Metformin differentially activates ER stress signaling pathways without inducing apoptosis

DMM Disease Models and Mechanisms

Volumn 5, Issue 2, 2012, Pages 259-269

  Quentin, Thomas ^a   Steinmetz, Michael ^a   Poppe, Andrea ^a   Thoms, Sven ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 4; ACTIVATING TRANSCRIPTION FACTOR 6; CCAAT ENHANCER BINDING PROTEIN; CCAAT ENHANCER BINDING PROTEIN HOMOLOGOUS PROTEIN; METFORMIN; PHOSPHOTRANSFERASE; PROTEIN BCL 2; PROTEIN IRE1; PROTEIN KINASE RNA LIKE ER KINASE; UNCLASSIFIED DRUG; X BOX BINDING PROTEIN 1;

ANIMAL CELL; APOPTOSIS; ARTICLE; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; HEART MUSCLE CELL; HEART PROTECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; UPREGULATION;

ACTIVATING TRANSCRIPTION FACTOR 4; ANIMALS; APOPTOSIS; CARDIOTONIC AGENTS; CELLS, CULTURED; DIABETES MELLITUS, TYPE 2; EIF-2 KINASE; ENDOPLASMIC RETICULUM; HEART DISEASES; HUMANS; HYPOGLYCEMIC AGENTS; METFORMIN; MODELS, BIOLOGICAL; MYOCYTES, CARDIAC; RATS; RNA, MESSENGER; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; TRANSCRIPTION FACTOR CHOP; UP-REGULATION;

RATTUS;

EID: 84858036346     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.008110     Document Type: Article

References (43)

1. Araki, E., Oyadomari, S. and Mori, M. (2003). Endoplasmic reticulum stress and diabetes mellitus. Intern. Med. 42, 7-14.
2. Azfer, A., Niu, J., Rogers, L. M., Adamski, F. M. and Kolattukudy, P. E. (2006). Activation of endoplasmic reticulum stress response during the development of ischemic heart disease. Am. J. Physiol. Heart Circ. Physiol. 291, H1411-H1420.
3. Barsotti, A., Giannoni, A., Di Napoli, P. and Emdin, M. (2009). Energy metabolism in the normal and in the diabetic heart. Curr. Pharm. Des. 15, 836-840.
4. 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.
5. Bhamra, G. S., Hausenloy, D. J., Davidson, S. M., Carr, R. D., Paiva, M., Wynne, A. M., Mocanu, M. M. and Yellon, D. M. (2008). Metformin protects the ischemic heart by the Akt-mediated inhibition of mitochondrial permeability transition pore opening. Basic Res. Cardiol. 103, 274-284.
6. Calvert, J. W., Gundewar, S., Jha, S., Greer, J. J., Bestermann, W. H., Tian, R. and Lefer, D. J. (2008). Acute metformin therapy confers cardioprotection against myocardial infarction via AMPK-eNOS-mediated signaling. Diabetes 57, 696-705.
7. Chen, X., Shen, J. and Prywes, R. (2002). The luminal domain of ATF6 senses endoplasmic reticulum (ER) stress and causes translocation of ATF6 from the ER to the Golgi. J. Biol. Chem. 277, 13045-13052.
8. Cheng, W. P., Wang, B. W. and Shyu, K. G. (2009). Regulation of GADD153 induced by mechanical stress in cardiomyocytes. Eur. J. Clin. Invest. 39, 960-971.
9. Eurich, D. T., McAlister, F. A., Blackburn, D. F., Majumdar, S. R., Tsuyuki, R. T., Varney, J. and Johnson, J. A. (2007). Benefits and harms of antidiabetic agents in patients with diabetes and heart failure: systematic review. BMJ 335, 497.
10. Fery, F., Plat, L. and Balasse, E. O. (1997). Effects of metformin on the pathways of glucose utilization after oral glucose in non-insulin-dependent diabetes mellitus patients. Metabolism 46, 227-233.
11. Fischer, H., Koenig, U., Eckhart, L. and Tschachler, E. (2002). Human caspase 12 has acquired deleterious mutations. Biochem. Biophys. Res. Commun. 293, 722-726.
12. Groenendyk, J., Sreenivasaiah, P. K., Kim, Do H., Agellon, L. B. and Michalak, M. (2010). Biology of endoplasmic reticulum stress in the heart. Circ. Res. 107, 1185-1197.
13. Halterman, M. W., Gill, M., DeJesus, C., Ogihara, M., Schor, N. F. and Federoff, H. J. (2010). The endoplasmic reticulum stress response factor CHOP-10 protects against hypoxia-induced neuronal death. J. Biol. Chem. 285, 21329-21340.
14. Hardy, B. and Raiter, A. (2010). Peptide-binding heat shock protein GRP78 protects cardiomyocytes from hypoxia-induced apoptosis. J. Mol. Med. 88, 1157-1167.
15. Khurana, R. and Malik, I. S. (2010). Metformin: safety in cardiac patients. Heart 96, 99-102.
16. Kim, I., Xu, W. and Reed, J. C. (2008). Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities. Nat. Rev. Drug Discov. 7, 1013-1030.
17. Li, J., Lee, B. and Lee, A. S. (2006). Endoplasmic reticulum stress-induced apoptosis: multiple pathways and activation of p53-up-regulated modulator of apoptosis (PUMA) and NOXA by p53. J. Biol. Chem. 281, 7260-7270.
18. Masoudi, F. A., Inzucchi, S. E., Wang, Y., Havranek, E. P., Foody, J. M. and Krumholz, H. M. (2005). Thiazolidinediones, metformin, and outcomes in older patients with diabetes and heart failure: an observational study. Circulation 111, 583-590.
19. McCullough, K. D., Martindale, J. L., Klotz, L. O., Aw, T. Y. and Holbrook, N. J. (2001). Gadd153 sensitizes cells to endoplasmic reticulum stress by down-regulating Bcl2 and perturbing the cellular redox state. Mol. Cell. Biol. 21, 1249-1259.
20. Minamino, T. and Kitakaze, M. (2010). ER stress in cardiovascular disease. J. Mol. Cell. Cardiol. 48, 1105-1110.
21. Nakagawa, T., Zhu, H., Morishima, N., Li, E., Xu, J., Yankner, B. A. and Yuan, J. (2000). Caspase-12 mediates endoplasmic-reticulum-specific apoptosis and cytotoxicity by amyloid-beta. Nature 403, 98-103.
22. Nickson, P., Toth, A. and Erhardt, P. (2007). PUMA is critical for neonatal cardiomyocyte apoptosis induced by endoplasmic reticulum stress. Cardiovasc. Res. 73, 48-56.
23. Okada, K., Minamino, T., Tsukamoto, Y., Liao, Y., Tsukamoto, O., Takashima, S., Hirata, A., Fujita, M., Nagamachi, Y., Nakatani, T. et al. (2004). Prolonged endoplasmic reticulum stress in hypertrophic and failing heart after aorticconstriction: possible contribution of endoplasmic reticulum stress to cardiac myocyte apoptosis. Circulation 110, 705-712.
24. Paiva, M. A., Goncalves, L. M., Providencia, L. A., Davidson, S. M., Yellon, D. M. and Mocanu, M. M. (2010). Transitory activation of AMPK at reperfusion protects the ischaemic-reperfused rat myocardium against infarction. Cardiovasc. Drugs Ther. 24, 25-32.
25. Puthalakath, H., O'Reilly, L. A., Gunn, P., Lee, L., Kelly, P. N., Huntington, N. D., Hughes, P. D., Michalak, E. M., McKimm-Breschkin, J., Motoyama, N. et al. (2007). ER stress triggers apoptosis by activating BH3-only protein Bim. Cell 129, 1337-1349.
26. Ron, D. and Walter, P. (2007). Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 8, 519-529.
27. Rutkowski, D. T. and Hegde, R. S. (2010). Regulation of basal cellular physiology by the homeostatic unfolded protein response. J. Cell Biol. 189, 783-794.
28. Shen, J., Chen, X., Hendershot, L. and Prywes, R. (2002). ER stress regulation of ATF6 localization by dissociation of BiP/GRP78 binding and unmasking of Golgi localization signals. Dev. Cell 3, 99-111.
29. Shintani-Ishida, K., Nakajima, M., Uemura, K. and Yoshida, K. (2006). Ischemic preconditioning protects cardiomyocytes against ischemic injury by inducing GRP78. Biochem. Biophys. Res. Commun. 345, 1600-1605.
30. Solskov, L., Lofgren, B., Kristiansen, S. B., Jessen, N., Pold, R., Nielsen, T. T., Botker, H. E., Schmitz, O. and Lund, S. (2008). Metformin induces cardioprotection against ischaemia/reperfusion injury in the rat heart 24 hours after administration. Basic Clin. Pharmacol. Toxicol. 103, 82-87.
31. Stumvoll, M., Nurjhan, N., Perriello, G., Dailey, G. and Gerich, J. E. (1995). Metabolic effects of metformin in non-insulin-dependent diabetes mellitus. N. Engl. J. Med. 333, 550-554.
32. Szegezdi, E., Duffy, A., O'Mahoney, M. E., Logue, S. E., Mylotte, L. A., O'Brien, T. and Samali, A. (2006). ER stress contributes to ischemia-induced cardiomyocyte apoptosis. Biochem. Biophys. Res. Commun. 349, 1406-1411.
33. Terai, K., Hiramoto, Y., Masaki, M., Sugiyama, S., Kuroda, T., Hori, M., Kawase, I. and Hirota, H. (2005). AMP-activated protein kinase protects cardiomyocytes against hypoxic injury through attenuation of endoplasmic reticulum stress. Mol. Cell. Biol. 25, 9554-9575.
34. Thompson, M. R., Xu, D. and Williams, B. R. (2009). ATF3 transcription factor and its emerging roles in immunity and cancer. J. Mol. Med. 87, 1053-1060.
35. Thoms, S., Gronborg, S. and Gartner, J. (2009). Organelle interplay in peroxisomal disorders. Trends Mol. Med. 15, 293-302.
36. Thuerauf, D. J., Marcinko, M., Gude, N., Rubio, M., Sussman, M. A. and Glembotski, C. C. (2006). Activation of the unfolded protein response in infarcted mouse heart and hypoxic cultured cardiac myocytes. Circ. Res. 99, 275-282.
37. Toth, A., Jeffers, J. R., Nickson, P., Min, J. Y., Morgan, J. P., Zambetti, G. P. and Erhardt, P. (2006). Targeted deletion of Puma attenuates cardiomyocyte death and improves cardiac function during ischemia-reperfusion. Am. J. Physiol. Heart Circ. Physiol. 291, H52-H60.
38. UKPDS. (1998). Effect of intensive blood-glucose control with metformin on complications in overweight patients with type 2 diabetes (UKPDS 34). UK Prospective Diabetes Study Group. Lancet 352, 854-865.
39. Upton, J. P., Austgen, K., Nishino, M., Coakley, K. M., Hagen, A., Han, D., Papa, F. R. and Oakes, S. A. (2008). Caspase-2 cleavage of BID is a critical apoptotic signal downstream of endoplasmic reticulum stress. Mol. Cell. Biol. 28, 3943-3951.
40. Voulgari, C., Papadogiannis, D. and Tentolouris, N. (2010). Diabetic cardiomyopathy: from the pathophysiology of the cardiac myocytes to current diagnosis and management strategies. Vasc. Health Risk Manag. 6, 883-903.
41. Weston, R. T. and Puthalakath, H. (2010). Endoplasmic reticulum stress and BCL-2 family members. Adv. Exp. Med. Biol. 687, 65-77.
42. Wong, W. W. and Puthalakath, H. (2008). Bcl-2 family proteins: the sentinels of the mitochondrial apoptosis pathway. IUBMB Life 60, 390-397.
43. Ye, J., Rawson, R. B., Komuro, R., Chen,X., Davé, U. P., Prywes, R., Brown, M. S. and Goldstein, J. L. (2000). ER stress induces cleavage of membrane-bound ATF6 by the same proteases that process SREBPs. Mol. Cell 6, 1355-1364.