Interactions between early life stress and metabolic stress in programming of mental and metabolic health

Current Opinion in Behavioral Sciences

Volumn 14, Issue , 2017, Pages 65-71

  Cirulli, Francesca ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; GLUCOCORTICOID;

BEHAVIOR; COGNITION; COGNITIVE DEFECT; EARLY LIFE STRESS; EPIGENETICS; GENETIC SUSCEPTIBILITY; HUMAN; IMMUNE SYSTEM; LIPID DIET; MATERNAL OBESITY; MENTAL DISEASE; MENTAL HEALTH; METABOLIC REGULATION; METABOLIC STRESS; NERVE CELL PLASTICITY; NONHUMAN; PERSONAL EXPERIENCE; PRIORITY JOURNAL; REVIEW;

EID: 85008957769     PISSN: None     EISSN: 23521546     Source Type: Journal    
DOI: 10.1016/j.cobeha.2016.12.009     Document Type: Review

References (57)

1. 1 McLaughlin, K.A., Sheridan, M.A., Tibu, F., Fox, N.A., Zeanah, C.H., Nelson, C.A. 3rd, Causal effects of the early caregiving environment on development of stress response systems in children. Proc Natl Acad Sci U S A 112 (2015), 5637–5642.
2. 2 McEwen, B.S., Gray, J.D., Nasca, C., 60 years of neuroendocrinology: redefining neuroendocrinology: stress, sex and cognitive and emotional regulation. J Endocrinol 226 (2015), T67–T83.
3. 3 Entringer, S., Buss, C., Wadhwa, P.D., Prenatal stress, development, health and disease risk: a psychobiological perspective-2015 Curt Richter Award Paper. Psychoneuroendocrinology 62 (2015), 366–375.
4. 4 Sherwin, E., Rea, K., Dinan, T.G., Cryan, J.F., A gut (microbiome) feeling about the brain. Curr Opin Gastroenterol 32 (2016), 96–102.
5. 5 Berry, A., Cirulli, F., Toward a diathesis-stress model of schizophrenia in a neurodevelopmental perspective. Pletnikov, M., Waddington, J., (eds.) Modeling the Psychopathological Dimensions of Schizophrenia. From Molecules to Behavior, 2016, Academic Press, 209–224 Huston JP (Series Editor): Handbook of Behavioral Neuroscience.
6. 6 Bock, J., Rether, K., Groger, N., Xie, L., Braun, K., Perinatal programming of emotional brain circuits: an integrative view from systems to molecules. Front Neurosci, 8, 2014, 11.
7. 7• Boersma, G.J., Bale, T.L., Casanello, P., Lara, H.E., Lucion, A.B., Suchecki, D., Tamashiro, K.L., Long-term impact of early life events on physiology and behaviour. J Neuroendocrinol 26 (2014), 587–602 This review discusses the effects of stress and nutrition throughout development and summarises studies investigating how exposure to stress or alterations in nutrition during the pre-conception, prenatal and early postnatal periods can affect the long-term health of an individual depending on the type and the timing of exposure.
8. 8 Daskalakis, N.P., Bagot, R.C., Parker, K.J., Vinkers, C.H., de Kloet, E.R., The three-hit concept of vulnerability and resilience: toward understanding adaptation to early-life adversity outcome. Psychoneuroendocrinology 38 (2013), 1858–1873.
9. 9 Ehlert, U., Enduring psychobiological effects of childhood adversity. Psychoneuroendocrinology 38 (2013), 1850–1857.
10. 10 Provencal, N., Binder, E.B., The effects of early life stress on the epigenome: from the womb to adulthood and even before. Exp Neurol 268 (2015), 10–20.
11. 11 Gavrieli, A., Farr, O.M., Davis, C.R., Crowell, J.A., Mantzoros, C.S., Early life adversity and/or posttraumatic stress disorder severity are associated with poor diet quality, including consumption of trans fatty acids, and fewer hours of resting or sleeping in a US middle-aged population: a cross-sectional and prospective study. Metabolism 64 (2015), 1597–1610.
12. 12 Mansur, R.B., Brietzke, E., McIntyre, R.S., Is there a “metabolic-mood syndrome”? A review of the relationship between obesity and mood disorders. Neurosci Biobehav Rev 52 (2015), 89–104.
13. 13 Mansur, R.B., Cunha, G.R., Asevedo, E., Zugman, A., Zeni-Graiff, M., Rios, A.C., Sethi, S., Maurya, P.K., Levandowski, M.L., Gadelha, A., et al. Socioeconomic disadvantage moderates the association between peripheral biomarkers and childhood psychopathology. PLoS One, 11, 2016, e0160455.
14. 14 Lee, C., Tsenkova, V., Carr, D., Childhood trauma and metabolic syndrome in men and women. Soc Sci Med 105 (2014), 122–130.
15. 15 Rivera, H.M., Christiansen, K.J., Sullivan, E.L., The role of maternal obesity in the risk of neuropsychiatric disorders. Front Neurosci, 9, 2015, 194.
16. 16 Tamashiro, K.L., Moran, T.H., Perinatal environment and its influences on metabolic programming of offspring. Physiol Behav 100 (2010), 560–566.
17. 17• Braithwaite, E.C., Kundakovic, M., Ramchandani, P.G., Murphy, S.E., Champagne, F.A., Maternal prenatal depressive symptoms predict infant NR3C1 1F and BDNF IV DNA methylation. Epigenetics 10 (2015), 408–417 Findings from this study highlight the susceptibility of male offspring to changes in NR3C1 DNA methylation and present novel evidence for altered BDNF exon IV DNA methylation in response to maternal depression during pregnancy.
18. 18 Dinan, T.G., Cryan, J.F., Microbes, immunity, and behavior: psychoneuroimmunology meets the microbiome. Neuropsychopharmacology 42:1 (2017), 178–192, 10.1038/npp.2016.103.
19. 19 Turecki, G., Ota, V.K., Belangero, S.I., Jackowski, A., Kaufman, J., Early life adversity, genomic plasticity, and psychopathology. Lancet Psychiatry 1 (2014), 461–466.
20. 20 Morris, M.J., Beilharz, J.E., Maniam, J., Reichelt, A.C., Westbrook, R.F., Why is obesity such a problem in the 21st century? The intersection of palatable food, cues and reward pathways, stress, and cognition. Neurosci Biobehav Rev 58 (2015), 36–45.
21. 21 Noble, E.E., Kanoski, S.E., Early life exposure to obesogenic diets and learning and memory dysfunction. Curr Opin Behav Sci 9 (2016), 7–14.
22. 22 Stout, S.A., Espel, E.V., Sandman, C.A., Glynn, L.M., Davis, E.P., Fetal programming of children's obesity risk. Psychoneuroendocrinology 53 (2015), 29–39.
23. 23 Yam, K.Y., Naninck, E.F., Schmidt, M.V., Lucassen, P.J., Korosi, A., Early-life adversity programs emotional functions and the neuroendocrine stress system: the contribution of nutrition, metabolic hormones and epigenetic mechanisms. Stress 18 (2015), 328–342.
24. 24 Mina, T.H., Raikkonen, K., Riley, S.C., Norman, J.E., Reynolds, R.M., Maternal distress associates with placental genes regulating fetal glucocorticoid exposure and IGF2: role of obesity and sex. Psychoneuroendocrinology 59 (2015), 112–122.
25. 25 Eriksson, J.G., Sandboge, S., Salonen, M.K., Kajantie, E., Osmond, C., Long-term consequences of maternal overweight in pregnancy on offspring later health: findings from the Helsinki Birth Cohort Study. Ann Med 46 (2014), 434–438.
26. 26 Cirulli, F., Berry, A., Alleva, E., Early disruption of the mother-infant relationship: effects on brain plasticity and implications for psychopathology. Neurosci Biobehav Rev 27 (2003), 73–82.
27. 27 Bellisario, V., Berry, A., Capoccia, S., Raggi, C., Panetta, P., Branchi, I., Piccaro, G., Giorgio, M., Pelicci, P.G., Cirulli, F., Gender-dependent resiliency to stressful and metabolic challenges following prenatal exposure to high-fat diet in the p66(Shc-/-) mouse. Front Behav Neurosci, 8, 2014, 285.
28. 28• Bellisario, V., Panetta, P., Balsevich, G., Baumann, V., Noble, J., Raggi, C., Nathan, O., Berry, A., Seckl, J., Schmidt, M., et al. Maternal high-fat diet acts as a stressor increasing maternal glucocorticoids’ signaling to the fetus and disrupting maternal behavior and brain activation in C57BL/6J mice. Psychoneuroendocrinology 60 (2015), 138–150 The present study provides, in a mouse model, a thorough investigation of the mechanisms underlying detrimental effects of high fat diet in pregnant females which is here shown to act as a stressful, metabolic stimulus, reinforcing neuroendocrine activation linked to parturition and delivery.
29. 29 Johnson, S.A., Javurek, A.B., Painter, M.S., Murphy, C.R., Conard, C.M., Gant, K.L., Howald, E.C., Ellersieck, M.R., Wiedmeyer, C.E., Vieira-Potter, V.J., et al. Effects of a maternal high-fat diet on offspring behavioral and metabolic parameters in a rodent model. J Dev Orig Health Dis, 2016, 1–14.
30. 30 Carlin, J., George, R., Reyes, T.M., Methyl donor supplementation blocks the adverse effects of maternal high fat diet on offspring physiology. PLoS One, 8, 2013, e63549.
31. 31 Maniam, J., Antoniadis, C.P., Morris, M.J., The effect of early-life stress and chronic high-sucrose diet on metabolic outcomes in female rats. Stress 18 (2015), 524–537.
32. 32 Lin, C., Shao, B., Huang, H., Zhou, Y., Lin, Y., Maternal high fat diet programs stress-induced behavioral disorder in adult offspring. Physiol Behav 152 (2015), 119–127.
33. 33 Boersma, G.J., Moghadam, A.A., Cordner, Z.A., Tamashiro, K.L., Prenatal stress and stress coping style interact to predict metabolic risk in male rats. Endocrinology 155 (2014), 1302–1312.
34. 34 Maniam, J., Antoniadis, C.P., Le, V., Morris, M.J., A diet high in fat and sugar reverses anxiety-like behaviour induced by limited nesting in male rats: impacts on hippocampal markers. Psychoneuroendocrinology 68 (2016), 202–209.
35. 35 Maniam, J., Antoniadis, C.P., Wang, K.W., Morris, M.J., Early life stress induced by limited nesting material produces metabolic resilience in response to a high-fat and high-sugar diet in male rats. Front Endocrinol (Lausanne), 6, 2015, 138.
36. 36 Paternain, L., de la Garza, A.L., Batlle, M.A., Milagro, F.I., Martinez, J.A., Campion, J., Prenatal stress increases the obesogenic effects of a high-fat-sucrose diet in adult rats in a sex-specific manner. Stress 16 (2013), 220–232.
37. 37 Cao-Lei, L., Dancause, K.N., Elgbeili, G., Massart, R., Szyf, M., Liu, A., Laplante, D.P., King, S., DNA methylation mediates the impact of exposure to prenatal maternal stress on BMI and central adiposity in children at age 13(1/2) years: Project Ice Storm. Epigenetics 10 (2015), 749–761.
38. 38•• Doherty, T.S., Forster, A., Roth, T.L., Global and gene-specific DNA methylation alterations in the adolescent amygdala and hippocampus in an animal model of caregiver maltreatment. Behav Brain Res 298 (2016), 55–61 Findings from this study demonstrate that the effects of the early caregiving environment are detectable in the adolescent brain at the level of the epigenome, with brain-region specific and sexually-dimorphic epigenetic consequences that could have relevance to adolescent mental health and behavior.
39. 39 Marosi, K., Mattson, M.P., BDNF mediates adaptive brain and body responses to energetic challenges. Trends Endocrinol Metab 25 (2014), 89–98.
40. 40 Mou, Z., Hyde, T.M., Lipska, B.K., Martinowich, K., Wei, P., Ong, C.J., Hunter, L.A., Palaguachi, G.I., Morgun, E., Teng, R., et al. Human obesity associated with an intronic snp in the brain-derived neurotrophic factor locus. Cell Rep 13 (2015), 1073–1080.
41. 41 van der Knaap, L.J., Oldehinkel, A.J., Verhulst, F.C., van Oort, F.V., Riese, H., Glucocorticoid receptor gene methylation and HPA-axis regulation in adolescents. The TRAILS study. Psychoneuroendocrinology 58 (2015), 46–50.
42. 42•• Turecki, G., Meaney, M.J., Effects of the social environment and stress on glucocorticoid receptor gene methylation: a systematic review. Biol Psychiatry 79 (2016), 87–96 A recent systematic review of the growing literature investigating the relationship between environmental experience, stress, and GR (NR3C1) gene methylation in relation to various psychological stressors, including parental stress. Results indicate great consistency among studies investigating early-life adversity and the effect of parental stress. Cross-species and cross-tissue comparisons are described.
43. 43 Bockmuhl, Y., Patchev, A.V., Madejska, A., Hoffmann, A., Sousa, J.C., Sousa, N., Holsboer, F., Almeida, O.F., Spengler, D., Methylation at the CpG island shore region upregulates Nr3c1 promoter activity after early-life stress. Epigenetics 10 (2015), 247–257.
44. 44• Boersma, G.J., Lee, R.S., Cordner, Z.A., Ewald, E.R., Purcell, R.H., Moghadam, A.A., Tamashiro, K.L., Prenatal stress decreases Bdnf expression and increases methylation of Bdnf exon IV in rats. Epigenetics 9 (2014), 437–447 This study investigated alterations inBDNF expression in prenatally stressed rat offspring. Data indicate that prenatal stress induces decreases in BDNF expression that may at least in part be mediated by increased DNA methylation of BDNF exon IV.
45. 45 Tyagi, E., Zhuang, Y., Agrawal, R., Ying, Z., Gomez-Pinilla, F., Interactive actions of Bdnf methylation and cell metabolism for building neural resilience under the influence of diet. Neurobiol Dis 73 (2015), 307–318.
46. 46 Jensen Pena, C., Monk, C., Champagne, F.A., Epigenetic effects of prenatal stress on 11beta-hydroxysteroid dehydrogenase-2 in the placenta and fetal brain. PLoS One, 7, 2012, e39791.
47. 47 Mattson, M.P., Lifelong brain health is a lifelong challenge: from evolutionary principles to empirical evidence. Ageing Res Rev 20 (2015), 37–45.
48. 48 Luoni, A., Berry, A., Calabrese, F., Capoccia, S., Bellisario, V., Gass, P., Cirulli, F., Riva, M.A., Delayed BDNF alterations in the prefrontal cortex of rats exposed to prenatal stress: preventive effect of lurasidone treatment during adolescence. Eur Neuropsychopharmacol 24 (2014), 986–995.
49. 49 van der Kooij, M.A., Grosse, J., Zanoletti, O., Papilloud, A., Sandi, C., The effects of stress during early postnatal periods on behavior and hippocampal neuroplasticity markers in adult male mice. Neuroscience 311 (2015), 508–518.
50. 50 Tzanoulinou, S., Sandi, C., The programming of the social brain by stress during childhood and adolescence: from rodents to humans. Curr Top Behav Neurosci, 2016, 10.1007/7854_2015_430.
51. 51 Berry, A., Panetta, P., Luoni, A., Bellisario, V., Capoccia, S., Riva, M.A., Cirulli, F., Decreased Bdnf expression and reduced social behavior in periadolescent rats following prenatal stress. Dev Psychobiol 57 (2015), 365–373.
52. 52 Dinan, T.G., Cryan, J.F., Mood by microbe: towards clinical translation. Genome Med, 8, 2016, 36.
53. 53 El Aidy, S., Stilling, R., Dinan, T.G., Cryan, J.F., Microbiome to brain: unravelling the multidirectional axes of communication. Adv Exp Med Biol 874 (2016), 301–336.
54. 54 Foster, J.A., Lyte, M., Meyer, E., Cryan, J.F., Gut microbiota and brain function: an evolving field in neuroscience. Int J Neuropsychopharmacol, 19, 2016.
55. 55 De Palma, G., Blennerhassett, P., Lu, J., Deng, Y., Park, A.J., Green, W., Denou, E., Silva, M.A., Santacruz, A., Sanz, Y., et al. Microbiota and host determinants of behavioural phenotype in maternally separated mice. Nat Commun, 6, 2015, 7735.
56. 56 Kelly, J.R., Clarke, G., Cryan, J.F., Dinan, T.G., Brain-gut-microbiota axis: challenges for translation in psychiatry. Ann Epidemiol 26 (2016), 366–372.
57. 57 Luczynski, P., Whelan, S.O., O'Sullivan, C., Clarke, G., Shanahan, F., Dinan, T.G., et al. Adult microbiota-deficient mice have distinct dendritic morphological changes: differential effects in the amygdala and hippocampus. Eur J Neurosci 44:9 (2016), 2654–2666, 10.1111/ejn.13291.