Perinatal protein malnutrition alters maternal behavior and leads to maladaptive stress response, neurodevelopmental delay and disruption on DNA methylation machinery in female mice offspring

Horm Behav. 2024 Aug:164:105603. doi: 10.1016/j.yhbeh.2024.105603. Epub 2024 Jul 18.

Abstract

Deficiencies in maternal nutrition have long-term consequences affecting brain development of the progeny and its behavior. In the present work, female mice were exposed to a normal-protein or a low-protein diet during gestation and lactation. We analyzed behavioral and molecular consequences of malnutrition in dams and how it affects female offspring at weaning. We have observed that a low-protein diet during pregnancy and lactation leads to anxiety-like behavior and anhedonia in dams. Protein malnutrition during the perinatal period delays physical and neurological development of female pups. Glucocorticoid levels increased in the plasma of malnourished female offspring but not in dams when compared to the control group. Interestingly, the expression of glucocorticoid receptor (GR) was reduced in hippocampus and amygdala on both malnourished dams and female pups. In addition, malnourished pups exhibited a significant increase in the expression of Dnmt3b, Gadd45b, and Fkbp5 and a reduction in Bdnf VI variant mRNA in hippocampus. In contrast, a reduction on Dnmt3b has been observed on the amygdala of weaned mice. No changes have been observed on global methylation levels (5-methylcytosine) in hippocampal genomic DNA neither in dams nor female offspring. In conclusion, deregulated behaviors observed in malnourished dams might be mediated by a low expression of GR in brain regions associated with emotive behaviors. Additionally, low-protein diet differentially deregulates the expression of genes involved in DNA methylation/demethylation machinery in female offspring but not in dams, providing an insight into regional- and age-specific mechanisms due to protein malnutrition.

Keywords: Anxiety-like behavior; DNA methylation; Early life stress; Glucocorticoid receptor; HPA axis; Malnutrition.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amygdala / metabolism
  • Animals
  • Animals, Newborn
  • Antigens, Differentiation
  • Anxiety / etiology
  • Brain-Derived Neurotrophic Factor* / genetics
  • Brain-Derived Neurotrophic Factor* / metabolism
  • DNA (Cytosine-5-)-Methyltransferases / genetics
  • DNA (Cytosine-5-)-Methyltransferases / metabolism
  • DNA Methylation*
  • DNA Methyltransferase 3B
  • Diet, Protein-Restricted
  • Female
  • GADD45 Proteins
  • Glucocorticoids / metabolism
  • Hippocampus* / metabolism
  • Maternal Behavior* / physiology
  • Maternal Nutritional Physiological Phenomena / physiology
  • Mice
  • Neurodevelopmental Disorders / etiology
  • Neurodevelopmental Disorders / genetics
  • Neurodevelopmental Disorders / metabolism
  • Pregnancy
  • Prenatal Exposure Delayed Effects* / metabolism
  • Protein Deficiency / complications
  • Protein Deficiency / metabolism
  • Receptors, Glucocorticoid* / genetics
  • Receptors, Glucocorticoid* / metabolism
  • Stress, Psychological / metabolism
  • Tacrolimus Binding Proteins* / genetics
  • Tacrolimus Binding Proteins* / metabolism

Substances

  • Receptors, Glucocorticoid
  • Tacrolimus Binding Proteins
  • Brain-Derived Neurotrophic Factor
  • tacrolimus binding protein 5
  • DNA (Cytosine-5-)-Methyltransferases
  • Gadd45b protein, mouse
  • DNA Methyltransferase 3B
  • Glucocorticoids
  • GADD45 Proteins
  • Antigens, Differentiation