Chronic glucocorticoid exposure-induced epididymal adiposity is associated with mitochondrial dysfunction in white adipose tissue of male C57BL/6J mice

PLoS ONE

Volumn 9, Issue 11, 2014, Pages

  Yu, Jie ^a   Yu, Bing ^a   He, Jun ^a   Zheng, Ping ^a   Mao, Xiangbing ^a   Han, Guoquan ^a   Chen, Daiwen ^a  

^a SICHUAN AGRICULTURAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

CATALASE; CORTICOSTERONE; CYTOCHROME C; FATTY ACID; FATTY ACID SYNTHASE; FIBROBLAST GROWTH FACTOR 21; GLUTATHIONE PEROXIDASE; HORMONE SENSITIVE LIPASE; INSULIN; LEPTIN; MITOCHONDRIAL DNA; NICOTINAMIDE ADENINE DINUCLEOTIDE; NUCLEAR RESPIRATORY FACTOR 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; REACTIVE OXYGEN METABOLITE; SIRTUIN 1; SUPEROXIDE DISMUTASE; TRIACYLGLYCEROL; FIBROBLAST GROWTH FACTOR; GLUCOCORTICOID;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATGL GENE; BIOGENESIS; BODY COMPOSITION; BODY WEIGHT; CELL HYPERPLASIA; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; CPT1 ALPHA GENE; CYTC GENE; DEFENSE MECHANISM; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ENZYME ACTIVITY; ENZYME LINKED IMMUNOSORBENT ASSAY; EPIDIDYMAL ADIPOSITY; EPIDIDYMIS FAT; FAS GENE; FATTY ACID BLOOD LEVEL; GENE EXPRESSION; HORMONE BLOOD LEVEL; HSL GENE; IDH3 ALPHA GENE; INSULIN BLOOD LEVEL; LIPID ANALYSIS; LONG TERM EXPOSURE; MALE; MITOCHONDRIAL GENE; MOUSE; NONHUMAN; NRF 1 GENE; NUCLEOTIDE METABOLISM; NUCLEOTIDE SEQUENCE; OBESITY; PGC1 ALPHA GENE; PPAR GAMMA GENE; PROTEIN BLOOD LEVEL; QUANTITATIVE ANALYSIS; RADIOIMMUNOASSAY; REAL TIME POLYMERASE CHAIN REACTION; SIRT1 GENE; TRIACYLGLYCEROL BLOOD LEVEL; UPREGULATION; WHITE ADIPOSE TISSUE; ANIMAL; BLOOD; DRUG EFFECTS; EATING; EPIDIDYMIS; METABOLISM; MITOCHONDRION; PHYSIOLOGY;

MUS;

ADIPOSE TISSUE, WHITE; ADIPOSITY; ANIMALS; BODY WEIGHT; CORTICOSTERONE; EATING; EPIDIDYMIS; FATTY ACIDS, NONESTERIFIED; FIBROBLAST GROWTH FACTORS; GLUCOCORTICOIDS; INSULIN; LEPTIN; MALE; MICE; MITOCHONDRIA; REACTIVE OXYGEN SPECIES; TRIGLYCERIDES;

EID: 84911486946     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0112628     Document Type: Article

References (51)

1. Anagnostis P, Athyros VG, Tziomalos K, Karagiannis A, Mikhailidis DP (2009) Clinical review: The pathogenetic role of cortisol in the metabolic syndrome: a hypothesis. J Clin Endocrinol Metab 94: 2692-2701.
2. Liu D, Diorio J, Tannenbaum B, Caldji C, Francis D, et al. (1997) Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 277: 1659-1662.
3. Davies NA, Gillett A, McAlpine C, Seabrook L, Baxter G, et al. (2013) The effect of ACTH upon faecal glucocorticoid excretion in the koala. J Endocrinol.
4. Buttgereit F, Burmester GR, Lipworth BJ (2005) Optimised glucocorticoid therapy: the sharpening of an old spear. Lancet 365: 801-803.
5. Arnaldi G, Angeli A, Atkinson AB, Bertagna X, Cavagnini F, et al. (2003) Diagnosis and complications of Cushing's syndrome: a consensus statement. J Clin Endocrinol Metab 88: 5593-5602.
6. Minami I, Tateno T, Yoshimoto T, Doi M, Izumiyama H, et al. (2006) Subclinical Cushings disease with amelioration of metabolic comorbidities after removal of pituitary tumor. Intern Med 45: 1231-1235.
7. Alemany M (2013) Relationship between energy dense diets and white adipose tissue inflammation in metabolic syndrome. Nutr Res 33: 1-11.
8. Mayo-Smith W, Hayes CW, Biller BM, Klibanski A, Rosenthal H, et al. (1989) Body fat distribution measured with CT: correlations in healthy subjects, patients with anorexia nervosa, and patients with Cushing syndrome. Radiology 170: 515-518.
9. Galitzky J, Bouloumie A (2013) Human visceral-fat-specific glucocorticoid tuning of adipogenesis. Cell Metab 18: 3-5.
10. Masuzaki H, Paterson J, Shinyama H, Morton NM, Mullins JJ, et al. (2001) A transgenic model of visceral obesity and the metabolic syndrome. Science 294: 2166-2170.
11. Liu Y, Park F, Pietrusz JL, Jia G, Singh RJ, et al. (2008) Suppression of 11betahydroxysteroid dehydrogenase type 1 with RNA interference substantially attenuates 3T3-L1 adipogenesis. Physiol Genomics 32: 343-351.
12. Slavin BG, Ong JM, Kern PA (1994) Hormonal regulation of hormone-sensitive lipase activity and mRNA levels in isolated rat adipocytes. J Lipid Res 35: 1535-1541.
13. Divertie GD, Jensen MD, Miles JM (1991) Stimulation of lipolysis in humans by physiological hypercortisolemia. Diabetes 40: 1228-1232.
14. Djurhuus CB, Gravholt CH, Nielsen S, Mengel A, Christiansen JS, et al. (2002) Effects of cortisol on lipolysis and regional interstitial glycerol levels in humans. Am J Physiol Endocrinol Metab 283: E172-177.
15. Campbell JE, Peckett AJ, D'Souza A M, Hawke TJ, Riddell MC (2011) Adipogenic and lipolytic effects of chronic glucocorticoid exposure. Am J Physiol Cell Physiol 300: C198-209.
16. Patti ME, Corvera S (2010) The role of mitochondria in the pathogenesis of type 2 diabetes. Endocr Rev 31: 364-395.
17. Starkov AA (2008) The role of mitochondria in reactive oxygen species metabolism and signaling. Ann N Y Acad Sci 1147: 37-52.
18. Owen OE, Kalhan SC, Hanson RW (2002) The key role of anaplerosis and cataplerosis for citric acid cycle function. J Biol Chem 277: 30409-30412.
19. Wilson-Fritch L, Nicoloro S, Chouinard M, Lazar MA, Chui PC, et al. (2004) Mitochondrial remodeling in adipose tissue associated with obesity and treatment with rosiglitazone. J Clin Invest 114: 1281-1289.
20. Rong JX, Qiu Y, Hansen MK, Zhu L, Zhang V, et al. (2007) Adipose mitochondrial biogenesis is suppressed in db/db and high-fat diet-fed mice and improved by rosiglitazone. Diabetes 56: 1751-1760.
21. Okamoto Y, Higashiyama H, Rong JX, McVey MJ, Kinoshita M, et al. (2007) Comparison of mitochondrial and macrophage content between subcutaneous and visceral fat in db/db mice. Exp Mol Pathol 83: 73-83.
22. Kaaman M, Sparks LM, van Harmelen V, Smith SR, Sjolin E, et al. (2007) Strong association between mitochondrial DNA copy number and lipogenesis in human white adipose tissue. Diabetologia 50: 2526-2533.
23. Tedesco L, Valerio A, Cervino C, Cardile A, Pagano C, et al. (2008)Cannabinoid type 1 receptor blockade promotes mitochondrial biogenesis through endothelial nitric oxide synthase expression in white adipocytes. Diabetes 57: 2028-2036.
24. Nishino N, Tamori Y, Tateya S, Kawaguchi T, Shibakusa T, et al. (2008) FSP27 contributes to efficient energy storage in murine white adipocytes by promoting the formation of unilocular lipid droplets. J Clin Invest 118: 2808-2821.
25. Karatsoreos IN, Bhagat SM, Bowles NP, Weil ZM, Pfaff DW, et al. (2010) Endocrine and physiological changes in response to chronic corticosterone: a potential model of the metabolic syndrome in mouse. Endocrinology 151: 2117-2127.
26. Seale P, Conroe HM, Estall J, Kajimura S, Frontini A, et al. (2011) Prdm16 determines the thermogenic program of subcutaneous white adipose tissue in mice. J Clin Invest 121: 96-105.
27. Liu J, Chen D, Yao Y, Yu B, Mao X, et al. (2012) Intrauterine growth retardation increases the susceptibility of pigs to high-fat diet-induced mitochondrial dysfunction in skeletal muscle. PLoS One 7: e34835.
28. Yu J, Zhao L, Wang A, Eleswarapu S, Ge X, et al. (2012) Growth hormone stimulates transcription of the fibroblast growth factor 21 gene in the liver through the signal transducer and activator of transcription 5. Endocrinology 153: 750-758.
29. Yu J, Yu B, Jiang H, Chen D (2012) Conjugated linoleic acid induces hepatic expression of fibroblast growth factor 21 through PPAR-alpha. Br J Nutr 107: 461-465.
30. D'Antona G, Ragni M, Cardile A, Tedesco L, Dossena M, et al. (2010) Branched-chain amino acid supplementation promotes survival and supports cardiac and skeletal muscle mitochondrial biogenesis in middle-aged mice. Cell Metab 12: 362-372.
31. Grundy SM, Brewer HB Jr, Cleeman JI, Smith SC Jr, Lenfant C (2004) Definition of metabolic syndrome: Report of the National Heart, Lung, and Blood Institute/American Heart Association conference on scientific issues related to definition. Circulation 109: 433-438.
32. Murray F, Smith DW, Hutson PH (2008) Chronic low dose corticosterone exposure decreased hippocampal cell proliferation, volume and induced anxiety and depression like behaviours in mice. Eur J Pharmacol 583: 115-127.
33. Rees SL, Panesar S, Steiner M, Fleming AS (2004) The effects of adrenalectomy and corticosterone replacement on maternal behavior in the postpartum rat. Horm Behav 46: 411-419.
34. Cassano AE, White JR, Penraat KA, Wilson CD, Rasmussen S, et al. (2012) Anatomic, hematologic, and biochemical features of C57BL/6NCrl mice maintained on chronic oral corticosterone. Comp Med 62: 348-360.
35. Stewart PM (2005) Tissue-specific Cushing's syndrome uncovers a new target in treating the metabolic syndrome-11beta-hydroxysteroid dehydrogenase type 1. Clin Med 5: 142-146.
36. Stewart PM (2003) Tissue-specific Cushing's syndrome, 11beta-hydroxysteroid dehydrogenases and the redefinition of corticosteroid hormone action. Eur J Endocrinol 149: 163-168.
37. Schuff KG (2003) Issues in the diagnosis of Cushing's syndrome for the primary care physician. Prim Care 30: 791-799.
38. Hassan-Smith Z, Morgan S, Sherlock M, Bujalska I, Tomlinson J, et al. (2014) 11b-hydroxysteroid dehydrogenase type 1 and age-associated muscle weakness in mice: implications for human ageing. The Lancet 383: S53.
39. Pezaro C, Mukherji D, Tunariu N, Cassidy A, Omlin A, et al. (2013) Sarcopenia and change in body composition following maximal androgen suppression with abiraterone in men with castration-resistant prostate cancer. British journal of cancer 109: 325-331.
40. Lee MJ, Fried SK (2012) Glucocorticoids antagonize tumor necrosis factor-alpha- stimulated lipolysis and resistance to the antilipolytic effect of insulin in human adipocytes. Am J Physiol Endocrinol Metab 303: E1126-1133.
41. Berdanier CD (1989) Role of glucocorticoids in the regulation of lipogenesis. FASEB J 3: 2179-2183.
42. Gathercole LL, Morgan SA, Bujalska IJ, Hauton D, Stewart PM, et al. (2011) Regulation of lipogenesis by glucocorticoids and insulin in human adipose tissue. PLoS One 6: e26223.
43. Xu C, He J, Jiang H, Zu L, Zhai W, et al. (2009) Direct effect of glucocorticoids on lipolysis in adipocytes. Mol Endocrinol 23: 1161-1170.
44. Lundgren M, Buren J, Lindgren P, Myrnas T, Ruge T, et al. (2008) Sex- and depot-specific lipolysis regulation in human adipocytes: interplay between adrenergic stimulation and glucocorticoids. Horm Metab Res 40: 854-860.
45. Nunnari J, Suomalainen A (2012) Mitochondria: in sickness and in health. Cell 148: 1145-1159.
46. Demonacos C, Djordjevic-Markovic R, Tsawdaroglou N, Sekeris CE (1995) The mitochondrion as a primary site of action of glucocorticoids: the interaction of the glucocorticoid receptor with mitochondrial DNA sequences showing partial similarity to the nuclear glucocorticoid responsive elements. J Steroid Biochem Mol Biol 55: 43-55.
47. Tsiriyotis C, Spandidos DA, Sekeris CE (1997) The mitochondrion as a primary site of action of glucocorticoids: mitochondrial nucleotide sequences, showing similarity to hormone response elements, confer dexamethasone inducibility to chimaeric genes transfected in LATK- cells. Biochem Biophys Res Commun 235: 349-354.
48. Tang VM, Young AH, Tan H, Beasley C, Wang JF (2013) Glucocorticoids increase protein carbonylation and mitochondrial dysfunction. Horm Metab Res 45: 709-715.
49. Murphy MP (2013) Mitochondrial dysfunction indirectly elevates ROS production by the endoplasmic reticulum. Cell Metab 18: 145-146.
50. Wang M (2005) The role of glucocorticoid action in the pathophysiology of the metabolic syndrome. Nutr Metab 2: 1-14.
51. Lu RH, Ji H, Chang ZG, Su SS, Yang GS (2010) Mitochondrial development and the influence of its dysfunction during rat adipocyte differentiation. Mol Biol Rep 37: 2173-2182.