The intracellular II-III loops of Cav1.2 and Cav1.3 uncouple L-type voltage-gated Ca2+ channels from glucagon-like peptide-1 potentiation of insulin secretion in INS-1 cells via displacement from lipid rafts

Journal of Pharmacology and Experimental Therapeutics

Volumn 330, Issue 1, 2009, Pages 283-293

  Jacobo, Sarah Melissa P ^a   Guerra, Marcy L ^b   Jarrard, Rachel E ^a   Przybyla, Julie A ^b   Liu, Guohong ^b   Watts, Val J ^b   Hockerman, Gregory H ^b,c  

^a PURDUE UNIVERSITY   (United States)

^b PURDUE UNIVERSITY   (United States)

^c NONE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 (2 BENZYLBENZOYL) 2,5 DIMETHYL 1H PYRROLE 3 CARBOXYLIC ACID METHYL ESTER; 8 BROMO CYCLIC AMP; CALCIUM CHANNEL L TYPE; CYCLIC AMP; GLUCAGON LIKE PEPTIDE 1; GLUCOSE; INSULIN; PICCOLO PROTEIN; PROTEIN; PROTEIN RIM 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CALCIUM CURRENT; CALCIUM TRANSPORT; CONTROLLED STUDY; HORMONAL REGULATION; HORMONE ACTION; INSULIN RELEASE; LIPID RAFT; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RAT;

ANIMALS; CALCIUM CHANNELS, L-TYPE; CELL LINE, TUMOR; GLUCAGON-LIKE PEPTIDE 1; GLUCOSE; HUMANS; INSULIN; INTRACELLULAR FLUID; MEMBRANE MICRODOMAINS; PROTEIN INTERACTION MAPPING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RATS; RECEPTORS, GLUCAGON;

EID: 67649859224     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.109.150672     Document Type: Article

References (33)

1. Asfari M, Janjic D, Meda P, Li G, Halban PA, and Wollheim CB (1992) Establishment of 2-mercaptoethanol-dependent differentiated insulin-secreting cell lines. Endocrinology 130:167-178.
2. Balijepalli RC, Foell JD, Hall DD, Hell JW, and Kamp TJ (2006) Localization of cardiac L-type Ca(2+) channels to a caveolar macromolecular signaling complex is required for beta(2)-adrenergic regulation. Proc Natl Acad Sci U S A 103:7500-7505. (Pubitemid 43727862)
3. Bergsten P (2002) Role of oscillations in membrane potential, cytoplasmic Ca2+, and metabolism for plasma insulin oscillations. Diabetes 51(Suppl 1):S171-S176. (Pubitemid 34761513)
4. Catterall WA (1995) Structure and function of voltage-gated ion channels. Annu Rev Biochem 64:493-531.
5. Cohen AW, Hnasko R, Schubert W, and Lisanti MP (2004) Role of caveolae and caveolins in health and disease. Physiol Rev 84:1341-1379. (Pubitemid 39287953)
6. 2+-sensitive adenylyl cyclases dictate their targeting to plasma membrane lipid rafts. J Biol Chem 280:6380-6391.
7. Cumbay MG and Watts VJ (2001) Heterologous sensitization of recombinant adenylate cyclases by activation of D2 dopamine receptors. J Pharmacol Exp Ther 297:1201-1209. (Pubitemid 32472522)
8. Delmeire D, Flamez D, Hinke SA, Cali JJ, Pipeleers D, and Schuit F (2003) Type VIII adenylyl cyclase in rat beta cells: coincidence signal detector/generator for glucose and GLP-1. Diabetologia 46:1383-1393. (Pubitemid 37297209)
9. Devis G, Somers G, Van Obberghen E, and Malaisse WJ (1975) Calcium antagonists and islet function. I. Inhibition of insulin release by verapamil. Diabetes 24:247-251.
10. 2+ entry requires localization in cholesterol- rich domains. J Biol Chem 275:26530-26537.
11. 2+ sensor in pancreatic beta-cells. Involvement of cAMP-GEFII. Rim2.Piccolo complex in cAMP-dependent exocytosis. J Biol Chem 277:50497-50502.
12. Griffith IP (1972) The effect of cross-links on the mobility of proteins in dodecyl sulphate-polyacrylamide gels. Biochem J 126:553-560.
13. Ji J, Yang SN, Huang X, Li X, Sheu L, Diamant N, Berggren PO, and Gaisano HY (2002) Modulation of L-type Ca2+ channels by distinct domains within snap-25. Diabetes 51:1425-1436. (Pubitemid 34826608)
14. Kang G, Chepurny OG, and Holz GG (2001) cAMP-regulated guanine nucleotide exchange factor II (Epac2) mediates Ca2+-induced Ca2+ release in INS-1 pancreatic beta-cells. J Physiol 536:375-385. (Pubitemid 32976119)
15. Leung YM, Kwan EP, Ng B, Kang Y, and Gaisano HY (2007) SNAREing voltagegated K+ and ATP-sensitive K+ channels: tuning beta-cell excitability with syntaxin- 1A and other exocytotic proteins. Endocr Rev 28:653-663. (Pubitemid 47606650)
16. Liu G, Dilmac N, Hilliard N, and Hockerman GH (2003) Ca(v)1.3 is preferentially coupled to glucose-stimulated insulin secretion in the pancreatic beta-cell line INS-1. J Pharmacol Exp Ther 305:271-278. (Pubitemid 36373861)
17. i oscillations in the pancreatic beta cell line INS-1. Mol Pharmacol 65:1269-1277.
18. Liu G, Jacobo SM, Hilliard N, and Hockerman GH (2006) Differential modulation of Cav1.2 and Cav1.3-mediated glucose-stimulated insulin secretion by cAMP in INS-1 cells: distinct roles for exchange protein directly activated by cAMP 2 (Epac2) and protein kinase A. J Pharmacol Exp Ther 318:152-160. (Pubitemid 43920752)
19. MacDonald PE, El-Kholy W, Riedel MJ, Salapatek AM, Light PE, and Wheeler MB (2002) The multiple actions of GLP-1 on the process of glucose-stimulated insulin secretion. Diabetes 51 (Suppl 3):S434-S442. (Pubitemid 35403427)
20. Rajan AS, Aguilar-Bryan L, Nelson DA, Yaney GC, Hsu WH, Kunze DL, and Boyd AE 3rd (1990) Ion channels and insulin secretion. Diabetes Care 13:340-363.
21. 2+-secretion coupling is impaired in diabetic Goto Kakizaki rats. J Gen Physiol 129:493-508.
22. 2+ channel in insulin granule exocytosis. J Biol Chem 279:7956-7961.
23. Shibasaki T, Takahashi H, Miki T, Sunaga Y, Matsumura K, Yamanaka M, Zhang C, Tamamoto A, Satoh T, Miyazaki J, et al. (2007) Essential role of Epac2/Rap1 signaling in regulation of insulin granule dynamics by cAMP. Proc Natl Acad Sci U S A 104:19333-19338.
24. Smith KE, Gu C, Fagan KA, Hu B, and Cooper DM (2002) Residence of adenylyl cyclase type 8 in caveolae is necessary but not sufficient for regulation by capacitative Ca(2+) entry. J Biol Chem 277:6025-6031. (Pubitemid 34968386)
25. Song H, Nie L, Rodriguez-Contreras A, Sheng ZH, and Yamoah EN (2003) Functional interaction of auxiliary subunits and synaptic proteins with Ca(v)1.3 may impart hair cell Ca2+ current properties. J Neurophysiol 89:1143-1149. (Pubitemid 36206158)
26. Syme CA, Zhang L, and Bisello A (2006) Caveolin-1 regulates cellular trafficking and function of the glucagon-like peptide 1 receptor. Mol Endocrinol 20:3400-3411. (Pubitemid 44833579)
27. Tsujikawa H, Song Y, Watanabe M, Masumiya H, Gupte SA, Ochi R, and Okada T (2008) Cholesterol depletion modulates basal L-type Ca2+ current and abolishes its adrenergic enhancement in ventricular myocytes. Am J Physiol Heart Circ Physiol 294:H285-H292.
28. Wiser O, Trus M, Hernandez A, Renstrom E, Barg S, Rorsman P, and Atlas D (1999) The voltage sensitive lc-type Ca2+ channel is functionally coupled to the exocytotic machinery. Proc Natl Acad Sci U S A 96:248-253. (Pubitemid 29036085)
29. Wollheim CB and Sharp GW (1981) Regulation of insulin release by calcium. Physiol Rev 61:914-973.
30. Xia F, Gao X, Kwan E, Lam PP, Chan L, Sy K, Sheu L, Wheeler MB, Gaisano HY, and Tsushima RG (2004) Disruption of pancreatic β-cell lipid rafts modifies Kv2.1 channel gating and insulin exocytosis. J Biol Chem 279:24685-24691. (Pubitemid 38725336)
31. Xia F, Xie L, Mihic A, Gao X, Chen Y, Gaisano HY, and Tsushima RG (2008) Inhibition of cholesterol biosynthesis impairs insulin secretion and voltage-gated calcium channel function in pancreatic beta-cells. Endocrinology 149:5136-5145.
32. Yang SN, Larsson O, Bränström R, Bertorello AM, Leibiger B, Leibiger IB, Moede T, Köhler M, Meister B, and Berggren PO (1999) Syntaxin 1 interacts with the L(D) subtype of voltage-gated Ca(2+) channels in pancreatic beta cells. Proc Natl Acad Sci U S A 96:10164-10169. (Pubitemid 29422530)
33. 2+ channel activator, in cardiac and vascular preparations. Mol Pharmacol 40:734-741.