Injectable gelatin derivative hydrogels with sustained vascular endothelial growth factor release for induced angiogenesis

Acta Biomaterialia

Volumn 13, Issue , 2015, Pages 88-100

  Li, Zhe ^a,b   Qu, Tiejun ^b,c   Ding, Chen ^b,d   Ma, Chi ^b   Sun, Hongchen ^e   Li, Shirong ^a   Liu, Xiaohua ^b  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

^b BAYLOR COLLEGE OF DENTISTRY   (United States)

^c FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^d SICHUAN UNIVERSITY   (China)

^e JILIN UNIVERSITY   (China)

Author keywords

Angiogenesis; Gelatin; Heparin; Injectable hydrogel; VEGF

Indexed keywords

AMINES; ANIMALS; BIOACTIVITY; BIOMECHANICS; BLOOD VESSELS; CATALYSIS; CROSSLINKING; ENDOTHELIAL CELLS; GELATION; POLYSACCHARIDES; TISSUE; TISSUE REGENERATION;

ANGIOGENESIS; GELATIN; GROWTH FACTOR; GROWTH FACTOR RELEASE; HORSE-RADISH PEROXIDASE; INJECTABLE BIOMATERIALS; INJECTABLE HYDROGELS; INJECTABLES; SOFT TISSUE; VASCULAR ENDOTHELIAL GROWTH FACTOR;

HYDROGELS;

GELATIN; HEPARIN; HORSERADISH PEROXIDASE; HYDROGEN PEROXIDE; TYRAMINE; VASCULOTROPIN; ANTICOAGULANT AGENT; DELAYED RELEASE FORMULATION; HYDROGEL; VASCULAR ENDOTHELIAL GROWTH FACTOR A, MOUSE; VASCULOTROPIN A;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOLOGICAL ACTIVITY; CATALYSIS; CELL INFILTRATION; CHORIOALLANTOIS; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CROSS LINKING; DENATURATION; GELATION; HYDROGEL; IN VITRO STUDY; INFRARED SPECTROSCOPY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; SUSTAINED DRUG RELEASE; ANIMAL; CHEMISTRY; CHICK EMBRYO; DELAYED RELEASE FORMULATION; DRUG EFFECTS; HUMAN; INTRAOCULAR DRUG ADMINISTRATION; PHARMACOLOGY; UMBILICAL VEIN ENDOTHELIAL CELL;

ANIMALIA; ARMORACIA RUSTICANA; MUS;

ANIMALS; ANTICOAGULANTS; CHICK EMBRYO; DELAYED-ACTION PREPARATIONS; GELATIN; HEPARIN; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; HYDROGELS; INJECTIONS, INTRAOCULAR; MICE; NEOVASCULARIZATION, PHYSIOLOGIC; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84920653354     PISSN: 17427061     EISSN: 18787568     Source Type: Journal    
DOI: 10.1016/j.actbio.2014.11.002     Document Type: Article

References (56)

1. C.W. Patrick Jr. Tissue engineering strategies for adipose tissue repair Anat Rec 263 2001 361 366
2. J.H. Choi, J.M. Gimble, K. Lee, K.G. Marra, J.P. Rubin, and J.J. Yoo Adipose tissue engineering for soft tissue regeneration Tissue Eng Part B 16 2010 413 426
3. 14.6 Million cosmetic plastic surgery procedures performed in 2012, < http://www.plasticsurgery.org/news/press-release-archives/2013/14-million-cosmetic-plastic-surgery-procedures-performed-in-2012.html > (retrieved on 28.03.14).
4. W. Wang, B. Cao, L. Cui, J. Cai, and J. Yin Adipose tissue engineering with human adipose tissue-derived adult stem cells and a novel porous scaffold J Biomed Mater Res B Appl Biomater 101 2013 68 75
5. F. Duranti, G. Salti, B. Bovani, M. Calandra, and M.L. Rosati Injectable hyaluronic acid gel for soft tissue augmentation - a clinical and histological study Dermatol Surg 24 1998 1317 1325
6. B.L. Eppley, and B. Dadvand Injectable soft-tissue fillers: clinical overview Plast Reconstr Surg 118 2006 98E 106E
7. G. Lemperle, V. Morhenn, and U. Charrier Human histology and persistence of various injectable filler substances for soft tissue augmentation Aesthetic Plast Surg 27 2003 354 366
8. L. Christensen, V. Breiting, M. Janssen, J. Vuust, and E. Hogdall Adverse reactions to injectable soft tissue permanent fillers Aesthetic Plast Surg 29 2005 34 48
9. N.J. Lowe, C.A. Maxwell, and R. Patnaik Adverse reactions to dermal fillers: review Dermatol Surg 31 2005 1616 1625
10. A. Alhadlaq, M. Tang, and J.J. Mao Engineered adipose tissue from human mesenchymal stem cells maintains predefined shape and dimension: implications in soft tissue augmentation and reconstruction Tissue Eng 11 2005 556 566
11. A. Casadei, R. Epis, L. Ferroni, I. Tocco, C. Gardin, and E. Bressan Adipose tissue regeneration: a state of the art J Biomed Biotechnol 2012
12. S. Lendeckel, A. Jodicke, P. Christophis, K. Heidinger, J. Wolff, and J.K. Fraser Autologous stem cells (adipose) and fibrin glue used to treat widespread traumatic calvarial defects: case report J Craniomaxillofac Surg 32 2004 370 373
13. N. Torio-Padron, N. Baerlecken, A. Momeni, G.B. Stark, and J. Borges Engineering of adipose tissue by injection of human preadipocytes in fibrin Aesthetic Plast Surg 31 2007 285 293
14. M. Vermette, V. Trottier, V. Menard, L. Saint-Pierre, A. Roy, and J. Fradette Production of a new tissue-engineered adipose substitute from human adipose-derived stromal cells Biomaterials 28 2007 2850 2860
15. Z.S. Patel, M. Yamamoto, H. Ueda, Y. Tabata, and A.G. Mikos Biodegradable gelatin microparticles as delivery systems for the controlled release of bone morphogenetic protein-2 Acta Biomater 4 2008 1126 1138
16. J.R. Sarkanen, V. Kaila, B. Mannerstrom, S. Raty, H. Kuokkanen, and S. Miettinen Human adipose tissue extract induces angiogenesis and adipogenesis in vitro Tissue Eng Part A 18 2012 17 25
17. A.V. Vashi, K.M. Abberton, G.P. Thomas, W.A. Morrison, A.J. O'Connor, and J.J. Cooper-White Adipose tissue engineering based on the controlled release of fibroblast growth factor-2 in a collagen matrix Tissue Eng 12 2006 3035 3043
18. J.H. Kang, J.M. Gimble, and D.L. Kaplan In vitro 3D model for human vascularized adipose tissue Tissue Eng Part A 15 2009 2227 2236
19. J.R. Sarkanen, P. Ruusuvuori, H. Kuokkanen, T. Paavonen, and T. Ylikomi Bioactive acellular implant induces angiogenesis and adipogenesis and sustained soft tissue restoration in vivo Tissue Eng Part A 18 2012 2568 2580
20. Y. Tabata, and Y. Ikada Protein release from gelatin matrices Adv Drug Deliv Rev 31 1998 287 301
21. X. Liu, L.A. Smith, J. Hu, and P.X. Ma Biomimetic nanofibrous gelatin/apatite composite scaffolds for bone tissue engineering Biomaterials 30 2009 2252 2258
22. X.H. Liu, and P.X. Ma Phase separation, pore structure, and properties of nanofibrous gelatin scaffolds Biomaterials 30 2009 4094 4103
23. Y. Sun, Y. Jiang, Q.J. Liu, T. Gao, J.Q. Feng, and P. Dechow Biomimetic engineering of nanofibrous gelatin scaffolds with noncollagenous proteins for enhanced bone regeneration Tissue Eng Part A 19 2013 1754 1763
24. T. Mazaki, Y. Shiozaki, K. Yamane, A. Yoshida, M. Nakamura, and Y. Yoshida A novel, visible light-induced, rapidly cross-linkable gelatin scaffold for osteochondral tissue engineering Sci Rep 4 2014 4457
25. R. Dash, M. Foston, and A.J. Ragauskas Improving the mechanical and thermal properties of gelatin hydrogels cross-linked by cellulose nanowhiskers Carbohydr Polym 91 2013 638 645
26. S. Sakai, K. Hirose, K. Taguchi, Y. Ogushi, and K. Kawakami An injectable, in situ enzymatically gellable, gelatin derivative for drug delivery and tissue engineering Biomaterials 30 2009 3371 3377
27. A.A. Amini, and L.S. Nair Enzymatically cross-linked injectable gelatin gel as osteoblast delivery vehicle J Bioact Compat Pol 27 2012 342 355
28. H.P. Gerber, K.J. Hillan, A.M. Ryan, J. Kowalski, G.A. Keller, and L. Rangell VEGF is required for growth and survival in neonatal mice Development 126 1999 1149 1159
29. P. Carmeliet, and R.K. Jain Molecular mechanisms and clinical applications of angiogenesis Nature 473 2011 298 307
30. S. Singh, B.M. Wu, and J.C.Y. Dunn The enhancement of VEGF-mediated angiogenesis by polycaprolactone scaffolds with surface cross-linked heparin Biomaterials 32 2011 2059 2069
31. K. Ono, H. Hattori, S. Takeshita, A. Kurita, and M. Ishihara Structural features in heparin that interact with VEGF(165) and modulate its biological activity Glycobiology 9 1999 705 711
32. D.B. Pike, S.S. Cai, K.R. Pomraning, M.A. Firpo, R.J. Fisher, and X.Z. Shu Heparin-regulated release of growth factors in vitro and angiogenic response in vivo to implanted hyaluronan hydrogels containing VEGF and bFGF Biomaterials 27 2006 5242 5251
33. K.M. Park, K.S. Ko, Y.K. Joung, H. Shin, and K.D. Park In situ cross-linkable gelatin-poly(ethylene glycol)-tyramine hydrogel via enzyme-mediated reaction for tissue regenerative medicine J Mater Chem 21 2011 13180 13187
34. X.H. Liu, L. Smith, G.B. Wei, Y.J. Won, and P.X. Ma Surface engineering of nano-fibrous poly(L-Lactic Acid) scaffolds via self-assembly technique for bone tissue engineering J Biomed Nanotechnol 1 2005 54 60
35. X.H. Liu, Y.J. Won, and P.X. Ma Surface engineering of nano-fibrous biodegradable poly(L-lactic acid) scaffolds for tissue engineering J. Aizenberg, W.J. Landis, C. Orme, R. Wang, Biological and bioinspired materials and devices 2004 Materials Research Society Warrendale, PA 243 248
36. X.H. Liu, Y.J. Won, and P.X. Ma Surface modification of interconnected porous scaffolds J Biomed Mater Res, Part A 74A 2005 84 91
37. G.C. Steffens, C. Yao, P. Prevel, M. Markowicz, P. Schenck, and E.M. Noah Modulation of angiogenic potential of collagen matrices by covalent incorporation of heparin and loading with vascular endothelial growth factor Tissue Eng 10 2004 1502 1509
38. A.J. Kuijpers, G.H. Engbers, J. Krijgsveld, S.A. Zaat, J. Dankert, and J. Feijen Cross-linking and characterisation of gelatin matrices for biomedical applications J Biomater Sci Polym Ed 11 2000 225 243
39. M. Gumusderelioglu, and S. Aday Heparin-functionalized chitosan scaffolds for bone tissue engineering Carbohydr Res 346 2011 606 613
40. K.M. Park, Y.M. Shin, Y.K. Joung, H. Shin, and K.D. Park In situ forming hydrogels based on tyramine conjugated 4-Arm-PPO-PEO via enzymatic oxidative reaction Biomacromolecules 11 2010 706 712
41. R. Jin, L.S. Moreira Teixeira, P.J. Dijkstra, M. Karperien, C.A. van Blitterswijk, and Z.Y. Zhong Injectable chitosan-based hydrogels for cartilage tissue engineering Biomaterials 30 2009 2544 2551
42. T.J. Qu, and X.H. Liu Nano-structured gelatin/bioactive glass hybrid scaffolds for the enhancement of odontogenic differentiation of human dental pulp stem cells J Mater Chem B 1 2013 4764 4772
43. T. Matsumoto, S. Bohman, J. Dixelius, T. Berge, A. Dimberg, and P. Magnusson VEGF receptor-2 Y951 signaling and a role for the adapter molecule TSAd in tumor angiogenesis EMBO J 24 2005 2342 2353
44. R. Bhattacharya, J. Kwon, X. Li, E. Wang, S. Patra, and J.P. Bida Distinct role of PLCbeta3 in VEGF-mediated directional migration and vascular sprouting J Cell Sci 122 2009 1025 1034
45. S. Singh, B.M. Wu, and J.C. Dunn Delivery of VEGF using collagen-coated polycaprolactone scaffolds stimulates angiogenesis J Biomed Mater Res A 100 2012 720 727
46. A. Bronckaers, P. Hilkens, Y. Fanton, T. Struys, P. Gervois, and C. Politis Angiogenic properties of human dental pulp stem cells PLoS One 8 2013 e71104
47. A.F. Martins, A.G.B. Pereira, A.R. Fajardo, A.F. Rubira, and E.C. Muniz Characterization of polyelectrolytes complexes based on N,N,N-trimethyl chitosan/heparin prepared at different pH conditions Carbohydr Polym 86 2011 1266 1272
48. A.L. Gao, F. Liu, and L.X. Xue Preparation and evaluation of heparin-immobilized poly (lactic acid) (PLA) membrane for hemodialysis J Membr Sci 452 2014 390 399
49. J.L. Wang, W. Hu, Q. Liu, and S.M. Zhang Dual-functional composite with anticoagulant and antibacterial properties based on heparinized silk fibroin and chitosan Colloid Surf B 85 2011 241 247
50. F. Namvar, R. Mohamad, J. Baharara, S. Zafar-Balanejad, F. Fargahi, and H.S. Rahman Antioxidant, antiproliferative, and antiangiogenesis effects of polyphenol-rich seaweed (Sargassum muticum) Biomed Res Int 2013 2013 604787
51. W.A. Bubnis, and C.M. Ofner The determination of epsilon-amino groups in soluble and poorly soluble proteinaceous by a spectrophotometric method using trinitrobenzenesulfonic acid Anal Biochem 207 1992 129 133
52. R. Kale, and A. Bajaj Ultraviolet spectrophotometric method for determination of gelatin crosslinking in the presence of amino groups J Young Pharm 2 2010 90 94
53. I. Capila, and R.J. Linhardt Heparin-protein interactions Angew Chem Int Ed 41 2002 391 412
54. H. Gitaygoren, S. Soker, I. Vlodavsky, and G. Neufeld The binding of vascular endothelial growth factor to its receptors is dependent on cell surface-associated heparin-like molecules J Biol Chem 267 1992 6093 6098
55. S. Nakamura, T. Kubo, and H. Ijima Heparin-conjugated gelatin as a growth factor immobilization scaffold J Biosci Bioeng 115 2013 562 567
56. O. Oliviero, M. Ventre, and P.A. Netti Functional porous hydrogels to study angiogenesis under the effect of controlled release of vascular endothelial growth factor Acta Biomater 8 2012 3294 3301