High-fat diet feeding induces a depot-dependent response on the pro-inflammatory state and mitochondrial function of gonadal white adipose tissue

British Journal of Nutrition

Volumn 109, Issue 3, 2013, Pages 413-424

  Amengual Cladera, E ^a,b   Llado I ^a,b   Proenza, A M ^a,b   Gianotti, M ^a,b  

^a UNIVERSITAT DE LES ILLES BALEARS   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

Adipokines; Insulin sensitivity; Mitochondrial biogenesis; Obesity; Rats

Indexed keywords

ADIPONECTIN; CD68 ANTIGEN; GLUCOSE; HYPOXIA INDUCIBLE FACTOR 1; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INSULIN; LEPTIN; MESSENGER RNA; PLASMINOGEN ACTIVATOR INHIBITOR 1; RESISTIN; TUMOR NECROSIS FACTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALORIC INTAKE; CELL FUNCTION; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; EPIDIDYMIS; EPIDIDYMIS FAT; FEMALE; GLUCOSE BLOOD LEVEL; GONAD; INSULIN BLOOD LEVEL; INSULIN SENSITIVITY; LIPID DIET; MALE; MITOCHONDRION; NONHUMAN; OBESITY; ORAL GLUCOSE TOLERANCE TEST; PROTEIN CONTENT; RAT; SEX DIFFERENCE; WEIGHT GAIN; WHITE ADIPOSE TISSUE;

ADIPOKINES; ADIPOSE TISSUE, WHITE; ADIPOSITY; ANIMALS; BIOLOGICAL MARKERS; CELLS, CULTURED; DIET, HIGH-FAT; ENERGY INTAKE; EPIDIDYMIS; FEMALE; INFLAMMATION MEDIATORS; INSULIN RESISTANCE; MALE; MITOCHONDRIA; MITOCHONDRIAL TURNOVER; OBESITY; OVARY; OXIDATIVE STRESS; RATS; RATS, WISTAR; SEX CHARACTERISTICS; SIGNAL TRANSDUCTION;

EID: 84875832074     PISSN: 00071145     EISSN: 14752662     Source Type: Journal    
DOI: 10.1017/S0007114512001171     Document Type: Article

References (75)

1. Galic S, Oakhill JS & Steinberg GR (2009) Adipose tissue as an endocrine organ. Mol Cell Endocrinol 316, 129-139.
2. Trayhurn P & Wood IS ( 2005) Signalling role of adipose tissue: Adipokines and inflammation in obesity. Biochem Soc Trans 33, 1078-1081. (Pubitemid 41659117)
3. Brochu-Gaudreau K, Rehfeldt C, Blouin R, et al. (2010) Adiponectin action from head to toe. Endocrine 37, 11-32.
4. Gesta S, Tseng YH & Kahn CR (2007) Developmental origin of fat: Tracking obesity to its source. Cell 131, 242-256. (Pubitemid 47576146)
5. Cancello R & Clement K (2006) Is obesity an inflammatory illness? Role of low-grade inflammation and macrophage infiltration in human white adipose tissue. BJOG 113, 1141-1147. (Pubitemid 44401207)
6. Subramanian V & Ferrante AW Jr (2009) Obesity, inflammation, and macrophages. Nestle Nutr Workshop Ser Pediatr Program 63, 151 -159, discussion 9-62, 259-268.
7. Trayhurn P, Wang B & Wood IS (2008) Hypoxia and the endocrine and signalling role of white adipose tissue. Arch Physiol Biochem 114, 267-276.
8. Murdoch C, Muthana M & Lewis CE (2005) Hypoxia regulates macrophage functions in inflammation. J Immunol 175, 6257-6263. (Pubitemid 41598863)
9. Arkan MC, Hevener AL, Greten FR, et al. (2005) IKK-beta links inflammation to obe sity-induced insulin resistance. Nat Med 11, 191-198. (Pubitemid 40321355)
10. Shi H, Kokoeva MV, Inouye K, et al. (2006) TLR4 links innate immunity and fatty acid-induced insulin resistance. J Clin Invest 116, 3015-3025. (Pubitemid 44684486)
11. Hotamisligil GS, Shargill NS & Spiegelman BM (1993) Adipose expression of tumor necrosis factor-alpha: Direct role in obesity-linked insulin resistance. Science 259, 87-91. (Pubitemid 23036092)
12. Feral CC, Neels JG, Kummer C, et al. (2008) Blockade of alpha4 integrin signaling ameliorates the metabolic consequences of high-fat diet-induced obesity. Diabetes 57, 1842-1851.
13. Bonnard C, Durand A, Peyrol S, et al. (2008) Mitochondrial dysfunction results from oxidative stress in the skeletal muscle of diet-induced insulin-resistant mice. J Clin Invest 118, 789-800. (Pubitemid 351206566)
14. Nadal-Casellas A, Amengual-Cladera E, Proenza AM, et al. (2010) Long-term high-fat-diet feeding impairs mitochondrial biogenesis in liver of male and female rats. Cell Physiol Biochem 26, 291-302.
15. Schrauwen P, Schrauwen-Hinderling V, Hoeks J, et al. (2010) Mitochondrial dysfunction and lipotoxicity. Biochim Biophys Acta 1801, 266-271.
16. Lee HC & Wei YH (2005) Mitochondrial biogenesis and mitochondrial DNA maintenance of mammalian cells under oxidative stress. Int J Biochem Cell Biol 37, 822-834.
17. Wilson-Fritch L, Burkart A, Bell G, et al. (2003) Mitochondrial biogenesis and remodeling during adipogenesis and in response to the insulin sensitizer rosiglitazone. Mol Cell Biol 23, 1085-1094. (Pubitemid 36133524)
18. Ishihara N, Eura Y & Mihara K (2004) Mitofusi n 1 and 2 play distinct roles in mitochondrial fusion reactions via GTPase activity. J Cell Sci 117, 6535-6546. (Pubitemid 40214575)
19. Yoon Y, Krueger EW, Oswald BJ, et al. (2003) The mitochondrial protein hFis1 regulates mitochondrial fission in mammalian cells through an interaction with the dynaminlike protein DLP1. Mol Cell Biol 23, 5409-5420. (Pubitemid 36950895)
20. Summers SA (2006) Ceramides in insulin resistance and lipotoxicity. Prog Lipid Res 45, 42-72. (Pubitemid 43170804)
21. Nishikawa T, Kukidome D, Sonoda K, et al. (2007) Impact of mitochondrial ROS production in the pathogenesis of insulin resistance. Diabetes Res Clin Pract 77, SUPPL.. 1, S161-S164. (Pubitemid 47212570)
22. Milagro FI, Campion J & Martinez JA (2006) Weight gain induced by high-fat feeding involves increased liver oxidative stress. Obesity (Silver Spring) 14, 1118-1123. (Pubitemid 46219677)
23. Esposito K, Ciotola M, Schisano B, et al. (2006) Oxidative stress in the metabolic syndrome . J Endocrinol Invest 29, 791-795. (Pubitemid 44869423)
24. Justo R, Boada J, Frontera M, et al. (2005) Gender dimorphism in rat liver mitochondrial oxidative metabolism and biogenesis. Am J Physiol Cell Physiol 289, C372-C378. (Pubitemid 41008883)
25. Gomez-Perez Y, Amengual-Cladera E, Catala-Niell A, et al. (2008) Gender dimorphism in high-fat-diet-induced insulin resistance in skeletal muscle of aged rats. Cell Physiol Biochem 22, 539-548.
26. Colom B, Alcolea MP, Valle A, et al. (2007) Skeletal muscle of female rats exhibit higher mitochondrial mass and oxidativephosphorylative capacities compared to males. Cel l Physiol Biochem 19, 205-212.
27. Nadal-Casellas A, Proenza AM, Gianotti M, et al. (2011) Brown adipose tissue redox status in response to dietaryinduced obesity-associated oxidative stress in male and female rats. Stress 14, 174-184.
28. Justo R, Frontera M, Pujol E, et al. (2005) Genderrelated differences in morphology and thermogenic capacity of brown adipose tissue mitochondrial subpopulations. Life Sci 76, 1147-1158. (Pubitemid 40037536)
29. Justo R, Oliver J & Gianotti M (2005) Brown adipose tissue mitochondrial subpopulations show different morphological and thermogenic characteristics. Mitochondrion 5, 45-53. (Pubitemid 40197724)
30. Guevara R, Santandreu FM, Valle A, et al. (2009) Sexdependent differences in aged rat brain mitochondrial function and oxidative stress. Free Radic Biol Med 46, 169-175.
31. Llado I, Rodriguez-Cuenca S, Pujol E, et al. (2002) Gender effects on adrenergic receptor expression and lipolysis in white adipose tissue of rats. Obes Res 10, 296-305. (Pubitemid 135688239)
32. Landt M, Gingerich RL, Havel PJ, et al. (1998) Radioimmunoassay of rat leptin: Sexual dimorphism reversed from humans. Clin Chem 44, 565-570. (Pubitemid 28141353)
33. Pickavance LC & Wilding JP (2007) Effects of S 15511, a therapeutic metabolite of the insulin-sensitizing agent S 15261, in the Zucker diabetic fatty rat. Diabetes Obes Metab 9, 114-120. (Pubitemid 44921049)
34. Thomas PS & Farquhar MN (1978) Specific measurement of DNA in nuclei and nucleic acids using diaminobenzoic acid. Anal Biochem 89, 35-44. (Pubitemid 9050339)
35. Lowry OH, Rosebrough NJ, Farr AL, et al. (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193, 265-275.
36. Koekemoer TC, Downing TG & Oelofsen W (1998) An alternative PCR assay for quantifying mito chondrial DNA in crude preparations. Nucleic Acids Res 26, 2829-2830. (Pubitemid 28297404)
37. Inagaki H, Hayashi T, Matsushima Y, et al. (2000) Isolation of rat mitochondrial transcription factor A (r-Tfam) cDNA. DNA Seq 11, 131-135. (Pubitemid 30448295)
38. Ali TK, Matragoon S, Pillai BA, et al. (2008) Peroxynitrite mediates retinal neurodegeneration by inhibiting nerve growth factor survival signaling in experimental and huma n diabetes. Diabetes 57, 889-898.
39. Virtue S & Vidal-Puig A (2010) Adipose tissue expandability, lipotoxicity and the metabolic syndrome-an allostatic perspective. Biochim Biophys Acta 1801, 338-349.
40. Bokarewa M, Nagaev I, Dahlberg L, et al. (2005) Resistin, an adipokine with potent proinflammatory properties. J Immunol 174, 5789-5795. (Pubitemid 40593223)
41. Fantuzzi G (2005) Adipose tissue, adipokines, and inflammation. J Allergy Clin Immunol 115, 911-919; quiz 20.
42. Perez C, Fernandez-Galaz C, Fernandez-Agullo T, et al. (2004) Leptin impairs insulin signaling in rat adipocytes. Diabetes 53, 347-353. (Pubitemid 38174549)
43. Rodriguez A, Catalan V, Becerril S, et al. (2008) Impaired adiponectin-AMPK signalling in insulin-sensitive tissues of hypertensive rats. Life Sci 83, 540-549.
44. Ye J (2011) Adipose tissue vascularization: Its role in chronic inflammation. Curr Diab Rep 11, 203-210.
45. Semenza GL (2004) Hydroxylation of HIF-1: Oxygen sensing at the molecular level. Physiology (Bethesda) 19, 176-182. (Pubitemid 39481932)
46. Forsythe JA, Jiang BH, Iyer NV, et al. (1996) Activation of vascular endothelial growth factor gene transcription by hypoxia-inducible factor Mol Cell Biol 16, 4604-4613. (Pubitemid 26272112)
47. Kietzmann T, Samoylenko A, Roth U, et al. (2003) Hypoxiainducible factor-1 and hypoxia response elements mediate the induction of plasminogen activator inhibitor-1 gene expression by insulin in primary rat hepatocyt es. Blood 101, 907-914. (Pubitemid 36139358)
48. Juhan-Vague I & Alessi MC (1997) PAI-1, obesity, insulin resistance and risk of cardiovascular events. Thromb Haemost 78, 656-660. (Pubitemid 27289322)
49. Gabriely I, Ma XH, Yang XM, et al. (2002) Removal of visceral fat prevents insulin resistance and glucose intolerance of aging: An adipokine-mediated process? Diabetes 51, 2951-2958.
50. Gui Y, Silha JV & Murphy LJ (2004) Sexual dimorphism and regulation of resistin, adiponectin, and leptin expression in the mouse. Obes Res 12, 1481-1491. (Pubitemid 41137454)
51. Harris RB, Ramsay TG, Smith SR, et al. (1996) Early and late stimulation of ob mRNA expression in meal-fed and overfed rats. J Clin Invest 97, 2020-2026. (Pubitemid 26143955)
52. La Cava A & Matarese G (2004) The weight of leptin in immunity. Nat Rev Immunol 4, 371-379. (Pubitemid 38649279)
53. Eells JT, Henry MM, Gross GJ, et al. (2000) Increased mitochondrial K(ATP) channel activity during chronic myocardial hypoxia: Is cardioprotection mediated by i mproved bioenergetics? Circ Res 87, 915-921.
54. Nisoli E, Clementi E, Moncada S, et al. (2004) Mitochondrial biogenesis as a cellular signaling framework. Biochem Pharmacol 67, 1-15. (Pubitemid 37518530)
55. Palmer CS, Osellame LD, Stojanovski D, et al. (2011) The regulation of mitochondrial morphology: Intricate mechanisms and dynamic machinery. Cell Signal 23, 1534-1545.
56. Cartoni R, Leger B, Hock MB, et al. (2005) Mitofusins 1/2 and ERRalpha expression are increased in human skeletal muscle after physical exercise. J Physiol 567, 349-358. (Pubitemid 41167327)
57. Pich S, Bach D, Briones P, et al. (2005) The Charcot- Marie-Tooth type 2A gene product, Mfn2, up-regulates fuel oxidation through expression of OXPHOS system. Hum Mol Genet 14, 1405-1415. (Pubitemid 40823451)
58. Chen H, Detmer SA, Ewald AJ, et al. (2003) Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development. J Cell Biol 160, 189-200. (Pubitemid 36254953)
59. Hori A, Yoshida M & Ling F (2011) Mitochondrial fusion increases the mitochondrial DNA copy number in budding yeast. Genes Cells 16, 527-544.
60. Chen H, McCaffery JM & Chan DC (2007) Mitochondrial fusion protects against neurodegeneration in the cerebellum. Cell 130, 548-562. (Pubitemid 47198302)
61. Chen H, Vermulst M, Wang YE, et al. (2010) Mitochondrial fusion is required for mtDNA stability in skeletal muscle and tolerance of mtDNA mutations. Cell 141, 280-289.
62. Ushio-Fukai M & Alexander RW (2004) Reactive oxyg en species as mediators of angiogenesis signaling: Role of NAD(P)H oxidase. Mol Cell Biochem 264, 85-97. (Pubitemid 39366107)
63. Bonello S, Zahringer C, BelAiba RS, et al. (2007) Reactive oxygen species activate the HIF-1alpha promoter via a functional NFkappaB site. Arterioscler Thromb Vasc Biol 27, 755-761. (Pubitemid 46606703)
64. Amengual-Cladera E, Lladó I, Gianotti M, et al. (2012) Sex differences in the effect of high -fat diet feeding on rat white adipose tissue mitochondrial function and insulin sensitivity. Metabolism (epublication ahead of print version 6 March 2012).
65. Romero M, Fernandez-Lopez JA, Esteve M, et al. (2009) Different modulation by dietary restriction of adipokine expression in white adipose tissue sites in the rat. Cardiovasc Diabetol 8, 42.
66. Frontini A & Cinti S (2010) Distribution and development of brown adipocytes in the murine and human adipose organ. Cell Metab 11, 253-256.
67. Gaidhu MP, Frontini A, Hung S, et al. (2011) Chronic AMP-kinase activation with AICAR reduces adiposity by remodel ing adipocyte metabolism and increasing leptin sensitivity. J Lipid Res 52, 1702-1711.
68. Salminen A, Hyttinen JM & Kaarniranta K (2011) AMPactivated protein kinase inhibits NF-kappaB signaling and inflammation: Impact on healthspan and lifespan. J Mol Med 89, 667-676.
69. Peairs A, Radjavi A, Davis S, et al. (2009) Activation of AMPK inhibits inflammation in MRL/lpr mouse mesangial cells. Clin Exp Immunol 156, 542-551.
70. Mattingly KA, Ivanova MM, Riggs KA, et al. (2008) Estradiol stimulates transcription of nuclear respiratory factor-1 and increases mitochondrial biogenesis. Mol Endocrinol 22, 609-622. (Pubitemid 351397789)
71. 71. Barros RP, Machado UF & Gustafsson JA (2006) Estrogen receptors: New players in diabetes mellitus. Trends Mol Med 12, 425-431. (Pubitemid 44308462)
72. Barros RP, Machado UF, Warner M, et al. (2006) Muscle GLUT4 regulation by estrogen receptors ERbeta and ERalpha. Proc Natl Acad Sci U S A 103, 1605-1608. (Pubitemid 43192077)
73. Riant E, Waget A, Cogo H , et al. (2009) Estrogens protect against high-fat diet-induced insulin resistance and glucose intolerance in mice. Endocrinology 150, 2109-2117.
74. Xu A, Chan KW, Hoo RL, et al. (2005) Testosterone selectively reduces the high molecular weight form of adiponectin by inhibiting its secretion from adipocytes. J Biol Chem 280, 18073-18080. (Pubitemid 41389052)
75. Hoyenga KB & Hoyenga KT (1982) Gender and energy balance: Sex differences in adaptations for feast and famine. Physiol Behav 28, 545-563. (Pubitemid 12116586)