Maternal immune activation in late gestation increases neuroinflammation and aggravates experimental autoimmune encephalomyelitis in the offspring

Brain, Behavior, and Immunity

Volumn 43, Issue , 2015, Pages 159-171

  Zager, Adriano ^a   Peron, Jean Pierre ^a   Mennecier, Gregory ^a   Rodrigues, Sandra C ^a   Aloia, Thiago P ^a   Palermo Neto, João ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

EAE; Macrophages; Maternal immune activation; Microglia; Mixed glial culture; Neuroinflammation; Prenatal LPS; T cells

Indexed keywords

CD11B ANTIGEN; CD45 ANTIGEN; GLIAL FIBRILLARY ACIDIC PROTEIN; INTERLEUKIN 10; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 6; IONIZED CALCIUM BINDING ADAPTOR MOLECULE 1; LIPOPOLYSACCHARIDE; MICROTUBULE ASSOCIATED PROTEIN 2; NITRITE; PROTEIN; UNCLASSIFIED DRUG; CYTOKINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CD4+ T LYMPHOCYTE; CELL INFILTRATION; CYTOKINE PRODUCTION; DISEASE SEVERITY; EXPERIMENTAL AUTOIMMUNE ENCEPHALOMYELITIS; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION; GESTATION PERIOD; GLIA CELL; GLIAL CELL CULTURE; GLIOSIS; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOFLUORESCENCE MICROSCOPY; LOCOMOTION; LYMPH NODE; LYMPH NODE CELL; MACROPHAGE; MALE; MICROGLIA; MONONUCLEAR CELL; MOUSE; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; OPEN FIELD TEST; PHENOTYPE; PRENATAL EXPOSURE; PROGENY; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY T LYMPHOCYTE; SPLEEN; SPLEEN CELL; TH1 CELL; TH17 CELL; WESTERN BLOTTING; ANIMAL; AUTOIMMUNITY; BRAIN; IMMUNOLOGY; INFLAMMATION; METABOLISM; MOTOR ACTIVITY; PREGNANCY;

ANIMALS; ASTROCYTES; AUTOIMMUNITY; BRAIN; CYTOKINES; ENCEPHALOMYELITIS, AUTOIMMUNE, EXPERIMENTAL; FEMALE; INFLAMMATION; MALE; MICE; MICROGLIA; MOTOR ACTIVITY; PREGNANCY;

EID: 84919443895     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2014.07.021     Document Type: Article

References (33)

1. Bilbo S.D., Schwarz J.M. Early-life programming of later-life brain and behavior: a critical role for the immune system. Front. Behav. Neurosci. 2009, 3:14.
2. Brown D.A., Sawchenko P.E. Time course and distribution of inflammatory and neurodegenerative events suggest structural bases for the pathogenesis of experimental autoimmune encephalomyelitis. J. Comp. Neurol. 2007, 502:236-260.
3. Carson M.J., Reilly C.R., Sutcliffe J.G., Lo D. Mature microglia resemble immature antigen-presenting cells. Glia 1998, 22:72-85.
4. Giovanoli S., Engler H., Engler A., Richetto J., Voget M., Willi R., Winter C., Riva M.A., Mortensen P.B., Schedlowski M., Meyer U. Stress in puberty unmasks latent neuropathological consequences of prenatal immune activation in mice. Science 2013, 339:1095-1099.
5. Glass C.K., Saijo K., Winner B., Marchetto M.C., Gage F.H. Mechanisms underlying inflammation in neurodegeneration. Cell 2010, 140:918-934.
6. Golan H.M., Lev V., Hallak M., Sorokin Y., Huleihel M. Specific neurodevelopmental damage in mice offspring following maternal inflammation during pregnancy. Neuropharmacology 2005, 48:903-917.
7. Golan H., Stilman M., Lev V., Huleihel M. Normal aging of offspring mice of mothers with induced inflammation during pregnancy. Neuroscience 2006, 141:1909-1918.
8. Gomez-Serrano M., Tonelli L., Listwak S., Sternberg E., Riley A.L. Effects of cross fostering on open-field behavior, acoustic startle, lipopolysaccharide-induced corticosterone release, and body weight in Lewis and Fischer rats. Behav. Genet. 2001, 31:427-436.
9. Goverman J., Perchellet A., Huseby E.S. The role of CD8(+) T cells in multiple sclerosis and its animal models. Curr. Drug Targets Inflamm. Allergy 2005, 4:239-245.
10. Handel A.E., Handunnetthi L., Giovannoni G., Ebers G.C., Ramagopalan S.V. Genetic and environmental factors and the distribution of multiple sclerosis in Europe. Eur. J. Neurol. 2010, 17:1210-1214.
11. Hauser S.L., Oksenberg J.R. The neurobiology of multiple sclerosis: genes, inflammation, and neurodegeneration. Neuron 2006, 52:61-76.
12. Hava G., Vered L., Yael M., Mordechai H., Mahoud H. Alterations in behavior in adult offspring mice following maternal inflammation during pregnancy. Dev. Psychobiol. 2006, 48:162-168.
13. Hsiao E.Y., Patterson P.H. Activation of the maternal immune system induces endocrine changes in the placenta via IL-6. Brain Behav. Immun. 2011, 25:604-615.
14. Ivanov I.I., McKenzie B.S., Zhou L., Tadokoro C.E., Lepelley A., Lafaille J.J., Cua D.J., Littman D.R. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 2006, 126:1121-1133.
15. Kleinewietfeld M., Manzel A., Titze J., Kvakan H., Yosef N., Linker R.A., Muller D.N., Hafler D.A. Sodium chloride drives autoimmune disease by the induction of pathogenic TH17 cells. Nature 2013, 496:518-522.
16. Kroenke M.A., Segal B.M. Th17 and Th1 responses directed against the immunizing epitope, as opposed to secondary epitopes, dominate the autoimmune repertoire during relapses of experimental autoimmune encephalomyelitis. J. Neurosci. Res. 2007, 85:1685-1693.
17. Krstic D., Madhusudan A., Doehner J., Vogel P., Notter T., Imhof C., Manalastas A., Hilfiker M., Pfister S., Schwerdel C., Riether C., Meyer U., Knuesel I. Systemic immune challenges trigger and drive Alzheimer-like neuropathology in mice. J. Neuroinflammation 2012, 9:151.
18. Ling Z., Chang Q.A., Tong C.W., Leurgans S.E., Lipton J.W., Carvey P.M. Rotenone potentiates dopamine neuron loss in animals exposed to lipopolysaccharide prenatally. Exp. Neurol. 2004, 190:373-383.
19. Ling Z., Zhu Y., Tong C., Snyder J.A., Lipton J.W., Carvey P.M. Progressive dopamine neuron loss following supra-nigral lipopolysaccharide (LPS) infusion into rats exposed to LPS prenatally. Exp. Neurol. 2006, 199:499-512.
20. Little A.R., O'Callagha J.P. Astrogliosis in the adult and developing CNS: is there a role for proinflammatory cytokines?. Neurotoxicology 2001, 22:607-618.
21. Mandal M., Marzouk A.C., Donnelly R., Ponzio N.M. Maternal immune stimulation during pregnancy affects adaptive immunity in offspring to promote development of TH17 cells. Brain Behav. Immun. 2010, 25:863-871.
22. Mandal M., Marzouk A.C., Donnelly R., Ponzio N.M. Preferential development of Th17 cells in offspring of immunostimulated pregnant mice. J. Reprod. Immunol. 2010, 87:97-100.
23. Mandal M., Donnelly R., Elkabes S., Zhang P., Davini D., David B.T., Ponzio N.M. Maternal immune stimulation during pregnancy shapes the immunological phenotype of offspring. Brain Behav. Immun. 2013, 33:33-45.
24. McQuillan K., Lynch M.A., Mills K.H. Activation of mixed glia by Abeta-specific Th1 and Th17 cells and its regulation by Th2 cells. Brain Behav. Immun. 2010, 24:598-607.
25. Murphy A.C., Lalor S.J., Lynch M.A., Mills K.H. Infiltration of Th1 and Th17 cells and activation of microglia in the CNS during the course of experimental autoimmune encephalomyelitis. Brain Behav. Immun. 2010, 24:641-651.
26. Neumann H. Molecular mechanisms of axonal damage in inflammatory central nervous system diseases. Curr. Opin. Neurol. 2003, 16:267-273.
27. Rodriguez M. Effectors of demyelination and remyelination in the CNS: implications for multiple sclerosis. Brain Pathol. 2007, 17:219-229.
28. Shrikant P., Benveniste E.N. The central nervous system as an immunocompetent organ: role of glial cells in antigen presentation. J. Immunol. 1996, 157:1819-1822.
29. Sospedra M., Martin R. Immunology of multiple sclerosis. Annu. Rev. Immunol. 2005, 23:683-747.
30. Voskuhl R.R., Palaszynski K. Sex hormones in experimental autoimmune encephalomyelitis: implications for multiple sclerosis. Neuroscientist 2001, 7:258-270.
31. Zager A., Mennecier G., Palermo-Neto J. Maternal immune activation in late gestation enhances locomotor response to acute but not chronic amphetamine treatment in male mice offspring: role of the D1 receptor. Behav. Brain Res. 2012, 232:30-36.
32. Zager A., Pinheiro M.L., Ferraz-de-Paula V., Ribeiro A., Palermo-Neto J. Increased cell-mediated immunity in male mice offspring exposed to maternal immune activation during late gestation. Int. Immunopharmacol. 2013, 17:633-637.
33. Zager A., Andersen M.L., Tufik S., Palermo-Neto J. Maternal immune activation increases the corticosterone response to acute stress without affecting the hypothalamic monoamine content and sleep patterns in male mice offspring. NeuroImmunoModulation 2014, 21:37-44.