Losartan, an angiotensin II type 1 receptor blocker, protects human islets from glucotoxicity through the phospholipase C pathway

FASEB Journal

Volumn 27, Issue 12, 2013, Pages 5122-5130

  Madec, Anne Marie ^a   Cassel, Roméo ^a   Dubois, Séverine ^a   Ducreux, Sylvie ^b   Vial, Guillaume ^a   Chauvin, Marie Agnès ^a   Mesnier, Aurélia ^a   Chikh, Karim ^a   Bosco, Domenico ^c   Rieusset, Jennifer ^a   Van Coppenolle, Fabien ^b   Thivolet, Charles ^a,b  

^a INSERM   (France)

^b UNIVERSITÉ LYON 1   (France)

^c GENEVA UNIVERSITY HOSPITALS   (Switzerland)

Author keywords

AT1R inhibitor; Calcium homeostasis; Diabetes; ER stress; Human pancreatic cells; PLC IP3 calcium pathway; RAS

Indexed keywords

1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 1H PYRROLE 2,5 DIONE; ACTIVATING TRANSCRIPTION FACTOR 4; ANGIOTENSIN 1 RECEPTOR; GLUCOSE; GLUCOSE REGULATED PROTEIN 78; LOSARTAN; PHOSPHOLIPASE C BETA; PHOSPHOLIPASE C GAMMA1; X BOX BINDING PROTEIN 1;

ARTICLE; ENDOPLASMIC RETICULUM STRESS; ENZYME INHIBITION; HOMEOSTASIS; HUMAN; HUMAN CELL; INSULIN RELEASE; INTOXICATION; OXIDATIVE STRESS; PANCREAS ISLET CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM;

AT1R INHIBITOR; CALCIUM HOMEOSTASIS; DIABETES; ER STRESS; HUMAN PANCREATIC Β-CELLS; PLC-IP3-CALCIUM PATHWAY; RAS;

ANGIOTENSIN II TYPE 1 RECEPTOR BLOCKERS; CALCIUM; CALCIUM SIGNALING; CELLS, CULTURED; ENDOPLASMIC RETICULUM STRESS; ESTRENES; GLUCOSE; HUMANS; INOSITOL 1,4,5-TRISPHOSPHATE RECEPTORS; INSULIN; INSULIN-SECRETING CELLS; LOSARTAN; PHOSPHOLIPASE C BETA; PHOSPHOLIPASE C GAMMA; PYRROLIDINONES; RECEPTOR, ANGIOTENSIN, TYPE 1; RENIN-ANGIOTENSIN SYSTEM; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES;

EID: 84890525402     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.13-234104     Document Type: Article

References (36)

1. Kahn, S. E. (2003) The relative contribution of insulin resistance and beta-cell dysfunction to the pathophysiology of type 2 diabetes. Diabetologia 46, 3-19
2. Del Guerra, S., Lupi, R., Marselli, L., Masini, M., Bugliani, M., Sbrana, S., Torri, S., Pollera, M., Boggi, U., Mosca, F., Del Prato, S., and Marchetti, P. (2005) Functional and molecular defects of pancreatic islets in human type 2 diabetes. Diabetes 54, 727-735
3. Bonnard, C., Durand, A., Peyrol, S., Chanseaume, E., Chauvin, M. A., Morio, B., Vidal, H., and Rieusset, J. (2008) Mitochondrial dysfunction results from oxidative stress in the skeletal muscle of diet-induced insulin-resistant mice. J. Clin. Invest. 118, 789-800
4. Ozcan, U., Cao, Q., Yilmaz, E., Lee, A. H., Iwakoshi, N. N., Ozdelen, E., Tuncman, G., Görgün, C., Glimcher, K. H., and Hotamisligil, G. S. (2004) Endoplasmic reticulum stress links obesity, insulin action and type 2 diabetes. Science 306, 457-461
5. Hotamisligil, G. S. (2010) Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 140, 900-917
6. Tanaka, Y., Tran, P. O., Harmon, J., and Robertson, R. P. (2002) A role for gluthathione peroxidase in protecting pancreatic beta cells against oxidative stress in a model of glucose toxicity. Proc. Natl. Acad. Sci. U. S. A. 99, 12363-12368
7. Lee, Y. Y., Hong, S. H., Lee, Y. J., Chung, S. S., Jung, H. S., Park, S. G., and Park, K. S. (2010) Tauroursodeoxycholate (TUDCA), chemical chaperone, enhances function of islets by reducing ER stress. BBRC 397, 735-739
8. The Navigator study group. (2010) Effect of Valsartan on the incidence of diabetes and cardiovascular events. N. Engl. J. Med. 362, 1477-1490
9. Geng, D., Jin, D. M., Wu, W., Xu, Y., and Wang, J. F. (2012) Angiotensin receptor blockers for prevention of new-onset type 2 diabetes: a meta-analysis of 59,862 patients. Int. J. Cardiol. 155, 236-242
10. Ramracheya, R. D., Muller, D. S., Wu, Y., Whitehouse, B. J., Huang, G. C., Amiel, S. A., Karalliedde, J., Viberti, G., Jones, P. M., and Persaud, S. J. (2006) Direct regulation of insulin secretion by angiotensin II in human islets of Langerhans. Diabetologia 49, 321-331
11. Chu, K. Y., and Leung, P. S. (2009) Angiotensin II in type 2 diabetes: current protein and peptides. Science 10, 75-84
12. Chu, K.Y., Lau, T., Carlsson, P. O., and Leung, P. S. (2006) Angiotensin II type 1 receptor blockade improves beta-cell function and glucose tolerance in a mouse model of type 2 diabetes. Diabetes 55, 367-374
13. Hunyadi, L., and Catt, K. J. (2006) Pleiotropic AT1 receptor signaling pathways mediating physiological and pathogenic actions of angiotensin II. Mol. Endocrinol. 20, 953-970
14. Yamazaki, H., Zawalich, K. C., and Zawalich, W. S. (2010) Physiologic implications of phosphoinositides and phospholipase C in the regulation of insulin secretion. J. Nutr. Sci. Vitaminol. 56, 1-8
15. Dubois, S., Madec, A. M., Mesnier, A., Armanet, M., Chikh, K., Berney, T., and Thivolet, C. (2010) Glucose inhibits angiogenesis of isolated human pancreatic islets, J. Mol. Endocrinol. 45, 99-105
16. Varadi, A., Molnar, E., Ostenson, C. G., and Ashcroft, S. J. H. (1996) Isoforms of endoplasmic reticulum Ca2-ATPase are differentially expressed in normal and diabetic islets of Langerhans. Biochem. J. 319, 521-5270
17. Lee, B., Jonas, J. C., Weir, G. C., and Laychock, S. G. (1999) Glucose regulates expression of inositol 1,2,5-triphosphate receptor isoforms in isolated rat pancreatic islets. Endocrinology 140, 2173-2182
18. Fiume, R., Ramazotti, G., Faenza, I., Piazzi, M., Bavelloni, A., Billi, A. M., and Cocco, L. (2012) Nuclear PLCs affect insulin secretion by targeting PPARg in pancreatic-cells. FASEB J. 26, 203-210
19. Poitout, V., and Robertson, R. P. (2008) Glucolipotoxocity: fuel excess and-cell dysfunction. Endocrin. Rev. 29, 351-366
20. Lupi, R., Guerra, S., Bugliani, M., Boggi, U., Mosca, F., Torri, S., Del Prato, S., and Marchetti, P. (2006) The direct effects of the angiotensin-converting enzyme inhibitors, zofenoprilat and enalaprilat, on isolated human pancreatic islets. Eur. J. Endocrinol. 154, 355-361
21. Henriksen, E. J. (2007) Improvement of insulin sensitivity by antagonism of the renin-angiotensin system. Am. J. Physiol. 293, R974-R980
22. Tikellis, C., Wookey, P. J., Candido, R., Andrikopoulos, S., Thomas, M. C., and Cooper, M. E. (2004) Improved islet morphology after blockade of the renin-angiotensin system in the ZDF rat. Diabetes 53, 989-997
23. Chu, K. Y., and Leung, P. S. (2007) Angiotensin II type 1 receptor antagonism mediates uncoupling protein 2-driven oxidative stress and ameliorates pancreatic beta-cell function in young type 2 diabetic mice. Antioxid. Redox Signal. 9, 869-878
24. Gillepsie, E. L., White, C. M., Karda, M., Lindberg, M., and Colmena, C. I. (2005) The impact of ACE inhibitors or angiotensin II type 1 receptor blockers on the development of new-onset type 2 diabetes. Diabetes Care 28, 2261-2266
25. Lau, T., and Carlsson, P. O., and Leung, P. S. (2004) Evidence for a local angiotensin-generating system and dose-dependent inhibition of glucose-stimulated insulin release by angiotensin II in isolated pancreatic islets. Diabetologia 47, 240-248
26. Michalak, M., Robert Parker, J. M., and Opas, M. (2002) Ca2+ signalling and calcium binding chaperones of the endoplasmic reticulum. Cell Calcium 32, 269-278
27. Mekahli, D., Bultynck, G., Pary, J. B., De Smedt, H., and Missiaen, L. (2011) Endoplasmic-reticulum calcium depletion and disease. Cold Spring Harb. Perspect. Biol. 3, 1-30
28. Ducreux, S., Zorzato, F., Ferreiro, A., Jungbluth, H., Muntoni, F., Monnier, N., Müller, C. R., and Treves, S. (2006) Functional properties of ryanodine receptors carrying three amino acid substitutions identified in patients affected by multi-minicore disease and central core disease, expressed in immortalized lymphocytes. Biochem. J. 395, 259-266
29. Brini, M., and Carafoli, E. (2009) Calcium pumps in health and disease. Physiol. Rev. 89, 1341-1378
30. Luciani, D. S., Gwazd, K. S., Yang, T. L., Kalynyak, T. B., Bychkiska, Y., Frey, M. H., Jeffrey, K. D., Sampaio, A. V., Underhill, T. M., and Johnson, J. D. (2009) Roles of IP3R and RyR Ca2+ channels in endoplasmic reticulum stress and betacell death. Diabetes 58, 422-432
31. Varadi, A., Lebel, L., Hashim, Y., Mehta, Z., and Ashcroft, S. J., Turner, R. (1999) Sequence variants of the sarco(endo)plasmic reticulum Ca2-transport ATPase 3 gene (SERCA3) in Caucasian type II diabetic patients (UK Prospective Diabetes Study 48). Diabetologia 42, 1240-1243
32. 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-activation restores pancreatic islet SERCA2 levels and prevent-cell dysfunction under conditions of hyperglycemic and cytokines stress. Mol. Endocrinol. 26, 257-271
33. Ravier, M. A., Daro, D., Roma, L. P., Jonas, J. C., Cheng-Xue, R., Schuit, F. C., and Gilon, P. (2011) Mechanisms of control of the free Ca2+ concentration in the endoplasmic reticulum of mouse pancreatic beta-cells: interplay with cell metabolism and [Ca2+]c, and role of SERCA2b and SERCA3. Diabetes 60, 2533-2545
34. Liu, M., Li, Y., Cavener, D., and Arvan, P. (2005) Proinsulin disulfide maturation and misfolding in the endoplasmic reticulum. J. Biol. Chem. 280, 13209-13212
35. Back, S. H., and Kaufman, R. J. (2012) Endoplasmic reticulum stress and type 2 diabetes. Annu. Rev. Biochem. 81, 767-793
36. Bensellam, M., Laybutt, D. R., and Jonas, J. C. (2012) The molecular mechanisms of pancreatic-cell glucotoxicity: recent findings and future research directions. Mol. Cell. Endocrinol. 364, 1-27