Estrogen deficiency worsens steatohepatitis in mice fed high-fat and high-cholesterol diet

American Journal of Physiology - Gastrointestinal and Liver Physiology

Volumn 301, Issue 6, 2011, Pages

  Kamada, Yoshihiro ^a   Kiso, Shinichi ^a   Yoshida, Yuichi ^a   Chatani, Norihiro ^a   Kizu, Takashi ^a   Hamano, Mina ^a   Tsubakio, Mayumi ^a   Takemura, Takayo ^a   Ezaki, Hisao ^a   Hayashi, Norio ^a,b   Takehara, Tetsuo ^a  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b KANSAI ROSAI HOSPITAL   (Japan)

Author keywords

Nonalcoholic steatohepatitis nonalcoholic fatty liver disease; Postmenopause

Indexed keywords

ALANINE AMINOTRANSFERASE; CD36 ANTIGEN; CHEMOKINE RECEPTOR CCR2; CHOLESTEROL; COLLAGEN TYPE 1; COLLAGEN TYPE 1 ALPHA1; ESTRADIOL; ESTROGEN; FATTY ACID; GAMMA INTERFERON; GLUCOSE; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; INDUCIBLE NITRIC OXIDE SYNTHASE; INSULIN; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 4; LOW DENSITY LIPOPROTEIN CHOLESTEROL; MONOCYTE CHEMOTACTIC PROTEIN 1; PLACEBO; TRANSFORMING GROWTH FACTOR BETA1; TRIACYLGLYCEROL; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VERY LOW DENSITY LIPOPROTEIN;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INFILTRATION; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL INTAKE; CONTROLLED STUDY; DISEASE EXACERBATION; ESTROGEN DEFICIENCY; ESTROGEN THERAPY; FATTY ACID BLOOD LEVEL; FEMALE; GENE EXPRESSION REGULATION; GLUCOSE BLOOD LEVEL; HYPERCHOLESTEROLEMIA; INSULIN BLOOD LEVEL; LIPID DIET; LIPOPROTEIN BLOOD LEVEL; LIVER FIBROSIS; LIVER LEVEL; MACROPHAGE; MONOCYTE; MOUSE; NONALCOHOLIC FATTY LIVER; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RISK FACTOR; TRIACYLGLYCEROL BLOOD LEVEL;

ANIMALS; CHEMOKINE CCL2; CHOLESTEROL; CHOLESTEROL, DIETARY; DIET, HIGH-FAT; ESTROGENS; FATTY LIVER; FEMALE; GENE EXPRESSION; LIPOPROTEINS; LIVER; LIVER CIRRHOSIS; MACROPHAGES; MICE; MICE, INBRED C57BL; MONOCYTES; OVARIECTOMY; POSTMENOPAUSE; RECEPTORS, CCR2; RISK FACTORS;

EID: 82455219461     PISSN: 01931857     EISSN: 15221547     Source Type: Journal    
DOI: 10.1152/ajpgi.00211.2011     Document Type: Article

References (53)

1. Argo CK, Loria P, Caldwell SH, Lonardo A. Statins in liver disease: a molehill, an iceberg, or neither? Hepatology 48: 662-669, 2008.
2. Arici A, Senturk LM, Seli E, Bahtiyar MO, Kim G. Regulation of monocyte chemotactic protein-1 expression in human endometrial stromal cells by estrogen and progesterone. Biol Reprod 61: 85-90, 1999.
3. Brown MS, Goldstein JL. The SREBP pathway: regulation of cholesterol metabolism by proteolysis of a membrane-bound transcription factor. Cell 89: 331-340, 1997.
4. Bruning JC, Lingohr P, Gillette J, Hanstein B, Avci H, Krone W, Muller-Wieland D, Kotzka J. Estrogen receptor-alpha and Sp1 interact in the induction of the low density lipoprotein-receptor. J Steroid Biochem Mol Biol 86: 113-121, 2003.
5. Brunt EM. Nonalcoholic steatohepatitis: definition and pathology. Semin Liver Dis 21: 3-16, 2001.
6. Castelli WP, Doyle JT, Gordon T, Hames CG, Hjortland MC, Hulley SB, Kagan A, Zukel WJ. HDL cholesterol and other lipids in coronary heart disease. The cooperative lipoprotein phenotyping study. Circulation 55: 767-772, 1977.
7. Chen Y, Green SR, Ho J, Li A, Almazan F, Quehenberger O. The mouse CCR2 gene is regulated by two promoters that are responsive to plasma cholesterol and peroxisome proliferator-activated receptor gamma ligands. Biochem Biophys Res Commun 332: 188-193, 2005.
8. Chico Y, Fresnedo O, Botham K, Lacort M, Ochoa B. Regulation of bile acid synthesis by estradiol and progesterone in primary cultures of rat hepatocytes. Exp Clin Endocrinol Diabetes 104: 137-144, 1996.
9. Deushi M, Nomura M, Kawakami A, Haraguchi M, Ito M, Okazaki M, Ishii H, Yoshida M. Ezetimibe improves liver steatosis and insulin resistance in obese rat model of metabolic syndrome. FEBS Lett 581: 5664-5670, 2007.
10. Di Croce L, Vicent GP, Pecci A, Bruscalupi G, Trentalance A, Beato M. The promoter of the rat 3-hydroxy-3-methylglutaryl coenzyme A reductase gene contains a tissue-specific estrogen-responsive region. Mol Endocrinol 13: 1225-1236, 1999.
11. Friedman SL. Mechanisms of hepatic fibrogenesis. Gastroenterology 134: 1655-1669, 2008.
12. Godsland IF. Oestrogens and insulin secretion. Diabetologia 48: 2213-2220, 2005.
13. Han KH, Han KO, Green SR, Quehenberger O. Expression of the monocyte chemoattractant protein-1 receptor CCR2 is increased in hypercholesterolemia. Differential effects of plasma lipoproteins on monocyte function. J Lipid Res 40: 1053-1063, 1999.
14. Han KH, Tangirala RK, Green SR, Quehenberger O. Chemokine receptor CCR2 expression and monocyte chemoattractant protein-1-mediated chemotaxis in human monocytes. A regulatory role for plasma LDL. Arterioscler Thromb Vasc Biol 18: 1983-1991, 1998.
15. Heine PA, Taylor JA, Iwamoto GA, Lubahn DB, Cooke PS. Increased adipose tissue in male and female estrogen receptor-alpha knockout mice. Proc Natl Acad Sci USA 97: 12729-12734, 2000.
16. Hewitt KN, Boon WC, Murata Y, Jones ME, Simpson ER. The aromatase knockout mouse presents with a sexually dimorphic disruption to cholesterol homeostasis. Endocrinology 144: 3895-3903, 2003.
17. Hong MK, Romm PA, Reagan K, Green CE, Rackley CE. Effects of estrogen replacement therapy on serum lipid values and angiographically defined coronary artery disease in postmenopausal women. Am J Cardiol 69: 176-178, 1992.
18. Huang H, He J, Yuan Y, Aoyagi E, Takenaka H, Itagaki T, Sannomiya K, Tamaki K, Harada N, Shono M, Shimizu I, Takayama T. Opposing effects of estradiol and progesterone on the oxidative stressinduced production of chemokine and proinflammatory cytokines in murine peritoneal macrophages. J Med Invest 55: 133-141, 2008.
19. Hyogo H, Tazuma S, Arihiro K, Iwamoto K, Nabeshima Y, Inoue M, Ishitobi T, Nonaka M, Chayama K. Efficacy of atorvastatin for the treatment of nonalcoholic steatohepatitis with dyslipidemia. Metabolism 57: 1711-1718, 2008.
20. Itagaki T, Shimizu I, Cheng X, Yuan Y, Oshio A, Tamaki K, Fukuno H, Honda H, Okamura Y, Ito S. Opposing effects of oestradiol and progesterone on intracellular pathways and activation processes in the oxidative stress induced activation of cultured rat hepatic stellate cells. Gut 54: 1782-1789, 2005.
21. Janis K, Hoeltke J, Nazareth M, Fanti P, Poppenberg K, Aronica SM. Estrogen decreases expression of chemokine receptors, and suppresses chemokine bioactivity in murine monocytes. Am J Reprod Immunol 51: 22-31, 2004.
22. Kamada Y, Matsumoto H, Tamura S, Fukushima J, Kiso S, Fukui K, Igura T, Maeda N, Kihara S, Funahashi T, Matsuzawa Y, Shimomura I, Hayashi N. Hypoadiponectinemia accelerates hepatic tumor formation in a nonalcoholic steatohepatitis mouse model. J Hepatol 47: 556-564, 2007.
23. Kamada Y, Yoshida Y, Saji Y, Fukushima J, Tamura S, Kiso S, Hayashi N. Transplantation of basic fibroblast growth factor-pretreated adipose tissue-derived stromal cells enhances regression of liver fibrosis in mice. Am J Physiol Gastrointest Liver Physiol 296: G157-G167, 2009.
24. Kiyici M, Gulten M, Gurel S, Nak SG, Dolar E, Savci G, Adim SB, Yerci O, Memik F. Ursodeoxycholic acid and atorvastatin in the treatment of nonalcoholic steatohepatitis. Can J Gastroenterol 17: 713-718, 2003.
25. Kleiner DE, Brunt EM, Van Natta M, Behling C, Contos MJ, Cummings OW, Ferrell LD, Liu YC, Torbenson MS, Unalp-Arida A, Yeh M, McCullough AJ, Sanyal AJ. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology 41: 1313- 1321, 2005.
26. Koruk M, Savas MC, Yilmaz O, Taysi S, Karakok M, Gundogdu C, Yilmaz A. Serum lipids, lipoproteins and apolipoproteins levels in patients with nonalcoholic steatohepatitis. J Clin Gastroenterol 37: 177-182, 2003.
27. Kotani K, Tokunaga K, Fujioka S, Kobatake T, Keno Y, Yoshida S, Shimomura I, Tarui S, Matsuzawa Y. Sexual dimorphism of age-related changes in whole-body fat distribution in the obese. Int J Obes Relat Metab Disord 18: 207-202, 1994.
28. Kushwaha RS, Lewis DS, Carey KD, McGill HC Jr. Effects of estrogen and progesterone on plasma lipoproteins and experimental atherosclerosis in the baboon (Papio sp.). Arterioscler Thromb 11: 23-31, 1991.
29. Larter CZ, Yeh MM. Animal models of NASH: getting both pathology and metabolic context right. J Gastroenterol Hepatol 23: 1635-1648, 2008.
30. Lemieux C, Phaneuf D, Labrie F, Giguere V, Richard D, Deshaies Y. Estrogen receptor alpha-mediated adiposity-lowering and hypocholesterolemic actions of the selective estrogen receptor modulator acolbifene. Int J Obes (Lond) 29: 1236-1244, 2005.
31. Ley CJ, Lees B, Stevenson JC. Sex-and menopause-associated changes in body-fat distribution. Am J Clin Nutr 55: 950-954, 1992.
32. Maffei L, Rochira V, Zirilli L, Antunez P, Aranda C, Fabre B, Simone ML, Pignatti E, Simpson ER, Houssami S, Clyne CD, Carani C. A novel compound heterozygous mutation of the aromatase gene in an adult man: reinforced evidence on the relationship between congenital oestrogen deficiency, adiposity and the metabolic syndrome. Clin Endocrinol (Oxf) 67: 218-224, 2007.
33. Mari M, Caballero F, Colell A, Morales A, Caballeria J, Fernandez A, Enrich C, Fernandez-Checa JC, Garcia-Ruiz C. Mitochondrial free cholesterol loading sensitizes to TNF-and Fas-mediated steatohepatitis. Cell Metab 4: 185-198, 2006.
34. Matsuzawa N, Takamura T, Kurita S, Misu H, Ota T, Ando H, Yokoyama M, Honda M, Zen Y, Nakanuma Y, Miyamoto K, Kaneko S. Lipid-induced oxidative stress causes steatohepatitis in mice fed an atherogenic diet. Hepatology 46: 1392-1403, 2007.
35. Mikkola TS, Clarkson TB. Estrogen replacement therapy, atherosclerosis, and vascular function. Cardiovasc Res 53: 605-619, 2002.
36. Musso G, Gambino R, De Michieli F, Cassader M, Rizzetto M, Durazzo M, Faga E, Silli B, Pagano G. Dietary habits and their relations to insulin resistance and postprandial lipemia in nonalcoholic steatohepatitis. Hepatology 37: 909-916, 2003.
37. Nabulsi AA, Folsom AR, White A, Patsch W, Heiss G, Wu KK, Szklo M. Association of hormone-replacement therapy with various cardiovascular risk factors in postmenopausal women. The Atherosclerosis Risk in Communities Study Investigators. N Engl J Med 328: 1069-1075, 1993.
38. Nemoto Y, Toda K, Ono M, Fujikawa-Adachi K, Saibara T, Onishi S, Enzan H, Okada T, Shizuta Y. Altered expression of fatty acid-metabolizing enzymes in aromatase-deficient mice. J Clin Invest 105: 1819-1825, 2000.
39. Oien KA, Moffat D, Curry GW, Dickson J, Habeshaw T, Mills PR, MacSween RN. Cirrhosis with steatohepatitis after adjuvant tamoxifen. Lancet 353: 36-37, 1999.
40. Pagano G, Pacini G, Musso G, Gambino R, Mecca F, Depetris N, Cassader M, David E, Cavallo-Perin P, Rizzetto M. Nonalcoholic steatohepatitis, insulin resistance, and metabolic syndrome: further evidence for an etiologic association. Hepatology 35: 367-372, 2002.
41. Pratt DS, Knox TA, Erban J. Tamoxifen-induced steatohepatitis. Ann Intern Med 123: 236, 1995.
42. Puri P, Baillie RA, Wiest MM, Mirshahi F, Choudhury J, Cheung O, Sargeant C, Contos MJ, Sanyal AJ. A lipidomic analysis of nonalcoholic fatty liver disease. Hepatology 46: 1081-1090, 2007.
43. Rogers A, Eastell R. The effect of 17beta-estradiol on production of cytokines in cultures of peripheral blood. Bone 29: 30-34, 2001.
44. Ruhl CE, Everhart JE. Epidemiology of nonalcoholic fatty liver. Clin Liver Dis 8: 501-519, vii, 2004.
45. Singh DK, Sakhuja P, Malhotra V, Gondal R, Sarin SK. Independent predictors of steatohepatitis and fibrosis in Asian Indian patients with non-alcoholic steatohepatitis. Dig Dis Sci 53: 1967-1976, 2008.
46. Somers KD, Koenig M, Schechter GL. Growth of head and neck squamous cell carcinoma in nude mice: potentiation of laryngeal carcinoma by 17 beta-estradiol. J Natl Cancer Inst 80: 688-691, 1988.
47. Targher G, Bertolini L, Poli F, Rodella S, Scala L, Tessari R, Zenari L, Falezza G. Nonalcoholic fatty liver disease and risk of future cardiovascular events among type 2 diabetic patients. Diabetes 54: 3541-3546, 2005.
48. Tous M, Ferre N, Rull A, Marsillach J, Coll B, Alonso-Villaverde C, Camps J, Joven J. Dietary cholesterol and differential monocyte chemoattractant protein-1 gene expression in aorta and liver of apo E-deficient mice. Biochem Biophys Res Commun 340: 1078-1084, 2006.
49. Usui S, Hara Y, Hosaki S, Okazaki M. A new on-line dual enzymatic method for simultaneous quantification of cholesterol and triglycerides in lipoproteins by HPLC. J Lipid Res 43: 805-814, 2002.
50. Wouters K, van Gorp PJ, Bieghs V, Gijbels MJ, Duimel H, Lutjohann D, Kerksiek A, van Kruchten R, Maeda N, Staels B, van Bilsen M, Shiri-Sverdlov R, Hofker MH. Dietary cholesterol, rather than liver steatosis, leads to hepatic inflammation in hyperlipidemic mouse models of nonalcoholic steatohepatitis. Hepatology 48: 474-486, 2008.
51. Yasutake K, Nakamuta M, Shima Y, Ohyama A, Masuda K, Haruta N, Fujino T, Aoyagi Y, Fukuizumi K, Yoshimoto T, Takemoto R, Miyahara T, Harada N, Hayata F, Nakashima M, Enjoji M. Nutritional investigation of non-obese patients with non-alcoholic fatty liver disease: the significance of dietary cholesterol. Scand J Gastroenterol 44: 471-477, 2009.
52. Yatsuji S, Hashimoto E, Tobari M, Tokushige K, Shiratori K. Influence of age and gender in Japanese patients with non-alcoholic steatohepatitis. Hepatol Res 37: 1034-1043, 2007.
53. Yoshimatsu M, Terasaki Y, Sakashita N, Kiyota E, Sato H, van der Laan LJ, Takeya M. Induction of macrophage scavenger receptor MARCO in nonalcoholic steatohepatitis indicates possible involvement of endotoxin in its pathogenic process. Int J Exp Pathol 85: 335-343, 2004.