Capture of endothelial progenitor cells by a bispecific protein/monoclonal antibody molecule induces reendothelialization of vascular lesions

Journal of Molecular Medicine

Volumn 88, Issue 7, 2010, Pages 687-699

  Langer, Harald F ^a   Von Der Ruhr, Jürgen W ^a   Daub, Karin ^a   Schoenberger, Tanja ^a   Stellos, Konstantinos ^a   May, Andreas E ^a   Schnell, Hannah ^a   Gau, Alexandra ^a   Hafner, Ramona ^a   Lang, Peter ^a   Schumm, Michael ^a   Bühring, Hans Jörg ^a   Klingel, Karin ^a   Conrad, Sabine ^a   Schaller, Martin ^a   Van Zandvoort, Marc ^b   Jung, Gundram ^a   Dimmeler, Stefanie ^c   Skutella, Thomas ^a,d,e   Gawaz, Meinrad ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b MAASTRICHT UNIVERSITY   (Netherlands)

^c GOETHE UNIVERSITY   (Germany)

^d Anatomisches Institut   (Germany)

^e Anatomisches Institut   (Germany)

Author keywords

Endothelialization; Guidance molecule; Progenitor cells; Regenerative medicine; Stem cells; Therapy; Vascular disease; Vascular injury

Indexed keywords

CD133 ANTIGEN; CD146 ANTIGEN; CD31 ANTIGEN; CELL ANTIBODY; ENDOGLIN; GLYCOPROTEIN VI; GLYCOPROTEIN VI CD133; MONOCLONAL ANTIBODY; UNCLASSIFIED DRUG; VON WILLEBRAND FACTOR; BIOLOGICAL MARKER; CD34 ANTIGEN; FIBRINOGEN RECEPTOR; GLYCOPROTEIN; HYBRID PROTEIN; LEUKOCYTE ANTIGEN; PEPTIDE; PLATELET MEMBRANE GLYCOPROTEIN VI;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL DIFFERENTIATION; CELL HOMING; CELL MATURATION; COLONY FORMING UNIT; CONTROLLED STUDY; ENDOTHELIALIZATION; ENDOTHELIUM CELL; FEMALE; FLOW CYTOMETRY; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; STEM CELL; TISSUE GROWTH; TRANSMISSION ELECTRON MICROSCOPY; UPREGULATION; VASCULAR LESION; WEIBEL PALADE BODY; ANGIOGENESIS; ANIMAL; BLOOD VESSEL; C57BL MOUSE; CYTOLOGY; GENETICS; METABOLISM; NONOBESE DIABETIC MOUSE; PATHOLOGY; PHYSIOLOGY; REGENERATION; SCID MOUSE; VASCULAR ENDOTHELIUM;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, CD; ANTIGENS, CD34; BIOLOGICAL MARKERS; BLOOD VESSELS; CELL ADHESION; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; GLYCOPROTEINS; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, SCID; NEOVASCULARIZATION, PHYSIOLOGIC; PEPTIDES; PLATELET MEMBRANE GLYCOPROTEINS; RECOMBINANT FUSION PROTEINS; REGENERATION; STEM CELLS;

EID: 77954542832     PISSN: 09462716     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00109-010-0614-5     Document Type: Article

References (40)

1. T Asahara T Murohara A Sullivan M Silver ZR van der T Li B Witzenbichler G Schatteman JM Isner 1997 Isolation of putative progenitor endothelial cells for angiogenesis Science 275 964 967 10.1126/science.275.5302.964 1:CAS:528:DyaK2sXht1Clu7k%3D 9020076 (Pubitemid 27087709)
2. S Rafii D Lyden 2003 Therapeutic stem and progenitor cell transplantation for organ vascularization and regeneration Nat Med 9 702 712 10.1038/nm0603-702 1:CAS:528:DC%2BD3sXktFOnuro%3D 12778169 (Pubitemid 36749219)
3. N Werner S Kosiol T Schiegl P Ahlers K Walenta A Link M Bohm G Nickenig 2005 Circulating endothelial progenitor cells and cardiovascular outcomes N Engl J Med 353 999 1007 10.1056/NEJMoa043814 1:CAS:528:DC%2BD2MXpvVOisbw%3D 16148285 (Pubitemid 41262334)
4. S Conrad M Renninger J Hennenlotter T Wiesner L Just M Bonin W Aicher HJ Buhring U Mattheus A Mack HJ Wagner S Minger M Matzkies M Reppel J Hescheler KD Sievert A Stenzl T Skutella 2008 Generation of pluripotent stem cells from adult human testis Nature 456 344 349 10.1038/nature07404 1:CAS:528: DC%2BD1cXhsVSjsLjI 18849962
5. CA Cowan I Klimanskaya J McMahon J Atienza J Witmyer JP Zucker S Wang CC Morton AP McMahon D Powers DA Melton 2004 Derivation of embryonic stem-cell lines from human blastocysts N Engl J Med 350 1353 1356 10.1056/NEJMsr040330 1:CAS:528:DC%2BD2cXisFyhsbw%3D 14999088 (Pubitemid 38375373)
6. A Moretti L Caron A Nakano JT Lam A Bernshausen Y Chen Y Qyang L Bu M Sasaki S Martin-Puig Y Sun SM Evans KL Laugwitz KR Chien 2006 Multipotent embryonic isl1+ progenitor cells lead to cardiac, smooth muscle, and endothelial cell diversification Cell 127 1151 1165 10.1016/j.cell.2006.10.029 1:CAS:528:DC%2BD2sXhs1egtA%3D%3D 17123592 (Pubitemid 44895618)
7. K Takahashi K Tanabe M Ohnuki M Narita T Ichisaka K Tomoda S Yamanaka 2007 Induction of pluripotent stem cells from adult human fibroblasts by defined factors Cell 131 861 872 10.1016/j.cell.2007.11.019 1:CAS:528: DC%2BD2sXhsVCntbbK 18035408 (Pubitemid 350138099)
8. J Yu MA Vodyanik K Smuga-Otto J ntosiewicz-Bourget JL Frane S Tian J Nie GA Jonsdottir V Ruotti R Stewart II Slukvin JA Thomson 2007 Induced pluripotent stem cell lines derived from human somatic cells Science 318 1917 1920 10.1126/science.1151526 1:CAS:528:DC%2BD2sXhsVGjsLbN 18029452
9. KR Chien 2008 Regenerative medicine and human models of human disease Nature 453 302 305 10.1038/nature07037 1:CAS:528:DC%2BD1cXlvV2qtbo%3D 18480810 (Pubitemid 351693135)
10. ZM Ruggeri 2002 Platelets in atherothrombosis Nat Med 8 1227 1234 10.1038/nm1102-1227 1:CAS:528:DC%2BD38XotlWmu78%3D 12411949 (Pubitemid 35373553)
11. S Massberg I Konrad A Bultmann C Schulz G Munch M Peluso M Lorenz S Schneider F Besta I Muller B Hu H Langer E Kremmer M Rudelius U Heinzmann M Ungerer M Gawaz 2004 Soluble glycoprotein VI dimer inhibits platelet adhesion and aggregation to the injured vessel wall in vivo FASEB J 18 397 399 1:CAS:528:DC%2BD2cXht1GjtLg%3D 14656994
12. C Stamm B Westphal HD Kleine M Petzsch C Kittner H Klinge C Schumichen CA Nienaber M Freund G Steinhoff 2003 Autologous bone-marrow stem-cell transplantation for myocardial regeneration Lancet 361 45 46 10.1016/S0140-6736(03)12110-1 12517467 (Pubitemid 36050962)
13. C Urbich S Dimmeler 2004 Endothelial progenitor cells: characterization and role in vascular biology Circ Res 95 343 353 10.1161/01.RES.0000137877. 89448.78 1:CAS:528:DC%2BD2cXmsVKlurs%3D 15321944 (Pubitemid 39100452)
14. + selected progenitor cells from alternative donors Br J Haematol 124 72 79 10.1046/j.1365-2141.2003.04747.x 14675410 (Pubitemid 38021625)
15. Bühring H, Marxer A, Lammers R, Wissinger B (2002) CD133 cluster report. In: Mason D, André P, Bensussan A, Buckley C, Civin C, Clark E, de Haas M, Goyert S, Hadam M, Hart D, Hoøejší V, Jones Y, Meuer S, Morrissey J, Schwartz-Albiez R, Shaw S, Simmons D, Turni L, Uguccioni M, van der Schoot E, Vivier E, Zola H (eds) Leucocyte Typing VII. White Cell Differentiation Antigens. Oxford University Press, Oxford, pp 622-623
16. G Jung CJ Honsik RA Reisfeld HJ Muller-Eberhard 1986 Activation of human peripheral blood mononuclear cells by anti-T3: killing of tumor target cells coated with anti-target-anti-T3 conjugates Proc Natl Acad Sci U S A 83 4479 4483 10.1073/pnas.83.12.4479 1:CAS:528:DyaL28XksVWjsbk%3D 3086885
17. H Langer AE May A Bultmann M Gawaz 2005 ADAM 15 is an adhesion receptor for platelet GPIIb-IIIa and induces platelet activation Thromb Haemost 94 555 561 1:CAS:528:DC%2BD2MXhtVaqurrM 16268472
18. EY Choi E Chavakis MA Czabanka HF Langer L Fraemohs M Economopoulou RK Kundu A Orlandi YY Zheng DA Prieto CM Ballantyne SL Constant WC Aird T Papayannopoulou CG Gahmberg MC Udey P Vajkoczy T Quertermous S Dimmeler C Weber T Chavakis 2008 Del-1, an endogenous leukocyte-endothelial adhesion inhibitor, limits inflammatory cell recruitment Science 322 1101 1104 10.1126/science. 1165218 1:CAS:528:DC%2BD1cXhtlGgsr7M 19008446
19. A Schafer C Schulz M Eigenthaler D Fraccarollo A Kobsar M Gawaz G Ertl U Walter J Bauersachs 2004 Novel role of the membrane-bound chemokine fractalkine in platelet activation and adhesion Blood 103 407 412 10.1182/blood-2002-10-3260 12969973 (Pubitemid 38140067)
20. H Langer AE May K Daub U Heinzmann P Lang M Schumm D Vestweber S Massberg T Schonberger I Pfisterer AK Hatzopoulos M Gawaz 2006 Adherent platelets recruit and induce differentiation of murine embryonic endothelial progenitor cells to mature endothelial cells in vitro Circ Res 98 e2 e10 10.1161/01.RES.0000201285.87524.9e 1:CAS:528:DC%2BD28Xnt1GjsA%3D%3D 16373597
21. S Massberg K Brand S Gruner S Page E Muller I Muller W Bergmeier T Richter M Lorenz I Konrad B Nieswandt M Gawaz 2002 A critical role of platelet adhesion in the initiation of atherosclerotic lesion formation J Exp Med 196 887 896 10.1084/jem.20012044 1:CAS:528:DC%2BD38Xnsl2rtL0%3D 12370251
22. M van Zandvoort W Engels K Douma L Beckers EM Oude M Daemen DW Slaaf 2004 Two-photon microscopy for imaging of the (atherosclerotic) vascular wall: a proof of concept study J Vasc Res 41 54 63 10.1159/000076246 14730202 (Pubitemid 38296300)
23. L Just M Timmer J Tinius F Stahl A Deiwick G Nikkhah A Bader 2003 Identification of human cells in brain xenografts and in neural co-cultures of rat by in situ hybridisation with Alu probe J Neurosci Methods 126 69 77 10.1016/S0165-0270(03)00065-7 1:CAS:528:DC%2BD3sXkt1entro%3D 12788503 (Pubitemid 36683058)
24. E De Falco D Porcelli AR Torella S Straino MG Iachininoto A Orlandi S Truffa P Biglioli M Napolitano MC Capogrossi M Pesce 2004 SDF-1 involvement in endothelial phenotype and ischemia-induced recruitment of bone marrow progenitor cells Blood 104 3472 3482 10.1182/blood-2003-12-4423 15284120 (Pubitemid 39564415)
25. M Hristov A Zernecke K Bidzhekov EA Liehn E Shagdarsuren A Ludwig C Weber 2007 Importance of CXC chemokine receptor 2 in the homing of human peripheral blood endothelial progenitor cells to sites of arterial injury Circ Res 100 590 597 10.1161/01.RES.0000259043.42571.68 1:CAS:528:DC%2BD2sXitFylsbc%3D 17272812 (Pubitemid 46673269)
26. M Gawaz H Langer AE May 2005 Platelets in inflammation and atherogenesis J Clin Invest 115 3378 3384 10.1172/JCI27196 1:CAS:528:DC%2BD2MXhtlSqtL3P 16322783 (Pubitemid 43121822)
27. S Massberg I Konrad K Schurzinger M Lorenz S Schneider D Zohlnhoefer K Hoppe M Schiemann E Kennerknecht S Sauer C Schulz S Kerstan M Rudelius S Seidl F Sorge H Langer M Peluso P Goyal D Vestweber NR Emambokus DH Busch J Frampton M Gawaz 2006 Platelets secrete stromal cell-derived factor 1α and recruit bone marrow-derived progenitor cells to arterial thrombi in vivo J Exp Med 203 1221 1233 10.1084/jem.20051772 1:CAS:528:DC%2BD28XkvFWiurg%3D 16618794 (Pubitemid 43736592)
28. S Massberg M Gawaz S Gruner V Schulte I Konrad D Zohlnhofer U Heinzmann B Nieswandt 2003 A crucial role of glycoprotein VI for platelet recruitment to the injured arterial wall in vivo J Exp Med 197 41 49 10.1084/jem.20020945 1:CAS:528:DC%2BD3sXjslWmug%3D%3D 12515812 (Pubitemid 36110256)
29. I Muller S Kordowich C Holzwarth C Spano G Isensee A Staiber S Viebahn F Gieseke H Langer M Gawaz E Horwitz P Conte R Handgretinger M Dominici 2006 Animal serum-free culture conditions for isolation and expansion of multipotent mesenchymal stromal cells from human BM Cytotherapy 8 437 444 10.1080/14653240600920782 1:STN:280:DC%2BD28nhs1Kksg%3D%3D 17050248 (Pubitemid 44596996)
30. HF Langer K Stellos C Steingen A Froihofer T Schonberger B Kramer B Bigalke AE May P Seizer I Muller F Gieseke D Siegel-Axel SG Meuth A Schmidt HP Wendel I Muller W Bloch M Gawaz 2009 Platelet derived bFGF mediates vascular integrative mechanisms of mesenchymal stem cells in vitro J Mol Cell Cardiol 47 315 325 10.1016/j.yjmcc.2009.03.011 1:CAS:528:DC%2BD1MXnsl2it7k%3D 19328809
31. DA Ingram LE Mead H Tanaka V Meade A Fenoglio K Mortell K Pollok MJ Ferkowicz D Gilley MC Yoder 2004 Identification of a novel hierarchy of endothelial progenitor cells using human peripheral and umbilical cord blood Blood 104 2752 2760 10.1182/blood-2004-04-1396 1:CAS:528:DC%2BD2cXpslKjtrg%3D 15226175 (Pubitemid 39434958)
32. MC Yoder LE Mead D Prater TR Krier KN Mroueh F Li R Krasich CJ Temm JT Prchal DA Ingram 2007 Redefining endothelial progenitor cells via clonal analysis and hematopoietic stem/progenitor cell principals Blood 109 1801 1809 10.1182/blood-2006-08-043471 1:CAS:528:DC%2BD2sXjtFeqtrc%3D 17053059 (Pubitemid 46348173)
33. DN Prater J Case DA Ingram MC Yoder 2007 Working hypothesis to redefine endothelial progenitor cells Leukemia 21 1141 1149 10.1038/sj.leu.2404676 1:CAS:528:DC%2BD2sXlsFOhs78%3D 17392816 (Pubitemid 46831802)
34. M Peichev AJ Naiyer D Pereira Z Zhu WJ Lane M Williams MC Oz DJ Hicklin L Witte MA Moore S Rafii 2000 Expression of VEGFR-2 and AC133 by circulating human CD34(+) cells identifies a population of functional endothelial precursors Blood 95 952 958 1:CAS:528:DC%2BD3cXotV2gsA%3D%3D 10648408
35. E Chavakis C Urbich S Dimmeler 2008 Homing and engraftment of progenitor cells: a prerequisite for cell therapy J Mol Cell Cardiol 45 514 522 10.1016/j.yjmcc.2008.01.004 1:CAS:528:DC%2BD1cXhtlSgsr3J 18304573
36. FH Seeger AM Zeiher S Dimmeler 2007 Cell-enhancement strategies for the treatment of ischemic heart disease Nat Clin Pract Cardiovasc Med 4 Suppl 1 S110 S113 10.1038/ncpcardio0734 1:CAS:528:DC%2BD2sXitVemurw%3D 17230207 (Pubitemid 46151914)
37. H Shao Y Tan D Eton Z Yang MG Uberti S Li A Schulick H Yu 2008 Statin and stromal cell-derived factor-1 additively promote angiogenesis by enhancement of progenitor cells incorporation into new vessels Stem Cells 26 1376 1384 10.1634/stemcells.2007-0785 1:CAS:528:DC%2BD1cXnsFCgurg%3D 18308946
38. K Sasaki C Heeschen A Aicher T Ziebart J Honold C Urbich L Rossig U Koehl M Koyanagi A Mohamed RP Brandes H Martin AM Zeiher S Dimmeler 2006 Ex vivo pretreatment of bone marrow mononuclear cells with endothelial NO synthase enhancer AVE9488 enhances their functional activity for cell therapy Proc Natl Acad Sci U S A 103 14537 14541 10.1073/pnas.0604144103 1:CAS:528: DC%2BD28XhtVOgtr3F 16983080 (Pubitemid 44484785)
39. IY Oh CH Yoon J Hur JH Kim TY Kim CS Lee KW Park IH Chae BH Oh YB Park HS Kim 2007 Involvement of E-selectin in recruitment of endothelial progenitor cells and angiogenesis in ischemic muscle Blood 110 3891 3899 10.1182/blood-2006-10-048991 1:CAS:528:DC%2BD2sXhtl2qsb7N 17699745 (Pubitemid 350248444)
40. JM Hill G Zalos JP Halcox WH Schenke MA Waclawiw AA Quyyumi T Finkel 2003 Circulating endothelial progenitor cells, vascular function, and cardiovascular risk N Engl J Med 348 593 600 10.1056/NEJMoa022287 12584367 (Pubitemid 36204953)