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Effects of maternal low-protein diet and spontaneous physical activity on the transcription of neurotrophic factors in the placenta and the brains of mothers and offspring rats

Published online by Cambridge University Press:  17 August 2020

Jéssica Fragoso ,
Gabriela Carvalho Jurema Santos ,
Helyson Thomaz da Silva ,
Emmanuelle Loizon ,
Viviane de Oliveira Nogueira Souza ,
Hubert Vidal ,
Rubem Carlos Araújo Guedes Open the ORCID record for Rubem Carlos Araújo Guedes [Opens in a new window] ,
João Henrique Costa-Silva ,
Raquel da Silva Aragão Open the ORCID record for Raquel da Silva Aragão [Opens in a new window]  and
Luciano Pirola Open the ORCID record for Luciano Pirola [Opens in a new window]
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Jéssica Fragoso
Affiliation:
Department of Nutrition, Federal University of Pernambuco, 50670-901Recife, PE, Brazil Department of Physical Education and Sports Science, Federal University of Pernambuco, 55608-680Vitória de Santo Antão, PE, Brazil
Gabriela Carvalho Jurema Santos
Affiliation:
Department of Physical Education and Sports Science, Federal University of Pernambuco, 55608-680Vitória de Santo Antão, PE, Brazil
Helyson Thomaz da Silva
Affiliation:
Department of Nutrition, Federal University of Pernambuco, 50670-901Recife, PE, Brazil
Emmanuelle Loizon
Affiliation:
CarMeN (Cardiology, Metabolism and Nutrition) Laboratory, INSERM U1060, Lyon-1 University, South Lyon Medical Faculty, 69921Oullins, France
Viviane de Oliveira Nogueira Souza
Affiliation:
Department of Physical Education and Sports Science, Federal University of Pernambuco, 55608-680Vitória de Santo Antão, PE, Brazil
Hubert Vidal
Affiliation:
CarMeN (Cardiology, Metabolism and Nutrition) Laboratory, INSERM U1060, Lyon-1 University, South Lyon Medical Faculty, 69921Oullins, France
Rubem Carlos Araújo Guedes
Affiliation:
Department of Nutrition, Federal University of Pernambuco, 50670-901Recife, PE, Brazil
João Henrique Costa-Silva
Affiliation:
Department of Physical Education and Sports Science, Federal University of Pernambuco, 55608-680Vitória de Santo Antão, PE, Brazil
Raquel da Silva Aragão
Affiliation:
Department of Physical Education and Sports Science, Federal University of Pernambuco, 55608-680Vitória de Santo Antão, PE, Brazil
Luciano Pirola*
Affiliation:
Department of Nutrition, Federal University of Pernambuco, 50670-901Recife, PE, Brazil CarMeN (Cardiology, Metabolism and Nutrition) Laboratory, INSERM U1060, Lyon-1 University, South Lyon Medical Faculty, 69921Oullins, France
Carol Gois Leandro
Affiliation:
Department of Nutrition, Federal University of Pernambuco, 50670-901Recife, PE, Brazil
*
Address for correspondence: Luciano Pirola, U1060 INSERM, INRA 1397, CARMEN Laboratory, Lyon South Hospital, Sector 2, 165 Chemin du grand Revoyet, F - 69310Pierre Benite, France. Email: [email protected]
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Abstract

Maternal protein restriction and physical activity can affect the interaction mother–placenta–fetus. This study quantified the gene expression of brain-derived neurotrophic factor (BDNF), neurothrophin 4, tyrosine kinase receptor B (TrkB/NTRK2), insulin-like growth factor (IGF-1), and insulin-like growth factor receptor (IGF-1r) in the different areas of mother’s brain (hypothalamus, hippocampus, and cortex), placenta, and fetus’ brain of rats. Female Wistar rats (n = 20) were housed in cages containing a running wheel for 4 weeks before gestation. According to the distance spontaneously traveled daily, rats were classified as inactive or active. During gestation, on continued access to the running wheel, active and inactive groups were randomized to receive normoprotein diet (18% protein) or a low-protein (LP) diet (8% protein). At day 20 of gestation, gene expression of neurotrophic factors was analyzed by quantitative polymerase chain reaction in different brain areas and the placenta. Dams submitted to a LP diet during gestation showed upregulation of IGF-1r and BDNF messenger RNA in the hypothalamus, IGF-1r and NTRK2 in the hippocampus, and BDNF, NTRK2, IGF-1 and IGF-1r in the cortex. In the placenta, there was a downregulation of IGF-1. In the brain of pups from mothers on LP diet, IGF-1r and NTRK2 were downregulated. Voluntary physical activity attenuated the effects of LP diet on IGF-1r in the hypothalamus, IGF-1r and NTRK2 in the hippocampus, IGF-1 in the placenta, and NTRK2 in the fetus’ brain. In conclusion, both maternal protein restriction and spontaneous physical activity influence the gene expression of BDNF, NTRK2, IGF-1, and IGF-1r, with spontaneous physical activity being able to normalize in part the defects caused by protein restriction during pregnancy.

Keywords

Physical activityprotein restrictionpregnancyneuroplasticitydevelopmental plasticityrats
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 12 , Issue 3 , June 2021 , pp. 505 - 512
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Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2020

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Footnotes

*

LP and CGL equally contributed to this work

References

Kominiarek, MA, Rajan, P. Nutrition Recommendations in Pregnancy and Lactation. Med Clin North Am. 2016; 100, 1199–1215.CrossRefGoogle ScholarPubMed
Belkacemi, L, Nelson, DM, Desai, M, Ross, MG. Maternal undernutrition influences placental-fetal development. Biol Reprod. 2010; 83, 325–331.CrossRefGoogle ScholarPubMed
de Brito Alves, JL, de Oliveira, JM, Ferreira, DJ, Barros, MA, Nogueira, VO, Alves, DS, Vidal, H, Leandro, CG, Lagranha, CJ, Pirola, L, da Costa-Silva, JH. Maternal protein restriction induced-hypertension is associated to oxidative disruption at transcriptional and functional levels in the medulla oblongata. Clin Exp Pharmacol Physiol. 2016; 43, 1177–1184.CrossRefGoogle ScholarPubMed
Fragoso, J, Lira, AO, Chagas, GS, Lucena Cavalcanti, CC, Beserra, R, de Santana-Muniz, G, Bento-Santos, A, Martins, G, Pirola, L, da Silva Aragao, R, Leandro, CG. Maternal voluntary physical activity attenuates delayed neurodevelopment in malnourished rats. Exp Physiol. 2017; 102, 1486–1499.CrossRefGoogle ScholarPubMed
Dos Santos, FK, Moura Dos Santos, MA, Almeida, MB, Nobre, IG, Nobre, GG, Ferreira, ESWT, Gomes, TN, Antonio Ribeiro Maia, J, Leandro, CG. Biological and behavioral correlates of body weight status among rural Northeast Brazilian schoolchildren. Am J Hum Biol. 2018; 30, e23096.CrossRefGoogle ScholarPubMed
Veena, SR, Gale, CR, Krishnaveni, GV, Kehoe, SH, Srinivasan, K, Fall, CH. Association between maternal nutritional status in pregnancy and offspring cognitive function during childhood and adolescence; a systematic review. BMC Pregnancy Childbirth. 2016; 16, 220.CrossRefGoogle ScholarPubMed
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
Fidalgo, M, Falcao-Tebas, F, Bento-Santos, A, de Oliveira, E, Nogueira-Neto, JF, de Moura, EG, Lisboa, PC, de Castro, RM, Leandro, CG. Programmed changes in the adult rat offspring caused by maternal protein restriction during gestation and lactation are attenuated by maternal moderate-low physical training. Br J Nutr. 2013; 109, 449–456.CrossRefGoogle ScholarPubMed
de Brito Alves, JL, Nogueira, VO, de Oliveira, GB, da Silva, GS, Wanderley, AG, Leandro, CG, Costa-Silva, JH. Short- and long-term effects of a maternal low-protein diet on ventilation, O(2)/CO(2) chemoreception and arterial blood pressure in male rat offspring. Br J Nutr. 2014; 111, 606–615.CrossRefGoogle Scholar
Tarrade, A, Panchenko, P, Junien, C, Gabory, A. Placental contribution to nutritional programming of health and diseases: epigenetics and sexual dimorphism. J Exp Biol. 2015; 218, 50–58.CrossRefGoogle ScholarPubMed
Amaral, AC, Jakovcevski, M, McGaughy, JA, Calderwood, SK, Mokler, DJ, Rushmore, RJ, Galler, JR, Akbarian, SA, Rosene, DL. Prenatal protein malnutrition decreases KCNJ3 and 2DG activity in rat prefrontal cortex. Neuroscience. 2015; 286, 79–86.CrossRefGoogle ScholarPubMed
Gonzalez-Maciel, A, Romero-Velazquez, RM, Reynoso-Robles, R, Uribe-Escamilla, R, Vargas-Sanchez, J, de la Garza-Montano, P, Alfaro-Rodriguez, A. Prenatal Protein Malnutrition Affects the Density of GABAergic Interneurons During Hippocampus Development in Rats. Rev Invest Clin. 2015; 67, 296–303.Google ScholarPubMed
Garces, MF, Sanchez, E, Torres-Sierra, AL, Ruiz-Parra, AI, Angel-Muller, E, Alzate, JP, Sanchez, AY, Gomez, MA, Romero, XC, Castaneda, ZE, Sanchez-Rebordelo, E, Dieguez, C, Nogueiras, R, Caminos, JE. Brain-derived neurotrophic factor is expressed in rat and human placenta and its serum levels are similarly regulated throughout pregnancy in both species. Clin Endocrinol (Oxf). 2014; 81, 141–151.CrossRefGoogle ScholarPubMed
Mayeur, S, Silhol, M, Moitrot, E, Barbaux, S, Breton, C, Gabory, A, Vaiman, D, Dutriez-Casteloot, I, Fajardy, I, Vambergue, A, Tapia-Arancibia, L, Bastide, B, Storme, L, Junien, C, Vieau, D, Lesage, J. Placental BDNF/TrkB signaling system is modulated by fetal growth disturbances in rat and human. Placenta. 2010; 31, 785–791.CrossRefGoogle ScholarPubMed
Jones, DG, Dyson, SE. The influence of protein restriction, rehabilitation and changing nutritional status on synaptic development: a quantitative study in rat brain. Brain Res. 1981; 208, 97–111.CrossRefGoogle ScholarPubMed
Ikeda, N, Shoji, H, Suganuma, H, Ohkawa, N, Kantake, M, Murano, Y, Sakuraya, K, Shimizu, T. Effect of insulin-like growth factor-I during the early postnatal period in intrauterine growth-restricted rats. Pediatr Int. 2016; 58, 353–358.CrossRefGoogle ScholarPubMed
Leandro, CG, Fidalgo, M, Bento-Santos, A, Falcao-Tebas, F, Vasconcelos, D, Manhaes-de-Castro, R, Carpinelli, AR, Hirabara, SM, Curi, R. Maternal moderate physical training during pregnancy attenuates the effects of a low-protein diet on the impaired secretion of insulin in rats: potential role for compensation of insulin resistance and preventing gestational diabetes mellitus. J Biomed Biotechnol. 2012; 2012, 805418.CrossRefGoogle ScholarPubMed
Ferrari, N, Graf, C. [Recommendations for Physical Activity During and After Pregnancy]. Gesundheitswesen. 2017; 79, S36–S39.Google 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
Robinson, AM, Bucci, DJ. Physical exercise during pregnancy improves object recognition memory in adult offspring. Neuroscience. 2014; 256, 53–60.CrossRefGoogle ScholarPubMed
Gomes da Silva, S, de Almeida, AA, Fernandes, J, Lopim, GM, Cabral, FR, Scerni, DA, de Oliveira-Pinto, AV, Lent, R, Arida, RM. 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
Santana Muniz, G, Beserra, R, da Silva Gde, P, Fragoso, J, Lira Ade, O, Nascimento, E, Manhaes de Castro, R, Leandro, CG. 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
Leandro, CG, Levada, AC, Hirabara, SM, Manhães-de-Castro, R, De-Castro, CB, Curi, R, Pithon-Curi, TC. A program of moderate physical training for Wistar rats based on maximal oxygen consumption. J Strength Cond Res. 2007; 21, 751–756.Google ScholarPubMed
Behura, SK, Kelleher, AM, Spencer, TE. Evidence for functional interactions between the placenta and brain in pregnant mice. FASEB J. 2018; fj201802037R.Google ScholarPubMed
Ferreira, DS, Liu, Y, Fernandes, MP, Lagranha, CJ. Perinatal low-protein diet alters brainstem antioxidant metabolism in adult offspring. Nutr Neurosci. 2016; 19, 369–375.CrossRefGoogle ScholarPubMed
Qasem, RJ, Li, J, Tang, HM, Pontiggia, L, D’Mello, A P. Maternal protein restriction during pregnancy and lactation alters central leptin signalling, increases food intake, and decreases bone mass in 1 year old rat offspring. Clin Exp Pharmacol Physiol. 2016; 43, 494–502.CrossRefGoogle ScholarPubMed
Berardino, BG, Fesser, EA, Canepa, ET. Perinatal protein malnutrition alters expression of miRNA biogenesis genes Xpo5 and Ago2 in mice brain. Neurosci Lett. 2017; 647, 38–44.CrossRefGoogle ScholarPubMed
Thanos, PK, Zhuo, J, Robison, L, Kim, R, Ananth, M, Choai, I, Grunseich, A, Grissom, NM, George, R, Delis, F, Reyes, TM. Suboptimal maternal diets alter mu opioid receptor and dopamine type 1 receptor binding but exert no effect on dopamine transporters in the offspring brain. Int J Dev Neurosci. 2018; 64, 21–28.CrossRefGoogle ScholarPubMed
Kim, P, Strathearn, L, Swain, JE. The maternal brain and its plasticity in humans. Horm Behav. 2016; 77, 113–123.CrossRefGoogle ScholarPubMed
Senna, SM, Torres, MK, Lopes, DA, Alheiros-Lira, MC, de Moura, DB, Pereira, VR, de Aguiar, FC Jr, Ferraz, JC, Leandro, CG. Moderate physical training attenuates perinatal low-protein-induced spleen lymphocyte apoptosis in endotoxemic adult offspring rats. Eur J Nutr. 2016; 55, 1113–1122.CrossRefGoogle ScholarPubMed
Butte, NF, King, JC. Energy requirements during pregnancy and lactation. Public Health Nutr. 2005; 8, 1010–1027.CrossRefGoogle ScholarPubMed
Patz, S, Wahle, P. Neurotrophins induce short-term and long-term changes of cortical neurotrophin expression. Eur J Neurosci. 2004; 20, 701–708.CrossRefGoogle ScholarPubMed
Coupe, B, Dutriez-Casteloot, I, Breton, C, Lefevre, F, Mairesse, J, Dickes-Coopman, A, Silhol, M, Tapia-Arancibia, L, Lesage, J, Vieau, D. Perinatal undernutrition modifies cell proliferation and brain-derived neurotrophic factor levels during critical time-windows for hypothalamic and hippocampal development in the male rat. J Neuroendocrinol. 2009; 21, 40–48.CrossRefGoogle ScholarPubMed
Dyer, AH, Vahdatpour, C, Sanfeliu, A, Tropea, D. The role of insulin-Like Growth Factor 1 (IGF-1) in brain development, maturation and neuroplasticity. Neuroscience. 2016; 325, 89–99.CrossRefGoogle ScholarPubMed
Wrigley, S, Arafa, D, Tropea, D. Insulin-like growth factor 1: at the crossroads of brain development and aging. Front Cell Neurosci. 2017; 11, 14.CrossRefGoogle ScholarPubMed
Turgut, S, Kaptanoglu, B, Emmungil, G, Turgut, G. Increased plasma levels of growth hormone, insulin-like growth factor (IGF)-I and IGF-binding protein 3 in pregnant rats with exercise. Tohoku J Exp Med. 2006; 208, 75–81.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
Gomez-Pinilla, F, Zhuang, Y, Feng, J, Ying, Z, Fan, G. Exercise impacts brain-derived neurotrophic factor plasticity by engaging mechanisms of epigenetic regulation. Eur J Neurosci. 2011; 33, 383–390.CrossRefGoogle ScholarPubMed
Lee, J, Duan, W, Mattson, MP. Evidence that brain-derived neurotrophic factor is required for basal neurogenesis and mediates, in part, the enhancement of neurogenesis by dietary restriction in the hippocampus of adult mice. J Neurochem. 2002; 82, 1367–1375.CrossRefGoogle ScholarPubMed
Lee, J, Seroogy, KB, Mattson, MP. Dietary restriction enhances neurotrophin expression and neurogenesis in the hippocampus of adult mice. J Neurochem. 2002; 80, 539–547.CrossRefGoogle ScholarPubMed
Lazo-de-la-Vega-Monroy, ML, Mata-Tapia, KA, Garcia-Santillan, JA, et al. Association of placental nutrient sensing pathways with birth weight. Reproduction. 2020; 160, 455–468.Google Scholar
Dubova, EA, Pavlov, KA, Lyapin, VM, Kulikova, GV, Shchyogolev, AI, Sukhikh, GT. Expression of insulin-like growth factors in the placenta in preeclampsia. Bull Exp Biol Med. 2014; 157, 103–107.CrossRefGoogle ScholarPubMed
Ma, M, Zhou, QJ, Xiong, Y, Li, B, Li, XT. Preeclampsia is associated with hypermethylation of IGF-1 promoter mediated by DNMT1. Am J Transl Res. 2018; 10, 16–39.Google ScholarPubMed
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