Intergenerational transmission of maternal care deficiency and offspring development delay induced by perinatal protein malnutrition

References

• Hoeijmakers L, Lucassen PJ, Korosi A. The interplay of early-life stress, nutrition, and immune activation programs adult hippocampal structure and function. Front Mol Neurosci 2015;7(January):1–16.
   Google Scholar
• Hoffmann A, Spengler D. DNA memories of early social life. Neuroscience 2014;264:64–75.
   PubMed Web of Science ®Google Scholar
• Fox SE, Levitt P, Nelson CA. How the timing and quality of early experiences influence the development of brain architecture. Child Dev 2010;81(1):28–40.
   PubMed Web of Science ®Google Scholar
• Krugers HJ, Arp JM, Xiong H, Kanatsou S, Lesuis SL, Korosi A, et al. Early life adversity: lasting consequences for emotional learning. Neurobiol Stress 2017;6:14–21.
   PubMed Web of Science ®Google Scholar
• Food Security Information Network. Global report on food crises. 2017.
   Google Scholar
• Walker SP, Wachs TD, Meeks Gardner J, Lozoff B, Wasserman GA, Pollitt E, et al. Child development: risk factors for adverse outcomes in developing countries. Lancet 2016;369(9556):145–57.
   Google Scholar
• Morgane PJ, Mokler DJ, Galler JR. Effects of prenatal protein malnutrition on the hippocampal formation. Neurosci Biobehav Rev 2002;26(4):471–83.
   PubMed Web of Science ®Google Scholar
• Kar BR, Rao SL, Chandramouli BA. Cognitive development in children with chronic protein energy malnutrition. Behav Brain Funct 2008;4:31.
   PubMed Web of Science ®Google Scholar
• Godoy MA, Souza AS, Lobo MA, Sampaio OV, Moraes L, Baldanza MR, et al. Effects of protein restriction during gestation and lactation on cell proliferation in the hippocampus and subventricular zone: functional implications. protein restriction alters hippocampal/SVZ cell proliferation. Brain Res 2013;1496:10–27.
   PubMed Web of Science ®Google Scholar
• Ranade SC, Rose A, Rao M, Gallego J, Gressens P, Mani S. Different types of nutritional deficiencies affect different domains of spatial memory function checked in a radial arm maze. Neuroscience 2008;152(4):859–66.
   PubMed Web of Science ®Google Scholar
• Maria Moreira Camargo L, de Sousa Almeida S. Early postnatal protein malnutrition changes the development of social play in rats. Physiol Behav 2005;85(3):246–51.
   PubMed Web of Science ®Google Scholar
• Reyes-Castro LA, Rodriguez JS, Charco R, Bautista CJ, Larrea F, Nathanielsz PW, et al. Maternal protein restriction in the rat during pregnancy and/or lactation alters cognitive and anxiety behaviors of female offspring. Int J Dev Neurosci 2012;30(1):39–45.
   PubMed Web of Science ®Google Scholar
• 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;129:237–54.
   PubMed Web of Science ®Google Scholar
• Belluscio LM, Alberca CD, Pregi N, Cánepa ET. Altered gene expression in hippocampus and depressive-like behavior in young adult female mice by early protein malnutrition. Genes, Brain Behav 2016;15(8):741–9.
   PubMed Web of Science ®Google Scholar
• Curley JP, Champagne FA. Influence of maternal care on the developing brain: mechanisms, temporal dynamics and sensitive periods. Front Neuroendocrinol 2016;40:52–66.
   PubMed Web of Science ®Google Scholar
• Meaney MJ, Szyf M. Maternal care as a model for experience-dependent chromatin plasticity? Trends Neurosci 2005;28(9):456–63.
   PubMed Web of Science ®Google Scholar
• Champagne FA, Meaney MJ. Stress during gestation alters postpartum maternal care and the development of the offspring in a rodent model. Biol Psychiatry 2006;59(12):1227–35.
   PubMed Web of Science ®Google Scholar
• Buschdorf JP, Meaney MJ. Epigenetics/programming in the HPA axis. Compr Physiol 2015;6(1):87–110.
   PubMed Web of Science ®Google Scholar
• Cameron N, Del Corpo A, Diorio J, McAllister K, Sharma S, Meaney MJ. Maternal programming of sexual behavior and hypothalamic-pituitary-gonadal function in the female rat. PLoS One 2008;3(5):e2210.
   PubMed Web of Science ®Google Scholar
• Peña CJ, Neugut YD, Calarco CA, Champagne FA. Effects of maternal care on the development of midbrain dopamine pathways and reward-directed behavior in female offspring. Eur J Neurosci 2014;39(6):946–56.
   PubMed Web of Science ®Google Scholar
• Meaney MJ. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci 2001;24:1161–92.
   PubMed Web of Science ®Google Scholar
• Champagne FA. Epigenetic mechanisms and the transgenerational effects of maternal care. Front Neuroendocrinol 2008;29(3):386–97.
   PubMed Web of Science ®Google Scholar
• Peña CJ, Neugut YD, Champagne FA. Developmental timing of the effects of maternal care on gene expression and epigenetic regulation of hormone receptor levels in female rats. Endocrinology 2013;154(11):4340–51.
   PubMed Web of Science ®Google Scholar
• Champagne FA, Francis DD, Mar A, Meaney MJ. Variations in maternal care in the rat as a mediating influence for the effects of environment on development. Physiol Behav 2003;79(3):359–71.
   PubMed Web of Science ®Google Scholar
• Baker S, Chebli M, Rees S, LeMarec N, Godbout R, Bielajew C. Effects of gestational stress: 1. evaluation of maternal and juvenile offspring behavior. Brain Res 2008;1213:98–110.
   PubMed Web of Science ®Google Scholar
• Brummelte S, Galea LAM. Chronic corticosterone during pregnancy and postpartum affects maternal care, cell proliferation and depressive-like behavior in the dam. Horm Behav 2010;58(5):769–79.
   PubMed Web of Science ®Google Scholar
• Nephew BC, Carini LM, Sallah S, Cotino C, Alyamani RAS, Pittet F, et al. Intergenerational accumulation of impairments in maternal behavior following postnatal social stress. Psychoneuroendocrinology 2017;82(May):98–106.
   PubMedGoogle Scholar
• 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):1939–51.
   PubMed Web of Science ®Google Scholar
• Berardino BG, Fesser EA, Cánepa ET. Perinatal protein malnutrition alters expression of miRNA biogenesis genes Xpo5 and Ago2 in mice brain. Neurosci Lett 2017;647:38–44.
   PubMed Web of Science ®Google Scholar
• Cohen J. A coefficient of agreement for nominal scales. Educ Psychol Meas 1960;20(1):37–46.
   Web of Science ®Google Scholar
• Hallgren KA. Computing inter-rater reliability for observational data: an overview and tutorial. Tutor Quant Methods Psychol 2012;8(1):23–34.
   PubMedGoogle Scholar
• Champagne FA, Curley JP, Keverne EB, Bateson PPG. Natural variations in postpartum maternal care in inbred and outbred mice. Physiol Behav 2007;91(2–3):325–34.
   PubMed Web of Science ®Google Scholar
• Ohishi T, Wang L, Akane H, Shiraki A, Sato A, Uematsu M, 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):345–52.
   PubMed Web of Science ®Google Scholar
• R Development Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vol. 0. Vienna: Austria; 2015. ISBN 3-900051-07-0.
   Google Scholar
• Bates D, Mächler M, Bolker B, Walker S. Fitting linear mixed-effects models using lme4. J Stat Softw 2015;67(1):51.
   Web of Science ®Google Scholar
• Pinheiro JC, Bates DM. Mixed-Effects models in S and S-PLUS. New York: Springer-Verlag; 2000. (Statistics and Computing).
   Google Scholar
• Gutièrrez-Mecinas M, Trollope AF, Collins A, Morfett H, Hesketh SA, Kersanté F, et al. Long-lasting behavioral responses to stress involve a direct interaction of glucocorticoid receptors with ERK1/2-MSK1-Elk-1 signaling. Proc Natl Acad Sci USA 2011;108(33):13806–11.
   PubMed Web of Science ®Google Scholar
• Pérez-García G, Guzmán-Quevedo O, Da Silva Aragão R, Bolaños-Jiménez F. Early malnutrition results in long-lasting impairments in pattern-separation for overlapping novel object and novel location memories and reduced hippocampal neurogenesis. Sci Rep 2016;6(August 2015):21275.
   PubMedGoogle Scholar
• Franková S. Relationship between nutrition during lactation and maternal behaviour of rats. Act Nerv Super (Praha) 1971;13(1):1–8.
   PubMedGoogle Scholar
• Smart JL, Preece J. Maternal behavior of undernourished mother rats. Anim Behav 1973;21(3):613–9.
   PubMedGoogle Scholar
• Chaplin TM, Visconti KJ, Molfese PJ, Susman EJ, Klein LC, Sinha R, et al. Prenatal cocaine exposure differentially affects stress responses in girls and boys: associations with future substance use. Dev Psychopathol 2015;27(01):163–80.
   PubMedGoogle Scholar
• Regalado M, Torrero C, Salas M. Maternal responsiveness of neonatally undernourished and sensory stimulated rats: rehabilitation of maternal behavior. Nutr Neurosci 1999;2(1):7–18.
   PubMedGoogle Scholar
• Massaro TF, Levitsky DA, Barnes RH. Protein malnutrition in the rat: its effects on maternal behavior and pup development. Dev Psychobiol 1974;7(6):551–61.
   PubMed Web of Science ®Google Scholar
• Crnic LS. Models of infantile malnutrition in rats: effects on maternal behavior. Dev Psychobiol 1980;13(6):615–28.
   PubMed Web of Science ®Google Scholar
• Rocha JBT, Soares FAA, de Mello CF. Influence of the test situation on pup retrieval behavior of normal and undernourished lactating rats. Brazilian J Med Biol Res 2002;35(1):91–7.
   PubMed Web of Science ®Google Scholar
• 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 2016;8305(May):1–6.
   Google Scholar
• Hall RD, Leahy JP, Robertson WM. The effects of protein malnutrition on the behavior of rats during the suckling period. Dev Psychobiol 1979;12(5):455–66.
   PubMed Web of Science ®Google Scholar
• Baram TZ, Davis EP, Obenaus A, Sandman CA, Small SL, Solodkin A, et al. Fragmentation and unpredictability of early-life experience in mental disorders. Am J Psychiatry 2012;169(9):907–15.
   PubMed Web of Science ®Google Scholar
• Ivy a S, Brunson KL, Sandman C, Baram TZ. Dysfunctional nurturing behavior in rat dams with limited access to nesting material: a clinically relevant model for early-life stress. Neuroscience 2008;154(3):1132–42.
   PubMed Web of Science ®Google Scholar
• Heun-Johnson H, Levitt P. Early-life stress paradigm transiently alters maternal behavior, dam-pup interactions, and offspring vocalizations in mice. Front Behav Neurosci 2016;10:142.
   PubMed Web of Science ®Google Scholar
• Balcombe JP, Barnard ND, Sandusky C. Laboratory routines cause animal stress. Contemp Top Lab Anim Sci 2004;43(6):42–51.
   PubMedGoogle Scholar
• Champagne FA, Meaney MJ. Transgenerational effects of social environment on variations in maternal care and behavioral response to novelty. Behav Neurosci 2007;121(6):1353–63.
   PubMed Web of Science ®Google Scholar
• Curley JP, Davidson S, Bateson P, Champagne FA. Social enrichment during postnatal development induces transgenerational effects on emotional and reproductive behavior in mice. Front Behav Neurosci 2009;3:25.
   PubMed Web of Science ®Google Scholar
• Galler JR, Propert KJ. Early maternal behaviors predictive of the survival of suckling rats with intergenerational malnutrition. J Nutr 1982;112(2):332–7.
   PubMed Web of Science ®Google Scholar
• Weaver ICG, Cervoni N, Champagne FA, D’Alessio AC, Sharma S, Seckl JR, et al. Epigenetic programming by maternal behavior. Nat Neurosci 2004;7(8):847–54.
   Google Scholar
• Stern JM. Offspring-induced nurturance; animal-human parallels. Dev Psychobiol 1997;31(1):19–37.
   PubMed Web of Science ®Google Scholar