Regulation of adipocyte 11β-hydroxysteroid dehydrogenase type 1 (11β-hsd1) by CCAAT/enhancer-binding protein (C/EBP) β isoforms, LIP and LAP

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Esteves, Cristina L ^a   Kelly, Val ^a   Bégay, Valérie ^b   Man, Tak Y ^a   Morton, Nicholas M ^a   Leutz, Achim ^b   Seckl, Jonathan R ^a   Chapman, Karen E ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

11BETA HYDROXYSTEROID DEHYDROGENASE 1; CCAAT ENHANCER BINDING PROTEIN BETA; LIVER ENRICHED ACTIVATOR PROTEIN; LIVER ENRICHED INHIBITOR PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN; MESSENGER RNA; RAPAMYCIN; TUNICAMYCIN; UNCLASSIFIED DRUG;

ADIPOCYTE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; DOWN REGULATION; ENDOPLASMIC RETICULUM STRESS; ENZYME REGULATION; LIPID DIET; MALE; MOUSE; NONHUMAN; OBESITY; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SUBCUTANEOUS FAT; TRANSCRIPTION REGULATION; UPREGULATION;

11-BETA-HYDROXYSTEROID DEHYDROGENASE TYPE 1; ADIPOCYTES; ADIPOSE TISSUE; ANIMALS; CCAAT-ENHANCER-BINDING PROTEIN-BETA; CELL LINE; DIET, HIGH-FAT; ENDOPLASMIC RETICULUM STRESS; GENE EXPRESSION REGULATION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PROMOTER REGIONS, GENETIC; PROTEIN ISOFORMS; PROTEIN TRANSPORT; RNA, MESSENGER; TOR SERINE-THREONINE KINASES; TRANSCRIPTION FACTOR CHOP; TUNICAMYCIN;

MUS;

EID: 84861470398     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037953     Document Type: Article

References (44)

1. Seckl JR, Morton NM, Chapman KE, Walker BR, (2004) Glucocorticoids and 11β-hydroxysteroid dehydrogenase in adipose tissue. Recent Prog Horm Res 59: 359-393.
2. Masuzaki H, Paterson J, Shinyama H, Morton NM, Mullins JJ, et al. (2001) A transgenic model of visceral obesity and the metabolic syndrome. Science 294: 2166-2170.
3. Lindsay RS, Wake DJ, Nair S, Bunt J, Livingstone DE, et al. (2003) Subcutaneous adipose 11β-hydroxysteroid dehydrogenase type 1 activity and messenger ribonucleic acid levels are associated with adiposity and insulinemia in Pima Indians and Caucasians. J Clin Endocrinol Metab 88: 2738-2744.
4. Wake DJ, Rask E, Livingstone DE, Soderberg S, Olsson T, et al. (2003) Local and systemic impact of transcriptional up-regulation of 11β-hydroxysteroid dehydrogenase type 1 in adipose tissue in human obesity. J Clin Endocrinol Metab 88: 3983-3988.
5. Masuzaki H, Yamamoto H, Kenyon CJ, Elmquist JK, Morton NM, et al. (2003) Transgenic amplification of glucocorticoid action in adipose tissue causes high blood pressure in mice. J Clin Invest 112: 83-90.
6. Morton NM, Paterson JM, Masuzaki H, Holmes MC, Staels B, et al. (2004) Novel adipose tissue-mediated resistance to diet-induced visceral obesity in 11β-hydroxysteroid dehydrogenase type 1-deficient mice. Diabetes 53: 931-938.
7. Hermanowski-Vosatka A, Balkovec JM, Cheng K, Chen HY, Hernandez M, et al. (2005) 11β-HSD1 inhibition ameliorates metabolic syndrome and prevents progression of atherosclerosis in mice. J Exp Med 202: 517-527.
8. Rosenstock J, Banarer S, Fonseca V, Inzucchi S, Hollis GF, et al. (2010) The 11β-hydroxysteroid dehydrogenase type 1 inhibitor INCB13739 improves hyperglycemia in patients with type 2 diabetes inadequately controlled by metformin monotherapy. Diabetes Care 33: 1516-1522.
9. Morton NM, Ramage L, Seckl JR, (2004) Down-regulation of adipose 11β-hydroxysteroid dehydrogenase type 1 by high-fat feeding in mice: a potential adaptive mechanism counteracting metabolic disease. Endocrinology 145: 2707-2712.
10. Drake AJ, Livingstone DE, Andrew R, Seckl JR, Morton NM, et al. (2005) Reduced adipose glucocorticoid reactivation and increased hepatic glucocorticoid clearance as an early adaptation to high-fat feeding in Wistar rats. Endocrinology 146: 913-919.
11. Man TY, Michailidou Z, Gokcel A, Ramage L, Chapman KE, et al. (2011) Dietary manipulation reveals an unexpected inverse relationship between fat mass and adipose 11β-hydroxysteroid dehydrogenase type 1. Am J Physiol Endocrinol Metab 300: E1076-1084.
12. Williams LJ, Lyons V, MacLeod I, Rajan V, Darlington GJ, et al. (2000) C/EBP regulates hepatic transcription of 11β-hydroxysteroid dehydrogenase type 1. A novel mechanism for cross-talk between the C/EBP and glucocorticoid signaling pathways. J Biol Chem 275: 30232-30239.
13. Gout J, Tirard J, Thevenon C, Riou JP, Begeot M, et al. (2006) CCAAT/enhancer-binding proteins (C/EBPs) regulate the basal and cAMP-induced transcription of the human 11β-hydroxysteroid dehydrogenase encoding gene in adipose cells. Biochimie 88: 1115-1124.
14. Arai N, Masuzaki H, Tanaka T, Ishii T, Yasue S, et al. (2007) Ceramide and adenosine 5′-monophosphate-activated protein kinase are two novel regulators of 11β-hydroxysteroid dehydrogenase type 1 expression and activity in cultured preadipocytes. Endocrinology 148: 5268-5277.
15. Yang Z, Guo C, Zhu P, Li W, Myatt L, et al. (2007) Role of glucocorticoid receptor and CCAAT/enhancer-binding protein α in the feed-forward induction of 11β-hydroxysteroid dehydrogenase type 1 expression by cortisol in human amnion fibroblasts. J Endocrinol 195: 241-253.
16. Sai S, Esteves CL, Kelly V, Michailidou Z, Anderson K, et al. (2008) Glucocorticoid regulation of the promoter of 11β-hydroxysteroid dehydrogenase type 1 is indirect and requires CCAAT/enhancer-binding protein-β. Mol Endocrinol 22: 2049-2060.
17. Cao Z, Umek RM, McKnight SL, (1991) Regulated expression of three C/EBP isoforms during adipose conversion of 3T3-L1 cells. Genes Dev 5: 1538-1552.
18. Wang ND, Finegold MJ, Bradley A, Ou CN, Abdelsayed SV, et al. (1995) Impaired energy homeostasis in C/EBPα knockout mice. Science 269: 1108-1112.
19. Tanaka T, Yoshida N, Kishimoto T, Akira S, (1997) Defective adipocyte differentiation in mice lacking the C/EBPβ and/or C/EBPδ gene. EMBO J 16: 7432-7443.
20. Otto TC, Lane MD, (2005) Adipose development: from stem cell to adipocyte. Crit Rev Biochem Mol Biol 40: 229-242.
21. Ariyama Y, Shimizu H, Satoh T, Tsuchiya T, Okada S, et al. (2007) Chop-deficient mice showed increased adiposity but no glucose intolerance. Obesity 15: 1647-1656.
22. Ossipow V, Descombes P, Schibler U, (1993) CCAAT/enhancer-binding protein mRNA is translated into multiple proteins with different transcription activation potentials. Proc Natl Acad Sci U S A 90: 8219-8223.
23. Welm AL, Timchenko NA, Darlington GJ, (1999) C/EBPα regulates generation of C/EBPβ isoforms through activation of specific proteolytic cleavage. Mol Cell Biol 19: 1695-1704.
24. Calkhoven CF, Muller C, Leutz A, (2000) Translational control of C/EBPα and C/EBPβ isoform expression. Genes Dev 14: 1920-1932.
25. Lin FT, MacDougald OA, Diehl AM, Lane MD, (1993) A 30-kDa alternative translation product of the CCAAT/enhancer binding protein α message: transcriptional activator lacking antimitotic activity. Proc Natl Acad Sci U S A 90: 9606-9610.
26. Duong DT, Waltner-Law ME, Sears R, Sealy L, Granner DK, (2002) Insulin inhibits hepatocellular glucose production by utilizing liver-enriched transcriptional inhibitory protein to disrupt the association of CREB-binding protein and RNA polymerase II with the phosphoenolpyruvate carboxykinase gene promoter. J Biol Chem 277: 32234-32242.
27. Masaki T, Matsuura T, Ohkawa K, Miyamura T, Okazaki I, et al. (2006) All-trans retinoic acid down-regulates human albumin gene expression through the induction of C/EBPβ-LIP. Biochem J 397: 345-353.
28. Siu F, Chen C, Zhong C, Kilberg MS, (2001) CCAAT/enhancer-binding protein-β is a mediator of the nutrient-sensing response pathway that activates the human asparagine synthetase gene. J Biol Chem 276: 48100-48107.
29. Payne VA, Au WS, Gray SL, Nora ED, Rahman SM, et al. (2007) Sequential regulation of diacylglycerol acyltransferase 2 expression by CAAT/enhancer-binding protein β (C/EBPβ) and C/EBPα during adipogenesis. J Biol Chem 282: 21005-21014.
30. Yang Z, Zhu X, Guo C, Sun K, (2009) Stimulation of 11β-HSD1 expression by IL-1β via a C/EBP binding site in human fetal lung fibroblasts. Endocrine 36: 404-411.
31. Smink JJ, Begay V, Schoenmaker T, Sterneck E, de Vries TJ, et al. (2009) Transcription factor C/EBPβ isoform ratio regulates osteoclastogenesis through MafB. EMBO J 28: 1769-1781.
32. Wethmar K, Begay V, Smink JJ, Zaragoza K, Wiesenthal V,et al. C/EBPβ ΔuORF mice-a genetic model for uORF-mediated translational control in mammals. Genes Dev 24: 15-20.
33. Napolitano A, Voice MW, Edwards CR, Seckl JR, Chapman KE, (1998) 11β-hydroxysteroid dehydrogenase 1 in adipocytes: expression is differentiation-dependent and hormonally regulated. J Steroid Biochem Mol Biol 64: 251-260.
34. Ozcan U, Cao Q, Yilmaz E, Lee AH, Iwakoshi NN, et al. (2004) Endoplasmic reticulum stress links obesity, insulin action, and type 2 diabetes. Science 306: 457-461.
35. Li Y, Bevilacqua E, Chiribau CB, Majumder M, Wang C, et al. (2008) Differential control of the CCAAT/enhancer-binding protein β (C/EBPβ) products liver-enriched transcriptional activating protein (LAP) and liver-enriched transcriptional inhibitory protein (LIP) and the regulation of gene expression during the response to endoplasmic reticulum stress. J Biol Chem 283: 22443-22456.
36. Ron D, Habener JF, (1992) CHOP, a novel developmentally regulated nuclear protein that dimerizes with transcription factors C/EBP and LAP and functions as a dominant-negative inhibitor of gene transcription. Genes Dev 6: 439-453.
37. Cucinotta M, Visalli M, Aguennouz M, Valenti A, Loddo S, et al. (2008) Regulation of Interleukin-8 Gene at a Distinct Site of Its Promoter by CCAAT Enhancer-binding Protein Homologous Protein in Prostaglandin E2-treated Human T Cells. J Biol Chem 283: 29760-29769.
38. Lee ES, Yoon CH, Kim YS, Bae YS, (2007) The double-strand RNA-dependent protein kinase PKR plays a significant role in a sustained ER stress-induced apoptosis. FEBS Lett 581: 4325-4332.
39. Gregor MF, Hotamisligil GS, (2007) Thematic review series: Adipocyte Biology. Adipocyte stress: the endoplasmic reticulum and metabolic disease. J Lipid Res 48: 1905-1914.
40. Arizmendi C, Liu S, Croniger C, Poli V, Friedman JE, (1999) The transcription factor CCAAT/enhancer-binding protein β regulates gluconeogenesis and phosphoenolpyruvate carboxykinase (GTP) gene transcription during diabetes. J Biol Chem 274: 13033-13040.
41. Liu S, Croniger C, Arizmendi C, Harada-Shiba M, Ren J, et al. (1999) Hypoglycemia and impaired hepatic glucose production in mice with a deletion of the C/EBPβ gene. J Clin Invest 103: 207-213.
42. Millward CA, Heaney JD, Sinasac DS, Chu EC, Bederman IR, et al. (2007) Mice with a deletion in the gene for CCAAT/enhancer-binding protein β are protected against diet-induced obesity. Diabetes 56: 161-167.
43. Rahman SM, Schroeder-Gloeckler JM, Janssen RC, Jiang H, Qadri I, et al. (2007) CCAAT/enhancing binding protein β deletion in mice attenuates inflammation, endoplasmic reticulum stress, and lipid accumulation in diet-induced nonalcoholic steatohepatitis. Hepatology 45: 1108-1117.
44. Christy RJ, Kaestner KH, Geiman DE, Lane MD, (1991) CCAAT/enhancer binding protein gene promoter: binding of nuclear factors during differentiation of 3T3-L1 preadipocytes. Proc Natl Acad Sci U S A 88: 2593-2597.