Hostname: page-component-848d4c4894-pftt2 Total loading time: 0 Render date: 2024-06-01T00:32:34.931Z Has data issue: false hasContentIssue false

Maternal protein restriction during the lactation period disrupts the ontogenetic development of behavioral traits in male Wistar rat offspring

Published online by Cambridge University Press:  26 April 2023

Juliana de Oliveira-Silva
Affiliation:
Laboratório de Neurofisiologia, Departamento de Ciências Fisiológicas, Instituto de Biologia Roberto Alcantara Gomes, Centro Biomédico, Universidade do Estado do Rio de Janeiro, Av. Prof. Manoel de Abreu 444, 5 andar – Vila Isabel, Rio de Janeiro, RJ, 20550-170, Brazil
Patrícia C. Lisboa
Affiliation:
Laboratório de Fisiologia Endócrina, Departamento de Ciências Fisiológicas, Instituto de Biologia Roberto Alcantara Gomes, Centro Biomédico, Universidade do Estado do Rio de Janeiro, Av. Prof. Manoel de Abreu 444, 5 andar – Vila Isabel, Rio de Janeiro, RJ, 20550-170, Brazil
Bruna Lotufo-Denucci
Affiliation:
Laboratório de Neurofisiologia, Departamento de Ciências Fisiológicas, Instituto de Biologia Roberto Alcantara Gomes, Centro Biomédico, Universidade do Estado do Rio de Janeiro, Av. Prof. Manoel de Abreu 444, 5 andar – Vila Isabel, Rio de Janeiro, RJ, 20550-170, Brazil
Mabel Fraga
Affiliation:
Laboratório de Neurofisiologia, Departamento de Ciências Fisiológicas, Instituto de Biologia Roberto Alcantara Gomes, Centro Biomédico, Universidade do Estado do Rio de Janeiro, Av. Prof. Manoel de Abreu 444, 5 andar – Vila Isabel, Rio de Janeiro, RJ, 20550-170, Brazil
Egberto G. de Moura
Affiliation:
Laboratório de Fisiologia Endócrina, Departamento de Ciências Fisiológicas, Instituto de Biologia Roberto Alcantara Gomes, Centro Biomédico, Universidade do Estado do Rio de Janeiro, Av. Prof. Manoel de Abreu 444, 5 andar – Vila Isabel, Rio de Janeiro, RJ, 20550-170, Brazil
Fernanda C. Nunes
Affiliation:
Laboratório de Neurofisiologia, Departamento de Ciências Fisiológicas, Instituto de Biologia Roberto Alcantara Gomes, Centro Biomédico, Universidade do Estado do Rio de Janeiro, Av. Prof. Manoel de Abreu 444, 5 andar – Vila Isabel, Rio de Janeiro, RJ, 20550-170, Brazil
Anderson Ribeiro-Carvalho
Affiliation:
Departamento de Ciências, Faculdade de Formação de Professores da Universidade do Estado do Rio de Janeiro, Rua Dr. Francisco Portela 1470 – Patronato, São Gonçalo, RJ, 24435-005, Brazil
Cláudio C. Filgueiras
Affiliation:
Laboratório de Neurofisiologia, Departamento de Ciências Fisiológicas, Instituto de Biologia Roberto Alcantara Gomes, Centro Biomédico, Universidade do Estado do Rio de Janeiro, Av. Prof. Manoel de Abreu 444, 5 andar – Vila Isabel, Rio de Janeiro, RJ, 20550-170, Brazil
Yael Abreu-Villaça
Affiliation:
Laboratório de Neurofisiologia, Departamento de Ciências Fisiológicas, Instituto de Biologia Roberto Alcantara Gomes, Centro Biomédico, Universidade do Estado do Rio de Janeiro, Av. Prof. Manoel de Abreu 444, 5 andar – Vila Isabel, Rio de Janeiro, RJ, 20550-170, Brazil
Alex C. Manhães*
Affiliation:
Laboratório de Neurofisiologia, Departamento de Ciências Fisiológicas, Instituto de Biologia Roberto Alcantara Gomes, Centro Biomédico, Universidade do Estado do Rio de Janeiro, Av. Prof. Manoel de Abreu 444, 5 andar – Vila Isabel, Rio de Janeiro, RJ, 20550-170, Brazil
*
Corresponding Author: Alex C. Manhães, Laboratório de Neurofisiologia, Departamento de Ciências Fisiológicas, Instituto de Biologia Roberto Alcantara Gomes, Centro Biomédico, Universidade do Estado do Rio de Janeiro. Av. Prof. Manuel de Abreu 444, 5 andar, Vila Isabel, Rio de Janeiro, RJ, 20550-170, Brazil. Email: ac_manhaes@yahoo.com.br

Abstract

Neonatal undernutrition in rats results in short- and long-term behavioral and hormonal alterations in the offspring. It is not clear, however, whether these effects are present since the original insult or if they develop at some specific age later in life. Here, we assessed the ontogenetic profile of behavioral parameters associated with anxiety, exploration and memory/learning of Wistar rat offspring that were subjected to protein malnutrition during lactation. Dams and respective litters were separated into two groups: (1) protein-restricted (PR), which received a hypoproteic chow (8% protein) from birth to weaning [postnatal day (PN) 21]; (2) control (C), which received normoproteic chow. Offspring’s behaviors, corticosterone, catecholamines, T3 and T4 levels were assessed at PN21 (weaning), PN45 (adolescence), PN90 (young adulthood) or PN180 (adulthood). PR offspring showed an age-independent reduction in the levels of anxiety-like behaviors in the Elevated Plus Maze and better memory performance in the Radial Arm Water Maze. PR offspring showed peak exploratory activity in the Open Field earlier in life, at PN45, than C, which showed theirs at PN90. Corticosterone was reduced in PR offspring, particularly at young adulthood, while catecholamines were increased at weaning and adulthood. The current study shows that considerable age-dependent variations in the expression of the observed behaviors and hormonal levels exist from weaning to adulthood in rats, and that protein restriction during lactation has complex variable-dependent effects on the ontogenesis of the assessed parameters.

Type
Original Article
Copyright
© The Author(s), 2023. Published by Cambridge University Press in association with International Society for Developmental Origins of Health and Disease

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Keats, EC, Das, JK, Salam, RA, et al. Effective interventions to address maternal and child malnutrition: an update of the evidence. Lancet Child Adolesc Health. 2021; 5(5): 367384. https://doi.org/10.1016/S2352-4642(20)30274-1 CrossRefGoogle ScholarPubMed
Owino, VO, Murphy-Alford, AJ, Kerac, M, et al. Measuring growth and medium- and longer-term outcomes in malnourished children. Matern Child Nutr. 2019; 15(3): e12790. https://doi.org/10.1111/mcn.12790 CrossRefGoogle ScholarPubMed
Reyes-Castro, LA, Padilla-Gómez, E, Parga-Martínez, NJ, et al. Hippocampal mechanisms in impaired spatial learning and memory in male offspring of rats fed a low-protein isocaloric diet in pregnancy and/or lactation. Hippocampus. 2018; 28(1): 1830. https://doi.org/10.1002/hipo.22798 CrossRefGoogle ScholarPubMed
Castro-Rodríguez, DC, Rodríguez-González, GL, Menjivar, M, Zambrano, E. Maternal interventions to prevent adverse fetal programming outcomes due to maternal malnutrition: Evidence in animal models. Placenta. 2020; 102: 4954. https://doi.org/10.1016/j.placenta.2020.04.002 CrossRefGoogle ScholarPubMed
Wells, JCK. Developmental plasticity as adaptation: adjusting to the external environment under the imprint of maternal capital. Philos Trans R Soc Lond B Biol Sci. 2019; 374(1770): 20180122. https://doi.org/10.1098/rstb.2018.0122 CrossRefGoogle Scholar
Gomez-Verjan, JC, Barrera-Vázquez, OS, García-Velázquez, L, Samper-Ternent, R, Arroyo, P. Epigenetic variations due to nutritional status in early-life and its later impact on aging and disease. Clin Genet. 2020; 98(4): 313321. https://doi.org/10.1111/cge.13748 CrossRefGoogle ScholarPubMed
Orozco-Solís, R, Matos, RJB, Guzmán-Quevedo, O, et al. Nutritional programming in the rat is linked to long-lasting changes in nutrient sensing and energy homeostasis in the hypothalamus. PLoS One. 2010; 5(10): e13537. https://doi.org/10.1371/journal.pone.0013537 CrossRefGoogle ScholarPubMed
Younes-Rapozo, V, De Moura, EG, Da Silva Lima, N, et al. Early weaning is associated with higher neuropeptide y (NPY) and lower cocaine- and amphetamine-regulated transcript (CART) expressions in the paraventricular nucleus (PVN) in adulthood. British Journal of Nutrition. 2012; 108(12): 22862295. https://doi.org/10.1017/S0007114512000487 CrossRefGoogle ScholarPubMed
Rocha, MLM, Fernandes, PP, Lotufo, BM, Manhães, AC, Barradas, PC, Tenorio, F. Undernutrition during early life alters neuropeptide Y distribution along the arcuate/paraventricular pathway. Neuroscience. 2014; 256: 379391. https://doi.org/10.1016/j.neuroscience.2013.10.040 CrossRefGoogle ScholarPubMed
Younes-Rapozo, V, Moura, EG, Manhães, AC, Peixoto-Silva, N, De Oliveira, E, Lisboa, PC. Early weaning by maternal prolactin inhibition leads to higher neuropeptide Y and astrogliosis in the hypothalamus of the adult rat offspring. British Journal of Nutrition. 2015; 113(3): 536545. https://doi.org/10.1017/S0007114514003882 CrossRefGoogle ScholarPubMed
Dutra-Tavares, AC, Silva, JO, Nunes-Freitas, AL, et al. Maternal undernutrition during lactation alters nicotine reward and DOPAC/dopamine ratio in cerebral cortex in adolescent mice, but does not affect nicotine-induced nAChRs upregulation. Int J Develop Neurosci. 2018; 65(July 2017): 4553. https://doi.org/10.1016/j.ijdevneu.2017.10.007 CrossRefGoogle Scholar
Rocha, MLM, Fernandes, PP, Tenório, F, Manhães, AC, Barradas, PC. Malnourishment during early lactation disrupts the ontogenetic distribution of the CART and α-MSH anorexigenic molecules in the arcuate/paraventricular pathway and lateral hypothalamus in male rats. Brain Res. 2020; 1743(May): 146906. https://doi.org/10.1016/j.brainres.2020.146906 CrossRefGoogle ScholarPubMed
Bertasso, IM, Pietrobon, CB, Da Silva, BS, et al. Hepatic lipid metabolism in adult rats using early weaning models: Sex-related differences. J Dev Orig Health Dis. 2020; 11(5): 499508. https://doi.org/10.1017/S2040174420000495 CrossRefGoogle ScholarPubMed
Soares, PN, Miranda, RA, Bertasso, IM, et al. Late effects of early weaning on food preference and the dopaminergic and endocannabinoid systems in male and female rats. J Dev Orig Health Dis. Published online March 2, 2021: 1-11. https://doi.org/10.1017/S2040174421000039 CrossRefGoogle Scholar
Brioni, JD, Orsingher, OA. Operant behavior and reactivity to the anticonflict effect of diazepam in perinatally undernourished rats. Physiol Behav. 1988; 44(2): 193198. https://doi.org/10.1016/0031-9384(88)90137-0 CrossRefGoogle Scholar
Tonkiss, J, Shultz, P, Galler, JR. An analysis of spatial navigation in prenatally protein malnourished rats. Physiol Behav. 1994; 55(2): 217224. https://doi.org/10.1016/0031-9384(94)90126-0 CrossRefGoogle ScholarPubMed
Strupp, BJ, Levitsky, DA. Enduring cognitive effects of early malnutrition: a theoretical reappraisal. J Nutr. 1995; 125(Suppl. 8): 2221S2232S. https://doi.org/10.1093/jn/125.suppl_8.2221S CrossRefGoogle ScholarPubMed
Valadares, CT, Fukuda, MTH, Françolin-Silva, AL, Hernandes, AS, Almeida, SS. Effects of postnatal protein malnutrition on learning and memory procedures. Nutr Neurosci. 2010; 13(6): 274282. https://doi.org/10.1179/147683010X12611460764769 CrossRefGoogle ScholarPubMed
Brioni, JD, Cordoba, N, Orsingher, OA. Decreased reactivity to the anticonflict effect of diazepam in perinatally undernourished rats. Behav Brain Res. 1989; 34(1-2): 159162. https://doi.org/10.1016/s0166-4328(89)80099-3 CrossRefGoogle Scholar
Santucci, LB, Daud, MM, Almeida, SS, de Oliveira, LM. Effects of early protein malnutrition and environmental stimulation upon the reactivity to diazepam in two animal models of anxiety. Pharmacol Biochem Behav. 1994; 49(2): 393398. https://doi.org/10.1016/0091-3057(94)90439-1 CrossRefGoogle ScholarPubMed
Almeida, SS, Tonkiss, J, Galler, JR. Prenatal protein malnutrition affects exploratory behavior of female rats in the elevated plus-maze test. Physiol Behav. 1996; 60(2): 675680. https://doi.org/10.1016/s0031-9384(96)80047-3 CrossRefGoogle ScholarPubMed
Hernandes, AS, Almeida, SS. Postnatal protein malnutrition affects inhibitory avoidance and risk assessment behaviors in two models of anxiety in rats. Nutr Neurosci. 2003; 6(4): 213219. https://doi.org/10.1080/1028415031000137527 CrossRefGoogle ScholarPubMed
Françolin-Silva, AL, da Silva Hernandes, A, Fukuda, MTH, Valadares, CT, Almeida, SS. Anxiolytic-like effects of short-term postnatal protein malnutrition in the elevated plus-maze test. Behav Brain Res. 2006; 173(2): 310314. https://doi.org/10.1016/j.bbr.2006.06.042 CrossRefGoogle ScholarPubMed
Pereira-da-Silva, MS, Cabral-Filho, JE, De-Oliveira, LM. Effect of early malnutrition and environmental stimulation in the performance of rats in the elevated plus maze. Behavioural brain research. 2009; 205(1): 286289. https://doi.org/10.1016/j.bbr.2009.05.031 CrossRefGoogle ScholarPubMed
Belluscio, LM, Berardino, BG, Ferroni, NM, Ceruti, JM, Cánepa, ET. Early protein malnutrition negatively impacts physical growth and neurological reflexes and evokes anxiety and depressive-like behaviors. Physiol Behav. 2014; 129: 237254. https://doi.org/10.1016/j.physbeh.2014.02.051 CrossRefGoogle ScholarPubMed
Ohishi, T, Wang, L, Akane, H, et al. Adolescent hyperactivity of offspring after maternal protein restriction during the second half of gestation and lactation periods in rats. J Toxicol Sci. 2012; 37(2): 345352. https://doi.org/10.2131/jts.37.345 CrossRefGoogle ScholarPubMed
Reyes-Castro, LA, Rodriguez, JS, Rodríguez-González, GL, et al. Pre- and/or postnatal protein restriction developmentally programs affect and risk assessment behaviors in adult male rats. Behav Brain Res. 2012; 227(2): 324329. https://doi.org/10.1016/j.bbr.2011.06.008 CrossRefGoogle ScholarPubMed
Dutra-Tavares, AC, Manhães, AC, Silva, JO, et al. Locomotor response to acute nicotine in adolescent mice is altered by maternal undernutrition during lactation. Int J Dev Neurosci. 2015; 47(Pt B): 278285. https://doi.org/10.1016/j.ijdevneu.2015.10.002 CrossRefGoogle ScholarPubMed
Fukuda, MTH, Françolin-Silva, AL, Almeida, SS. Early postnatal protein malnutrition affects learning and memory in the distal but not in the proximal cue version of the Morris water maze. Behav Brain Res. 2002; 133(2): 271277. https://doi.org/10.1016/s0166-4328(02)00010-4 CrossRefGoogle Scholar
Lynn, DA, Brown, GR. The ontogeny of exploratory behavior in male and female adolescent rats (Rattus norvegicus). Dev Psychobiol. 2009; 51(6): 513520. https://doi.org/10.1002/dev.20386 CrossRefGoogle ScholarPubMed
Lynn, DA, Brown, GR. The ontogeny of anxiety-like behavior in rats from adolescence to adulthood. Dev Psychobiol. 2010; 52(8): 731739. https://doi.org/10.1002/dev.20468 CrossRefGoogle ScholarPubMed
Moreira, EG, Vassilieff, I, Vassilieff, VS. Developmental lead exposure: behavioral alterations in the short and long term. Neurotoxicol Teratol. 2001; 23(5): 489495. https://doi.org/10.1016/s0892-0362(01)00159-3 CrossRefGoogle ScholarPubMed
Estanislau, C, Morato, S. Behavior ontogeny in the elevated plus-maze: prenatal stress effects. Int J Dev Neurosci. 2006; 24(4): 255262. https://doi.org/10.1016/j.ijdevneu.2006.03.001 CrossRefGoogle ScholarPubMed
Seliger, DL. Effects of age, sex, and brightness of rield on open-field behaviors of rats. Percept Mot Skills. 1977; 45(3 Pt 2): 10591067. https://doi.org/10.2466/pms.1977.45.3f.1059 CrossRefGoogle ScholarPubMed
Kobayashi, S, Kametani, H, Ugawa, Y, Osanai, M. Age difference of response strategy in radial maze performance of Fischer-344 rats. Physiol Behav. 1988; 42(3): 277280. https://doi.org/10.1016/0031-9384(88)90082-0 CrossRefGoogle ScholarPubMed
Lindner, MD. Reliability, distribution, and validity of age-related cognitive deficits in the Morris water maze. Neurobiol Learn Mem. 1997; 68(3): 203220. https://doi.org/10.1006/nlme.1997.3782 CrossRefGoogle ScholarPubMed
Jonasson, Z. Meta-analysis of sex differences in rodent models of learning and memory: a review of behavioral and biological data. Neurosci Biobehav Rev. 2005; 28(8): 811825. https://doi.org/10.1016/j.neubiorev.2004.10.006 CrossRefGoogle ScholarPubMed
Lotufo, BM, Tenório, F, Barradas, PC, et al. Maternal protein-free diet during lactation programs male wistar rat offspring for increased novelty-seeking, locomotor activity, and visuospatial performance. Behav Neurosci. 2018; 132(2): 114127. https://doi.org/10.1037/bne0000234 CrossRefGoogle ScholarPubMed
Fagundes, ATS, Moura, EG, Passos, MCF, et al. Maternal low-protein diet during lactation programmes body composition and glucose homeostasis in the adult rat offspring. Br J Nutr. 2007; 98(5): 922928. https://doi.org/10.1017/S0007114507750924 CrossRefGoogle ScholarPubMed
Lisboa, PC, Fagundes, ATS, Denolato, ATA, et al. Neonatal low-protein diet changes deiodinase activities and pituitary TSH response to TRH in adult rats. Exp Biol Med (Maywood). 2008; 233(1): 5763. https://doi.org/10.3181/0705-RM-146 CrossRefGoogle ScholarPubMed
de Oliveira, JC, Gomes, RM, Miranda, RA, et al. Protein restriction during the last third of pregnancy malprograms the neuroendocrine axes to induce metabolic syndrome in adult male rat offspring. Endocrinology. 2016; 157(5): 17991812. https://doi.org/10.1210/en.2015-1883 CrossRefGoogle ScholarPubMed
Ladyman, SR, Brooks, VL. Central actions of insulin during pregnancy and lactation. J Neuroendocrinol. 2021; 33(4): e12946. https://doi.org/10.1111/jne.12946 CrossRefGoogle ScholarPubMed
Fagundes, ATS, Moura, EG, Passos, MCF, et al. Temporal evaluation of body composition, glucose homeostasis and lipid profile of male rats programmed by maternal protein restriction during lactation. Hormone Metabol Res. 2009; 41(12): 866873. https://doi.org/10.1055/s-0029-1233457 CrossRefGoogle ScholarPubMed
Lisboa, P, Oliveira, E, Fagundes, AT, et al. Postnatal low protein diet programs leptin signaling in the hypothalamic-pituitary-thyroid axis and pituitary TSH response to leptin in adult male rats. Hormone Metabol Res. 2012; 44(02): 114122. https://doi.org/10.1055/s-0031-1299747 Google ScholarPubMed
Lisboa, PC, Fagundes, ATS, Denolato, ATA, et al. Neonatal low-protein diet changes deiodinase activities and pituitary TSH response to TRH in adult rats. Exp Biol Med. 2008; 233(1): 5763. https://doi.org/10.3181/0705-RM-146 CrossRefGoogle ScholarPubMed
Ramos, CF, Teixeira, C V, Passos, MC, et al. Low-protein diet changes thyroid function in lactating rats. Proc Soc Exp Biol Med. 2000; 224(4): 256263. https://doi.org/10.1046/j.1525-1373.2000.22429.x CrossRefGoogle ScholarPubMed
Fagundes, ATS, Moura, EG, Passos, MCF, et al. Maternal low-protein diet during lactation programmes body composition and glucose homeostasis in the adult rat offspring. Br J Nutr. 2007; 98(5): 922928. https://doi.org/10.1017/S0007114507750924 CrossRefGoogle ScholarPubMed
Passos, MC, Ramos, CF, Bernardo-Filho, M, de Mattos, DM, Moura, EG. The effect of protein or energy restriction on the biodistribution of Na99TcmO4 in Wistar rats. Nucl Med Commun. 2000; 21(11): 10591062. https://doi.org/10.1097/00006231-200011000-00012 CrossRefGoogle ScholarPubMed
Quinn, R. Comparing rat’s to human’s age: How old is my rat in people years? Nutrition. 2005; 21(6): 775777. https://doi.org/10.1016/j.nut.2005.04.002 CrossRefGoogle ScholarPubMed
Passos, MC, Vicente, LL, Lisboa, PC, de Moura, EG. Absence of anorectic effect to acute peripheral leptin treatment in adult rats whose mothers were malnourished during lactation. Horm Metab Res. 2004; 36(9): 625629. https://doi.org/10.1055/s-2004-825927 CrossRefGoogle ScholarPubMed
Reeves, PG, Nielsen, FH, Fahey, GC. AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr. 1993; 123(11): 19391951. https://doi.org/10.1093/jn/123.11.1939 CrossRefGoogle Scholar
Fraga-Marques, MC, Moura, EG, Claudio-Neto, S, et al. Neonatal hyperleptinaemia programmes anxiety-like and novelty seeking behaviours but not memory/learning in adult rats. Horm Behav. 2009; 55(2): 272279. https://doi.org/10.1016/j.yhbeh.2008.11.010 CrossRefGoogle Scholar
Fraga-Marques, MC, Moura, EG, Silva, JO, et al. Effects of maternal hyperleptinaemia during lactation on short-term memory/learning, anxiety-like and novelty-seeking behavioral traits of adult male rats. Behav Brain Res. 2010; 206(1): 147150. https://doi.org/10.1016/j.bbr.2009.08.029 CrossRefGoogle ScholarPubMed
Fraga, MC, Moura, EG, Silva, JO, et al. Maternal prolactin inhibition at the end of lactation affects learning/memory and anxiety-like behaviors but not novelty-seeking in adult rat progeny. Pharmacol Biochem Behav. 2011; 100(1): 165173. https://doi.org/10.1016/j.pbb.2011.07.007 CrossRefGoogle Scholar
Pinheiro, CR, Moura, EG, Manhães, AC, et al. Maternal nicotine exposure during lactation alters food preference, anxiety-like behavior and the brain dopaminergic reward system in the adult rat offspring. Physiol Behav. 2015; 149: 131141. https://doi.org/10.1016/j.physbeh.2015.05.040 CrossRefGoogle ScholarPubMed
Abreu-Villaça, Y, Cavina, CC, Ribeiro-Carvalho, A, et al. Combined exposure to tobacco smoke and ethanol during adolescence leads to short- and long-term modulation of anxiety-like behavior. Drug Alcohol Depend. 2013; 133(1): 5260. https://doi.org/10.1016/j.drugalcdep.2013.05.033 CrossRefGoogle Scholar
da Silva, BS, Pietrobon, CB, Bertasso, IM, et al. Short and long-term effects of bisphenol S (BPS) exposure during pregnancy and lactation on plasma lipids, hormones, and behavior in rats. Environmental Pollution. 2019; 250: 312322. https://doi.org/10.1016/j.envpol.2019.03.100 CrossRefGoogle Scholar
Fraga, MC, de Moura, EG, da Silva Lima, N, et al. Anxiety-like, novelty-seeking and memory/learning behavioral traits in male Wistar rats submitted to early weaning. Physiol Behav. 2014; 124: 100106. https://doi.org/10.1016/j.physbeh.2013.11.001 CrossRefGoogle ScholarPubMed
Pellow, S, Chopin, P, File, SE, Briley, M. Validation of open:closed arm entries in an elevated plus-maze as a measure of anxiety in the rat. J Neurosci Methods. 1985; 14(3): 149167. https://doi.org/10.1016/0165-0270(85)90031-7 CrossRefGoogle Scholar
Rodgers, RJ, Cao, BJ, Dalvi, A, Holmes, A. Animal models of anxiety: an ethological perspective. Braz J Med Biol Res. 1997; 30(3): 289304. https://doi.org/10.1590/s0100-879x1997000300002 CrossRefGoogle ScholarPubMed
Carobrez, AP, Bertoglio, LJ. Ethological and temporal analyses of anxiety-like behavior: the elevated plus-maze model 20 years on. Neurosci Biobehav Rev. 2005; 29(8): 11931205. https://doi.org/10.1016/j.neubiorev.2005.04.017 CrossRefGoogle Scholar
Manhães, AC, Guthierrez, MCS, Filgueiras, CC, Abreu-Villaça, Y. Anxiety-like behavior during nicotine withdrawal predict subsequent nicotine consumption in adolescent C57BL/6 mice. Behavioural Brain Research. 2008; 193(2): 216224. https://doi.org/10.1016/j.bbr.2008.05.018 CrossRefGoogle ScholarPubMed
Crawley, JN. Behavioral phenotyping of transgenic and knockout mice: experimental design and evaluation of general health, sensory functions, motor abilities, and specific behavioral tests. Brain Res. 1999; 835(1): 1826. https://doi.org/10.1016/s0006-8993(98)01258-x CrossRefGoogle ScholarPubMed
Prut, L, Belzung, C. The open field as a paradigm to measure the effects of drugs on anxiety-like behaviors: a review. Eur J Pharmacol. 2003; 463(1-3): 333. https://doi.org/10.1016/s0014-2999(03)01272-x CrossRefGoogle Scholar
Jarrard, LE. On the role of the hippocampus in learning and memory in the rat. Behav Neural Biol. 1993; 60(1): 926. https://doi.org/10.1016/0163-1047(93)90664-4 CrossRefGoogle ScholarPubMed
Buresová, O, Bures, J, Oitzl, MS, Zahálka, A. Radial maze in the water tank: an aversively motivated spatial working memory task. Physiol Behav. 1985; 34(6): 10031005. https://doi.org/10.1016/0031-9384(85)90028-9 CrossRefGoogle ScholarPubMed
Tomás Pereira, I, Burwell, RD. Using the spatial learning index to evaluate performance on the water maze. Behav Neurosci. 2015; 129(4): 533539. https://doi.org/10.1037/bne0000078 CrossRefGoogle ScholarPubMed
Soares, PN, Rodrigues, VST, Peixoto, TC, et al. Cigarette smoke during breastfeeding in rats changes glucocorticoid and vitamin D status in obese adult offspring. Int J Mol Sci. 2018; 19(10). https://doi.org/10.3390/ijms19103084 Google Scholar
Miranda, RA, de Moura, EG, Soares, PN, et al. Thyroid redox imbalance in adult Wistar rats that were exposed to nicotine during breastfeeding. Sci Rep. 2020; 10(1): 112. https://doi.org/10.1038/s41598-020-72725-w CrossRefGoogle ScholarPubMed
Trevenzoli, IH, Pinheiro, CR, Conceição, EPS, et al. Programming of rat adrenal medulla by neonatal hyperleptinemia: adrenal morphology, catecholamine secretion, and leptin signaling pathway. Am J Physiol Endocrinol Metab. 2010; 298(5): E941E949. https://doi.org/10.1152/ajpendo.00734.2009 CrossRefGoogle ScholarPubMed
Huynh, H, Feldt, LS. Estimation of the Box correction for degrees of freedom from the sample data in randomized block and split-plot designs. J Educ Stat. 1976; 1(1): 6982.CrossRefGoogle Scholar
Snedocor, GW, Cochran, WC. Statistical Methods. 6th ed. Iowa State University Press, 1967.Google Scholar
Bautista, CJ, Bautista, RJ, Montaño, S, et al. Effects of maternal protein restriction during pregnancy and lactation on milk composition and offspring development. Br J Nutr. 2019; 122(2): 141151. https://doi.org/10.1017/S0007114519001120 CrossRefGoogle ScholarPubMed
Hall, B. Changing composition of human milk and early development of an appetite control. Lancet. 1975; 1(7910): 779781. https://doi.org/10.1016/s0140-6736(75)92440-x CrossRefGoogle ScholarPubMed
Bautista, CJ, Boeck, L, Larrea, F, Nathanielsz, PW, Zambrano, E. Effects of a maternal low protein isocaloric diet on milk leptin and progeny serum leptin concentration and appetitive behavior in the first 21 days of neonatal life in the rat. Pediatr Res. 2008; 63(4): 358363. https://doi.org/10.1203/01.pdr.0000304938.78998.21 CrossRefGoogle ScholarPubMed
Liu, Z, Roy, NC, Guo, Y, et al. Human breast milk and infant formulas differentially modify the intestinal microbiota in human infants and host physiology in rats. J Nutr. 2016; 146(2): 191199. https://doi.org/10.3945/jn.115.223552 CrossRefGoogle ScholarPubMed
Lisboa, PC, Passos, MC, Dutra, SC, et al. Leptin and prolactin, but not corticosterone, modulate body weight and thyroid function in protein-malnourished lactating rats. Horm Metab Res. 2006; 38(5): 295299. https://doi.org/10.1055/s-2006-925390 CrossRefGoogle Scholar
Teixeira, C, Passos, M, Ramos, C, Dutra, S, Moura, E. Leptin serum concentration, food intake and body weight in rats whose mothers were exposed to malnutrition during lactation. J Nutr Biochem. 2002; 13(8): 493. https://doi.org/10.1016/s0955-2863(02)00197-3 CrossRefGoogle ScholarPubMed
de Moura, EG, Lisboa, PC, Custódio, CM, Nunes, MT, de Picoli Souza, K, Passos, MCF. Malnutrition during lactation changes growth hormone mRNA expression in offspring at weaning and in adulthood. J Nutr Biochem. 2007; 18(2): 134139. https://doi.org/10.1016/j.jnutbio.2006.04.002 CrossRefGoogle ScholarPubMed
Almeida, SS, de Oliveira, LM, Graeff, FG. Early life protein malnutrition changes exploration of the elevated plus-maze and reactivity to anxiolytics. Psychopharmacology (Berl). 1991; 103(4): 513518. https://doi.org/10.1007/BF02244251 CrossRefGoogle ScholarPubMed
Almeida, SS, Garcia, RA, de Oliveira, LM. Effects of early protein malnutrition and repeated testing upon locomotor and exploratory behaviors in the elevated plus-maze. Physiol Behav. 1993; 54(4): 749752. https://doi.org/10.1016/0031-9384(93)90086-u CrossRefGoogle ScholarPubMed
Batista, TH, Veronesi, VB, Ribeiro, ACAF, Giusti-Paiva, A, Vilela, FC. Protein malnutrition during pregnancy alters maternal behavior and anxiety-like behavior in offspring. Nutr Neurosci. 2017; 20(8): 437442. https://doi.org/10.1080/1028415X.2016.1177320 CrossRefGoogle ScholarPubMed
Cintra, L, Díaz-Cintra, S, Galván, A, Kemper, T, Morgane, PJ. Effects of protein undernutrition on the dentate gyrus in rats of three age groups. Brain Res. 1990; 532(1-2): 271277. https://doi.org/10.1016/0006-8993(90)91769-d CrossRefGoogle ScholarPubMed
Córdoba, NE, Cuadra, GR, Brioni, JD, Orsingher, OA. Perinatal protein deprivation enhances the anticonflict effect measured after chronic ethanol administration in adult rats. J Nutr. 1992; 122(7): 15361541. https://doi.org/10.1093/jn/122.7.1536 CrossRefGoogle ScholarPubMed
Matos, RJB, Orozco-Solís, R, Lopes de Souza, S, Manhães-de-Castro, R, Bolaños-Jiménez, F. Nutrient restriction during early life reduces cell proliferation in the hippocampus at adulthood but does not impair the neuronal differentiation process of the new generated cells. Neuroscience. 2011; 196: 1624. https://doi.org/10.1016/j.neuroscience.2011.08.071 CrossRefGoogle Scholar
Austin, KB, Bronzino, J, Morgane, PJ. Prenatal protein malnutrition affects synaptic potentiation in the dentate gyrus of rats in adulthood. Brain Res. 1986; 394(2): 267273. https://doi.org/10.1016/0165-3806(86)90102-1 CrossRefGoogle ScholarPubMed
Blatt, GJ, Chen, JC, Rosene, DL, Volicer, L, Galler, JR. Prenatal protein malnutrition effects on the serotonergic system in the hippocampal formation: an immunocytochemical, ligand binding, and neurochemical study. Brain Res Bull. 1994; 34(5): 507518. https://doi.org/10.1016/0361-9230(94)90025-6 CrossRefGoogle ScholarPubMed
Del Angel-Meza, AR, Ramírez-Cortes, L, Adame-González, IG, González Burgos, I, Beas-Zárate, C. Cerebral GABA release and GAD activity in protein- and tryptophan-restricted rats during development. Int J Dev Neurosci. 2002; 20(1): 4754. https://doi.org/10.1016/s0736-5748(01)00066-1 CrossRefGoogle ScholarPubMed
Bryant, KG, Barker, JM. Arbitration of approach-avoidance conflict by ventral hippocampus. Front Neurosci. 2020; 14: 615337. https://doi.org/10.3389/fnins.2020.615337 CrossRefGoogle ScholarPubMed
Puzzo, D, Lee, L, Palmeri, A, Calabrese, G, Arancio, O. Behavioral assays with mouse models of Alzheimer’s disease: practical considerations and guidelines. Biochem Pharmacol. 2014; 88(4): 450467. https://doi.org/10.1016/j.bcp.2014.01.011 CrossRefGoogle ScholarPubMed
Kesner, RP, Crutcher, KA, Measom, MO. Medial septal and nucleus basalis magnocellularis lesions produce order memory deficits in rats which mimic symptomatology of Alzheimer’s disease. Neurobiol Aging. 1986; 7(4): 287295. https://doi.org/10.1016/0197-4580(86)90009-6 CrossRefGoogle ScholarPubMed
Wong, CC, Döhler, KD, Atkinson, MJ, Geerlings, H, Hesch, RD, von zur Mühlen A. Circannual variations in serum concentrations of pituitary, thyroid, parathyroid, gonadal and adrenal hormones in male laboratory rats. J Endocrinol. 1983; 97(2): 179185. https://doi.org/10.1677/joe.0.0970179 CrossRefGoogle ScholarPubMed
Young, JB. Programming of sympathoadrenal function. Trends Endocrinol Metab. 2002; 13(9): 381385. https://doi.org/10.1016/s1043-2760(02)00661-6 CrossRefGoogle ScholarPubMed
Matthews, SG, McGowan, PO. Developmental programming of the HPA axis and related behaviours: epigenetic mechanisms. J Endocrinol. 2019; 242(1): T69T79. https://doi.org/10.1530/JOE-19-0057 CrossRefGoogle ScholarPubMed
Venci, RdO, Ramos, GB, Martins, IP, et al. Malnutrition during late pregnancy exacerbates high-fat-diet-induced metabolic dysfunction associated with lower sympathetic nerve tonus in adult rat offspring. Nutr Neurosci. 2020; 23(6): 432443. https://doi.org/10.1080/1028415X.2018.1516845 CrossRefGoogle ScholarPubMed
de Oliveira, JC, Grassiolli, S, Gravena, C, de Mathias, PCF. Early postnatal low-protein nutrition, metabolic programming and the autonomic nervous system in adult life. Nutr Metab (Lond). 2012; 9(1): 80. https://doi.org/10.1186/1743-7075-9-80 CrossRefGoogle ScholarPubMed
Coleoni, AH, Munaro, N, Recúpero, AR, Cherubini, O. Nuclear triiodothyronine receptors and metabolic response in perinatally protein-deprived rats. Acta Endocrinol (Copenh). 1983; 104(4): 450455. https://doi.org/10.1530/acta.0.1040450 Google ScholarPubMed
Ramos, CF, Teixeira, CV, Passos, MCF, et al. Low-protein diet changes thyroid function in lactating rats. Proc Soc Exp Biol Med. 2000; 224(4): 256263. https://doi.org/10.1046/j.1525-1373.2000.22429.x CrossRefGoogle ScholarPubMed
Passos, MCF, Ramos, CF, Dutra, SCP, Bernardo-Filho, M, Moura, EG. Biodistribution of 99mTc-O4Na changes in adult rats whose mothers were malnourished during lactation. J Nucl Med. 2002; 43(1): 8991.Google ScholarPubMed
Passos, MC, da Fonte Ramos, C, Dutra, SC, Mouço, T, de Moura, EG. Long-term effects of malnutrition during lactation on the thyroid function of offspring. Hormone Metab Res. 2002; 34(1): 4043. https://doi.org/10.1055/s-2002-19966 CrossRefGoogle ScholarPubMed
Lisboa, P, Passos, M, Dutra, S, et al. Increased 5’-iodothyronine deiodinase activity is a maternal adaptive mechanism in response to protein restriction during lactation. Journal of Endocrinology. 2003; 177(2): 261267. https://doi.org/10.1677/joe.0.1770261 CrossRefGoogle ScholarPubMed
Lisboa, PC, Fagundes, ATS, Denolato, ATA, et al. Neonatal low-protein diet changes deiodinase activities and pituitary TSH response to TRH in adult rats. Exp Biol Med (Maywood). 2008; 233(1): 5763. https://doi.org/10.3181/0705-RM-146 CrossRefGoogle ScholarPubMed
Zambrano, E, Bautista, CJ, Deás, M, et al. A low maternal protein diet during pregnancy and lactation has sex- and window of exposure-specific effects on offspring growth and food intake, glucose metabolism and serum leptin in the rat. J Physiol. 2006; 571(1): 221230. https://doi.org/10.1113/jphysiol.2005.100313 CrossRefGoogle ScholarPubMed
Bertasso, IM, de Moura, EG, Pietrobon, CB, et al. Low protein diet during lactation programs hepatic metabolism in adult male and female rats. J Nutr Biochem. 2022; 108: 109096. https://doi.org/10.1016/j.jnutbio.2022.109096 CrossRefGoogle ScholarPubMed
Supplementary material: PDF

de Oliveira-Silva et al. supplementary material

de Oliveira-Silva et al. supplementary material

Download de Oliveira-Silva et al. supplementary material(PDF)
PDF 630.5 KB