Sex-dependent hepatic transcripts and metabolites in the development of glucose intolerance and insulin resistance in zucker diabetic fatty rats

Journal of Molecular Endocrinology

Volumn 47, Issue 2, 2011, Pages 129-143

  Gustavsson, Carolina ^a   Soga, Tomoyoshi ^b   Wahlström, Erik ^a   Vesterlund, Mattias ^a   Azimi, Alireza ^a   Norstedt, Gunnar ^a   Tollet Egnell, Petra ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b KEIO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GLUCOSE; GLUTATHIONE; INSULIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CAPILLARY ELECTROPHORESIS; CONTROLLED STUDY; FATTY ACID OXIDATION; FEMALE; GLUCOSE BLOOD LEVEL; GLUCOSE INTOLERANCE; HORMONE SYNTHESIS; IMPAIRED GLUCOSE TOLERANCE; INSULIN BLOOD LEVEL; INSULIN RESISTANCE; INSULIN SENSITIVITY; LIPID DIET; LIPOGENESIS; LIVER FUNCTION; MALE; METABOLITE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; SEX DIFFERENCE; TIME OF FLIGHT MASS SPECTROMETRY; WEIGHT GAIN; ZUCKER DIABETIC FATTY RAT;

ANIMALS; BLOOD GLUCOSE; DIETARY FATS; FEMALE; GENE EXPRESSION PROFILING; GLUCOSE INTOLERANCE; IMMUNOBLOTTING; INSULIN RESISTANCE; LIVER; MALE; MASS SPECTROMETRY; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHOSPHORYLATION; RATS; RATS, ZUCKER; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEX FACTORS;

EID: 80054820905     PISSN: 09525041     EISSN: 14796813     Source Type: Journal    
DOI: 10.1530/JME-11-0007     Document Type: Article

References (61)

1. Arenas IA, Armstrong SJ, Xu Y & Davidge ST 2005 Chronic tumor necrosis factor-a inhibition enhances NO modulation of vascular function in estrogen-deficient rats. Hypertension 46 76-81. (doi:10.1161/01.HYP.0000168925.98963.ef)
2. Ayaz M, Celik H, Aydin H & Turan B 2006 Sodium selenite protects against diabetes-induced alterations in the antioxidant defense system of the liver. Diabetes/Metabolism Research and Reviews 22 295-299. (doi:10.1002/dmrr.601)
3. Baba T, Shimizu T, Suzuki Y, Ogawara M, Isono K, Koseki H, Kuosawa H & Shirasawa T 2005 Estrogen, insulin and dietary signals cooperatively regulate longevity signals to enhance resistance to oxidative stress in mice. Journal of Biological Chemistry 280 16417-16426. (doi:10.1074/jbc.M500924200)
4. Baulande S, Lasnier F, Lucas M & Pairault J 2001 Adiponutrin, a transmembrane protein corresponding to a novel dietary- and obesity-linked mRNA specifically expressed in the adipose lineage. Journal of Biological Chemistry 276 33336-33344. (doi:10.1074/jbc.M105193200)
5. Borrás C, Gambini J, Gómez-Cabrera MC, Sastre J, Pallardó FV, Mann GE & Viña J 2005 17β-Oestradiol up-regulates longevity-related, antioxidant enzyme expression via the ERK1 and ERK2[MAPK]/NFκB cascade. Aging Cell 4 113-118. (doi:10.1111/j.1474-9726.2005.00151.x)
6. Bryzgalova G, Gao H, Ahren B, Zierath JR, Galuska D, Steiler TL, Dahlman-Wright K, Nilsson S, Gustafsson JÃ, Efendic S et al. 2006 Evidence that oestrogen receptor-a plays an important role in the regulation of glucose homeostasis in mice: insulin sensitivity in the liver. Diabetologia 49 588-597. (doi:10.1007/s00125-005-0105-3)
7. Cai L 2004 Metallothionein as an adaptive protein prevents diabetes and its toxicity. Nonlinearity in Biology, Toxicology and Medicine 2 89-103. (doi:10.1080/15401420490464367)
8. Cai L, Chen S, Evans T, Cherian M & Chakrabarti S 2002 Endothelin-1-mediated alteration of metallothionein and trace metals in the liver and kidneys of chronically diabetic rats. International Journal of Experimental Diabetes Research 3 193-198. (doi:10.1080/15604280214281)
9. Cheung O & Sanyal A 2010 Recent advances in nonalcoholic fatty liver disease. Current Opinion in Gastroenterology 26 202-208. (doi:10.1097/MOG.0b013e328337b0c4)
10. Chiaverini N & De Ley M 2010 Protective effect of metallothionein on oxidative stress-induced DNA damage. Free Radical Research 44 605-613. (doi:10.3109/10715761003692511)
11. Clark J, Palmer C & Shaw W 1983 The diabetic Zucker fatty rat. Proceedings of the Society for Experimental Biology and Medicine 173 68-75.
12. Colombo M, Kruhoeffer M, Gregersen S, Agger A, Jeppesen P, Oerntoft T & Hermansen K 2006 Energy restriction prevents the development of type 2 diabetes in Zucker diabetic fatty rats: coordinated patterns of gene expression for energy metabolism in insulin-sensitive tissues and pancreatic islets determined by oligonucleotide microarray analysis. Metabolism: Clinical and Experimental 55 43-52. (doi:10.1016/j.metabol.2005.07.005)
13. Corsetti JP, Sparks JD, Peterson RG, Smith RL & Sparks CE 2000 Effect of dietary fat on the development of non-insulin dependent diabetes mellitus in obese Zucker diabetic fatty male and female rats. Atherosclerosis 148 231-241. (doi:10.1016/S0021-9150(99)00265-8)
14. D'Eon TM, Souza SC, Aronovitz M, Obin MS, Fried SK & Greenberg AS 2005 Estrogen regulation of adiposity and fuel partitioning. Journal of Biological Chemistry 280 35983-35991. (doi:10.1074/jbc.M507339200)
15. Engelking LJ, Kuriyama H, Hammer RE, Horton JD, Brown MS, Goldstein JL & LiangG2004 Overexpression of Insig-1 in the livers of transgenic mice inhibits SREBP processing and reduces insulinstimulated lipogenesis. Journal of Clinical Investigation 113 1168-1175. (doi:10.1172/JCI20978)
16. Gustavsson C, Parini P, Ostojic J, Cheung L, Hu J, Zadjali F, Tahir F, Brismar K, Norstedt G & Tollet-Egnell P 2009 Cocoa butter and safflower oil elicit different effects on hepatic gene expression and lipid metabolism in rats. Lipids 44 1011-1027. (doi:10.1007/s11745-009-3352-0)
17. Gustavsson C, Yassin K, Wahlström E, Cheung L, Lindberg J, Brismar K, Östenson C-G, Norstedt G & Tollet-Egnell P 2010 Sex-different hepatic glycogen content and glucose output in rats. BMC Biochemistry 23 38. (doi:10.1186/1471-2091-11-38)
18. Hawkins J, Jones W, Bonner F & Gibson G 1987 The effect of peroxisome proliferators on microsomal, peroxisomal, and mitochondrial enzyme activities in the liver and kidney. Drug Metabolism Reviews 18 441-515. (doi:10.3109/03602538708994130)
19. Hirosumi J, Tuncman G, Chang L, Gorgun CZ, Uysal KT, Maeda K, Karin M & Hotamisligil GS 2002 A central role for JNK in obesity and insulin resistance. Nature 420 333-336. (doi:10.1038/nature01137)
20. Horton TJ, Gayles EC, Prach PA, Koppenhafer TA & Pagliassotti MJ 1997 Female rats do not develop sucrose-induced insulin resistance. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 272 R1571-R1576.
21. Houstis N, Rosen ED & Lander ES 2006 Reactive oxygen species have a causal role in multiple forms of insulin resistance. Nature 440 944-948. (doi:10.1038/nature04634)
22. Isomaa B, Almgren P, Tuomi T, Forsen B, Lahti K, Nissen M, Taskinen M-R & Groop L 2001 Cardiovascular morbidity and mortality associated with the metabolic syndrome. Diabetes Care 24 683-689. (doi:10.2337/diacare.24.4.683)
23. Kawashima Y, Uy-Yu N & Kozuka H 1989a Sex-related difference in the inductions by perfluoro-octanoic acid of peroxisomal betaoxidation, microsomal 1-acylglycerophosphocholine acyltransferase and cytosolic long-chain acyl-CoA hydrolase in rat liver. Biochemical Journal 261 595-600.
24. Kawashima Y, Uy-Yu N & Kozuka H 1989b Sex-related differences in the enhancing effects of perfluoro-octanoic acid on stearoyl-CoA desaturase and its influence on the acyl composition of phospholipid in rat liver. Comparison with clofibric acid and tiadenol. Biochemical Journal 263 897-904.
25. Kim HJ, Kim HJ, Lee KE, Kim DJ, Kim SK, Ahn CW, Lim S-K, Kim KR, Lee HC, Huh KB et al. 2004 Metabolic significance of nonalcoholic fatty liver disease in nonobese, nondiabetic adults. Archives of Internal Medicine 164 2169-2175. (doi:10.1001/archinte.164.19.2169)
26. Kim S, Min W-K, Chun S, Lee W, Chung H-J, Lee PR & Kim A 2009 Quantitative risk estimation for large for gestational age using the area under the 100-g oral glucose tolerance test curve. Journal of Clinical Laboratory Analysis 23 231-236. (doi:10.1002/jcla.20326)
27. Kollerits B, Coassin S, Beckmann ND, Teumer A, Kiechl S, Döring A, Kavousi M, Hunt SC, Lamina C, Paulweber B et al. 2009 Genetic evidence for a role of adiponutrin in the metabolism of apolipoprotein B-containing lipoproteins. Human Molecular Genetics 18 4669-4676. (doi:10.1093/hmg/ddp424)
28. Koneru B, Reddy M, dela Torre A, Patel D, Ippolito T & Ferrante R 1995 Studies on hepatic warm ischemia in the obese Zucker rat. Transplantation 59 942-946. (doi:10.1097/00007890-199504150-00003)
29. Kotronen A, Johansson L, Johansson L, Roos C, Westerbacka J, Hamsten A, Bergholm R, Arkkila P, Arola J, Kiviluoto T et al. 2009 A common variant in PNPLA3, which encodes adiponutrin, is associated with liver fat content in humans. Diabetologia 52 1056-1060. (doi:10.1007/s00125-009-1285-z)
30. Kushlan MC, Gollan JL, Ma W-L & Ockner RK 1981 Sex differences in hepatic uptake of long chain fatty acids in single-pass perfused rat liver. Journal of Lipid Research 22 431-436.
31. Lake AC, Sun Y, Li J-L, Kim JE, Johnson JW, Li D, Revett T, Shih HH, Liu W, Paulsen JE et al. 2005 Expression, regulation, and triglyceride hydrolase activity of Adiponutrin family members. Journal of Lipid Research 46 2477-2487. (doi:10.1194/jlr.M500290-JLR200)
32. Legato MJ, Gelzer A, Goland R, Ebner SA, Rajan S, Villagra V & Kosowski M 2006 Gender-specific care of the patient with diabetes: review and recommendations. Gender Medicine 3 131-158. (doi:10.1016/S1550-8579(06)80202-0)
33. Li X, Chen H & Epstein P 2004 Metallothionein protects islets from hypoxia and extends islet graft survival by scavenging most kinds of reactive oxygen species. Journal of Biological Chemistry 279 765-771. (doi:10.1074/jbc.M307907200)
34. Louet J, LeMay C & Mauvais-Jarvis F 2004 Antidiabetic actions of estrogen: insight from human and genetic mouse models. Current Atherosclerosis Reports 6 180-185. (doi:10.1007/s11883-004-0030-9)
35. Manrique C, Lastra G, Gardner M & Sowers JR 2009 The renin angiotensin aldosterone system in hypertension: roles of insulin resistance and oxidative stress. Medical Clinics of North America 93 569-582. (doi:10.1016/j.mcna.2009.02.014)
36. Moldes M, Beauregard G, Faraj M, Peretti N, Ducluzeau P-H, Laville M, Rabasa-Lhoret R, Vidal H & Clement K 2006 Adiponutrin gene is regulated by insulin and glucose in human adipose tissue. European Journal of Endocrinology 155 461-468. (doi:10.1530/eje.1.02229)
37. Moran A, Jacobs DR Jr, Steinberger J, Steffen LM, Pankow JS, Hong C-P & Sinaiko AR 2008 Changes in insulin resistance and cardiovascular risk during adolescence: establishment of differential risk in males and females. Circulation 117 2361-2368. (doi:10.1161/CIRCULATIONAHA.107.704569)
38. Ohashi N, Urushihara M, Satou R & Kobori H 2010 Glomerular angiotensinogen is induced in mesangial cells in diabetic rats via reactive oxygen species - ERK/JNK pathways. Hypertension Research 33 1174-1181. (doi:10.1038/hr.2010.143)
39. Ohly P, Dohle C, Abel J, Seissler J & Gleichmann H 2000 Zinc sulphate induces metallothionein in pancreatic islets of mice and protects against diabetes induced by multiple low doses of streptozotocin. Diabetologia 43 1020-1030. (doi:10.1007/s001250050009)
40. Orci L, Ravazzola M, Baetens D, Inman L, Amherdt M, Peterson RG, Newgard CB, Johnson JH & Unger RH 1990 Evidence that downregulation of beta-cell glucose transporters in non-insulin-dependent diabetes may be the cause of diabetic hyperglycemia. PNAS 87 9953-9957. (doi:10.1073/pnas.87.24.9953)
41. Perrone G, Liu Y, Capri O, Critelli C, Barillaro F, Galoppi P & Zichella L 1999 Evaluation of the body composition and fat distribution in long-term users of hormone replacement therapy. Gynecologic and Obstetric Investigation 48 52-55. (doi:10.1159/000010134)
42. Polson D & Thompson M 2003 Adiponutrin gene expression in 3T3-L1 adipocytes is downregulated by troglitazone. Hormone and Metabolic Research 35 508-510. (doi:10.1055/s-2003-41811)
43. Regitz-Zagrosek V, Lehmkuhl E & Mahmoodzadeh S 2007 Gender aspects of the role of the metabolic syndrome as a risk factor for cardiovascular disease. Gender Medicine 4 S162-S177. (doi:10.1016/S1550-8579(07)80056-8)
44. Riant E, Waget A, Cogo H, Arnal J-F, Burcelin R & Gourdy P 2009 Estrogens protect against high-fat diet-induced insulin resistance and glucose intolerance in mice. Endocrinology 150 2109-2117. (doi:10.1210/en.2008-0971)
45. Romeo S, Kozlitina J, Xing C, Pertsemlidis A, Cox D, Pennacchio LA, Boerwinkle E, Cohen JC & Hobbs HH 2008 Genetic variation in PNPLA3 confers susceptibility to nonalcoholic fatty liver disease. Nature Genetics 40 1461-1465. (doi:10.1038/ng.257)
46. Serkova N, Jackman M, Brown J, Liu T, Hirose R, Roberts J, Maher J & Niemann C 2006 Metabolic profiling of livers and blood from obese Zucker rats. Journal of Hepatology 44 956-962. (doi:10.1016/j.jhep.2005.07.009)
47. Soga T & Heiger DN 2000 Amino acid analysis by capillary electrophoresis electrospray ionization mass spectrometry. Analytical Chemistry 72 1236-1241. (doi:10.1021/ac990976y)
48. Soga T, Baran R, Suematsu M, Ueno Y, Ikeda S, Sakurakawa T, Kakazu Y, Ishikawa T, Robert M, Nishioka T et al. 2006 Differential metabolomics reveals ophthalmic acid as an oxidative stress biomarker indicating hepatic glutathione consumption. Journal of Biological Chemistry 281 16768-16776. (doi:10.1074/jbc.M601876200)
49. Soler-Argilaga C & Heimberg M 1976 Comparison of metabolism of free fatty acid by isolated perfused livers from male and female rats. Journal of Lipid Research 17 605-615.
50. Soler-Argilaga C, Danon A, Goh E, Wilcox HG & Heimberg M 1975 The effect of sex on the uptake of very low density lipoprotein triglyceride fatty acid from the plasma of the rat in vivo. Biochemical and Biophysical Research Communications 66 1237-1242. (doi:10.1016/0006-291X(75)90491-X)
51. Soltys K, Dikdan G & Koneru B 2001 Oxidative stress in fatty livers of obese Zucker rats: rapid amelioration and improved tolerance to warm ischemia with tocopherol. Hepatology 34 13-18. (doi:10.1053/jhep.2001.25452)
52. Song Y, Wang J, Li Y, Du Y, Arteel G, Saari J, Kang Y & Cai L 2005 Cardiac metallothionein synthesis in streptozotocin-induced diabetic mice, and its protection against diabetes-induced cardiac injury. American Journal of Pathology 167 17-26. (doi:10.1016/S0002-9440(10)62949-5)
53. Ståhlberg N, Rico-Bautista E, Fischer RM, Wu X, Cheung L, Flores-Morales A, Tybring G, Norstedt G & Tollet-Egnell P 2004 Femalepredominant expression of fatty acid translocase/CD36 in rat and human liver. Endocrinology 145 1972-1979. (doi:10.1210/en.2003-0874)
54. Sugimoto M, Koseki T, Hirayama A, Abe S, Sano T, Tomita M & Soga T 2009 Correlation between sensory evaluation scores of Japanese sake and metabolome profiles. Journal of Agricultural and Food Chemistry 58 374-383. (doi:10.1021/jf903680d)
55. Sugimoto M, Hirayama A, Ishikawa T, Robert M, Baran R, Uehara K, Kawai K & Soga T 2010a Differential metabolomics software for capillary electrophoresis-mass spectrometry data analysis. Metabolomics 6 27-41. (doi:10.1007/s11306-009-0175-1)
56. Sugimoto M, Wong D, Hirayama A, Soga T & Tomita M 2010b Capillary electrophoresis mass spectrometry-based saliva metabolomics identified oral, breast and pancreatic cancerspecific profiles. Metabolomics 6 78-95. (doi:10.1007/s11306-009-0178-y)
57. Svoboda D, Azarnoff D & Reddy J 1969 Microbodies in experimentally altered cells: II. The relationship of microbody proliferation to endocrine glands. Journal of Cell Biology 40 734-746. (doi:10.1083/jcb.40.3.734)
58. Takaishi K, Duplomb L, Wang M-Y, Li J & Unger RH 2004 Hepatic insig-1 or -2 overexpression reduces lipogenesis in obese Zucker diabetic fatty rats and in fasted/refed normal rats. PNAS 101 7106-7111. (doi:10.1073/pnas.0401715101)
59. Tang Y, Yang Q, Lu J, Zhang X, Suen D, Tan Y, Jin L, Xiao J, Xie R, Rane M et al. 2010 Zinc supplementation partially prevents renal pathological changes in diabetic rats. Journal of Nutritional Biochemistry 21 237-246. (doi:10.1016/j.jnutbio.2008.12.010)
60. Wilson PA, Gardner SD, Lambie NM, Commans SA & Crowther DJ 2006 Characterization of the human patatin-like phospholipase family. Journal of Lipid Research 47 1940-1949. (doi:10.1194/jlr.M600185-JLR200)
61. Yuan X, Waterworth D, Perry JRB, Lim N, Song K, Chambers JC, Zhang W, Vollenweider P, Stirnadel H, Johnson T et al. 2008 Population-based genome-wide association studies reveal six loci influencing plasma levels of liver enzymes. American Journal of Human Genetics 83 520-528. (doi:10.1016/j.ajhg.2008.09.012)