SUMO1 enhances cAMP-dependent exocytosis and glucagon secretion from pancreatic α-cells

Journal of Physiology

Volumn 592, Issue 17, 2014, Pages 3715-3726

  Dai, Xiao Qing ^a,b   Spigelman, Aliya F ^a,b   Khan, Shara ^a,b   Braun, Matthias ^a,b   Manning Fox, Jocelyn E ^a,b   MacDonald, Patrick E ^a,b  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADRENALIN; CALCIUM CHANNEL L TYPE; CYCLIC AMP; EXENDIN 4; GLUCAGON; GLUCAGON LIKE PEPTIDE 1 RECEPTOR; ION CHANNEL; SUMO 1 PROTEIN; SUMO SPECIFIC PROTEASE 1; UNCLASSIFIED DRUG; GLUCAGON RECEPTOR; GLUCAGON-LIKE PEPTIDE-1 RECEPTOR; PROTEINASE; SENP1 PROTEIN, HUMAN; SODIUM; SUMO1 PROTEIN, HUMAN;

ACTION POTENTIAL; ANIMAL CELL; ARTICLE; CELL FUNCTION; CONTROLLED STUDY; EXOCYTOSIS; GENE SILENCING; GLUCAGON RELEASE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NONHUMAN; PANCREAS ISLET ALPHA CELL; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; UPREGULATION; AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; C57BL MOUSE; CELL CULTURE; GENETICS; METABOLISM; PHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; CALCIUM CHANNELS, L-TYPE; CELLS, CULTURED; CYCLIC AMP; ENDOPEPTIDASES; EXOCYTOSIS; GLUCAGON; GLUCAGON-SECRETING CELLS; HUMANS; MICE; MICE, INBRED C57BL; RECEPTORS, GLUCAGON; SODIUM; SUMO-1 PROTEIN;

EID: 84906935413     PISSN: 00223751     EISSN: 14697793     Source Type: Journal    
DOI: 10.1113/jphysiol.2014.274084     Document Type: Article

References (39)

1. Andersson SA, Pedersen MG, Vikman J & Eliasson L (2011). Glucose-dependent docking and SNARE protein-mediated exocytosis in mouse pancreatic α-cell. Pflugers Arch 462, 443-454.
2. Aukrust I, Bjørkhaug L, Negahdar M, Molnes J, Johansson BB, Müller Y, Haas W, Gygi SP, Søvik O, Flatmark T, Kulkarni RN & Njølstad PR (2013). SUMOylation of pancreatic glucokinase regulates its cellular stability and activity. J Biol Chem 288, 5951-5962.
3. Baggio LL & Drucker DJ (2007). Biology of incretins: GLP-1 and GIP. Gastroenterology 132, 2131-2157.
4. Barg S, Galvanovskis J, Göpel SO, Rorsman P & Eliasson L (2000). Tight coupling between electrical activity and exocytosis in mouse glucagon-secreting α-cells. Diabetes 49, 1500-1510.
5. Benson MD, Li Q-J, Kieckhafer K, Dudek D, Whorton MR, Sunahara RK, Iñiguez-Lluhí JA & Martens JR (2007). SUMO modification regulates inactivation of the voltage-gated potassium channel Kv1.5. Proc Natl Acad Sci U S A 104, 1805-1810.
6. Cryer PE (2012). Minireview: glucagon in the pathogenesis of hypoglycemia and hyperglycemia in diabetes. Endocrinology 153, 1039-1048.
7. da Silva Xavier G, Farhan H, Kim H, Caxaria S, Johnson P, Hughes S, Bugliani M, Marselli L, Marchetti P, Birzele F, Sun G, Scharfmann R, Rutter J, Siniakowicz K, Weir G, Parker H, Reimann F, Gribble FM & Rutter GA (2011). Per-Arnt-Sim (PAS) domain-containing protein kinase is downregulated in human islets in type 2 diabetes and regulates glucagon secretion. Diabetologia 54, 819-827.
8. da Silva Xavier G, Rutter J & Rutter GA (2004). Involvement of Per-Arnt-Sim (PAS) kinase in the stimulation of preproinsulin and pancreatic duodenum homeobox 1 gene expression by glucose. Proc Natl Acad Sci U S A 101, 8319-8324.
9. Dai XQ, Kolic J, Marchi P, Sipione S & MacDonald PE (2009). SUMOylation regulates Kv2.1 and modulates pancreatic β-cell excitability. J Cell Sci 122, 775-779.
10. Dai XQ, Plummer G, Casimir M, Kang Y, Hajmrle C, Gaisano HY, Manning Fox JE & MacDonald PE (2011). SUMOylation regulates insulin exocytosis downstream of secretory granule docking in rodents and humans. Diabetes 60, 838-847.
11. Davila MA, Chan H & Piedras-Renteria ES (2010). Sumoylation of voltage-gated αA1a calcium channels. Biophysical J 98, 692a-693a.
12. 2+ channel-dependent exocytosis. Cell Metab 11, 543-553.
13. Dunning BE & Taborsky GJ (1991). Neural control of islet function by norepinephrine and sympathetic neuropeptides. Adv Exp Med Biol 291, 107-127.
14. Ernst SJ, Aguilar-Bryan L & Noebels JL (2009). Sodium channel β1 regulatory subunit deficiency reduces pancreatic islet glucose-stimulated insulin and glucagon secretion. Endocrinology 150, 1132-1139.
15. Feligioni M, Nishimune A & Henley JM (2009). Protein SUMOylation modulates calcium influx and glutamate release from presynaptic terminals. Eur J Neurosci 29, 1348-1356.
16. Fontés G, Semache M, Hagman DK, Tremblay C, Shah R, Rhodes CJ, Rutter J & Poitout V (2009). Involvement of Per-Arnt-Sim kinase and extracellular-regulated kinases-1/2 in palmitate inhibition of insulin gene expression in pancreatic β-cells. Diabetes 58, 2048-2058.
17. + channels. J Physiol (Lond) 528, 509-520.
18. Gromada J & Rorsman P (2004). New insights into the regulation of glucagon secretion by glucagon-like peptide-1. Horm Metab Res 36, 822-829.
19. Hare KJ, Vilsbøll T, Asmar M, Deacon CF, Knop FK & Holst JJ (2010). The glucagonostatic and insulinotropic effects of glucagon-like peptide 1 contribute equally to its glucose-lowering action. Diabetes 59, 1765-1770.
20. Henry RR, Smith SR, Schwartz SL, Mudaliar SR, Deacon CF, Holst JJ, Duan RY, Chen RS & List JF (2011). Effects of saxagliptin on β-cell stimulation and insulin secretion in patients with type 2 diabetes. Diabetes Obes Metab 13, 850-858.
21. Kho C, Lee A, Jeong D, Oh JG, Chaanine AH, Kizana E, Park WJ & Hajjar RJ (2011). SUMO1-dependent modulation of SERCA2a in heart failure. Nature 477, 601-605.
22. Lovshin JA & Drucker DJ (2009). Incretin-based therapies for type 2 diabetes mellitus. Nat Rev Endocrinol 5, 262-269.
23. MacDonald PE, De Marinis YZ, Ramracheya R, Salehi A, Ma X, Johnson PRV, Cox R, Eliasson L & Rorsman P (2007). A K ATP channel-dependent pathway within α cells regulates glucagon release from both rodent and human islets of Langerhans. PLoS Biol 5, e143.
24. Manning Fox JE, Hajmrle C & MacDonald PE (2012). Novel roles of SUMO in pancreatic β-cells: thinking outside the nucleus. Can J Physiol Pharmacol 90, 765-770.
25. Plant LD, Dementieva IS, Kollewe A, Olikara S, Marks JD & Goldstein SAN (2010). One SUMO is sufficient to silence the dimeric potassium channel K2P1. Proc Natl Acad Sci U S A 107, 10743-10748.
26. Plant LD, Dowdell EJ, Dementieva IS, Marks JD & Goldstein SAN (2011). SUMO modification of cell surface Kv2.1 potassium channels regulates the activity of rat hippocampal neurons. J Gen Physiol 137, 441-454.
27. + channel K2P1. Cell 121, 37-47.
28. Rajan S, Torres J, Thompson MS & Philipson LH (2012). SUMO downregulates GLP-1-stimulated cAMP generation and insulin secretion. Am J Physiol Endocrinol Metab 302, E714-E723.
29. Ramracheya R, Ward C, Shigeto M, Walker JN, Amisten S, Zhang Q, Johnson PR, Rorsman P & Braun M (2010). Membrane potential-dependent inactivation of voltage-gated ion channels in α-cells inhibits glucagon secretion from human islets. Diabetes 59, 2198-2208.
30. Rauch T, Graefe-Mody U, Deacon CF, Ring A, Holst JJ, Woerle H-J, Dugi KA & Heise T (2012). Linagliptin increases incretin levels, lowers glucagon, and improves glycemic control in type 2 diabetes mellitus. Diabetes Ther 3, 10.
31. Rorsman P, Braun M & Zhang Q (2012). Regulation of calcium in pancreatic α- and β-cells in health and disease. Cell Calcium 51, 300-308.
32. Schuit FC & Pipeleers DG (1986). Differences in adrenergic recognition by pancreatic A and B cells. Science 232, 875-877.
33. + channels are positive regulators of α cell action potential generation and glucagon secretion in mice and humans. Diabetologia 53, 1917-1926.
34. Straub SG & Sharp GWG (2012). Evolving insights regarding mechanisms for the inhibition of insulin release by norepinephrine and heterotrimeric G proteins. Am J Physiol Cell Physiol 302, C1687-C1698.
35. Tian G, Sandler S, Gylfe E & Tengholm A (2011). Glucose- and hormone-induced cAMP oscillations in α- and β-cells within intact pancreatic islets. Diabetes 60, 1535-1543.
36. Vieira E, Liu Y-J & Gylfe E (2004). Involvement of α1 and β-adrenoceptors in adrenaline stimulation of the glucagon-secreting mouse α-cell. Naunyn Schmiedebergs Arch Pharmacol 369, 179-183.
37. Vignali S, Leiss V, Karl R, Hofmann F & Welling A (2006). Characterization of voltage-dependent sodium and calcium channels in mouse pancreatic A- and B-cells. J Physiol (Lond) 572, 691-706.
38. Wyatt D, Malik R, Vesecky AC & Marchese A (2011). Small ubiquitin-like modifier modification of arrestin-3 regulates receptor trafficking. J Biol Chem 286, 3884-3893.
39. Yeh ETH (2009). SUMOylation and de-SUMOylation: wrestling with life's processes. J Biol Chem 284, 8223-8227.