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Maternal physical activity-induced adaptive transcriptional response in brain and placenta of mothers and rat offspring

Part of: DOHaD on International Women's Day 2020

Published online by Cambridge University Press:  17 June 2019

Jéssica Fragoso ,
Gabriela Carvalho Jurema Santos ,
Helyson Thomaz da Silva ,
Viviane Oliveira Nogueira ,
Emmanuelle Loizon ,
Hubert Vidal ,
João Henrique Costa-Silva ,
Raquel da Silva Aragão Open the ORCID record for Raquel da Silva Aragão [Opens in a new window] ,
Luciano Pirola  and
Carol Gois Leandro Open the ORCID record for Carol Gois Leandro [Opens in a new window]
Jéssica Fragoso
Affiliation:
Department of Nutrition, Federal University of Pernambuco, 50670-901 Recife, PE, Brazil
Gabriela Carvalho Jurema Santos
Affiliation:
Department of Physical Education and Sports Science, Federal University of Pernambuco, 55608-680 Vitória de Santo Antão, PE, Brazil;
Helyson Thomaz da Silva
Affiliation:
Department of Nutrition, Federal University of Pernambuco, 50670-901 Recife, PE, Brazil
Viviane Oliveira Nogueira
Affiliation:
Department of Physical Education and Sports Science, Federal University of Pernambuco, 55608-680 Vitória de Santo Antão, PE, Brazil;
Emmanuelle Loizon
Affiliation:
CarMeN (Cardiology, Metabolism and Nutrition) Laboratory, INSERM U1060, Lyon-1 University, South Lyon Medical Faculty, 69921 Oullins, France
Hubert Vidal
Affiliation:
CarMeN (Cardiology, Metabolism and Nutrition) Laboratory, INSERM U1060, Lyon-1 University, South Lyon Medical Faculty, 69921 Oullins, France
João Henrique Costa-Silva
Affiliation:
Department of Physical Education and Sports Science, Federal University of Pernambuco, 55608-680 Vitória de Santo Antão, PE, Brazil;
Raquel da Silva Aragão
Affiliation:
Department of Physical Education and Sports Science, Federal University of Pernambuco, 55608-680 Vitória de Santo Antão, PE, Brazil;
Luciano Pirola
Affiliation:
CarMeN (Cardiology, Metabolism and Nutrition) Laboratory, INSERM U1060, Lyon-1 University, South Lyon Medical Faculty, 69921 Oullins, France
Carol Gois Leandro*
Affiliation:
Department of Physical Education and Sports Science, Federal University of Pernambuco, 55608-680 Vitória de Santo Antão, PE, Brazil;
*
Address for correspondence: Carol Gois Leandro, Núcleo de Nutrição, Universidade Federal de Pernambuco, Centro Acadêmico de Vitória – CAV, Vitória de Santo Antão, PE, Brazil E-mail: [email protected]
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Abstract

Maternal physical activity induces brain functional changes and neuroplasticity, leading to an improvement of cognitive functions, such as learning and memory in the offspring. This study investigated the effects of voluntary maternal physical activity on the gene expression of the neurotrophic factors (NTFs): BDNF, NTF4, NTRK2, IGF-1 and IGF-1r in the different areas of mother’s brain, placenta and foetus brain of rats. Female Wistar rats (n = 15) were individually housed in voluntary physical activity cages, containing a running wheel, for 4 weeks (period of adaptation) before gestation. Rats were classified as inactive (I, n = 6); active (A, n = 4) and very active (VA, n = 5) according to daily distance spontaneously travelled. During gestation, the dams continued to have access to the running wheel. At the 20th day of gestation, gene expression of NTFs was analysed in different areas of mother’s brain (cerebellum, hypothalamus, hippocampus and cortex), placenta and the offspring’s brain. NTFs gene expression was evaluated using quantitative PCR. Very active mothers showed upregulation of IGF-1 mRNA in the cerebellum (36.8%) and NTF4 mRNA expression in the placenta (24.3%). In the cortex, there was a tendency of up-regulation of NTRK2 mRNA (p = 0.06) in the A and VA groups when compared to I group. There were no noticeable changes in the gene expression of NTFs in the offspring’s brain. Our findings suggest the existence of a developmental plasticity induced by maternal physical activity in specific areas of the brain and placenta representing the first investment for offspring during development.

Keywords

Physical exercisepregnancyneuroplasticityratsneurotrophic factors
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 11 , Issue 2 , April 2020 , pp. 108 - 117
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2019

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References

Robinson, AM, Bucci, DJ.Physical exercise during pregnancy improves object recognition memory in adult offspring. Neuroscience. 2014; 256, 53–60.CrossRefGoogle ScholarPubMed
Labonte-Lemoyne, E, Curnier, D, Ellemberg, D.Exercise during pregnancy enhances cerebral maturation in the newborn: a randomized controlled trial. J Clin Exp Neuropsychol. 2017; 39, 347–354.CrossRefGoogle ScholarPubMed
Ferrari, N, Bae-Gartz, I, Bauer, C, et al.Exercise during pregnancy and its impact on mothers and offspring in humans and mice. J Dev Orig Health Dis. 2018; 9, 63–76.CrossRefGoogle ScholarPubMed
Gomes da Silva, S, de Almeida, AA, Fernandes, J, et al. Maternal exercise during pregnancy increases BDNF levels and cell numbers in the hippocampal formation but not in the cerebral cortex of adult rat offspring. PLoS One. 2016; 11, e0147200.CrossRefGoogle Scholar
Skaper, SD.Neurotrophic Factors: an overview. Methods Mol Biol. 2018; 1727, 1–17.CrossRefGoogle ScholarPubMed
Solvsten, CAE, Daugaard, TF, Luo, Y, de Paoli, F, Christensen, JH, Nielsen, AL. The effects of voluntary physical exercise-activated neurotrophic signaling in rat hippocampus on mRNA levels of downstream signaling molecules. J Mol Neurosci. 2017; 62, 142–153.10.1007/s12031-017-0918-9CrossRefGoogle ScholarPubMed
Neeper, SA, Gomez-Pinilla, F, Choi, J, Cotman, CW.Physical activity increases mRNA for brain-derived neurotrophic factor and nerve growth factor in rat brain. Brain Res. 1996; 726, 49–56.CrossRefGoogle ScholarPubMed
Miki, T, Lee, KY, Yokoyama, T, et al. Differential effects of neonatal maternal separation on the expression of neurotrophic factors in rat brain. II: regional differences in the cerebellum versus the cerebral cortex. Okajimas Folia Anat Jpn. 2013; 90, 53–58.CrossRefGoogle ScholarPubMed
Solvsten, CAE, de Paoli, F, Christensen, JH, Nielsen, AL.Voluntary physical exercise induces expression and epigenetic remodeling of VegfA in the rat hippocampus. Mol Neurobiol. 2018; 55, 567–582.CrossRefGoogle ScholarPubMed
Tapia-Arancibia, L, Rage, F, Givalois, L, Arancibia, S.Physiology of BDNF: focus on hypothalamic function. Front Neuroendocrinol. 2004; 25, 77–107.10.1016/j.yfrne.2004.04.001CrossRefGoogle ScholarPubMed
Yau, SY, Gil-Mohapel, J, Christie, BR, So, KF.Physical exercise-induced adult neurogenesis: a good strategy to prevent cognitive decline in neurodegenerative diseases? Biomed Res Int. 2014; 2014, 403120.CrossRefGoogle ScholarPubMed
Arnardottir, NY, Koster, A, Domelen, DRV, et al. Association of change in brain structure to objectively measured physical activity and sedentary behavior in older adults: age, gene/environment susceptibility-Reykjavik study. Behav Brain Res. 2016; 296, 118–124.CrossRefGoogle ScholarPubMed
Mayeur, S, Silhol, M, Moitrot, E, et al. Placental BDNF/TrkB signaling system is modulated by fetal growth disturbances in rat and human. Placenta. 2010; 31, 785–791.CrossRefGoogle ScholarPubMed
Kawamura, K, Kawamura, N, Sato, W, Fukuda, J, Kumagai, J, Tanaka, T.Brain-derived neurotrophic factor promotes implantation and subsequent placental development by stimulating trophoblast cell growth and survival. Endocrinology. 2009; 150, 3774–3782.CrossRefGoogle ScholarPubMed
Fowden, AL, Sferruzzi-Perri, AN, Coan, PM, Constancia, M, Burton, GJ.Placental efficiency and adaptation: endocrine regulation. J Physiol. 2009; 587, 3459–3472.CrossRefGoogle ScholarPubMed
Dey, SK, Lim, H, Das, SK, et al. Molecular cues to implantation. Endocr Rev. 2004; 25, 341–373.CrossRefGoogle Scholar
Jones, HN, Crombleholme, T, Habli, M.Adenoviral-mediated placental gene transfer of IGF-1 corrects placental insufficiency via enhanced placental glucose transport mechanisms. PLoS One. 2013; 8, e74632.CrossRefGoogle ScholarPubMed
Clapp, JF, 3rd. The effects of maternal exercise on fetal oxygenation and feto-placental growth. Eur J Obstet Gynecol Reprod Biol. 2003; 110 Suppl1, S80–85.10.1016/S0301-2115(03)00176-3CrossRefGoogle Scholar
Hsiao, EY, Patterson, PH.Placental regulation of maternal-fetal interactions and brain development. Dev Neurobiol. 2012; 72, 1317–1326.CrossRefGoogle ScholarPubMed
Clapp, JF, 3rd, Kim, H, Burciu, B, Lopez, B.Beginning regular exercise in early pregnancy: effect on fetoplacental growth. Am J Obstet Gynecol. 2000; 183, 1484–1488.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, 906–913.CrossRefGoogle ScholarPubMed
Du, MC, Ouyang, YQ, Nie, XF, Huang, Y, Redding, SR.Effects of physical exercise during pregnancy on maternal and infant outcomes in overweight and obese pregnant women: a meta-analysis. Birth. 2018; doi: 10.1111/birt.12396.CrossRefGoogle Scholar
Davenport, MH, Meah, VL, Ruchat, SM, et al. Impact of prenatal exercise on neonatal and childhood outcomes: a systematic review and meta-analysis. Br J Sports Med. 2018; 52, 1386–1396.CrossRefGoogle ScholarPubMed
Rosa, BV, Firth, EC, Blair, HT, Vickers, MH, Morel, PC.Voluntary exercise in pregnant rats positively influences fetal growth without initiating a maternal physiological stress response. Am J Physiol Regul Integr Comp Physiol. 2011; 300, R1134–1141.CrossRefGoogle ScholarPubMed
Fragoso, J, Lira, AO, Chagas, GS, et al. Maternal voluntary physical activity attenuates delayed neurodevelopment in malnourished rats. Exp Physiol. 2017; 102, 1486–1499.CrossRefGoogle ScholarPubMed
Santana Muniz, G, Beserra, R, da Silva Gde, P, et al. Active maternal phenotype is established before breeding and leads offspring to align growth trajectory outcomes and reflex ontogeny. Physiol Behav. 2014; 129, 1–10.CrossRefGoogle ScholarPubMed
Knab, AM, Bowen, RS, Hamilton, AT, Gulledge, AA, Lightfoot, JT.Altered dopaminergic profiles: implications for the regulation of voluntary physical activity. Behav Brain Res. 2009; 204, 147–152.CrossRefGoogle ScholarPubMed
Knab, AM, Bowen, RS, Hamilton, AT, Lightfoot, JT.Pharmacological manipulation of the dopaminergic system affects wheel-running activity in differentially active mice. J Biol Regul Homeost Agents. 2012; 26, 119–129.Google ScholarPubMed
Tsao, TS, Li, J, Chang, KS, et al. Metabolic adaptations in skeletal muscle overexpressing GLUT4: effects on muscle and physical activity. FASEB J. 2001; 15, 958–969.CrossRefGoogle ScholarPubMed
Moore, T.Review: parent-offspring conflict and the control of placental function. Placenta. 2012; 33 (Suppl), S33–36.CrossRefGoogle ScholarPubMed
Newcomer, SC, Taheripour, P, Bahls, M, et al. Impact of porcine maternal aerobic exercise training during pregnancy on endothelial cell function of offspring at birth. J Dev Orig Health Dis. 2012; 3, 4–9.10.1017/S2040174411000687CrossRefGoogle ScholarPubMed
Wells, JC.The thrifty phenotype hypothesis: thrifty offspring or thrifty mother? J Theor Biol. 2003; 221, 143–161.CrossRefGoogle ScholarPubMed
Ke, Z, Yip, SP, Li, L, Zheng, XX, Tong, KY.The effects of voluntary, involuntary, and forced exercises on brain-derived neurotrophic factor and motor function recovery: a rat brain ischemia model. PLoS One. 2011; 6, e16643.CrossRefGoogle ScholarPubMed
De Assis, GG, Gasanov, EV, de Sousa, MBC, Kozacz, A, Murawska-Cialowicz, E.Brain derived neutrophic factor, a link of aerobic metabolism to neuroplasticity. J Physiol Pharmacol. 2018; 69, 351–358.Google ScholarPubMed
Kim, P, Strathearn, L, Swain, JE.The maternal brain and its plasticity in humans. Horm Behav. 2016; 77, 113–123.CrossRefGoogle ScholarPubMed
Wessels, JM, Leyland, NA, Agarwal, SK, Foster, WG.Estrogen induced changes in uterine brain-derived neurotrophic factor and its receptors. Hum Reprod. 2015; 30, 925–936.CrossRefGoogle ScholarPubMed
Antonio-Santos, J, Ferreira, DJ, Gomes Costa, GL, et al. Resistance training alters the proportion of skeletal muscle fibers but not brain neurotrophic factors in young adult rats. J Strength Cond Res. 2016; 30, 3531–3538.CrossRefGoogle Scholar
Leasure, JL, Jones, M.Forced and voluntary exercise differentially affect brain and behavior. Neuroscience. 2008; 156, 456–465.CrossRefGoogle ScholarPubMed
Fernandez, C, Tatard, VM, Bertrand, N, Dahmane, N.Differential modulation of sonic-hedgehog-induced cerebellar granule cell precursor proliferation by the IGF signaling network. Dev Neurosci. 2010; 32, 59–70.CrossRefGoogle ScholarPubMed
Anderson, MF, Aberg, MA, Nilsson, M, Eriksson, PS.Insulin-like growth factor-I and neurogenesis in the adult mammalian brain. Brain Res Dev Brain Res. 2002; 134, 115–122.10.1016/S0165-3806(02)00277-8CrossRefGoogle ScholarPubMed
Llorens-Martin, M, Torres-Aleman, I, Trejo, JL.Growth factors as mediators of exercise actions on the brain. Neuromolecular Med. 2008; 10, 99–107.10.1007/s12017-008-8026-1CrossRefGoogle Scholar
Wells, JCK.Life history trade-offs and the partitioning of maternal investment: implications for health of mothers and offspring. Evol Med Public Health. 2018; 2018, 153–166.CrossRefGoogle ScholarPubMed
Rebelato, HJ, Esquisatto, MA, Moraes, C, Amaral, ME, Catisti, R.Gestational protein restriction induces alterations in placental morphology and mitochondrial function in rats during late pregnancy. J Mol Histol. 2013; 44, 629–637.CrossRefGoogle ScholarPubMed
Manokhina, I, Del Gobbo, GF, Konwar, C, Wilson, SL, Robinson, WP.Review: placental biomarkers for assessing fetal health. Hum Mol Genet. 2017; 26, R237–R245.CrossRefGoogle ScholarPubMed