Circulation Research. 2004;94:671-677
Published online before print February 12, 2004, doi: 10.1161/01.RES.0000122041.73808.B5
Published online before print February 12, 2004, doi: 10.1161/01.RES.0000122041.73808.B5
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© 2004 American Heart Association, Inc.
Integrative Physiology |
Collateral Artery Growth (Arteriogenesis) After Experimental Arterial Occlusion Is Impaired in Mice Lacking CC-Chemokine Receptor-2
From the Department of Experimental Cardiology (M.H., T.Z., S.W., B.F., A.H., S.M., S.T., W.S.), Max-Planck-Institute for Physiological and Clinical Research, Bad Nauheim, Germany; Protein Design Labs, Inc. (W.A.K.), Fremont, Calif; Kerckhoff-Clinic (G.B.), Bad Nauheim, Germany.
Correspondence to Matthias Heil, Benekestr. 2, 61231 Bad Nauheim, Germany. E-mail m.heil{at}kerckhoff.mpg.de
Arteriogenesis has been associated with the presence of monocytes/macrophages within the collateral vessel wall. Induced macrophage migration in vivo is driven by the binding of monocyte chemoattractant protein-1 (MCP-1, or CCL2 in the new nomenclature) to the CCR2-chemokine receptor on macrophages. To determine whether the CCL2-CCR2 signaling pathway is involved in the accumulation of macrophages in growing collateral vessels, we used mice that are deficient in CCR2 in a model of experimental arterial occlusion and collateral vessel growth. In an in vitro CCL2-driven chemotaxis assay, mononuclear cells isolated from wild-type BALB/c mice exhibited CCL2 concentration–dependent migration, whereas this migration was abolished in cells from CCR2-/- mice on a BALB/c genetic background. In vivo, blood flow recovery as measured by laser Doppler (LDI) and MRI (MRI) was impaired in CCR2-/- mice on either the BALB/c or C57BL/6 genetic backgrounds. Three weeks after femoral artery ligation, LDI perfusion ratio of operated versus nonoperated distal hindlimb in BALB/c wild-type mice increased to 0.45±0.06 and in CCR2-/- animals only to 0.21±0.03 (P<0.01). In C57BL/6 mice, ratio increased to 0.96±0.09 and 0.85±0.08 (P<0.05), respectively. MRI at 3 weeks (0.76±0.06 versus 0.62±0.01; P<0.05) and hemoglobin oxygen saturation measurements confirmed these findings. Active foot movement score significantly decreased and gastrocnemius muscle atrophy was significantly greater in CCR2-/- mice. Morphometric analysis showed a lesser increase in collateral vessel diameters in CCR2-/- mice. Importantly, the number of invaded monocytes/macrophages in the perivascular space of collateral arteries of CCR2-/- animals was dramatically reduced in comparison to wild-type mice. In conclusion, our results demonstrate that the CCR2 signaling pathway is essential for efficient collateral artery growth.
Key Words: collateral artery growth • monocytes • CCL2 • CCR2 • hindlimb ischemia
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|
|
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|
|
|
|
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|
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|
|
|
|
 |
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
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|
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|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
 |
|
 Y. Yamada and N. Takakura Physiological pathway of differentiation of hematopoietic stem cell population into mural cells J. Exp. Med., April 17, 2006; 203(4): 1055 - 1065. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
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|
|
|
|
 |
|
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|
|
|
|
|
|
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|
|
|
|
|
|
G. Gruionu, J. B. Hoying, A. R. Pries, and T. W. Secomb Structural remodeling of mouse gracilis artery after chronic alteration in blood supply Am J Physiol Heart Circ Physiol, May 1, 2005; 288(5): H2047 - H2054. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
|
|
|
|
|
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|
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