Intracardiac injection of erythropoietin induces stem cell recruitment and improves cardiac functions in a rat myocardial infarction model

Journal of Cellular and Molecular Medicine

Volumn 13, Issue 4, 2009, Pages 664-679

  Klopsch, Christian ^a   Furlani, Dario ^a   Gäbel, Ralf ^a   Li, Wenzhong ^a   Pittermann, Erik ^a   Ugurlucan, Murat ^a   Kundt, Guenther ^a   Zingler, Christiana ^a   Titze, Ulf ^a   Wang, Weiwei ^a   Ong, Lee Lee ^a   Wagner, Klaus ^c   Li, Ren Ke ^d   Ma, Nan ^a,b   Steinhoff, Gustav ^a  

^a UNIVERSITY OF ROSTOCK   (Germany)

^b INSTITUTE OF MATERIALS RESEARCH   (Germany)

^c Südstadt Clinic   (Germany)

^d UNIVERSITY OF TORONTO   (Canada)

Author keywords

Cardiac regeneration; Chemoattractant; Ischaemia; Stem and progenitor cells

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; CXCR4 PROTEIN, RAT; ERYTHROPOIETIN RECEPTOR; GELATINASE A; RECOMBINANT ERYTHROPOIETIN; STROMAL CELL DERIVED FACTOR 1; TROPONIN T;

ANGIOGENESIS; ANIMAL; APOPTOSIS; ARTICLE; CELL SURVIVAL; CYTOLOGY; DISEASE MODEL; DRUG EFFECT; ENZYMOLOGY; HEART FUNCTION TEST; HEART INFARCTION; HEART MUSCLE CELL; HEMATOCRIT; HUMAN; INJECTION; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; RAT; STEM CELL MOBILIZATION; UPREGULATION;

ANIMALS; APOPTOSIS; CELL SURVIVAL; CHEMOKINE CXCL12; DISEASE MODELS, ANIMAL; ERYTHROPOIETIN, RECOMBINANT; HEART FUNCTION TESTS; HEMATOCRIT; HEMATOPOIETIC STEM CELL MOBILIZATION; HUMANS; INJECTIONS; MATRIX METALLOPROTEINASE 2; MYOCARDIAL INFARCTION; MYOCYTES, CARDIAC; NEOVASCULARIZATION, PHYSIOLOGIC; RATS; RECEPTORS, CXCR4; RECEPTORS, ERYTHROPOIETIN; TROPONIN T; UP-REGULATION;

RATTUS;

EID: 65249153722     PISSN: 15821838     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1582-4934.2008.00546.x     Document Type: Article

References (52)

1. Jelkmann W, Wagner K. Beneficial and ominous aspects of the pleiotropic action of erythropoietin. Ann Hematol. 2004 83 : 673 86.
2. Zwezdaryk KJ, Coffelt SB, Figueroa YG, Liu J, Phinney DG, LaMarca HL, Florez L, Morris CB, Hoyle GW, Scandurro AB. Erythropoietin, a hypoxia-regulated factor, elicits a pro-angiogenic program in human mesenchymal stem cells. Exp Hematol. 2007 35 : 640 52.
3. Calvillo L, Latini R, Kajstura J, Leri A, Anversa P, Ghezzi P, Salio M, Cerami A, Brines M. Recombinant human erythro-poietin protects the myocardium from ischemia-reperfusion injury and promotes beneficial remodeling. Proc Natl Acad Sci USA. 2003 100 : 4802 6.
4. Parsa CJ, Matsumoto A, Kim J, Riel RU, Pascal LS, Walton GB, Thompson RB, Petrofski JA, Annex BH, Stamler JS, Koch WJ. A novel protective effect of ery-thropoietin in the infarcted heart. J Clin Invest. 2003 112 : 999 1007.
5. Tramontano AF, Muniyappa R, Black AD, Blendea MC, Cohen I, Deng L, Sowers JR, Cutaia MV, El-Sherif N. Erythropoietin protects cardiac myocytes from hypoxia-induced apoptosis through an Akt-depend-ent pathway. Biochem Biophys Res Commun. 2003 308 : 990 4.
6. Vandervelde S, van Luyn MJ, Tio RA, Harmsen MC. Signaling factors in stem cell-mediated repair of infarcted myocardium. J Mol Cell Cardiol. 2005 39 : 363 76.
7. Moon C, Krawczyk M, Ahn D, Ahmet I, Paik D, Lakatta EG, Talan MI. Erythropoietin reduces myocardial infarction and left ventricular functional decline after coronary artery ligation in rats. Proc Natl Acad Sci USA. 2003 100 : 11612 7.
8. Asaumi Y, Kagaya Y, Takeda M, Yamaguchi N, Tada H, Ito K, Ohta J, Shiroto T, Shirato K, Minegishi N, Shimokawa H. Protective role of endogenous erythropoietin system in non-hematopoietic cells against pressure overload-induced left ventricular dysfunction in mice. Circulation. 2007 115 : 2022 32.
9. Cai Z, Manalo DJ, Wei G, Rodriguez ER, Fox-Talbot K, Lu H, Zweier JL, Semenza GL. Hearts from rodents exposed to intermittent hypoxia or erythropoietin are protected against ischemia-reperfusion injury. Circulation. 2003 108 : 79 85.
10. Lipsic E, Van Der Meer P, Henning RH, Suurmeijer AJ, Boddeus KM, van Veldhuisen DJ, van Gilst WH, Schoemaker RG. Timing of erythropoietin treatment for cardioprotection in ischemia/reperfusion. J Cardiovasc Pharmacol. 2004 44 : 473 9.
11. Asahara T, Masuda H, Takahashi T, Kalka C, Pastore C, Silver M, Kearne M, Magner M, Isner JM. Bone marrow origin of endothelial progenitor cells responsible for postnatal vasculogenesis in physiological and pathological neovascularization. Circ Res. 1999 85 : 221 8.
12. Crosby JR, Kaminski WE, Schatteman G, Martin PJ, Raines EW, Seifert RA, Bowen-Pope DF. Endothelial cells of hematopoietic origin make a significant contribution to adult blood vessel formation. Circ Res. 2000 87 : 728 30.
13. Kalka C, Masuda H, Takahashi T, Kalka-Moll WM, Silver M, Kearney M, Li T, Isner JM, Asahara T. Transplantation of ex vivo expanded endothelial progenitor cells for therapeutic neovascularization. Proc Natl Acad Sci USA. 2000 97 : 3422 7.
14. Takahashi T, Kalka C, Masuda H, Chen D, Silver M, Kearney M, Magner M, Isner JM, Asahara T. Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization. Nat Med. 1999 5 : 434 8.
15. Schatteman GC, Hanlon HD, Jiao C, Dodds SG, Christy BA. Blood-derived angioblasts accelerate blood-flow restoration in diabetic mice. J Clin Invest. 2000 106 : 571 8.
16. Edelberg JM, Tang L, Hattori K, Lyden D, Rafii S. Young adult bone marrow-derived endothelial precursor cells restore aging-impaired cardiac angiogenic function. Circ Res. 2002 90 : E89 93.
17. Kawamoto A, Gwon HC, Iwaguro H, Yamaguchi JI, Uchida S, Masuda H, Silver M, Ma H, Kearney M, Isner JM, Asahara T. Therapeutic potential of ex vivo expanded endothelial progenitor cells for myocardial ischemia. Circulation. 2001 103 : 634 7.
18. Heeschen C, Aicher A, Lehmann R, Fichtlscherer S, Vasa M, Urbich C, Mildner-Rihm C, Martin H, Zeiher AM, Dimmeler S. Erythropoietin is a potent physiologic stimulus for endothelial progenitor cell mobilization. Blood. 2003 102 : 1340 6.
19. Bahlmann FH, DeGroot, K, Duckert T, Niemczyk E, Bahlmann E, Boehm SM, Haller H, Fliser D. Endothelial progenitor cell proliferation and differentiation is regulated by erythropoietin. Kidney Int. 2003 64 : 1648 52.
20. Bahlmann FH, De Groot K, Spandau JM, Landry AL, Hertel B, Duckert T, Boehm SM, Menne J, Haller H, Fliser D. Erythropoietin regulates endothelial progenitor cells. Blood. 2004 103 : 921 6.
21. George J, Goldstein E, Abashidze A, Wexler D, Hamed S, Shmilovich H, Deutsch V, Miller H, Keren G, Roth A. Erythropoietin promotes endothelial progenitor cell proliferative and adhesive properties in a PI 3-kinase-dependent manner. Cardiovasc Res. 2005 68 : 299 306.
22. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using realtime quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2001 25 : 402 8.
23. Hessel M H, Steendijk, P, den Adel, B, Schutte CI, Van Der Laarse A. Characterization of right ventricular function after monocrotaline-induced pulmonary hypertension in the intact rat. Am J Physiol Heart Circ Physiol. 2006 291 : H2424 30.
24. Agata, J, Chao, L, Chao J. Kallikrein gene delivery improves cardiac reserve and attenuates remodeling after myocardial infarction. Hypertension. 2002 40 : 653 9.
25. Lindahl B, Toss H, Siegbahn A, Venge P, Wallentin L. Markers of myocardial damage and inflammation in relation to long-term mortality in unstable coronary artery disease. FRISC Study Group. Fragmin during Instability in Coronary Artery Disease. N Engl J Med. 2000 343 : 1139 47.
26. Moller JE, Hillis GS, Oh JK, Pellikka PA. Prognostic importance of secondary pulmonary hypertension after acute myocar-dial infarction. Am J Cardiol. 2005 96 : 199 203.
27. Nishiya, D, Omura, T, Shimada, K, Matsumoto, R, Kusuyama, T, Enomoto, S, Iwao, H, Takeuchi, K, Yoshikawa, J, Yoshiyama M. Effects of erythropoietin on cardiac remodeling after myocardial infarction. J Pharmacol Sci. 2006 101 : 31 9.
28. Jasmin JF, Calderone A, Leung TK, Villeneuve L, Dupuis J. Lung structural remodeling and pulmonary hypertension after myocardial infarction: complete reversal with irbesartan. Cardiovasc Res. 2003 58 : 621 31.
29. Gao E, Boucher M, Chuprun JK, Zhou RH, Eckhart AD, Koch WJ. Darbepoetin alfa, a long-acting erythropoietin analog, offers novel and delayed cardioprotection for the ischemic heart. Am J Physiol Heart Circ Physiol. 2007 293 : H60 8.
30. Prunier F, Pfister O, Hadri L, Liang L, Del Monte F, Liao R, Hajjar RJ. Delayed ery-thropoietin therapy reduces post-MI cardiac remodeling only at a dose that mobilizes endothelial progenitor cells. Am J Physiol Heart Circ Physiol. 2007 292 : H522 9.
31. Besarab A, Bolton WK, Browne JK, Egrie JC, Nissenson AR, Okamoto DM, Schwab SJ, Goodkin DA. The effects of normal as compared with low hematocrit values in patients with cardiac disease who are receiving hemodialysis and epoetin. N Engl J Med. 1998 339 : 584 90.
32. van der Meer P, Voors AA, Lipsic E, Smilde TD, van Gilst WH, van Veldhuisen DJ. Prognostic value of plasma erythro-poietin on mortality in patients with chronic heart failure. J Am Coll Cardiol. 2004 44 : 63 7.
33. Ma N, Stamm C, Kaminski A, Li W, Kleine HD, Muller-Hilke B, Zhang L, Ladilov Y, Egger D, Steinhoff G. Human cord blood cells induce angiogenesis following myocardial infarction in NOD/scid-mice. Cardiovasc Res. 2005 66 : 45 54.
34. Elmadbouh I, Haider H, Jiang S, Idris NM, Lu G, Ashraf M. Ex vivo delivered stromal cell-derived factor-1alpha promotes stem cell homing and induces angiomyogenesis in the infarcted myocardium. J Mol Cell Cardiol. 2007 42 : 792 803.
35. 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, Mlirayama 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 72.
36. Stamm C, Westphal B, Klelne HD, Petzsch M, Klttner C, Kllnge H, Schumlchen C, Nlenaber CA, Freund M, Stelnhoff G. Autologous bone-marrow stem-cell transplantation for myocardial regeneration. Lancet. 2003 361 : 45 6.
37. Ratajczak MZ, Kucla M, Reca R, Majka M, Janowska-Wleczorek A, Ratajczak J. Stem cell plasticity revisited: CXCR4-posi-tive cells expressing mRNA for early muscle, liver and neural cells 'hide out' in the bone marrow. Leukemia. 2004 18 : 29 40.
38. Jaffredo T, Nottingham W, Llddlard K, Bollerot K, Pouget C, de Bruijn M. From hemangioblast to hematopoietic stem cell: an endothelial connection? Exp Hematol. 2005 33 : 1029 40.
39. Lapldot T, Dar A, Kollet O. How do stem cells find their way home? Blood. 2005 106 : 1901 10.
40. Cimini M, Fazel S, Zhuo S, Xaymardan M, Fujii H, Weisel RD, LI RK. c-kit dysfunction impairs myocardial healing after infarction. Circulation. 2007 116 : I77 82.
41. Kawamoto A, Iwasakl H, Kusano K, Murayama T, Oyamada A, Silver M, Hulbert C, Gavin M, Hanley A, Ma H, Kearney M, Zak V, Asahara T, Losordo DW. CD34-positive cells exhibit increased potency and safety for therapeutic neovas-cularization after myocardial infarction compared with total mononuclear cells. Circulation. 2006 114 : 2163 9.
42. Shlngo T, Sorokan ST, Shlmazakl T, Weiss S. Erythropoietin regulates the in vitro and in vivo production of neuronal progenitors by mammalian forebrain neural stem cells. J Neurosci. 2001 21 : 9733 43.
43. Beltraml AP, Barlucchl L, Torella D, Baker M, Llmana F, Chlmentl S, Kasahara H, Rota M, Musso E, Urbanek K, Lerl A, Kajstura J, Nadal-Glnard B, Anversa P. Adult cardiac stem cells are multipotent and support myocardial regeneration. Cell. 2003 114 : 763 76.
44. Burger D, Lei M, Geoghegan-Morphet N, Lu X, Xenocostas A, Feng Q. Erythropoietin protects cardiomyocytes from apoptosis via up-regulation of endothelial nitric oxide synthase. Cardiovasc Res. 2006 72 : 51 9.
45. Feng Q. Beyond erythropoiesis: the anti-inflammatory effects of erythropoietin. Cardiovasc Res. 2006 71 : 615 7.
46. Kamlnskl A, Ma N, Donndorf P, Llndenblatt N, Feldmeler G, Ong LL, Furlanl D, Skrabal CA, Llebold A, Vollmar B, Stelnhoff G. Endothelial NOS is required for SDF-1alpha/CXCR4-mediated peripheral endothelial adhesion of c-kit+ bone marrow stem cells. Lab Invest. 2008 88 : 58 69.
47. Kobayashi, H, Minatoguchi, S, Yasutla, S, Bao, N, Kawarnlira, I, Iwasa, M, Yamaki, T, Sumi, S, Misao, Y, Ushikoshi, H, Nishigaki, K, Takemura, G, Fujiwara, T, Tabata, Y, Fujiwara H. Post-infarct treatment with an erythropoietin-gelatin hydrogel drug delivery system for cardiac repair. Cardiovasc Res. 2008 79 : 611 20.
48. LI Y, Takemura G, Okada H, Mlyata S, Maruyama R, LI L, Hlguchl M, Minatoguchi S, Fujiwara T, Fujiwara H. Reduction of inflammatory cytokine expression and oxidative damage by erythropoietin in chronic heart failure. Cardiovasc Res. 2006 71 : 684 94.
49. Relmer KA, Lowe JE, Rasmussen MM, Jennings RB. The wavefront phenomenon of ischemic cell death. 1. Myocardial infarct size versus duration of coronary occlusion in dogs. Circulation. 1977 56 : 786 94.
50. Hlrayama A, Adachl T, Asada S, Mlshlma M, Nanto S, Kusuoka H, Yamamoto K, Matsumura Y, Horl M, Inoue M. Late reperfusion for acute myocardial infarction limits the dilatation of left ventricle without the reduction of infarct size. Circulation. 1993 88 : 2565 74.
51. Kocher AA, Schuster MD, Szabolcs MJ, Takuma S, Burkhoff D, Wang J, Homma S, Edwards NM, Itescu S. Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents car-diomyocyte apoptosis, reduces remodeling and improves cardiac function. Nat Med. 2001 7 : 430 6.
52. Hlrata A, Minamino T, Asanuma H, Fujita M, Wakeno M, Myolshl M, Tsukamoto O, Okada K, Koyama H, Komamura K, Takashlma S, Shlnozakl Y, Mori H, Shlraga M, Kltakaze M, Horl M. Erythropoietin enhances neovascularization of ischemic myocardium and improves left ventricular dysfunction after myocardial infarction in dogs. J Am Coll Cardiol. 2006 48 : 176 84.