Nifedipine protects INS-1 β-cell from high glucose-induced ER stress and apoptosis

International Journal of Molecular Sciences

Volumn 12, Issue 11, 2011, Pages 7569-7580

  Wang, Yao ^a,b   Gao, Lu ^b   Li, Yuan ^a   Chen, Hong ^a   Sun, Zilin ^a  

^a SOUTHEAST UNIVERSITY   (China)

^b NANJING MEDICAL UNIVERSITY   (China)

Author keywords

cell; Apoptosis; Ca 2+ homeostasis; Endoplasmic reticulum stress; High glucose; Nifedipine

Indexed keywords

CALCIUM CHANNEL BLOCKING AGENT; CALCIUM CHANNEL L TYPE; CALCIUM ION; CASPASE 3; GLUCOSE; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INITIATION FACTOR 2ALPHA; INSULIN; NIFEDIPINE; CALCIUM;

ANIMAL CELL; APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CALCIUM HOMEOSTASIS; CALCIUM TRANSPORT; CELL PROTECTION; CELL VIABILITY; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; INSULIN RELEASE; NONHUMAN; PANCREAS ISLET BETA CELL; PROTEIN EXPRESSION; RAT; ANIMAL; CELL LINE; DRUG EFFECTS; METABOLISM; SECRETION (PROCESS);

ANIMALS; APOPTOSIS; CALCIUM; CALCIUM CHANNEL BLOCKERS; CELL LINE; ENDOPLASMIC RETICULUM STRESS; GLUCOSE; INSULIN; INSULIN-SECRETING CELLS; NIFEDIPINE; RATS;

EID: 82255181748     PISSN: None     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms12117569     Document Type: Article

References (56)

1. Kahn, B.B. Type 2 diabetes: When insulin secretion fails to compensate for insulin resistance. Cell 1998, 92, 593-596.
2. Leonardi, O.; Mints, G.; Hussain, M.A. Beta-cell apoptosis in the pathogenesis of human type 2 diabetes mellitus. Eur. J. Endocrinol. 2003, 149, 99-102.
3. 2+ influx and extracellular signal-regulated kinase (ERK) 1/2 activation and is prevented by a sulfonylurea receptor 1/inwardly rectifying K+ channel 6.2 (SUR/Kir6.2) selective potassium channel opener in human islets. Diabetes 2004, 53, 1706-1713.
4. Fei, H.; Zhao, B.; Zhao, S.; Wang, Q. Requirements of calcium fluxes and ERK kinase activation for glucose- and interleukin-1beta-induced beta-cell apoptosis. Mol. Cell. Biochem. 2008, 315, 75-84.
5. Maedler, K.; Spinas, G.A.; Lehmann, R.; Sergeev, P.; Weber, M.; Fontana, A.; Kaiser, N.; Donath, M.Y. Glucose induces beta-cell apoptosis via upregulation of the Fas receptor in human islets. Diabetes 2001, 50, 1683-1690.
6. Widenmaier, S.B.; Ao, Z.; Kim, S.J.; Warnock, G.; McIntosh, C.H. Suppression of p38 MAPK and JNK via Akt-mediated inhibition of apoptosis signal-regulating kinase 1 constitutes a core component of the beta-cell pro-survival effects of glucose-dependent insulinotropic polypeptide. J. Biol. Chem. 2009, 284, 30372-30382.
7. Zhang, Z.; Liew, C.W.; Handy, D.E.; Zhang, Y.; Leopold, J.A.; Hu, J.; Guo, L.; Kulkarni, R.N.; Loscalzo, J.; Stanton, R.C. High glucose inhibits glucose-6-phosphate dehydrogenase, leading to increased oxidative stress and beta-cell apoptosis. FASEB J. 2010, 24, 1497-1505.
8. Lupi, R.; Dotta, F.; Marselli, L.; del Guerra, S.; Masini, M.; Santangelo, C.; Patane, G.; Boggi, U.; Piro, S.; Anello, M., et al. Prolonged exposure to free fatty acids has cytostatic and pro-apoptotic effects on human pancreatic islets: Evidence that beta-cell death is caspase mediated, partially dependent on ceramide pathway, and Bcl-2 regulated. Diabetes 2002, 51, 1437-1442.
9. Cnop, M.; Ladriere, L.; Igoillo-Esteve, M.; Moura, R.F.; Cunha, D.A. Causes and cures for endoplasmic reticulum stress in lipotoxic beta-cell dysfunction. Diabetes Obes. Metab. 2010, 12, 76-82.
10. Lupi, R.; del Prato, S. Beta-cell apoptosis in type 2 diabetes: Quantitative and functional consequences. Diabetes Metab. 2008, 34, S56-S64.
11. Mooradian, A.D.; Haas, M.J. Glucose-induced endoplasmic reticulum stress is independent of oxidative stress: A mechanistic explanation for the failure of antioxidant therapy in diabetes. Free Radic. Biol. Med. 2011, 50, 1140-1143.
12. Federici, M.; Hribal, M.; Perego, L.; Ranalli, M.; Caradonna, Z.; Perego, C.; Usellini, L.; Nano, R.; Bonini, P.; Bertuzzi, F.; et al. High glucose causes apoptosis in cultured human pancreatic islets of Langerhans: A potential role for regulation of specific Bcl family genes toward an apoptotic cell death program. Diabetes 2001, 50, 1290-1301.
13. Dyntar, D.; Eppenberger-Eberhardt, M.; Maedler, K.; Pruschy, M.; Eppenberger, H.M.; Spinas, G.A.; Donath, M. Y. Glucose and palmitic acid induce degeneration of myofibrils and modulate apoptosis in rat adult cardiomyocytes. Diabetes 2001, 50, 2105-2113.
14. Diakogiannaki, E.; Morgan, N.G. Differential regulation of the ER stress response by long-chain fatty acids in the pancreatic beta-cell. Biochem. Soc. Trans. 2008, 36, 959-962.
15. 2+ release through the c-Jun N-terminal kinase pathway. Mol. Cell. Biochem. 2009, 324, 183-190.
16. Harding, H.P.; Calfon, M.; Urano, F.; Novoa, I.; Ron, D. Transcriptional and translational control in the Mammalian unfolded protein response. Annu. Rev. Cell. Dev. Biol. 2002, 18, 575-599.
17. Zhang, K.; Kaufman, R.J. Signaling the unfolded protein response from the endoplasmic reticulum. J. Biol. Chem. 2004, 279, 25935-25938.
18. Thomas, S.E.; Dalton, L.E.; Daly, M.L.; Malzer, E.; Marciniak, S.J. Diabetes as a disease of endoplasmic reticulum stress. Diabetes Metab. Res. Rev. 2010, 26, 611-621.
19. Oyadomari, S.; Mori, M. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ. 2004, 11, 381-389.
20. Xu, C.; Bailly-Maitre, B.; Reed, J.C. Endoplasmic reticulum stress: Cell life and death decisions. J. Clin. Invest. 2005, 115, 2656-2664.
21. Seino, S.; Shibasaki, T.; Minami, K. Dynamics of insulin secretion and the clinical implications for obesity and diabetes. J. Clin. Invest. 2011, 121, 2118-2125.
22. Ashcroft, S.J.; Ashcroft, F.M. Properties and functions of ATP-sensitive K-channels. Cell. Signal. 1990, 2, 197-214.
23. Chen, M.; He, H.; Zhan, S.; Krajewski, S.; Reed, J.C.; Gottlieb, R.A. Bid is cleaved by calpain to an active fragment in vitro and during myocardial ischemia/reperfusion. J. Biol. Chem. 2001, 276, 30724-30728.
24. 2+-induced apoptosis through calcineurin dephosphorylation of BAD. Science 1999, 284, 339-343.
25. Nunemaker, C.S.; Satin, L.S. Comparison of metabolic oscillations from mouse pancreatic beta cells and islets. Endocrine 2004, 25, 61-67.
26. Ji, Y.; Lu, G.; Chen, G.; Huang, B.; Zhang, X.; Shen, K.; Wu, S. Microcystin-LR Induces Apoptosis via NF-kappaB/iNOS Pathway in INS-1 Cells. Int. J. Mol. Sci. 2011, 12, 4722-4734.
27. Meng, Z.X.; Nie, J.; Ling, J.J.; Sun, J.X.; Zhu, Y.X.; Gao, L.; Lv, J.H.; Zhu, D.Y.; Sun, Y.J.; Han, X. Activation of liver X receptors inhibits pancreatic islet beta cell proliferation through cell cycle arrest. Diabetologia 2009, 52, 125-135.
28. Hu, H.; He, L.Y.; Gong, Z.; Li, N.; Lu, Y.N.; Zhai, Q.W.; Liu, H.; Jiang, H.L.; Zhu, W.L.; Wang, H.Y. A novel class of antagonists for the FFAs receptor GPR40. Biochem. Biophys. Res. Commun. 2009, 390, 557-563.
29. Martinez, S.C.; Tanabe, K.; Cras-Meneur, C.; Abumrad, N.A.; Bernal-Mizrachi, E.; Permutt, M.A. Inhibition of Foxo1 protects pancreatic islet beta-cells against fatty acid and endoplasmic reticulum stress-induced apoptosis. Diabetes 2008, 57, 846-859.
30. 2+ homeostasis in beta-cells. Am. J. Physiol. Endocrinol. Metab. 2009, 296, E690-E701.
31. Laybutt, D.R.; Preston, A.M.; Akerfeldt, M.C.; Kench, J.G.; Busch, A.K.; Biankin, A.V.; Biden, T.J. Endoplasmic reticulum stress contributes to beta cell apoptosis in type 2 diabetes. Diabetologia 2007, 50, 752-763.
32. Rizzuto, R.; Pinton, P.; Ferrari, D.; Chami, M.; Szabadkai, G.; Magalhaes, P.J.; Di Virgilio, F.; Pozzan, T. Calcium and apoptosis: Facts and hypotheses. Oncogene 2003, 22, 8619-8627.
33. Schnell, S.; Schaefer, M.; Schofl, C. Free fatty acids increase cytosolic free calcium and stimulate insulin secretion from beta-cells through activation of GPR40. Mol. Cell. Endocrinol. 2007, 263, 173-180.
34. Wilding, J.P. The importance of free fatty acids in the development of Type 2 diabetes. Diabet. Med. 2007, 24, 934-945.
35. Ammala, C.; Eliasson, L.; Bokvist, K.; Larsson, O.; Ashcroft, F.M.; Rorsman, P. Exocytosis elicited by action potentials and voltage-clamp calcium currents in individual mouse pancreatic B-cells. J. Physiol. 1993, 472, 665-688.
36. 2+ as evidences in single pancreatic islets. J. Biol. Chem. 1993, 268, 22265-22268.
37. Matsuda, Y.; Saegusa, H.; Zong, S.; Noda, T.; Tanabe, T. Mice lacking Ca(v)2.3 (alpha1E) calcium channel exhibit hyperglycemia. Biochem. Biophys. Res. Commun. 2001, 289, 791-795.
38. Ekinci, F.J.; Linsley, M.D.; Shea, T.B. Beta-amyloid-induced calcium influx induces apoptosis in culture by oxidative stress rather than tau phosphorylation. Brain Res. Mol. Brain Res. 2000, 76, 389-395.
39. Sorkin, E.M.; Clissold, S.P.; Brogden, R.N. Nifedipine. A review of its pharmacodynamic and pharmacokinetic properties, and therapeutic efficacy, in ischaemic heart disease, hypertension and related cardiovascular disorders. Drugs 1985, 30, 182-274.
40. 2+ channel blockers verapamil and nifedipine inhibit apoptosis induced by 25-hydroxycholesterol in human aortic smooth muscle cells. J. Lipid Res. 1997, 38, 2049-2061.
41. Sugano, M.; Tsuchida, K.; Makino, N. Nifedipine prevents apoptosis of endothelial cells induced by oxidized low-density lipoproteins. J. Cardiovasc. Pharmacol. 2002, 40, 146-152.
42. 2+ and is tetanus toxin resistant. Cell. Physiol. Biochem. 2010, 26, 197-208.
43. Yang, S.N.; Berggren, P.O. The role of voltage-gated calcium channels in pancreatic beta-cell physiology and pathophysiology. Endocr. Rev. 2006, 27, 621-676.
44. Vasseur, M.; Debuyser, A.; Joffre, M. Sensitivity of pancreatic beta cell to calcium channel blockers. An electrophysiologic study of verapamil and nifedipine. Fundam. Clin. Pharmacol. 1987, 1, 95-113.
45. Jeffrey, K.D.; Alejandro, E.U.; Luciani, D.S.; Kalynyak, T.B.; Hu, X.; Li, H.; Lin, Y.; Townsend, R.R.; Polonsky, K.S.; Johnson, J.D. Carboxypeptidase E mediates palmitate-induced beta-cell ER stress and apoptosis. Proc. Natl. Acad. Sci. USA 2008, 105, 8452-8457.
46. 2+-mediated apoptotic signals in palmitate-induced MIN6N8a beta cell death. Mol. Cell. Endocrinol. 2007, 272, 50-62.
47. Navarro-Tableros, V.; Fiordelisio, T.; Hernandez-Cruz, A.; Hiriart, M. Physiological development of insulin secretion, calcium channels, and GLUT2 expression of pancreatic rat beta-cells. Am. J. Physiol. Endocrinol. Metab. 2007, 292, E1018-E1029.
48. Nolan, C.J.; Madiraju, M.S.; Delghingaro-Augusto, V.; Peyot, M.L.; Prentki, M. Fatty acid signaling in the beta-cell and insulin secretion. Diabetes 2006, 55, S16-S23.
49. Tamareille, S.; Mignen, O.; Capiod, T.; Rucker-Martin, C.; Feuvray, D. High glucose-induced apoptosis through store-operated calcium entry and calcineurin in human umbilical vein endothelial cells. Cell Calcium 2006, 39, 47-55.
50. Rudijanto, A. Calcium channel blocker (diltiazem) inhibits apoptosis of vascular smooth muscle cell exposed to high glucose concentration through lectin-like oxidized low density lipoprotein receptor-1 (LOX-1) pathway. Acta Med. Indones. 2010, 42, 59-65.
51. Prentki, M.; Nolan, C.J. Islet beta cell failure in type 2 diabetes. J. Clin. Invest. 2006, 116, 1802-1812.
52. Shafrir, E. Development and consequences of insulin resistance: Lessons from animals with hyperinsulinaemia. Diabetes Metab. 1996, 22, 122-131.
53. Karaskov, E.; Scott, C.; Zhang, L.; Teodoro, T.; Ravazzola, M.; Volchuk, A. Chronic palmitate but not oleate exposure induces endoplasmic reticulum stress, which may contribute to INS-1 pancreatic beta-cell apoptosis. Endocrinology 2006, 147, 3398-3407.
54. Taylor, J.T.; Huang, L.; Keyser, B.M.; Zhuang, H.; Clarkson, C.W.; Li, M. Role of high-voltage-activated calcium channels in glucose-regulated beta-cell calcium homeostasis and insulin release. Am. J. Physiol. Endocrinol. Metab. 2005, 289, E900-E908.
55. Yang, M.; Chisholm, J.W.; Soelaiman, S.; Shryock, J.C. Sulfonylureas uncouple glucose- dependence for GPR40-mediated enhancement of insulin secretion from INS-1E cells. Mol. Cell. Endocrinol. 2010, 315, 308-313.
56. Yang, J.; Robert, C.E.; Burkhardt, B.R.; Young, R.A.; Wu, J.; Gao, Z.; Wolf, B.A. Mechanisms of glucose-induced secretion of pancreatic-derived factor (PANDER or FAM3B) in pancreatic beta-cells. Diabetes 2005, 54, 3217-3228.