TRB3 mediates homocysteine-induced inhibition of endothelial cell proliferation

Journal of Cellular Physiology

Volumn 226, Issue 11, 2011, Pages 2782-2789

  Zou, Tong ^a   Liu, Wen Jing ^b   Li, Shu De ^c   Zhou, Wei ^b   Yang, Jie Fu ^a   Zou, Cheng Gang ^b  

^a BEIJING HOSPITAL   (China)

^b YUNNAN UNIVERSITY   (China)

^c KUNMING MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP; CYCLIN DEPENDENT KINASE INHIBITOR 1B; DNA; HOMOCYSTEINE; PROTEIN; SMALL INTERFERING RNA; THYMIDINE DERIVATIVE; TRIBBLES RELATED PROTEIN 3; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL CYCLE ARREST; CELL CYCLE G1 PHASE; CELL PROLIFERATION; CONTROLLED STUDY; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; UMBILICAL VEIN ENDOTHELIAL CELL; UPREGULATION;

CELL CYCLE PROTEINS; CELL PROLIFERATION; CELLS, CULTURED; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; CYCLIN-DEPENDENT KINASE INHIBITOR P27; ENDOTHELIAL CELLS; GENE KNOCKDOWN TECHNIQUES; HOMOCYSTEINE; HUMANS; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS C-AKT; REPRESSOR PROTEINS; RNA, SMALL INTERFERING; UP-REGULATION;

EID: 79960774841     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.22554     Document Type: Article

References (40)

1. Artwohl M, Muth K, Kosulin K, de Martin R, Holzenbein T, Rainer G, Freudenthaler A, Huttary N, Schmetterer L, Waldhausl WK, Baumgartner-Parzer SM. 2007. R-(+)-alpha-lipoic acid inhibits endothelial cell apoptosis and proliferation: Involvement of Akt and retinoblastoma protein/E2F-1. Am J Physiol Endocrinol Metab 293: E681-E689.
2. Bao XM, Wu CF, Lu GP. 2010. Atorvastatin inhibits homocysteine-induced dysfunction and apoptosis in endothelial progenitor cells. Acta Pharmacol Sin 31: 476-484.
3. Bryant P, Zheng Q, Pumiglia K. 2006. Focal adhesion kinase controls cellular levels of p27/Kip1 and p21/Cip1 through Skp2-dependent and -independent mechanisms. Mol Cell Biol 26: 4201-4213.
4. Burgering BM, Medema RH. 2003. Decisions on life and death: FOXO Forkhead transcription factors are in command when PKB/Akt is off duty. J Leukoc Biol 73: 689-701.
5. Cantley LC, Neel BG. 1999. New insights into tumor suppression: PTEN suppresses tumor formation by restraining the phosphoinositide 3-kinase/AKT pathway. Proc Natl Acad Sci USA 96: 4240-4245.
6. Chao CL, Kuo TL, Lee YT. 2000. Effects of methionine-induced hyperhomocysteinemia on endothelium-dependent vasodilation and oxidative status in healthy adults. Circulation 101: 485-490.
7. Collado M, Medema RH, Garcia-Cao I, Dubuisson ML, Barradas M, Glassford J, Rivas C, Burgering BM, Serrano M, Lam EW. 2000. Inhibition of the phosphoinositide 3-kinase pathway induces a senescence-like arrest mediated by p27Kip1. J Biol Chem 275: 21960-21968.
8. Dayal S, Arning E, Bottiglieri T, Boger RH, Sigmund CD, Faraci FM, Lentz SR. 2004. Cerebral vascular dysfunction mediated by superoxide in hyperhomocysteinemic mice. Stroke 35: 1957-1962.
9. Du K, Herzig S, Kulkarni RN, Montminy M. 2003. TRB3: A tribbles homolog that inhibits Akt/PKB activation by insulin in liver. Science 300: 1574-1577.
10. Eberhardt RT, Forgione MA, Cap A, Leopold JA, Rudd MA, Trolliet M, Heydrick S, Stark R, Klings ES, Moldovan NI, Yaghoubi M, Goldschmidt-Clermont PJ, Farber HW, Cohen R, Loscalzo J. 2000. Endothelial dysfunction in a murine model of mild hyperhomocyst(e)inemia. J Clin Invest 106: 483-491.
11. Goukassian D, Diez-Juan A, Asahara T, Schratzberger P, Silver M, Murayama T, Isner JM, Andres V. 2001. Overexpression of p27(Kip1) by doxycycline-regulated adenoviral vectors inhibits endothelial cell proliferation and migration and impairs angiogenesis. FASEB J 15: 1877-1885.
12. Gupta S, Kuhnisch J, Mustafa A, Lhotak S, Schlachterman A, Slifker MJ, Klein-Szanto A, High KA, Austin RC, Kruger WD. 2009. Mouse models of cystathionine beta-synthase deficiency reveal significant threshold effects of hyperhomocysteinemia. FASEB J 23: 883-893.
13. Herzig S, Long F, Jhala US, Hedrick S, Quinn R, Bauer A, Rudolph D, Schutz G, Yoon C, Puigserver P, Spiegelman B, Montminy M. 2001. CREB regulates hepatic gluconeogenesis through the coactivator PGC-1. Nature 413: 179-183.
14. Jamaluddin MD, Chen I, Yang F, Jiang X, Jan M, Liu X, Schafer AI, Durante W, Yang X, Wang H. 2007. Homocysteine inhibits endothelial cell growth via DNA hypomethylation of the cyclin A gene. Blood 110: 3648-3655.
15. Jiang X, Yang F, Tan H, Liao D, Bryan RM, Jr., Randhawa JK, Rumbaut RE, Durante W, Schafer AI, Yang X, Wang H. 2005. Hyperhomocystinemia impairs endothelial function and eNOS activity via PKC activation. Arterioscler Thromb Vasc Biol 25: 2515-2521.
16. Kehrer JP, Biswal SS, La E, Thuillier P, Datta K, Fischer SM, Vanden Heuvel JP. 2001. Inhibition of peroxisome-proliferator-activated receptor (PPAR)alpha by MK886. Biochem J 356: 899-906.
17. Kim TY, Kim WI, Smith RE, Kay ED. 2001. Role of p27(Kip1) in cAMP- and TGF-beta2-mediated antiproliferation in rabbit corneal endothelial cells. Invest Ophthalmol Vis Sci 42: 3142-3149.
18. Koo SH, Satoh H, Herzig S, Lee CH, Hedrick S, Kulkarni R, Evans RM, Olefsky J, Montminy M. 2004. PGC-1 promotes insulin resistance in liver through PPAR-alpha-dependent induction of TRB-3. Nat Med 10: 530-534.
19. Lee HT, Kay EP. 2003a. Regulatory role of cAMP on expression of Cdk4 and p27(Kip1) by inhibiting phosphatidylinositol 3-kinase in corneal endothelial cells. Invest Ophthalmol Vis Sci 44: 3816-3825.
20. Lee HT, Kay EP. 2003b. Regulatory role of PI 3-kinase on expression of Cdk4 and p27, nuclear localization of Cdk4, and phosphorylation of p27 in corneal endothelial cells. Invest Ophthalmol Vis Sci 44: 1521-1528.
21. Lee JG, Kay EP. 2010. Activation of PI 3-kinase/Rac1 and ERK1/2 regulates FGF-2-mediated cell proliferation through phosphorylation of p27 at Ser10 by KIS and at Thr187 by Cdc25A/Cdk2. Invest Ophthalmol Vis Sci. DOI: 10.1167/iovs.10-6140.
22. Mata J, Curado S, Ephrussi A, Rorth P. 2000. Tribbles coordinates mitosis and morphogenesis in Drosophila by regulating string/CDC25 proteolysis. Cell 101: 511-522.
23. McCully KS. 1969. Vascular pathology of homocysteinemia: Implications for the pathogenesis of arteriosclerosis. Am J Pathol 56: 111-128.
24. McCully KS. 2009. Chemical pathology of homocysteine. IV. Excitotoxicity, oxidative stress, endothelial dysfunction, and inflammation. Ann Clin Lab Sci 39: 219-232.
25. Narita Y, Nagane M, Mishima K, Huang HJ, Furnari FB, Cavenee WK. 2002. Mutant epidermal growth factor receptor signaling down-regulates p27 through activation of the phosphatidylinositol 3-kinase/Akt pathway in glioblastomas. Cancer Res 62: 6764-6769.
26. Ohoka N, Yoshii S, Hattori T, Onozaki K, Hayashi H. 2005. TRB3, a novel ER stress-inducible gene, is induced via ATF4-CHOP pathway and is involved in cell death. EMBO J 24: 1243-1255.
27. Outinen PA, Sood SK, Pfeifer SI, Pamidi S, Podor TJ, Li J, Weitz JI, Austin RC. 1999. Homocysteine-induced endoplasmic reticulum stress and growth arrest leads to specific changes in gene expression in human vascular endothelial cells. Blood 94: 959-967.
28. Ovcharenko D, Jarvis R, Hunicke-Smith S, Kelnar K, Brown D. 2005. High-throughput RNAi screening in vitro: From cell lines to primary cells. RNA 11: 985-993.
29. Potente M, Fisslthaler B, Busse R, Fleming I. 2003. 11, 12-Epoxyeicosatrienoic acid-induced inhibition of FOXO factors promotes endothelial proliferation by down-regulating p27Kip1. J Biol Chem 278: 29619-29625.
30. Sherr CJ, Roberts JM. 1995. Inhibitors of mammalian G1 cyclin-dependent kinases. Genes Dev 9: 1149-1163.
31. Stayrook KR, Bramlett KS, Savkur RS, Ficorilli J, Cook T, Christe ME, Michael LF, Burris TP. 2005. Regulation of carbohydrate metabolism by the farnesoid X receptor. Endocrinology 146: 984-991.
32. Suhara T, Fukuo K, Yasuda O, Tsubakimoto M, Takemura Y, Kawamoto H, Yokoi T, Mogi M, Kaimoto T, Ogihara T. 2004. Homocysteine enhances endothelial apoptosis via upregulation of Fas-mediated pathways. Hypertension 43: 1208-1213.
33. Wang H, Jiang X, Yang F, Chapman GB, Durante W, Sibinga NE, Schafer AI. 2002. Cyclin A transcriptional suppression is the major mechanism mediating homocysteine-induced endothelial cell growth inhibition. Blood 99: 939-945.
34. Woo CW, Siow YL, O K. 2006. Homocysteine activates cAMP-response element binding protein in HepG2 through cAMP/PKA signaling pathway. Arterioscler Thromb Vasc Biol 26: 1043-1050.
35. Yoon JC, Puigserver P, Chen G, Donovan J, Wu Z, Rhee J, Adelmant G, Stafford J, Kahn CR, Granner DK, Newgard CB, Spiegelman BM. 2001. Control of hepatic gluconeogenesis through the transcriptional coactivator PGC-1. Nature 413: 131-138.
36. Zhang C, Cai Y, Adachi MT, Oshiro S, Aso T, Kaufman RJ, Kitajima S. 2001. Homocysteine induces programmed cell death in human vascular endothelial cells through activation of the unfolded protein response. J Biol Chem 276: 35867-35874.
37. Zhu JH, Chen JZ, Wang XX, Xie XD, Sun J, Zhang FR. 2006. Homocysteine accelerates senescence and reduces proliferation of endothelial progenitor cells. J Mol Cell Cardiol 40: 648-652.
38. Zou CG, Banerjee R. 2003. Tumor necrosis factor-alpha-induced targeted proteolysis of cystathionine beta-synthase modulates redox homeostasis. J Biol Chem 278: 16802-16808.
39. Zou CG, Banerjee R. 2005. Homocysteine and redox signaling. Antioxid Redox Signal 7: 547-559.
40. Zou CG, Cao XZ, Zhao YS, Gao SY, Li SD, Liu XY, Zhang Y, Zhang KQ. 2009. The molecular mechanism of endoplasmic reticulum stress-induced apoptosis in PC-12 neuronal cells: The protective effect of insulin-like growth factor I. Endocrinology 150: 277-285.