Regulation of human CETP gene expression: Role of SP1 and SP3 transcription factors at promoter sites -690, -629, and -37

Journal of Lipid Research

Volumn 44, Issue 7, 2003, Pages 1322-1331

  Le Goff, Wilfried ^a   Guerin, Maryse ^a   Petit, Laure ^a   Chapman, M John ^a   Thillet, Joëlle ^a  

^a PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

Author keywords

Atherosclerosis; Reverse cholesterol transport; Transcriptional repression

Indexed keywords

CHOLESTEROL ESTER TRANSFER PROTEIN; LUCIFERASE; TRANSCRIPTION FACTOR SP1; TRANSCRIPTION FACTOR SP3;

ANIMAL CELL; ARTICLE; ATHEROGENESIS; BINDING SITE; CHOLESTEROL TRANSPORT; DYSLIPIDEMIA; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE REPRESSION; HUMAN; HUMAN CELL; INSECT CELL; LIVER CELL CARCINOMA; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; SITE DIRECTED MUTAGENESIS;

ANIMALS; BINDING SITES; BLOTTING, WESTERN; CARRIER PROTEINS; CELL LINE; CHOLESTEROL ESTER TRANSFER PROTEINS; DEOXYRIBONUCLEASE I; DEOXYRIBONUCLEASES; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; GLYCOPROTEINS; HUMANS; INSECTS; LUCIFERASES; MODELS, GENETIC; MUTAGENESIS, SITE-DIRECTED; PHENOTYPE; PLASMIDS; PROMOTER REGIONS (GENETICS); SP1 TRANSCRIPTION FACTOR; SP3 TRANSCRIPTION FACTOR; TRANSCRIPTION FACTORS; TRANSFECTION;

EID: 0142042381     PISSN: 00222275     EISSN: None     Source Type: Journal    
DOI: 10.1194/jlr.M200425-JLR200     Document Type: Article

References (63)

1. Yamashita, S., K. Hirano, N. Sakai, and Y. Matsuzawa. 2000. Molecular biology and pathophysiological aspects of plasma cholesteryl ester transfer protein. Biochim. Biophys. Acta. 1529(1-3): 257-275.
2. Marotti, K. R., C. K. Castle, T. P. Boyle, A. H. Lin, R. W. Murray, and G. W. Melchior. 1993. Severe atherosclerosis in transgenic mice expressing simian cholesteryl ester transfer protein. Nature. 364: 73-75.
3. Zhong, S., D. S. Sharp, J. S. Grove, C. Bruce, K. Yano, J. D. Curb, and A. R. Tall. 1996. Increased coronary heart disease in Japanese-American men with mutation in the cholesteryl ester transfer protein gene despite increased HDL levels. J. Clin. Invest. 97: 2917-2923.
4. Tato, F., G. L. Vega, A. R. Tall, and S. M. Grundy. 1995. Relation between cholesterol ester transfer protein activities and lipoprotein cholesterol in patients with hypercholesterolemia and combined hyperlipidemia. Arterioscler. Thromb. Vasc. Biol. 15: 112-120.
5. McPherson, R., C. J. Mann, A. R. Tall, M. Hogue, L. Martin, R. W. Milne, and Y. L. Marcel. 1991. Plasma concentrations of cholesteryl ester transfer protein in hyperlipoproteinemia. Relation to cholesteryl ester transfer protein activity and other lipoprotein variables. Arterioscler. Thromb. 11: 797-804.
6. Guerin, M., P. J. Dolphin, and M. J. Chapman, 1994. Preferential cholesteryl ester acceptors among the LDL subspecies of subjects with familial hypercholesterolemia. Arterioscler. Thromb. 14: 679-685.
7. de Grooth, G. J., J. A. Kuivenhoven, A. F. Stalenhoef, J. de Graaf, A. H. Zwinderman, J. L. Posma, A. van Tol, and J. J. Kastelein. 2002. Efficacy and safety of a novel cholesteryl ester transfer protein inhibitor, JTT-705, in humans: a randomized phase II dose-response study. Circulation. 105: 2159-2165.
8. Okamoto, H., F. Yonemori, K. Wakitani, T. Minowa, K. Maeda, and H. Shinkai. 2000. A cholesteryl ester transfer protein inhibitor attenuates atherosclerosis in rabbits. Nature. 406: 203-207.
9. McPherson, R., S. M. Grundy, R. Guerra, and J. C. Cohen. 1996. Allelic variation in the gene encoding the cholesteryl ester transfer protein is associated with variation in the plasma concentrations of cholesteryl ester transfer protein. J. Lipid Res. 37: 1743-1748.
10. Radeau, T., M. Robb, P. Lau, J. Borthwick, and R. McPherson, 1998. Relationship of adipose tissue cholesteryl ester transfer protein (CETP) mRNA to plasma concentrations of CETP in man. Atherosclerosis, 139: 369-376.
11. Jiang, X. C., L. B. Agellon, A. Walsh, J. L. Breslow, and A. Tall. 1992. Dietary cholesterol increases transcription of the human cholesteryl ester transfer protein gene in transgenic mice. Dependence on natural flanking sequences. J. Clin. Invest. 90: 1290-1295.
12. Hirano, R., O. Igarashi, K. Kondo, H. Itakura, and A. Matsumoto. 2001. Regulation by long-chain fatty acids of the expression of cholesteryl ester transfer protein in HepG2 cells. Lipids. 36: 401-406.
13. Chang, C. K., and J. T. Snook. 2001. The cholesterolaemic effects of dietary fats in cholesteryl ester transfer protein transgenic mice. Br. J. Nutr. 85: 643-648.
14. Masucci-Magoulas, L., P. Moulin, X. C. Jiang, H. Richardson, A. Walsh, J. L. Breslow, and A. Tall. 1995. Decreased cholesteryl ester transfer protein (CETP) mRNA and protein and increased high density lipoprotein following lipopolysaccharide administration in human CETP transgenic mice. J. Clin. Invest. 95: 1587-1594.
15. Agellon, L. B., P. Zhang, X. C. Jiang, L. Mendelsohn, and A. R. Tall. 1992. The CCAAT/enhancer-binding protein trans-activates the human cholesteryl ester transfer protein gene promoter. J. Biol. Chem. 267: 22336-22339.
16. Chouinard, R. A., Jr., Y. Luo, T. F. Osborne, A. Walsh, and A. R. Tall. 1998. Sterol regulatory element binding protein-1 activates the cholesteryl ester transfer protein gene in vivo but is not required for sterol up-regulation of gene expression. J. Biol. Chem. 273: 22409-22414.
17. Dachet, C., O. Poirier, F. Cambien, J. Chapman, and M. Rouis. 2000. New functional promoter polymorphism, CETP/-629, in cholesteryl ester transfer protein (CETP) gene related to CETP mass and high density lipoprotein cholesterol levels: role of Sp1/Sp3 in transcriptional regulation. Arterioscler. Thromb. Vasc. Biol. 20: 507-515.
18. Gaudet, F., and G. S. Ginsburg. 1995. Transcriptional regulation of the cholesteryl ester transfer protein gene by the orphan nuclear hormone receptor apolipoprotein AI regulatory protein-1. J. Biol. Chem. 270: 29916-29922.
19. Gauthier, B., M. Robb, F. Gaudet, G. S. Ginsburg, and R. McPherson. 1999. Characterization of a cholesterol response element (CRE) in the promoter of the cholesteryl ester transfer protein gene: functional role of the transcription factors SREBP-1a, -2, and YY1. J. Lipid Res. 40: 1284-1293.
20. Jeoung, N. H., W. G. Jang, J. I. Nam, Y. K. Pak, and Y. B. Park. 1999. Identification of retinoic acid receptor element in human cholesteryl ester transfer protein gene. Biochem. Biophys. Res. Commun. 258: 411-415.
21. Luo, Y., and A. R. Tall. 2000. Sterol upregulation of human CETP expression in vitro and in transgenic mice by an LXR element. J. Clin. Invest. 105: 513-520.
22. Luo, Y., C. P. Liang, and A. R. Tall. 2001. The orphan nuclear receptor LRH-1 potentiates the sterol-mediated induction of the human CETP gene by LXR. J. Biol. Chem. 276: 24767-24773.
23. Quinet, E. M., L. B. Agellon, P. A. Kroon, Y. L. Marcel, Y. C. Lee, M. E. Whitlock, and A. R. Tall. 1990. Atherogenic diet increases cholesteryl ester transfer protein messenger RNA levels in rabbit liver. J. Clin. Invest. 85: 357-363.
24. Oliveira, H. C. F., R. A. Chouinard, L. B. Agellon, C. Bruce, L. Ma, A. Walsh, J. L. Breslow, and A. R. Tall. 1996. Human cholesteryl ester transfer protein gene proximal promoter contains dietary cholesterol positive responsive elements and mediates expression in small intestine and periphery while predominant liver and spleen expression is controlled by 5′-distal sequences. Cis-acting sequences mapped in transgenic mice. J. Biol. Chem. 271: 31831-31838.
25. Suske, G. 1999. The Sp-family of transcription factors. Gene. 238: 291-300.
26. Rajakumar, R. A., S. Thamotharan, R. K. Menon, and S. U. Devaskar. 1998. Sp1 and Sp3 regulate transcriptional activity of the facilitative glucose transporter isoform-3 gene in mammalian neuroblasts and trophoblasts. J. Biol. Chem. 273: 27474-27483.
27. Campos-Caro, A., C. Carrasco-Serrano, L. M. Valor, S. Viniegra, J. J. Ballesta, and M. Criado. 1999. Multiple functional Sp1 domains in the minimal promoter region of the neuronal nicotinic receptor alpha5 subunit gene. J. Biol. Chem. 274: 4693-4701.
28. Baker, D. L., V. Dave, T. Reed, and M. Periasamy. 1996. Multiple Sp1 binding sites in the cardiac/slow twitch muscle sarcoplasmic reticulum Ca2+-ATPase gene promoter are required for expression in So18 muscle cells. J. Biol. Chem. 271: 5921-5928.
29. Feng, X., S. L. Teitelbaum, M. E. Quiroz, S. L. Cheng, C. F. Lai, L. V. Avioli, and F. P. Ross. 2000. Sp1/Sp3 and PU.1 differentially regulate beta(5) integrin gene expression in macrophages and osteoblasts. J. Biol. Chem. 275: 8331-8340.
30. Li, N., S. Seetharam, and B. Seetharam. 1998. Characterization of the human transcobalamin II promoter. A proximal GC/GT box is a dominant negative element. J. Biol. Chem. 273: 16104-16111.
31. Dignam, J. D., R. M. Lebovitz, and R. G. Roeder. 1983. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11: 1475-1489.
32. Di Nocera, P. P., and I. B. Dawid. 1983. Transient expression of genes introduced into cultured cells of Drosophila. Proc. Natl. Acad. Sci. USA. 80: 7095-7098.
33. Lee, J. S., K. M. Galvin, and Y. Shi. 1993. Evidence for physical interaction between the zinc-finger transcription factors YY1 and Sp1. Proc. Natl. Acad. Sci. USA. 90: 6145-6149.
34. Turner, J., and M. Crossley. 1999. Mammalian Kruppel-like transcription factors: more than just a pretty finger. Trends Biochem. Sci. 24: 236-240.
35. Swenson, T. L., J. S. Simmons, C. B. Hesler, C. Bisgaier, and A. R. Tall. 1987. Cholesteryl ester transfer protein is secreted by Hep G2 cells and contains asparagine-linked carbohydrate and sialic acid. J. Biol. Chem. 262: 16271-16274.
36. Faust, R. A., and J. J. Albers. 1987. Synthesis and secretion of plasma cholesteryl ester transfer protein by human hepatocarcinoma cell line, HepG2. Arteriosclerosis. 7: 267-275.
37. Courey, A. J., and R. Tjian. 1988. Analysis of Sp1 in vivo reveals multiple transcriptional domains, including a novel glutamine-rich activation motif. Cell. 55: 887-898.
38. Majello, B., P. De Luca, and L. Lania. 1997. Sp3 is a bifunctional transcription regulator with modular independent activation and repression domains. J. Biol. Chem. 272: 4021-4026.
39. Datta, P. K., P. Raychaudhuri, and S. Bagchi. 1995. Association of p107 with Sp1: genetically separable regions of p107 are involved in regulation of E2F- and Sp1-dependent transcription. Mol. Cell. Biol. 15: 5444-5452.
40. Merika, M., and S. H. Orkin. 1995. Functional synergy and physical interactions of the erythroid transcription factor GATA-1 with the Kruppel family proteins Sp1 and EKLF. Mol. Cell. Biol. 15: 2437-2447.
41. Roder, K., S. S. Wolf, K. J. Larkin, and M. Schweizer. 1999. Interaction between the two ubiquitously expressed transcription factors NF-Y and Sp1. Gene. 234: 61-69.
42. Udvadia, A. J., K. T. Rogers, P. D. Higgins, Y. Murata, K. H. Martin, P. A. Humphrey, and J. M. Horowitz. 1993. Sp-1 binds promoter elements regulated by the RB protein and Sp-1-mediated transcription is stimulated by RB coexpression. Proc. Natl. Acad. Sci. USA. 90: 3265-3269.
43. Majello, B., P. De Luca, G. Hagen, G. Suske, and L. Lania. 1994. Different members of the Sp1 multigene family exert opposite transcriptional regulation of the long terminal repeat of HIV-1. Nucleic Acids Res. 22: 4914-4921.
44. Liang, Y., D. F. Robinson, J. Dennig, G. Suske, and W. E. Fahl. 1996. Transcriptional regulation of the SIS/PDGF-B gene in human osteosarcoma cells by the Sp family of transcription factors. J. Biol. Chem. 271: 11792-11797.
45. Hagen, G., J. Dennig, A. Preiss, M. Beato, and G. Suske. 1995. Functional analyses of the transcription factor Sp4 reveal properties distinct from Sp1 and Sp3. J. Biol. Chem. 270: 24989-24994.
46. Pascal, E., and R. Tjian. 1991. Different activation domains of Sp1 govern formation of multimers and mediate transcriptional synergism. Genes Dev. 5: 1646-1656.
47. Biggs, J. R., J. E. Kudlow, and A. S. Kraft. 1996. The role of the transcription factor Sp1 in regulating the expression of the WAF1/CIP1 gene in U937 leukemic cells. J. Biol. Chem. 271: 901-906.
48. Prowse, D. M., L. Bolgan, A. Molnar, and G. P. Dotto. 1997. Involvement of the Sp3 transcription factor in induction of p21Cip1/WAF1 in keratinocyte differentiation. J. Biol. Chem. 272: 1308-1314.
49. Udvadia, A. J., D. J. Templeton, and J. M. Horowitz. 1995. Functional interactions between the retinoblastoma (Rb) protein and Sp-family members: superactivation by Rb requires amino acids necessary for growth suppression. Proc. Natl. Acad. Sci. USA. 92: 3953-3957.
50. Hagen, G., S. Muller, M. Beato, and G. Suske. 1994. Sp1-mediated transcriptional activation is repressed by Sp3. EMBO J. 13: 3843-3851.
51. Wildhage, I., H. Trusheim, B. Goke, and B. Lankat-Buttgereit. 1999. Gene expression of the human glucagon-like peptide-1 receptor is regulated by Sp1 and Sp3. Endocrinology. 140: 624-631.
52. Kingsley, C., and A. Winoto. 1992. Cloning of GT box-binding proteins: a novel Sp1 multigene family regulating T-cell receptor gene expression. Mol. Cell. Biol. 12: 4251-4261.
53. Hagen, G., S. Muller, M. Beato, and G. Suske. 1992. Cloning by recognition site screening of two novel GT box binding proteins: a family of Sp1 related genes. Nucleic Acids Res. 20: 5519-5525.
54. Saffer, J. D., S. P. Jackson, and M. B. Annarella. 1991. Developmental expression of Sp1 in the mouse. Mol. Cell. Biol. 11: 2189-2199.
55. Hata, Y., E. Duh, K. Zhang, G. S. Robinson, and L. P. Aiello. 1998. Transcription factors Sp1 and Sp3 alter vascular endothelial growth factor receptor expression through a novel recognition sequence. J. Biol. Chem. 273: 19294-19303.
56. Cook, T., B. Gebelein, K. Mesa, A. Mladek, and R. Urrutia. 1998. Molecular cloning and characterization of TIEG2 reveals a new subfamily of transforming growth factor-beta-inducible Sp1-like zinc finger-encoding genes involved in the regulation of cell growth. J. Biol. Chem. 273: 25929-25936.
57. Kaczynski, J., J. S. Zhang, V. Ellenrieder, A. Conley, T. Duenes, H. Kester, B. van Der Burg, and R. Urrutia. 2001. The Sp1-like protein BTEB3 inhibits transcription via the basic transcription element box by interacting with mSin3A and HDAC-1 co-repressors and competing with Sp1. J. Biol. Chem. 276: 36749-36756.
58. van Vliet, J., J. Turner, and M. Crossley. 2000. Human Kruppel-like factor 8: a CACCC-box binding protein that associates with CtBP and represses transcription. Nucleic Acids Res. 28: 1955-1962.
59. Shie, J. L., Z. Y. Chen, M. Fu, R. G. Pestell, and C. C. Tseng. 2000. Gut-enriched Kruppel-like factor represses cyclin D1 promoter activity through Sp1 motif. Nucleic Acids Res. 28: 2969-2976.
60. Jackson, S. P., J. J. MacDonald, S. Lees-Miller, and R. Tjian. 1990. GC box binding induces phosphorylation of Sp1 by a DNA-dependent protein kinase. Cell. 63: 155-165.
61. Braun, H., R. Koop, A. Ertmer, S. Nacht, and G. Suske. 2001. Transcription factor Sp3 is regulated by acetylation. Nucleic Acids Res. 29: 4994-5000.
62. Denson, L. A., R. K. Menon, A. Shaufl, H. S. Bajwa, C. R. Williams, and S. J. Karpen. 2001. TNF-alpha downregulates murine hepatic growth hormone receptor expression by inhibiting Sp1 and Sp3 binding. J. Clin. Invest. 107: 1451-1458.
63. Berendji-Grun, D., V. Kolb-Bachofen, and K. D. Kroncke. 2001. Nitric oxide inhibits endothelial IL-1 [beta]-induced ICAM-1 gene expression at the transcriptional level decreasing Sp1 and AP-1 activity. Mol. Med. 7: 748-754.