Evaluating the interaction between early postnatal inflammation and maternal care in the programming of adult anxiety and depression-related behaviors
The perinatal development of the nervous system is influenced by different external and internal stimuli. Previous data show that maternal care and perinatal inflammation can induce long-term changes in anxiety- and depression-related behavior. Our hypothesis is that both maternal care and perinatal...
Guardado en:
| Autor principal: | |
|---|---|
| Otros Autores: | , , |
| Formato: | Capítulo de libro |
| Lenguaje: | Inglés |
| Publicado: |
2010
|
| Acceso en línea: | Registro en Scopus DOI Handle Registro en la Biblioteca Digital |
| Aporte de: | Registro referencial: Solicitar el recurso aquí |
| Sumario: | The perinatal development of the nervous system is influenced by different external and internal stimuli. Previous data show that maternal care and perinatal inflammation can induce long-term changes in anxiety- and depression-related behavior. Our hypothesis is that both maternal care and perinatal inflammation act through interacting biological pathways to program adult behavior. To evaluate this interaction, we combined a protocol of maternal care variation in mice (C57BL/6J × BALB/c reciprocal F1 offspring) with the administration of bacterial wall lipopolysaccharide (LPS) at a previously reported sensitive development age (postnatal day 3, P3). The analysis of maternal behavior revealed that pups from C57BL/6J dams received more maternal attention than those taken care by BALB/c dams. Pups receiving LPS at P3 showed an acute corticosterone response, and a dose-dependent desensitization of this hormonal response when challenged with LPS at adulthood. We analyzed adult behavior on 6 highly validated tests and found an interaction between maternal care and early postnatal LPS on 7 anxiety-related behaviors in 4 different tests. In particular, early postnatal LPS treatment resulted in higher anxiety-related behavior when administered to females receiving more maternal care (C57 pedigree), but reduced depression-related behavior in males of the same pedigree. These results suggest that specific coping strategies are sensitive to maternal care and/or postnatal inflammation programming of adult anxiety- and depression-related behaviors, suggesting that both divergent and convergent mechanisms participate in this programming. © 2010 Elsevier B.V. |
|---|---|
| Bibliografía: | Karrow, N.A., Activation of the hypothalamic-pituitary-adrenal axis and autonomic nervous system during inflammation and altered programming of the neuroendocrine-immune axis during fetal and neonatal development: lessons learned from the model inflammagen, lipopolysaccharide (2006) Brain Behav Immun, 20, pp. 144-158 Heim, C., Nemeroff, C.B., The role of childhood trauma in the neurobiology of mood and anxiety disorders: preclinical and clinical studies (2001) Biol Psychiatry, 49, pp. 1023-1039 Agid, O., Shapira, B., Zislin, J., Ritsner, M., Hanin, B., Murad, H., Environment and vulnerability to major psychiatric illness: a case control study of early parental loss in major depression, bipolar disorder and schizophrenia (1999) Mol Psychiatry, 4, pp. 163-172 Chapman, D.P., Whitfield, C.L., Felitti, V.J., Dube, S.R., Edwards, V.J., Anda, R.F., Adverse childhood experiences and the risk of depressive disorders in adulthood (2004) J Affect Disord, 82, pp. 217-225 Kendler, K.S., Prescott, C.A., Myers, J., Neale, M.C., The structure of genetic and environmental risk factors for common psychiatric and substance use disorders in men and women (2003) Arch Gen Psychiatry, 60, pp. 929-937 Weaver, I.C., Meaney, M.J., Szyf, M., Maternal care effects on the hippocampal transcriptome and anxiety-mediated behaviors in the offspring that are reversible in adulthood (2006) Proc Natl Acad Sci USA, 103, pp. 3480-3485 Romeo, R.D., Fossella, J.A., Bateup, H.S., Sisti, H.M., Brake, W.G., McEwen, B.S., Maternal separation suppresses TGF alpha mRNA expression in the prefrontal cortex of male and female neonatal C57BL/6 mice (2004) Brain Res Dev Brain Res, 152, pp. 73-77 Caldji, C., Diorio, J., Anisman, H., Meaney, M.J., Maternal behavior regulates benzodiazepine/GABAA receptor subunit expression in brain regions associated with fear in BALB/c and C57BL/6 mice (2004) Neuropsychopharmacology, 29, pp. 1344-1352 Caldji, C., Tannenbaum, B., Sharma, S., Francis, D., Plotsky, P.M., Meaney, M.J., Maternal care during infancy regulates the development of neural systems mediating the expression of fearfulness in the rat (1998) Proc Natl Acad Sci USA, 95, pp. 5335-5340 Hava, G., Vered, L., Yael, M., Mordechai, H., Mahoud, H., Alterations in behavior in adult offspring mice following maternal inflammation during pregnancy (2006) Dev Psychobiol, 48, pp. 162-168 Shi, L., Fatemi, S.H., Sidwell, R.W., Patterson, P.H., Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring (2003) J Neurosci, 23, pp. 297-302 Meyer, U., Yee, B.K., Feldon, J., The neurodevelopmental impact of prenatal infections at different times of pregnancy: the earlier the worse? (2007) Neuroscientist, 13, pp. 241-256 Meyer, U., Nyffeler, M., Engler, A., Urwyler, A., Schedlowski, M., Knuesel, I., The time of prenatal immune challenge determines the specificity of inflammation-mediated brain and behavioral pathology (2006) J Neurosci, 26, pp. 4752-4762 Bilbo, S.D., Newsum, N.J., Sprunger, D.B., Watkins, L.R., Rudy, J.W., Maier, S.F., Differential effects of neonatal handling on early life infection-induced alterations in cognition in adulthood (2007) Brain Behav Immun, 21, pp. 332-342 Walker, F.R., March, J., Hodgson, D.M., Endotoxin exposure in early life alters the development of anxiety-like behaviour in the Fischer 344 rat (2004) Behav Brain Res, 154, pp. 63-69 Liu, D., Diorio, J., Tannenbaum, B., Caldji, C., Francis, D., Freedman, A., Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress (1997) Science, 277, pp. 1659-1662 del Rey, A., Furukawa, H., Monge-Arditi, G., Kabiersch, A., Voigt, K.H., Besedovsky, H.O., Alterations in the pituitary-adrenal axis of adult mice following neonatal exposure to interleukin-1 (1996) Brain Behav Immun, 10, pp. 235-248 Anisman, H., Zaharia, M.D., Meaney, M.J., Merali, Z., Do early-life events permanently alter behavioral and hormonal responses to stressors? (1998) Int J Dev Neurosci, 16, pp. 149-164 Barbazanges, A., Vallee, M., Mayo, W., Day, J., Simon, H., Le Moal, M., Early and later adoptions have different long-term effects on male rat offspring (1996) J Neurosci, 16, pp. 7783-7790 Calatayud, F., Belzung, C., Emotional reactivity in mice, a case of nongenetic heredity? (2001) Physiol Behav, 74, pp. 355-362 Lehmann, J., Feldon, J., Long-term biobehavioral effects of maternal separation in the rat: consistent or confusing? (2000) Rev Neurosci, 11, pp. 383-408 Granger, D.A., Hood, K.E., Ikeda, S.C., Reed, C.L., Block, M.L., Neonatal endotoxin exposure alters the development of social behavior and the hypothalamic-pituitary-adrenal axis in selectively bred mice (1996) Brain Behav Immun, 10, pp. 249-259 Hood, K.E., Dreschel, N.A., Granger, D.A., Maternal behavior changes after immune challenge of neonates with developmental effects on adult social behavior (2003) Dev Psychobiol, 42, pp. 17-34 Shanks, N., Larocque, S., Meaney, M.J., Neonatal endotoxin exposure alters the development of the hypothalamic-pituitary-adrenal axis: early illness and later responsivity to stress (1995) J Neurosci, 15, pp. 376-384 Shanks, N., Windle, R.J., Perks, P.A., Harbuz, M.S., Jessop, D.S., Ingram, C.D., Early-life exposure to endotoxin alters hypothalamic-pituitary-adrenal function and predisposition to inflammation (2000) Proc Natl Acad Sci USA, 97, pp. 5645-5650 Bumiller, A., Gotz, F., Rohde, W., Dorner, G., Effects of repeated injections of interleukin 1beta or lipopolysaccharide on the HPA axis in the newborn rat (1999) Cytokine, 11, pp. 225-230 Witek-Janusek, L., Pituitary-adrenal response to bacterial endotoxin in developing rats (1988) Am J Physiol, 255, pp. E525-E530 Greenberg, P.E., Sisitsky, T., Kessler, R.C., Finkelstein, S.N., Berndt, E.R., Davidson, J.R., The economic burden of anxiety disorders in the 1990s (1999) J Clin Psychiatry, 60, pp. 427-435 Scott, J., Dickey, B., Global burden of depression: the intersection of culture and medicine (2003) Br J Psychiatry, 183, pp. 92-94 Kajantie, E., Fetal origins of stress-related adult disease (2006) Ann N Y Acad Sci, 1083, pp. 11-27 Depino, A.M., Tsetsenis, T., Gross, C., GABA homeostasis contributes to the developmental programming of anxiety-related behavior (2008) Brain Res, 1210, pp. 189-199 Carola, V., Gross, C., BDNF moderates early environmental risk factors for anxiety in mouse (2010) Genes Brain Behav Calatayud, F., Coubard, S., Belzung, C., Emotional reactivity in mice may not be inherited but influenced by parents (2004) Physiol Behav, 80, pp. 465-474 Barr, C.S., Newman, T.K., Schwandt, M., Shannon, C., Dvoskin, R.L., Lindell, S.G., Sexual dichotomy of an interaction between early adversity and the serotonin transporter gene promoter variant in rhesus macaques (2004) Proc Natl Acad Sci USA, 101, pp. 12358-12363 McCormick, C.M., Smythe, J.W., Sharma, S., Meaney, M.J., Sex-specific effects of prenatal stress on hypothalamic-pituitary-adrenal responses to stress and brain glucocorticoid receptor density in adult rats (1995) Brain Res Dev Brain Res, 84, pp. 55-61 Papaioannou, A., Gerozissis, K., Prokopiou, A., Bolaris, S., Stylianopoulou, F., Sex differences in the effects of neonatal handling on the animal's response to stress and the vulnerability for depressive behaviour (2002) Behav Brain Res, 129, pp. 131-139 Park, M.K., Hoang, T.A., Belluzzi, J.D., Leslie, F.M., Gender specific effect of neonatal handling on stress reactivity of adolescent rats (2003) J Neuroendocrinol, 15, pp. 289-295 Smythe, J.W., McCormick, C.M., Rochford, J., Meaney, M.J., The interaction between prenatal stress and neonatal handling on nociceptive response latencies in male and female rats (1994) Physiol Behav, 55, pp. 971-974 Spencer, S.J., Boisse, L., Mouihate, A., Pittman, Q.J., Long term alterations in neuroimmune responses of female rats after neonatal exposure to lipopolysaccharide (2005) Brain Behav Immun Weinberg, J., Krahn, E.A., Levine, S., Differential effects of handling on exploration in male and female rats (1978) Dev Psychobiol, 11, pp. 251-259 Cameron, O.G., Hill, E.M., Women and anxiety (1989) Psychiatr Clin North Am, 12, pp. 175-186 Maier, W., Gansicke, M., Gater, R., Rezaki, M., Tiemens, B., Urzua, R.F., Gender differences in the prevalence of depression: a survey in primary care (1999) J Affect Disord, 53, pp. 241-252 Ragueneau, S., Early development in mice. IV: Quantity and gross composition of milk in five inbred strains (1987) Physiol Behav, 40, pp. 431-435 Levine, S., The ontogeny of the hypothalamic-pituitary-adrenal axis. The influence of maternal factors (1994) Ann NY Acad Sci, 746, pp. 275-288. , [discussion 89-93] Macri, S., Mason, G.J., Wurbel, H., Dissociation in the effects of neonatal maternal separations on maternal care and the offspring's HPA and fear responses in rats (2004) Eur J Neurosci, 20, pp. 1017-1024 Zaharia, M.D., Kulczycki, J., Shanks, N., Meaney, M.J., Anisman, H., The effects of early postnatal stimulation on Morris water-maze acquisition in adult mice: genetic and maternal factors (1996) Psychopharmacology (Berl), 128, pp. 227-239 Ladd, C.O., Thrivikraman, K.V., Huot, R.L., Plotsky, P.M., Differential neuroendocrine responses to chronic variable stress in adult Long Evans rats exposed to handling-maternal separation as neonates (2005) PNEC, 30, pp. 520-533 Priebe, K., Romeo, R.D., Francis, D.D., Sisti, H.M., Mueller, A., McEwen, B.S., Maternal influences on adult stress and anxiety-like behavior in C57BL/6J and BALB/cJ mice: a cross-fostering study (2005) Dev Psychobiol, 47, pp. 398-407 Vallee, M., Mayo, W., Dellu, F., Le Moal, M., Simon, H., Maccari, S., Prenatal stress induces high anxiety and postnatal handling induces low anxiety in adult offspring: correlation with stress-induced corticosterone secretion (1997) J Neurosci, 17, pp. 2626-2636 Roy, V., Merali, Z., Poulter, M.O., Anisman, H., Anxiety responses, plasma corticosterone and central monoamine variations elicited by stressors in reactive and nonreactive mice and their reciprocal F1 hybrids (2007) Behav Brain Res, 185, pp. 49-58 Griebel, G., Belzung, C., Perrault, G., Sanger, D.J., Differences in anxiety-related behaviours and in sensitivity to diazepam in inbred and outbred strains of mice (2000) Psychopharmacology (Berl), 148, pp. 164-170 Crawley, J.N., Belknap, J.K., Collins, A., Crabbe, J.C., Frankel, W., Henderson, N., Behavioral phenotypes of inbred mouse strains: implications and recommendations for molecular studies (1997) Psychopharmacology (Berl), 132, pp. 107-124 Rogers, D.C., Jones, D.N., Nelson, P.R., Jones, C.M., Quilter, C.A., Robinson, T.L., Use of SHIRPA and discriminant analysis to characterise marked differences in the behavioural phenotype of six inbred mouse strains (1999) Behav Brain Res, 105, pp. 207-217 Trullas, R., Skolnick, P., Differences in fear motivated behaviors among inbred mouse strains (1993) Psychopharmacology (Berl), 111, pp. 323-331 Espejo, E.F., Effects of weekly or daily exposure to the elevated plus-maze in male mice (1997) Behav Brain Res, 87, pp. 233-238 Carola, V., D'Olimpio, F., Brunamonti, E., Mangia, F., Renzi, P., Evaluation of the elevated plus-maze and open-field tests for the assessment of anxiety-related behaviour in inbred mice (2002) Behav Brain Res, 134, pp. 49-57 Sapolsky, R.M., Meaney, M.J., Maturation of the adrenocortical stress response: neuroendocrine control mechanisms and the stress hyporesponsive period (1986) Brain Res, 396, pp. 64-76 Walker, C.D., Perrin, M., Vale, W., Rivier, C., Ontogeny of the stress response in the rat: role of the pituitary and the hypothalamus (1986) Endocrinology, 118, pp. 1445-1451 Schmidt, M.V., Enthoven, L., van der Mark, M., Levine, S., de Kloet, E.R., Oitzl, M.S., The postnatal development of the hypothalamic-pituitary-adrenal axis in the mouse (2003) Int J Dev Neurosci, 21, pp. 125-132 Shanks, N., Meaney, M.J., Hypothalamic-pituitary-adrenal activation following endotoxin administration in the developing rat: a CRH-mediated effect (1994) J Neuroendocrinol, 6, pp. 375-383 Besedovsky, H.O., del Rey, A., Klusman, I., Furukawa, H., Monge Arditi, G., Kabiersch, A., Cytokines as modulators of the hypothalamus-pituitary-adrenal axis (1991) J Steroid Biochem Mol Biol, 40, pp. 613-618 Boisse, L., Mouihate, A., Ellis, S., Pittman, Q.J., Long-term alterations in neuroimmune responses after neonatal exposure to lipopolysaccharide (2004) J Neurosci, 24, pp. 4928-4934 Takemura, T., Makino, S., Takao, T., Asaba, K., Suemaru, S., Hashimoto, K., Hypothalamic-pituitary-adrenocortical responses to single vs. repeated endotoxin lipopolysaccharide administration in the rat (1997) Brain Res, 767, pp. 181-191 Spencer, S.J., Martin, S., Mouihate, A., Pittman, Q.J., Early-life immune challenge: defining a critical window for effects on adult responses to immune challenge (2006) Neuropsychopharmacology, 31, pp. 1910-1918 Spencer, S.J., Heida, J.G., Pittman, Q.J., Early life immune challenge-effects on behavioural indices of adult rat fear and anxiety (2005) Behav Brain Res, 164, pp. 231-238 Elin, R.J., Sandberg, A.L., Rosentreich, D.L., Comparison of the pyrogenicity, Limulus activity mitogenicity and complement reactivity of several bacterial endotoxins and related compounds (1976) J Immunol, 117, pp. 1238-1242 Meyer, U., Nyffeler, M., Yee, B.K., Knuesel, I., Feldon, J., Adult brain and behavioral pathological markers of prenatal immune challenge during early/middle and late fetal development in mice (2008) Brain Behav Immun, 22, pp. 469-486 Tilders, F.J., DeRijk, R.H., Van Dam, A.M., Vincent, V.A., Schotanus, K., Persoons, J.H., Activation of the hypothalamus-pituitary-adrenal axis by bacterial endotoxins: routes and intermediate signals (1994) PNEC, 19, pp. 209-232 Pitossi, F., del Rey, A., Kabiersch, A., Besedovsky, H., Induction of cytokine transcripts in the central nervous system and pituitary following peripheral administration of endotoxin to mice (1997) J Neurosci Res, 48, pp. 287-298 Cunningham, C., Campion, S., Teeling, J., Felton, L., Perry, V.H., The sickness behaviour and CNS inflammatory mediator profile induced by systemic challenge of mice with synthetic double-stranded RNA (poly I:C) (2007) Brain Behav Immun, 21, pp. 490-502 Depino, A.M., Alonso, M., Ferrari, C., del Rey, A., Anthony, D., Besedovsky, H., Learning modulation by endogenous hippocampal IL-1: blockade of endogenous IL-1 facilitates memory formation (2004) Hippocampus, 14, pp. 526-535 |
| ISSN: | 01664328 |
| DOI: | 10.1016/j.bbr.2010.04.032 |