Association of a MET genetic variant with autism-associated maternal autoantibodies to fetal brain proteins and cytokine expression

Translational Psychiatry

Volumn 1, Issue , 2011, Pages

  Heuer, L ^a,b   Braunschweig, D ^a,b   Ashwood, P ^a,b   Van De Water, J ^a,b   Campbell, D B ^c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

autism; cytokine; gene; immune; maternal

Indexed keywords

AUTOANTIBODY; FETOPROTEIN; INTERLEUKIN 10; MET PROTEIN, HUMAN; NERVE PROTEIN; SCATTER FACTOR RECEPTOR;

ADULT; ARTICLE; AUTISM; BIOSYNTHESIS; BRAIN; DOWN REGULATION; DRUG ANTAGONISM; FEMALE; FETOMATERNAL TRANSFUSION; GENETICS; HUMAN; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; MALE; METABOLISM; PREGNANCY; PRENATAL DEVELOPMENT; PRESCHOOL CHILD;

ADULT; AUTISTIC DISORDER; AUTOANTIBODIES; BRAIN; CHILD, PRESCHOOL; DOWN-REGULATION; FEMALE; FETAL PROTEINS; HUMANS; IMMUNE TOLERANCE; INTERLEUKIN-10; MALE; MATERNAL-FETAL EXCHANGE; NERVE TISSUE PROTEINS; PREGNANCY; PROTO-ONCOGENE PROTEINS C-MET;

EID: 80054823145     PISSN: None     EISSN: 21583188     Source Type: Journal    
DOI: 10.1038/tp.2011.48     Document Type: Article

References (61)

1. Gupta AR, State MW. Recent advances in the genetics of autism. Biol Psychiatry 2007; 61: 429-437. (Pubitemid 46185337)
2. Geschwind DH, Levitt P. Autism spectrum disorders: developmental disconnection syndromes. Curr Opin Neurobiol 2007; 17: 103-111. (Pubitemid 46237744)
3. Levitt P, Campbell DB. The genetic and neurobiologic compass points toward common signaling dysfunctions in autism spectrum disorders. J Clin Invest 2009; 119: 747-754.
4. 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 Jul 4.
5. Ashwood P, Van de Water J. A review of autism and the immune response. Clin Dev Immunol 2004; 11: 165-174. (Pubitemid 38955074)
6. 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. (Pubitemid 44841805)
7. Garbett K, Ebert PJ, Mitchell A, Lintas C, Manzi B, Mirnics K et al. Immune transcriptome alterations in the temporal cortex of subjects with autism. Neurobiol Dis 2008; 30: 303-311.
8. 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.
9. Comi AM, Zimmerman AW, Frye VH, Law PA, Peeden JN. Familial clustering of autoimmune disorders and evaluation of medical risk factors in autism. J Child Neurol 1999; 14: 388-394. (Pubitemid 29321099)
10. Atladóttir HÓ , Thorsen P, stergaard 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.
11. 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. (Pubitemid 40194181)
12. Dalton P, Deacon R, Blamire A, Pike M, McKinlay I, Stein J et al. Maternal neuronal antibodies associated with autism and a language disorder. Ann Neurol 2003; 53: 533-537. (Pubitemid 36373267)
13. Zimmerman AW, Connors SL, Matteson KJ, Lee LC, Singer HS, Castaneda JA et al. Maternal antibrain antibodies in autism. Brain Behav Immun 2007; 21: 351-357. (Pubitemid 46199109)
14. Singer HS, Morris CM, Gause CD, Gillin PK, Crawford S, Zimmerman AW. Antibodies against fetal brain in sera of mothers with autistic children. J Neuroimmunol 2008; 194: 165-172.
15. Braunschweig D, Ashwood P, Krakowiak P, Hertz-Picciotto I, Hansen R, Croen LA et al. Autism: maternally derived antibodies specific for fetal brain proteins. Neurotoxicology 2008; 29: 226-231.
16. Martin LA, Ashwood P, Braunschweig D, Cabanlit M, Van de Water J, Amaral DG. Stereotypes and hyperactivity in rhesus monkeys exposed to IgG from mothers of children with autism. Brain Behav Immun 2008; 22: 806-816.
17. Singer HS, Morris C, Gause C, Pollard M, Zimmerman AW, Pletnikov M. Prenatal exposure to antibodies from mothers of children with autism produces neurobehavioral alterations: a pregnant dam mouse model. J Neuroimmunol 2009; 211: 39-48.
18. Campbell DB, Sutcliffe JS, Ebert PJ, Militerni R, Bravaccio C, Trillo S et al. A genetic variant that disrupts MET transcription is associated with autism. Proc Natl Acad Sci USA 2006; 103: 16834-16839. (Pubitemid 44737339)
19. Campbell DB, Li C, Sutcliffe JS, Persico AM, Levitt P. Genetic evidence implicating multiple genes in the MET receptor tyrosine kinase pathway in autism spectrum disorder. Autism Res 2008; 1: 158-168.
20. Jackson PB, Boccuto L, Skinner C, Collins JS, Neri G, Gurrieri F et al. Further evidence that the rs1858830 C variant in the promoter region of the MET gene is associated with autistic disorder. Autism Res 2009; 2: 232-236.
21. Campbell DB, Buie TM, Winter H, Bauman M, Sutcliffe JS, Perrin JM et al. Distinct genetic risk based on association of MET in families with co-occurring autism and gastrointestinal conditions. Pediatrics 2009; 123: 1018-1024.
22. Campbell DB, Warren D, Sutcliffe JS, Lee EB, Levitt P. Association of MET with social and communication phenotypes in individuals with autism spectrum disorder. Am J Med Genet B Neuropsychiatr Genet 2010; 153B: 438-446.
23. Russo AJ, Krigsman A, Jepson B, Wakefield A. Decreased serum hepatocyte growth factor (HGF) in autistic children with severe gastrointestinal disease. Biomark Insights 2009; 4: 181-190.
24. Kuroiwa T, Iwasaki T, Imado T, Sekiguchi M, Fujimoto J, Sano H. Hepatocyte growth factor prevents lupus nephritis in a murine lupus model of chronic graft-versus-host disease. Arthritis Res Ther 2006; 8: R123.
25. Futamatsu H, Suzuki J, Mizuno S, Koga N, Adachi S, Kosuge H et al. Hepatocyte growth factor ameliorates the progression of experimental autoimmune myocarditis: a potential role for induction of T helper 2 cytokines. Circ Res 2005; 96: 823-830. (Pubitemid 40604965)
26. Okunishi K, Dohi M, Fujio K, Nakagome K, Tabata Y, Okasora T et al. Hepatocyte growth factor significantly suppresses collagen-induced arthritis in mice. J Immunol 2007; 179: 5504-5513.
27. Okunishi K, Dohi M, Nakagome K, Tanaka R, Mizuno S, Matsumoto K et al. A novel role of hepatocyte growth factor as an immune regulator through suppressing dendritic cell function. J Immunol 2005; 175: 4745-4753. (Pubitemid 41362016)
28. Rutella S, Bonanno G, Procoli A, Mariotti A, de Ritis DG, Curti A et al. Hepatocyte growth factor favors monocyte differentiation into regulatory interleukin (IL)-10++IL-12low/neg accessory cells with dendritic-cell features. Blood 2006; 108: 218-227. (Pubitemid 43990632)
29. Campbell DB, D'Oronzio R, Garbett K, Ebert PJ, Mirnics K, Levitt P et al. Disruption of cerebral cortex MET signaling in autism spectrum disorder. Ann Neurol 2007; 62: 243-250. (Pubitemid 47525400)
30. Hertz-Picciotto I, Croen LA, Hansen R, Jones CR, van de Water J, Pessah IN. The CHARGE study: an epidemiologic investigation of genetic and environmental factors contributing to autism. Environ Health Perspect 2006; 114: 1119-1125. (Pubitemid 44018911)
31. Lord C, Pickles A, McLennan J, Rutter M, Bregman J, Folstein S et al. Diagnosing autism: analyses of data from the Autism Diagnostic Interview. J Autism Dev Disord 1997; 27: 501-517. (Pubitemid 27513149)
32. DiLavore PC, Lord C, Rutter M. The pre-linguistic autism diagnostic observation schedule. J Autism Dev Disord 1995; 25: 355-379.
33. Joseph RM, Tager-Flusberg H, Lord C. Cognitive profiles and social-communicative functioning in children with autism spectrum disorder. J Child Psychol Psychiatry 2002; 43: 807-821. (Pubitemid 36939261)
34. Lord C, Leventhal BL, Cook Jr EH. Quantifying the phenotype in autism spectrum disorders. Am J Med Genet 2001; 105: 36-38.
35. Owley T, McMahon W, Cook EH, Laulhere T, South M, Mays LZ et al. Multisite, doubleblind, placebo-controlled trial of porcine secretin in autism. J Am Acad Child Adolesc Psychiatry 2001; 40: 1293-1299. (Pubitemid 32995797)
36. APA. Diagnostic and Statistical Manual of Mental Disorders: DSM-IV. 4th edn American Psychiatric Association: Washington, DC, 1994.
37. Steinhausen HC, Erdin A. Abnormal psychosocial situations and ICD-10 diagnoses in children and adolescents attending a psychiatric service. J Child Psychol Psychiatry 1992; 33: 731-740.
38. Braunschweig D, Duncanson P, Boyce R, Hansen R, Ashwood P, Pessah I et al. Behavioral correlates of maternal antibody status among children with autism. J Autism Dev Disord 2011 (in press).
39. Birchmeier C, Birchmeier W, Gherardi E, Vande Woude GF. Met, metastasis, motility and more. Nat Rev Mol Cell Biol 2003; 4: 915-925. (Pubitemid 37493640)
40. Huh CG, Factor VM, Sanchez A, Uchida K, Conner EA, Thorgeirsson SS. Hepatocyte growth factor/c-met signaling pathway is required for efficient liver regeneration and repair. Proc Natl Acad Sci USA 2004; 101: 4477-4482. (Pubitemid 38437436)
41. Tahara Y, Ido A, Yamamoto S, Miyata Y, Uto H, Hori T et al. Hepatocyte growth factor facilitates colonic mucosal repair in experimental ulcerative colitis in rats. J Pharmacol Exp Ther 2003; 307: 146-151. (Pubitemid 37151900)
42. Arthur LG, Schwartz MZ, Kuenzler KA, Birbe R. Hepatocyte growth factor treatment ameliorates diarrhea and bowel inflammation in a rat model of inflammatory bowel disease. J Pediatr Surg 2004; 39: 139-143; discussion 139-143. (Pubitemid 38146424)
43. Ido A, Numata M, Kodama M, Tsubouchi H. Mucosal repair and growth factors: recombinant human hepatocyte growth factor as an innovative therapy for inflammatory bowel disease. J Gastroenterol 2005; 40: 925-931. (Pubitemid 41662515)
44. Beilmann M, Odenthal M, Jung W, Vande Woude GF, Dienes HP, Schirmacher P. Neoexpression of the c-met/hepatocyte growth factor-scatter factor receptor gene in activated monocytes. Blood 1997; 90: 4450-4458. (Pubitemid 27508450)
45. Beilmann M, Vande Woude GF, Dienes HP, Schirmacher P. Hepatocyte growth factorstimulated invasiveness of monocytes. Blood 2000; 95: 3964-3969. (Pubitemid 30412875)
46. Ito W, Kanehiro A, Matsumoto K, Hirano A, Ono K, Maruyama H et al. Hepatocyte growth factor attenuates airway hyperresponsiveness, inflammation, and remodeling. Am J Respir Cell Mol Biol 2005; 32: 268-280. (Pubitemid 40478302)
47. Yamaura K, Ito K, Tsukioka K, Wada Y, Makiuchi A, Sakaguchi M et al. Suppression of acute and chronic rejection by hepatocyte growth factor in a murine model of cardiac transplantation: induction of tolerance and prevention of cardiac allograft vasculopathy. Circulation 2004; 110: 1650-1657. (Pubitemid 39297989)
48. Adams DH, Harvath L, Bottaro DP, Interrante R, Catalano G, Tanaka Y et al. Hepatocyte growth factor and macrophage inflammatory protein 1 beta: structurally distinct cytokines that induce rapid cytoskeletal changes and subset-preferential migration in T cells. Proc Natl Acad Sci USA 1994; 91: 7144-7148. (Pubitemid 24226819)
49. Chen Q, DeFrances MC, Zarnegar R. Induction of met proto-oncogene (hepatocyte growth factor receptor) expression during human monocyte-macrophage differentiation. Cell Growth Differ 1996; 7: 821-832. (Pubitemid 26360750)
50. van der Voort R, Taher TE, Keehnen RM, Smit L, Groenink M, Pals ST. Paracrine regulation of germinal center B cell adhesion through the c-met-hepatocyte growth factor/scatter factor pathway. J Exp Med 1997; 185: 2121-2131. (Pubitemid 27265996)
51. Galimi F, Cottone E, Vigna E, Arena N, Boccaccio C, Giordano S et al. Hepatocyte growth factor is a regulator of monocyte-macrophage function. J Immunol 2001; 166: 1241-1247. (Pubitemid 32060285)
52. Benkhoucha M, Santiago-Raber M-L, Schneiter G, Chofflon M, Funakoshi H, Nakamura T et al. Hepatocyte growth factor inhibits CNS autoimmunity by inducing tolerogenic dendritic cells and CD25+Foxp3+ regulatory T cells. Proc Natl Acad Sci USA 2010; 107: 6424-6429.
53. Coudriet GM, He J, Trucco M, Mars WM, Piganelli JD. Hepatocyte growth factor modulates interleukin-6 production in bone marrow derived macrophages: implications for inflammatory mediated diseases. PLoS ONE 2010; 5: e15384.
54. Ashwood P, Wakefield AJ. Immune activation of peripheral blood and mucosal CD3+ lymphocyte cytokine profiles in children with autism and gastrointestinal symptoms. J Neuroimmunol 2006; 173: 126-134.
55. Jyonouchi H, Geng L, Ruby A, Zimmerman-Bier B. Dysregulated innate immune responses in young children with autism spectrum disorders: their relationship to gastrointestinal symptoms and dietary intervention. Neuropsychobiology 2005; 51: 77-85. (Pubitemid 40522799)
56. Jyonouchi H, Geng L, Cushing-Ruby A, Quraishi H. Impact of innate immunity in a subset of children with autism spectrum disorders: a case control study. J Neuroinflammation 2008; 5: 52.
57. Molloy CA, Morrow AL, Meinzen-Derr J, Schleifer K, Dienger K, Manning-Courtney P et al. Elevated cytokine levels in children with autism spectrum disorder. J Neuroimmunol 2006; 172: 198-205. (Pubitemid 43277506)
58. Li X, Chauhan A, Sheikh AM, Patil S, Chauhan V, Li X-M et al. Elevated immune response in the brain of autistic patients. J Neuroimmunol 2009; 207: 111-116.
59. Gupta S, Aggarwal S, Rashanravan B, Lee T. Th1-and Th2-like cytokines in CD4+ and CD8+ T cells in autism. J Neuroimmunol 1998; 85: 106-109. (Pubitemid 28255444)
60. Croonenberghs J, Bosmans E, Deboutte D, Kenis G, Maes M. Activation of the inflammatory response system in autism. Neuropsychobiology 2002; 45: 1-6. (Pubitemid 34117721)
61. Emanuele E, Orsi P, Boso M, Broglia D, Brondino N, Barale F et al. Low-grade endotoxemia in patients with severe autism. Neurosci Lett 2010; 471: 162-165.