Growth differentiation factor 15 deficiency protects against atherosclerosis by attenuating CCR2-mediated macrophage chemotaxis

Journal of Experimental Medicine

Volumn 208, Issue 2, 2011, Pages 217-225

  De Jager, Saskia C A ^a   Bermúdez, Beatriz ^b,h   Bot, Ilze ^a   Koenen, Rory R ^c,d,h   Bot, Martine ^a   Kavelaars, Annemieke ^f   De Waard, Vivian ^e   Heijnen, Cobi J ^f   Muriana, Francisco J G ^b   Weber, Christian ^c,d,g   Van Berkel, Theo J C ^a   Kuiper, Johan ^a   Lee, Se Jin ^g   Abia, Rocio ^b   Biessen, Erik A L ^a,h  

^a LEIDEN UNIVERSITY   (Netherlands)

^b INSTITUTO DE LA GRASA   (Spain)

^c UNIVERSITY HOSPITAL RWTH AACHEN   (Germany)

^d UNIVERSITY OF MUNICH   (Germany)

^e UNIVERSITY OF AMSTERDAM   (Netherlands)

^f UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^g JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^h MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR CCR2; COLLAGEN; GROWTH DIFFERENTIATION FACTOR 15; LOW DENSITY LIPOPROTEIN RECEPTOR; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATHEROSCLEROSIS; CELL DEATH; CONTROLLED STUDY; DISEASE COURSE; IN VITRO STUDY; INFLAMMATORY INFILTRATE; MACROPHAGE; MALE; MOUSE; NECROSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; RECEPTOR UPREGULATION;

ANIMALS; APOPTOSIS; ATHEROSCLEROSIS; BONE MARROW TRANSPLANTATION; CHEMOTAXIS; DNA PRIMERS; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GROWTH DIFFERENTIATION FACTOR 15; IMMUNOHISTOCHEMISTRY; MACROPHAGES; MICE; MICE, KNOCKOUT; PHAGOCYTOSIS; RECEPTORS, CCR2; RECEPTORS, LDL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 79951708423     PISSN: 00221007     EISSN: 15409538     Source Type: Journal    
DOI: 10.1084/jem.20100370     Document Type: Article

References (28)

1. Ait-Oufella, H., V. Pouresmail, T. Simon, O. Blanc-Brude, K. Kinugawa, R. Merval, G. Offenstadt, G. Lesèche, P.L. Cohen, A. Tedgui, and Z. Mallat. 2008. Defective mer receptor tyrosine kinase signaling in bone marrow cells promotes apoptotic cell accumulation and accelerates atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 28:1429-1431. doi:10.1161/ATVBAHA.108.169078
2. Aragay, A.M., M. Mellado, J.M. Frade, A.M. Martin, M.C. Jimenez-Sainz, C. Martinez-A, and F. Mayor Jr. 1998. Monocyte chemoattractant protein-1-induced CCR2B receptor desensitization mediated by the G protein-coupled receptor kinase 2. Proc. Natl. Acad. Sci. USA. 95: 2985-2990. doi:10.1073/pnas.95.6.2985 (Pubitemid 28135841)
3. Bootcov, M.R., A.R. Bauskin, S.M. Valenzuela, A.G. Moore, M. Bansal, X.Y. He, H.P. Zhang, M. Donnellan, S. Mahler, K. Pryor, et al. 1997. MIC-1, a novel macrophage inhibitory cytokine, is a divergent member of the TGF-beta superfamily. Proc. Natl. Acad. Sci. USA. 94:11514-11519. doi:10.1073/pnas.94.21. 11514 (Pubitemid 27451030)
4. Bouzas-Mosquera, A., J. Peteiro, J.M. Vázquez-Rodríguez, and N. Alvarez-García. 2008. Growth-differentiation factor-15 for risk stratification in patients with acute chest pain. Eur. Heart J. 29:2947, author reply :2947-2948. doi:10.1093/eurheartj/ehn457
5. Brown, D.A., J. Moore, H. Johnen, T.J. Smeets, A.R. Bauskin, T. Kuffner, H. Weedon, S.T. Milliken, P.P. Tak, M.D. Smith, and S.N. Breit. 2007. Serum macrophage inhibitory cytokine 1 in rheumatoid arthritis: a potential marker of erosive joint destruction. Arthritis Rheum. 56:753-764. doi:10.1002/art.22410 (Pubitemid 46399422)
6. Eggers, K.M., T. Kempf, T. Allhoff, B. Lindahl, L. Wallentin, and K.C. Wollert. 2008. Growth-differentiation factor-15 for early risk stratification in patients with acute chest pain. Eur. Heart J. 29:2327-2335. doi:10.1093/eurheartj/ehn339
7. Engelse, M.A., J.M. Neele, T.A. van Achterberg, B.E. van Aken, R.H. van Schaik, H. Pannekoek, and C.J. de Vries. 1999. Human activin-A is expressed in the atherosclerotic lesion and promotes the contractile phenotype of smooth muscle cells. Circ. Res. 85:931-939. (Pubitemid 29534168)
8. Guo, J., M. Van Eck, J. Twisk, N. Maeda, G.M. Benson, P.H. Groot, and T.J. Van Berkel. 2003. Transplantation of monocyte CC-chemokine receptor 2-deficient bone marrow into ApoE3-Leiden mice inhibits atherogenesis. Arterioscler. Thromb. Vasc. Biol. 23:447-453. doi:10.1161/01.ATV.0000058431. 78833.F5 (Pubitemid 36337221)
9. Guo, J., V. de Waard, M. Van Eck, R.B. Hildebrand, E.J. van Wanrooij, J. Kuiper, N. Maeda, G.M. Benson, P.H. Groot, and T.J. Van Berkel. 2005. Repopulation of apolipoprotein E knockout mice with CCR2-deficient bone marrow progenitor cells does not inhibit ongoing atherosclerotic lesion development. Arterioscler. Thromb. Vasc. Biol. 25:1014-1019. doi:10.1161/01.ATV.0000163181. 40896.42 (Pubitemid 40627848)
10. Ho, J., E. Cocolakis, V.M. Dumas, B.I. Posner, S.A. Laporte, and J.J. Lebrun. 2005. The G protein-coupled receptor kinase-2 is a TGFbeta-inducible antagonist of TGFbeta signal transduction. EMBO J. 24:3247-3258. doi:10.1038/sj.emboj.7600794 (Pubitemid 41348699)
11. Hogan, B.L. 1996. Bone morphogenetic proteins in development. Curr. Opin. Genet. Dev. 6:432-438. doi:10.1016/S0959-437X(96)80064-5 (Pubitemid 26280795)
12. Hsiao, E.C., L.G. Koniaris, T. Zimmers-Koniaris, S.M. Sebald, T.V. Huynh, and S.J. Lee. 2000. Characterization of growth-differentiation factor 15, a transforming growth factor beta superfamily member induced following liver injury. Mol. Cell. Biol. 20:3742-3751. doi:10.1128/MCB.20.10.3742-3751.2000 (Pubitemid 30243919)
13. Kempf, T., M. Eden, J. Strelau, M. Naguib, C. Willenbockel, J. Tongers, J. Heineke, D. Kotlarz, J. Xu, J.D. Molkentin, et al. 2006. The transforming growth factor-beta superfamily member growth-differentiation factor-15 protects the heart from ischemia/reperfusion injury. Circ. Res. 98:351-360. doi:10.1161/01.RES.0000202805.73038.48
14. Khan, S.Q., K. Ng, O. Dhillon, D. Kelly, P. Quinn, I.B. Squire, J.E. Davies, and L.L. Ng. 2009. Growth differentiation factor-15 as a prognostic marker in patients with acute myocardial infarction. Eur. Heart J. 30:1057-1065. doi:10.1093/eurheartj/ehn600
15. Kingsley, D.M. 1994. The TGF-beta superfamily: new members, new receptors, and new genetic tests of function in different organisms. Genes Dev. 8:133-146. doi:10.1101/gad.8.2.133
16. Liu, A., and L.A. Niswander. 2005. Bone morphogenetic protein signalling and vertebrate nervous system development. Nat. Rev. Neurosci. 6:945-954. doi:10.1038/nrn1805 (Pubitemid 41753088)
17. Lutgens, E., M. Gijbels, M. Smook, P. Heeringa, P. Gotwals, V.E. Koteliansky, and M.J. Daemen. 2002. Transforming growth factor-beta mediates balance between inflammation and fibrosis during plaque progression. Arterioscler. Thromb. Vasc. Biol. 22:975-982. doi:10.1161/01.ATV.0000019729. 39500.2F (Pubitemid 34655226)
18. Mallat, Z., A. Gojova, C. Marchiol-Fournigault, B. Esposito, C. Kamaté, R. Merval, D. Fradelizi, and A. Tedgui. 2001. Inhibition of transforming growth factor-beta signaling accelerates atherosclerosis and induces an unstable plaque phenotype in mice. Circ. Res. 89:930-934. doi:10.1161/hh2201.099415 (Pubitemid 34627899)
19. Massagué, J. 1998. TGF-beta signal transduction. Annu. Rev. Biochem. 67:753-791. doi:10.1146/annurev.biochem.67.1.753
20. Massagué, J., S.W. Blain, and R.S. Lo. 2000. TGFbeta signaling in growth control, cancer, and heritable disorders. Cell. 103:295-309. doi:10.1016/S0092-8674(00)00121-5
21. Schlittenhardt, D., A. Schober, J. Strelau, G.A. Bonaterra, W. Schmiedt, K. Unsicker, J. Metz, and R. Kinscherf. 2004. Involvement of growth differentiation factor-15/macrophage inhibitory cytokine-1 (GDF-15/MIC-1) in oxLDL-induced apoptosis of human macrophages in vitro and in arteriosclerotic lesions. Cell Tissue Res. 318:325-333. doi:10.1007/s00441-004-0986-3 (Pubitemid 39506502)
22. Shi, Y., and J. Massagué. 2003. Mechanisms of TGF-beta signaling from cell membrane to the nucleus. Cell. 113:685-700. doi:10.1016/S0092-8674(03) 00432-X (Pubitemid 36724933)
23. Tacke, F., D. Alvarez, T.J. Kaplan, C. Jakubzick, R. Spanbroek, J. Llodra, A. Garin, J. Liu, M. Mack, N. van Rooijen, et al. 2007. Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J. Clin. Invest. 117:185-194. doi:10.1172/JCI28549 (Pubitemid 46048465)
24. Thorp, E., D. Cui, D.M. Schrijvers, G. Kuriakose, and I. Tabas. 2008. Mertk receptor mutation reduces efferocytosis efficiency and promotes apoptotic cell accumulation and plaque necrosis in atherosclerotic lesions of apoe-/- mice. Arterioscler. Thromb. Vasc. Biol. 28:1421-1428. doi:10.1161/ATVBAHA.108. 167197
25. Vergunst, C.E., D.M. Gerlag, L. Lopatinskaya, L. Klareskog, M.D. Smith, F. van den Bosch, H.J. Dinant, Y. Lee, T. Wyant, E.W. Jacobson, et al. 2008. Modulation of CCR2 in rheumatoid arthritis: a double-blind, randomized, placebo-controlled clinical trial. Arthritis Rheum. 58:1931-1939. doi:10.1002/art.23591 (Pubitemid 351988084)
26. Vroon, A., C.J. Heijnen, and A. Kavelaars. 2006. GRKs and arrestins: regulators of migration and inflammation. J. Leukoc. Biol. 80:1214-1221. doi:10.1189/jlb.0606373 (Pubitemid 44904958)
27. Wollert, K.C., T. Kempf, T. Peter, S. Olofsson, S. James, N. Johnston, B. Lindahl, R. Horn-Wichmann, G. Brabant, M.L. Simoons, et al. 2007. Prognostic value of growth-differentiation factor-15 in patients with non-ST-elevation acute coronary syndrome. Circulation. 115:962-971. doi:10.1161/CIRCULATIONAHA. 106.650846 (Pubitemid 46328289)
28. Xu, J., T.R. Kimball, J.N. Lorenz, D.A. Brown, A.R. Bauskin, R. Klevitsky, T.E. Hewett, S.N. Breit, and J.D. Molkentin. 2006. GDF15/MIC-1 functions as a protective and antihypertrophic factor released from the myocardium in association with SMAD protein activation. Circ. Res. 98:342-350. doi:10.1161/01.RES.0000202804.84885.d0