Mechanical tension modulates local and global vesicle dynamics in neurons

Cellular and Molecular Bioengineering

Volumn 5, Issue 2, 2012, Pages 155-164

  Ahmed, W W ^a   Li, T C ^b   Rubakhin, S S ^a   Chiba, A ^b   Sweedler, J V ^a   Saif, T A ^a,c  

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

^b Department of Biology   (United States)

^c University of Illinois at Urbana Champaign   (United States)

Author keywords

Aplysia; Cell mechanics; Drosophila; Live imaging; Subcellular; Vesicle tracking

Indexed keywords

CALCIUM ION;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APLYSIA; BIOACCUMULATION; BRAIN NERVE CELL; CELL VACUOLE; CONFERENCE PAPER; DROSOPHILA; EMBRYO; IN VITRO STUDY; IN VIVO STUDY; LARGE DENSE CORE VESICLE; MECHANICAL STRESS; MOLECULAR DYNAMICS; MOLECULAR IMAGING; NERVE COMPRESSION; NEURITE; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; SYNAPSE VESICLE;

APLYSIA;

EID: 84863725748     PISSN: 18655025     EISSN: 18655033     Source Type: Journal    
DOI: 10.1007/s12195-012-0223-1     Document Type: Conference Paper

References (53)

1. Abramoff, M. D., P. J. Magalhaes, and S. J. Ram. Image processing with ImageJ. Biophoton. Int. 11(7):36-41, 2004. (Pubitemid 43863211)
2. Ahmed, W. W., M. H. Kural, and T. A. Saif. A novel platform for in situ investigation of cells and tissues under mechanical strain. Acta Biomater. 6(8):2979-2990, 2010.
3. Ayali, A. The function of mechanical tension in neuronal and network development. Integr. Biol. 2(4):178-182, 2010.
4. Bernal, R., P. A. Pullarkat, and F. Melo. Mechanical properties of axons. Phys. Rev. Lett. 99(1):018301, 2007.
5. Bixby, J. L. Ultrastructural observations on synapse elimination in neonatal rabbit skeletal muscle. J. Neurocytol. 10(1):81-100, 1981. (Pubitemid 11145909)
6. Bloom, O., E. Evergren, N. Tomilin, O. Kjaerulff, P. Low, L. Brodin, V. A. Pieribone, P. Greengard, and O. Shupliakov. Colocalization of synapsin and actin during synaptic vesicle recycling. J. Cell Biol. 161(4):737-747, 2003. (Pubitemid 36648757)
7. Bray, D. Mechanical tension produced by nerve cells in tissue culture. J. Cell Sci. 37:391-410, 1979. (Pubitemid 9200804)
8. Budnik, V., and C. Ruiz-Canada. The Fly Neuromuscular Junction. San Diego: Elsevier, p. 421, 2006.
9. Chen, B. M., and A. D. Grinnell. Integrins and modulation of transmitter release from motor nerve terminals by stretch. Science 269(5230):1578-1580, 1995.
10. 2+ dependence, and biophysical properties of integrin-mediated mechanical modulation of transmitter release from frog motor nerve terminals. J. Neurosci. 17(3):904-916, 1997. (Pubitemid 27043949)
11. Cingolani, L. A., and Y. Goda. Actin in action: the interplay between the actin cytoskeleton and synaptic efficacy. Nat. Rev. Neurosci. 9(5):344-356, 2008. (Pubitemid 351556045)
12. Ciobanu, L., S. S. Rubakhin, J. N. Stuart, R. R. Fuller, A. G. Webb, and J. V. Sweedler. Characterization of the physicochemical parameters of dense core atrial gland and lucent red hemiduct vesicles in Aplysia californica. Anal. Chem. 76(8):2331-2335, 2004. (Pubitemid 38496076)
13. Dennerll, T. J., P. Lamoureux, R. E. Buxbaum, and S. R. Heidemann. The cytomechanics of axonal elongation and retraction. J. Cell Biol. 109(6):3073-3083, 1989. (Pubitemid 20011931)
14. Dillon, C., and Y. Goda. The actin cytoskeleton: integrating form and function at the synapse. Annu. Rev. Neurosci. 28(1):25-55, 2005. (Pubitemid 41098898)
15. Duffy, J. B. GAL4 system in Drosophila: a fly geneticist's swiss army knife. Genesis 34:1-15, 2002.
16. Fatt, P., and B. Katz. Spontaneous subthreshold activity at motor nerve endings. J. Physiol. (Lond.) 117(1):109-128, 1952.
17. Forscher, P., and S. J. Smith. Actions of cytochalasins on the organization of actin filaments and microtubules in a neuronal growth cone. J. Cell Biol. 107(4):1505-1516, 1988.
18. Franze, K., J. Gerdelmann, M. Weick, T. Betz, S. Pawlizak, M. Lakadamyali, J. Bayer, K. Rillich, M. Gogler, Y. Lu, A. Reichenbach, P. A. Janmey, and J. A. Kas. Neurite branch retraction is caused by a threshold-dependent mechanical impact. Biophys. J. 97(7):1883-1890, 2009.
19. Franze, K., and J. Guck. The biophysics of neuronal growth. Rep. Prog. Phys. 73:094601, 2010.
20. Franze, K., A. Reichenbach, and J. Kas. Biomechanics of the CNS. In: Mechanosensitivity of the Nervous System, Vol. 10, edited by A. Kamkin, and I. Kiseleva. Dordrecht: Springer, 2008, pp. 173-213.
21. Gittes, F., E. Meyhofer, S. Baek, and J. Howard. Directional loading of the kinesin motor molecule as it buckles a microtubule. Biophys. J. 70(1):418-429, 1996. (Pubitemid 26021480)
22. Goldberg, D. J., and D. W. Burmeister. Stages in axon formation: observations of growth of Aplysia axons in culture using video-enhanced contrast-differential interference contrast microscopy. J. Cell Biol. 103(5):1921-1931, 1986. (Pubitemid 17189048)
23. Grinnell, A. D., B. M. Chen, A. Kashani, J. Lin, K. Suzuki, and Y. Kidokoro. The role of integrins in the modulation of neurotransmitter release from motor nerve terminals by stretch and hypertonicity. J. Neurocytol. 32(5-8):489-503, 2003. (Pubitemid 39011242)
24. Hawkins, R. D., E. R. Kandel, and S. A. Siegelbaum. Learning to modulate transmitter release: themes and variations in synaptic plasticity. Annu. Rev. Neurosci. 16:625-665, 1993. (Pubitemid 23074022)
25. Heidemann, S. R., and R. E. Buxbaum. Tension as a regulator and integrator of axonal growth. Cell Motil. Cytoskelet. 17(1):6-10, 1990. (Pubitemid 20313040)
26. Hummon, A. B., A. Amare, and J. V. Sweedler. Discovering new invertebrate neuropeptides using mass spectrometry. Mass Spectrom. Rev. 25(1):77-98, 2006.
27. Kamber, D., H. Erez, and M. E. Spira. Local calciumdependent mechanisms determine whether a cut axonal end assembles a retarded endbulb or competent growth cone. Exp. Neurol. 219(1):112-125, 2009.
28. Keshishian, H., K. S. Broadie, A. Chiba, and M. Bate. The drosophila neuromuscular junction: a model system for studying synaptic development and function. Annu. Rev. Neurosci. 19:545-575, 1996. (Pubitemid 26080839)
29. Korneliussen, H., and J. K. Jansen. Morphological aspects of the elimination of polyneuronal innervation of skeletal muscle fibres in newborn rats. J. Neurocytol. 5(8):591-604, 1976.
30. Lamoureux, P., R. E. Buxbaum, and S. R. Heidemann. Direct evidence that growth cones pull. Nature 340(6229): 159-162, 1989. (Pubitemid 19175371)
31. Morrison-Graham, K. An anatomical and electrophysiological study of synapse elimination at the developing frog neuromuscular junction. Dev. Biol. 99(2):298-311, 1983.
32. O'Toole, M., P. Lamoureux, and K. E. Miller. A physical model of axonal elongation: force, viscosity, and adhesions govern the mode of outgrowth. Biophys. J. 94(7):2610-2620, 2008.
33. O'Toole, M., R. Latham, R. M. Baqri, and K. E. Miller. Modeling mitochondrial dynamics during in vivo axonal elongation. J. Theor. Biol. 255(4):369-377, 2008.
34. O'Toole, M., and K. E. Miller. The role of stretching in slow axonal transport. Biophys. J. 100(2):351-360, 2011.
35. Owald, D., and S. J. Sigrist. Assembling the presynaptic active zone. Curr. Opin. Neurobiol. 19(3):311-318, 2009.
36. Pender, N., and C. A. McCulloch. Quantitation of actin polymerization in two human fibroblast sub-types responding to mechanical stretching. J. Cell Sci. 100:187-193, 1991. (Pubitemid 21925049)
37. Pfister, B. J., D. P. Bonislawski, D. H. Smith, and A. S. Cohen. Stretch-grown axons retain the ability to transmit active electrical signals. FEBS Lett. 580(14):3525-3531, 2006. (Pubitemid 43795912)
38. Pfister, B. J., A. Iwata, D. F. Meaney, and D. H. Smith. Extreme stretch growth of integrated axons. J. Neurosci. 24(36):7978-7983, 2004. (Pubitemid 39215704)
39. Putnam, A. J., K. Schultz, and D. J. Mooney. Control of microtubule assembly by extracellular matrix and externally applied strain. AJP-Cell Physiol. 280(3):C556-C564, 2001.
40. Rajagopalan, J., A. Tofangchi, and T. A. Saif. Drosophila neurons actively regulate axonal tension in vivo. Biophys. J. 99(10):3208-3215, 2010.
41. Rogers, S. S., T. A. Waigh, X. Zhao, and J. R. Lu. Precise particle tracking against a complicated background: polynomial fitting with gaussian weight. Phys. Biol. 4:220-227, 2007. (Pubitemid 47568918)
42. Romanova, E. V., S. P. Oxley, S. S. Rubakhin, P. W. Bohn, and J. V. Sweedler. Self-assembled monolayers of alkanethiols on gold modulate electrophysiological parameters and cellular morphology of cultured neurons. Biomaterials 27(8):1665-1669, 2006. (Pubitemid 41739592)
43. Rubakhin, S. S., R. W. Garden, R. R. Fuller, and J. V. Sweedler. Measuring the peptides in individual organelles withmass spectrometry.Nat. Biotechnol. 18(2):172-175, 2000. (Pubitemid 30091177)
44. Shemesh, O. A., H. Erez, I. Ginzburg, and M. E. Spira. Tau-induced traffic jams reflect organelles accumulation at points of microtubule polar mismatching. Traffic 9(4):458-471, 2008. (Pubitemid 351351608)
45. Shemesh, O. A., and M. E. Spira. Paclitaxel induces axonal microtubules polar reconfiguration and impaired organelle transport: implications for the pathogenesis of paclitaxelinduced polyneuropathy. Acta Neuropathol. 119(2):235-248, 2010.
46. Siechen, S., S. Yang, A. Chiba, and T. A. Saif. Mechanical tension contributes to clustering of neurotransmitter vesicles at presynaptic terminals. Proc. Natl Acad. Sci. USA 106(31):12611-12616, 2009.
47. Sigrist, S. J., D. F. Reiff, P. R. Thiel, J. R. Steinert, and C. M. Schuster. Experience-dependent strengthening of Drosophila neuromuscular junctions. J. Neurosci. 23(16): 6546-6556, 2003. (Pubitemid 36909881)
48. Smith, D. H., J. A. Wolf, and D. F. Meaney. A new strategy to produce sustained growth of central nervous system axons: continuous mechanical tension. Tissue Eng. 7(2):131-139, 2001. (Pubitemid 32295148)
49. Suter, D. M., L. D. Errante, V. Belotserkovsky, and P. Forscher. The Ig superfamily cell adhesion molecule, apCAM, mediates growth cone steering by substratecytoskeletal coupling. J. Cell Biol. 141(1):227-240, 1998. (Pubitemid 28182654)
50. Suter, D. M., and P. Forscher. Transmission of growth cone traction force through apCAM-cytoskeletal linkages is regulated by src family tyrosine kinase activity. J. Cell Biol. 155(3):427-438, 2001. (Pubitemid 34289333)
51. Suter, D. M., and K. E. Miller. The emerging role of forces in axonal elongation. Prog. Neurobiol. 94:91-101, 2011.
52. Weiss, P. Experiments on cell and axon orientation in vitro; the role of colloidal exudates in tissue organization. J. Exp. Zool. 100:353-386, 1945.
53. Zhang, Y. Q., C. K. Rodesch, and K. S. Broadie. Living synaptic vesicle marker: synaptotagmin-GFP. Genesis 34(1-2):142-145, 2002.