Collagen functionalized bioactive nanofiber matrices for osteogenic differentiation of mesenchymal stem cells: Bone tissue engineering

Journal of Biomedical Nanotechnology

Volumn 10, Issue 2, 2014, Pages 287-298

  Cheng, Yixing ^a,b   Ramos, Daisy ^c,d,e   Lee, Paul ^a   Liang, Danni ^a   Yu, Xiaojun ^a   Kumbar, Sangamesh G ^c,d,e  

^a Stevens Institute of Technology   (United States)

^b UNIVERSITY OF SOUTH CAROLINA   (United States)

^c UNIVERSITY OF CONNECTICUT HEALTH CENTER   (United States)

^d Institute for Regenerative Engineering   (United States)

^e UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

Bone; Chitosan; Collagen; Nanofibers; Polycaprolactone (PCL); Scaffolds; Stem Cells; Tissue Engineering

Indexed keywords

ALKALINE PHOSPHATASE ACTIVITY; BONE TISSUE ENGINEERING; COLLAGEN IMMOBILIZATION; ELECTROSPINNING PARAMETERS; ELECTROSPUN NANOFIBERS; GENE EXPRESSION PROFILES; OSTEOGENIC DIFFERENTIATION; TISSUE ENGINEERING APPLICATIONS;

BONE; CELL CULTURE; CHITOSAN; COLLAGEN; GENE EXPRESSION; NANOFIBERS; PHOSPHATASES; POLYCAPROLACTONE; SCAFFOLDS; STEM CELLS; TISSUE; TISSUE ENGINEERING;

SCAFFOLDS (BIOLOGY);

ALKALINE PHOSPHATASE; CHITOSAN; COLLAGEN TYPE 1; CYANAMIDE; NANOFIBER; OSTEOCALCIN; OSTEOPONTIN; POLYCAPROLACTONE; POLYMER;

ADSORPTION KINETICS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BONE DEVELOPMENT; BONE MARROW CELL; BONE MARROW DERIVED STROMAL CELL; BONE MINERALIZATION; BONE TISSUE; CELL ADHESION; CELL DIFFERENTIATION; CELL FUNCTION; CELL ISOLATION; CONTROLLED STUDY; CROSS COUPLING REACTION; DRUG DELIVERY SYSTEM; ELECTROSPINNING; ENZYME ACTIVITY; GENE EXPRESSION PROFILING; IMMOBILIZATION; MESENCHYMAL STEM CELL; NANOFABRICATION; NONHUMAN; PARTICLE SIZE; PHENOTYPE; PHYSICAL CHEMISTRY; POLYMERIZATION; STROMA CELL; TISSUE ENGINEERING;

ALKALINE PHOSPHATASE; ANIMALS; BIOCOMPATIBLE MATERIALS; BIOLOGICAL MARKERS; BONE AND BONES; CALCIUM; CELL ADHESION; CELL COUNT; CELL DIFFERENTIATION; CELL MOVEMENT; CELL PROLIFERATION; CHITOSAN; COLLAGEN; FLUORESCEIN-5-ISOTHIOCYANATE; GENE EXPRESSION REGULATION; IMMOBILIZED PROTEINS; MESENCHYMAL STROMAL CELLS; NANOFIBERS; OSTEOGENESIS; POLYESTERS; RATS; TISSUE ENGINEERING;

EID: 84893205476     PISSN: 15507033     EISSN: 15507041     Source Type: Journal    
DOI: 10.1166/jbn.2014.1753     Document Type: Article

References (72)

1. S.-Y. Chou, C.-M. Cheng, and P. R. LeDuc, Composite polymer systems with control of local substrate elasticity and their effect on cytoskeletal and morphological characteristics of adherent cells. Biomaterials 30, 3136 (2009).
2. J. Huang, S. V. Gräter, F. Corbellini, S. Rinck, E. Bock, R. Kemkemer, H. Kessler, J. Ding, and J. P. Spatz, Impact of order and disorder in rgd nanopatterns on cell adhesion. Nano Lett. 9, 1111 (2009).
3. V. Brunetti, G. Maiorano, L. Rizzello, B. Sorce, S. Sabella, R. Cingolani, and P. P. Pompa, Neurons sense nanoscale roughness with nanometer sensitivity. Proceedings of the National Academy of Sciences 107, 6264 (2010).
4. C. T. Laurencin, S. G. Kumbar, and S. P. Nukavarapu, Nanotechnology and orthopedics: A personal perspective. Wiley Interdisciplinary Reviews: Nanomedicine and Nanobiotechnology 1, 6 (2009).
5. O. Z. Fisher, A. Khademhosseini, R. Langer, and N. A. Peppas, Bioinspired materials for controlling stem cell fate. Accounts of Chemical Research 43, 419 (2009).
6. G. Kaur, M. T. Valarmathi, J. D. Potts, and Q. Wang, The promotion of osteoblastic differentiation of rat bone marrow stromal cells by a polyvalent plant mosaic virus. Biomaterials 29, 4074 (2008).
7. G. Kaur, C. Wang, J. Sun, and Q. Wang, The synergistic effects of multivalent ligand display and nanotopography on osteogenic differentiation of rat bone marrow stem cells. Biomaterials 31, 5813 (2010).
8. F. Guilak, D. M. Cohen, B. T. Estes, J. M. Gimble, W. Liedtke, and C. S. Chen, Control of stem cell fate by physical interactions with the extracellular matrix. Cell Stem cell 5, 17 (2009).
9. G. Kaur, M. T. Valarmathi, J. D. Potts, E. Jabbari, T. Sabo- Attwood, and Q. Wang, Regulation of osteogenic differentiation of rat bone marrow stromal cells on 2D nanorod substrates. Biomaterials 31, 1732 (2010).
10. H.-J. Shao, Y.-T. Lee, C.-S. Chen, J.-H. Wang, and T.-H. Young, Modulation of gene expression and collagen production of anterior cruciate ligament cells through cell shape changes on polycaprolactone/ chitosan blends. Biomaterials 31, 4695 (2010).
11. O. Hartman, C. Zhang, E. L. Adams, M. C. Farach-Carson, N. J. Petrelli, B. D. Chase, and J. F. Rabolt, Biofunctionalization of electrospun PCL-based scaffolds with perlecan domain IV peptide to create a 3-D pharmacokinetic cancer model. Biomaterials 31, 5700 (2010).
12. R. Ayala, C. Zhang, D. Yang, Y. Hwang, A. Aung, S. S. Shroff, F. T. Arce, R. Lal, G. Arya, and S. Varghese, Engineering the cellmaterial interface for controlling stem cell adhesion, migration, and differentiation. Biomaterials 32, 3700 (2011).
13. Y. I. Cho, J. S. Choi, S. Y. Jeong, and H. S. Yoo, Nerve growth factor (NGF)-conjugated electrospun nanostructures with topographical cues for neuronal differentiation of mesenchymal stem cells. Acta Biomaterialia 6, 4725 (2010).
14. J.-Y. Lee, J.-E. Choo, Y.-S. Choi, J.-S. Suh, S.-J. Lee, C.-P. Chung, and Y.-J. Park, Osteoblastic differentiation of human bone marrow stromal cells in self-assembled BMP-2 receptor-binding peptideamphiphiles. Biomaterials 30, 3532 (2009).
15. X. Xin, M. Hussain, and J. J. Mao, Continuing differentiation of human mesenchymal stem cells and induced chondrogenic and osteogenic lineages in electrospun PLGA nanofiber scaffold. Biomaterials 28, 316 (2007).
16. W.-J. Li, R. Tuli, X. Huang, P. Laquerriere, and R. S. Tuan, Multilineage differentiation of human mesenchymal stem cells in a threedimensional nanofibrous scaffold. Biomaterials 26, 5158 (2005).
17. V. Beachley and X. Wen, Polymer nanofibrous structures: Fabrication, biofunctionalization, and cell interactions. Prog. Polym. Sci. 35, 868 (2010).
18. S. Kumbar, R. James, S. Nukavarapu, and C. Laurencin, Electrospun nanofiber scaffolds: Engineering soft tissues. Biomedical Materials 3, 034002 (2008).
19. J.-H. Jang, O. Castano and H.-W. Kim, Electrospun materials as potential platforms for bone tissue engineering. Advanced Drug Delivery Reviews 61, 1065 (2009).
20. L. Ghasemi-Mobarakeh, M. P. Prabhakaran, M. Morshed, M.-H. Nasr-Esfahani, and S. Ramakrishna, Electrospun poly([var epsilon]-caprolactone)/gelatin nanofibrous scaffolds for nerve tissue engineering. Biomaterials 29, 4532 (2008).
21. W.-J. Li, R. Tuli, C. Okafor, A. Derfoul, K. G. Danielson, D. J. Hall and R. S. Tuan, A three-dimensional nanofibrous scaffold for cartilage tissue engineering using human mesenchymal stem cells. Biomaterials 26, 599 (2005).
22. M. S. Peach, R. James, U. S. Toti, M. Deng, N. L. Morozowich, H. R. Allcock, C. T. Laurencin, and S. G. Kumbar, Polyphosphazene functionalized polyester fiber matrices for tendon tissue engineering: In vitro evaluation with human mesenchymal stem cells. Biomedical Materials 7, 045016 (2012).
23. M. S. Peach, S. G. Kumbar, R. James, U. S. Toti, D. Balasubramaniam, M. Deng, B. Ulery, A. D. Mazzocca, M. B. McCarthy, and N. L. Morozowich, Design and optimization of polyphosphazene functionalized fiber matrices for soft tissue regeneration. Journal of Biomedical Nanotechnology 8, 107 (2012).
24. K. Ma, C. K. Chan, S. Liao, W. Y. K. Hwang, Q. Feng, and S. Ramakrishna, Electrospun nanofiber scaffolds for rapid and rich capture of bone marrow-derived hematopoietic stem cells. Biomaterials 29, 2096 (2008).
25. H. Yoshimoto, Y. M. Shin, H. Terai, and J. P. Vacanti, A biodegradable nanofiber scaffold by electrospinning and its potential for bone tissue engineering. Biomaterials 24, 2077 (2003).
26. J. Hu, X. Liu, and P. X. Ma, Induction of osteoblast differentiation phenotype on poly(l-lactic acid) nanofibrous matrix. Biomaterials 29, 3815 (2008).
27. C. Li, C. Vepari, H.-J. Jin, H. J. Kim, and D. L. Kaplan, Electrospun silk-BMP-2 scaffolds for bone tissue engineering. Biomaterials 27, 3115 (2006).
28. E. K. F. Yim, A. C. A. Wan, C. Le Visage, I. C. Liao, and K. W. Leong, Proliferation and differentiation of human mesenchymal stem cell encapsulated in polyelectrolyte complexation fibrous scaffold. Biomaterials 27, 6111 (2006).
29. J. S. Park, J. S. Chu, A. D. Tsou, R. Diop, Z. Tang, A. Wang, and S. Li, The effect of matrix stiffness on the differentiation of mesenchymal stem cells in response to TGF-[beta]. Biomaterials 32, 3921 (2011).
30. M. Deng, S. G. Kumbar, L. S. Nair, A. L. Weikel, H. R. Allcock, and C. T. Laurencin, Biomimetic Structures: Biological implications of dipeptide - substituted polyphosphazene-polyester blend nanofiber matrices for load - bearing bone regeneration. Adv. Funct. Mater. 21, 2641 (2011).
31. S. Shao, S. Zhou, L. Li, J. Li, C. Luo, J. Wang, X. Li, and J. Weng, Osteoblast function on electrically conductive electrospun PLA/MWCNTs nanofibers. Biomaterials 32, 2821 (2011).
32. M. A. Schwartz and D. W. DeSimone, Cell adhesion receptors in mechanotransduction. Current Opinion in Cell Biology 20, 551 (2008).
33. J. Chen, B. Chu, and B. S. Hsiao, Mineralization of hydroxyapatite in electrospun nanofibrous poly(L-lactic acid) scaffolds. Journal of Biomedical Materials Research Part A 79A, 307 (2006).
34. H. S. Koh, T. Yong, C. K. Chan, and S. Ramakrishna, Enhancement of neurite outgrowth using nano-structured scaffolds coupled with laminin. Biomaterials 29, 3574 (2008).
35. W. He, Z. Ma, T. Yong, W. E. Teo, and S. Ramakrishna, Fabrication of collagen-coated biodegradable polymer nanofiber mesh and its potential for endothelial cells growth. Biomaterials 26, 7606 (2005).
36. T. D. Sargeant, M. S. Rao, C.-Y. Koh, and S. I. Stupp, Covalent functionalization of NiTi surfaces with bioactive peptide amphiphile nanofibers. Biomaterials 29, 1085 (2008).
37. C. M. Valmikinathan, S. Defroda, and X. Yu, Polycaprolactone and bovine serum albumin based nanofibers for controlled release of nerve growth factor. Biomacromolecules 10, 1084 (2009).
38. A. Martins, A. R. C. Duarte, S. Faria, A. P. Marques, R. L. Reis, and N. M. Neves, Osteogenic induction of hBMSCs by electrospun scaffolds with dexamethasone release functionality. Biomaterials 31, 5875 (2010).
39. D. I. Zeugolis, S. T. Khew, E. S. Y. Yew, A. K. Ekaputra, Y. W. Tong, L.-Y. L. Yung, D. W. Hutmacher, C. Sheppard, and M. Raghunath, Electro-spinning of pure collagen nano-fibres - Just an expensive way to make gelatin? Biomaterials 29, 2293 (2008).
40. X. Pang and C.-C. Chu, Synthesis, characterization and biodegradation of functionalized amino acid-based poly(ester amide)s. Biomaterials 31, 3745 (2010).
41. B. C. U. Tai, A. C. A. Wan, and J. Y. Ying, Modified polyelectrolyte complex fibrous scaffold as a matrix for 3D cell culture. Biomaterials 31, 5927 (2010).
42. G. Dubey and K. Mequanint, Conjugation of fibronectin onto three-dimensional porous scaffolds for vascular tissue engineering applications. Acta Biomaterialia 7, 1114 (2011).
43. C.-H. K. Wang and S. H. Pun, Substrate-mediated nucleic acid delivery from self-assembled monolayers. Trends Biotechnol. 29, 119 (2011).
44. C. T. Laurencin, T. Jiang, S. G. Kumbar, and L. S. Nair, Biologically active chitosan systems for tissue engineering and regenerative medicine. Current Topics in Medicinal Chemistry 8, 354 (2008).
45. P. Ye, Z.-K. Xu, J. Wu, C. Innocent, and P. Seta, Nanofibrous poly(acrylonitrile-co-maleic acid) membranes functionalized with gelatin and chitosan for lipase immobilization. Biomaterials 27, 4169 (2006).
46. J. L. Moreau and H. H. K. Xu, Mesenchymal stem cell proliferation and differentiation on an injectable calcium phosphate - Chitosan composite scaffold. Biomaterials 30, 2675 (2009).
47. X. Yang, X. Chen, and H. Wang, Acceleration of osteogenic differentiation of preosteoblastic cells by chitosan containing nanofibrous scaffolds. Biomacromolecules 10, 2772 (2009).
48. B. G. Keselowsky, D. M. Collard, and A. J. Garcia, Integrin binding specificity regulates biomaterial surface chemistry effects on cell differentiation. Proc. Natl. Acad Sci. USA 102, 5953 (2005).
49. H. W. Kim, L. H. Li, E. J. Lee, S. H. Lee, and H. E. Kim, Fibrillar assembly and stability of collagen coating on titanium for improved osteoblast responses. J. Biomed. Mater. Res. A 75, 629 (2005).
50. A. K. Kundu and A. J. Putnam, Vitronectin and collagen I differentially regulate osteogenesis in mesenchymal stem cells. Biochem. Biophys. Res. Commun. 347, 347 (2006).
51. A. Aravamudhan, D. Ramos, J. Nip, M. Harmon, E. James, M. Deng, C. T. Laurencin, X. Yu, and S. G. Kumbar, Cellulose and collagen derived micro-nano structured scaffolds for bone tissue engineering. J. Biomed. Nanotechnol. 9, 1 (2013).
52. Y. Zhang, J. Venugopal, Z.-M. Huang, C. Lim, and S. Ramakrishna, Characterization of the surface biocompatibility of the electrospun PCL-collagen nanofibers using fibroblasts. Biomacromolecules 6, 2583 (2005).
53. A. Peister, J. A. Mellad, B. L. Larson, B. M. Hall, L. F. Gibson, and D. J. Prockop, Adult stem cells from bone marrow (MSCs) isolated from different strains of inbred mice vary in surface epitopes, rates of proliferation, and differentiation potential. Blood 103, 1662 (2004).
54. C. Chun, H. J. Lim, K.-Y. Hong, K.-H. Park, and S.-C. Song, The use of injectable, thermosensitive poly(organophosphazene)-RGD conjugates for the enhancement of mesenchymal stem cell osteogenic differentiation. Biomaterials 30, 6295 (2009).
55. S. Kumbar, A. Kulkarni, and T. Aminabhavi, Crosslinked chitosan microspheres for encapsulation of diclofenac sodium: Effect of crosslinking agent. Journal of Microencapsulation 19, 173 (2002).
56. A. A. Sawyer, K. M. Hennessy, and S. L. Bellis, Regulation of mesenchymal stem cell attachment and spreading on hydroxyapatite by RGD peptides and adsorbed serum proteins. Biomaterials 26, 1467 (2005).
57. M. N. Bongiovanni, D. B. Scanlon, and S. L. Gras, Functional fibrils derived from the peptide TTR1-cycloRGDfK that target cell adhesion and spreading. Biomaterials 32, 6099 (2011).
58. K. A. Kilian, B. Bugarija, B. T. Lahn, and M. Mrksich, Geometric cues for directing the differentiation of mesenchymal stem cells. Proceedings of the National Academy of Sciences 107, 4872 (2010).
59. O. D. Krishna, A. K. Jha, X. Jia, and K. L. Kiick, Integrinmediated adhesion and proliferation of human MSCs elicited by a hydroxyproline-lacking, collagen-like peptide. Biomaterials 32, 6412 (2011).
60. Y. M. Shin, K.-S. Kim, Y. M. Lim, Y. C. Nho, and H. Shin, Modulation of spreading, proliferation, and differentiation of human mesenchymal stem cells on gelatin-immobilized poly(l-lactide-co-ε-caprolactone) substrates. Biomacromolecules 9, 1772 (2008).
61. H. Oshina, S. Sotome, T. Yoshii, I. Torigoe, Y. Sugata, H. Maehara, E. Marukawa, K. Omura, and K. Shinomiya, Effects of continuous dexamethasone treatment on differentiation capabilities of bone marrow-derived mesenchymal cells. Bone 41, 575 (2007).
62. Y. Takahashi, M. Yamamoto, and Y. Tabata, Osteogenic differentiation of mesenchymal stem cells in biodegradable sponges composed of gelatin and [beta]-tricalcium phosphate. Biomaterials 26, 3587 (2005).
63. K. M. Hennessy, B. E. Pollot, W. C. Clem, M. C. Phipps, A. A. Sawyer, B. K. Culpepper, and S. L. Bellis, The effect of collagen I mimetic peptides on mesenchymal stem cell adhesion and differentiation, and on bone formation at hydroxyapatite surfaces. Biomaterials 30, 1898 (2009).
64. J. R. Porter, A. Henson, and K. C. Popat, Biodegradable poly([var epsilon]-caprolactone) nanowires for bone tissue engineering applications. Biomaterials 30, 780 (2009).
65. K. Na, S. W. Kim, B. K. Sun, D. G. Woo, H. N. Yang, H. M. Chung, and K. H. Park, Osteogenic differentiation of rabbit mesenchymal stem cells in thermo-reversible hydrogel constructs containing hydroxyapatite and bone morphogenic protein-2 (BMP-2). Biomaterials 28, 2631 (2007).
66. M. J. McClure, S. A. Sell, D. G. Simpson, B. H. Walpoth, and G. L. Bowlin, A three-layered electrospun matrix to mimic native arterial architecture using polycaprolactone, elastin, and collagen: A preliminary study. Acta Biomaterialia 6, 2422 (2010).
67. L. C. Ionescu, G. C. Lee, B. J. Sennett, J. A. Burdick, and R. L. Mauck, An anisotropic nanofiber/microsphere composite with controlled release of biomolecules for fibrous tissue engineering. Biomaterials 31, 4113 (2010).
68. E. Schnell, K. Klinkhammer, S. Balzer, G. Brook, D. Klee, P. Dalton, and J. Mey, Guidance of glial cell migration and axonal growth on electrospun nanofibers of poly-[epsilon]-caprolactone and a collagen/poly-[epsilon]- caprolactone blend. Biomaterials 28, 3012 (2007).
69. J. S. Choi, K. W. Leong, and H. S. Yoo, In vivo wound healing of diabetic ulcers using electrospun nanofibers immobilized with human epidermal growth factor (EGF). Biomaterials 29, 587 (2008).
70. B. S. Kim, J. M. Oh, K. S. Kim, K. S. Seo, J. S. Cho, G. Khang, H. B. Lee, K. Park, and M. S. Kim, BSA-FITC-loaded microcapsules for in vivo delivery. Biomaterials 30, 902 (2009).
71. H. Nie and C.-H. Wang, Fabrication and characterization of PLGA/HAp composite scaffolds for delivery of BMP-2 plasmid DNA. J. Controlled Release 120, 111 (2007).
72. H. Nie, B. W. Soh, Y.-C. Fu, and C.-H. Wang, Three-dimensional fibrous PLGA/HAp composite scaffold for BMP-2 delivery. Biotechnology and Bioengineering 99, 223 (2008).