Female stem cells are superior to males in preserving myocardial function following endotoxemia

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 300, Issue 6, 2011, Pages 1506-1514

  Manukyan, Mariuxi C ^a   Weil, Brent R ^a   Wang, Yue ^a   Abarbanell, Aaron M ^a   Herrmann, Jeremy L ^a   Poynter, Jeffrey A ^a   Brewster, Benjamin D ^a   Meldrum, Daniel R ^a,b,c,d  

^a Dep of Orthopaedic Surgery   (United States)

^b Cellular and Integrative Physiology   (United States)

^c INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d METHODIST HOSPITAL   (United States)

Author keywords

Apoptosis; Mesenchymal stem cell; Myocardial injury; Sepsis; Sex

Indexed keywords

CYTOKINE; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN BAX; PROTEIN BCL XL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD LEVEL; DONOR; ENDOTOXEMIA; FEMALE; HEART DISEASE; HEART FUNCTION; HEART PROTECTION; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MOUSE; MYOCARDITIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SEX DIFFERENCE; TISSUE LEVEL;

ANIMALS; BCL-2-ASSOCIATED X PROTEIN; BCL-X PROTEIN; CARDIOMYOPATHIES; DISEASE MODELS, ANIMAL; ENDOTOXEMIA; FEMALE; LIPOPOLYSACCHARIDES; MALE; MESENCHYMAL STEM CELL TRANSPLANTATION; MESENCHYMAL STEM CELLS; MICE; MICE, INBRED C57BL; MYOCARDIUM; P38 MITOGEN-ACTIVATED PROTEIN KINASES; RATS; RATS, SPRAGUE-DAWLEY; TISSUE THERAPY;

EID: 79958862538     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00518.2010     Document Type: Article

References (47)

1. Abarbanell AM, Wang Y, Herrmann JL, Weil BR, Poynter JA, Manukyan MC, Meldrum DR. Toll-like receptor 2 mediates mesenchy-mal stem cell-associated myocardial recovery and VEGF production following acute ischemia-reperfusion injury. Am J Physiol Heart Circ Physiol 298: H1529-H1536, 2010.
2. Aggarwal S, Pittenger MF. Human mesenchymal stem cells modulate allogeneic immune cell responses. Blood 105: 1815-1822, 2005.
3. Atoui R, Asenjo JF, Duong M, Chen G, Chiu RC, Shum-Tim D. Marrow stromal cells as universal donor cells for myocardial regenerative therapy: their unique immune tolerance. Ann Thorac Surg 85: 571-579, 2008.
4. Ba ZF, Wang P, Koo DJ, Zhou M, Cioffi WG, Bland KI, Chaudry IH. Testosterone receptor blockade after trauma and hemorrhage attenuates depressed adrenal function. Am J Physiol Regul Integr Comp Physiol 279: R1841-R1848, 2000.
5. Choudhry MA, Schwacha MG, Hubbard WJ, Kerby JD, Rue LW, Bland KI, Chaudry IH. Gender differences in acute response to trauma-hemorrhage. Shock 24 Suppl 1: 101-106, 2005.
6. Crisostomo PR, Markel TA, Wang M, Lahm T, Lillemoe KD, Mel-drum DR. In the adult mesenchymal stem cell population, source gender is a biologically relevant aspect of protective power. Surgery 142: 215-221, 2007.
7. Crisostomo PR, Wang M, Herring CM, Markel TA, Meldrum KK, Lillemoe KD, Meldrum DR. Gender differences in injury induced mes-enchymal stem cell apoptosis and VEGF, TNF, IL-6 expression: role of the 55 kDa TNF receptor (TNFR1). J Mol Cell Cardiol 42: 142-149, 2007.
8. Crisostomo PR, Wang M, Herring CM, Morrell ED, Seshadri P, Meldrum KK, Meldrum DR. Sex dimorphisms in activated mesenchy-mal stem cell function. Shock 26: 571-574, 2006.
9. Crisostomo PR, Wang M, Wairiuko GM, Morrell ED, Meldrum DR. Brief exposure to exogenous testosterone increases death signaling and adversely affects myocardial function after ischemia. Am J Physiol Regul Integr Comp Physiol 290: R1168-R1174, 2006.
10. Dhanantwari P, Nadaraj S, Kenessey A, Chowdhury D, Al-Abed Y, Miller EJ, Ojamaa K. Macrophage migration inhibitory factor induces cardiomyocyte apoptosis. Biochem Biophys Res Commun 371: 298-303, 2008.
11. Di Nicola M, Carlo-Stella C, Magni M, Milanesi M, Longoni PD, Matteucci P, Grisanti S, Gianni AM. Human bone marrow stromal cells suppress T-lymphocyte proliferation induced by cellular or nonspecific mitogenic stimuli. Blood 99: 3838-3843, 2002.
12. Erwin GS, Crisostomo PR, Wang Y, Wang M, Markel TA, Guzman M, Sando IC, Sharma R, Meldrum DR. Estradiol-treated mesenchymal stem cells improve myocardial recovery after ischemia. J Surg Res 152: 319-324, 2009.
13. Frink M, Pape HC, van Griensven M, Krettek C, Chaudry IH, Hildebrand F. Influence of sex and age on MODS and cytokines after multiple injuries. Shock 27: 151-156, 2007.
14. Gonzalez-Rey E, Anderson P, Gonzalez MA, Rico L, Buscher D, Delgado M. Human adult stem cells derived from adipose tissue protect against experimental colitis and sepsis. Gut 58: 929-939, 2009.
15. Guerra S, Leri A, Wang X, Finato N, Di Loreto C, Beltrami CA, Kajstura J, Anversa P. Myocyte death in the failing human heart is gender dependent. Circ Res 85: 856-866, 1999.
16. Gupta N, Su X, Popov B, Lee JW, Serikov V, Matthay MA. Intrapul-monary delivery of bone marrow-derived mesenchymal stem cells improves survival and attenuates endotoxin-induced acute lung injury in mice. J Immunol 179: 1855-1863, 2007.
17. Hong L, Sultana H, Paulius K, Zhang G. Steroid regulation of proliferation and osteogenic differentiation of bone marrow stromal cells: a gender difference. J Steroid Biochem Mol Biol 114: 180-185, 2009.
18. Kelsey SF, James M, Holubkov AL, Holubkov R, Cowley MJ, Detre KM. Results of percutaneous transluminal coronary angioplasty in women. 1985-1986 National Heart, Lung, and Blood Institute's Coronary Angioplasty Registry. Circulation 87: 720-727, 1993.
19. Kher A, Wang M, Tsai BM, Pitcher JM, Greenbaum ES, Nagy RD, Patel KM, Wairiuko GM, Markel TA, Meldrum DR. Sex differences in the myocardial inflammatory response to acute injury. Shock 23: 1-10, 2005.
20. Lee JW, Fang X, Gupta N, Serikov V, Matthay MA. Allogeneic human mesenchymal stem cells for treatment of E. coli endotoxin-induced acute lung injury in the ex vivo perfused human lung. Proc Natl Acad Sci USA 106: 16357-16362, 2009.
21. MacDonald DJ, Luo J, Saito T, Duong M, Bernier PL, Chiu RC, Shum-Tim D. Persistence of marrow stromal cells implanted into acutely infarcted myocardium: observations in a xenotransplant model. J Thorac Cardiovasc Surg 130: 1114-1121, 2005.
22. Markel TA, Crisostomo PR, Wang M, Herrmann JL, Abarbanell AM, Meldrum DR. Right ventricular TNF resistance during endotoxemia: the differential effects on ventricular function. Am J Physiol Regul Integr Comp Physiol 293: R1893-R1897, 2007.
23. Mehilli J, Ndrepepa G, Kastrati A, Nekolla SG, Markwardt C, Bollwein H, Pache J, Martinoff S, Dirschinger J, Schwaiger M, Schomig A. Gender and myocardial salvage after reperfusion treatment in acute myocardial infarction. J Am Coll Cardiol 45: 828-831, 2005.
24. Mei SH, Haitsma JJ, Dos Santos CC, Deng Y, Lai PF, Slutsky AS, Liles WC, Stewart DJ. Mesenchymal stem cells reduce inflammation while enhancing bacterial clearance and improving survival in sepsis. Am J Respir Crit Care Med 182: 1047-1057, 2010.
25. Meldrum DR, Wang M, Tsai BM, Kher A, Pitcher JM, Brown JW, Meldrum KK. Intracellular signaling mechanisms of sex hormones in acute myocardial inflammation and injury. Front Biosci 10: 1835-1867, 2005.
26. Nemeth K, Leelahavanichkul A, Yuen PS, Mayer B, Parmelee A, Doi K, Robey PG, Leelahavanichkul K, Koller BH, Brown JM, Hu X, Jelinek I, Star RA, Mezey E. Bone marrow stromal cells attenuate sepsis via prostaglandin E(2)-dependent reprogramming of host macrophages to increase their interleukin-10 production. Nat Med 15: 42-49, 2009.
27. Peister A, Mellad JA, Larson BL, Hall BM, Gibson LF, Prockop DJ. Adult stem cells from bone marrow (MSCs) isolated from different strains of inbred mice vary in surface epitopes, rates of proliferation, and differentiation potential. Blood 103: 1662-1668, 2004.
28. Peng T, Zhang T, Lu X, Feng Q. JNK1/c-fos inhibits cardiomyocyte TNF-alpha expression via a negative crosstalk with ERK and p38 MAPK in endotoxaemia. Cardiovasc Res 81: 733-741, 2009.
29. Pevsner-Fischer M, Morad V, Cohen-Sfady M, Rousso-Noori L, Zanin-Zhorov A, Cohen S, Cohen IR, Zipori D. Toll-like receptors and their ligands control mesenchymal stem cell functions. Blood 109: 1422-1432, 2007.
30. Raju R, Chaudry IH. Sex steroids/receptor antagonist: their use as adjuncts after trauma-hemorrhage for improving immune/cardiovascular responses and for decreasing mortality from subsequent sepsis. Anesth Analg 107: 159-166, 2008.
31. Ray R, Herring CM, Markel TA, Crisostomo PR, Wang M, Weil B, Lahm T, Meldrum DR. Deleterious effects of endogenous and exogenous testosterone on mesenchymal stem cell VEGF production. Am J Physiol Regul Integr Comp Physiol 294: R1498-R1503, 2008.
32. Ray R, Novotny NM, Crisostomo PR, Lahm T, Abarbanell A, Meldrum DR. Sex steroids and stem cell function. Mol Med 14: 493-501, 2008.
33. Remick DG, Newcomb DE, Bolgos GL, Call DR. Comparison of the mortality and inflammatory response of two models of sepsis: lipopoly-saccharide vs. cecal ligation and puncture. Shock 13: 110-116, 2000.
34. Rudiger A, Singer M. Mechanisms of sepsis-induced cardiac dysfunction. Crit Care Med 35: 1599-1608, 2007.
35. Schroder J, Kahlke V, Book M, Stuber F. Gender differences in sepsis: genetically determined? Shock 14: 307-310; discussion 310-303, 2000.
36. Sharma AC. Sepsis-induced myocardial dysfunction. Shock 28: 265-269, 2007.
37. Sperry JL, Minei JP. Gender dimorphism following injury: making the connection from bench to bedside. J Leukoc Biol 83: 499-506, 2008.
38. Wang M, Baker L, Tsai BM, Meldrum KK, Meldrum DR. Sex differences in the myocardial inflammatory response to ischemia-reperfu-sion injury. Am J Physiol Endocrinol Metab 288: E321-E326, 2005.
39. Wang M, Sankula R, Tsai BM, Meldrum KK, Turrentine M, March KL, Brown JW, Dinarello CA, Meldrum DR. P38 MAPK mediates myocardial proinflammatory cytokine production and endotoxin-induced contractile suppression. Shock 21: 170-174, 2004.
40. Wang M, Tsai BM, Reiger KM, Brown JW, Meldrum DR. 17-fj-Estradiol decreases p38 MAPK-mediated myocardial inflammation and dysfunction following acute ischemia. J Mol Cell Cardiol 40: 205-212, 2006.
41. Weil BR, Manukyan MC, Herrmann JL, Wang Y, Abarbanell AM, Poynter JA, Meldrum DR. Mesenchymal stem cells attenuate myocardial functional depression and reduce systemic and myocardial inflammation during endotoxemia. Surgery 148: 444-452.
42. Weil BR, Markel TA, Herrmann JL, Abarbanell AM, Kelly ML, Meldrum DR. Stem cells in sepsis. Ann Surg 250: 19-27, 2009.
43. Xu J, Woods CR, Mora AL, Joodi R, Brigham KL, Iyer S, Rojas M. Prevention of endotoxin-induced systemic response by bone marrow-derived mesenchymal stem cells in mice. Am J Physiol Lung Cell Mol Physiol 293: L131-L141, 2007.
44. Yu HP, Chaudry IH. The role of estrogen and receptor agonists in maintaining organ function after trauma-hemorrhage. Shock 31: 227-237, 2009.
45. Zanotti-Cavazzoni SL, Hollenberg SM. Cardiac dysfunction in severe sepsis and septic shock. Curr Opin Crit Care 15: 392-397, 2009.
46. Zeller CN, Wang Y, Markel TA, Weil B, Abarbanell A, Herrmann JL, Kelly ML, Coffey A, Meldrum DR. Role of tumor necrosis factor receptor 1 in sex differences of stem cell mediated cardioprotection. Ann Thorac Surg 87: 812-819, 2009.
47. Zhu H, Shan L, Peng T. Rac1 mediates sex difference in cardiac tumor necrosis factor-alpha expression via NADPH oxidase-ERK1/2/p38 MAPK pathway in endotoxemia. J Mol Cell Cardiol 47: 264-274, 2009.