Imaging analysis reveals mechanistic differences between first- and second-phase insulin exocytosis

Journal of Cell Biology

Volumn 177, Issue 4, 2007, Pages 695-705

  Ohara Imaizumi, Mica ^a   Fujiwara, Tomonori ^a   Nakamichi, Yoko ^a   Okamura, Tadashi ^b   Akimoto, Yoshihiro ^a   Kawai, Junko ^a,c   Matsushima, Satsuki ^a   Kawakami, Hayato ^a   Watanabe, Takashi ^a   Akagawa, Kimio ^a   Nagamatsu, Shinya ^a  

^a KYORIN UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b NATIONAL CENTER FOR GLOBAL HEALTH AND MEDICINE   (Japan)

^c JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

INSULIN; SYNTAXIN; SYNTAXIN 1A; SYNTAXIN 3; SYNTAXIN 4; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; EXOCYTOSIS; FLUORESCENCE ANALYSIS; INSULIN RELEASE; KNOCKOUT MOUSE; MALE; MEMBRANE FUSION; MOLECULAR IMAGING; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION;

ANIMALS; CELLS, CULTURED; EXOCYTOSIS; INSULIN; ISLETS OF LANGERHANS; MALE; MICE; MICE, KNOCKOUT; MICROSCOPY, FLUORESCENCE;

MUS;

EID: 34249103872     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200608132     Document Type: Article

References (44)

1. Akimoto, Y., L.K. Kreppel, H. Hirano, and G.W. Hart. 1999. Localization of the O-linked N-acetylglucosamine transferase in rat pancreas. Diabetes. 48:2407-2413.
2. Bennett, M.K., N. Calakos, and R.H. Scheller. 1992. Syntaxin: a synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones. Science. 257:255-259.
3. Cerasi, E. 1994. Aetiology of type II diabetes. In Insulin-Molecular Biology to Pathology. F.M. Ashcroft and S.J.H. Ashcroft, editors. IRL Press, Oxford, England. 352-392.
4. Cherniske, E.M., T.O. Carpenter, C. Klaiman, E. Young, J. Bregman, K. Insogna, R.T. Schultz, and B.R. Pober. 2004. Multisystem study of 20 older adults with Williams syndrome. Am. J. Med. Genet. A. 131:255-264.
5. Curry, D.L., L.L. Bennett, and G.M. Grodsky. 1968. Dynamics of insulin secretion by the perfused rat pancreas. Endocrinology. 83:572-584.
6. Ewart, A.K., C.A. Morris, D. Atkinson, W. Jim, K. Sternes, P. Spallone, A.D. Stock, M. Leppert, and M.T. Keating. 1993. Hemizygosity at the elastin locus in a developmental disorder, Williams syndrome. Nat. Genet. 5:11-16.
7. Fujiwara, T., T. Mishima, T. Kofuji, T. Chiba, K. Tanaka, A. Yamamoto, and K. Akagawa. 2006. Analysis of knockout mice to determine the role of HPC-1/syntaxin 1A in expressing synaptic plasticity. J. Neurosci. 26:5767-5776.
8. Gaisano, H.Y., C.G. Ostenson, L. Sheu, M.B. Wheeler, and S. Efendic. 2002. Abnormal expression of pancreatic islet exocytotic soluble N-ethylmaleimide-sensitive factor attachment protein receptors in Goto-Kakizaki rats in partially restored by phlorizin treatment and accentuated by high glucose treatment. Endocrinology. 143:4218-4226.
9. Henquin, J.C. 2000. Triggering and amplifying pathways of regulation of insulin secretion by glucose. Diabetes. 49:1751-1760.
10. Inoue, A., K. Obata, and K. Akagawa. 1992. Cloning and sequence analysis of cDNA for a neuronal cell membrane antigen, HPC-1. J. Biol. Chem. 267:10613-10619.
11. Jacobsson, G., A.J. Bean, R.H. Scheller, L. Juntti-Berggren, J.T. Deeney, P.O. Berggren, and B. Meister. 1994. Identification of synaptic proteins and their isoform mRNAs in compartments of pancreatic endocrine cells. Proc. Natl. Acad. Sci. USA. 91:12487-12491.
12. Jahn, R., and T.C. Südhof. 1999. Membrane fusion and exocytosis. Annu. Rev. Biochem. 68:863-911.
13. Jahn, R., T. Lang, and T.C. Südhof. 2003. Membrane fusion. Cell. 112:519-533.
14. Kang, Y., X. Huang, E.A. Pasyk, J. Ji, G.G. Holz, M.B. Wheeler, R.G. Tsushima, and H.Y. Gaisano. 2002. Syntaxin-3 and syntaxin-1A inhibit L-type calcium channel activity, insulin biosynthesis and exocytosis in beta-cell lines. Diabetologia. 45:231-241.
15. Lam, P.P., Y.M. Leung, L. Sheu, J. Ellis, R.G. Tsushima, L.R. Osborne, and H.Y. Gaisano. 2005. Transgenic mouse overexpressing syntaxin-1A as a diabetes model. Diabetes. 54:2744-2754.
16. Lang, T., M. Margittai, H. Holzler, and R. Jahn. 2002. SNAREs in native plasma membranes are active and readily form core complexes with endogenous and exogenous SNAREs. J. Cell Biol. 158:751-760.
17. Lizunov, V.A., H. Matsumoto, J. Zimmerberg, S.W. Cushman, and V.A. Frolov. 2005. Insulin stimulates the halting, tethering, and fusion of mobile GLUT4 vesicles in rat adipose cells. J. Cell Biol. 169:481-489.
18. Morris, C.A., S.A. Demsey, C.O. Leorard, C. Dilts, and B.L. Blackburn. 1988. Natural history of Williams syndrome: physical characteristics. J. Pediatr. 113:318-326.
19. Nagamatsu, S., T. Fujiwara, Y. Nakamichi, T. Watanabe, H. Katahira, H. Sawa, and K. Akagawa. 1996. Expression and functional role of syntaxin 1/HPC-1 in pancreatic β cells. J. Biol. Chem. 271:1160-1165.
20. Nagamatsu, S., Y. Nakamichi, C. Yamamura, S. Matsushima, T. Watanabe, S. Ozawa, H. Furukawa, and H. Ishida. 1999. Decreased expression of t-SNARE, syntaxin 1 and SNAP-25 in pancreatic beta-cells is involved in impaired insulin secretion from diabetic GK rat islets: restoration of decreased t-SNARE proteins improves impaired insulin secretion. Diabetes. 48:2367-2373.
21. O'Connor, V., C. Heuss, W.M. De Bello, T. Dresbach, M.P. Charlton, J.H. Hunt, L.L. Pellegrini, A. Hodel, M.M. Burger, H. Betz, et al. 1997. Disruption of syntaxin-mediated protein interactions blocks neurotransmitter secretion. Proc. Natl. Acad. Sci. USA. 94:12186-12191.
22. Ohara-Imaizumi, M., Y. Nakamichi, T. Tanaka, H. Ishida, and S. Nagamatsu. 2002a. Imaging exocytosis of single insulin secretory granules with evanescent wave microscopy: distinct behavior of granule motion in biphasic insulin release. J. Biol. Chem. 277:3805-3808.
23. Ohara-Imaizumi, M., Y. Nakamichi, C. Nishiwaki, and S. Nagamatsu. 2002b. Transduction of MIN6 beta cells with TAT-syntaxin SNARE motif inhibits insulin exocytosis in biphasic insulin release in a distinct mechanism analyzed by evanescent wave microscopy. J. Biol. Chem. 277:50805-50811.
24. Ohara-Imaizumi, M., C. Nishiwaki, T. Kikuta, K. Kumakura, Y. Nakamichi, and S. Nagamatsu. 2004a. 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. 279:8403-8408.
25. Ohara-Imaizumi, M., C. Nishiwaki, T. Kikuta, S. Nagai, Y. Nakamichi, and S. Nagamatsu. 2004b. TIRF imaging of docking and fusion of single insulin granule motion in primary rat pancreatic beta-cells: different behaviour of granule motion between normal and Goto-Kakizaki diabetic rat beta-cells. Biochem. J. 381:13-18.
26. Ohara-Imaizumi, M., T. Ohtsuka, S. Matsushima, Y. Akimoto, C. Nishiwaki, Y. Nakamichi, T. Kikuta, S. Nagai, H. Kawakami, T. Watanabe, and S. Nagamatsu. 2005. ELKS, a protein structurally related to the active zone-associated protein CAST, is expressed in pancreatic beta cells and functions in insulin exocytosis: interaction of ELKS with exocytotic microscopy. Mol. Biol. Cell. 16:3289-3300.
27. O'Rahilly, S.P., A.S. Rudenski, M.A. Burnett, Z. Nugent, J.P. Hosker, and P. Darling. 1986. Beta-cell dysfunction rather than insulin insensitivity is the primary defect in familial type 2 diabetes. Lancet. 2:360-364.
28. Osborne, L.R., S. Soder, X.M. Shi, B. Pober, T. Costa, S.W. Scherer, and L.C. Tsui. 1997. Hemizygous deletion of the syntaxin 1A gene in individuals with Williams syndrome. Am. J. Hum. Genet. 61:449-452.
29. Ostenson, C.G., A. Khan, S.M. Abdel-Halim, A. Guenifi , K. Suzuki, Y. Goto, and S. Efendic. 1993. Abnormal insulin secretion and glucose metabolism in pancreatic islets from the spontaneously diabetic GK rat. Diabetologia. 36:3-8.
30. Ostenson, C.G., H. Gaisano, L. Sheu, A. Tibell, and T. Bartfai. 2006. Impaired gene and protein expression of exocytotic soluble N-ethylmaleimide attachment protein receptor complex proteins in pancreatic islets of type 2 diabetic patients. Diabetes. 55:435-440.
31. Parsons, T.D., J.R. Coorssen, H. Horstmann, and W. Almers. 1995. Docked granules, the exocytic burst, and the need for ATP hydrolysis in endocrine cells. Neuron. 15:1085-1096.
32. Rorsman, P., and E. Renstrom. 2003. Insulin granule dynamics in pancreatic beta cells. Diabetologia. 46:1029-1045.
33. Rorsman, P., L. Eliasson, E. Renstrom, J. Gromada, S. Barg, and S. Gopel. 2000. The cell physiology of biphasic insulin secretion. News Physiol. Sci. 15:72-77.
34. Saito, T., S. Okada, E. Yamada, K. Ohshima, H. Shimizu, K. Shimomura, M. Sato, J.E. Pessin, and M. Mori. 2003. Syntaxin 4 and Synip (syntaxin 4 interacting protein) regulate insulin secretion in the pancreatic βHC-9 cell. J. Biol. Chem. 278:36718-36725.
35. Schoch, S., F. Deaf, A. Konigstorfer, M. Mozhayeva, Y. Sara, T.C. Südhof, and E.T. Kavalali. 2001. SNARE function analyzed in synaptobrevin/VAMP knockout mice. Science. 294:1117-1122.
36. Spurlin, B.A., and D.C. Thurmond. 2006. Syntaxin 4 facilitates biphasic glucose-stimulated insulin secretion from pancreatic beta-cells. Mol. Endocrinol. 20:183-193.
37. Südhof, T.C. 2004. The synaptic vesicle cycle. Annu. Rev. Neurosci. 27:509-547.
38. Ward, W.K., D.C. Bolgiano, B. McKnight, J.B. Halter, and D. Porte Jr. 1984. Diminished β-cell secretory capacity in patients with non-insulin dependent diabetes mellitus. J. Clin. Invest. 74:1318-1328.
39. Washbourne, P., P.M. Thompson, M. Carta, E.T. Costa, J.R. Mathews, G. Lopez-Bendito, Z. Molnar, M.W. Becher, C.F. Valenzuela, L.D. Partridge, and M.C. Wilson. 2002. Genetic ablation of the t-SNARE SNAP-25 distinguishes mechanisms of neuroexocytosis. Nat. Neurosci. 5:19-26.
40. Wheeler, M.B., L. Sheu, M. Ghai, A. Bouquillon, G. Grondin, U. Waller, A.R. Beaudoin, M.K. Bennett, W.S. Trimble, and H.Y. Gaisano. 1996. Characterization of SNARE protein expression in β cell lines and pancreatic islets. Endocrinology. 137:1340-1348.
41. 2+ channels in pancreatic beta cells. Proc. Natl. Acad. Sci. USA. 96:10164-10169.
42. Zenisek, D., J.A. Steyer, and W. Almers. 2000. Transport, capture and exocytosis of single synaptic vesicles at active zones. Nature. 406:849-854.
43. Zhang, W., A. Khan, C.G. Ostenson, P.O. Berggren, S. Efendic, and B. Meister. 2002. Down-regulated expression of exocytotic proteins in pancreatic islets of diabetic GK rats. Biochem. Biophys. Res. Commun. 291:1038-1044.
44. Zhong, P., Y.A. Chen, D. Tam, D. Chung, R.H. Scheller, and G.P. Miljanich. 1997. An alpha-helical minimal binding domain within the H3 domain of syntaxin is required for SNAP-25 binding. Biochemistry. 36:4317-4326.