cAMP-secretion coupling is impaired in diabetic GK/Par rat β-cells: A defect counteracted by GLP-1

American Journal of Physiology - Endocrinology and Metabolism

Volumn 301, Issue 5, 2011, Pages

  Dolz, Manuel ^a,b   Movassat, Jamileh ^a,b   Bailbé, Danielle ^a,b   le Stunff, Hervé ^a,b   Giroix, Marie Hélène ^a,b   Fradet, Magali ^a,b   Kergoat, Micheline ^c   Portha, Bernard ^a,b  

^a UNIVERSITÉ PARIS DESCARTES   (France)

^b CNRS   (France)

^c Metabrain Research   (France)

Author keywords

Calcium metabolism; Cyclic AMP metabolism; Cyclic AMP resistance; Glucagon like peptide 1; Insulin secretion; Type 2 diabetes

Indexed keywords

2',5' DIDEOXYADENOSINE; ADENYLATE CYCLASE; CALCIUM ION; CYCLIC AMP; FORSKOLIN; GLUCAGON LIKE PEPTIDE 1; ISOBUTYLMETHYLXANTHINE; PHOSPHODIESTERASE III;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; GLUCOSE METABOLISM; INSULIN LIKE ACTIVITY; INSULIN RELEASE; MALE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; STIMULUS SECRETION COUPLING;

ANIMALS; CELLS, CULTURED; CYCLIC AMP; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 2; DISEASE MODELS, ANIMAL; GLUCAGON-LIKE PEPTIDE 1; GLUCOSE; INSULIN; INSULIN-SECRETING CELLS; MALE; RATS; RATS, WISTAR; SECRETORY PATHWAY; STREPTOZOCIN;

EID: 80054965549     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00652.2010     Document Type: Article

References (39)

1. Abdel-Halim SM, Guenifi A, Khan A, Larsson O, Berggren PO, Östenson CG, Efendic S. Impaired coupling of glucose signal to the exocytotic machinery in diabetic GK rats: a defect ameliorated by cAMP. Diabetes 45: 934-940, 1996.
2. Abdel-Halim SM, Guenifi He B, Yang B, Mustafa M, Hojeberg B, Hillert J, Bakhiet M, Efendic S. Mutations in the promoter of adenylyl cyclase (AC)-III gene, overexpression of AC-III mRNA, and enhanced cAMP generation in islets from spontaneously diabetic GK rat model of type-2 diabetes. Diabetes 47: 498-504, 1998.
3. Dachicourt N, Serradas P, Giroix MH, Gangnerau MN, Portha B. Decreased glucose-induced cAMP and insulin release in islets of diabetic rats: reversal by IBMX, glucagon, and GIP. Am J Physiol Endocrinol Metab 271: E725-E732, 1996.
4. Dachicourt N, Serradas P, Bailbe D, Kergoat M, Doare L, Portha B. Glucagon-like peptide-1(7-36)-amide confers glucose sensitivity to previously glucose-incompetent β-cells in diabetic rats: in vivo and in vitro studies. J Endocrinol 155: 369-376, 1997.
5. Ding WG, Gromada J. Protein kinase A-dependent stimulation of exocytosis in mouse pancreatic β-cells by glucose-dependent insulinotropic polypeptide. Diabetes 46: 615-621, 1997.
6. Dolz M, Bailbe D, Giroix MH, Calderari S, Gangnerau MN, Serradas P, Rickenbach K, Irminger JC, Portha B. Restitution of defective glucose-stimulated insulin secretion in diabetic GK rat by acetylcholine uncovers paradoxical stimulatory effect of β-cell muscarinic receptor activation on cAMP production. Diabetes 54: 3229-3237, 2005.
7. Dyachok ME, Isakov Y, Sagetorp J, Tengholm A. Oscillations of cyclic AMP in hormone-stimulated insulin-secreting β-cells. Nature 439: 349-352, 2006.
8. Frayon S, Pessah M, Giroix MH, Mercan D, Boissard C, Malaisse WJ, Portha B, Garel JM. Galphaolf identification by RT-PCR in purified normal pancreatic B cells and in islets from rat models of non-insulindependent diabetes. Biochem Biophys Res Commun 254: 269-272, 1999.
9. Gromada J, Dissing S, Bokvist K, Renstrom E, Frokjaer-Jensen J, Wulff BS, Rorsman P. Glucagon-like peptide I increases cytoplasmic calcium in insulin-secreting βTC3-cells by enhancement of intracellular calcium mobilization. Diabetes 44: 767-774, 1995.
10. Gromada J, Ding WG, Barg S, Renstrom E, Rorsman P. Multisite regulation of insulin secretion by cAMP-increasing agonists: evidence that glucagon-like peptide 1 and glucagon act via distinct receptors. Pflügers Arch 434: 515-524, 1997.
11. Gromada J, Bokvist K, Ding WG, Holst JJ, Nielsen JH, Rorsman P. Glucagon-like peptide 1 (7-36) amide stimulates exocytosis in human pancreatic β-cells by both proximal and distal regulatory steps in stimulussecretion coupling. Diabetes 47: 57-65, 1998.
12. Guenifi A, Portela-Gomes GM, Grimelius L, Efendic S, Abdel-Halim SM. Adenylyl cyclase isoform expression in non-diabetic and diabetic Goto-Kakizaki (GK) rat pancreas. Evidence for distinct overexpression of type-8 adenylyl cyclase in diabetic GK rat islets. Histochem Cell Biol 113: 81-89, 2000.
13. Guenifi A, Abdel-Halim SM. Glucose enhances adenylyl cyclase responses in normal but not diabetic GK rat islets. Pancreas 22: 65-68, 2001.
14. Han P, Werber J, Surana M, Fleischer N, Michaeli T. The calcium/calmodulin-dependent phosphodiesterase PDE1C down-regulates glucose-induced insulin secretion. J Biol Chem 274: 22337-22344, 1999.
15. Harndahl L, Jing XJ, Ivarsson R, Degerman E, Ahren B, Manganiello VC, Renstrom E, Holst LS. Important role of phosphodiesterase 3B for the stimulatory action of cAMP on pancreatic βcell exocytosis and release of insulin. J Biol Chem 277: 37446-37455, 2002.
16. Henquin JC. Regulation of insulin secretion: a matter of phase control and amplitude modulation. Diabetologia 2: 739-751, 2009.
17. 2+ /calmodulin and cyclic 3,5' adenosine monophosphate control movement of secretory granules through protein phosphorylation/dephosphorylation in the pancreatic β-cell. Endocrinology 137: 4644-4649, 1996.
18. Holz GG, Kuhtreiber WM, Habener JF. Pancreatic β-cells are rendered glucose-competent by the insulinotropic hormone glucagon-like peptide- 1(7-37). Nature 361: 362-365, 1993.
19. Insel PA, Ostrom RS. Forskolin as a tool for examining adenylyl cyclase expression, regulation, and G protein signaling. Cell Mol Neurobiol 23: 305-314, 2003.
20. 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 276: 46046-46053, 2001.
21. Lacraz G, Figeac F, Movassat J, Kassis N, Portha B. Diabetic GK/Par rat β-cells are spontaneously protected against oxidative stress inducedapoptosis. A cAMP-dependent adaptive response. Am J Physiol Endocrinol Metab 298: E17-E27, 2010.
22. 2+ and cAMP signaling in the insulin-secreting MIN6 β-cell line. J Biol Chem 280: 31294-31302, 2005.
23. Le Stunff H, Dokhac L, Bourgoin S, Bader MF, Harbon S. Phospholipase D in rat myometrium: occurrence of a membrane-bound ARF6 (ADP-ribosylation factor 6)-regulated activity controlled by βgamma subunits of heterotrimeric G-proteins. Biochem J 352: 491-491, 2000.
24. Ma YH, Landis C, Tchao N, Wang J, Rodd G, Hanahan D, Bourne HR, Grodsky GM. Constitutively active stimulatory G-protein alpha s in β-cells of transgenic mice causes counterregulation of the increased adenosine 3',5'-monophosphate and insulin secretion. Endocrinology 134: 42-47, 1994.
25. Malaisse WJ, Malaisse-Lagae F. The role of cyclic AMP in insulin release. Experientia 40: 1068-1074, 1984
26. Ozaki N, Shibasaki T, Kashima Y, Miki T, Takahashi K, Ueno H, Sunaga Y, Yano H, Matsuura Y, Iwanaga T, Takai Y, Seino S. cAMP-GEFII is a direct target of cAMP in regulated exocytosis. Nat Cell Biol 2: 805-811, 2000.
27. Peyot ML, Gray JP, Lamontagne J, Smith P, Holz GG, Madiraju SRM, Prentki M, Heart E. Glucagon-like peptide-1 induced signaling and insulin secretion do not drive fuel and energy metabolism in primary rodent pancreatic β-cells. PLoS ONE 4, e6221: 1-10, 2009.
28. Phan HH, Boissard C, Pessah M, Regnauld K, Emami S, Gespach C, Rosselin G. Decreased ADP-ribosylation of the Galpha(olf) and Galpha(s) subunits by high glucose in pancreatic B-cells. Biochem Biophys Res Commun 271: 86-90, 2000.
29. Portela-Gomes GM, Abdel-Halim SM. Overexpression of Gs proteins and adenylyl cyclase in normal and diabetic islets. Pancreas 25: 176-181, 2002.
30. Portela-Gomes GM, Lukinius A, Ljungberg O, Efendic S, Ahren B, Abdel-Halim SM. PACAP is expressed in secretory granules of insulin and glucagon cells in human and rodent pancreas. Evidence for generation of cAMP compartments uncoupled from hormone release in diabetic islets. Regul Pept 113: 31-39, 2003.
31. Portha B, Lacraz G, Kergoat M, Homo-Delarche F, Giroix MH, Bailbé D, Gangnerau MN, Dolz M, Tourrel-Cuzin C, Movassat J. The GK rat β-cell: a prototype for the diseased human β-cell in type 2 diabetes? Mol Cell Endocrinol 297: 73-85, 2009.
32. Portha B, Movassat J, Cuzin-Tourrel C, Bailbé D, Giroix MH, Serradas P, Dolz M, Kergoat M. The neonatally streptozotocin-induced (n-STZ) rat model of Type 2 diabetes. Several variants with multiple and complementary talents. In: Animal Models of Diabetes, edited by Shafrir E Taylor and Francis Group. Boca Raton, FL: CRC Press, 2007, p. 223-250.
33. Portha B, Lacraz G, Chavey A, Figeac F, Fradet M, Tourrel-Cuzin C, Homo-Delarche F, Giroix MH, Bailbé D, Gangnerau MN, Movassat J. Islet structure and function in the GK rat. In: The Islets of Langerhans: Advances in Experimental Medicine and Biology, edited by Islam S. Springer 654: 479-500, 2010.
34. Ramos LS, Hale Zippin J, Kamenetsky M, Buck J, Levin LR. Glucose and GLP-1 stimulate cAMP production via distinct adenylyl cyclases in INS-1E insulinoma cells. J Gen Physiol 132: 329-338, 2008.
35. Seino S, Shibasaki T. PKA-dependent and PKA-independent pathways for cAMP-regulated exocytosis. Physiol Rev 85: 1303-1342, 2005.
36. Sharp GW. The adenylate cyclase-cyclic AMP system in islets of Langerhans and its role in the control of insulin release. Diabetologia 16: 87-96, 1979.
37. 2+-independent insulin secretion from permeabilized RINm5F cells. J Biol Chem 262: 5049-5056, 1987.
38. Valverde I, Garcia-Morales P, Ghiglione M, Malaisse WJ. The stimulus secretion coupling of glucose-induced insulin release. III. Calciumdependency of the cyclic AMP response to nutrient secretagogues. Horm Metab Res 15: 62-68, 1983.
39. 2+ channel activity. Endocrinology 133: 1685-1692, 1993.