Generation and characterization of a mouse model of the metabolic syndrome: Apolipoprotein E and aromatase double knockout mice

American Journal of Physiology - Endocrinology and Metabolism

Volumn 302, Issue 5, 2012, Pages

  Scott, Nicola J A ^a   Cameron, Vicky A ^a   Raudsepp, Sara ^a   Lewis, Lynley K ^a   Simpson, Evan R ^b   Mark Richards, A ^a   Ellmers, Leigh J ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ADIPONECTIN; APOLIPOPROTEIN E; AROMATASE; C REACTIVE PROTEIN; CHOLESTEROL; HIGH DENSITY LIPOPROTEIN; INSULIN; INTERLEUKIN 6; LEPTIN; LOW DENSITY LIPOPROTEIN; RESISTIN; TRIACYLGLYCEROL; TUMOR NECROSIS FACTOR ALPHA; VERY LOW DENSITY LIPOPROTEIN CHOLESTEROL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATHEROSCLEROTIC PLAQUE; BLOOD PRESSURE; BODY WEIGHT; CHOLESTEROL BLOOD LEVEL; COLORIMETRY; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FATTY LIVER; FEMALE; GENE INACTIVATION; HEART RATE; HISTOLOGY; HYPERTENSION; IMPAIRED GLUCOSE TOLERANCE; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; INSULIN TOLERANCE TEST; LIPID ANALYSIS; MALE; METABOLIC SYNDROME X; MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; ORAL GLUCOSE TOLERANCE TEST; PHENOTYPE; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; TRIACYLGLYCEROL BLOOD LEVEL; WILD TYPE;

ADIPOSE TISSUE, WHITE; ANIMALS; AORTA; APOLIPOPROTEINS E; AROMATASE; ATHEROSCLEROSIS; C-REACTIVE PROTEIN; CROSSES, GENETIC; CYTOKINES; DISEASE MODELS, ANIMAL; FATTY LIVER; FEMALE; GLUCOSE INTOLERANCE; HYPERLIPIDEMIAS; HYPERTENSION; INSULIN RESISTANCE; LIVER; MALE; METABOLIC SYNDROME X; MICE; MICE, KNOCKOUT; OBESITY, ABDOMINAL;

EID: 84857263400     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00222.2011     Document Type: Article

References (48)

1. Alexander CM, Landsman PB, Teutsch SM, Haffner SM. NCEPdefined metabolic syndrome, diabetes, and prevalence of coronary heart disease among NHANES III participants age 50 years and older. Diabetes 52: 1210-1214, 2003.
2. Alexandersen P, Haarbo J, Byrjalsen I, Lawaetz H, Christiansen C. Natural androgens inhibit male atherosclerosis: a study in castrated, cholesterol-fed rabbits. Circ Res 84: 813-819, 1999.
3. Arad Y, Newstein D, Cadet F, Roth M, Guerci AD. Association of multiple risk factors and insulin resistance with increased prevalence of asymptomatic coronary artery disease by an electron-beam computed tomographic study. Arterioscler Thromb Vasc Biol 21: 2051-2058, 2001.
4. Banerji MA, Faridi N, Atluri R, Chaiken RL, Lebovitz HE. Body composition, visceral fat, leptin, and insulin resistance in Asian Indian men. J Clin Endocrinol Metab 84: 137-144, 1999.
5. Baumgartl J, Baudler S, Scherner M, Babaev V, Makowski L, Suttles J, McDuffie M, Tobe K, Kadowaki T, Fazio S, Kahn CR, Hotamisligil GS, Krone W, Linton M, Bruning JC. Myeloid lineage cell-restricted insulin resistance protects apolipoproteinE-deficient mice against atherosclerosis. Cell Metab 3: 247-256, 2006.
6. Bayturan O, Tuzcu EM, Lavoie A, Hu T, Wolski K, Schoenhagen P, Kapadia S, Nissen SE, Nicholls SJ. The metabolic syndrome, its component risk factors, and progression of coronary atherosclerosis. Arch Intern Med 170: 478-484, 2010.
7. Bennet AM, Di Angelantonio E, Ye Z, Wensley F, Dahlin A, Ahlbom A, Keavney B, Collins R, Wiman B, de Faire U, Danesh J. Association of apolipoprotein E genotypes with lipid levels and coronary risk. JAMA 298: 1300-1311, 2007.
8. Bourassa PA, Milos PM, Gaynor BJ, Breslow JL, Aiello RJ. Estrogen reduces atherosclerotic lesion development in apolipoprotein E-deficient mice. Proc Natl Acad Sci USA 93: 10022-10027, 1996.
9. Elhage R, Arnal JF, Pieraggi MT, Duverger N, Fievet C, Faye JC, Bayard F. 17 Beta-estradiol prevents fatty streak formation in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 17: 2679-2684, 1997.
10. Ellmers LJ, Scott NJ, Piuhola J, Maeda N, Smithies O, Frampton CM, Richards AM, Cameron VA. Npr1-regulated gene pathways contributing to cardiac hypertrophy and fibrosis. J Mol Endocrinol 38: 245-257, 2007.
11. Fisher CR, Graves KH, Parlow AF, Simpson ER. Characterization of mice deficient in aromatase (ArKO) because of targeted disruption of the cyp19 gene. Proc Natl Acad Sci USA 95: 6965-6970, 1998.
12. Gruen ML, Saraswathi V, Nuotio-Antar AM, Plummer MR, Coenen KR, Hasty AH. Plasma insulin levels predict atherosclerotic lesion burden in obese hyperlipidemic mice. Atherosclerosis 186: 54-64, 2006.
13. Gupte M, Boustany-Kari CM, Bharadwaj K, Police S, Thatcher S, Gong MC, English VL, Cassis LA. ACE2 is expressed in mouse adipocytes and regulated by a high-fat diet. Am J Physiol Regul Integr Comp Physiol 295: R781-R788, 2008.
14. Haffner SM, Lehto S, Ronnemaa T, Pyorala K, Laakso M. Mortality from coronary heart disease in subjects with type 2 diabetes and in nondiabetic subjects with and without prior myocardial infarction. N Engl J Med 339: 229-234, 1998.
15. Hao M, Head WS, Gunawardana SC, Hasty AH, Piston DW. Direct effect of cholesterol on insulin secretion: a novel mechanism for pancreatic beta-cell dysfunction. Diabetes 56: 2328-2338, 2007.
16. Hasty AH, Shimano H, Osuga J, Namatame I, Takahashi A, Yahagi N, Perrey S, Iizuka Y, Tamura Y, Amemiya-Kudo M, Yoshikawa T, Okazaki H, Ohashi K, Harada K, Matsuzaka T, Sone H, Gotoda T, Nagai R, Ishibashi S, Yamada N. Severe hypercholesterolemia, hypertriglyceridemia, and atherosclerosis in mice lacking both leptin and the low density lipoprotein receptor. J Biol Chem 276: 37402-37408, 2001.
17. Hu G, Jousilahti P, Qiao Q, Katoh S, Tuomilehto J. Sex differences in cardiovascular and total mortality among diabetic and non-diabetic individuals with or without history of myocardial infarction. Diabetologia 48: 856-861, 2005.
18. Irace C, Cortese C, Fiaschi E, Carallo C, Sesti G, Farinaro E, Gnasso A. Components of the metabolic syndrome and carotid atherosclerosis: role of elevated blood pressure. Hypertension 45: 597-601, 2005.
19. Jones ME, Boon WC, Proietto J, Simpson ER. Of mice and men: the evolving phenotype of aromatase deficiency. Trends Endocrinol Metab 17: 55-64, 2006.
20. Jones ME, Thorburn AW, Britt KL, Hewitt KN, Wreford NG, Proietto J, Oz OK, Leury BJ, Robertson KM, Yao S, Simpson ER. Aromatase-deficient (ArKO) mice have a phenotype of increased adiposity. Proc Natl Acad Sci USA 97: 12735-12740, 2000.
21. Karatsoreos IN, Bhagat SM, Bowles NP, Weil ZM, Pfaff DW, McEwen BS. Endocrine and physiological changes in response to chronic corticosterone: a potential model of the metabolic syndrome in mouse. Endocrinology 151: 2117-2127, 2010.
22. Ken-Dror G, Talmud PJ, Humphries SE, Drenos F. APOE/C1/C4/C2 gene cluster genotypes, haplotypes and lipid levels in prospective coronary heart disease risk among UK healthy men. Mol Med 16: 389-399, 2010.
23. Kennedy AJ, Ellacott KL, King VL, Hasty AH. Mouse models of the metabolic syndrome. Dis Models Mech 3: 156-166, 2010.
24. King VL, Hatch NW, Chan HW, de Beer MC, de Beer FC, Tannock LR. A murine model of obesity with accelerated atherosclerosis. Obesity (Silver Spring) 18: 35-41, 2010.
25. Kotronen A, Juurinen L, Hakkarainen A, Westerbacka J, Corner A, Bergholm R, Yki-Jarvinen H. Liver fat is increased in type 2 diabetic patients and underestimated by serum alanine aminotransferase compared with equally obese nondiabetic subjects. Diabetes Care 31: 165-169, 2008.
26. Laakso M, Lehto S. Epidemiology of risk factors for cardiovascular disease in diabetes and impaired glucose tolerance. Atherosclerosis 137 Suppl: S65-S73, 1998.
27. Laaksonen DE, Lakka HM, Niskanen LK, Kaplan GA, Salonen JT, Lakka TA. Metabolic syndrome and development of diabetes mellitus: application and validation of recently suggested definitions of the metabolic syndrome in a prospective cohort study. Am J Epidemiol 156: 1070-1077, 2002.
28. Lakka HM, Laaksonen DE, Lakka TA, Niskanen LK, Kumpusalo E, Tuomilehto J, Salonen JT. The metabolic syndrome and total and cardiovascular disease mortality in middle-aged men. JAMA 288: 2709-2716, 2002.
29. ob/ob mice devoid of ApoE or Ldlr. Am J Physiol Endocrinol Metab 294: E496-E505, 2008.
30. Luc G, Bard JM, Arveiler D, Evans A, Cambou JP, Bingham A, Amouyel P, Schaffer P, Ruidavets JB, Cambien F, et al. Impact of apolipoprotein E polymorphism on lipoproteins and risk of myocardial infarction The ECTIM Study. Arterioscler Thromb 14: 1412-1419, 1994.
31. Masuzaki H, Paterson J, Shinyama H, Morton NM, Mullins JJ, Seckl JR, Flier JS. A transgenic model of visceral obesity and the metabolic syndrome. Science 294: 2166-2170, 2001.
32. Meinhardt U, Mullis PE. The essential role of the aromatase/p450arom. Semin Reprod Med 20: 277-284, 2002.
33. Nakashima Y, Plump AS, Raines EW, Breslow JL, Ross R. ApoEdeficient mice develop lesions of all phases of atherosclerosis throughout the arterial tree. Arterioscler Thromb 14: 133-140, 1994.
34. Nathan L, Shi W, Dinh H, Mukherjee TK, Wang X, Lusis AJ, Chaudhuri G. Testosterone inhibits early atherogenesis by conversion to estradiol: critical role of aromatase. Proc Natl Acad Sci USA 98: 3589-3593, 2001.
35. Nishina PM, Naggert JK, Verstuyft J, Paigen B. Atherosclerosis in genetically obese mice: the mutants obese, diabetes, fat, tubby, and lethal yellow. Metabolism: clinical and experimental 43: 554-558, 1994.
36. Pai JK, Pischon T, Ma J, Manson JE, Hankinson SE, Joshipura K, Curhan GC, Rifai N, Cannuscio CC, Stampfer MJ, Rimm EB. Inflammatory markers and the risk of coronary heart disease in men and women. N Engl J Med 351: 2599-2610, 2004.
37. Phillips GB. Is atherosclerotic cardiovascular disease an endocrinological disorder? The estrogen-androgen paradox. J Clin Endocrinol Metab 90: 2708-2711, 2005.
38. Piedrahita JA, Zhang SH, Hagaman JR, Oliver PM, Maeda N. Generation of mice carrying a mutant apolipoprotein E gene inactivated by gene targeting in embryonic stem cells. Proc Natl Acad Sci USA 89: 4471-4475, 1992.
39. Rader DJ. Effect of insulin resistance, dyslipidemia, and intra-abdominal adiposity on the development of cardiovascular disease and diabetes mellitus. Am J Med 120: S12-18, 2007.
40. Reddick RL, Zhang SH, Maeda N. Atherosclerosis in mice lacking apo E. Evaluation of lesional development and progression. Arterioscler Thromb 14: 141-147, 1994.
41. Rees DA, Alcolado JC. Animal models of diabetes mellitus. Diabet Med 22: 359-370, 2005.
42. Ridker PM. High-sensitivity C-reactive protein: potential adjunct for global risk assessment in the primary prevention of cardiovascular disease. Circulation 103: 1813-1818, 2001.
43. Ridker PM, Buring JE, Cook NR, Rifai N. C-reactive protein, the metabolic syndrome, and risk of incident cardiovascular events: an 8-year follow-up of 14 719 initially healthy American women. Circulation 107: 391-397, 2003.
44. Schillaci G, Pirro M, Vaudo G, Gemelli F, Marchesi S, Porcellati C, Mannarino E. Prognostic value of the metabolic syndrome in essential hypertension. J Am Coll Cardiol 43: 1817-1822, 2004.
45. Seppala-Lindroos A, Vehkavaara S, Hakkinen AM, Goto T, Westerbacka J, Sovijarvi A, Halavaara J, Yki-Jarvinen H. Fat accumulation in the liver is associated with defects in insulin suppression of glucose production and serum free fatty acids independent of obesity in normal men. J Clin Endocrinol Metab 87: 3023-3028, 2002.
46. Tayama K, Inukai T, Shimomura Y. Preperitoneal fat deposition estimated by ultrasonography in patients with non-insulin-dependent diabetes mellitus. Diabetes Res Clin Pract 43: 49-58, 1999.
47. Tzou WS, Douglas PS, Srinivasan SR, Bond MG, Tang R, Chen W, Berenson GS, Stein JH. Increased subclinical atherosclerosis in young adults with metabolic syndrome: the Bogalusa Heart Study. J Am Coll Cardiol 46: 457-463, 2005.
48. Wu KK, Wu TJ, Chin J, Mitnaul LJ, Hernandez M, Cai TQ, Ren N, Waters MG, Wright SD, Cheng K. Increased hypercholesterolemia and atherosclerosis in mice lacking both ApoE and leptin receptor. Atherosclerosis 181: 251-259, 2005.