Inhibition of FOXO1/3 promotes vascular calcification

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 35, Issue 1, 2015, Pages 175-183

  Deng, Liang ^a   Huang, Lu ^a   Sun, Yong ^a   Heath, Jack M ^a   Wu, Hui ^b   Chen, Yabing ^a,c  

^a 710 Shelby Biomedical Research Bldg   (United States)

^b BIRMINGHAM VA MEDICAL CENTER   (United States)

^c UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

Author keywords

AKT; FOXO1 3; PTEN; Runx2; ubiquitination; vascular calcification

Indexed keywords

CALCIUM; COLLAGEN TYPE 1; OSTEOCALCIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; POLYUBIQUITIN; PROTEIN KINASE B; SERINE; SHORT HAIRPIN RNA; THREONINE; TRANSCRIPTION FACTOR FKHR; TRANSCRIPTION FACTOR FKHRL1; TRANSCRIPTION FACTOR RUNX2; ACTIN BINDING PROTEIN; APOLIPOPROTEIN E; CRE RECOMBINASE; FORKHEAD TRANSCRIPTION FACTOR; FOXO1 PROTEIN, MOUSE; FOXO3 PROTEIN, MOUSE; INTEGRASE; MUSCLE PROTEIN; PTEN PROTEIN, MOUSE; RUNX2 PROTEIN, MOUSE; TAGLN PROTEIN, MOUSE;

ANIMAL CELL; AORTA; ARTERY CALCIFICATION; ARTICLE; BLOOD VESSEL CALCIFICATION; CANCER CELL; CELL CULTURE; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EMBRYONIC STEM CELL; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; EX VIVO STUDY; EXON; FIBROBLAST; GENE SILENCING; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MOUSE; NONHUMAN; OSTEOBLAST; PROSTATE CANCER; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; SMOOTH MUSCLE FIBER; UBIQUITINATION; UPREGULATION; VASCULAR SMOOTH MUSCLE; VASCULAR SMOOTH MUSCLE CELL; WESTERN BLOTTING; ANIMAL; AORTA DISEASE; ATHEROSCLEROSIS; DEFICIENCY; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; GENETICS; GENOTYPE; KNOCKOUT MOUSE; METABOLISM; PATHOLOGY; PHENOTYPE; PHOSPHORYLATION; PROTEIN TRANSPORT; RNA INTERFERENCE; SIGNAL TRANSDUCTION; SMOOTH MUSCLE CELL; TIME FACTOR;

ANIMALS; AORTA; AORTIC DISEASES; APOLIPOPROTEINS E; ATHEROSCLEROSIS; CELLS, CULTURED; CORE BINDING FACTOR ALPHA 1 SUBUNIT; DISEASE MODELS, ANIMAL; ENZYME ACTIVATION; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION; GENOTYPE; INTEGRASES; MICE, KNOCKOUT; MICROFILAMENT PROTEINS; MUSCLE PROTEINS; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; PHENOTYPE; PHOSPHORYLATION; PROTEIN TRANSPORT; PROTO-ONCOGENE PROTEINS C-AKT; PTEN PHOSPHOHYDROLASE; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFECTION; UBIQUITINATION; VASCULAR CALCIFICATION;

EID: 84920264031     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.114.304786     Document Type: Article

References (49)

1. Wilson PW, Kauppila LI, O'Donnell CJ, Kiel DP, Hannan M, Polak JM, Cupples LA. Abdominal aortic calcifc deposits are an important predictor of vascular morbidity and mortality. Circulation. 2001;103:1529-1534.
2. Towler DA, Demer LL. Thematic series on the pathobiology of vascular calcifcation: an introduction. Circ Res. 2011;108:1378-1380.
3. Bastos Gonçalves F, Voûte MT, Hoeks SE, Chonchol MB, Boersma EE, Stolker RJ, Verhagen HJ. Calcifcation of the abdominal aorta as an independent predictor of cardiovascular events: a meta-analysis. Heart. 2012;98:988-994.
4. Witztum JL. The oxidation hypothesis of atherosclerosis. Lancet. 1994;344:793-795.
5. Mody N, Parhami F, Sarafan TA, Demer LL. Oxidative stress modulates osteoblastic differentiation of vascular and bone cells. Free Radic Biol Med. 2001;31:509-519.
6. Steitz SA, Speer MY, Curinga G, Yang HY, Haynes P, Aebersold R, Schinke T, Karsenty G, Giachelli CM. Smooth muscle cell phenotypic transition associated with calcifcation: upregulation of Cbfa1 and downregulation of smooth muscle lineage markers. Circ Res. 2001;89:1147-1154.
7. Bostrm KI. Cell differentiation in vascular calcifcation. Z Kardiol. 2000; 89 Suppl 2: 69-74.
8. Giachelli CM. Vascular calcifcation mechanisms. J Am Soc Nephrol. 2004;15:2959-2964.
9. Shanahan CM, Cary NR, Salisbury JR, Proudfoot D, Weissberg PL, Edmonds ME. Medial localization of mineralization-regulating proteins in association with Mönckeberg's sclerosis: evidence for smooth muscle cell-mediated vascular calcifcation. Circulation. 1999;100:2168-2176.
10. Yao Y, Jumabay M, Ly A, Radparvar M, Cubberly MR, Boström KI. A role for the endothelium in vascular calcifcation. Circ Res. 2013;113:495-504.
11. Komori T, Yagi H, Nomura S, Yamaguchi A, Sasaki K, Deguchi K, Shimizu Y, Bronson RT, Gao YH, Inada M, Sato M, Okamoto R, Kitamura Y, Yoshiki S, Kishimoto T. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell. 1997;89:755-764.
12. Otto F, Thornell AP, Crompton T, Denzel A, Gilmour KC, Rosewell IR, Stamp GW, Beddington RS, Mundlos S, Olsen BR, Selby PB, Owen MJ. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell. 1997;89:765-771.
13. Byon CH, Javed A, Dai Q, Kappes JC, Clemens TL, Darley-Usmar VM, McDonald JM, Chen Y. Oxidative stress induces vascular calcifcation through modulation of the osteogenic transcription factor Runx2 by AKT signaling. J Biol Chem. 2008;283:15319-15327.
14. Sun Y, Byon CH, Yuan K, Chen J, Mao X, Heath JM, Javed A, Zhang K, Anderson PG, Chen Y. Smooth muscle cell-specifc runx2 defciency inhibits vascular calcifcation. Circ Res. 2012;111:543-552.
15. Heath J, Sun Y, Yuan K, Bradley WE, Litovsky S, Dell'italia LJ, Chatham JC, Wu H, Chen Y. Activation of AKT by O-linked N-acetyglucosamine induces vascular calcifcation in diabetes. Circ Res. 2014;114:1094-1102.
16. Steck PA, Pershouse MA, Jasser SA, Yung WK, Lin H, Ligon AH, Langford LA, Baumgard ML, Hattier T, Davis T, Frye C, Hu R, Swedlund B, Teng DH, Tavtigian SV. Identifcation of a candidate tumour suppressor gene, MMAC1, at chromosome 10q23.3 that is mutated in multiple advanced cancers. Nat Genet. 1997;15:356-362.
17. Li J, Yen C, Liaw D, et al. PTEN, a putative protein tyrosine phospha-tase gene mutated in human brain, breast, and prostate cancer. Science. 1997;275:1943-1947.
18. Carracedo A, Pandolf PP. The PTEN-PI3K pathway: of feedbacks and cross-talks. Oncogene. 2008;27:5527-5541.
19. Huang J, Kontos CD. Inhibition of vascular smooth muscle cell proliferation, migration, and survival by the tumor suppressor protein PTEN. Arterioscler Thromb Vasc Biol. 2002;22:745-751.
20. Mourani PM, Garl PJ, Wenzlau JM, Carpenter TC, Stenmark KR, Weiser-Evans MC. Unique, highly proliferative growth phenotype expressed by embryonic and neointimal smooth muscle cells is driven by constitutive Akt, mTOR, and p70S6K signaling and is actively repressed by PTEN. Circulation. 2004;109:1299-1306.
21. Nemenoff RA, Simpson PA, Furgeson SB, Kaplan-Albuquerque N, Crossno J, Garl PJ, Cooper J, Weiser-Evans MC. Targeted deletion of PTEN in smooth muscle cells results in vascular remodeling and recruitment of progenitor cells through induction of stromal cell-derived factor-1alpha. Circ Res. 2008;102:1036-1045.
22. Nemenoff RA, Horita H, Ostriker AC, Furgeson SB, Simpson PA, VanPutten V, Crossno J, Offermanns S, Weiser-Evans MC. SDF-1α induction in mature smooth muscle cells by inactivation of PTEN is a critical mediator of exacerbated injury-induced neointima formation. Arterioscler Thromb Vasc Biol. 2011;31:1300-1308.
23. Hernando E, Charytonowicz E, Dudas ME, Menendez S, Matushansky I, Mills J, Socci ND, Behrendt N, Ma L, Maki RG, Pandolf PP, Cordon-Cardo C. The AKT-mTOR pathway plays a critical role in the development of leiomyosarcomas. Nat Med. 2007;13:748-753.
24. Andrés V, Gascón-Irún M, Pandolf PP, González-Navarro H. Atheroma development in apolipoprotein E-null mice is not affected by partial inac-tivation of PTEN. Front Biosci. 2006;11:2739-2745.
25. Chen WJ, Lin KH, Lai YJ, Yang SH, Pang JH. Protective effect of pro-pylthiouracil independent of its hypothyroid effect on atherogenesis in cholesterol-fed rabbits: PTEN induction and inhibition of vascular smooth muscle cell proliferation and migration. Circulation. 2004;110:1313-1319.
26. Anderson MJ, Viars CS, Czekay S, Cavenee WK, Arden KC. Cloning and characterization of three human forkhead genes that comprise an FKHR-like gene subfamily. Genomics. 1998;47:187-199.
27. Biggs WH III, Cavenee WK, Arden KC. Identifcation and characterization of members of the FKHR (FOX O) subclass of winged-helix transcription factors in the mouse. Mamm Genome. 2001;12:416-425.
28. Jacobs FM, van der Heide LP, Wijchers PJ, Burbach JP, Hoekman MF, Smidt MP. FoxO6, a novel member of the FoxO class of transcription factors with distinct shuttling dynamics. J Biol Chem. 2003;278:35959-35967.
29. Kim DH, Zhang T, Lee S, Dong HH. FoxO6 in glucose metabolism (FoxO6). J Diabetes. 2013;5:233-240.
30. Biggs WH III, Meisenhelder J, Hunter T, Cavenee WK, Arden KC. Protein kinase B/Akt-mediated phosphorylation promotes nuclear exclusion of the winged helix transcription factor FKHR1. Proc Natl Acad Sci USA. 1999;96:7421-7426.
31. Siqueira MF, Flowers S, Bhattacharya R, Faibish D, Behl Y, Kotton DN, Gerstenfeld L, Moran E, Graves DT. FOXO1 modulates osteoblast differentiation. Bone. 2011;48:1043-1051.
32. Tseng PC, Hou SM, Chen RJ, Peng HW, Hsieh CF, Kuo ML, Yen ML. Resveratrol promotes osteogenesis of human mesenchymal stem cells by upregulating RUNX2 gene expression via the SIRT1/FOXO3A axis. J Bone Miner Res. 2011;26:2552-2563.
33. Rached MT, Kode A, Silva BC, Jung DY, Gray S, Ong H, Paik JH, DePinho RA, Kim JK, Karsenty G, Kousteni S. FoxO1 expression in osteoblasts regulates glucose homeostasis through regulation of osteocalcin in mice. J Clin Invest. 2010;120:357-368.
34. Zhang H, Pan Y, Zheng L, Choe C, Lindgren B, Jensen ED, Westendorf JJ, Cheng L, Huang H. FOXO1 inhibits Runx2 transcriptional activity and prostate cancer cell migration and invasion. Cancer Res. 2011;71:3257-3267.
35. Lesche R, Groszer M, Gao J, Wang Y, Messing A, Sun H, Liu X, Wu H. Cre/loxP-mediated inactivation of the murine Pten tumor suppressor gene. Genesis. 2002;32:148-149.
36. Mao X, Debenedittis P, Sun Y, Chen J, Yuan K, Jiao K, Chen Y. Vascular smooth muscle cell Smad4 gene is important for mouse vascular development. Arterioscler Thromb Vasc Biol. 2012;32:2171-2177.
37. Furgeson SB, Simpson PA, Park I, Vanputten V, Horita H, Kontos CD, Nemenoff RA, Weiser-Evans MC. Inactivation of the tumour suppressor, PTEN, in smooth muscle promotes a pro-infammatory phenotype and enhances neointima formation. Cardiovasc Res. 2010;86:274-282.
38. Jonason JH, Xiao G, Zhang M, Xing L, Chen D. Post-translational regulation of Runx2 in bone and cartilage. J Dent Res. 2009;88:693-703.
39. Bae SC, Lee YH. Phosphorylation, acetylation and ubiquitination: the molecular basis of RUNX regulation. Gene. 2006;366:58-66.
40. Abid MR, Yano K, Guo S, Patel VI, Shrikhande G, Spokes KC, Ferran C, Aird WC. Forkhead transcription factors inhibit vascular smooth muscle cell proliferation and neointimal hyperplasia. J Biol Chem. 2005;280:29864-29873.
41. Essaghir A, Dif N, Marbehant CY, Coffer PJ, Demoulin JB. The transcription of FOXO genes is stimulated by FOXO3 and repressed by growth factors. J Biol Chem. 2009;284:10334-10342.
42. Boström KI, Jumabay M, Matveyenko A, Nicholas SB, Yao Y. Activation of vascular bone morphogenetic protein signaling in diabetes mellitus. Circ Res. 2011;108:446-457.
43. Bialek P, Kern B, Yang X, Schrock M, Sosic D, Hong N, Wu H, Yu K, Ornitz DM, Olson EN, Justice MJ, Karsenty G. A twist code determines the onset of osteoblast differentiation. Dev Cell. 2004;6:423-435.
44. Karsenty G. Transcriptional control of skeletogenesis. Annu Rev Genomics Hum Genet. 2008;9:183-196.
45. Zhao M, Qiao M, Oyajobi BO, Mundy GR, Chen D. E3 ubiquitin ligase Smurf1 mediates core-binding factor alpha1/Runx2 degradation and plays a specifc role in osteoblast differentiation. J Biol Chem. 2003;278:27939-27944.
46. Shen R, Wang X, Drissi H, Liu F, O'Keefe RJ, Chen D. Cyclin D1-cdk4 induce runx2 ubiquitination and degradation. J Biol Chem. 2006;281:16347-16353.
47. Jones DC, Wein MN, Oukka M, Hofstaetter JG, Glimcher MJ, Glimcher LH. Regulation of adult bone mass by the zinc fnger adapter protein Schnurri-3. Science. 2006;312:1223-1227.
48. Shen R, Chen M, Wang YJ, Kaneki H, Xing L, O'keefe RJ, Chen D. Smad6 interacts with Runx2 and mediates Smad ubiqui-tin regulatory factor 1-induced Runx2 degradation. J Biol Chem. 2006;281:3569-3576.
49. Li M, Chiu JF, Gagne J, Fukagawa NK. Age-related differences in insulin-like growth factor-1 receptor signaling regulates Akt/FOXO3a and ERK/Fos pathways in vascular smooth muscle cells. J Cell Physiol. 2008;217:377-387.