Topography and nanomechanics of live neuronal growth cones analyzed by atomic force microscopy

Biophysical Journal

Volumn 96, Issue 12, 2009, Pages 5060-5072

  Xiong, Ying ^a   Aih, Cheun Lee ^b   Suter, Daniel M ^a,b   Lee, Gil U ^a,c  

^a PURDUE UNIVERSITY   (United States)

^b PURDUE UNIVERSITY   (United States)

^c UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN;

ACTIN FILAMENT; APLYSIA; ARTICLE; ATOMIC FORCE MICROSCOPY; CALCULATION; LAMELLIPODIUM; MEASUREMENT; MOLECULAR MECHANICS; MOLECULAR WEIGHT; NERVE CELL DIFFERENTIATION; NERVE CELL GROWTH; NERVE REGENERATION; NONHUMAN; TOPOGRAPHY; YOUNG MODULUS;

APLYSIA;

EID: 68949086359     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2009.03.032     Document Type: Article

References (82)

1. Charron, F., and M. Tessier-Lavigne. 2005. Novel brain wiring functions for classical morphogens: a role as graded positional cues in axon guidance. Development. 132:2251-2262.
2. Dickson, B. J. 2002. Molecular mechanisms of axon guidance. Science. 298:1959-1964.
3. Song, H., and M. Poo. 2001. The cell biology of neuronal navigation. Nat. Cell Biol. 3:E81-E88.
4. Huber, A. B., A. L. Kolodkin, D. D. Ginty, and J. F. Cloutier. 2003. Signaling at the growth cone: ligand-receptor complexes and the control of axon growth and guidance. Annu. Rev. Neurosci. 26:509-563.
5. Dent, E. W., and F. B. Gertler. 2003. Cytoskeletal dynamics and transport in growth cone motility and axon guidance. Neuron. 40:209-227.
6. Bridgman, P. C., and M. E. Dailey. 1989. The organization of myosin and actin in rapid frozen nerve growth cones. J. Cell Biol. 108:95-109.
7. Lewis, A. K., and P. C. Bridgman. 1992. Nerve growth cone lamellipodia contain two populations of actin filaments that differ in organization and polarity. J. Cell Biol. 119:1219-1243.
8. Korobova, F., and T. Svitkina. 2008. Arp2/3 complex is important for filopodia formation, growth cone motility, and neuritogenesis in neuronal cells. Mol. Biol. Cell. 19:1561-1574.
9. Mongiu, A. K., E. L. Weitzke, O. Y. Chaga, and G. G. Borisy. 2007. Kinetic-structural analysis of neuronal growth cone veil motility. J. Cell Sci. 120:1113-1125.
10. Forscher, P., and S. J. Smith. 1988. Actions of cytochalasins on the organization of actin filaments and microtubules in a neuronal growth cone. J. Cell Biol. 107:1505-1516.
11. Rochlin, M. W., M. E. Dailey, and P. C. Bridgman. 1999. Polymerizing microtubules activate site-directed F-actin assembly in nerve growth cones. Mol. Biol. Cell. 10:2309-2327.
12. Schaefer, A. W., N. Kabir, and P. Forscher. 2002. Filopodia and actin arcs guide the assembly and transport of two populations of microtubules with unique dynamic parameters in neuronal growth cones. J. Cell Biol. 158:139-152.
13. Zhang, X. F., A. W. Schaefer, D. T. Burnette, V. T. Schoonderwoert, and P. Forscher. 2003. Rho-dependent contractile responses in the neuronal growth cone are independent of classical peripheral retrograde actin flow. Neuron. 40:931-944.
14. Lin, C. H., E. M. Espreafico, M. S. Mooseker, and P. Forscher. 1996. Myosin drives retrograde F-actin flow in neuronal growth cones. Neuron. 16:769-782.
15. Medeiros, N. A., D. T. Burnette, and P. Forscher. 2006. Myosin II functions in actin-bundle turnover in neuronal growth cones. Nat. Cell Biol. 8:215-226.
16. Tanaka, E. M., and M. W. Kirschner. 1991. Microtubule behavior in the growth cones of living neurons during axon elongation. J. Cell Biol. 115:345-363.
17. Buck, K. B., and J. Q. Zheng. 2002. Growth cone turning induced by direct local modification of microtubule dynamics. J. Neurosci. 22:9358-9367.
18. Challacombe, J. F., D. M. Snow, and P. C. Letourneau. 1997. Dynamic microtubule ends are required for growth cone turning to avoid an inhibitory guidance cue. J. Neurosci. 17:3085-3095.
19. Marsh, L., and P. C. Letourneau. 1984. Growth of neurites without filopodial or lamellipodial activity in the presence of cytochalasin B. J. Cell Biol. 99:2041-2047.
20. O'Connor, T. P., and D. Bentley. 1993. Accumulation of actin in subsets of pioneer growth cone filopodia in response to neural and epithelial guidance cues in situ. J. Cell Biol. 123:935-948.
21. Suter, D. M., A. W. Schaefer, and P. Forscher. 2004. Microtubule dynamics are necessary for SRC family kinase-dependent growth cone steering. Curr. Biol. 14:1194-1199.
22. Tanaka, E., and M. W. Kirschner. 1995. The role of microtubules in growth cone turning at substrate boundaries. J. Cell Biol. 128:127-137.
23. Williamson, T., P. R. Gordon-Weeks, M. Schachner, and J. Taylor. 1996. Microtubule reorganization is obligatory for growth cone turning. Proc. Natl. Acad. Sci. USA. 93:15221-15226.
24. Henderson, E., P. G. Haydon, and D. S. Sakaguchi. 1992. Actin filament dynamics in living glial cells imaged by atomic force microscopy. Science. 257:1944-1946.
25. Rotsch, C., F. Braet, E. Wisse, and M. Radmacher. 1997. AFM imaging and elasticity measurements on living rat liver macrophages. Cell Biol. Int. 21:685-696.
26. Mathur, A. B., G. A. Truskey, and W. M. Reichert. 2000. Atomic force and total internal reflection fluorescence microscopy for the study of force transmission in endothelial cells. Biophys. J. 78:1725-1735.
27. Braet, F., C. Rotsch, E. Wisse, and M. Radmacher. 1998. Comparison of fixed and living liver endothelial cells by atomic force microscopy. Appl. Phys. A Mat. Sci. Processing. 66:S575-S578.
28. Chang, L., T. Kious, M. Yorgancioglu, D. Keller, and J. Pfeiffer. 1993. Cytoskeleton of living, unstained cells imaged by scanning force microscopy. Biophys. J. 64:1282-1286.
29. Pesen, D., and J. H. Hoh. 2005. Micromechanical architecture of the endothelial cell cortex. Biophys. J. 88:670-679.
30. Schneider, S. W., K. C. Sritharan, J. P. Geibel, H. Oberleithner, and B. P. Jena. 1997. Surface dynamics in living acinar cells imaged by atomic force microscopy: identification of plasma membrane structures involved in exocytosis. Proc. Natl. Acad. Sci. USA. 94:316-321.
31. Tojima, T., Y. Yamane, H. Takagi, T. Takeshita, T. Sugiyama, et al. 2000. Three-dimensional characterization of interior structures of exocytotic apertures of nerve cells using atomic force microscopy. Neuroscience. 101:471-481.
32. Lal, R., B. Drake, D. Blumberg, D. R. Saner, P. K. Hansma, et al. 1995. Imaging real-time neurite outgrowth and cytoskeletal reorganization with an atomic force microscope. Am. J. Physiol. 269:C275-C285.
33. McNally, H. A., and R. B. Borgens. 2004. Three-dimensional imaging of living and dying neurons with atomic force microscopy. J. Neurocytol. 33:251-258.
34. McNally, H. A., B. Rajwa, J. Sturgis, and J. P. Robinson. 2005. Comparative three-dimensional imaging of living neurons with confocal and atomic force microscopy. J. Neurosci. Methods. 142:177-184.
35. Parpura, V., P. G. Haydon, and E. Henderson. 1993. Three-dimensional imaging of living neurons and glia with the atomic force microscope. J. Cell Sci. 104:427-432.
36. Ricci, D., M. Grattarola, and M. Tedesco. 2004. Growth cones of living neurons probed by atomic force microscopy. Methods Mol. Biol. 242:125-140.
37. Yunxu, S., L. Danying, R. Yanfang, H. Dong, and M. Wanyun. 2006. Three-dimensional structural changes in living hippocampal neurons imaged using magnetic AC mode atomic force microscopy. J. Electron Microsc. (Tokyo). 55:165-172.
38. Grzywa, E. L., A. C. Lee, G. U. Lee, and D. M. Suter. 2006. High resolution analysis of neuronal growth cone morphology by comparative atomic force and optical microscopy. J. Neurobiol. 66:1529-1543.
39. Meyer, E. 2002. Nanoscience: Friction and Rheology at the Nanometer Scale. World Scientific Publishing Company, Hackensack, NJ.
40. Weisenhorn, A. L., M. Khorsandi, S. Kasas, V. Gotzos, and H. J. Butt. 1993. Deformation and height anomaly of soft surfaces studied with an AFM. Nanotechnology. 4:106-113.
41. Radmacher, M., M. Fritz, C. M. Kacher, J. P. Cleveland, and P. K. Hansma. 1996. Measuring the viscoelastic properties of human platelets with the atomic force microscope. Biophys. J. 70:556-567.
42. Radmacher, M. 2002. Measuring the elastic properties of living cells by the atomic force microscope. Methods Cell Biol. 68:67-90.
43. Rotsch, C., and M. Radmacher. 2000. Drug-induced changes in cytoskeletal structure and mechanics in fibroblasts: an atomic force microscopy study. Biophys. J. 78:520-535.
44. Laurent, V. M., S. Kasas, A. Yersin, T. E. Schaffer, S. Catsicas, et al. 2005. Gradient of rigidity in the lamellipodia of migrating cells revealed by atomic force microscopy. Biophys. J. 89:667-675.
45. Rotsch, C., K. Jacobson, J. Condeelis, and M. Radmacher. 2001. EGF-stimulated lamellipod extension in adenocarcinoma cells. Ultramicroscopy. 86:97-106.
46. Rotsch, C., K. Jacobson, and M. Radmacher. 1999. Dimensional and mechanical dynamics of active and stable edges in motile fibroblasts investigated by using atomic force microscopy. Proc. Natl. Acad. Sci. USA. 96:921-926.
47. Suter, D. M., L. D. Errante, V. Belotserkovsky, and P. Forscher. 1998. The Ig superfamily cell adhesion molecule, apCAM, mediates growth cone steering by substrate-cytoskeletal coupling. J. Cell Biol. 141:227-240.
48. Lee, A. C., B. Decourt, and D. M. Suter. 2008. Neuronal cell cultures from aplysia for high resolution imaging of growth cones. J. Vis. Exp. 20; doi: 10.3791/662.
49. Martin, Y., C. C. Williams, and H. K. Wickramasinghe. 1987. Atomic force microscope-force mapping and profiling on a sub 100-Å scale. J. Appl. Phys. 61:4723-4729.
50. Zhong, Q., D. Innis, K. Kjoller, and V. B. Elings. 1993. Fractured polymer silica fiber surface studied by tapping mode atomic-force microscopy. Surf. Sci. 290:L688-L692.
51. Schneider, J., Y. F. Dufrene, W. R. Barger Jr., and G. U. Lee. 2000. Atomic force microscope image contrast mechanisms on supported lipid bilayers. Biophys. J. 79:1107-1118.
52. Sader, J. E., J. W. M. Chon, and P. Mulvaney. 1999. Calibration of rectangular atomic force microscope cantilevers. Rev. Sci. Instrum. 70:3967-3969.
53. Higgins, M. J., R. Proksch, J. E. Sader, M. Polcik, S. Mc Endoo, et al. 2006. Noninvasive determination of optical lever sensitivity in atomic force microscopy. Rev. Sci. Instrum. 77:013701-013701-5.
54. Sheiko, S. S., M. Moller, E. M. Reuvekamp, and H. W. Zandbergen. 1993. Calibration and evaluation of scanning-force-microscopy probes. Phys. Rev. B Condens. Matter. 48:5675-5678.
55. Hertz, H. 1881. Ueber die Beruehrung fester elastischer Koerper. J. Reine Angew. Math. 92:156-171.
56. Burnette, D. T., A. W. Schaefer, L. Ji, G. Danuser, and P. Forscher. 2007. Filopodial actin bundles are not necessary for microtubule advance into the peripheral domain of Aplysia neuronal growth cones. Nat. Cell Biol. 9:1360-1369.
57. Wu, D. Y., and D. J. Goldberg. 1993. Regulated tyrosine phosphorylation at the tips of growth cone filopodia. J. Cell Biol. 123:653-664.
58. Suter, D. M., and P. Forscher. 2001. Transmission of growth cone traction force through apCAM-cytoskeletal linkages is regulated by Src family tyrosine kinase activity. J. Cell Biol. 155:427-438.
59. Welnhofer, E. A., L. Zhao, and C. S. Cohan. 1997. Actin dynamics and organization during growth cone morphogenesis in Helisoma neurons. Cell Motil. Cytoskeleton. 37:54-71.
60. Letourneau, P. C. 1983. Differences in the organization of actin in the growth cones compared with the neurites of cultured neurons from chick embryos. J. Cell Biol. 97:963-973.
61. Strasser, G. A., N. A. Rahim, K. E. VanderWaal, F. B. Gertler, and L. M. Lanier. 2004. Arp2/3 is a negative regulator of growth cone translocation. Neuron. 43:81-94.
62. Putman, C. A. J., K. O. Vanderwerf, B. G. Degrooth, N. F. Vanhulst, and J. Greve. 1994. Viscoelasticity of living cells allows high resolution imaging by tapping mode atomic-force microscopy. Biophys. J. 67:1749-1753.
63. Johnson, K. L. 1985. Contact Mechanics. Cambridge University Press, Cambridge, MA.
64. Janmey, P. A., and C. A. McCulloch. 2007. Cell mechanics: integrating cell responses to mechanical stimuli. Annu. Rev. Biomed. Eng. 9:1-34.
65. Wagner, B., R. Tharmann, I. Haase, M. Fischer, and A. R. Bausch. 2006. Cytoskeletal polymer networks: the molecular structure of cross-linkers determines macroscopic properties. Proc. Natl. Acad. Sci. USA. 103:13974-13978.
66. Gittes, F., B. Mickey, J. Nettleton, and J. Howard. 1993. Flexural rigidity of microtubules and actin filaments measured from thermal fluctuations in shape. J. Cell Biol. 120:923-934.
67. Laney, D. E., R. A. Garcia, S. M. Parsons, and H. G. Hansma. 1997. Changes in the elastic properties of cholinergic synaptic vesicles as measured by atomic force microscopy. Biophys. J. 72:806-813.
68. Discher, D. E., P. Janmey, and Y. L. Wang. 2005. Tissue cells feel and respond to the stiffness of their substrate. Science. 310:1139-1143.
69. Lee, G. U., L. A. Chrisey, and R. J. Colton. 1994. Direct measurement of the interaction forces between complementary strands of DNA with atomic force microscopy. Science. 266:771-775.
70. Na, S., O. Collin, F. Chowdhury, B. Tay, M. Ouyang, et al. 2008. Rapid signal transduction in living cells is a unique feature of mechanotransduction. Proc. Natl. Acad. Sci. USA. 105:6626-6631.
71. Bridgman, P. C., S. Dave, C. F. Asnes, A. N. Tullio, and R. S. Adelstein. 2001. Myosin IIB is required for growth cone motility. J. Neurosci. 21:6159-6169.
72. Heidemann, S. R., P. Lamoureux, and R. E. Buxbaum. 1990. Growth cone behavior and production of traction force. J. Cell Biol. 111:1949-1957.
73. O'Connor, T. P., J. S. Duerr, and D. Bentley. 1990. Pioneer growth cone steering decisions mediated by single filopodial contacts in situ. J. Neurosci. 10:3935-3946.
74. Cojoc, D., F. Difato, E. Ferrari, R. B. Shahapure, J. Laishram, et al. 2007. Properties of the force exerted by filopodia and lamellipodia and the involvement of cytoskeletal components. PLoS ONE. 2:e1072.
75. Domke, J., and M. Radmacher. 1998. Measuring the elastic properties of thin polymer films with the atomic force microscope. Langmuir. 14:3320-3325.
76. Reference deleted in proof.
77. Costa, K. D., A. J. Sim, and F. C. Yin. 2006. Non-Hertzian approach to analyzing mechanical properties of endothelial cells probed by atomic force microscopy. J. Biomech. Eng. 128:176-184.
78. Radmacher, M., M. Fritz, and P. K. Hansma. 1995. Imaging soft samples with the atomic-force microscope - gelatin in water and propanol. Biophys. J. 69:264-270.
79. Schwarzer, N. 2000. Arbitrary load distribution on a layered half space. ASME. J. Tribol. 122:672-681.
80. Stone, D. S. 1998. Elastic rebound between an indenter and a layered specimen. Part I. Model. J. Mat. Res. 13:3207-3213.
81. Lulevich, V., T. Zink, H. Y. Chen, F. T. Liu, and G. Y. Liu. 2006. Cell mechanics using atomic force microscopy-based single-cell compression. Langmuir. 22:8151-8155.
82. Pampaloni, F., G. Lattanzi, A. Jonas, T. Surrey, E. Frey, et al. 2006. Thermal fluctuations of grafted microtubules provide evidence of length-dependent persistence length. Proc. Natl. Acad. Sci. USA. 103:10248-10253.