DRD2 and PPP1R1B (DARPP-32) polymorphisms independently confer increased risk for autism spectrum disorders and additively predict affected status in male-only affected sib-pair families

Behavioral and Brain Functions

Volumn 8, Issue , 2012, Pages

  Hettinger, Joe A ^a   Liu, Xudong ^a,b   Hudson, Melissa L ^a,b,c   Lee, Alana ^a,b,c   Cohen, Ira L ^c,d   Michaelis, Ron C ^e   Schwartz, Charles E ^f   Lewis, Suzanne M E ^c,g,h   Holden, Jeanette J A ^a,b,c,i  

^a QUEEN S UNIVERSITY   (Canada)

^b Ongwanada Resource Centre   (Canada)

^c Autism Spectrum Disorders Canadian American Research Consortium   (Canada)

^d NEW YORK STATE INSTITUTE FOR BASIC RESEARCH IN DEVELOPMENTAL DISABILITIES   (United States)

^e WESTERN CAROLINA UNIVERSITY   (United States)

^f GREENWOOD GENETIC CENTER   (United States)

^g UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^h UNIVERSITY OF BRITISH COLUMBIA   (Canada)

ⁱ QUEEN S UNIVERSITY   (Canada)

Author keywords

Association study; Autism spectrum disorders; Candidate gene; DARPP 32; Dopamine receptors

Indexed keywords

DOPAMINE; DOPAMINE 2 RECEPTOR; PHOSPHOPROTEIN DARPP 32;

ALLELE; ARTICLE; AUTISM; COHORT ANALYSIS; CONTROLLED STUDY; EMOTION; EXECUTIVE FUNCTION; GENDER; GENE FREQUENCY; GENE LINKAGE DISEQUILIBRIUM; GENE LOCUS; GENETIC POLYMORPHISM; GENETIC PREDISPOSITION; GENETIC RISK; GENOTYPE; GENOTYPE PHENOTYPE CORRELATION; HUMAN; INTERPERSONAL COMMUNICATION; LEARNING; MAJOR CLINICAL STUDY; MALE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RECEPTOR GENE; SIBLING; SOCIAL INTERACTION; STEREOTYPY;

ALLELES; CHILD; CHILD DEVELOPMENT DISORDERS, PERVASIVE; DOPAMINE AND CAMP-REGULATED PHOSPHOPROTEIN 32; GENETIC ASSOCIATION STUDIES; GENETIC LOCI; GENETIC PREDISPOSITION TO DISEASE; GENOTYPE; HUMANS; LINKAGE DISEQUILIBRIUM; MALE; POLYMORPHISM, SINGLE NUCLEOTIDE; RECEPTORS, DOPAMINE D2; SIBLINGS;

EID: 84860509643     PISSN: None     EISSN: 17449081     Source Type: Journal    
DOI: 10.1186/1744-9081-8-19     Document Type: Article

References (79)

1. Bacchelli E, Maestrini E. Autism spectrum disorders: molecular genetic advances. Am J Med Genet C Semin Med Genet 2006, 142C:13-23.
2. Zhao X, Leotta A, Kustanovich V, Lajonchere C, Geschwind DH, Law K, Law P, Qiu S, Lord C, Sebat J, et al. A unified genetic theory for sporadic and inherited autism. Proc Natl Acad Sci U S A 2007, 104:12831-12836.
3. Persico AM, Bourgeron T. Searching for ways out of the autism maze: genetic, epigenetic and environmental clues. Trends Neurosci 2006, 29:349-358.
4. Muhle R, Trentacoste SV, Rapin I. The genetics of autism. Pediatrics 2004, 113:e472-e486.
5. Hettinger JA, Liu X, Schwartz CE, Michaelis RC, Holden JJ. A DRD1 haplotype is associated with risk for autism spectrum disorders in male-only affected sib-pair families. Am J Med Genet B Neuropsychiatr Genet 2008, 147B:628-636.
6. Carlsson A. A paradigm shift in brain research. Science 2001, 294:1021-1024.
7. Crofts HS, Dalley JW, Collins P, Van Denderen JC, Everitt BJ, Robbins TW, Roberts AC. Differential effects of 6-OHDA lesions of the frontal cortex and caudate nucleus on the ability to acquire an attentional set. Cereb Cortex 2001, 11:1015-1026.
8. Rinaldi A, Mandillo S, Oliverio A, Mele A. D1 and D2 receptor antagonist injections in the prefrontal cortex selectively impair spatial learning in mice. Neuropsychopharmacology 2007, 32:309-319.
9. Pezze MA, Feldon J. Mesolimbic dopaminergic pathways in fear conditioning. Prog Neurobiol 2004, 74:301-320.
10. Coldren JT, Halloran C. Spatial reversal as a measure of executive functioning in children with autism. J Genet Psychol 2003, 164:29-41.
11. Gaigg SB, Bowler DM. Differential fear conditioning in Asperger's syndrome: implications for an amygdala theory of autism. Neuropsychologia 2007, 45:2125-2134.
12. Hill EL. Executive dysfunction in autism. Trends Cogn Sci 2004, 8:26-32.
13. Vilensky JA, Damasio AR, Maurer RG. Gait disturbances in patients with autistic behavior: a preliminary study. Arch Neurol 1981, 38:646-649.
14. Wang Z, Yu G, Cascio C, Liu Y, Gingrich B, Insel TR. Dopamine D2 receptor-mediated regulation of partner preferences in female prairie voles (Microtus ochrogaster): a mechanism for pair bonding?. Behav Neurosci 1999, 113:602-611.
15. Karler R, Calder LD, Thai LH, Bedingfield JB. A dopaminergic-glutamatergic basis for the action of amphetamine and cocaine. Brain Res 1994, 658:8-14.
16. Ernst M, Zametkin AJ, Matochik JA, Pascualvaca D, Cohen RM. Low medial prefrontal dopaminergic activity in autistic children. Lancet 1997, 350:638.
17. Gillberg C, Svennerholm L. CSF monoamines in autistic syndromes and other pervasive developmental disorders of early childhood. Br J Psychiatry 1987, 151:89-94.
18. Robinson PD, Schutz CK, Macciardi F, White BN, Holden JJ. Genetically determined low maternal serum dopamine beta-hydroxylase levels and the etiology of autism spectrum disorders. Am J Med Genet 2001, 100:30-36.
19. Eubanks JH, Djabali M, Selleri L, Grandy DK, Civelli O, McElligott DL, Evans GA. Structure and linkage of the D2 dopamine receptor and neural cell adhesion molecule genes on human chromosome 11q23. Genomics 1992, 14:1010-1018.
20. Grandy DK, Litt M, Allen L, Bunzow JR, Marchionni M, Makam H, Reed L, Magenis RE, Civelli O. The human dopamine D2 receptor gene is located on chromosome 11 at q22-q23 and identifies a TaqI RFLP. Am J Hum Genet 1989, 45:778-785.
21. Onali P, Olianas MC. Involvement of adenylate cyclase inhibition in dopamine autoreceptor regulation of tyrosine hydroxylase in rat nucleus accumbens. Neurosci Lett 1989, 102:91-96.
22. Mercuri NB, Saiardi A, Bonci A, Picetti R, Calabresi P, Bernardi G, Borrelli E. Loss of autoreceptor function in dopaminergic neurons from dopamine D2 receptor deficient mice. Neuroscience 1997, 79:323-327.
23. Mehta MA, Sahakian BJ, McKenna PJ, Robbins TW. Systemic sulpiride in young adult volunteers simulates the profile of cognitive deficits in Parkinson's disease. Psychopharmacology (Berl) 1999, 146:162-174.
24. Meintzschel F, Ziemann U. Modification of practice-dependent plasticity in human motor cortex by neuromodulators. Cereb Cortex 2006, 16:1106-1115.
25. Greba Q, Gifkins A, Kokkinidis L. Inhibition of amygdaloid dopamine D2 receptors impairs emotional learning measured with fear-potentiated startle. Brain Res 2001, 899:218-226.
26. Baik JH, Picetti R, Saiardi A, Thiriet G, Dierich A, Depaulis A, Le Meur M, Borrelli E. Parkinsonian-like locomotor impairment in mice lacking dopamine D2 receptors. Nature 1995, 377:424-428.
27. McDougle CJ, Holmes JP, Carlson DC, Pelton GH, Cohen DJ, Price LH. A double-blind, placebo-controlled study of risperidone in adults with autistic disorder and other pervasive developmental disorders. Arch Gen Psychiatry 1998, 55:633-641.
28. Ouimet CC, Miller PE, Hemmings HC, Walaas SI, Greengard P. DARPP-32, a dopamine- and adenosine 3':5'-monophosphate-regulated phosphoprotein enriched in dopamine-innervated brain regions. III. Immunocytochemical localization. J Neurosci 1984, 4:111-124.
29. Fienberg AA, Greengard P. The DARPP-32 knockout mouse. Brain Res Brain Res Rev 2000, 31:313-319.
30. Fienberg AA, Hiroi N, Mermelstein PG, Song W, Snyder GL, Nishi A, Cheramy A, O'Callaghan JP, Miller DB, Cole DG, et al. DARPP-32: regulator of the efficacy of dopaminergic neurotransmission. Science 1998, 281:838-842.
31. Heyser CJ, Fienberg AA, Greengard P, Gold LH. DARPP-32 knockout mice exhibit impaired reversal learning in a discriminated operant task. Brain Res 2000, 867:122-130.
32. Meyer-Lindenberg A, Straub RE, Lipska BK, Verchinski BA, Goldberg T, Callicott JH, Egan MF, Huffaker SS, Mattay VS, Kolachana B, et al. Genetic evidence implicating DARPP-32 in human frontostriatal structure, function, and cognition. J Clin Invest 2007, 117:672-682.
33. Ogden CA, Rich ME, Schork NJ, Paulus MP, Geyer MA, Lohr JB, Kuczenski R, Niculescu AB. Candidate genes, pathways and mechanisms for bipolar (manic-depressive) and related disorders: an expanded convergent functional genomics approach. Mol Psychiatry 2004, 9:1007-1029.
34. Ishikawa M, Mizukami K, Iwakiri M, Asada T. Immunohistochemical and immunoblot analysis of Dopamine and cyclic AMP-regulated phosphoprotein, relative molecular mass 32,000 (DARPP-32) in the prefrontal cortex of subjects with schizophrenia and bipolar disorder. Prog Neuropsychopharmacol Biol Psychiatry 2007, 31:1177-1181.
35. Stahlberg O, Soderstrom H, Rastam M, Gillberg C. Bipolar disorder, schizophrenia, and other psychotic disorders in adults with childhood onset AD/HD and/or autism spectrum disorders. J Neural Transm 2004, 111:891-902.
36. Comings DE, Comings BG, Muhleman D, Dietz G, Shahbahrami B, Tast D, Knell E, Kocsis P, Baumgarten R, Kovacs BW, et al. The dopamine D2 receptor locus as a modifying gene in neuropsychiatric disorders. JAMA 1991, 266:1793-1800.
37. Philippe A, Guilloud-Bataille M, Martinez M, Gillberg C, Rastam M, Sponheim E, Coleman M, Zappella M, Aschauer H, Penet C, et al. Analysis of ten candidate genes in autism by association and linkage. Am J Med Genet 2002, 114:125-128.
38. Noble EP. D2 dopamine receptor gene in psychiatric and neurologic disorders and its phenotypes. Am J Med Genet B Neuropsychiatr Genet 2003, 116B:103-125.
39. Schroer RJ, Phelan MC, Michaelis RC, Crawford EC, Skinner SA, Cuccaro M, Simensen RJ, Bishop J, Skinner C, et al. Autism and maternally derived aberrations of chromosome 15q. Am J Med Genet 1998, 76:327-336.
40. Geschwind DH, Sowinski J, Lord C, Iversen P, Shestack J, Jones P, Ducat L, Spence SJ. The autism genetic resource exchange: a resource for the study of autism and related neuropsychiatric conditions. Am J Hum Genet 2001, 69:463-466.
41. Mulvihill B, et al. Prevalence of autism spectrum disorders - autism and developmental disabilities monitoring network, United States, 2006. MMWR Surveill Summ 2009, 58:1-20.
42. Barrett JC, Fry B, Maller J, Daly MJ. Haploview: analysis and visualization of LD and haplotype maps. Bioinformatics 2005, 21:263-265.
43. Dubertret C, Gouya L, Hanoun N, Deybach JC, Ades J, Hamon M, Gorwood P. The 3′ region of the DRD2 gene is involved in genetic susceptibility to schizophrenia. Schizophr Res 2004, 67:75-85.
44. Laird NM, Horvath S, Xu X. Implementing a unified approach to family-based tests of association. Genet Epidemiol 2000, 19(Suppl 1):S36-S42.
45. Lord C, Rutter M, Le Couteur A. Autism diagnostic interview-revised: a revised version of a diagnostic interview for caregivers of individuals with possible pervasive developmental disorders. J Autism Dev Disord 1994, 24:659-685.
46. Benjamini Y, Drai D, Elmer G, Kafkafi N, Golani I. Controlling the false discovery rate in behavior genetics research. Behav Brain Res 2001, 125:279-284.
47. Benjamini Y, Yekutieli D. The control of the false discovery rate in multiple testing under dependency. Ann Stat 2001, 29:1165-1188.
48. Conde L, Vaquerizas JM, Dopazo H, Arbiza L, Reumers J, Rousseau F, Schymkowitz J, Dopazo J. PupaSuite: finding functional single nucleotide polymorphisms for large-scale genotyping purposes. Nucleic Acids Res 2006, 34:W621-W625.
49. Yuan HY, Chiou JJ, Tseng WH, Liu CH, Liu CK, Lin YJ, Wang HH, Yao A, Chen YT, Hsu CN. FASTSNP: an always up-to-date and extendable service for SNP function analysis and prioritization. Nucleic Acids Res 2006, 34(Web Server issue):W635-W641.
50. Houlihan LM, Harris SE, Luciano M, Gow AJ, Starr JM, Visscher PM, Deary IJ. Replication study of candidate genes for cognitive abilities: the Lothian Birth Cohort 1936. Genes Brain Behav 2009, 8:238-247.
51. Arinami T, Gao M, Hamaguchi H, Toru M. A functional polymorphism in the promoter region of the dopamine D2 receptor gene is associated with schizophrenia. Hum Mol Genet 1997, 6:577-582.
52. Zhang Y, Bertolino A, Fazio L, Blasi G, Rampino A, Romano R, Lee ML, Xiao T, Papp A, et al. Polymorphisms in human dopamine D2 receptor gene affect gene expression, splicing, and neuronal activity during working memory. Proc Natl Acad Sci U S A 2007, 104:20552-20557.
53. Bertolino A, Fazio L, Caforio G, Blasi G, Rampino A, Romano R, Di Giorgio A, Taurisano P, Papp A, Pinsonneault J, et al. Functional variants of the dopamine receptor D2 gene modulate prefronto-striatal phenotypes in schizophrenia. Brain 2009, 132:417-425.
54. Bertolino A, Taurisano P, Pisciotta NM, Blasi G, Fazio L, Romano R, Gelao B, Lo Bianco L, Lozupone M, Di Giorgio A, et al. Genetically determined measures of striatal D2 signaling predict prefrontal activity during working memory performance. PLoS One 2010, 5.
55. Troost PW, Lahuis BE, Steenhuis MP, Ketelaars CE, Buitelaar JK, van Engeland H, Scahill L, Minderaa RB, Hoekstra PJ. Long-term effects of risperidone in children with autism spectrum disorders: a placebo discontinuation study. J Am Acad Child Adolesc Psychiatry 2005, 44:1137-1144.
56. Floresco SB, Magyar O, Ghods-Sharifi S, Vexelman C, Tse MT. Multiple dopamine receptor subtypes in the medial prefrontal cortex of the rat regulate set-shifting. Neuropsychopharmacology 2006, 31:297-309.
57. Nader K, LeDoux JE. Inhibition of the mesoamygdala dopaminergic pathway impairs the retrieval of conditioned fear associations. Behav Neurosci 1999, 113:891-901.
58. Hotte M, Thuault S, Lachaise F, Dineley KT, Hemmings HC, Nairn AC, Jay TM. D1 receptor modulation of memory retrieval performance is associated with changes in pCREB and pDARPP-32 in rat prefrontal cortex. Behav Brain Res 2006, 171:127-133.
59. Steele SD, Minshew NJ, Luna B, Sweeney JA. Spatial working memory deficits in autism. J Autism Dev Disord 2007, 37:605-612.
60. Kruzich PJ, Mitchell SH, Younkin A, Grandy DK. Dopamine D2 receptors mediate reversal learning in male C57BL/6 J mice. Cogn Affect Behav Neurosci 2006, 6:86-90.
61. Calabresi P, Gubellini P, Centonze D, Picconi B, Bernardi G, Chergui K, Svenningsson P, Fienberg AA, Greengard P. Dopamine and cAMP-regulated phosphoprotein 32 kDa controls both striatal long-term depression and long-term potentiation, opposing forms of synaptic plasticity. J Neurosci 2000, 20:8443-8451.
62. Centonze D, Picconi B, Gubellini P, Bernardi G, Calabresi P. Dopaminergic control of synaptic plasticity in the dorsal striatum. Eur J Neurosci 2001, 13:1071-1077.
63. Bissiere S, Humeau Y, Luthi A. Dopamine gates LTP induction in lateral amygdala by suppressing feedforward inhibition. Nat Neurosci 2003, 6:587-592.
64. Hare TA, Tottenham N, Davidson MC, Glover GH, Casey BJ. Contributions of amygdala and striatal activity in emotion regulation. Biol Psychiatry 2005, 57:624-632.
65. Bachevalier J. Medial temporal lobe structures and autism: a review of clinical and experimental findings. Neuropsychologia 1994, 32:627-648.
66. Canales JJ, Graybiel AM. A measure of striatal function predicts motor stereotypy. Nat Neurosci 2000, 3:377-383.
67. Jiang YH, Bressler J, Beaudet AL. Epigenetics and human disease. Annu Rev Genomics Hum Genet 2004, 5:479-510.
68. Kato MV, Ikawa Y, Hayashizaki Y, Shibata H. Paternal imprinting of mouse serotonin receptor 2A gene Htr2 in embryonic eye: a conserved imprinting regulation on the RB/Rb locus. Genomics 1998, 47:146-148.
69. Vaillancourt C, Petit A, Belisle S. Expression of human placental D2-dopamine receptor during normal and abnormal pregnancies. Placenta 1998, 19:73-80.
70. Yanagawa T, Kishimoto Y, Tada K, Arai F, Kondo Y, Kudo T. Presence of dopamine DA-1 receptors in human decidua. Placenta 1997, 18:169-172.
71. Brana C, Caille I, Pellevoisin C, Charron G, Aubert I, Caron MG, Carles D, Vital C, Bloch B. Ontogeny of the striatal neurons expressing the D1 dopamine receptor in humans. J Comp Neurol 1996, 370:23-34.
72. Brana C, Aubert I, Charron G, Pellevoisin C, Bloch B. Ontogeny of the striatal neurons expressing the D2 dopamine receptor in humans: an in situ hybridization and receptor-binding study. Brain Res Mol Brain Res 1997, 48:389-400.
73. Stratakis CA, Mitsiades NS, Chrousos GP, Margioris AN. Dopamine affects the in vitro basal secretion of rat placenta opioids in an opioid and dopamine receptor type-specific manner. Eur J Pharmacol 1996, 315:53-58.
74. Petit A, Gallo-Payet N, Vaillancourt C, Bellabarba D, Lehoux JG, Belisle S. A role for extracellular calcium in the regulation of placental lactogen release by angiotensin-II and dopamine in human term trophoblastic cells. J Clin Endocrinol Metab 1993, 77:670-676.
75. Reinoso BS, Undie AS, Levitt P. Dopamine receptors mediate differential morphological effects on cerebral cortical neurons in vitro. J Neurosci Res 1996, 43:439-453.
76. Schmidt U, Beyer C, Oestreicher AB, Reisert I, Schilling K, Pilgrim C. Activation of dopaminergic D1 receptors promotes morphogenesis of developing striatal neurons. Neuroscience 1996, 74:453-460.
77. Shen HM, Nakamura A, Sugimoto J, Sakumoto N, Oda T, Jinno Y, Okazaki Y. Tissue specificity of methylation and expression of human genes coding for neuropeptides and their receptors, and of a human endogenous retrovirus K family. J Hum Genet 2006, 51:440-450.
78. Glaser RL, Ramsay JP, Morison IM. The imprinted gene and parent-of-origin effect database now includes parental origin of de novo mutations. Nucleic Acids Res 2006, 34:D29-D31.
79. Yamasaki K, Joh K, Ohta T, Masuzaki H, Ishimaru T, Mukai T, Niikawa N, Ogawa M, Wagstaff J, Kishino T. Neurons but not glial cells show reciprocal imprinting of sense and antisense transcripts of Ube3a. Hum Mol Genet 2003, 12:837-847.