Abstract
The myosin super family is an extended family of actin-based motor proteins that can be divided into 15–18 structurally distinct classes (Sellers, J. R (2000) Biochemica et Biophysica Acta, 1496, 3–22; Hodge, T. & Cope, M. J. T. V. (2000) Journal of Cell Science, 113, 3353–3354; Berg, J. S., Powell, B. C. & Cheney, R. E. (2001) Molecular Biology of the Cell, 12, 780–794). Many myosin classes contain multiple members, including different isoforms within the same species as well as homologous proteins from different species. A number of the myosin classes are expressed in multiple cell types in vertebrates, including neurons. Surprisingly little is known about the neuronal function of these different myosins. In this review we concentrate on the vertebrate myosins known to be present in neuronal axons. We take a simplistic view of this topic, addressing a number of specific questions. (1) Which myosins are present in neurons? (2) Do their levels change during development? (3) Are the neuronal forms unique in any way? (4) Which neuronal myosins are located in axons and how are they distributed? (5) What do these myosins do and are they essential for a specific neuronal function?
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AMANO, M., CHIHARA, K., NAKAMURA, N., FUKATA, Y., YANO, T., SHIBATA, M., IKEBE, M. & KAIBUCHI, K. (1998) Myosin II activation promotes neurite retraction during the action of Rho and Rho-kinase. Genes to Cells 3, 177-188.
BAHLER, M., KROSCHEWSKI, R., STOFFLER, H.-E. & BERHMAN, T. (1994) Rat myr 4 defines a novel subclass of myosin I: Identification, distribution, localization, and mapping of calmodulin-binding sites with differential calcium sensitivity. Journal of Cell Biology 126, 375-389.
BENTLEY, D. & TOROIAN-RAYMOND, A. (1986) A disoriented pathfinding by pioneer neurone growth cone deprived of filopodia by cytochalasin treatment. Nature 323, 712-715.
BERG, J. S., POWELL, B. C. & CHENEY, R. E. (2001) A Millennial Myosin Census. Molecular Biology of the Cell, 12, 780-794.
BRAY, D. (1982) Filopodia contraction and growth cone guidance. In Cell Behavior edited by BELLAIRS, R., CURTIS, A. & DUNN, G. Cambridge University Press, Cambridge, 299-319.
BRIDGMAN, P. C. (1999) Myosin Va movements in normal and dilute-lethal axons provide support for a dual filament motor complex. Journal of Cell Biology 146, 1045-1060.
CHIEREGATTI, E., GARTNER, A., STOFFLER, H. E. & BAHLER, M. (1998) Myr 7 is a novel myosin IX RhoGAP expressed in rat brain. Journal of Cell Science 111, 3597-3608.
DENNERLL, T. J., LAMOUREUX, P., BUXBAUM, R. E. & HEIDEMANN, S. R. (1989) The cytomechanics of axonal elongation and retraction. Journal of Cell Biology 109, 3073-3083.
DRENGK, A. C., KAJIWARA, J. K., GARCIA, S. B., CARMO, V. S., LARSON, R. E., ZUCOLOTO, S. & ESPREAFICO, E. M. (2000) Immunolocalisation of myosin-V in the enteric nervous system of the rat. Journal of the Autonomic Nervous System 78, 109-112.
ESPINDOLA, F. S., ESPREAFICO, E. M., COELHO, M. V., MARTINS, A. R., COSTA, F. R. C., MOOSEKER, M. S. & LARSON, R. E. (1992) Biochemical and immunological characterization of p190-calmodulin complex from vertebrate brain: a novel calmodulin-binding myosin. Journal of Cell Biology 118, 359-368.
EVANS, L. L. & BRIDGMAN, P. C. (1995) Particles move along actin filament bundles in nerve growth cones. Proceedings of the National Academy of Sciences, USA 92, 10954-10958.
EVANS, L. L., HAMMER, J. & BRIDGMAN, P. C. (1997) Subcellular localization of myosin V in nerve growth cones and outgrowth from dilute-lethal neurons. Journal of Cell Science 110, 439-449.
EVANS, L. L., LEE, A. J., BRIDGMAN, P. C. & MOOSEKER, M. S. (1998) Vesicle-associated brain myosin-V can be activated to catalyze actin-based transport. Journal of Cell Science 111, 2055-2066.
GREWAL, P. K., JONES, A. M., MACONCHI, M., LEMMERS, R. J. F., FRANTS, R. R. & HEWITT, J. E. (1999) Cloning of the murine unconventional myosin gene Myo9b and identification of alternative splicing. Gene 240, 389-398.
HASSON, T., GILLESPIE, P. G., GARCIA, J. A., MACDONALD, R. B., ZHAO, Y.-D., YEE, A. G., MOOSEKER, M. S. & COREY, D. P. (1997) Unconventional myosins in inner-ear sensory epithelia. Journal of Cell Biology 137, 1287-1307.
HEIDEMANN, S. R., LAMOUREUX, P. & BUXBAUM, R. E. (1990) Growth cone behavior and production of traction force. Journal of Cell Biology 111, 1949-1957.
HODGE, T. & COPE, M. J. T. V. (2000) A myosin family tree. Journal of Cell Science 113, 3353-3354.
ITOH, K. & ADELSTEIN, R. S. (1995) Neuronal cell expression of inserted isoforms of vertebrate nonmuscle myosin heavy chain II-B. Journal of Biological Chemistry 270, 14533-14540.
KAWAMOTO, S. & ADLESTEIN, R. S. (1991) Chicken nonmuscle myosin heavy chains: differential expression of two mRNAs and evidence for two different polypeptides. Journal of Cell Biology 112, 915-924.
KATER, S. B. & REHDER, V. (1995) The sensory-motor role of growth cone filopodia. Current Opinion in Neurobiology 5, 68-74.
LANGFORD, G. M. & MOLYNEAUX, B. J. (1998) Myosin V in the brain: mutations lead to neurological defects. Brain Research Brain Research Reviews 28, 1-8.
LAMOUREUX, P., BUXBAUM, R. E. & HEIDEMANN, S. R. (1989) Direct evidence that growth cones pull. Nature 340, 159-162.
LAMBERT, J., NAEYAERT, J. M., CALLENS, T., DEPAEPA, A. & MESSIAEN, L. (1998) Human myosin V gene produces different transcripts in a cell typespecific manner. Biochemical & Biophysical Research Communications 252, 329-333.
LECHLER, T., SHEVCHENKO, A. & LI, R. (2000) Direct involvement of yeast type I myosins in Cdc42-dependent actin polymerization. Journal of Cell Biology 148, 363-373.
LEWIS, A. K. & BRIDGMAN, P. C. (1992) Nerve growth cone lamellipodia contain two populations of actin filaments that differ in organization and polarity. Journal of Cell Biology 119, 1219-1243.
LEWIS, A. K. & BRIDGMAN, P. C. (1996) Mammalian myosin Iα is concentrated near the plasma membrane in nerve growth cones. Cell Motility and the Cytoskeleton 33, 130-150.
LIN, C. H., ESPREAFICO, E. M., MOOSEKER, M. S. & FORSCHER, P. (1996) Myosin drives retrograde F-actin flow in neuronal growth cones. Neuron 16, 769-782.
LICHTMAN, J. W. & COLMAN, H. (2000) Synapse elimination and indelible memory. Neuron 25, 269-278.
MATSUMURA, S., KUMON, A. & CHIBA, T. (1985) Proteolytic substructure of brain myosin. Journal of Biological Chemistry 260, 1959-1966.
MARTIN, M. A. E., HURD, D. D. & SAXTON, W. M. (1999) Kinesins in the nervous system. Cellular and Molecular Life Sciences 56, 200-216.
MERCER, J. A., SEPERACK, P. K., STROBEL, M. C., COPELAND, N. G. & JENKINS, N. A. (1991) Novel myosin heavy chain encoded by murine dilute coat colour locus. Nature 349, 709-713.
MILLER, M., BOWER, E., LEVITT, P., LI, D. & 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.
MORI, Y., MINORU, W., ODA, S.-I., FLETCHER, C., SEKIGUCHI, N., MORI, E., COPELAND, N. G., JENKINS, N. A., MATSUSHITA, K. & IMOTO, K. (2000) Reduced voltage sensitivity of activation of P/Qtype Ca2+ channels is associated with the ataxic mouse mutation rolling nagoya (tgrol). Journal of Neuroscience 20, 5654-5662.
PREKARIS, R. & TERRIAN, D. M. (1997) Brain myosin V is a synaptic vesicle-associated motor protein: Evidence for a Ca2+-dependent interaction with the synaptobrevinsynaptophysin complex. Journal of Cell Biology 137, 1589-1601.
POLLARD, T. D., DOBERSTEIN, S. K. & ZOT, H. G. (1991) Myosin-I Annual Review of Physiology 53, 653-681.
REINHARD, J., SCHEEL, A., DIEKMANN, D., HALL, A., RUPPERT, C. & BAHLER, M. (1995) A novel type of myosin implicated in signaling by rho family of GTPases. EMBO Journal 14, 697-704.
RHYU, I. J., ABBOT, L. C., WALKER, D. B. & SOTELO, C. (1999) An ultrastructural study of granule cell/Purkinje cell synapses in tottering (tgla/tgla) and compound heterozygous tottering/leaner (tg/tgla) mice. Neuroscience 90, 717-728.
RIDLEY, A. J. & HALL, A. (1992) The small GTP-binding protein rho regulates the assembly of focal adhesion and actin stress fibers in response to growth factors. Cell 70, 389-399.
ROBINSON, D. N. & SPUDICH, J. A. (2000) Towards a molecular understanding of cytokinesis. Trends in Cell Biology 10, 228-237.
ROCHLIN, M. W., ITOH, K., ADELSTEIN, R. S. & BRIDGMAN, P. C. (1995) Localization of myosin II A and B isoforms in cultured neurons. Journal of Cell Science 108, 3661-3670.
RUPPERT, C., KROSCHEWSKI, & BAHLER, M. (1993). Identification, characterization and cloning of myr 1, a mammalian myosin-I. Journal of Cell Biology 120, 1393-1403.
RUPPERT, C., GODEL, J., MULLER, R. T., KROSCHEWSKI, R., REINHARD, J. & BAHLER, M. (1995) Localization of the rat myosin I molecules myr 1 and myr 2 and in vivo targeting of their tail domains. Journal of Cell Science 108, 3775-3786.
SELF, T. J., SOBE, T., COPELAND, N. G. & JENKINS, N. A. (1999) Role of myosin VI in the differentiation of cochlear hair cells. Developmental Biology 214, 331-341.
SELLERS, J. R. (2000) Myosins: a diverse superfamily. Biochemica et Biophysica Acta 1496, 3-22.
SEPERACK, P. K., MERCER, J. A., STROBEL, M. C., COPELAND, N. G. & JENKINS, N. A. (1995) Retroviral sequences located within an intron of the dilute gene alter dilute expression in a tissue-specific manner. EMBO Journal 14, 2326-2332.
SHERR, E. H., JOYCE, M. P. & GREENE, L. A. (1993) Mammalian myosin Iα, Iβ, and Iγ: New widely expressed genes of the myosin I family. Journal of Cell Biology 120, 1405-1416.
SUTER, D. M., ESPINDOLA, F. S., LIN, C.-H., FORSCHER, P. & MOOSEKER, M. S. (2000) Localization of unconventional myosins V and VI in neuronal growth cones. Journal of Neurobiology 42, 370-382.
SVITKINA, T. M., VERHOVSKY, A. B., MCQUADE, K. M. & BORISY, G. G. (1997) Analysis of the actin-myosin II system in fish epidermal keratocytes mechanism of cell body translocation. Journal of Cell Biology 139, 397-415.
TABB, J. S., MOLYNEAUX, B. J., COHEN, D. L., KUZNETSOV, S. A. & LANFORD, G. M. (1998) Transport of ER vesicles on actin filaments in neurons by myosin V. Journal of Cell Science 111, 3221-3234.
TAKAHASHI, M., HIRANO, T., UCHIDA, K. & YAMAGISHI, A. (1999) Developmentally regulated expression of a nonmuscle myosin heavy chain IIB inserted isoform in rat brain. Biochemical & Biophysical Research Communications 259, 29-33.
TAKAGISHI, Y., ODA, S. I., HAYASKA, S., DEKKEROHNE, K., SHIKATA, T., INOUYE, M. & YAMAMURA, H. (1996) The dilute-lethal (dl) gene attacks a Ca2+ store in the dendritic spine of Purkinje cells in mice. Neuroscience Letters 215, 169-172.
TULLIO, A. N., ACCILI, D., FERRANS, V. J., YU, Z.-X., TAKEDA, K., GRINBERG, A., WESTPHAL, H., PRESTON, Y. A. & ADELSTEIN, R. S. (1997) Nonmuscle myosin II-B is required for normal development of the mouse heart. Proceedings of the National Academy of Sciences USA 94, 12407-12412.
TULLIO, A. D., BRIDGMAN, P. C., TRESSER, N. J., CHAN, C.-C., CONTI, M. A., ADELSTEIN, R. S. & HARA, Y. (2001) Structural abnormalities develop in the brain following ablation of the gene encoding nonmuscle myosin II-B heavy chain. Journal of Comparative Neurology, 433, 62-74.
VERKHOVSKY, A. B., SVITKINA, T. M. & BORISY, G. G. (1995) Myosin II filament assemblies in the active lamella of fibroblasts: Their morphogenesis and role in the formation of actin filament bundles. Journal of Cell Biology 131, 989-1002.
WAGNER, M. C., BARYLKO, B. & ALBANESI, J. B. (1992) Tissue distribution and subcellular localization of mammalian myosin I. Journal of Cell Biology 119, 163-170.
WANG, F.-S., WOLENSKI, J. S., CHENEY, R. E., MOOSEKER, M. S. & JAY, D. G. (1996) Function of myosin-V in filopodia extension of neuronal growth cones. Science 273, 660-663.
WELLS, A. L., LIN, A. W., CHEN, L. Q. & SWEENY, H. L. (1999) Myosin VI is an actin-based motor that moves backwards. Nature 401, 505-508.
WIRTH, J. A., JENSEN, K. A., POST, P. L., BEMENT, W. M. & MOOSEKER, M. (1996) Human myosin IXb, an unconventional myosin with a chimerin-like rho/rac GTPase-activating protein domain in its tail. Journal of Cell Science 109, 653-661.
WU, X., JUNG, G. & HAMMER III, J. A. (2000) Functions of unconventional myosins. Current Opinion in Cell Biology 12, 42-51.
WYLIE, S. R., WU, P. J., PATEL, H. & CHANTLER, P. D. (1998) A conventional myosin motor drives neurite outgrowth. Proceedings of the National Academy of Sciences of the United States of America 95, 12967-12972.
ZHAO, L.-P., KOSLOVSKY, J. S., REINHARD, J., BAHLER, M., WITT, A. E., PROVANCE, D. W. & MERCER, J. A. (1996) Cloning and characterization of myr 6, an unconventional myosin of the dilute/myosin-V family. Proceedings of the National Academy of Science, USA 93, 10826-10831.
ZHENG, J. Q., WAN, J.-J. & POO, M.-M. (1996) Essential role of filopodia in chemotropic turning of nerve growth cone induced by a glutamate gradient. Journal of Neuroscience 16, 1140-1149.
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Bridgman, P.C., Elkin, L.L. Axonal myosins. J Neurocytol 29, 831–841 (2000). https://doi.org/10.1023/A:1010947525181
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DOI: https://doi.org/10.1023/A:1010947525181