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.
KEYWORDS
Platelets - stromal cell-derived factor-1 (SDF-1) - progenitor cells - 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