Sex differences play a role in cardiac endoplasmic reticulum stress (ERS) and ERS-initiated apoptosis induced by pressure overload and thapsigargin

Cardiovascular Pathology

Volumn 20, Issue 5, 2011, Pages 281-290

  Sari, Flori R ^a,b   Watanabe, Kenichi ^a   Widyantoro, Bambang ^c   Thandavarayan, Rajarajan A ^a   Harima, Meilei ^a   Kodama, Makoto ^d   Aizawa, Yoshifusa ^d  

^a NIIGATA UNIVERSITY OF PHARMACY AND APPLIED LIFE SCIENCES   (Japan)

^b State Islamic University   (Indonesia)

^c Division of Cardiovascular Medicine   (Japan)

^d NIIGATA UNIVERSITY GRADUATE SCHOOL OF MEDICAL AND DENTAL SCIENCES   (Japan)

Author keywords

Apoptosis; Ascending aortic banding; Endoplasmic reticulum stress; Sex differences; Thapsigargin

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN; ENZYME; GLUCOSE REGULATED PROTEIN 78; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INOSITOL REQUIRING ENZYME 1 ALPHA; SARCOPLASMIC RETICULUM CALCIUM TRANSPORTING ADENOSINE TRIPHOSPHATASE; THAPSIGARGIN; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 2; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ASCENDING AORTA SURGERY; CARDIOMEGALY; CONTROLLED STUDY; DISEASE ASSOCIATION; ENDOPLASMIC RETICULUM STRESS; FEMALE; HEART; HEART LEFT VENTRICLE OVERLOAD; HEART MUSCLE CELL; HISTOPATHOLOGY; IMMUNOREACTIVITY; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; SEX DIFFERENCE; TISSUE REACTION; WESTERN BLOTTING;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; AORTA; APOPTOSIS; CCAAT-BINDING FACTOR; DISEASE MODELS, ANIMAL; ENDOPLASMIC RETICULUM STRESS; ENZYME INHIBITORS; FEMALE; HEART; HEAT-SHOCK PROTEINS; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MYOCARDIUM; PRESSURE; PROTEIN-SERINE-THREONINE KINASES; SARCOPLASMIC RETICULUM; SARCOPLASMIC RETICULUM CALCIUM-TRANSPORTING ATPASES; SEX FACTORS; THAPSIGARGIN; TRANSCRIPTION FACTOR CHOP;

EID: 80052430271     PISSN: 10548807     EISSN: 18791336     Source Type: Journal    
DOI: 10.1016/j.carpath.2010.07.006     Document Type: Article

References (41)

1. Szegezdi E, Logue SE, Gorman AM, and Samali A Mediators of endoplasmic reticulum stress-induced apoptosis EMBO Rep 7 2006 880 885 (Pubitemid 44523966)
2. Xu C, Bailly-Maitre B, and Reed JC Endoplasmic reticulum stress: cell life and death decisions J Clin Invest 115 2005 2656 2664 (Pubitemid 41434389)
3. Kim I, Xu W, and Reed JC Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities Nat Rev Drug Discov 7 2008 1013 1030
4. Urano F, Wang X, Bertolotti A, Zhang Y, Chung P, and Harding HP Coupling of stress in the ER to activation of JNK protein kinases by transmembrane protein kinase IRE1 Science 287 2000 664 666 (Pubitemid 30070916)
5. Urano F, Bertolotti A, and Ron D IRE1 and efferent signaling from the endoplasmic reticulum J Cell Sci 113 2000 3697 3702
6. Li Z, Zhang T, Dai H, Liu G, Wang H, and Sun Y Endoplasmic reticulum stress is involved in myocardial apoptosis of streptozocin-induced diabetic rats J Endocrinol 196 2008 565 572 (Pubitemid 351425512)
7. Liu G, Sun Y, Li Z, Song T, Wang H, and Zhang Y Apoptosis induced by endoplasmic reticulum stress involved in diabetic kidney disease Biochem Biophys Res Commun 370 2008 651 656
8. Okada K, Minamino T, Tsukamoto Y, Liao Y, Tsukamoto O, and Takashima S Prolonged endoplasmic reticulum stress in hypertrophic and failing heart after aortic constriction: possible contribution of endoplasmic reticulum stress to cardiac myocyte apoptosis Circulation 110 2004 705 712 (Pubitemid 39056270)
9. Mallat Z, Fornes P, Costagliola R, Esposito B, Belmin J, and Lecomte D Age and gender effects on cardiomyocyte apoptosis in the normal human heart J Gerontol A Biol Sci Med Sci 56 2001 M719 723
10. Guerra S, Leri A, Wang X, Finato N, Di Loreto C, and Beltrami CA Myocyte death in the failing human heart is gender dependent Circ Res 85 1999 856 866 (Pubitemid 29504161)
11. Dent MR, Tappia PS, and Dhalla NS Gender differences in apoptotic signaling in heart failure due to volume overload Apoptosis 15 2010 499 510
12. Ren J Influence of gender on oxidative stress, lipid peroxidation, protein damage and apoptosis in hearts and brains from spontaneously hypertensive rats Clin Exp Pharmacol Physiol 34 2007 432 438 (Pubitemid 46494467)
13. Meldrum DR, Wang M, Tsai BM, Kher A, Pitcher JM, and Brown JW Intracellular signaling mechanisms of sex hormones in acute myocardial inflammation and injury Front Biosci 10 2005 1835 1867 (Pubitemid 40529042)
14. Camper-Kirby D, Welch S, Walker A, Shiraishi I, Setchell KD, and Schaefer E Myocardial Akt activation and gender: increased nuclear activity in females versus males Circ Res 88 2001 1020 1027 (Pubitemid 34137114)
15. Bae S, and Zhang L Gender differences in cardioprotection against ischemia/reperfusion injury in adult rat hearts: focus on Akt and protein kinase C signaling J Pharmacol Exp Ther 315 2005 1125 1135 (Pubitemid 41635399)
16. Tarnavski O, McMullen JR, Schinke M, Nie Q, Kong S, and Izumo S Mouse cardiac surgery: comprehensive techniques for the generation of mouse models of human diseases and their application for genomic studies Physiol Genomics 16 2004 349 360 (Pubitemid 38420055)
17. Hiramatsu N, Kasai A, Du S, Takeda M, Hayakawa K, and Okamura M Rapid, transient induction of ER stress in the liver and kidney after acute exposure to heavy metal: evidence from transgenic sensor mice FEBS Lett 581 2007 2055 2059 (Pubitemid 46670134)
18. Gurusamy N, Watanabe K, Ma M, Zhang S, Muslin AJ, and Kodama M Inactivation of 14-3-3 protein exacerbates cardiac hypertrophy and fibrosis through enhanced expression of protein kinase C beta 2 in experimental diabetes Biol Pharm Bull 28 2005 957 962 (Pubitemid 40880296)
19. Takizawa T, Arai M, Tomaru K, Koitabashi N, Baker DL, and Periasamy M Transcription factor Sp1 regulates SERCA2 gene expression in pressure-overloaded hearts: a study using in vivo direct gene transfer into living myocardium J Mol Cell Cardiol 7 2003 777 783 (Pubitemid 36773590)
20. Carroll JD, Carroll EP, Feldman T, Ward DM, Lang RM, and McGaughey D Sex-associated differences in left ventricular function in aortic stenosis of the elderly Circulation 86 1992 1099 1107
21. Buttrick P, and Scheuer J Sex-associated differences in left ventricular function in aortic stenosis of the elderly Circulation 86 1992 1336 1338
22. Aurigemma GP, Silver KH, McLaughlin M, Mauser J, and Gaasch WH Impact of chamber geometry and gender on left ventricular systolic function in patients >60 years of age with aortic stenosis Am J Cardiol 74 1994 794 798 (Pubitemid 24312973)
23. Aurigemma GP, and Gaasch WH Gender differences in older patients with pressure-overload hypertrophy of the left ventricle Cardiology 86 1995 310 317
24. Liao Y, Cooper RS, Mensah GA, and McGee DL Left ventricular hypertrophy has a greater impact on survival in women than in men Circulation 92 1995 805 810
25. Douglas PS, Katz SE, Weinberg EO, Chen MH, Bishop SP, and Lorell BH Hypertrophic remodeling: gender differences in the early response to left ventricular pressure overload J Am Coll Cardiol 32 1998 1118 1125 (Pubitemid 28459608)
26. Weinberg EO, Thienelt CD, Katz SE, Bartunek J, Tajima M, and Rohrbach S Gender differences in molecular remodeling in pressure overload hypertrophy J Am Coll Cardiol 34 1999 264 273
27. Skavdahl M, Steenbergen C, Clark J, Myers P, Demianenko T, and Mao L Estrogen receptor-beta mediates male-female differences in the development of pressure overload hypertrophy Am J Physiol Heart Circ Physiol 288 2005 H469 H476
28. Zhang ZY, Liu XH, Ye YJ, Sun S, Rong F, and Guo XS C/EBP homologous protein-mediated endoplasmic reticulum stress-related apoptosis pathway is involved in abdominal aortic constriction-induced myocardium hypertrophy in rats Sheng Li Xue Bao 61 2009 161 168
29. Saleh MC, Connell BJ, and Saleh TM Estrogen may contribute to ischemic tolerance through modulation of cellular stress-related proteins Neurosci Res 63 2009 273 279
30. Segawa T, Nau ME, Xu LL, Chilukuri RN, Makarem M, Zhang W, and Petrovics G Androgen-induced expression of endoplasmic reticulum (ER) stress response genes in prostate cancer cells Oncogene 21 2002 8749 8758 (Pubitemid 36132396)
31. Thuerauf DJ, Hoover H, Meller J, Hernandez J, Su L, and Andrews C Sarco/endoplasmic reticulum calcium ATPase-2 expression is regulated by ATF6 during the endoplasmic reticulum stress response: intracellular signaling of calcium stress in a cardiac myocyte model system J Biol Chem 276 2001 48309 48317
32. Pavlovic M, Schaller A, Steiner B, Berdat P, Carrel T, and Pfammatter JP Gender modulates the expression of calcium-regulating proteins in pediatric atrial myocardium Exp Biol Med 230 2005 853 859 (Pubitemid 41785885)
33. Chu SH, Sutherland K, Beck J, Kowalski J, Goldspink P, and Schwertz D Sex differences in expression of calcium-handling proteins and beta-adrenergic receptors in rat heart ventricle Life Sci 76 2005 2735 2749 (Pubitemid 40404060)
34. Kirby MS, Sagara Y, Gaa S, Inesi G, Lederer WJ, and Rogers TB Thapsigargin inhibits contraction and Ca2+ transient in cardiac cells by specific inhibition of the sarcoplasmic reticulum Ca2+ pump J Biol Chem 267 1992 12545 12551
35. Zhang ZY, Liu XH, Hu WC, Rong F, and Wu XD The calcineurin-myocyte enhancer factor 2c pathway mediates cardiac hypertrophy induced by endoplasmic reticulum stress in neonatal rat cardiomyocytes Am J Physiol Heart Circ Physiol 298 2010 H1499 1509
36. Taskinen P, and Ruskoaho H Stretch-induced increase in atrial natriuretic peptide secretion is blocked by thapsigargin Eur J Pharmacol 308 1996 295 300 (Pubitemid 26255013)
37. Oyadomari S, Araki E, and Mori M Endoplasmic reticulum stress-mediated apoptosis in pancreatic beta-cells Apoptosis 7 2002 335 345 (Pubitemid 34832258)
38. Park YJ, Jang YM, and Kwon YH Isoflavones prevent endoplasmic reticulum stress-mediated neuronal degeneration by inhibiting tau hyperphosphorylation in SH-SY5Y cells J Med Food 12 2009 528 535
39. Nishitoh H, Matsuzawa A, Tobiume K, Saegusa K, Takeda K, and Inoue K ASK1 is essential for endoplasmic reticulum stress-induced neuronal cell death triggered by expanded polyglutamine repeats Genes Dev 16 2002 1345 1355 (Pubitemid 34615088)
40. Kim YH, Joo HS, and Kim DS Nitric oxide induction of IRE1-alpha-dependent CREB phosphorylation in human glioma cells Nitric Oxide 2010
41. Linford NJ, and Dorsa DM 17beta-Estradiol and the phytoestrogen genistein attenuate neuronal apoptosis induced by the endoplasmic reticulum calcium-ATPase inhibitor thapsigargin Steroids 67 2002 1029 1040 (Pubitemid 35345166)