Effect of dynamic stiffness of the substrates on neurite outgrowth by using a DNA-crosslinked hydrogel

Tissue Engineering - Part A

Volumn 16, Issue 6, 2010, Pages 1873-1889

  Jiang, Frank Xue ^a   Yurke, Bernard ^b,c   Schloss, Rene S ^a   Firestein, Bonnie L ^d   Langrana, Noshir A ^a,d  

^a RUTGERS UNIVERSITY   (United States)

^b BOISE STATE UNIVERSITY   (United States)

^c Boise State University   (United States)

^d RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESION; CELL CULTURE; CELL PROLIFERATION; DENDRITES (METALLOGRAPHY); DNA; DOSIMETRY; DYNAMIC RESPONSE; ENZYME ACTIVITY; GELS; GENES; HISTOLOGY; HYDROGELS; NEURONS; RIGID STRUCTURES; STIFFNESS; STIFFNESS MATRIX; SUBSTRATES; TISSUE;

CELL POPULATIONS; CENTRAL NERVOUS SYSTEM TISSUES; CROSS-LINKED HYDROGELS; DYNAMIC CUES; DYNAMIC STIFFNESS; EXTERNAL LOADS; EXTRACELLULAR MATRICES; FOCAL ADHESION KINASE; MECHANICAL COMPLIANCE; MECHANICAL STIFFNESS; MECHANOSENSING; MICROENVIRONMENTS; NEURITE OUTGROWTH; NEURITES; NEURONAL CELL; NEURONAL RESPONSE; ON DYNAMICS; PATHOLOGICAL PROCESS; PRIMARY DENDRITE; RAT SPINAL CORD; SPINAL CORD INJURY; TIME DIMENSION; TISSUE TYPES;

DYNAMICS;

RATTUS;

DNA;

ANIMAL; ARTICLE; CELL CULTURE; CHEMISTRY; CYTOLOGY; DRUG EFFECT; HYDROGEL; NERVE CELL; NEURITE; RAT; SPINAL CORD; TISSUE ENGINEERING;

ANIMALS; CELLS, CULTURED; DNA; HYDROGEL; NEURITES; NEURONS; RATS; SPINAL CORD; TISSUE ENGINEERING;

EID: 77953354136     PISSN: 19373341     EISSN: 1937335X     Source Type: Journal    
DOI: 10.1089/ten.tea.2009.0574     Document Type: Article

References (83)

1. Flanagan, L.A., Ju, Y.E., Marg, B., Osterfield, M., and Jan-mey, P.A. Neurite branching on deformable substrates. Neuroreport 13, 2411, 2002.
2. Georges, P.C., Miller, W.J., Meaney, D.F., Sawyer, E.S., and Janmey, P.A. Matrices with compliance comparable to that of brain tissue select neuronal over glial growth in mixed cortical cultures. Biophys J 90, 3012, 2006.
3. Sundararaghavan, H.G., Monteiro, G.A., Firestein, B.L., and Shreiber, D.I. Neurite growth in 3D collagen gels with gradients of mechanical properties. Biotechnol Bioeng 102, 632, 2009.
4. Willits, R.K., and Skornia, S.L. Effect of collagen gel stiffness on neurite extension. J Biomater Sci Polym Ed 15, 1521, 2004.
5. Janmey, P.A., Winer, J.P., Murray, M.E., and Wen, Q. The hard life of soft cells. Cell Motil Cytoskeleton 66, 597, 2009.
6. Jiang, F.X., Yurke, B., Firestein, B.L., and Langrana, N.A. Neurite outgrowth on a DNA crosslinked hydrogel with tunable stiffnesses. Ann Biomed Eng 36, 1565, 2008.
7. Jiang, X., Georges, P.C., Li, B., Du, Y., Kutzing, M.K., Pre-vitera, M.L., Langrana, N.A., and Firestein, B.L. Cell growth in response to mechanical stiffness is affected by neuron-astroglia interactions. Open Neurosci J 1, 7, 2007.
8. Li, L., Sharma, N., Chippada, U., Jiang, X., Schloss, R., Yarmush, M.L., and Langrana, N.A. Functional modulation of ES-derived hepatocyte lineage cells via substrate compliance alteration. Ann Biomed Eng 36, 865, 2008.
9. Gunn, J.W., Turner, S.D., and Mann, B.K. Adhesive and mechanical properties of hydrogels influence neurite extension. J Biomed Mater Res A 72, 91, 2005.
10. Leach, J.B., Brown, X.Q., Jacot, J.G., Dimilla, P.A., and Wong, J.Y. Neurite outgrowth and branching of PC12 cells on very soft substrates sharply decreases below a threshold of substrate rigidity. J Neural Eng 4, 26, 2007.
11. Hachiya, N.S., Kozuka, Y., and Kaneko, K. Mechanical stress and formation of protein aggregates in neurodegenerative disorders. Med Hypotheses 70, 1034, 2008.
12. De, R., Zemel, A., and Safran, S.A. Dynamics of cell orientation. Nat Phys 3, 655, 2007.
13. Reinhart-King, C.A., Dembo, M., and Hammer, D.A. The dynamics and mechanics of endothelial cell spreading. Bio-phys J 89, 676, 2005.
14. Shreiber, D.I., Barocas, V.H., and Tranquillo, R.T. Temporal variations in cell migration and traction during fibroblast-mediated gel compaction. Biophys J 84, 4102, 2003.
15. Tseng, Y., Kole, T.P., Lee, S.-H.J., and Wirtz, D. Local dynamics and viscoelastic properties of cell biological systems. Curr Opin Colloid Interface Sci 7, 210, 2002.
16. Petroll, W.M., and Ma, L. Direct, dynamic assessment of cell-matrix interactions inside fibrillar collagen lattices. Cell Motil Cytoskeleton 55, 254, 2003.
17. Viidik, A. A rheological model for uncalcified parallel-fibred collagenous tissue. J Biomech 1, 3, 1968.
18. Maikos, J.T., Elias, R.A., and Shreiber, D.I. Mechanical properties of dura mater from the rat brain and spinal cord. J Neurotrauma 25, 38, 2008.
19. Sparrey, C.J., Choo, A.M., Liu, J., Tetzlaff, W., and Oxland, T.R. The distribution of tissue damage in the spinal cord is influenced by the contusion velocity. Spine 33, E812, 2008.
20. Gefen, A., Gefen, N., Zhu, Q., Raghupathi, R., and Margulies, S.S. Age-dependent changes in material properties of the brain and braincase of the rat. J Neurotrauma 20, 1163, 2003.
21. Levitan, I.B., and Kaczmarek, L.K. The Neuron: Cell and Molecular Biology. New York: Oxford University Press, 1997.
22. Escuin, S., and Georges-Labouesse, E. Adhesion-induced intracellular mechanisms of neurite elongation. In: de Curtis, I., ed. Intracellular Mechanisms for Neuritogenesis. New York: Springer, 2006, pp. 1-24.
23. Fallenstein, G.T., Hulce, V.D., and Melvin, J.W. Dynamic mechanical properties of human brain tissue. J Biomech 2, 217, 1969.
24. Hrapko, M., van Dommelen, J.A., Peters, G.W., and Wis-mans, J.S. The mechanical behaviour of brain tissue: large strain response and constitutive modelling. Biorheology 43, 623, 2006.
25. Toga, A.W., and Thompson, P.M. Temporal dynamics of brain anatomy. Annu Rev Biomed Eng 5, 119, 2003.
26. Cheng, S., Clarke, E.C., and Bilston, L.E. Rheological properties of the tissues of the central nervous system: a review. Med Eng Phys 30, 1318, 2008.
27. Abbott, N.L., Gorman, C.B., and Whitesides, G.M. Active control of wetting using applied electrical potentials and self-assembled monolayers. Langmuir 11, 16, 1995.
28. Yousaf, M.N., Houseman, B.T., and Mrksich, M. Using electroactive substrates to pattern the attachment of two different cell populations. Proc Natl Acad Sci USA 98, 5992, 2001.
29. Lahann, J., and Langer, R. Smart materials with dynamically controllable surfaces. MRS Bull 30, 185, 2005.
30. Mrksich, M. Dynamic substrates for cell biology. MRS Bull 30, 180, 2005.
31. Roy, I., and Gupta, M.N. Smart polymeric materials: emerging biochemical applications. Chem Biol 10, 1161, 2003.
32. Trotter, J.A., Tipper, J., Lyons-Levy, G., Chino, K., Heuer, A.H., Liu, Z., Mrksich, M., Hodneland, C., Dillmore, W.S., Koob, T.J., Koob-Emunds, M.M., Kadler, K., and Holmes, D. Towards a fibrous composite with dynamically controlled stiffness: lessons from echinoderms. Biochem Soc Trans 28, 357, 2000.
33. Wang, X., Berggren, M., and Inganas, O. Dynamic control of surface energy and topography of microstructured conducting polymer films. Langmuir 24, 5942, 2008.
34. Yang, J., Yamato, M., and Okano, T. Cell-sheet engineering using intelligent surfaces. MRS Bull 30, 189, 2005.
35. Yeo, W.-S., Yousaf, M.N., and Mrksich, M. Dynamic interfaces between cells and surfaces: electroactive substrates that sequentially release and attach cells. J Am Chem Soc 125, 14994, 2003.
36. Cullen, D.K., Lessing, M.C., and LaPlaca, M.C. Collagen-dependent neurite outgrowth and response to dynamic deformation in three-dimensional neuronal cultures. Ann Biomed Eng 35, 835, 2007.
37. Petroll, W.M., Vishwanath, M., and Ma, L. Corneal fibro-blasts respond rapidly to changes in local mechanical stress. Invest Ophthalmol Vis Sci 45, 3466, 2004.
38. Lin, D., Langrana, N., and Yurke, B. Inducing reversible stiffness changes in DNA-crosslinked gels. J Mater Res 20, 1456, 2006.
39. Lin, D.C., Yurke, B., and Langrana, N.A. Mechanical properties of a reversible, DNA-crosslinked polyacrylamide hy-drogel. J Biomech Eng 126, 104, 2004.
40. Yurke, B., Turberfield, A.J., Mills, A.P., Jr., Simmel, F.C., and Neumann, J.L. A DNA-fuelled molecular machine made of DNA. Nature 406, 605, 2000.
41. Li, Y., White, J., Stokes, D., Sayler, G., and Sepaniak, M. Capillary electrophoresis as a method to study DNA re-association. Biotechnol Prog 17, 348, 2001.
42. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lip-man, D.J. Basic local alignment search tool. J Mol Biol 215, 403, 1990.
43. Tung, P.S., Burdzy, K., Wong, K., and Fritz, I.B. Competition between cell-substratum interactions and cell-cell interactions. J Cell Physiol 152, 410, 1992.
44. Discher, D.E., Janmey, P., and Wang, Y.L. Tissue cells feel and respond to the stiffness of their substrate. Science 310, 1139, 2005.
45. Kostic, A., Sap, J., and Sheetz, M.P. RPTPalpha is required for rigidity-dependent inhibition of extension and differentiation of hippocampal neurons. J Cell Sci 120, 3895, 2007.
46. Jiang, F.X. Engineer cell growth using a dna crosslinked hydrogel with static and dynamic stiffnesses [Dissertation]. Biomedical Engineering, Rutgers University, New Brunswick, NJ, 2009.
47. Jiang, F.X., Yurke, B., Schloss, R.S., Firestein, B.L., and Lan-grana, N.A. The relationship between fibroblast growth and the dynamic stiffnesses of a DNA crosslinked hydrogel. Biomaterials 31, 1199, 2010.
48. Poole, A.R. Proteoglycans in health and disease: structures and functions. Biochem J 236, 1, 1986.
49. Small, D.H., Mok, S.S., Williamson, T.G., and Nurcombe, V. Role of proteoglycans in neural development, regeneration, and the aging brain. J Neurochem 67, 889, 1996.
50. Bao, G., and Suresh, S. Cell and molecular mechanics of biological materials. Nat Mater 2, 715, 2003.
51. Wottawah, F., Schinkinger, S., Lincoln, B., Ananthakrishnan, R., Romeyke, M., Guck, J., and Kas, J. Optical rheology of biological cells. Phys Rev Lett 94, 098103, 2005.
52. Engler, A., Bacakova, L., Newman, C., Hategan, A., Griffin, M., and Discher, D. Substrate compliance versus ligand density in cell on gel responses. Biophys J 86, 617, 2004.
53. Goffin, J.M., Pittet, P., Csucs, G., Lussi, J.W., Meister, J.J., and Hinz, B. Focal adhesion size controls tension-dependent recruitment of alpha-smooth muscle actin to stress fibers. J Cell Biol 172, 259, 2006.
54. Angers-Loustau, A., Cote, J.F., Charest, A., Dowbenko, D., Spencer, S., Lasky, L.A., and Tremblay, M.L. Protein tyro-sine phosphatase-PEST regulates focal adhesion disassembly, migration, and cytokinesis in fibroblasts. J Cell Biol 144, 1019, 1999.
55. Levitan, I.B., and Kaczmarek, L.K. The Neuron: Cell and Molecular Biology. New York: Oxford University Press, 1997.
56. Acheson, A., Sunshine, J.L., and Rutishauser, U. NCAM polysialic acid can regulate both cell-cell and cell-substrate interactions. J Cell Biol 114, 143, 1991.
57. Bonanomi, D., and Valtorta, F. Focal adhesion kinase in neuritogenesis. In: de Curtis, I., ed. Intracellular Mechanisms for Neuritogenesis. New York: Springer, 2006, pp. 155-179.
58. Prag, S., Lepekhin, E.A., Kolkova, K., Hartmann-Petersen, R., Kawa, A., Walmod, P.S., Belman, V., Gallagher, H.C., Berezin, V., Bock, E., and Pedersen, N. NCAM regulates cell motility. J Cell Sci 115, 283, 2002.
59. Buskirk, D.R., Thiery, J.P., Rutishauser, U., and Edelman, G.M. Antibodies to a neural cell adhesion molecule disrupt histogenesis in cultured chick retinae. Nature 285, 488, 1980.
60. Escuin, S., and Georges-Labouesse, E. Adhesion-induced intracellular mechanisms of neurite elongation. In: de Curtis, I., ed. Intracellular Mechanisms for Neuritogenesis. New York: Springer, 2006, pp. 1-24.
61. Savtchenko, L.P., Kulahin, N., Korogod, S.M., and Rusakov, D.A. Electric fields of synaptic currents could influence diffusion of charged neurotransmitter molecules. Synapse 51, 270, 2004.
62. Dityatev, A. Synaptic functions of the neural cell adhesion molecule, NCAM. In: Dityatev, A., and El-Husseini, A., eds. Molecular Mechanisms of Synaptogenesis. New York: Springer, 2006.
63. Muller, D., Mendez, P., De Roo, M., Klauser, P., Steen, S., and Poglia, L. Role of NCAM in spine dynamics and sy-naptogenesis. (In press).
64. Rougon, G., and Hobert, O. New insights into the diversity and function of neuronal immunoglobulin superfamily molecules. Annu Rev Neurosci 26, 207, 2003.
65. Crossin, K.L. Cell and substrate adhesion molecules in embryonic and neural development. Clin Chem 35, 738, 1989.
66. Miller, P.D., Styren, S.D., Lagenaur, C.F., and DeKosky, S.T. Embryonic neural cell adhesion molecule (N-CAM) is elevated in the denervated rat dentate gyrus. J Neurosci 14, 4217, 1994.
67. van den Pol, A.N., di Porzio, U., and Rutishauser, U. Growth cone localization of neural cell adhesion molecule on central nervous system neurons in vitro. J Cell Biol 102, 2281, 1986.
68. Lehembre, F., Yilmaz, M., Wicki, A., Schomber, T., Stritt-matter, K., Ziegler, D., Kren, A., Went, P., Derksen, P.W., Berns, A., Jonkers, J., and Christofori, G. NCAM-induced focal adhesion assembly: a functional switch upon loss of E-cadherin. EMBO J 27, 2603, 2008.
69. Sytnyk, V., Leshchyns'ka, I., Nikonenko, A.G., and Schach-ner, M. NCAM promotes assembly and activity-dependent remodeling of the postsynaptic signaling complex. J Cell Biol 174, 1071, 2006.
70. Garner, J.A., Watanabe, M., and Rutishauser, U. Rapid ax-onal transport of the neural cell adhesion molecule. J Neu-rosci 6, 3242, 1986.
71. Yeung, T., Georges, P.C., Flanagan, L.A., Marg, B., Ortiz, M., Funaki, M., Zahir, N., Ming, W., Weaver, V., and Janmey, P.A. Effects of substrate stiffness on cell morphology, cyto-skeletal structure, and adhesion. Cell Motil Cytoskelet 60, 24, 2005.
72. Solon, J., Levental, I., Sengupta, K., Georges, P.C., and Jan-mey, P.A. Fibroblast adaptation and stiffness matching to soft elastic substrates. Biophys J 93, 4453, 2007.
73. Fass, J.N., and Odde, D.J. Tensile force-dependent neurite elicitation via anti-beta1 integrin antibody-coated magnetic beads. Biophys J 85, 623, 2003.
74. Zheng, J., Lamoureux, P., Santiago, V., Dennerll, T., Bux-baum, R.E., and Heidemann, S.R. Tensile regulation of ax-onal elongation and initiation. J Neurosci 11, 1117, 1991.
75. Heidemann, S.R., and Buxbaum, R.E. Growth cone motility. Curr Opin Neurobiol 1, 339, 1991.
76. Fischer, T.M., Steinmetz, P.N., and Odde, D.J. Robust mi-cromechanical neurite elicitation in synapse-competent neurons via magnetic bead force application. Ann Biomed Eng 33, 1229, 2005.
77. Huang, S., and Ingber, D.E. Cell tension, matrix mechanics, and cancer development. Cancer Cell 8, 175, 2005.
78. Bray, D. Axonal growth in response to experimentally applied mechanical tension. Dev Biol 102, 379, 1984.
79. Giniger, E. How do Rho family GTPases direct axon growth and guidance? A proposal relating signaling pathways to growth cone mechanics. Differentiation 70, 385, 2002.
80. Lafont, F., Rouget, M., Rousselet, A., Valenza, C., and Pro-chiantz, A. Specific responses of axons and dendrites to cy-toskeleton perturbations: an in vitro study. J Cell Sci 104 (Pt 2), 433, 1993.
81. Suter, D.M., and Forscher, P. Substrate-cytoskeletal coupling as a mechanism for the regulation of growth cone motility and guidance. J Neurobiol 44, 97, 2000.
82. Chicurel, M.E., Chen, C.S., and Ingber, D.E. Cellular control lies in the balance of forces. Curr Opin Cell Biol 10, 232, 1998.
83. Balgude, A.P., Yu, X., Szymanski, A., and Bellamkonda, R.V. Agarose gel stiffness determines rate of DRG neurite extension in 3D cultures. Biomaterials 22, 1077, 2001.