Maternal immune stimulation during pregnancy affects adaptive immunity in offspring to promote development of TH17 cells

Brain, Behavior, and Immunity

Volumn 25, Issue 5, 2011, Pages 863-871

  Mandal, Mili ^a   Marzouk, Atara C ^b   Donnelly, Robert ^a,b   Ponzio, Nicholas M ^a,b  

^a UNIVERSITY OF MEDICINE AND DENTISTRY OF NEW JERSEY   (United States)

^b RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

Autism; Cytokines; IL 6; Immune stimulation; Pregnancy; Schizophrenia; TH17 cells

Indexed keywords

CD4 ANTIGEN; GAMMA INTERFERON; INTERLEUKIN 17; INTERLEUKIN 6; POLYINOSINIC POLYCYTIDYLIC ACID;

ADAPTIVE IMMUNITY; AMNION FLUID; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL DIFFERENTIATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; HETEROZYGOSITY; IMMUNOSTIMULATION; MATERNAL SERUM; MEMORY CELL; MOUSE; NONHUMAN; PHENOTYPE; PLACENTA; PREGNANCY; PRIORITY JOURNAL; PROGENY; SUPERNATANT; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; TH17 CELL; WILD TYPE;

ADAPTIVE IMMUNITY; AMNIOTIC FLUID; ANIMALS; FEMALE; FLOW CYTOMETRY; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; IMMUNITY, CELLULAR; IMMUNITY, HUMORAL; IMMUNITY, MATERNALLY-ACQUIRED; IMMUNOLOGIC MEMORY; INTERLEUKIN-6; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PREGNANCY; TH17 CELLS;

EID: 79957917993     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2010.09.011     Document Type: Article

References (83)

1. Ashwood P., Van de Water J. Is autism an autoimmune disease?. Autoimmun. Rev. 2004, 3:557-562.
2. Ashwood P., Wills S., Van de Water J. The immune response in autism: a new frontier for autism research. J. Leukoc. Biol. 2006, 80:1-15.
3. Barrett E.G. Maternal influence in the transmission of asthma susceptibility. Pulm. Pharmacol. Ther. 2008, 21:474-484.
4. Bell M., Hallenbeck J. Effects of intrauterine inflammation on developing rat brain. J. Neurosci. Res. 2002, 70:570-579.
5. Bell M., Hallenbeck J., Gallo V. Determining the fetal inflammatory response in an experimental model of intrauterine inflammation in rats. Pediatr. Res. 2004, 56:541-546.
6. Bellinger D.L., Lubahn C., Lorton D. Maternal and early life stress effects on immune function: relevance to immunotoxicology. J. Immunotoxicol. 2008, 5:419-444.
7. Bettelli E., Carrier Y., Gao W., Korn T., Strom T., Oukka M., Weiner H., Kuchroo V. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006, 441:235-238.
8. Bilbo S.D., Schwarz J.M. Early-life programming of later-life brain and behavior: critical role for the immune system. Front. Behav. Neurosci. 2009, 3:1-14.
9. Boksa P. Effects of prenatal infection on brain development and behavior: a review of findings from animal models. Brain Behav. Immun. 2010, 24:881-897.
10. Carvey P., Chang Q., Lipton J., Ling Z. Prenatal exposure to the bacteriotoxin lipopolysaccharide leads to long-term losses of dopamine neurons in offspring: a potential, new model of Parkinson's disease. Front. Biosci. 2003, 8:s826-s837.
11. Chez M., Dowling T., Patel P., Khanna P., Kominsky M. Elevation of tumor necrosis factor-alpha in cerebrospinal fluid of autistic children. Pediatr. Neurol. 2007, 36:361-365.
12. Chung Y., Chang S.H., Martinez G.J., Yang X.O., Nurieva R., Kang H.S., Ma L., Watowich S.S., Jetten A.M., Tian Q., Dong C. Critical regulation of early Th17 cell differentiation by interleukin-1 signaling. Immunity 2009, 30:576-587.
13. Connolly A.M., Chez M., Streif E.M., Keeling R.M., Golumbek P.T., Kwon J.M., Riviello J.J., Robinson R.G., Neuman R.J., Deuel R.M. Brain-derived neurotrophic factor and autoantibodies to neural antigens in sera of children with autistic spectrum disorders, Landau-Kleffner syndrome, and epilepsy. Biol. Psychiatry 2006, 59:354-363.
14. Conrad M.L., Ferstl R., Teich R., Brand S., Blumer N., Yildirim A.O., Patrascan C.C., Hanuszkiewicz A., Akira S., Wagner H., Holst O., von Mutius E., Pfefferle P.I., Kirschning C.J., Garn H., Renz H. Maternal TLR signaling is required for prenatal asthma protection by the nonpathogenic microbe Acinetobacter lwoffii F78. J. Exp. Med. 2009, 206:2869-2877.
15. Conroy S., Nguyen V., Quina L., Blakely-Gonzales P., Ur C., Netzeband J., Prieto A., DL G. Interleukin-6 produces neuronal loss in developing cerebellar granule neuron cultures. J. Neuroimmunol. 2004, 155:43-54.
16. Croonenberghs J., Bosmans E., Deboutte D., Kenis G., Maes M. Activation of the inflammatory response system in autism. Neuropsychobiology 2002, 45:1-6.
17. 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). Brain Behav. Immun. 2007, 21:490-502.
18. Dammann O., Leviton A. Maternal intrauterine infection, cytokines, and brain damage in the preterm newborn. Pediatr. Res. 1997, 42:1-8.
19. Dantzer R., Kelley K.W. Twenty years of research on cytokine-induced sickness behavior. Brain Behav. Immun. 2007, 21:153-160.
20. Dantzer R., O'Connor J.C., Freund G.G., Johnson R.W., Kelley K.W. From inflammation to sickness and depression: when the immune system subjugates the brain. Nat. Rev. Neurosci. 2008, 9:46-56.
21. de Moura E.G., Lisboa P.C., Passos M.C. Neonatal programming of neuroimmunomodulation - role of adipocytokines and neuropeptides. Neuroimmunomodulation 2008, 15:176-188.
22. Deykin E., MacMahon B. Viral exposure and autism. Am. J. Epidemiol. 1979, 109:628-638.
23. DiCicco-Bloom E., Lord C., Zwaigenbaum L., Courchesne E., Dager S.R., Schmitz C., Schultz R.T., Crawley J., Young L.J. The developmental neurobiology of autism spectrum disorder. J. Neurosci. 2006, 26:6897-6906.
24. Elovitz M., Mrinalini C., Sammel M. Elucidating the early signal transduction pathways leading to fetal brain injury in preterm birth. Pediatr. Res. 2006, 59:50-55.
25. Fatemi S., Earle J., Kanodia R., Kist D., Emamian E., Patterson P., Shi L., Sidwell R. Prenatal viral infection leads to pyramidal cell atrophy and macrocephaly in adulthood: implications for genesis of autism and schizophrenia. Clin. Mol. Neurobiol. 2002, 22:25-33.
26. Fernandes, H., Ramanathan, M., Limson, F., Shah, S., Ponzio, N.M., 2009. Maternal cytokine gene regulation in the pathogenesis of autism. In: International Meeting for Autism Research, Philadelphia, PA. Available from: http://imfar.confex.com/imfar/2010/webprogram/Paper6123.html.
27. Fortier M.E., Joober R., Luheshi G.N., Boksa P. Maternal exposure to bacterial endotoxin during pregnancy enhances amphetamine-induced locomotion and startle responses in adult rat offspring. J. Psychiatr. Res. 2004, 38:335-345.
28. Fortier M.E., Kent S., Ashdown H., Poole S., Boksa P., Luheshi G.N. The viral mimic, polyinosinic:polycytidylic acid, induces fever in rats via an interleukin-1-dependent mechanism. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2004, 287:R759-R766.
29. Furuzawa-Carballeda J., Vargas-Rojas M., Cabral A. Autoimmune inflammation from the Th17 perspective. Autoimmun. Rev. 2007, 6:169-175.
30. Gayle D.A., Beloosesky R., Desai M., Amidi F., Nunez S.E., Ross M.G. Maternal LPS induces cytokines in the amniotic fluid and corticotropin releasing hormone in the fetal rat brain. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2004, 286:R1024-R1029.
31. Gilmore J., Fredrik J., Vadlamudi S., Lauder J. Prenatal infection and risk for schizophrenia: IL-1beta, IL-6, and TNFalpha inhibit cortical neuron dendrite development. Neuropsychopharmacology 2004, 29:1221-1229.
32. Hagberg H., Mallard C. Effect of inflammation on central nervous system development and vulnerability: review. Curr. Opin. Neurol. 2005, 18:117-123.
33. Herberman R., Nunn M., Holden H. Low density of Th-1 antigen on mouse effector cells mediating natural cytotoxicity against tumor cells. J. Immunol. 1978, 121:988-997.
34. Hirota K., Martin B., Veldhoen M. Development, regulation and functional capacities of Th17 cells. Semin. Immunopathol. 2010, 32:3-16.
35. Hornig M., Solbrig M., Horscroft N., Weissenbock H., Lipkin W. Borna disease virus infection of adult and neonatal rats: models for neuropsychiatric disease. Curr. Top. Microbiol. Immunol. 2001, 253:157-177.
36. Hornig M., Weissenbock H., Horscroft N., Lipkin W.I. An infection-based model of neurodevelopmental damage. Proc. Natl. Acad. Sci. 1999, 96:12101-12107.
37. Ito H.T., Smith S.E., Hsiao E., Patterson P.H. Maternal immune activation alters nonspatial information processing in the hippocampus of the adult offspring. Brain Behav. Immun. 2010, 24:930-941.
38. Jonakait G. The effects of maternal inflammation on neuronal development: possible mechanisms. Int. J. Dev. Neurosci. 2007, 25:415-425.
39. Khader S.A., Gaffen S.L., Kolls J.K. Th17 cells at the crossroads of innate and adaptive immunity against infectious diseases at the mucosa. Mucosal Immunol. 2009, 2:403-411.
40. Kipnis J., Cohen H., Cardon M., Ziv Y., Schwartz M. T cell deficiency leads to cognitive dysfunction: implications for therapeutic vaccination for schizophrenia and other psychiatric conditions. Proc. Natl. Acad. Sci. USA 2004, 101:8180-8185.
41. Kipnis J., Derecki N.C., Yang C., Scrable H. Immunity and cognition: what do age-related dementia, HIV-dementia and 'chemo-brain' have in common. Trends Immunol. 2008, 29:455-463.
42. Korn T., Bettelli E., Gao W., Awasthi A., Jager A., Strom T.B., Oukka M., Kuchroo V.K. IL-21 initiates an alternative pathway to induce proinflammatory T(H)17 cells. Nature 2007, 448:484-487.
43. Korn T., Bettelli E., Oukka M., Kuchroo V. IL-17 and TH17 cells. Ann. Rev. Immunol. 2009, 27:485-517.
44. Korn T., Oukka M., Kuchroo V., Bettelli E. Th17 cells: effector T cells with inflammatory properties. Semin. Immunol. 2007, 19:362-371.
45. Lancaster K., Dietz D., Moran T., Pletnikov M. Abnormal social behaviors in young and adult rats neonatally infected with Borna disease virus. Behav. Brain Res. 2007, 176:141-148.
46. Langrish C.L., Chen Y., Blumenschein W.M., Mattson J., Basham B., Sedgwick J.D., McClanahan T., Kastelein R.A., Cua D.J. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 2005, 201:233-240.
47. Lin Y., Zeng Y., Zeng S., Wang T. Potential role of toll-like receptor 3 in a murine model of polyinosinic-polycytidylic acid-induced embryo resorption. Fertil. Steril. 2006, 85(Suppl. 1):1125-1129.
48. Lipkin W., Hornig M. Microbiology and immunology of autism spectrum disorders. Novartis Found. Symp. 2003, 251:129-143.
49. Malek-Ahmadi P. Cytokines and etiopathogenesis of pervasive developmental disorders. Med. Hypotheses 2001, 56:321-324.
50. Mangan P., Harrington L., O'Quinn D., Helms W., Bullard D., Elson C., Hatton R., Wahl S., Schoeb T., Weaver C. Transforming growth factor-β induces development of the Th17 lineage. Nature 2006, 441:231-234.
51. McAleer J.P., Liu B., Li Z., Ngoi S.M., Dai J., Oft M., Vella A.T. Potent intestinal Th17 priming through peripheral lipopolysaccharide-based immunization. J. Leukoc. Biol. 2010, 88:21-31.
52. Merlot E., Couret D., Otten W. Prenatal stress, fetal imprinting and immunity. Brain Behav. Immun. 2008, 22:42-51.
53. Meyer U., Feldon J., Fatemi S.H. In-vivo rodent models for the experimental investigation of prenatal immune activation effects in neurodevelopmental brain disorders. Neurosci. Biobehav. Rev. 2009, 33:1061-1079.
54. Meyer U., Feldon J., Schedlowski M., Yee B.K. Immunological stress at the maternal-foetal interface: a link between neurodevelopment and adult psychopathology. Brain Behav. Immun. 2006, 20:378-388.
55. Meyer U., Nyffeler M., Engler A., Urwyler A., Schedlowski M., Knuesel I., Yee B.K., Feldon J. The time of prenatal immune challenge determines the specificity of inflammation-mediated brain and behavioral pathology. J. Neurosci. 2006, 26:4752-4762.
56. 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. Brain Behav. Immun. 2008, 22:469-486.
57. Nawa H., Takei N. Recent progress in animal modeling of immune inflammatory processes in schizophrenia: implication of specific cytokines. Neurosci. Res. 2006, 56:2-13.
58. Ozawa K., Hashimoto K., Kishimoto T., Shimizu E., Ishikura H., Iyo M. Immune activation during pregnancy in mice leads to dopaminergic hyperfunction and cognitive impairment in the offspring: a neurodevelopmental animal model of schizophrenia. Biol. Psychiatry 2006, 59:546-554.
59. Pardo C., Eberhart C. The neurobiology of autism. Brain Pathol. 2007, 17:434-447.
60. Pardo C.A., Vargas D.L., Zimmerman A.W. Immunity, neuroglia and neuroinflammation in autism. Int. Rev. Psychiatry (Abingdon, England) 2005, 17:485-495.
61. Patterson P. Maternal infection: window on neuroimmune interactions in fetal brain development and mental illness. Curr. Opin. Neurobiol. 2002, 12:115-118.
62. Phillips D.I. External influences on the fetus and their long-term consequences. Lupus 2006, 15:794-800.
63. Pletnikov M.V., Jones M.L., Rubin S.A., Moran T.H., Carbone K.M. Rat model of autism spectrum disorders. Genetic background effects on Borna disease virus-induced development brain damage. Ann. NY Acad. Sci. 2001, 939:318-319.
64. Pletnikov M.V., Rubin S.A., Vansudevan K., Moran T.H., Carbone K.M. Developmental brain injury associated with abnormal play behavior in neonatally borna disease virus-infected lewis rats: a model of autism. Behav. Brain Res. 1999, 100.
65. Ponzio N.M., Servatius R., Beck K., Marzouk A., Kreider T. Cytokine levels during pregnancy influence immunological profiles and neurobehavioral patterns of the offspring. Ann. NY Acad. Sci. 2007, 1107:118-128.
66. Rousset C., Chalon S., Cantagrel S., Bodard S., Andres C., Gressens P., Saliba E. Maternal exposure to LPS induces hypomyelination in the internal capsule and programmed cell death in the deep gray matter in newborn rats. Pediatr. Res. 2006, 59:428-433.
67. Samuelsson A., Jennische E., Hansson H., Holmang A. Prenatal exposure to Interleukin-6 results in inflammatory neurodegeneration in hippocampus with NMDA/GABA(A) dysregulation and impaired spatial learning. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2006, 290:R1345-R1356.
68. Schlotz W., Phillips D.I. Fetal origins of mental health: evidence and mechanisms. Brain Behav. Immun. 2009, 23:905-916.
69. Schroder K., Sweet M.J., Hume D.A. Signal integration between IFNgamma and TLR signalling pathways in macrophages. Immunobiology 2006, 211:511-524.
70. Shi L., Fatemi S.H., Sidwell R.W., Patterson P.H. Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring. J. Neurosci. 2003, 23:297-302.
71. Shi L., Smith S.E., Malkova N., Tse D., Su Y., Patterson P.H. Activation of the maternal immune system alters cerebellar development in the offspring. Brain Behav. Immun. 2009, 23:116-123.
72. Singh V.K. Phenotypic expression of autoimmune autistic disorder (AAD): a major subset of autism. Ann. Clin. Psychiatry 2009, 21:148-161.
73. Smith S.E., Li J., Garbett K., Mirnics K., Patterson P.H. Maternal immune activation alters fetal brain development through interleukin-6. J. Neurosci. 2007, 27:10695-10702.
74. Vargas D.L., Nascimbene C., Krishnan C., Zimmerman A.W., Pardo C.A. Neuroglial activation and neuroinflammation in the brain of patients with autism. Ann. Neurol. 2005, 57:67-81.
75. Veldhoen M., Hocking R.J., Atkins C.J., Locksley R.M., Stockinger B. TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 2006, 24:179-189.
76. Weaver C.T., Hatton R.D., Mangan P.R., Harrington L.E. IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu. Rev. Immunol. 2007, 25:821-852.
77. Weissenbock H., Hornig M., Hickey W., Lipkin W. Microglial activation and neuronal apoptosis in Bornavirus infected neonatal Lewis rats. Brain Pathol. 2000, 10.
78. Winter C., Djodari-Irani A., Sohr R., Morgenstern R., Feldon J., Juckel G., Meyer U. Prenatal immune activation leads to multiple changes in basal neurotransmitter levels in the adult brain: implications for brain disorders of neurodevelopmental origin such as schizophrenia. Int. J. Neuropsychopharmacol. 2009, 12:513-524.
79. Wonderlich J., Shearer G., Livingston A., Brooks A. Induction and measurement of cytotoxic T lymphocyte activity. Current Protocols in Immunology 2006, 3.11.1-3.11.23. John Wiley & Sons, Hoboken, NJ. J.E. Coligan (Ed.).
80. Zenclussen A. CD4(+)CD25+ T regulatory cells in murine pregnancy. J. Reprod. Immunol. 2005, 65:101-110.
81. Zenclussen A.C., Gerlof K., Zenclussen M.L., Ritschel S., Zambon Bertoja A., Fest S., Hontsu S., Ueha S., Matsushima K., Leber J., Volk H.D. Regulatory T cells induce a privileged tolerant microenvironment at the fetal-maternal interface. Eur. J. Immunol. 2006, 36:82-94.
82. Zuckerman L., Rehavi M., Nachman R., Weiner I. Immune activation during pregnancy in rats leads to postpubertal emergence of disrupted latent inhibition, dopaminergic hyperfunction, and altered limbic morphology in the offspring: a novel neurodevelopmental model of schizophrenia. Neuropsychopharmacology 2003, 28:1778-1789.
83. Zuckerman L., Weiner I. Maternal immune activation leads to behavioral and pharmacological changes in the adult offspring. J. Psychiatr. Res. 2005, 39:311-323.