Heparin disrupts the CXCR4/SDF-1 axis and impairs the functional capacity of bone marrow-derived mononuclear cells used for cardiovascular repair

Circulation Research

Volumn 111, Issue 7, 2012, Pages 854-862

  Seeger, Florian H ^a   Rasper, Tina ^a   Fischer, Ariane ^a   Muhly Reinholz, Marion ^a   Hergenreider, Eduard ^a   Leistner, David M ^a   Sommer, Katharina ^a   Manavski, Yosif ^a   Henschler, Reinhard ^a   Chavakis, Emmanouil ^a   Assmus, Birgit ^a   Zeiher, Andreas M ^a   Dimmeler, Stefanie ^a  

^a GOETHE UNIVERSITY   (Germany)

Author keywords

bivalirudin; bone marrow cells; cell migration; cell therapy; cell transplantation; heparin; myocardial infarction

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; HEPARIN; HIRULOG; STROMAL CELL DERIVED FACTOR 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BONE MARROW BIOPSY; BONE MARROW CELL; BONE MARROW DERIVED MONONUCLEAR CELL; CELL FUNCTION; CELL HOMING; CELL INVASION; COLONY FORMATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG EFFECT; DRUG RECEPTOR BINDING; EAR INJURY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IN VIVO STUDY; INTRACELLULAR SIGNALING; LIGAND BINDING; MONONUCLEAR CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; RECEPTOR BLOCKING; TISSUE REPAIR; WOUND;

ANIMALS; ANTICOAGULANTS; ANTITHROMBINS; BONE MARROW CELLS; CELL MOVEMENT; CELLS, CULTURED; CHEMOKINE CXCL12; DISEASE MODELS, ANIMAL; FEMALE; HEPARIN; HIRUDINS; HUMANS; LEUKOCYTES, MONONUCLEAR; MICE; MICE, INBRED STRAINS; MYOCARDIAL INFARCTION; PEPTIDE FRAGMENTS; RECEPTORS, CXCR4; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION; TISSUE THERAPY;

EID: 84866532849     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.112.265678     Document Type: Article

References (40)

1. Pitt B, Remme W, Zannad F, Neaton J, Martinez F, Roniker B, Bittman R, Hurley S, Kleiman J, Gatlin M. Eplerenone, a selective aldosterone blocker, in patients with left ventricular dysfunction after myocardial infarction. N Engl J Med. 2003;348:1309-1321.
2. Pfeffer MA, McMurray JJ, Velazquez EJ, et al. Valsartan, captopril, or both in myocardial infarction complicated by heart failure, left ventricular dysfunction, or both. N Engl J Med. 2003;349:1893-1906.
3. Steinhauser ML, Lee RT. Regeneration of the heart. EMBO Mol Med. 2011;3:701-712.
4. Zimmet H, Porapakkham P, Sata Y, Haas SJ, Itescu S, Forbes A, Krum H. Short-and long-term outcomes of intracoronary and endogenously mobilized bone marrow stem cells in the treatment of ST-segment elevation myocardial infarction: a meta-analysis of randomized control trials. Eur J Heart Fail. 2012;14:91-105.
5. Lipinski MJ, Biondi-Zoccai GG, Abbate A, Khianey R, Sheiban I, Bartunek J, Vanderheyden M, Kim HS, Kang HJ, Strauer BE, Vetrovec GW. Impact of intracoronary cell therapy on left ventricular function in the setting of acute myocardial infarction: a collaborative systematic review and meta-analysis of controlled clinical trials. J Am Coll Cardiol. 2007;50:1761-1767.
6. Martin-Rendon E, Brunskill SJ, Hyde CJ, Stanworth SJ, Mathur A, Watt SM. Autologous bone marrow stem cells to treat acute myocardial infarction: a systematic review. Eur Heart J. 2008;29:1807-1818.
7. Schachinger V, Erbs S, Elsasser A, Haberbosch W, Hambrecht R, Holschermann H, Yu J, Corti R, Mathey DG, Hamm CW, Suselbeck T, Assmus B, Tonn T, Dimmeler S, Zeiher AM. Intracoronary bone marrow-derived progenitor cells in acute myocardial infarction. N Engl J Med. 2006;355:1210-1221.
8. Schachinger V, Erbs S, Elsasser A, et al. Improved clinical outcome after intracoronary administration of bone-marrow-derived progenitor cells in acute myocardial infarction: final 1-year results of the REPAIR-AMI trial. Eur Heart J. 2006;27:2775-2783.
9. Askari AT, Unzek S, Popovic ZB, Goldman CK, Forudi F, Kiedrowski M, Rovner A, Ellis SG, Thomas JD, DiCorleto PE, Topol EJ, Penn MS. Effect of stromal-cell-derived factor 1 on stem-cell homing and tissue regeneration in ischaemic cardiomyopathy. Lancet. 2003;362:697-703.
10. Ceradini DJ, Kulkarni AR, Callaghan MJ, Tepper OM, Bastidas N, Kleinman ME, Capla JM, Galiano RD, Levine JP, Gurtner GC. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med. 2004;10:858-864.
11. Salcedo R, Wasserman K, Young HA, Grimm MC, Howard OM, Anver MR, Kleinman HK, Murphy WJ, Oppenheim JJ. Vascular endothelial growth factor and basic fibroblast growth factor induce expression of CXCR4 on human endothelial cells: in vivo neovascularization induced by stromal-derived factor-1alpha. Am J Pathol. 1999;154:1125-1135.
12. Walter DH, Haendeler J, Reinhold J, Rochwalsky U, Seeger F, Honold J, Hoffmann J, Urbich C, Lehmann R, Arenzana-Seisdesdos F, Aicher A, Heeschen C, Fichtlscherer S, Zeiher AM, Dimmeler S. Impaired CXCR4 signaling contributes to the reduced neovascularization capacity of endo-thelial progenitor cells from patients with coronary artery disease. Circ Res. 2005;97:1142-1151.
13. Zhang D, Fan GC, Zhou X, Zhao T, Pasha Z, Xu M, Zhu Y, Ashraf M, Wang Y. Over-expression of CXCR4 on mesenchymal stem cells augments myoangiogenesis in the infarcted myocardium. J Mol Cell Cardiol. 2008;44:281-292.
14. Seeger FH, Rasper T, Koyanagi M, Fox H, Zeiher AM, Dimmeler S. CXCR4 expression determines functional activity of bone marrow-derived mononuclear cells for therapeutic neovascularization in acute ischemia. Arterioscler Thromb Vasc Biol. 2009;29:1802-1809.
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.
16. Heeschen C, Lehmann R, Honold J, Assmus B, Aicher A, Walter DH, Martin H, Zeiher AM, Dimmeler S. Profoundly reduced neovascular-ization capacity of bone marrow mononuclear cells derived from patients with chronic ischemic heart disease. Circulation. 2004;109:1615-1622.
17. Li TS, Mikamo A, Takahashi M, Suzuki R, Ueda K, Ikeda Y, Matsuzaki M, Hamano K. Comparison of cell therapy and cytokine therapy for functional repair in ischemic and nonischemic heart failure. Cell Transplant. 2007;16:365-374.
18. Lunde K, Solheim S, Aakhus S, et al. Intracoronary injection of mono-nuclear bone marrow cells in acute myocardial infarction. N Engl J Med. 2006;355:1199-1209.
19. Hirsch A, Nijveldt R, van der Vleuten PA, Tijssen JG, van der Giessen WJ, Tio RA, Waltenberger J, ten Berg JM, Doevendans PA, Aengevaeren WR, Zwaginga JJ, Biemond BJ, van Rossum AC, Piek JJ, Zijlstra F. Intracoronary infusion of mononuclear cells from bone marrow or peripheral blood compared with standard therapy in patients after acute myocardial infarction treated by primary percutaneous coronary intervention: results of the randomized controlled HEBE trial. Eur Heart J. 2011;32:1736-1747.
20. Vulliet PR, Greeley M, Halloran SM, MacDonald KA, Kittleson MD. Intra-coronary arterial injection of mesenchymal stromal cells and micro-infarction in dogs. Lancet. 2004;363:783-784.
21. Kang HJ, Kim HS, Park YB. Stem cell therapy for myocardial infarction. CMAJ. 2004;171:442-443.
22. Freyman T, Polin G, Osman H, Crary J, Lu M, Cheng L, Palasis M, Wilensky RL. A quantitative, randomized study evaluating three methods of mesenchymal stem cell delivery following myocardial infarction. Eur Heart J. 2006;27:1114-1122.
23. Sadir R, Baleux F, Grosdidier A, Imberty A, Lortat-Jacob H. Characterization of the stromal cell-derived factor-1alpha-heparin complex. J Biol Chem. 2001;276:8288-8296.
24. Murphy JW, Cho Y, Sachpatzidis A, Fan C, Hodsdon ME, Lolis E. Structural and functional basis of CXCL12 (stromal cell-derived factor-1 alpha) binding to heparin. J Biol Chem. 2007;282:10018-10027.
25. Harvey JR, Mellor P, Eldaly H, Lennard TW, Kirby JA, Ali S. Inhibition of CXCR4-mediated breast cancer metastasis: a potential role for hepa-rinoids? Clin Cancer Res. 2007;13:1562-1570.
26. Ma L, Qiao H, He C, Yang Q, Cheung CH, Kanwar JR, Sun X. Modulating the interaction of CXCR4 and CXCL12 by low-molecular-weight heparin inhibits hepatic metastasis of colon cancer. Invest New Drugs. 2012;30:508-517.
27. Warkentin TE, Greinacher A, Koster A. Bivalirudin. Thromb Haemost. 2008;99:830-839.
28. Kapur NK, Shenoy C, Yunis AA, Mohammad NN, Wilson S, Paruchuri V, Mackey EE, Qiao X, Shah A, Esposito ML, Karas RH, Jaffe IZ. Distinct effects of unfractionated heparin versus bivalirudin on circulating angiogenic peptides. PLoS One. 2012;7:e34344.
29. Assmus B, Honold J, Schachinger V, Britten MB, Fischer-Rasokat U, Lehmann R, Teupe C, Pistorius K, Martin H, Abolmaali ND, Tonn T, Dimmeler S, Zeiher AM. Transcoronary transplantation of progenitor cells after myocardial infarction. N Engl J Med. 2006;355:1222-1232.
30. Rubin JB, Kung AL, Klein RS, Chan JA, Sun Y, Schmidt K, Kieran MW, Luster AD, Segal RA. A small-molecule antagonist of CXCR4 inhibits intracranial growth of primary brain tumors. Proc Natl Acad Sci U S A. 2003;100:13513-13518.
31. Wu M, Chen Q, Li D, Li X, Huang C, Tang Y, Zhou Y, Wang D, Tang K, Cao L, Shen S, Li G. LRRC4 inhibits human glioblastoma cells proliferation, invasion, and proMMP-2 activation by reducing SDF-1 alpha/CXCR4-mediated ERK1/2 and Akt signaling pathways. J Cell Biochem. 2008;103:245-255.
32. Vander Kooi CW, Jusino MA, Perman B, Neau DB, Bellamy HD, Leahy DJ. Structural basis for ligand and heparin binding to neuropilin B domains. Proc Natl Acad Sci U S A. 2007;104:6152-6157.
33. Ashikari-Hada S, Habuchi H, Kariya Y, Itoh N, Reddi AH, Kimata K. Characterization of growth factor-binding structures in heparin/heparan sulfate using an octasaccharide library. J Biol Chem. 2004;279:12346-12354.
34. Kan M, Wang F, Xu J, Crabb JW, Hou J, McKeehan WL. An essential heparin-binding domain in the fibroblast growth factor receptor kinase. Science. 1993;259:1918-1921.
35. Walter DH, Rochwalsky U, Reinhold J, Seeger F, Aicher A, Urbich C, Spyridopoulos I, Chun J, Brinkmann V, Keul P, Levkau B, Zeiher AM, Dimmeler S, Haendeler J. Sphingosine-1-phosphate stimulates the functional capacity of progenitor cells by activation of the CXCR4-dependent signaling pathway via the S1P3 receptor. Arterioscler Thromb Vasc Biol. 2007;27:275-282.
36. Narsinh KH, Lan F, Liu J, Robbins RC, Wu JC. Site specific reporter gene imaging of stem cell transplantation: early engraftment predicts late improvement in cardiac function. Circulation. 2011;124:A556. Abstract 9306.
37. Seeger FH, Tonn T, Krzossok N, Zeiher AM, Dimmeler S. Cell isolation procedures matter: a comparison of different isolation protocols of bone marrow mononuclear cells used for cell therapy in patients with acute myocardial infarction. Eur Heart J. 2007;28:766-772.
38. Hamm CW, Bassand JP, Agewall S, et al. ESC guidelines for the management of acute coronary syndromes in patients presenting without persistent ST-segment elevation: the task force for the management of acute coronary syndromes (ACS) in patients presenting without persistent ST-segment elevation of the European Society of Cardiology (ESC). Eur Heart J. 2011;32:2999-3054.
39. Stone GW, Witzenbichler B, Guagliumi G, Peruga JZ, Brodie BR, Dudek D, Kornowski R, Hartmann F, Gersh BJ, Pocock SJ, Dangas G, Wong SC, Fahy M, Parise H, Mehran R. Heparin plus a glycoprotein IIb/IIIa inhibitor versus bivalirudin monotherapy and paclitaxel-eluting stents versus bare-metal stents in acute myocardial infarction (HORIZONS-AMI): final 3-year results from a multicentre, randomised controlled trial. Lancet. 2011;377:2193-2204.
40. Lee MS, Liao H, Yang T, Dhoot J, Tobis J, Fonarow G, Mahmud E. Comparison of bivalirudin versus heparin plus glycoprotein IIb/IIIa inhibitors in patients undergoing an invasive strategy: a meta-analysis of randomized clinical trials. Int J Cardiol. 2011;152:369-374.