Molecular mechanism of Myosin Va recruitment to dense core secretory granules

Traffic

Volumn 13, Issue 1, 2012, Pages 54-69

  Brozzi, Flora ^a   Diraison, Frederique ^a   Lajus, Sophie ^a   Rajatileka, Shavanthi ^a   Philips, Thomas ^a   Regazzi, Romano ^b   Fukuda, Mitsunori ^c   Verkade, Paul ^d   Molnár, Elek ^e   Váradi, Anikó ^a  

^a UNIVERSITY OF THE WEST OF ENGLAND   (United Kingdom)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c TOHOKU UNIVERSITY   (Japan)

^d UNIVERSITY OF BRISTOL   (United Kingdom)

^e UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Dense core secretory granules; Granuphilin a b; Hormone secretion; Hormone and neuropeptide secreting cell; Myosin Va; Rab27; Rabphilin 3A; Tripartite complex

Indexed keywords

MYOSIN VA; NEUROPEPTIDE;

ARTICLE; CELL MEMBRANE; HORMONE RELEASE; NEUROSECRETORY CELL; NUCLEOTIDE SEQUENCE; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN PROTEIN INTERACTION; SECRETORY GRANULE;

ANIMALS; BRAIN; CELL MEMBRANE; HORMONES; INSULIN-SECRETING CELLS; INSULINOMA; MYOSIN HEAVY CHAINS; MYOSIN TYPE V; PANCREATIC NEOPLASMS; PC12 CELLS; PROTEIN BINDING; PROTEIN ISOFORMS; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; RATS; SECRETORY VESICLES; VESICULAR TRANSPORT PROTEINS;

EID: 83255167070     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/j.1600-0854.2011.01301.x     Document Type: Article

References (61)

1. Park JJ, Loh YP. How peptide hormone vesicles are transported to the secretion site for exocytosis. Mol Endocrinol 2008;22:2583-2595.
2. Rudolf R, Salm T, Rustom A, Gerdes HH. Dynamics of immature secretory granules: role of cytoskeletal elements during transport, cortical restriction, and F-actin-dependent tethering. Mol Biol Cell 2001;12:1353-1365.
3. Varadi A, Ainscow EK, Allan VJ, Rutter GA. Involvement of conventional kinesin in glucose-stimulated secretory granule movements and exocytosis in clonal pancreatic beta-cells. J Cell Sci 2002;115:4177-4189.
4. Steyer JA, Almers W. Tracking single secretory granules in live chromaffin cells by evanescent-field fluorescence microscopy. Biophys J 1999;76:2262-2271.
5. Rosé SD, Lejen T, Casaletti L, Larson RE, Pene TD, Trifaró JM. Myosins II and V in chromaffin cells: myosin V is a chromaffin vesicle molecular motor involved in secretion. J Neurochem 2003;85:287-298.
6. Rudolf R, Kögel T, Kuznetsov SA, Salm T, Schlicker O, Hellwig A, Hammer JA III, Gerdes HH. Myosin Va facilitates the distribution of secretory granules in the F-actin rich cortex of PC12cells. J Cell Sci 2003;116:1339-1348.
7. Varadi A, Tsuboi T, Rutter GA. Myosin Va transports dense core secretory vesicles in pancreatic MIN6 beta-cells. Mol Biol Cell 2005;16:2670-2680.
8. Desnos C, Schonn JS, Huet S, Tran VS, El-Amraoui A, Raposo G, Fanget I, Chapuis C, Ménasché G, de Saint Basile G, Petit C, Cribier S, Henry JP, Darchen F. Rab27A and its effector MyRIP link secretory granules to F-actin and control their motion towards release sites. J Cell Biol 2003;163:559-570.
9. Distinct roles of myosin Va in membrane remodeling and exocytosis of secretory granules. Traffic 2010;11:637-650.
10. Desnos C, Huet S, Fanget I, Chapuis C, Böttiger C, Racine V, Sibarita JB, Henry JP, Darchen F. Myosin va mediates docking of secretory granules at the plasma membrane. J Neurosci 2007;27:10636-10645.
11. Bittins CM, Eichler TW, Hammer JA III, Gerdes HH. Dominant-negative myosin Va impairs retrograde but not anterograde axonal transport of large dense core vesicles. Cell Mol Neurobiol 2009;30:369-379.
12. Hirokawa N, Niwa S, Tanaka Y. Molecular motors in neurons: transport mechanisms and roles in brain function, development, and disease. Neuron 2010;68:610-638.
13. Wollert T, Patel A, Lee YT, Provance DW, Vought VE, Cosqrove MS, Mercer JA, Langford GM. Myosin5a tail associates directly with Rab3A-containing compartments in neurons. J Biol Chem 2011;286:14354-14361.
14. Lapierre LA, Kumar R, Hales CM, Navarre J, Bhartur SG, Burnette JO, Provance DW Jr, Mercer JA, Bähler M, Goldenring JR. Myosin vb is associated with plasma membrane recycling systems. Mol Biol Cell 2001;12:1843-1857.
15. Hales CM, Vaerman JP, Goldenring JR. Rab11 family interacting protein 2 associates with Myosin Vb and regulates plasma membrane recycling. J Biol Chem 2002;277:50415-50421.
16. Volpicelli LA, Lah JJ, Fang G, Goldenring JR, Levey AI. Rab11a and myosin Vb regulate recycling of the M4muscarinic acetylcholine receptor. J Neurosci 2002;22:9776-9784.
17. Roland JT, Kenworthy AK, Peranen J, Caplan S, Goldenring JR. Myosin Vb interacts with Rab8a on a tubular network containing EHD1 and EHD3. Mol Biol Cell 2007;18:2828-2837.
18. Correia SS, Bassani S, Brown TC, Lisé MF, Backos DS, El-Husseini A, Passafaro M, Esteban JA. Motor protein-dependent transport of AMPA receptors into spines during long-term potentiation. Nat Neurosci 2008;11:457-466.
19. Roland JT, Lapierre LA, Goldenring JR. Alternative splicing in class V myosins determines association with Rab10. J Biol Chem 2009;284:1213-1223.
20. Wu X, Wang F, Rao K, Sellers JR, Hammer JA III. Rab27a is an essential component of melanosome receptor for myosin Va. Mol Biol Cell 2002;13:1735-1749.
21. Fukuda M, Kuroda TS, Mikoshiba K. Slac2-a/melanophilin, the missing link between Rab27 and myosin Va: implications of a tripartite protein complex for melanosome transport. J Biol Chem 2002;277:12432-12436.
22. Strom M, Hume AN, Tarafder AK, Barkagianni E, Seabra MC. A family of Rab27-binding proteins. Melanophilin links Rab27a and myosin Va function in melanosome transport. J Biol Chem 2002;277:25423-25430.
23. Ostrowski M, Carmo NB, Krumeich S, Fanget I, Raposo G, Savina A, Moita CF, Schauer K, Hume AN, Freitas RP, Goud B, Benaroch P, Hacohen N, Fukuda M, Desnos C, et al. Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat Cell Biol 2010;12:19-30.
24. Fukuda M. Regulation of secretory vesicle traffic by Rab small GTPases. Cell Mol Life Sci 2008;65:2801-2813.
25. Van Gele M, Dynoodt P, Lambert J. Griscelli syndrome: a model system to study vesicular trafficking. Pigment Cell Melanoma Res 2009;22:268-282.
26. Seperack PK, Mercer JA, Strobel MC, Copeland NG, Jenkins NA. Retroviral sequences located within an intron of the dilute gene alter dilute expression in a tissue-specific manner. EMBO J 1995;14:2326-2332.
27. Coppola T, Frantz C, Perret-Menoud V, Gattesco S, Hirling H, Regazzi R. Pancreatic beta-cell protein granuphilin binds Rab3 and Munc-18 and controls exocytosis. Mol Biol Cell 2002;13:1906-1915.
28. Tsuboi T, Fukuda M. The C2B domain of rabphilin directly interacts with SNAP-25 and regulates the docking step of dense core vesicle exocytosis in PC12cells. J Biol Chem 2005;280:39253-39259.
29. Ohyama A, Komiya Y, Igarashi H. Globular tail of myosin-V is bound to VAMP/synaptobrevin. Biochem Biophys Res Commun 2001;280:988-991.
30. Torii S, Zhao S, Yi Z, Takeuchi T, Izumi T. Granuphilin modulates the exocytosis of secretory granules through interaction with syntaxin 1a. Mol Cell Biol 2002;22:5518-5526.
31. Tomas A, Meda P, Regazzi R, Pessin JE, Halban PA. Munc 18-1 and granuphilin collaborate during insulin granule exocytosis. Traffic 2008;9:813-832.
32. Gomi H, Mizutani S, Kasai K, Itohara S, Izumi T. Granuphilin molecularly docks insulin granules to the fusion machinery. J Cell Biol 2005;171:99-109.
33. Wang J, Takeuchi T, Yokota H, Izumi T. Novel rabphilin-3-like protein associates with insulin-containing granules in pancreatic beta cells. J Biol Chem 1999;274:28542-28548.
34. Arribas M, Regazzi R, Garcia E, Wollheim CB, De Camilli P. The stimulatory effect of rabphilin 3a on regulated exocytosis from insulin-secreting cells does not require an association-dissociation cycle with membranes mediated by Rab 3. Eur J Cell Biol 1997;74:209-216.
35. Thomas A, Meda P, Regazzi R, Pessin JE, Halban PA. Munc 18-1 and granuphillin collaborate during insulin granule exocytosis. Traffic 2008;9:813-832.
36. Ivarsson R, Jing X, Waselle L, Regazzi R, Renström E. Myosin 5a controls insulin granule recruitment during late-phase secretion. Traffic 2005;6:1027-1035.
37. Wu XS, Rao K, Zhang H, Wang F, Sellers JR, Matesic LE, Copeland NG, Jenkins NA, Hammer JA III. Identification of an organelle receptor for myosin-Va. Nat Cell Biol 2002;4:271-278.
38. Waselle L, Coppola T, Fukuda M, Lezzi M, El-Amraoui A, Petit C, Regazzi R. Involvement of the Rab27 binding protein Slac2c/MyRIP in insulin exocytosis. Mol Biol Cell 2003;14:4103-4113.
39. Wagner W, Fodor E, Ginsburg A, Hammer JA III. The binding of DYNLL2 to myosin Va requires alternatively spliced exon B and stabilizes a portion of the myosin's coiled-coil domain. Biochemistry 2006;45:11564-11577.
40. Nedvetsky PI, Stefan E, Frische S, Santamaria K, Wiesner B, Valenti G, Hammer JA III, Nielsen S, Goldenring JR, Rosenthal W, Klussmann E. A Role of myosin Vb and Rab11-FIP2 in the aquaporin-2 shuttle. Traffic 2007;8:110-123.
41. Rodriguez OC, Cheney RE. Human myosin-Vc is a novel class V myosin expressed in epithelial cells. J Cell Sci 2002;115:991-1004.
42. Fukuda M. Slp4-a/granuphilin-a inhibits dense-core vesicle exocytosis through interaction with the GDP-bound form of Rab27A in PC12cells. J Biol Chem 2003;278:15390-15396.
43. Yi Z, Yokota H, Torii S, Aoki T, Hosaka M, Zhao S, Takata K, Takeuchi T, Izumi T. The Rab27a/granuphilin complex regulates the exocytosis of insulin-containing dense-core granules. Mol Cell Biol 2002;22:1858-1867.
44. 2+-inhibitory phospholipid-binding activity of the C2A domain. Mol Biol Cell 2007;18:688-696.
45. Gomi H, Mori K, Itohara S, Izumi T. Rab27b is expressed in a wide range of exocytic cells and involved in the delivery of secretory granules near the plasma membrane. Mol Biol Cell 2007;18:4377-4386.
46. Barral DC, Ramalho JS, Anders R, Hume AN, Knapton HJ, Tolmachova T, Collinson LM, Goulding D, Authi KS, Seabra MC. Functional redundancy of Rab27 proteins and the pathogenesis of Griscelli syndrome. J Clin Invest 2002;110:247-257.
47. Westbroek W, Lambert J, De Schepper S, Kleta R, Van Den Bossche K, Seabra MV, Huizing M, Mommaas M, Naeyaert JM. Rab27b is up-regulated in human Griscelli syndrome type II melanocytes and linked to the actin cytoskeleton via exon F-Myosin Va transcripts. Pigment Cell Res 2004;17:498-505.
48. Lambert J, Naeyaert JM, Callens T, De Paepe A, Messiaen L. Human myosin V gene produces different transcripts in a cell type-specific manner. Biochem Biophys Res Commun 1998;252:329-333.
49. Huang JD, Mermall V, Strobel MC, Russell LB, Mooseker MS, Copeland NG, Jenkins NA. Molecular genetic dissection of mouse unconventional myosin-VA: tail region mutations. Genetics 1998;148:1963-1972.
50. Tsuboi T, Fukuda M. The Slp4-a linker domain controls exocytosis through interaction with Munc18-1·syntaxin-1a complex 2006. Mol Biol Cell 2006;17:2101-2112.
51. Kasai K, Fujita T, Gomi H, Izumi T. Docking is not a prerequisite but a temporal constraint for fusion of secretory granules. Traffic 2008;9:1191-1203.
52. Ishihara H, Asano T, Tsukuda K, Katagiri H, Inukai K, Anai M, Kikuchi M, Yazaki Y, Miyazaki JI, Oka Y. Pancreatic beta cell line MIN6 exhibits characteristics of glucose metabolism and glucose-stimulated insulin secretion similar to those of normal islets. Diabetologia 1993;36:1139-1145.
53. Tsuboi T, Kitaguchi T, Karasawa S, Fukuda M, Miyawaki A. Age-dependent preferential dense-core vesicle exocytosis in neuroendocrine cells revealed by newly developed monomeric fluorescent timer protein. Mol Biol Cell 2010;21:87-94.
54. Diraison F, Ravier MA, Richards SK, Smith RM, Shimano H, Rutter GA. SREBP1 is required for the induction by glucose of pancreatic beta-genes involved in glucose sensing. J Lipid Res 2008;49:814-822.
55. Coppola T, Hirling H, Perret-Menoud V, Gattesco S, Catsicas S, Joberty G, Macara IG, Regazzi R. Rabphilin dissociated from Rab3 promotes endocytosis through interaction with Rabaptin-5. J Cell Sci 2001;114:1757-1764.
56. Fukuda M, Kuroda TS. Missense mutations in the globular tail of myosin-Va in dilute mice partially impair binding of Slac2-a/melanophilin. J Cell Sci 2004;117:583-591.
57. Fukuda M, Kanno E, Ogata Y, Mikoshiba K. Mechanism of the SDS-resistant synaptotagmin clustering mediated by the cysteine cluster at the interface between the transmembrane and spacer domains. J Biol Chem 2001;276:40319-40325.
58. Fukuda M, Kuroda TS. Slac2-c (synaptotagmin-like protein homologue lacking C2 domains-c), a novel linker protein that interacts with Rab27, myosin Va/VIIa, and actin. J Biol Chem 2002;277:43096-43103.
59. Varadi A, Johnson-Cadwell LI, Cirulli V, Yoon Y, Allan VJ, Rutter GA. Cytoplasmic dynein regulates the subcellular distribution of mitochondria by controlling the recruitment of the fission factor dynamin-related protein-1. J Cell Sci 2004;117:4389-4400.
60. Scheiffele P, Verkade P, Fra AM, Virta H, Simons K, Ikonen E. Caveolin-1 and -2 in the exocytic pathway of MDCK cells. J Cell Biol 1998;140:795-806.
61. van Weering JRT, Brown E, Sharp TH, Mantell J, Cullen PJ, Verkade P. Intracellular membrane traffic at high resolution. Methods Cell Biol 2010;96:619-648.