Circulation Research. 2005;96:784-791
Published online before print March 10, 2005, doi: 10.1161/01.RES.0000162100.52009.38
Published online before print March 10, 2005, doi: 10.1161/01.RES.0000162100.52009.38
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
© 2005 American Heart Association, Inc.
Integrative Physiology |
SDF-1
/CXCR4 Axis Is Instrumental in Neointimal Hyperplasia and Recruitment of Smooth Muscle Progenitor Cells
From the Departments of Molecular Cardiovascular Research and Cardiology (A.Z., A.S., P.v.H., E.A.L., C.W.), University Hospital, Rheinisch-Westfälische Technische Hochschule, Aachen, Germany; Division of Biopharmaceutics (I.B., E.A.B.), Gorlaeus Laboratories, Leiden University, The Netherlands; Department of Pharmacology and Toxicology (B.M., P.G.), University of Ulm, Germany; and Physiology and Physiopathology Unit (M.M.), Pierre and Marie Curie University (PARIS 6), France.
Correspondence to Christian Weber, MD, Kardiovaskuläre Molekularbiologie, Universitätsklinikum Aachen, Pauwelsstraße 30, 52074 Aachen, Germany. E-mail cweber{at}ukaachen.de
Recent evidence infers a contribution of smooth muscle cell (SMC) progenitors and stromal cell-derived factor (SDF)-1
to neointima formation after arterial injury. Inhibition of plaque area and SMC content in apolipoprotein E-deficient mice repopulated with LacZ+ or CXCR4–/– BM or lentiviral transfer of an antagonist reveals a crucial involvement of local SDF-1 and its receptor CXCR4 in neointimal hyperplasia via recruitment of BM-derived SMC progenitors. After arterial injury, SDF-1 expression in medial SMCs is preceded by apoptosis and inhibited by blocking caspase-dependent apoptosis. SDF-1 binds to platelets at the site of injury, triggers CXCR4- and P-selectin-dependent arrest of progenitor cells on injured arteries or matrix-adherent platelets, preferentially mobilizes and recruits c-kit–/platelet–derived growth factor receptor (PDGFR)-ß+/lineage–/sca-1+ progenitors for neointimal SMCs without being required for their differentiation. Hence, the SDF-1/CXCR4 axis is pivotal for vascular remodeling by recruiting a subset of SMC progenitors in response to apoptosis and in concert with platelets, epitomizing its importance for tissue repair and identifying a prime target to limit lesion development.
Key Words: chemokines • atherosclerosis • smooth muscle cells • progenitor cells • restenosis
This article has been cited by other articles:
 |
|
 |
|
  E. A. Lasater, W. K. Bessler, L. E. Mead, W. E. Horn, D. W. Clapp, S. J. Conway, D. A. Ingram, and F. Li Nf1+/- mice have increased neointima formation via hyperactivation of a Gleevec sensitive molecular pathway Hum. Mol. Genet., August 1, 2008; 17(15): 2336 - 2344. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 F. Vogt, A. Zernecke, M. Beckner, N. Krott, A.-K. Bosserhoff, R. Hoffmann, M. A.M.J. Zandvoort, T. Jahnke, M. Kelm, C. Weber, et al. Blockade of Angio-Associated Migratory Cell Protein Inhibits Smooth Muscle Cell Migration and Neointima Formation in Accelerated Atherosclerosis J. Am. Coll. Cardiol., July 22, 2008; 52(4): 302 - 311. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. Frommhold, A. Ludwig, M. G. Bixel, A. Zarbock, I. Babushkina, M. Weissinger, S. Cauwenberghs, L. G. Ellies, J. D. Marth, A. G. Beck-Sickinger, et al. Sialyltransferase ST3Gal-IV controls CXCR2-mediated firm leukocyte arrest during inflammation J. Exp. Med., June 9, 2008; 205(6): 1435 - 1446. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. A. Nemenoff, P. A. Simpson, S. B. Furgeson, N. Kaplan-Albuquerque, J. Crossno, P. J. Garl, J. Cooper, and M. C.M. Weiser-Evans Targeted Deletion of PTEN in Smooth Muscle Cells Results in Vascular Remodeling and Recruitment of Progenitor Cells Through Induction of Stromal Cell-Derived Factor-1{alpha} Circ. Res., May 9, 2008; 102(9): 1036 - 1045. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. Chen, J. M. Abrahams, L. M. Smith, J. H. McVey, R. I. Lechler, and A. Dorling Regenerative repair after endoluminal injury in mice with specific antagonism of protease activated receptors on CD34+ vascular progenitors Blood, April 15, 2008; 111(8): 4155 - 4164. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Zernecke, J. Bernhagen, and C. Weber Macrophage Migration Inhibitory Factor in Cardiovascular Disease Circulation, March 25, 2008; 117(12): 1594 - 1602. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Y. Diao, S. Guthrie, S.-L. Xia, X. Ouyang, L. Zhang, J. Xue, P. Lee, M. Grant, E. Scott, and M. S. Segal Long-Term Engraftment of Bone Marrow-Derived Cells in the Intimal Hyperplasia Lesion of Autologous Vein Grafts Am. J. Pathol., March 1, 2008; 172(3): 839 - 848. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. C. Rafii, B. Psaila, J. Butler, D. K. Jin, and D. Lyden Regulation of Vasculogenesis by Platelet-Mediated Recruitment of Bone Marrow-Derived Cells Arterioscler. Thromb. Vasc. Biol., February 1, 2008; 28(2): 217 - 222. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Zernecke, I. Bot, Y. Djalali-Talab, E. Shagdarsuren, K. Bidzhekov, S. Meiler, R. Krohn, A. Schober, M. Sperandio, O. Soehnlein, et al. Protective Role of CXC Receptor 4/CXC Ligand 12 Unveils the Importance of Neutrophils in Atherosclerosis Circ. Res., February 1, 2008; 102(2): 209 - 217. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. Yang, M. Koupenova, D. J. McCrann, K. J. Kopeikina, H. M. Kagan, B. M. Schreiber, and K. Ravid The A2b adenosine receptor protects against vascular injury PNAS, January 15, 2008; 105(2): 792 - 796. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. Shagdarsuren, K. Bidzhekov, Y. Djalali-Talab, E. A. Liehn, M. Hristov, R. A. Matthijsen, W. A. Buurman, A. Zernecke, and C. Weber C1-Esterase Inhibitor Protects Against Neointima Formation After Arterial Injury in Atherosclerosis-Prone Mice Circulation, January 1, 2008; 117(1): 70 - 78. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. Karshovska, A. Zernecke, G. Sevilmis, A. Millet, M. Hristov, C. D. Cohen, H. Schmid, F. Krotz, H.-Y. Sohn, V. Klauss, et al. Expression of HIF-1{alpha} in Injured Arteries Controls SDF-1{alpha} Mediated Neointima Formation in Apolipoprotein E Deficient Mice Arterioscler. Thromb. Vasc. Biol., December 1, 2007; 27(12): 2540 - 2547. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. F. Bentzon, C. S. Sondergaard, M. Kassem, and E. Falk Smooth Muscle Cells Healing Atherosclerotic Plaque Disruptions Are of Local, Not Blood, Origin in Apolipoprotein E Knockout Mice Circulation, October 30, 2007; 116(18): 2053 - 2061. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Morimoto, M. Takahashi, Y. Shiba, A. Izawa, H. Ise, M. Hongo, K. Hatake, K. Motoyoshi, and U. Ikeda Bone Marrow-Derived CXCR4+ Cells Mobilized by Macrophage Colony-Stimulating Factor Participate in the Reduction of Infarct Area and Improvement of Cardiac Remodeling after Myocardial Infarction in Mice Am. J. Pathol., September 1, 2007; 171(3): 755 - 766. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. Sathyanarayana, M. P. Menon, O. Bogacheva, O. Bogachev, K. Niss, W. S. Kapelle, E. Houde, J. Fang, and D. M. Wojchowski Erythropoietin modulation of podocalyxin and a proposed erythroblast niche Blood, July 15, 2007; 110(2): 509 - 518. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Y. Bosse, K. Maghni, and T. J. Hudson 1{alpha},25-Dihydroxy-vitamin D3 stimulation of bronchial smooth muscle cells induces autocrine, contractility, and remodeling processes Physiol Genomics, April 24, 2007; 29(2): 161 - 168. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Hristov, A. Zernecke, K. Bidzhekov, E. A. Liehn, E. Shagdarsuren, A. Ludwig, and C. Weber Importance of CXC Chemokine Receptor 2 in the Homing of Human Peripheral Blood Endothelial Progenitor Cells to Sites of Arterial Injury Circ. Res., March 2, 2007; 100(4): 590 - 597. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Shiba, M. Takahashi, T. Yoshioka, N. Yajima, H. Morimoto, A. Izawa, H. Ise, K. Hatake, K. Motoyoshi, and U. Ikeda M-CSF Accelerates Neointimal Formation in the Early Phase After Vascular Injury in Mice: The Critical Role of the SDF-1-CXCR4 System Arterioscler. Thromb. Vasc. Biol., February 1, 2007; 27(2): 283 - 289. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. von Hundelshausen and C. Weber Platelets as Immune Cells: Bridging Inflammation and Cardiovascular Disease Circ. Res., January 5, 2007; 100(1): 27 - 40. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. F. Bentzon, C. Weile, C. S. Sondergaard, J. Hindkjaer, M. Kassem, and E. Falk Smooth Muscle Cells in Atherosclerosis Originate From the Local Vessel Wall and Not Circulating Progenitor Cells in ApoE Knockout Mice Arterioscler. Thromb. Vasc. Biol., December 1, 2006; 26(12): 2696 - 2702. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J.-S. Shao, J. Cai, and D. A. Towler Molecular Mechanisms of Vascular Calcification: Lessons Learned From The Aorta Arterioscler. Thromb. Vasc. Biol., July 1, 2006; 26(7): 1423 - 1430. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H.C. de Boer, C. Verseyden, L.H. Ulfman, J.J. Zwaginga, I. Bot, E.A. Biessen, T.J. Rabelink, and A.J. van Zonneveld Fibrin and Activated Platelets Cooperatively Guide Stem Cells to a Vascular Injury and Promote Differentiation Towards an Endothelial Cell Phenotype Arterioscler. Thromb. Vasc. Biol., July 1, 2006; 26(7): 1653 - 1659. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Yu, K. Sliedregt-Bol, H. Overkleeft, G. A. van der Marel, T. J.C. van Berkel, and E. A.L. Biessen Therapeutic Potential of a Synthetic Peptide Inhibitor of Nuclear Factor of Activated T Cells as Antirestenotic Agent Arterioscler. Thromb. Vasc. Biol., July 1, 2006; 26(7): 1531 - 1537. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Massberg, I. Konrad, K. Schurzinger, M. Lorenz, S. Schneider, D. Zohlnhoefer, K. Hoppe, M. Schiemann, E. Kennerknecht, S. Sauer, et al. Platelets secrete stromal cell-derived factor 1{alpha} and recruit bone marrow-derived progenitor cells to arterial thrombi in vivo J. Exp. Med., May 15, 2006; 203(5): 1221 - 1233. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
K. Bidzhekov, A. Zernecke, and C. Weber MCP-1 Induces a Novel Transcription Factor With Proapoptotic Activity Circ. Res., May 12, 2006; 98(9): 1107 - 1109. [Full Text] [PDF]
|
|
|
|
|
|
A. Zernecke, K. Bidzhekov, B. Ozuyaman, L. Fraemohs, E. A. Liehn, J. M. Luscher-Firzlaff, B. Luscher, J. Schrader, and C. Weber CD73/Ecto-5'-Nucleotidase Protects Against Vascular Inflammation and Neointima Formation Circulation, May 2, 2006; 113(17): 2120 - 2127. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L.-N. Zhang, D. W. Wilson, V. da Cunha, M. E. Sullivan, R. Vergona, J. C. Rutledge, and Y.-X. Wang Endothelial NO Synthase Deficiency Promotes Smooth Muscle Progenitor Cells in Association With Upregulation of Stromal Cell-Derived Factor-1{alpha} in a Mouse Model of Carotid Artery Ligation Arterioscler. Thromb. Vasc. Biol., April 1, 2006; 26(4): 765 - 772. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
C. Weber Killing Two Birds With One Stone: Targeting Chemokine Receptors in Atherosclerosis and HIV Infection Arterioscler. Thromb. Vasc. Biol., December 1, 2005; 25(12): 2448 - 2450. [Full Text] [PDF]
|
|
|
|
 |
|
 Md. R. Abid, K. Yano, S. Guo, V. I. Patel, G. Shrikhande, K. C. Spokes, C. Ferran, and W. C. Aird Forkhead Transcription Factors Inhibit Vascular Smooth Muscle Cell Proliferation and Neointimal Hyperplasia J. Biol. Chem., August 19, 2005; 280(33): 29864 - 29873. [Abstract] [Full Text] [PDF]
|
|