Applications and emerging trends of hyaluronic acid in tissue engineering, as a dermal filler and in osteoarthritis treatment

Acta Biomaterialia

Volumn 9, Issue 7, 2013, Pages 7081-7092

  Fakhari, A ^a   Berkland, C ^a,b  

^a University of Kansas   (United States)

^b UNIVERSITY OF KANSAS   (United States)

Author keywords

Crosslinking; Dermal filler; Hyaluronic acid; Viscosupplement

Indexed keywords

BIODEGRADABLE POLYMERS; BODY FLUIDS; COLLAGEN; CROSSLINKING; FILLERS; HISTOLOGY; MUSCULOSKELETAL SYSTEM; ORGANIC ACIDS; SCAFFOLDS (BIOLOGY); TISSUE; VISCOELASTICITY;

CONNECTIVE TISSUES; DERMAL FILLERS; EMERGING TRENDS; EXTRACELLULAR MATRICES; NATURALLY OCCURRING; SYNOVIAL FLUID; TISSUES ENGINEERINGS; VISCOSUPPLEMENT; VISCOSUPPLEMENTATION; VITREOUS HUMOR;

HYALURONIC ACID;

1,4 BUTANEDIOL DIGLYCIDAL ETHER; BETA GLUCURONIDASE; BETA N ACETYLHEXOSAMINIDASE; CROSS LINKING REAGENT; DERMAL FILLER; FILLER; GLUCURONIC ACID; HERMES ANTIGEN; HYALURONIC ACID; HYALURONIDASE; INTERCELLULAR ADHESION MOLECULE 1; LYMPHATIC VESSEL ENDOTHELIAL HA RECEPTOR; N ACETYLGLUCOSAMINE; RECEPTOR; RECEPTOR FOR HA MEDIATED MOTILITY; UNCLASSIFIED DRUG;

BIOSYNTHESIS; CARTILAGE CELL; CATABOLISM; CHEMICAL MODIFICATION; CHEMICAL REACTION; CHEMICAL STRUCTURE; CROSS LINKING; DOWN REGULATION; EMBRYONIC STEM CELL; ENCAPSULATION; ENZYMATIC DEGRADATION; EXTRACELLULAR MATRIX; FLOW KINETICS; HYDRODYNAMICS; HYDROGEN BOND; HYDROLYSIS; ION CURRENT; MELANOCYTE; MOLECULAR WEIGHT; OSTEOARTHRITIS; PRIORITY JOURNAL; REVIEW; SHEAR STRESS; SIGNAL TRANSDUCTION; STATIC ELECTRICITY; SYNOVIAL FLUID; TISSUE ENGINEERING; TURNOVER TIME; VISCOELASTICITY; WOUND HEALING;

EID: 84878315369     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2013.03.005     Document Type: Review

References (154)

1. M. Kurisawa, J. Chung, Y. Yang, S. Gao, and H. Uyama Injectable biodegradable hydrogels composed of hyaluronic acid-tyramine conjugates for drug delivery and tissue engineering Chem Commun 2005 2005 4312 4314
2. H.G. Garg, and C.A. Hales Chemistry and biology of hyaluronan 2004 Elsevier Science Oxford ISBN:978-0-08-044382-9
3. P. Andre New trends in face rejuvenation by hyaluronic acid injections J Cosmet Dermatol 7 2008 251 258
4. J. Necas, L. Bartosikova, P. Brauner, and J. Kolar Hyaluronic acid (hyaluronan): a review Vet Med 53 2008 397 411
5. S. Falcone, D. Palmeri, and R. Berg Biomedical applications of hyaluronic acid 2006 ACS Publications p. 155-74
6. X. Zheng Shu, Y. Liu, F. Palumbo, Y. Luo, and G. Prestwich In situ crosslinkable hyaluronan hydrogels for tissue engineering Biomaterials 25 2004 1339 1348
7. L. Vejlens Glycosaminoglycans of human bone tissue Calcif Tissue Int 7 1971 175 190
8. S. Dumitriu Polymeric biomaterials 2002 Marcel Dekker New York ISBN:0-8247-8969-5
9. T. Segura, B. Anderson, P. Chung, R. Webber, K. Shull, and L. Shea Crosslinked hyaluronic acid hydrogels: a strategy to functionalize and pattern Biomaterials 26 2005 359 371
10. B. Toole Hyaluronan: from extracellular glue to pericellular cue Nat Rev Cancer 4 2004 528 539
11. S. Cai, Y. Xie, T. Bagby, M. Cohen, and M. Forrest Intralymphatic chemotherapy using a hyaluronan-cisplatin conjugate J Surg Res 147 2008 247
12. C. Underhill CD44: the hyaluronan receptor J Cell Sci 103 1992 293
13. D. Eng, M. Caplan, M. Preul, and A. Panitch Hyaluronan scaffolds - a balance between backbone functionalization and bioactivity Acta Biomater 6 2010 2407 2414
14. J. Kim, I. Kim, T. Cho, K. Lee, S. Hwang, and G. Tae Bone regeneration using hyaluronic acid-based hydrogel with bone morphogenic protein-2 and human mesenchymal stem cells Biomaterials 28 2007 1830 1837
15. Y. Luo, K. Kirker, and G. Prestwich Cross-linked hyaluronic acid hydrogel films: new biomaterials for drug delivery J Controlled Release 69 2000 169 184
16. K. Lee, and D. Mooney Hydrogels for tissue engineering Chem Rev 101 2001 1869 1880
17. J. Drury, and D. Mooney Hydrogels for tissue engineering: scaffold design variables and applications Biomaterials 24 2003 4337 4351
18. J.A. Burdick, and G.D. Prestwich Hyaluronic acid hydrogels for biomedical applications Adv Mater 23 2011 H41 H56
19. G.M. Campo, A. Avenoso, S. Campo, A.M. Ferlazzo, C. Micali, and L. Zanghì Hyaluronic acid and chondroitin-4-sulphate treatment reduces damage in carbon tetrachloride-induced acute rat liver injury Life Sci 74 2004 1289 1305
20. A.K. Yadav, P. Mishra, and G.P. Agrawal An insight on hyaluronic acid in drug targeting and drug delivery J Drug Target 16 2008 91 107
21. S. Rossi, G. Sandri, and C.M. Caramella Buccal drug delivery: a challenge already won? Drug Discov Today Technol 2 2005 59 65
22. M. Hamidi, A. Azadi, and P. Rafiei Hydrogel nanoparticles in drug delivery Adv Drug Deliv Rev 60 2008 1638 1649
23. J. Whelan The biology of hyaluronan 1989 John Wiley & Sons New York ISBN:0471923052
24. J. Sheehan, C. Arundel, and C. Phelps Effect of the cations sodium, potassium and calcium on the interaction of hyaluronate chains: a light scattering and viscometric study Int J Biol Macromol 5 1983 222 228
25. B.P. Toole Hyaluronan in morphogenesis Semin Cell Dev Biol 12 2001 79 87
26. B.P. Toole, T.N. Wight, and M.I. Tammi Hyaluronan-cell interactions in cancer and vascular disease J Biol Chem 277 2002 4593
27. P.W. Noble Hyaluronan and its catabolic products in tissue injury and repair Matrix Biol 21 2002 25 29
28. B. Toole Hyaluronan in morphogenesis J Intern Med 242 1997 35 40
29. E.A. Turley, P.W. Noble, and L.Y. Bourguignon Signaling properties of hyaluronan receptors J Biol Chem 277 2002 4589 4592
30. G. Christofori Changing neighbours, changing behaviour: cell adhesion molecule-mediated signalling during tumour progression EMBO J 22 2003 2318 2323
31. T.H. Lee, H.-G. Wisniewski, and J. Vilcek A novel secretory tumor necrosis factor-inducible protein (TSG-6) is a member of the family of hyaluronate binding proteins, closely related to the adhesion receptor CD44 J Cell Biol 116 1992 545 557
32. G. Perides, R. Asher, M. Lark, W. Lane, R. Robinson, and A. Bignami Glial hyaluronate-binding protein: a product of metalloproteinase digestion of versican? Biochem J 312 1995 377
33. G. Perides, R. Asher, D. Dahl, and A. Bignamic Glial hyaluronate-binding protein (GHAP) optic nerve and retina Brain Res 512 1990 309 316
34. M. Leppilahti, P. Hellström, and T.L. Tammela Effect of diagnostic hydrodistension and four intravesical hyaluronic acid instillations on bladder ICAM-1 intensity and association of ICAM-1 intensity with clinical response in patients with interstitial cystitis Urology 60 2002 46 51
35. J.A. Weigel, R.C. Raymond, and P.H. Weigel The hyaluronan receptor for endocytosis (HARE) is not CD44 or CD54 (ICAM-1) Biochem Biophys Res Commun 294 2002 918 922
36. S. Banerji, J. Ni, S.-X. Wang, S. Clasper, J. Su, and R. Tammi LYVE-1, a new homologue of the CD44 glycoprotein, is a lymph-specific receptor for hyaluronan J Cell Biol 144 1999 789 801
37. C.M. Carreira, S.M. Nasser, E. di Tomaso, T.P. Padera, Y. Boucher, and S.I. Tomarev LYVE-1 is not restricted to the lymph vessels expression in normal liver blood sinusoids and down-regulation in human liver cancer and cirrhosis Cancer Res 61 2001 8079 8084
38. D.G. Jackson The lymphatics revisited: new perspectives from the hyaluronan receptor LYVE-1 Trends Cardiovasc Med 13 2003 1 7
39. R. Prevo, S. Banerji, D.J. Ferguson, S. Clasper, and D.G. Jackson Mouse LYVE-1 is an endocytic receptor for hyaluronan in lymphatic endothelium J Biol Chem 276 2001 19420 19430
40. S. Akira, K. Tokeda, and T. Kaisho Toll-like receptors: critical proteins linking innate and acquired immunity Nat Immunol 2 2001 675 680
41. K. Takeda, and S. Akira Toll-like receptors Curr Protoc Immunol 2007 14.12.1-14.12.3
42. F.L. Rock, G. Hardiman, J.C. Timans, R.A. Kastelein, and J.F. Bazan A family of human receptors structurally related to Drosophila Toll Proc Nat Acad Sci 95 1998 588 593
43. M. Rescigno, F. Granucci, and P. Ricciardi-Castagnoli Molecular events of bacterial-induced maturation ofdendritic cells J Clin Immunol 20 2000 161 166
44. A. Poltorak, X. He, I. Smirnova, M.-Y. Liu, C. Van Huffel, and X. Du Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene Science 282 1998 2085 2088
45. O. Takeuchi, K. Hoshino, T. Kawai, H. Sanjo, H. Takada, and T. Ogawa Differential roles of TLR2 and TLR4 in recognition of gram-negative and gram-positive bacterial cell wall components Immunity 11 1999 443 451
46. C.M. McKee, M.B. Penno, M. Cowman, M.D. Burdick, R.M. Strieter, and C. Bao Hyaluronan (HA) fragments induce chemokine gene expression in alveolar macrophages. The role of HA size and CD44 J Clin Invest 98 1996 2403
47. S. Gariboldi, M. Palazzo, L. Zanobbio, S. Selleri, M. Sommariva, and L. Sfondrini Low molecular weight hyaluronic acid increases the self-defense of skin epithelium by induction of β-defensin 2 via TLR2 and TLR4 J Immunol 181 2008 2103 2110
48. K.A. Scheibner, M.A. Lutz, S. Boodoo, M.J. Fenton, J.D. Powell, and M.R. Horton Hyaluronan fragments act as an endogenous danger signal by engaging TLR2 J Immunol 177 2006 1272 1281
49. B. Oertli, X. Fan, and R.P. Wüthrich Characterization of CD44-mediated hyaluronan binding by renal tubular epithelial cells Nephrol Dial Transplant 13 1998 271
50. W.Y.J. Chen, and G. Abatangelo Functions of hyaluronan in wound repair Wound Repair Regen 7 1999 79 89
51. H.-G. Wisniewski, J. Hua, D.M. Poppers, D. Naime, J. Vilcek, and B.N. Cronstein TNF/IL-1-inducible protein TSG-6 potentiates plasmin inhibition by inter-alpha-inhibitor and exerts a strong anti-inflammatory effect in vivo J Immunol 156 1996 1609 1615
52. H. Kobayashi, and T. Terao Hyaluronic acid-specific regulation of cytokines by human uterine fibroblasts Am J Physiol Cell Physiol 273 1997 C1151 C1159
53. T.C. Laurent The chemistry, biology and medical applications of hyaluronan and its derivatives 1998 Portland Press London
54. B. Barnhart, S. Cox, and P. Kraemer Detachment variants of Chinese hamster cells: hyaluronic acid as a modulator of cell detachment Exp Cell Res 119 1979 327 332
55. M. Mohamadzadeh, H. DeGrendele, H. Arizpe, P. Estess, and M. Siegelman Proinflammatory stimuli regulate endothelial hyaluronan expression and CD44/HA-dependent primary adhesion J Clin Invest 101 1998 97
56. Y. Liu, X. Zheng Shu, and G.D. Prestwich Biocompatibility and stability of disulfide-crosslinked hyaluronan films Biomaterials 26 2005 4737 4746
57. M. Brecht, U. Mayer, E. Schlosser, and P. Prehm Increased hyaluronate synthesis is required for fibroblast detachment and mitosis Biochem J 239 1986 445
58. N. Mian Analysis of cell-growth-phase-related variations in hyaluronate synthase activity of isolated plasma-membrane fractions of cultured human skin fibroblasts Biochem J 237 1986 333
59. G. Abatangelo, R. Cortivo, M. Martelli, and P. Vecchia Cell detachment mediated by hyaluronic acid Exp Cell Res 137 1982 73 78
60. G.M. Morriss-Kay, F. Tuckett, and M. Solursh The effects of streptomyces hyaluronidase on tissue organization and cell cycle time in rat embryos J Embryol Exp Morphol 98 1986 59 70
61. E. Turley, L. Austen, D. Moore, and K. Hoare Ras-transformed cells express both CD44 and RHAMM hyaluronan receptors: only RHAMM is essential for hyaluronan-promoted locomotion Exp Cell Res 207 1993 277
62. W. Chen, M.E. Grant, A. Schor, and S. Schor Differences between adult and foetal fibroblasts in the regulation of hyaluronate synthesis: correlation with migratory activity J Cell Sci 94 1989 577 584
63. I. Ellis, A. Grey, A.M. Schor, and S.L. Schor Antagonistic effects of TGF-beta 1 and MSF on fibroblast migration and hyaluronic acid synthesis. Possible implications for dermal wound healing J Cell Sci 102 1992 447 456
64. I. Ellis, J. Banyard, and S. Schor Differential response of fetal and adult fibroblasts to cytokines: cell migration and hyaluronan synthesis Development 124 1997 1593 1600
65. C. Wang, A.D. Thor, D. Moore, Y. Zhao, R. Kerschmann, and R. Stern The overexpression of RHAMM, a hyaluronan-binding protein that regulates ras signaling, correlates with overexpression of mitogen-activated protein kinase and is a significant parameter in breast cancer progression Clin Cancer Res 4 1998 567 576
66. C. Hall, L. Lange, D. Prober, S. Zhang, and E. Turley Pp 60 (c-src) is required for cell locomotion regulated by the hyaluronanreceptor RHAMM Oncogene 13 1996 2213
67. R. Pratt, M. Larsen, and M. Johnston Migration of cranial neural crest cells in a cell-free hyaluronate-rich matrix Dev Biol 44 1975 298 305
68. E.A. Turley Hyaluronan-binding proteins and receptors Adv Drug Deliv Rev 7 1991 257 264
69. L. Thomas, H.R. Byers, J. Vink, and I. Stamenkovic CD44H regulates tumor cell migration on hyaluronate-coated substrate J Cell Biol 118 1992 971 977
70. P. Rooney, M. Wang, P. Kumar, and S. Kumar Angiogenic oligosaccharides of hyaluronan enhance the production of collagens by endothelial cells J Cell Sci 105 1993 213 218
71. P.W. Noble, F. Lake, P. Henson, and D. Riches Hyaluronate activation of CD44 induces insulin-like growth factor-1 expression by a tumor necrosis factor-alpha-dependent mechanism in murine macrophages J Clin Invest 91 1993 2368
72. P.W. Noble, C.M. McKee, M. Cowman, and H.S. Shin Hyaluronan fragments activate an NF-kappa B/I-kappa B alpha autoregulatory loop in murine macrophages J Exp Med 183 1996 2373 2378
73. H. Dvorak, V. Harvey, P. Estrella, L. Brown, J. McDonagh, and A. Dvorak Fibrin containing gels induce angiogenesis. Implications for tumor stroma generation and wound healing Lab Invest 57 1987 673
74. D.C. West, and S. Kumar The effect of hyaluronate and its oligosaccharides on endothelial cell proliferation and monolayer integrity Exp Cell Res 183 1989 179 196
75. V.C. Lees, T. Fan, and D.C. West Angiogenesis in a delayed revascularization model is accelerated by angiogenic oligosaccharides of hyaluronan Lab Invest 73 1995 259
76. F. Arnold, C. Jia, C. He, G.W. Cherry, B. Carbow, and W. Meyer-Ingold Hyaluronan, heterogeneity, and healing: the effects of ultrapure hyaluronan of defined molecular size on the repair of full-thickness pig skin wounds Wound Repair Regen 3 2002 299 310
77. A. Sattar, P. Rooney, S. Kumar, D. Pye, D.C. West, and I. Scott Application of angiogenic oligosaccharides of hyaluronan increases blood vessel numbers in rat skin J Invest Dermatol 103 1994 576 579
78. D. West, and D. Shaw Tumour hyaluronan in relation to angiogenesis and metastasis Wenner Gren Int Ser 1998 227 234
79. B.A. Mast, J.H. Haynes, T.M. Krummel, R.F. Diegelmann, and I.K. Cohen In vivo degradation of fetal wound hyaluronic acid results in increased fibroplasia, collagen deposition, and neovascularization Plast Reconstr Surg 89 1992 503
80. R. Tammi, J.A. Ripellino, R.U. Margolis, and M. Tammi Localization of epidermal hyaluronic acid using the hyaluronate binding region of cartilage proteoglycan as a specific probe J Invest Dermatol 90 1988 412 414
81. R. Tammi, J.A. Ripellino, R.U. Margolis, H.I. Maibach, and M. Tammi Hyaluronate accumulation in human epidermis treated with retinoic acid in skin organ culture J Invest Dermatol 92 1989 326 332
82. C. Wang, M. Tammi, and R. Tammi Distribution of hyaluronan and its CD44 receptor in the epithelia of human skin appendages Histochem Cell Biol 98 1992 105 112
83. A.-L. Tuhkanen, M. Tammi, A. Pelttari, U.M. Ågren, and R. Tammi Ultrastructural analysis of human epidermal CD44 reveals preferential distribution on plasma membrane domains facing the hyaluronan-rich matrix pouches J Histochem Cytochem 46 1998 241 248
84. G. Kaya, I. Rodriguez, J.L. Jorcano, P. Vassalli, and I. Stamenkovic Selective suppression of CD44 in keratinocytes of mice bearing an antisense CD44 transgene driven by a tissue-specific promoter disrupts hyaluronate metabolism in the skin and impairs keratinocyte proliferation Genes Dev 11 1997 996 1007
85. M.T. Longaker, E.S. Chiu, N.S. Adzick, M. Stern, M.R. Harrison, and R. Stern Studies in fetal wound healing. V. A prolonged presence of hyaluronic acid characterizes fetal wound fluid Ann Surg 213 1991 292
86. D.C. West, D.M. Shaw, P. Lorenz, N.S. Adzick, and M.T. Longaker Fibrotic healing of adult and late gestation fetal wounds correlates with increased hyaluronidase activity and removal of hyaluronan Int J Biochem Cell Biol 29 1997 201 210
87. J.Y. Lee, and A.P. Spicer Hyaluronan: a multifunctional, megaDalton, stealth molecule Curr Opin Cell Biol 12 2000 581 586
88. A. Ramamurthi, and I. Vesely Evaluation of the matrix-synthesis potential of crosslinked hyaluronan gels for tissue engineering of aortic heart valves Biomaterials 26 2005 999 1010
89. M.K. Cowman, and S. Matsuoka Experimental approaches to hyaluronan structure Carbohydr Res 340 2005 791 809
90. T.C. Laurent, and J. Fraser Hyaluronan FASEB J 6 1992 2397 2404
91. R. Stern, G. Kogan, M.J. Jedrzejas, and L. Soltés The many ways to cleave hyaluronan Biotechnol Adv 25 2007 537 557
92. N. Volpi, J. Schiller, R. Stern, and L. Soltes Role, metabolism, chemical modifications and applications of hyaluronan Curr Med Chem 16 2009 1718 1745
93. L. Šoltés, R. Mendichi, G. Kogan, J. Schiller, M. Stankovska, and J. Arnhold Degradative action of reactive oxygen species on hyaluronan Biomacromolecules 7 2006 659 668
94. E. Maheu, X. Ayral, and M. Dougados A hyaluronan preparation (500-730 kDa) in the treatment of osteoarthritis: a review of clinical trials with hyalgan Int J Clin Pract 56 2002 804
95. J. Arrich, F. Piribauer, P. Mad, D. Schmid, K. Klaushofer, and M. Müllner Intra-articular hyaluronic acid for the treatment of osteoarthritis of the knee: systematic review and meta-analysis Can Med Assoc J 172 2005 1039
96. V. Goldberg, and J. Buckwalter Hyaluronans in the treatment of osteoarthritis of the knee: evidence for disease-modifying activity Osteoarthritis Cartilage 13 2005 216 224
97. A. Migliore, and M. Granata Intra-articular use of hyaluronic acid in the treatment of osteoarthritis Clin Interv Aging 3 2008 365
98. D.D. Allison, and K.J. Grande-Allen Review. Hyaluronan: a powerful tissue engineering tool Tissue Eng 12 2006 2131 2140
99. D. Jiang, J. Liang, and P.W. Noble Hyaluronan in tissue injury and repair Annu Rev Cell Dev Biol 23 2007 435 461
100. K. Tomihata, and Y. Ikada Crosslinking of hyaluronic acid with water soluble carbodiimide J Biomed Mater Res 37 1997 243 251
101. K.P. Vercruysse, D.M. Marecak, J.F. Marecek, and G.D. Prestwich Synthesis and in vitro degradation of new polyvalent hydrazide cross-linked hydrogels of hyaluronic acid Bioconjug Chem 8 1997 686 694
102. Y. Luo, K.R. Kirker, and G.D. Prestwich Cross-linked hyaluronic acid hydrogel films: new biomaterials for drug delivery J Controlled Release 69 2000 169 184
103. J. Baier Leach, K.A. Bivens, C.W. Patrick Jr., and C.E. Schmidt Photocrosslinked hyaluronic acid hydrogels: natural, biodegradable tissue engineering scaffolds Biotechnol Bioeng 82 2003 578 589
104. J.B. Leach, K.A. Bivens, C.N. Collins, and C.E. Schmidt Development of photocrosslinkable hyaluronic acid-polyethylene glycol-peptide composite hydrogels for soft tissue engineering J Biomed Mater Res Part A 70 2004 74 82
105. E.A. Balazs, and J.L. Denlinger Viscosupplementation: a new concept in the treatment of osteoarthritis J Rheumatol Suppl 39 1993 3
106. Y. Jin, J. Yamanaka, S. Sato, I. Miyata, C. Yomota, and M. Yonese Recyclable characteristics of hyaluronate-polyhydroxyethyl acrylate blend hydrogel for controlled releases J Controlled Release 73 2001 173 181
107. L. Weng, A. Gouldstone, Y. Wu, and W. Chen Mechanically strong double network photocrosslinked hydrogels from N,N-dimethylacrylamide and glycidyl methacrylated hyaluronan Biomaterials 29 2008 2153 2163
108. X. Jia, J.A. Burdick, J. Kobler, R.J. Clifton, J.J. Rosowski, and S.M. Zeitels Synthesis and characterization of in situ cross-linkable hyaluronic acid-based hydrogels with potential application for vocal fold regeneration Macromolecules 37 2004 3239 3248
109. K. Miyamoto, M. Sasaki, Y. Minamisawa, Y. Kurahashi, H. Kano, and S. Ishikawa Evaluation of in vivo biocompatibility and biodegradation of photocrosslinked hyaluronate hydrogels (HADgels) J Biomed Mater Res Part A 70 2004 550 559
110. J.A. Burdick, C. Chung, X. Jia, M.A. Randolph, and R. Langer Controlled degradation and mechanical behavior of photopolymerized hyaluronic acid networks Biomacromolecules 6 2005 386 391
111. M.D. Brigham, A. Bick, E. Lo, A. Bendali, J.A. Burdick, and A. Khademhosseini Mechanically robust and bioadhesive collagen and photocrosslinkable hyaluronic acid semi-interpenetrating networks Tissue Eng Part A 15 2008 1645 1653
112. J.L. Ifkovits, E. Tous, M. Minakawa, M. Morita, J.D. Robb, and K.J. Koomalsingh Injectable hydrogel properties influence infarct expansion and extent of postinfarction left ventricular remodeling in an ovine model Proc Nat Acad Sci 107 2010 11507 11512
113. K.S. Masters, D.N. Shah, G. Walker, L.A. Leinwand, and K.S. Anseth Designing scaffolds for valvular interstitial cells: cell adhesion and function on naturally derived materials J Biomed Mater Res Part A 71 2004 172 180
114. E. Figallo, C. Cannizzaro, S. Gerecht, J.A. Burdick, R. Langer, and N. Elvassore Micro-bioreactor array for controlling cellular microenvironments Lab Chip 7 2007 710 719
115. L. Cen, K. Neoh, Y. Li, and E. Kang Assessment of in vitro bioactivity of hyaluronic acid and sulfated hyaluronic acid functionalized electroactive polymer Biomacromolecules 5 2004 2238 2246
116. J.H. Collier, J.P. Camp, T.W. Hudson, and C.E. Schmidt Synthesis and characterization of polypyrrole-hyaluronic acid composite biomaterials for tissue engineering applications J Biomed Mater Res 50 2000 574 584
117. J.Y. Lee, and C.E. Schmidt Pyrrole-hyaluronic acid conjugates for decreasing cell binding to metals and conducting polymers Acta Biomater 6 2010 4396 4404
118. J. Aigner, J. Tegeler, P. Hutzler, D. Campoccia, A. Pavesio, and C. Hammer Cartilage tissue engineering with novel nonwoven structured biomaterial based on hyaluronic acid benzyl ester J Biomed Mater Res 42 1998 172 181
119. S. Ibrahim, Q.K. Kang, and A. Ramamurthi The impact of hyaluronic acid oligomer content on physical, mechanical, and biologic properties of divinyl sulfone crosslinked hyaluronic acid hydrogels J Biomed Mater Res Part A 94 2010 355 370
120. X.Z. Shu, Y. Liu, F. Palumbo, and G.D. Prestwich Disulfide-crosslinked hyaluronan-gelatin hydrogel films: a covalent mimic of the extracellular matrix for in vitro cell growth Biomaterials 24 2003 3825 3834
121. X.Z. Shu, Y. Liu, Y. Luo, M.C. Roberts, and G.D. Prestwich Disulfide cross-linked hyaluronan hydrogels Biomacromolecules 3 2002 1304 1311
122. M.A. Serban, A. Scott, and G.D. Prestwich Use of hyaluronan-derived hydrogels for three-dimensional cell culture and tumor xenografts Curr Protoc Cell Biol 10 2008 1
123. G.D. Prestwich Hyaluronic acid-based clinical biomaterials derived for cell and molecule delivery in regenerative medicine J Controlled Release 155 2011 193 199
124. A.K. Jha, R.A. Hule, T. Jiao, S.S. Teller, R.J. Clifton, and R.L. Duncan Structural analysis and mechanical characterization of hyaluronic acid-based doubly cross-linked networks Macromolecules 42 2009 537 546
125. A. Darr, and A. Calabro Synthesis and characterization of tyramine-based hyaluronan hydrogels J Mater Sci Mater Med 20 2009 33 44
126. V. Crescenzi, L. Cornelio, C. Di Meo, S. Nardecchia, and R. Lamanna Novel hydrogels via click chemistry: synthesis and potential biomedical applications Biomacromolecules 8 2007 1844 1850
127. X. Zheng Shu, Y. Liu, F.S. Palumbo, Y. Luo, and G.D. Prestwich In situ crosslinkable hyaluronan hydrogels for tissue engineering Biomaterials 25 2004 1339 1348
128. Y. Yeo, C.B. Highley, E. Bellas, T. Ito, R. Marini, and R. Langer In situ cross-linkable hyaluronic acid hydrogels prevent post-operative abdominal adhesions in a rabbit model Biomaterials 27 2006 4698 4705
129. Y. Yeo, T. Ito, E. Bellas, C.B. Highley, R. Marini, and D.S. Kohane In situ cross-linkable hyaluronan hydrogels containing polymeric nanoparticles for preventing postsurgical adhesions Ann Surg 245 2007 819
130. A. Tezel, and G.H. Fredrickson The science of hyaluronic acid dermal fillers J Cosmet Laser Ther 10 2008 35 42
131. N.S. Sadick, C. Karcher, and L. Palmisano Cosmetic dermatology of the aging face Clin Dermatol 27 2009 S3 S12
132. G.J. Fisher, J. Varani, and J.J. Voorhees Looking older: fibroblast collapse and therapeutic implications Arch Dermatol 144 2008 666
133. I. Sánchez-Carpintero, D. Candelas, and R. Ruiz-Rodríguez Dermal fillers: types, indications, and complications Actas Dermosifiliogr (Engl Ed) 101 2010 381 393
134. L.H. Christensen Host tissue interaction, fate, and risks of degradable and nondegradable gel fillers Dermatol Surg 35 2009 1612 1619
135. F.S. Brandt, and A. Cazzaniga Hyaluronic acid gel fillers in the management of facial aging Clin Interv Aging 3 2008 153
136. M.H. Gold Use of hyaluronic acid fillers for the treatment of the aging face Clin Interv Aging 2 2007 369
137. I. Buck, W. Donald, M. Alam, and J. Kim Injectable fillers for facial rejuvenation: a review J Plast Reconstr Aesthet Surg 62 2009 11 18
138. G.D. Monheit, and C.L. Prather Hyaluronic acid fillers for the male patient Dermatol Ther 20 2007 394 406
139. J. Kablik, G.D. Monhit, L. Yu, G. Chang, and J. Gershkovich Comparative physical properties of hyaluronic acid dermal fillers Dermatol Surg 35 2009 302 312
140. D. Stroumpoulis, C.S. Mudd, and A. Tezel Polysaccaride gel formation having increased longevity Google Patents 2008
141. L.W. Moreland Intra-articular hyaluronan (hyaluronic acid) and hylans for the treatment of osteoarthritis: mechanisms of action Arthritis Res Ther 5 2003 54 67
142. M.J. Yaszemski Tissue engineering and novel delivery systems 2003 CRC Press Boca Raton, FL ISBN:0-8247-4786-0
143. B.P. Conrad The effects of glucosamine and chondroitin on the viscosity of synovial fluid in patients with osteoarthritis 2001 Citeseer
144. R. Altman, and R. Moskowitz Intraarticular sodium hyaluronate (Hyalgan) in the treatment of patients with osteoarthritis of the knee: a randomized clinical trial. Hyalgan Study Group J Rheumatol 25 1998 2203
145. J.R. Watterson, and J.M. Esdaile Viscosupplementation: therapeutic mechanisms and clinical potential in osteoarthritis of the knee J Am Acad Orthop Surg 8 2000 277
146. CARE FONP Hyaluronic acid products for osteoarthritis of the knee CPJ 140 2007 195
147. S.F. Sun, Y.J. Chou, C.W. Hsu, and W.L. Chen Hyaluronic acid as a treatment for ankle osteoarthritis Curr Rev Musculoskelet Med 2 2009 78 82
148. S.S. Leopold, W.J. Warme, P.D. Pettis, and S. Shott Increased frequency of acute local reaction to intra-articular hylan GF-20 (synvisc) in patients receiving more than one course of treatment J Bone Joint Surg Am 84 2002 1619
149. N. Kotevoglu, P.C. Iyibozkurt, O. Hiz, H. Toktas, and B. Kuran A prospective randomised controlled clinical trial comparing the efficacy of different molecular weight hyaluronan solutions in the treatment of knee osteoarthritis Rheumatol Int 26 2006 325 330
150. H. Fam, J. Bryant, and M. Kontopoulou Rheological properties of synovial fluids Biorheology 44 2007 59 74
151. F. Duranti, G. Salti, B. Bovani, M. Calandra, and M.L. Rosati Injectable hyaluronic acid gel for soft tissue augmentation Dermatol Surg 24 1998 1317 1325
152. M. Olenius The first clinical study using a new biodegradable implant for the treatment of lips, wrinkles, and folds Aesthet Plast Surg 22 1998 97 101
153. N. Rydell, and E.A. Balazs Effect of intra-articular injection of hyaluronic acid on the clinical symptoms of osteoarthritis and on granulation tissue formation Clin Orthop Relat Res 80 1971 25 32
154. J.G. Peyron, and E. Balazs Preliminary clinical assessment of Na-hyaluronate injection into human arthritic joints Pathol Biol 22 1974 731