Behavioral impact of maternal allergic-asthma in two genetically distinct mouse strains

Brain, Behavior, and Immunity

Volumn 63, Issue , 2017, Pages 99-107

  Schwartzer, Jared J ^a   Careaga, Milo ^b,c   Coburn, Morgan A ^a   Rose, Destanie R ^b,c   Hughes, Heather K ^b,c   Ashwood, Paul ^b,c  

^a MOUNT HOLYOKE COLLEGE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Allergies; Animal model; ASD; Asthma; Autism; Maternal immune activation; Translational

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 13; INTERLEUKIN 17; INTERLEUKIN 1BETA; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5; INTERLEUKIN 6; OVALBUMIN; PHOSPHATE BUFFERED SALINE; TUMOR NECROSIS FACTOR; CYTOKINE;

ADULT; ALLERGIC ASTHMA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; AUTISM; BEHAVIOR; C57BL 6 MOUSE; CONTROLLED STUDY; CYTOKINE RESPONSE; FEMALE; GENETIC PREDISPOSITION; GENETICALLY DISTINCT MOUSE STRAIN; GROOMING; IMMUNE RESPONSE; LOCOMOTION; MALE; MARBLE BURYING BEHAVIOR; MARE; MOUSE; MOUSE STRAIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; SOCIAL INTERACTION; ANIMAL; ANIMAL BEHAVIOR; ASTHMA; C57BL MOUSE; DISEASE MODEL; DRUG EFFECTS; GENETICS; GENOTYPE ENVIRONMENT INTERACTION; IMMUNOLOGY; MATERNAL EXPOSURE; PHYSIOLOGY; PREGNANCY; PRENATAL EXPOSURE; TH2 CELL;

ANIMALS; ASTHMA; AUTISM SPECTRUM DISORDER; BEHAVIOR, ANIMAL; CYTOKINES; DISEASE MODELS, ANIMAL; FEMALE; GENE-ENVIRONMENT INTERACTION; MALE; MATERNAL EXPOSURE; MICE; MICE, INBRED C57BL; OVALBUMIN; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; TH2 CELLS;

EID: 85010934278     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2016.09.007     Document Type: Article

References (47)

1. Abdallah, M.W., Larsen, N., Grove, J., Norgaard-Pedersen, B., Thorsen, P., Mortensen, E.L., Hougaard, D.M., Amniotic fluid inflammatory cytokines: potential markers of immunologic dysfunction in autism spectrum disorders. World J. Biol. Psychiatry 14 (2013), 528–538.
2. Association, A.P. (Ed.), 2013. Diagnostic and statistical manual of mental disorders (5th ed.).
3. Atladottir, H.O., Pedersen, M.G., Thorsen, P., Mortensen, P.B., Deleuran, B., Eaton, W.W., Parner, E.T., Association of family history of autoimmune diseases and autism spectrum disorders. Pediatrics 124 (2009), 687–694.
4. Barak, B., Feng, G., Neurobiology of social behavior abnormalities in autism and Williams syndrome. Nat. Neurosci. 19 (2016), 647–655.
5. Bettelli, E., Carrier, Y., Gao, W., Korn, T., Strom, T.B., Oukka, M., Weiner, H.L., Kuchroo, V.K., Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441 (2006), 235–238.
6. Boksa, P., Effects of prenatal infection on brain development and behavior: a review of findings from animal models. Brain Behav. Immun. 24 (2010), 881–897.
7. Bolivar, V.J., Walters, S.R., Phoenix, J.L., Assessing autism-like behavior in mice: variations in social interactions among inbred strains. Behav. Brain Res. 176 (2007), 21–26.
8. Brown, A.S., Epidemiologic studies of exposure to prenatal infection and risk of schizophrenia and autism. Dev. Neurobiol., 2012.
9. Choi, G.B., Yim, Y.S., Wong, H., Kim, S., Kim, H., Kim, S.V., Hoeffer, C.A., Littman, D.R., Huh, J.R., The maternal interleukin-17a pathway in mice promotes autism-like phenotypes in offspring. Science 351 (2016), 933–939.
10. Clancy, B., Darlington, R.B., Finlay, B.L., Translating developmental time across mammalian species. Neuroscience 105 (2001), 7–17.
11. Crabbe, J.C., Wahlsten, D., Dudek, B.C., Genetics of mouse behavior: interactions with laboratory environment. Science 284 (1999), 1670–1672.
12. Crawley, J.N., Mouse behavioral assays relevant to the symptoms of autism. Brain Pathol. 17 (2007), 448–459.
13. Croen, L.A., Grether, J.K., Yoshida, C.K., Odouli, R., Van de Water, J., Maternal autoimmune diseases, asthma and allergies, and childhood autism spectrum disorders: a case-control study. Arch. Pediatr. Adolesc. Med. 159 (2005), 151–157.
14. Deacon, R.M., Digging and marble burying in mice: simple methods for in vivo identification of biological impacts. Nat. Protoc. 1 (2006), 122–124.
15. Errijgers, V., Van Dam, D., Gantois, I., Van Ginneken, C.J., Grossman, A.W., D'Hooge, R., De Deyn, P.P., Kooy, R.F., FVB.129P2-Pde6b(+) Tyr(c-ch)/Ant, a sighted variant of the FVB/N mouse strain suitable for behavioral analysis. Genes Brain Behav. 6 (2007), 552–557.
16. Goines, P.E., Croen, L.A., Braunschweig, D., Yoshida, C.K., Grether, J., Hansen, R., Kharrazi, M., Ashwood, P., Van de Water, J., Increased midgestational IFN-gamma, IL-4 and IL-5 in women bearing a child with autism: a case-control study. Mol. Autism, 2, 2011, 13.
17. Gosch, A., Pankau, R., Social-emotional and behavioral adjustment in children with Williams-Beuren syndrome. Am. J. Med. Genet. 53 (1994), 335–339.
18. Hallmayer, J., Cleveland, S., Torres, A., Phillips, J., Cohen, B., Torigoe, T., Miller, J., Fedele, A., Collins, J., Smith, K., Lotspeich, L., Croen, L.A., Ozonoff, S., Lajonchere, C., Grether, J.K., Risch, N., Genetic heritability and shared environmental factors among twin pairs with autism. Arch. Gen. Psychiatry 68 (2011), 1095–1102.
19. Ichimaru, Y., Egawa, T., Sawa, A., 5-HT1A-receptor subtype mediates the effect of fluvoxamine, a selective serotonin reuptake inhibitor, on marble-burying behavior in mice. Jpn. J. Pharmacol. 68 (1995), 65–70.
20. Jiang, H.Y., Xu, L.L., Shao, L., Xia, R.M., Yu, Z.H., Ling, Z.X., Yang, F., Deng, M., Ruan, B., Maternal infection during pregnancy and risk of autism spectrum disorders: a systematic review and meta-analysis. Brain Behav. Immun., 2016.
21. Knuesel, I., Chicha, L., Britschgi, M., Schobel, S.A., Bodmer, M., Hellings, J.A., Toovey, S., Prinssen, E.P., Maternal immune activation and abnormal brain development across CNS disorders. Nat. Rev. Neurol. 10 (2014), 643–660.
22. Krakowiak, P., Goines, P.E., Tancredi, D.J., Ashwood, P., Hansen, R.L., Hertz-Picciotto, I., Van de Water, J., Neonatal cytokine profiles associated with autism spectrum disorder. Biol. Psychiatry, 2015.
23. 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. 44 (2014), 1546–1555.
24. McFarlane, H.G., Kusek, G.K., Yang, M., Phoenix, J.L., Bolivar, V.J., Crawley, J.N., Autism-like behavioral phenotypes in BTBR T+tf/J mice. Genes Brain Behav. 7 (2008), 152–163.
25. Meyer, U., Prenatal poly(I:C) exposure and other developmental immune activation models in rodent systems. Biol. Psychiatry, 2013.
26. Moloney, R.D., Dinan, T.G., Cryan, J.F., Strain-dependent variations in visceral sensitivity: relationship to stress, anxiety and spinal glutamate transporter expression. Genes Brain Behav. 14 (2015), 319–329.
27. Moy, S.S., Nadler, J.J., Young, N.B., Perez, A., Holloway, L.P., Barbaro, R.P., Barbaro, J.R., Wilson, L.M., Threadgill, D.W., Lauder, J.M., Magnuson, T.R., Crawley, J.N., Mouse behavioral tasks relevant to autism: phenotypes of 10 inbred strains. Behav. Brain Res. 176 (2007), 4–20.
28. Muehlmann, A.M., Edington, G., Mihalik, A.C., Buchwald, Z., Koppuzha, D., Korah, M., Lewis, M.H., Further characterization of repetitive behavior in C58 mice: developmental trajectory and effects of environmental enrichment. Behav. Brain Res. 235 (2012), 143–149.
29. Nadler, J.J., Moy, S.S., Dold, G., Trang, D., Simmons, N., Perez, A., Young, N.B., Barbaro, R.P., Piven, J., Magnuson, T.R., Crawley, J.N., Automated apparatus for quantitation of social approach behaviors in mice. Genes Brain Behav. 3 (2004), 303–314.
30. Ngoc, P.L., Gold, D.R., Tzianabos, A.O., Weiss, S.T., Celedon, J.C., Cytokines, allergy, and asthma. Curr. Opin. Allergy Clin. Immunol. 5 (2005), 161–166.
31. Pellis, S.M., Pasztor, T.J., The developmental onset of a rudimentary form of play fighting in C57 mice. Dev. Psychobiol. 34 (1999), 175–182.
32. Raz, R., Roberts, A.L., Lyall, K., Hart, J.E., Just, A.C., Laden, F., Weisskopf, M.G., Autism spectrum disorder and particulate matter air pollution before, during, and after pregnancy: a nested case-control analysis within the Nurses’ Health Study II Cohort. Environ. Health Perspect. 123 (2015), 264–270.
33. Sakurai, T., Dorr, N.P., Takahashi, N., McInnes, L.A., Elder, G.A., Buxbaum, J.D., Haploinsufficiency of Gtf2i, a gene deleted in Williams Syndrome, leads to increases in social interactions. Autism Res. 4 (2011), 28–39.
34. Schwartzer, J.J., Careaga, M., Chang, C., Onore, C.E., Ashwood, P., Allergic fetal priming leads to developmental, behavioral and neurobiological changes in mice. Transl. Psychiatry, 5, 2015, e543.
35. Silverman, J.L., Yang, M., Lord, C., Crawley, J.N., Behavioural phenotyping assays for mouse models of autism. Nat. Rev. Neurosci. 11 (2010), 490–502.
36. Smith, S.E., Li, J., Garbett, K., Mirnics, K., Patterson, P.H., Maternal immune activation alters fetal brain development through interleukin-6. J. Neurosci. 27 (2007), 10695–10702.
37. Sungur, A.O., Vorckel, K.J., Schwarting, R.K., 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.
38. van Wyk, M., Schneider, S., Kleinlogel, S., Variable phenotypic expressivity in inbred retinal degeneration mouse lines: a comparative study of C3H/HeOu and FVB/N rd1 mice. Mol. Vis. 21 (2015), 811–827.
39. Vijayakumar, N.T., Judy, M.V., Autism spectrum disorders: integration of the genome, transcriptome and the environment. J. Neurol. Sci. 364 (2016), 167–176.
40. Volk, H.E., Hertz-Picciotto, I., Delwiche, L., Lurmann, F., McConnell, R., Residential proximity to freeways and autism in the CHARGE study. Environ. Health Perspect. 119 (2011), 873–877.
41. Wahlsten, D., Metten, P., Phillips, T.J., Boehm, S.L. 2nd, Burkhart-Kasch, S., Dorow, J., Doerksen, S., Downing, C., Fogarty, J., Rodd-Henricks, K., Hen, R., McKinnon, C.S., Merrill, C.M., Nolte, C., Schalomon, M., Schlumbohm, J.P., Sibert, J.R., Wenger, C.D., Dudek, B.C., Crabbe, J.C., Different data from different labs: lessons from studies of gene-environment interaction. J. Neurobiol. 54 (2003), 283–311.
42. Walf, A.A., Frye, C.A., The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nat. Protoc. 2 (2007), 322–328.
43. Whitehead, G.S., Walker, J.K., Berman, K.G., Foster, W.M., Schwartz, D.A., Allergen-induced airway disease is mouse strain dependent. Am. J. Physiol. Lung Cell. Mol. Physiol. 285 (2003), L32–42.
44. Wolff, R.J., Solitary and social play in wild Mus-Musculus (Mammalia). J. Zool. 195 (1981), 405–412.
45. Yang, M., Loureiro, D., Kalikhman, D., Crawley, J.N., Male mice emit distinct ultrasonic vocalizations when the female leaves the social interaction arena. Front. Behav. Neurosci., 7, 2013, 159.
46. Young, E.J., Lipina, T., Tam, E., Mandel, A., Clapcote, S.J., Bechard, A.R., Chambers, J., Mount, H.T., Fletcher, P.J., Roder, J.C., Osborne, L.R., Reduced fear and aggression and altered serotonin metabolism in Gtf2ird1-targeted mice. Genes Brain Behav. 7 (2008), 224–234.
47. Zhu, W., Gilmour, M.I., Comparison of allergic lung disease in three mouse strains after systemic or mucosal sensitization with ovalbumin antigen. Immunogenetics 61 (2009), 199–207.