Perceived stress during pregnancy and the catechol-O-methyltransferase (COMT) rs165599 polymorphism impacts on childhood IQ

Cognition

Volumn 132, Issue 3, 2014, Pages 461-470

  Lamb, Yvette N ^a   Thompson, John M D ^a   Murphy, Rinki ^a   Wall, Clare ^a   Kirk, Ian J ^a   Morgan, Angharad R ^a   Ferguson, Lynnette R ^a   Mitchell, Edwin A ^a   Waldie, Karen E ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

Child development; Gene environment; Intelligence; Longitudinal; Maternal stress

Indexed keywords

CATECHOL METHYLTRANSFERASE; STRESS HORMONE; CATECHOL O-METHYLTRANSFERASE;

ALLELE; ARTICLE; BIRTH WEIGHT; CHILD; CHILD DEVELOPMENT; COGNITION; COGNITIVE DEVELOPMENT; DNA POLYMORPHISM; FEMALE; FETUS DEVELOPMENT; FOLLOW UP; GENETIC SUSCEPTIBILITY; GENOTYPE; GENOTYPE ENVIRONMENT INTERACTION; GESTATIONAL AGE; HETEROZYGOTE; HOMOZYGOTE; HUMAN; INTELLIGENCE QUOTIENT; MAJOR CLINICAL STUDY; MATERNAL AGE; MATERNAL STRESS; NERVE CELL DIFFERENTIATION; PERCEIVED STRESS SCALE; PREGNANCY; PRENATAL STRESS; PRESCHOOL CHILD; PRIORITY JOURNAL; PROGENY; SCHOOL CHILD; GENE-ENVIRONMENT INTERACTION; GENETICS; HUMANS; INTELLIGENCE; INTELLIGENCE TESTS; LONGITUDINAL STUDIES; MALE; POLYMORPHISM, SINGLE NUCLEOTIDE; PRENATAL EXPOSURE DELAYED EFFECTS; PSYCHOLOGY; STRESS, PSYCHOLOGICAL;

CATECHOL O-METHYLTRANSFERASE; CHILD; FEMALE; GENE-ENVIRONMENT INTERACTION; HUMANS; INTELLIGENCE; INTELLIGENCE TESTS; LONGITUDINAL STUDIES; MALE; POLYMORPHISM, SINGLE NUCLEOTIDE; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; STRESS, PSYCHOLOGICAL;

EID: 84902677319     PISSN: 00100277     EISSN: 18737838     Source Type: Journal    
DOI: 10.1016/j.cognition.2014.05.009     Document Type: Article

References (67)

1. Antonow-Schlorke I., Schwab M., Li C., Nathanielsz P.W. Glucocorticoid exposure at the dose used clinically alters cytoskeletal proteins and presynaptic terminals in the fetal baboon brain. Journal of Physiology 2003, 547:117-123. 10.1111/j.1469-7793.2003.00117.x.
2. Arnsten A.F.T. Stress signalling pathways that impair prefrontal cortex structure and function. Nature Reviews Neuroscience 2009, 10:410-422. 10.1038/nrn2648.
3. Barker D.J.P. In utero programming of chronic disease. Clinical Science 1998, 95:115-128. 10.1042/CS19980019.
4. Barnett J.H., Heron J., Goldman D., Jones P.B., Xu K. Effects of catechol-O-methyltransferase on normal variation of the cognitive function in children. American Journal of Psychiatry 2009, 166:909-916. 10.1176/appi.ajp.2009.08081251.
5. Barnett J.H., Heron J., Ring S.M., Golding J., Goldman D., Xu K., et al. Gender-specific effects of the catechol-O-methyltransferase val108/158met polymorphism on cognitive function in children. American Journal of Psychiatry 2007, 164:142-149. 10.1176/appi.ajp.164.1.142.
6. Barnett J.H., Scoriels L., Munafò M.R. Meta-analysis of the cognitive effects of the catechol-O-methyltransferase gene val158/108met polymorphism. Biological Psychiatry 2008, 64:137-144. 10.1016/j.biopsych.2008.01.005.
7. Bergman K., Sarkar P., O'Connor T.G., Modi N., Glover V. Maternal stress during infancy predicts cognitive ability and fearfulness in infancy. Journal of the American Academy of Child and Adolescent Psychiatry 2007, 46:1454-1463. 10.1097/chi.0b013e31814a62f6.
8. Beydoun H., Saftlas A.F. Physical and mental health outcomes of prenatal maternal stress in human and animal studies: A review of recent evidence. Paediatric and Perinatal Epidemiology 2008, 22:438-466. 10.1111/j.1365-3016.2008.00951.x.
9. Bilder R.M., Volavka J., Czobor P., Malhotra A.K., Kennedy J.L., Ni X., et al. Neurocognitive correlates of the COMT val158met polymorphism in chronic schizophrenia. Biological Psychiatry 2002, 52:701-707. 10.1016/S0006-3223(02.
10. Bliss T.V.P., Collingridge G.L. A synaptic model of memory: Long-term potentiation in the hippocampus. Nature 1993, 361:31-39. 10.1038//361031a0.
11. Bray N.J., Buckland P.R., Williams N.M., Williams H.J., Norton N., Owen M.J., et al. A haplotype implicated in schizophrenia susceptibility is associated with reduced COMT expression in human brain. American Journal of Human Genetics 2003, 73:152-161. 10.1086/376578.
12. Burdick K.E., Funke B., Goldberg J.F., Bates J.A., Jaeger J., Kucherlapati R., et al. COMT genotype increases risk for bipolar 1 disorder and influences neurocognitive performance. Bipolar Disorders 2007, 9:370-376. 10.1111/j.1399-5618.2007.00384.x.
13. Caspi A., Moffitt T.E. Gene-environment interactions in psychiatry: Joining forces with neuroscience. Nature Reviews Neuroscience 2006, 7:583-590. 10.1038/nrn1925.
14. Chan R.C.K., Chen R.Y.L., Chen E.Y.H., Hui T.C.K., Cheung E.F.C., Cheung H.K., et al. The differential clinical and neurocognitive profiles of COMT SNP rs165599 genotypes in schizophrenia. Journal of the International Neuropsychological Society 2005, 11:202-204. 10.1017/S1355617705050241.
15. Chen J., Lipska B.K., Halim N., Ma Q.D., Matsumoto M., Melhem S., et al. Functional analysis of genetic variation in catechol-O-methyltransferase (COMT): Effects on mRNA, protein, and enzyme activity in post-mortem human brain. American Journal of Human Genetics 2004, 75:807-821. 10.1086/425589.
16. Cohen S., Williamson G. Perceived stress in a probability sample of the United States. The Social Psychology of Health: Claremont Symposium on Applied Social Psychology 1988, 31-67. Sage, Newbury Park, CA. S. Spacapan, S. Oskamp (Eds.).
17. Cooke S.F., Bliss T.V.P. Plasticity in the human central nervous system. Brain 2006, 129:1659-1673. 10.1093/brain/awl082.
18. Davis E.P., Snidman N., Wadhwa P.D., Glynn L.M., Schetter C.D., Sandman C.A. Prenatal maternal depression and anxiety predict negative behavioural reactivity in infancy. Infancy 2004, 6:319-331. 10.1207/s15327078in0603_1.
19. de Frias C.M., Annerbrink K., Westberg L., Eriksson E., Adolfsson R., Nilsson L.-G. COMT gene polymorphism is associated with declarative memory in adulthood and old age. Behavior Genetics 2004, 34:533-539. 10.1023/B:BEGE.0000038491.06972.8c.
20. Diamond D.M., Rose G.M. Stress impairs LTP and hippocampal-dependent memory. Annals of the New York Academy of Sciences 1994, 746:411-414. 10.1111/j.1749-6632.1994.tb39271.x.
21. Dumontheil I., Roggeman C., Ziermans T., Peyrard-Janvid M., Matsson H., Kere J., et al. Influence of the COMT genotype on working memory and brain activity changes during development. Biological Psychiatry 2011, 70:222-229. 10.1016/j.biopsych.2011.02.027.
22. Durand G.M., Kovalchuk Y., Konnerth A. Long-term potentiation and functional synapse induction in developing hippocampus. Nature 1996, 381:71-75. 10.1038/381071a0.
23. Egan M.F., Goldberg T.E., Kolachana B.S., Callicott J.H., Mazzanti C.M., Straub R.E., et al. Effect of COMT Val108/158Met genotype on frontal lobe function and risk for schizophrenia. Proceedings of the National Academy of Sciences 2001, 98:6917-6922. 10.1073/pnas.111134598.
24. Finlay J.M., Zigmond M.J., Abercrombie E.D. Increased dopamine and norepinephrine release in medial prefrontal cortex induced by acute and chronic stress: Effects of diazepam. Neuroscience 1995, 64:619-628. 10.1016/0306-4522(94)00331-X.
25. Gabriel S., Ziaugra L., Tabbaa D. Unit 2.12 SNP genotyping using the Sequenom MassARRAY iPLEX platform. Current Protocols in Human Genetics 2009, 60:2.12.1-2.12.18. 10.1002/0471142905.hg0212s60.
26. Gaysina D., Xu M.K., Barnett J.H., Croudace T.J., Wong A., Richards M., et al. The catechol-O-methyltransferase (COMT) gene and cognitive function from childhood through adolescence. Biological Psychology 2013, 92:359-364. 10.1016/j.biopsycho.2012.11.007.
27. Giedd J.N. Structural magnetic resonance imaging of the adolescent brain. Annals of the New York Academy of Sciences 2004, 1021:77-85. 10.1196/annals.1308.009.
28. Glatt S.J., Faraone S.V., Tsuang M.T. Association between a functional catechol-O-methyltransferase gene polymorphism and schizophrenia: Meta-analysis of case-control and family-based studies. American Journal of Psychiatry 2003, 160:469-476. 10.1176/appi.ajp.160.3.469.
29. Glover V., O'Connor T.G., O'Donnell K. Prenatal stress and the programming of the HPA axis. Neuroscience and Biobehavioral Reviews 2010, 35:17-22. 10.1016/j.neubiorev.2009.11.008.
30. Huizink A.C., Robles de Medina P.G., Mulder E.J.H., Visser G.H.A., Buitelaar J.K. Stress during pregnancy is associated with developmental outcome in infancy. Journal of Child Psychology and Psychiatry 2003, 44:810-818. 10.1111/1469-7610.00166.
31. Kerr D.S., Huggett A.M., Abraham W.C. Modulation of hippocampal long-term potentiation and long-term depression by corticosteroid receptor activation. Psychobiology 1994, 22:123-133.
32. Kirschbaum C., Wolf O.T., May M., Wippich W., Hellhammer D.H. Stress- and treatment-induced elevations of cortisol levels associated with impaired declarative memory in healthy adults. Life Sciences 1996, 58:1475-1483. 10.1016/0024-3205(96)00118-X.
33. Kong F.Z., Peng Z.Z., Jiang T.Y., Hong X.H. An association study of COMT gene polymorphisms with schizophrenia. Zhonghua Yi Xue Yi Chuan Xue Za Zhi 2011, 28:208-211. 10.3760/cma.j.issn.1003-9406.2011.02019.
34. Kostović I., Judaš M., Petanjek Z., Šimić G. Ontogenesis of goal-directed behaviour: Anatomo-functional considerations. International Journal of Psychophysiology 1995, 19:85-102. 10.1016/0167-8760(94)00081-O.
35. Lachman, H.M., Papolos, D.F., Saito, T., Yu, Y.-M., Szumlanski, C.L., & Weinshilboum, R.M. (1996). Human catechol-O-methyltransferase pharmacogenetics: Description of a functional polymorphism and its potential application to neuropsychiatric disorders. Pharmacogenetics, 6, 243-250. <> Retrieved. http://ovidsp.tx.ovid.com.
36. LaPlante D.P., Barr R.G., Brunet A., Du Fort G.G., Meaney M.L., Saucier J.-F., et al. Stress during pregnancy affects general intellectual and language functioning in human toddlers. Pediatric Research 2004, 56:400-410. 10.1203/01.PDR.0000136281.34035.44.
37. LaPlante D.P., Brunet A., Schmitz N., Ciampi A., King S. Project ice storm: Prenatal maternal stress affects cognitive and linguistic functioning in 51/2-year-old children. Journal of the American Academy of Child and Adolescent Psychiatry 2008, 47:1063-1072. 10.1097/CHI.0b013c31817eec80.
38. Luine V., Villegas M., Martinez C., McEwen B.S. Repeated stress causes reversible impairments of spatial memory performance. Brain Research 1994, 639:167-170. 10.1016/0006-8993(94)91778-7.
39. Lupien S.J., Gaudreau S., Tchiteya B.M., Maheu F., Sharma S., Nair N.P.V., et al. Stress-induced declarative memory impairments in healthy elderly subjects: Relationship to cortisol reactivity. Journal of Clinical Endocrinology and Metabolism 1997, 82:2070-2075. 10.1210/jc.82.7.2070.
40. Malhotra A.K., Kestler L.J., Mazzanti C., Bates J.A., Goldberg T., Goldman D. A functional polymorphism in the COMT gene and performance on a test of prefrontal cognition. American Journal of Psychiatry 2002, 159:652-654. 10.1176/appi.ajp.159.4.652.
41. Maroun, M., & Richter-Levin, G. (2003). Exposure to acute stress blocks the induction of long-term potentiation of the amygdala-prefrontal cortex pathway in vivo. Journal of Neuroscience, 23, 4406-4409. <> Retrieved. http://www.jneurosci.org.
42. McAllister A.K. Dynamic aspects of synapse formation. Annual Review of Neuroscience 2007, 30:425-450. 10.1146/annurev.neuro.29.051605.112830.
43. Mrzljak L., Uylings H.B.H., Kostovic I., Van Eden C. Prenatal development of neurons in the human prefrontal cortex: 1. A qualitative golgi study. Journal of Comparative Neurology 1988, 271:355-386. 10.1002/cne.902710306.
44. O'Connor T.G., Heron J., Golding J., Beveridge M., Glover V. Maternal antenatal anxiety and children's behavioural/emotional problems at 4years: Report from the Avon longitudinal study of parents and children. The British Journal of Psychiatry 2002, 180:502-508. 10.1192/bjp.180.6.502.
45. Okochi T., Ikeda M., Kishi T., Kawashima K., Kinoshita Y., Kitajima T., et al. Meta-analysis of association between genetic variants in COMT and schizophrenia: An update. Schizophrenia Research 2009, 110:140-148. 10.1016/j.schres.2009.02.019.
46. Oswald L.M., McCaul M., Choi L., Yang X., Wand G.S. Catechol-O-methyltransferase polymorphism alters hypothalamic-pituitary-adrenal axis responses to naloxone: A preliminary report. Biological Psychiatry 2004, 55:102-105. 10.1016/j.biopsych.2003.07.003.
47. Pianta R.C., Egeland B. Predictors of instability in children's mental test performance at 24, 48 and 96months. Intelligence 1994, 18:145-163. 10.1016/0160-2896(94)90025-6.
48. Rice F., Harold G.T., Boivin J., van den Bree M., Hay D.F., Thapar A. The links between prenatal stress and offspring development and psychopathology: Disentangling environmental and inherited influences. Psychological Medicine 2010, 40:335-445. 10.1017/S0033291709005911.
49. Roberti J.W., Harrington L.N., Storch E.A. Further psychometric support for the 10-item version of the perceived stress scale. Journal of College Counseling 2005, 9:135-147. 10.1002/j.2161-1882.2006.tb00100.x.
50. Shifman S., Bronstein M., Sternfeld M., Pisanté-Shalom A., Lev-Lehman E., Weizman A., et al. A highly significant association between a COMT haplotype and schizophrenia. American Journal of Human Genetics 2002, 71:1296-1302. 10.1086/344514.
51. Shors T.J., Gallegos R.A., Breindl A. Transient and persistent consequences of acute stress on long-term potentiation (LTP), synaptic efficacy, theta rhythms and bursts in area CA1 of the hippocampus. Synapse (New York, N.Y.) 1997, 26:209-217. 10.1002/(SICI)1098-2396(199707.
52. Snider S.R., Kuchel O. Dopamine: An important neurohormone of the sympathoadrenal system. Significance of increased peripheral dopamine release for the human stress response and hypertension. Endocrine Reviews 1983, 4:291-309. 10.1210/edrv-4-3-291.
53. Soronen P., Silander K., Antila M., Palo O.M., Tuulio-Henriksson A., Kieseppa T., et al. Association of a nonsynonymous variant of DAOA with visiospatial ability in a bipolar family sample. Biological Psychiatry 2008, 64:438-442. 10.1016/j.biopsych.2008.03.028.
54. Talge N.M., Neal C., Glover V. Antenatal maternal stress and long-term effects on child neurodevelopment: How and why?. Journal of Child Psychology and Psychiatry 2007, 48(3):245-261. 10.1111/j.1469-7610.2006.01714.x.
55. Thompson J.M.D., Clark P.M., Robinson E., Becroft D.M.O., Pattison N.S., Glavish N., et al. Risk factors for small-for-gestational-age babies: The Auckland birthweight collaborative study. Journal of Paediatrics and Child Health 2001, 37:369-375. 10.1046/j.1440-1754.2001.00684.x.
56. Thompson J.M.D., Sonuga-Barke E.J., Morgan A.R., Cornforth C.M., Turic D., Ferguson L.R., et al. The catechol-O-methyltransferase (COMT) Val158Met polymorphism moderates the effect of antenatal stress on childhood behavioural problems: Longitudinal evidence across multiple ages. Developmental Medicine and Child Neurology 2012, 54:148-154. 10.1111/j.1469-8749.2011.04129.x.
57. Tsigos C., Chrousos G.P. Hypothalamic-pituitary-adrenal axis, neuroendocrine factors and stress. Journal of Psychosomatic Research 2002, 53:865-871. 10.1016/S0022-3999(02)00429-4.
58. Van den Bergh B.R.H., Marcoen A. High antenatal maternal anxiety is related to ADHD symptoms, externalising problems, and anxiety in 8- and 9-year-olds. Child Development 2004, 75:1085-1097. 10.1111/j.1467-8624.2004.00727.x.
59. Van den Bergh B.R.H., Mennes M., Oosterlaan J., Stevens V., Stiers P., Marcoen A., et al. High antenatal maternal anxiety is related to impulsivity during performance on cognitive tasks in 14- and 15-year-olds. Neuroscience and Biobehavioral Reviews 2005, 29:259-269. 10.1016/j.neubiorev.2004.10.010.
60. Van den Bergh B.R.H., Mulder E.J.H., Mennes M., Glover V. Antenatal maternal anxiety and stress and the neurobehavioural development of the fetus and child: Links and possible mechanisms. A review. Neuroscience and Biobehavioral Reviews 2005, 29:237-258. 10.1016/j.neubiorev.2004.10.007.
61. Walder D.J., Trotman H.D., Cubells J.F., Brasfield J., Tang Y., Walker E.F. Catechol-O-methyltransferase (COMT) modulation of cortisol secretion in psychiatrically at-risk and healthy adolescents. Psychiatric Genetics 2010, 20:166-170. 10.1097/YPG.0b013e32833a1ff3.
62. Wechsler D. Wechsler Intelligence Scale for Children 1991, Psychological Corporation, New York, NY. 3rd ed.
63. Wechsler D. WASI Manual 1999, Psychological Corporation, San Antonio.
64. Wong E.Y.H., Herbert J. Raised circulating corticosterone inhibits neuronal differentiation of progenitor cells in the adult hippocampus. Neuroscience 2006, 137:83-92. 10.1016/j.neuroscience.2005.08.073.
65. Xu T.-X., Sotnikova T.D., Liang C., Zang J., Jung J.U., Spealman R.D., et al. Hyperdopaminergic tone erodes prefrontal long-term potential via a D2 receptor-operated protein phosphatase gate. Journal of Neuroscience 2009, 17:8528-8535. 10.1523/JNEUROSCI.0974-09.2009.
66. Young E.A., Abelson J.L., Cameron O.G. Interaction of brain noradrenergic system and the hypothalamic-pituitary-adrenal (HPA) axis in man. Psychoneuroendocrinology 2005, 30:807-814. 10.1016/j.psyneuen.2005.03.009.
67. Zubieta J.-K., Heitzeg M.M., Smith Y.R., Bueller J.A., Xu K., Xu Y., et al. COMT val158met genotype affects mu-opioid neurotransmitter responses to a pain stressor. Science 2003, 299:1240-1243. 10.1126/science.1078546.