Chromanol 293B, an inhibitor of KCNQ1 channels, enhances glucose-stimulated insulin secretion and increases glucagon-like peptide-1 level in mice

Islets

Volumn 6, Issue 4, 2014, Pages

  Liu, Lijie ^a   Wang, Fanfan ^b   Lu, Haiying ^b   Ren, Xiaomei ^c   Zou, Jihong ^c  

^a MEDICAL SCHOOL OF SOUTHEAST UNIVERSITY   (China)

^b SOUTHEAST UNIVERSITY   (China)

^c AFFILIATED ZHONGDA HOSPITAL OF SOUTHEAST UNIVERSITY   (China)

Author keywords

Chromanol 293B; GLP 1; GSIS; IPGTT; Islets of Langerhans; ITT; KCNQ1; OGTT

Indexed keywords

CHROMANOL 293B; GLUCAGON LIKE PEPTIDE 1; GLUCOSE; INSULIN; POTASSIUM CHANNEL KCNQ1; 6-CYANO-4-(N-ETHYLSULFONYL-N-METHYLAMINO)-3-HYDROXY-2,2-DIMETHYLCHROMANE; CHROMAN DERIVATIVE; SULFONAMIDE;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD ANALYSIS; CONTROLLED STUDY; GLUCOSE TOLERANCE; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; INSULIN RELEASE; INSULIN SENSITIVITY; INSULIN TOLERANCE TEST; MALE; MOUSE; NONHUMAN; ORAL GLUCOSE TOLERANCE TEST; PROTEIN EXPRESSION; ANIMAL; ANTAGONISTS AND INHIBITORS; BLOOD; CHEMISTRY; DRUG EFFECTS; FLUORESCENT ANTIBODY TECHNIQUE; GLUCOSE TOLERANCE TEST; IN VITRO STUDY; INSULIN RESISTANCE; INTESTINE; PANCREAS; PANCREAS ISLET; PHYSIOLOGY; SECRETION (PROCESS);

ANIMALS; CHROMANS; FLUORESCENT ANTIBODY TECHNIQUE; GLUCAGON-LIKE PEPTIDE 1; GLUCOSE; GLUCOSE TOLERANCE TEST; IN VITRO TECHNIQUES; INSULIN; INSULIN RESISTANCE; INTESTINES; ISLETS OF LANGERHANS; KCNQ1 POTASSIUM CHANNEL; MICE; PANCREAS; SULFONAMIDES;

EID: 84937611269     PISSN: 19382014     EISSN: 19382022     Source Type: Journal    
DOI: 10.4161/19382014.2014.962386     Document Type: Article

References (40)

1. Butler AE, Janson J, Bonner-Weir S, Ritzel R, Rizza RA, Butler PC. Beta-cell deficit and increased beta-cell apoptosis in humans with type 2 diabetes. Diabetes 2003; 52:102-10. PMID:12502499. http://dx.doi.org/10.2337/diabetes.52.1.102
2. Rathmann W, Scheidt-Nave C, Roden M, Herder C. Type 2 diabetes: prevalence and relevance of genetic and acquired factors for its prediction. Deut Arzteblatt Int 2013; 110:331-7. PMID:23762204
3. Mensink M. Lifestyle intervention, glucose tolerance, and risk of developing type 2 diabetes mellitus. Metabolic Syndrome and Rel Dis 2005; 3:26-34. PMID:18370707. http://dx.doi.org/10.1089/met.2005.3.26
4. Neuman RJ, Wasson J, Atzmon G, Wainstein J, Yerushalmi Y, Cohen J, Barzilai N, Blech I, Glaser B, Permutt MA. Gene-gene interactions lead to higher risk for development of type 2 diabetes in an Ashkenazi Jewish population. PloS One 2010; 5:e9903. PMID:20361036. http://dx.doi.org/10.1371/journal.pone.0009903
5. Holmkvist J, Banasik K, Andersen G, Unoki H, Jensen TS, Pisinger C, Borch-Johnsen K, Sandbaek A, Lauritzen T, Brunak S, et al. The type 2 diabetes associated minor allele of rs2237895 KCNQ1 associates with reduced insulin release following an oral glucose load. PloS One 2009; 4:e5872. PMID:19516902. http://dx.doi.org/10.1371/journal.pone.0005872
6. Kasuga M. KCNQ1, a susceptibility gene for type 2 diabetes. J Diabetes Invest 2011; 2:413-4. PMID:24843522. http://dx.doi.org/10.1111/j.2040-1124.2011.00178.x
7. Unoki H, Takahashi A, Kawaguchi T, Hara K, Horikoshi M, Andersen G, Ng DP, Holmkvist J, Borch-Johnsen K, Jorgensen T, et al. SNPs in KCNQ1 are associated with susceptibility to type 2 diabetes in East Asian and European populations. Nat Genet 2008; 40:1098-102. PMID:18711366. http://dx.doi.org/10.1038/ng.208
8. Yasuda K, Miyake K, Horikawa Y, Hara K, Osawa H, Furuta H, Hirota Y, Mori H, Jonsson A, Sato Y, et al. Variants in KCNQ1 are associated with susceptibility to type 2 diabetes mellitus. Nat Genet 2008; 40:1092-7. PMID:18711367. http://dx.doi.org/10.1038/ng.207
9. Robbins J. KCNQ potassium channels: physiology, pathophysiology, and pharmacology. Pharm Therap 2001; 90:1-19. PMID:11448722. http://dx.doi.org/10.1016/S0163-7258(01)00116-4
10. Demolombe S, Franco D, de Boer P, Kuperschmidt S, Roden D, Pereon Y, Jarry A, Moorman AF, Escande D. Differential expression of KvLQT1 and its regulator IsK in mouse epithelia. Am J Physiol Cell Physiol 2001; 280:C359-72. PMID:11208532
11. Jespersen T, Grunnet M, Olesen SP. The KCNQ1 potassium channel: from gene to physiological function. Physiology (Bethesda) 2005; 20:408-16. PMID:16287990. http://dx.doi.org/10.1152/physiol.00031.2005
12. Wang Q, Curran ME, Splawski I, Burn TC, Millholland JM, VanRaay TJ, Shen J, Timothy KW, Vincent GM, de Jager T, et al. Positional cloning of a novel potassium channel gene: KVLQT1 mutations cause cardiac arrhythmias. Nat Genet 1996; 12:17-23. PMID:8528244. http://dx.doi.org/10.1038/ng0196-17
13. Hayashi M, Wang J, Hede SE, Novak I. An intermediate-conductance Ca2C-activated KC channel is important for secretion in pancreatic duct cells. Am J Physiol Cell Physiol 2012; 303:C151-9. PMID:22555847. http://dx.doi.org/10.1152/ajpcell.00089.2012
14. Yamagata K, Senokuchi T, Lu M, Takemoto M, Fazlul Karim M, Go C, Sato Y, Hatta M, Yoshizawa T, Araki E, et al. Voltage-gated KC channel KCNQ1 regulates insulin secretion in MIN6 betacell line. Biochem Biophys Res Commun 2011; 407:620-5. PMID:21426901. http://dx.doi.org/10.1016/j.bbrc.2011.03.083
15. Ullrich S, Su J, Ranta F, Wittekindt OH, Ris F, Rosler M, Gerlach U, Heitzmann D, Warth R, Lang F. Effects of I(Ks) channel inhibitors in insulin-secreting INS-1 cells. Pflugers Archiv : Eur J Physiol 2005; 451:428-36. PMID:16133261. http://dx.doi.org/10.1007/s00424-005-1479-2
16. Mussig K, Staiger H, Machicao F, Kirchhoff K, Guthoff M, Schafer SA, Kantartzis K, Silbernagel G, Stefan N, Holst JJ, et al. Association of type 2 diabetes candidate polymorphisms in KCNQ1 with incretin and insulin secretion. Diabetes 2009; 58:1715-20. PMID:19366866. http://dx.doi.org/10.2337/db08-1589
17. Boini KM, Graf D, Hennige AM, Koka S, Kempe DS, Wang K, Ackermann TF, Foller M, Vallon V, Pfeifer K, et al. Enhanced insulin sensitivity of gene-targeted mice lacking functional KCNQ1. Am J Physiol Regul, Integr Comp Physiol 2009; 296:R1695-701. PMID:19369585. http://dx.doi.org/10.1152/ajpregu.90839.2008
18. Schroeder BC, Waldegger S, Fehr S, Bleich M, Warth R, Greger R, Jentsch TJ. A constitutively open potassium channel formed by KCNQ1 and KCNE3. Nature 2000; 403:196-9. PMID:10646604. http://dx.doi.org/10.1038/35003200
19. Neal AM, Taylor HC, Millar ID, Kibble JD, White SJ, Robson L. Renal defects in KCNE1 knockout mice are mimicked by chromanol 293B in vivo: identification of a KCNE1-regulated KC conductance in the proximal tubule. J Physiol 2011; 589:3595-609. PMID:21576273. http://dx.doi.org/10.1113/jphysiol.2011.209155
20. Warth R, Garcia Alzamora M, Kim JK, Zdebik A, Nitschke R, Bleich M, Gerlach U, Barhanin J, Kim SJ. The role of KCNQ1/KCNE1 K(C) channels in intestine and pancreas: lessons from the KCNE1 knockout mouse. Pflugers Archiv : Eur J Physiol 2002; 443:822-8. PMID:11889581. http://dx.doi.org/10.1007/s00424-001-0751-3
21. Rogers GJ, Tolhurst G, Ramzan A, Habib AM, Parker HE, Gribble FM, Reimann F. Electrical activity-triggered glucagon-like peptide-1 secretion from primary murine L-cells. J Physiol 2011; 589:1081-93. PMID:21224236. http://dx.doi.org/10.1113/jphysiol.2010.198069
22. Preston P, Wartosch L, Gunzel D, Fromm M, Kongsuphol P, Ousingsawat J, Kunzelmann K, Barhanin J, Warth R, Jentsch TJ. Disruption of the KC channel beta-subunit KCNE3 reveals an important role in intestinal and tracheal Cl-transport. J Biol Chemi 2010; 285:7165-75. PMID:20051516. http://dx.doi.org/10.1074/jbc.M109.047829
23. MacDonald PE, El-Kholy W, Riedel MJ, Salapatek AM, Light PE, Wheeler MB. The multiple actions of GLP-1 on the process of glucose-stimulated insulin secretion. Diabetes 2002; 51 Suppl 3:S434-42. http://dx.doi.org/10.2337/diabetes.51.2007.S434
24. Finol-Urdaneta RK, Remedi MS, Raasch W, Becker S, Clark RB, Struver N, Pavlov E, Nichols CG, French RJ, Terlau H. Block of Kv1.7 potassium currents increases glucose-stimulated insulin secretion. EMBO Mol Med 2012; 4:424-34. PMID:22438204. http://dx.doi.org/10.1002/emmm.201200218
25. Drews G, Krippeit-Drews P, Dufer M. Electrophysiology of islet cells. Adv Exp Med Biol 2010; 654:115-63. PMID:20217497. http://dx.doi.org/10.1007/978-90-481-3271-3_7
26. Wang H, Iguchi N, Rong Q, Zhou M, Ogunkorode M, Inoue M, Pribitkin EA, Bachmanov AA, Margolskee RF, Pfeifer K, et al. Expression of the voltage-gated potassium channel KCNQ1 in mammalian taste bud cells and the effect of its null-mutation on taste preferences. J Comp Neurol 2009; 512:384-98. PMID:19006182. http://dx.doi.org/10.1002/cne.21899
27. Lee WK, Torchalski B, Roussa E, Thevenod F. Evidence for KCNQ1 KC channel expression in rat zymogen granule membranes and involvement in cholecystokinin-induced pancreatic acinar secretion. Am J Physiol Cell Physiol 2008; 294:C879-92. PMID:18216164. http://dx.doi.org/10.1152/ajpcell.00490.2007
28. van Vliet-Ostaptchouk JV, van Haeften TW, Landman GW, Reiling E, Kleefstra N, Bilo HJ, Klungel OH, de Boer A, van Diemen CC, Wijmenga C, et al. Common variants in the type 2 diabetes KCNQ1 gene are associated with impairments in insulin secretion during hyperglycaemic glucose clamp. PloS One 2012; 7: e32148. PMID:22403629. http://dx.doi.org/10.1371/journal.pone.0032148
29. Torekov SS, Iepsen E, Christiansen M, Linneberg A, Pedersen O, Holst JJ, Kanters JK, Hansen T. KCNQ1 Long QT syndrome patients have hyperinsulinemia and symptomatic hypoglycemia. Diabetes 2013. PMID:24357532
30. Seino S, Shibasaki T, Minami K. Dynamics of insulin secretion and the clinical implications for obesity and diabetes. J Clin Invest 2011; 121:2118-25. PMID:21633180. http://dx.doi.org/10.1172/JCI45680
31. Lerche C, Bruhova I, Lerche H, Steinmeyer K, Wei AD, Strutz-Seebohm N, Lang F, Busch AE, Zhorov BS, Seebohm G. Chromanol 293B binding in KCNQ1 (Kv7.1) channels involves electrostatic interactions with a potassium ion in the selectivity filter. Mol Pharmacol 2007; 71:1503-11. PMID:17347319. http://dx.doi.org/10.1124/mol.106.031682
32. Caicedo A. Paracrine and autocrine interactions in the human islet: more than meets the eye. Semin Cell Dev Biol 2013; 24:11-21. PMID:23022232. http://dx.doi.org/10.1016/j.semcdb.2012.09.007
33. Parker HE, Adriaenssens A, Rogers G, Richards P, Koepsell H, Reimann F, Gribble FM. Predominant role of active versus facilitative glucose transport for glucagon-like peptide-1 secretion. Diabetologia 2012; 55:2445-55. PMID:22638549. http://dx.doi.org/10.1007/s00125-012-2585-2
34. Diakogiannaki E, Gribble FM, Reimann F. Nutrient detection by incretin hormone secreting cells. Physiol Behav 2012; 106:387-93. PMID:22182802. http://dx.doi.org/10.1016/j.physbeh.2011.12.001
35. Purtell K, Paroder-Belenitsky M, Reyna-Neyra A, Nicola JP, Koba W, Fine E, Carrasco N, Abbott GW. The KCNQ1-KCNE2 K(C) channel is required for adequate thyroid I(-) uptake. FASEB J 2012; 26:3252-9. PMID:22549510. http://dx.doi.org/10.1096/fj.12-206110
36. Sun ZQ, Thomas GP, Antzelevitch C. Chromanol 293B inhibits slowly activating delayed rectifier and transient outward currents in canine left ventricular myocytes. J Cardiovasc Electrophysiol 2001; 12:472-8. PMID:11332571. http://dx.doi.org/10.1046/j.1540-8167.2001.00472.x
37. Bachmann A, Quast U, Russ U. Chromanol 293B, a blocker of the slow delayed rectifier KC current (IKs), inhibits the CFTR Cl-current. Naunyn-Schmiedeberg’s archives Pharmacol 2001; 363:590-6. PMID:11414653. http://dx.doi.org/10.1007/s002100100410
38. Li DS, Yuan YH, Tu HJ, Liang QL, Dai LJ. A protocol for islet isolation from mouse pancreas. Nat Protoc 2009; 4:1649-52. PMID:19876025. http://dx.doi.org/10.1038/nprot.2009.150
39. Taylor BL, Liu FF, Sander M. Nkx6.1 is essential for maintaining the functional state of pancreatic beta cells. Cell Reports 2013; 4:1262-75. PMID:24035389. http://dx.doi.org/10.1016/j.celrep.2013.08.010
40. Marguet D, Baggio L, Kobayashi T, Bernard AM, Pierres M, Nielsen PF, Ribel U, Watanabe T, Drucker DJ, Wagtmann N. Enhanced insulin secretion and improved glucose tolerance in mice lacking CD26. Proc Nat Acad Sci U S A 2000; 97:6874-9. PMID:10823914. http://dx.doi.org/10.1073/pnas.120069197