Allergic fetal priming leads to developmental, behavioral and neurobiological changes in mice

Translational Psychiatry

Volumn 5, Issue , 2015, Pages e543-

  Schwartzer, J J ^a   Careaga, M ^b   Chang, C ^b   Onore, C E ^b   Ashwood, P ^b  

^a MOUNT HOLYOKE COLLEGE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OVALBUMIN; SEROTONIN TRANSPORTER; SLC6A4 PROTEIN, MOUSE;

ALLERGIC ASTHMA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR DISORDER; BODY HEIGHT; BODY WEIGHT; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; ENVIRONMENTAL EXPOSURE; FEMALE; GROOMING; HYPERACTIVITY; HYPOACTIVITY; MALE; MOUSE; NEUROLOGIC DISEASE; NONHUMAN; PREGNANCY; PROGENY; PROTEIN EXPRESSION; SEX DIFFERENCE; SOCIAL BEHAVIOR; ANIMAL; ANIMAL BEHAVIOR; ASTHMA; BRAIN CORTEX; C57BL MOUSE; DISEASE MODEL; GROWTH DISORDER; IMMUNOLOGY; METABOLISM; MOTHER; PATHOPHYSIOLOGY; PRENATAL EXPOSURE; WESTERN BLOTTING;

ANIMALS; ASTHMA; BEHAVIOR, ANIMAL; BLOTTING, WESTERN; CEREBRAL CORTEX; DISEASE MODELS, ANIMAL; FEMALE; GROWTH DISORDERS; MALE; MICE; MICE, INBRED C57BL; MOTHERS; OVALBUMIN; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS;

EID: 84927166595     PISSN: None     EISSN: 21583188     Source Type: Journal    
DOI: 10.1038/tp.2015.40     Document Type: Article

References (87)

1. Fatemi SH, Folsom TD. The neurodevelopmental hypothesis of schizophrenia, revisited. Schizophr Bull 2009; 35: 528-548.
2. Bale TL, Baram TZ, Brown AS, Goldstein JM, Insel TR, McCarthy MM et al. Early life programming and neurodevelopmental disorders. Biol Psychiatry 2010; 68: 314-319.
3. Meyer U, Feldon J, Dammann O. Schizophrenia and autism: both shared and disorder-specific pathogenesis via perinatal inflammation? Pediatr Res 2011; 69: 26R-33R.
4. Cross-Disorder Group of the Psychiatric Genomics Consortium. Genetic relationship between five psychiatric disorders estimated from genome-wide SNPs. Nat Genet 2013; 45: 984-994.
5. Atladottir HO, Thorsen P, Ostergaard L, Schendel DE, Lemcke S, Abdallah M et al. Maternal infection requiring hospitalization during pregnancy and autism spectrum disorders. J Autism Dev Disord 2010; 40: 1423-1430.
6. Goines PE, Croen LA, Braunschweig D, Yoshida CK, Grether J, Hansen R et al. Increased midgestational IFN-gamma, IL-4 and IL-5 in women bearing a child with autism: a case-control study. Mol Autism 2011; 2: 13.
7. Brown AS. Epidemiologic studies of exposure to prenatal infection and risk of schizophrenia and autism. Dev Neurobiol 2012; 72: 1272-1276.
8. Okada H, Kuhn C, Feillet H, Bach JF. The 'hygiene hypothesis' for autoimmune and allergic diseases: an update. Clin Exp Immunol 2010; 160: 1-9.
9. Akinbami LJ, Moorman JE, Bailey C, Zahran HS, King M, Johnson CA et al. Trends in asthma prevalence, health care use, and mortality in the United States, 2001-2010. NCHS Data Brief 2012; 1-8.
10. Moorman JE, Akinbami LJ, Bailey CM, Zahran HS, King ME, Johnson CA et al. National surveillance of asthma: United States, 2001-2010. National Center for Health Statistics. Vital Health Stat 3 2012; 1-67.
11. Atladottir HO, Gyllenberg D, Langridge A, Sandin S, Hansen SN, Leonard H et al. The increasing prevalence of reported diagnoses of childhood psychiatric disorders: a descriptive multinational comparison. Eur Child Adolesc Psychiatry 2014; 24: 173-183.
12. Pineda DA, Palacio LG, Puerta IC, Merchan V, Arango CP, Galvis AY et al. Environmental influences that affect attention deficit/hyperactivity disorder: study of a genetic isolate. Eur Child Adolesc Psychiatry 2007; 16: 337-346.
13. Howerton CL, Bale TL. Prenatal programing: at the intersection of maternal stress and immune activation. Horm Behav 2012; 62: 237-242.
14. Parboosing R, Bao Y, Shen L, Schaefer CA, Brown AS. Gestational influenza and bipolar disorder in adult offspring. JAMA Psychiatry 2013; 70: 677-685.
15. Meyer U. Prenatal Poly(I:C) exposure and other developmental immune activation models in rodent systems. Biol Psychiatry 2013; 75: 307-315.
16. Schiller JS, Lucas JW, Peregoy JA. Summary health statistics for U.S. adults: National Health Interview Survey, 2010. Vital Health Stat 10 2012; 1-207.
17. Croen LA, Grether JK, Yoshida CK, Odouli R, Van de Water J. Maternal autoimmune diseases, asthma and allergies, and childhood autism spectrum disorders: a casecontrol study. Arch Pediatr Adolesc Med 2005; 159: 151-157.
18. Lyall K, Ashwood P, Van de Water J, Hertz-Picciotto I. Maternal immune-mediated conditions, autism spectrum disorders, and developmental delay. J Autism Dev Disord 2014; 44: 1546-1555.
19. 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.
20. Shi L, Fatemi SH, Sidwell RW, Patterson PH. Maternal influenza infection causes marked behavioral and pharmacological changes in the offspring. J Neurosci 2003; 23: 297-302.
21. Malkova NV, Yu CZ, Hsiao EY, Moore MJ, Patterson PH. Maternal immune activation yields offspring displaying mouse versions of the three core symptoms of autism. Brain Behav Immun 2012; 26: 607-616.
22. Meyer U, Nyffeler M, Engler A, Urwyler A, Schedlowski M, Knuesel I et al. The time of prenatal immune challenge determines the specificity of inflammationmediated brain and behavioral pathology. J Neurosci 2006; 26: 4752-4762.
23. 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.
24. Armstrong GL, Conn LA, Pinner RW. Trends in infectious disease mortality in the United States during the 20th century. JAMA 1999; 281: 61-66.
25. Autism and Developmental Disabilities Monitoring Network Surveillance Year 2008 Principal Investigators. Prevalence of autism spectrum disorders-Autism and Developmental Disabilities Monitoring Network, 14 sites, United States, 2008. MMWR Surveill Summ 2012; 61: 1-19.
26. Baganz NL, Blakely RD. A dialogue between the immune system and brain, spoken in the language of serotonin. ACS Chem Neurosci 2013; 4: 48-63.
27. Gaspar P, Cases O, Maroteaux L. The developmental role of serotonin: news from mouse molecular genetics. Nat Rev Neurosci 2003; 4: 1002-1012.
28. Kinast K, Peeters D, Kolk SM, Schubert D, Homberg JR. Genetic and pharmacological manipulations of the serotonergic system in early life: neurodevelopmental underpinnings of autism-related behavior. Front Cell Neurosci 2013; 7: 72.
29. Buznikov GA, Lambert HW, Lauder JM. Serotonin and serotonin-like substances as regulators of early embryogenesis and morphogenesis. Cell Tissue Res 2001; 305: 177-186.
30. Bonnin A, Goeden N, Chen K, Wilson ML, King J, Shih JC et al. A transient placental source of serotonin for the fetal forebrain. Nature 2011; 472: 347-350.
31. Clancy B, Darlington RB, Finlay BL. Translating developmental time across mammalian species. Neuroscience 2001; 105: 7-17.
32. Meyer U, Nyffeler M, Yee BK, 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.
33. Schwartzer JJ, Careaga M, Onore CE, Rushakoff JA, Berman RF, Ashwood P. Maternal immune activation and strain specific interactions in the development of autism-like behaviors in mice. Transl Psychiatry 2013; 3: e240.
34. Nadler JJ, Moy SS, Dold G, Trang D, Simmons N, Perez A et al. Automated apparatus for quantitation of social approach behaviors in mice. Genes Brain Behav 2004; 3: 303-314.
35. Yang M, Silverman JL, Crawley JN. Automated three-chambered social approach task for mice. Curr Protoc Neurosci 2011; Chapter 8: Unit 8.26.
36. Spencer CM, Alekseyenko O, Serysheva E, Yuva-Paylor LA, Paylor R. Altered anxiety-related and social behaviors in the Fmr1 knockout mouse model of fragile X syndrome. Genes Brain Behav 2005; 4: 420-430.
37. Holson RR, Freshwater L, Maurissen JP, Moser VC, Phang W. Statistical issues and techniques appropriate for developmental neurotoxicity testing: a report from the ILSI Research Foundation/Risk Science Institute expert working group on neurodevelopmental endpoints. Neurotoxicol Teratol 2008; 30: 326-348.
38. Lazic SE, Essioux L. Improving basic and translational science by accounting for litter-to-litter variation in animal models. BMC Neurosci 2013; 14: 37.
39. Whitehead GS, Walker JK, Berman KG, Foster WM, Schwartz DA. Allergen-induced airway disease is mouse strain dependent. Am J Physiol Lung Cell Mol Physiol 2003; 285: L32-L42.
40. Nials AT, Uddin S. Mouse models of allergic asthma: acute and chronic allergen challenge. Dis Model Mech 2008; 1: 213-220.
41. Conrad ML, Yildirim AO, Sonar SS, Kilic A, Sudowe S, Lunow M et al. Comparison of adjuvant and adjuvant-free murine experimental asthma models. Clin Exp Allergy 2009; 39: 1246-1254.
42. Zhu W, Gilmour MI. Comparison of allergic lung disease in three mouse strains after systemic or mucosal sensitization with ovalbumin antigen. Immunogenetics 2009; 61: 199-207.
43. Thomas A, Burant A, Bui N, Graham D, Yuva-Paylor LA, Paylor R. Marble burying reflects a repetitive and perseverative behavior more than novelty-induced anxiety. Psychopharmacology (Berl) 2009; 204: 361-373.
44. Muehlmann AM, Edington G, Mihalik AC, Buchwald Z, Koppuzha D, Korah M et al. Further characterization of repetitive behavior in C58 mice: developmental trajectory and effects of environmental enrichment. Behav Brain Res 2012; 235: 143-149.
45. Sungur AO, Vorckel KJ, Schwarting RK, Wohr M. Repetitive behaviors in the Shank1 knockout mouse model for autism spectrum disorder: Developmental aspects and effects of social context. J Neurosci Methods 2014; 234: 92-100.
46. Dawson G, Webb SJ, Wijsman E, Schellenberg G, Estes A, Munson J et al. Neurocognitive and electrophysiological evidence of altered face processing in parents of children with autism: implications for a model of abnormal development of social brain circuitry in autism. Dev Psychopathol 2005; 17: 679-697.
47. Pelphrey KA, Yang DY, McPartland JC. Building a social neuroscience of autism spectrum disorder. Curr Top Behav Neurosci 2014; 16: 215-233.
48. Levin ED, Bushnell PJ, Rezvani AH. Attention-modulating effects of cognitive enhancers. Pharmacol Biochem Behav 2011; 99: 146-154.
49. Careaga M, Schwartzer J, Ashwood P. Inflammatory profiles in the BTBR mouse: how relevant are they to autism spectrum disorders? Brain Behav Immun 2014; 43: 11-16.
50. Braunschweig D, Golub MS, Koenig CM, Qi L, Pessah IN, Van de Water J et al. Maternal autism-associated IgG antibodies delay development and produce anxiety in a mouse gestational transfer model. J Neuroimmunol 2012; 252: 56-65.
51. Rundle A, Hoepner L, Hassoun A, Oberfield S, Freyer G, Holmes D et al. Association of childhood obesity with maternal exposure to ambient air polycyclic aromatic hydrocarbons during pregnancy. Am J Epidemiol 2012; 175: 1163-1172.
52. Cancello R, Clement K. Is obesity an inflammatory illness? Role of low-grade inflammation and macrophage infiltration in human white adipose tissue. BJOG 2006; 113: 1141-1147.
53. Das UN. Is metabolic syndrome X a disorder of the brain with the initiation of lowgrade systemic inflammatory events during the perinatal period? J Nutr Biochem 2007; 18: 701-713.
54. Heindel JJ, vom Saal FS. Role of nutrition and environmental endocrine disrupting chemicals during the perinatal period on the aetiology of obesity. Mol Cell Endocrinol 2009; 304: 90-96.
55. Giulivi C, Napoli E, Schwartzer J, Careaga M, Ashwood P. Gestational exposure to a viral mimetic poly(i:C) results in long-lasting changes in mitochondrial function by leucocytes in the adult offspring. Mediators Inflamm 2013; 2013: 609602.
56. Naviaux RK, Zolkipli Z, Wang L, Nakayama T, Naviaux JC, Le TP et al. Antipurinergic therapy corrects the autism-like features in the poly(IC) mouse model. PLoS One 2013; 8: e57380.
57. Giulivi C, Zhang YF, Omanska-Klusek A, Ross-Inta C, Wong S, Hertz-Picciotto I et al. Mitochondrial dysfunction in autism. JAMA 2010; 304: 2389-2396.
58. Khalife N, Kantomaa M, Glover V, Tammelin T, Laitinen J, Ebeling H et al. Childhood attention-deficit/hyperactivity disorder symptoms are risk factors for obesity and physical inactivity in adolescence. J Am Acad Child Adolesc Psychiatry 2014; 53: 425-436.
59. Rosenfeld M, Brenner-Lavie H, Ari SG, Kavushansky A, Ben-Shachar D. Perturbation in mitochondrial network dynamics and in complex I dependent cellular respiration in schizophrenia. Biol Psychiatry 2011; 69: 980-988.
60. Mossner R, Daniel S, Schmitt A, Albert D, Lesch KP. Modulation of serotonin transporter function by interleukin-4. Life Sci 2001; 68: 873-880.
61. Zhu CB, Lindler KM, Owens AW, Daws LC, Blakely RD, Hewlett WA. Interleukin-1 receptor activation by systemic lipopolysaccharide induces behavioral despair linked to MAPK regulation of CNS serotonin transporters. Neuropsychopharmacology 2010; 35: 2510-2520.
62. Malynn S, Campos-Torres A, Moynagh P, Haase J. The pro-inflammatory cytokine TNF-alpha regulates the activity and expression of the serotonin transporter (SERT) in astrocytes. Neurochem Res 2013; 38: 694-704.
63. Hirano K, Kimura R, Sugimoto Y, Yamada J, Uchida S, Kato Y et al. Relationship between brain serotonin transporter binding, plasma concentration and behavioural effect of selective serotonin reuptake inhibitors. Br J Pharmacol 2005; 144: 695-702.
64. Nordquist N, Oreland L. Serotonin, genetic variability, behaviour, and psychiatric disorders-a review. Ups J Med Sci 2010; 115: 2-10.
65. Daly E, Ecker C, Hallahan B, Deeley Q, Craig M, Murphy C et al. Response inhibition and serotonin in autism: a functional MRI study using acute tryptophan depletion. Brain 2014; 137: 2600-2610.
66. Lesch KP, Waider J. Serotonin in the modulation of neural plasticity and networks: implications for neurodevelopmental disorders. Neuron 2012; 76: 175-191.
67. Gabriele S, Sacco R, Persico AM. Blood serotonin levels in autism spectrum disorder: a systematic review and meta-analysis. Eur Neuropsychopharmacol 2014; 24: 919-929.
68. Selvaraj S, Arnone D, Cappai A, Howes O. Alterations in the serotonin system in schizophrenia: a systematic review and meta-analysis of postmortem and molecular imaging studies. Neurosci Biobehav Rev 2014; 45: 233-245.
69. Veenstra-VanderWeele J, Muller CL, Iwamoto H, Sauer JE, Owens WA, Shah CR et al. Autism gene variant causes hyperserotonemia, serotonin receptor hypersensitivity, social impairment and repetitive behavior. Proc Natl Acad Sci USA 2012; 109: 5469-5474.
70. Ohkawara T, Katsuyama T, Ida-Eto M, Narita N, Narita M. Maternal viral infection during pregnancy impairs development of fetal serotonergic neurons. Brain Dev 2014; 37: 88-93.
71. Wegmann M, Hauber HP. Experimental approaches towards allergic asthma therapy-murine asthma models. Recent Pat Inflamm Allergy Drug Discov 2010; 4: 37-53.
72. Wills-Karp M. Murine models of asthma in understanding immune dysregulation in human asthma. Immunopharmacology 2000; 48: 263-268.
73. Watanabe H, Numata K, Ito T, Takagi K, Matsukawa A. Innate immune response in Th1- and Th2-dominant mouse strains. Shock 2004; 22: 460-466.
74. Moy SS, Nadler JJ, Young NB, Nonneman RJ, Segall SK, Andrade GM et al. Social approach and repetitive behavior in eleven inbred mouse strains. Behav Brain Res 2008; 191: 118-129.
75. Magnan AO, Mely LG, Camilla CA, Badier MM, Montero-Julian FA, Guillot CM et al. Assessment of the Th1/Th2 paradigm in whole blood in atopy and asthma. Increased IFN-gamma-producing CD8(+) T cells in asthma. Am J Respir Crit Care Med 2000; 161: 1790-1796.
76. Wong CK, Ho CY, Ko FW, Chan CH, Ho AS, Hui DS et al. Proinflammatory cytokines (IL-17, IL-6, IL-18 and IL-12) and Th cytokines (IFN-gamma, IL-4, IL-10 and IL-13) in patients with allergic asthma. Clin Exp Immunol 2001; 125: 177-183.
77. Tamasi L, Bohacs A, Pallinger E, Falus A, Rigo J Jr., Muller V et al. Increased interferon-gamma- and interleukin-4-synthesizing subsets of circulating T lymphocytes in pregnant asthmatics. Clin Exp Allergy 2005; 35: 1197-1203.
78. Abdallah MW, Larsen N, Grove J, Norgaard-Pedersen B, Thorsen P, Mortensen EL et al. Amniotic fluid inflammatory cytokines: potential markers of immunologic dysfunction in autism spectrum disorders. World J Biol Psychiatry 2013; 14: 528-538.
79. Ashdown H, Dumont Y, Ng M, Poole S, Boksa P, Luheshi GN. The role of cytokines in mediating effects of prenatal infection on the fetus: implications for schizophrenia. Mol Psychiatry 2006; 11: 47-55.
80. Smith SE, Li J, Garbett K, Mirnics K, Patterson PH. Maternal immune activation alters fetal brain development through interleukin-6. J Neurosci 2007; 27: 10695-10702.
81. Raghupathy R, Kalinka J. Cytokine imbalance in pregnancy complications and its modulation. Front Biosci 2008; 13: 985-994.
82. Ghio AJ, Smith CB, Madden MC. Diesel exhaust particles and airway inflammation. Curr Opin Pulm Med 2012; 18: 144-150.
83. Volk HE, Lurmann F, Penfold B, Hertz-Picciotto I, McConnell R. Traffic-related air pollution, particulate matter, and autism. JAMA Psychiatry 2013; 70: 71-77.
84. Testa C, Nuti F, Hayek J, De Felice C, Chelli M, Rovero P et al. Di-(2-ethylhexyl) phthalate and autism spectrum disorders. ASN Neuro 2012; 4: 223-229.
85. Li XJ, Jiang L, Chen L, Chen HS, Li X. Neurotoxicity of dibutyl phthalate in brain development following perinatal exposure: a study in rats. Environ Toxicol Pharmacol 2013; 36: 392-402.
86. Schwartzer JJ, Koenig CM, Berman RF. Using mouse models of autism spectrum disorders to study the neurotoxicology of gene-environment interactions. Neurotoxicol Teratol 2013; 36: 17-35.
87. North ML, Takaro TK, Diamond ML, Ellis AK. Effects of phthalates on the development and expression of allergic disease and asthma. Ann Allergy Asthma Immunol 2014; 112: 496-502.