Concerted trafficking regulation of Kv2.1 and KATP channels by leptin in pancreatic β-cells

Journal of Biological Chemistry

Volumn 290, Issue 50, 2015, Pages 29676-29690

  Wu, Yi ^a   Shyng, Show Ling ^a   Chen, Pei Chun ^b  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOLOGY; PROTEINS;

BETA CELL; CHANNEL DENSITY; LEPTIN SIGNALING; PANCREATIC BETA CELLS;

HORMONES;

ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE KINASE; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE KINASE BETA; CALCIUM ION; CYCLIC AMP DEPENDENT PROTEIN KINASE; GLUCOSE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; LEPTIN; POTASSIUM CHANNEL KV2.1; SODIUM ION; UNCLASSIFIED DRUG; VOLTAGE GATED POTASSIUM CHANNEL; ADENYLATE KINASE; CALCIUM; INSULIN; MITOCHONDRIAL K(ATP) CHANNEL; POTASSIUM CHANNEL; SHAB POTASSIUM CHANNEL; SODIUM;

ACTION POTENTIAL; ANIMAL CELL; ARTICLE; CELL MEMBRANE DEPOLARIZATION; CELL MEMBRANE POTENTIAL; CELL MIGRATION; CELL SURFACE; CONTROLLED STUDY; DEPOLYMERIZATION; HUMAN; HUMAN CELL; HYPERPOLARIZATION; INSULIN RELEASE; NONHUMAN; PANCREAS ISLET BETA CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPOLARIZATION; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; CELL LINE; CYTOLOGY; DRUG EFFECTS; METABOLISM; PANCREAS ISLET; PROTEIN TRANSPORT; SECRETION (PROCESS);

ADENYLATE KINASE; ANIMALS; CALCIUM; CELL LINE; CYCLIC AMP-DEPENDENT PROTEIN KINASES; HUMANS; INSULIN; ISLETS OF LANGERHANS; LEPTIN; POTASSIUM CHANNELS; PROTEIN TRANSPORT; SHAB POTASSIUM CHANNELS; SODIUM;

EID: 84949668664     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.670877     Document Type: Article

References (63)

1. Jacobson, D. A., and Philipson, L. H. (2007) Action potentials and insulin secretion: new insights into the role of Kv channels. Diabetes Obes. Metab. 9, 89-98
2. Rorsman, P., and Braun, M. (2013) Regulation of insulin secretion in human pancreatic islets. Annu. Rev. Physiol. 75, 155-179
3. Yang, S. N., Shi, Y., Yang, G., Li, Y., Yu, J., and Berggren, P. O. (2014) Ionic mechanisms in pancreatic beta cell signaling. Cell. Mol. life Sci. 71, 4149-4177
4. Aguilar-Bryan, L., and Bryan, J. (1999) Molecular biology of adenosine triphosphate-sensitive potassium channels. Endocr. Rev. 20, 101-135
5. Ashcroft, F. M. (2006) K(ATP) channels and insulin secretion: a key role in health and disease. Biochem. Soc. Trans. 34, 243-246
6. Nichols, C. G. (2006) KATP channels as molecular sensors of cellular metabolism. Nature 440, 470-476
7. Ashcroft, F. M. (2005) ATP-sensitive potassium channelopathies: focus on insulin secretion. J. Clin. Invest. 115, 2047-2058
8. Yan, L., Figueroa, D. J., Austin, C. P., Liu, Y., Bugianesi, R. M., Slaughter, R. S., Kaczorowski, G. J., and Kohler, M. G. (2004) Expression of voltagegated potassium channels in human and rhesus pancreatic islets. Diabetes 53, 597-607
9. Tamarina, N. A., Kuznetsov, A., Fridlyand, L. E., and Philipson, L. H. (2005) Delayed-rectifier (KV2.1) regulation of pancreatic beta-cell calcium responses to glucose: inhibitor specificity and modeling. Am. J. Physiol. Endocrinol. Metab. 289, E578-E585
10. Jacobson, D. A., Kuznetsov, A., Lopez, J. P., Kash, S., Ammälä, C. E., and Philipson, L. H. (2007) Kv2.1 ablation alters glucose-induced islet electrical activity, enhancing insulin secretion. Cell Metab. 6, 229-235
11. Komatsu, M., Takei, M., Ishii, H., and Sato, Y. (2013) Glucose-stimulated insulin secretion: a newer perspective. J. Diabetes Investig. 4, 511-516
12. Kieffer, T. J., Heller, R. S., Leech, C. A., Holz, G. G., and Habener, J. F. (1997) Leptin suppression of insulin secretion by the activation of ATPsensitive K+ channels in pancreatic beta-cells. Diabetes 46, 1087-1093
13. Chen, P. C., Kryukova, Y. N., and Shyng, S. L. (2013) Leptin regulates KATP channel trafficking in pancreatic beta-cells by a signaling mechanism involving AMP-activated protein kinase (AMPK) and cAMP-dependent protein kinase (PKA). J. Biol. Chem. 288, 34098-34109
14. Park, S. H., Ryu, S. Y., Yu, W. J., Han, Y. E., Ji, Y. S., Oh, K., Sohn, J. W., Lim, A., Jeon, J. P., Lee, H., Lee, K. H., Lee, S. H., Berggren, P. O., Jeon, J. H., and Ho, W. K. (2013) Leptin promotes K(ATP) channel trafficking by AMPK signaling in pancreatic beta-cells. Proc. Natl. Acad. Sci. U.S.A. 110, 12673-12678
15. Hohmeier, H. E., BeltrandelRio, H., Clark, S. A., Henkel-Rieger, R., Normington, K., and Newgard, C. B. (1997) Regulation of insulin secretion from novel engineered insulinoma cell lines. Diabetes 46, 968-977
16. Jensen, M. V., Haldeman, J. M., Zhang, H., Lu, D., Huising, M. O., Vale, W. W., Hohmeier, H. E., Rosenberg, P., and Newgard, C. B. (2013) Control of voltage-gated potassium channel Kv2.2 expression by pyruvate-isocitrate cycling regulates glucose-stimulated insulin secretion. J. Biol. Chem. 288, 23128-23140
17. Bokvist, K., Rorsman, P., and Smith, P. A. (1990) Effects of external tetraethylammonium ions and quinine on delayed rectifying K+ channels in mouse pancreatic beta-cells. J. Physiol. 423, 311-325
18. Escoubas, P., Diochot, S., Célérier, M. L., Nakajima, T., and Lazdunski, M. (2002) Novel tarantula toxins for subtypes of voltage-dependent potassium channels in the Kv2 and Kv4 subfamilies. Mol. Pharmacol. 62, 48-57
19. Baver, S. B., Hope, K., Guyot, S., Bjørbaek, C., Kaczorowski, C., and O'Connell, K. M. (2014) Leptin modulates the intrinsic excitability of AgRP/NPY neurons in the arcuate nucleus of the hypothalamus. J. Neurosci. 34, 5486-5496
20. Ashcroft, F. M., Kelly, R. P., and Smith, P. A. (1990) Two types of Ca channel in rat pancreatic beta-cells. Pflugers Arch. 415, 504-506
21. Satin, L. S., and Cook, D. L. (1988) Evidence for two calcium currents in insulin-secreting cells. Pflugers Arch. 411, 401-409
22. Sher, E., Giovannini, F., Codignola, A., Passafaro, M., Giorgi-Rossi, P., Volsen, S., Craig, P., Davalli, A., and Carrera, P. (2003) Voltage-operated calcium channel heterogeneity in pancreatic beta cells: physiopathological implications. J. Bioenerg. Biomembr. 35, 687-696
23. Hardie, D. G., Ross, F. A., and Hawley, S. A. (2012) AMP-activated protein kinase: a target for drugs both ancient and modern. Chem. Biol. 19, 1222-1236
24. Ning, K., Miller, L. C., Laidlaw, H. A., Burgess, L. A., Perera, N. M., Downes, C. P., Leslie, N. R., and Ashford, M. L. (2006) A novel leptin signalling pathway via PTEN inhibition in hypothalamic cell lines and pancreatic beta-cells. EMBO J. 25, 2377-2387
25. Holzinger, A. (2009) Jasplakinolide: an actin-specific reagent that promotes actin polymerization. Methods Mol. Biol. 586, 71-87
26. Ashcroft, F. M., Rorsman, P., and Trube, G. (1989) Single calcium channel activity in mouse pancreatic beta-cells. Ann. N. Y. Acad. Sci. 560, 410-412
27. Göpel, S., Kanno, T., Barg, S., Galvanovskis, J., and Rorsman, P. (1999) Voltage-gated and resting membrane currents recorded from B-cells in intact mouse pancreatic islets. J. Physiol. 521, 717-728
28. Satin, L. S., and Cook, D. L. (1985) Voltage-gated Ca2+ current in pancreatic B-cells. Pflugers Arch. 404, 385-387
29. Smolen, P., Rinzel, J., and Sherman, A. (1993) Why pancreatic islets burst but single beta cells do not. The heterogeneity hypothesis. Biophys. J. 64, 1668-1680
30. Rorsman, P., and Trube, G. (1986) Calcium and delayed potassium currents in mouse pancreatic beta-cells under voltage clamp conditions. J. Physiol. 374, 531-550
31. Braun, M., Ramracheya, R., Bengtsson, M., Zhang, Q., Karanauskaite, J., Partridge, C., Johnson, P. R., and Rorsman, P. (2008) Voltage-gated ion channels in human pancreatic beta-cells: electrophysiological characterization and role in insulin secretion. Diabetes 57, 1618-1628
32. Houamed, K. M., Sweet, I. R., and Satin, L. S. (2010) BK channels mediate a novel ionic mechanism that regulates glucose-dependent electrical activity and insulin secretion in mouse pancreatic beta-cells. J. Physiol. 588, 3511-3523
33. Jacobson, D. A., Mendez, F., Thompson, M., Torres, J., Cochet, O., and Philipson, L. H. (2010) Calcium-activated and voltage-gated potassium channels of the pancreatic islet impart distinct and complementary roles during secretagogue induced electrical responses. J. Physiol. 588, 3525-3537
34. Herrington, J., Sanchez, M., Wunderler, D., Yan, L., Bugianesi, R. M., Dick, I. E., Clark, S. A., Brochu, R. M., Priest, B. T., Kohler, M. G., and McManus, O. B. (2005) Biophysical and pharmacological properties of the voltagegated potassium current of human pancreatic beta-cells. J. Physiol. 567, 159-175
35. MacDonald, P. E., Ha, X. F., Wang, J., Smukler, S. R., Sun, A. M., Gaisano, H. Y., Salapatek, A. M., Backx, P. H., and Wheeler, M. B. (2001) Members of the Kv1 and Kv2 voltage-dependent K+ channel families regulate insulin secretion. Mol. Endocrinol. 15, 1423-1435
36. Park, S. H., Ho, W. K., and Jeon, J. H. (2013) AMPK regulates K(ATP) channel trafficking via PTEN inhibition in leptin-treated pancreatic betacells. Biochem. Biophys. Res. Commun. 440, 539-544
37. Kieffer, T. J., and Habener, J. F. (2000) The adipoinsular axis: effects of leptin on pancreatic beta-cells. Am. J. Physiol. Endocrinol. Metab. 278, E1-E14
38. Harvey, J., and Ashford, M. L. (1998) Insulin occludes leptin activation of ATP-sensitive K+ channels in rat CRI-G1 insulin secreting cells. J. Physiol. 511, 695-706
39. Harvey, J., and Ashford, M. L. (1998) Role of tyrosine phosphorylation in leptin activation of ATP-sensitive K+ channels in the rat insulinoma cell line CRI-G1. J. Physiol. 510, 47-61
40. Harvey, J., Hardy, S. C., Irving, A. J., and Ashford, M. L. (2000) Leptin activation of ATP-sensitive K+ (KATP) channels in rat CRI-G1 insulinoma cells involves disruption of the actin cytoskeleton. J. Physiol. 527, 95-107
41. Holz, G. G., Chepurny, O. G., and Leech, C. A. (2013) Leptin-stimulated KATP channel trafficking: a new paradigm for beta-cell stimulus-secretion coupling? Islets 5, 229-232
42. Li, X. N., Herrington, J., Petrov, A., Ge, L., Eiermann, G., Xiong, Y., Jensen, M. V., Hohmeier, H. E., Newgard, C. B., Garcia, M. L., Wagner, M., Zhang, B. B., Thornberry, N. A., Howard, A. D., Kaczorowski, G. J., and Zhou, Y. P. (2013) The role of voltage-gated potassium channels Kv2.1 and Kv2.2 in the regulation of insulin and somatostatin release from pancreatic islets. J. Pharmacol. Exp. Ther. 344, 407-416
43. MacDonald, P. E., Sewing, S., Wang, J., Joseph, J. W., Smukler, S. R., Sakellaropoulos, G., Wang, J., Saleh, M. C., Chan, C. B., Tsushima, R. G., Salapatek, A. M., and Wheeler, M. B. (2002) Inhibition of Kv2.1 voltagedependent K+ channels in pancreatic beta-cells enhances glucose-dependent insulin secretion. J. Biol. Chem. 277, 44938-44945
44. Roe, M. W., Worley, J. F., 3rd, Mittal, A. A., Kuznetsov, A., DasGupta, S., Mertz, R. J., Witherspoon, S. M., 3rd, Blair, N., Lancaster, M. E., McIntyre, M. S., Shehee, W. R., Dukes, I. D., and Philipson, L. H. (1996) Expression and function of pancreatic beta-cell delayed rectifier K+ channels. Role in stimulus-secretion coupling. J. Biol. Chem. 271, 32241-32246
45. Meda, P. (2003) Cx36 involvement in insulin secretion: characteristics and mechanism. Cell Commun. Adhes. 10, 431-435
46. Head, W. S., Orseth, M. L., Nunemaker, C. S., Satin, L. S., Piston, D. W., and Benninger, R. K. (2012) Connexin-36 gap junctions regulate in vivo first- and second-phase insulin secretion dynamics and glucose tolerance in the conscious mouse. Diabetes 61, 1700-1707
47. Silva, J. R., Cooper, P., and Nichols, C. G. (2014) Modeling K, ATP-dependent excitability in pancreatic islets. Biophys. J. 107, 2016-2026
48. Rocheleau, J. V., Remedi, M. S., Granada, B., Head, W. S., Koster, J. C., Nichols, C. G., and Piston, D. W. (2006) Critical role of gap junction coupled KATP channel activity for regulated insulin secretion. PLoS Biol. 4, e26
49. Benninger, R. K., Zhang, M., Head, W. S., Satin, L. S., and Piston, D. W. (2008) Gap junction coupling and calcium waves in the pancreatic islet. Biophys. J. 95, 5048-5061
50. Lim, A., Park, S. H., Sohn, J. W., Jeon, J. H., Park, J. H., Song, D. K., Lee, S. H., and Ho, W. K. (2009) Glucose deprivation regulates KATP channel trafficking via AMP-activated protein kinase in pancreatic beta-cells. Diabetes 58, 2813-2819
51. Yang, S. N., Wenna, N. D., Yu, J., Yang, G., Qiu, H., Yu, L., Juntti-Berggren, L., Köhler, M., and Berggren, P. O. (2007) Glucose recruits K(ATP) channels via non-insulin-containing dense-core granules. Cell Metab. 6, 217-228
52. Kalsbeek, A., Fliers, E., Romijn, J. A., La Fleur, S. E., Wortel, J., Bakker, O., Endert, E., and Buijs, R. M. (2001) The suprachiasmatic nucleus generates the diurnal changes in plasma leptin levels. Endocrinology 142, 2677-2685
53. Rayner, D. V., and Trayhurn, P. (2001) Regulation of leptin production: sympathetic nervous system interactions. J. Mol. Med. 79, 8-20
54. Szkudelski, T. (2007) Intracellular mediators in regulation of leptin secretion from adipocytes. Physiol. Res. 56, 503-512
55. Cases, J. A., Gabriely, I., Ma, X. H., Yang, X. M., Michaeli, T., Fleischer, N., Rossetti, L., and Barzilai, N. (2001) Physiological increase in plasma leptin markedly inhibits insulin secretion in vivo. Diabetes 50, 348-352
56. Licinio, J., Mantzoros, C., Negrão, A. B., Cizza, G., Wong, M. L., Bongiorno, P. B., Chrousos, G. P., Karp, B., Allen, C., Flier, J. S., and Gold, P. W. (1997) Human leptin levels are pulsatile and inversely related to pituitaryadrenal function. Nat. Med. 3, 575-579
57. Geng, X., Li, L., Watkins, S., Robbins, P. D., and Drain, P. (2003) The insulin secretory granule is the major site of K(ATP) channels of the endocrine pancreas. Diabetes 52, 767-776
58. Varadi, A., Grant, A., McCormack, M., Nicolson, T., Magistri, M., Mitchell, K. J., Halestrap, A. P., Yuan, H., Schwappach, B., and Rutter, G. A. (2006) Intracellular ATP-sensitive K+ channels in mouse pancreatic beta cells: against a role in organelle cation homeostasis. Diabetologia 49, 1567-1577
59. Dai, X. Q., Manning Fox, J. E., Chikvashvili, D., Casimir, M., Plummer, G., Hajmrle, C., Spigelman, A. F., Kin, T., Singer-Lahat, D., Kang, Y., Shapiro, A. M., Gaisano, H. Y., Lotan, I., and Macdonald, P. E. (2012) The voltagedependent potassium channel subunit Kv2.1 regulates insulin secretion from rodent and human islets independently of its electrical function. Diabetologia 55, 1709-1720
60. Pal, S. K., Takimoto, K., Aizenman, E., and Levitan, E. S. (2006) Apoptotic surface delivery of K+ channels. Cell Death Differ. 13, 661-667
61. Kim, S. J., Widenmaier, S. B., Choi, W. S., Nian, C., Ao, Z., Warnock, G., and McIntosh, C. H. (2012) Pancreatic beta-cell prosurvival effects of the incretin hormones involve post-translational modification of Kv2.1 delayed rectifier channels. Cell Death Differ. 19, 333-344
62. Moult, P. R., Cross, A., Santos, S. D., Carvalho, A. L., Lindsay, Y., Connolly, C. N., Irving, A. J., Leslie, N. R., and Harvey, J. (2010) Leptin regulates AMPA receptor trafficking via PTEN inhibition. J. Neurosci. 30, 4088-4101
63. Dhar, M., Wayman, G. A., Zhu, M., Lambert, T. J., Davare, M. A., and Appleyard, S. M. (2014) Leptin-induced spine formation requires TrpC channels and the CaM kinase cascade in the hippocampus. J. Neurosci. 34, 10022-10033