Neuromechanics: The Role of Tension in Neuronal Growth and Memory

Nano and Cell Mechanics: Fundamentals and Frontiers

Volumn , Issue , 2012, Pages 35-61

  Ahmed, Wylie W ^a   Rajagopalan, Jagannathan ^b   Tofangchi, Alireza ^a   Saif, Taher A ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^b ARIZONA STATE UNIVERSITY   (United States)

Author keywords

Cell mechanics; Learning; Mechanotransduction; Memory; Neuromechanics; Neuron function; Synaptic plasticity; Vesicle dynamics

Indexed keywords

EID: 84875781635     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9781118482568.ch3     Document Type: Chapter

References (86)

1. Pelham, R.J. and Wang, Y.L. (1997) Cell locomotion and focal adhesions are regulated by substrate flexibility. Proceedings of the National Academy of Sciences of the United States of America, 94 (25), 13661-13665.
2. Vogel, V. and Sheetz, M.P. (2006) Local force and geometry sensing regulate cell functions. Nature Reviews Molecular Cell Biology, 7 (4), 265-275.
3. Engler, A.J., Sen, S., Sweeney, H.L., and Discher, D.E. (2006) Matrix elasticity directs stem cell lineage specification. Cell, 126 (4), 677-689, doi:10.1016/j.cell.2006.06.044.
4. Lecuit, T. and Lenne, P.F. (2007) Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis. Nature Reviews Molecular Cell Biology, 8 (8), 633-644, doi:10.1038/nrm2222.
5. Janmey, P.A. and McCulloch, C.A. (2007) Cell mechanics: integrating cell responses to mechanical stimuli. Annual Review of Biomedical Engineering, 9, 1-34, doi:10.1146/annurev.bioeng.9.060906.151927.
6. Fletcher, D.A. and Mullins, R.D. (2010) Cell mechanics and the cytoskeleton. Nature, 463 (7280), 485-492, doi:10.1038/nature08908.
7. Furchgott, R. and Vanhoutte, P. (1989) Endothelium-derived relaxing and contracting factors. The FASEB Journal: Official Publication of the Federation of American Societies for Experimental Biology, 3 (9), 2007-2018.
8. Huxley, A.F. and Simmons, R.M. (1971) Proposed mechanism of force generation in striated muscle. Nature, 233 (5321), 533-538.
9. Wirtz, H. and Dobbs, L. (1990) Calcium mobilization and exocytosis after one mechanical stretch of lung epithelial cells. Science, 250 (4985), 1266-1269.
10. Wozniak, M.A. and Chen, C.S. (2009) Mechanotransduction in development: a growing role for contractility. Nature Reviews Molecular Cell Biology, 10 (1), 34-43, doi:10.1038/nrm2592.
11. Gorfinkiel, N., Blanchard, G., and Adams, R. (2009) Mechanical control of global cell behaviour during dorsal closure in Drosophila. Development, 136, 1889-1898, http://dev.biologists.org/cgi/content/abstract/136/11/1889.
12. Lecuit, T. (2008) "developmental mechanics": cellular patterns controlled by adhesion, cortical tension and cell division. HFSP Journal, 2 (2), 72-78, doi:10.2976/1.2896332.
13. Rauzi, M., Verant, P., Lecuit, T., and Lenne, P.F. (2008) Nature and anisotropy of cortical forces orienting Drosophila tissue morphogenesis. Nature Cell Biology, 10 (12), 1401-1410, doi:10.1038/ncb1798.
14. Martin, A.C., Kaschube, M., and Wieschaus, E.F. (2009) Pulsed contractions of an actin-myosin network drive apical constriction. Nature, 457 (7228), 495-499, doi:10.1038/nature07522.
15. Thompson, D.W. (1917) On Growth and Form, University Press, Cambridge.
16. Chen, B.M. and Grinnell, A.D. (1995) Integrins and modulation of transmitter release from motor nerve terminals by stretch. Science, 269 (5230), 1578-1580.
17. Lowery, L.A. and Vactor, D.V. (2009) The trip of the tip: understanding the growth cone machinery. Nature Reviews Molecular Cell Biology, 10 (5), 332-343, doi:10.1038/nrm2679.
18. Siechen, S., Yang, S., Chiba, A., and Saif, M.T.A. (2009) Mechanical tension contributes to clustering of neurotransmitter vesicles at presynaptic terminals. Proceedings of the National Academy of Sciences of the United States of America, 106 (31), 12611-12616, doi:10.1073/pnas.0901867106.
19. Franze, K. and Guck, J. (2010) The biophysics of neuronal growth. Reports on Progress in Physics, 73, 094601.
20. Bao, G. and Suresh, S. (2003) Cell and molecular mechanics of biological materials. Nature Materials, 2 (11), 715-725, doi:10.1038/nmat1001.
21. Van Vliet, K.J., Bao, G., and Suresh, S. (2003) The biomechanics toolbox: experimental approaches for living cells and biomolecules. Acta Materialia, 51 (19), 5881-5905.
22. Rajagopalan, J. and Saif, M. (2011) MEMS sensors and microsystems for cell mechanobiology. Journal of Micromechanics and Microengineering, 21, 054002.
23. Levitan, I. and Kaczmarek, L. (2002) The Neuron: Cell and Molecular Biology, Oxford Univerity Press.
24. Alberts, B., Johnson, A., Lewis, J. et al. (2002) Molecular Biology of The Cell , 4th edn., Garland Science, New York.
25. Fischer, M., Kaech, S., Knutti, D., and Matus, A. (1998) Rapid actin-based plasticity in dendritic spines. Neuron, 20 (5), 847-854.
26. Dent, E.W. and Gertler, F.B. (2003) Cytoskeletal dynamics and transport in growth cone motility and axon guidance. Neuron, 40 (2), 209-227.
27. Letourneau, P. (2009) Actin in axons: stable scaffolds and dynamic filaments. Results and Problems in Cell Differentiation, 48, 65-90, doi:10.1007/400_2009_15.
28. Lee, M.K. and Cleveland, D.W. (1996) Neuronal intermediate filaments. Annual Review of Neuroscience, 19, 187-217, doi:10.1146/annurev.ne.19.030196.001155.
29. Hirokawa, N. and Takemura, R. (2005) Molecular motors and mechanisms of directional transport in neurons. Nature Reviews Neuroscience, 6 (3), 201-214, doi:10.1038/nrn1624.
30. Kulic, I.M., Brown, A.E.X., Kim, H. et al. (2008) The role of microtubule movement in bidirectional organelle transport. Proceedings of the National Academy of Sciences of the United States of America, 105 (29), 10011-10016, doi:10.1073/pnas.0800031105, http://www.pnas.org/content/105/29/10011.
31. Rasband, M.N. (2010) The axon initial segment and the maintenance of neuronal polarity. Nature Reviews Neuroscience, 11 (8), 552-562, doi:10.1038/nrn2852.
32. Barnes, A.P. and Polleux, F. (2009) Establishment of axon-dendrite polarity in developing neurons. Annual Review of Neuroscience, 32, 347-381, doi:10.1146/annurev.neuro.31.060407.125536.
33. De Vos, K.J., Grierson, A.J., Ackerley, S., and Miller, C.C.J. (2008) Role of axonal transport in neurodegenerative diseases. Annual Review of Neuroscience, 31, 151-173, doi:10.1146 /annurev.neuro.31.061307.090711.
34. Hawkins, R.D., Kandel, E.R., and Siegelbaum, S.A. (1993) Learning to modulate transmitter release: themes and variations in synaptic plasticity. Annual Review of Neuroscience, 16, 625-665, doi:10.1146/annurev.ne.16.030193.003205.
35. Martin, S.J., Grimwood, P.D., and Morris, R.G. (2000) Synaptic plasticity and memory: an evaluation of the hypothesis. Annual Review of Neuroscience, 23, 649-711, doi:10.1146/annurev.neuro.23.1.649.
36. Kandel, E., Schwartz, J., and Jessell, T. (eds.) (2000) Principles of Neural Science, 4th edn., McGraw-Hill, New York.
37. DePina, A.S. and Langford, G.M. (1999) Vesicle transport: the role of actin filaments and myosin motors. Microscopy Research and Technique, 47 (2), 93-106, doi:10.1002/(SICI)1097-0029(19991015)47:2<93::AID-JEMT2<3.0.CO;2-P.
38. Bridgman, P.C. (2004) Myosin-dependent transport in neurons. Journal of Neurobiology, 58 (2), 164-174, doi:10.1002/neu.10320.
39. Bridgman, P.C. (2009) Myosin motor proteins in the cell biology of axons and other neuronal compartments. Results and Problems in Cell Differentiation, 48, 91-105, doi:10.1007/400_2009_10.
40. Lodish, H., Berk, A., Matsudaira, P. et al. (2003) Molecular Cell Biology, 5th edn., W.H. Freeman.
41. Hirokawa, N., Nitta, R., and Okada, Y. (2009) The mechanisms of kinesin motor motility: lessons from the monomeric motor KIF1A. Nature Reviews Molecular Cell Biology, 10 (12), 877-884, doi:10.1038/nrm2807.
42. Verhey, K.J. and Hammond, J.W. (2009) Traffic control: regulation of kinesin motors. Nature Reviews Molecular Cell Biology, 10 (11), 765-777, doi:10.1038/nrm2782.
43. Kardon, J.R. and Vale, R.D. (2009) Regulators of the cytoplasmic dynein motor. Nature Reviews Molecular Cell Biology, 10 (12), 854-865, doi:10.1038/nrm2804.
44. Takamori, S., Holt, M., Stenius, K. et al. (2006) Molecular anatomy of a trafficking organelle. Cell, 127 (4), 831-846, doi:10.1016/j.cell.2006.10.030.
45. Kidokoro, Y., Kuromi, H., Delgado, R. et al. (2004) Synaptic vesicle pools and plasticity of synaptic transmission at the Drosophila synapse. Brain Research Reviews, 47 (1-3), 18-32, doi:10.1016 /j.brainresrev.2004.05.004.
46. Kelly, R.B. (1993) Storage and release of neurotransmitters. Cell, 72 (Suppl), 43-53.
47. Hökfelt, T., Broberger, C., Xu, Z.Q. et al. (2000) Neuropeptides - an overview. Neuropharmacology, 39 (8), 1337-1356.
48. Kandel, E.R. (2001) The molecular biology of memory storage: a dialogue between genes and synapses. Science, 294 (5544), 1030-1038, doi:10.1126/science.1067020.
49. Holtmaat, A. and Svoboda, K. (2009) Experience-dependent structural synaptic plasticity in the mammalian brain. Nature Reviews Neuroscience, 10 (9), 647-658, doi:10.1038/nrn2699.
50. Cingolani, L.A. and Goda, Y. (2008) Actin in action: the interplay between the actin cytoskeleton and synaptic efficacy. Nature Reviews Neuroscience, 9 (5), 344-356, doi:10.1038/nrn2373.
51. Dillon, C. and Goda, Y. (2005) The actin cytoskeleton: integrating form and function at the synapse. Annual Review of Neuroscience, 28 (1), 25-55, doi:10.1146/neuro.2005.28.issue-1.
52. Dityatev, A., Schachner, M., and Sonderegger, P. (2010) The dual role of the extracellular matrix in synaptic plasticity and homeostasis. Nature Reviews Neuroscience, 11 (11), 735-746, doi:10.1038/nrn2898.
53. Siegelbaum, S.A. and Kandel, E.R. (1991) Learning-related synaptic plasticity: LTP and LTD. Current Opinion in Neurobiology, 1 (1), 113-120.
54. Lamoureux, P., Buxbaum, R.E., and Heidemann, S.R. (1989) Direct evidence that growth cones pull. Nature, 340 (6229), 159-162, doi:10.1038/340159a0.
55. Dennerll, T.J., Lamoureux, P., Buxbaum, R.E., and Heidemann, S.R. (1989) The cytomechanics of axonal elongation and retraction. The Journal of Cell Biology, 109 (6 Pt 1), 3073-3083, http://www .jcb.org/cgi/reprint/109/6/3073.
56. Heidemann, S.R. and Buxbaum, R.E. (1990) Tension as a regulator and integrator of axonal growth. Cell Motility and the Cytoskeleton, 17 (1), 6-10, doi:10.1002/cm.970170103.
57. Weiss, P. (1945) Experiments on cell and axon orientation in vitro; the role of colloidal exudates in tissue organization. The Journal of Experimental Zoology, 100, 353-386.
58. Bray, D. (1979) Mechanical tension produced by nerve cells in tissue culture. Journal of Cell Science, 37, 391-410.
59. Bray, D. (1984) Axonal growth in response to experimentally applied mechanical tension. Developmental Biology, 102 (2), 379-389.
60. Zheng, J., Buxbaum, R.E., and Heidemann, S.R. (1993) Investigation of microtubule assembly and organization accompanying tension-induced neurite initiation. Journal of Cell Science, 104 (Pt 4), 1239-1250.
61. Dennerll, T.J., Joshi, H.C., Steel, V.L. et al. (1988) Tension and compression in the cytoskeleton of PC-12 neurites. II: Quantitative measurements. The Journal of Cell Biology, 107 (2), 665-674.
62. Zheng, J., Lamoureux, P., Santiago, V. et al. (1991) Tensile regulation of axonal elongation and initiation. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 11 (4), 1117-1125.
63. Korneliussen, H. and Jansen, J.K. (1976) Morphological aspects of the elimination of polyneuronal innervation of skeletal muscle fibres in newborn rats. Journal of Neurocytology, 5 (8), 591-604.
64. Bixby, J.L. (1981) Ultrastructural observations on synapse elimination in neonatal rabbit skeletal muscle. Journal of Neurocytology, 10 (1), 81-100.
65. Morrison-Graham, K. (1983) An anatomical and electrophysiological study of synapse elimination at the developing frog neuromuscular junction. Developmental Biology, 99 (2), 298-311.
66. Van Essen, D.C. (1997) A tension-based theory of morphogenesis and compact wiring in the central nervous system. Nature, 385 (6614), 313-318, doi:10.1038/385313a0.
67. Rajagopalan, J., Tofangchi, A., and Saif, T. (2010) Drosophila neurons actively regulate axonal tension in vivo. Biophysical Journal, 99 (10), 3208-3215, doi:10.1016/j.bpj.2010.09.029.
68. Lamoureux, P., Heidemann, S.R., Martzke, N.R., and Miller, K.E. (2010) Growth and elongation within and along the axon. Developmental Neurobiology, 70 (3), 135-149, doi:10.1002/dneu.20764.
69. Pfister, B.J., Iwata, A., Meaney, D.F., and Smith, D.H. (2004) Extreme stretch growth of integrated axons. The Journal of Adhesion Neuroscience: The Official Journal of the Society for Neuroscience, 24 (36), 7978-7983, doi:10.1523/JNEUROSCI.1974-04.2004.
70. Pfister, B.J., Bonislawski, D.P., Smith, D.H., and Cohen, A.S. (2006) Stretch-grown axons retain the ability to transmit active electrical signals. FEBS Letters, 580 (14), 3525-3531, doi:10.1016/j.febslet.2006.05.030.
71. Suter, D.M. and Miller, K.E. (2011) The emerging role of forces in axonal elongation. Progress in Neurobiology, 94, 91-101, doi:10.1016/j.pneurobio.2011.04.002.
72. Dotti, C.G. and Banker, G.A. (1987) Experimentally induced alteration in the polarity of developing neurons. Nature, 330 (6145), 254-256, doi:10.1038/330254a0.
73. Goslin, K. and Banker, G. (1989) Experimental observations on the development of polarity by hippocampal neurons in culture. The Journal of Cell Biology, 108 (4), 1507-1516.
74. Lamoureux, P., Ruthel, G., Buxbaum, R.E., and Heidemann, S.R. (2002) Mechanical tension can specify axonal fate in hippocampal neurons. The Journal of Cell Biology, 159 (3), 499-508, doi:10.1083/jcb.200207174.
75. Suter, D.M., Errante, L.D., Belotserkovsky, V., and Forscher, P. (1998) The Ig superfamily cell adhesion molecule, apCAM, mediates growth cone steering by substrate-cytoskeletal coupling. The Journal of Cell Biology, 141 (1), 227-240.
76. Anava, S., Greenbaum, A., Ben Jacob, E. et al. (2009) The regulative role of neurite mechanical tension in network development. Biophysical Journal, 96 (4), 1661-1670, doi:10.1016/j.bpj.2008.10.058.
77. Flanagan, L.A., Ju, Y.E., Marg, B. et al. (2002) Neurite branching on deformable substrates. Neuroreport, 13 (18), 2411-2415, doi:10.1097/01.wnr.0000048003.96487.97.
78. Franze, K., Gerdelmann, J., Weick, M. et al. (2009) Neurite branch retraction is caused by a thresholddependent mechanical impact. Biophysical Journal, 97 (7), 1883-1890, doi:10.1016/j.bpj.2009.07.033.
79. Fatt, P. and Katz, B. (1952) Spontaneous subthreshold activity at motor nerve endings. The Journal of Physiology, 117 (1), 109-128.
80. Chen, B.M. and Grinnell, A.D. (1997) Kinetics, Ca2+ dependence, and biophysical properties of integrinmediated mechanical modulation of transmitter release from frog motor nerve terminals. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 17 (3), 904-916.
81. Grinnell, A.D., Chen, B.M., Kashani, A. et al. (2003) The role of integrins in the modulation of neurotransmitter release from motor nerve terminals by stretch and hypertonicity. Journal of Neurocytology, 32 (5-8), 489-503, doi:10.1023/B:NEUR.0000020606.58265.b5.
82. Ahmed, W., Li, T., Rubakhin, S. et al. (2012) Mechanical tension modulates local and global vesicle dynamics in neurons. Cellular and Molecular Bioengineering, 5, 115-164.
83. Pender, N. and McCulloch, C.A. (1991) Quantitation of actin polymerization in two human fibroblast sub-types responding to mechanical stretching. Journal of Cell Science, 100 (Pt 1), 187-193.
84. Ahmed, W.W., Kural, M.H., and Saif, T.A. (2010) A novel platform for in situ investigation of cells and tissues under mechanical strain. Acta Biomaterialia, 6 (8), 2979-2990, doi:10.1016/j.actbio.2010.02.035.
85. Bernal, R., Pullarkat, P.A., and Melo, F. (2007) Mechanical properties of axons. Physical Review Letters, 99 (1), 018301, http://scitation.aip.org/getabs/servlet/GetabsServlet?prog=normal&id=PRLTAO000099000001018301000001&idtype=cvips&gifs=yes.
86. Howard, J. (2009) Mechanical signaling in networks of motor and cytoskeletal proteins. Annual Review of Biophysics, 38, 217-234, doi:10.1146/annurev.biophys.050708.133732.