Semin Thromb Hemost 2007; 33(2): 159-164
DOI: 10.1055/s-2007-969029
Copyright © 2007 by Thieme Medical Publishers, Inc., 333 Seventh Avenue, New York, NY 10001, USA.

Platelets and Stromal Cell-Derived Factor-1 in Progenitor Cell Recruitment

Konstantinos Stellos1 , Meinrad Gawaz1
  • 1Medizinische Klinik III, Eberhard Karls-Universität Tübingen, Tübingen, Germany
Further Information

Publication History

Publication Date:
06 March 2007 (online)

ABSTRACT

Stromal cell-derived factor-1 (SDF-1) is a CXC chemokine that binds to its sole counterreceptor, CXCR4. It is well reported that the SDF-1/CXCR4 signaling pathway is of vital importance to human development and to various pathophysiological phenomena, including hematopoiesis, angiogenesis, atherosclerosis, cancer growth, metastasis, and human immunodeficiency virus infection. SDF-1 promotes mobilization of bone marrow-derived endothelial progenitor cells (EPCs) to the circulation in response to vascular injury. Recently, we found that platelets express and release SDF-1 into the microcirculation upon activation and we observed that platelet-derived SDF-1 is functionally involved in recruitment of EPCs to arterial thrombi in vivo. This review discusses the unique functions of this chemokine and the newly discovered impact of platelet-derived SDF-1 into the recruitment of progenitor cells to vascular injury areas, and its subsequent effects in atherosclerosis, vascular repair, and angiogenesis.

REFERENCES

  • 1 Aiuti A, Webb I J, Bleul C et al.. 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(1) 111-120
  • 2 Shirozu M, Nakano T, Inazawa J et al.. Structure and chromosomal localization of the human stromal cell-derived factor 1 (SDF1) gene.  Genomics. 1995;  28(3) 495-500
  • 3 Bleul C C, Fuhlbrigge R C, Casasnovas J M et al.. A highly efficacious lymphocyte chemoattractant, stromal cell-derived factor 1 (SDF-1).  J Exp Med. 1996;  184(3) 1101-1109
  • 4 Dorshkind K. Regulation of hemopoiesis by bone marrow stromal cells and their products.  Annu Rev Immunol. 1990;  8 111-137
  • 5 Fuchs E, Tumbar T, Guasch G. Socializing with the neighbors: stem cells and their niche.  Cell. 2004;  116(6) 769-778
  • 6 Wright D E, Bowman E P, Wagers A J et al.. Hematopoietic stem cells are uniquely selective in their migratory response to chemokines.  J Exp Med. 2002;  195(9) 1145-1154
  • 7 Lataillade J J, Clay D, Dupuy C et al.. Chemokine SDF-1 enhances circulating CD34( + ) cell proliferation in synergy with cytokines: possible role in progenitor survival.  Blood. 2000;  95(3) 756-768
  • 8 Lataillade J J, Clay D, Bourin P et al.. 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(4) 1117-1129
  • 9 Peled A, Petit I, Kollet O et al.. Dependence of human stem cell engraftment and repopulation of NOD/SCID mice on CXCR4.  Science. 1999;  283(5403) 845-848
  • 10 Nagasawa T, Hirota S, Tachibana K et al.. Defects of B-cell lymphopoiesis and bone-marrow myelopoiesis in mice lacking the CXC chemokine PBSF/SDF-1.  Nature. 1996;  382(6592) 635-638
  • 11 Zou Y R, Kottmann A H, Kuroda M et al.. Function of the chemokine receptor CXCR4 in haematopoiesis and in cerebellar development.  Nature. 1998;  393(6685) 595-599
  • 12 Bajetto A, Barbieri F, Dorcaratto A et al.. Expression of CXC chemokine receptors 1-5 and their ligands in human glioma tissues: role of CXCR4 and SDF1 in glioma cell proliferation and migration.  Neurochem Int. 2006;  49 423-432
  • 13 Simmons G, Reeves J D, Hibbitts S et al.. Co-receptor use by HIV and inhibition of HIV infection by chemokine receptor ligands.  Immunol Rev. 2000;  177 112-126
  • 14 Coll B, Alonso-Villaverde C, Parra S et al.. The stromal derived factor-1 mutated allele (SDF1-3′A) is associated with a lower incidence of atherosclerosis in HIV-infected patients.  AIDS. 2005;  19(16) 1877-1883
  • 15 Ross R, Glomset J, Harker L. Response to injury and atherogenesis.  Am J Pathol. 1977;  86(3) 675-684
  • 16 Carmeliet P, Moons L, Stassen J M et al.. Vascular wound healing and neointima formation induced by perivascular electric injury in mice.  Am J Pathol. 1997;  150(2) 761-776
  • 17 Natori T, Sata M, Washida M et al.. G-CSF stimulates angiogenesis and promotes tumor growth: potential contribution of bone marrow-derived endothelial progenitor cells.  Biochem Biophys Res Commun. 2002;  297(4) 1058-1061
  • 18 Hu Y, Zhang Z, Torsney E et al.. Abundant progenitor cells in the adventitia contribute to atherosclerosis of vein grafts in ApoE-deficient mice.  J Clin Invest. 2004;  113(9) 1258-1265
  • 19 Werner N, Priller J, Laufs U et al.. Bone marrow-derived progenitor cells modulate vascular reendothelialization and neointimal formation: effect of 3-hydroxy-3-methylglutaryl coenzyme a reductase inhibition.  Arterioscler Thromb Vasc Biol. 2002;  22(10) 1567-1572
  • 20 Saiura A, Sata M, Hirata Y et al.. Circulating smooth muscle progenitor cells contribute to atherosclerosis.  Nat Med. 2001;  7(4) 382-383
  • 21 Orlic D, Kajstura J, Chimenti S et al.. Bone marrow cells regenerate infarcted myocardium.  Nature. 2001;  410(6829) 701-705
  • 22 Takahashi T, Kalka C, Masuda H et al.. Ischemia- and cytokine-induced mobilization of bone marrow-derived endothelial progenitor cells for neovascularization.  Nat Med. 1999;  5(4) 434-438
  • 23 Kawamoto A, Gwon H C, Iwaguro H et al.. Therapeutic potential of ex vivo expanded endothelial progenitor cells for myocardial ischemia.  Circulation. 2001;  103(5) 634-637
  • 24 Kalka C, Masuda H, Takahashi T et al.. Transplantation of ex vivo expanded endothelial progenitor cells for therapeutic neovascularization.  Proc Natl Acad Sci USA. 2000;  97(7) 3422-3427
  • 25 Tateishi-Yuyama E, Matsubara H, Murohara T et al.. Therapeutic angiogenesis for patients with limb ischaemia by autologous transplantation of bone-marrow cells: a pilot study and a randomised controlled trial.  Lancet. 2002;  360(9331) 427-435
  • 26 Assmus B, Schachinger V, Teupe C et al.. Transplantation of Progenitor Cells and Regeneration Enhancement in Acute Myocardial Infarction (TOPCARE-AMI).  Circulation. 2002;  106(24) 3009-3017
  • 27 Mohle R, Bautz F, Rafii S et al.. The chemokine receptor CXCR-4 is expressed on CD34 + hematopoietic progenitors and leukemic cells and mediates transendothelial migration induced by stromal cell-derived factor-1.  Blood. 1998;  91(12) 4523-4530
  • 28 Yamaguchi J, Kusano K F, Masuo O et al.. Stromal cell-derived factor-1 effects on ex vivo expanded endothelial progenitor cell recruitment for ischemic neovascularization.  Circulation. 2003;  107(9) 1322-1328
  • 29 Petit I, Szyper-Kravitz M, Nagler A et al.. G-CSF induces stem cell mobilization by decreasing bone marrow SDF-1 and up-regulating CXCR4.  Nat Immunol. 2002;  3(7) 687-694
  • 30 Heissig B, Hattori K, Dias S et al.. Recruitment of stem and progenitor cells from the bone marrow niche requires MMP-9 mediated release of kit-ligand.  Cell. 2002;  109(5) 625-637
  • 31 Hattori K, Heissig B, Tashiro K et al.. Plasma elevation of stromal cell-derived factor-1 induces mobilization of mature and immature hematopoietic progenitor and stem cells.  Blood. 2001;  97(11) 3354-3360
  • 32 Peled A, Kollet O, Ponomaryov T et al.. The chemokine SDF-1 activates the integrins LFA-1, VLA-4, and VLA-5 on immature human CD34( + ) cells: role in transendothelial/stromal migration and engraftment of NOD/SCID mice.  Blood. 2000;  95(11) 3289-3296
  • 33 Schober A, Knarren S, Lietz M et al.. Crucial role of stromal cell-derived factor-1alpha in neointima formation after vascular injury in apolipoprotein E-deficient mice.  Circulation. 2003;  108(20) 2491-2497
  • 34 Ceradini D J, Kulkarni A R, Callaghan M J et al.. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1.  Nat Med. 2004;  10(8) 858-864
  • 35 Schioppa T, Uranchimeg B, Saccani A et al.. Regulation of the chemokine receptor CXCR4 by hypoxia.  J Exp Med. 2003;  198(9) 1391-1402
  • 36 Zernecke A, Schober A, Bot I et al.. SDF-1alpha/CXCR4 axis is instrumental in neointimal hyperplasia and recruitment of smooth muscle progenitor cells.  Circ Res. 2005;  96(7) 784-791
  • 37 Massberg S, Konrad I, Schurzinger K et al.. Platelets secrete stromal cell-derived factor 1alpha and recruit bone marrow-derived progenitor cells to arterial thrombi in vivo.  J Exp Med. 2006;  203(5) 1221-1233
  • 38 Abi-Younes S, Sauty A, Mach F et al.. The stromal cell-derived factor-1 chemokine is a potent platelet agonist highly expressed in atherosclerotic plaques.  Circ Res. 2000;  86(2) 131-138
  • 39 Massberg S, Gawaz M, Gruner S et al.. A crucial role of glycoprotein VI for platelet recruitment to the injured arterial wall in vivo.  J Exp Med. 2003;  197(1) 41-49
  • 40 Chen J, Lopez J A. Interactions of platelets with subendothelium and endothelium.  Microcirculation. 2005;  12(3) 235-246
  • 41 Gawaz M, Langer H, May A E. Platelets in inflammation and atherogenesis.  J Clin Invest. 2005;  115(12) 3378-3384
  • 42 Jin D K, Shido K, Kopp H G et al.. Cytokine-mediated deployment of SDF-1 induces revascularization through recruitment of CXCR4 + hemangiocytes.  Nat Med. 2006;  12(5) 557-567
  • 43 Ma N, Stamm C, Kaminski A et al.. Human cord blood cells induce angiogenesis following myocardial infarction in NOD/scid-mice.  Cardiovasc Res. 2005;  66(1) 45-54
  • 44 Misao Y, Takemura G, Arai M et al.. Importance of recruitment of bone marrow-derived CXCR4( + ) cells in post-infarct cardiac repair mediated by G-CSF.  Cardiovasc Res. 2006;  71(3) 455-465
  • 45 Walter D H, Haendeler J, Reinhold J et al.. Impaired CXCR4 signaling contributes to the reduced neovascularization capacity of endothelial progenitor cells from patients with coronary artery disease.  Circ Res. 2005;  97(11) 1142-1151
  • 46 Orimo A, Gupta P B, Sgroi D C et al.. Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion.  Cell. 2005;  121(3) 335-348
  • 47 Guleng B, Tateishi K, Ohta M et al.. Blockade of the stromal cell-derived factor-1/CXCR4 axis attenuates in vivo tumor growth by inhibiting angiogenesis in a vascular endothelial growth factor-independent manner.  Cancer Res. 2005;  65(13) 5864-5871

Meinrad GawazM.D. 

Medizinische Klinik III, Universitätsklinikum Tübingen

Otfried-Müller Str. 10, 72076 Tübingen, Germany

Email: meinrad.gawaz@med.uni-tuebingen.de