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Maternal exercise during pregnancy modulates mitochondrial function and redox status in a sex-dependent way in adult offspring’s skeletal muscle

Published online by Cambridge University Press:  05 May 2021

R.M. Hözer Open the ORCID record for R.M. Hözer [Opens in a new window] ,
B.G. dos Santos Open the ORCID record for B.G. dos Santos [Opens in a new window] ,
P.M. August ,
K.S. Rodrigues ,
R.M. Maurmann ,
E.B. Flores  and
C. Matté Open the ORCID record for C. Matté [Opens in a new window]
R.M. Hözer
Affiliation:
Programa de Pós-Graduação em Ciências Biológicas – Bioquímica, Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil
B.G. dos Santos
Affiliation:
Programa de Pós-Graduação em Ciências Biológicas – Bioquímica, Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil
P.M. August
Affiliation:
Programa de Pós-Graduação em Ciências Biológicas – Bioquímica, Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil
K.S. Rodrigues
Affiliation:
Programa de Pós-Graduação em Ciências Biológicas – Bioquímica, Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil
R.M. Maurmann
Affiliation:
Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil
E.B. Flores
Affiliation:
Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil
C. Matté*
Affiliation:
Programa de Pós-Graduação em Ciências Biológicas – Bioquímica, Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil Programa de Pós-graduação em Ciências Biológicas – Fisiologia, Instituto de Ciências Básicas da Saúde, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil
*
Address for correspondence: C. Matté, Programa de Pós-Graduação em Ciências Biológicas – Bioquímica, Departamento de Bioquímica, Instituto de Ciências Básicas da Saúde, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil. Email: [email protected]
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Abstract

Maternal exercise has shown beneficial effects on mother and child. Literature confirm progeny’s cognition improvement, and upregulation in neurotrophins, antioxidant network, and DNA repair system. Considering that there is a lack of information demonstrating the impact of maternal exercise on offspring’s skeletal muscle, we aimed to investigate the mitochondrial and redox effects elicited by maternal swimming. Adult female Wistar rats were divided into three groups: control sedentary, free swimming, and swimming with overload (2% of the body weight). Exercised groups were submitted weekly to five swimming sessions (30 min/day), starting 1 week prior to the mating and lasting to the delivery. Gastrocnemius and soleus muscle from 60-day-old offspring were analyzed. Our results clearly showed a sex-dependent effect. Male soleus showed increased mitochondrial functionality in the overload group. Female muscle from the overload group adapted deeply. Considering the redox status, the female offspring delivered to overload exercised dams presented reduced oxidants levels and protein damage, allied to downregulated antioxidant defenses. We also observed an increase in the mitochondrial function in the gastrocnemius muscle of the female offspring born from overload exercised dams. Soleus from female delivered to the overload exercise group presented reduced mitochondrial activity, as well as reduced reactive species, protein carbonyls, and antioxidant network, when compared to the male. In conclusion, maternal exercise altered the redox status and mitochondrial function in the offspring’s skeletal muscle in a sex-dependent way. The clinical implication was not investigated; however, the sexual dimorphism in response to maternal exercise might impact exercise resilience in adulthood.

Keywords

Maternal exercisesexual dimorphismskeletal musclemitochondriaredox statusantioxidant
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 13 , Issue 2 , April 2022 , pp. 204 - 211
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Copyright
© The Author(s), 2021. Published by Cambridge University Press in association with International Society for Developmental Origins of Health and Disease

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References

Bale, TL, Baram, TZ, Brown, AS, et al. Early life programming and neurodevelopmental disorders. Biol Psychiatry. 2010; 68(4), 314–319.CrossRefGoogle ScholarPubMed
Gluckman, PD, Hanson, MA. Developmental origins of disease paradigm: a mechanistic and evolutionary perspective. Pediatr Res. 2004; 56(3), 311–317.CrossRefGoogle ScholarPubMed
Moyer, C, Reoyo, OR, May, L. The influence of prenatal exercise on offspring health: a review. Clin Med Insights Womens Health. 2016; 9, 37–42.Google ScholarPubMed
Eclarinal, JD, Zhu, S, Baker, MS, et al. Maternal exercise during pregnancy promotes physical activity in adult offspring. FASEB J. 2016; 30(7), 2541–2548.CrossRefGoogle ScholarPubMed
McCloskey, K, Ponsonby, AL, Collier, F, et al. The association between higher maternal pre-pregnancy body mass index and increased birth weight, adiposity and inflammation in the newborn. Pediatr Obes. 2018; 13(1), 46–53.CrossRefGoogle ScholarPubMed
Stone, V, Crestani, MS, Saccomori, AB, et al. Gestational caloric restriction improves redox homeostasis parameters in the brain of Wistar rats: a screening from birth to adulthood. J Nutr Biochem. 2019; 67, 138–148.CrossRefGoogle ScholarPubMed
Dipietro, L, Evenson, KR, Bloodgood, B, et al. Benefits of physical activity during pregnancy and postpartum: an umbrella review. Med Sci Sports Exerc. 2019; 51(6), 1292–1302.CrossRefGoogle Scholar
Physical activity and exercise during pregnancy and the postpartum period: ACOG Committee Opinion, Number 804. Obstet Gynecol. 2020; 135(4), e178–e188.CrossRefGoogle Scholar
Siti, F, Dubouchaud, H, Hininger, I, et al. Maternal exercise before and during gestation modifies liver and muscle mitochondria in rat offspring. J Exp Biol. 2019; 222(10), jeb194969.Google ScholarPubMed
Lee, HH, Kim, H, Lee, JW, et al. Maternal swimming during pregnancy enhances short-term memory and neurogenesis in the hippocampus of rat pups. Brain Dev. 2006; 28(3), 147–154.CrossRefGoogle ScholarPubMed
Akhavan, MM, Emami-Abarghoie, M, Safari, M, et al. Serotonergic and noradrenergic lesions suppress the enhancing effect of maternal exercise during pregnancy on learning and memory in rat pups. Neuroscience. 2008; 151(4), 1173–1183.CrossRefGoogle ScholarPubMed
Marcelino, TB, Longoni, A, Kudo, KY, et al. Evidences that maternal swimming exercise improves antioxidant defenses and induces mitochondrial biogenesis in the brain of young Wistar rats. Neuroscience. 2013; 246, 28–39.CrossRefGoogle ScholarPubMed
Landen, S, Voisin, S, Craig, JM, McGee, SL, Lamon, S, Eynon, N. Genetic and epigenetic sex-specific adaptations to endurance exercise. Epigenetics. 2019; 14(6), 523–535.CrossRefGoogle ScholarPubMed
Laaksonen, DE, Lakka, HM, Salonen, JT, Niskanen, LK, Rauramaa, R, Lakka, TA. Low levels of leisure-time physical activity and cardiorespiratory fitness predict development of the metabolic syndrome. Diabetes Care. 2002; 25(9), 1612–1618.CrossRefGoogle ScholarPubMed
Myers, J, Kaykha, A, George, S, et al. Fitness versus physical activity patterns in predicting mortality in men. Am J Med. 2004; 117(12), 912–918.CrossRefGoogle ScholarPubMed
Camps, J, García-Heredia, A, Hernández-Aguilera, A, Joven, J. Paraoxonases, mitochondrial dysfunction and non-communicable diseases. Chem Biol Interact. 2016; 259(Pt B), 382–387.CrossRefGoogle ScholarPubMed
Hernández-Aguilera, A, Rull, A, Rodríguez-Gallego, E, et al. Mitochondrial dysfunction: a basic mechanism in inflammation-related non-communicable diseases and therapeutic opportunities. Mediators Inflamm. 2013; 2013, 135698.CrossRefGoogle ScholarPubMed
Mikovic, J, Lamon, S. The effect of maternal metabolic status on offspring health: a role for skeletal muscle? J Physiol. 2018; 596(21), 5079–5080.CrossRefGoogle ScholarPubMed
Amorim, MF, dos Santos, JA, Hirabara, SM, et al. Can physical exercise during gestation attenuate the effects of a maternal perinatal low-protein diet on oxygen consumption in rats? Exp Physiol. 2009; 94(8), 906–913.CrossRefGoogle ScholarPubMed
Zierath, JR, Hawley, JA. Skeletal muscle fiber type: influence on contractile and metabolic properties. PLoS Biol. 2004; 2(10), e348.CrossRefGoogle ScholarPubMed
Pattanakuhar, S, Pongchaidecha, A, Chattipakorn, N, Chattipakorn, SC. The effect of exercise on skeletal muscle fibre type distribution in obesity: From cellular levels to clinical application. Obes Res Clin Pract. 2017; 11(5 Suppl 1), 112–132.CrossRefGoogle ScholarPubMed
Ventura-Clapier, R, Piquereau, J, Veksler, V, Garnier, A. Estrogens, estrogen receptors effects on cardiac and skeletal muscle mitochondria. Front Endocrinol (Lausanne). 2019; 10, 557.CrossRefGoogle ScholarPubMed
Bolisetty, S, Jaimes, EA. Mitochondria and reactive oxygen species: physiology and pathophysiology. Int J Mol Sci. 2013; 14(3), 6306–6344.CrossRefGoogle ScholarPubMed
Viña, J, Gomez-Cabrera, MC, Lloret, A, et al. Free radicals in exhaustive physical exercise: mechanism of production, and protection by antioxidants. IUBMB Life. 2000; 50(4–5), 271–277.CrossRefGoogle ScholarPubMed
Rech, A, Radaelli, R, De Assis, AM, et al. The effects of strength, aerobic, and concurrent exercise on skeletal muscle damage in rats. Muscle Nerve. 2014; 50(1), 79–86.CrossRefGoogle ScholarPubMed
Vina, J, Sanchis-Gomar, F, Martinez-Bello, V, Gomez-Cabrera, MC. Exercise acts as a drug; the pharmacological benefits of exercise. Br J Pharmacol. 2012; 167(1), 1–12.CrossRefGoogle ScholarPubMed
Misra, HP, Fridovich, I. The role of superoxide anion in the autoxidation of epinephrine and a simple assay for superoxide dismutase. J Biol Chem. 1972; 247(10), 3170–3175.CrossRefGoogle Scholar
LeBel, CP, Ischiropoulos, H, Bondy, SC. Evaluation of the probe 2ʼ,7ʼ-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem Res Toxicol. 1992; 5(2), 227–231.CrossRefGoogle ScholarPubMed
Aebi, H. Catalase in vitro. Methods Enzymol. 1984; 105, 121–126.CrossRefGoogle ScholarPubMed
Wendel, A. Glutathione peroxidase. Methods Enzymol. 1981; 77, 325–333.CrossRefGoogle ScholarPubMed
Thornalley, PJ, Tisdale, MJ. Inhibition of proliferation of human promyelocytic leukaemia HL60 cells by S-D-lactoylglutathione in vitro. Leukemia Res. 1988; 12(11–12), 897–904.CrossRefGoogle ScholarPubMed
Browne, RW, Armstrong, D. Reduced glutathione and glutathione disulfide. Methods Mol Biol. 1998; 108, 347–352.Google ScholarPubMed
Reznick, AZ, Packer, L. Oxidative damage to proteins: spectrophotometric method for carbonyl assay. Methods Enzymol. 1994; 233, 357–363.CrossRefGoogle ScholarPubMed
Lowry, OH, Rosebrough, NJ, Farr, AL, Randall, RJ. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951; 193(1), 265–275.CrossRefGoogle ScholarPubMed
Tal, MC, Sasai, M, Lee, HK, Yordy, B, Shadel, GS, Iwasaki, A. Absence of autophagy results in reactive oxygen species-dependent amplification of RLR signaling. Proc Natl Acad Sci U S A. 2009; 106(8), 2770–2775.CrossRefGoogle ScholarPubMed
Bloemberg, D, Quadrilatero, J. Rapid determination of myosin heavy chain expression in rat, mouse, and human skeletal muscle using multicolor immunofluorescence analysis. PLoS One. 2012; 7(4), e35273.CrossRefGoogle ScholarPubMed
Cornachione, AS, Benedini-Elias, PC, Polizello, JC, Carvalho, LC, Mattiello-Sverzut, AC. Characterization of fiber types in different muscles of the hindlimb in female weanling and adult Wistar rats. Acta Histochem Cytochem. 2011; 44(2), 43–50.CrossRefGoogle ScholarPubMed
Ustunel, I, Demir, R. A histochemical, morphometric and ultrastructural study of gastrocnemius and soleus muscle fiber type composition in male and female rats. Acta Anat (Basel). 1997; 158(4), 279–286.CrossRefGoogle ScholarPubMed
Liu, J, Lee, I, Feng, HZ, et al. Aerobic exercise preconception and during pregnancy enhances oxidative capacity in the hindlimb muscles of mice offspring. J Strength Cond Res. 2018; 32(5), 1391–1403.CrossRefGoogle ScholarPubMed
Klein, CP, Hoppe, JB, Saccomori, AB, et al. Physical exercise during pregnancy prevents cognitive impairment induced by amyloid-beta in adult offspring rats. Mol Neurobiol. 2019; 56(3), 2022–2038.CrossRefGoogle ScholarPubMed
Bell, MB, Bush, Z, McGinnis, GR, Rowe, GC. Adult skeletal muscle deletion of Mitofusin 1 and 2 impedes exercise performance and training capacity. J Appl Physiol (1985). 2019; 126(2), 341–353.CrossRefGoogle ScholarPubMed
Cartoni, R, Leger, B, Hock, MB, et al. Mitofusins 1/2 and ERRalpha expression are increased in human skeletal muscle after physical exercise. J Physiol. 2005; 567(Pt 1), 349–358.CrossRefGoogle ScholarPubMed
Zorzano, A. Regulation of mitofusin-2 expression in skeletal muscle. Appl Physiol Nutr Metab. 2009; 34(3), 433–439.CrossRefGoogle ScholarPubMed
Theilen, NT, Kunkel, GH, Tyagi, SC. The role of exercise and TFAM in preventing skeletal muscle atrophy. J Cell Physiol. 2017; 232(9), 2348–2358.CrossRefGoogle ScholarPubMed
Jornayvaz, FR, Shulman, GI. Regulation of mitochondrial biogenesis. Essays Biochem. 2010; 47, 69–84.Google ScholarPubMed
Costello, JT, Bieuzen, F, Bleakley, CM. Where are all the female participants in sports and exercise medicine research? Eur J Sport Sci. 2014; 14(8), 847–851.CrossRefGoogle ScholarPubMed
Farhat, F, Amérand, A, Simon, B, Guegueniat, N, Moisan, C. Gender-dependent differences of mitochondrial function and oxidative stress in rat skeletal muscle at rest and after exercise training. Redox Rep. 2017; 22(6), 508–514.CrossRefGoogle ScholarPubMed
Montero, D, Madsen, K, Meinild-Lundby, AK, Edin, F, Lundby, C. Sexual dimorphism of substrate utilization: differences in skeletal muscle mitochondrial volume density and function. Exp Physiol. 2018; 103(6), 851–859.CrossRefGoogle ScholarPubMed
Tarnopolsky, MA. Sex differences in exercise metabolism and the role of 17-beta estradiol. Med Sci Sports Exerc. 2008; 40(4), 648–654.CrossRefGoogle ScholarPubMed
Malorni, W, Campesi, I, Straface, E, Vella, S, Franconi, F. Redox features of the cell: a gender perspective. Antioxid Redox Signal. 2007; 9(11), 1779–1801.CrossRefGoogle ScholarPubMed
Ventura-Clapier, R, Moulin, M, Piquereau, J, et al. Mitochondria: a central target for sex differences in pathologies. Clin Sci (Lond). 2017; 131(9), 803–822.CrossRefGoogle ScholarPubMed
Viña, J, Borrás, C, Gambini, J, Sastre, J, Pallardó, FV. Why females live longer than males? Importance of the upregulation of longevity-associated genes by oestrogenic compounds. FEBS Lett. 2005; 579(12), 2541–2545.CrossRefGoogle ScholarPubMed
Mallay, S, Gill, R, Young, A, Mailloux, RJ. Sex-dependent differences in the bioenergetics of liver and muscle mitochondria from mice containing a deletion for. Antioxidants (Basel). 2019; 8(8), 245.CrossRefGoogle Scholar
Enns, DL, Tiidus, PM. The influence of estrogen on skeletal muscle: sex matters. Sports Med. 2010; 40(1), 41–58.CrossRefGoogle ScholarPubMed
Lemoine, S, Granier, P, Tiffoche, C, et al. Effect of endurance training on oestrogen receptor alpha transcripts in rat skeletal muscle. Acta Physiol Scand. 2002; 174(3), 283–289.CrossRefGoogle ScholarPubMed
Hamilton, DJ, Minze, LJ, Kumar, T, et al. Estrogen receptor alpha activation enhances mitochondrial function and systemic metabolism in high-fat-fed ovariectomized mice. Physiol Rep. 2016; 4(17), e12913.CrossRefGoogle ScholarPubMed
Calvino-Núñez, C, Domínguez-del-Toro, E. Clonidine treatment delays postnatal motor development and blocks short-term memory in young mice. PLoS One. 2014; 9(12), e114869.CrossRefGoogle ScholarPubMed
Heyser, CJ. Assessment of developmental milestones in rodents. Curr Protocols Neurosci. 2004; Chapter 8: Unit 8.18.Google Scholar
Chen, C, Tang, Y, Jiang, X, et al. Early postnatal benzo(a)pyrene exposure in Sprague-Dawley rats causes persistent neurobehavioral impairments that emerge postnatally and continue into adolescence and adulthood. Toxicol Sci. 2012; 125(1), 248–261.CrossRefGoogle ScholarPubMed
Tamashiro, KL, Wakayama, T, Blanchard, RJ, Blanchard, DC, Yanagimachi, R. Postnatal growth and behavioral development of mice cloned from adult cumulus cells. Biol Reproduct. 2000; 63(1), 328–334.CrossRefGoogle ScholarPubMed