Sex differences in endothelial STAT3 mediate sex differences in myocardial inflammation

American Journal of Physiology - Endocrinology and Metabolism

Volumn 293, Issue 3, 2007, Pages

  Wang, Meijing ^a   Zhang, Wenjun ^a   Crisostomo, Paul ^a   Markel, Troy ^a   Meldrum, Kirstan K ^a   Fu, Xin Y ^a   Meldrum, Daniel R ^a,b  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Emerson Hall 215 ^*  (United States)

Author keywords

Ischemia reperfusion; Myocardial function; Signal transducer and activator of transcription 3

Indexed keywords

INTERLEUKIN 1BETA; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE P38; STAT3 PROTEIN; TUMOR NECROSIS FACTOR RECEPTOR;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENDOTHELIUM CELL; HEART FUNCTION; ISCHEMIA; MALE; MOUSE; MYOCARDITIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN FUNCTION; REPERFUSION; SEX DIFFERENCE;

ANIMALS; ENDOTHELIUM, VASCULAR; FEMALE; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MYOCARDIAL REPERFUSION INJURY; MYOCARDITIS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; SEX FACTORS; STAT3 TRANSCRIPTION FACTOR;

EID: 34548420524     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00251.2007     Document Type: Article

References (40)

1. Bjornstrom L, Sjoberg M. Signal transducers and activators of transcription as downstream targets of nongenomic estrogen receptor actions. Mol Endocrinol 16: 2202-2214, 2002.
2. Bromberg J. Stat proteins and oncogenesis. J Clin Invest 109: 1139-1142, 2002.
3. Cain BS, Meldrum DR, Dinarello CA, Meng X, Joo KS, Banerjee A, Harken AH. Tumor necrosis factor-alpha and interleukin-1beta synergistically depress human myocardial function. Crit Care Med 27: 1309-1318, 1999.
4. Cain BS, Meldrum DR, Meng X, Dinarello CA, Shames BD, Banerjee A, Harken AH. p38 MAPK inhibition decreases TNF-alpha production and enhances postischemic human myocardial function. J Surg Res 83: 7-12, 1999.
5. Canesi L, Ciacci C, Betti M, Lorusso LC, Marchi B, Burattini S, Falcieri E, Gallo G. Rapid effects of 17beta-estradiol on cell signaling and function of Mytilus hemocytes. Gen Comp Endocrinol 136: 58-71, 2004.
6. Chin YE, Kitagawa M, Su WC, You ZH, Iwamoto Y, Fu XY. Cell growth arrest and induction of cyclin-dependent kinase inhibitor p21 WAF1/CIP1 mediated by STAT1. Science 272: 719-722, 1996.
7. Fu XY. From PTK-STAT signaling to caspase expression and apoptosis induction. Cell Death Differ 6: 1201-1208, 1999.
8. Gao H, Bryzgalova G, Hedman E, Khan A, Efendic S, Gustafsson JA, Dahlman-Wright K. Long-term administration of estradiol decreases expression of hepatic lipogenic genes and improves insulin sensitivity in ob/ob mice: a possible mechanism is through direct regulation of signal transducer and activator of transcription 3. Mol Endocrinol 20: 1287-1299, 2006.
9. Grutkoski PS, Chen Y, Chung CS, Ayala A. Sepsis-induced SOCS-3 expression is immunologically restricted to phagocytes. J Leukocyte Bioly 74: 916-922, 2003.
10. Hilfiker-Kleiner D, Hilfiker A, Drexler H. Many good reasons to have STAT3 in the heart. Pharmacol Ther 107: 131-137, 2005.
11. Hilfiker-Kleiner D, Hilfiker A, Fuchs M, Kaminski K, Schaefer A, Schieffer B, Hillmer A, Schmiedl A, Ding Z, Podewski E, Podewski E, Poli V, Schneider MD, Schulz R, Park JK, Wollert KC, Drexler H. Signal transducer and activator of transcription 3 is required for myocardial capillary growth, control of interstitial matrix deposition, and heart protection from ischemic injury. Circ Res 95: 187-195, 2004.
12. Hilfiker-Kleiner D, Limbourg A, Drexler H. STAT3-mediated activation of myocardial capillary growth. Trends Cardiovasc Med 15: 152-157, 2005.
13. Jacoby JJ, Kalinowski A, Liu MG, Zhang SS, Gao Q, Chai GX, Ji L, Iwamoto Y, Li E, Schneider M, Russell KS, Fu XY. Cardiomyocyte-restricted knockout of STAT3 results in higher sensitivity to inflammation, cardiac fibrosis, and heart failure with advanced age. Proc Natl Acad Sci USA 100: 12929-12934, 2003.
14. Jiang S, Haider H, Idris NM, Salim A, Ashraf M. Supportive interaction between cell survival signaling and angiocompetent factors enhances donor cell survival and promotes angiomyogenesis for cardiac repair. Circ Res 99: 776-784, 2006.
15. Kaiser RA, Bueno OF, Lips DJ, Doevendans PA, Jones F, Kimball TF, Molkentin JD. Targeted inhibition of p38 mitogen-activated protein kinase antagonizes cardiac injury and cell death following ischemia-reperfusion in vivo. J Biol Chem 279: 15524-15530, 2004.
16. Liao P, Wang SQ, Wang S, Zheng M, Zhang SJ, Cheng H, Wang Y, Xiao RP. p38 Mitogen-activated protein kinase mediates a negative inotropic effect in cardiac myocytes. Circ Res 90: 190-196, 2002.
17. Liu HW, Iwai M, Takeda-Matsubara Y, Wu L, Li JM, Okumura M, Cui TX, Horiuchi M. Effect of estrogen and AT1 receptor blocker on neointima formation. Hypertension 40: 448-457, 2002.
18. Ma XL, Kumar S, Gao F, Louden CS, Lopez BL, Christopher TA, Wang C, Lee JC, Feuerstein GZ, Yue TL. Inhibition of p38 mitogen-activated protein kinase decreases cardiomyocyte apoptosis and improves cardiac function after myocardial ischemia and reperfusion. Circulation 99: 1685-1691, 1999.
19. Meldrum DR. Tumor necrosis factor in the heart. Am J Physiol Regul Integr Comp Physiol 274: R577-R595, 1998.
20. Mendelsohn ME, Karas RH. Molecular and cellular basis of cardiovascular sex differences. Science 308: 1583-1587, 2005.
21. Negoro S, Kunisada K, Fujio Y, Funamoto M, Darville MI, Eizirik DL, Osugi T, Izumi M, Oshima Y, Nakaoka Y, Hirota H, Kishimoto T, Yamauchi-Takihara K. Activation of signal transducer and activator of transcription 3 protects cardiomyocytes from hypoxia/reoxygenation-induced oxidative stress through the upregulation of manganese superoxide dismutase. Circulation 104: 979-981, 2001.
22. Negoro S, Kunisada K, Tone E, Funamoto M, Oh H, Kishimoto T, Yamauchi-Takihara K. Activation of JAK/STAT pathway transduces cytoprotective signal in rat acute myocardial infarction. Cardiovasc Res 47: 797-805, 2000.
23. Niagara MI, Haider H, Jiang S, Ashraf M. Pharmacologically preconditioned skeletal myoblasts are resistant to oxidative stress and promote angiomyogenesis via release of paracrine factors in the infarcted heart. Circ Res 100: 545-555, 2007.
24. Pober JS, Cotran RS. The role of endothelial cells in inflammation. Transplantation 50: 537-544, 1990.
25. Pober JS, Doukas J, Hughes CC, Savage CO, Munro JM, Cotran RS. The potential roles of vascular endothelium in immune reactions. Hum Immunol 28: 258-262, 1990.
26. Salituro FG, Germann UA, Wilson KP, Bemis GW, Fox T, Su MS. Inhibitors of p38 MAP kinase: therapeutic intervention in cytokine-mediated diseases. Curr Med Chem 6: 807-823, 1999.
27. Samy TS, Schwacha MG, Cioffi WG, Bland KI, Chaudry IH. Androgen and estrogen receptors in splenic T lymphocytes: effects of flutamide and trauma-hemorrhage. Shock 14: 465-470, 2000.
28. Schwarze MM, Hawley RG. Prevention of myeloma cell apoptosis by ectopic bcl-2 expression or interleukin 6-mediated up-regulation of bcl-xL. Cancer Res 55: 2262-2265, 1995.
29. Song GY, Chung CS, Chaudry IH, Ayala A. MAPK p38 antagonism as a novel method of inhibiting lymphoid immune suppression in polymicrobial sepsis. Am J Physiol Cell Physiol 281: C662-C669, 2001.
30. Su WC, Kitagawa M, Xue N, Xie B, Garofalo S, Cho J, Deng C, Horton WA, Fu XY. Activation of Stat1 by mutant fibroblast growth-factor receptor in thanatophoric dysplasia type II dwarfism. Nature 386: 288-292, 1997.
31. Tunstall-Pedoe H, Morrison C, Woodward M, Fitzpatrick B, Watt G. Sex differences in myocardial infarction and coronary deaths in the Scottish MONICA population of Glasgow 1985 to 1991. Presentation, diagnosis, treatment, and 28-day case fatality of 3991 events in men and 1551 events in women. Circulation 93: 1981-1992, 1996.
32. Uemura R, Xu M, Ahmad N, Ashraf M. Bone marrow stem cells prevent left ventricular remodeling of ischemic heart through paracrine signaling. Circ Res 98: 1414-1421, 2006.
33. Wang M, Baker L, Tsai BM, Meldrum KK, Meldrum DR. Sex differences in the myocardial inflammatory response to ischemia-reperfusion injury. Am J Physiol Endocrinol Metab 288: E321-E326, 2005.
34. Wang M, Markel T, Crisostomo P, Herring C, Meldrum KK, Lillemoe KD, Meldrum DR. Deficiency of TNFR1 protects myocardium through SOCS3 and IL-6, but not p38 MAPK or IL-1 . Am J Physiol Heart Circ Physiol 292: H1694-H1699, 2007.
35. Wang M, Tsai BM, Crisostomo PR, Meldrum DR. Tumor necrosis factor receptor 1 signaling resistance in the female myocardium during ischemia. Circulation 114: I282-I289, 2006.
36. Wang M, Tsai BM, Reiger KM, Brown JW, Meldrum DR. 17-Beta-estradiol decreases p38 MAPK-mediated myocardial inflammation and dysfunction following acute ischemia. J Mol Cell Cardiol 40: 205-212, 2006.
37. Welte T, Leitenberg D, Dittel BN, al-Ramadi BK, Xie B, Chin YE, Janeway CA Jr, Bothwell AL, Bottomly K, Fu XY. STAT5 interaction with the T cell receptor complex and stimulation of T cell proliferation. Science 283: 222-225, 1999.
38. Welte T, Zhang SS, Wang T, Zhang Z, Hesslein DG, Yin Z, Kano A, Iwamoto Y, Li E, Craft JE, Bothwell AL, Fikrig E, Koni PA, Flavell RA, Fu XY. STAT3 deletion during hematopoiesis causes Crohn's disease-like pathogenesis and lethality: a critical role of STAT3 in innate immunity. Proc Natl Acad Sci USA 100: 1879-1884, 2003.
39. Yang S, Hu S, Choudhry MA, Rue LW, 3rd Bland KI, Chaudry IH. Anti-rat soluble IL-6 receptor antibody down-regulates cardiac IL-6 and improves cardiac function following trauma-hemorrhage. J Mol Cell Cardiol 42: 620-630, 2007.
40. Yasukawa H, Ohishi M, Mori H, Murakami M, Chinen T, Aki D, Hanada T, Takeda K, Akira S, Hoshijima M, Hirano T, Chien KR, Yoshimura A. IL-6 induces an anti-inflammatory response in the absence of SOCS3 in macrophages. Nat Immunol 4: 551-556, 2003.