Annexin I Stimulates Insulin Secretion through Regulation of Cytoskeleton and PKC Activity

  • Kang, Na-Na (Department of Biological Sciences and Institute for Basic Sciences, Sungkyunkwan University) ;
  • Won, Jong-Hak (Department of Pharmacology and Physiology, University of Rochester) ;
  • Park, Young-Min (Department of Biological Sciences and Institute for Basic Sciences, Sungkyunkwan University)
  • 발행 : 2009.03.31

초록

In previous studies, we found that Annexin I (Anx I) was co-secreted with insulin in response to glucose, and that extracellular Anx I stimulated the release of insulin via the Anx I binding site in rat pancreatic islets and the &-cell line. However, the role that Anx I plays in the insulin secretion was not established. Therefore, in this study, we evaluated the insulin secretion pattern in response to Anx I and the involvement of the cytoskeleton or PKC in Anx Istimulated insulin secretion in MIN6N8a cells. The peak time of insulin secretion in response to Anx I treatment corresponded with the second phase insulin secretion by glucose in the perifused pseudoislets. In addition, Anx I-stimulated insulin secretion was not affect by readily releasable pool depletion. Taken together, these findings indicate that Anx I treatment was associated with movement of the reserve pool of insulin. Furthermore, Anx I-stimulated insulin secretion was attenuated by treatment with a microfilament inhibitor, cytochalasin B, as well as by PKC down regulation. These results indicate that Anx I may be a regulator of second phase insulin secretion.

키워드

참고문헌

  1. Ammala C, Eliasson L, Bokvist K, Larsson O, Ashcroft FM, and Rorsman P (1993) Exocytosis elicited by action potentials and voltage-clamp calcium currents in individual mouse pancreatic B-cells. J Physiol 472: 665-88 https://doi.org/10.1113/jphysiol.1993.sp019966
  2. Aunis D and Bader MF (1988) The cytoskeleton as a barrier to exocytosis in secretory cells. J Exp Biol 139: 253-66
  3. Bader MF, Doussau F, Chasserot-Golaz S, Vitale N, and Gasman S (2004) Coupling actin and membrane dynamics during calcium-regulated exocytosis: a role for Rho and ARF GTPases. Biochim Biophys Acta 1742: 37-49 https://doi.org/10.1016/j.bbamcr.2004.09.028
  4. Bratanova-Tochkova TK, Cheng H, Daniel S, Gunawardana S, Liu YJ, Mulvaney-Musa J, Schermerhorn T, Straub SG, Yajima H, and Sharp GW (2002) Triggering and augmentation mechanisms, granule pools, and biphasic insulin secretion. Diabetes 51 Suppl 1: S83-90 https://doi.org/10.2337/diabetes.51.2007.S83
  5. Christian HC, Taylor AD, Flower RJ, Morris JF, and Buckingham JC (1997) Characterization and localization of lipocortin 1-binding sites on rat anterior pituitary cells by fluorescenceactivated cell analysis/sorting and electron microscopy. Endocrinology 138: 5341-51 https://doi.org/10.1210/en.138.12.5341
  6. Curry DL, Bennett LL, and Grodsky GM (1968) Dynamics of insulin secretion by the perfused rat pancreas. Endocrinology 83: 572-84 https://doi.org/10.1210/endo-83-3-572
  7. Easom RA (2000) Beta-granule transport and exocytosis. Semin Cell Dev Biol 11: 253-66 https://doi.org/10.1006/scdb.2000.0174
  8. Eitzen G (2003) Actin remodeling to facilitate membrane fusion. Biochim Biophys Acta 1641: 175-81 https://doi.org/10.1016/S0167-4889(03)00087-9
  9. Forscher P and Smith SJ (1988) Actions of cytochalasins on the organization of actin filaments and microtubules in a neuronal growth cone. J Cell Biol 107: 1505-16 https://doi.org/10.1083/jcb.107.4.1505
  10. Ganesan S, Calle R, Zawalich K, Greenawalt K, Zawalich W, Shulman GI, and Rasmussen H (1992) Immunocytochemical localization of alpha-protein kinase C in rat pancreatic betacellsduring glucose-induced insulin secretion. J Cell Biol 119: 313-24 https://doi.org/10.1083/jcb.119.2.313
  11. Ganesan S, Calle R, Zawalich K, Smallwood JI, Zawalich WS, and Rasmussen H (1990) Glucose-induced translocation of protein kinase C in rat pancreatic islets. Proc Natl Acad Sci USA 87: 9893-7 https://doi.org/10.1073/pnas.87.24.9893
  12. Gasman S, Chasserot-Golaz S, Malacombe M, Way M, and Bader MF (2004) Regulated exocytosis in neuroendocrine cells: a role for subplasmalemmal Cdc42/N-WASP-induced actin filaments. Mol Biol Cell 15: 520-31 https://doi.org/10.1091/mbc.E03-06-0402
  13. Gerke V and Moss SE (2002) Annexins: from structure to function. Physiol Rev 82: 331-71 https://doi.org/10.1152/physrev.00030.2001
  14. Gilon P, Jonas JC, and Henquin JC (1994) Culture duration and conditions affect the oscillations of cytoplasmic calcium concentration induced by glucose in mouse pancreatic islets. Diabetologia 37: 1007-14 https://doi.org/10.1007/BF00400464
  15. Grodsky GM, Epstein GH, Fanska R, and Karam JH (1977) Pancreatic action of the sulfonylureas. Fed Proc 36: 2714-9
  16. Gylfe E, Grapengiesser E, and Hellman B (1991) Propagation of cytoplasmic Ca2+ oscillations in clusters of pancreatic betacells exposed to glucose. Cell Calcium 12: 229-40 https://doi.org/10.1016/0143-4160(91)90023-8
  17. Hao M, Li X, Rizzo MA, Rocheleau JV, Dawant BM, and Piston DW (2005) Regulation of two insulin granule populations within the reserve pool by distinct calcium sources. J Cell Sci 118: 5873-84 https://doi.org/10.1242/jcs.02684
  18. Hauge-Evans AC, Squires PE, Persaud SJ, and Jones PM (1999) Pancreatic beta-cell-to-beta-cell interactions are required for integrated responses to nutrient stimuli: enhanced Ca2+ and insulin secretory responses of MIN6 pseudoislets. Diabetes 48: 1402-8 https://doi.org/10.2337/diabetes.48.7.1402
  19. Henquin JC (2000) Triggering and amplifying pathways of regulation of insulin secretion by glucose. Diabetes 49: 1751-60 https://doi.org/10.2337/diabetes.49.11.1751
  20. Hong SH, Won JH, Yoo SA, Auh CK, and Park YM (2002) Effect of annexin I on insulin secretion through surface binding sites in rat pancreatic islets. FEBS Lett 532: 17-20 https://doi.org/10.1016/S0014-5793(02)03613-X
  21. Huang KS, Wallner BP, Mattaliano RJ, Tizard R, Burne C, Frey A, Hession C, McGray P, Sinclair LK, Chow EP, and et al. (1986) Two human 35 kd inhibitors of phospholipase A2 are related to substrates of pp60v-src and of the epidermal growth factor receptor/kinase. Cell 46: 191-9 https://doi.org/10.1016/0092-8674(86)90736-1
  22. Iino S, Sudo T, Niwa T, Fukasawa T, Hidaka H, and Niki I (2000) Annexin XI may be involved in Ca2+ - or GTP-gammaSinduced insulin secretion in the pancreatic beta-cell. FEBS Lett 479: 46-50 https://doi.org/10.1016/S0014-5793(00)01877-9
  23. Kekow J, Ulrichs K, Muller-Ruchholtz W, and Gross WL (1988) Measurement of rat insulin. Enzyme-linked immunosorbent assay with increased sensitivity, high accuracy, and greater practicability than established radioimmunoassay. Diabetes 37: 321-6 https://doi.org/10.2337/diabetes.37.3.321
  24. Lang J (1999) Molecular mechanisms and regulation of insulin exocytosis as a paradigm of endocrine secretion. Eur J Biochem 259: 3-17 https://doi.org/10.1046/j.1432-1327.1999.00043.x
  25. Li G, Rungger-Brandle E, Just I, Jonas JC, Aktories K, and Wollheim CB (1994) Effect of disruption of actin filaments by Clostridium botulinum C2 toxin on insulin secretion in HITT15 cells and pancreatic islets. Mol Biol Cell 5: 1199-213 https://doi.org/10.1091/mbc.5.11.1199
  26. Lim LH, Solito E, Russo-Marie F, Flower RJ, and Perretti M (1998) Promoting detachment of neutrophils adherent to murine postcapillary venules to control inflammation: effect of lipocortin 1. Proc Natl Acad Sci USA 95: 14535-9 https://doi.org/10.1073/pnas.95.24.14535
  27. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65: 55-63 https://doi.org/10.1016/0022-1759(83)90303-4
  28. Nesher R, Anteby E, Yedovizky M, Warwar N, Kaiser N, and Cerasi E (2002) Beta-cell protein kinases and the dynamics of the insulin response to glucose. Diabetes 51 Suppl 1: S68-73 https://doi.org/10.2337/diabetes.51.2007.S68
  29. Park YS, Hur EM, Choi BH, Kwak E, Jun DJ, Park SJ, and Kim KT (2006) Involvement of protein kinase C-epsilon in activity-dependent potentiation of large dense-core vesicle exocytosis in chromaffin cells. J Neurosci 26: 8999-9005 https://doi.org/10.1523/JNEUROSCI.2828-06.2006
  30. Parsons TD, Coorssen JR, Horstmann H, and Almers W (1995) Docked granules, the exocytic burst, and the need for ATP hydrolysis in endocrine cells. Neuron 15: 1085-96 https://doi.org/10.1016/0896-6273(95)90097-7
  31. Perretti M, Croxtall JD, Wheller SK, Goulding NJ, Hannon R, and Flower RJ (1996) Mobilizing lipocortin 1 in adherent human leukocytes downregulates their transmigration. Nat Med 2: 1259-62 https://doi.org/10.1038/nm1196-1259
  32. Perretti M and Flower RJ (1996) Measurement of lipocortin 1 levels in murine peripheral blood leukocytes by flow cytometry: modulation by glucocorticoids and inflammation. Br J Pharmacol 118: 605-10 https://doi.org/10.1111/j.1476-5381.1996.tb15444.x
  33. Prentki M and Matschinsky FM (1987) Ca2+, cAMP, and phospholipid-derived messengers in coupling mechanisms of insulin secretion. Physiol Rev 67: 1185-248 https://doi.org/10.1152/physrev.1987.67.4.1185
  34. Rorsman P (1997) The pancreatic beta-cell as a fuel sensor: an electrophysiologist's viewpoint. Diabetologia 40: 487-95 https://doi.org/10.1007/s001250050706
  35. Rorsman P, Eliasson L, Renstrom E, Gromada J, Barg S, and Gopel S (2000) The Cell Physiology of Biphasic Insulin Secretion. News Physiol Sci 15: 72-77
  36. Rorsman P and Renstrom E (2003) Insulin granule dynamics in pancreatic beta cells. Diabetologia 46: 1029-45 https://doi.org/10.1007/s00125-003-1153-1
  37. Sharp GW (1979) The adenylate cyclase-cyclic AMP system in islets of Langerhans and its role in the control of insulin release. Diabetologia 16: 287-96 https://doi.org/10.1007/BF01223617
  38. Smith SJ (1988) Neuronal cytomechanics: the actin-based motility of growth cones. Science 242: 708-15 https://doi.org/10.1126/science.3055292
  39. Squires PE, Hauge-Evans AC, Persaud SJ, and Jones PM (2000) Synchronization of Ca(2+)-signals within insulin-secreting pseudoislets: effects of gap-junctional uncouplers. Cell Calcium 27: 287-96 https://doi.org/10.1054/ceca.2000.0117
  40. Srivastava M, Atwater I, Glasman M, Leighton X, Goping G, Caohuy H, Miller G, Pichel J, Westphal H, Mears D, Rojas E, and Pollard HB (1999) Defects in inositol 1,4,5-trisphosphate receptor expression, Ca(2+) signaling, and insulin secretion in the anx7(+/-) knockout mouse. Proc Natl Acad Sci USA 96: 13783-8 https://doi.org/10.1073/pnas.96.24.13783
  41. Straub SG and Sharp GW (2004) Hypothesis: one rate-limiting step controls the magnitude of both phases of glucosestimulated insulin secretion. Am J Physiol Cell Physiol 287: C565-71 https://doi.org/10.1152/ajpcell.00079.2004
  42. Sun HQ, Yamamoto M, Mejillano M, and Yin HL (1999) Gelsolin, a multifunctional actin regulatory protein. J Biol Chem 274: 33179-82 https://doi.org/10.1074/jbc.274.47.33179
  43. Taylor AD, Flower RJ, and Buckingham JC (1995) Dexamethasone inhibits the release of TSH from the rat anterior pituitary gland in vitro by mechanisms dependent on de novo protein synthesis and lipocortin 1. J Endocrinol 147: 533-44 https://doi.org/10.1677/joe.0.1470533
  44. Thurmond DC, Gonelle-Gispert C, Furukawa M, Halban PA, and Pessin JE (2003) 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: 732-42 https://doi.org/10.1210/me.2002-0333
  45. Trifaro JM, Gasman S, and Gutierrez LM (2008) Cytoskeletal control of vesicle transport and exocytosis in chromaffin cells. Acta Physiol (Oxf) 192: 165-172 https://doi.org/10.1111/j.1748-1716.2007.01808.x
  46. Trifaro JM, Lejen T, Rose SD, Pene TD, Barkar ND, and Seward EP (2002) Pathways that control cortical F-actin dynamics during secretion. Neurochem Res 27: 1371-85 https://doi.org/10.1023/A:1021627800918
  47. Vadakekalam J, Rabaglia ME, Chen QH, and Metz SA (1996) Role for GTP in glucose-induced phospholipase C activation in pancreatic islets. Am J Physiol 271: E85-95 https://doi.org/10.1152/ajpcell.1996.271.1.C85
  48. Valdeolmillos M, Nadal A, Soria B, and Garcia-Sancho J (1993) Fluorescence digital image analysis of glucose-induced [Ca2+]i oscillations in mouse pancreatic islets of Langerhans. Diabetes 42: 1210-4 https://doi.org/10.2337/diabetes.42.8.1210
  49. Vitale ML, Seward EP, and Trifaro JM (1995) Chromaffin cell cortical actin network dynamics control the size of the release-ready vesicle pool and the initial rate of exocytosis. Neuron 14: 353-63 https://doi.org/10.1016/0896-6273(95)90291-0
  50. Wasmeier C and Hutton JC (2001) Secretagogue-dependent phosphorylation of the insulin granule membrane protein phogrin is mediated by cAMP-dependent protein kinase. J Biol Chem 276: 31919-28 https://doi.org/10.1074/jbc.M102580200
  51. Wilson JR, Ludowyke RI, and Biden TJ (2001) A redistribution of actin and myosin IIA accompanies Ca(2+)-dependent insulin secretion. FEBS Lett 492: 101-6 https://doi.org/10.1016/S0014-5793(01)02241-4
  52. Won JH, Kang NN, Auh CK, and Park YM (2003) The surface receptor is involved in annexin I-stimulated insulin secretion in MIN6N8a cells. BBRC 307: 389-394 https://doi.org/10.1016/S0006-291X(03)01197-5
  53. Yagi N, Yokono K, Amano K, Nagata M, Tsukamoto K, Hasegawa Y, Yoneda R, Okamoto N, Moriyama H, Miki M, and et al. (1995) Expression of intercellular adhesion molecule 1 on pancreatic beta-cells accelerates beta-cell destruction by cytotoxic T-cells in murine autoimmune diabetes. Diabetes 44: 744-52 https://doi.org/10.2337/diabetes.44.7.744
  54. Yu W, Niwa T, Fukasawa T, Hidaka H, Senda T, Sasaki Y, and Niki I (2000) Synergism of protein kinase A, protein kinase C, and myosin light-chain kinase in the secretory cascade of the pancreatic beta-cell. Diabetes 49: 945-52 https://doi.org/10.2337/diabetes.49.6.945
  55. Zawalich WS, Bonnet-Eymard M, and Zawalich KC (2000) Insulin secretion, inositol phosphate levels, and phospholipase C isozymes in rodent pancreatic islets. Metabolism 49: 1156-63 https://doi.org/10.1053/meta.2000.8613
  56. Zawalich WS, Zawalich KC, Ganesan S, Calle R, and Rasmussen H (1991) Influence of staurosporine on glucose-mediated and glucose-conditioned insulin secretion. Biochem J 279 (Pt 3): 807-13 https://doi.org/10.1042/bj2790807
  57. Zawalich WS, Zawalich KC, and Kelley GG (1995) Regulation of insulin release by phospholipase C activation in mouse islets: differential effects of glucose and neurohumoral stimulation. Endocrinology 136: 4903-9 https://doi.org/10.1210/en.136.11.4903