Dynamic exchange of myosin VI on endocytic structures

Journal of Biological Chemistry

Volumn 287, Issue 46, 2012, Pages 38646-68646

  Bond, Lisa M ^a,b   Arden, Susan D ^b   Kendrick Jones, John ^c   Buss, Folma ^b   Sellers, James R ^a  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN-BASED MOLECULAR MOTORS; ENDOSOMES; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; ISOFORMS; MYOSIN VI; TURNOVER RATE; WILD TYPES;

DIMERS; MOLECULAR BIOLOGY; PHOTOBLEACHING;

PROTEINS;

CLATHRIN; DIMER; MONOMER; MYOSIN IV; GREEN FLUORESCENT PROTEIN; ISOPROTEIN; MYOSIN; MYOSIN HEAVY CHAIN; MYOSIN VI;

ANIMAL CELL; ARTICLE; CELL STRUCTURE; CONTROLLED STUDY; ENDOCYTOSIS; ENDOSOME; FEMALE; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN METABOLISM; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; SIGNAL TRANSDUCTION; WILD TYPE; ANIMAL; BIOLOGICAL MODEL; BLEACHING; CHEMISTRY; CHO CELL; DIMERIZATION; HAMSTER; HELA CELL; HUMAN; METABOLISM; TWO HYBRID SYSTEM;

ANIMALS; CHO CELLS; CLATHRIN; CRICETINAE; DIMERIZATION; ENDOCYTOSIS; ENDOSOMES; GREEN FLUORESCENT PROTEINS; HELA CELLS; HUMANS; MODELS, BIOLOGICAL; MYOSIN HEAVY CHAINS; MYOSINS; PHOTOBLEACHING; PROTEIN ISOFORMS; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84869070327     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.373969     Document Type: Article

References (48)

1. Wells, A. L., Lin, A. W., Chen, L. Q., Safer, D., Cain, S. M., Hasson, T., Carragher, B. O., Milligan, R. A., and Sweeney, H. L. (1999) Myosin VI is an actin-based motor that moves backwards. Nature 401, 505-508
2. Park, H., Li, A., Chen, L. Q., Houdusse, A., Selvin, P. R., and Sweeney, H. L. (2007) The unique insert at the end of the myosin VI motor is the sole determinant of directionality. Proc. Natl. Acad. Sci. U.S.A. 104, 778-783 (Pubitemid 46154687)
3. Warner, C. L., Stewart, A., Luzio, J. P., Steel, K. P., Libby, R. T., Kendrick-Jones, J., and Buss, F. (2003) Loss of myosin VI reduces secretion and the size of the Golgi in fibroblasts from Snell's waltzer mice. EMBO J. 22, 569-579 (Pubitemid 36193601)
4. Chibalina, M. V., Poliakov, A., Kendrick-Jones, J., and Buss, F. (2010) Myosin VI and optineurin are required for polarized EGFR delivery and directed migration. Traffic 11, 1290-1303
5. Au, J. S., Puri, C., Ihrke, G., Kendrick-Jones, J., and Buss, F. (2007) Myosin VI is required for sorting of AP-1B-dependent cargo to the basolateral domain in polarized MDCK cells. J. Cell Biol. 177, 103-114 (Pubitemid 46588405)
6. Bond, L. M., Peden, A. A., Kendrick-Jones, J., Sellers, J. R., and Buss, F. (2011) Myosin VI and its binding partner optineurin are involved in secretory vesicle fusion at the plasma membrane. Mol. Biol. Cell 22, 54-65
7. Buss, F., Arden, S. D., Lindsay, M., Luzio, J. P., and Kendrick-Jones, J. (2001) Myosin VI isoform localized to clathrin-coated vesicles with a role in clathrin-mediated endocytosis. EMBO J. 20, 3676-3684 (Pubitemid 32691779)
8. Taylor, M. J., Perrais, D., and Merrifield, C. J. (2011) A high precision survey of the molecular dynamics of mammalian clathrin-mediated endocytosis. PLoS Biol. 9, e1000604
9. Ameen, N., and Apodaca, G. (2007) Defective CFTR apical endocytosis and enterocyte brush border in myosin VI-deficient mice. Traffic 8, 998-1006 (Pubitemid 47074034)
10. Osterweil, E., Wells, D. G., and Mooseker, M. S. (2005) A role for myosin VI in postsynaptic structure and glutamate receptor endocytosis. J. Cell Biol. 168, 329-338 (Pubitemid 40248229)
11. Aschenbrenner, L., Lee, T., and Hasson, T. (2003) Myo6 facilitates the translocation of endocytic vesicles from cell peripheries. Mol. Biol. Cell 14, 2728-2743 (Pubitemid 36871517)
12. Inoue, T., Kon, T., Ohkura, R., Yamakawa, H., Ohara, O., Yokota, J., and Sutoh, K. (2008) BREK/LMTK2 is a myosin VI-binding protein involved in endosomal membrane trafficking. Genes Cells 13, 483-495 (Pubitemid 351567049)
13. Chibalina, M. V., Seaman, M. N., Miller, C. C., Kendrick-Jones, J., and Buss, F. (2007) Myosin VI and its interacting protein LMTK2 regulate tubule formation and transport to the endocytic recycling compartment. J. Cell Sci. 120, 4278-4288
14. Yoshida, H., Cheng, W., Hung, J., Montell, D., Geisbrecht, E., Rosen, D., Liu, J., and Naora, H. (2004) Lessons from border cell migration in the Drosophila ovary: a role for myosin VI in dissemination of human ovarian cancer. Proc. Natl. Acad. Sci. U.S.A. 101, 8144-8149 (Pubitemid 38698068)
15. Dunn, T. A., Chen, S., Faith, D. A., Hicks, J. L., Platz, E. A., Chen, Y., Ewing, C. M., Sauvageot, J., Isaacs, W. B., De Marzo, A. M., and Luo, J. (2006) A novel role of myosin VI in human prostate cancer. Am. J. Pathol. 169, 1843-1854 (Pubitemid 351182013)
16. Mohiddin, S. A., Ahmed, Z. M., Griffith, A. J., Tripodi, D., Friedman, T. B., Fananapazir, L., and Morell, R. J. (2004) Novel association of hypertrophic cardiomyopathy, sensorineural deafness, and a mutation in unconventional myosin VI (MYO6). J. Med. Genet. 41, 309-314 (Pubitemid 38496779)
17. Melchionda, S., Ahituv, N., Bisceglia, L., Sobe, T., Glaser, F., Rabionet, R., Arbones, M. L., Notarangelo, A., Di Iorio, E., Carella, M., Zelante, L., Estivill, X., Avraham, K. B., and Gasparini, P. (2001) MYO6, the human homologue of the gene responsible for deafness in Snell's waltzer mice, is mutated in autosomal dominant nonsyndromic hearing loss. Am. J. Hum. Genet. 69, 635-640 (Pubitemid 32777701)
18. Ahmed, Z. M., Morell, R. J., Riazuddin, S., Gropman, A., Shaukat, S., Ahmad, M. M., Mohiddin, S. A., Fananapazir, L., Caruso, R. C., Husnain, T., Khan, S. N., Riazuddin, S., Griffith, A. J., Friedman, T. B., and Wilcox, E. R. (2003) Mutations of MYO6 are associated with recessive deafness, DFNB37. Am. J. Hum. Genet. 72, 1315-1322 (Pubitemid 36530020)
19. Avraham, K. B., Hasson, T., Steel, K. P., Kingsley, D. M., Russell, L. B., Mooseker, M. S., Copeland, N. G., and Jenkins, N. A. (1995) The mouse Snell's waltzer deafness gene encodes an unconventional myosin required for structural integrity of inner ear hair cells. Nat. Genet. 11, 369-375
20. Knudsen, B. (2006) Migrating with myosin VI. Am. J. Pathol. 169, 1523-1526
21. Buss, F., Luzio, J. P., and Kendrick-Jones, J. (2001) Myosin VI, a new force in clathrin mediated endocytosis. FEBS Lett. 508, 295-299 (Pubitemid 33135457)
22. Hasson, T. (2003) Myosin VI: two distinct roles in endocytosis. J. Cell Sci. 116, 3453-3461
23. Rock, R. S., Ramamurthy, B., Dunn, A. R., Beccafico, S., Rami, B. R., Morris, C., Spink, B. J., Franzini-Armstrong, C., Spudich, J. A., and Sweeney, H. L. (2005)Aflexible domain is essential for the large step size and processivity of myosin VI. Mol. Cell 17, 603-609 (Pubitemid 40269124)
24. Lister, I., Schmitz, S., Walker, M., Trinick, J., Buss, F., Veigel, C., and Kendrick-Jones, J. (2004) A monomeric myosin VI with a large working stroke. EMBO J. 23, 1729-1738 (Pubitemid 38649636)
25. Umeki, N., Jung, H. S., Watanabe, S., Sakai, T., Li, X. D., Ikebe, R., Craig, R., and Ikebe, M. (2009) The tail binds to the head-neck domain, inhibiting ATPase activity of myosin VIIA. Proc. Natl. Acad. Sci. U.S.A. 106, 8483-8488
26. Yang, Y., Baboolal, T. G., Siththanandan, V., Chen, M., Walker, M. L., Knight, P. J., Peckham, M., and Sellers, J. R. (2009) A FERM domain autoregulates Drosophila myosin 7a activity. Proc. Natl. Acad. Sci. U.S.A. 106, 4189-4194
27. Buss, F., Spudich, G., and Kendrick-Jones, J. (2004) Myosin VI: cellular functions and motor properties. Annu. Rev. Cell Dev. Biol. 20, 649-676 (Pubitemid 39488653)
28. Spink, B. J., Sivaramakrishnan, S., Lipfert, J., Doniach, S., and Spudich, J. A. (2008) Long single α-helical tail domains bridge the gap between structure and function of myosin VI. Nat. Struct. Mol. Biol. 15, 591-597 (Pubitemid 351799136)
29. Trybus, K. M., Freyzon, Y., Faust, L. Z., and Sweeney, H. L. (1997) Spare the rod, spoil the regulation: necessity for a myosin rod. Proc. Natl. Acad. Sci. U.S.A. 94, 48-52 (Pubitemid 27027162)
30. Rock, R. S., Rice, S. E., Wells, A. L., Purcell, T. J., Spudich, J. A., and Sweeney, H. L. (2001) Myosin VI is a processive motor with a large step size. Proc. Natl. Acad. Sci. U.S.A. 98, 13655-13659 (Pubitemid 33115953)
31. Yeh, E., Haase, J., Paliulis, L. V., Joglekar, A., Bond, L., Bouck, D., Salmon, E. D., and Bloom, K. S. (2008) Pericentric chromatin is organized into an intramolecular loop in mitosis. Curr. Biol. 18, 81-90
32. Spudich, G., Chibalina, M. V., Au, J. S., Arden, S. D., Buss, F., and Kendrick-Jones, J. (2007) Myosin VI targeting to clathrin-coated structures and dimerization is mediated by binding to Disabled-2 and PtdIns(4,5)P2. Nat. Cell Biol. 9, 176-183 (Pubitemid 46420860)
33. Morris, S. M., Arden, S. D., Roberts, R. C., Kendrick-Jones, J., Cooper, J. A., Luzio, J. P., and Buss, F. (2002) Myosin VI binds to and localises with Dab2, potentially linking receptor-mediated endocytosis and the actin cytoskeleton. Traffic 3, 331-341 (Pubitemid 34461043)
34. Kirchhausen, T. (2000) Clathrin. Annu. Rev. Biochem. 69, 699-727
35. Nishikawa, S., Homma, K., Komori, Y., Iwaki, M., Wazawa, T., Hikikoshi Iwane, A., Saito, J., Ikebe, R., Katayama, E., Yanagida, T., and Ikebe, M. (2002) Class VI myosin moves processively along actin filaments backward with large steps. Biochem. Biophys. Res. Commun. 290, 311-317 (Pubitemid 34694501)
36. Okten, Z., Churchman, L. S., Rock, R. S., and Spudich, J. A. (2004) Myosin VI walks hand-over-hand along actin. Nat. Struct. Mol. Biol. 11, 884-887 (Pubitemid 39128806)
37. Wu, X., Zhao, X., Baylor, L., Kaushal, S., Eisenberg, E., and Greene, L. E. (2001) Clathrin exchange during clathrin-mediated endocytosis. J. Cell Biol. 155, 291-300 (Pubitemid 34289304)
38. Murthy, K., and Wadsworth, P. (2005) Myosin-II-dependent localization and dynamics of F-actin during cytokinesis. Curr. Biol. 15, 724-731 (Pubitemid 40599926)
39. Saffarian, S., Cocucci, E., and Kirchhausen, T. (2009) Distinct dynamics of endocytic clathrin-coated pits and coated plaques. PLoS Biol. 7, e1000191
40. Massol, R. H., Boll, W., Griffin, A. M., and Kirchhausen, T. (2006) A burst of auxilin recruitment determines the onset of clathrin-coated vesicle uncoating. Proc. Natl. Acad. Sci. U.S.A. 103, 10265-10270 (Pubitemid 44051155)
41. Ehrlich, M., Boll, W., Van Oijen, A., Hariharan, R., Chandran, K., Nibert, M. L., and Kirchhausen, T. (2004) Endocytosis by random initiation and stabilization of clathrin-coated pits. Cell 118, 591-605 (Pubitemid 39179712)
42. Biemesderfer, D., Mentone, S. A., Mooseker, M., and Hasson, T. (2002) Expression of myosin VI within the early endocytic pathway in adult and developing proximal tubules. Am. J. Physiol. Renal Physiol. 282, F785-794 (Pubitemid 34654483)
43. Kondo, T., Hamao, K., Kamijo, K., Kimura, H., Morita, M., Takahashi, M., and Hosoya, H. (2011) Enhancement of myosin II/actin turnover at the contractile ring induces slower furrowing in dividing HeLa cells. Biochem. J. 435, 569-576
44. Park, H., Ramamurthy, B., Travaglia, M., Safer, D., Chen, L. Q., Franzini- Armstrong, C., Selvin, P. R., and Sweeney, H. L. (2006) Full-length myosin VI dimerizes and moves processively along actin filaments upon monomer clustering. Mol. Cell 21, 331-336 (Pubitemid 43163528)
45. Yu, C., Feng, W., Wei, Z., Miyanoiri, Y., Wen, W., Zhao, Y., and Zhang, M. (2009) Myosin VI undergoes cargo-mediated dimerization. Cell 138, 537-548
46. Phichith, D., Travaglia, M., Yang, Z., Liu, X., Zong, A. B., Safer, D., and Sweeney, H. L. (2009) Cargo binding induces dimerization of myosin VI. Proc. Natl. Acad. Sci. U.S.A. 106, 17320-17324
47. Spudich, J. A., and Sivaramakrishnan, S. (2010) Myosin VI: an innovative motor that challenged the swinging lever arm hypothesis. Nat. Rev. Mol. Cell Biol. 11, 128-137
48. Buss, F., and Kendrick-Jones, J. (2008) How are the cellular functions of myosin VI regulated within the cell? Biochem. Biophys. Res. Commun. 369, 165-175