Identification and characterization of multiple novel Rab-myosin Va interactions

Molecular Biology of the Cell

Volumn 24, Issue 21, 2013, Pages 3420-3434

  Lindsay, Andrew J ^a,b   Jollivet, Florence ^b   Horgan, Conor P ^a   Khan, Amir R ^a   Raposo, Graça ^b   McCaffrey, Mary W ^b,c   Goud, Bruno ^b  

^a Biochemistry Department   (Ireland)

^b INSTITUT CURIE   (France)

^c TRINITY COLLEGE DUBLIN   (Ireland)

Author keywords

[No Author keywords available]

Indexed keywords

MYOSIN VA; RAB PROTEIN;

ARTICLE; CONTROLLED STUDY; ENDOSOME; FEMALE; GOLGI COMPLEX; HUMAN; HUMAN CELL; INTRACELLULAR MEMBRANE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; TWO HYBRID SYSTEM;

BINDING SITES; BLOTTING, WESTERN; CELL LINE, TUMOR; ENDOSOMES; GOLGI APPARATUS; GREEN FLUORESCENT PROTEINS; HELA CELLS; HUMANS; MICROSCOPY, CONFOCAL; MICROSCOPY, FLUORESCENCE; MODELS, BIOLOGICAL; MUTATION; MYOSIN HEAVY CHAINS; MYOSIN TYPE V; PROTEIN BINDING; RAB GTP-BINDING PROTEINS; RNA INTERFERENCE; TIME-LAPSE IMAGING; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84887069906     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E13-05-0236     Document Type: Article

References (55)

1. Chen W, Feng Y, Chen D., Wandinger-Ness A (1998). Rab11 is required for trans-Golgi network-to-plasma membrane transport and a preferential target for GDP dissociation inhibitor. Mol Biol Cell 9, 3241-3257. (Pubitemid 28516634)
2. Darchen F, Goud B. (2000). Multiple aspects of Rab protein action in the secretory pathway: focus on Rab3 and Rab6. Biochimie 82, 375-384. (Pubitemid 30391915)
3. Delevoye C et al. (2009). AP-1 and KIF13A coordinate endosomal sorting and positioning during melanosome biogenesis. J Cell Biol 187, 247-264.
4. Desnos C et al. (2003). Rab27A and its effector MyRIP link secretory granules to F-actin and control their motion towards release sites. J Cell Biol 163, 559-570. (Pubitemid 37429869)
5. English AR, Voeltz G.K. (2013). Rab10 GTPase regulates ER dynamics and morphology. Nat Cell Biol 15, 169-178.
6. Estrada P, Kim J, Coleman J., Walker L, Dunn B, Takizawa P., Novick P, Ferro-Novick S (2003). Myo4p and She3p are required for cortical ER inheritance in Saccharomyces cerevisiae. J. Cell Biol. 163, 1255-1266. (Pubitemid 38032087)
7. Fukuda M, Kuroda TS, Mikoshiba K. (2002). Slac2-a/melanophilin, the missing link between Rab27 and myosin Va: implications of a tripartite protein complex for melanosome transport. J Biol Chem 277, 12432-12436. (Pubitemid 34952817)
8. Giannandrea M et al. (2010). Mutations in the small GTPase gene RAB39B are responsible for X-linked mental retardation associated with autism, epilepsy, and macrocephaly. Am J Hum Genet 86, 185-195.
9. Grigoriev I et al. (2011). Rab6, Rab8, and MICAL3 cooperate in controlling docking and fusion of exocytotic carriers Rab6 regulates transport and targeting of exocytotic carriers. Curr Biol 21, 967-974.
10. Hammer JA 3rd, Sellers JR (2011). Walking to work: roles for class V myosins as cargo transporters. Nat Rev Mol Cell Biol 13, 13-26.
11. Huang JD, Mermall V, Strobel M.C., Russell LB, Mooseker MS, Copeland NG, Jenkins N.A. (1998). Molecular genetic dissection of mouse unconventional myosin-VA: tail region mutations. Genetics 148, 1963-1972. (Pubitemid 28180720)
12. Hume AN, Collinson LM, Hopkins C.R., Strom M., Barral DC, Bossi G, Grififiths GM, Seabra M.C. (2002). The leaden gene product is required with Rab27a to recruit myosin Va to melanosomes in melanocytes. Traffic 3, 193-202. (Pubitemid 34555477)
13. Hutagalung AH, Novick P.J. (2011). Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev 91, 119-149.
14. Janoueix-Lerosey I., Jollivet F, Camonis J., Marche PN, Goud B. (1995). Two-hybrid system screen with the small GTP-binding protein Rab6. Identification of a novel mouse GDP dissociation inhibitor isoform and two other potential partners of Rab6. J Biol Chem 270, 14801-14808.
15. Jin Y, Sultana A, Gandhi P., Franklin E, Hamamoto S, Khan A.R., Munson M., Schekman R, Weisman L.S. (2011). Myosin V transports secretory vesicles via a Rab GTPase cascade and interaction with the exocyst complex. Dev Cell 21, 1156-1170.
16. Junutula JR, De Maziere AM, Peden AA, Ervin KE, Advani RJ, van Dijk SM, Klumperman J, Scheller R.H. (2004). Rab14 is involved in membrane trafficking between the Golgi complex and endosomes. Mol Biol Cell 15, 2218-2229. (Pubitemid 38580640)
17. Kelly EE, Horgan C P, Adams C, Patzer T.M., Ní Shúilleabháin DM, Norman JC, McCaffrey MW (2009). Class I Rab11-family interacting proteins are binding targets for the Rab14 GTPase. Biol Cell 102, 51-62.
18. Kelly EE, Horgan C P, Goud B, McCaffrey M.W. (2012). The Rab family of proteins: 25 years on. Biochem Soc Trans 40, 1337-1347.
19. Kogel T, Gerdes H.H. (2010). Roles of myosin Va and Rab3D in membrane remodeling of immature secretory granules. Cell Mol Neurobiol 30, 1303-1308.
20. Kogel T, Rudolf R, Hodneland E., Hellwig A, Kuznetsov SA, Seiler F, Sollner T.H., Barroso J., Gerdes H.H. (2010). Distinct roles of myosin Va in membrane remodeling and exocytosis of secretory granules. Traffic 11, 637-650.
21. Lambert J, Naeyaert JM, Callens T, De Paepe A, Messiaen L. (1998). Human myosin V gene produces different transcripts in a cell type-specific manner. Biochem Biophys Res Commun 252, 329-333. (Pubitemid 28542886)
22. Larance M et al. (2005). Characterization of the role of the Rab GTPase-activating protein AS160 in insulin-regulated GLUT4 trafficking. J Biol Chem 280, 37803-37813. (Pubitemid 41642391)
23. Li XD, Jung HS, Mabuchi K, Craig R., Ikebe M. (2006). The globular tail domain of myosin Va functions as an inhibitor of the myosin Va motor. J Biol Chem 281, 21789-21798. (Pubitemid 44181883)
24. Li XD, Jung HS, Wang Q, Ikebe R., Craig R, Ikebe M. (2008). The globular tail domain puts on the brake to stop the ATPase cycle of myosin Va. Proc Natl Acad Sci USA 105, 1140-1145. (Pubitemid 351397020)
25. Linford A, Yoshimura S, Nunes Bastos R, Langemeyer L, Gerondopoulos A., Rigden DJ, Barr F.A. (2012). Rab14 and its exchange factor FAM116 link endocytic recycling and adherens junction stability in migrating cells. Dev Cell 22, 952-966.
26. Lipatova Z, Tokarev AA, Jin Y, Mulholland J., Weisman LS, Segev N. (2008). Direct interaction between a myosin V motor and the Rab GTPases Ypt31/32 is required for polarized secretion. Mol Biol Cell 19, 4177-4187.
27. Liu J, Taylor DW, Krementsova E.B., Trybus KM, Taylor K.A. (2006). Three-dimensional structure of the myosin V inhibited state by cryoelectron tomography. Nature 442, 208-211. (Pubitemid 44086568)
28. Mercer JA, Seperack PK, Strobel M.C., Copeland NG, Jenkins N.A. (1991). Novel myosin heavy chain encoded by murine dilute coat colour locus. Nature 349, 709-713. (Pubitemid 21912144)
29. Miserey-Lenkei S et al. (2007). Rab6-interacting protein 1 links Rab6 and Rab11 function. Traffic 8, 1385-1403. (Pubitemid 47394243)
30. Miserey-Lenkei S., Chalancon G, Bardin S., Formstecher E, Goud B, Echard A. (2010). Rab and actomyosin-dependent fission of transport vesicles at the Golgi complex. Nat Cell Biol 12, 645-654.
31. Morel E, Parton RG, Gruenberg J. (2009). Annexin A2-dependent polymerization of actin mediates endosome biogenesis. Dev Cell 16, 445-457.
32. Nagashima K, Torii S, Yi Z., Igarashi M, Okamoto K, Takeuchi T., Izumi T. (2002). Melanophilin directly links Rab27a and myosin Va through its distinct coiled-coil regions. FEBS Lett 517, 233-238. (Pubitemid 34327666)
33. Ng EL, Wang Y, Tang B.L. (2007). Rab22B's role in trans-Golgi network membrane dynamics. Biochem Biophys Res Commun 361, 751-757. (Pubitemid 47238034)
34. Nizak C, Monier S, del Nery E, Moutel S, Goud B., Perez F. (2003). Recombinant antibodies to the small GTPase Rab6 as conformation sensors. Science 300, 984-987. (Pubitemid 36548886)
35. Pereira-Leal J.B., Seabra M.C. (2001). Evolution of the Rab family of small GTP-binding proteins. J Mol Biol 313, 889-901. (Pubitemid 33063434)
36. Poteryaev D, Datta S, Ackema K., Zerial M, Spang A. (2010). Identification of the switch in early-to-late endosome transition. Cell 141, 497-508.
37. Rahajeng J, Panapakkam Giridharan SS, Cai B, Naslavsky N, Caplan S. (2012). MICAL-L1 is a tubular endosomal membrane hub that connects Rab35 and Arf6 with Rab8a. Traffic 13, 82-93.
38. Rink J, Ghigo E, Kalaidzidis Y., Zerial M. (2005). Rab conversion as a mechanism of progression from early to late endosomes. Cell 122, 735-749. (Pubitemid 41242638)
39. Roland JT, Kenworthy AK, Peranen J, Caplan S., Goldenring J.R. (2007). Myosin Vb interacts with Rab8a on a tubular network containing EHD1 and EHD3. Mol Biol Cell 18, 2828-2837. (Pubitemid 47235291)
40. Roland JT, Lapierre LA, Goldenring J.R. (2009). Alternative splicing in class v myosins determines association with rab10. J Biol Chem 284, 1213-1223.
41. Rossi G, Brennwald P. (2011). Yeast homologues of lethal giant larvae and type V myosin cooperate in the regulation of Rab-dependent vesicle clustering and polarized exocytosis. Mol Biol Cell 22, 842-857.
42. Santiago-Tirado F.H., Legesse-Miller A, Schott D., Bretscher A. (2011). PI4P and Rab inputs collaborate in myosin-V-dependent transport of secretory compartments in yeast. Dev Cell 20, 47-59.
43. Seperack PK, Mercer JA, Strobel M.C., Copeland NG, Jenkins N.A. (1995). Retroviral sequences located within an intron of the dilute gene alter dilute expression in a tissue-specific manner. EMBO J 14, 2326-2332.
44. Stenmark H (2009). Rab GTPases as coordinators of vesicle traffic. Nat Rev Mol Cell Biol 10, 513-525.
45. Stenmark H, Parton RG, Steele-Mortimer O, Lutcke A., Gruenberg J, Zerial M. (1994). Inhibition of rab5 GTPase activity stimulates membrane fusion in endocytosis. EMBO J 13, 1287-1296. (Pubitemid 24090209)
46. Strom M, Hume AN, Tarafder A.K., Barkagianni E., Seabra M.C. (2002). A family of Rab27-binding proteins. Melanophilin links Rab27a and myosin Va function in melanosome transport. J Biol Chem 277, 25423-25430. (Pubitemid 34951855)
47. Thirumurugan K, Sakamoto T, Hammer JA 3rd, Sellers JR, Knight PJ (2006). The cargo-binding domain regulates structure and activity of myosin 5. Nature 442, 212-215. (Pubitemid 44086569)
48. Trybus KM, Gushchin MI, Lui H, Hazelwood L., Krementsova EB, Volkmann N, Hanein D. (2007). Effect of calcium on calmodulin bound to the IQ motifs of myosin V. J Biol Chem 282, 23316-23325. (Pubitemid 47311916)
49. Vale RD (2003). The molecular motor toolbox for intracellular transport. Cell 112, 467-480. (Pubitemid 36263080)
50. Wagner W, Brenowitz SD, Hammer JA 3rd (2011). Myosin-Va transports the endoplasmic reticulum into the dendritic spines of Purkinje neurons. Nat Cell Biol 13, 40-48.
51. Wollert T, Patel A, Lee Y.L., Provance DW Jr, Vought VE, Cosgrove MS, Mercer JA, Langford G.M. (2011). Myosin5a tail associates directly with Rab3A-containing compartments in neurons. J Biol Chem 286, 14352-14361.
52. Woolner S, Bement W.M. (2009). Unconventional myosins acting unconventionally. Trends Cell Biol 19, 245-252.
53. Wu X, Bowers B, Rao K., Wei Q, Hammer JA 3rd (1998). Visualization of melanosome dynamics within wild-type and dilute melanocytes suggests a paradigm for myosin V function In vivo. J Cell Biol 143, 1899-1918. (Pubitemid 29022612)
54. Wu X, Wang F, Rao K., Sellers JR, Hammer JA 3rd (2002a). Rab27a is an essential component of melanosome receptor for myosin Va. Mol Biol Cell 13, 1735-1749. (Pubitemid 34522652)
55. Wu XS, Rao K, Zhang H., Wang F, Sellers JR, Matesic L.E., Copeland NG, Jenkins NA, Hammer JA 3rd (2002b). Identification of an organelle receptor for myosin-Va. Nat Cell Biol 4, 271-278. (Pubitemid 34308852)