Autism with intellectual disability is associated with increased levels of maternal cytokines and chemokines during gestation

Molecular Psychiatry

Volumn 22, Issue 2, 2017, Pages 273-279

  Jones, K L ^a,b   Croen, L A ^c   Yoshida, C K ^c   Heuer, L ^a,b   Hansen, R ^a,b   Zerbo, O ^c   Delorenze, G N ^c   Kharrazi, M ^d   Yolken, R ^e   Ashwood, P ^a,b   Van De Water, J ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c DIVISION OF RESEARCH   (United States)

^d CALIFORNIA DEPARTMENT OF PUBLIC HEALTH   (United States)

^e JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CYTOKINE; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; INTERLEUKIN 1ALPHA; INTERLEUKIN 6; INTERLEUKIN 8; MONOCYTE CHEMOTACTIC PROTEIN 1;

ADULT; ARTICLE; AUTISM; BLOOD LEVEL; CONTROLLED STUDY; DISEASE ACTIVITY; DISEASE ASSOCIATION; FEMALE; GROWTH RETARDATION; HUMAN; INTELLECTUAL IMPAIRMENT; MAJOR CLINICAL STUDY; MALE; MOLECULAR PATHOLOGY; NEWBORN; PREGNANCY; PROTEIN DETERMINATION; PROTEIN FUNCTION; RISK ASSESSMENT; RISK FACTOR; SCORING SYSTEM; AUTISM SPECTRUM DISORDER; AUTISTIC DISORDER; BLOOD; CASE CONTROL STUDY; CHILD; CHILD DEVELOPMENT; CHILD DEVELOPMENT DISORDERS, PERVASIVE; COMPLICATION; DEVELOPMENTAL DISORDER; INFANT; INTELLECTUAL DISABILITY; MOTHER; PATHOLOGY; PRENATAL EXPOSURE; PRESCHOOL CHILD;

ADULT; AUTISM SPECTRUM DISORDER; AUTISTIC DISORDER; CASE-CONTROL STUDIES; CHEMOKINES; CHILD; CHILD DEVELOPMENT; CHILD DEVELOPMENT DISORDERS, PERVASIVE; CHILD, PRESCHOOL; CYTOKINES; DEVELOPMENTAL DISABILITIES; FEMALE; HUMANS; INFANT; INTELLECTUAL DISABILITY; MALE; MOTHERS; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS;

EID: 84969815937     PISSN: 13594184     EISSN: 14765578     Source Type: Journal    
DOI: 10.1038/mp.2016.77     Document Type: Article

References (49)

1. American Psychiatric Association. Diagnostic and Statistical Manual of Mental Disorders, 5th edn. American Psychiatric Publishing: Arlington, VA, USA, 2013.
2. Developmental Disabilities Monitoring Network Surveillance Year 2010 Principal Investigators, (CDC) CfDCaP. Prevalence of autism spectrum disorder among children aged 8 years-autism and developmental disabilities monitoring network, 11 sites, United States, 2010. Morb Mort Wkly Report Surv (Washington, DC: 2002) 2014; 63: 1-21.
3. Hallmayer J, Cleveland S, Torres A, Phillips J, Cohen B, Torigoe T, et al. Genetic heritability and shared environmental factors among twin pairs with autism. Arch Gen Psychiatry 2011; 68: 1095-1102.
4. Gronborg TK, Schendel DE, Parner ET. Recurrence of autism spectrum disorders in full-and half-siblings and trends over time: a population-based cohort study. JAMA Pediatr 2013; 167: 947-953.
5. Kim YS, Leventhal BL. Genetic epidemiology and insights into interactive genetic and environmental effects in autism spectrum disorders. Biol Psychiatry 2015; 77: 66-74.
6. Atladottir HO, Pedersen MG, Thorsen P, Mortensen PB, Deleuran B, Eaton WW, et al. Association of family history of autoimmune diseases and autism spectrum disorders. Pediatrics 2009; 124: 687-694.
7. Croen LA, Grether JK, Yoshida CK, 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 2005; 159: 151-157.
8. Wu S, Ding Y, Wu F, Li R, Xie G, Hou J, et al. Family history of autoimmune diseases is associated with an increased risk of autism in children: a systematic review and meta-analysis. Neurosci Biobehav Rev 2015; 55: 322-332.
9. 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.
10. Lee BK, Magnusson C, Gardner RM, Blomstrom A, Newschaffer CJ, Burstyn I, et al. Maternal hospitalization with infection during pregnancy and risk of autism spectrum disorders. Brain Behav Immun 2015; 44: 100-105.
11. Zerbo O, Qian Y, Yoshida C, Grether JK, Van de Water J, Croen LA. Maternal infection during pregnancy and autism spectrum disorders. J Autism Dev Disord 2015; 45: 4015-4025.
12. Li X, Chauhan A, Sheikh AM, Patil S, Chauhan V, Li XM, et al. Elevated immune response in the brain of autistic patients. J Neuroimmunol 2009; 207: 111-116.
13. Morgan JT, Chana G, Pardo CA, Achim C, Semendeferi K, Buckwalter J, et al. Microglial activation and increased microglial density observed in the dorsolateral prefrontal cortex in autism. Biol Psychiatry 2010; 68: 368-376.
14. Suzuki K, Sugihara G, Ouchi Y, Nakamura K, Futatsubashi M, Takebayashi K, et al. Microglial activation in young adults with autism spectrum disorder. JAMA Psychiatry 2013; 70: 49-58.
15. Vargas DL, Nascimbene C, Krishnan C, Zimmerman AW, Pardo CA. Neuroglial activation and neuroinflammation in the brain of patients with autism. Ann Neurol 2005; 57: 67-81.
16. Wei H, Zou H, Sheikh AM, Malik M, Dobkin C, Brown WT, et al. IL-6 is increased in the cerebellum of autistic brain and alters neural cell adhesion, migration and synaptic formation. J Neuroinflamm 2011; 8: 52.
17. Croonenberghs J, Wauters A, Devreese K, Verkerk R, Scharpe S, Bosmans E, et al. Increased serum albumin, gamma globulin, immunoglobulin IgG, and IgG2 and IgG4 in autism. Psychol Med 2002; 32: 1457-1463.
18. Enstrom A, Krakowiak P, Onore C, Pessah IN, Hertz-Picciotto I, Hansen RL, et al. Increased IgG4 levels in children with autism disorder. Brain Behav Immun 2009; 23: 389-395.
19. Heuer L, Ashwood P, Schauer J, Goines P, Krakowiak P, Hertz-Picciotto I, et al. Reduced levels of immunoglobulin in children with autism correlates with behavioral symptoms. Autism Res 2008; 1: 275-283.
20. Sweeten TL, Posey DJ, McDougle CJ. High blood monocyte counts and neopterin levels in children with autistic disorder. Am J Psychiatry 2003; 160: 1691-1693.
21. Mead J, Ashwood P. Evidence supporting an altered immune response in ASD. Immunol Lett 2015; 163: 49-55.
22. Abdallah MW, Larsen N, Grove J, Bonefeld-Jorgensen EC, Norgaard-Pedersen B, Hougaard DM, et al. Neonatal chemokine levels and risk of autism spectrum disorders: findings from a Danish historic birth cohort follow-up study. Cytokine 2013; 61: 370-376.
23. Ashwood P, Krakowiak P, Hertz-Picciotto I, Hansen R, Pessah I, Van de Water J. Elevated plasma cytokines in autism spectrum disorders provide evidence of immune dysfunction and are associated with impaired behavioral outcome. Brain Behav Immun 2011; 25: 40-45.
24. Ashwood P, Krakowiak P, Hertz-Picciotto I, Hansen R, Pessah IN, Van de Water J. Associations of impaired behaviors with elevated plasma chemokines in autism spectrum disorders. J Neuroimmunol 2011; 232: 196-199.
25. Zerbo O, Yoshida C, Grether JK, Van de Water J, Ashwood P, Delorenze GN, et al. Neonatal cytokines and chemokines and risk of Autism Spectrum Disorder: the Early Markers for Autism (EMA) study: a case-control study. J Neuroinflamm 2014; 11: 113.
26. Braunschweig D, Van de Water J. Maternal autoantibodies in autism. Arch Neurol 2012; 69: 693-699.
27. Braunschweig D, Krakowiak P, Duncanson P, Boyce R, Hansen RL, Ashwood P, et al. Autism-specific maternal autoantibodies recognize critical proteins in developing brain. Transl Psychiatry 2013; 3: e277.
28. Wegmann TG, Lin H, Guilbert L, Mosmann TR. Bidirectional cytokine interactions in the maternal-fetal relationship: is successful pregnancy a TH2 phenomenon? Immunol today 1993; 14: 353-356.
29. Chaouat G. The Th1/Th2 paradigm: still important in pregnancy? Semin Immunopathol 2007; 29: 95-113.
30. Zaretsky MV, Alexander JM, Byrd W, Bawdon RE. Transfer of inflammatory cytokines across the placenta. Obstet Gynecol 2004; 103: 546-550.
31. 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.
32. Samuelsson AM, Jennische E, Hansson HA, 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 Compar Physiol 2006; 290: R1345-R1356.
33. Hauguel-de Mouzon S, Guerre-Millo M. The placenta cytokine network and inflammatory signals. Placenta 2006; 27: 794-798.
34. Mehler MF, Kessler JA. Cytokines in brain development and function. Adv Protein Chem 1998; 52: 223-251.
35. 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.
36. Yeargin-Allsopp M, Rice C, Karapurkar T, Doernberg N, Boyle C, Murphy C. Prevalence of autism in a US metropolitan area. JAMA 2003; 289: 49-55.
37. Matson JL, Shoemaker M. Intellectual disability and its relationship to autism spectrum disorders. Res Dev Disabil 2009; 30: 1107-1114.
38. Abdallah MW, Larsen N, Grove J, Norgaard-Pedersen B, Thorsen P, Mortensen EL, et al. Amniotic fluid chemokines and autism spectrum disorders: an exploratory study utilizing a Danish Historic Birth Cohort. Brain Behav Immun 2012; 26: 170-176.
39. 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.
40. Chow SS, Craig ME, Jones CA, Hall B, Catteau J, Lloyd AR, et al. Differences in amniotic fluid and maternal serum cytokine levels in early midtrimester women without evidence of infection. Cytokine 2008; 44: 78-84.
41. Deverman BE, Patterson PH. Cytokines and CNS development. Neuron 2009; 64: 61-78.
42. Stuart MJ, Baune BT. Chemokines and chemokine receptors in mood disorders, schizophrenia, and cognitive impairment: a systematic review of biomarker studies. Neurosci Biobehav Rev 2014; 42: 93-115.
43. Bilbo SD, Schwarz JM. The immune system and developmental programming of brain and behavior. Front Neuroendocrinol 2012; 33: 267-286.
44. Li L, Walker TL, Zhang Y, Mackay EW, Bartlett PF. Endogenous interferon gamma directly regulates neural precursors in the non-inflammatory brain. J Neurosci 2010; 30: 9038-9050.
45. Robinson DP, Klein SL. Pregnancy and pregnancy-associated hormones alter immune responses and disease pathogenesis. Horm Behav 2012; 62: 263-271.
46. Denney JM, Nelson EL, Wadhwa PD, Waters TP, Mathew L, Chung EK, et al. Longitudinal modulation of immune system cytokine profile during pregnancy. Cytokine 2011; 53: 170-177.
47. Goines PE, Ashwood P. Cytokine dysregulation in autism spectrum disorders (ASD): possible role of the environment. Neurotoxicol Teratol 2013; 36: 67-81.
48. Heuer L, Braunschweig D, Ashwood P, Van de Water J, Campbell DB. Association of a MET genetic variant with autism-associated maternal autoantibodies to fetal brain proteins and cytokine expression. Transl Psychiatry 2011; 1: e48.
49. Zhou X, Fragala MS, McElhaney JE, Kuchel GA. Conceptual and methodological issues relevant to cytokine and inflammatory marker measurements in clinical research. Curr Opin Clin Nutr Metab care 2010; 13: 541-547.