Kinetics of Rab27a-dependent actions on vesicle docking and priming in pancreatic β-cells

Journal of Physiology

Volumn 586, Issue 22, 2008, Pages 5367-5381

  Merrins, Matthew J ^a   Stuenkel, Edward L ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; DOCKING PROTEIN; GLUCOSE; RAB PROTEIN; RAB27A PROTEIN; CALCIUM ION; CYCLIC AMP DEPENDENT PROTEIN KINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM TRANSPORT; CONTROLLED STUDY; DOWNSTREAM PROCESSING; EXOCYTOSIS; INSULIN RELEASE; MEMBRANE DEPOLARIZATION; MEMBRANE VESICLE; MOLECULAR DOCKING; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; WILD TYPE; CELL GRANULE; CELLULAR PARAMETERS; EVOKED RESPONSE; MEMBRANE CAPACITANCE; PROTEIN ANALYSIS; PROTEIN PROTEIN INTERACTION; VESICLE POOL REFILLING; VESICLE PRIMING;

ANIMALS; CARRIER PROTEINS; CYCLIC AMP; EXOCYTOSIS; FEMALE; GLUCOSE; GUANINE NUCLEOTIDE EXCHANGE FACTORS; INSULIN; INSULIN-SECRETING CELLS; KINETICS; MALE; MICE; MICE, INBRED C3H; MICE, KNOCKOUT; RAB GTP-BINDING PROTEINS; RAB3A GTP-BINDING PROTEIN; SIGNAL TRANSDUCTION;

EID: 56649111420     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2008.158477     Document Type: Article

References (57)

1. Ammala C, Ashcroft FM & Rorsman P (1993a). Calcium-independent potentiation of insulin release by cyclic AMP in single β-cells. Nature 363, 356-358.
2. Ammala C, Eliasson L, Bokvist K, Berggren PO, Honkanen RE, Sjoholm A & Rorsman P (1994). Activation of protein kinases and inhibition of protein phosphatases play a central role in the regulation of exocytosis in mouse pancreatic β-cells. Proc Natl Acad Sci U S A 91, 4343-4347.
3. Ammala C, Eliasson L, Bokvist K, Larsson O, Ashcroft FM & Rorsman P (1993b). Exocytosis elicited by action potentials and voltage-clamp calcium currents in individual mouse pancreatic β-cells. J Physiol 472, 665-688.
4. 2+ channels accounts for first-phase insulin secretion in mouse β-cells. Diabetes 51 (Suppl. 1), S74-S82.
5. 2+ channels in insulin-secreting mouse pancreatic β-cells. Biophys J 81, 3308-3323.
6. Betz A, Thakur P, Junge HJ, Ashery U, Rhee JS, Scheuss V, Rosenmund C, Rettig J & Brose N (2001). Functional interaction of the active zone proteins Munc13-1 and RIM1 in synaptic vesicle priming. Neuron 30, 183-196.
7. Bratanova-Tochkova TK, Cheng H, Daniel S, Gunawardana S, Liu YJ, Mulvaney-Musa J, Schermerhorn T, Straub SG, Yajima H & Sharp GW (2002). Triggering and augmentation mechanisms, granule pools, and biphasic insulin secretion. Diabetes 51 (Suppl. 1), S83-S90.
8. Burgoyne RD & Morgan A (2003). Secretory granule exocytosis. Physiol Rev 83, 581-632.
9. Cheviet S, Coppola T, Haynes LP, Burgoyne RD & Regazzi R (2004). The Rab-binding protein Noc2 is associated with insulin-containing secretory granules and is essential for pancreatic b-cell exocytosis. Mol Endocrinol 18, 117-126.
10. Coppola T, Frantz C, Perret-Menoud V, Gattesco S, Hirling H & Regazzi R (2002). Pancreatic b-cell protein granuphilin binds Rab3 and Munc-18 and controls exocytosis. Mol Biol Cell 13, 1906-1915.
11. Dean PM (1973). Ultrastructural morphometry of the pancreatic b-cell. Diabetologia 9, 115-119.
12. de Wit H, Cornelisse LN, Toonen RF & Verhage M (2006). Docking of secretory vesicles is syntaxin dependent. PLoS ONE 1, e126.
13. Eliasson L, Renstrom E, Ammala C, Berggren PO, Bertorello AM, Bokvist K, Chibalin A, Deeney JT, Flatt PR, Gabel J, Gromada J, Larsson O, Lindstrom P, Rhodes CJ & Rorsman P (1996). PKC-dependent stimulation of exocytosis by sulfonylureas in pancreatic β cells. Science 271, 813-815.
14. 2+- induced exocytosis in mouse pancreatic β-cells. J Physiol 503, 399-412.
15. Fukuda M (2003). Slp4-a/granuphilin-a inhibits dense-core vesicle exocytosis through interaction with the GDP-bound form of Rab27A in PC12 cells. J Biol Chem 278, 15390-15396.
16. Fukuda M (2005). Versatile role of Rab27 in membrane trafficking: Focus on the Rab27 effector families. J Biochem (Tokyo) 137, 9-16.
17. Fukuda M, Kanno E & Yamamoto A (2004). Rabphilin and Noc2 are recruited to dense-core vesicles through specific interaction with Rab27A in PC12 cells. J Biol Chem 279, 13065-13075.
18. 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.
19. Gillis KD & Misler S (1992). Single cell assay of exocytosis from pancreatic islet β cells. Pflugers Arch 420, 121-123.
20. Gillis KD, Mossner R & Neher E (1996). Protein kinase C enhances exocytosis from chromaffin cells by increasing the size of the readily releasable pool of secretory granules. Neuron 16, 1209-1220.
21. Gomi H, Mizutani S, Kasai K, Itohara S & Izumi T (2005). Granuphilin molecularly docks insulin granules to the fusion machinery. J Cell Biol 171, 99-109.
22. Gromada J, Hoy M, Renstrom E, Bokvist K, Eliasson L, Gopel S & Rorsman P (1999). CaM kinase II-dependent mobilization of secretory granules underlies acetylcholine-induced stimulation of exocytosis in mouse pancreatic β-cells. J Physiol 518, 745-759.
23. Gulyas-Kovacs A, de Wit H, Milosevic I, Kochubey O, Toonen R, Klingauf J, Verhage M & Sorensen JB (2007). Munc18-1: Sequential interactions with the fusion machinery stimulate vesicle docking and priming. J Neurosci 27, 8676-8686.
24. 2+- regulated exocytosis in neuroendocrine cells. J Biol Chem 276, 9726-9732.
25. Holz GG, Chepurny OG & Schwede F (2008). Epac-selective cAMP analogs: New tools with which to evaluate the signal transduction properties of cAMP-regulated guanine nucleotide exchange factors. Cell Signal 20, 10-20.
26. Hume AN, Collinson LM, Rapak A, Gomes AQ, Hopkins CR & Seabra MC (2001). Rab27a regulates the peripheral distribution of melanosomes in melanocytes. J Cell Biol 152, 795-808.
27. Iezzi M, Escher G, Meda P, Charollais A, Baldini G, Darchen F, Wollheim CB & Regazzi R (1999). Subcellular distribution and function of Rab3A, B, C, and D isoforms in insulin-secreting cells. Mol Endocrinol 13, 202-212.
28. Jones PM, Fyles JM & Howell SL (1986). Regulation of insulin secretion by cAMP in rat islets of Langerhans permeabilised by high-voltage discharge. FEBS Lett 205, 205-209.
29. Kang L, He Z, Xu P, Fan J, Betz A, Brose N & Xu T (2006). Munc13-1 is required for the sustained release of insulin from pancreatic β cells. Cell Metab 3, 463-468.
30. 2+ release and exocytosis in pancreatic β-cells. J Biol Chem 278, 8279-8285.
31. Kanno T, Ma X, Barg S, Eliasson L, Galvanovskis J, Gopel S, Larsson M, Renstrom E & Rorsman P (2004). Large dense-core vesicle exocytosis in pancreatic β-cells monitored by capacitance measurements. Methods 33, 302-311.
32. Kasai K, Ohara-Imaizumi M, Takahashi N, Mizutani S, Zhao S, Kikuta T, Kasai H, Nagamatsu S, Gomi H & Izumi T (2005). Rab27a mediates the tight docking of insulin granules onto the plasma membrane during glucose stimulation. J Clin Invest 115, 388-396.
33. - channel current that is activated by cell swelling, cAMP, and glyburide in insulin-secreting cells. Diabetes 44, 1461-1466.
34. Kondo H, Shirakawa R, Higashi T, Kawato M, Fukuda M, Kita T & Horiuchi H (2006). Constitutive GDP/GTP exchange and secretion-dependent GTP hydrolysis activity for Rab27 in platelets. J Biol Chem 281, 28657-28665.
35. Kotake K, Ozaki N, Mizuta M, Sekiya S, Inagaki N & Seino S (1997). Noc2, a putative zinc finger protein involved in exocytosis in endocrine cells. J Biol Chem 272, 29407-29410.
36. Mahoney TR, Liu Q, Itoh T, Luo S, Hadwiger G, Vincent R, Wang ZW, Fukuda M & Nonet ML (2006). Regulation of synaptic transmission by RAB-3 and RAB-27 in Caenorhabditis elegans. Mol Biol Cell 17, 2617-2625.
37. Miley HE, Brown PD & Best L (1999). Regulation of a volume-sensitive anion channel in rat pancreatic β-cells by intracellular adenine nucleotides. J Physiol 515, 413-417.
38. Olofsson CS, Gopel SO, Barg S, Galvanovskis J, Ma X, Salehi A, Rorsman P & Eliasson L (2002). Fast insulin secretion reflects exocytosis of docked granules in mouse pancreatic β-cells. Pflugers Arch 444, 43-51.
39. Renstrom E, Eliasson L & Rorsman P (1997). Protein kinase A-dependent and-independent stimulation of exocytosis by cAMP in mouse pancreatic β-cells. J Physiol 502, 105-118.
40. Rosengren A, Filipsson K, Jing XJ, Reimer MK & Renstrom E (2002). Glucose dependence of insulinotropic actions of pituitary adenylate cyclase-activating polypeptide in insulin-secreting INS-1 cells. Pflugers Arch 444, 556-567.
41. Shibasaki T, Takahashi H, Miki T, Sunaga Y, Matsumura K, Yamanaka M, Zhang C, Tamamoto A, Satoh T, Miyazaki J & Seino S (2007). Essential role of Epac2/Rap1 signaling in regulation of insulin granule dynamics by cAMP. Proc Natl Acad Sci U S A 104, 19333-19338.
42. Stinchcombe JC, Barral DC, Mules EH, Booth S, Hume AN, Machesky LM, Seabra MC & Griffiths GM (2001). Rab27a is required for regulated secretion in cytotoxic T lymphocytes. J Cell Biol 152, 825-834.
43. Straub SG & Sharp GW (2002). Glucose-stimulated signaling pathways in biphasic insulin secretion. Diabetes Metab Res Rev 18, 451-463.
44. Strom M, Hume AN, Tarafder AK, Barkagianni E & Seabra MC (2002). A family of Rab27-binding proteins. Melanophilin links Rab27a and myosin Va function in melanosome transport. J Biol Chem 277, 25423-25430.
45. Takahashi N, Kadowaki T, Yazaki Y, Miyashita Y & Kasai H (1997). Multiple exocytotic pathways in pancreatic β cells. J Cell Biol 138, 55-64.
46. Torii S, Zhao S, Yi Z, Takeuchi T & Izumi T (2002). Granuphilin modulates the exocytosis of secretory granules through interaction with syntaxin 1a. Mol Cell Biol 22, 5518-5526.
47. Tsuboi T & Fukuda M (2006a). Rab3A and Rab27A cooperatively regulate the docking step of dense-core vesicle exocytosis in PC12 cells. J Cell Sci 119, 2196-2203.
48. Tsuboi T & Fukuda M (2006b). The Slp4-a linker domain controls exocytosis through interaction with Munc18-1.syntaxin-1a complex. Mol Biol Cell 17, 2101-2112.
49. Voets T, Toonen RF, Brian EC, de Wit H, Moser T, Rettig J, Sudhof TC, Neher E & Verhage M (2001). Munc18-1 promotes large dense-core vesicle docking. Neuron 31, 581-591.
50. 2+. J Gen Physiol 124, 653-662.
51. Wang X, Thiagarajan R, Wang Q, Tewolde T, Rich MM & Engisch KL (2008). Regulation of quantal shape by Rab3A: Evidence for a fusion pore-dependent mechanism. J Physiol 586, 3949-3962.
52. Waselle L, Coppola T, Fukuda M, Iezzi M, El-Amraoui A, Petit C & Regazzi R (2003). Involvement of the Rab27 binding protein Slac2c/MyRIP in insulin exocytosis. Mol Biol Cell 14, 4103-4113.
53. Wilson SM, Yip R, Swing DA, O'Sullivan TN, Zhang Y, Novak EK, Swank RT, Russell LB, Copeland NG & Jenkins NA (2000). A mutation in Rab27a causes the vesicle transport defects observed in ashen mice. Proc Natl Acad Sci U S A 97, 7933-7938.
54. Wu X, Wang F, Rao K, Sellers JR & Hammer JA 3rd (2002). Rab27a is an essential component of melanosome receptor for myosin Va. Mol Biol Cell 13, 1735-1749.
55. Yaekura K, Julyan R, Wicksteed BL, Hays LB, Alarcon C, Sommers S, Poitout V, Baskin DG, Wang Y, Philipson LH & Rhodes CJ (2003). Insulin secretory deficiency and glucose intolerance in Rab3A null mice. J Biol Chem 278, 9715-9721.
56. 2+-sensitive pool of granules is regulated by glucose and protein kinases in insulin-secreting INS-1 cells. J Gen Physiol 124, 641-651.
57. Yi Z, Yokota H, Torii S, Aoki T, Hosaka M, Zhao S, Takata K, Takeuchi T & Izumi T (2002). The Rab27a/granuphilin complex regulates the exocytosis of insulin-containing dense-core granules. Mol Cell Biol 22, 1858-1867.