Impaired LRP6-TCF7L2 Activity Enhances Smooth Muscle Cell Plasticity and Causes Coronary Artery Disease

Cell Reports

Volumn 13, Issue 4, 2015, Pages 746-759

  Srivastava, Roshni ^a   Zhang, Jiasheng ^a   Go, Gwang woong ^a,b   Narayanan, Anand ^a   Nottoli, Timothy P ^a   Mani, Arya ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Kookmin University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

LOW DENSITY LIPOPROTEIN RECEPTOR RELATED PROTEIN 6; PLATELET DERIVED GROWTH FACTOR; TRANSCRIPTION FACTOR 7 LIKE 2; TRANSCRIPTION FACTOR SP1; WNT PROTEIN; WNT3A PROTEIN; LRP6 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; CORONARY ARTERY ATHEROSCLEROSIS; CORONARY ARTERY DISEASE; MOLECULAR PATHOLOGY; MOUSE; NEOINTIMA; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; TRANSCRIPTION REGULATION; ANIMAL; CELL CULTURE; CELL PLASTICITY; CYTOLOGY; GENETICS; HUMAN; METABOLISM; MUTANT MOUSE STRAIN; PHYSIOLOGY; SMOOTH MUSCLE CELL;

ANIMALS; CELL PLASTICITY; CELLS, CULTURED; CORONARY ARTERY DISEASE; HUMANS; LOW DENSITY LIPOPROTEIN RECEPTOR-RELATED PROTEIN-6; MICE; MICE, MUTANT STRAINS; MYOCYTES, SMOOTH MUSCLE; TRANSCRIPTION FACTOR 7-LIKE 2 PROTEIN;

EID: 84945546762     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.09.028     Document Type: Article

References (40)

1. Ait-Oufella H., Taleb S., Mallat Z., Tedgui A. Recent advances on the role of cytokines in atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 2011, 31:969-979.
2. Allahverdian S., Chehroudi A.C., McManus B.M., Abraham T., Francis G.A. Contribution of intimal smooth muscle cells to cholesterol accumulation and macrophage-like cells in human atherosclerosis. Circulation 2014, 129:1551-1559.
3. Cheng Z., Biechele T., Wei Z., Morrone S., Moon R.T., Wang L., Xu W. Crystal structures of the extracellular domain of LRP6 and its complex with DKK1. Nat. Struct. Mol. Biol. 2011, 18:1204-1210.
4. Cheng S.L., Ramachandran B., Behrmann A., Shao J.S., Mead M., Smith C., Krchma K., Bello Arredondo Y., Kovacs A., Kapoor K., et al. Vascular smooth muscle LRP6 limits arteriosclerotic calcification in diabetic LDLR-/- mice by restraining noncanonical Wnt signals. Circ. Res. 2015, 117:142-156.
5. Deniaud E., Baguet J., Chalard R., Blanquier B., Brinza L., Meunier J., Michallet M.C., Laugraud A., Ah-Soon C., Wierinckx A., et al. Overexpression of transcription factor Sp1 leads to gene expression perturbations and cell cycle inhibition. PLoS ONE 2009, 4:e7035.
6. Dienz O., Rincon M. The effects of IL-6 on CD4 T cell responses. Clin. Immunol. 2009, 130:27-33.
7. Farb A., Burke A.P., Tang A.L., Liang T.Y., Mannan P., Smialek J., Virmani R. Coronary plaque erosion without rupture into a lipid core. A frequent cause of coronary thrombosis in sudden coronary death. Circulation 1996, 93:1354-1363.
8. Feil S., Fehrenbacher B., Lukowski R., Essmann F., Schulze-Osthoff K., Schaller M., Feil R. Transdifferentiation of vascular smooth muscle cells to macrophage-like cells during atherogenesis. Circ. Res. 2014, 115:662-667.
9. Giannetti M., Schroeder H.A., Zalewski A., Gonsalves N., Bryce P.J. Dysregulation of the Wnt pathway in adult eosinophilic esophagitis. Dis. Esophagus 2014, Published online August 28, 2014. 10.1111/dote.12273.
10. Go G.W., Srivastava R., Hernandez-Ono A., Gang G., Smith S.B., Booth C.J., Ginsberg H.N., Mani A. The combined hyperlipidemia caused by impaired Wnt-LRP6 signaling is reversed by Wnt3a rescue. Cell Metab. 2014, 19:209-220.
11. Gomez D., Owens G.K. Smooth muscle cell phenotypic switching in atherosclerosis. Cardiovasc. Res. 2012, 95:156-164.
12. Gustavson M.D., Crawford H.C., Fingleton B., Matrisian L.M. Tcf binding sequence and position determines beta-catenin and Lef-1 responsiveness of MMP-7 promoters. Mol. Carcinog. 2004, 41:125-139.
13. Hatzis P., van der Flier L.G., van Driel M.A., Guryev V., Nielsen F., Denissov S., Nijman I.J., Koster J., Santo E.E., Welboren W., et al. Genome-wide pattern of TCF7L2/TCF4 chromatin occupancy in colorectal cancer cells. Mol. Cell. Biol. 2008, 28:2732-2744.
14. Ishitani T., Ninomiya-Tsuji J., Nagai S., Nishita M., Meneghini M., Barker N., Waterman M., Bowerman B., Clevers H., Shibuya H., Matsumoto K. The TAK1-NLK-MAPK-related pathway antagonizes signalling between beta-catenin and transcription factor TCF. Nature 1999, 399:798-802.
15. Ishitani T., Ninomiya-Tsuji J., Matsumoto K. Regulation of lymphoid enhancer factor 1/T-cell factor by mitogen-activated protein kinase-related Nemo-like kinase-dependent phosphorylation in Wnt/beta-catenin signaling. Mol. Cell. Biol. 2003, 23:1379-1389.
16. Lin X., Wang Z., Gu L., Deuel T.F. Functional analysis of the human platelet-derived growth factor A-chain promoter region. J. Biol. Chem. 1992, 267:25614-25619.
17. Mani A., Radhakrishnan J., Wang H., Mani A., Mani M.A., Nelson-Williams C., Carew K.S., Mane S., Najmabadi H., Wu D., Lifton R.P. LRP6 mutation in a family with early coronary disease and metabolic risk factors. Science 2007, 315:1278-1282.
18. Milewicz D.M., Kwartler C.S., Papke C.L., Regalado E.S., Cao J., Reid A.J. Genetic variants promoting smooth muscle cell proliferation can result in diffuse and diverse vascular diseases: evidence for a hyperplastic vasculomyopathy. Genet. Med. 2010, 12:196-203.
19. Mill C., George S.J. Wnt signalling in smooth muscle cells and its role in cardiovascular disorders. Cardiovasc. Res. 2012, 95:233-240.
20. Muendlein A., Saely C.H., Geller-Rhomberg S., Sonderegger G., Rein P., Winder T., Beer S., Vonbank A., Drexel H. Single nucleotide polymorphisms of TCF7L2 are linked to diabetic coronary atherosclerosis. PLoS ONE 2011, 6:e17978.
21. Nalesso G., Sherwood J., Bertrand J., Pap T., Ramachandran M., De Bari C., Pitzalis C., Dell'accio F. WNT-3A modulates articular chondrocyte phenotype by activating both canonical and noncanonical pathways. J. Cell Biol. 2011, 193:551-564.
22. Nusse R. Wnt signaling. Cold Spring Harb. Perspect. Biol. 2012, 4. pii: a011163.
23. Park G.H., Plummer H.K., Krystal G.W. Selective Sp1 binding is critical for maximal activity of the human c-kit promoter. Blood 1998, 92:4138-4149.
24. Pereira C.P., Bachli E.B., Schoedon G. The wnt pathway: a macrophage effector molecule that triggers inflammation. Curr. Atheroscler. Rep. 2009, 11:236-242.
25. Ray J.L., Leach R., Herbert J.M., Benson M. Isolation of vascular smooth muscle cells from a single murine aorta. Methods Cell Sci. 2001, 23:185-188.
26. Ross R., Glomset J.A. Atherosclerosis and the arterial smooth muscle cell: Proliferation of smooth muscle is a key event in the genesis of the lesions of atherosclerosis. Science 1973, 180:1332-1339.
27. Schwartz S.M., deBlois D., O'Brien E.R. The intima. Soil for atherosclerosis and restenosis. Circ. Res. 1995, 77:445-465.
28. Shankman L.S., Gomez D., Cherepanova O.A., Salmon M., Alencar G.F., Haskins R.M., Swiatlowska P., Newman A.A., Greene E.S., Straub A.C., et al. KLF4-dependent phenotypic modulation of smooth muscle cells has a key role in atherosclerotic plaque pathogenesis. Nat. Med. 2015, 21:628-637.
29. Shen S., Klamer G., Xu N., O'Brien T.A., Dolnikov A. GSK-3β inhibition preserves naive T cell phenotype in bone marrow reconstituted mice. Exp. Hematol. 2013, 41. 1016-27.e1.
30. Singh R., De Aguiar R.B., Naik S., Mani S., Ostadsharif K., Wencker D., Sotoudeh M., Malekzadeh R., Sherwin R.S., Mani A. LRP6 enhances glucose metabolism by promoting TCF7L2-dependent insulin receptor expression and IGF receptor stabilization in humans. Cell Metab. 2013, 17:197-209.
31. Singh R., Smith E., Fathzadeh M., Liu W., Go G.W., Subrahmanyan L., Faramarzi S., McKenna W., Mani A. Rare nonconservative LRP6 mutations are associated with metabolic syndrome. Hum. Mutat. 2013, 34:1221-1225.
32. Sousa A.G., Selvatici L., Krieger J.E., Pereira A.C. Association between genetics of diabetes, coronary artery disease, and macrovascular complications: exploring a common ground hypothesis. Rev. Diabet. Stud. 2011, 8:230-244.
33. Tan N.Y., Khachigian L.M. Sp1 phosphorylation and its regulation of gene transcription. Mol. Cell. Biol. 2009, 29:2483-2488.
34. van Loosdregt J., Fleskens V., Tiemessen M.M., Mokry M., van Boxtel R., Meerding J., Pals C.E., Kurek D., Baert M.R., Delemarre E.M., et al. Canonical Wnt signaling negatively modulates regulatory T cell function. Immunity 2013, 39:298-310.
35. Virmani R., Kolodgie F.D., Burke A.P., Farb A., Schwartz S.M. Lessons from sudden coronary death: a comprehensive morphological classification scheme for atherosclerotic lesions. Arterioscler. Thromb. Vasc. Biol. 2000, 20:1262-1275.
36. Wang H., Zhang W., Tang R., Hebbel R.P., Kowalska M.A., Zhang C., Marth J.D., Fukuda M., Zhu C., Huo Y. Core2 1-6-N-glucosaminyltransferase-I deficiency protects injured arteries from neointima formation in ApoE-deficient mice. Arterioscler. Thromb. Vasc. Biol. 2009, 29:1053-1059.
37. Wang H., Liu Q.J., Chen M.Z., Li L., Zhang K., Cheng G.H., Ma L., Gong Y.Q. Association of common polymorphisms in the LRP6 gene with sporadic coronary artery disease in a Chinese population. Chin. Med. J. (Engl.) 2012, 125:444-449.
38. Wang S., Song K., Srivastava R., Dong C., Go G.-W., Li N., Iwakiri Y., Mani A. Nonalcoholic fatty liver disease induced by noncanonical Wnt and its rescue by Wnt3a. FASEB J. 2015, 29:3436-3445. 10.1096/fj.15-271171.
39. Xu Y., Gong W., Peng J., Wang H., Huang J., Ding H., Wang D.W. Functional analysis LRP6 novel mutations in patients with coronary artery disease. PLoS ONE 2014, 9:e84345.
40. Zhang X., Diab I.H., Zehner Z.E. ZBP-89 represses vimentin gene transcription by interacting with the transcriptional activator, Sp1. Nucleic Acids Res. 2003, 31:2900-2914.