Structural basis of myosin v Rab GTPase-dependent cargo recognition

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 51, 2013, Pages 20443-20448

  Pylypenko, Olena ^a,b   Attanda, Wikayatou ^a,b   Gauquelin, Charles ^a,b   Lahmani, Marion ^a,b   Coulibaly, Doudouh ^a,b   Baron, Bruno ^b,c   Hoos, Sylviane ^b,c   Titus, Margaret A ^d   England, Patrick ^b,c   Houdusse, Anne M ^a,b  

^a INSTITUT CURIE   (France)

^b CNRS   (France)

^c INSTITUT PASTEUR   (France)

^d UNIVERSITY OF MINNESOTA   (United States)

Author keywords

DIL motif; GTPases; Intracellular traffic; Rab effector

Indexed keywords

MOLECULAR MOTOR; MYOSIN V; MYOSIN VA; RAB PROTEIN;

ARTICLE; CELL FUNCTION; CRYSTAL STRUCTURE; CYTOSKELETON; MELANOSOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN STRUCTURE;

EID: 84890825644     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1314329110     Document Type: Article

References (40)

1. Richards TA, Cavalier-Smith T (2005) Myosin domain evolution and the primary divergence of eukaryotes. Nature 436(7054):1113-1118.
2. Liu J, Taylor DW, Krementsova EB, Trybus KM, Taylor KA (2006) Three-Dimensional structure of the myosin V inhibited state by cryoelectron tomography. Nature 442(7099):208-211.
3. Thirumurugan K, Sakamoto T, Hammer JA, 3rd, Sellers JR, Knight PJ (2006) The cargobinding domain regulates structure and activity of myosin Nature 442(7099): 212-215.
4. Hammer JA, Sellers JR (2012) Walking to work: Roles for class V myosins as cargo transporters. Nat Rev Mol Cell Biol 13(1):13-26.
5. Seperack PK, Mercer JA, Strobel MC, Copeland NG, Jenkins NA (1995) Retroviral sequences located within an intron of the dilute gene alter dilute expression in a tissuespecific manner. EMBO J 14(10):2326-2332.
6. Roland JT, Lapierre LA, Goldenring JR (2009) Alternative splicing in class V myosins determines association with Rab10. J Biol Chem 284(2):1213-1223.
7. Pastural E, et al. (1997) Griscelli disease maps to chromosome 15q21 and is associated with mutations in the myosin-Va gene. Nat Genet 16(3):289-292.
8. Ruemmele FM, et al. (2010) Loss-Of-Function of MYO5B is the main cause of microvillus inclusion disease: 15 novel mutations and a CaCo-2 RNAi cell model. Hum Mutat 31(5):544-551.
9. Roland JT, et al. (2011) Rab GTPase-Myo5B complexes control membrane recycling and epithelial polarization. Proc Natl Acad Sci USA 108(7):2789-2794.
10. Hutagalung AH, Novick PJ (2011) Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev 91(1):119-149.
11. 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(14):12432-12436.
12. Hales CM, Vaerman J-P, Goldenring JR (2002) Rab11 family interacting protein 2 associates with Myosin Vb and regulates plasma membrane recycling. J Biol Chem 277(52):50415-50421.
13. Jin Y, et al. (2011) Myosin V transports secretory vesicles via a Rab GTPase cascade and interaction with the exocyst complex. Dev Cell 21(6):1156-1170.
14. Li BX, Satoh AK, Ready DF (2007) Myosin V, Rab11, and dRip11 direct apical secretion and cellular morphogenesis in developing Drosophila photoreceptors. J Cell Biol 177(4):659-669.
15. Wei Z, Liu X, Yu C, Zhang M (2013) Structural basis of cargo recognitions for class V myosins. Proc Natl Acad Sci USA 110(28):11314-11319.
16. Matsui T, Ohbayashi N, Fukuda M (2012) The Rab interacting lysosomal protein (RILP) homology domain functions as a novel effector domain for small GTPase Rab36: Rab36 regulates retrograde melanosome transport in melanocytes. J Biol Chem 287(34):28619-28631.
17. Pashkova N, Jin Y, Ramaswamy S, Weisman LS (2006) Structural basis for myosin V discrimination between distinct cargoes. EMBO J 25(4):693-700.
18. Heuck A, et al. (2010) The structure of the Myo4p globular tail and its function in ASH1 mRNA localization. J Cell Biol 189(3):497-510.
19. Karcher RL, et al. (2001) Cell cycle regulation of myosin-V by calcium/calmodulindependent protein kinase II. Science 293(5533):1317-1320.
20. Yoshizaki T, et al. (2007) Myosin 5a is an insulin-Stimulated Akt2 (protein kinase Bbeta) substrate modulating GLUT4 vesicle translocation. Mol Cell Biol 27(14): 5172-5183.
21. Li X-D, et al. (2008) The globular tail domain puts on the brake to stop the ATPase cycle of myosin Va. Proc Natl Acad Sci USA 105(4):1140-1145.
22. Lipatova Z, et al. (2008) Direct interaction between a myosin V motor and the Rab GTPases Ypt31/32 is required for polarized secretion. Mol Biol Cell 19(10):4177-4187.
23. Lee M-TG, Mishra A, Lambright DG (2009) Structural mechanisms for regulation of membrane traffic by rab GTPases. Traffic 10(10):1377-1389.
24. Merithew E, et al. (2001) Structural plasticity of an invariant hydrophobic triad in the switch regions of Rab GTPases is a determinant of effector recognition. J Biol Chem 276(17):13982-13988.
25. Eathiraj S, Mishra A, Prekeris R, Lambright DG (2006) Structural basis for Rab11-Mediated recruitment of FIP3 to recycling endosomes. J Mol Biol 364(2):121-135.
26. Kelly EE, et al. (2010) Class I Rab11-Family interacting proteins are binding targets for the Rab14 GTPase. Biol Cell 102(1):51-62.
27. Mishra A, Eathiraj S, Corvera S, Lambright DG (2010) Structural basis for Rab GTPase recognition and endosome tethering by the C2H2 zinc finger of Early Endosomal Autoantigen 1 (EEA1). Proc Natl Acad Sci USA 107(24):10866-10871.
28. Wang Z, et al. (2008) Myosin Vb mobilizes recycling endosomes and AMPA receptors for postsynaptic plasticity. Cell 135(3):535-548.
29. Lindsay AJ, McCaffrey MW (2004) The C2 domains of the class I Rab11 family of interacting proteins target recycling vesicles to the plasma membrane. J Cell Sci 117(Pt 19): 4365-4375.
30. Wu X, Sakamoto T, Zhang F, Sellers JR, Hammer JA, 3rd (2006) In vitro reconstitution of a transport complex containing Rab27a, melanophilin and myosin Va. FEBS Lett 580(25):5863-5868.
31. Wasmeier C, Hume AN, Bolasco G, Seabra MC (2008) Melanosomes at a glance. J Cell Sci 121(Pt 24):3995-3999.
32. Fukuda M, Kuroda TS (2004) Missense mutations in the globular tail of myosin-Va in dilute mice partially impair binding of Slac2-A/melanophilin. J Cell Sci 117(Pt 4): 583-591.
33. Geething NC, Spudich JA (2007) Identification of a minimal myosin Va binding site within an intrinsically unstructured domain of melanophilin. J Biol Chem 282(29): 21518-21528.
34. Wu XS, et al. (2002) Identification of an organelle receptor for myosin-Va. Nat Cell Biol 4(4):271-278.
35. Mercer JA, Seperack PK, Strobel MC, Copeland NG, Jenkins NA (1991) Novel myosin heavy chain encoded by murine dilute coat colour locus. Nature 349(6311):709-713.
36. Huang JD, et al. (1998) Molecular genetic dissection of mouse unconventional myosin-VA: Tail region mutations. Genetics 148(4):1963-1972.
37. Lanzarotti E, Biekofsky RR, Estrin DA, Marti MA, Turjanski AG (2011) Aromatic-Aromatic interactions in proteins: Beyond the dimer. J Chem Inf Model 51(7):1623-1633.
38. Li X-D, Ikebe R, Ikebe M (2005) Activation of myosin Va function by melanophilin, a specific docking partner of myosin Va. J Biol Chem 280(18):17815-17822.
39. Sellers JR, Thirumurugan K, Sakamoto T, Hammer JA, 3rd, Knight PJ (2008) Calcium and cargoes as regulators of myosin 5a activity. Biochem Biophys Res Commun 369(1): 176-181.
40. Sckolnick M, Krementsova EB, Warshaw DM, Trybus KM (2013) More than just a cargo adapter, melanophilin prolongs and slows processive runs of Myosin va. J Biol Chem 288(41):29313-29322.