Altered gene expression in hippocampus and depressive-like behavior in young adult female mice by early protein malnutrition

Genes, Brain and Behavior

Volumn 15, Issue 8, 2016, Pages 741-749

  Belluscio, L M ^a,b   Alberca, C D ^a   Pregi, N ^a,b   Canepa E T ^a,b  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

Author keywords

c fos; Calcineurin; depressive like behavior; early life stress; Egr1; forced swimming test; hippocampus; malnutrition; mice; perinatal period

Indexed keywords

CALCINEURIN; EARLY GROWTH RESPONSE FACTOR 1; PROTEIN C FOS;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR; CONTROLLED STUDY; COPING BEHAVIOR; DEPRESSION; FEMALE; FORCED SWIM TEST; GENE EXPRESSION; HIPPOCAMPUS; KWASHIORKOR; MALNUTRITION; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; ANIMAL; ANIMAL BEHAVIOR; ANXIETY; DISEASE MODEL; GENETICS; MALE; MENTAL STRESS; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; PREGNANCY; PROTEIN CALORIE MALNUTRITION; PSYCHOLOGY;

ADAPTATION, PSYCHOLOGICAL; ANIMALS; ANXIETY; BEHAVIOR, ANIMAL; DEPRESSION; DEPRESSIVE DISORDER; DISEASE MODELS, ANIMAL; FEMALE; GENE EXPRESSION; HIPPOCAMPUS; MALE; MICE; NEURONAL PLASTICITY; PREGNANCY; PROTEIN-ENERGY MALNUTRITION; STRESS, PSYCHOLOGICAL;

EID: 84990040798     PISSN: 16011848     EISSN: 1601183X     Source Type: Journal    
DOI: 10.1111/gbb.12322     Document Type: Article

References (61)

1. Alamy, M. & Bengelloun, W.A. (2012) Malnutrition and brain development: an analysis of the effects of inadequate diet during different stages of life in rat. Neurosci Biobehav Rev 36, 1463–1480.
2. Altemus, M. (2006) Sex differences in depression and anxiety disorders: potential biological determinants. Horm Behav 50, 534–538.
3. Andersen, S.L. (2003) Trajectories of brain development: point of vulnerability or window of opportunity? Neurosci Biobehav Rev 27, 3–18.
4. Bahi, A., Mineur, Y.S. & Picciotto, M.R. (2009) Blockade of protein phosphatase 2B activity in the amygdala increases anxiety- and depression-like behaviors in mice. Biol Psychiatry 66, 1139–1146.
5. Bale, T.L. & Epperson, C.N. (2015) Sex differences and stress across the lifespan. Nat Neurosci 18, 35–42.
6. Belluscio, L.M., Berardino, B.G., Ferroni, N.M., Ceruti, J.M. & Cánepa, E.T. (2014) Early protein malnutrition negatively impacts physical growth and neurological reflexes and evokes anxiety and depressive-like behaviors. Physiol Behav 129, 237–254.
7. Bilang-Bleuel, A., Rech, J., De Carli, S., Holsboer, F. & Reul, J.M.H.M. (2002) Forced swimming evokes a biphasic response in CREB phosphorylation in extrahypothalamic limbic and neocortical brain structures in the rat. Eur J Neurosci 15, 1048–1060.
8. Burdge, G.C. & Lillycrop, K.A. (2010) Nutrition, epigenetics, and developmental plasticity: implications for understanding human disease. Annu Rev Nutr 30, 315–339.
9. Carter, S.D., Mifsud, K.R. & Reul, J.M.H.M. (2015) Distinct epigenetic and gene expression changes in rat hippocampal neurons after Morris water maze training. Front Behav Neurosci 9, 156.
10. Chmurzynska, A. (2010) Fetal programming: link between early nutrition, DNA methylation, and complex diseases. Nutr Rev 68, 87–98.
11. Costa, A.P.R., Vieira, C., Bohner, L.O.L., Silva, C.F., Santos, E.C.D.S., De Lima, T.C.M. & Lino-de-Oliveira, C. (2013) A proposal for refining the forced swim test in Swiss mice. Prog Neuropsychopharmacol Biol Psychiatry 45, 150–155.
12. Crozatier, C., Farley, S., Mansuy, I.M., Dumas, S., Giros, B. & Tzavara, E.T. (2007) Calcineurin (protein phosphatase 2B) is involved in the mechanisms of action of antidepressants. Neuroscience 144, 1470–1476.
13. Curley, J.P. & Champagne, F.A. (2015) Influence of maternal care on the developing brain: mechanisms, temporal dynamics and sensitive periods. Front Neuroendocrinol 40, 52–66.
14. Danese, A. & McEwen, B.S. (2012) Adverse childhood experiences, allostasis, allostatic load, and age-related disease. Physiol Behav 106, 29–39.
15. Ericsson, C., Peredo, I. & Nistér, M. (2007) Optimized protein extraction from cryopreserved brain tissue samples. Acta Oncol 46, 10–20.
16. Fox, S.E., Levitt, P. & Nelson, C.A. (2010) How the timing and quality of early experiences influence the development of brain architecture. Child Dev 81, 28–40.
17. Franklin, K.B.J. & Paxinos, G. (2007) The Mouse Brain in Stereotaxic Coordinates, 3rd edn. Academic Press, London.
18. de la Fuente, V., Federman, N., Fustiñana, M.S., Zalcman, G. & Romano, A. (2014) Calcineurin phosphatase as a negative regulator of fear memory in hippocampus: control on nuclear factor-κB signaling in consolidation and reconsolidation. Hippocampus 24, 1549–1561.
19. Galler, J.R., Bryce, C.P., Waber, D., Hock, R.S., Exner, N., Eaglesfield, D., Fitzmaurice, G. & Harrison, R. (2010) Early childhood malnutrition predicts depressive symptoms at ages 11–17. J Child Psychol Psychiatry 51, 789–798.
20. Gerges, N.Z., Aleisa, A.M., Schwarz, L.A. & Alkadhi, K.A. (2003) Chronic psychosocial stress decreases calcineurin in the dentate gyrus: a possible mechanism for preservation of early LTP. Neuroscience 117, 869–874.
21. de Godoy, M.A., de Souza, A.S., Lobo, M.A., Sampaio, O.V.K., Moraes, L., Baldanza, M.R., Magri, T.P.R., Wernerck de Castro, J.P.S., Tavares do Carmo, M.D.G., Soares-Mota, M., Rocha, M.S., Mendez-Otero, R. & Santiago, M.F. (2013) 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 1496, 10–27.
22. Gomez, J.L. & Luine, V.N. (2014) Female rats exposed to stress and alcohol show impaired memory and increased depressive-like behaviors. Physiol Behav 123, 47–54.
23. Gutièrrez-Mecinas, M., Trollope, A.F., Collins, A., Morfett, H., Hesketh, S.A., Kersanté, F. & Reul, J.M.H.M. (2011) Long-lasting behavioral responses to stress involve a direct interaction of glucocorticoid receptors with ERK1/2-MSK1-Elk-1 signaling. Proc Natl Acad Sci U S A 108, 13806–13811.
24. Hao, Y., Huang, W., Nielsen, D.A. & Kosten, T.A. (2011) Litter gender composition and sex affect maternal behavior and DNA methylation levels of the Oprm1 gene in rat offspring. Front Psychiatry 2, 21.
25. Herrera, D.G. & Robertson, H.A. (1996) Activation of c-fos in the brain. Prog Neurobiol 50, 83–107.
26. Kar, B.R., Rao, S.L. & Chandramouli, B.A. (2008) Cognitive development in children with chronic protein energy malnutrition. Behav Brain Funct 4, 31.
27. Kim, P., Evans, G. & Angstadt, M. (2013) Effects of childhood poverty and chronic stress on emotion regulatory brain function in adulthood. Proc Natl Acad Sci U S A 110, 18442–18447.
28. Klee, C.B., Ren, H. & Wang, X. (1998) Regulation of the calmodulin-stimulated protein phosphatase, calcineurin. J Biol Chem 273, 13367–13370.
29. Korosi, A., Naninck, E.F.G., Oomen, C.A., Schouten, M., Krugers, H., Fitzsimons, C. & Lucassen, P.J. (2012) Early-life stress mediated modulation of adult neurogenesis and behavior. Behav Brain Res 227, 400–409.
30. Laus, M.F., Vales, L.D.M.F., Costa, T.M.B. & Almeida, S.S. (2011) Early postnatal protein-calorie malnutrition and cognition: a review of human and animal studies. Int J Environ Res Public Health 8, 590–612.
31. Lukoyanov, N.V. & Andrade, J.P. (2000) Behavioral effects of protein deprivation and rehabilitation in adult rats: relevance to morphological alterations in the hippocampal formation. Behav Brain Res 112, 85–97.
32. Lupien, S.J., McEwen, B.S., Gunnar, M.R. & Heim, C. (2009) Effects of stress throughout the lifespan on the brain, behaviour and cognition. Nat Rev Neurosci 10, 434–445.
33. MacQueen, G.M., Campbell, S., McEwen, B.S., Macdonald, K., Amano, S., Joffe, R.T., Nahmias, C. & Young, L.T. (2003) Course of illness, hippocampal function, and hippocampal volume in major depression. Proc Natl Acad Sci U S A 100, 1387–1392.
34. Mansuy, I.M. (2003) Calcineurin in memory and bidirectional plasticity. Biochem Biophys Res Commun 311, 1195–1208.
35. Maria Moreira Camargo, L. & de Sousa Almeida, S. (2005) Early postnatal protein malnutrition changes the development of social play in rats. Physiol Behav 85, 246–251.
36. Matos, R.J.B., Orozco-Solís, R., Lopes de Souza, S., Manhães-de-Castro, R. & Bolaños-Jiménez, F. (2011) 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 196, 16–24.
37. McCrory, E., De Brito, S.A. & Viding, E. (2011) The impact of childhood maltreatment: a review of neurobiological and genetic factors. Front Psychiatry 2, 48.
38. McEwen, B.S., Bowles, N.P., Gray, J.D., Hill, M.N., Hunter, R.G., Karatsoreos, I.N. & Nasca, C. (2015) Review mechanisms of stress in the brain. Nat Neurosci 18, 1353–1363.
39. McGaughy, J.A., Amaral, A.C., Rushmore, R.J., Mokler, D.J., Morgane, P.J., Rosene, D.L. & Galler, J.R. (2014) Prenatal malnutrition leads to deficits in attentional set shifting and decreases metabolic activity in prefrontal subregions that control executive function. Dev Neurosci 36, 532–541.
40. Mifsud, K.R., Gutièrrez-Mecinas, M., Trollope, A.F., Collins, A., Saunderson, E.A. & Reul, J.M.H.M. (2011) Epigenetic mechanisms in stress and adaptation. Brain Behav Immun 25, 1305–1315.
41. Mineur, Y.S., Taylor, S.R. & Picciotto, M.R. (2014) Calcineurin downregulation in the amygdala is sufficient to induce anxiety-like and depression-like behaviors in C57BL/6J male mice. Biol Psychiatry 75, 991–998.
42. Miyakawa, T., Leiter, L.M., Gerber, D.J., Gainetdinov, R.R., Sotnikova, T.D., Zeng, H., Caron, M.G. & Tonegawa, S. (2003) Conditional calcineurin knockout mice exhibit multiple abnormal behaviors related to schizophrenia. Proc Natl Acad Sci U S A 100, 8987–8992.
43. Morgane, P.J., Mokler, D.J. & Galler, J.R. (2002) Effects of prenatal protein malnutrition on the hippocampal formation. Neurosci Biobehav Rev 26, 471–483.
44. Ogara, M.F., Belluscio, L.M., de la Fuente, V., Berardino, B.G., Sonzogni, S.V., Byk, L., Marazita, M. & Cánepa, E.T. (2014) CDK5-mediated phosphorylation of p19INK4d avoids DNA damage-induced neurodegeneration in mouse hippocampus and prevents loss of cognitive functions. Biochim Biophys Acta 1843, 1309–1324.
45. Papaioannou, A., Gerozissis, K., Prokopiou, A., Bolaris, S. & Stylianopoulou, F. (2002) Sex differences in the effects of neonatal handling on the animal's response to stress and the vulnerability for depressive behaviour. Behav Brain Res 129, 131–139.
46. Power, K.L. & Moore, C.L. (1986) Prenatal stress eliminates differential maternal attention to male offspring in Norway rats. Physiol Behav 38, 667–671.
47. Ranade, S.C., Rose, A., Rao, M., Gallego, J., Gressens, P. & Mani, S. (2008) Different types of nutritional deficiencies affect different domains of spatial memory function checked in a radial arm maze. Neuroscience 152, 859–866.
48. Reeves, P.G., Nielsen, F.H. & Fahey, G.C. (1993) 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 123, 1939–1951.
49. Reul, J.M.H.M. (2014) Making memories of stressful events: a journey along epigenetic, gene transcription, and signaling pathways. Front Psychiatry 5, 1–11.
50. Reyes-Castro, L.A., Rodriguez, J.S., Charco, R., Bautista, C.J., Larrea, F., Nathanielsz, P.W. & Zambrano, E. (2012) Maternal protein restriction in the rat during pregnancy and/or lactation alters cognitive and anxiety behaviors of female offspring. Int J Dev Neurosci 30, 39–45.
51. Rotta, L.N., Leszczinski, D.N., Brusque, A.M., Pereira, P., Brum, L.F.S., Nogueira, C.W., Frizzo, M.E.S., Perry, M.L.S. & Souza, D.O. (2008) Effects of undernutrition on glutamatergic parameters in the cerebral cortex of young rats. Physiol Behav 94, 580–585.
52. Ruijter, J.M., Ramakers, C., Hoogaars, W.M.H., Karlen, Y., Bakker, O., Van Den Hoff, M.J.B. & Moorman, A.F.M. (2009) Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res 37, e45.
53. Ruocco, A.C., Amirthavasagam, S. & Zakzanis, K.K. (2012) Amygdala and hippocampal volume reductions as candidate endophenotypes for borderline personality disorder: a meta-analysis of magnetic resonance imaging studies. Psychiatry Res 201, 245–252.
54. Sahay, A. & Hen, R. (2007) Adult hippocampal neurogenesis in depression. Nat Neurosci 10, 1110–1115.
55. Scott, K.M. (2011) Sex differences in the disability associated with mental disorders. Curr Opin Psychiatry 24, 331–335.
56. Takase, K., Yamamoto, Y. & Yagami, T. (2012) Maternal deprivation in the middle of a stress hyporesponsive period decreases hippocampal calcineurin expression and causes abnormal social and cognitive behaviours in adult male Wistar rats: relevance to negative symptoms of schizophrenia. Behav Brain Res 232, 306–315.
57. Veyrac, A., Besnard, A., Caboche, J., Davis, S. & Laroche, S. (2014) The transcription factor Zif268/Egr1, brain plasticity, and memory. In Zafar, U.K. & Muly, E.C. (eds), Progress in Molecular Biology and Translational Science. Academic Press, London, pp. 89–129.
58. Waber, D.P., Eaglesfield, D., Fitzmaurice, G.M., Bryce, C., Harrison, R.H. & Galler, J.R. (2011) Cognitive impairment as a mediator in the developmental pathway from infant malnutrition to adolescent depressive symptoms in Barbadian youth. J Dev Behav Pediatr 32, 225–232.
59. World Health Organization. (2012) Global burden of disease. URL http://www.who.int/healthinfo/global_burden_disease/gbd/en/ (Date of last access 2 January 2016).
60. Xia, Z. & Storm, D.R. (2005) The role of calmodulin as a signal integrator for synaptic plasticity. Nat Rev Neurosci 6, 267–276.
61. Zhu, W.L., Shi, H.S., Wang, S.J., Wu, P., Ding, Z.B. & Lu, L. (2011) Hippocampal CA3 calcineurin activity participates in depressive-like behavior in rats. J Neurochem 117, 1075–1086.