A latent modeling approach to genotype-phenotype relationships: Maternal problem behavior clusters, prenatal smoking, and MAOA genotype

Archives of Women's Mental Health

Volumn 15, Issue 4, 2012, Pages 269-282

  McGrath, L M ^a   Mustanski, B ^b   Metzger, A ^c   Pine, D S ^d   Kistner Griffin, E ^e   Cook, E ^f   Wakschlag, L S ^b  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b NORTHWESTERN UNIVERSITY   (United States)

^c WEST VIRGINIA UNIVERSITY   (United States)

^d NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^e MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^f UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

Antisocial behavior; Female problem behavior; Gene environment interaction; Monoamine oxidase A (MAOA); Prenatal smoking

Indexed keywords

AMINE OXIDASE (FLAVIN CONTAINING) ISOENZYME A;

AGGRESSION; ANTISOCIAL BEHAVIOR; ARTICLE; BEHAVIOR DISORDER; CONTROLLED STUDY; DISEASE ASSOCIATION; FEMALE; GENE; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC POLYMORPHISM; GENETIC RISK; GENOTYPE ENVIRONMENT INTERACTION; GENOTYPE PHENOTYPE CORRELATION; GENOTYPING TECHNIQUE; HUMAN; IMPULSIVENESS; MAJOR CLINICAL STUDY; MATERNAL SMOKING; MATHEMATICAL COMPUTING; MATHEMATICAL MODEL; MONOAMINE OXIDASE A GENE; PRIORITY JOURNAL; PROSPECTIVE STUDY; RISK ASSESSMENT; RISK FACTOR; STRUCTURAL EQUATION MODELING; SUBSTANCE ABUSE; SYNDROME DELINEATION;

ADOLESCENT; ADULT; ANTISOCIAL PERSONALITY DISORDER; CHILD; CHILD ABUSE; FACTOR ANALYSIS, STATISTICAL; FEMALE; GENE-ENVIRONMENT INTERACTION; GENETIC ASSOCIATION STUDIES; GENOTYPE; HUMANS; MATERNAL BEHAVIOR; MODELS, THEORETICAL; MONOAMINE OXIDASE; MULTIVARIATE ANALYSIS; PHENOTYPE; POLYMORPHISM, GENETIC; PREGNANCY; PROSPECTIVE STUDIES; QUESTIONNAIRES; SMOKING;

EID: 84865410559     PISSN: 14341816     EISSN: 14351102     Source Type: Journal    
DOI: 10.1007/s00737-012-0286-y     Document Type: Article

References (80)

1. Arbuckle JL (2007a) Amos 16.0 User's Guide. SPSS, Chicago
2. Arbuckle JL (2007b) Amos (version 16.0). SPSS, Chicago
3. Aslund C, Nordquist N, Comasco E, Leppert J, Oreland L, Nilsson KW (2011) Maltreatment, MAOA, and delinquency: sex differences in gene-environment interaction in a large population-based cohort ofadolescents. Behav Genet 41(2):262-272
4. Baler RD, Volkow ND, Fowler JS, Benveniste H (2008) Is fetal brain monoamine oxidase inhibition the missing link between maternal smoking and conduct disorders? J Psychiatry Neurosci 33 (3):187-195
5. Benjamin D, Van Bakel I, Craig IW (2000) A novel expression based approach for assessing the inactivation status of human X-linked genes. Eur J Hum Genet 8(2):103-108
6. Bernstein DP, Fink L, Handelsman L, Foote J, Lovejoy M, Wenzel K, Sapareto E, Ruggiero J (1994) Initial reliability and validity of a new retrospective measure of child abuse and neglect. Am J Psychiatry 151(8):1132-1136
7. Bloss CS, Schiabor KM, Schork NJ (2010) Human behavioral informatics in genetic studies ofneuropsychiatric disease: multivariate profile-based analysis. Brain Res Bull 83(3-4):177-188
8. Buckholtz JW, Meyer-Lindenberg A (2008) MAOA and the neurogenetic architecture of human aggression. Trends Neurosci 31 (3):120-129
9. Byrne BM (2004) Testing for multigroup invariance using AMOS graphics: a road less traveled structural equation modeling. A Multidiscip J 11(2):272-300
10. Carrel L, Willard HF (2005) X-inactivation profile reveals extensive variability in X-linked gene expression in females. Nature 434 (7031):400-404
11. Caspi A, McClay J, Moffitt TE, Mill J, Martin J, Craig IW, Taylor A, Poulton R (2002) Role of genotype in the cycle of violence in maltreated children. Science 297(5582):851-854
12. Caspi A, Hariri AR, Holmes A, Uher R, Moffitt TE (2010) Genetic sensitivity to the environment: the case of the serotonin transporter gene and its implications for studying complex diseases and traits. Am J Psychiatry 167(5):509-527
13. Chakravorty SG, Halbreich U (1997) The influence of estrogen on monoamine oxidase activity. Psychopharmacol Bull 33 (2):229-233
14. Costa PT Jr, McCrae RR (1997) Longitudinal stability of adult person-ality. In: Hogan R, Johnson JA, Briggs SR (eds) Handbook of personality psychology Academic Press, San Diego, pp 269-290
15. Deckert J, Catalano M, Syagailo YV, Bosi M, Okladnova O, Di Bella D, Nothen MM, Maffei P, Franke P, Fritze J, Maier W, Propping P, Beckmann H, Bellodi L, Lesch KP (1999) Excess ofhigh activity monoamine oxidase A gene promoter alleles in female patients with panic disorder. Hum Mol Genet 8(4):621-624
16. D'Onofrio BM, Van Hulle CA, Waldman ID, Rodgers JL, Harden KP, Rathouz PJ, Lahey BB (2008) Smoking during pregnancy and offspring externalizing problems: an exploration of genetic and environmental confounds. Dev Psychopathol 20(1):139-164
17. D'Onofrio BM, Singh AL, Iliadou A, Lambe M, Hultman CM, Grann M, Neiderhiser JM, Langstrom N, Lichtenstein P (2010) Familial confounding of the association between maternal smoking during pregnancy and offspring criminality: a population-based study in Sweden. Arch Gen Psychiatry 67(5):529-538
18. Ducci F, Enoch MA, Hodgkinson C, Xu K, Catena M, Robin RW, Goldman D (2008) Interaction between a functional MAOA locus and childhood sexual abuse predicts alcoholism and antisocial personality disorder in adult women. Mol Psychia-try 13(3):334-347
19. Dukic VM, Niessner M, Benowitz N, Hans S, Wakschlag L (2007) Modeling the relationship of cotinine and self-reported measures ofmaternal smoking during pregnancy: a deterministic approach. Nicotine Tob Res 9(4):453-465
20. Duncan LE, Keller MC (2011)A critical review of the first 10 years of candidate gene-by-environment interaction research in psychiatry. Am J Psychiatry 168(10):1041-1049. doi:10.1176/appi.ajp.2011.11020191
21. Fergusson DM, Horwood LJ, Ridder EM (2005) Show me the child at seven: the consequences of conduct problems in childhood for psychosocial functioning in adulthood. J Child Psychol Psychiatr 46(8):837-849
22. Ferreira MA, Purcell SM (2009) A multivariate test of association. Bioinformatics 25(1):132-133
23. Fontaine N, Carbonneau R, Vitaro F, Barker ED, Tremblay RE (2009) Research review: a critical review of studies on the developmental trajectories of antisocial behavior in females. J Child Psychol Psychiatry 50(4):363-385
24. Frazzetto G, Di Lorenzo G, Carola V, Proietti L, Sokolowska E, Siracusano A, Gross C, Troisi A (2007) Early trauma and in-creased risk for physical aggression during adulthood: the mod-erating role of MAOA genotype. PLoS One 2(5):e486
25. Gilman SE, Gardener H, Buka SL (2008) Maternal smoking during pregnancy and children's cognitive and physical development: a causal risk factor? Am J Epidemiol 168(5):522-531
26. Hall MH, Smoller JW (2010) A new role for endophenotypes in the GWAS era: functional characterization ofriskvariants. Harv Rev Psychiatry 18(1):67-74
27. Hanrahan JP, Tager IB, Segal MR, Tosteson TD, Castile RG, Van Vunakis H, Weiss ST, Speizer FE (1992) The effect ofmaternal smoking during pregnancy on early infant lung function. Am Rev Respir Dis 145(5):1129-1135
28. Hendriks RW, Chen ZY, Hinds H, Schuurman RK, Craig IW (1992) An X chromosome inactivation assay based on differential meth-ylation of a CpG island coupled to a VNTR polymorphism at the 5' end of the monoamine oxidase A gene. Hum Mol Genet 1 (3):187-194
29. Hetherington EM, Clingempeel WG, Anderson ER, Deal JE, Hagan MS, Hollier EA, Lindner MS (1992) Coping with marital transi-tions: a family systems perspective. Monogr Soc Res Child Dev 57(2/3)
30. Houle D, Govindaraju DR, Omholt S (2010) Phenomics: the next challenge. Nat Rev Genet 11(12):855-866
31. Huang YY, Cate SP, Battistuzzi C, Oquendo MA, Brent D, Mann JJ (2004) An association between a functional polymorphism in the monoamine oxidase a gene promoter, impulsive traits and early abuse experiences. Neuropsychopharmacology 29(8):1498-1505
32. Jaffee SR, Belsky J, Harrington H, Caspi A, Moffitt TE (2006) When parents have a history of conduct disorder: how is the caregiving environment affected? J Abnorm Psychol 115(2):309-319
33. Jesor R, Jessor SL (1977) Problem behavior and psychosocial develop-ment: a longitudinal study ofyouth. Academic Press, New York
34. 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. Arch Gen Psychiatry. doi:10.1001/ archgenpsychiatry.2010.189
35. Keenan K, Wroblewski K, Hipwell A, Loeber R, Stouthamer-Loeber M (2010) Age ofonset, symptom threshold, and expansion of the nosology of conduct disorder for girls. J Abnorm Psychol 119 (4):689-698
36. Kerig PK (1996) Assessing the links between interparental conflict and child adjustment: the conflicts and problem-solving scales. J Fam Psychol 10(4):454-473
37. Kim-Cohen J, Caspi A, Taylor A, Williams B, Newcombe R, Craig IW, Moffitt TE (2006) MAOA, maltreatment, and gene-environment interaction predicting children's mental health: new evidence and ameta-analysis. Mol Psychiatry 11(10):903-913
38. Kline RB (2005) Principles and practice of structural equation model-ing, 2nd edn. Guilford Press, New York
39. Krueger RF, Hicks BM, Patrick CJ, Carlson SR, Iacono WG, McGue M (2002) Etiologic connections among substance dependence, antisocial behavior, and personality: modeling the externalizing spectrum. J Abnorm Psychol 111(3):411-424
40. Krueger RF, Markon KE, Patrick CJ, Benning SD, Kramer MD (2007) Linking antisocial behavior, substance use, and personality: an integrative quantitative model of the adult externalizing spectrum. JAbnormPsychol 116(4):645-666
41. Lange C, Silverman EK, Xu X, Weiss ST, Laird NM (2003) A multi-variate family-based association test using generalized estimating equations: FBAT-GEE. Biostatistics 4(2):195-206
42. Loeber R (1991) Antisocial behavior: more enduring than changeable? J Am Acad Child Adolesc Psychiatry 30(3):393-397
43. Loehlin JC (2004) Latent variable models, 4th edn. Lawrence Erlbaum Associates, Mahwah
44. Maughan B, Taylor A, Caspi A, Moffitt TE (2004) Prenatal smoking and early childhood conduct problems: testing genetic and envi-ronmental explanations of the association. Arch Gen Psychiatry 61(8):836-843
45. Medland SE, Neale MC (2010) An integrated phenomic approach to multivariate allelic association. Eur J Hum Genet 18(2):233-239
46. Middeldorp CM, Landt MC Slof-Op't, Medland SE, van Beijsterveldt CE, Bartels M, Willemsen G, Hottenga JJ, de Geus EJ, Suchiman E, Dolan CV, Neale MC, Slagboom PE, Boomsma DI (2010) Anxiety and depression in children and adults: influence ofseroto-nergic andneurotrophic genes? Genes Brain Behav 9(7):808-816
47. Moffitt TE, Caspi A, Rutter M, Silva PA (2001) Sex differences in antisocial behavior. Cambridge University Press, Cambridge
48. Munafo MR, Durrant C, Lewis G, Flint J (2009) Gene × environment interactions at the serotonin transporter locus. Biol Psychiatry 65 (3):211-219
49. Neale MC, Boker SM, Xie G, Maes HH (2002) Mx: statistical model-ing, 6th edn. Departmentt of Psychiatry, Virginia Commonwealth University, Richmond
50. Nilsson KW, Comasco E, Aslund C, Nordquist N, Leppert J, Oreland L (2011) MAOA genotype, family relations and sexual abuse in relation to adolescent alcohol consumption. Addict Biol 16 (2):347-355
51. Nordquist N, Oreland L (2006) Monoallelic expression of MAOA in skin fibroblasts. Biochem Biophys Res Commun 348(2):763-767
52. Ou XM, Chen K, Shih JC (2006) Glucocorticoid and androgen activation of monoamine oxidase A is regulated differently by R1 and Sp1. J Biol Chem 281(30):21512-21525
53. Plomin R, Haworth CM, Davis OS (2009) Common disorders are quantitative traits. Nat Rev Genet 10(12):872-878
54. Prom-Wormley EC, Eaves LJ, Foley DL, Gardner CO, Archer KJ, Wormley BK, Maes HH, Riley BP, Silberg JL (2009) Monoamine oxidase A and childhood adversity as risk factors for conduct disorder in females. Psychol Med 39(4):579-590
55. Risch N, Herrell R, Lehner T, Liang KY, Eaves L, Hoh J, Griem A, Kovacs M, Ott J, Merikangas KR (2009) Interaction between the serotonin transporter gene (5-HTTLPR), stressful life events, and risk ofdepression: a meta-analysis. JAMA 301(23):2462-2471
56. Roberts BW, Caspi A, Moffitt TE (2001) The kids are alright: growth and stability in personality development from adolescence to adulthood. J Pers Soc Psychol 81(4):670-683
57. Sabol SZ, Hu S, Hamer D (1998) A functional polymorphism in the monoamine oxidase A gene promoter. Hum Genet 103(3):273-279
58. Sakai JT, Boardman JD, Gelhorn HL, Smolen A, Corley RP, Huizinga D, Menard S, Hewitt JK, Stallings MC (2010) Using trajectory analyses to refine phenotype for genetic association: conduct problems and the serotonin transporter (5HTTLPR). Psychiatr Genet 20(5):199-206
59. Schulze TG, McMahon FJ (2004) Defining the phenotype in human genetic studies: forward genetics and reverse phenotyping. Hum Hered 58(3-4):131-138
60. Serbin LA, Stack DM, De Jenna M, Grunzeweig N, Temcheff CE, Schwartzman AE, Ledingham J (2004) When aggressive girls become mothers. In: Putallaz M, Bierman KL (eds) Aggression, antisocial behavior and violence among girls. Guilford Press, New York, pp 262-285
61. Silberg JL, Parr T, Neale MC, Rutter M, Angold A, Eaves LJ (2003) Maternal smoking during pregnancy and risk to boys' conduct disturbance: an examination of the causal hypothesis. Biol Psychiatry 53(2):130-135
62. Sjoberg RL, Nilsson KW, Wargelius HL, Leppert J, Lindstrom L, Oreland L (2007) Adolescent girls and criminal activity: role of MAOA-LPR genotype and psychosocial factors. Am J Med Genet B Neuropsychiatr Genet 144B(2):159-164
63. Skinner HA (1982) The drug abuse screening test. Addict Behav 7 (4):363-371
64. Sörbom D (1974) A general method for studying differences in factor means and factor structure between groups. Br J Mat Stat Psychol 27:229-239
65. Sullivan PF (2007) Spurious genetic associations. Biol Psychiatry 61 (10):1121-1126
66. Tager IB, Ngo L, Hanrahan JP (1995) Maternal smoking during pregnancy. Effects on lung function during the first 18 months of life. Am J Respir Crit Care Med 152(3):977-983
67. Thapar A, Rice F, Hay D, Boivin J, Langley K, van den Bree M, Rutter M, Harold G (2009) Prenatal smoking might not cause attention-deficit/hyperactivity disorder: evidence from a novel design. Biol Psychiatry 66(8):722-727
68. Wakschlag LS, Kistner EO, Pine DS, Biesecker G, Pickett KE, Skol AD, et al. (2010) Interaction of prenatal exposure to cigarettes and MAOA genotype in pathways to youth antisocial behavior Mol Psychiatry 15(9):928-937
69. Wakschlag LS, Pickett KE, Cook E Jr, Benowitz NL, Leventhal BL (2002) Maternal smoking during pregnancy and severe antisocial behavior in offspring: a review. Am J Public Health 92(6):966-974
70. Wakschlag LS, Pickett KE, Middlecamp MK, Walton LL, Tenzer P, Leventhal BL (2003) Pregnant smokers who quit, pregnant smok-ers who don't: does history of problem behavior make a differ-ence? Soc Sci Med 56(12):2449-2460
71. Wakschlag LS, Pickett KE, Kasza KE, Loeber R (2006) Is prenatal smoking associated with a developmental pattern of conduct problems in young boys? J Am Acad Child Adolesc Psychiatry 45(4):461-467
72. Wang X, Tager IB, Van Vunakis H, Speizer FE, Hanrahan JP (1997) Maternal smoking during pregnancy, urine cotinine concentra-tions, and birth outcomes. A prospective cohort study. Int J Epidemiol 26(5):978-988
73. Widom CS, Brzustowicz LM (2006) MAOA and the "cycle of violence:" childhood abuse and neglect, MAOA genotype, and risk for violent and antisocial behavior. Biol Psychiatry 60(7):684-689
74. Xue F, Tian XC, Du F, Kubota C, Taneja M, Dinnyes A, Dai Y, Levine H, Pereira LV, Yang X (2002) Aberrant patterns of X chromosome inactivation in bovine clones. Nat Genet 31(2):216-220
75. Zoccolillo M (1993) Gender and the development ofconduct disorder. Dev Psychopathol 5:65-78
76. Zoccolillo M, Paquette D, Azar R, Cote S, Tremblay RE (2004) Parenting as an important outcome of conduct disorder in girls. In: Putallaz M, Bierman KL (eds) Aggression, antisocial behavior and violence among girls. Guilford Press, New York, pp 242-261
77. Zuckerman M (1994) Impulsive unsocialized sensation seeking: the biological foundations of a basic dimension of personality. In: Bates JE, Wachs TD (eds) Temperament: individual differences at the interface of biology and behavior. American Psychological Association, Washington, DC
78. Zuckerman M (2002) An alternative five-factorial model. In: Raad BD, M. P (eds) Big Five Assessment. Hogrefe and Huber, Ashland, OH, pp. 377-396
79. Zucker RA, Noll RB, Ham HP, Fitzgerald HE, Sullivan LS (1994) Assessing antisociality with the Antisocial Behavior Checklist: Reliability and validity studies. (Unpublished manuscript)
80. Zung BJ (1982) Evaluation of the Michigan Alcoholism Screening Test (MAST) in assessing lifetime and recent problems. J Clin Psychol 38(2):425-439