Perinatal programming of depressive-like behavior by inflammation in adult offspring mice whose mothers were fed polluted eels: Gender selective effects
[en] Several lines of evidence indicate that early-life inflammation may predispose to mental illness, including depression, in later-life. We investigated the impact of perinatal exposure to polluted eels on
neonatal, postnatal, and adult brain inflammation, and on the resignation behavior of male and female
adult offspring mice. The effects of maternal standard diet (laboratory food) were compared to the
same diet enriched with low, intermediate, or highly polluted eels. Brain inflammatory markers including cytokines were assessed in offspring mice on the day of birth (i.e., on the postnatal day–PND 1), upon weaning (PND 21) and at adulthood (PND 100). Plasma myeloperoxidase and corticosterone levels were evaluated at PND 100. Immobility behavior of offspring was assessed in adulthood (i.e., at PNDs 95–100), using the tail suspension and forced swimming tests. Chronic brain inflammation was found in male and female offspring mice compared to controls, as assessed at PNDs 1, 21, and 100. The level of myeloperoxidase was found to be significantly higher in both adult males and females vs. control offspring. However, high corticosterone levels were only found in male offspring mice that were perinatally exposed to eels, suggesting a gender-selective dysregulation of the adult hypothalamicpituitaryadrenal (HPA) axis. Gender-specific differences were also detected in adulthood in regard to offspring resignation behavior. Thus, compared to controls, males, but not females, whose mothers were fed eels during pregnancy and lactation exhibited a depressive-like behavior in adult age in both behavioral models of depression. Depressive symptoms were more pronounced in male mice perinatally exposed to either intermediate or highly polluted eels than those exposed to only lowly polluted eels. Our results indicate that early-life inflammatory insult is a plausible causative factor that induce the depressive phenotype exhibited by male adult offspring mice, most likely through a gender-specific HPA axis enhanced activation.
Research center :
CART - Centre Interfacultaire d'Analyse des Résidus en Traces - ULiège
Disciplines :
Neurology
Author, co-author :
Soualed, Nidhal
Dridi, Imen
Eppe, Gauthier ; Université de Liège > Département de chimie (sciences) > Chimie analytique inorganique
Némos, Christophe
Soulimani, Rachid
Bouayed, Jaouad
Language :
English
Title :
Perinatal programming of depressive-like behavior by inflammation in adult offspring mice whose mothers were fed polluted eels: Gender selective effects
Andersen, S.L., Trajectories of brain development: point of vulnerability or window of opportunity? (2003) Neurosci. Biobehav. Rev., 27, pp. 3-18
Arain, M., Haque, M., Johal, L., Mathur, P., Nel, W., Rais, A., Sandhu, R., Sharma, S., Maturation of the adolescent brain (2013) Neuropsychiatr. Dis. Treat., 9, pp. 449-461
Belzung, C., Innovative drugs to treat depression: did animal models fail to be predictive or did clinical trials fail to detect effects? (2014) Neuropsychopharmacology, 39, pp. 1041-1051
Berger, D.F., Lombardo, J.P., Jeffers, P.M., Hunt, A.E., Bush, B., Casey, A., Quimby, F., Hyperactivity and impulsiveness in rats fed diets supplemented with either Aroclor 1248 or PCB-contaminated St. Lawrence river fish (2001) Behav. Brain Res., 126, pp. 1-11
Bilbo, S.D., Schwarz, J.M., Early-life programming of later-life brain and behavior: a critical role for the immune system (2009) Front. Behav. Neurosci., 3, p. 14
Bohn, T., Cocco, E., Gourdol, L., Guignard, C., Hoffmann, L., Determination of atrazine and degradation products in Luxembourgish drinking water: origin and fate of potential endocrine-disrupting pesticides (2011) Food Addit. Contam. Part A Chem. Anal. Control Expo Risk Assess, 28, pp. 1041-1054
Bolton, J.L., Bilbo, S.D., Developmental programming of brain and behavior by perinatal diet: focus on inflammatory mechanisms (2014) Dialogues Clin. Neurosci., 16, pp. 307-320
Bouayed, J., Desor, F., Rammal, H., Kiemer, A.K., Tybl, E., Schroeder, H., Rychen, G., Soulimani, R., Effects of lactational exposure to benzo[alpha]pyrene (B[α]P) on postnatal neurodevelopment, neuronal receptor gene expression and behaviour in mice (2009) Toxicology, 259, pp. 97-106
Bouayed, J., Bohn, T., Tybl, E., Kiemer, A.K., Soulimani, R., Benzo[α]pyrene-induced anti-depressive-like behaviour in adult female mice: role of monoaminergic systems (2012) Basic Clin. Pharmacol. Toxicol., 110, pp. 544-550
Cai, G., Ziko, I., Barwood, J., Soch, A., Sominsky, L., Molero, J.C., Spencer, S.J., Overfeeding during a critical postnatal period exacerbates hypothalamic-pituitary-adrenal axis responses to immune challenge: a role for adrenal melanocortin 2 receptors (2016) Sci. Rep., 6, p. 21097
Cardenas-Gonzalez, M., Gaspar-Ramirez, O., Perez-Vazquez, F.J., Alegria-Torres, J.A., Gonzalez-Amaro, R., Perez-Maldonado, I.N., P, p’-DDE, a DDT metabolite, induces proinflammatory molecules in human peripheral blood mononuclear cells “in vitro” (2013) Exp. Toxicol. Pathol., 65, pp. 661-665
Charney, D.S., Manji, H.K., Life stress, genes, and depression: multiple pathways lead to increased risk and new opportunities for intervention (2004) Sci. STKE, (2004), p. re5
Cryan, J.F., Leonard, B.E., (2010) Depression: From Psychopathology to Pharmacotherapy, , Karger
Cryan, J.F., Mombereau, C., Vassout, A., The tail suspension test as a model for assessing antidepressant activity: review of pharmacological and genetic studies in mice (2005) Neurosci. Biobehav. Rev., 29, pp. 571-625
Damaceno-Rodrigues, N.R., Veras, M.M., Negri, E.M., Zanchi, A.C., Rhoden, C.R., Saldiva, P.H., Dolhnikoff, M., Caldini, E.G., Effect of pre- and postnatal exposure to urban air pollution on myocardial lipid peroxidation levels in adult mice (2009) Inhal. Toxicol., 21, pp. 1129-1137
Dangour, A.D., Uauy, R., N-3 long-chain polyunsaturated fatty acids for optimal function during brain development and ageing (2008) Asia Pac. J. Clin. Nutr., 17, pp. 185-188
Dietert, R.R., Misregulated inflammation as an outcome of early-life exposure to endocrine-disrupting chemicals (2012) Rev. Environ. Health, 27, pp. 117-131
Dietert, R.R., Effects of Endocrine Disrupters on Immune Function and Inflammation (2015), Mica Haley USA
Dirsch, V.M., Stuppner, H., Vollmar, A.M., The Griess assay: suitable for a bio-guided fractionation of anti-inflammatory plant extracts? (1998) Planta Med., 64, pp. 423-426
Dridi, I., Leroy, D., Guignard, C., Scholl, G., Bohn, T., Landoulsi, A., Thome, J.P., Bouayed, J., Dietary early-life exposure to contaminated eels does not impair spatial cognitive performances in adult offspring mice as assessed in the Y-maze and the Morris water maze (2014) Nutr. Res., 34, pp. 1075-1084
Dridi, I., Soualeh, N., Bohn, T., Soulimani, R., Bouayed, J., Chemically contaminated eel fed to pregnant and lactating mouse dams causes hyperactivity in their offspring (2016) Int. J. Vitamin Nutr. Res.
EFSA, European Food Safety Authority. Opinion of the scientific panel on contaminants in the food chain on a request from the commission related to the presence of non dioxine-like polychlorinated biphenyles (PCB) in feed and Food (2005) EFSA J., pp. 1-137
EFSA, European Food Safety Authority Scientific report of EFSA. Results of the monitoring of non dioxin-like PCBs in food and feed (2010) EFSA J., 8, pp. 1-38
Elnar, A.A., Diesel, B., Desor, F., Feidt, C., Bouayed, J., Kiemer, A.K., Soulimani, R., Neurodevelopmental and behavioral toxicity via lactational exposure to the sum of six indicator non-dioxin-like-polychlorinated biphenyls (∑6 NDL-PCBs) in mice (2012) Toxicology, 299, pp. 44-54
Fall, C., Maternal nutrition: effects on health in the next generation (2009) Indian J. Med. Res., 130, pp. 593-599
Focant, J.F., Eppe, G., Pirard, C., De Pauw, E., Fast clean-up for polychlorinated dibenzo-p-dioxins, dibenzofurans and coplanar polychlorinated biphenyls analysis of high-fat-content biological samples (2001) J. Chromatogr. A, 925, pp. 207-221
Genuis, S.J., To sea or not to sea: benefits and risks of gestational fish consumption (2008) Reprod. Toxicol., 26, pp. 81-85
Gioiosa, L., Parmigiani, S., Vom Saal, F.S., Palanza, P., The effects of bisphenol A on emotional behavior depend upon the timing of exposure, age and gender in mice (2013) Horm. Behav., 63, pp. 598-605
Gore, A.C., Martien, K.M., Gagnidze, K., Pfaff, D., Implications of prenatal steroid perturbations for neurodevelopment, behavior, and autism (2014) Endocrinol. Rev., 35, pp. 961-991
Green, L.C., Wagner, D.A., Glogowski, J., Skipper, P.L., Wishnok, J.S., Tannenbaum, S.R., Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids (1982) Anal. Biochem., 126, pp. 131-138
Hale, M.W., Spencer, S.J., Conti, B., Jasoni, C.L., Kent, S., Radler, M.E., Reyes, T.M., Sominsky, L., Diet, behavior and immunity across the lifespan (2014) Neurosci. Biobehav. Rev., 58, pp. 46-62
Henn, F., Vollmayr, B., Sartorius, A., Mechanisms of depression: the role of neurogenesis (2004) Drug Discov. Today Dis. Mech., 1, pp. 407-411
Ingber, S.Z., Pohl, H.R., Windows of sensitivity to toxic chemicals in the motor effects development (2016) Regul. Toxicol. Pharmacol., 74, pp. 93-104
Juruena, M.F., Early-life stress and HPA axis trigger recurrent adulthood depression (2014) Epilepsy Behav., 38, pp. 148-159
Kalueff, A.V., Keisala, T., Minasyan, A., Kuuslahti, M., Miettinen, S., Tuohimaa, P., Behavioural anomalies in mice evoked by “Tokyo” disruption of the Vitamin D receptor gene (2006) Neurosci. Res., 54, pp. 254-260
Kim, S.H., Johnson, V.J., Sharma, R.P., Mercury inhibits nitric oxide production but activates proinflammatory cytokine expression in murine macrophage: differential modulation of NF-kappaB and p38 MAPK signaling pathways (2002) Nitric Oxide, 7, pp. 67-74
Lauritzen, L., Hansen, H.S., Jorgensen, M.H., Michaelsen, K.F., The essentiality of long chain n-3 fatty acids in relation to development and function of the brain and retina (2001) Prog. Lipid Res., 40, pp. 1-94
Li, Y., Xiao, B., Qiu, W., Yang, L., Hu, B., Tian, X., Yang, H., Altered expression of CD4(+) CD25(+) regulatory T cells and its 5-HT(1a) receptor in patients with major depression disorder (2010) J. Affect. Disord., 124, pp. 68-75
Lichtenstein, A.H., Appel, L.J., Brands, M., Carnethon, M., Daniels, S., Franch, H.A., Franklin, B., Wylie-Rosett, J., (2006), Diet and life style recommendations revision: A scientific statement from the American Heart Association Nutrition Committee Circulation
Liu, D., Perkins, J.T., Petriello, M.C., Hennig, B., Exposure to coplanar PCBs induces endothelial cell inflammation through epigenetic regulation of NF-kappaB subunit p65 (2015) Toxicol. Appl. Pharmacol., 289, pp. 457-465
Macgregor, K., Oliver, I.W., Harris, L., Ridgway, I.M., Persistent organic pollutants (PCB, DDT, HCH, HCB & BDE) in eels (Anguilla anguilla) in Scotland: current levels and temporal trends (2010) Environ. Pollut., 158, pp. 2402-2411
Maes, M., Evidence for an immune response in major depression: a review and hypothesis (1995) Prog. Neuropsychopharmacol. Biol. Psychiatry, 19, pp. 11-38
Manuelpillai, U., Ligam, P., Smythe, G., Wallace, E.M., Hirst, J., Walker, D.W., Identification of kynurenine pathway enzyme mRNAs and metabolites in human placenta: up-regulation by inflammatory stimuli and with clinical infection (2005) Am. J. Obstet. Gynecol., 192, pp. 280-288
Marques, A.H., O'Connor, T.G., Roth, C., Susser, E., Bjorke-Monsen, A.L., The influence of maternal prenatal and early childhood nutrition and maternal prenatal stress on offspring immune system development and neurodevelopmental disorders (2013) Front. Neurosci., 7, p. 120
Miller, A.H., Raison, C.L., The role of inflammation in depression: from evolutionary imperative to modern treatment target (2016) Nat. Rev. Immunol., 16, pp. 22-34
Miller, A.H., Maletic, V., Raison, C.L., Inflammation and its discontents: the role of cytokines in the pathophysiology of major depression (2009) Biol. Psychiatry, 65, pp. 732-741
Oken, E., Wright, R.O., Kleinman, K.P., Bellinger, D., Amarasiriwardena, C.J., Hu, H., Rich-Edwards, J.W., Gillman, M.W., Maternal fish consumption, hair mercury, and infant cognition in a U.S (2005) Cohort. Environ. Health Perspect., 113, pp. 1376-1380
Osgood, R.S., Upham, B.L., Hill, T., 3rd, Helms, K.L., Velmurugan, K., Babica, P., Bauer, A.K., Polycyclic aromatic hydrocarbon-induced signaling events relevant to inflammation and tumorigenesis in lung cells are dependent on molecular structure (2013) PLoS One, 8, p. e65150
Pace, T.W., Mletzko, T.C., Alagbe, O., Musselman, D.L., Nemeroff, C.B., Miller, A.H., Heim, C.M., Increased stress-induced inflammatory responses in male patients with major depression and increased early life stress (2006) Am. J. Psychiatry, 163, pp. 1630-1633
Palanza, P., Nagel, S.C., Parmigiani, S., Vom Saal, F.S., Perinatal exposure to endocrine disruptors: sex, timing and behavioral endpoints (2016) Curr. Opin. Behav. Sci., 7, pp. 69-75
Paliwoda, R.E., Newbigging, A.M., Wang, Z., Le, X.C., Benefits and risks associated with consumption of Great Lakes fish containing omega-3 fatty acids and polychlorinated biphenyls (PCBs) (2016) J. Environ. Sci. (China), 41, pp. 1-5
Paykel, E.S., Life events and affective disorders (2003) Acta Psychiatr. Scand. Suppl., pp. 61-66
Porsolt, R.D., Le Pichon, M., Jalfre, M., Depression: a new animal model sensitive to antidepressant treatments (1977) Nature, 266, pp. 730-732
Roegge, C.S., Schantz, S.L., Motor function following developmental exposure to PCBS and/or MEHG (2006) Neurotoxicol. Teratol., 28, pp. 260-277
Roegge, C.S., Wang, V.C., Powers, B.E., Klintsova, A.Y., Villareal, S., Greenough, W.T., Schantz, S.L., Motor impairment in rats exposed to PCBs and methylmercury during early development (2004) Toxicol. Sci., 77, pp. 315-324
Scientific advisory committee on nutrition (SACN), 2004. Advice on fish consumption: benefits and risks. London
Sipka, S., Eum, S.Y., Son, K.W., Xu, S., Gavalas, V.G., Hennig, B., Toborek, M., Oral administration of pcbs induces proinflammatory and prometastatic responses (2008) Environ. Toxicol. Pharmacol., 25, pp. 251-259
Sitarek, K., Gralewicz, S., Early developmental effects of separate or combined perinatal exposure to methylmercury (MeHg) and 2,2’,4,4’,5,5’-hexachlorobiphenyl (PCB 153) in the rat (2009) Int. J. Occup. Med. Environ. Health, 22, pp. 89-105
Spencer, S.J., Perinatal nutrition programs neuroimmune function long-term: mechanisms and implications (2013) Front. Neurosci., 7, p. 144
Spencer, S.J., Hyland, N.P., Sharkey, K.A., Pittman, Q.J., Neonatal immune challenge exacerbates experimental colitis in adult rats: potential role for TNF-alpha (2007) Am. J. Physiol. Regul. Integr. Comp. Physiol., 292, pp. R308-R315
Spencer, S.J., Emmerzaal, T.L., Kozicz, T., Andrews, Z.B., Ghrelin's role in the hypothalamic-pituitary-adrenal axis stress response: implications for mood disorders (2014) Biol. Psychiatry, 78, pp. 19-27
Steru, L., Chermat, R., Thierry, B., Simon, P., The tail suspension test: a new method for screening antidepressants in mice (1985) Psychopharmacology, 85, pp. 367-370
Sugawara, N., Ohba, T., Nakai, K., Kakita, A., Nakamura, T., Suzuki, K., Kameo, S., Satoh, H., Effects of perinatal coexposure to methylmercury and polychlorinated biphenyls on neurobehavioral development in mice (2008) Arch. Toxicol., 82, pp. 387-397
Szlinder-Richert, J., Usydus, Z., Pelczarski, W., Organochlorine pollutants in European eel (Anguilla anguilla L.) from Poland (2010) Chemosphere, 80, pp. 93-99
Talarowska, M., Szemraj, J., Galecki, P., Myeloperoxidase gene expression and cognitive functions in depression (2015) Adv. Med. Sci., 60, pp. 1-5
Thompson, C., Syddall, H., Rodin, I., Osmond, C., Barker, D.J., Birth weight and the risk of depressive disorder in late life (2001) Br. J. Psychiatry, 179, pp. 450-455
Tofoli, S.M., Baes, C., Martins, C.M., Juruena, M.F., Early life stress, HPA axis, and depression (2011) Front. Psychiatry, 4, pp. 229-234
Tsukamoto, K., Kuroki, M., Eels and Humans (2014), Springer Tokyo
Vaccarino, V., Brennan, M.L., Miller, A.H., Bremner, J.D., Ritchie, J.C., Lindau, F., Veledar, E., Hazen, S.L., Association of major depressive disorder with serum myeloperoxidase and other markers of inflammation: a twin study (2008) Biol. Psychiatry, 64, pp. 476-483
Veldhuis, J.D., Sharma, A., Roelfsema, F., Age-dependent and gender-dependent regulation of hypothalamic-adrenocorticotropic-adrenal axis (2013) Endocrinol. Metab. Clin. North Am., 42, pp. 201-225
Veyrand, B., Brosseaud, A., Sarcher, L., Varlet, V., Monteau, F., Marchand, P., Andre, F., Le Bizec, B., Innovative method for determination of 19 polycyclic aromatic hydrocarbons in food and oil samples using gas chromatography coupled to tandem mass spectrometry based on an isotope dilution approach (2007) J. Chromatogr. A, 1149, pp. 333-344
Viggiano, D., The hyperactive syndrome: metanalysis of genetic alterations, pharmacological treatments and brain lesions which increase locomotor activity (2008) Behav. Brain Res., 194, pp. 1-14
Vyskocil, A., Cizkova, M., Tejnorova, I., Effect of prenatal and postnatal exposure to lead on kidney function in male and female rats (1995) J. Appl. Toxicol., 15, pp. 327-328
Wainwright, P.E., Dietary essential fatty acids and brain function: a developmental perspective on mechanisms (2002) Proc. Nutr. Soc., 61, pp. 61-69
Wilson, C.J., Finch, C.E., Cohen, H.J., Cytokines and cognition–the case for a head-to-toe inflammatory paradigm (2002) J. Am. Geriatr. Soc., 50, pp. 2041-2056
Zhao, Y., Ma, R., Shen, J., Su, H., Xing, D., Du, L., A mouse model of depression induced by repeated corticosterone injections (2008) Eur. J. Pharmacol., 581, pp. 113-120