Gender difference in proteome of brown adipose tissues between male and female rats exposed to a high fat diet

Cellular Physiology and Biochemistry

Volumn 28, Issue 5, 2011, Pages 933-948

  Choi, Duk Kwon ^a   Oh, Tae Seok ^a   Choi, Jung Won ^a   Mukherjee, Rajib ^a   Wang, Xia ^a   Liu, Hao ^a   Yun, Jong Won ^a  

^a Daegu University   (South Korea)

Author keywords

2 DE; Brown adipose tissue; Gender differences; High fat diet; Obesity; Proteome

Indexed keywords

PROTEOME;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BROWN ADIPOSE TISSUE; CONTROLLED STUDY; ENERGY EXPENDITURE; FEMALE; LEAN BODY WEIGHT; LIPID DIET; LIPOGENESIS; MALE; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOUSE MUTANT; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RANDOMIZED CONTROLLED TRIAL; RAT; SEX DIFFERENCE; THERMOGENESIS; WEIGHT GAIN;

EID: 83755182945     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000335807     Document Type: Article

References (66)

1. Kautzky-Willer A, Handisurya A: Metabolic diseases and associated complications: Sex and gender matter! Eur J Clin Invest 2009;39:631-648.
2. Sweeting H, West P, Young R: Obesity among scottish 15 year olds 1987-2006: Prevalence and associations with socioeconomic status, well-being and worries about weight. BMC Public Health 2008;8:404-410.
3. Blouin K, Boivin A, Tchernof A: Androgens and body fat distribution. J Steroid Biochem Mol Biol 2008;108:272-280. (Pubitemid 351179628)
4. Nguyen TT, Hernandez Mijares A, Johnson CM, Jensen MD: Postprandial leg and splanchnic fatty acid metabolism in nonobese men and women. Am J Physiol 1996;271:E965-972. (Pubitemid 27030589)
5. Blaak E: Gender differences in fat metabolism. Curr Opin Clin Nutr Metab Care 2001;4:499-502. (Pubitemid 34755406)
6. Llado I, Estrany ME, Rodriguez E, Amengual B, Roca P, Palou A: Effects of cafeteria diet feeding on beta3-adrenoceptor expression and lipolytic activity in white adipose tissue of male and female rats. Int J Obes Relat Metab Disord 2000;24:1396-1404.
7. Llado I, Rodriguez-Cuenca S, Pujol E, Monjo M, Estrany ME, Roca P, Palou A: Gender effects on adrenergic receptor expression and lipolysis in white adipose tissue of rats. Obes Res 2002;10:296-305. (Pubitemid 135688239)
8. Shi H, Seeley RJ, Clegg DJ: Sexual differences in the control of energy homeostasis. Front Neuroendocrinol 2009;30:396-404.
9. Zillikens MC, Yazdanpanah M, Pardo LM, Rivadeneira F, Aulchenko YS, Oostra BA, Uitterlinden AG, Pols HA, van Duijn CM: Sex-specific genetic effects influence variation in body composition. Diabetologia 2008;51:2233-2241.
10. Schousboe K, Willemsen G, Kyvik KO, Mortensen J, Boomsma DI, Cornes BK, Davis CJ, Fagnani C, Hjelmborg J, Kaprio J, De Lange M, Luciano M, Martin NG, Pedersen N, Pietilainen KH, Rissanen A, Saarni S, Sorensen TI, Van Baal GC, Harris JR: Sex differences in heritability of bmi: A comparative study of results from twin studies in eight countries. Twin Res 2003;6:409-421. (Pubitemid 38019779)
11. Arciero PJ, Goran MI, Poehlman ET: Resting metabolic rate is lower in women than in men. J Appl Physiol 1993;75:2514-2520. (Pubitemid 24008367)
12. Tarnopolsky MA, Atkinson SA, Phillips SM, MacDougall JD: Carbohydrate loading and metabolism during exercise in men and women. J Appl Physiol 1995;78:1360-1368.
13. Komi PV, Karlsson J: Skeletal muscle fibre types, enzyme activities and physical performance in young males and females. Acta Physiol Scand 1978;103:210-218. (Pubitemid 8353600)
14. Henderson GC, Fattor JA, Horning MA, Faghihnia N, Johnson ML, Luke-Zeitoun M, Brooks GA: Glucoregulation is more precise in women than in men during postexercise recovery. Am J Clin Nutr 2008;87:1686-1694. (Pubitemid 351872631)
15. Rodriguez AM, Palou A: Uncoupling proteins: Gender dependence and their relation to body weight control. Int J Obes Relat Metab Disord 2004;28:500-502. (Pubitemid 38491139)
16. Roca P, Rodriguez AM, Oliver P, Bonet ML, Quevedo S, Pico C, Palou A: Brown adipose tissue response to cafeteria dietfeeding involves induction of the ucp2 gene and is impaired in female rats as compared to males. Pflugers Arch 1999;438:628-634. (Pubitemid 29454977)
17. Bjorntorp P: Hormonal control of regional fat distribution. Hum Reprod 1997;12 Suppl 1:21-25.
18. Rodriguez-Cuenca S, Pujol E, Justo R, Frontera M, Oliver J, Gianotti M, Roca P: Sex-dependent thermogenesis, differences in mitochondrial morphology and function, and adrenergic response in brown adipose tissue. J Biol Chem 2002;277:42958-42963. (Pubitemid 35285674)
19. Allan CA, Strauss BJ, Burger HG, Forbes EA, McLachlan RI: Testosterone therapy prevents gain in visceral adipose tissue and loss of skeletal muscle in nonobese aging men. J Clin Endocrinol Metab 2008;93:139-146.
20. Quevedo S, Roca P, Pico C, Palou A: Sexassociated differences in cold-induced ucp1 synthesis in rodent brown adipose tissue. Pflugers Arch 1998;436:689-695. (Pubitemid 28421366)
21. Rodriguez AM, Quevedo-Coli S, Roca P, Palou A: Sex-dependent dietary obesity, induction of ucps, and leptin expression in rat adipose tissues. Obes Res 2001;9:579-588. (Pubitemid 33610179)
22. Valle A, Catala-Niell A, Colom B, Garcia-Palmer FJ, Oliver J, Roca P: Sex-related differences in energy balance in response to caloric restriction. Am J Physiol Endocrinol Metab 2005;289:E15-22. (Pubitemid 40874929)
23. Macotela Y, Boucher J, Tran TT, Kahn CR: Sex and depot differences in adipocyte insulin sensitivity and glucose metabolism. Diabetes 2009;58:803-812.
24. Wang GJ, Volkow ND, Telang F, Jayne M, Ma Y, Pradhan K, Zhu W, Wong CT, Thanos PK, Geliebter A, Biegon A, Fowler JS: Evidence of gender differences in the ability to inhibit brain activation elicited by food stimulation. Proc Natl Acad Sci U S A 2009;106:1249-1254.
25. Matsuda Y, Tanioka T, Yoshioka T, Nagano T, Hiroi T, Yoshikawa K, Okabe K, Nagamine I, Takasaka Y: Gender differences in association of plasma adiponectin with obesity reflect resultant insulin resistance in non-diabetic japanese patients with schizophrenia. Psychiatry Clin Neurosci 2005;59:266-273. (Pubitemid 40897197)
26. Fujiki N, Yoshida Y, Zhang S, Sakurai T, Yanagisawa M, Nishino S: Sex difference in body weight gain and leptin signaling in hypocretin/orexin deficient mouse models. Peptides 2006;27:2326-2331. (Pubitemid 44437559)
27. Havel PJ, Kasim-Karakas S, Dubuc GR, Mueller W, Phinney SD: Gender differences in plasma leptin concentrations. Nat Med 1996;2:949-950. (Pubitemid 26306822)
28. Clegg DJ, Riedy CA, Smith KA, Benoit SC, Woods SC: Differential sensitivity to central leptin and insulin in male and female rats. Diabetes 2003;52:682-687. (Pubitemid 36323575)
29. Frank S, Laharnar N, Kullmann S, Veit R, Canova C, Hegner YL, Fritsche A, Preissl H: Processing of food pictures: Influence of hunger, gender and calorie content. Brain Res 2010;1350:159-166.
30. Magkos F, Mittendorfer B: Gender differences in lipid metabolism and the effect of obesity. Obstet Gynecol Clin North Am 2009;36:245-265, vii.
31. Hong J, Stubbins RE, Smith RR, Harvey AE, Nunez NP: Differential susceptibility to obesity between male, female and ovariectomized female mice. Nutr J 2009;8:11.
32. Legato MJ: Gender-specific aspects of obesity. Int J Fertil Womens Med 1997;42:184-197.
33. Gayle DA, Desai M, Casillas E, Beloosesky R, Ross MG: Gender-specific orexigenic and anorexigenic mechanisms in rats. Life Sci 2006;79:1531-1536. (Pubitemid 44301268)
34. Catala-Niell A, Estrany ME, Proenza AM, Gianotti M, Llado I: Skeletal muscle and liver oxidative metabolism in response to a voluntary isocaloric intake of a high fat diet in male and female rats. Cell Physiol Biochem 2008;22:327-336.
35. Justo R, Boada J, Frontera M, Oliver J, Bermudez J, Gianotti M: Gender dimorphism in rat liver mitochondrial oxidative metabolism and biogenesis. Am J Physiol Cell Physiol 2005;289:C372-378. (Pubitemid 41008883)
36. Valle A, Guevara R, Garcia-Palmer FJ, Roca P, Oliver J: Sexual dimorphism in liver mitochondrial oxidative capacity is conserved under caloric restriction conditions. Am J Physiol Cell Physiol 2007;293:C1302-1308. (Pubitemid 47556746)
37. Miike K, Aoki M, Yamashita R, Takegawa Y, Saya H, Miike T, Yamamura K: Proteome profiling reveals gender differences in the composition of human serum. Proteomics 2010;10:2678-2691.
38. Eidelman O, Jozwik C, Huang W, Srivastava M, Rothwell SW, Jacobowitz DM, Ji X, Zhang X, Guggino W, Wright J, Kiefer J, Olsen C, Adimi N, Mueller GP, Pollard HB: Gender dependence for a subset of the low-abundance signaling proteome in human platelets. Hum Genomics Proteomics 2010;2010:164906.
39. Metskas LA, Kulp M, Scordilis SP: Gender dimorphism in the exercise-naive murine skeletal muscle proteome. Cell Mol Biol Lett 2010;15:507-516.
40. Amelina H, Cristobal S: Proteomic study on gender differences in aging kidney of mice. Proteome Sci 2009;7:16.
41. Martins-de-Souza D, Schmitt A, Roder R, Lebar M, Schneider-Axmann T, Falkai P, Turck CW: Sex-specific proteome differences in the anterior cingulate cortex of schizophrenia. J Psychiatr Res 2010;44:989-991.
42. Shetty J, Naaby-Hansen S, Shibahara H, Bronson R, Flickinger CJ, Herr JC: Human sperm proteome: Immunodominant sperm surface antigens identified with sera from infertile men and women. Biol Reprod 1999;61:61-69. (Pubitemid 29295968)
43. Schmid GM, Converset V, Walter N, Sennitt MV, Leung KY, Byers H, Ward M, Hochstrasser DF, Cawthorne MA, Sanchez JC: Effect of high-fat diet on the expression of proteins in muscle, adipose tissues, and liver of c57bl/6 mice. Proteomics 2004;4:2270-2282. (Pubitemid 39025327)
44. Joo JI, Oh TS, Kim DH, Choi DK, Wang X, Choi JW, Yun JW: Differential expression of adipose tissue proteins between obesity-susceptible and-resistant rats fed a high-fat diet. Proteomics 2011;11:1429-1448.
45. Bradford MM: A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976;72:248-254.
46. Kim DH, Choi JW, Joo JI, Wang X, Choi DK, Oh TS, Yun JW: Changes in expression of skeletal muscle proteins between obesity-prone and obesityresistant rats induced by a high-fat diet. J Proteome Res 2011;10:1281-1292.
47. Borras C, Sastre J, Garcia-Sala D, Lloret A, Pallardo FV, Vina J: Mitochondria from females exhibit higher antioxidant gene expression and lower oxidative damage than males. Free Radic Biol Med 2003;34:546-552. (Pubitemid 36254828)
48. Vale RD, Reese TS, Sheetz MP: Identification of a novel force-generating protein, kinesin, involved in microtubulebased motility. Cell 1985;42:39-50. (Pubitemid 16237554)
49. Kull FJ, Sablin EP, Lau R, Fletterick RJ, Vale RD: Crystal structure of the kinesin motor domain reveals a structural similarity to myosin. Nature 1996;380:550-555. (Pubitemid 26110647)
50. Skowronek KJ, Kocik E, Kasprzak AA: Subunits interactions in kinesin motors. Eur J Cell Biol 2007;86:559-568. (Pubitemid 47233380)
51. Wang Q, Bilan PJ, Tsakiridis T, Hinek A, Klip A: Actin filaments participate in the relocalization of phosphatidylinositol3-kinase to glucose transporter-containing compartments and in the stimulation of glucose uptake in 3t3-l1 adipocytes. Biochem J 1998;331:917-928. (Pubitemid 28211918)
52. Omata W, Shibata H, Li L, Takata K, Kojima I: Actin filaments play a critical role in insulin-induced exocytotic recruitment but not in endocytosis of glut4 in isolated rat adipocytes. Biochem J 2000;346:321-328. (Pubitemid 30148116)
53. Semiz S, Park JG, Nicoloro SM, Furcinitti P, Zhang C, Chawla A, Leszyk J, Czech MP: Conventional kinesin kif5b mediates insulin-stimulated glut4 movements on microtubules. EMBO J 2003;22:2387-2399. (Pubitemid 36604978)
54. Davenport JR, Watts AJ, Roper VC, Croyle MJ, van Groen T, Wyss JM, Nagy TR, Kesterson RA, Yoder BK: Disruption of intraflagellar transport in adult mice leads to obesity and slow-onset cystic kidney disease. Curr Biol 2007;17:1586-1594. (Pubitemid 47380400)
55. Festuccia WT, Guerra-Sa R, Kawashita NH, Garofalo MA, Evangelista EA, Rodrigues V, Kettelhut IC, Migliorini RH: Expression of glycerokinase in brown adipose tissue is stimulated by the sympathetic nervous system. Am J Physiol Regul Integr Comp Physiol 2003;284:R1536-1541. (Pubitemid 36617493)
56. Franckhauser S, Munoz S, Elias I, Ferre T, Bosch F: Adipose overexpression of phosphoenolpyruvate carboxykinase leads to high susceptibility to diet-induced insulin resistance and obesity. Diabetes 2006;55:273-280. (Pubitemid 43343253)
57. MacDougald OA, Burant CF: Obesity and metabolic perturbations after loss of aquaporin 7, the adipose glycerol transporter. Proc Natl Acad Sci U S A 2005;102:10759-10760. (Pubitemid 41105935)
58. Smith RG, Gauthier DA, Dennis DT, Turpin DH: Malate-and pyruvatedependent fatty acid synthesis in leucoplasts from developing castor endosperm. Plant Physiol 1992;98:1233-1238.
59. Albrektsen T, Richter HE, Clausen JT, Fleckner J: Identification of a novel integral plasma membrane protein induced during adipocyte differentiation. Biochem J 2001;359:393-402. (Pubitemid 32999785)
60. Ran Q, Wadhwa R, Kawai R, Kaul SC, Sifers RN, Bick RJ, Smith JR, Pereira-Smith OM: Extramitochondrial localization of mortalin/mthsp70/pbp74/ grp75. Biochem Biophys Res Commun 2000;275:174-179. (Pubitemid 30663648)
61. Lee AS: The glucose-regulated proteins: Stress induction and clinical applications. Trends Biochem Sci 2001;26:504-510. (Pubitemid 32735452)
62. Little E, Ramakrishnan M, Roy B, Gazit G, Lee AS: The glucose-regulated proteins (grp78 and grp94): Functions, gene regulation, and applications. Crit Rev Eukaryot Gene Expr 1994;4:1-18. (Pubitemid 24238439)
63. Jernas M, Olsson B, Arner P, Jacobson P, Sjostrom L, Walley A, Froguel P, McTernan PG, Hoffstedt J, Carlsson LM: Regulation of carboxylesterase 1 (ces1) in human adipose tissue. Biochem Biophys Res Commun 2009;383:63-67.
64. Demozay D, Rocchi S, Mas JC, Grillo S, Pirola L, Chavey C, Van Obberghen E: Fatty aldehyde dehydrogenase: Potential role in oxidative stress protection and regulation of its gene expression by insulin. J Biol Chem 2004;279:6261-6270. (Pubitemid 38258224)
65. 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 U S A 2000;97:12729-12734.
66. 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 U S A 2000;97:12735-12740.