Maternal serotonin transporter genotype affects risk for ASD with exposure to prenatal stress

Autism Research

Volumn 9, Issue 11, 2016, Pages 1151-1160

  Hecht, Patrick M ^a,b,f   Hudson, Melissa ^c   Connors, Susan L ^d,g   Tilley, Michael R ^e   Liu, Xudong ^c   Beversdorf, David Q ^a,b  

^a UNIVERSITY OF MISSOURI   (United States)

^b University of Missouri   (United States)

^c QUEEN S UNIVERSITY   (Canada)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

^e Central Methodist University   (United States)

^f UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^g UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

autism spectrum disorders; development; environmental influences; prenatal stress; serotonin; stress

Indexed keywords

SEROTONIN TRANSPORTER; SLC6A4 PROTEIN, HUMAN;

ADULT; ARTICLE; AUTISM; CHILD; COHORT ANALYSIS; CONTROLLED STUDY; DISEASE REGISTRY; ENVIRONMENTAL STRESS; FEMALE; GENE AMPLIFICATION; GENE FREQUENCY; GENETIC POLYMORPHISM; GENETIC SUSCEPTIBILITY; GENETIC VARIABILITY; GENOTYPE; HOMOZYGOSITY; HUMAN; MAJOR CLINICAL STUDY; MALE; MATERNAL AGE; PRENATAL STRESS; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN PROTEIN INTERACTION; RISK ASSESSMENT; STRESS; ALLELE; COMPLICATION; GENETICS; MENTAL STRESS; MOTHER; PREGNANCY; PRENATAL EXPOSURE; PSYCHOLOGY; RISK;

ADULT; ALLELES; AUTISM SPECTRUM DISORDER; CHILD; FEMALE; GENOTYPE; HUMANS; MOTHERS; POLYMORPHISM, GENETIC; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RISK; SEROTONIN PLASMA MEMBRANE TRANSPORT PROTEINS; STRESS, PSYCHOLOGICAL;

EID: 84963968530     PISSN: 19393792     EISSN: 19393806     Source Type: Journal    
DOI: 10.1002/aur.1629     Document Type: Article

References (53)

1. American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders, 5th ed. Washington: American Psychiatric Association.
2. Anderson, G.M., Horne, W.C., Chatterjee, D., & Cohen, D.J. (1990). The hyperserotonemia of autism. Annals of the New York Academy of Science, 600, 331–340; discussion 341-332.
3. Bengel, D., Murphy, D.L., Andrews, A.M., Wichems, C.H., Feltner, D., Heils, A., et al. (1998). Altered brain serotonin homeostasis and locomotor insensitivity to 3, 4-methylenedioxymethamphetamine (“Ecstasy”) in serotonin transporter-deficient mice. Molecular Pharmacology, 53(4), 649–655.
4. Beversdorf, D.Q., Manning, S.E., Hillier, A., Anderson, S.L., Nordgren, R.E., Walters, S.E., et al. (2005). Timing of prenatal stressors and autism. Journal of Autism and Developmental Disorders, 35(4), 471–478.
5. Braunschweig, D., Krakowiak, P., Duncanson, P., Boyce, R., Hansen, R.L., Ashwood, P., et al. (2013). Autism-specific maternal autoantibodies recognize critical proteins in developing brain. Translational Psychiatry, 3:e277. doi: 10.1038/tp.2013.50.
6. Canli, T., & Lesch, K.P. (2007). Long story short: the serotonin transporter in emotion regulation and social cognition. Nature Neuroscience, 10(9), 1103–1109.
7. Caspi, A., Sugden, K., Moffitt, T.E., Taylor, A., Craig, I.W., Harrington H., et al. (2003). Influence of life stress on depression: moderation by a polymorphism in the 5-HTT gene. Science, 301(5631), 386–389.
8. Class, Q.A., Abel, K.M., Khashan, A.S., Rickert, M.E., Dalman, C., Larsson, H., et al. (2014). Offspring psychopathology following preconception, prenatal and postnatal maternal bereavement stress. Psychological Medicine, 44(1), 71–84.
9. Cohen, I.L., Schmidt-Lackner, S., Romanczyk, R., & Sudhalter, V. (2003). The PDD Behavior Inventory: a rating scale for assessing response to intervention in children with pervasive developmental disorder. Journal of Autism Developmental Disorders, 33(1), 31–45.
10. Conroy, J., Meally, E., Kearney, G., Fitzgerald, M., Gill, M., & Gallagher, L. (2004). Serotonin transporter gene and autism: a haplotype analysis in an Irish autistic population. Molecular Psychiatry, 9(6), 587–593.
11. Cook, E.H., Jr., Courchesne, R., Lord, C., Cox, N.J., Yan, S., Lincoln, A., et al. (1997). Evidence of linkage between the serotonin transporter and autistic disorder. Molecular Psychiatry, 2(3), 247–250.
12. Devlin, B., Cook, E.H., Jr., Coon, H., Dawson, G., Grigorenko, E.L., McMahon, W., et al. (2005). Autism and the serotonin transporter: the long and short of it. Molecular Psychiatry, 10(12), 1110–1116.
13. Domschke, K., & Dannlowski, U. (2010). Imaging genetics of anxiety disorders. NeuroImage, 53(3), 822–831.
14. Hariri, A.R., Mattay, V.S., Tessitore, A., Kolachana, B., Fera, F., Goldman, D., et al. (2002). Serotonin transporter genetic variation and the response of the human amygdala. Science, 297(5580), 400–403.
15. Heils, A., Teufel, A., Petri, S., Stober, G., Riederer, P., Bengel, D., & Lesch, K.P. (1996). Allelic variation of human serotonin transporter gene expression. Journal of Neurochemistry, 66(6), 2621–2624.
16. Hoffmann, T.J., Windham, G.C., Anderson, M., Croen, L.A., Grether, J.K., & Risch, N. (2014). Evidence of reproductive stoppage in families with autism spectrum disorder: a large, population-based cohort study. JAMA Psychiatry. 71(8), 943–951.
17. Holmes, T.H., & Rahe, R.H. (1967). The Social Readjustment Rating Scale. Journal of Psychosomatic Research, 11(2), 213–218.
18. Hu, X.Z., Lipsky, R.H., Zhu, G., Akhtar, L.A., Taubman, J., Greenberg, B.D., et al. (2006). Serotonin transporter promoter gain-of-function genotypes are linked to obsessive-compulsive disorder. American Journal of Human Genetics, 78, 815–826.
19. Hyde, L.W., Bogdan, R., & Hariri, A.R. (2011). Understanding risk for psychopathology through imaging gene-envionment interactions. Trends in Cognitive Sciences, 15(9), 417–427.
20. Jones, K.L., Smith, R.M., Edwards, K.S., Givens, B., Tilley, M.R., & Beversdorf, D.Q. (2010). Combined effect of maternal serotonin transporter genotype and prenatal stress in modulating offspring social interaction in mice. International Journal of Developmental Neuroscience, 28(6), 529–536.
21. Karg, K., Burmeister, M., Shedden, K., & Sen, S. (2011). The serotonin transporter promoter variant (5-HTTLPR), stress, and depression meta-analysis revisited: evidence of genetic moderation. Archives of General Psychiatry, 68(5), 444–454.
22. King, S., & Laplante, D.P. (2005). The effects of prenatal maternal stress on children's cognitive development: Project Ice Storm. Stress, 8(1), 35–45.
23. Kinney, D.K., Miller, A.M., Crowley, D.J., Huang, E., & Gerber, E. (2008). Autism prevalence following prenatal exposure to hurricanes and tropical storms in Louisiana. Journal of Autism and Developmental Disorders, 38(3), 481–488.
24. Klauck, S.M., Poustka, F., Benner, A., Lesch, K.P., & Poustka, A. (1997). Serotonin transporter (5-HTT) gene variants associated with autism? Human Molecular Genetics, 6(13), 2233–2238.
25. Lanfumey, L., Mannoury La Cour, C., Froger, N., & Hamon, M. (2000). 5-HT-HPA interactions in two models of transgenic mice relevant to major depression. Neurochemical Research, 25(9-10), 1199–1206.
26. Lee, H.J., Lee, M.S., Kang, R.H., Kim, H., Kim, S.D., Kee, B.S., et al. (2005) Influence of the serotonin transporter promoter gene polymorphism on susceptibility to posttraumatic stress disorder. Depression and Anxiety, 21(3), 135–139.
27. Lesch, K.P., Bengel, D., Heils, A., Sabol, S.Z., Greenberg, B.D., Petri, S., et al. (1996). Association of anxiety-related traits with a polymorphism in the serotonin transporter gene regulatory region. Science, 274(5292), 1527–1531.
28. Li, J., Vestergaard, M., Obel, C., Christensen, J., Precht, D.H., Lu, M. & Olsen, J. (2009). A nationwide study on the risk of autism after prenatal stress exposure to maternal bereavement. Pediatrics, 123(4), 1102–1107.
29. Li, Q. (2006). Cellular and molecular alterations in mice with deficient and reduced serotonin transporters. Molecular Neurobiology, 34(1), 51–66.
30. Lord, C., Rutter, N., Goode, S., Heemsbergen, J., Jordan, H., Mawhood, L., & Schopler, E. (1989). Autism diagnostic observation schedule: a standardized observation of communicative and social behavior. Journal of Autism and Developmental Disorders, 19, 185–212.
31. Lord, C., Rutter, N., & LeCouteur, A. (1994). Autism Diagnostic Interview-Revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. Journal of Autism and Developmental Disorders, 24, 659–685.
32. MacKenzie, A., & Quinn, J. (1999). A serotonin transporter gene intron 2 polymorphic region, correlated with affective disorders, has allele-dependent differential enhancer-like properties in the mouse embryo. Proceedings National Academy of Science U.S.A. 96, 15251−15255.
33. McCauley, J.L., Olson, L.M., Dowd, M., Amin, T., Steele, A., Blakely, R.D., et al. (2004). Linkage and association analysis at the serotonin transporter (SLC6A4) locus in a rigid-compulsive subset of autism. American Journal of Medical Genetics, Part B, Neuropsychiatric Genetics, 127B(1), 104–112.
34. Miller, R., Wankerl, M., Stalder, T., Kirschbaum, C., & Alexander, N. (2013). The serotonin transporter gene-linked polymorphic region (5-HTTLPR) and cortisol stress reactivity: a meta-analysis. Molecular Psychiatry, 18(9), 1018–1024.
35. Murphy, D.L., Maile, M.S., & Vogt, N.M. (2013). 5HTTLPR: White Knight or Dark Blight? American Chemical Society: Chemical Neuroscience, 4(1), 13–15.
36. Noskova, T., Pivac, N., Nedic, G., Kazantseva, A., Gaysina, D., Faskhutdinova, G., et al. (2008). Ethnic differences in the serotonin transporter polymorphism (5-HTTLPR) in several European populations. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 32(7), 1735–1739.
37. Odgerel, Z., Talati, A., Hamilton, S.P., Levinson, D.F., & Weissman, M.M. (2013). Genotyping serotonin transporter polymorphisms 5-HTTLPR and rs25531 in European- and African-American subjects from the National Institute of Mental Health's Collaborative Center for Genomic Studies. Translational Psychiatry, 3, e307.
38. Olsson, A., Kross, E., Nordberg, S.S., Weinberg, A., Weber, J., Schmer-Galunder, S., et al. (2015). Neural and genetic markers of vulnerability to post-traumatic stress symptoms among survivors of the World Trade Center attacks. Social Cognitive and Affective Neuroscience, 10(6), 863–868. doi:10.1093/scan/nsu125.
39. Perez, X.A., & Andrews, A.M. (2005). Chronoamperometry to determine differential reductions in uptake in brain synaptosomes from serotonin transporter knockout mice. Analytical Chemistry, 77(3), 818–826.
40. Prasad, H.C., Zhu, C.B., McCauley, J.L., Samuvel, D.J., Ramamoorthy, S., Shelton, R.C., Hewlett, W.A., et al. (2005). Human serotonin transporter variants display altered sensitivity to protein kinase G and p38 mitogen-activated protein kinase. Proceedings of the National Academy of Sciences of the USA, 102(32), 11545–11550.
41. Rhodes, R.A., Murthy, N.V., Dresner, M.A., Selvaraj, S., Stavrakakis, N., Babar, S., et al. (2007). Human 5-HT transporter availability predicts amygdala reactivity in vivo. Journal of Neuroscience, 27(34), 9233–9237.
42. Sandin, S., Lichtenstein, P., Kuja-Halkola, R., Larsson, H., Hultman, C.M., & Reichenberg, A. (2014). The familial risk of autism. Journal of the American Medical Association, 311(17), 1770–1777.
43. Sen, S., Burmeister, M., & Ghosh, D. (2004). Meta-analysis of the association between a serotonin transporter promoter polymorphism (5-HTTLPR) and anxiety-related personality traits. American Journal of Medical Genetics, Part B, Neuropsychiatric Genetics, 127B(1), 85–89.
44. Sodhi, M.S., & Sanders-Bush, E. (2004). Serotonin and brain development. International Review of Neurobiology, 59, 111–174.
45. Sutcliffe, J.S., Delahanty, R.J., Prasad, H.C., McCauley, J.L., Han, Q., Jiang, L., et al. (2005). Allelic heterogeneity at the serotonin transporter locus (SLC6A4) confers susceptibility to autism and rigid-compulsive behaviors. American Journal of Medical Genetics, 77(2), 265–279.
46. van den Hove, D.L., Jakob, S.B., Schraut, K.G., Kenis, G., Schmitt, A.G., Kneitz, S., et al. (2011). Differential effects of prenatal stress in 5-Htt deficient mice: towards molecular mechanisms of gene x environment interactions. PloS One, 6(8), e22715.
47. Ward, A.J. (1990). A comparison and analysis of the presence of family problems during pregnancy of mothers of “autistic” children and mothers of normal children. Child Psychiatry and Human Development, 20(4), 279–288.
48. Warren, R.P., & Singh, V.K. (1996). Elevated serotonin levels in autism: association with the major histocompatibility complex. Neuropsychobiology, 34(2), 72–75.
49. Wendland, J.R., Martin, B.J., Kruse, M.R., Lesch, K.P., & Murphy, D.L. (2006). Simultaneous genotyping of four functional loci of human SLC6A4, with a reappraisal of 5-HTTLPR and rs25531. Molecular Psychiatry, 11(3), 224–226.
50. Wendland, J.R., Moya, P.R., Kruse, M.R., Ren-Patterson, R.F., Jensen, C.L., Timpano, K.R., et al. (2008). A novel, putative gain-of-function haplotype at SLC6A4 associates with obsessive-compulsive disorder. Human Molecular Genetics. 17, 717−723.
51. Whitaker-Azmitia, P.M. (2001). Serotonin and brain development: role in human developmental diseases. Brain Research Bulletin, 56(5), 479–485.
52. Yirmiya, N., Pilowsky, T., Nemanov, L., Arbelle, S., Feinsilver, T., Fried, I., & Ebstein, R.P. (2001). Evidence for an association with the serotonin transporter promoter region polymorphism and autism. American Journal of Medical Genetics, 105(4), 381–386.
53. Zalsman, G., Huang, Y.Y., Oquendo, M.A., Burke, A.K., Hu, X.Z., Brent, D.A., et al. (2006). Association of a triallelic serotonin transporter gene promoter region (5-HTTLPR) polymorphism with stressful life events and severity of depression. American Journal of Psychiatry, 163(9), 1588–1593.