CXCL12 promotes the stabilization of atherosclerotic lesions mediated by smooth muscle progenitor cells in apoe-deficient mice

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 33, Issue 4, 2013, Pages 679-686

  Akhtar, Shamima ^a   Gremse, Felix ^c   Kiessling, Fabian ^c   Weber, Christian ^a,d   Schober, Andreas ^a,b,d  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^b RWTH AACHEN UNIVERSITY   (Germany)

^c RWTH AACHEN UNIVERSITY   (Germany)

^d DZHK GERMAN CENTRE FOR CARDIOVASCULAR RESEARCH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GALACTOSIDASE; COLLAGEN; PLATELET DERIVED GROWTH FACTOR BETA RECEPTOR; STROMAL CELL DERIVED FACTOR 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTERY DIAMETER; ARTICLE; CAROTID ARTERY LIGATION; CAROTID ATHEROSCLEROSIS; CHIMERA; CONTROLLED STUDY; FLOW CYTOMETRY; GENE SILENCING; HEMATOPOIETIC STEM CELL; MACROPHAGE; MICRO-COMPUTED TOMOGRAPHY; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SMOOTH MUSCLE FIBER; STEM CELL;

ANIMALS; ANTIGENS, LY; APOLIPOPROTEINS E; BIOLOGICAL MARKERS; BONE MARROW TRANSPLANTATION; CAROTID ARTERIES; CAROTID ARTERY DISEASES; CELLS, CULTURED; CHEMOKINE CXCL2; CHEMOTAXIS; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; FIBROSIS; FLOW CYTOMETRY; GENOTYPE; INJECTIONS, INTRAVENOUS; MACROPHAGES; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MICROFILAMENT PROTEINS; MUSCLE PROTEINS; MYOCYTES, SMOOTH MUSCLE; PHENOTYPE; PLAQUE, ATHEROSCLEROTIC; PROTO-ONCOGENE PROTEINS C-SIS; RNA INTERFERENCE; STEM CELLS; X-RAY MICROTOMOGRAPHY;

EID: 84875365366     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.112.301162     Document Type: Article

References (33)

1. Ylä-Herttuala S, Bentzon JF, Daemen M, et al. Stabilisation of atherosclerotic plaques. Position paper of the European Society of Cardiology (ESC) Working Group on atherosclerosis and vascular biology. Thromb Haemost. 2011;106:1-19.
2. Falk E, Shah PK, Fuster V. Coronary plaque disruption. Circulation. 1995;92:657-671.
3. Burke AP, Kolodgie FD, Farb A, Weber DK, Malcom GT, Smialek J, Virmani R. Healed plaque ruptures and sudden coronary death: evidence that subclinical rupture has a role in plaque progression. Circulation. 2001;103:934-940.
4. Davies MJ, Richardson PD, Woolf N, Katz DR, Mann J. Risk of thrombosis in human atherosclerotic plaques: role of extracellular lipid, macrophage, and smooth muscle cell content. Br Heart J. 1993;69: 377-381.
5. Virmani R, Burke AP, Farb A, Kolodgie FD. Pathology of the vulnerable plaque. J Am Coll Cardiol. 2006;47(8 suppl):C13-C18.
6. Clarke MC, Figg N, Maguire JJ, Davenport AP, Goddard M, Littlewood TD, Bennett MR. Apoptosis of vascular smooth muscle cells induces features of plaque vulnerability in atherosclerosis. Nat Med. 2006;12:1075-1080.
7. von der Thüsen JH, van Vlijmen BJ, Hoeben RC, Kockx MM, Havekes LM, van Berkel TJ, Biessen EA. Induction of atherosclerotic plaque rupture in apolipoprotein E-/- mice after adenovirus-mediated transfer of p53. Circulation. 2002;105:2064-2070.
8. van der Wal AC, Becker AE, van der Loos CM, Das PK. Site of intimal rupture or erosion of thrombosed coronary atherosclerotic plaques is characterized by an inflammatory process irrespective of the dominant plaque morphology. Circulation. 1994;89:36-44.
9. Zoll J, Fontaine V, Gourdy P, Barateau V, Vilar J, Leroyer A, Lopes-Kam I, Mallat Z, Arnal JF, Henry P, Tobelem G, Tedgui A. Role of human smooth muscle cell progenitors in atherosclerotic plaque development and composition. Cardiovasc Res. 2008;77:471-480.
10. Yu H, Stoneman V, Clarke M, Figg N, Xin HB, Kotlikoff M, Littlewood T, Bennett M. Bone marrow-derived smooth muscle-like cells are infrequent in advanced primary atherosclerotic plaques but promote atherosclerosis. Arterioscler Thromb Vasc Biol. 2011;31:1291-1299.
11. Bentzon JF, Weile C, Sondergaard CS, Hindkjaer J, Kassem M, Falk E. Smooth muscle cells in atherosclerosis originate from the local vessel wall and not circulating progenitor cells in ApoE knockout mice. Arterioscler Thromb Vasc Biol. 2006;26:2696-2702.
12. Han CI, Campbell GR, Campbell JH. Circulating bone marrow cells can contribute to neointimal formation. J Vasc Res. 2001;38:113-119.
13. Sahara M, Sata M, Matsuzaki Y, Tanaka K, Morita T, Hirata Y, Okano H, Nagai R. Comparison of various bone marrow fractions in the ability to participate in vascular remodeling after mechanical injury. Stem Cells. 2005;23:874-878.
14. Tanaka K, Sata M, Hirata Y, Nagai R. Diverse contribution of bone marrow cells to neointimal hyperplasia after mechanical vascular injuries. Circ Res. 2003;93:783-790.
15. Sata M, Saiura A, Kunisato A, Tojo A, Okada S, Tokuhisa T, Hirai H, Makuuchi M, Hirata Y, Nagai R. Hematopoietic stem cells differentiate into vascular cells that participate in the pathogenesis of atherosclerosis. Nat Med. 2002;8:403-409.
16. Schober A, Knarren S, Lietz M, Lin EA, Weber C. Crucial role of stromal cell-derived factor-1alpha in neointima formation after vascular injury in apolipoprotein E-deficient mice. Circulation. 2003;108:2491-2497.
17. Zernecke A, Schober A, Bot I, von Hundelshausen P, Liehn EA, Möpps B, Mericskay M, Gierschik P, Biessen EA, Weber C. SDF-1alpha/CXCR4 axis is instrumental in neointimal hyperplasia and recruitment of smooth muscle progenitor cells. Circ Res. 2005;96: 784-791.
18. Subramanian P, Karshovska E, Reinhard P, Megens RT, Zhou Z, Akhtar S, Schumann U, Li X, van Zandvoort M, Ludin C, Weber C, Schober A. Lysophosphatidic acid receptors LPA1 and LPA3 promote CXCL12-mediated smooth muscle progenitor cell recruitment in neointima formation. Circ Res. 2010;107:96-105.
19. Hamesch K, Subramanian P, Li X, Dembowsky K, Chevalier E, Weber C, Schober A. The CXCR4 antagonist POL5551 is equally effective as sirolimus in reducing neointima formation without impairing re-endothelialisation. Thromb Haemost. 2012;107:356-368.
20. Karshovska E, Zagorac D, Zernecke A, Weber C, Schober A. A small molecule CXCR4 antagonist inhibits neointima formation and smooth muscle progenitor cell mobilization after arterial injury. J Thromb Haemost. 2008;6:1812-1815.
21. Sakihama H, Masunaga T, Yamashita K, Hashimoto T, Inobe M, Todo S, Uede T. Stromal cell-derived factor-1 and CXCR4 interaction is critical for development of transplant arteriosclerosis. Circulation. 2004;110:2924-2930.
22. Schober A, Hristov M, Kofler S, et al. CD34+CD140b+ cells and circulating CXCL12 correlate with the angiographically assessed severity of cardiac allograft vasculopathy. Eur Heart J. 2011;32:476-484.
23. Zernecke A, Bidzhekov K, Noels H, Shagdarsuren E, Gan L, Denecke B, Hristov M, Köppel T, Jahantigh MN, Lutgens E, Wang S, Olson EN, Schober A, Weber C. Delivery of microRNA-126 by apoptotic bodies induces CXCL12-dependent vascular protection. Sci Signal. 2009;2:ra81.
24. Zernecke A, Bot I, Djalali-Talab Y, Shagdarsuren E, Bidzhekov K, Meiler S, Krohn R, Schober A, Sperandio M, Soehnlein O, Bornemann J, Tacke F, Biessen EA, Weber C. Protective role of CXC receptor 4/ CXC ligand 12 unveils the importance of neutrophils in atherosclerosis. Circ Res. 2008;102:209-217.
25. Damas JK, Waehre T, Yndestad A, Ueland T, Müller F, Eiken HG, Holm AM, Halvorsen B, Frøland SS, Gullestad L, Aukrust P. Stromal cellderived factor-1alpha in unstable angina: potential antiinflammatory and matrix-stabilizing effects. Circulation. 2002;106:36-42.
26. Mehta NN, Li M, William D, et al. The novel atherosclerosis locus at 10q11 regulates plasma CXCL12 levels. Eur Heart J. 2011;32:963-971.
27. Petit I, Szyper-Kravitz M, Nagler A, Lahav M, Peled A, Habler L, Ponomaryov T, Taichman RS, Arenzana-Seisdedos F, Fujii N, Sandbank J, Zipori D, Lapidot T. G-CSF induces stem cell mobilization by decreasing bone marrow SDF-1 and up-regulating CXCR4. Nat Immunol. 2002;3:687-694.
28. Sweeney EA, Lortat-Jacob H, Priestley GV, Nakamoto B, Papayannopoulou T. Sulfated polysaccharides increase plasma levels of SDF-1 in monkeys and mice: involvement in mobilization of stem/progenitor cells. Blood. 2002;99:44-51.
29. Dar A, Schajnovitz A, Lapid K, et al. Rapid mobilization of hematopoietic progenitors by AMD3100 and catecholamines is mediated by CXCR4-dependent SDF-1 release from bone marrow stromal cells. Leukemia. 2011;25:1286-1296.
30. Nam D, Ni CW, Rezvan A, Suo J, Budzyn K, Llanos A, Harrison D, Giddens D, Jo H. Partial carotid ligation is a model of acutely induced disturbed flow, leading to rapid endothelial dysfunction and atherosclerosis. Am J Physiol Heart Circ Physiol. 2009;297:H1535-H1543.
31. Moessler H, Mericskay M, Li Z, Nagl S, Paulin D, Small JV. The SM 22 promoter directs tissue-specific expression in arterial but not in venous or visceral smooth muscle cells in transgenic mice. Development. 1996;122:2415-2425.
32. Hattori K, Heissig B, Tashiro K, Honjo T, Tateno M, Shieh JH, Hackett NR, Quitoriano MS, Crystal RG, Rafii S, Moore MA. Plasma elevation of stromal cell-derived factor-1 induces mobilization of mature and immature hematopoietic progenitor and stem cells. Blood. 2001;97:3354-3360.
33. Karshovska E, Zernecke A, Sevilmis G, Millet A, Hristov M, Cohen CD, Schmid H, Krotz F, Sohn HY, Klauss V, Weber C, Schober A. Expression of HIF-1alpha in injured arteries controls SDF-1alpha mediated neointima formation in apolipoprotein E deficient mice. Arterioscler Thromb Vasc Biol. 2007;27:2540-2547.