Genetically-manipulated adult stem cells as therapeutic agents and gene delivery vehicle for wound repair and regeneration

Journal of Controlled Release

Volumn 157, Issue 3, 2012, Pages 321-330

  Peng, Li Hua ^a   Tsang, Suk Ying ^b   Tabata, Yasuhiko ^c   Gao, Jian Qing ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b CHINESE UNIVERSITY OF HONG KONG   (Hong Kong)

^c KYOTO UNIVERSITY   (Japan)

Author keywords

Adult stem cells; Gene delivery; Regeneration; Wound repair

Indexed keywords

ADULT STEM CELLS; BIOACTIVE MOLECULES; DRUG DELIVERY SYSTEM; GENE DELIVERY; MOLECULAR BEHAVIOR; OPTIMAL ENVIRONMENT; REGENERATION; REGENERATION MEDICINE; REGENERATIVE CELL; SCAR FORMATION; SIGNALS CONTROL; SKIN REGENERATION; THERAPEUTIC AGENTS; TOPICAL APPLICATION; WOUND MANAGEMENT; WOUND REPAIR; WOUND SITE;

BIOMIMETICS; DRUG DELIVERY; GENE EXPRESSION; GENE TRANSFER; STEM CELLS; TISSUE;

GENE THERAPY;

LIPOSOME; POLYMER; VIRUS VECTOR;

ADIPOSE DERIVED STEM CELL; ADULT STEM CELL; EPIDERMIS; GENE DELIVERY SYSTEM; HAIR FOLLICLE; HEMATOPOIETIC STEM CELL; HUMAN; MULTIPOTENT STEM CELL; NONHUMAN; PRIORITY JOURNAL; REVIEW; SCAR FORMATION; TISSUE REGENERATION; WOUND HEALING;

ADULT STEM CELLS; ANIMALS; BIOMIMETIC MATERIALS; DRUG DELIVERY SYSTEMS; GENE THERAPY; GENE TRANSFER TECHNIQUES; HUMANS; REGENERATION; WOUND HEALING;

EID: 84055207623     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2011.08.027     Document Type: Review

References (95)

1. R.F. Diegelmann, and M.C. Evans Wound healing: an overview of acute, fibrotic and delayed healing Front. Biosci. 9 2004 283 289 (Pubitemid 38925460)
2. R.E. Horch, J. Kopp, U. Kneser, J. Beier, and A.D. Bach Tissue engineering of cultured skin substitutes J. Cell. Mol. Med. 9 2005 592 608 (Pubitemid 44159327)
3. P.V. Giannoudis, C.C. Tzioupis, and E. Tsiridis Gene therapy in orthopaedics Injury 37 Suppl. 1 2006 S30 S40
4. S. Werner, and R. Grose Regulation of wound healing by growth factors and cytokines Physiol. Rev. 83 2002 835 870
5. S. Shilo, S. Roy, S. Khanna, and C.K. Sen MicroRNA in cutaneous wound healing: a new paradigm DNA Cell Biol. 26 2007 227 237 (Pubitemid 46776607)
6. S. Barrientos, O. Stojadinovic, M.S. Golinko, H. Brem, and T.C. Marjana Growth factors and cytokines in wound healing Wound Repair Regen. 16 2008 585 601
7. R. Gillitzer, and M. Goebeler Chemokines in cutaneous wound healing J. Leukoc. Biol. 69 2001 513 521 (Pubitemid 32294835)
8. Y. Shi, G. Hu, J. Su, W. Li, Q. Chen, P. Shou, C. Xu, X. Chen, Y. Huang, Z. Zhu, X. Huang, X. Han, N. Xie, and G. Ren Mesenchymal stem cells: a new strategy for immunosuppression and tissue repair Cell Res. 20 2010 510 518
9. A.M. Hocking, and N.S. Gibran Mesenchymal stem cells: paracrine signaling and differentiation during cutaneous wound repair Exp. Cell Res. 316 2010 2213 2219
10. M. Kamstrup, A. Faurschou, R. Gniadecki, and H.C. Wulf Epidermal stem cells - role in normal, wounded and pathological psoriatic and cancer skin Curr. Stem Cell Res. Ther. 3 2008 146 150 (Pubitemid 352024860)
11. X. Fu, J. Li, X. Sun, T. Sun, and Z. Shen Wound Repair Regen. 13 2005 102 108
12. Gharzi, A.J. Reynolds, and C.A. Jahoda Plasticity of hair follicle dermal cells in wound healing and induction Exp. Dermatol. 12 2003 126 136 (Pubitemid 36934697)
13. S. Tiede, J.E. Kloepper, E. Bodò, S. Tiwari, C. Kruse, and R. Paus Hair follicle stem cells: walking the maze Eur. J. Cell Biol. 86 2007 355 376 (Pubitemid 46971920)
14. M. Ito, Y. Liu, Z. Yang, J. Nguyen, F. Liang, R.J. Morris, and G. Cotsarelis Stem cells in the hair follicle bulge contribute to wound repair but not to homeostasis of the epidermis Nat. Med. 11 2005 1351 1354 (Pubitemid 41752917)
15. Y. Wu, J. Wang, P.G. Scott, and E.E. Tredget Bone marrow-derived stem cells in wound healing: a review Wound Repair Regen. Suppl. 1 2007 S18 S26
16. L. Chen, E.E. Tredget, P.Y. Wu, and Y. Wu Paracrine factors of mesenchymal stem cells recruit macrophages and endothelial lineage cells and enhance wound healing PLoS One 3 2008 e1886
17. H. Li, X. Fu, Y. Ouyang, C. Cai, J. Wang, and T. Sun Adult bone-marrow-derived mesenchymal stem cells contribute to wound healing of skin appendages Cell Tissue Res. 326 2006 725 736 (Pubitemid 44786372)
18. Y.C. Shang, S.H. Wang, F. Xiong, C.P. Zhao, F.N. Peng, S.W. Feng, M.S. Li, Y. Li, and C. Zhang Wnt3a signaling promotes proliferation, myogenic differentiation, and migration of rat bone marrow mesenchymal stem cells Acta Pharmacol. Sin. 28 2007 1761 1774 (Pubitemid 350029333)
19. J. Mauney, B.R. Olsen, and V. Volloch Matrix remodeling as stem cell recruitment event: a novel in vitro model for homing of human bone marrow stromal cells to the site of injury shows crucial role of extracellular collagen matrix Matrix Biol. 29 2010 657 663
20. J. Koerner, D. Nesic, J.D. Romero, W. Brehm, P. Mainil-Varlet, and S.P. Grogan Equine peripheral blood-derived progenitors in comparison to bone marrow-derived mesenchymal stem cells Stem Cells 24 2006 1613 1619 (Pubitemid 44464679)
21. H. Lang, Y. Ebihara, R.A. Schmiedt, H. Minamiguchi, D. Zhou, N. Smythe, L. Liu, M. Ogawa, and B.A. Schulte Contribution of bone marrow hematopoietic stem cells to adult mouse inner ear: mesenchymal cells and fibrocytes J. Comp. Neurol. 496 2006 187 201
22. J.M. Daniel, W. Bielenberg, P. Stieger, S. Weinert, H. Tillmanns, and D.G. Sedding Time-course analysis on the differentiation of bone marrow-derived progenitor cells into smooth muscle cells during neointima formation Arterioscler. Thromb. Vasc. Biol. 30 2010 1890 1896
23. J.H. Jeong Adipose stem cells and skin repair Curr. Stem Cell Res. Ther. 5 2010 137 140
24. K.M. Malinda, G.S. Sidhu, K.K. Banaudha, J.P. Gaddipati, R.K. Maheshwari, A.L. Goldstein, and H.K. Kleinman Thymosin a1 Stimulates Endothelial Cell Migration, Angiogenesis, and Wound Healing J. Immunol. 160 1998 1001 1006 (Pubitemid 28049346)
25. W.S. Kim, B.S. Park, J.H. Sung, J.M. Park, S.B. Kwak, and S.J. Park Wound healing effect of adipose-derived stem cells: a critical role of secretory factors on human dermal fibroblasts J. Dermatol. Sci. 48 2007 15 24
26. C. Nie, D. Yang, J. Xu, Z. Si, X. Jin, and J. Zhang Locally administered adipose-derived stem cells accelerate wound healing through differentiation and vasculogenesis Cell Transplant. 20 2011 205 216
27. D. Kim, E. Monaco, A. Maki, A.S. Lima, H.J. Kong, W.L. Hurley, and M.B. Wheeler Morphologic and transcriptomic comparison of adipose- and bone-marrow-derived porcine stem cells cultured in alginate hydrogels Cell Tissue Res. 341 2010 359 370
28. L. Li, K.M. Fukunaga, H. Yu, X. Xu, J. Kong, J.T. Lee, and M. Herlyn Human dermal stem cells differentiate into functional epidermal melanocytes J. Cell Sci. 123 2010 853 860
29. P. Carmeliet, and A. Luttun The emerging role of the bone marrow-derived stem cells in [therapeutic] angiogenesis Haemost. Thromb. 86 2001 289 297 (Pubitemid 32663959)
30. D.S. Kwon, X. Gao, Y.B. Liu, D.S. Dulchavsky, A.L. Danyluk, M. Bansal, M. Chopp, K. McIntosh, A.S. Arbab, S.A. Dulchavsky, and S.C. Gautam Treatment with bone marrow-derived stromal cells accelerates wound healing in diabetic rats Int. Wound J. 5 2008 453 463 (Pubitemid 351874520)
31. Y. Xin, Y.M. Wang, H. Zhang, J. Li, W. Wang, Y.J. Wei, and S.S. Hu Aging adversely impacts biological properties of human bone marrow-derived mesenchymal stem cells: implications for tissue engineering heart valve construction Artif. Organs 34 2010 215 222
32. A. Schaffler, and C. Buchler Concise review: adipose tissue-derived stromal cells-basic and clinical implications for novel cell-based therapies Stem Cells 25 2007 818 827 (Pubitemid 46572577)
33. S. Liu, H. Zhang, X. Zhang, W. Lu, X. Huang, H. Xie, J. Zhou, W. Wang, Y. Zhang, Y. Liu, Z. Deng, and Y. Jin Synergistic angiogenesis promoting effects of extracellular matrix scaffolds and adipose-derived stem cells during wound repair Tissue Eng. Part A 17 2011 725 739
34. R. Dong, X. Liu, Y. Liu, Z. Deng, X. Nie, X. Wang, and Y. Jin Enrichment of epidermal stem cells by rapid adherence and analysis of the reciprocal interaction of epidermal stem cells with neighboring cells using an organotypic system Cell Biol. Int. 31 2007 733 740 (Pubitemid 46765130)
35. J.L. Xie, T.Z. Li, S.H. Qi, B. Huang, X.G. Chen, and J.D. Chen A study of using tissue-engineered skin reconstructed by candidate epidermal stem cells to cover the nude mice with full-thickness skin defect J. Plast. Reconstr. Aesthet. Surg. 60 2007 983 990 (Pubitemid 47087212)
36. A.J. Gharzi, and C.A. Reynolds Plasticity of hair follicle dermal cells in wound healing and induction Exp. Dermatol. 12 2003 126 136
37. W.B. Slayton, X.M. Li, J. Butler, S.M. Guthrie, M.L. Jorgensen, J.R. Wingard, and E.W. Scott The role of the donor in the repair of the marrow vascular niche following hematopoietic stem cell transplant Stem Cells 25 2007 2945 2955 (Pubitemid 350127880)
38. X.B. Fu, and X.Y. Sun Can hematopoietic stem cells be an alternative source for skin regeneration? Ageing Res. Rev. 8 2009 244 249
39. R. Higashiyama, Y. Inagaki, Y.Y. Hong, M. Kushida, S. Nakao, M. Niioka, T. Watanabe, H. Okano, Y. Matsuzaki, G. Shiota, and I. Okazaki Bone marrow-derived cells express matrix metalloproteinases and contribute to regression of liver fibrosis in mice Hepatology 45 2007 213 222 (Pubitemid 46144381)
40. A.J. Wagers, R.I. Sherwood, J.L. Christensen, and I.L. Weissman Little evidence for developmental plasticity of adult hematopoietic stem cells Science 297 2002 2256 2259
41. J.M. Nygren, S. Jovinge, M. Breitbach, P. Sawen, W. Roll, J. Hescheler, J. Taneera, B.K. Fleischmann, and S.E. Jacobsen Bone marrow-derived hematopoietic cells generate cardiomyocytes at a low frequency through cell fusion, but not transdifferentiation Nat. Med. 10 2004 494 501 (Pubitemid 38667908)
42. F.M. Chen, M. Zhang, and Z.F. Wu Toward delivery of multiple growth factors in tissue engineering Biomaterials 31 2010 6279 6308
43. E.H. Young, C. Duplaa, R. Katz, T. Thompson, K.C. Hawkins, A.N. Boev, N.L. Henson, M. Heaton, R.S.D. Ashley, C. Stout, J.H. Morgan III, P.N. Uchakin, M. Rimando, G.F. Long, and C.T. Jee Adult-derived stem cells and their potential for use in tissue repair and molecular medicine J. Cell. Mol. Med. 9 2005 753 769 (Pubitemid 44151964)
44. S.A. Eming, T. Krieg, and J.M. Davidson Gene transfer in tissue repair: status, challenges and future directions Expert Opin. Biol. Ther. 4 2004 1373 1386 (Pubitemid 39222971)
45. J.C. Vogel Nonviral skin gene therapy Hum. Gene Ther. 11 2000 2253 2259
46. Y.L. Hu, Y.H. Fu, Y. Tabata, and J.Q. Gao Mesenchymal stem cells: a promising targeted-delivery vehicle in cancer gene therapy J. Control. Release 147 2010 154 162
47. B. Hall, M. Andreeff, and F. Marini The participation of mesenchymal stem cells in tumor stroma formation and their application as targeted-gene delivery vehicles Handb. Exp. Pharmacol. 180 2007 263 283
48. X. Guo, Q. Zheng, S. Yang, Z. Shao, Q. Yuan, Z. Pan, S. Tang, K. Liu, and D. Quan Repair of full-thickness articular cartilage defects by cultured mesenchymal stem cells transfected with the transforming growth factor beta1 gene Biomed. Mater. 1 2006 206 215 (Pubitemid 46217612)
49. M. Waterhouse, M. Themeli, H. Bertz, N. Zoumbos, J. Finke, and A. Spyridonidis Horizontal DNA transfer from donor to host cells as an alternative mechanism of epithelial chimerism after allogeneic hematopoietic cell transplantation Biol. Blood Marrow Transplant. 17 2011 319 329
50. A. Hadjantonakis, and V. Papaioannou The stem cells of early embryos Differentiation 68 2001 159 166 (Pubitemid 33754988)
51. T.C. Mackenzie, and A.W. Flake Human mesenchymal stem cells persist, demonstrate site-specific multipotential differentiation, and are present in sites of wound healing and tissue regeneration after transplantation into fetal sheep Blood Cells Mol. Dis. 27 2001 601 604 (Pubitemid 32757054)
52. M.F. Pittenger, A.M. Mackay, S.C. Beck, R.K. Jaiswal, R. Douglas, J.D. Mosca, M.A. Moorman, D.W. Simonetti, S. Craig, and D.R. Marshak Multilineage potential of adult human mesenchymal stem cells Science 284 1999 143 147 (Pubitemid 29282067)
53. J. Chan, K. O'Donoghue, J. Fuente, I.A. Robert, S. Kumar, J.E. Morgan, and N.M. Fisk Human fetal mesenchymal stem cells as vehicles for gene delivery Stem Cells 23 2005 93 102 (Pubitemid 40105295)
54. T. Saito, J.Q. Kuang, B. Bittira, A.A. Khaldi, and R.C.J. Chiu Xenotransplant cardiac chimera: immune tolerance of adult stem cells Ann. Thorac. Surg. 74 2002 19 24 (Pubitemid 34741999)
55. M. Studeny, F.C. Marini, R.E. Champlin, C. Zompetta, I.J. Fidler, and M. Andreeff Bone marrow-derived mesenchymal stem cells as vehicles for interferon-beta delivery into tumors Cancer Res. 62 2002 3603 3608 (Pubitemid 34728832)
56. S.A. Collins, B.A. Guinn, P.T. Harrison, M.F. Scallan, G.C. O'Sullivan, and M. Tangney Viral vectors in cancer immunotherapy: which vector for which strategy? Curr. Gene Ther. 8 2008 66 78
57. C.B. Doering Retroviral modification of mesenchymal stem cells for gene therapy of hemophilia Methods Mol. Biol. 433 2008 203 212
58. T. Hirsch, P.S. Von, G.B. Du, D. Mittler, F. Jacobsen, M. Lehnhardt, E. Eriksson, H.U. Steinau, and L. Steinstraesser Adenoviral gene delivery to primary human cutaneous cells and burn wounds Mol. Med. 12 2006 199 207 (Pubitemid 44925018)
59. W.I. Lee, H. Heo, O. Shin, Y.K. Kwon, and H. Lee Stable gene expression by self-complementary adeno-associated viruses in human MSCs Biochem. Biophys. Res. Commun. 360 2007 573 579 (Pubitemid 47048138)
60. D. Lechardeur, A.S. Verkman, and G.L. Lukacs Intracellular routing of plasmid DNA during non-viral gene transfer Adv. Drug Deliv. Rev. 57 2005 755 767 (Pubitemid 40332601)
61. M.R. Park, K.O. Han, I.K. Han, M.H. Cho, J.W. Nah, Y.J. Choi, and C.S. Cho Degradable polyethylenimine-alt-poly(ethylene glycol) copolymers as novel gene carriers J. Control. Release 105 2005 367 380
62. T.G. Park, J.H. Jeong, and S.W. Kim Current status of polymeric gene delivery systems Adv. Drug Deliv. Rev. 58 2006 467 486 (Pubitemid 43949425)
63. G.P. Tang, J.M. Zeng, S.J. Gao, Y.X. Ma, L. Shi, Y. Li, H.P. Too, and S. Wang Polyethylene glycol modified polyethylenimine for improved CNS gene transfer: effects of PEGylation extent Biomaterials 24 2003 2351 2362 (Pubitemid 36434055)
64. G.P. Tang, H.Y. Guo, F. Alexis, X. Wang, S. Zeng, T.M. Lim, J. Ding, Y.Y. Yang, and S. Wang Low molecular weight polyethylenimines linked by beta-cyclodextrin for gene transfer into the nervous system J. Gene Med. 6 2006 736 744
65. Q.Q. Zhao, J.L. Chen, T.F. Lv, C.X. He, G.P. Tang, W.Q. Liang, Y. Tabata, and J.Q. Gao N/P ratio significantly influences the transfection efficiency and cytotoxicity of a polyethylenimine/chitosan/DNA complex biol Pharm. Bull. 32 2009 706 710
66. J. Jo, A. Okazaki, K. Nagane, M. Yamamoto, and Y. Tabata Preparation of cationized polysaccharides as gene transfection carrier for bone marrow-derived mesenchymal stem cells J. Biomater. Sci. Polym. Ed. 21 2010 185 204
67. I. Kanatani, T. Ikai, A. Okazaki, J. Jo, M. Yamamoto, M. Imamura, A. Kanematsu, S. Yamamoto, N. Ito, O. Ogawa, and Y. Tabata Efficient gene transfer by pullulan-spermine occurs through both clathrin- and raft/caveolae-dependent mechanisms J. Control. Release 116 2006 75 82 (Pubitemid 44792302)
68. Y.Z. Chen, X.L. Yao, Y. Tabata, S. Nakagawa, J.Q. Gao, Gene carriers and transfection systems used in the recombination of dendritic cells for effective cancer immunotherapy, Clin. Dev. Immunol. (in press) doi: 10.1155/2010/565643.
69. K. Nagane, J. Jo, and Y. Tabata Promoted adipogenesis of rat mesenchymal stem cells by transfection of small interfering RNA complexed with a cationized dextran Tissue Eng. Part A 16 2010 21 31
70. D.K. Thakor, Y.D. Teng, H. Obata, K. Nagane, S. Saito, and Y. Tabata Nontoxic genetic engineering of mesenchymal stem cells using serum-compatible pullulan-spermine/DNA anioplexes Tissue Eng. Part C Methods 17 2011 131 144
71. J. Jo, N. Nagaya, Y. Miyahara, M. Kataoka, S.M. Harada, K. Kangawa, and Y. Tabata Transplantation of genetically engineered mesenchymal stem cells improves cardiac function in rats with myocardial infarction: benefit of a novel nonviral vector, cationized dextran Tissue Eng. 13 2007 313 322
72. A. Okazaki, J. Jo, and Y. Tabata A reverse transfection technology to genetically engineer adult stem cells Tissue Eng. 13 2007 245 251
73. L. Garcia, M. Bunuales, N. Duzgunes, and T.D. Ilarduya Serum-resistant lipopolyplexes for gene delivery to liver tumour cells Eur. J. Pharm. Biopharm. 67 2007 58 66 (Pubitemid 46991330)
74. S.J. Bruce, B.B. Gardiner, L.J. Burke, M.M. Gongora, S.M. Grimmond, and A.C. Perkins Dynamic transcription programs during ES cell differentiation towards mesoderm in serum versus serum-freeBMP4 culture BMC Genomics 8 2007 365 391
75. J. Jo, N. Nagaya, Y. Miyahara, M. Kataoka, M. Harada-Shiba, K. Kangawa, and Y. Tabata Transplantation of genetically engineered mesenchymal stem cells improves cardiac function in rats with myocardial infarction: benefit of a novel nonviral vector, cationized dextran Tissue Eng. 13 2007 313 322
76. E.J. Wallenstein, J. Barminko, R.S. Schloss, and M.L. Yarmush Serum starvation improves transient transfection efficiency in differentiating embryonic stem cells Biotechnol. Prog. 26 2010 1714 1723
77. L. Garcia, M. Bunuales, and N. Duzgunes Serum-resistant lipopolyplexes for gene delivery to liver tumour cells Eur. J. Pharm. Biopharm. 67 2007 58 66 (Pubitemid 46991330)
78. C.X. He, N. Li, Y.L. Hu, X.M. Zhu, H.J. Li, M. Han, P.H. Miao, Z.J. Hu, G. Wang, W.Q. Liang, Y. Tabata, and J.Q. Gao Effective gene delivery to mesenchymal stem cells based on the reverse transfection and three-dimensional cell culture system Pharm. Res. 28 2011 1577 1590
79. J. Bonadio, E. Smiley, P. Patil, and S. Goldstein Localized, direct plasmid gene delivery in vivo: prolonged therapy results in reproducible tissue regeneration Nat. Med. 5 1999 753 759 (Pubitemid 29318608)
80. J. Bonadio Tissue engineering via local gene delivery J. Mol. Med. 78 2000 303 311
81. H. Hosseinkhani, T. Azzam, H. Kobayashi, Y. Hiraoka, H. Shimokawa, A. Domb, and Y. Tabata Combination of 3D tissue engineered scaffold and non-viral gene carrier enhance in vitro DNA expression of mesenchymal stem cells Biomaterials 27 2006 4269 4278 (Pubitemid 44294360)
82. H.J. Kong, J. Liu, K. Riddle, T. Matsumoto, K. Leach, and D.J. Mooney Non-viral gene delivery regulated by stiffness of cell adhesion substrates Nat. Mater. 4 2005 460 464 (Pubitemid 40774051)
83. J. Zhang, Y.J. Duan, D. Wei, L.Y. Wang, H.J. Wang, Z.W. Gu, and D.L. Kong Co-electrospun fibrous scaffold-adsorbed DNA for substrate-mediated gene delivery J. Biomed. Mater. Res. A 96A 2010 212 220
84. K.M. Woo, V.J. Chen, and P.X. Ma Nano-fibrous scaffolding architecture selectively enhances protein adsorption contributing to cell attachment J. Biomed. Mater. Res. 67A 2003 531 537 (Pubitemid 37522460)
85. W. Ji, Y. Sun, F. Yang, J.J. van den Beucken, M. Fan, Z. Chen, and J.A. Jansen Bioactive electrospun scaffolds delivering growth factors and genes for tissue engineering applications Pharm. Res. 28 2011 1259 1272
86. A. Saraf, L.S. Baggett, R.M. Raphael, F.K. Kasper, and A.G. Mikos Regulated non-viral gene delivery from coaxial electrospun fiber mesh scaffolds J. Control. Release 143 2009 95 103
87. A. Weinand, M. Nabili, J.R. Khumar, J.R. Dunn, J.C. Roman, M.H. Jeng, and Y. Tabata Factors of osteogenesis influencing various human stem cells on third-generation gelatin/b-tricalcium phosphate scaffold material Rejuvenation Res. 14 2011 10.1089/rej.2010.1105
88. W.W. Thein, and R.D.K. Misra Biomimetic chitosan-nanohydroxyapatite composite scaffolds for bone tissue engineering Acta Biomater. 5 2009 1182 1197
89. X.D. Guo, Q.X. Zheng, S.H. Yang, and Z.W. Shao Repair of full-thickness articular cartilage defects by cultured mesenchymal stem cells transfected with the transforming growth factor β1 gene Biomed. Mater. 1 2006 206 215
90. H. Hall, V. Djonov, M. Ehrbar, M. Hoechli, and J.A. Hubbell Heterophilic interactions between cell adhesion molecule L1 and alphavbeta3-integrin induce HUVEC process extension in vitro and angiogenesis in vivo Angiogenesis 7 2004 213 223
91. D. Trentin, H. Hall, S. Wechsler, and J.A. Hubbell Peptide-matrixmediated gene transfer of an oxygen-sensitive hypoxia-inducible factor-1 variant for local induction of angiogenesis Proc. Natl. Acad. Sci. U. S. A. 103 2006 2506 2511
92. K. Yamahara, K. Doi, T. Kushibiki, M. Yamamoto, H. Itoh, T. Ikeda, Y. Tabata, and M. Komeda Simultaneous application of basic fibroblast growth factor and hepatocyte growth factor to enhance the blood vessels formation J. Vasc. Surg. 41 2005 82 90 (Pubitemid 40193345)
93. S. Ohya, H. Sonoda, Y. Nakayama, and T. Matsuda The potential of poly(N-isopropylacrylamide) (PNIPAM)-grafted hyaluronan and PNIPAM-grafted gelatin in the control of post-surgical tissue adhesions Biomaterials 26 2005 655 659 (Pubitemid 38988307)
94. M. Ehrbar, A. Metters, and P. Zammaretti Endothelial cell proliferation and progenitor maturation by fibrin-bound VEGF variants with differential susceptibilities to local cellular activity J. Control. Release 101 2005 93 109 (Pubitemid 39600975)
95. Y.H. An, D. Webb, A. Gutowska, V.A. Mironov, and R.J. Friedman Regaining chondrocyte phenotype in thermosensitive gel culture Anat. Rec. 263 2001 336 3341