Insulin secretion and Ca2+ dynamics in β-cells are regulated by PERK (EIF2AK3) in concert with calcineurin

Journal of Biological Chemistry

Volumn 288, Issue 47, 2013, Pages 33824-33836

  Wang, Rong ^a   McGrath, Barbara C ^a   Kopp, Richard F ^b   Roe, Michael W ^b   Tang, Xin ^a   Chen, Gong ^a   Cavener, Douglas R ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b SUNY UPSTATE MEDICAL UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATP-ASE ACTIVITY; ENDOPLASMIC RETICULUM; GENETIC ABLATION; INSULIN SECRETION; PHARMACOLOGICAL INHIBITION; PROTEIN KINASE; SARCOPLASMIC; SPECIFIC INHIBITORS;

ABLATION; CALCIUM; CELL MEMBRANES; CYTOLOGY; DEFECTS; ENZYME INHIBITION; INSULIN; PHYSIOLOGY;

CELL SIGNALING;

CALCINEURIN; PROTEIN KINASE R; PROTEIN KINASE R LIKE ENDOPLASMIC RETICULUM KINASE; UNCLASSIFIED DRUG; CALCIUM; EIF2AK3 PROTEIN, HUMAN; INSULIN; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; PERK KINASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; B LYMPHOCYTE; CALCIUM METABOLISM; CALCIUM SIGNALING; CALCIUM TRANSPORT; CONTROLLED STUDY; DIABETES MELLITUS; ENDOPLASMIC RETICULUM; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME REGULATION; HUMAN; HUMAN CELL; HUMAN TISSUE; INSULIN RELEASE; NONHUMAN; PRIORITY JOURNAL; RAT; STIMULUS SECRETION COUPLING; ANIMAL; CALCIUM DYNAMICS; CALCIUM IMAGING; CELL LINE; CYTOLOGY; ENDOPLASMIC RETICULUM STRESS; GENETICS; METABOLISM; MOUSE; MUTANT MOUSE STRAIN; PANCREAS ISLET BETA CELL; PERK; PERK KINASE; PHYSIOLOGY; SARCOPLASMIC ENDOPLASMIC RETICULUM-CALCIUM ATPASE; SARCOPLASMIC RETICULUM; SECRETION (PROCESS); SPRAGUE DAWLEY RAT; STORE-OPERATED CALCIUM ENTRY;

CALCINEURIN; CALCIUM DYNAMICS; CALCIUM IMAGING; DIABETES; ER STRESS; INSULIN SECRETION; PERK; SARCOPLASMIC ENDOPLASMIC RETICULUM-CALCIUM ATPASE; STORE-OPERATED CALCIUM ENTRY;

ANIMALS; CALCINEURIN; CALCIUM; CALCIUM SIGNALING; CELL LINE; EIF-2 KINASE; HUMANS; INSULIN; INSULIN-SECRETING CELLS; MICE; MICE, MUTANT STRAINS; RATS; RATS, SPRAGUE-DAWLEY; SARCOPLASMIC RETICULUM; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES;

EID: 84888385616     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.503664     Document Type: Article

References (57)

1. Straub, S. G., and Sharp, G. W. (2002) Glucose-stimulated signaling pathways in biphasic insulin secretion. Diabetes Metab. Res. Rev. 18, 451-463
2. Henquin, J. C. (2000) Triggering and amplifying pathways of regulation of insulin secretion by glucose. Diabetes 49, 1751-1760
3. Uchida, K., and Tominaga, M. (2011) The role of thermosensitive TRP (transient receptor potential) channels in insulin secretion. Endocr. J. 58, 1021-1028
4. c and role of SERCA2b and SERCA3. Diabetes 60, 2533-2545
5. Kono, T., Ahn, G., Moss, D. R., Gann, L., Zarain-Herzberg, A., Nishiki, Y., Fueger, P. T., Ogihara, T., and Evans-Molina, C. (2012) PPAR-7 activation restores pancreatic islet SERCA2 levels and prevents beta-cell dysfunction under conditions of hyperglycemic and cytokine stress. Mol. Endocrinol. 26, 257-271
6. Evans-Molina, C., Robbins, R. D., Kono, T., Tersey, S. A., Vestermark, G. L., Nunemaker, C. S., Garmey, J. C., Deering, T. G., Keller, S. R., Maier, B., and Mirmira, R. G. (2009) Peroxisomeproliferator-activatedreceptor 7 activation restores islet function in diabetic mice through reduction of endoplasmic reticulum stress and maintenance of euchromatin structure. Mol. Cell. Biol. 29, 2053-2067
7. 2+, leading to induction of endoplasmic reticulum stress in pancreatic beta-cells. Diabetes 54, 452-461
8. Chen, L., Koh, D. S., and Hille, B. (2003) Dynamics of calcium clearance in mouse pancreatic beta-cells. Diabetes 52, 1723-1731
9. Ahrén, B. (2000) Autonomic regulation of islet hormone secretion. Implications for health and disease. Diabetologia 43, 393-410
10. Gilon, P., and Henquin, J. C. (2001) Mechanisms and physiological significance of the cholinergic control of pancreatic beta-cell function. Endocr. Rev. 22, 565-604
11. 2+ entry in insulin-releasing pancreatic beta-cells. Cell Calcium 22, 277-286
12. Delépine, M., Nicolino, M., Barrett, T., Golamaully, M., Lathrop, G. M., and Julier, C. (2000) EIF2AK3, encoding translation initiation factor 2-α kinase 3, is mutated in patients with Wolcott-Rallison syndrome. Nat. Genet. 25, 406-409
13. -/- mice reveals a role for translational control in secretory cell survival. Mol. Cell 7, 1153-1163
14. Zhang, P., McGrath, B., Li, S., Frank, A., Zambito, F., Reinert, J., Gannon, M., Ma, K., McNaughton, K., and Cavener, D. R. (2002) The PERK eukaryotic initiation factor 2a kinase is required for the development of the skeletal system, postnatal growth, and the function and viability of the pancreas. Mol. Cell. Biol. 22, 3864-3874
15. Shi, Y., Vattem, K. M., Sood, R., An, J., Liang, J., Stramm, L., and Wek, R. C. (1998) Identification and characterization of pancreatic eukaryotic initiation factor 2 α-subunit kinase, PEK, involved in translational control. Mol. Cell. Biol. 18, 7499-7509
16. Harding, H. P., Zhang, Y., and Ron, D. (1999) Protein translation and folding are coupled by an endoplasmic-reticulum-resident kinase. Nature 397, 271-274
17. Harding, H. P., Zhang, Y., Bertolotti, A., Zeng, H, and Ron, D. (2000) Perk is essential for translational regulation and cell survival during the unfolded protein response. Mol. Cell 5, 897-904
18. Cavener, D. R., Gupta, S., and McGrath, B. C. (2010) PERK in beta cell biology and insulin biogenesis. Trends Endocrinol. Metab. 21, 714-721
19. Zhang, W., Feng, D., Li, Y., Iida, K., McGrath, B., and Cavener, D. R. (2006) PERK EIF2AK3 control of pancreatic beta cell differentiation and proliferation is required for postnatal glucose homeostasis. Cell Metab. 4, 491-497
20. Gupta, S., McGrath, B., and Cavener, D. R. (2010) PERK (EIF2AK3) regulates proinsulin trafficking and quality control in the secretory pathway. Diabetes 59, 1937-1947
21. Senée, V., Vattem, K. M., Delépine, M., Rainbow, L. A., Haton, C, Lecoq, A., Shaw, N. J., Robert, J. J., Rooman, R., Diatloff-Zito, C, Michaud, J. L., Bin-Abbas, B., Taha, D., Zabel, B., Franceschini, P., Topaloglu, A. K., Lathrop, G. M., Barrett, T. G., Nicolino, M., Wek, R. C, and Julier, C. (2004) Wolcott-Rallison Syndrome. Clinical, genetic, and functional study of EIF2AK3 mutations and suggestion of genetic heterogeneity. Diabetes 53, 1876-1883
22. Axten, J. M., Medina, J. R., Feng, Y., Shu, A., Romeril, S. P., Grant, S. W., Li, W. H, Heerding, D. A., Minthorn, E., Mencken, T., Atkins, C, Liu, Q., Rabindran, S., Kumar, R., Hong, X., Goetz, A., Stanley, T., Taylor, J. D., Sigethy, S. D., Tomberlin, G. H, Hassell, A. M., Kahler, K. M., Shewchuk, L. M., and Gampe, R. T. (2012) Discovery of 7-methyl-5-(1-{[3-(trifluoromethyl) phenyl]acetyl}-2, 3-dihydro-1H-indol-5-yl)-7H-p yrrolo[2, 3-d]pyrimidin-4-amine (GSK2606414), a potent and selective first-in-class inhibitor of protein kinase R (PKR)-like endoplasmic reticulum kinase (PERK). J. Med. Chem. 55, 7193-7207
23. Atkins, C, Liu, Q., Minthorn, E., Zhang, S. Y., Figueroa, D. J., Moss, K., Stanley, T. B., Sanders, B., Goetz, A., Gaul, N, Choudhry, A. E., Alsaid, H, Jucker, B. M., Axten, J. M., and Kumar, R. (2013) Characterization of a novel PERK kinase inhibitor with anti-tumor and anti-angiogenic activity. Cancer Res., 73, 1993-2002
24. Heit, J. J. (2007) Calcineurin/NFAT signaling in the beta-cell. From diabetes to new therapeutics. Bioessays 29, 1011-1021
25. Goodyer, W. R., Gu, X., Liu, Y., Bottino, R., Crabtree, G. R., and Kim, S. K. (2012) Neonatal beta cell development in mice and humans is regulated by calcineurin/NFAT. Dev. Cell 23, 21-34
26. Bollo, M., Paredes, R. M., Holstein, D., Zheleznova, N, Camacho, P., and Lechleiter, J. D. (2010) Calcineurin interacts with PERK and dephosphorylates calnexin to relieve ER stress in mammals and frogs. PloS One 5, e11925
27. Feng, D., Wei, J., Gupta, S., McGrath, B. C, and Cavener, D. R. (2009) Acute ablation of PERK results in ER dysfunctions followed by reduced insulin secretion and cell proliferation. BMC Cell Biol. 10, 61
28. Kitamura, T., Kido, Y., Nef, S., Merenmies, J., Parada, L. F., and Accili, D. (2001) Preserved pancreatic beta-cell development and function in mice lacking the insulin receptor-related receptor. Mol. Cell. Biol. 21, 5624-5630
29. Quesada, I., Tudurí, E., Ripoll, C, and Nadal, A. (2008) Physiology of the pancreatic alpha-cell and glucagon secretion. Role in glucose homeostasis and diabetes. J. Endocrinol. 199, 5-19
30. Roe, M. W., Fiekers, J. F., Philipson, L. H, and Bindokas, V. P. (2006) Visualizing calcium signaling in cells by digitized wide-field and confocal fluorescent microscopy. Methods Mol. Biol. 319, 37-66
31. Moore, C. E., Omikorede, O., Gomez, E., Willars, G. B., and Herbert, T. P. (2011) PERK activation at low glucose concentration is mediated by SERCA pump inhibition and confers preemptive cytoprotection to pancreatic beta-cells. Mol. Endocrinol. 25, 315-326
32. Liang, S. H, Zhang, W., McGrath, B. C, Zhang, P., and Cavener, D. R. (2006) PERK (eIF2α kinase) is required to activate the stress-activated MAPKs and induce the expression of immediate-early genes upon disruption of ER calcium homoeostasis. Biochem. J. 393, 201-209
33. Islam, M. S. (2010) Calcium signaling in the islets. Adv. Exp. Med. Biol. 654, 235-259
34. Berridge, M. J. (2002) The endoplasmic reticulum. A multifunctional signaling organelle. Cell Calcium 32, 235-249
35. 2+ release. FASEBJ. 16, 1145-1150
36. Bird, G. S., De Haven, W. I., Smyth, J. T., and Putney, J. W., Jr. (2008) Methods for studying store-operated calcium entry. Methods 46, 204-212
37. 2+ analyzed with an improved genetically encoded fluorescent sensor. Proc. Natl. Acad. Sci. U. S. A. 101, 17404-17409
38. 2+ oscillations via an interaction with SERCA2b. J. Cell Biol. 149, 1235-1248
39. Turner, H, Gomez, M., McKenzie, E., Kirchem, A., Lennard, A., and Cantrell, D. A. (1998) Rac-1 regulates nuclear factor of activated T cells (NFAT) C1 nuclear translocation in response to Fce receptor type 1 stimulation of mast cells. J. Exp. Med. 188, 527-537
40. Hogan, P. G., Chen, L., Nardone, J., and Rao, A. (2003) Transcriptional regulation by calcium, calcineurin, and NFAT. Genes Dev. 17, 2205-2232
41. Enan, E., and Matsumura, F. (1992) Specific inhibition of calcineurin by type II synthetic pyrethroid insecticides. Biochem. Pharmacol. 43, 1777-1784
42. Tong, L., Song, Y., Jia, Z., Zhang, W., and Wei, Q. (2007) Calmodulin-dependent activation of calcineurin by chlorogenic acid. IUBMB Life 59, 402-407
43. Aguilar-Bryan, L., and Bryan, J. (2008) Neonatal diabetes mellitus. Endocr. Rev. 29, 265-291
44. Rubio-Cabezas, O., Patch, A. M., Minton, J. A., Flanagan, S. E., Edghill, E. L., Hussain, K., Balafrej, A., Deeb, A., Buchanan, C. R., Jefferson, I. G., Mutair, A., Neonatal Diabetes International Collaborative Group, Hattersley, A. T., and Ellard, S. (2009) Wolcott-Rallison syndrome is the most common genetic cause of permanent neonatal diabetes in consanguineous families. J. Clin. Endocrinol. Metab. 94, 4162-4170
45. 2+ in pancreatic beta-cells exhibits graded dependence on the filling of the endoplasmic reticulum. J. Cell Sci. 114, 2179-2186
46. Tamarina, N. A., Kuznetsov, A., and Philipson, L. H. (2008) Reversible translocation of EYFP-tagged STIM1 is coupled to calcium influx in insulin secreting beta-cells. Cell Calcium 44, 533-544
47. Jacobson, D. A., and Philipson, L. H. (2007) TRP channels of the pancreatic beta cell. Handb. Exp. Pharmacol. 179, 409-424
48. 2+ in insulin-secreting beta-cells. J. Cell Sci. 118, 4463-4471
49. Togashi, K., Inada, H., and Tominaga, M. (2008) Inhibition of the transient receptor potential cation channel TRPM2 by 2-aminoethoxydiphenyl borate (2-APB). Br. J. Pharmacol. 153, 1324-1330
50. Putney, J. W., Jr. (1986) A model for receptor-regulated calcium entry. Cell Calcium 7, 1-12
51. Trinh, M. A., Kaphzan, H., Wek, R. C, Pierre, P., Cavener, D. R., and Klann, E. (2012) Brain-specific disruption of the eIF2α kinase PERK decreases ATF4 expression and impairs behavioral flexibility. Cell Rep. 1, 676-688
52. Scheuner, D., Song, B., McEwen, E., Liu, C, Laybutt, R., Gillespie, P., Saunders, T., Bonner-Weir, S., and Kaufman, R. J. (2001) Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol. Cell 7, 1165-1176
53. Bollo, M., Paredes, R. M., Holstein, D., Zheleznova, N., Camacho, P., and Lechleiter, J. D. (2010) Calcineurin interacts with PERK and dephosphorylates calnexin to relieve ER stress in mammals and frogs. PLoS One 5, e11925
54. Gill, D. L., and Patterson, R. L. (2004) Toward a consensus on the operation of receptor-induced calcium entry signals. Sci. STKE 2004, pe39
55. Bertolotti, A., Zhang, Y., Hendershot, L. M., Harding, H. P., and Ron, D. (2000) Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat. Cell. Biol. 2, 326-332
56. Llinás, R., Steinberg, I. Z., and Walton, K. (1981) Relationship between presynaptic calcium current and postsynaptic potential in squid giant synapse. Biophys. J. 33, 323-351
57. Shaw, J. A., Matlovich, N., Rushlow, W., Cain, P., and Rajakumar, N. (2012) Role of calcineurin in inhibiting disadvantageous associations. Neuroscience 203, 144-152