Upstream Stimulatory Factors 1 and 2 activate the human hepatic lipase promoter via E-box dependent and independent mechanisms

Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids

Volumn 1791, Issue 4, 2009, Pages 229-237

  van Deursen, Diederik ^a   van Leeuwen, Marije ^a   Vaulont, Sophie ^b   Jansen, Hans ^a   Verhoeven, Adrie J M ^a  

^a ERASMUS UNIVERSITY ROTTERDAM   (Netherlands)

^b INSTITUT COCHIN   (France)

Author keywords

Hepatic lipase; LIPC; Promoter polymorphism; Transcriptional regulation; Upstream Stimulatory Factor 1; Upstream Stimulatory Factor 2

Indexed keywords

LIVER TRIACYLGLYCEROL LIPASE; UPSTREAM STIMULATORY FACTOR 1; UPSTREAM STIMULATORY FACTOR 2;

ANIMAL CELL; ARTICLE; CELL STRAIN COS1; CELL STRAIN HEPG2; E BOX ELEMENT; GENE CONTROL; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; RNA INTERFERENCE; TATA BOX; TRANSCRIPTION REGULATION;

ANIMALS; CARCINOMA, HEPATOCELLULAR; CERCOPITHECUS AETHIOPS; CHROMATIN IMMUNOPRECIPITATION; COS CELLS; E-BOX ELEMENTS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; LIPASE; LIVER NEOPLASMS; PROMOTER REGIONS, GENETIC; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING; TUMOR CELLS, CULTURED; UPSTREAM STIMULATORY FACTORS;

EID: 62249208013     PISSN: 13881981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbalip.2009.01.017     Document Type: Article

References (50)

1. Perret B., Mabile L., Martinez L., Terce F., Barbaras R., and Collet X. Hepatic lipase: structure/function relationship, synthesis, and regulation. J. Lipid Res. 43 (2002) 1163-1169
2. Santamarina-Fojo S., Gonzalez-Navarro H., Freeman L., Wagner E., and Nong Z. Hepatic lipase, lipoprotein metabolism, and atherogenesis. Arterioscler. Thromb. Vasc. Biol. 24 (2004) 1750-1754
3. Jansen H., Verhoeven A.J., and Sijbrands E.J. Hepatic lipase: a pro- or anti-atherogenic protein?. J. Lipid Res. 43 (2002) 1352-1362
4. Zambon A., Hokanson J.E., Brown B.G., and Brunzell J.D. Evidence for a new pathophysiological mechanism for coronary artery disease regression: hepatic lipase-mediated changes in LDL density. Circulation 99 (1999) 1959-1964
5. Carr M.C., Hokanson J.E., Deeb S.S., Purnell J.Q., Mitchell E.S., and Brunzell J.D. A hepatic lipase gene promoter polymorphism attenuates the increase in hepatic lipase activity with increasing intra-abdominal fat in women. Arterioscler. Thromb. Vasc. Biol. 19 (1999) 2701-2707
6. Tan K.C., Shiu S.W., and Chu B.Y. Effects of gender, hepatic lipase gene polymorphism and type 2 diabetes mellitus on hepatic lipase activity in Chinese. Atherosclerosis 157 (2001) 233-239
7. Berk-Planken I.I., Hoogerbrugge N., Stolk R.P., Bootsma A.H., and Jansen H. Atorvastatin dose-dependently decreases hepatic lipase activity in type 2 diabetes: effect of sex and the LIPC promoter variant. Diabetes Care 26 (2003) 427-432
8. Allayee H., Dominguez K.M., Aouizerat B.E., Krauss R.M., Rotter J.I., Lu J., Cantor R.M., de Bruin T.W., and Lusis A.J. Contribution of the hepatic lipase gene to the atherogenic lipoprotein phenotype in familial combined hyperlipidemia. J. Lipid Res. 41 (2000) 245-252
9. Deeb S.S., Zambon A., Carr M.C., Ayyobi A.F., and Brunzell J.D. Hepatic lipase and dyslipidemia: interactions among genetic variants, obesity, gender, and diet. J. Lipid Res. 44 (2003) 1279-1286
10. Pihlajamaki J., Karjalainen L., Karhapaa P., Vauhkonen I., Taskinen M.R., Deeb S.S., and Laakso M. G-250A substitution in promoter of hepatic lipase gene is associated with dyslipidemia and insulin resistance in healthy control subjects and in members of families with familial combined hyperlipidemia. Arterioscler. Thromb. Vasc. Biol. 20 (2000) 1789-1795
11. Nimmo L., McColl A.J., Rosankiewicz J.Z., Richmond W., and Elkeles R.S. Regulation of hepatic lipase expression in HepG2 cells. Biochem. Soc. Trans. 25 (1997) S689
12. Botma G.J., van Deursen D., Vieira D., van Hoek M., Jansen H., and Verhoeven A.J. Sterol-regulatory-element binding protein inhibits upstream stimulatory factor-stimulated hepatic lipase gene expression. Atherosclerosis 179 (2005) 61-67
13. Tu A.Y., and Albers J.J. Glucose regulates the transcription of human genes relevant to HDL metabolism: responsive elements for peroxisome proliferator-activated receptor are involved in the regulation of phospholipid transfer protein. Diabetes 50 (2001) 1851-1856
14. van Deursen D., Jansen H., and Verhoeven A.J. Glucose increases hepatic lipase expression in HepG2 liver cells through upregulation of upstream stimulatory factors 1 and 2. Diabetologia 51 (2008) 2078-2087
15. Botma G.J., Verhoeven A.J., and Jansen H. Hepatic lipase promoter activity is reduced by the C-480T and G-216A substitutions present in the common LIPC gene variant, and is increased by Upstream Stimulatory Factor. Atherosclerosis 154 (2001) 625-632
16. Corre S., and Galibert M.D. Upstream stimulating factors: highly versatile stress-responsive transcription factors. Pigment Cell Res. 18 (2005) 337-348
17. Wang D., and Sul H.S. Upstream stimulatory factors bind to insulin response sequence of the fatty acid synthase promoter. USF1 is regulated. J. Biol. Chem. 270 (1995) 28716-28722
18. Casado M., Vallet V.S., Kahn A., and Vaulont S. Essential role in vivo of upstream stimulatory factors for a normal dietary response of the fatty acid synthase gene in the liver. J. Biol. Chem. 274 (1999) 2009-2013
19. Ribeiro A., Pastier D., Kardassis D., Chambaz J., and Cardot P. Cooperative binding of upstream stimulatory factor and hepatic nuclear factor 4 drives the transcription of the human apolipoprotein A-II gene. J. Biol. Chem. 274 (1999) 1216-1225
20. Pastier D., Lacorte J.M., Chambaz J., Cardot P., and Ribeiro A. Two initiator-like elements are required for the combined activation of the human apolipoprotein C-III promoter by upstream stimulatory factor and hepatic nuclear factor-4. J. Biol. Chem. 277 (2002) 15199-15206
21. Nowak M., Helleboid-Chapman A., Jakel H., Martin G., Duran-Sandoval D., Staels B., Rubin E.M., Pennacchio L.A., Taskinen M.R., Fruchart-Najib J., and Fruchart J.C. Insulin-mediated down-regulation of apolipoprotein A5 gene expression through the phosphatidylinositol 3-kinase pathway: role of upstream stimulatory factor. Mol. Cell. Biol. 25 (2005) 1537-1548
22. Salero E., Gimenez C., and 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. 370 (2003) 979-986
23. Vallet V.S., Casado M., Henrion A.A., Bucchini D., Raymondjean M., Kahn A., and Vaulont S. Differential roles of upstream stimulatory factors 1 and 2 in the transcriptional response of liver genes to glucose. J. Biol. Chem. 273 (1998) 20175-20179
24. Iynedjian P.B. Identification of upstream stimulatory factor as transcriptional activator of the liver promoter of the glucokinase gene. Biochem. J. 333 Pt 3 (1998) 705-712
25. Portois L., Tastenoy M., Viollet B., and Svoboda M. Functional analysis of the glucose response element of the rat glucagon receptor gene in insulin-producing INS-1 cells. Biochim. Biophys. Acta 1574 (2002) 175-186
26. Matsukawa T., Inoue Y., Oishi Y., Kato H., and Noguchi T. Up-regulation of upstream stimulatory factors by protein malnutrition and its possible role in regulation of the IGF-binding protein-1 gene. Endocrinology 142 (2001) 4643-4651
27. Zeggini E., Damcott C.M., Hanson R.L., Karim M.A., Rayner N.W., Groves C.J., Baier L.J., Hale T.C., Hattersley A.T., Hitman G.A., Hunt S.E., Knowler W.C., Mitchell B.D., Ng M.C., O'Connell J.R., Pollin T.I., Vaxillaire M., Walker M., Wang X., Whittaker P., Xiang K., Jia W., Chan J.C., Froguel P., Deloukas P., Shuldiner A.R., Elbein S.C., and McCarthy M.I. Variation within the gene encoding the upstream stimulatory factor 1 does not influence susceptibility to type 2 diabetes in samples from populations with replicated evidence of linkage to chromosome 1q. Diabetes 55 (2006) 2541-2548
28. Pajukanta P., Lilja H.E., Sinsheimer J.S., Cantor R.M., Lusis A.J., Gentile M., Duan X.J., Soro-Paavonen A., Naukkarinen J., Saarela J., Laakso M., Ehnholm C., Taskinen M.R., and Peltonen L. Familial combined hyperlipidemia is associated with upstream transcription factor 1 (USF1). Nat. Genet. 36 (2004) 371-376
29. Coon H., Xin Y., Hopkins P.N., Cawthon R.M., Hasstedt S.J., and Hunt S.C. Upstream stimulatory factor 1 associated with familial combined hyperlipidemia, LDL cholesterol, and triglycerides. Hum. Genet. 117 (2005) 444-451
30. Isaacs A., Sayed-Tabatabaei F.A., Njajou O.T., Witteman J.C., and van Duijn C.M. The - 514 C->T hepatic lipase promoter region polymorphism and plasma lipids: a meta-analysis. J. Clin. Endocrinol. Metab. 89 (2004) 3858-3863
31. Sambrook J F.E., and Maniatis T. Molecular Cloning: A Laboratory Manual. 2nd Ed. (1989), Cold Spring Harbor Laboratory Press, New York
32. van Deursen D., Botma G.J., Jansen H., and Verhoeven A.J. Comparative genomics and experimental promoter analysis reveal functional liver-specific elements in mammalian hepatic lipase genes. BMC Genomics 8 (2007) 99
33. Ameis D., Stahnke G., Kobayashi J., McLean J., Lee G., Buscher M., Schotz M.C., and Will H. Isolation and characterization of the human hepatic lipase gene. J. Biol. Chem. 265 (1990) 6552-6555
34. Gregor P.D., Sawadogo M., and Roeder R.G. The adenovirus major late transcription factor USF is a member of the helix-loop-helix group of regulatory proteins and binds to DNA as a dimer. Genes. Dev. 4 (1990) 1730-1740
35. Higuchi R., Krummel B., and Saiki R.K. A general method of in vitro preparation and specific mutagenesis of DNA fragments: study of protein and DNA interactions. Nucleic Acids Res. 16 (1988) 7351-7367
36. Schreiber E., Matthias P., Muller M.M., and Schaffner W. Rapid detection of octamer binding proteins with 'mini-extracts', prepared from a small number of cells. Nucleic Acids Res. 17 (1989) 6419
37. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 (1970) 680-685
38. McMurray H.R., and McCance D.J. Human papillomavirus type 16 E6 activates TERT gene transcription through induction of c-Myc and release of USF-mediated repression. J. Virol. 77 (2003) 9852-9861
39. Carthew R.W., Chodosh L.A., and Sharp P.A. An RNA polymerase II transcription factor binds to an upstream element in the adenovirus major late promoter. Cell 43 (1985) 439-448
40. Du H., Roy A.L., and Roeder R.G. Human transcription factor USF stimulates transcription through the initiator elements of the HIV-1 and the Ad-ML promoters. EMBO J. 12 (1993) 501-511
41. Kiermaier A., Gawn J.M., Desbarats L., Saffrich R., Ansorge W., Farrell P.J., Eilers M., and Packham G. DNA binding of USF is required for specific E-box dependent gene activation in vivo. Oncogene 18 (1999) 7200-7211
42. Deeb S.S., and Peng R. The C-514T polymorphism in the human hepatic lipase gene promoter diminishes its activity. J. Lipid Res. 41 (2000) 155-158
43. Bidder M., Shao J.S., Charlton-Kachigian N., Loewy A.P., Semenkovich C.F., and Towler D.A. Osteopontin transcription in aortic vascular smooth muscle cells is controlled by glucose-regulated upstream stimulatory factor and activator protein-1 activities. J. Biol. Chem. 277 (2002) 44485-44496
44. Weigert C., Brodbeck K., Sawadogo M., Haring H.U., and Schleicher E.D. Upstream stimulatory factor (USF) proteins induce human TGF-beta1 gene activation via the glucose-response element - 1013/- 1002 in mesangial cells: up-regulation of USF activity by the hexosamine biosynthetic pathway. J. Biol. Chem. 279 (2004) 15908-15915
45. Wang S., Skorczewski J., Feng X., Mei L., and Murphy-Ullrich J.E. Glucose up-regulates thrombospondin 1 gene transcription and transforming growth factor-beta activity through antagonism of cGMP-dependent protein kinase repression via upstream stimulatory factor 2. J. Biol. Chem. 279 (2004) 34311-34322
46. Shi L., Liu S., Nikolic D., and Wang S. High glucose levels upregulate upstream stimulatory factor 2 gene transcription in mesangial cells. J. Cell. Biochem. 103 (2008) 1952-1961
47. Cheung E., Mayr P., Coda-Zabetta F., Woodman P.G., and Boam D.S. DNA-binding activity of the transcription factor upstream stimulatory factor 1 (USF-1) is regulated by cyclin-dependent phosphorylation. Biochem. J. 344 Pt 1 (1999) 145-152
48. Ng M.C., Miyake K., So W.Y., Poon E.W., Lam V.K., Li J.K., Cox N.J., Bell G.I., and Chan J.C. The linkage and association of the gene encoding upstream stimulatory factor 1 with type 2 diabetes and metabolic syndrome in the Chinese population. Diabetologia 48 (2005) 2018-2024
49. Smih F., Rouet P., Lucas S., Mairal A., Sengenes C., Lafontan M., Vaulont S., Casado M., and Langin D. Transcriptional regulation of adipocyte hormone-sensitive lipase by glucose. Diabetes 51 (2002) 293-300
50. Rufibach L.E., Duncan S.A., Battle M., and Deeb S.S. Transcriptional regulation of the human hepatic lipase (LIPC) gene promoter. J. Lipid Res. 47 (2006) 1463-1477