Estradiol stimulates mitochondrial biogenesis and adiponectin expression in skeletal muscle

Journal of Endocrinology

Volumn 221, Issue 3, 2014, Pages 391-403

  Capllonch Amer, Gabriela ^a   Sbert Roig, Miquel ^a   Galmés Pascual, Bel M ^a   Proenza, Ana M ^a,b   Lladó, Isabel ^a,b   Gianotti, Magdalena ^a,b   García Palmer, Francisco J ^a,b  

^a UNIVERSITAT DE LES ILLES BALEARS   (Spain)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

17 estradiol; Adiponectin; L6E9; Mitochondrial biogenesis; Mitochondrial dynamics; Ovariectomy; Skeletal muscle; Testosterone

Indexed keywords

ADIPONECTIN; ADIPONECTIN RECEPTOR 1; ESTRADIOL; MARKER; PROGESTERONE; SEX HORMONE; TESTOSTERONE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOGENESIS; CONTROLLED STUDY; FEMALE; HORMONE BLOOD LEVEL; IN VITRO STUDY; IN VIVO STUDY; MITOCHONDRION; MYOTUBE; NONHUMAN; OVARIECTOMY; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SEX DIFFERENCE; SKELETAL MUSCLE; UPREGULATION;

17Β-ESTRADIOL; ADIPONECTIN; L6E9; MITOCHONDRIAL BIOGENESIS; MITOCHONDRIAL DYNAMICS; OVARIECTOMY; SKELETAL MUSCLE; TESTOSTERONE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADIPONECTIN; ANIMALS; ANIMALS, NEWBORN; BLOTTING, WESTERN; CELLS, CULTURED; ESTRADIOL; ESTROGENS; FATTY ACIDS, NONESTERIFIED; FEMALE; MALE; MICROSCOPY, CONFOCAL; MITOCHONDRIA, MUSCLE; MITOCHONDRIAL PROTEINS; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; OVARIECTOMY; OXIDATION-REDUCTION; PROGESTERONE; RATS; RATS, WISTAR; RECEPTORS, ADIPONECTIN; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TESTOSTERONE;

EID: 84901645527     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1530/JOE-14-0008     Document Type: Article

References (70)

1. Amengual-Cladera E, Llado I, Gianotti M & Proenza AM 2012a Retroperitoneal white adipose tissue mitochondrial function and adiponectin expression in response to ovariectomy and 17β-estradiol replacement. Steroids 77 659-665. (doi:10.1016/j.steroids.2012.02.012)
2. Amengual-Cladera E, Llado I, Gianotti M & Proenza AM 2012b Sex differences in the effect of high-fat diet feeding on rat white adipose tissue mitochondrial function and insulin sensitivity. Metabolism 61 1108-1117. (doi:10.1016/j.metabol.2011.12.016)
3. Amengual-Cladera E, Llado I, Proenza AM & GianottiM 2012c 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 109 413-424. (doi:10.1016/j.metabol.2011. 12.016)
4. 2 generation. American Journal of Physiology. Cell Physiology 290 C844-C851. (doi:10.1152/ajpcell.00402.2005)
5. Attardi G & Schatz G 1988 Biogenesis of mitochondria. Annual Review of Cell Biology 4 289-333. (doi:10.1146/annurev.cb.04.110188.001445)
6. Ayres S, Tang M & Subbiah MT 1996 Estradiol-17β as an antioxidant: some distinct features when compared with common fat-soluble antioxidants. Journal of Laboratory and Clinical Medicine 128 367-375. (doi:10.1016/S0022-2143(96)80008-4)
7. Bradford MM 1976 A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72 248-254. (doi:10.1016/0003-2697(76)90527-3)
8. Brand MD, Pamplona R, Portero-Otin M, Requena JR, Roebuck SJ, Buckingham JA, Clapham JC & Cadenas S 2002 Oxidative damage and phospholipid fatty acyl composition in skeletal muscle mitochondria from mice underexpressing or overexpressing uncoupling protein 3. Biochemical Journal 368 597-603. (doi:10.1042/BJ20021077)
9. Burelle Y & Hochachka PW 2002 Endurance training induces musclespecific changes in mitochondrial function in skinned muscle fibers. Journal of Applied Physiology 92 2429-2438. (doi:10.1152/japplphysiol. 01024.2001)
10. Català-Niell A, Estrany ME, Proenza AM, GianottiM& Llado I 2008 Skeletal muscle and liver oxidative metabolism in response to a voluntary isocaloric intake of a high fat diet in male and female rats. Cellular Physiology and Biochemistry 22 327-336. (doi:10.1159/000149811)
11. Cavalcanti-de-Albuquerque JP, Salvador ID,Martins EG, Jardim-MessederD, Werneck de Castro JP, Galina A & de Carvalho DP 2014 Role of estrogen on skeletal muscle mitochondrial function in ovariectomized rats: a time course study in different fiber types. Journal of Applied Physiology 116 779-789. (doi:10.1152/japplphysiol.00121.2013)
12. Chen H & Chan DC 2004 Mitochondrial dynamics in mammals. Current Topics in Developmental Biology 59 119-144. (doi:10.1016/S0070-2153(04)59005-1)
13. Chen J, Li Y, Lavigne JA, Trush MA & Yager JD 1999 Increased mitochondrial superoxide production in rat liver mitochondria, rat hepatocytes, and HepG2 cells following ethinyl estradiol treatment. Toxicological Sciences 51 224-235. (doi:10.1093/toxsci/51.2.224)
14. Chen JQ, Brown TR & Russo J 2009 Regulation of energy metabolism pathways by estrogens and estrogenic chemicals and potential implications in obesity associated with increased exposure to endocrine disruptors. Biochimica et Biophysica Acta 1793 1128-1143. (doi:10.1016/j.bbamcr.2009.03.009)
15. Chrzanowska-Lightowlers ZM, Turnbull DM & Lightowlers RN 1993 A microtiter plate assay for cytochrome c oxidase in permeabilized whole cells. Analytical Biochemistry 214 45-49. (doi:10.1006/abio. 1993.1454)
16. Civitarese AE, Ukropcova B, Carling S, Hulver M, DeFronzo RA, Mandarino L, Ravussin E & Smith SR 2006 Role of adiponectin in human skeletal muscle bioenergetics. Cell Metabolism 4 75-87. (doi:10.1016/j.cmet.2006.05.002)
17. Colom B, Alcolea MP, Valle A, Oliver J, Roca P & Garcia-Palmer FJ 2007a Skeletal muscle of female rats exhibit higher mitochondrial mass and oxidative-phosphorylative capacities compared to males. Cellular Physiology and Biochemistry 19 205-212. (doi:10.1159/000099208)
18. Colom B, Oliver J, Roca P & Garcia-Palmer FJ 2007b Caloric restriction and gender modulate cardiac muscle mitochondrial H2O2 production and oxidative damage. Cardiovascular Research 74 456-465. (doi:10.1016/j.cardiores.2007.02.001)
19. Deepa SS & Dong LQ 2009 APPL1: role in adiponectin signaling and beyond. American Journal of Physiology. Endocrinology and Metabolism 296 E22-E36. (doi:10.1152/ajpendo.90731.2008)
20. Dighe AS & Sluss PM 2004 Improved detection of serum estradiol after sample extraction procedure. Clinical Chemistry 50 764-766. (doi:10.1373/clinchem.2003.029553)
21. Ding G, Qin Q, He N, Francis-David SC, Hou J, Liu J, Ricks E & Yang Q 2007 Adiponectin and its receptors are expressed in adult ventricular cardiomyocytes and upregulated by activation of peroxisome proliferator-activated receptor g. Journal of Molecular and Cellular Cardiology 43 73-84. (doi:10.1016/j.yjmcc.2007.04.014)
22. Gómez-Pérez Y, Amengual-Cladera E, Catala-Niell A, Thomas-Moya E, Gianotti M, Proenza AM & Llado I 2008 Gender dimorphism in high-fat-diet-induced insulin resistance in skeletal muscle of aged rats. Cellular Physiology and Biochemistry 22 539-548. (doi:10.1159/000185538)
23. Gómez-Pérez Y, Gianotti M, Proenza AM& Llado I 2011 Age-related decline of skeletal muscle insulin sensitivity in rats: effect of sex and muscle type. Rejuvenation Research 14 153-161. (doi:10.1089/rej.2010.1107)
24. Gómez-Pérez Y, Capllonch-Amer G, Gianotti M, Llado I & Proenza AM 2012 Long-term high-fat-diet feeding induces skeletal muscle mitochondrial biogenesis in rats in a sex-dependent and muscle-type specific manner. Nutrition and Metabolism 9 15. (doi:10.1186/1743-7075-9-15)
25. Guevara R, Santandreu FM, Valle A, Gianotti M, Oliver J & Roca P 2009 Sex-dependent differences in aged rat brain mitochondrial function and oxidative stress. Free Radical Biology & Medicine 46 169-175. (doi:10.1016/j.freeradbiomed.2008.09.035)
26. Harwood HJ Jr 2012 The adipocyte as an endocrine organ in the regulation of metabolic homeostasis. Neuropharmacology 63 57-75. (doi:10.1016/j.neuropharm.2011.12.010)
27. Iwabu M, Yamauchi T, Okada-Iwabu M, Sato K, Nakagawa T, Funata M, Yamaguchi M, Namiki S, Nakayama R, TabataMet al. 2010 Adiponectin and AdipoR1 regulate PGC-1a and mitochondria by Ca2C and AMPK/SIRT1. Nature 464 1313-1319. (doi:10.1038/nature08991)
28. Jortay J, Senou M, Abou-Samra M, Noel L, Robert A, Many MC & Brichard SM 2012 Adiponectin and skeletal muscle: pathophysiological implications in metabolic stress. American Journal of Pathology 181 245-256. (doi:10.1016/j.ajpath.2012.03.035)
29. Klinge CM 2008 Estrogenic control of mitochondrial function and biogenesis. Journal of Cellular Biochemistry 105 1342-1351. (doi:10.1002/jcb.21936)
30. Koh EH, Park JY, Park HS, Jeon MJ, Ryu JW, Kim M, Kim SY, Kim MS, Kim SW, Park IS et al. 2007 Essential role of mitochondrial function in adiponectin synthesis in adipocytes. Diabetes 56 2973-2981. (doi:10.2337/db07-0510)
31. Krause MP, Liu Y, Vu V, Chan L, Xu A, Riddell MC, Sweeney G & Hawke TJ 2008 Adiponectin is expressed by skeletal muscle fibers and influences muscle phenotype and function. American Journal of Physiology. Cell Physiology 295 C203-C212. (doi:10.1152/ajpcell.00030.2008)
32. Liu Y, Chewchuk S, Lavigne C, Brule S, Pilon G, Houde V, Xu A, Marette A & Sweeney G 2009a Functional significance of skeletal muscle adiponectin production, changes in animal models of obesity and diabetes, and regulation by rosiglitazone treatment. American Journal of Physiology. Endocrinology and Metabolism 297 E657-E664. (doi:10.1152/ajpendo.00186.2009)
33. Liu YH, Huang Y & Shao X 2009b Effects of estrogen on genioglossal muscle contractile properties and fiber-type distribution in chronic intermittent hypoxia rats. European Journal of Oral Sciences 117 685-690. (doi:10.1111/j.1600-0722.2009.00681.x)
34. Liu YH, Jia SS & Hou YX 2009c Effects of ovariectomy on rat genioglossal muscle contractile properties and fiber-type distribution. Angle Orthodontist 79 509-514. (doi:10.2319/031608-149.1)
35. 3 regulates global mitochondrial lysine acetylation. Molecular and Cellular Biology 27 8807-8814. (doi:10.1128/MCB.01636-07)
36. Macari C, Teyssier C, Tribollet V, Mouzat K, Forcet C, Horard B, Lobaccaro JM & Vanacker JM 2010 Estrogens repress PGC1-a expression in the uterus. Molecular and Cellular Endocrinology 330 33-40. (doi:10.1016/j.mce.2010.08.003)
37. Mattingly KA, Ivanova MM, Riggs KA, Wickramasinghe NS, Barch MJ & Klinge CM 2008 Estradiol stimulates transcription of nuclear respiratory factor-1 and increases mitochondrial biogenesis. Molecular Endocrinology 22 609-622. (doi:10.1210/me.2007-0029)
38. Mattson MP, Robinson N & Guo Q 1997 Estrogens stabilize mitochondrial function and protect neural cells against the pro-apoptotic action of mutant presenilin-1. Neuroreport 8 3817-3821. (doi:10.1097/00001756-199712010-00031)
39. Moran AL, Warren GL & Lowe DA 2006 Removal of ovarian hormones from mature mice detrimentally affects muscle contractile function and myosin structural distribution. Journal of Applied Physiology 100 548-559. (doi:10.1152/japplphysiol.01029.2005)
40. Moran AL, Nelson SA, Landisch RM, Warren GL & Lowe DA 2007 Estradiol replacement reverses ovariectomy-induced muscle contractile and myosin dysfunction in mature femalemice. Journal of Applied Physiology 102 1387-1393. (doi:10.1152/japplphysiol.01305.2006)
41. Moreira PI, Custodio JB, Nunes E, Oliveira PJ, Moreno A, Seica R, Oliveira CR & Santos MS 2011 Mitochondria from distinct tissues are differently affected by 17β-estradiol and tamoxifen. Journal of Steroid Biochemistry and Molecular Biology 123 8-16. (doi:10.1016/j.jsbmb.2010. 09.004)
42. Nadal-Casellas A, Proenza AM, Gianotti M & Lladó I 2011a Brown adipose tissue redox status in response to dietary-induced obesity-associated oxidative stress in male and female rats. Stress 14 174-184. (doi:10.3109/10253890.2010.52468)
43. Nadal-Casellas A, Proenza AM, Llado I & Gianotti M 2011b Effects of ovariectomy and 17-b estradiol replacement on rat brown adipose tissue mitochondrial function. Steroids 76 1051-1056. (doi:10.1016/j.steroids.2011.04.009)
44. Nadal-Casellas A, Proenza AM, Llado I & Gianotti M 2012 Sex-dependent differences in rat hepatic lipid accumulation and insulin sensitivity in response to diet-induced obesity. Biochemistry and Cell Biology 90 164-172. (doi:10.1139/o11-069)
45. Nakano K, Tarashima M, Tachikawa E, Noda N, Nakayama T, Sasaki K, Mizoguchi E, Matsuzaki M & Osawa M 2005 Platelet mitochondrial evaluation during cytochrome c and dichloroacetate treatments of MELAS. Mitochondrion 5 426-433. (doi:10.1016/j.mito.2005.10.002)
46. Pantaleao TU, Mousovich F, Rosenthal D, Padron AS, Carvalho DP & da Costa VM 2010 Effect of serum estradiol and leptin levels on thyroid function, food intake and body weight gain in female Wistar rats. Steroids 75 638-642. (doi:10.1016/j.steroids.2010.03.009)
47. Patel SA, Hoehn KL, Lawrence RT, Sawbridge L, Talbot NA, Tomsig JL, Turner N, Cooney GJ, Whitehead JP, Kraegen EW et al. 2012 Overexpression of the adiponectin receptor AdipoR1 in rat skeletal muscle amplifies local insulin sensitivity. Endocrinology 153 5231-5246. (doi:10.1210/en.2012-1368)
48. Picard M, Csukly K, Robillard ME, Godin R, Ascah A, Bourcier-Lucas C & Burelle Y 2008 Resistance to Ca2C-induced opening of the permeability transition pore differs in mitochondria from glycolytic and oxidative muscles. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 295 R659-R668. (doi:10.1152/ajpregu. 90357.2008)
49. Picard M, Hepple RT & Burelle Y 2012 Mitochondrial functional specialization in glycolytic and oxidative muscle fibers: tailoring the organelle for optimal function. American Journal of Physiology. Cell Physiology 302 C629-C641. (doi:10.1152/ajpcell.00368.2011)
50. Puigserver P & Spiegelman BM 2003 Peroxisome proliferator-activated receptor-g coactivator 1a (PGC-1a): transcriptional coactivator and metabolic regulator. Endocrine Reviews 24 78-90. (doi:10.1210/er.2002-0012)
51. Quick KL, Hardt JI & Dugan LL 2000 Rapid microplate assay for superoxide scavenging efficiency. Journal of Neuroscience Methods 97 139-144. (doi:10.1016/S0165-0270(00)00179-5)
52. Riestra P, Garcia-Anguita A, Ortega L & Garces C 2013 Relationship of adiponectin with sex hormone levels in adolescents. Hormone Research in Paediatrics 79 83-87. (doi:10.1159/000346898)
53. Rodríguez-Cuenca S, Monjo M, Gianotti M, Proenza AM & Roca P 2007 Expression of mitochondrial biogenesis-signaling factors in brown adipocytes is influenced specifically by 17β-estradiol, testosterone, and progesterone. American Journal of Physiology. Endocrinology and Metabolism 292 E340-E346. (doi:10.1152/ajpendo.00175.2006)
54. Scarpulla RC 2011 Metabolic control of mitochondrial biogenesis through the PGC-1 family regulatory network. Biochimica et Biophysica Acta 1813 1269-1278. (doi:10.1016/j.bbamcr.2010.09.019)
55. Schwer B, Bunkenborg J, Verdin RO, Andersen JS & Verdin E 2006 Reversible lysine acetylation controls the activity of the mitochondrial enzyme acetyl-CoA synthetase 2. PNAS 103 10224-10229. (doi:10.1073/pnas.0603968103)
56. Simpson ER 2003 Sources of estrogen and their importance. Journal of Steroid Biochemistry and Molecular Biology 86 225-230. (doi:10.1016/S0960-0760(03)00360-1)
57. Smith AD, Morris VC & Levander OA 2001 Rapid determination of glutathione peroxidase and thioredoxin reductase activities using a 96-well microplate format: comparison to standard cuvette-based assays. International Journal for Vitamin and Nutrition Research 71 87-92. (doi:10.1024/0300-9831.71.1.87)
58. Thomas PS & Farquhar MN 1978 Specific measurement of DNA in nuclei and nucleic acids using diaminobenzoic acid. Analytical Biochemistry 89 35-44. (doi:10.1016/0003-2697(78)90724-8)
59. Uribe M, Zamora-Valdes D, Moreno-Portillo M, Bermejo-Martinez L, Pichardo-Bahena R, Baptista-Gonzalez HA, Ponciano-Rodriguez G, Uribe MH, Medina-Santillan R & Mendez-Sanchez N 2008 Hepatic expression of ghrelin and adiponectin and their receptors in patients with nonalcoholic fatty liver disease. Annals of Hepatology 7 67-71.
60. Valle A, Garcia-Palmer FJ, Oliver J & Roca P 2007a Sex differences in brown adipose tissue thermogenic features during caloric restriction. Cellular Physiology and Biochemistry 19 195-204. (doi:10.1159/000099207)
61. Valle A, Guevara R, Garcia-Palmer FJ, Roca P & Oliver J 2007b Sexual dimorphism in liver mitochondrial oxidative capacity is conserved under caloric restriction conditions. American Journal of Physiology. Cell Physiology 293 C1302-C1308. (doi:10.1152/ajpcell. 00203.2007)
62. Ventura-Clapier R, Garnier A & Veksler V 2008 Transcriptional control of mitochondrial biogenesis: the central role of PGC-1a. Cardiovascular Research 79 208-217. (doi:10.1093/cvr/cvn098)
63. Vidal-Puig AJ, Grujic D, Zhang CY, Hagen T, Boss O, Ido Y, Szczepanik A, Wade J, Mootha V, Cortright R et al. 2000 Energy metabolism in uncoupling protein 3 gene knockout mice. Journal of Biological Chemistry 275 16258-16266. (doi:10.1074/jbc.M910179199)
64. Viña J, Gambini J, Lopez-Grueso R, Abdelaziz KM, Jove M & Borras C 2011 Females live longer than males: role of oxidative stress. Current Pharmaceutical Design 17 3959-3965. (doi:10.2174/138161211798764942)
65. Wang CH, Wang CC, Huang HC & Wei YH 2013 Mitochondrial dysfunction leads to impairment of insulin sensitivity and adiponectin secretion in adipocytes. FEBS Journal 280 1039-1050. (doi:10.1111/febs.12096)
66. Wildman RP, Wang D, Fernandez I, Mancuso P, Santoro N, Scherer PE & Sowers MR 2013 Associations of testosterone and sex hormone binding globulin with adipose tissue hormones in midlife women. Obesity 21 629-636. (doi:10.1002/oby.20256)
67. Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, Troy A, Cinti S, Lowell B, Scarpulla RC et al. 1999 Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98 115-124. (doi:10.1016/S0092-8674(00)80611-X)
68. Yaffe D 1968 Retention of differentiation potentialities during prolonged cultivation of myogenic cells. PNAS 61 477-483. (doi:10.1073/pnas.61. 2.477)
69. Yamauchi T, Kamon J, Ito Y, Tsuchida A, Yokomizo T, Kita S, Sugiyama T, Miyagishi M, Hara K, Tsunoda M et al. 2003 Cloning of adiponectin receptors that mediate antidiabetic metabolic effects. Nature 423 762-769. (doi:10.1038/nature01705)
70. Zhao H, Tian Z, Hao J & Chen B 2005 Extragonadal aromatization increases with time after ovariectomy in rats. Reproductive Biology and Endocrinology 3 6. (doi:10.1186/1477-7827-3-6)