The bispecific SDF1-GPVI fusion protein preserves myocardial function after transient ischemia in Mice

Circulation

Volumn 125, Issue 5, 2012, Pages 685-696

  Ziegler, Melanie ^a   Elvers, Margitta ^a   Baumer, Yvonne ^b,e   Leder, Christoph ^a   Ochmann, Carmen ^a   Schönberger, Tanja ^a   Jürgens, Tobias ^a   Geisler, Tobias ^a   Schlosshauer, Burkhard ^b   Lunov, Oleg ^c   Engelhardt, Stefan ^d   Simmet, Thomas ^c   Gawaz, Meinrad ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c UNIVERSITY OF ULM   (Germany)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^e UNIVERSITY OF HAWAII   (United States)

Author keywords

cells; GPVI; myocardial infarction; SDF 1; tissue repair

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; COLLAGEN; GLYCOPROTEIN VI; SCLEROPROTEIN; STROMAL CELL DERIVED FACTOR 1; STROMAL CELL DERIVED FACTOR 1 GLYCOPROTEIN VI FUSION PROTEIN; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CELL DIFFERENTIATION; CHEMOTAXIS; CONTROLLED STUDY; DRUG RECEPTOR BINDING; HEART FUNCTION; HEART INFARCTION; HEART INFARCTION SIZE; HEART MUSCLE REPERFUSION; IN VITRO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; UPREGULATION;

ANIMALS; BONE MARROW CELLS; CELL DIFFERENTIATION; CELL SURVIVAL; CHEMOKINE CXCL12; COLLAGEN; HEART; ISCHEMIC ATTACK, TRANSIENT; MICE; MICE, INBRED C57BL; MODELS, ANIMAL; MYOCARDIAL INFARCTION; MYOCYTES, CARDIAC; NEOVASCULARIZATION, PHYSIOLOGIC; PLATELET MEMBRANE GLYCOPROTEINS; PROTEIN BINDING; RECEPTORS, CXCR4; RECOMBINANT FUSION PROTEINS; TISSUE THERAPY; TREATMENT OUTCOME;

EID: 84857048486     PISSN: 00097322     EISSN: 15244539     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.111.070508     Document Type: Article

References (47)

1. Saxena A, Fish JE, White MD, Yu S, Smyth JW, Shaw RM, DiMaio JM, Srivastava D. Stromal cell-derived factor-1alpha is cardioprotective after myocardial infarction. Circulation. 2008;117:2224-2231.
2. 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. (Pubitemid 37101067)
3. Werner N, Kosiol S, Schiegl T, Ahlers P, Walenta K, Link A, Bohm M, Nickenig G. Circulating endothelial progenitor cells and cardiovascular outcomes. N Engl J Med. 2005;353:999-1007. (Pubitemid 41262334)
4. Schmidt-Lucke C, Rossig L, Fichtlscherer S, Vasa M, Britten M, Kamper U, Dimmeler S, Zeiher AM. Reduced number of circulating endothelial progenitor cells predicts future cardiovascular events: proof of concept for the clinical importance of endogenous vascular repair. Circulation. 2005;111:2981-2987. (Pubitemid 40814192)
5. Asahara T, Murohara T, Sullivan A, Silver M, van der Zee R, Li T, Witzenbichler B, Schatteman G, Isner JM. Isolation of putative progenitor endothelial cells for angiogenesis. Science. 1997;275:964-967. (Pubitemid 27087709)
6. Rafii S, Lyden D. Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration. Nat Med. 2003;9:702-712. (Pubitemid 36749219)
7. Orlic D, Kajstura J, Chimenti S, Jakoniuk I, Anderson SM, Li B, Pickel J, McKay R, Nadal-Ginard B, Bodine DM, Leri A, Anversa P. Bone marrow cells regenerate infarcted myocardium. Nature. 2001;410: 701-705. (Pubitemid 32290358)
8. Matsuura K, Honda A, Nagai T, Fukushima N, Iwanaga K, Tokunaga M, Shimizu T, Okano T, Kasanuki H, Hagiwara N, Komuro I. Transplantation of cardiac progenitor cells ameliorates cardiac dysfunction after myocardial infarction in mice. J Clin Invest. 2009;119:2204-2217.
9. Christoforou N, Oskouei BN, Esteso P, Hill CM, Zimmet JM, Bian W, Bursac N, Leong KW, Hare JM, Gearhart JD. Implantation of mouse embryonic stem cell-derived cardiac progenitor cells preserves function of infarcted murine hearts. PLoS One. 2010;5:e11536.
10. Cho HJ, Lee N, Lee JY, Choi YJ, Ii M, Wecker A, Jeong JO, Curry C, Qin G, Yoon YS. Role of host tissues for sustained humoral effects after endothelial progenitor cell transplantation into the ischemic heart. J Exp Med. 2007;204:3257-3269.
11. Sutton MG, Sharpe N. Left ventricular remodeling after myocardial infarction: pathophysiology and therapy. Circulation. 2000;101: 2981-2988. (Pubitemid 30415891)
12. 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)
13. Wollert KC, Meyer GP, Lotz J, Ringes-Lichtenberg S, Lippolt P, Breidenbach C, Fichtner S, Korte T, Hornig B, Messinger D, Arseniev L, Hertenstein B, Ganser A, Drexler H. Intracoronary autologous bonemarrow cell transfer after myocardial infarction: the BOOST randomised controlled clinical trial. Lancet. 2004;364:141-148. (Pubitemid 38891685)
14. 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 marrowderived progenitor cells in acute myocardial infarction. N Engl J Med. 2006;355:1210-1221. (Pubitemid 44427445)
15. Lunde K, Solheim S, Aakhus S, Arnesen H, Abdelnoor M, Egeland T, Endresen K, Ilebekk A, Mangschau A, Fjeld JG, Smith HJ, Taraldsrud E, Grogaard HK, Bjornerheim R, Brekke M, Muller C, Hopp E, Ragnarsson A, Brinchmann JE, Forfang K. Intracoronary injection of mononuclear bone marrow cells in acute myocardial infarction. N Engl J Med. 2006; 355:1199-1209. (Pubitemid 44427444)
16. Meyer GP, Wollert KC, Lotz J, Pirr J, Rager U, Lippolt P, Hahn A, Fichtner S, Schaefer A, Arseniev L, Ganser A, Drexler H. Intracoronary bone marrow cell transfer after myocardial infarction: 5-year follow-up from the randomized-controlled BOOST trial. Eur Heart J. 2009;30: 2978-2984.
17. Lapidot T, Dar A, Kollet O. How do stem cells find their way home? Blood. 2005;106:1901-1910. (Pubitemid 41291700)
18. Hu X, Dai S, Wu WJ, Tan W, Zhu X, Mu J, Guo Y, Bolli R, Rokosh G. Stromal cell derived factor-1 alpha confers protection against myocardial ischemia/reperfusion injury: role of the cardiac stromal cell derived factor-1 alpha CXCR4 axis. Circulation. 2007;116:654-663. (Pubitemid 47356350)
19. Massberg S, Konrad I, Schurzinger K, Lorenz M, Schneider S, Zohlnhoefer D, Hoppe K, Schiemann M, Kennerknecht E, Sauer S, Schulz C, Kerstan S, Rudelius M, Seidl S, Sorge F, Langer H, Peluso M, Goyal P, Vestweber D, Emambokus NR, Busch DH, Frampton J, Gawaz M. Platelets secrete stromal cell-derived factor 1alpha and recruit bone marrow-derived progenitor cells to arterial thrombi in vivo. J Exp Med. 2006;203:1221-1233. (Pubitemid 43736592)
20. Stellos K, Langer H, Daub K, Schoenberger T, Gauss A, Geisler T, Bigalke B, Mueller I, Schumm M, Schaefer I, Seizer P, Kraemer BF, Siegel-Axel D, May AE, Lindemann S, Gawaz M. Platelet-derived stromal cell-derived factor-1 regulates adhesion and promotes differentiation of human CD34-cells to endothelial progenitor cells. Circulation. 2008;117:206-215.
21. Stellos K, Bigalke B, Langer H, Geisler T, Schad A, Kogel A, Pfaff F, Stakos D, Seizer P, Muller I, Htun P, Lindemann S, Gawaz M. Expression of stromal-cell-derived factor-1 on circulating platelets is increased in patients with acute coronary syndrome and correlates with the number of CD34(+) progenitor cells. Eur Heart J. 2009;30:584-593.
22. Frederick JR, Fitzpatrick JR III, McCormick RC, Harris DA, Kim AY, Muenzer JR, Marotta N, Smith MJ, Cohen JE, Hiesinger W, Atluri P, Woo YJ. Stromal cell-derived factor-1alpha activation of tissueengineered endothelial progenitor cell matrix enhances ventricular function after myocardial infarction by inducing neovasculogenesis. Circulation. 2010;122:S107-S117.
23. Massberg S, Konrad I, Bultmann A, Schulz C, Munch G, Peluso M, Lorenz M, Schneider S, Besta F, Muller I, Hu B, Langer H, Kremmer E, Rudelius M, Heinzmann U, Ungerer M, Gawaz M. Soluble glycoprotein VI dimer inhibits platelet adhesion and aggregation to the injured vessel wall in vivo. FASEB J. 2004;18:397-399.
24. Daub K, Siegel-Axel D, Schonberger T, Leder C, Seizer P, Muller K, Schaller M, Penz S, Menzel D, Buchele B, Bultmann A, Munch G, Lindemann S, Simmet T, Gawaz M. Inhibition of foam cell formation using a soluble CD68-Fc fusion protein. J Mol Med. 2010;88:909-920.
25. Seizer P, Ochmann C, Schonberger T, Zach S, Rose M, Borst O, Klingel K, Kandolf R, Macdonald HR, Nowak RA, Engelhardt S, Lang F, Gawaz M, May AE. Disrupting the EMMPRIN (CD147)-cyclophilin A interaction reduces infarct size and preserves systolic function after myocardial ischemia and reperfusion. Arterioscler Thromb Vasc Biol. 2011; 31:1377-1386.
26. Borst O, Ochmann C, Schonberger T, Jacoby C, Stellos K, Seizer P, Flogel U, Lang F, Gawaz M. Methods employed for induction and analysis of experimental myocardial infarction in mice. Cell Physiol Biochem. 2011;28:1-12.
27. Lataillade JJ, Clay D, Bourin P, Herodin F, Dupuy C, Jasmin C, Bousse-Kerdiles MC. Stromal cell-derived factor 1 regulates primitive hematopoiesis by suppressing apoptosis and by promoting G(0)/G(1) transition in CD34(+) cells: evidence for an autocrine/paracrine mechanism. Blood. 2002;99:1117-1129. (Pubitemid 34547062)
28. Hristov M, Weber C. Endothelial progenitor cells in vascular repair and remodeling. Pharmacol Res. 2008;58:148-151.
29. Dejana E, Corada M, Lampugnani MG. Endothelial cell-to-cell junctions. FASEB J. 1995;9:910-918.
30. Zeibig S, Li Z, Wagner S, Holthoff HP, Ungerer M, Bultmann A, Uhland K, Vogelmann J, Simmet T, Gawaz M, Munch G. Effect of the oxLDL binding protein Fc-CD68 on plaque extension and vulnerability in atherosclerosis. Circ Res. 2011;108:695-703.
31. Ungerer M, Rosport K, Bultmann A, Piechatzek R, Uhland K, Schlieper P, Gawaz M, Munch G. Novel antiplatelet drug revacept (dimeric glycoprotein VI-Fc) specifically and efficiently inhibited collagen-induced platelet aggregation without affecting general hemostasis in humans. Circulation. 2011;123:1891-1899.
32. Ruggeri ZM. Platelets in atherothrombosis. Nat Med. 2002;8:1227-1234. (Pubitemid 35373553)
33. Clemetson KJ, Clemetson JM. Platelet collagen receptors. Thromb Haemost. 2001;86:189-197. (Pubitemid 32663952)
34. Bultmann A, Li ZM, Wagner S, Peluso M, Schonberger T, Weis C, Konrad I, Stellos K, Massberg S, Nieswandt B, Gawaz M, Ungerer M, Munch G. Impact of glycoprotein VI and platelet adhesion on atherosclerosis: a possible role of fibronectin. J Mol Cell Cardiol. 2010;49: 532-542.
35. Langer H, May AE, Daub K, Heinzmann U, Lang P, Schumm M, Vestweber D, Massberg S, Schonberger T, Pfisterer I, Hatzopoulos AK, Gawaz M. Adherent platelets recruit and induce differentiation of murine embryonic endothelial progenitor cells to mature endothelial cells in vitro. Circ Res. 2006;98:E2-E10.
36. Aiuti A, Webb IJ, Bleul C, Springer T, GutierrezRamos 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)
37. Bleul CC, Farzan M, Choe H, Parolin C, Clark-Lewis I, Sodroski J, Springer TA. The lymphocyte chemoattractant SDF-1 is a ligand for LESTR/fusin and blocks HIV-1 entry. Nature. 1996;382:829-833. (Pubitemid 26299570)
38. Kraemer BF, Borst O, Gehring EM, Schoenberger T, Urban B, Ninci E, Seizer P, Schmidt C, Bigalke B, Koch M, Martinovic I, Daub K, Merz T, Schwanitz L, Stellos K, Fiesel F, Schaller M, Lang F, Gawaz M, Lindemann S. PI3 kinase-dependent stimulation of platelet migration by stromal cell-derived factor 1 (SDF-1). J Mol Med. 2010;88:1277-1288.
39. 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. (Pubitemid 39070860)
40. 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)
41. Segers VF, Tokunou T, Higgins LJ, MacGillivray C, Gannon J, Lee RT. Local delivery of protease-resistant stromal cell derived factor-1 for stem cell recruitment after myocardial infarction. Circulation. 2007;116: 1683-1692. (Pubitemid 47537842)
42. Jin DK, Shido K, Kopp HG, Petit I, Shmelkov SV, Young LM, Hooper AT, Amano H, Avecilla ST, Heissig B, Hattori K, Zhang F, Hicklin DJ, Wu Y, Zhu ZP, Dunn A, Salari H, Werb Z, Hackett NR, Crystal RG, Lyden D, Rafii S. Cytokine-mediated deployment of SDF-1 induces revascularization through recruitment of CXCR4(+) hemangiocytes. Nat Med. 2006;12:557-567.
43. Zhang M, Mal N, Kiedrowski M, Chacko M, Askari AT, Popovic ZB, Koc ON, Penn MS. SDF-1 expression by mesenchymal stem cells results in trophic support of cardiac myocytes after myocardial infarction. FASEB J. 2007;21:3197-3207. (Pubitemid 47565538)
44. Takahashi M. Role of the SDF-1/CXCR4 system in myocardial infarction. Circ J. 2010;74:418-423.
45. Chien KR. Regenerative medicine and human models of human disease. Nature. 2008;453:302-305. (Pubitemid 351693135)
46. Zaruba MM, Theiss HD, Vallaster M, Mehl U, Brunner S, David R, Fischer R, Krieg L, Hirsch E, Huber B, Nathan P, Israel L, Imhof A, Herbach N, Assmann G, Wanke R, Mueller-Hoecker J, Steinbeck G, Franz WM. Synergy between CD26/DPP-IV inhibition and G-CSF improves cardiac function after acute myocardial infarction. Cell Stem Cell. 2009;4:313-323.
47. George J, Afek A, Abashidze A, Shmilovich H, Deutsch V, Kopolovich J, Miller H, Keren G. Transfer of endothelial progenitor and bone marrow cells influences atherosclerotic plaque size and composition in apolipoprotein E knockout mice. Arterioscler Thromb Vasc Biol. 2005;25:2636-2641. (Pubitemid 43732290)