Insulin secretion induced by glucose-dependent insulinotropic polypeptide requires phosphatidylinositol 3-kinase γ in rodent and human β-cells

Journal of Biological Chemistry

Volumn 289, Issue 46, 2014, Pages 32109-32120

  Kolic, Jelena ^a   Spigelman, Aliya F ^a   Smith, Alannah M ^a   Fox, Jocelyn E Manning ^a   MacDonald, Patrick E ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; CYTOLOGY; ENZYMES; GLUCOSE; INSULIN; PEPTIDES; PHYSIOLOGY;

CATALYTIC SUBUNITS; GLUCAGON-LIKE PEPTIDE-1; HUMAN ISLETS; INSULIN SECRETION; LATRUNCULIN B; PHOSPHATIDYLINOSITOL 3-KINASE; RECEPTOR ACTIVATION; SMALL GTPASE;

PROTEINS;

GASTRIC INHIBITORY POLYPEPTIDE; PHOSPHATIDYLINOSITOL 3 KINASE GAMMA; PROTEIN P110; RAC1 PROTEIN; 1,3 DIOXOLANE DERIVATIVE; 2,4 THIAZOLIDINEDIONE DERIVATIVE; 5-(2,2-DIFLUOROBENZO(1,3)DIOXOL-5-YLMETHYLENE)THIAZOLIDINE-2,4-DIONE; ACTIN; GLUCOSE; INSULIN; NEUROPEPTIDE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE 3 KINASE; RAC1 PROTEIN, MOUSE;

ADULT; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DEPOLYMERIZATION; ENZYME ACTIVATION; EXOCYTOSIS; HUMAN; HUMAN CELL; IMMUNOBLOTTING; INSULIN LIKE ACTIVITY; INSULIN RELEASE; MALE; MIDDLE AGED; MOUSE; NONHUMAN; PANCREAS ISLET BETA CELL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; ANIMAL; C57BL MOUSE; CHEMISTRY; ELECTROPHYSIOLOGY; GENE EXPRESSION REGULATION; IC50; METABOLISM; NON INSULIN DEPENDENT DIABETES MELLITUS; PANCREAS ISLET; PROTEIN TERTIARY STRUCTURE; SECRETION (PROCESS);

RODENTIA;

ACTINS; ANIMALS; CLASS IB PHOSPHATIDYLINOSITOL 3-KINASE; DIABETES MELLITUS, TYPE 2; DIOXOLES; ELECTROPHYSIOLOGY; EXOCYTOSIS; GASTRIC INHIBITORY POLYPEPTIDE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GLUCOSE; HUMANS; INHIBITORY CONCENTRATION 50; INSULIN; INSULIN-SECRETING CELLS; ISLETS OF LANGERHANS; MALE; MICE; MICE, INBRED C57BL; MIDDLE AGED; NEUROPEPTIDES; PROTEIN STRUCTURE, TERTIARY; RAC1 GTP-BINDING PROTEIN; THIAZOLIDINEDIONES;

EID: 84911127363     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.577510     Document Type: Article

References (59)

1. Thorens, B., Porret, A., Bühler, L., Deng, S. P., Morel, P., and Widmann, C. (1993) Cloning and functional expression of the human islet GLP-1 receptor: demonstration that exendin-4 is an agonist and exendin-(9-39) an antagonist of the receptor. Diabetes 42, 1678-1682
2. Dillon, J. S., Tanizawa, Y., Wheeler, M. B., Leng, X. H., Ligon, B. B., Rabin, D. U., Yoo-Warren, H., Permutt, M. A., and Boyd, A. E. (1993) Cloning and functional expression of the human glucagon-like peptide-1 (GLP-1) receptor. Endocrinology 133, 1907-1910
3. Volz, A., Göke, R., Lankat-Buttgereit, B., Fehmann, H. C., Bode, H. P., and Göke, B. (1995) Molecular cloning, functional expression, and signal transduction of the GIP-receptor cloned from a human insulinoma. FEBS Lett. 373, 23-29
4. Usdin, T. B., Mezey, E., Button, D. C., Brownstein, M. J., and Bonner, T. I. (1993) Gastric inhibitory polypeptide receptor, a member of the secretinvasoactive intestinal peptide receptor family, is widely distributed in peripheral organs and the brain. Endocrinology 133, 2861-2870
5. Gremlich, S., Porret, A., Hani, E. H., Cherif, D., Vionnet, N., Froguel, P., and Thorens, B. (1995) Cloning, functional expression, and chromosomal localization of the human pancreatic islet glucose-dependent insulinotropic polypeptide receptor. Diabetes 44, 1202-1208
6. Pederson, R. A., and Brown, J. C. (1976) The insulinotropic action of gastric inhibitory polypeptide in the perfused isolated rat pancreas. Endocrinology 99, 780-785
7. Mojsov, S., Weir, G. C., and Habener, J. F. (1987) Insulinotropin: glucagonlike peptide I (7-37) co-encoded in the glucagon gene is a potent stimulator of insulin release in the perfused rat pancreas. J. Clin. Invest. 79, 616-619
8. Holst, J. J., and Gromada, J. (2004) Role of incretin hormones in the regulation of insulin secretion in diabetic and nondiabetic humans. Am. J. Physiol. Endocrinol. Metab. 287, E199-E206
9. Drucker, D. J. (2006) The biology of incretin hormones. Cell Metab. 3, 153-165
10. Nauck, M., Stöckmann, F., Ebert, R., and Creutzfeldt, W. (1986) Reduced incretin effect in type 2 (non-insulin-dependent) diabetes. Diabetologia 29, 46-52
11. Knop, F. K., Vilsbøll, T., Højberg, P. V., Larsen, S., Madsbad, S., Vølund, A., Holst, J. J., and Krarup, T. (2007) Reduced incretin effect in type 2 diabetes: cause or consequence of the diabetic state? Diabetes 56, 1951-1959
12. Calanna, S., Christensen, M., Holst, J. J., Laferrère, B., Gluud, L. L., Vilsbøll, T., and Knop, F. K. (2013) Secretion of glucose-dependent insulinotropic polypeptide in patients with type 2 diabetes: systematic review and metaanalysis of clinical studies. Diabetes Care 36, 3346-3352
13. Vilsbøll, T., Krarup, T., Deacon, C. F., Madsbad, S., and Holst, J. J. (2001) Reduced postprandial concentrations of intact biologically active glucagonlike peptide 1 in type 2 diabetic patients. Diabetes 50, 609-613
14. Nauck, M. A., Heimesaat, M. M., Orskov, C., Holst, J. J., Ebert, R., and Creutzfeldt, W. (1993) Preserved incretin activity of glucagon-like peptide 1 [7-36 amide] but not of synthetic human gastric inhibitory polypeptide in patients with type-2 diabetes mellitus. J. Clin. Invest. 91, 301-307
15. Vilsbøll, T., and Knop, F. K. (2007) [Effect of incretin hormones GIP and GLP-1 for the pathogenesis of type 2 diabetes mellitus]. Ugeskr. Laeg. 169, 2101-2105
16. Thorens, B. (1992) Expression cloning of the pancreaticβ cell receptor for the gluco-incretin hormone glucagon-like peptide 1. Proc. Natl. Acad. Sci. U. S. A. 89, 8641-8645
17. Seino, S., Takahashi, H., Fujimoto, W., and Shibasaki, T. (2009) Roles of cAMP signalling in insulin granule exocytosis. Diabetes Obes. Metab. 11, (Suppl. 4) 180-188
18. Yabe, D., and Seino, Y. (2011) Two incretin hormones GLP-1 and GIP: comparison of their actions in insulin secretion and β cell preservation. Prog. Biophys. Mol. Biol. 107, 248-256
19. Drucker, D. J. (2013) Incretin action in the pancreas: potential promise, possible perils, and pathological pitfalls. Diabetes 62, 3316-3323
20. Roscioni, S. S., Elzinga, C. R. S., and Schmidt, M. (2008) Epac: effectors and biological functions. Naunyn Schmiedeberg's Arch. Pharmacol. 377, 345-357
21. Song, W.-J., Seshadri, M., Ashraf, U., Mdluli, T., Mondal, P., Keil, M., Azevedo, M., Kirschner, L. S., Stratakis, C. A., and Hussain, M. A. (2011) Snapin mediates incretin action and augments glucose-dependent insulin secretion. Cell Metab. 13, 308-319
22. Barnett, A. (2007) Exenatide. Expert Opin. Pharmacother. 8, 2593-2608
23. Edwards, C. M. (2004) GLP-1: target for a new class of antidiabetic agents? J. R. Soc. Med. 97, 270-274
24. Friedrichsen, B. N., Neubauer, N., Lee, Y. C., Gram, V. K., Blume, N., Petersen, J. S., Nielsen, J. H., and Møldrup, A. (2006) Stimulation of pancreatic β-cell replication by incretins involves transcriptional induction of cyclin D1 via multiple signalling pathways. J. Endocrinol. 188, 481-492
25. Trümper, A., Trümper, K., Trusheim, H., Arnold, R., Göke, B., and Hörsch, D. (2001) Glucose-dependent insulinotropic polypeptide is a growth factor for β (INS-1) cells by pleiotropic signaling. Mol. Endocrinol. 15, 1559-1570
26. 2+]1 and a wortmannin-sensitive signalling pathway. Biochem. Biophys. Res. Commun. 224, 369-374
27. Kaneko, K., Ueki, K., Takahashi, N., Hashimoto, S., Okamoto, M., Awazawa, M., Okazaki, Y., Ohsugi, M., Inabe, K., Umehara, T., Yoshida, M., Kakei, M., Kitamura, T., Luo, J., Kulkarni, R. N., Kahn, C. R., Kasai, H., Cantley, L. C., and Kadowaki, T. (2010) Class IA phosphatidylinositol 3-kinase in pancreatic β cells controls insulin secretion by multiple mechanisms. Cell Metab. 12, 619-632
28. Stoyanov, B., Volinia, S., Hanck, T., Rubio, I., Loubtchenkov, M., Malek, D., Stoyanova, S., Vanhaesebroeck, B., Dhand, R., and Nürnberg, B. (1995) Cloning and characterization of a G protein-activated human phosphoinositide-3 kinase. Science 269, 690-693
29. Pigeau, G. M., Kolic, J., Ball, B. J., Hoppa, M. B., Wang, Y. W., Rückle, T., Woo, M., Manning Fox, J. E., and MacDonald, P. E. (2009) Insulin granule recruitment and exocytosis is dependent on p110γ in insulinoma and human β-cells. Diabetes 58, 2084-2092
30. Kolic, J., Spigelman, A. F., Plummer, G., Leung, E., Hajmrle, C., Kin, T., Shapiro, A. M., Manning Fox, J. E., and MacDonald, P. E. (2013) Distinct and opposing roles for the phosphatidylinositol 3-OH kinase catalytic subunits p110α and p110β in the regulation of insulin secretion from rodent and human β cells. Diabetologia 56, 1339-1349
31. Camps, M., Rückle, T., Ji, H., Ardissone, V., Rintelen, F., Shaw, J., Ferrandi, C., Chabert, C., Gillieron, C., Françon, B., Martin, T., Gretener, D., Perrin, D., Leroy, D., Vitte, P.-A., Hirsch, E., Wymann, M. P., Cirillo, R., Schwarz, M. K., and Rommel, C. (2005) Blockade of PI3Kγ suppresses joint inflammation and damage in mouse models of rheumatoid arthritis. Nat. Med. 11, 936-943
32. MacDonald, P. E., Joseph, J. W., Yau, D., Diao, J., Asghar, Z., Dai, F., Oudit, G. Y., Patel, M. M., Backx, P. H., and Wheeler, M. B. (2004) Impaired glucose-stimulated insulin secretion, enhanced intraperitoneal insulin tolerance, and increased β-cell mass in mice lacking the p110γ isoform of phosphoinositide 3-kinase. Endocrinology 145, 4078-4083
33. Li, L.-X., MacDonald, P. E., Ahn, D. S., Oudit, G. Y., Backx, P. H., and Brubaker, P. L. (2006) Role of phosphatidylinositol 3-kinaseγ in theβ-cell: interactions with glucagon-like peptide-1. Endocrinology 147, 3318-3325
34. Kalwat, M. A., and Thurmond, D. C. (2013) Signaling mechanisms of glucose-induced F-actin remodeling in pancreatic islet β cells. Exp. Mol. Med. 45, e37
35. Wang, Z., and Thurmond, D. C. (2009) Mechanisms of biphasic insulingranule exocytosis: roles of the cytoskeleton, small GTPases and SNARE proteins. J. Cell Sci. 122, 893-903
36. Li, J., Luo, R., Kowluru, A., and Li, G. (2004) Novel regulation by Rac1 of glucose- and forskolin-induced insulin secretion in INS-1 β-cells. Am. J. Physiol. Endocrinol. Metab. 286, E818-E827
37. Asahara, S., Shibutani, Y., Teruyama, K., Inoue, H. Y., Kawada, Y., Etoh, H., Matsuda, T., Kimura-Koyanagi, M., Hashimoto, N., Sakahara, M., Fujimoto, W., Takahashi, H., Ueda, S., Hosooka, T., Satoh, T., Inoue, H., Matsumoto, M., Aiba, A., Kasuga, M., and Kido, Y. (2013) Ras-related C3 botulinum toxin substrate 1 (RAC1) regulates glucose-stimulated insulin secretion via modulation of F-actin. Diabetologia 56, 1088-1097
38. Jewell, J. L., Luo, W., Oh, E., Wang, Z., and Thurmond, D. C. (2008) Filamentous actin regulates insulin exocytosis through direct interaction with Syntaxin 4. J. Biol. Chem. 283, 10716-10726
39. Holz, G. G., 4th, Kühtreiber, W. M., and Habener, J. F. (1993) Pancreatic β-cells are rendered glucose-competent by the insulinotropic hormone glucagon-like peptide-1 (7-37). Nature 361, 362-365
40. Kieffer, T. J., and Habener, J. F. (1999) The glucagon-like peptides. Endocr. Rev. 20, 876-913
41. MacDonald, P. E., El-Kholy, W., Riedel, M. J., Salapatek, A. M. F., Light, P. E., and Wheeler, M. B. (2002) The multiple actions of GLP-1 on the process of glucose-stimulated insulin secretion. Diabetes 51 (Suppl. 3) S434-S442
42. Merrins, M. J., and Stuenkel, E. L. (2008) Kinetics of Rab27a-dependent actions on vesicle docking and priming in pancreatic β-cells. J. Physiol. 586, 5367-5381
43. Straub, S. G., James, R. F., Dunne, M. J., and Sharp, G. W. (1998) Glucose activates both KATP channel-dependent and KATP channel-independent signaling pathways in human islets. Diabetes 47, 758-763
44. McClenaghan, N. H., Flatt, P. R., and Ball, A. J. (2006) Actions of glucagonlike peptide-1 on KATP channel-dependent and -independent effects of glucose, sulphonylureas and nateglinide. J. Endocrinol. 190, 889-896
45. Campbell, J. E., and Drucker, D. J. (2013) Pharmacology, physiology, and mechanisms of incretin hormone action. Cell Metab. 17, 819-837
46. Jung, I. D., Lee, J., Lee, K. B., Park, C. G., Kim, Y. K., Seo, D. W., Park, D., Lee, H. W., Han, J.-W., and Lee, H. Y. (2004) Activation of p21-activated kinase 1 is required for lysophosphatidic acid-induced focal adhesion kinase phosphorylation and cell motility in human melanoma A2058 cells. Eur. J. Biochem. 271, 1557-1565
47. Buteau, J., Foisy, S., Joly, E., and Prentki, M. (2003) Glucagon-like peptide 1 induces pancreatic β-cell proliferation via transactivation of the epidermal growth factor receptor. Diabetes 52, 124-132
48. Wymann, M. P., and Solinas, G. (2013) Inhibition of phosphoinositide 3-kinase γ attenuates inflammation, obesity, and cardiovascular risk factors. Ann. N. Y. Acad. Sci. 1280, 44-47
49. Becattini, B., Marone, R., Zani, F., Arsenijevic, D., Seydoux, J., Montani, J.-P., Dulloo, A. G., Thorens, B., Preitner, F., Wymann, M. P., and Solinas, G. (2011) PI3Kγ within a nonhematopoietic cell type negatively regulates diet-induced thermogenesis and promotes obesity and insulin resistance. Proc. Natl. Acad. Sci. U. S. A. 108, E854-63
50. Kobayashi, N., Ueki, K., Okazaki, Y., Iwane, A., Kubota, N., Ohsugi, M., Awazawa, M., Kobayashi, M., Sasako, T., Kaneko, K., Suzuki, M., Nishikawa, Y., Hara, K., Yoshimura, K., Koshima, I., Goyama, S., Murakami, K., Sasaki, J., Nagai, R., Kurokawa, M., Sasaki, T., and Kadowaki, T. (2011) Blockade of class IB phosphoinositide-3 kinase ameliorates obesity-induced inflammation and insulin resistance. Proc. Natl. Acad. Sci. U. S. A. 108, 5753-5758
51. Bernstein, H. G., Keilhoff, G., Reiser, M., Freese, S., and Wetzker, R. (1998) Tissue distribution and subcellular localization of a G-protein activated phosphoinositide 3-kinase. An immunohistochemical study. Cell Mol. Biol. (Noisy-le-grand) 44, 973-983
52. Randis, T. M., Puri, K. D., Zhou, H., and Diacovo, T. G. (2008) Role of PI3Kγ and PI3Kγ in inflammatory arthritis and tissue localization of neutrophils. Eur. J. Immunol. 38, 1215-1224
53. Rommel, C., Camps, M., and Ji, H. (2007) PI3Kγ and PI3Kγ: partners in crime in inflammation in rheumatoid arthritis and beyond? Nat. Rev. Immunol. 7, 191-201
54. Weiss-Haljiti, C., Pasquali, C., Ji, H., Gillieron, C., Chabert, C., Curchod, M.-L., Hirsch, E., Ridley, A. J., Hooft van Huijsduijnen, R., Camps, M., and Rommel, C. (2004) Involvement of phosphoinositide 3-kinase γ, Rac, and PAK signaling in chemokine-induced macrophage migration. J. Biol. Chem. 279, 43273-43284
55. Innocenti, M., Frittoli, E., Ponzanelli, I., Falck, J. R., Brachmann, S. M., Di Fiore, P. P., and Scita, G. (2003) Phosphoinositide 3-kinase activates Rac by entering in a complex with Eps8, Abi1, and Sos-1. J. Cell Biol. 160, 17-23
56. Welch, H. C., Coadwell, W. J., Ellson, C. D., Ferguson, G. J., Andrews, S. R., Erdjument-Bromage, H., Tempst, P., Hawkins, P. T., and Stephens, L. R. (2002) P-Rex1, a PtdIns (3, 4, 5) P3- and Gβγ-regulated guanine-nucleotide exchange factor for Rac. Cell 108, 809-821
57. Tomas, A., Yermen, B., Min, L., Pessin, J. E., and Halban, P. A. (2006) Regulation of pancreatic β-cell insulin secretion by actin cytoskeleton remodelling: role of gelsolin and cooperation with the MAPK signalling pathway. J. Cell Sci. 119, 2156-2167
58. Thurmond, D. C., Gonelle-Gispert, C., Furukawa, M., Halban, P. A., and Pessin, J. E. (2003) Glucose-stimulated insulin secretion is coupled to the interaction of actin with the t-SNARE (target membrane soluble N-ethylmaleimidesensitive factor attachment protein receptor protein) complex. Mol. Endocrinol. 17, 732-742
59. Orci, L., Gabbay, K. H., and Malaisse, W. J. (1972) Pancreatic β-cell web: its possible role in insulin secretion. Science 175, 1128-1130