trappmann B, Gautrot JE, Connelly JT, Strange DGT, Li Y, Oyen ML, Stuart MAC, Boehm H, Li BJ, Vogel V, Spatz JP, Watt FM, Huck WTS. Extracellular-matrix tethering regulates stem-cell fate. Nat. Mater. 2012; 11: 642-649.
83. Trappmann B, Gautrot JE, Connelly JT, Strange DGT, Li Y, Oyen ML, Cohen Stuart MAC, Boehm H, Li BJ, Vogel V, Spatz JP, Watt FM, Huck WTS. Extracellular-matrix tethering regulates stem-cell fate. Nat. Mater. 2012; 11: 742.
84. Murphy CM, Matsiko A, Haugh MG, Gleeson JP, OBrien FJ. Mesenchymal stem cell fate is regulated by the composition and mechanical properties of collagen-glycosaminoglycan scaffolds. J. Mech. Behav. Biomed. 2012; 11: 53-62.
85. Ayala R, Zhang C, Yang D, Hwang Y, Aung A, Shroff SS, Arce FT, Lal R, Arya G, Varghese S. Engineering the cell-material interface for controlling stem cell adhesion, migration, and differentiation. Biomaterials. 2011; 32: 3700-3711.
86. Bilston LE. Neural tissue biomechanics. Vol. 3. Randwick: Springer; 2011.
87. Tamura A, Hayashi S, Watanabe I, Nagayama K, Matsumoto T. Mechanical characterization of brain tissue in high-rate compression. J. Biomech. Sci. Eng. 2007; 2: 115-126.
88. Taylor Z, Miller K. Reassessment of brain elasticity for analysis of biomechanisms of hydrocephalus. J. Biomech. 2004; 37: 1263-1269.
89. Jin X, Zhu F, Mao HJ, Shen M, Yang KH. A comprehensive experimental study on material properties of human brain tissue. J. Biomech. 2013; 46: 2795-2801.
90. Green MA, Bilston LE, Sinkus R. In vivo brain viscoelastic properties measured by magnetic resonance elastography. NMR Biomed. 2008; 21: 755-764.
91. Klatt D, Hamhaber U, Asbach P, Braun J, Sack I. Noninvasive assessment of the rheological behavior of human organs using multifrequency MR elastography: a study of brain and liver viscoelasticity. Phys. Med. Biol. 2007; 52: 7281-7294.
92. Collins MN, Birkinshaw C. Physical properties of crosslinked hyaluronic acid hydrogels. J. Mater. Sci. Mater. Med. 2008; 19: 3335-3343.
93. Leipzig ND, Shoichet MS. The effect of substrate stiffness on adult neural stem cell behavior. Biomaterials. 2009; 30: 6867-6878.
94. Teixeira AI, Ilkhanizadeh S, Wigenius JA, Duckworth JK, Inganäs O, Hermanson O. The promotion of neuronal maturation on soft substrates. Biomaterials. 2009; 30: 4567-4572.
95. Saha K, Keung AJ, Irwin EF, Li Y, Little L, Schaffer DV, Healy KE. Substrate modulus directs neural stem cell behavior. Biophys. J. 2008; 95: 4426-4438.