Metallothionein prevents intermittent hypoxia-induced cardiac endoplasmic reticulum stress and cell death likely via activation of Akt signaling pathway in mice

Toxicology Letters

Volumn 227, Issue 2, 2014, Pages 113-123

  Zhou, Shanshan ^a,b   Yin, Xia ^a,b   Zheng, Yang ^a   Miao, Xiao ^b,c   Feng, Wenke ^b   Cai, Jun ^b   Cai, Lu ^b  

^a THE FIRST HOSPITAL OF JILIN UNIVERSITY   (China)

^b University of Louisville School of Medicine   (United States)

^c THE SECOND HOSPITAL OF JILIN UNIVERSITY   (China)

Author keywords

Cardiomyopathy; ER stress; Intermittent hypoxia; Metallothionein; Obstructive sleep apnea

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; CASPASE 12; CASPASE 3; METALLOTHIONEIN; PROTEIN BAX; PROTEIN BCL 2; PROTEIN KINASE B; TUNICAMYCIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CARDITIS; CELL DEATH; CHRONIC INTERMITTENT HYPOXIA; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; HEART PROTECTION; HEART STRESS; IN VITRO STUDY; MALE; MOUSE; NICK END LABELING; NONHUMAN; PRIMARY CELL CULTURE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; UPREGULATION; WESTERN BLOTTING;

CARDIOMYOPATHY; ER STRESS; INTERMITTENT HYPOXIA; METALLOTHIONEIN; OBSTRUCTIVE SLEEP APNEA;

ANIMALS; ANOXIA; APOPTOSIS; CELL DEATH; CELL LINE; DRUG ADMINISTRATION SCHEDULE; ENDOPLASMIC RETICULUM; GENE DELETION; GENE EXPRESSION REGULATION; MALE; METALLOTHIONEIN; MICE; MYOCARDIUM; OXYGEN; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; RATS; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL;

EID: 84899096445     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2014.03.011     Document Type: Article

References (54)

1. Arnaud C., Beguin P.C., Lantuejoul S., Pepin J.L., Guillermet C., Pelli G., Burger F., Buatois V., Ribuot C., Baguet J.P., Mach F., Levy P., Dematteis M. The inflammatory preatherosclerotic remodeling induced by intermittent hypoxia is attenuated by RANTES/CCL5 inhibition. Am. J. Respir. Crit. Care Med. 2011, 184:724-731.
2. Bhandary B., Marahatta A., Kim H.R., Chae H.J. An involvement of oxidative stress in endoplasmic reticulum stress and its associated diseases. Int. J. Mol. Sci. 2012, 14:434-456.
3. Cai J., Tuong C.M., Gozal D. A neonatal mouse model of intermittent hypoxia associated with features of apnea in premature infants. Respir. Physiol. Neurobiol. 2011, 178:210-217.
4. Cai J., Tuong C.M., Zhang Y., Shields C.B., Guo G., Fu H., Gozal D. Mouse intermittent hypoxia mimicking apnoea of prematurity: effects on myelinogenesis and axonal maturation. J. Pathol. 2012, 226:495-508.
5. Cai L. Suppression of nitrative damage by metallothionein in diabetic heart contributes to the prevention of cardiomyopathy. Free Radic. Biol. Med. 2006, 41:851-861.
6. Cai L. Diabetic cardiomyopathy and its prevention by metallothionein: experimental evidence, possible mechanisms and clinical implications. Curr. Med. Chem. 2007, 14:2193-2203.
7. Cai L. Metallothionein and cardiomyopathy. Metallothioneins in Biochemistry and Pathology 2008, 1:227-269. World Scientific, New Jersey.
8. Cai L., Satoh M., Tohyama C., Cherian M.G. Metallothionein in radiation exposure: its induction and protective role. Toxicology 1999, 132:85-98.
9. Cai L., Wang J., Li Y., Sun X., Wang L., Zhou Z., Kang Y.J. Inhibition of superoxide generation and associated nitrosative damage is involved in metallothionein prevention of diabetic cardiomyopathy. Diabetes 2005, 54:1829-1837.
10. Ceylan-Isik A.F., Zhao P., Zhang B., Xiao X., Su G., Ren J. Cardiac overexpression of metallothionein rescues cardiac contractile dysfunction and endoplasmic reticulum stress but not autophagy in sepsis. J. Mol. Cell Cardiol. 2010, 48:367-378.
11. Chen L.M., Kuo W.W., Yang J.J., Wang S.G., Yeh Y.L., Tsai F.J., Ho Y.J., Chang M.H., Huang C.Y., Lee S.D. Eccentric cardiac hypertrophy was induced by long-term intermittent hypoxia in rats. Exp. Physiol. 2007, 92:409-416.
12. Chen T.I., Lai C.J., Hsieh C.J., Tsai K.L., Yang K.T. Differences in left ventricular cardiomyocyte loss induced by chronic intermittent hypoxia between spontaneously hypertensive and Wistar-Kyoto rats. Sleep Breath. 2011, 15:845-854.
13. Dickhout J.G., Carlisle R.E., Austin R.C. Interrelationship between cardiac hypertrophy, heart failure, and chronic kidney disease: endoplasmic reticulum stress as a mediator of pathogenesis. Circ. Res. 2011, 108:629-642.
14. Dong M., Hu N., Hua Y., Xu X., Kandadi M.R., Guo R., Jiang S., Nair S., Hu D., Ren J. Chronic Akt activation attenuated lipopolysaccharide-induced cardiac dysfunction via Akt/GSK3beta-dependent inhibition of apoptosis and ER stress. Biochim. Biophys. Acta 2013, 1832:848-863.
15. Doroudgar S., Thuerauf D.J., Marcinko M.C., Belmont P.J., Glembotski C.C. Ischemia activates the ATF6 branch of the endoplasmic reticulum stress response. J. Biol. Chem. 2009, 284:29735-29745.
16. Dyugovskaya L., Lavie P., Lavie L. Phenotypic and functional characterization of blood gammadelta T cells in sleep apnea. Am. J. Respir. Crit. Care Med. 2003, 168:242-249.
17. Fu J., Lv H.J., Guan H.X., Ma X.Y., Ji M.J., He N.Y., Shi B.Y., Hou P. Metallothionein 1G functions as a tumor suppressor in thyroid cancer through modulating the PI3K/Akt signaling pathway. BMC Cancer 2013, 13:462.
18. Gao J., Ding X.S., Zhang Y.M., Dai D.Z., Liu M., Zhang C., Dai Y. Hypoxia/oxidative stress alters the pharmacokinetics of CPU86017-RS through mitochondrial dysfunction and NADPH oxidase activation. Acta Pharmacol. Sin. 2013, 34:1575-1584.
19. Ge W., Zhang Y., Han X., Ren J. Cardiac-specific overexpression of catalase attenuates paraquat-induced myocardial geometric and contractile alteration: role of ER stress. Free Radic. Biol. Med. 2010, 49:2068-2077.
20. Gotoh T., Endo M., Oike Y. Endoplasmic reticulum stress-related inflammation and cardiovascular diseases. Int. J. Inflammation 2011, 2011:259462.
21. Greenberg H., Ye X., Wilson D., Htoo A.K., Hendersen T., Liu S.F. Chronic intermittent hypoxia activates nuclear factor-kappaB in cardiovascular tissues in vivo. Biochem. Biophys. Res. Commun. 2006, 343:591-596.
22. Groenendyk J., Agellon L.B., Michalak M. Coping with endoplasmic reticulum stress in the cardiovascular system. Annu. Rev. Physiol. 2013, 75:49-67.
23. Guo R., Ma H., Gao F., Zhong L., Ren J. Metallothionein alleviates oxidative stress-induced endoplasmic reticulum stress and myocardial dysfunction. J. Mol. Cell Cardiol. 2009, 47:228-237.
24. Hamid T., Guo S.Z., Kingery J.R., Xiang X., Dawn B., Prabhu S.D. Cardiomyocyte NF-kappaB p65 promotes adverse remodelling, apoptosis, and endoplasmic reticulum stress in heart failure. Cardiovasc. Res. 2011, 89:129-138.
25. Han Q., Yeung S.C., Ip M.S., Mak J.C. Cellular mechanisms in intermittent hypoxia-induced cardiac damage in vivo. J. Physiol. Biochem. 2013, (Epub ahead of print, PubMed PMID: 24122132, Oct 12).
26. Khayat R., Patt B., Hayes D. Obstructive sleep apnea: the new cardiovascular disease. Part I: Obstructive sleep apnea and the pathogenesis of vascular disease. Heart Fail. Rev. 2009, 14:143-153.
27. Kondoh M., Tsukada M., Kuronaga M., Higashimoto M., Takiguchi M., Himeno S., Watanabe Y., Sato M. Induction of hepatic metallothionein synthesis by endoplasmic reticulum stress in mice. Toxicol. Lett. 2004, 148:133-139.
28. Kost K.M. Endoscopic percutaneous dilatational tracheotomy: a prospective evaluation of 500 consecutive cases. Laryngoscope 2005, 115:1-30.
29. Liao J., Sun A., Xie Y., Isse T., Kawamoto T., Zou Y., Ge J. Aldehyde dehydrogenase-2 deficiency aggravates cardiac dysfunction elicited by endoplasmic reticulum stress induction. Mol. Med. 2012, 18:785-793.
30. Liu Q., Wang G., Zhou G., Tan Y., Wang X., Wei W., Liu L., Xue W., Feng W., Cai L. Angiotensin II-induced p53-dependent cardiac apoptotic cell death: its prevention by metallothionein. Toxicol. Lett. 2009, 191:314-320.
31. Manukyan M.C., Weil B.R., Wang Y., Abarbanell A.M., Herrmann J.L., Poynter J.A., Meldrum D.R. The phosphoinositide-3 kinase survival signaling mechanism in sepsis. Shock 2010, 34:442-449.
32. Millott R., Dudek E., Michalak M. The endoplasmic reticulum in cardiovascular health and disease. Can. J. Physiol. Pharmacol. 2012, 90:1209-1217.
33. Minamino T., Kitakaze M. ER stress in cardiovascular disease. J. Mol. Cell. Cardiol. 2010, 48:1105-1110.
34. Okada K., Minamino T., Tsukamoto Y., Liao Y., Tsukamoto O., Takashima S., Hirata A., Fujita M., Nagamachi Y., Nakatani T., Yutani C., Ozawa K., Ogawa S., Tomoike H., Hori M., Kitakaze M. Prolonged endoplasmic reticulum stress in hypertrophic and failing heart after aortic constriction: possible contribution of endoplasmic reticulum stress to cardiac myocyte apoptosis. Circulation 2004, 110:705-712.
35. Peng Y.J., Prabhakar N.R. Reactive oxygen species in the plasticity of respiratory behavior elicited by chronic intermittent hypoxia. J. Appl. Physiol. 2003, 94:2342-2349.
36. Prabhakar N.R., Fields R.D., Baker T., Fletcher E.C. Intermittent hypoxia: cell to system. Am. J. Physiol. Lung Cell Mol. Physiol. 2001, 281:L524-L528.
37. Prabhakar N.R., Kline D.D. Ventilatory changes during intermittent hypoxia: importance of pattern and duration. High Alt. Med. Biol. 2002, 3:195-204.
38. Punjabi N.M. The epidemiology of adult obstructive sleep apnea. Proc. Am. Thorac. Soc. 2008, 5:136-143.
39. Ron D., Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 2007, 8:519-529.
40. Rosamond W., Flegal K., Friday G., Furie K., Go A., Greenlund K., Haase N., Ho M., Howard V., Kissela B., Kittner S., Lloyd-Jones D., McDermott M., Meigs J., Moy C., Nichol G., O'Donnell C.J., Roger V., Rumsfeld J., Sorlie P., Steinberger J., Thom T., Wasserthiel-Smoller S., Hong Y. Heart disease and stroke statistics-2007 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 2007, 115:e69-e171.
41. Rosamond W., Flegal K., Furie K., Go A., Greenlund K., Haase N., Hailpern S.M., Ho M., Howard V., Kissela B., Kittner S., Lloyd-Jones D., McDermott M., Meigs J., Moy C., Nichol G., O'Donnell C., Roger V., Sorlie P., Steinberger J., Thom T., Wilson M., Hong Y. Heart disease and stroke statistics-2008 update: a report from the American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Circulation 2008, 117:e25-e146.
42. Su J., Zhou L., Kong X., Yang X., Xiang X., Zhang Y., Li X., Sun L. Endoplasmic reticulum is at the crossroads of autophagy, inflammation, and apoptosis signaling pathways and participates in the pathogenesis of diabetes mellitus. J. Diabetes Res. 2013, 2013:193461.
43. Toth A., Nickson P., Mandl A., Bannister M.L., Toth K., Erhardt P. Endoplasmic reticulum stress as a novel therapeutic target in heart diseases. Cardiovasc. Hematol. Disord. Drug Targets 2007, 7:205-218.
44. Wang J., Song Y., Elsherif L., Song Z., Zhou G., Prabhu S.D., Saari J.T., Cai L. Cardiac metallothionein induction plays the major role in the prevention of diabetic cardiomyopathy by zinc supplementation. Circulation 2006, 113:544-554.
45. Williams A.L., Chen L., Scharf S.M. Effects of allopurinol on cardiac function and oxidant stress in chronic intermittent hypoxia. Sleep Breath. 2010, 14:51-57.
46. Xu C., Bailly-Maitre B., Reed J.C. Endoplasmic reticulum stress: cell life and death decisions. J. Clin. Invest. 2005, 115:2656-2664.
47. Xu J., Wang G., Wang Y., Liu Q., Xu W., Tan Y., Cai L. Diabetes and angiotensin II-induced cardiac endoplasmic reticulum stress and cell death: metallothionein protection. J. Cell. Mol. Med. 2009, 13:1499-1512.
48. Xu J., Zhou Q., Xu W., Cai L. Endoplasmic reticulum stress and diabetic cardiomyopathy. Exp. Diabetes Res. 2012, 2012:827971.
49. Xue W., Liu Q., Cai L., Wang Z., Feng W. Stable overexpression of human metallothionein-IIA in a heart-derived cell line confers oxidative protection. Toxicol. Lett. 2009, 188:70-76.
50. Yin X., Zhou S., Zheng Y., Tan Y., Kong M., Wang B., Feng W., Epstein P.N., Cai J., Cai L. Metallothionein as a compensatory component prevents intermittent hypoxia-induced cardiomyopathy in mice. Toxicol. Appl. Pharmacol. 2014, PII: S0041-008X(14)00093-3. 10.1016/j.taap.2014.03.007.
51. Younce C.W., Kolattukudy P.E. MCP-1 causes cardiomyoblast death via autophagy resulting from ER stress caused by oxidative stress generated by inducing a novel zinc-finger protein MCPIP. Biochem. J. 2010, 426:43-53.
52. Zhang Y., Ren J. Thapsigargin triggers cardiac contractile dysfunction via NADPH oxidase-mediated mitochondrial dysfunction: role of Akt dephosphorylation. Free Radic. Biol. Med. 2011, 51:2172-2184.
53. Zhang Y., Xia Z., La Cour K.H., Ren J. Activation of Akt rescues endoplasmic reticulum stress-impaired murine cardiac contractile function via glycogen synthase kinase-3beta-mediated suppression of mitochondrial permeation pore opening. Antioxid. Redox Signal. 2011, 15:2407-2424.
54. Zhou G., Li X., Hein D.W., Xiang X., Marshall J.P., Prabhu S.D., Cai L. Metallothionein suppresses angiotensin II-induced nicotinamide adenine dinucleotide phosphate oxidase activation, nitrosative stress, apoptosis, and pathological remodeling in the diabetic heart. J. Am. Coll. Cardiol. 2008, 52:655-666.