Distinct actions of rab3 and rab27 gtpases on late stages of exocytosis of insulin

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Volumn 15, Issue 9, 2014, Pages 997-1015

  Cazares, Victor A ^a,b   Subramani, Arasakumar ^a   Saldate, Johnny J ^a,b   Hoerauf, Widmann ^a,b   Stuenkel, Edward L ^a,b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Exocytosis; GTPase; Insulin secretion; Membrane fusion; Rab proteins

Indexed keywords

INSULIN; NUCLEOTIDE; RAB PROTEIN; RAB27A PROTEIN; GUANOSINE TRIPHOSPHATASE; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN;

ARTICLE; CELL KINETICS; EXOCYTOSIS; HUMAN; INSULIN RELEASE; MEMBRANE FUSION; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SECRETORY GRANULE; SPONTANEOUS MUTATION; ANIMAL; C3H MOUSE; CELL GRANULE; METABOLISM; MOUSE; NUCLEOLUS; PHYSIOLOGY; PROTEIN TRANSPORT; SECRETORY VESICLE;

ANIMALS; CELL NUCLEOLUS; CYTOPLASMIC GRANULES; EXOCYTOSIS; GTP PHOSPHOHYDROLASES; GTPASE-ACTIVATING PROTEINS; INSULIN; INSULIN-SECRETING CELLS; MICE; MICE, INBRED C3H; PROTEIN TRANSPORT; RAB3 GTP-BINDING PROTEINS; SECRETORY VESICLES;

EID: 84906314076     PISSN: 13989219     EISSN: 16000854     Source Type: Journal    
DOI: 10.1111/tra.12182     Document Type: Article

References (105)

1. Porte D, Kahn SE. Beta-cell dysfunction and failure in type 2 diabetes: potential mechanisms. Diabetes 2001;50(Suppl 1):S160-S163.
2. Ashcroft FM, Rorsman P. KATP channels and islet hormone secretion: new insights and controversies. Nat Rev Endocrinol 2013;9:660-669.
3. Henquin JC. Triggering and amplifying pathways of regulation of insulin secretion by glucose. Diabetes 2000;49:1751-1760.
4. Straub SG, Sharp GWG. Glucose-stimulated signaling pathways in biphasic insulin secretion. Diabetes Metab Res Rev 2002;18:451-463.
5. Rutter GA. Visualising insulin secretion. The Minkowski Lecture 2004. Diabetologia 2004;47:1861-1872.
6. MacDonald PE, Joseph JW, Rorsman P. Glucose-sensing mechanisms in pancreatic beta-cells. Philos Trans R Soc Lond B Biol Sci 2005;360:2211-2225.
7. Sadoul K, Lang J, Montecucco C, Weller U, Regazzi R, Catsicas S, Wollheim CB, Halban PA. SNAP-25 is expressed in islets of Langerhans and is involved in insulin release. J Cell Biol 1995;128:1019-1028.
8. Nagamatsu S, Fujiwara T, Nakamichi Y, Watanabe T, Katahira H, Sawa H, Akagawa K. Expression and functional role of syntaxin 1/HPC-1 in pancreatic beta cells. Syntaxin 1A, but not 1B, plays a negative role in regulatory insulin release pathway. J Biol Chem 1996;271:1160-1165.
9. Gaisano HY, Ostenson C-G, Sheu L, Wheeler MB, Efendic S. Abnormal expression of pancreatic islet exocytotic soluble N-ethylmaleimide-sensitive factor attachment protein receptors in Goto-Kakizaki rats is partially restored by phlorizin treatment and accentuated by high glucose treatment. Endocrinology 2002;143:4218-4226.
10. Zerial M, McBride H. Rab proteins as membrane organizers. Nat Rev Mol Cell Biol 2001;2:107-117.
11. Hutagalung AH, Novick PJ. Role of Rab GTPases in membrane traffic and cell physiology. Physiol Rev 2011;91:119-149.
12. Regazzi R, Vallar L, Ullrich S, Ravazzola M, Kikuchi A, Takai Y, Wollheim CB. Characterization of small-molecular-mass guanine-nucleotide-binding regulatory proteins in insulin-secreting cells and PC12 cells. Eur J Biochem 1992;208:729-737.
13. Merrins MJ, Stuenkel EL. Kinetics of Rab27a-dependent actions on vesicle docking and priming in pancreatic beta-cells. J Physiol (Lond) 2008;586:5367-5381.
14. Schlüter OM, Schmitz F, Jahn R, Rosenmund C, Südhof TC. A complete genetic analysis of neuronal Rab3 function. J Neurosci 2004;24:6629-6637.
15. Regazzi R, Ravazzola M, Iezzi M, Lang J, Zahraoui A, Andereggen E, Morel P, Takai Y, Wollheim CB. Expression, localization and functional role of small GTPases of the Rab3 family in insulin-secreting cells. J Cell Sci 1996;109:2265-2273.
16. Coppola T, Perret-Menoud V, Lüthi S, Farnsworth CC, Glomset JA, Regazzi R. Disruption of Rab3-calmodulin interaction, but not other effector interactions, prevents Rab3 inhibition of exocytosis. EMBO J 1999;18:5885-5891.
17. Chung SH, Joberty G, Gelino EA, Macara IG, Holz RW. Comparison of the effects on secretion in chromaffin and PC12 cells of Rab3 family members and mutants. Evidence that inhibitory effects are independent of direct interaction with Rabphilin3. J Biol Chem 1999;274:18113-18120.
18. Fukuda M. Assay and functional interactions of Rim2 with Rab3. Methods Enzymol 2005;403:457-468.
19. Yasuda T, Shibasaki T, Minami K, Takahashi H, Mizoguchi A, Uriu Y, Numata T, Mori Y, Miyazaki J-I, Miki T, Seino S. Rim2a determines docking and priming states in insulin granule exocytosis. Cell Metab 2010;12:117-129.
20. Zhao S, Torii S, Yokota-Hashimoto H, Takeuchi T, Izumi T. Involvement of Rab27b in the regulated secretion of pituitary hormones. Endocrinology 2002;143:1817-1824.
21. Waselle L, Coppola T, Fukuda M, Iezzi 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.
22. Lam AD, Ismail S, Wu R, Yizhar O, Passmore DR, Ernst SA, Stuenkel EL. Mapping dynamic protein interactions to insulin secretory granule behavior with TIRF-FRET. Biophys J 2010;99:1311-1320.
23. Haddad EK, Wu X, Hammer JA, Henkart PA. Defective granule exocytosis in Rab27a-deficient lymphocytes from Ashen mice. J Cell Biol 2001;152:835-842.
24. Kasai K, Ohara-Imaizumi M, Takahashi N, Mizutani S, Zhao S, Kikuta T, Kasai H, Nagamatsu S, Gomi H, Izumi T. Rab27a mediates the tight docking of insulin granules onto the plasma membrane during glucose stimulation. J Clin Invest 2005;115:388-396.
25. 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.
26. Pavlos NJ, Jahn R. Distinct yet overlapping roles of Rab GTPases on synaptic vesicles. Small GTPases 2011;2:77-81.
27. Iezzi M, Escher G, Meda P, Charollais A, Baldini G, Darchen F, Wollheim CB, Regazzi R. Subcellular distribution and function of Rab3A, B, C, and D isoforms in insulin-secreting cells. Mol Endocrinol 1999;13:202-212.
28. Barr F, Lambright DG. Rab GEFs and GAPs. Curr Opin Cell Biol 2010;22:461-470.
29. Figueiredo AC, Wasmeier C, Tarafder AK, Ramalho JS, Baron RA, Seabra MC. Rab3GEP is the non-redundant guanine nucleotide exchange factor for Rab27a in melanocytes. J Biol Chem 2008;283:23209-23216.
30. Tanaka M, Miyoshi J, Ishizaki H, Togawa A, Ohnishi K, Endo K, Matsubara K, Mizoguchi A, Nagano T, Sato M, Sasaki T, Takai Y. Role of Rab3 GDP/GTP exchange protein in synaptic vesicle trafficking at the mouse neuromuscular junction. Mol Biol Cell 2001;12:1421-1430.
31. Itoh T, Fukuda M. Identification of EPI64 as a GTPase-activating protein specific for Rab27A. J Biol Chem 2006;281:31823-31831.
32. Handley MTW, Haynes LP, Burgoyne RD. Differential dynamics of Rab3A and Rab27A on secretory granules. J Cell Sci 2007;120:973-984.
33. 2+-triggered exocytosis. J Neurosci 2010;30:13441-13453.
34. Kimura T, Kaneko Y, Yamada S, Ishihara H, Senda T, Iwamatsu A, Niki I. The GDP-dependent Rab27a effector coronin 3 controls endocytosis of secretory membrane in insulin-secreting cell lines. J Cell Sci 2008;121:3092-3098.
35. Fukuda M. Slp4-a/granuphilin-a inhibits dense-core vesicle exocytosis through interaction with the GDP-bound form of Rab27A in PC12 cells. J Biol Chem 2003;278:15390-15396.
36. Kondo H, Shirakawa R, Higashi T, Kawato M, Fukuda M, Kita T, Horiuchi H. Constitutive GDP/GTP exchange and secretion-dependent GTP hydrolysis activity for Rab27 in platelets. J Biol Chem 2006;281:28657-28665.
37. Fukuda M. Rab27 and its effectors in secretory granule exocytosis: a novel docking machinery composed of a Rab27.effector complex. Biochem Soc Trans 2006;34:691-695.
38. Fukuda M. Distinct Rab binding specificity of Rim1, Rim2, rabphilin, and Noc2. Identification of a critical determinant of Rab3A/Rab27A recognition by Rim2. J Biol Chem 2003;278:15373-15380.
39. Cheviet S, Waselle L, Regazzi R. Noc-king out exocrine and endocrine secretion. Trends Cell Biol 2004;14:525-528.
40. Shirakawa R. Munc13-4 is a GTP-Rab27-binding protein regulating dense core granule secretion in platelets. J Biol Chem 2003;279:10730-10737.
41. Handley MTW, Burgoyne RD. The Rab27 effector Rabphilin, unlike Granuphilin and Noc2, rapidly exchanges between secretory granules and cytosol in PC12 cells. Biochem Biophys Res Commun 2008;373:275-281.
42. Göpel S, Kanno T, Barg S, Galvanovskis J, Rorsman P. Voltage-gated and resting membrane currents recorded from B-cells in intact mouse pancreatic islets. J Physiol (Lond) 1999;521:717-728.
43. Huang Y-C, Rupnik M, Gaisano HY. Unperturbed islet α-cell function examined in mouse pancreas tissue slices. J Physiol (Lond) 2011;589:395-408.
44. Fukui K, Sasaki T, Imazumi K, Matsuura Y, Nakanishi H, Takai Y. Isolation and characterization of a GTPase activating protein specific for the Rab3 subfamily of small G proteins. J Biol Chem 1997;272:4655-4658.
45. Grosshans BL, Andreeva A, Gangar A, Niessen S, Yates JR, Brennwald P, Novick P. The yeast lgl family member Sro7p is an effector of the secretory Rab GTPase Sec4p. J Cell Biol 2006;172:55-66.
46. Tsuboi T, Fukuda M. Rab3A and Rab27A cooperatively regulate the docking step of dense-core vesicle exocytosis in PC12 cells. J Cell Sci 2006;119:2196-2203.
47. Stevens DR, Schirra C, Becherer U, Rettig J. Vesicle pools: lessons from adrenal chromaffin cells. Front Synaptic Neurosci 2011;3:2.
48. Feng W, Liang T, Yu J, Zhou W, Zhang Y, Wu Z, Xu T. RAB-27 and its effector RBF-1 regulate the tethering and docking steps of DCV exocytosis in C. elegans. Sci China Life Sci 2012;55:228-235.
49. Leenders AG, Lopes da Silva FH, Ghijsen WE, Verhage M. Rab3a is involved in transport of synaptic vesicles to the active zone in mouse brain nerve terminals. Mol Biol Cell 2001;12:3095-3102.
50. Coleman WL, Bill CA, Bykhovskaia M. Rab3a deletion reduces vesicle docking and transmitter release at the mouse diaphragm synapse. Neuroscience 2007;148:1-6.
51. 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.
52. Johnson JL, Brzezinska AA, Tolmachova T, Munafo DB, Ellis BA, Seabra MC, Hong H, Catz SD. Rab27a and Rab27b regulate neutrophil azurophilic granule exocytosis and NADPH oxidase activity by independent mechanisms. Traffic 2010;11:533-547.
53. Burke NV, Han W, Li D, Takimoto K, Watkins SC, Levitan ES. Neuronal peptide release is limited by secretory granule mobility. Neuron 1997;19:1095-1102.
54. Oheim M, Loerke D, Stühmer W, Chow RH. The last few milliseconds in the life of a secretory granule. Docking, dynamics and fusion visualized by total internal reflection fluorescence microscopy (TIRFM). Eur Biophys J 1998;27:83-98.
55. Steyer JA, Almers W. Tracking single secretory granules in live chromaffin cells by evanescent-field fluorescence microscopy. Biophys J 1999;76:2262.
56. Johns LM. Restriction of secretory granule motion near the plasma membrane of chromaffin cells. J Cell Biol 2001;153:177-190.
57. Degtyar VE, Allersma MW, Axelrod D, Holz RW. Increased motion and travel, rather than stable docking, characterize the last moments before secretory granule fusion. Proc Natl Acad Sci U S A 2007;104:15929-15934.
58. Straub SG, Shanmugam G, Sharp GWG. Stimulation of insulin release by glucose is associated with an increase in the number of docked granules in the beta-cells of rat pancreatic islets. Diabetes 2004;53:3179-3183.
59. 2+ channels accounts for first-phase insulin secretion in mouse beta-cells. Diabetes 2002;51(Suppl 1):S74-S82.
60. Olofsson CS, Göpel SO, Barg S, Galvanovskis J, Ma X, Salehi A, Rorsman P, Eliasson L. Fast insulin secretion reflects exocytosis of docked granules in mouse pancreatic B-cells. Pflugers Arch 2002;444:43-51.
61. 2+-exocytosis coupling in isolated mouse pancreatic beta cells. Acta Pharmacol Sin 2006;27:933-938.
62. 2+-sensitive pool of granules is regulated by glucose and protein kinases in insulin-secreting INS-1 cells. J Gen Physiol 2004;124:641-651.
63. Regazzi R, Kikuchi A, Takai Y, Wollheim CB. The small GTP-binding proteins in the cytosol of insulin-secreting cells are complexed to GDP dissociation inhibitor proteins. J Biol Chem 1992;267:17512-17519.
64. Reczek D. Identification of EPI64, a TBC/rabGAP domain-containing microvillar protein that binds to the first PDZ domain of EBP50 and E3KARP. J Cell Biol 2001;153:191-206.
65. Malaisse WJ, Malaisse-Lagae F, Mayhew D. A possible role for the adenylcyclase system in insulin secretion. J Clin Invest 1967;46:1724-1734.
66. Montague W, Howell SL. The mode of action of adenosine 3':5'-cyclic monophosphate in mammalian islets of Langerhans. Preparation and properties of islet-cell protein phosphokinase. Biochem J 1972;129:551-560.
67. Pipeleers DG, in't Veld PA, Van de Winkel M, Maes E, Schuit FC, Gepts W. A new in vitro model for the study of pancreatic A and B cells. Endocrinology 1985;117:806-816.
68. Kashima Y, Miki T, Shibasaki T, Ozaki N, Miyazaki M, Yano H, Seino S. Critical role of cAMP-GEFII--Rim2 complex in incretin-potentiated insulin secretion. J Biol Chem 2001;276:46046-46053.
69. 2+ channel in insulin granule exocytosis. J Biol Chem 2004;279:7956-7961.
70. Sakane A, Manabe S, Ishizaki H, Tanaka-Okamoto M, Kiyokage E, Toida K, Yoshida T, Miyoshi J, Kamiya H, Takai Y, Sasaki T. Rab3 GTPase-activating protein regulates synaptic transmission and plasticity through the inactivation of Rab3. Proc Natl Acad Sci U S A 2006;103:10029-10034.
71. Müller M, Liu KSY, Sigrist SJ, Davis GW. RIM controls homeostatic plasticity through modulation of the readily-releasable vesicle pool. J Neurosci 2012;32:16574-16585.
72. Weiss N, Sandoval A, Kyonaka S, Felix R, Mori Y, de Waard M. Rim1 modulates direct G-protein regulation of Ca(v)2.2 channels. Pflugers Arch 2011;461:447-459.
73. 2+ channel density and vesicle docking at the presynaptic active zone. Neuron 2011;69:304-316.
74. 2+ channels to presynaptic active zones via a direct PDZ-domain interaction. Cell 2011;144:282-295.
75. Bustos MA, Lucchesi O, Ruete MC, Mayorga LS, Tomes CN. Rab27 and Rab3 sequentially regulate human sperm dense-core granule exocytosis. Proc Natl Acad Sci U S A 2012;109:E2057-E2066.
76. Tsuboi T, Fukuda M. The Slp4-a linker domain controls exocytosis through interaction with Munc18-1.syntaxin-1a complex. Mol Biol Cell 2006;17:2101-2112.
77. Südhof TC. Function of Rab3 GDP-GTP exchange. Neuron 1997;18:519-522.
78. Fischer von Mollard G, Südhof TC, Jahn R. A small GTP-binding protein dissociates from synaptic vesicles during exocytosis. Nature 1991;349:79-81.
79. Coppola T, Perret-Menoud V, Gattesco S, Magnin S, Pombo I, Blank U, Regazzi R. The death domain of Rab3 guanine nucleotide exchange protein in GDP/GTP exchange activity in living cells. Biochem J 2002;362:273-279.
80. Maycox PR, Link E, Reetz A, Morris SA, Jahn R. Clathrin-coated vesicles in nervous tissue are involved primarily in synaptic vesicle recycling. J Cell Biol 1992;118:1379-1388.
81. Graham ME, Handley MTW, Barclay JW, Ciufo LF, Barrow SL, Morgan A, Burgoyne RD. A gain-of-function mutant of Munc18-1 stimulates secretory granule recruitment and exocytosis and reveals a direct interaction of Munc18-1 with Rab3. Biochem J 2008;409:407-416.
82. Dulubova I, Lou X, Lu J, Huryeva I, Alam A, Schneggenburger R, Südhof TC, Rizo J. A Munc13/RIM/Rab3 tripartite complex: from priming to plasticity? EMBO J 2005;24:2839-2850.
83. Iezzi M, Regazzi R, Wollheim CB. The Rab3-interacting molecule RIM is expressed in pancreatic beta-cells and is implicated in insulin exocytosis. FEBS Lett 2000;474:66-70.
84. 2+ signals in insulin granule exocytosis. Diabetes 2004;53(Suppl 3):S59-S62.
85. Staunton J, Ganetzky B, Nonet ML. Rabphilin potentiates soluble N-ethylmaleimide sensitive factor attachment protein receptor function independently of rab3. J Neurosci 2001;21:9255-9264.
86. Johannes L, Doussau F, Clabecq A, Henry JP, Darchen F, Poulain B. Evidence for a functional link between Rab3 and the SNARE complex. J Cell Sci 1996;109:2875-2884.
87. Henry JP, Johannes L, Dousseau F, Poulain B, Darchen F. Role of Rab3a in neurotransmitter and hormone release: a discussion of recent data. Biochem Soc Trans 1996;24:657-661.
88. Ohya T, Miaczynska M, Coskun U, Lommer B, Runge A, Drechsel D, Kalaidzidis Y, Zerial M. Reconstitution of Rab- and SNARE-dependent membrane fusion by synthetic endosomes. Nature 2009;459:1091-1097.
89. Ohara-Imaizumi M, Nagamatsu S. Insulin exocytotic mechanism by imaging technique. J Biochem 2006;140:1-5.
90. Ohara-Imaizumi M, Fujiwara T, Nakamichi Y, Okamura T, Akimoto Y, Kawai J, Matsushima S, Kawakami H, Watanabe T, Akagawa K, Nagamatsu S. Imaging analysis reveals mechanistic differences between first- and second-phase insulin exocytosis. J Cell Biol 2007;177:695-705.
91. Straub SG, Sharp GWG. Evolving insights regarding mechanisms for the inhibition of insulin release by norepinephrine and heterotrimeric G proteins. Am J Physiol Cell Physiol 2012;302:C1687-C1698.
92. Ohara-Imaizumi M, Nakamichi Y, Tanaka T, Ishida H, Nagamatsu S. Imaging exocytosis of single insulin secretory granules with evanescent wave microscopy: distinct behavior of granule motion in biphasic insulin release. J Biol Chem 2002;277:3805-3808.
93. Ohara-Imaizumi M, Nishiwaki C, Kikuta T, Kumakura K, Nakamichi Y, Nagamatsu S. Site of docking and fusion of insulin secretory granules in live MIN6 beta cells analyzed by TAT-conjugated anti-syntaxin 1 antibody and total internal reflection fluorescence microscopy. J Biol Chem 2004;279:8403-8408.
94. Michael DJ, Xiong W, Geng X, Drain P, Chow RH. Human insulin vesicle dynamics during pulsatile secretion. Diabetes 2007;56:1277-1288.
95. Shibasaki T, Takahashi H, Miki T, Sunaga Y, Matsumura K, Yamanaka M, Zhang C, Tamamoto A, Satoh T, Miyazaki J-I, Seino S. Essential role of Epac2/Rap1 signaling in regulation of insulin granule dynamics by cAMP. Proc Natl Acad Sci U S A 2007;104:19333-19338.
96. Lin C-C, Huang C-C, Lin K-H, Cheng K-H, Yang D-M, Tsai Y-S, Ong R-Y, Huang Y-N, Kao L-S. Visualization of Rab3A dissociation during exocytosis: a study by total internal reflection microscopy. J Cell Physiol 2007;211:316-326.
97. Larijani B, Hume AN, Tarafder AK, Seabra MC. Multiple factors contribute to inefficient prenylation of Rab27a in Rab prenylation diseases. J Biol Chem 2003;278:46798-46804.
98. Tiwari S, Italiano JE, Barral DC, Mules EH, Novak EK, Swank RT, Seabra MC, Shivdasani RA. A role for Rab27b in NF-E2-dependent pathways of platelet formation. Blood 2003;102:3970-3979.
99. 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.
100. 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.
101. Fukuda M. Versatile role of Rab27 in membrane trafficking: focus on the Rab27 effector families. J Biochem 2005;137:9-16.
102. Kimura T, Niki I. Rab27a, actin and beta-cell endocytosis. Endocr J 2011;58:1-6.
103. Kimura T, Taniguchi S, Niki I. Actin assembly controlled by GDP-Rab27a is essential for endocytosis of the insulin secretory membrane. Arch Biochem Biophys 2010;496:33-37.
104. Göpel S, Zhang Q, Eliasson L, Ma X-S, Galvanovskis J, Kanno T, Salehi A, Rorsman P. Capacitance measurements of exocytosis in mouse pancreatic alpha-, beta- and delta-cells within intact islets of Langerhans. J Physiol (Lond) 2004;556:711-726.
105. Allersma MW, Bittner MA, Axelrod D, Holz RW. Motion matters: secretory granule motion adjacent to the plasma membrane and exocytosis. Mol Biol Cell 2006;17:2424-2438.