Interleukin-10 deficiency impairs bone marrow-derived endothelial progenitor cell survival and function in ischemic myocardium

Circulation Research

Volumn 109, Issue 11, 2011, Pages 1280-1289

  Krishnamurthy, Prasanna ^a   Thal, Melissa ^a   Verma, Suresh ^a   Hoxha, Eneda ^a   Lambers, Erin ^a   Ramirez, Veronica ^a   Qin, Gangjian ^a   Losordo, Douglas ^a   Kishore, Raj ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

angiogenesis; bone marrow transplantation; endothelial progenitor cells; IL 10; inflammation; left ventricular remodeling; myocardial infarction; survival

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; GREEN FLUORESCENT PROTEIN; INTERLEUKIN 10; PLERIXAFOR; STAT3 PROTEIN; STROMAL CELL DERIVED FACTOR 1; VASCULOTROPIN;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL FUNCTION; CELL SURVIVAL; CONTROLLED STUDY; ENDOTHELIAL PROGENITOR CELL; HEART INFARCTION; HEART INFARCTION SIZE; HEART LEFT VENTRICLE FUNCTION; HEART MUSCLE FIBROSIS; HEART MUSCLE ISCHEMIA; HEMATOPOIETIC STEM CELL TRANSPLANTATION; IMMUNE DEFICIENCY; KNOCKOUT MOUSE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL MOBILIZATION;

ANIMALS; BONE MARROW CELLS; CELL HYPOXIA; CELL SURVIVAL; CHEMOKINE CXCL12; ENDOTHELIAL CELLS; GRAFT SURVIVAL; HEART; HEMATOPOIETIC STEM CELL TRANSPLANTATION; INTERLEUKIN-10; MICE; MICE, KNOCKOUT; MYOCARDIAL INFARCTION; NEOVASCULARIZATION, PHYSIOLOGIC; RECEPTORS, CXCR4; RECOMBINANT PROTEINS; REGENERATION; STAT3 TRANSCRIPTION FACTOR; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VENTRICULAR REMODELING;

EID: 81355127625     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.111.248369     Document Type: Article

References (61)

1. Cottage CT, Bailey B, Fischer KM, Avitable D, Collins B, Tuck S, Quijada P, Gude N, Alvarez R, Muraski J, Sussman MA. Cardiac progenitor cell cycling stimulated by pim-1 kinase. Circ Res. 2010;106: 891-901.
2. D'Amario D, Cabral-Da-Silva MC, Zheng H, Fiorini C, Goichberg P, Steadman E, Ferreira-Martins J, Sanada F, Piccoli M, Cappetta D, D'Alessandro DA, Michler RE, Hosoda T, Anastasia L, Rota M, Leri A, Anversa P, Kajstura J. Insulin-like growth factor-1 receptor identifies a pool of human cardiac stem cells with superior therapeutic potential for myocardial regeneration. Circ Res. 2011;108:1467-1481.
3. D'Amario D, Fiorini C, Campbell PM, Goichberg P, Sanada F, Zheng H, Hosoda T, Rota M, Connell JM, Gallegos RP, Welt FG, Givertz MM, Mitchell RN, Leri A, Kajstura J, Pfeffer MA, Anversa P. Functionally competent cardiac stem cells can be isolated from endomyocardial biopsies of patients with advanced cardiomyopathies. Circ Res. 2011; 108:857-861.
4. Fischer KM, Din S, Gude N, Konstandin MH, Wu W, Quijada P, Sussman MA. Cardiac progenitor cell commitment is inhibited by nuclear Akt expression. Circ Res. 2011;108:960-970.
5. Hosoda T, Zheng H, Cabral-da-Silva M, Sanada F, Ide-Iwata N, Ogorek B, Ferreira-Martins J, Arranto C, D'Amario D, del Monte F, Urbanek K, D'Alessandro DA, Michler RE, Anversa P, Rota M, Kajstura J, Leri A. Human cardiac stem cell differentiation is regulated by a mircrine mechanism. Circulation. 2011;123:1287-1296.
6. Kanashiro-Takeuchi RM, Schulman IH, Hare JM. Pharmacologic and genetic strategies to enhance cell therapy for cardiac regeneration. J Mol Cell Cardiol. 2011;51:619-625.
7. Madonna R, Rokosh G, De Caterina R, Bolli R. Hepatocyte growth factor/Met gene transfer in cardiac stem cells: potential for cardiac repair. Basic Res Cardiol. 2010;105:443-452.
8. Ii M, Nishimura H, Iwakura A, Wecker A, Eaton E, Asahara T, Losordo DW. Endothelial progenitor cells are rapidly recruited to myocardium and mediate protective effect of ischemic preconditioning via "imported" nitric oxide synthase activity. Circulation. 2005;111:1114-1120. (Pubitemid 40365471)
9. Spyridopoulos I, Sullivan AB, Kearney M, Isner JM, Losordo DW. Estrogen-receptor-mediated inhibition of human endothelial cell apopto-sis: estradiol as a survival factor. Circulation. 1997;95:1505-1514. (Pubitemid 27142809)
10. Kajstura J, Rota M, Whang B, Cascapera S, Hosoda T, Bearzi C, Nurzynska D, Kasahara H, Zias E, Bonafe M, Nadal-Ginard B, Torella D, Nascimbene A, Quaini F, Urbanek K, Leri A, Anversa P. Bone marrow cells differentiate in cardiac cell lineages after infarction independently of cell fusion. Circ Res. 2005;96:127-137. (Pubitemid 40095762)
11. Masuda H, Kalka C, Takahashi T, Yoshida M, Wada M, Kobori M, Itoh R, Iwaguro H, Eguchi M, Iwami Y, Tanaka R, Nakagawa Y, Sugimoto A, Ninomiya S, Hayashi S, Kato S, Asahara T. Estrogen-mediated endothelial progenitor cell biology and kinetics for physiological postnatal vas-culogenesis. Circ Res. 2007;101:598-606. (Pubitemid 351325877)
12. Strehlow K, Werner N, Berweiler J, Link A, Dirnagl U, Priller J, Laufs K, Ghaeni L, Milosevic M, Bohm M, Nickenig G. Estrogen increases bone marrow-derived endothelial progenitor cell production and diminishes neointima formation. Circulation. 2003;107:3059-3065. (Pubitemid 36758980)
13. Zuba-Surma EK, Guo Y, Taher H, Sanganalmath SK, Hunt G, Vincent RJ, Kucia M, Abdel-Latif A, Tang XL, Ratajczak MZ, Dawn B, Bolli R. Transplantation of expanded bone marrow-derived very small embryonic-like stem cells (VSEL-SCs) improves left ventricular function and remodelling after myocardial infarction. J Cell Mol Med. 2011;15: 1319-1328.
14. Assmus B, Schachinger V, Teupe C, Britten M, Lehmann R, Dobert N, Grunwald F, Aicher A, Urbich C, Martin H, Hoelzer D, Dimmeler S, Zeiher AM. Transplantation of Progenitor Cells and Regeneration Enhancement in Acute Myocardial Infarction (TOPCARE-AMI). Circulation. 2002;106: 3009-3017. (Pubitemid 35440281)
15. Britten MB, Abolmaali ND, Assmus B, Lehmann R, Honold J, Schmitt J, Vogl TJ, Martin H, Schachinger V, Dimmeler S, Zeiher AM. Infarct remodeling after intracoronary progenitor cell treatment in patients with acute myocardial infarction (TOPCARE-AMI): mechanistic insights from serial contrast-enhanced magnetic resonance imaging. Circulation. 2003; 108:2212-2218. (Pubitemid 37368893)
16. Losordo DW, Schatz RA, White CJ, Udelson JE, Veereshwarayya V, Durgin M, Poh KK, Weinstein R, Kearney M, Chaudhry M, Burg A, Eaton L, Heyd L, Thorne T, Shturman L, Hoffmeister P, Story K, Zak V, Dowling D, Traverse JH, Olson RE, Flanagan J, Sodano D, Murayama T, Kawamoto A, Kusano KF, Wollins J, Welt F, Shah P, Soukas P, Asahara T, Henry TD. Intramyocardial transplantation of autologous CD34 + stem cells for intractable angina: a phase I/IIa double-blind, randomized controlled trial. Circulation. 2007;115:3165-3172. (Pubitemid 47018140)
17. Strauer BE, Brehm M, Zeus T, Kostering M, Hernandez A, Sorg RV, Kogler G, Wernet P. Repair of infarcted myocardium by autologous intracoronary mononuclear bone marrow cell transplantation in humans. Circulation. 2002;106:1913-1918. (Pubitemid 35176294)
18. Trachtenberg B, Velazquez DL, Williams AR, McNiece I, Fishman J, Nguyen K, Rouy D, Altman P, Schwarz R, Mendizabal A, Oskouei B, Byrnes J, Soto V, Tracy M, Zambrano JP, Heldman AW, Hare JM. Rationale and design of the Transendocardial Injection of Autologous Human Cells (bone marrow or mesenchymal) in Chronic Ischemic Left Ventricular Dysfunction and Heart Failure Secondary to Myocardial Infarction (TAC-HFT) trial: a randomized, double-blind, placebo-controlled study of safety and efficacy. Am Heart J. 2011;161:487-493.
19. Grisar J, Aletaha D, Steiner CW, Kapral T, Steiner S, Seidinger D, Weigel G, Schwarzinger I, Wolozcszuk W, Steiner G, Smolen JS. Depletion of endothelial progenitor cells in the peripheral blood of patients with rheumatoid arthritis. Circulation. 2005;111:204-211. (Pubitemid 40139733)
20. Werner N, Nickenig G. Influence of cardiovascular risk factors on endothelial progenitor cells: limitations for therapy? Arterioscler Thromb Vasc Biol. 2006;26:257-266. (Pubitemid 43732183)
21. Swijnenburg RJ, Schrepfer S, Cao F, Pearl JI, Xie X, Connolly AJ, Robbins RC, Wu JC. In vivo imaging of embryonic stem cells reveals patterns of survival and immune rejection following transplantation. Stem Cells Dev. 2008;17:1023-1029.
22. Burchfield JS, Iwasaki M, Koyanagi M, Urbich C, Rosenthal N, Zeiher AM, Dimmeler S. Interleukin-10 from transplanted bone marrow mononuclear cells contributes to cardiac protection after myocardial infarction. Circ Res. 2008;103:203-211.
23. Frangogiannis NG. Targeting the inflammatory response in healing myocardial infarcts. Curr Med Chem. 2006;13:1877-1893.
24. Frangogiannis NG, Mendoza LH, Lindsey ML, Ballantyne CM, Michael LH, Smith CW, Entman ML. IL-10 is induced in the reperfused myocardium and may modulate the reaction to injury. J Immunol. 2000;165: 2798-2808. (Pubitemid 30660731)
25. Stumpf C, Petzi S, Seybold K, Wasmeier G, Arnold M, Raaz D, Yilmaz A, Daniel WG, Garlichs CD. Atorvastatin enhances interleukin-10 levels and improves cardiac function in rats after acute myocardial infarction. Clin Sci (Lond). 2009;116:45-52.
26. Tang J, Wang J, Yang J, Kong X, Zheng F, Guo L, Zhang L, Huang Y. Mesenchymal stem cells over-expressing SDF-1 promote angiogenesis and improve heart function in experimental myocardial infarction in rats. Eur J Cardiothorac Surg. 2009;36:644-650.
27. Wang X, Li C, Chen Y, Hao Y, Zhou W, Chen C, Yu Z. Hypoxia enhances CXCR4 expression favoring microglia migration via HIF-1alpha activation. Biochem Biophys Res Commun. 2008;371:283-288.
28. Krishnamurthy P, Lambers E, Verma S, Thorne T, Qin G, Losordo DW, Kishore R. Myocardial knockdown of mRNA-stabilizing protein HuR attenuates post-MI inflammatory response and left ventricular dysfunction in IL-10-null mice. FASEB J. 2010;24:2484-2494.
29. Krishnamurthy P, Rajasingh J, Lambers E, Qin G, Losordo DW, Kishore R. IL-10 inhibits inflammation and attenuates left ventricular remodeling after myocardial infarction via activation of STAT3 and suppression of HuR. Circ Res. 2009;104:e9-e18.
30. 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. 2004;95:187-195. (Pubitemid 38988685)
31. Hilfiker-Kleiner D, Limbourg A, Drexler H. STAT3-mediated activation of myocardial capillary growth. Trends Cardiovasc Med. 2005;15: 152-157. (Pubitemid 41138880)
32. Wei D, Le X, Zheng L, Wang L, Frey JA, Gao AC, Peng Z, Huang S, Xiong HQ, Abbruzzese JL, Xie K. Stat3 activation regulates the expression of vascular endothelial growth factor and human pancreatic cancer angiogenesis and metastasis. Oncogene. 2003;22:319-329. (Pubitemid 36194328)
33. Losordo DW, Henry TD, Davidson C, Sup Lee J, Costa MA, Bass T, Mendelsohn F, Fortuin FD, Pepine CJ, Traverse JH, Amrani D, Ewenstein BM, Riedel N, Story K, Barker K, Povsic TJ, Harrington RA, Schatz RA. Intramyocardial, autologous CD34 + cell therapy for refractory angina. Circ Res. 2011;109:428-436.
34. Shintani S, Murohara T, Ikeda H, Ueno T, Honma T, Katoh A, Sasaki K, Shimada T, Oike Y, Imaizumi T. Mobilization of endothelial progenitor cells in patients with acute myocardial infarction. Circulation. 2001;103: 2776-2779. (Pubitemid 32550062)
35. Aiuti A, Webb IJ, Bleul C, Springer T, Gutierrez-Ramos JC. The chemokine SDF-1 is a chemoattractant for human CD34+hematopoietic progenitor cells and provides a new mechanism to explain the mobilization of CD34+progenitors to peripheral blood. J Exp Med. 1997;185: 111-120. (Pubitemid 27039446)
36. Ganju RK, Brubaker SA, Meyer J, Dutt P, Yang Y, Qin S, Newman W, Groopman JE. The alpha-chemokine, stromal cell-derived factor-1alpha, binds to the transmembrane G-protein-coupled CXCR-4 receptor and activates multiple signal transduction pathways. J Biol Chem. 1998;273: 23169-23175. (Pubitemid 28417500)
37. Abbott JD, Huang Y, Liu D, Hickey R, Krause DS, Giordano FJ. Stromal cell-derived factor-1alpha plays a critical role in stem cell recruitment to the heart after myocardial infarction but is not sufficient to induce homing in the absence of injury. Circulation. 2004;110:3300-3305. (Pubitemid 39557491)
38. Jujo K, Hamada H, Iwakura A, Thorne T, Sekiguchi H, Clarke T, Ito A, Misener S, Tanaka T, Klyachko E, Kobayashi K, Tongers J, Roncalli J, Tsurumi Y, Hagiwara N, Losordo DW. CXCR4 blockade augments bone marrow progenitor cell recruitment to the neovasculature and reduces mortality after myocardial infarction. Proc Natl Acad Sci USA. 2010; 107:11008-11013.
39. Honold J, Lehmann R, Heeschen C, Walter DH, Assmus B, Sasaki K, Martin H, Haendeler J, Zeiher AM, Dimmeler S. Effects of granulocyte colony simulating factor on functional activities of endothelial progenitor cells in patients with chronic ischemic heart disease. Arterioscler Thromb Vasc Biol. 2006;26:2238-2243. (Pubitemid 44465717)
40. Wang GL, Semenza GL. Desferoxamine induces erythropoietin gene expression and hypoxia-inducible factor 1 DNA-binding activity: implications for models of hypoxia signal transduction. Blood. 1993;82: 3610-3615. (Pubitemid 24006041)
41. Vengellur A, LaPres JJ. The role of hypoxia inducible factor 1alpha in cobalt chloride induced cell death in mouse embryonic fibroblasts. Toxicol Sci. 2004;82:638-646. (Pubitemid 39600093)
42. Xi L, Taher M, Yin C, Salloum F, Kukreja RC. Cobalt chloride induces delayed cardiac preconditioning in mice through selective activation of HIF-1alpha and AP-1 and iNOS signaling. Am J Physiol Heart Circ Physiol. 2004;287:H2369-H2375. (Pubitemid 39557104)
43. Ricchetti GA, Williams LM, Foxwell BM. Heme oxygenase 1 expression induced by IL-10 requires STAT-3 and phosphoinositol-3 kinase and is inhibited by lipopolysaccharide. J Leukoc Biol. 2004;76:719-726. (Pubitemid 39129106)
44. Sun M, Chen M, Dawood F, Zurawska U, Li JY, Parker T, Kassiri Z, Kirshenbaum LA, Arnold M, Khokha R, Liu PP. Tumor necrosis factor-alpha mediates cardiac remodeling and ventricular dysfunction after pressure overload state. Circulation. 2007;115:1398-1407. (Pubitemid 46648375)
45. Sun M, Dawood F, Wen WH, Chen M, Dixon I, Kirshenbaum LA, Liu PP. Excessive tumor necrosis factor activation after infarction contributes to susceptibility of myocardial rupture and left ventricular dysfunction. Circulation. 2004;110:3221-3228. (Pubitemid 39525069)
46. Bishopric NH. Mesenchymal stem cell-derived IL-10 and recovery from infarction: a third pitch for the chord. Circ Res. 2008;103:125-127.
47. Crisostomo PR, Markel TA, Wang Y, Meldrum DR. Surgically relevant aspects of stem cell paracrine effects. Surgery. 2008;143:577-581.
48. Rabelink TJ, de Boer HC, de Koning EJ, van Zonneveld AJ. Endothelial progenitor cells: more than an inflammatory response? Arterioscler Thromb Vasc Biol. 2004;24:834-838. (Pubitemid 38620859)
49. Andreou I, Tousoulis D, Tentolouris C, Antoniades C, Stefanadis C. Potential role of endothelial progenitor cells in the pathophysiology of heart failure: clinical implications and perspectives. Atherosclerosis. 2006;189:247-254. (Pubitemid 44634506)
50. Landmesser U, Engberding N, Bahlmann FH, Schaefer A, Wiencke A, Heineke A, Spiekermann S, Hilfiker-Kleiner D, Templin C, Kotlarz D, Mueller M, Fuchs M, Hornig B, Haller H, Drexler H. Statin-induced improvement of endothelial progenitor cell mobilization, myocardial neovascularization, left ventricular function, and survival after experimental myocardial infarction requires endothelial nitric oxide synthase. Circulation. 2004;110:1933-1939. (Pubitemid 39331904)
51. Seeger FH, Haendeler J, Walter DH, Rochwalsky U, Reinhold J, Urbich C, Rossig L, Corbaz A, Chvatchko Y, Zeiher AM, Dimmeler S. p38 mitogen-activated protein kinase downregulates endothelial progenitor cells. Circulation. 2005;111:1184-1191. (Pubitemid 40365481)
52. Moore KW, de Waal Malefyt R, Coffman RL, O'Garra A. Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol. 2001;19:683-765. (Pubitemid 32368050)
53. Molina-Holgado E, Vela JM, Arevalo-Martin A, Guaza C. LPS/IFN-gamma cytotoxicity in oligodendroglial cells: role of nitric oxide and protection by the anti-inflammatory cytokine IL-10. Eur J Neurosci. 2001;13:493-502. (Pubitemid 32158781)
54. Moreno R, Hernandez-Antolin R, Alfonso F, Macaya C. Diabetes mellitus and acute myocardial infarction: more data supporting a poorer microvasculature reperfusion. Am Heart J. 2003;146:E6.
55. Williams L, Bradley L, Smith A, Foxwell B. Signal transducer and activator of transcription 3 is the dominant mediator of the anti-inflammatory effects of IL-10 in human macrophages. J Immunol. 2004; 172:567-576. (Pubitemid 38020514)
56. Dhingra S, Sharma AK, Arora RC, Slezak J, Singal PK. IL-10 attenuates TNF-alpha-induced NF kappaB pathway activation and cardiomyocyte apoptosis. Cardiovasc Res. 2009;82:59-66.
57. Kawamoto A, Tkebuchava T, Yamaguchi J, Nishimura H, Yoon YS, Milliken C, Uchida S, Masuo O, Iwaguro H, Ma H, Hanley A, Silver M, Kearney M, Losordo DW, Isner JM, Asahara T. Intramyocardial transplantation of autologous endothelial progenitor cells for therapeutic neo-vascularization of myocardial ischemia. Circulation. 2003;107:461-468. (Pubitemid 36158050)
58. Uemura R, Xu M, Ahmad N, Ashraf M. Bone marrow stem cells prevent left ventricular remodeling of ischemic heart through paracrine signaling. Circ Res. 2006;98:1414-1421. (Pubitemid 43948066)
59. Badorff C, Brandes RP, Popp R, Rupp S, Urbich C, Aicher A, Fleming I, Busse R, Zeiher AM, Dimmeler S. Transdifferentiation of blood-derived human adult endothelial progenitor cells into functionally active cardio-myocytes. Circulation. 2003;107:1024-1032. (Pubitemid 36258727)
60. Murasawa S, Kawamoto A, Horii M, Nakamori S, Asahara T. Niche-dependent translineage commitment of endothelial progenitor cells, not cell fusion in general, into myocardial lineage cells. Arterioscler Thromb Vasc Biol. 2005;25:1388-1394. (Pubitemid 40923357)
61. Brunner S, Huber BC, Fischer R, Groebner M, Hacker M, David R, Zaruba MM, Vallaster M, Rischpler C, Wilke A, Gerbitz A, Franz WM. G-CSF treatment after myocardial infarction: impact on bone marrow-derived vs cardiac progenitor cells. Exp Hematol. 2008;36:695-702.