Vitamin D treatment during pregnancy prevents autism-related phenotypes in a mouse model of maternal immune activation

Molecular Autism

Volumn 8, Issue 1, 2017, Pages

  Vuillermot, Stephanie ^a   Luan, Wei ^b   Meyer, Urs ^c   Eyles, Darryl ^b  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Autism; Cytokines; Dopamine; Maternal immune activation; Neurodevelopmental disorders; Schizophrenia; Vitamin D

Indexed keywords

CALCITRIOL; DRUG VEHICLE; INTERLEUKIN 1BETA; INTERLEUKIN 6; POLYINOSINIC POLYCYTIDYLIC ACID; TUMOR NECROSIS FACTOR; CYTOKINE; POLYNUCLEOTIDE; POLYRIBOINOSINIC-POLYRIBOCYTIDYLIC ACID; VITAMIN D;

ACTIVE IMMUNIZATION; ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ANXIETY; ARTICLE; AUTISM; BRAIN LEVEL; CONTROLLED STUDY; EMOTION; FEAR CONDITIONING TEST; FEMALE; FETUS; IMMUNOMODULATION; JUVENILE; LEARNING; MALE; MATERNAL IMMUNE ACTIVATION; MATERNAL NUTRITION; MEMORY; MOUSE; NEUROPROTECTION; NONHUMAN; PHENOTYPE; PREGNANCY; PRENATAL DRUG EXPOSURE; PROTEIN BLOOD LEVEL; SOCIAL INTERACTION; STEREOTYPY; VITAMIN SUPPLEMENTATION; ANIMAL; ANIMAL BEHAVIOR; BLOOD; CHEMICALLY INDUCED; CHILD DEVELOPMENT DISORDERS, PERVASIVE; DISEASE MODEL; DRUG EFFECTS; HUMAN; PRENATAL EXPOSURE; PREVENTION AND CONTROL; SOCIAL BEHAVIOR;

ANIMALS; BEHAVIOR, ANIMAL; CHILD DEVELOPMENT DISORDERS, PERVASIVE; CYTOKINES; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; MICE; PHENOTYPE; POLYNUCLEOTIDES; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; SOCIAL BEHAVIOR; STEREOTYPED BEHAVIOR; VITAMIN D;

EID: 85015153925     PISSN: None     EISSN: 20402392     Source Type: Journal    
DOI: 10.1186/s13229-017-0125-0     Document Type: Article

References (71)

1. Brown AS, Derkits EJ. Prenatal infection and schizophrenia: a review of epidemiologic and translational studies. Am J Psychiatry. 2010;167:261-80.
2. Chess S. Autism in children with congenital rubella. J Autism Child Schizophr. 1971;1:33-47.
3. Patterson PH. Maternal infection and immune involvement in autism. Trends Mol Med. 2011;17:389-94.
4. Meyer U, Feldon J, Dammann O. Schizophrenia and autism: both shared and disorder-specific pathogenesis via perinatal inflammation? Pediatr Res. 2011;69:26R-33R.
5. Atladottir HO, Thorsen P, Ostergaard L, Schendel DE, Lemcke S, Abdallah M, Parner ET. Maternal infection requiring hospitalization during pregnancy and autism spectrum disorders. J Autism Dev Disord. 2010;40:1423-30.
6. Lee BK, Magnusson C, Gardner RM, Blomstrom A, Newschaffer CJ, Burstyn I, Karlsson H, Dalman C. Maternal hospitalization with infection during pregnancy and risk of autism spectrum disorders. Brain Behav Immun. 2015;44:100-5.
7. Smith SEP, Li J, Garbett K, Mirnics K, Patterson PH. Maternal immune activation alters fetal brain development through interleukin-6. J Neurosci. 2007;27:10695-702.
8. Meyer U, Murray PJ, Urwyler A, Yee BK, Schedlowski M, Feldon J. Adult behavioral and pharmacological dysfunctions following disruption of the fetal brain balance between pro-inflammatory and IL-10-mediated anti-inflammatory signaling. Mol Psychiatry. 2008;13:208-21.
9. Choi GB, Yim YS, Wong H, Kim S, Kim H, Kim SV, Hoeffer CA, Littman DR, Huh JR. The maternal interleukin-17a pathway in mice promotes autism-like phenotypes in offspring. Science. 2016;351:933-9.
10. Lante F, Meunier J, Guiramand J, De Jesus Ferreira M-C, Cambonie G, Aimar R, Cohen-Solal C, Maurice T, Vignes M, Barbanel G. Late N-acetylcysteine treatment prevents the deficits induced in the offspring of dams exposed to an immune stress during gestation. Hippocampus. 2008;18:602-9.
11. Aguilar-Valles A, Flores C, Luheshi GN. Prenatal inflammation-induced hypoferremia alters dopamine function in the adult offspring in rat: relevance for schizophrenia. PLoS One. 2010;5:e10967.
12. Coyle P, Tran N, Fung JNT, Summers BL, Rofe AM. Maternal dietary zinc supplementation prevents aberrant behaviour in an object recognition task in mice offspring exposed to LPS in early pregnancy. Behav Brain Res. 2009;197:210-8.
13. Girard S, Tremblay L, Lepage M, Sebire G. IL-1 receptor antagonist protects against placental and neurodevelopmental defects induced by maternal inflammation. J Immunol. 2010;184:3997-4005.
14. Lipina TV, Zai C, Hlousek D, Roder JC, Wong AHC. Maternal immune activation during gestation interacts with Disc1 point mutation to exacerbate schizophrenia-related behaviors in mice. J Neurosci. 2013;33:7654-66.
15. Meyer U, Schwendener S, Feldon J, Yee BK. Prenatal and postnatal maternal contributions in the infection model of schizophrenia. Exp Brain Res. 2006;173:243-57.
16. Zuckerman L, Rehavi M, Nachman R, Weiner I. Immune activation during pregnancy in rats leads to a postpubertal emergence of disrupted latent inhibition, dopaminergic hyperfunction, and altered limbic morphology in the offspring: a novel neurodevelopmental model of schizophrenia. Neuropsychopharmacology. 2003;28:1778-89.
17. 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.
18. Meyer U, Feldon J, Schedlowski M, Yee BK. Towards an immuno-precipitated neurodevelopmental animal model of schizophrenia. Neurosci Biobehav Rev. 2005;29:913-47.
19. 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;26:607-16.
20. 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.
21. Weber-Stadlbauer U, Richetto J, Labouesse MA, Bohacek J, Mansuy IM, Meyer U. Transgenerational transmission and modification of pathological traits induced by prenatal immune activation. Mol Psychiatry. 2017;22(1):102-112.
22. McGrath JJ, Burne TH, Féron F, Mackay-Sim A, Eyles DW. Developmental vitamin D deficiency and risk of schizophrenia: a 10-year update. Schizophr Bull. 2010;36:1073-8.
23. DeLuca GC, Kimball SM, Kolasinski J, Ramagopalan SV, Ebers GC. Review: the role of vitamin D in nervous system health and disease. Neuropathol Appl Neurobiol. 2013;39:458-84.
24. Whitehouse AJO, Holt BJ, Serralha M, Holt PG, Hart PH, Kusel MMH. Maternal vitamin D levels and the autism phenotype among offspring. J Autism Dev Disord. 2013;43:1495-504.
25. Keim SA, Bodnar LM, Klebanoff MA. Maternal and cord blood 25(OH)-vitamin D concentrations in relation to child development and behaviour. Paediatr Perinat Epidemiol. 2014;28:434-44.
26. Fernell E, Bejerot S, Westerlund J, Miniscalco C, Simila H, Eyles D, Gillberg C, Humble MB. Autism spectrum disorder and low vitamin D at birth: a sibling control study. Mol Autism. 2015;6:3.
27. Wang T, Shan L, Du L, Feng J, Xu Z, Staal WG, Jia F. Serum concentration of 25-hydroxyvitamin D in autism spectrum disorder: a systematic review and meta-analysis. Eur Child Adolesc Psychiatry. 2016;25:341-50.
28. Wobke TK, Sorg BL, Steinhilber D. Vitamin D in inflammatory diseases. Front Physiol. 2014;5:244.
29. Zhang Y, Leung DYM, Richers BN, Liu Y, Remigio LK, Riches DW, Goleva E. Vitamin D inhibits monocyte/macrophage proinflammatory cytokine production by targeting MAPK phosphatase-1. J Immunol (Baltimore, Md: 1950). 2012;188:2127-35.
30. Nonn L, Peng L, Feldman D, Peehl DM. Inhibition of p38 by vitamin D reduces interleukin-6 production in normal prostate cells via mitogen-activated protein kinase phosphatase 5: implications for prostate cancer prevention by vitamin D. Cancer Res. 2006;66:4516-24.
31. Joshi S, Pantalena L-C, Liu XK, Gaffen SL, Liu H, Rohowsky-Kochan C, Ichiyama K, Yoshimura A, Steinman L, Christakos S, et al. 1,25-dihydroxyvitamin D(3) ameliorates Th17 autoimmunity via transcriptional modulation of interleukin-17A. Mol Cell Biol. 2011;31:3653-69.
32. Harvey L, Burne THJ, McGrath JJ, Eyles DW. Developmental vitamin D3 deficiency induces alterations in immune organ morphology and function in adult offspring. J Steroid Biochem Mol Biol. 2010;121:239-42.
33. Eyles D, Brown J, Mackay-Sim A, McGrath J, Feron F. Vitamin D3 and brain development. Neuroscience. 2003;118:641-53.
34. Eyles D, Feldon J, Meyer U. Schizophrenia: do all roads lead to dopamine or is this where they start? Evidence from two epidemiologically informed developmental rodent models. Transl Psychiatry. 2012;2:e81.
35. Kesby JP, Cui X, Ko P, McGrath JJ, Burne THJ, Eyles DW. Developmental vitamin D deficiency alters dopamine turnover in neonatal rat forebrain. Neurosci Lett. 2009;461:155-8.
36. Kesby JP, O'Loan JC, Alexander S, Deng C, Huang X-F, McGrath JJ, Eyles DW, Burne THJ. Developmental vitamin D deficiency alters MK-801-induced behaviours in adult offspring. Psychopharmacology (Berl). 2012;220:455-63.
37. Meyer U, Feldon J. Epidemiology-driven neurodevelopmental animal models of schizophrenia. Prog Neurobiol. 2010;90:285-326.
38. Brown AS, Hooton J, Schaefer CA, Zhang H, Petkova E, Babulas V, Perrin M, Gorman JM, Susser ES. Elevated maternal interleukin-8 levels and risk of schizophrenia in adult offspring. Am J Psychiatry. 2004;161:889-95.
39. Arad M, Weiner I. Fluctuation of latent inhibition along the estrous cycle in the rat: modeling the cyclicity of symptoms in schizophrenic women? Psychoneuroendocrinology. 2008;33:1401-10.
40. O'Loan J, Eyles DW, Kesby J, Ko P, McGrath JJ, Burne THJ. Vitamin D deficiency during various stages of pregnancy in the rat; its impact on development and behaviour in adult offspring. Psychoneuroendocrinology. 2007;32:227-34.
41. Deacon RMJ. Digging and marble burying in mice: simple methods for in vivo identification of biological impacts. Nat Protoc. 2006;1:122-4.
42. Burne THJ, McGrath JJ, Eyles DW, Mackay-Sim A. Behavioural characterization of vitamin D receptor knockout mice. Behav Brain Res. 2005;157:299-308.
43. Richmond MA, Murphy CA, Pouzet B, Schmid P, Rawlins JN, Feldon J. A computer controlled analysis of freezing behaviour. J Neurosci Methods. 1998;86:91-9.
44. Meyer U, Nyffeler M, Engler A, Urwyler A, Schedlowski M, Knuesel I, Yee BK, Feldon J. The time of prenatal immune challenge determines the specificity of inflammation-mediated brain and behavioral pathology. J Neurosci. 2006;26:4752-62.
45. Burguillos MA. Use of meso-scale discovery to examine cytokine content in microglia cell supernatant. Methods Mol Biol (Clifton, NJ). 2013;1041:93-100.
46. Kvaskoff D, Heath AK, Simila HA, Ko P, English DR, Eyles DW. Minimizing matrix effects for the accurate quantification of 25-Hydroxyvitamin D metabolites in dried blood spots by LC-MS/MS. Clin Chem. 2016;62:639-46.
47. Brown AS, Sourander A, Hinkka-Yli-Salomaki S, McKeague IW, Sundvall J, Surcel H-M. Elevated maternal C-reactive protein and autism in a national birth cohort. Mol Psychiatry. 2014;19:259-64.
48. Bitanihirwe BKY, Peleg-Raibstein D, Mouttet F, Feldon J, Meyer U. Late prenatal immune activation in mice leads to behavioral and neurochemical abnormalities relevant to the negative symptoms of schizophrenia. Neuropsychopharmacology. 2010;35:2462-78.
49. Meyer U. Prenatal poly(i:C) exposure and other developmental immune activation models in rodent systems. Biol Psychiatry. 2014;75:307-15.
50. Vuillermot S, Weber L, Feldon J, Meyer U. A longitudinal examination of the neurodevelopmental impact of prenatal immune activation in mice reveals primary defects in dopaminergic development relevant to schizophrenia. J Neurosci. 2010;30:1270-87.
51. Richetto J, Calabrese F, Riva MA, Meyer U. Prenatal immune activation induces maturation-dependent alterations in the prefrontal GABAergic transcriptome. Schizophr Bull. 2014;40:351-61.
52. Maren S, Phan KL, Liberzon I. The contextual brain: implications for fear conditioning, extinction and psychopathology. Nat Rev Neurosci. 2013;14:417-28.
53. Maren S, Quirk GJ. Neuronal signalling of fear memory. Nat Rev Neurosci. 2004;5:844-52.
54. Mabunga DFN, Gonzales ELT, Kim J-W, Kim KC, Shin CY. Exploring the validity of valproic acid animal model of autism. Exp Neurobiol. 2015;24:285-300.
55. Banerjee A, Engineer CT, Sauls BL, Morales AA, Kilgard MP, Ploski JE. Abnormal emotional learning in a rat model of autism exposed to valproic acid in utero. Front Behav Neurosci. 2014;8:387.
56. Piontkewitz Y, Arad M, Weiner I. Abnormal trajectories of neurodevelopment and behavior following in utero insult in the rat. Biol Psychiatry. 2011;70:842-51.
57. Silverman JL, Yang M, Lord C, Crawley JN. Behavioural phenotyping assays for mouse models of autism. Nat Rev Neurosci. 2010;11:490-502.
58. Pasciuto E, Borrie SC, Kanellopoulos AK, Santos AR, Cappuyns E, D'Andrea L, Pacini L, Bagni C. Autism spectrum disorders: translating human deficits into mouse behavior. Neurobiol Learn Mem. 2015;124:71-87.
59. Njung'e K, Handley SL. Evaluation of marble-burying behavior as a model of anxiety. Pharmacol Biochem Behav. 1991;38:63-7.
60. Liu PT, Stenger S, Li H, Wenzel L, Tan BH, Krutzik SR, Ochoa MT, Schauber J, Wu K, Meinken C, et al. Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science. 2006;311:1770-3.
61. Brosbol-Ravnborg A, Bundgaard B, Hollsberg P. Synergy between vitamin D(3) and Toll-like receptor agonists regulates human dendritic cell response during maturation. Clin Dev Immunol. 2013;2013:807971.
62. Soumiya H, Fukumitsu H, Furukawa S. Prenatal immune challenge compromises the normal course of neurogenesis during development of the mouse cerebral cortex. J Neurosci Res. 2011;89:1575-85.
63. Cui X, McGrath JJ, Burne THJ, Mackay-Sim A, Eyles DW. Maternal vitamin D depletion alters neurogenesis in the developing rat brain. Int J Dev Neurosci. 2007;25:227-32.
64. Ko P, Burkert R, McGrath J, Eyles D. Maternal vitamin D3 deprivation and the regulation of apoptosis and cell cycle during rat brain development. Brain Res Dev Brain Res. 2004;153:61-8.
65. Nemeth E, Rivera S, Gabayan V, Keller C, Taudorf S, Pedersen BK, Ganz T. IL-6 mediates hypoferremia of inflammation by inducing the synthesis of the iron regulatory hormone hepcidin. J Clin Invest. 2004;113:1271-6.
66. Pankhurst MW, Bennett W, Kirkcaldie MTK, West AK, Chung RS. Increased circulating leukocyte numbers and altered macrophage phenotype correlate with the altered immune response to brain injury in metallothionein (MT)-I/II null mutant mice. J Neuroinflammation. 2011;8:172.
67. Schwalfenberg GK, Genuis SJ. Vitamin D, essential minerals, and toxic elements: exploring interactions between nutrients and toxicants in clinical medicine. Sci World J. 2015;2015:318595.
68. Monlezun DJ, Camargo CAJ, Mullen JT, Quraishi SA. Vitamin D status and the risk of anemia in community-dwelling adults: results from the national health and nutrition examination survey 2001-2006. Medicine. 2015;94:e1799.
69. Claro da Silva T, Hiller C, Gai Z, Kullak-Ublick GA: Vitamin D transactivates the zinc and manganese transporter SLC30A10 via the Vitamin D receptor. J Steroid Biochem Mol Biol. 2016;163:77-87.
70. Gilmore JH, Jarskog LF, Vadlamudi S. Maternal poly I:C exposure during pregnancy regulates TNF alpha, BDNF, and NGF expression in neonatal brain and the maternal-fetal unit of the rat. J Neuroimmunol. 2005;159:106-12.
71. Feng J, Shan L, Du L, Wang B, Li H, Wang W, Wang T, Dong H, Yue X, Xu Z, Staal, WG, Jia F. Clinical improvement following vitamin D3 supplementation in autism spectrum disorder. Nutr Neurosci. 2016;8305:1-7.