Id3 Is a novel atheroprotective factor containing a functionally significant single-nucleotide polymorphism associated with intima-media thickness in humans

Circulation Research

Volumn 106, Issue 7, 2010, Pages 1303-1311

  Doran, Amanda C ^a,b   Lehtinen, Allison B ^b,c   Meller, Nahum ^a,b   Lipinski, Michael J ^a,b   Slayton, R Parker ^a,b   Oldham, Stephanie N ^a,b   Skaflen, Marcus D ^a,b   Yeboah, Joseph ^b   Rich, Stephen S ^b   Bowden, Donald W ^c   McNamara, Coleen A ^a,b  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

^c WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Atherosclerosis; Diabetes mellitus; Genetics

Indexed keywords

ALANINE; APOLIPOPROTEIN E; INHIBITOR OF DIFFERENTIATION 3; THREONINE;

ALLELE; AMINO ACID SUBSTITUTION; ANIMAL CELL; ANIMAL EXPERIMENT; ARTERIAL WALL THICKNESS; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; CAROTID ARTERY; CONTROLLED STUDY; GENE SEQUENCE; HEART PROTECTION; HUMAN; IMMUNOPRECIPITATION; INTIMA; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; SITE DIRECTED MUTAGENESIS; SMOOTH MUSCLE FIBER; TRANSCRIPTION INITIATION; TUNICA MEDIA; VASCULAR SMOOTH MUSCLE;

AGED; ANIMALS; APOLIPOPROTEINS E; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CAROTID ARTERIES; CAROTID ARTERY DISEASES; DIABETES MELLITUS, TYPE 2; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE FREQUENCY; GENETIC PREDISPOSITION TO DISEASE; HUMANS; IMMUNOPRECIPITATION; INHIBITOR OF DIFFERENTIATION PROTEINS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MIDDLE AGED; MUSCLE, SMOOTH, VASCULAR; MUTAGENESIS, SITE-DIRECTED; NEOPLASM PROTEINS; NIH 3T3 CELLS; PHENOTYPE; POLYMORPHISM, SINGLE NUCLEOTIDE; PROTEIN BINDING; RISK ASSESSMENT; RISK FACTORS; TRANSFECTION; TUNICA INTIMA; TUNICA MEDIA;

EID: 77951277633     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.109.210294     Document Type: Article

References (41)

1. Lusis AJ. Atherosclerosis. Nature. 2000;407:233-241.
2. Geng YJ, Libby P. Progression of atheroma: a struggle between death and procreation. Arterioscler Thromb Vasc Biol. 2002;22:1370-1380.
3. Stary HC. Natural history and histological classification of atherosclerotic lesions: an update. Arterioscler Thromb Vasc Biol. 2000;20:1177-1178.
4. Berenson GS, Srinivasan SR, Bao W, Newman WP, III, Tracy RE, Wattigney WA. Association between multiple cardiovascular risk factors and atherosclerosis in children and young adults. The Bogalusa Heart Study. N Engl J Med. 1998;338:1650-1656. (Pubitemid 28267909)
5. Lusis AJ, Mar R, Pajukanta P. Genetics of atherosclerosis. Annu Rev Genomics Hum Genet. 2004;5:189-218. (Pubitemid 39362746)
6. Wang Q, Rao S, Shen GQ, Li L, Moliterno DJ, Newby LK, Rogers WJ, Cannata R, Zirzow E, Elston RC, Topol EJ. Premature myocardial infarction novel susceptibility locus on chromosome 1P34-36 identified by genomewide linkage analysis. Am J Hum Genet. 2004;74:262-271. (Pubitemid 38168614)
7. Welch CL, Bretschger S, Latib N, Bezouevski M, Guo Y, Pleskac N, Liang CP, Barlow C, Dansky H, Breslow JL, Tall AR. Localization of atherosclerosis susceptibility loci to chromosomes 4 and 6 using the Ldlr knockout mouse model. Proc Natl Acad Sci USA. 2001;98:7946-7951. (Pubitemid 32642667)
8. Doran AC, Meller N, Cutchins A, Deliri H, Slayton RP, Oldham SN, Kim JB, Keller SR, McNamara CA. The helix-loop-helix factors Id3 and E47 are novel regulators of adiponectin. Circ Res. 2008;103:624-634.
9. Kumar MS, Hendrix JA, Johnson AD, Owens GK. Smooth muscle alpha-actin gene requires two E-boxes for proper expression in vivo and is a target of class I basic helix-loop-helix proteins. Circ Res. 2003;92: 840-847.
10. Murre C. Helix-loop-helix proteins and lymphocyte development. Nat Immunol. 2005;6:1079-1086. (Pubitemid 41541785)
11. Forrest ST, Barringhaus KG, Perlegas D, Hammarskjold ML, McNamara CA. Intron retention generates a novel Id3 isoform that inhibits vascular lesion formation. J Biol Chem. 2004;279:32897-32903. (Pubitemid 39014749)
12. Matsumura ME, Li F, Berthoux L, Wei B, Lobe DR, Jeon C, Hammar-skjold ML, McNamara CA. Vascular injury induces posttranscriptional regulation of the Id3 gene: cloning of a novel Id3 isoform expressed during vascular lesion formation in rat and human atherosclerosis. Arte-rioscler Thromb Vasc Biol. 2001;21:752-758. (Pubitemid 32448764)
13. Taylor AM, Li F, Thimmalapura P, Gerrity RG, Sarembock IJ, Forrest S, Rutherford S, McNamara CA. Hyperlipemia and oxidation of LDL induce vascular smooth muscle cell growth: an effect mediated by the HLH factor Id3. J Vasc Res. 2006;43:123-130. (Pubitemid 43247993)
14. Matsumura ME, Lobe DR, McNamara CA. Contribution of the helix-loop-helix factor Id2 to regulation of vascular smooth muscle cell proliferation. J Biol Chem. 2002;277:7293-7297. (Pubitemid 34953123)
15. Mueller C, Baudler S, Welzel H, Bohm M, Nickenig G. Identification of a novel redox-sensitive gene, Id3, which mediates angiotensin II-induced cell growth. Circulation. 2002;105:2423-2428. (Pubitemid 34556396)
16. Nickenig G, Baudler S, Muller C, Werner C, Werner N, Welzel H, Strehlow K, Bohm M. Redox-sensitive vascular smooth muscle cell proliferation is mediated by GKLF and Id3 in vitro and in vivo. FASEB J. 2002;16: 1077-1086. (Pubitemid 34753514)
17. Kuhel DG, Zhu B, Witte DP, Hui DY. Distinction in genetic determinants for injury-induced neointimal hyperplasia and diet-induced atherosclerosis in inbred mice. Arterioscler Thromb Vasc Biol. 2002;22:955-960. (Pubitemid 34655223)
18. Orford JL, Selwyn AP, Ganz P, Popma JJ, Rogers C. The comparative pathobiology of atherosclerosis and restenosis. Am J Cardiol. 2000;86: 6H-11H.
19. Bowden DW, Rudock M, Ziegler J, Lehtinen AB, Xu J, Wagenknecht LE, Herrington D, Rich SS, Freedman BI, Carr JJ, Langefeld CD. Coincident linkage of type 2 diabetes, metabolic syndrome, and measures of cardiovascular disease in a genome scan of the diabetes heart study. Diabetes. 2006;55:1985-1994. (Pubitemid 44509971)
20. Lange LA, Bowden DW, Langefeld CD, Wagenknecht LE, Carr JJ, Rich SS, Riley WA, Freedman BI. Heritability of carotid artery intima-medial thickness in type 2 diabetes. Stroke. 2002;33:1876-1881. (Pubitemid 34761079)
21. Barrett JC, Fry B, Maller J, Daly MJ. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics. 2005;21:263-265. (Pubitemid 40202029)
22. Chen B, Han BH, Sun XH, Lim RW. Inhibition of muscle-specific gene expression by Id3: requirement of the C-terminal region of the protein for stable expression and function. Nucleic Acids Res. 1997;25:423-430. (Pubitemid 27303338)
23. Jung F, Johnson AD, Kumar MS, Wei B, Hautmann M, Owens GK, McNamara C. Characterization of an E-box-dependent cis element in the smooth muscle alpha-actin promoter. Arterioscler Thromb Vasc Biol. 1999;19:2591-2599. (Pubitemid 29536032)
24. O'Leary DH, Polak JF, Kronmal RA, Manolio TA, Burke GL, Wolfson SK Jr. Carotid-artery intima and media thickness as a risk factor for myocardial infarction and stroke in older adults. Cardiovascular Health Study Collaborative Research Group. N Engl J Med. 1999;340:14-22. (Pubitemid 29024679)
25. Persson J, Stavenow L, Wikstrand J, Israelsson B, Formgren J, Berglund G. Noninvasive quantification of atherosclerotic lesions. Reproducibility of ultrasonographic measurement of arterial wall thickness and plaque size. Arterioscler Thromb. 1992;12:261-266.
26. Hodis HN, Mack WJ, LaBree L, Selzer RH, Liu CR, Liu CH, Azen SP. The role of carotid arterial intima-media thickness in predicting clinical coronary events. Ann Intern Med. 1998;128:262-269.
27. Lorenz MW, von Kegler S, Steinmetz H, Markus HS, Sitzer M. Carotid intima-media thickening indicates a higher vascular risk across a wide age range: prospective data from the Carotid Atherosclerosis Progression Study (CAPS). Stroke. 2006;37:87-92. (Pubitemid 43732053)
28. Deed RW, Jasiok M, Norton JD. Attenuated function of a variant form of the helix-loop-helix protein, Id-3, generated by an alternative splicing mechanism. FEBS Lett. 1996;393:113-116. (Pubitemid 26298242)
29. Norton JD. ID helix-loop-helix proteins in cell growth, differentiation and tumorigenesis. J Cell Sci. 2000;113(Pt 22):3897-3905. (Pubitemid 32194515)
30. Szalai AJ, Wu J, Lange EM, McCrory MA, Langefeld CD, Williams A, Zakharkin SO, George V, Allison DB, Cooper GS, Xie F, Fan Z, Edberg JC, Kimberly RP. Single-nucleotide polymorphisms in the C-reactive protein (CRP) gene promoter that affect transcription factor binding, alter transcriptional activity, and associate with differences in baseline serum CRP level. J Mol Med. 2005;83:440-447. (Pubitemid 40922166)
31. Salero E, Gimenez C, Zafra F. Identification of a non-canonical E-box motif as a regulatory element in the proximal promoter region of the apolipoprotein E gene. Biochem J. 2003;370:979-986. (Pubitemid 36399091)
32. Horton JD, Goldstein JL, Brown MS. SREBPs: activators of the complete program of cholesterol and fatty acid synthesis in the liver. J Clin Invest. 2002;109:1125-1131.
33. Forrest ST, Taylor AM, Sarembock IJ, Perlegas D, McNamara CA. Phosphorylation regulates Id3 function in vascular smooth muscle cells. Circ Res. 2004;95:557-559. (Pubitemid 39274369)
34. Providence KM, White LA, Tang J, Gonclaves J, Staiano-Coico L, Higgins PJ. Epithelial monolayer wounding stimulates binding of USF-1 to an E-box motif in the plasminogen activator inhibitor type 1 gene. J Cell Sci. 2002;115:3767-3777. (Pubitemid 35203603)
35. Moldes M, Boizard M, Liepvre XL, Feve B, Dugail I, Pairault J. Functional antagonism between inhibitor of DNA binding (Id) and adipocyte determination and differentiation factor 1/sterol regulatory element-binding protein-1c (ADD1/SREBP-1c) trans-factors for the regulation of fatty acid synthase promoter in adipocytes. Biochem J. 1999;344(Pt 3):873-880. (Pubitemid 30032537)
36. Towle HC, Kaytor EN, Shih HM. Regulation of the expression of lipogenic enzyme genes by carbohydrate. Annu Rev Nutr. 1997;17: 405-433. (Pubitemid 27328807)
37. Naya FJ, Stellrecht CM, Tsai MJ. Tissue-specific regulation of the insulin gene by a novel basic helix-loop-helix transcription factor. Genes Dev. 1995;9:1009-1019.
38. Eberle D, Hegarty B, Bossard P, Ferre P, Foufelle F. SREBP transcription factors: master regulators of lipid homeostasis. Biochimie. 2004;86: 839-848. (Pubitemid 39602764)
39. Rothenberg EV, Taghon T. Molecular genetics of T cell development. Annu Rev Immunol. 2005;23:601-649. (Pubitemid 40563181)
40. Sugai M, Gonda H, Nambu Y, Yokota Y, Shimizu A. Role of Id proteins in B lymphocyte activation: new insights from knockout mouse studies. J Mol Med. 2004;82:592-599. (Pubitemid 39312664)
41. Benezra R, Rafii S, Lyden D. The Id proteins and angiogenesis. Oncogene. 2001;20:8334-8341. (Pubitemid 34121904)