Cell-fiber interactions on aligned and suspended nanofiber scaffolds

Journal of Biomaterials and Tissue Engineering

Volumn 3, Issue 4, 2013, Pages 355-368

  Sheets, Kevin ^a   Wang, Ji ^a,b   Meehan, Sean ^b   Sharma, Puja ^a   Ng, Colin ^b   Khan, Mohammad ^b   Koons, Brian ^b   Behkam, Bahareh ^a,b   Nain, Amrinder S ^a,b  

^a VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^b Virginia Polytechnic Institute and State University   (United States)

Author keywords

Cellular dynamics; ECM; Fiber alignment; Mechanobiology; Nanofiber

Indexed keywords

MOLECULAR SCAFFOLD; POLY (METHYL METHACRYLATE); POLYETHYLENE; POLYSTYRENE; POLYURETHAN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL CULTURE; CELL DIFFERENTIATION; CELL FIBER INTERACTION; CELL FUNCTION; CELL INTERACTION; CELL MIGRATION; CELL STRUCTURE; EXTRACELLULAR MATRIX; FLUORESCENCE IMAGING; MOUSE; MYOBLAST; NANOFABRICATION; NONHUMAN; PHASE CONTRAST MICROSCOPY; PHYSICAL PARAMETERS; SINGLE CELL ANALYSIS; TISSUE ENGINEERING;

EID: 84891601126     PISSN: 21579083     EISSN: 21579091     Source Type: Journal    
DOI: 10.1166/jbt.2013.1105     Document Type: Article

References (63)

1. T. R. Cox and J. T. Erler, Remodeling and homeostasis of the extracellular matrix: Implications for fibrotic diseases and cancer. Disease Models and Mechanisms 4, 165 (2011).
2. P. P. Provenzano and R. Vanderby, Collagen fibril morphology and organization: Implications for force transmission in ligament and tendon. Matrix Biology: Journal of the International Society for Matrix Biology. 25, 71 (2006).
3. J. C. Patterson-Kane, D. L. Becker, and T. Rich, The pathogenesis of tendon microdamage in athletes: The horse as a natural model for basic cellular research. Journal of Comparative Pathology 147, 227 (2012).
4. S. D. Subramony, B. R. Dargis, M. Castillo, E. U. Azeloglu, M. S. Tracey, A. Su, and H. H. Lu, The guidance of stem cell differentiation by substrate alignment and mechanical stimulation. Biomater. 34, 1942 (2013).
5. T. Rozario and D. W. DeSimone, The extracellular matrix in development and morphogenesis: A dynamic view. Developmental Biology 341, 126 (2010).
6. B. Wehrle-Haller, Structure and function of focal adhesions. Current Opinion in Cell Biology 24, 116 (2011).
7. 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 of the United States of America, March (2010), Vol. 107, pp. 4872-7.
8. R. S. Reneman and A. P. G. Hoeks, Wall shear stress as measured in vivo: Consequences for the design of the arterial system. Medical and Biological Engineering and Computing 46, 499 (2008).
9. N. J. B. Driessen, G. W. M. Peters, J. M. Huyghe, C. V. C. Bouten, and F. P. T. Baaijens, Remodelling of continuously distributed collagen fibres in soft connective tissues. Journal of Biomechanics 36, 1151 (2003).
10. A. Yegorov, L. Kakurin, and Y. Nefyodov, Effects of an 18-day flight on the human body. Life Sciences and Space Research 57 (1972).
11. S. M. Smith, M. E. Wastney, B. V Morukov, I. M. Larina, E. Laurence, S. A. Abrams, E. N. Taran, C. Shih, J. L. Nillen, E. Janis, B. L. Rice, and H. W. Lane, Calcium metabolism before, during, and after a 3-mo spaceflight: Kinetic and biochemical changes. Am. J. Physiol. Regulatory, Integrative and Comp. Physiol. 277, R1 (1999).
12. W. Neuman, Calcium metabolism in space flight. Life Sci. Space Res. 8, 309 (1970).
13. C. A. Simmons, S. Matlis, A. J. Thornton, S. Chen, C.-Y. Wang, and D. J. Mooney, Cyclic strain enhances matrix mineralization by adult human mesenchymal stem cells via the extracellular signalregulated kinase (ERK1/2) signaling pathway. Journal of Biomechanics 36, 1087 (2003).
14. M. Schmelter, B. Ateghang, S. Helmig, M. Wartenberg, and H. Sauer, Embryonic stem cells utilize reactive oxygen species as transducers of mechanical strain-induced cardiovascular differentiation. FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology 20, 1182 (2006).
15. H. Yamaguchi, J. Wyckoff, and J. Condeelis, Cell migration in tumors. Current Opinion in Cell Biology 17, 559 (2005).
16. M. J. Buehler, Nature designs tough collagen: Explaining the nanostructure of collagen fibrils, Proceedings of the National Academy of Sciences of the United States of America August (2006), Vol. 103, pp. 12285-90.
17. B. M. Baker and R. L. Mauck, The effect of nanofiber alignment on the maturation of engineered meniscus constructs. Biomater. 28, 1967 (2007).
18. C. Erisken, X. Zhang, K. L. Moffat, W. N. Levine, and H. H. Lu, Scaffold fiber diameter regulates human tendon fibroblast growth and differentiation. Tissue Engineering. Part A 19, 519 (2013).
19. Y. Liu, Y. Ji, K. Ghosh, R. a F. Clark, L. Huang, and M. H. Rafailovich, Effects of fiber orientation and diameter on the behavior of human dermal fibroblasts on electrospun PMMA scaffolds. Journal of Biomedical Materials Research. Part A 90, 1092 (2009).
20. A. M. Kloxin, K. J. R. Lewis, C. a Deforest, G. Seedorf, M. W. Tibbitt, V. Balasubramaniam, and K. S. Anseth, Responsive culture platform to examine the influence of microenvironmental geometry on cell function in 3D. Integrative Biology 4, 1540 (2012).
21. M. E. Berginski, E. a Vitriol, K. M. Hahn, and S. M. Gomez, Highresolution quantification of focal adhesion spatiotemporal dynamics in living cells. PloS One 6, e22025 (2011).
22. R. A. Neal, A. Jean, H. Park, P. B. Wu, J. Hsiao, G. C. Engelmayr, R. Langer, and L. E. Freed, Three-dimensional elastomeric scaffolds designed with cardiac-mimetic structural and mechanical features. Tissue Engineering. Part A 19, 793 (2013).
23. M. Nikkhah, F. Edalat, S. Manoucheri, and A. Khademhosseini, Engineering microscale topographies to control the cell-substrate interface. Biomater. 33, 5230 (2012).
24. G. V Shivashankar, Mechanosignaling to the cell nucleus and gene regulation. Annual Review of Biophysics 40, 361 (2011).
25. Y. Liu, A. Franco, L. Huang, D. Gersappe, R. a F. Clark, and M. H. Rafailovich, Control of cell migration in two and three dimensions using substrate morphology. Experimental Cell Research 315, 2544 (2009).
26. W. Tutak, S. Sarkar, S. Lin-Gibson, T. M. Farooque, G. Jyotsnendu, D. Wang, J. Kohn, D. Bolikal, and C. G. Simon, The support of bone marrow stromal cell differentiation by airbrushed nanofiber scaffolds. Biomater. 34, 2389 (2013).
27. G. Vidal, B. Delord, W. Neri, S. Gounel, O. Roubeau, C. Bartholome, I. Ly, P. Poulin, C. Labrugère, E. Sellier, M.-C. Durrieu, J. Amédée, and J.-P. Salvetat, The effect of surface energy, adsorbed RGD peptides and fibronectin on the attachment and spreading of cells on multiwalled carbon nanotube papers. Carbon 49, 2318 (2011).
28. T. J. Sill and H. a von Recum, Electrospinning: Applications in drug delivery and tissue engineering. Biomater. 29, 1989 (2008).
29. G. Chang, G. Song, J. Yang, R. Huang, A. Kozinda, and J. Shen, Morphology control of nanohelix by electrospinning. Appl. Phys. Lett. 101, 263503 (2012).
30. B. Sundaray, V. Subramanian, T. S. Natarajan, R.-Z. Xiang, C.-C. Chang, and W.-S. Fann, Electrospinning of continuous aligned polymer fibers. Appl. Phys. Lett. 84, 1222 (2004).
31. W. Han Bing, E. M. Michael, M. C. Jared, H. Andres, O. Martin, T. T. Matthew, and J. G. Ryan, Creation of highly aligned electrospun poly-L-lactic acid fibers for nerve regeneration applications. Journal of Neural Engineering 6, 16001 (2009).
32. Z.-M. Huang, Y. Z. Zhang, M. Kotaki, and S. Ramakrishna, A review on polymer nanofibers by electrospinning and their applications in nanocomposites. Composites Science and Technology 63, 2223 (2003).
33. J. A. Matthews, G. E. Wnek, D. G. Simpson, and G. L. Bowlin, Electrospinning of collagen nanofibers. Biomacromolecules 3, 232 (2002).
34. A. S. Nain, M. Sitti, A. Jacobson, T. Kowalewski, and C. Amon, Dry spinning based spinneret based tunable engineered parameters (STEP) technique for controlled and aligned deposition of polymeric nanofibers. Macromolecular Rapid Communications 30, 1406 (2009).
35. A. S. Nain, J. C. Wong, C. Amon, and M. Sitti, Drawing suspended polymer micro-/nanofibers using glass micropipettes. Appl. Phys. Lett. 89, 183105 (2006).
36. A. S. Nain and J. Wang, Polymeric nanofibers: Isodiametric design space and methodology for depositing aligned nanofiber arrays in single and multiple layers. Polym. J (2013).
37. F. Family and P. Meakin, Scaling of the droplet-size distribution in vapor-deposited thin films. Phys. Rev. Lett. 61, 428 (1988).
38. L. Wang, C.-L. Pai, M. C. Boyce, and G. C. Rutledge, Wrinkled surface topographies of electrospun polymer fibers. Appl. Phys. Lett. 94, 151913 (2009).
39. C.-L. Pai, M. C. Boyce, and G. C. Rutledge, Morphology of porous and wrinkled fibers of polystyrene electrospun from dimethylformamide. Macromolecules 42, 2102 (2009).
40. J. Wang, J. H, M. Ellis, and A. S. Nain, Organized long titanium dioxide nanofibers/nanotubes with controlled morphology using a sol-gel combined STEP technique. New J. Chem. 37, 571 (2013).
41. Y. Yang, J. Wang, J. Li, D. Viehland, and A. S. Nain, Nanoparticles deposition at specific sites using aligned fiber networks. OJINM 2, 55 (2012).
42. S. L. Shenoy, W. D. Bates, H. L. Frisch, and G. E. Wnek, Role of chain entanglements on fiber formation during electrospinning of polymer solutions: Good solvent, non-specific polymer-polymer interaction limit. Polymer 46, 3372 (2005).
43. D. W. Mead, R. G. Larson, and M. Doi, A molecular theory for fast flows of entangled polymers. Macromolecules 31, 7895 (1998).
44. K. Sheets, S. Wunsch, C. Ng, and A. S. Nain, Shape-dependent cell migration and focal adhesion organization on suspended and aligned nanofiber scaffolds. Acta Biomaterialia 9, 7169 (2013).
45. J. C. Yarrow, Z. E. Perlman, N. J. Westwood, and T. J. Mitchison, A high-throughput cell migration assay using scratch wound healing, a comparison of image-based readout methods. BMC Biotechnology 4, 21 (2004).
46. T. Dvir, B. P. Timko, D. S. Kohane, and R. Langer, Complex tissues. Nature Publishing Group 6, 13 (2010).
47. D. A. Lauffenburger and a F. Horwitz, Cell migration: A physically integrated molecular process. Cell 84, 359 (1996).
48. M. L. Gardel, I. C. Schneider, Y. Aratyn-Schaus, and C. M. Waterman, Mechanical integration of actin and adhesion dynamics in cell migration. Annual Review of Cell and Developmental Biology 26, 315 (2010).
49. T. A. Ulrich, E. M. de Juan Pardo, and S. Kumar, The mechanical rigidity of the extracellular matrix regulates the structure, motility, and proliferation of glioma cells. Cancer Research 69, 4167 (2009).
50. D. N. Louis, Molecular pathology of malignant gliomas. Annu. Rev. Pathol. 1, 97 (2006).
51. P. Sharma, K. Sheets, E. Subbiah, and A. S. Nain, The mechanistic influence of aligned nanofiber networks on cell shape, migration and blebbing dynamics of glioma cells. Integr. Biol. In Press (2013).
52. A. J. Engler, S. Sen, H. L. Sweeney, and D. E. Discher, Matrix elasticity directs stem cell lineage specification. Cell 126, 677 (2006).
53. R. H. W. Lam, S. Weng, W. Lu, and J. Fu, Live-cell subcellular measurement of cell stiffness using a microengineered stretchable micropost array membrane. Integrative Biology 4, 1289 (2012).
54. S. Even-Ram and K. M. Yamada, Cell migration in 3D matrix. Current Opinion in Cell Biology 17, 524 (2005).
55. D. Wirtz, K. Konstantopoulos, and P. C. Searson, The physics of cancer: The role of physical interactions and mechanical forces in metastasis. Nat. Rev. Cancer 11, 512 (2011).
56. E. D. Ker, A. S. Nain, L. E. Weiss, J. Wang, J. Suhan, C. H. Amon, and P. G. Campbell, Bioprinting of growth factors onto aligned submicron fibrous scaffolds for simultaneous control of cell differentiation and alignment. Biomater. 32, 8097 (2011).
57. M. Yamato, Nanotechnology-based cell sheet engineering for regenerative medicine, Micro-NanoMechatronics and Human Science, 2005 IEEE International Symposium (2005), pp. 251-254.
58. S. Bakhru, A. S. Nain, C. Highley, J. Wang, P. Campbell, C. Amon, and S. Zappe, Direct and cell signaling-based, geometry-induced neuronal differentiation of neural stem cells. Integrative Biology 3, 1207 (2011).
59. V. Chaurey, P.-C. Chiang, C. Polanco, Y.-H. Su, C.-F. Chou, and N. S. Swami, Interplay of electrical forces for alignment of sub-100 nm electrospun nanofibers on insulator gap collectors. Langmuir 26, 19022 (2010).
60. D. Li, Y. Wang, and Y. Xia, Electrospinning nanofibers as uniaxially aligned arrays and layer-by-layer stacked films. Advanced Materials 16, 361 (2004).
61. Y. Liu, X. Zhang, Y. Xia, and H. Yang, Magnetic-field-assisted electrospinning of aligned straight and wavy polymeric nanofibers. Adv. Mater. 22, 2454 (2010).
62. A. Jafari, J.-H. Jeon, and I.-K. Oh, Well-aligned nano-fiberous membranes based on three-pole electrospinning with channel electrode. Macromol. Rapid Commun. 32, 921 (2011).
63. S. Sarkar, S. Deevi, and G. Tepper, Biased ac electrospinning of aligned polymer nanofibers. Macromol. Rapid Commun. 28, 1034 (2007).