Gelatin nanofiber matrices derived from schiff base derivative for tissue engineering applications

Journal of Biomedical Nanotechnology

Volumn 11, Issue 11, 2015, Pages 2067-2080

  Jaiswal, Devina ^a,b   James, Roshan ^a,b   Shelke, Namdev B ^a,b   Harmon, Matthew D ^a,b,c   Brown, Justin L ^d   Hussain, Fazle ^e   Kumbar, Sangamesh G ^a,b,c  

^a UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^b Institute for Regenerative Engineering   (United States)

^c UNIVERSITY OF CONNECTICUT   (United States)

^d PENNSYLVANIA STATE UNIVERSITY   (United States)

^e Department of Electrical and Computer Engineering   (United States)

Author keywords

Gelatin; Nanofibers; PCL; Schiff Base; Tissue Engineering; Wound Healing

Indexed keywords

CELL PROLIFERATION; INFRARED SPECTROSCOPY; ORGANIC POLYMERS; POLYMERS; PROTEINS; TISSUE; TISSUE ENGINEERING;

GELATIN; HYDROPHOBIC MODIFICATION; PCL; SCHIFF-BASE; SYNTHESIS AND CHARACTERIZATIONS; TISSUE ENGINEERING APPLICATIONS; VOLATILE ORGANIC SOLVENTS; WOUND HEALING;

NANOFIBERS;

2 NITROBENZYL GELATIN; GELATIN; NANOFIBER; POLYCAPROLACTONE; SCHIFF BASE; UNCLASSIFIED DRUG;

ARTICLE; BIOLOGICAL ACTIVITY; CELL ADHESION; CELL PROLIFERATION; CELL PROLIFERATION ASSAY; CELL SPREADING; CELL STRUCTURE; CELL VIABILITY; CHEMICAL MODIFICATION; ELECTROSPINNING; HUMAN; HUMAN CELL; HYDROPHOBICITY; INFRARED SPECTROSCOPY; MESENCHYMAL STEM CELL; NANOFABRICATION; PHOTOACTIVATION; SCANNING ELECTRON MICROSCOPY; SKELETAL MUSCLE; TISSUE ENGINEERING; ULTRAVIOLET RADIATION; CELL CULTURE; CELL SURVIVAL; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; FIBROBLAST; PROCEDURES; SKIN;

CELL PROLIFERATION; CELL SURVIVAL; CELLS, CULTURED; FIBROBLASTS; GELATIN; HUMANS; NANOFIBERS; SKIN; TISSUE ENGINEERING;

EID: 84956594083     PISSN: 15507033     EISSN: 15507041     Source Type: Journal    
DOI: 10.1166/jbn.2015.2100     Document Type: Article

References (78)

1. S. Bhattacharyya, S. G. Kumbar, Y. M. Khan, L. S. Nair, A. Singh, N. R. Krogman, P. W. Brown, H. R. Allcock, and C. T. Laurencin, Biodegradable polyphosphazene-nanohydroxyapatite composite nanofibers: Scaffolds for bone tissue engineering. J. Biomed. Nanotechnol. 5, 69 (2009).
2. J. Doshi and D. H. Reneker, Electrospinning process and applications of electrospun fibers, Journal of Electrostatics; Selected papers from the special technical session, Electrostatics in Polymer Processing and Charge Monitoring, 1993 IEEE Industry Applications Society Meeting (1995), Vol. 35, pp. 151-160.
3. R. James, S. G. Kumbar, C. T. Laurencin, G. Balian, and A. B. Chhabra, Tendon tissue engineering: Adipose-derived stem cell and GDF-5 mediated regeneration using electrospun matrix systems, Biomedical Materials, Bristol, England, 6, 025011-026041/025016/025012/025011, Epub. 022011 March 025024 (2011).
4. R. James, U. S. Toti, C. T. Laurencin, and S. G. Kumbar, Electrospun nanofibrous scaffolds for engineering soft connective tissues.Methods in Molecular Biology (Clifton, N.J.) 726, 243 (2011).
5. S. G. Kumbar, R. James, S. P. Nukavarapu and C. T. Laurencin, Electrospun nanofiber scaffolds: Engineering soft tissues. Biomedical Materials (Bristol, England) 3, 034002-036041/034003/034003/034002. Epub. 032008 August 034008 (2008).
6. S. G. Kumbar, L. S. Nair, S. Bhattacharyya, and C. T. Laurencin, Polymeric nanofibers as novel carriers for the delivery of therapeutic molecules. J. Nanosci. Nanotechnol. 6, 2591 (2006).
7. W. J. Li, C. T. Laurencin, E. J. Caterson, R. S. Tuan, and F. K. Ko, Electrospun nanofibrous structure: A novel scaffold for tissue engineering. J. Biomed. Mater. Res. 60, 613 (2002).
8. J. A. Matthews, G. E. Wnek, D. G. Simpson, and G. L. Bowlin, Electrospinning of collagen nanofibers. Biomacromolecules 3, 232 (2002).
9. S. G. Kumbar, S. P. Nukavarapu, R. James, M. V. Hogan, and C. T. Laurencin, Recent patents on electrospun biomedical nanostructures: An overview. Recent Patents on Biomedical Engineering 1, 68 (2008).
10. A. S. Badami, M. R. Kreke, M. S. Thompson, J. S. Riffle, and A. S. Goldstein, Effect of fiber diameter on spreading, proliferation, and differentiation of osteoblastic cells on electrospun poly(lactic acid) substrates. Biomaterials 27, 596 (2006).
11. S. G. Kumbar, S. P. Nukavarapu, R. James, L. S. Nair, and C. T. Laurencin, Electrospun poly(lactic acid-co-glycolic acid) scaffolds for skin tissue engineering. Biomaterials 29, 4100 (2008).
12. D. R. Nisbet, J. S. Forsythe, W. Shen, D. I. Finkelstein, and M. K. Horne, Review paper: A review of the cellular response on electrospun nanofibers for tissue engineering. J. Biomater. Appl. 24, 7 (2009).
13. E. D. Boland, J. A. Matthews, K. J. Pawlowski, D. G. Simpson, G. E. Wnek, and G. L. Bowlin, Electrospinning collagen and elastin: Preliminary vascular tissue engineering, Frontiers in bioscience, A Journal and Virtual Library 9, 1422 (2004).
14. J. S. Choi, S. J. Lee, G. J. Christ, A. Atala, and J. J. Yoo, The influence of electrospun aligned poly(epsilon-caprolactone)/collagen nanofiber meshes on the formation of self-aligned skeletal muscle myotubes. Biomaterials 29, 2899 (2008).
15. A. Francesko and T. Tzanov, Chitin, chitosan and derivatives for wound healing and tissue engineering. Adv. Biochem. Eng./Biotechnol. 125, 1 (2011).
16. T. Jiang, S. G. Kumbar, L. S. Nair, and C. T. Laurencin, Biologically active chitosan systems for tissue engineering and regenerative medicine. Curr. Top. Med. Chem. 8, 354 (2008).
17. H. W. Kang, Y. Tabata, and Y. Ikada, Fabrication of porous gelatin scaffolds for tissue engineering. Biomaterials 20, 1339 (1999).
18. M. Li, M. J. Mondrinos, X. Chen, M. R. Gandhi, F. K. Ko, and P. I. Lelkes, Co-electrospun poly(lactide-co-glycolide), gelatin, and elastin blends for tissue engineering scaffolds. Journal of Biomedical Materials Research Part A, 79, 963 (2006).
19. Y. Z. Zhang, J. Venugopal, Z. M. Huang, C. T. Lim, and S. Ramakrishna, Characterization of the surface biocompatibil-ity of the electrospun PCL-collagen nanofibers using fibroblasts. Biomacromolecules 6, 2583 (2005).
20. C. S. Ki, D. H. Baek, K. D. Gang, K. H. Lee, I. C. Um, and Y. H. Park, Characterization of gelatin nanofiber prepared from gelatin-formic acid solution. Polymer 46, 5094 (2005).
21. J. H. Song, H. E. Kim, and H. W. Kim, Production of electrospun gelatin nanofiber by water-based co-solvent approach. Journal of Materials Science. Materials in Medicine 19, 95 (2008).
22. H. Fong, I. Chun, and D. H. Reneker, Beaded nanofibers formed during electrospinning. Polymer 40, 4585 (1999).
23. M. W. Frey, Electrospinning Cellulose and Cellulose Derivatives. Polymer Reviews 48, 378 (2008).
24. Y. Zhou, H. Yang, X. Liu, J. Mao, S. Gu, and W. Xu, Electrospinning of carboxyethyl chitosan/poly(vinyl alcohol)/silk fibroin nanoparti-cles for wound dressings. Int. J. Biol. Macromol. 53, 88 (2013).
25. W. He, T. Yong, W. E. Teo, Z. Ma, and S. Ramakrishna, Fabrication and endothelialization of collagen-blended biodegradable polymer nanofibers: Potential vascular graft for blood vessel tissue engineering. Tissue Eng. 11, 1574 (2005).
26. J.-W. Lu, Y.-L. Zhu, Z.-X. Guo, P. Hu, and J. Yu, Electrospinning of sodium alginate with poly(ethylene oxide). Polymer 47, 8026 (2006).
27. M. V. Jose, V. Thomas, D. R. Dean, and E. Nyairo, Fabrication and characterization of aligned nanofibrous PLGA/Collagen blends as bone tissue scaffolds. Polymer 50, 3778 (2009).
28. H. W. Kim, J. H. Song, and H. E. Kim, Nanofiber generation of gelatin? Hydroxyapatite biomimetics for guided tissue regeneration. Adv. Funct. Mater. 15, 1988 (2005).
29. R. Narayani and K. Panduranga Rao, Biodegradable microspheres using two different gelatin drug conjugates for the controlled delivery of methotrexate. Int. J. Pharm. 128, 261 (1996).
30. J. Y. Lai, Biocompatibility of chemically cross-linked gelatin hydro-gels for ophthalmic use. Journal of Materials Science. Materials in Medicine 21, 1899 (2010).
31. S. E. Noorjahan and T. P. Sastry, An in vivo study of hydrogels based on physiologically clotted fibrin-gelatin composites as wound-dressing materials. Journal of Biomedical Materials Research Part B: Applied Biomaterials 71B, 305 (2004).
32. K. R. Stevens, N. J. Einerson, J. A. Burmania, and W. J. Kao, In vivo biocompatibility of gelatin-based hydrogels and interpenetrating networks. Journal of Biomaterials Science. Polymer Edition 13, 1353 (2002).
33. M. Cheng, J. Deng, F. Yang, Y. Gong, N. Zhao, and X. Zhang, Study on physical properties and nerve cell affinity of composite films from chitosan and gelatin solutions. Biomaterials 24, 2871 (2003).
34. N. Choktaweesap, K. Arayanarakul, D. Aht-Ong, C. Meechaisue and P. Supaphol, Electrospun gelatin fibers: Effect of solvent system on morphology and fiber diameters. Polym. J. 39, 622 (2007).
35. Z.-M. Huang, Y. Z. Zhang, S. Ramakrishna, and C. T. Lim, Elec-trospinning and mechanical characterization of gelatin nanofibers. Polymer 45, 5361 (2004).
36. S.-Y. Gu, Z.-M. Wang, J. Ren, and C.-Y. Zhang, Electrospinning of gelatin and gelatin/poly(l-lactide) blend and its characteristics for wound dressing. Mater. Sci. Eng.: C 29, 1822 (2009).
37. A. Bigi, G. Cojazzi, S. Panzavolta, K. Rubini, and N. Roveri, Mechanical and thermal properties of gelatin films at different degrees of glutaraldehyde crosslinking. Biomaterials 22, 763 (2001).
38. Y. Liu, L. Ma, and C. Gao, Facile fabrication of the glutaraldehyde cross-linked collagen/chitosan porous scaffold for skin tissue engineering. Mater. Sci. Eng.: C 32, 2361 (2012).
39. D. N. Heo, D. H. Yang, J. B. Lee, M. S. Bae, J. H. Kim, S. H. Moon, H. J. Chun, C. H. Kim, H. N. Lim, and I. K. Kwon, Burn-wound healing effect of gelatin/polyurethane nanofiber scaffold containing silver-sulfadiazine. J. Biomed. Nanotechnol. 9, 511 (2013).
40. H.-W. Kim, H.-S. Yu, and H.-H. Lee, Nanofibrous matrices of poly(lactic acid) and gelatin polymeric blends for the improvement of cellular responses. Journal of Biomedical Materials Research Part A 87A, 25 (2008).
41. S. Gautam, A. K. Dinda, and N. C. Mishra, Fabrication and characterization of PCL/gelatin composite nanofibrous scaffold for tissue engineering applications by electrospinning method, Mater. Sci. Eng. C, Materials for Biological Applications 33, 1228 (2013).
42. E. J. Chong, T. T. Phan, I. J. Lim, Y. Z. Zhang, B. H. Bay, S. Ramakrishna, and C. T. Lim, Evaluation of electrospun PCL/gelatin nanofibrous scaffold for wound healing and layered dermal reconstitution. Acta Biomaterialia 3, 321 (2007).
43. Y. Zhang, H. Ouyang, C. T. Lim, S. Ramakrishna, and Z. M. Huang, Electrospinning of gelatin fibers and gelatin/PCL composite fibrous scaffolds. Journal of Biomedical Materials Research. Part B, Applied Biomaterials 72, 156 (2005).
44. B. Feng, H. Duan, W. Fu, Y. Cao, W. Jie Zhang, and Y. Zhang, Effect of inhomogeneity of the electrospun fibrous scaffolds of gelatin/polycaprolactone hybrid on cell proliferation. Journal of Biomedical Materials Research. Part A [Epub ahead of print] (2014).
45. B. Feng, H. Tu, H. Yuan, H. Peng, and Y. Zhang, Acetic-acid-mediated miscibility toward electrospinning homogeneous composite nanofibers of GT/PCL. Biomacromolecules 13, 3917 (2012).
46. C. N. Pace, H. Fu, K. L. Fryar, J. Landua, S. R. Trevino, B. A. Shirley, M. M. Hendricks, S. Iimura, K. Gajiwala, J. M. Scholtz, and G. R. Grimsley, Contribution of hydrophobic interactions to protein stability. J. Mol. Biol. 408, 514 (2011).
47. A. A. Nada, R. James, N. B. Shelke, M. D. Harmon, H. M. Awad, R. K. Nagarale, and S. G. Kumbar, A smart methodology to fabricate electrospun chitosan nanofiber matrices for regenerative engineering applications. Polym. Adv. Technol. 25, 507 (2014).
48. D. Jaiswal and J. L. Brown, Nanofiber diameter-dependent MAPK activity in osteoblasts. J. Biomed. Mater. Res. A 100, 2921 (2012).
49. T. Ozdemir, L.-C. Xu, C. Siedlecki, and J. L. Brown, Substrate curvature sensing through Myosin IIa upregulates early osteogenesis. Integrative Biology 5, 1407 (2013).
50. A. E. Carpenter, T. R. Jones, M. R. Lamprecht, C. Clarke, I. H. Kang, O. Friman, D. A. Guertin, J. H. Chang, R. A. Lindquist, and J. Moffat, CellProfiler: Image analysis software for identifying and quantifying cell phenotypes. Genome Biology 7, R100 (2006).
51. M. Abrigo, S. L. McArthur, and P. Kingshott, Electrospun nano-fibers as dressings for chronic wound care: Advances, challenges, and future prospects. Macromolecular Bioscience 14, 772 (2014).
52. S. Lyu, C. Huang, H. Yang, and X. Zhang, Electrospun fibers as a scaffolding platform for bone tissue repair. Journal of Orthopaedic Research: Official Publication of the Orthopaedic Research Society 31, 1382 (2013).
53. L. Soffer, X. Wang, X. Zhang, J. Kluge, L. Dorfmann, D. L. Kaplan, and G. Leisk, Silk-based electrospun tubular scaffolds for tissue-engineered vascular grafts. J. Biomater. Sci., Polym. Ed. 19, 653 (2008).
54. L. Jin, T. Wang, M. L. Zhu, M. K. Leach, Y. I. Naim, J. M. Corey, Z. Q. Feng, and Q. Jiang, Electrospun fibers and tissue engineering. J. Biomed Nanotechnol. 8, 1 (2012).
55. S. A. Sell, P. S. Wolfe, K. Garg, J. M. McCool, I. A. Rodriguez, and G. L. Bowlin, The use of natural polymers in tissue engineering: A focus on electrospun extracellular matrix analogues. Polymers 2, 522 (2010).
56. Z. Li, H. R. Ramay, K. D. Hauch, D. Xiao, and M. Zhang, Chitosan-alginate hybrid scaffolds for bone tissue engineering. Biomaterials 26, 3919 (2005).
57. W. H. Lin and W. B. Tsai. In situ UV-crosslinking gelatin electrospun fibers for tissue engineering applications. Biofabrication 5, 035008-035082/035005/035003/035008. Epub 032013 Jul 035009 (2013).
58. T. H. Nguyen and B. T. Lee, Fabrication and characterization of cross-linked gelatin electro-spun nano-fibers. Journal of Biomedical Science and Engineering 3, 1117 (2010).
59. S. G. Kumbar, A. R. Kulkarni, and T. M. Aminabhavi, Crosslinked chitosan microspheres for encapsulation of diclofenac sodium: Effect of crosslinking agent. J. Microencapsulation 19, 173 (2002).
60. J. M. Allen, S. K. Allen, and S. W. Baertschi, 2-Nitrobenzaldehyde: A convenient UV-A and UV-B chemical actinometer for drug pho-tostability testing. J. Pharm. Biomed. Anal. 24, 167 (2000).
61. E. S. Galbavy, K. Ram, and C. Anastasio, 2-Nitrobenzaldehyde as a chemical actinometer for solution and ice photochemistry. J. Pho-tochem. Photobiol. A: Chemistry 209, 186 (2010).
62. C. Longstaff, R. D. Calhoon, and R. R. Rando, Deprotonation of the Schiff base of rhodopsin is obligate in the activation of the G protein. Proc. Natl. Acad. Sci. USA 83, 4209 (1986).
63. S. G. Muhamad, First photolysis of benzidine schiff base in non aqueous solvents. International Journal of Chemistry 3, 142 (2011).
64. M. Deng, L. S. Nair, S. P. Nukavarapu, S. G. Kumbar, T. Jiang, N. R. Krogman, A. Singh, H. R. Allcock, and C. T. Laurencin, Miscibility and in vitro osteocompatibility of biodegradable blends of poly[(ethyl alanato) (p-phenyl phenoxy) phosphazene] and poly(lactic acid-glycolic acid). Biomaterials 29, 337 (2008).
65. R. A. de Carvalho, and C. R. F. Grosso, Characterization of gelatin based films modified with transglutaminase, glyoxal and formaldehyde. Food Hydrocolloids 18, 717 (2004).
66. V. Micard, R. Belamri, M. H. Morel, and S. Guilbert, Properties of chemically and physically treated wheat gluten films. J. Agric. Food. Chem. 48, 2948 (2000).
67. V. Guarino, M. Alvarez-Perez, V. Cirillo, and L. Ambrosio, hMSC interaction with PCL and PCL/gelatin platforms: A comparative study on films and electrospun membranes. Journal of Bioactive and Compatible Polymers 26, 144 (2011).
68. N. S. Binulal, A. Natarajan, D. Menon, V. K. Bhaskaran, U. Mony, and S. V. Nair, PCL-gelatin composite nanofibers electrospun using diluted acetic acid-ethyl acetate solvent system for stem cell-based bone tissue engineering. J. Biomater. Sci. Polym. Ed. 25, 325 (2014).
69. Z. X. Cai, X. M. Mo, K. H. Zhang, L. P. Fan, A. L. Yin, C. L. He, and H. S. Wang, Fabrication of chitosan/silk fibroin composite nanofibers for wound-dressing applications. International Journal of Molecular Sciences 11, 3529 (2010).
70. H. M. Powell and S. T. Boyce, Engineered human skin fabricated using electrospun collagen-PCL blends: Morphogenesis and mechanical properties. Tissue Eng. Part A 15, 2177 (2009).
71. B. Dhandayuthapani, U. M. Krishnan, and S. Sethuraman, Fabrication and characterization of chitosan-gelatin blend nanofibers for skin tissue engineering. Journal of Biomedical Materials Research. Part B, Applied Biomaterials 94, 264 (2010).
72. X. Liang and S. A. Boppart, Biomechanical properties of in vivo human skin from dynamic optical coherence elastography. IEEE Transactions on Bio-Medical Engineering 57, 953 (2010).
73. M. G. Haugh, C. M. Murphy, R. C. McKiernan, C. Altenbuchner, and F. J. O'Brien, Crosslinking and mechanical properties significantly influence cell attachment, proliferation, and migration within collagen glycosaminoglycan scaffolds. Tissue Eng. Part A 17, 1201 (2011).
74. L. S. Wang, J. Boulaire, P. P. Chan, J. E. Chung, and M. Kurisawa, The role of stiffness of gelatin-hydroxyphenylpropionic acid hydro-gels formed by enzyme-mediated crosslinking on the differentiation of human mesenchymal stem cell. Biomaterials 31, 8608 (2010).
75. P. S. Mathieu and E. G. Loboa, Cytoskeletal and focal adhesion influences on mesenchymal stem cell shape, mechanical properties, and differentiation down osteogenic, adipogenic, and chondrogenic pathways. Tissue Eng. Part B: Reviews 18, 436 (2012).
76. A. Born, M. Rottmar, S. Lischer, M. Pleskova, A. Bruinink, and K. Maniura-Weber, Correlating cell architecture with osteogenesis: First steps towards live single cell monitoring. Eur. Cell Mater. 18, 49 (2009).
77. R. McBeath, D. M. Pirone, C. M. Nelson, K. Bhadriraju, and C. S. Chen, Cell shape, cytoskeletal tension, and RhoA regulate stem cell lineage commitment. Dev. Cell 6, 483 (2004).
78. D. Docheva, D. Padula, C. Popov, W. Mutschler, H. Clausen-Schaumann, and M. Schieker, Researching into the cellular shape, volume and elasticity of mesenchymal stem cells, osteoblasts and osteosarcoma cells by atomic force microscopy. J. Cell Mol. Med. 12, 537 (2008).