The nuclear hormone receptor PPARγ counteracts vascular calcification by inhibiting Wnt5a signalling in vascular smooth muscle cells

Nature Communications

Volumn 3, Issue , 2012, Pages

  Woldt, Estelle ^a   Terrand, Jérome ^a   Mlih, Mohamed ^a   Matz, Rachel L ^a   Bruban, Véronique ^a   Coudane, Fanny ^a   Foppolo, Sophie ^a   El Asmar, Zeina ^a   Chollet, Maria Eugenia ^b   Ninio, Ewa ^b   Bednarczyk, Audrey ^a   Thiersé, Danièle ^a   Schaeffer, Christine ^a   Van Dorsselaer, Alain ^a   Boudier, Christian ^a   Wahli, Walter ^c   Chambon, Pierre ^a   Metzger, Daniel ^a   Herz, Joachim ^d   Boucher, Philippe ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b INSERM   (France)

^c UNIVERSITY OF LAUSANNE   (Switzerland)

^d UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HORMONE RECEPTOR; LOW DENSITY LIPOPROTEIN CHOLESTEROL; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; SECRETED FRIZZLED RELATED PROTEIN 2; WNT5A PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ATHEROSCLEROSIS; BLOOD VESSEL CALCIFICATION; CONTROLLED STUDY; CORONARY ARTERY; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SECRETION; VASCULAR SMOOTH MUSCLE;

ANIMALS; HUMANS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; IN SITU HYBRIDIZATION; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-1; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MODELS, BIOLOGICAL; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; PPAR GAMMA; THIAZOLIDINEDIONES; VASCULAR CALCIFICATION; WNT PROTEINS;

MUS;

EID: 84866975779     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms2087     Document Type: Article

References (46)

1. Wilson, P. W. et al. Abdominal aortic calcific deposits are an important predictor of vascular morbidity and mortality. Circulation 103, 1529-1534 (2001). (Pubitemid 32226260)
2. Sage, A. P., Tintut, Y. & Demer, L. L. Regulatory mechanisms in vascular calcification. Nat. Rev. Cardiol. 7, 528-536 (2010).
3. Walsh, C. R. et al. Abdominal aortic calcific deposits are associated with increased risk for congestive heart failure: the Framingham Heart Study. Am. Heart J. 144, 733-739 (2002).
4. Guzman, R. J. Clinical, cellular, and molecular aspects of arterial calcification. J. Vasc. Surg. 45 (Suppl A), A57-A63 (2007).
5. Karreth, F., Hoebertz, A., Scheuch, H., Eferl, R. & Wagner, E. F. The AP1 transcription factor Fra2 is required for efficient cartilage development. Development 131, 5717-5725 (2004). (Pubitemid 39625214)
6. Shao, J. S. et al. Msx2 promotes cardiovascular calcification by activating paracrine Wnt signals. J. Clin. Invest. 115, 1210-1220 (2005).
7. Zhao, Q., Behringer, R. R. & de Crombrugghe, B. Prenatal folic acid treatment suppresses acrania and meroanencephaly in mice mutant for the Cart1 homeobox gene. Nat. Genet. 13, 275-283 (1996). (Pubitemid 26230492)
8. Logan, C. Y. & Nusse, R. The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20, 781-810 (2004). (Pubitemid 39488658)
9. Kawakami, Y. et al. Involvement of Wnt-5a in chondrogenic pattern formation in the chick limb bud. Dev. Growth Differ. 41, 29-40 (1999). (Pubitemid 29088843)
10. Yamaguchi, T. P., Bradley, A., McMahon, A. P. & Jones, S. A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo. Development 126, 1211-1223 (1999). (Pubitemid 29182117)
11. May, P., Woldt, E., Matz, R. L. & Boucher, P. The LDL receptor-related protein (LRP) family: an old family of proteins with new physiological functions. Ann. Med. 39, 219-228 (2007). (Pubitemid 46676481)
12. Terrand, J. et al. LRP1 controls intracellular cholesterol storage and fatty acid synthesis through modulation of Wnt signaling. J. Biol. Chem. 284, 381-388 (2009).
13. Boucher, P., Gotthardt, M., Li, W. P., Anderson, R. G. & Herz, J. LRP: role in vascular wall integrity and protection from atherosclerosis. Science 300, 329-332 (2003). (Pubitemid 36433724)
14. Zhou, L., Takayama, Y., Boucher, P., Tallquist, M. D. & Herz, J. LRP1 regulates architecture of the vascular wall by controlling PDGFRbeta-dependent phosphatidylinositol 3-kinase activation. PLoS One 4, e6922 (2009).
15. Boucher, P. et al. LRP1 functions as an atheroprotective integrator of TGFbeta and PDFG signals in the vascular wall: implications for Marfan syndrome. PloS One 2, e448 (2007).
16. Tontonoz, P. & Spiegelman, B. M. Fat and beyond: the diverse biology of PPARgamma. Annu. Rev. Biochem. 77, 289-312 (2008).
17. Cock, T. A. et al. Enhanced bone formation in lipodystrophic PPARgamma(hyp/hyp) mice relocates haematopoiesis to the spleen. EMBO Rep. 5, 1007-1012 (2004).
18. Akune, T. et al. PPARgamma insufficiency enhances osteogenesis through osteoblast formation from bone marrow progenitors. J. Clin. Invest. 113, 846-855 (2004). (Pubitemid 38544143)
19. Imai, T. et al. Peroxisome proliferator-activated receptor gamma is required in mature white and brown adipocytes for their survival in the mouse. Proc. Natl Acad. Sci. USA 101, 4543-4547 (2004). (Pubitemid 38437447)
20. Ishibashi, S. et al. Hypercholesterolemia in low density lipoprotein receptor knockout mice and its reversal by adenovirus-mediated gene delivery. J. Clin. Invest. 92, 883-893 (1993). (Pubitemid 23262411)
21. Subramanian, V., Golledge, J., Ijaz, T., Bruemmer, D. & Daugherty, A. Pioglitazone-induced reductions in atherosclerosis occur via smooth muscle cell-specific interaction with PPAR\{gamma\}. Circ. Res. 107, 953-958 (2010).
22. Shao, J. S., Cai, J. & Towler, D. A. Molecular mechanisms of vascular calcification: lessons learned from the aorta. Arterioscler. Thromb. Vasc. Biol. 26, 1423-1430 (2006). (Pubitemid 44288965)
23. Bostrom, K. et al. Bone morphogenetic protein expression in human atherosclerotic lesions. J. Clin. Invest. 91, 1800-1809 (1993). (Pubitemid 23127387)
24. Tyson, K. L. et al. Osteo/chondrocytic transcription factors and their target genes exhibit distinct patterns of expression in human arterial calcification. Arterioscler. Thromb. Vasc. Biol. 23, 489-494 (2003). (Pubitemid 36337227)
25. Church, V., Nohno, T., Linker, C., Marcelle, C. & Francis-West, P. Wnt regulation of chondrocyte differentiation. J. Cell Sci. 115, 4809-4818 (2002). (Pubitemid 36054634)
26. Morello, R. et al. Brachy-syndactyly caused by loss of Sfrp2 function. J. Cell Physiol. 217, 127-137 (2008).
27. Keen, H. L. et al. Bioinformatic analysis of gene sets regulated by ligand-activated and dominant-negative peroxisome proliferator-activated receptor gamma in mouse aorta. Arterioscler. Thromb. Vasc. Biol. 30, 518-525 (2010).
28. Lemay, D. G. & Hwang, D. H. Genome-wide identification of peroxisome proliferator response elements using integrated computational genomics. J. Lipid Res. 47, 1583-1587 (2006). (Pubitemid 44079913)
29. Zhou, L., Choi, H. Y., Li, W. P., Xu, F. & Herz, J. LRP1 controls cPLA2 phosphorylation, ABCA1 expression and cellular cholesterol export. PLoS One 4, e6853 (2009).
30. Abedin, M. et al. N-3 fatty acids inhibit vascular calcification via the p38-mitogen-activated protein kinase and peroxisome proliferator-activated receptor-gamma pathways. Circ. Res. 98, 727-729 (2006).
31. Lencel, P. et al. Cell-specific effects of TNF-alpha and IL-1beta on alkaline phosphatase: implication for syndesmophyte formation and vascular calcification. Lab Invest. 91, 1434-1442 (2011).
32. Alfaro, M. P. et al. SFRP2 suppression of BMP and WNT signaling mediates mesenchymal stem cell (MSC) self-renewal promoting engraftment and myocardial repair. J. Biol. Chem. 285, 35645-53 (2010).
33. Yang, Y., Topol, L., Lee, H. & Wu, J. Wnt5a and Wnt5b exhibit distinct activities in coordinating chondrocyte proliferation and differentiation. Development 130, 1003-1015 (2003). (Pubitemid 36372019)
34. Daumer, K. M., Tufan, A. C. & Tuan, R. S. Long-term in vitro analysis of limb cartilage development: involvement of Wnt signaling. J. Cell. Biochem. 93, 526-541 (2004). (Pubitemid 44264188)
35. Rosen, E. D. et al. PPAR gamma is required for the differentiation of adipose tissue in vivo and in vitro. Mol. Cell. 4, 611-617 (1999). (Pubitemid 29531140)
36. Wan, Y. PPARgamma in bone homeostasis. Trends Endocrinol. Metab. 12, 722-8 (2010).
37. Wan, Y., Chong, L. W. & Evans, R. M. PPAR-gamma regulates osteoclastogenesis in mice. Nat. Med. 13, 1496-1503 (2007).
38. Naik, V. et al. Sources of cells that contribute to atherosclerotic intimal calcification: an in vivo genetic fate mapping study. Cardiovasc. Res. 94, 545-554 (2012).
39. Iyemere, V. P., Proudfoot, D., Weissberg, P. L. & Shanahan, C. M. Vascular smooth muscle cell phenotypic plasticity and the regulation of vascular calcification. J. Intern. Med. 260, 192-210 (2006). (Pubitemid 44253633)
40. Speer, M. Y. et al. Smooth muscle cells give rise to osteochondrogenic precursors and chondrocytes in calcifying arteries. Circ. Res. 104, 733-741 (2009).
41. Shanahan, C. M. et al. Medial localization of mineralization-regulating proteins in association with Monckeberg's sclerosis: evidence for smooth muscle cell-mediated vascular calcification. Circulation 100, 2168-2176 (1999).
42. Steitz, S. A. et al. Smooth muscle cell phenotypic transition associated with calcification: upregulation of Cbfa1 and downregulation of smooth muscle lineage markers. Circ. Res. 89, 1147-1154 (2001). (Pubitemid 34627872)
43. Shanahan, C. M., Weissberg, P. L. & Metcalfe, J. C. Isolation of gene markers of differentiated and proliferating vascular smooth muscle cells. Circ. Res. 73, 193-204 (1993). (Pubitemid 23173070)
44. Willert, K. et al. Wnt proteins are lipid-modified and can act as stem cell growth factors. Nature 423, 448-452 (2003). (Pubitemid 36626997)
45. Pan, Q. et al. Sox9, a key transcription factor of bone morphogenetic protein-2-induced chondrogenesis, is activated through BMP pathway and a CCAAT box in the proximal promoter. J. Cell. Physiol. 217, 228-241 (2008).
46. Compe, E. et al. Dysregulation of the peroxisome proliferator-activated receptor target genes by XPD mutations. Mol. Cell. Biol. 25, 6065-6076 (2005). (Pubitemid 40946558)