Myosin drives retrograde F-actin flow in neuronal growth cones

Neuron

Volumn 16, Issue 4, 1996, Pages 769-782

  Lin, C H ^a   Espreafico, E M ^c   Mooseker, M S ^b   Forscher, P ^b  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b YALE UNIVERSITY   (United States)

^c NONE

Author keywords

[No Author keywords available]

Indexed keywords

2,3 BUTANEDIONE; F ACTIN; MYOSIN; MYOSIN ADENOSINE TRIPHOSPHATASE; MYOSIN SUBFRAGMENT 1;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; ATTENUATION; CELL MOTILITY; CELL TRANSPORT; CHICKEN; CYTOSKELETON; DOSE RESPONSE; GROWTH CONE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL;

EID: 0029863153     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(00)80097-5     Document Type: Article

References (60)

1. Abercrombie, M., Heaysman, J.E.M., and Pegrum, S.M. (1970). The locomotion of fibroblasts in culture. III. Movement of particles on the dorsal surfaces of leading lamella. Exp. Cell Res. 62, 389-398.
2. Alpert, N.R., Blanchard, E.M., and Mulieri, L.A. (1989). Tension-independent heat in rabbit papillary muscle. J. Physiol. 414, 433-453.
3. Backx, P.M., Gao, W.D., Azon-Backx, M.D., and Marban, E. (1994). Mechanisms of force inhibition by 2,3-butanedione monoxime in rat cardiac muscle: roles of calcium and crossbridge kinetics. J. Physiol. 476, 487-500.
4. Bahler, M., Kroschewski, R., Stoffler, H.E., and Behrmann, T. (1994). Rat myr4 defines a novel subclass of myosin I: identification, distribution, localization, and mapping of calmodulin-binding sites with differential calcium sensitivity. J. Cell Biol. 126, 375-389.
5. Bentley, D., and Toroion-Raymond, A. (1986). Disordered pathfinding by pioneer neuron growth cones deprived of filopodia by cytochalasin treatment. Nature 323, 712-715.
6. Bray, D. (1970). The surface movement during growth of single explanted neurons. Proc. Natl. Acad. Sci. USA 65, 905-910.
7. Bray, D., and White, J.G. (1988). Cortical flow in animal cells. Science 239, 883-888.
8. Cande, W.Z. (1986). Preparation of N-ethylmaleimide-modified heavy meromyosin and its use as a functional probe of actomyosin-based motility. Meth. Enzymol. 134, 473-477.
9. Cheney, R.E., O'Oshea, M.A., Heuser, J.E., Coelho, M.V., Wolenski, J.S., Espreafico, E.M., Forscher, P., Larson, R.E., and Mooseker, M.S. (1993). Brain myosin-V is a two-headed unconventional myosin with motor activity. Cell 75, 13-23.
10. Cheng, T.P., Murakami, N., and Elzinga, M. (1992). Localization of myosin IIB at the leading edge of growth cones from rat dorsal root ganglionic cells. FEBS Lett. 311, 91-94.
11. Cramer, L.P. and Mitchison, T.J. (1995). Myosin is involved in postmitotic cell spreading. J. Cell Biol. 131, 179-189.
12. Cramer, L.P., Mitchison, T.J., and Theriot, J.A. (1994). Actin-dependent motile forces and cell motility. Curr. Opin. Cell Biol. 6, 82-86.
13. Detmers, P., Weber, A., Elzinga, M., Stephens, R.E. (1981). 7-Chloro-4-nitrobenzeno-2-oxa-1,3-diazole actin as a probe for actin polymerization. J. Biol. Chem. 256, 99-105.
14. Espreafico, E.M., Cheney, R.E., Matteoli, M., Nascimento, A.A., De Camilli, P.V., Larson, R.E., and Mooseker, M.S. (1992). Primary structure and cellular localization of chicken brain myosin-V (p190), an unconventional myosin with calmodulin light chains. J. Cell Biol. 119, 1541-1557.
15. Fisher, G.W., Conrad, P.A., DeBiasio, R.L., and Taylor, D.L. (1988). Centripetal transport of cytoplasm, actin, and the cell surface in lamellipodia of fibroblasts. Cell Motil. Cytoskel. 11, 235-247.
16. Forscher, P., and Smith, S.J. (1988). Actions of cytochalasins on the organization of actin filaments and microtubules in a neuronal growth cone. J. Cell Biol. 107, 1505-1516.
17. Forscher, P., and Smith, S.J. (1990). Cytoplasmic actin filaments move particles on the surface of a neuronal growth cone. In Optical Microscopy for Biology. (New York: Wiley-Liss), pp. 459-471.
18. Forscher, P., Lin, C.-H., and Thompson, C. (1992). Novel form of growth cone motility involving site-directed actin filament assembly. Nature 357, 515-518.
19. Fryer, M.W., Neering, L.R., and Stephenson, D.G. (1988). Effects of 2,3-butanedione monoxime on the contractile activation properties of fast- and slow-twitch rat muscle fibers. J. Physiol. (Lond.) 407, 53-75.
20. Grazi, E., Ferri, A., Lanzara, V., Magri, E., Zaccarini, M. (1980). G-actin modified by plasma membrane interaction polymerizes only in the presence of filamentous myosin. FEBS Lett 112, 67-69.
21. Gwathmey, G.K., Hajjar, R.J., and Solaro, J.R. (1992). Contractile deactivation and the uncoupling of crossbridge: effects of 2,3-butanedione monoxime. Circ. Res. 69, 1280-1292.
22. Heath, J.P., and Holifield, B.F. (1991). Cell locomotion: new research tests old idea on membrane and cytoskeletal flow. Cell Motil. Cytoskel. 18, 245-257.
23. Herrmann, C., Wray, J., Travers, F., and Barman, T. (1992). Effect of 2,3-butanedione monoxime on myosin and myofibrillar ATPase: an example of an uncompetitive inhibitor. Biochemistry 31, 12227-12232.
24. Higuchi, H., and Takemori, S. (1989). Butanedione monoxime suppresses contraction and ATPase activity of rabbit skeletal muscle. J. Biochem. 105, 638-643.
25. Horiuti, K., Higuchi, H., Umazume, Y., Konoshi, M., Okazaki, O., and Kurihara, S. (1988). Mechanisms of action of 2,3-butanedione 2-monoxime on contraction of frog skeletal muscle fibers. J. Muscle Res. Cell Motil. 9, 156-164.
26. Kennedy, T.E., and Tessier-Lavigne, M. (1995). Guidance and induction of branch formation in developing axons by target-derived diffusible factors. Curr. Opin. Neurobiol. 5, 83-90.
27. Kielley, W.W., and Harrington, W.F. (1959). A model for myosin molecule. Biochim. Biophys. Acta 41, 401-421.
28. Lee, J., Ishihara, A., Theriot, J.A., and Jacobson, K. (1993). Principles of locomotion for simple-shaped cells. Nature 362, 167-171.
29. Lee, J., Leonard, M., Oliver, T., Ishihara, A., and Jacobson, K. (1994). Traction forces generated by locomoting keratocytes. J. Cell Biol. 127, 1957-1964.
30. Lewis, A.K., and Bridgman, P.C. (1992). Nerve growth cone lamellipodia contain two populations of actin filaments that differ in organization and polarity. J. Cell Biol. 119, 1219-1243.
31. Lin, C.-H., and Forscher, P. (1993). Cytoskeletal remodeling during growth cone-target interactions. J. Cell Biol. 121, 1369-1383.
32. Lin, C.-H., and Forscher, P. (1995). Growth cone advance is inversely proportional to retrograde F-actin flow. Neuron 14, 763-771.
33. Lin, C.-H., Thompson, C.A., and Forscher, P. (1994). Cytoskeletal reorganization underlying growth cone motility. Curr. Opin. Neurobiol. 4, 640-647.
34. Margossian, S.S., and Lowey, S. (1982). Preparation of myosin and its subfragments from rabbit skeletal muscle. Meth. Enzymol. 85, 55-71.
35. McKillop, K.F., Fortsne, N.S., Ranatunga, K.W., and Geeves, M.A. (1994). The influence of 2,3-butanedione-2-monoxime on the interactions between actin and myosin in solution and skinned muscle fibers. J. Muscle Res. Cell Motil. 15, 309-318.
36. Meeusen, R.L., and Cande, W.Z. (1979). N-Ethylmaleimide modified heavy meromyosin: a probe for actomyosin interactions. J. Cell Biol. 82, 57-65.
37. Miller, L., Phillips, M., and Reisler, E. (1988). Polymerization of G-actin by myosin subfragment 1. J. Biol. Chem. 4, 1996-2002.
38. Miller, M., Bower, E., Levitt, P., Li, D., and Chantler, P.D. (1992). Myosin II distribution in neurons is consistent with a role in growth cone motility but not synaptic vesicle mobilization. Neuron 8, 25-44.
39. Mitchison, T., and Kirschner, M. (1988). Cytoskeletal dynamics and nerve growth. Neuron 1, 761-772.
40. Mooseker, M.S., and Cheney, R.E. (1995). Unconventional Myosins. Annu. Rev. Cell Biol. 11, 633-675.
41. Pollard, T.D. (1986). Rate constants for the reactions of ATP- and ADP-actin with the ends of actin filaments. J. Cell Biol. 103, 2747-2754.
42. Pollard, T.D., and Cooper, J.A. (1986). Actin and actin-binding proteins: a critical evaluation of mechanisms and functions. Annu. Rev. Biochem. 55, 987-1035.
43. Rochlin, M.W., Itoh, K.I., Adelstein, R.S., and Bridgman, P.C. (1995). Localization of myosin II A and B isoforms in cultured neurons. J. Cell Sci. 108, 3661-3670.
44. Ruppert, C., Kroschewski, R., and Bahler, M. (1993). Identification, characterization and cloning of myr 1, a mammalian myosin-I. J. Cell Biol. 120, 1393-1403.
45. Schramm, M., Klieber, H.G., and Daut, J. (1994). The energy expenditure of actomyosin ATPase, calcium-ATPase and sodium-potassium-ATPase in guinea pig cardiac ventricular muscle. J. Physiol. 481, 647-662.
46. Smith, S.J. (1988). Neuronal cytomechanics: the actin-based motility of growth cones. Science 242, 708-715.
47. Spudich, J.A., and Watt, S. (1971). The regulation of rabbit skeletal muscle contraction. I. Biochemical studies of the interaction of the tropomyosin-troponin complex with actin and the proteolytic fragments of myosin. J. Biol. Chem. 246, 4866-4871.
48. Steele, D.S., and Smith, G.L. (1993). Effects of 2,3-butanedione monoxime on sarcoplasmic reticulum of saponin-treated rat cardiac muscle. Am. J. Physiol. 265, H1493-1500.
49. Steinen, G.J.M., Zaremba, R., and Elzinga, G. (1995). ATP utilization for calcium uptake and force production in skinned muscle fibers of Xenopus laevis. J. Physiol. 482, 109-122.
50. Svoboda, K., and Block, S.M. (1994). Biological applications of optical forces. Annu. Rev. Biophys. Biomol. Struc. 23, 247-285.
51. Tanaka, E., and Sabry, J. (1995). Making the connection: cytoskeletal rearrangements during growth cone guidance. Cell 83, 171-176.
52. Tessier-Lavigne, M. (1992). Axon guidance by molecular gradients. Curr. Opin. Neurobiol. 2, 60-65.
53. Theriot, J.A., and Mitchison, T.J. (1991). Actin microfilament dynamics in locomoting cells. Nature 352, 126-131.
54. Theriot, J.A., and Mitchison, T.J. (1992a). The nucleation-release model of actin filament dynamics in cell motility. Tr. Cell Biol. 2, 219-222.
55. Theriot, J.A., Mitchison, T.J., Tilney, L.G., and Portnoy, D.A. (1992b). The rate of actin-based motility of intracellular Listeria monocytogenes equals the rate of actin polymerization. Nature 357, 257-260.
56. Tung, L., Sperelakis, N., Ten Erick, R.E., and Solaro, R.J. (1985). Effects of diacetyl monoxime on cardiac excitation-contraction coupling. J. Pharm. Exp. Ther. 232, 688-695.
57. Wang, Y.L. (1985). Exchange of actin subunits at the leading edge of living fibroblasts: possible role of treadmilling. J. Cell Biol. 101, 597-602.
58. West, J.M., and Stephenson, D.G. (1989). Contractile activation and the effects of 2,3-butanedione monoxime (BDM) in skinned cardiac preparation from normal and dystrophic mice (129/ReJ). Pflügers Arch. 413, 546-552.
59. Yamada, K.M., and Wessells, N.K. (1973). Cytochalasin B: effects on membrane ruffling, growth cone and microspike activity, and microfilament structure not due to altered glucose transport. Dev. Biol. 31, 413-420.
60. Zhao, Y., and Kawai, M. (1994). BDM affects nucleotide binding and force generation steps of the crossbridge cycle in rabbit psoas muscle fibers. Am. J. Physiol. 266, C437-447.