Myosin VI: A structural role in actin organization important for protein and organelle localization and trafficking

Current Opinion in Cell Biology

Volumn 16, Issue 2, 2004, Pages 189-194

  Frank, Deborah J ^a   Noguchi, Tatsuhiko ^a   Miller, Kathryn G ^a  

^a WASHINGTON UNIVERSITY   (United States)

Author keywords

actin related protein; Arp

Indexed keywords

ACTIN; ACTIN RELATED PROTEIN 2; ACTIN RELATED PROTEIN 3; MYOSIN; MYOSIN VI; UNCLASSIFIED DRUG;

ACTIN FILAMENT; CELL MEMBRANE; CELL ORGANELLE; CROSS LINKING; DROSOPHILA MELANOGASTER; ENDOCYTOSIS; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STABILITY; PROTEIN STRUCTURE; REGULATORY MECHANISM; REVIEW;

ACTINS; ANIMALS; CELL COMPARTMENTATION; HUMANS; INTRACELLULAR MEMBRANES; MICROFILAMENTS; MODELS, ANIMAL; MYOSIN HEAVY CHAINS; ORGANELLES; PROTEIN BINDING; PROTEIN TRANSPORT;

DROSOPHILA MELANOGASTER; MAMMALIA; MELANOGASTER;

EID: 2942592305     PISSN: 09550674     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ceb.2004.02.001     Document Type: Review

References (33)

1. Wells A.L., Lin A.W., Chen L.Q., Safer D., Cain S.M., Hasson T., Carragher B.O., Milligan R.A., Sweeney H.L. Myosin VI is an actin-based motor that moves backwards. Nature. 401:1999;505-508
2. Rock R.S., Rice S.E., Wells A.L., Purcell T.J., Spudich J.A., Sweeney H.L. Myosin VI is a processive motor with a large step size. Proc Natl Acad Sci U S A. 98:2001;13655-13659
3. Nishikawa S., Homma K., Komori Y., Iwaki M., Wazawa T., Hikikoshi Iwane A., Saito J., Ikebe R., Katayama E., Yanagida T., et al. Class VI myosin moves processively along actin filaments backward with large steps. Biochem Biophys Res Commun. 290:2002;311-317 This paper confirms the results of Rock, et al. [2] showing that myosin VI is processive and has a large step size. The authors also present electron microscopy data suggesting that binding of myosin VI promotes the formation of actin filament 'hot spots' that attract a myosin head to a position 36 nm, or one helical turn, away.
4. De La Cruz E.M., Ostap E.M., Sweeney H.L. Kinetic mechanism and regulation of myosin VI. J Biol Chem. 276:2001;32373-32381
5. Mehta A.D., Rock R.S., Rief M., Spudich J.A., Mooseker M.S., Cheney R.E. Myosin-V is a processive actin-based motor. Nature. 400:1999;590-593
6. Rogers S.L., Gelfand V.I. Myosin cooperates with microtubule motors during organelle transport in melanophores. Curr Biol. 8:1998;161-164
7. Gross S.P., Tuma M.C., Deacon S.W., Serpinskaya A.S., Reilein A.R., Gelfand V.I. Interactions and regulation of molecular motors in Xenopus melanophores. J Cell Biol. 156:2002;855-865
8. Schott D.H., Collins R.N., Bretscher A. Secretory vesicle transport velocity in living cells depends on the myosin-V lever arm length. J Cell Biol. 156:2002;35-40
9. Rief M., Rock R.S., Mehta A.D., Mooseker M.S., Cheney R.E., Spudich J.A. Myosin-V stepping kinetics: a molecular model for processivity. Proc Natl Acad Sci U S A. 97:2000;9482-9486
10. Yildiz A., Forkey J.N., McKinney S.A., Ha T., Goldman Y.E., Selvin P.R. Myosin V walks hand-over-hand: single fluorophore imaging with 1.5-nm localization. Science. 300:2003;2061-2065
11. Buss F., Arden S.D., Lindsay M., Luzio J.P., Kendrick-Jones J. Myosin VI isoform localized to clathrin-coated vesicles with a role in clathrin-mediated endocytosis. EMBO J. 20:2001;3676-3684
12. Petritsch C., Tavosanis G., Turck C.W., Jan L.Y., Jan Y.N. The Drosophila myosin VI jaguar is required for basal protein targeting and correct spindle orientation in mitotic neuroblasts. Dev Cell. 4:2003;273-281 Using three different methods (analysis of a newly generated null allele, RNA interference, and expression of a dominant-negative form of the protein), these authors show that myosin VI is involved in the localization of cell fate determinants in dividing neuroblasts.
13. Geisbrecht E.R., Montell D.J. Myosin VI is required for E-cadherin-mediated border cell migration. Nat Cell Biol. 4:2002;616-620 Myosin VI is shown to be expressed in border cells during their migration. Reduction of myosin VI expression results in a failure of migration. The authors also show that myosin VI is in a complex with β-catenin (armadillo) and cadherin; loss of myosin VI causes a reduction of the expression of both of these proteins. Overexpression of cadherin can rescue the migration defect. Thus the role of myosin VI in border cell migration seems to be to stabilize the β-catenin/cadherin complex.
14. Hicks J.L., Deng W.M., Rogat A.D., Miller K.G., Bownes M. Class VI unconventional myosin is required for spermatogenesis in Drosophila. Mol Biol Cell. 10:1999;4341-4353
15. Noguchi T., Miller K.G. A role for actin dynamics in individualization during spermatogenesis in Drosophila melanogaster. Development. 130:2003;1805-1816
16. Rogat A.D., Miller K.G. A role for myosin VI in actin dynamics at sites of membrane remodeling during Drosophila spermatogenesis. J Cell Sci. 115:2002;4855-4865 Myosin VI is at the fronts of actin cones that travel down sperm axonemes during individualization. This paper shows that Arp2/3 complex, cortactin and capping protein are also localized to this region. Loss of myosin VI leads to delocalization of these actin-regulating proteins.
17. Avraham K.B., Hasson T., Steel K.P., Kingsley D.M., Russell L.B., Mooseker M.S., Copeland N.G., Jenkins N.A. The mouse Snell's waltzer deafness gene encodes an unconventional myosin required for structural integrity of inner ear hair cells. Nat Genet. 11:1995;369-375
18. Self T., Sobe T., Copeland N.G., Jenkins N.A., Avraham K.B., Steel K.P. Role of myosin VI in the differentiation of cochlear hair cells. Dev Biol. 214:1999;331-341
19. Hasson T., Gillespie P.G., Garcia J.A., MacDonald R.B., Zhao Y., Yee A.G., Mooseker M.S., Corey D.P. Unconventional myosins in inner-ear sensory epithelia. J Cell Biol. 137:1997;1287-1307
20. Kelleher J.F., Mandell M.A., Moulder G., Hill K.L., L'Hernault S.W., Barstead R., Titus M.A. Myosin VI is required for asymmetric segregation of cellular components during C. elegans spermatogenesis. Curr Biol. 10:2000;1489-1496
21. Mermall V., McNally J.G., Miller K.G. Transport of cytoplasmic particles catalysed by an unconventional myosin in living Drosophila embryos. Nature. 369:1994;560-562
22. Mermall V., Miller K.G. The 95F unconventional myosin is required for proper organization of the Drosophila syncytial blastoderm. J Cell Biol. 129:1995;1575-1588
23. Buss F., Kendrick-Jones J., Lionne C., Knight A.E., Cote G.P., Paul Luzio J. The localization of myosin VI at the golgi complex and leading edge of fibroblasts and its phosphorylation and recruitment into membrane ruffles of A431 cells after growth factor stimulation. J Cell Biol. 143:1998;1535-1545
24. Warner C.L., Stewart A., Luzio J.P., Steel K.P., Libby R.T., Kendrick-Jones J., Buss F. Loss of myosin VI reduces secretion and the size of the Golgi in fibroblasts from Snell's waltzer mice. EMBO J. 22:2003;569-579 This paper demonstrates that myosin VI is a peripheral Golgi protein in normal rat kidney cells. The authors then use fibroblasts derived from myosin-VI-mutant mice to show that loss of this motor results in smaller Golgi and reduced secretion; these phenotypes are rescued by expression of full-length myosin VI.
25. Biemesderfer D., Mentone S.A., Mooseker M., Hasson T. Expression of myosin VI within the early endocytic pathway in adult and developing proximal tubules. Am J Physiol Renal Physiol. 282:2002;F785-F794 Localization of myosin VI to the endocytic region at the base of the microvilli in renal tubules is demonstrated in this study.
26. Heintzelman M.B., Hasson T., Mooseker M.S. Multiple unconventional myosin domains of the intestinal brush border cytoskeleton. J Cell Sci. 107:1994;3535-3543
27. Inoue A., Sato O., Homma K., Ikebe M. DOC-2/DAB2 is the binding partner of myosin VI. Biochem Biophys Res Commun. 292:2002;300-307
28. Morris S.M., Arden S.D., Roberts R.C., Kendrick-Jones J., Cooper J.A., Luzio J.P., Buss F. Myosin VI binds to and Localises with Dab2, potentially linking receptor-mediated endocytosis and the actin cytoskeleton. Traffic. 3:2002;331-341 In this paper and [27], the endocytic protein, Dab2, is identified an a binding partner for myosin VI.
29. Aschenbrenner L., Lee T., Hasson T. Myo6 facilitates the translocation of endocytic vesicles from cell peripheries. Mol Biol Cell. 14:2003;2728-2743 Employing fast pulse-chase experiments, these authors demonstrate that myosin VI is on endocytic vesicles immediately after clathrin uncoating and just before fusion with the endosome. Furthermore, expression of a dominant-negative form of myosin VI stalls vesicles in this state and delays transferrin uptake. These results indicate that myosin VI is required transiently (for <1 min) for efficient transit of vesicles to the early endosome.
30. Hasson T., Mooseker M.S. Porcine myosin-VI: characterization of a new mammalian unconventional myosin. J Cell Biol. 127:1994;425-440
31. Merrifield C.J., Moss S.E., Ballestrem C., Imhof B.A., Giese G., Wunderlich I., Almers W. Endocytic vesicles move at the tips of actin tails in cultured mast cells. Nat Cell Biol. 1:1999;72-74
32. Kaksonen M., Sun Y., Drubin D.G. A pathway for association of receptors, adaptors and actin during endocytic internalization. Cell. 115:2003;475-487
33. Merrifield C.J., Feldman M.E., Wan L., Almers W. Imaging actin and dynamin recruitment during invagination of single clathrin-coated pits. Nat Cell Biol. 4:2002;691-698