20 ans après: A second mutation in MAOA identified by targeted high-throughput sequencing in a family with altered behavior and cognition

European Journal of Human Genetics

Volumn 22, Issue 6, 2014, Pages 776-783

  Piton, Aḿlie ^a,b   Poquet, H́lène ^c,d   Redin, Claire ^a,b   Masurel, Alice ^c   Lauer, Julia ^e   Muller, Jean ^a,e   Thevenon, Julien ^c,f   Herenger, Yvan ^e   Chancenotte, Sophie ^c,g   Bonnet, Marlène ^g   Pinoit, Jean Michel ^d   Huet, Fŕd́ric ^c   Thauvin Robinet, Christel ^c,f   Jaeger, Anne Sophie ^e   Le Gras, St́phanie ^h   Jost, Bernard ^h   Gérard, Béńdicte ^e   Peoc'H, Katell ⁱ   Launay, Jean Marie ⁱ   Faivre, Laurence ^c,f   Mandel, Jean Louis ^a,b,e   more..

^a UNIVERSITÉ DE STRASBOURG   (France)

^b Departmento de Génétique Humaine Collège de France ^*  (France)

^c Medical University of Dijon   (France)

^d Service de pédopsychiatrie Ch du Luxembourg   (France)

^e UNIVERSITY HOSPITAL OF STRASBOURG   (France)

^f UNIVERSITÉ DE BOURGOGNE   (France)

^g Centre Référent des Troubles du Langage et des Apprentissages Hô Pital d'Enfants   (France)

^h INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

ⁱ SAINT LOUIS HOSPITAL   (France)

Author keywords

autism; behavioral abnormalities; high throughput sequencing; monoamine oxidase A; X linked intellectual deficiency

Indexed keywords

AMINE OXIDASE (FLAVIN CONTAINING) ISOENZYME A; PSYCHOTROPIC AGENT; SEDATIVE AGENT; AMINE OXIDASE (FLAVIN CONTAINING);

ARTICLE; ATTENTION DEFICIT DISORDER; AUTISM; BEHAVIOR DISORDER; CHILD; CLINICAL EXAMINATION; COGNITIVE DEFECT; CONTROLLED STUDY; ENZYME ACTIVITY; FACIAL EXPRESSION; FAMILY HISTORY; FECES INCONTINENCE; FEEDING DIFFICULTY; GENE IDENTIFICATION; GENE TARGETING; GENOTYPE; GENOTYPE ENVIRONMENT INTERACTION; HIGH THROUGHPUT SEQUENCING; HUMAN; INTELLECTUAL IMPAIRMENT; MAJOR CLINICAL STUDY; MALE; MATERNAL DIABETES MELLITUS; MISSENSE MUTATION; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; PSYCHOMOTOR DEVELOPMENT; PSYCHOMOTOR PERFORMANCE; SCHOOL CHILD; VARIABLE NUMBER OF TANDEM REPEAT; X CHROMOSOME INACTIVATION; AMINO ACID SEQUENCE; CASE REPORT; CHEMICAL STRUCTURE; CHEMISTRY; FAMILY HEALTH; FEMALE; GENETIC PREDISPOSITION; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PEDIGREE; PROCEDURES; PROTEIN TERTIARY STRUCTURE;

AMINO ACID SEQUENCE; ATTENTION DEFICIT AND DISRUPTIVE BEHAVIOR DISORDERS; BASE SEQUENCE; CHILD DEVELOPMENT DISORDERS, PERVASIVE; FAMILY HEALTH; FEMALE; GENETIC PREDISPOSITION TO DISEASE; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HUMANS; INTELLECTUAL DISABILITY; MALE; MODELS, MOLECULAR; MONOAMINE OXIDASE; MUTATION, MISSENSE; PEDIGREE; PROTEIN STRUCTURE, TERTIARY;

EID: 84901025075     PISSN: 10184813     EISSN: 14765438     Source Type: Journal    
DOI: 10.1038/ejhg.2013.243     Document Type: Article

References (46)

1. Collins FA, Murphy DL, Reiss AL et al: Clinical, biochemical, and neuropsychiatric evaluation of a patient with a contiguous gene syndrome due to a microdeletion Xp11.3 including the Norrie disease locus and monoamine oxidase (MAOA and MAOB) genes. Am J Med Genet 1992; 42: 127-134.
2. Whibley A, Urquhart J, Dore J et al: Deletion of MAOA and MAOB in a male patient causes severe developmental delay, intermittent hypotonia and stereotypical hand movements. Eur J Hum Genet, 18: 1095-1099.
3. O'Leary RE, Shih JC, Hyland K, Kramer N, Asher YJ, Graham JM Jr: De novo microdeletion of Xp11.3 exclusively encompassing the monoamine oxidase A and B genes in a male infant with episodic hypotonia: a genomics approach to personalized medicine. Eur J Med Genet 2012; 55: 349-353.
4. Saito M, Yamagata T, Matsumoto A et al: MAOA/B deletion syndrome in male siblings with severe developmental delay and sudden loss of muscle tonus. Brain Dev 2013; S0387-7604: 00020-0002.
5. Brunner HG, Nelen MR, van Zandvoort P et al: X-linked borderline mental retardation with prominent behavioral disturbance: phenotype, genetic localization, and evidence for disturbed monoamine metabolism. Am J Hum Genet 1993; 52: 1032-1039.
6. Brunner HG, Nelen M, Breakefield XO, Ropers HH, van Oost BA: Abnormal behavior associated with a point mutation in the structural gene for monoamine oxidase A. Science 1993; 262: 578-580.
7. Cases O, Seif I, Grimsby J et al: Aggressive behavior and altered amounts of brain serotonin and norepinephrine in mice lacking MAOA. Science 1995; 268: 1763-1766.
8. Bortolato M, Godar SC, Alzghoul L et al: Monoamine oxidase A and A/B knockout mice display autistic-like features. Int J Neuropsychopharmacol 2013; 16: 869-888.
9. Scott AL, Bortolato M, Chen K, Shih JC: Novel monoamine oxidase A knock out mice with human-like spontaneous mutation. Neuroreport 2008; 19: 739-743.
10. Schuback DE, Mulligan EL, Sims KB et al: Screen for MAOA mutations in target human groups. Am J Med Genet 1999; 88: 25-28.
11. Haavik J, Blau N, Thony B: Mutations in human monoamine-related neurotransmitter pathway genes. Hum Mutat 2008; 29: 891-902.
12. Piton A, Gauthier J, Hamdan FF et al: Systematic resequencing of X-chromosome synaptic genes in autism spectrum disorder and schizophrenia. Mol Psychiatry 2011; 16: 867-880.
13. Sabol SZ, Hu S, Hamer D: A functional polymorphism in the monoamine oxidase A gene promoter. Hum Genet 1998; 103: 273-279.
14. Caspi A, McClay J, Moffitt TE et al: Role of genotype in the cycle of violence in maltreated children. Science 2002; 297: 851-854.
15. Cohen IL, Liu X, Schutz C et al: Association of autism severity with a monoamine oxidase A functional polymorphism. Clin Genet 2003; 64: 190-197.
16. May ME, Srour A, Hedges LK et al: Monoamine oxidase a promoter gene associated with problem behavior in adults with intellectual/developmental disabilities. Am J Intellect Dev Disabil 2009; 114: 269-273.
17. Lubs HA, Stevenson RE, Schwartz CE: Fragile X and X-linked intellectual disability: four decades of discovery. Am J Hum Genet 2012; 90: 579-590.
18. Ropers HH: Genetics of early onset cognitive impairment. Annu Rev Genomics Hum Genet 2010; 11: 161-187.
19. Redin C, Le Gras S, Mhamdi O et al: Targeted high-throughput sequencing for diagnosis of genetically heterogeneous diseases: efficient mutation detection in Bardet-Biedl and Alstrom syndromes. J Med Genet 2012; 49: 502-512.
20. Li H, Handsaker B, Wysoker A et al: The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009; 25: 2078-2079.
21. Ng PC, Henikoff S: SIFT: Predicting amino acid changes that affect protein function. Nucleic Acids Res 2003; 31: 3812-3814.
22. Adzhubei IA, Schmidt S, Peshkin L et al: A method and server for predicting damaging missense mutations. Nat Methods 2010; 7: 248-249.
23. Schwarz JM, Rodelsperger C, Schuelke M, Seelow D: MutationTaster evaluates disease-causing potential of sequence alterations. Nat Methods 2010; 7: 575-576.
24. Luu TD, Rusu A, Walter V et al: KD4v: comprehensible knowledge discovery system for missense variant. Nucleic Acids Res 2012; 40: W71-W75.
25. Yeo G, Burge CB: Maximum entropy modeling of short sequence motifs with applications to RNA splicing signals. J Comput Biol 2004; 11: 377-394.
26. Reese MG, Eeckman FH, Kulp D, Haussler D: Improved splice site detection in Genie. J Comput Biol 1997; 4: 311-323.
27. Pertea M, Lin X, Salzberg SL: GeneSplicer: a new computational method for splice site prediction. Nucleic Acids Res 2001; 29: 1185-1190.
28. Desmet FO, Hamroun D, Lalande M, Collod-Beroud G, Claustres M, Beroud C: Human Splicing Finder: an online bioinformatics tool to predict splicing signals. Nucleic Acids Res 2009; 37: e67.
29. Lung FW, Tzeng DS, Huang MF, Lee MB: Association of the MAOA promoter uVNTR polymorphism with suicide attempts in patients with major depressive disorder. BMC Med Genet 2011; 12: 74.
30. Allen RC, Zoghbi HY, Moseley AB, Rosenblatt HM, Belmont JW: Methylation of HpaII and HhaI sites near the polymorphic CAG repeat in the human androgen-receptor gene correlates with X chromosome inactivation. Am J Hum Genet 1992; 51: 1229-1239.
31. Pussard E, Neveux M, Guigueno N: Reference intervals for urinary catechola-mines and metabolites from birth to adulthood. Clin Biochem 2009; 42: 536-539.
32. Kema IP, de Vries EG, Slooff MJ, Biesma B, Muskiet FA: Serotonin, catecholamines, histamine, and their metabolites in urine, platelets, and tumor tissue of patients with carcinoid tumors. Clin Chem 1994; 40: 86-95.
33. Denney RM, Fritz RR, Patel NT, Abell CW: Human liver MAO-A and MAO-B separated by immunoaffinity chromatography with MAO-B-specific monoclonal antibody. Science 1982; 215: 1400-1403.
34. Cesura AM, Bos M, Galva MD, Imhof R, Da Prada M: Characterization of the binding of [3H]Ro 41-1049 to the active site of human monoamine oxidase-A. Mol Pharmacol 1990; 37: 358-366.
35. Lord C, Rutter M, Goode S et al: Autism diagnostic observation schedule: a standardized observation of communicative and social behavior. J Autism Dev Disord 1989; 19: 185-212.
36. Sparrow SS, Cicchetti DV: Diagnostic uses of the Vineland Adaptive Behavior Scales. J Pediatr Psychol 1985; 10: 215-225.
37. Son SY, Ma J, Kondou Y, Yoshimura M, Yamashita E, Tsukihara T: Structure of human monoamine oxidase A at 2.2-A resolution: the control of opening the entry for substrates/inhibitors. Proc Natl Acad Sci USA 2008; 105: 5739-5744.
38. Celada P, Artigas F: Plasma 5-hydroxyindoleacetic acid as an indicator of monoamine oxidase-A inhibition in rat brain and peripheral tissues. J Neurochem 1993; 61: 2191-2198.
39. Eisenhofer G, Finberg JP: Different metabolism of norepinephrine and epinephrine by catechol-O-methyltransferase and monoamine oxidase in rats. J Pharmacol Exp Ther 1994; 268: 1242-1251.
40. Wu HF, Chen K, Shih JC: Site-directed mutagenesis of monoamine oxidase A and B: role of cysteines. Mol Pharmacol 1993; 43: 888-893.
41. Fergusson DM, Boden JM, Horwood LJ, Miller AL, Kennedy MA: MAOA, abuse exposure and antisocial behaviour: 30-year longitudinal study. Br J Psychiatry 2011; 198: 457-463.
42. Kim-Cohen J, Caspi A, Taylor A et al: MAOA, maltreatment, and gene-environment interaction predicting children's mental health: new evidence and a meta-analysis. Mol Psychiatry 2006; 11: 903-913.
43. Tarpey PS, Smith R, Pleasance E et al: A systematic, large-scale resequencing screen of X-chromosome coding exons in mental retardation. Nat Genet 2009; 41: 535-543.
44. Piton A, Redin C, Mandel JL: XLID-causing mutations and associated genes challenged in light of data from large-scale human exome sequencing. Am J Human Genet 2013; S0002-9297: 00282-00286.
45. Fox MA, Panessiti MG, Moya PR et al: Mutations in monoamine oxidase (MAO) genes in mice lead to hypersensitivity to serotonin-enhancing drugs: implications for drug side effects in humans. Pharmacogenomics J 2013; 13: 551-557.
46. Jou RJ, Handen BL, Hardan AY: Retrospective assessment of atomoxetine in children and adolescents with pervasive developmental disorders. J Child Adolesc Psycho-pharmacol 2005; 15: 325-330.