Strength in the periphery: Growth cone biomechanics and substrate rigidity response in peripheral and central nervous system neurons

Biophysical Journal

Volumn 102, Issue 3, 2012, Pages 452-460

  Koch, Daniel ^a   Rosoff, William J ^a   Jiang, Jiji ^a   Geller, Herbert M ^b   Urbach, Jeffrey S ^a  

^a GEORGETOWN UNIVERSITY   (United States)

^b NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; ARTICLE; BIOMECHANICS; CYTOLOGY; CYTOSKELETON; GROWTH CONE; HIPPOCAMPUS; MECHANICS; METABOLISM; RAT; SPINAL GANGLION; TIME;

ANIMALS; BIOMECHANICS; CYTOSKELETON; GANGLIA, SPINAL; GROWTH CONES; HIPPOCAMPUS; MECHANICAL PROCESSES; RATS; TIME FACTORS;

EID: 84856740623     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2011.12.025     Document Type: Article

References (51)

1. M. Tessier-Lavigne, and C.S. Goodman The molecular biology of axon guidance Science 274 1996 1123 1133 (Pubitemid 26389268)
2. J.K. Chilton Molecular mechanisms of axon guidance Dev. Biol. 292 2006 13 24 (Pubitemid 44262112)
3. N.R. Farrar, and G.E. Spencer Pursuing a 'turning point' in growth cone research Dev. Biol. 318 2008 102 111
4. S. Geraldo, and P.R. Gordon-Weeks Cytoskeletal dynamics in growth-cone steering J. Cell Sci. 122 2009 3595 3604
5. L.A. Lowery, and D. Van Vactor The trip of the tip: understanding the growth cone machinery Nat. Rev. Mol. Cell Biol. 10 2009 332 343
6. K. Franze, and J. Guck The biophysics of neuronal growth Rep. Prog. Phys. 73 2010 094601
7. D.M. Suter, and K.E. Miller The emerging role of forces in axonal elongation Prog. Neurobiol. 94 2011 91 101
8. D.E. Discher, P. Janmey, and Y.L. Wang Tissue cells feel and respond to the stiffness of their substrate Science 310 2005 1139 1143 (Pubitemid 41681732)
9. S.W. Moore, P. Roca-Cusachs, and M.P. Sheetz Stretchy proteins on stretchy substrates: the important elements of integrin-mediated rigidity sensing Dev. Cell 19 2010 194 206
10. A.J. Engler, and S. Sen D.E. Discher Matrix elasticity directs stem cell lineage specification Cell 126 2006 677 689 (Pubitemid 44233625)
11. L.A. Flanagan, and Y.E. Ju P.A. Janmey Neurite branching on deformable substrates Neuroreport 13 2002 2411 2415 (Pubitemid 36143534)
12. P.C. Georges, and W.J. Miller P.A. Janmey Matrices with compliance comparable to that of brain tissue select neuronal over glial growth in mixed cortical cultures Biophys. J. 90 2006 3012 3018
13. A. Kostic, J. Sap, and M.P. Sheetz RPTPα is required for rigidity-dependent inhibition of extension and differentiation of hippocampal neurons J. Cell Sci. 120 2007 3895 3904 (Pubitemid 350187370)
14. Y.B. Lu, and K. Franze A. Reichenbach Viscoelastic properties of individual glial cells and neurons in the CNS Proc. Natl. Acad. Sci. USA 103 2006 17759 17764 (Pubitemid 44852233)
15. A.F. Christ, and K. Franze J. Guck Mechanical difference between white and gray matter in the rat cerebellum measured by scanning force microscopy J. Biomech. 43 2010 2986 2992
16. D. Bray Mechanical tension produced by nerve cells in tissue culture J. Cell Sci. 37 1979 391 410 (Pubitemid 9200804)
17. P. Lamoureux, R.E. Buxbaum, and S.R. Heidemann Direct evidence that growth cones pull Nature 340 1989 159 162 (Pubitemid 19175371)
18. P.C. Bridgman, and S. Dave R.S. Adelstein Myosin IIB is required for growth cone motility J. Neurosci. 21 2001 6159 6169 (Pubitemid 32737748)
19. S.R. Heidemann, P. Lamoureux, and R.E. Buxbaum Growth cone behavior and production of traction force J. Cell Biol. 111 1990 1949 1957
20. C.E. Chan, and D.J. Odde Traction dynamics of filopodia on compliant substrates Science 322 2008 1687 1691
21. P. Lamoureux, and G. Ruthel S.R. Heidemann Mechanical tension can specify axonal fate in hippocampal neurons J. Cell Biol. 159 2002 499 508 (Pubitemid 35332836)
22. J. Rajagopalan, A. Tofangchi, and M.T. A Saif Drosophila neurons actively regulate axonal tension in vivo Biophys. J. 99 2010 3208 3215
23. R.J. Pelham Jr., and Y. Wang Cell locomotion and focal adhesions are regulated by substrate flexibility Proc. Natl. Acad. Sci. USA 94 1997 13661 13665 (Pubitemid 28009639)
24. B. Sabass, and M.L. Gardel U.S. Schwarz High resolution traction force microscopy based on experimental and computational advances Biophys. J. 94 2008 207 220
25. M.T. Frey, and A. Engler Y.L. Wang Microscopic methods for measuring the elasticity of gel substrates for cell culture: microspheres, microindenters, and atomic force microscopy Methods Cell Biol. 83 2007 47 65
26. M. Dembo, and Y.L. Wang Stresses at the cell-to-substrate interface during locomotion of fibroblasts Biophys. J. 76 1999 2307 2316 (Pubitemid 29266384)
27. J.P. Butler, and I.M. Tolić-Nørrelykke J.J. Fredberg Traction fields, moments, and strain energy that cells exert on their surroundings Am. J. Physiol. Cell Physiol. 282 2002 C595 C605
28. C.G. Dotti, C.A. Sullivan, and G.A. Banker The establishment of polarity by hippocampal neurons in culture J. Neurosci. 8 1988 1454 1468
29. T. Mitchison, and M. Kirschner Cytoskeletal dynamics and nerve growth Neuron 1 1988 761 772
30. D.G. Jay The clutch hypothesis revisited: ascribing the roles of actin-associated proteins in filopodial protrusion in the nerve growth cone J. Neurobiol. 44 2000 114 125
31. E.W. Dent, S.L. Gupton, and F.B. Gertler The growth cone cytoskeleton in axon outgrowth and guidance Cold Spring Harb. Perspect. Biol. 3 2011 3
32. N.A. Medeiros, D.T. Burnette, and P. Forscher Myosin II functions in actin-bundle turnover in neuronal growth cones Nat. Cell Biol. 8 2006 215 226 (Pubitemid 43336063)
33. S. Kurklinsky, J. Chen, and M.A. McNiven Growth cone morphology and spreading are regulated by a dynamin-cortactin complex at point contacts in hippocampal neurons J. Neurochem. 117 2011 48 60
34. A. Renaudin, and M. Lehmann L. McKerracher Organization of point contacts in neuronal growth cones J. Neurosci. Res. 55 1999 458 471 (Pubitemid 29110553)
35. A.P. Balgude, and X. Yu R.V. Bellamkonda Agarose gel stiffness determines rate of DRG neurite extension in 3D cultures Biomaterials 22 2001 1077 1084 (Pubitemid 32229933)
36. H.G. Sundararaghavan, and G.A. Monteiro D.I. Shreiber Neurite growth in 3D collagen gels with gradients of mechanical properties Biotechnol. Bioeng. 102 2009 632 643
37. L.L. Norman, and H. Aranda-Espinoza Cortical neuron outgrowth is insensitive to substrate stiffness Cell. Mol. Bioeng 3 2010 398 414
38. W.J. Rosoff, and J.S. Urbach G.J. Goodhill A new chemotaxis assay shows the extreme sensitivity of axons to molecular gradients Nat. Neurosci. 7 2004 678 682 (Pubitemid 38691909)
39. M. O'Toole, P. Lamoureux, and K.E. Miller A physical model of axonal elongation: force, viscosity, and adhesions govern the mode of outgrowth Biophys. J. 94 2008 2610 2620
40. S. Geraldo, and U.K. Khanzada P.R. Gordon-Weeks Targeting of the F-actin-binding protein drebrin by the microtubule plus-tip protein EB3 is required for neuritogenesis Nat. Cell Biol. 10 2008 1181 1189
41. T. Betz, and D. Koch J.A. Käs Stochastic actin polymerization and steady retrograde flow determine growth cone advancement Biophys. J. 96 2009 5130 5138
42. S. Woo, and T.M. Gomez Rac1 and RhoA promote neurite outgrowth through formation and stabilization of growth cone point contacts J. Neurosci. 26 2006 1418 1428 (Pubitemid 43237012)
43. A.M. Pasapera, and I.C. Schneider C.M. Waterman Myosin II activity regulates vinculin recruitment to focal adhesions through FAK-mediated paxillin phosphorylation J. Cell Biol. 188 2010 877 890
44. B. Geiger, J.P. Spatz, and A.D. Bershadsky Environmental sensing through focal adhesions Nat. Rev. Mol. Cell Biol. 10 2009 21 33
45. A.W. Schaefer, and V.T. Schoonderwoert P. Forscher Coordination of actin filament and microtubule dynamics during neurite outgrowth Dev. Cell 15 2008 146 162 (Pubitemid 351895599)
46. D.A. Spero, and F.J. Roisen Neuro-2a neuroblastoma cells form neurites in the presence of taxol and cytochalasin D Brain Res. 355 1985 155 159 (Pubitemid 16209592)
47. H. Rösner, and W. Möller M. Blum Attenuation of actinomyosinII contractile activity in growth cones accelerates filopodia-guided and microtubule-based neurite elongation Brain Res. 1176 2007 1 10 (Pubitemid 47553114)
48. P.C. Letourneau, T.A. Shattuck, and A.H. Ressler "Pull" and "push" in neurite elongation: observations on the effects of different concentrations of cytochalasin B and taxol Cell Motil. Cytoskeleton 8 1987 193 209 (Pubitemid 18006648)
49. P. Lamoureux, and V.L. Steel S.R. Heidemann Extracellular matrix allows PC12 neurite elongation in the absence of microtubules J. Cell Biol. 110 1990 71 79
50. J.A. Brown, R.B. Wysolmerski, and P.C. Bridgman Dorsal root ganglion neurons react to semaphorin 3A application through a biphasic response that requires multiple myosin II isoforms Mol. Biol. Cell 20 2009 1167 1179
51. E.M. Hur, and I.H. Yang F.Q. Zhou Engineering neuronal growth cones to promote axon regeneration over inhibitory molecules Proc. Natl. Acad. Sci. USA 108 2011 5057 5062