Stimulation of fat accumulation in hepatocytes by PGE2-dependent repression of hepatic lipolysis,β-oxidation and VLDL-synthesis

Laboratory Investigation

Volumn 92, Issue 11, 2012, Pages 1597-1606

  Henkel, Janin ^a   Frede, Katja ^a   Schanze, Nancy ^a   Vogel, Heike ^b   Schürmann, Annette ^b   Spruss, Astrid ^c   Bergheim, Ina ^c   Püschel, Gerhard P ^a  

^a UNIVERSITY OF POTSDAM   (Germany)

^b GERMAN INSTITUTE OF HUMAN NUTRITION   (Germany)

^c UNIVERSITY OF HOHENHEIM   (Germany)

Author keywords

cyclooxygenase; hepatic steatosis; mPGES; NAFLD; NASH; PGC1 ; type 2 diabetes (T2DM)

Indexed keywords

ACETOACETIC ACID; CARBON 14; CYCLOOXYGENASE 2; FAT DROPLET; FATTY ACID SYNTHASE; GLUCOKINASE; GLUCOSE; INSULIN; PROSTAGLANDIN E SYNTHASE 1; PROSTAGLANDIN E2; PROSTANOID; PROTEIN KINASE B; STEROL REGULATORY ELEMENT BINDING PROTEIN 1C; TRANSCRIPTION FACTOR FKHR; TRIACYLGLYCEROL; VERY LOW DENSITY LIPOPROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME REPRESSION; FATTY ACID OXIDATION; FATTY ACID SYNTHESIS; FATTY LIVER; LEPTIN DEFICIENCY; LIPID STORAGE; LIPOLYSIS; LIPOPROTEIN SECRETION; LIPOPROTEIN SYNTHESIS; LIVER CELL; MALE; METABOLIC INHIBITION; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; TRANSCRIPTION INITIATION;

EID: 84868561019     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2012.128     Document Type: Article

References (52)

1. Dowman JK, Tomlinson JW, Newsome PN. Pathogenesis of nonalcoholic fatty liver disease. Qjm 2010;103:71-83.
2. Fabbrini E, Sullivan S, Klein S. Obesity and nonalcoholic fatty liver disease: biochemical, metabolic, and clinical implications. Hepatology 2010;51:679-689.
3. Tiniakos DG, Vos MB, Brunt EM. Nonalcoholic fatty liver disease: pathology and pathogenesis. Annu Rev Pathol 2010;5:145-171.
4. Kmiec Z. Cooperation of liver cells in health and disease. Adv Anat Embryol Cell Biol 2001). 161III-XIII, 1-151.
5. Sampey AV, Monrad S, Crofford LJ. Microsomal prostaglandin E synthase-1: the inducible synthase for prostaglandin E2. Arthritis Res Ther 2005;7:114-117. (Pubitemid 40775173)
6. Hara S, Kamei D, Sasaki Y, et al. Prostaglandin E synthases: understanding their pathophysiological roles through mouse genetic models. Biochimie 2010;92:651-659.
7. Pü schel GP, Jungermann K. Integration of function in the hepatic acinus: intercellular communication in neural and humoral control of liver metabolism. Prog Liver Dis 1994;12:19-46. (Pubitemid 24349143)
8. Henkel J, Neuschafer-Rube F, Pathe-Neuschafer-Rube A, et al. Aggravation by prostaglandin E2 of interleukin-6-dependent insulin resistance in hepatocytes. Hepatology 2009;50:781-790.
9. Hespeling U, Jungermann K, Pü schel GP. Feedback-inhibition of glucagon-stimulated glycogenolysis in hepatocyte/Kupffer cell cocultures by glucagon-elicited prostaglandin production in Kupffer cells. Hepatology 1995;22:1577-1583.
10. Fennekohl A, Lucas M, Puschel GP. Induction by interleukin 6 of G(s)-coupled prostaglandin E(2) receptors in rat hepatocytes mediating a prostaglandin E(2)-dependent inhibition of the hepatocyte's acute phase response. Hepatology 2000;31:1128-1134. (Pubitemid 30233238)
11. Perez S, Aspichueta P, Ochoa B, et al. The 2-series prostaglandins suppress VLDL secretion in an inflammatory condition-dependent manner in primary rat hepatocytes. Biochim Biophys Acta 2006;1761:160-171.
12. Enomoto N, Ikejima K, Yamashina S, et al. Kupffer cell-derived prostaglandin E(2) is involved in alcohol-induced fat accumulation in rat liver. Am J Physiol Gastrointest Liver Physiol 2000;279:G100-G106. (Pubitemid 30612687)
13. Mater MK, Thelen AP, Jump DB. Arachidonic acid and PGE2 regulation of hepatic lipogenic gene expression. J Lipid Res 1999;40:1045-1052. (Pubitemid 29287875)
14. Bjornsson OG, Sparks JD, Sparks CE, et al. Prostaglandins suppress VLDL secretion in primary rat hepatocyte cultures: relationships to hepatic calcium metabolism. J Lipid Res 1992;33:1017-1027.
15. Spruss A, Kanuri G, Wagnerberger S, et al. Toll-like receptor 4 is involved in the development of fructose-induced hepatic steatosis in mice. Hepatology 2009;50:1094-1104.
16. Jurgens HS, Schurmann A, Kluge R, et al. Hyperphagia, lower body temperature, and reduced running wheel activity precede development of morbid obesity in New Zealand obese mice. Physiol Genomics 2006;25:234-241.
17. Vogel H, Nestler M, Ruschendorf F, et al. Characterization of Nob3, a major quantitative trait locus for obesity and hyperglycemia on mouse chromosome 1. Physiol Genomics 2009;38:226-232.
18. Wieneke N, Neuschafer-Rube F, Bode LM, et al. Synergistic acceleration of thyroid hormone degradation by phenobarbital and the PPAR alpha agonist WY14643 in rat hepatocytes. Toxicol Appl Pharmacol 2009;240:99-107.
19. Meredith MJ. Rat hepatocytes prepared without collagenase: prolonged retention of differentiated characteristics in culture. Cell Biol Toxicol 1988;4:405-425. (Pubitemid 19115551)
20. Neuschäfer-Rube F, Mö ller U, Pü schel GP. Structure of the 50-flanking region of the rat prostaglandin F(2alpha) receptor gene and its transcriptional control functions in hepatocytes. Biochem Biophys Res Commun 2000;278:278-285.
21. Walker PG. A colorimetric method for the estimation of acetoacetate. Biochem J 1954;58:699-704.
22. Henkel J, Gartner D, Dorn C, et al. Oncostatin M produced in Kupffer cells in response to PGE(2): possible contributor to hepatic insulin resistance and steatosis. Lab Invest 2011;91:1107-1117.
23. Murakami M, Nakashima K, Kamei D, et al. Cellular prostaglandin E2 production by membrane-bound prostaglandin E synthase-2 via both cyclooxygenases-1 and-2. J Biol Chem 2003;278:37937-37947. (Pubitemid 37175324)
24. Hansmannel F, Mordier S, Iynedjian PB. Insulin induction of glucokinase and fatty acid synthase in hepatocytes: analysis of the roles of sterol-regulatory-element-binding protein-1c and liver X receptor. Biochem J 2006;399:275-283. (Pubitemid 44570290)
25. Watt MJ, Spriet LL. Triacylglycerol lipases and metabolic control: implications for health and disease. Am J Physiol Endocrinol Metab 2010;299:E162-E168.
26. Ong KT, Mashek MT, Bu SY, et al. Adipose triglyceride lipase is a major hepatic lipase that regulates triacylglycerol turnover and fatty acid signaling and partitioning. Hepatology 2011;53:116-126.
27. Chakrabarti P, Kandror KV. FoxO1 controls insulin-dependent adipose triglyceride lipase (ATGL) expression and lipolysis in adipocytes. J Biol Chem 2009;284:13296-13300.
28. Trebino CE, Stock JL, Gibbons CP, et al. Impaired inflammatory and pain responses in mice lacking an inducible prostaglandin E synthase. Proc Natl Acad Sci USA 2003;100:9044-9049. (Pubitemid 36899220)
29. Uematsu S, Matsumoto M, Takeda K, et al. Lipopolysaccharidedependent prostaglandin E(2) production is regulated by the glutathione-dependent prostaglandin E(2) synthase gene induced by the Toll-like receptor 4/MyD88/NF-IL6 pathway. J Immunol 2002;168:5811-5816. (Pubitemid 34556168)
30. Luyendyk JP, Sullivan BP, Guo GL, et al. Tissue factor-deficiency and protease activated receptor-1-deficiency reduce inflammation elicited by diet-induced steatohepatitis in mice. Am J Pathol 2010;176:177-186.
31. Kassel KM, Guo GL, Tawfik O, et al. Monocyte chemoattractant protein-1 deficiency does not affect steatosis or inflammation in livers of mice fed a methionine-choline-deficient diet. Lab Invest 2010;90:1794-1804.
32. Yu J, Ip E, Dela Pena A, et al. COX-2 induction in mice with experimental nutritional steatohepatitis: role as pro-inflammatory mediator. Hepatology 2006;43:826-836.
33. Ii H, Hatakeyama S, Tsutsumi K, et al. Group IVA phospholipase A(2) is associated with the storage of lipids in adipose tissue and liver. Prostaglandins Other Lipid Mediat 2008;11:11.
34. Ii H, Yokoyama N, Yoshida S, et al. Alleviation of high-fat diet-induced fatty liver damage in group IVA phospholipase A2-knockout mice. PLoS One 2009;4:e8089.
35. Reid BN, Ables GP, Otlivanchik OA, et al. Hepatic overexpression of hormone-sensitive lipase and adipose triglyceride lipase promotes fatty acid oxidation, stimulates direct release of free fatty acids, and ameliorates steatosis. J Biol Chem 2008;283:13087-13099.
36. Stefanovic-Racic M, Perdomo G, Mantell BS, et al. A moderate increase in carnitine palmitoyltransferase 1a activity is sufficient to substantially reduce hepatic triglyceride levels. Am J Physiol Endocrinol Metab 2008;294:E969-E977.
37. Mollica MP, Lionetti L, Moreno M, et al. 3,5-diiodo-l-thyronine, by modulating mitochondrial functions, reverses hepatic fat accumulation in rats fed a high-fat diet. J Hepatol 2009;51:363-370.
38. Forcheron F, Abdallah P, Basset A, et al. Nonalcoholic hepatic steatosis in Zucker diabetic rats: spontaneous evolution and effects of metformin and fenofibrate. Obesity 2009;17:1381-1389.
39. Rector RS, Thyfault JP, Uptergrove GM, et al. Mitochondrial dysfunction precedes insulin resistance and hepatic steatosis and contributes to the natural history of non-alcoholic fatty liver disease in an obese rodent model. J Hepatol 2010;52:727-736.
40. Aires CC, Ijlst L, Stet F, et al. Inhibition of hepatic carnitine palmitoyl-transferase I (CPT IA) by valproyl-CoA as a possible mechanism of valproate-induced steatosis. Biochem Pharmacol 2009; 79:792-799.
41. Ibdah JA, Perlegas P, Zhao Y, et al. Mice heterozygous for a defect in mitochondrial trifunctional protein develop hepatic steatosis and insulin resistance. Gastroenterology 2005;128:1381-1390. (Pubitemid 40712187)
42. Zhang D, Liu ZX, Choi CS, et al. Mitochondrial dysfunction due to longchain Acyl-CoA dehydrogenase deficiency causes hepatic steatosis and hepatic insulin resistance. Proc Natl Acad Sci USA 2007;104: 17075-17080. (Pubitemid 350210994)
43. Shindo N, Fujisawa T, Sugimoto K, et al. Involvement of microsomal triglyceride transfer protein in nonalcoholic steatohepatitis in novel spontaneous mouse model. J Hepatol 2010;52:903-912.
44. Letteron P, Sutton A, Mansouri A, et al. Inhibition of microsomal triglyceride transfer protein: another mechanism for drug-induced steatosis in mice. Hepatology 2003;38:133-140. (Pubitemid 36775804)
45. Sugimoto T, Yamashita S, Ishigami M, et al. Decreased microsomal triglyceride transfer protein activity contributes to initiation of alcoholic liver steatosis in rats. J Hepatol 2002;36:157-162. (Pubitemid 34146421)
46. Yamaguchi K, Yang L, McCall S, et al. Inhibiting triglyceride synthesis improves hepatic steatosis but exacerbates liver damage and fibrosis in obese mice with nonalcoholic steatohepatitis. Hepatology 2007;45: 1366-1374. (Pubitemid 46918320)
47. Monetti M, Levin MC, Watt MJ, et al. Dissociation of hepatic steatosis and insulin resistance in mice overexpressing DGAT in the liver. Cell Metab 2007;6:69-78. (Pubitemid 46995777)
48. Nakanishi T, Oikawa D, Koutoku T, et al. Gamma-linolenic acid prevents conjugated linoleic acid-induced fatty liver in mice. Nutrition 2004;20:390-393. (Pubitemid 38388515)
49. Oikawa D, Tsuyama S, Akimoto Y, et al. Arachidonic acid prevents fatty liver induced by conjugated linoleic acid in mice. Br J Nutr 2009;101:1558-1563.
50. Yoon JC, Puigserver P, Chen G, et al. Control of hepatic gluconeogenesis through the transcriptional coactivator PGC-1. Nature 2001;413:131-138. (Pubitemid 32867868)
51. Pü schel GP, Christ B. Inhibition by PGE2 of glucagon-induced increase in phosphoenolpyruvate carboxykinase mRNA and acceleration of mRNA degradation in cultured rat hepatocytes. FEBS Lett 1994;351:353-356. (Pubitemid 2138689)
52. Leone TC, Lehman JJ, Finck BN, et al. PGC-1alpha deficiency causes multi-system energy metabolic derangements: muscle dysfunction, abnormal weight control and hepatic steatosis. PLoS Biol 2005;3:e101.