Myosin Va transports dense core secretory vesicles in pancreatic MIN6 β-cells

Molecular Biology of the Cell

Volumn 16, Issue 6, 2005, Pages 2670-2680

  Varadi, Aniko ^a,b   Tsuboi, Takashi ^a   Rutter, Guy A ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

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

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; GREEN FLUORESCENT PROTEIN; INSULIN; MYOSIN VA; RNA;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; DENSE BODY; EXOCYTOSIS; FLUORESCENCE ACTIVATED CELL SORTING; FLUORESCENCE MICROSCOPY; IMMUNOREACTIVITY; INSULIN RELEASE; MITOCHONDRION; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; RNA INTERFERENCE; SECRETORY VESICLE;

ANIMALS; BIOLOGICAL MARKERS; BIOLOGICAL TRANSPORT; CELL CULTURE TECHNIQUES; CELL LINE, TUMOR; CELL MEMBRANE; CENTRIFUGATION, DENSITY GRADIENT; EXOCYTOSIS; GLUCOSE; GREEN FLUORESCENT PROTEINS; HUMANS; IMMUNOHISTOCHEMISTRY; INSULIN; ISLETS OF LANGERHANS; MEMBRANE PROTEINS; MICE; MICROSCOPY, INTERFERENCE; MUTATION; MYOSIN HEAVY CHAINS; MYOSIN TYPE V; PANCREAS; PROTEIN STRUCTURE, TERTIARY; PROTEIN-TYROSINE-PHOSPHATASE; RNA INTERFERENCE; SECRETORY VESICLES;

EID: 19644364331     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E04-11-1001     Document Type: Article

References (81)

1. Al Haddad, A., et al. (2001). Myosin Va bound to phagosomes binds to F-actin and delays microtubule-dependent motility. Mol. Biol. Cell 12, 2742-2755.
2. Au, J. S., and Huang, J. D. (2002). A tissue-specific exon of myosin Va is responsible for selective cargo binding in melanocytes. Cell Motil. Cytoskeleton 53, 89-102.
3. Axelrod, D. (1981). Cell-substrate contacts illuminated by total internal reflection fluorescence. J. Cell Biol. 89, 141-145.
4. Boldogh, I., Vojtov, N., Karmon, S., and Pon, L. A. (1998). Interaction between mitochondria and the actin cytoskeleton in budding yeast requires two integral mitochondrial outer membrane proteins, Mmm1p and Mdm10p. J. Cell Biol. 141, 1371-1381.
5. Boldogh, I. R., Ramcharan, S. L., Yang, H. C., and Pon, L. A. (2004). A type V myosin (Myo2p) and a Rab-like G-protein (Ypt11p) are required for retention of newly inherited mitochondria in yeast cells during cell division. Mol. Biol. Cell 15, 3994-4002.
6. Bonner-Weir, S. (1988). Morphological evidence for pancreatic polarity of beta cells within islets of Langerhans. Diabetes 37, 616-621.
7. Bowman, A. B., Kamal, A., Ritchings, B. W., Philp, A. V., McGrail, M., Gindhart, J. G., and Goldstein, L. S. (2000). Kinesin-dependent axonal transport is mediated by the Sunday driver (SYD) protein. Cell 103, 583-594.
8. Bratanova-Tochkova, T. K., Cheng, H., Daniel, S., Gunawardana, S., Liu, Y. J., Mulvaney-Musa, J., Schermerhorn, T., Straub, S. G., Yajima, H., and Sharp, G. W. (2002). Triggering and augmentation mechanisms, granule pools, and biphasic insulin secretion. Diabetes 51 (suppl 1), S83-S90, S83-S90.
9. Bridgman, P. C. (1999). Myosin Va movements in normal and dilute-lethal axons provide support for a dual filament motor complex. J. Cell Biol. 146, 1045-1060.
10. Brown, M. S., and Goldstein, J. L. (1997). The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell 89, 331-340.
11. Cao, T. T., Chang, W., Masters, S. E., and Mooseker, M. S. (2004). Myosin-Va binds to and mechanochemically couples microtubules to actin filaments. Mol. Biol. Cell 15, 151-161.
12. Cheney, R. E., O'Shea, M. K., Heuser, J. E., Coelho, M. V., Wolenski, J. S., Espreafico, E. M., Forscher, P., Larson, R. E., and Mooseker, M. S. (1993). Brain myosin-V is a two-headed unconventional myosin with motor activity. Cell 75, 13-23.
13. Coppola, T., Frantz, C., Perret-Menoud, V., Gattesco, S., Hirling, H., and Regazzi, R. (2002). Pancreatic beta-cell protein granuphilin binds Rab3 and Munc-18 and controls exocytosis. Mol. Biol. Cell 13, 1906-1915.
14. Da Silva Xavier, G., Qian, Q., Cullen, P. J., and Rutter, G. A. (2004). Distinct roles for insulin and insulin-like growth factor-1 receptors in pancreatic beta-cell glucose sensing revealed by RNA silencing. Biochem. J. 377, 149-158.
15. Deacon, S. W., and Gelfand, V.I. (2001). Of yeast, mice, and men. Rab proteins and organelle transport. J. Cell Biol. 152, F21-F24.
16. DePina, A. S., and Langford, G. M. (1999). Vesicle transport: the role of actin filaments and myosin motors. Microsc. Res. Tech. 472, 93-106.
17. 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.
18. Elbashir, S. M., Harborth, J., Lendeckel, W., Yalcin, A., Weber, K., and Tuschl, T. (2001). Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411, 494-498.
19. Evans, L. L., Lee, A. J., Bridgman, P. C., and Mooseker, M. S. (1998). Vesicle-associated brain myosin-V can be activated to catalyze actin-based transport. J. Cell Sci. 111, 2055-2066.
20. Fukuda, M., Kuroda, T. S., and 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.
21. 2+ indicators with greatly improved fluorescence properties. J. Biol. Chem. 260, 3440-3450.
22. He, T. C., Zhou, S., da Costa, L. T., Yu, J., Kinzler, K. W., and Vogelstein, B. (1998). A simplified system for generating recombinant adenoviruses. Proc. Natl. Acad. Sci. USA 95, 2509-2514.
23. Hoepfner, D., van den Berg, M., Philippsen, P., Tabak, H. F., and Hettema, E. H. (2001). A role for Vps1p, actin, and the Myo2p motor in peroxisome abundance and inheritance in Saccharomyces cerevisiae. J. Cell Biol. 155, 979-990.
24. Huang, J. D., Cope, M. J., Mermall, V., Strobel, M. C., Kendrick-Jones, J., Russell, L. B., Mooseker, M. S., Copeland, N. G., and Jenkins, N. A. (1998a). Molecular genetic dissection of mouse unconventional myosin-VA: head region mutations. Genetics 148, 1951-1961.
25. Huang, J. D., Mermall, V., Strobel, M. C., Russell, L. B., Mooseker, M. S., Copeland, N. G., and Jenkins, N. A. (1998b). Molecular genetic dissection of mouse unconventional myosin-VA: tail region mutations. Genetics 148, 1963-1972.
26. Huang, J. D., Brady, S. T., Richards, B. W., Stenolen, D., Resau, J. H., Copeland, N. G., and Jenkins, N. A. (1999). Direct interaction of microtubule- and actin-based transport motors. Nature 397, 267-270.
27. Hume, A. N., Collinson, L. M., Hopkins, C. R., Strom, M., Barral, D. C., Bossi, G., Griffiths, G. M., and Seabra, M. C. (2002). The leaden gene product is required with Rab27a to recruit myosin Va to melanosomes in melanocytes. Traffic 3, 193-202.
28. Ishikawa, K., Catlett, N. L., Novak, J. L., Tang, F., Nau, J. J., and Weisman, L. S. (2003). Identification of an organelle-specific myosin V receptor. J. Cell Biol. 160, 887-897.
29. Itoh, T., Watabe, A., Toh, E., and Matsui, Y. (2002). Complex formation with Yp11p, a rab-type small GTPase, is essential to facilitate the function of Myo2p, a class V myosin, in mitochondrial distribution in Saccharomyces cerevisiae. Mol. Cell. Biol. 22, 7744-7757.
30. Izumi, T., Gomi, H., Kasai, K., Mizutani, S., and Torii, S. (2003). The roles of Rab27 and its effectors in the regulated secretory pathways. Cell Struct. Funct. 28, 465-474.
31. Karcher, R. L., Deacon, S. W., and Gelfand, V. I. (2002). Motor-cargo interactions: the key to transport specificity. Trends Cell Biol. 12, 21-27.
32. Kuroda, T. S., Fukuda, M., Ariga, H., and Mikoshiba, K. (2002). The Sip homology domain of synaptotagmin-like proteins 1-4 and Slac2 functions as a novel Rab27A binding domain. J. Biol. Chem. 277, 9212-9218.
33. Langford, G. M. (2002). Myosin-V, a versatile motor for short-range vesicle transport. Traffic 3, 859-865.
34. Luzio, J. P., Brake, B., Banting, G., Howell, K. E., Braghetta, P., and Stanley, K. K. (1990). Identification, sequencing and expression of an integral membrane protein of the trans-Golgi network (TGN38). Biochem. J. 270, 97-102.
35. Matesic, L. E., Yip, R., Reuss, A. E., Swing, D. A., O'Sullivan, T. N., Fletcher, C. F., Copeland, N. G., and Jenkins, N. A. (2001). Mutations in Mlph, encoding a member of the Rab effector family, cause the melanosome transport defects observed in leaden mice. Proc. Natl. Acad. Sci. USA 98, 10238-10243.
36. Mercer, J. A., Seperack, P. K., Strobel, M. C., Copeland, N. G., and Jenkins, N. A. (1991). Novel myosin heavy chain encoded by murine dilute coat colour locus. Nature 349, 709-713.
37. Mermall, V., Post, P. L., and Mooseker, M. S. (1998). Unconventional myosins in cell movement, membrane traffic, and signal transduction. Science 279, 527-533.
38. Miller, K. E., and Sheetz, M. P. (2000), Characterization of myosin V binding to brain vesicles. J. Biol. Chem. 275, 2598-2606.
39. Molnar, E., Varadi, A., McIlhinney, R.A.J., and Ashcroft, S.J.H (1995). Identification of functional ionotropic glutamate receptor proteins in pancreatic beta-cells and in islets of Langerhans. FEBS Lett. 371, 253-257.
40. Nagashima, K., Torii, S., Yi, Z., Igarashi, M., Okamoto, K., Takeuchi, T., and Izumi, T. (2002). Melanophilin directly links Rab27a and myosin Va through its distinct coiled-coil regions. FEES Lett. 517, 233-238.
41. Nakata, T., and Hirokawa, N. (1992). Organization of cortical cytoskeleton of cultured chromaffin cells and involvement in secretion as revealed by quick-freeze, deep-etching, and double-label Immunoelectron microscopy, J. Neurosci. 12, 2186-2197.
42. Nascimento, A. A., Amaral, R. G., Bizario, J. C., Larson, R. E., and Espreafico, E. M. (1997). Subcellular localization of myosin-V in the B16 melanoma cells, a wild-type cell line for the dilute gene. Mol. Biol. Cell 10, 1971-1988.
43. Pinton, P., Tsuboi, T., Ainscow, E. K., Pozzan, T., Rizzuto, R., and Rutter, G. A. (2002). Dynamics of glucose-induced recruitment of protein kinase C βII in living pancreatic islet β-cells. J. Biol. Chem. 277, 37702-37710.
44. Pouli, A. E., Emmanouilidou, E., Zhao, C., Wasmeier, C., Hutton, J. C., and Rutter, G. A. (1998). Secretory granule dynamics visualised in vivo with a phogrin-green fluorescent protein chimaera. Biochem. J. 333, 193-199.
45. Prekeris, R., and Terrian, D. M. (1997). Brain myosin V is a synaptic vesicle-associated motor protein; evidence for a Ca2+-dependent interaction with the synaptobrevin-synaptophysin complex. J. Cell Biol. 137, 1589-1601.
46. Provance, D. W., Jr., Wei, M., Ipe, V., and Mercer, J. A. (1996). Cultured melanocytes from dilute mutant mice exhibit dendritic morphology and altered melanosome distribution. Proc. Natl. Acad, Sci. USA 93, 14554-14558.
47. Provance, D. W., James, T. L., and Mercer, J. A. (2002). Melanophilin, the product of the leaden locus, is required for targeting of myosin-Va to melanosomes. Traffic 2, 124-132.
48. Reck-Peterson, S. L., Provance, D. W., Jr., Mooseker, M. S., and Mercer, J. A. (2000). Class V myosins. Biochim. Biophys. Acta 1496, 36-51.
49. Regazzi, R., Ravazzola, M., Lezzi, M., Lang, J. C., Zahraoui, A., Andereggen, E., Morel, P., Takai, Y., and Wollheim, C. B. (1996), Expression, localization and functional role of small GTPases of the Rab3 family in insulin-secreting cells. J. Cell Sci. 109, 2265-2273.
50. Rudolf, R., Kogel, T., Kuznetsov, S. A., Salm, T., Schlicker, O., Hellwig, A., Hammer, J. A., 3rd, and Gerdes, H. H. (2003). Myosin Va facilitates the distribution of secretory granules in the F-actin rich cortex of PC12 cells. J. Cell Sci. 116, 1339-1348.
51. Rutter, G. A. (2001). Nutrient-secretion coupling in the pancreatic islet β-cell: recent advances. Mol. Asp. Med. 22, 247-284.
52. Rutter, G. A. (2004) Visualising Insulin Secretion. The Minkowski Lecture 2004. Diabetologia 47, 1861-1872.
53. Schliwa, M. (1999). Molecular motors join forces. Nature 397, 204-205.
54. Schott, D., Ho, J., Pruyne, D., and Bretscher, A. (1999), The COOH-terminal domain of Myo2p, a yeast myosin V, has a direct role in secretory vesicle targeting. J. Cell Biol. 147, 791-808.
55. Seperack, P. K., Mercer, J. A., Strobel, M. C., Copeland, N. G., and 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.
56. Simon, V. R., Swayne, T. C., and Pon, L. A. (1995). Actin-dependent mitochondrial motility in mitotic yeast and cell-free systems: identification of a motor activity on the mitochondrial surface. J. Cell Biol. 130, 345-354.
57. Strobel, M. C., Seperack, P. K., Copeland, N. G., and Jenkins, N. A. (1990), Molecular analysis of two mouse dilute locus deletion mutations: spontaneous dilute lethal20J and radiation-induced dilute prenatal lethal Aa2 alleles. Mol. Cell. Biol. 10, 501-509.
58. Tabb, J. S., Molyneaux, B. J., Cohen, D. L., Kuznetsov, S. A., and Langford, G. M. (1998). Transport of ER vesicles on actin filaments in neurons by myosin V. J. Cell Sci. 111, 3221-3234.
59. Takagishi, Y., Oda, S., Hayasaka, S., Dekker-Ohno, K., Shikata, T., Inouye, M., and Yamamura, H. (1996). The dilute-lethal (dl) gene attacks a Ca2+ store in the dendritic spine of Purkinje cells in mice. Neurosci. Lett. 215, 169-172.
60. Torii, S., Takeuchi, T., Nagamatsu, S., and Izumi, T. (2004). Rab27 effector granuphilin promotes the plasma membrane targeting of insulin granules via interaction with syntaxin 1a. J. Biol. Chem. 279, 22532-22538.
61. Torii, S., Zhao, S., Yi, Z., Takeuchi, T., and Izumi, T. (2002). Granuphilin modulates the exocytosis of secretory granules through interaction with syntaxin 1a. Mol. Cell. Biol. 22, 5518-5526.
62. Tsuboi, T., Da Silva Xavier, G., Leclerc, I., and Rutter, G. A. (2003). 5′ AMP-activated protein kinase controls insulin-containing secretory vesicle dynamics. J. Biol. Chem. 278, 52042-52051.
63. Tsuboi, T., and Rutter, G, A. (2003) Multiple forms of kiss and run exocytosis revealed by evanescent wave microscopy. Curr. Biol. 13, 563-567.
64. Tsuboi, T., Zhao, C., Terakawa, S., and Rutter, G. A. (2000). Simultaneous evanescent wave imaging of insulin vesicle membrane and cargo during a single exocytotic event. Curr. Biol. 10, 1307-1310.
65. Vallee, R. B, and Sheetz, M. P. (1996), Targeting of motor proteins. Science 271, 1539-1544.
66. Varadi, A., Ainscow, E. K., Allan, V. J., and Rutter, G. A. (2002). Involvement of conventional kinesin in glucose-stimulated secretory-granule movements and exocytosis in clonal pancreatic β-cells. J. Cell Sci. 115, 4177-4189.
67. Varadi, A., Molnar, E., Ostenson, C. G., and Ashcroft, S. J. (1996). Isoforms of endoplasmic reticulum Ca(2+)-ATPase are differentially expressed in normal and diabetic islets of Langerhans. Biochem. J. 319, 521-527.
68. Varadi, A., Johnson-Cadwell, L. I., Cirulli, V., Yoon, Y., Allan, V. J., and Rutter, G. A. (2004). Cytoplasmic dynein regulates the subcellular distribution of mitochondria by controlling the recruitment of the fission factor dynamin-related protein-1. J. Cell Sci. 117, 4389-4400.
69. 2+] in MIN6 β-cells using recombinant chameleons: roles of SERCA2 and ryanodine receptors. Diabetes 51, S190-S201.
70. Varadi, A., Tsuboi, T., Johnson-Cadwell, L. I., Allan, V. J., and Rutter, G. A. (2003), Kinesin I and cytoplasmic dynein orchestrate glucose-stimulated insulin-containing vesicle movements in clonal MIN6 beta-cells. Biochem. Biophys. Res. Commun. 311, 272-282.
71. Verhey, K. J., Meyer, D., Deehan, R., Blenis, J., Schnapp, B. J., Rapoport, T. A., and Margolis, B. (2001). Cargo of kinesin identified as JIP scaffolding proteins and associated signaling molecules. J. Cell Biol. 152, 959-970.
72. Wang, J., Takeuchi, T., Yokota, H., and Izumi, T. (1999). Novel rabphilin-3-like protein associates with insulin-containing granules in pancreatic beta cells. J. Biol. Chem. 274, 28542-28548.
73. Waselle, L., Coppola, T., Fukuda, M., Iezzi, M., El Amraoui, A., Petit, C., and Regazzi, R. (2003). Involvement of the Rab27 binding protein Slac2c/MyRIP in insulin exocytosis. Mol. Biol. Cell 14, 4103-4113.
74. Wasmeier, C., and Hutton, J. C. (1996). Molecular cloning of phogrin, a protein-tyrosine phosphatase homologue localized to insulin secretory granule membranes. J. Biol. Chem. 271, 18161-18170.
75. Weber, K. L., Sokac, A. M., Berg, J. S., Cheney, R. E., and Bement, W. M. (2004). A microtubule-binding myosin required for nuclear anchoring and spindle assembly. Nature 431, 325-329.
76. Wu, X., Bowers, B., Rao, K., Wei, Q., and Hammer, J. A. (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.
77. Wu, X. S., Rao, K., Zhang, H., Wang, F., Sellers, J. R., Matesic, L. E., Copeland, N, G., Jenkins, N. A., and Hammer, J. A., 3rd. (2002a) Identification of an organelle receptor for myosin-Va. Nat. Cell Biol. 4, 271-278.
78. Wu, X., Wang, F., Rao, K., Sellers, J. R., and Hammer, J. A., 3rd. (2002b) Rab27a is an essential component of melanosome receptor for myosin Va. Mol. Biol. Cell 5, 1735-1749.
79. Yaekura, K., et al. (2003). Insulin secretory deficiency and glucose intolerance in Rab3A null mice. J. Biol. Chem. 278, 9715-9721.
80. Yi, M., Weaver, D., and Hajnoczky, G. (2004). Control of mitochondrial motility and distribution by the calcium signal: a homeostatic circuit. J. Cell Biol. 167, 661-672.
81. Yi, Z., Yokota, H., Torii, S., Aoki, T., Hosaka, M., Zhao, S., Takata, K., Takeuchi, T., and Izumi, T. (2002). The Rab27a/granuphilin complex regulates the exocytosis of insulin-containing dense-core granules. Mol. Cell. Biol. 22, 1858-1867.