Resistance training prevents dynamics and mitochondrial respiratory dysfunction in vastus lateralis muscle of ovariectomized rats

Experimental Gerontology - Tập 173 - Trang 112081 - 2023
Cecília Tardivo Marin1,2, Anderson Diogo de Souza Lino1, Iara Dinik Santos Avelar1, Marina Rodrigues Barbosa3, Gabriel Carlos Goulart Scarlato1, Diego Felipe Cavalini1, Fábio Tamanini1, André Vessoni Alexandrino1,4, Anibal Eugênio Vercesi5, Gilberto Eiji Shiguemoto1,2
1Department of Physiological Sciences, Interinstitutional Post-Graduate Program of Physiological Sciences, Federal University of São Carlos, UFSCar, Brazil
2Post-Graduate Program of Physiotherapy, Federal University of São Carlos, UFSCar, Brazil
3Federal University of Uberlândia, Uberlândia, MG, Brazil
4University Center Central Paulista – UNICEP, Brazil
5Laboratory of Mitochondrial Bioenergetics, State University of Campinas, Campinas, SP, Brazil

Tài liệu tham khảo

Anagnostis, 2015, Sarcopenia in post-menopausal women: is there any role for vitamin D?, Maturitas, 82, 56, 10.1016/j.maturitas.2015.03.014 Bach, 2003, Mitofusin-2 determines mitochondrial network architecture and mitochondrial metabolism a novel regulatory mechanism altered in obesity, J. Biol. Chem., 278, 17190, 10.1074/jbc.M212754200 Baker, 2007, Mitochondrial protein-import machinery: correlating structure with function, Trends Cell Biol., 17, 456, 10.1016/j.tcb.2007.07.010 Barbieri, 2013, Mitohormesis in muscle cells: a morphological, molecular, and proteomic approach, Muscles Ligaments Tendons J., 3, 254, 10.32098/mltj.04.2013.05 Barbosa, 2016, Resistance training and ovariectomy: antagonic effects in mitochondrial biogenesis markers in rat skeletal muscle, Int. J. Sports Med., 37, 841, 10.1055/s-0042-107247 Borrás, 2003, Mitochondria from females exhibit higher antioxidant gene expression and lower oxidative damage than males, Free Radic. Biol. Med., 34, 546, 10.1016/S0891-5849(02)01356-4 Brinton, 2012, Minireview: translational animal models of human menopause: challenges and emerging opportunities, Endocrinology, 153, 3571, 10.1210/en.2012-1340 Broskey, 2014, Skeletal muscle mitochondria in the elderly: effects of physical fitness and exercise training, J. Clin. Endocrinol. Metab., 99, 1852, 10.1210/jc.2013-3983 Brown, 2008, Skeletal muscle and bone: effect of sex steroids and aging, Adv. Physiol. Educ., 32, 120, 10.1152/advan.90111.2008 Brown, 2017, Expert consensus document: mitochondrial function as a therapeutic target in heart failure, Nat. Rev. Cardiol., 14, 238, 10.1038/nrcardio.2016.203 Campbell, 2003, 17beta-estradiol upregulates the expression of peroxisome proliferator-activated receptor alpha and lipid oxidative genes in skeletal muscle, J. Mol. Endocrinol., 31, 37, 10.1677/jme.0.0310037 Capllonch-Amer, 2014, Estradiol stimulates mitochondrial biogenesis and adiponectin expression in skeletal muscle, J. Endocrinol., 221, 391, 10.1530/JOE-14-0008 Carter, 2015, Mitochondria, muscle health, and exercise with advancing age, Physiology, 30, 208, 10.1152/physiol.00039.2014 Cartoni, 2005, Mitofusins 1/2 and ERRα expression are increased in human skeletal muscle after physical exercise, J. Physiol., 567, 349, 10.1113/jphysiol.2005.092031 Cavalcanti-de-Albuquerque, 2014, Role of estrogen on skeletal muscle mitochondrial function in ovariectomized rats: a time course study in different fiber types, J. Appl. Physiol., 116, 779, 10.1152/japplphysiol.00121.2013 Chance, 1955, Respiratory enzymes in oxidative phosphorylation I. Kinetics of oxygen utilization, J. Biol. Chem., 217, 383, 10.1016/S0021-9258(19)57189-7 Chen, 2004, Mitochondrial dynamics in mammals, Vol. 59, 119 Chen, 2003, Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development, J. Cell Biol., 160, 189, 10.1083/jcb.200211046 Chung, 2016, Association between leukocyte count and sarcopenia in postmenopausal women: the korean National Health and nutrition examination survey, Maturitas, 84, 89, 10.1016/j.maturitas.2015.11.011 Conceição, 2013, Sixteen weeks of resistance training can decrease the risk of metabolic syndrome in healthy postmenopausal women, Clin. Interv. Aging, 8, 1221, 10.2147/CIA.S44245 Dillon, 2012, The role of PGC-1 coactivators in aging skeletal muscle and heart, IUBMB Life, 64, 231, 10.1002/iub.608 Divakaruni, 2011, The regulation and physiology of mitochondrial proton leak, Physiology, 26, 192, 10.1152/physiol.00046.2010 Domingos, 2012, Resistance training restores the gene expression of molecules related to fat oxidation and lipogenesis in the liver of ovariectomized rats, Eur. J. Appl. Physiol., 112, 1437, 10.1007/s00421-011-2098-6 Figueiredo, 2008, Age-induced morphological, biochemical, and functional alterations in isolated mitochondria from murine skeletal muscle, J. Gerontol. Ser. A Biol. Med. Sci., 63, 350, 10.1093/gerona/63.4.350 Fisher, 1985, A transcription factor required for promoter recognition by human mitochondrial RNA polymerase. Accurate initiation at the heavy-and light-strand promoters dissected and reconstituted in vitro, J. Biol. Chem., 260, 11330, 10.1016/S0021-9258(17)39184-6 Fisher, 2000, Food restriction suppresses muscle growth and augments osteopenia in ovariectomized rats, J. Appl. Physiol., 88, 265, 10.1152/jappl.2000.88.1.265 Fonseca, 2012, Physical inactivity is a major contributor to ovariectomy-induced sarcopenia, Int. J. Sports Med., 33, 268, 10.1055/s-0031-1297953 Frankish, 2021, Effects of voluntary wheel running on mitochondrial content and dynamics in rat skeletal muscle, J. Muscle Res. Cell Motil., 42, 67, 10.1007/s10974-020-09580-9 Geukes, 2016, The impact of menopause on work ability in women with severe menopausal symptoms, Maturitas, 90, 3, 10.1016/j.maturitas.2016.05.001 Gnaiger, 2009, Capacity of oxidative phosphorylation in human skeletal muscle: new perspectives of mitochondrial physiology, Int. J. Biochem. Cell Biol., 41, 1837, 10.1016/j.biocel.2009.03.013 Gnaiger, 2012 Goncalves, 2015, Sites of superoxide and hydrogen peroxide production by muscle mitochondria assessed ex vivo under conditions mimicking rest and exercise, J. Biol. Chem., 290, 209, 10.1074/jbc.M114.619072 Griffiths, 2013, Menopause and work: an electronic survey of employees’ attitudes in the UK, Maturitas, 76, 155, 10.1016/j.maturitas.2013.07.005 Groennebaek, 2017, Impact of resistance training on skeletal muscle mitochondrial biogenesis, content, and function, Front. Physiol., 8, 713, 10.3389/fphys.2017.00713 Grundy, 2015 Halling, 2019, PGC-1α regulates mitochondrial properties beyond biogenesis with aging and exercise training, Am. J. Physiol. Endocrinol. Metab., 317, E513, 10.1152/ajpendo.00059.2019 Holloszy, 1967, Biochemical adaptations in muscle effects of exercise on mitochondrial oxygen uptake and respiratory enzyme activity in skeletal muscle, J. Biol. Chem., 242, 2278, 10.1016/S0021-9258(18)96046-1 Horcajada, 2008, Hesperidin inhibits ovariectomized-induced osteopenia and shows differential effects on bone mass and strength in young and adult intact rats, J. Appl. Physiol., 104, 648, 10.1152/japplphysiol.00441.2007 Hornberger, 2004, Physiological hypertrophy of the FHL muscle following 8 weeks of progressive resistance exercise in the rat, Can. J. Appl. Physiol., 29, 16, 10.1139/h04-002 Ignacio, 2022, Physical exercise improves mitochondrial function in ovariectomized rats, J. Endocrinol., 254, 77, 10.1530/JOE-22-0057 Jacobs, 2013, Mitochondria express enhanced quality as well as quantity in association with aerobic fitness across recreationally active individuals up to elite athletes, J. Appl. Physiol., 114, 344, 10.1152/japplphysiol.01081.2012 Johnston, 2008, Resistance training, sarcopenia, and the mitochondrial theory of aging, Appl. Physiol. Nutr. Metab., 33, 191, 10.1139/H07-141 Joseph, 2016, Beneficial effects of exercise on age-related mitochondrial dysfunction and oxidative stress in skeletal muscle, J. Physiol., 594, 5105, 10.1113/JP270659 Kim, 2017, Impact of aging and exercise on mitochondrial quality control in skeletal muscle, Oxidative Med. Cell. Longev., 2017, 10.1155/2017/3165396 Kitaoka, 2016, Combined effects of resistance training and calorie restriction on mitochondrial fusion and fission proteins in rat skeletal muscle, J. Appl. Physiol., 121, 806, 10.1152/japplphysiol.00465.2016 Kraemer, 2004, Fundamentals of resistance training: progression and exercise prescription, Med. Sci. Sports Exerc., 36, 674, 10.1249/01.MSS.0000121945.36635.61 Kuznetsov, 2008, Analysisof mitochondrialfunction in situ in permeabilizedmusclefibers, tis- sues andcells, Nat. Protoc., 3, 965, 10.1038/nprot.2008.61 Larsen, 2012, Biomarkers of mitochondrial content in skeletal muscle of healthy young human subjects, J. Physiol., 590, 3349, 10.1113/jphysiol.2012.230185 Legros, 2002, Mitochondrial fusion in human cells is efficient, requires the inner membrane potential, and is mediated by mitofusins, Mol. Biol. Cell, 13, 4343, 10.1091/mbc.e02-06-0330 Leite, 2009, Effects of ovariectomy and resistance training on lipid content in skeletal muscle, liver, and heart; fat depots; and lipid profile, Appl. Physiol. Nutr. Metab., 34, 1079, 10.1139/H09-116 Leite, 2010, Menopause: highlighting the effects of resistance training, Int. J. Sports Med., 31, 761, 10.1055/s-0030-1263117 Letellier, 1992, Mitochondrial myopathy studies on permeabilized muscle fibers 1, Pediatr. Res., 32, 17, 10.1203/00006450-199207000-00004 Lino, 2018, Resistance training and caloric restriction prevent systolic blood pressure rise by improving the nitric oxide effect on smooth muscle and morphological changes in the aorta of ovariectomized rats, PloS One, 13, 10.1371/journal.pone.0201843 Lionetti, 2013 Livak, 2001, Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method, Methods, 25, 402, 10.1006/meth.2001.1262 Manfredi, 2013, Post-menopausal effects of resistance training on muscle damage and mitochondria, J. Strength Cond. Res., 27, 556, 10.1519/JSC.0b013e318277a1e4 Marzetti, 2013, Mitochondrial dysfunction and sarcopenia of aging: from signaling pathways to clinical trials, Int. J. Biochem. Cell Biol., 45, 2288, 10.1016/j.biocel.2013.06.024 Medina-Contreras, 2020, Ovariectomized rodents as a menopausal metabolic syndrome model. A minireview, Mol. Cell. Biochem., 1 2011 Nilsson, 2019, Mitochondria and aging—The role of exercise as a countermeasure, Biology, 8, 40, 10.3390/biology8020040 No, 2020, Effects of aging and exercise training on mitochondrial function and apoptosis in the rat heart, Pflugers Arch. - Eur. J. Physiol., 472, 179, 10.1007/s00424-020-02357-6 Pereira, 2010, Effects of ovariectomy and resistance training on MMP-2 activity in rat calcaneal tendon, Connect. Tissue Res., 51, 459, 10.3109/03008201003676330 Pesta, 2011, Similar qualitative and quantitative changes of mitochondrial respiration following strength and endurance training in normoxia and hypoxia in sedentary humans, Am. J. Phys. Regul. Integr. Comp. Phys., 301, R1078 Peterson, 2012, Skeletal muscle mitochondria and aging: a review, J. Aging Res., 2012, 10.1155/2012/194821 Pighon, 2009, Resistance training attenuates fat mass regain after weight loss in ovariectomized rats, Maturitas, 64, 52, 10.1016/j.maturitas.2009.07.005 Porter, 2015, Resistance exercise training alters mitochondrial function in human skeletal muscle, Med. Sci. Sports Exerc., 47, 1922, 10.1249/MSS.0000000000000605 Prestes, 2009, Effects of ovariectomy and resistance training on MMP-2 activity in skeletal muscle, Appl. Physiol. Nutr. Metab., 34, 700, 10.1139/H09-059 Prestes, 2012, Resistance training and glycogen content in ovariectomized rats, Int. J. Sports Med., 33, 550, 10.1055/s-0032-1304646 Puigserver, 1998, A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis, Cell, 92, 829, 10.1016/S0092-8674(00)81410-5 Ribas, 2016, Skeletal muscle action of estrogen receptor α is critical for the maintenance of mitochondrial function and metabolic homeostasis in females, Sci. Transl. Med., 8, 10.1126/scitranslmed.aad3815 Rohas, 2007, A fundamental system of cellular energy homeostasis regulated by PGC-1α, Proc. Natl. Acad. Sci., 104, 7933, 10.1073/pnas.0702683104 Rolfe, 1996, Contribution of mitochondrial proton leak to skeletal muscle respiration and to standard metabolic rate, Am. J. Phys. Cell Phys., 271, C1380 Rolfe, 1999, Contribution of mitochondrial proton leak to respiration rate in working skeletal muscle and liver and to SMR, Am. J. Phys. Cell Phys., 276, C692 Salvadego, 2013, Skeletal muscle oxidative function in vivo and ex vivo in athletes with marked hypertrophy from resistance training, J. Appl. Physiol., 114, 1527, 10.1152/japplphysiol.00883.2012 Santel, 2003, Mitofusin-1 protein is a generally expressed mediator of mitochondrial fusion in mammalian cells, J. Cell Sci., 116, 2763, 10.1242/jcs.00479 Seo, 2010, New insights into the role of mitochondria in aging: mitochondrial dynamics and more, J. Cell Sci., 123, 2533, 10.1242/jcs.070490 Shepherd, 1969, Citrate synthase from rat liver:[EC 4.1. 3.7 citrate oxaloacetage-lyase (CoA-acetylating)], Vol. 13, 11 Sherk, 2017, Prior weight loss exacerbates the biological drive to gain weight after the loss of ovarian function, Physiol. Rep., 5, 10.14814/phy2.13272 Sherk, 2019, Impact of exercise and activity on weight regain and musculoskeletal health post-ovariectomy, Med. Sci. Sports Exerc., 51, 2465, 10.1249/MSS.0000000000002082 Shiguemoto, 2012, Effects of resistance training on matrix metalloproteinase-2 activity and biomechanical and physical properties of bone in ovariectomized and intact rats, Scand. J. Med. Sci. Sports, 22, 607, 10.1111/j.1600-0838.2010.01284.x Shimomura, 2002, Is leptin a key factor which develops obesity by ovariectomy?, Endocr. J., 49, 417, 10.1507/endocrj.49.417 Short, 2004, Age and aerobic exercise training effects on whole body and muscle protein metabolism, Am. J. Physiol. Endocrinol. Metab., 286, E92, 10.1152/ajpendo.00366.2003 Silva, 2009, Physical exercise increases mitochondrial function and reduces oxidative damage in skeletal muscle, Eur. J. Appl. Physiol., 105, 861, 10.1007/s00421-008-0971-8 Souza, 2007, Role of exercise training in cardiovascular autonomic dysfunction and mortality in diabetic ovariectomized rats, Hypertension, 50, 786, 10.1161/HYPERTENSIONAHA.107.095000 Tepp, 2011, High efficiency of energy flux controls within mitochondrial interactosome in cardiac intracellular energetic units, Biochim. Biophys. Acta, 1807, 1540 Torres, 2018, 17b-estradiol directly lowers mitochondrial membrane microviscosity and improves bioenergetic function in skeletal muscle, Cell Metab., 27, 167, 10.1016/j.cmet.2017.10.003 Viña, 2009, Mitochondrial biogenesis in exercise and in ageing, Adv. Drug Deliv. Rev., 61, 1369, 10.1016/j.addr.2009.06.006 Wang, 2010, Mitochondrial dysfunction in insulin insensitivity: implication of mitochondrial role in type 2 diabetes, Ann. N. Y. Acad. Sci., 1201, 157, 10.1111/j.1749-6632.2010.05625.x Wen, 2013, Increased muscle coenzyme Q10 in riboflavin responsive MADD with ETFDH gene mutations due to secondary mitochondrial proliferation, Mol. Genet. Metab., 109, 154, 10.1016/j.ymgme.2013.04.007 Wend, 2012, Tissue-specific effects of loss of estrogen during menopause and aging, Front. Endocrinol., 3, 19, 10.3389/fendo.2012.00019 Westermann, 2010, Mitochondrial fusion and fission in cell life and death, Nat. Rev. Mol. Cell Biol., 11, 872, 10.1038/nrm3013 Westermann, 2012, Bioenergetic role of mitochondrial fusion and fission, Biochim. Biophys. Acta Bioenerg., 1817, 1833, 10.1016/j.bbabio.2012.02.033 Wu, 1999, Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1, Cell, 98, 115, 10.1016/S0092-8674(00)80611-X Yan, 2012, Exercise training-induced regulation of mitochondrial quality, Exerc. Sport Sci. Rev., 40, 159, 10.1097/JES.0b013e3182575599 Yoo, 2018, Role of exercise in age-related sarcopenia, J. Exerc. Rehabil., 14, 551, 10.12965/jer.1836268.134 Yubero, 2016, A statistical algorithm showing coenzyme Q10 and citrate synthase as biomarkers for mitochondrial respiratory chain enzyme activities, Sci. Rep., 6, 1 Zoll, 2002, Physical activity changes the regulation of mitochondrial respiration in human skeletal muscle, J. Physiol., 543, 191, 10.1113/jphysiol.2002.019661