Kinesin I and cytoplasmic dynein orchestrate glucose-stimulated insulin-containing vesicle movements in clonal MIN6 β-cells

Biochemical and Biophysical Research Communications

Volumn 311, Issue 2, 2003, Pages 272-282

  Varadi, Aniko ^a   Tsuboi, Takashi ^a   Johnson Cadwell, Linda I ^a   Allan, Victoria J ^b   Rutter, Guy A ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Dynein; Insulin; Islet; Kinesin; Secretion; Trafficking; Vesicle

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE; GLUCOSE; GREEN FLUORESCENT PROTEIN; INSULIN; KINESIN; PROTEIN SUBUNIT;

ARTICLE; B LYMPHOCYTE; CELL ACTIVITY; CELL STRAIN; CELL VACUOLE; CONTROLLED STUDY; CYTOPLASM; EXOCYTOSIS; HUMAN; HUMAN CELL; IMAGING; MICROTUBULE; MOLECULAR CLONING; MOTOR ACTIVITY; PRIORITY JOURNAL;

EID: 0242362834     PISSN: 0006291X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbrc.2003.09.208     Document Type: Article

References (50)

1. Rorsman P., Eliasson L., Renstrom E., Gromada J., Barg S., Gopel S. The cell physiology of biphasic insulin secretion. News Physiol. Sci. 15:2000;72-77.
2. Rhodes C.J. Introduction: the molecular cell biology of insulin production. Semin. Cell Dev. Biol. 11:2000;223-2255.
3. Malaisse W.J., Sener A. Glucose-induced changes in cytosolic ATP content in pancreatic islets. Biochim. Biophys. Acta. 927:1987;190-195.
4. Kennedy H.J., Pouli A.E., Jouaville L.S., Rizzuto R., Rutter G.A. Glucose-induced ATP microdomains in single islet β-cells. J. Biol. Chem. 274:1999;13281-13291.
5. AguilarBryan L., Bryan J. Molecular biology of adenosine triphosphate-sensitive potassium channels. Endocr. Rev. 20:1999;101-135.
6. Safayhi H., Haase H., Kramer U., Bihlmayer A., Roenfeldt M., Ammon H.P.T., Froschmayr M., Cassidy T.N., Morano I., Ahlijanian M.K., Striessnig J. L-type calcium channels in insulin-secreting cells: biochemical characterization and phosphorylation in RINm5F cells. Mol. Endocrinol. 11:1997;619-629.
7. Henquin J.C. Triggering and amplifying pathways of regulation of insulin secretion by glucose. Diabetes. 49:2000;175-1760.
8. Rutter G.A. Nutrient-secretion coupling in the pancreatic islet beta-cell: recent advances. Mol. Aspects Med. 22:2001;247-284.
9. Grodsky G.M., Curry D., Landahl H., Bennett L. Further studies on the dynamic aspects of insulin release in vitro with evidence for a two-compartmental storage system. Acta Diabetol. Lat. 6:1969;554-578.
10. 2+ in rat pancreatic islets. Proc. Natl. Acad. Sci. USA. 92:1995;10728-10732.
11. Pouli A.E., Emmanouilidou E., Zhao C., Wasmeier C., Hutton J.C., Rutter G.A. Secretory granule dynamics visualised in vivo with a phogrin-green fluorescent protein chimaera. Biochem. J. 333:1998;193-199.
12. Varadi A., Ainscow E.K., Allan V.J., Rutter G.A. Involvement of conventional kinesin in glucose-stimulated secretory granule movements and exocytosis in clonal pancreatic β-cells. J. Cell Sci. 115:2002;4177-4189.
13. Li G., Rungger-Brandle E., Just I., Jonas J.C., Aktories K., Wollheim C.B. Effect of disruption of actin filaments by Clostridium botulinum C2 toxin on insulin secretion in HIT-T15 cells and pancreatic islets. Mol. Biol. Cell. 5:1994;1199-1213.
14. Thurmond D.C., Gonelle-Gispert C., Furukawa M., Halban P.A., Pessin J. Glucose-stimulated insulin secretion is coupled to the interaction of actin with the t-SNARE (Target membrane soluble N-ethylmaleimide-sensitive factor attachment protein receptor protein) complex. Mol. Endocrinol. 17:2003;732-742.
15. Schliwa M., Woehlke G. Molecular motors. Nature. 422:2003;759-765.
16. Vale R.D. The molecular motor toolbox for intracellular transport. Cell. 122:2003;467-480.
17. Holzbaur E.L., Vallee R.B. Dyneins: molecular structure and cellular function. Annu. Rev. Cell Biol. 10:1994;339-372.
18. Allan V., Dynactin Curr. Biol. 10:2000;R432.
19. Burkhardt J.K., Echeverri C.J., Nilsson T., Vallee R.B. Over-expression of the dynamitin (p50) subunit of the dynactin complex disrupts dynein-dependent maintenance of membrane organelle distribution. J. Cell Biol. 139:1997;469-484.
20. Valetti C., Wetzel D.M., Schrader M., Hasbani M.J., Gill S.R., Kreis T.E., Schroer T.A. Role of dynactin in endocytic traffic: effects of dynamitin over-expression and co-localization with CLIP-170. Mol. Biol. Cell. 10:1999;4107-4120.
21. Fisher R.J., Burgoyne R.D. The effect of transfection with botulinum neurotoxin C1 light chain on exocytosis measured in cell populations and by single-cell amperometry in PC12 cells. Pflugers Arch. 437:1999;754-762.
22. Molnar E., Varadi A., McIlhinney R.A.J., Ashcroft S.J.H. Identification of functional ionotropic glutamate receptor proteins in pancreatic beta-cells and in islets of Langerhans. FEBS Lett. 371:1995;253-257.
23. 2+] in MIN6 β-cells using recombinant chameleons: roles of SERCA2 and ryanodine receptors. Diabetes. 51:2002;S190-S201.
24. Tsuboi T., Zhao C., Terakawa S., Rutter G.A. Simultaneous evanescent wave imaging of insulin vesicle membrane and cargo during a single exocytotic event. Curr. Biol. 10:2000;1307-1310.
25. Pinton P., Tsuboi T., Ainscow E.K., Pozzan T., Rizzuto R., Rutter G.A. Dynamics of glucose-induced membrane recruitment of protein kinase C beta II in living pancreatic islet beta-cells. J. Biol. Chem. 277:2002;37702-37710.
26. Tsuboi T., Rutter G.A. Multiple forms of "Kiss-and-Run" exocytosis revealed by evanescent wave microscopy. Curr. Biol. 13:2003;563-567.
27. Betz W.J., Bewick G.S. Optical analysis of synaptic vesicle recycling at the frog neuromuscular junction. Science. 255:1992;200-203.
28. Aravanis A.M., Pyle J.L., Tsien R.W. Single synaptic vesicles fusing transiently and successively without loss of identity. Nature. 423:2003;643-664.
29. Tanaka Y., Kanai Y., Okada Y., Nonaka S., Takeda S., Harada A., Hirokawa N. Targeted disruption of mouse conventional kinesin heavy chain, kif5B, results in abnormal perinuclear clustering of mitochondria. Cell. 93:1998;1147-1158.
30. Rietdorf J., Ploubidou A., Reckmann I., Holmsrom A., Frischknecht F., Zettl M., Zimmermann T., Way M. Kinesin-dependent movement on microtubules precedes actin-based motility of vaccinia virus. Nat. Cell Biol. 3:2002;992-1000.
31. Galjart N., Prez F. A plus-end raft to control microtubule dynamics and function. Curr. Opin. Cell Biol. 15:2003;48-53.
32. Wasmeier C., Hutton J.C. Molecular cloning of phogrin, a protein-tyrosine phosphatase homologue localized to insulin secretory granule membranes. J. Biol. Chem. 271:1996;18161-18170.
33. 2+-dependent dephosphorylation of kinesin heavy chain on beta-granules in pancreatic beta-cells. Implications for regulated beta-granule transport and insulin exocytosis. J. Biol. Chem. 277:2002;24232-24242.
34. Howel S.L., Hii C.S., Shaikh S., Tyhurst M. Effect of taxol and nocodazole on insulin secretion from isolated rat islets of Langerhans. Biosci. Rep. 2:1982;795-801.
35. Farshori P.Q., Goode D. Effects of the microtubule deploymerizing and stabilizing agent nocodazole and taxol on glucose-induced insulin secretion from hamster islet tumor (HIT) cells. J. Submicrosc. Cytol. Pathol. 26:1994;137-146.
36. Orci L., Gabbay K.H., Malaisse W.J. Pancreatic β-cell web: its possible role in insulin secretion. Science. 175:1972;1128-1130.
37. Lang T., Wacker I., Wunderlich I., Rohrbach A., Giese G., Soldati T., Almers W. Role of actin cortex in the subplasmalemmal transport of secretory granules in PC-12 cells. Biophys. J. 78:2000;2863-2877.
38. A.K. Nevins, D.C. Thurmond, Glucose regulates the cortical actin network through modulation of Cdc42 cycling to stimulate insulin secretion in pancreatic beta cells, Am. J. Physiol. Cell Physiol. (2003) May 21 [Epub ahead of print].
39. Barg S., Olofsson C.S., Schriever-Alben J., Wendt A., Gebre-Medhin S., Renstrom E., Rorsman P. Delay between fusion pore opening and peptide release from large dense-core vesicles in neuroendocrine cells. Neuron. 33:2002;287-299.
40. 2+ channels and insulin-containing secretory granules and its significance for the initiation of exocytosis in mouse pancreatic β-cells. EMBO J. 14:1995;50-57.
41. 2+ channel is functionally coupled to the exocytotic machinery. Proc. Natl. Acad. Sci. USA. 96:1999;248-253.
42. Chamberlain L.H., Burgoyne R.D., Gould G.W. SNARE proteins are highly enriched in lipid rafts in PC12 cells: implications for the spatial control of exocytosis. Proc. Natl. Acad. Sci. USA. 98:2001;5619-5624.
43. Richards D.A., Guatimosim C., Betz W.J. Two endocytic recycling routes selectively fill two vesicle pools in frog motor nerve terminals. Neuron. 27:2000;551-559.
44. Ales E., Tabares L., Poyato J.M., Valero V., Lindau M., Alvarez de Toledo G. High calcium concentrations shift the mode of exocytosis to the kiss-and-run mechanism. Nat. Cell Biol. 1:1999;40-44.
45. Elbashir S.M., Harborth J., Lendeckel W., Yalcin A., Weber K., Tuschl T. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature. 411:2001;494-498.
46. Martin M., Iyadurai S.J., Gassman A., Gindhart J.G., Hays T.S., Saxton W.M. Cytoplasmic dynein, the dynactin complex, and kinesin are interdependent and essential for fast axonal transport. Mol. Biol. Cell. 10:1999;3717-3728.
47. Januschke J., Gervais L., Dass S.J.A., Kaltschmidt H., Lopez-Schier D.S., Johnston A.H., Brand S., Roth S., Guichet A. Polar transport in the Drosophila oocyte requires Dynein and Kinesin I cooperation. Curr. Biol. 12:2002;1971-1981.
48. Deacon S.W., Serpinskaya A.S., Vaughan P.S., Fanarraga M.L., Vernos I., Vaughan K.T., Gelfand V.I. Dynactin is required for bidirectional organelle transport. J. Cell Biol. 160:2003;297-301.
49. Gross S.P., Welte M.A., Block S.M., Wieschaus E.F. Coordination of opposite-polarity microtubule motors. J. Cell Biol. 156:2002;715-724.
50. Iida Y., Senda T., Matsukawa Y., Onoda K., Miyazaki J.-I., Sakaguchi H., Nimura Y., Hidaka H., Niki I. Myosin light-chain phosphorylation controls insulin secretion at a proximal step in the secretory cascade. Am. J. Physiol. 273:1999;E782-E789.