Genetic evidence implicating DARPP-32 in human frontostriatal structure, function, and cognition

Journal of Clinical Investigation

Volumn 117, Issue 3, 2007, Pages 672-682

  Meyer Lindenberg, Andreas ^a   Straub, Richard E ^a   Lipska, Barbara K ^a   Verchinski, Beth A ^a   Goldberg, Terry ^a   Callicott, Joseph H ^a   Egan, Michael F ^a   Huffaker, Stephen S ^a   Mattay, Venkata S ^a   Kolachana, Bhaskar ^a   Kleinman, Joel E ^a   Weinberger, Daniel R ^a,b  

^a NATIONAL INSTITUTE OF MENTAL HEALTH   (United States)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATECHOL METHYLTRANSFERASE; ISOPROTEIN; MESSENGER RNA; PHOSPHOPROTEIN DARPP 32;

ARTICLE; BRAIN FUNCTION; BRAIN SIZE; COGNITION; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC ACTIVITY; FRONTAL LOBE; GENE LINKAGE DISEQUILIBRIUM; GENETIC IDENTIFICATION; GENETIC VARIABILITY; GENOTYPE; HAPLOTYPE; HUMAN; HUMAN TISSUE; MAJOR CLINICAL STUDY; NEOSTRIATUM; NERVE CELL PLASTICITY; NEUROIMAGING; NEUROTRANSMISSION; PHENOTYPE; POSTSYNAPTIC POTENTIAL; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SCHIZOPHRENIA; SEQUENCE ANALYSIS; SINGLE NUCLEOTIDE POLYMORPHISM;

CHROMOSOMES, HUMAN; COGNITION; DOPAMINE AND CAMP-REGULATED PHOSPHOPROTEIN 32; HAPLOTYPES; HUMANS; NEOSTRIATUM; POLYMORPHISM, SINGLE NUCLEOTIDE; PREFRONTAL CORTEX; RISK; SCHIZOPHRENIA; SEQUENCE ANALYSIS, DNA;

EID: 33847407101     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI30413     Document Type: Article

References (66)

1. Walaas, S.I., Aswad, D.W., and Greengard, P. 1983. A dopamine- and cyclic AMP-regulated phosphoprotein enriched in dopamine-innervated brain regions. Nature. 301:69-71.
2. Hemmings, H.C., Jr., Greengard, P., Tung, H.Y., and Cohen, P. 1984. DARPP-32, a dopamine-regulated neuronal phosphoprotein, is a potent inhibitor of protein phosphatase-1. Nature. 310:503-505.
3. Svenningsson, P., et al. 2004. DARPP-32: an integrator of neurotransmission. Annu. Rev. Pharmacol. Toxicol. 44:269-296.
4. Goldman-Rakic, P.S. 1998. The cortical dopamine system: role in memory and cognition. Adv. Pharmacol. 42:707-711.
5. Schultz, W. 1998. Predictive reward signal of dopamine neurons. J. Neurophysiol. 80:1-27.
6. Weinberger, D.R. 1987. Implications of normal brain development for the pathogenesis of schizophrenia. Arch. Gen. Psychiatry. 44:660-669.
7. Grace, A.A. 2000. The tonic/phasic model of dopamine system regulation and its implications for understanding alcohol and psychostimulant craving. Addiction. 95(Suppl. 2):S119-S128.
8. Fiorillo, C.D., Tobler, P.N., and Schultz, W. 2003. Discrete coding of reward probability and uncertainty by dopamine neurons. Science. 299:1898-1902.
9. Svenningsson, P., et al. 2003. Diverse psychotomimetics act through a common signaling pathway. Science. 302:1412-1415.
10. Zachariou, V., et al. 2006. Phosphorylation of DARPP-32 at Threonine-34 is required for cocaine action. Neuropsychopharmacology. 31:555-562.
11. Ouimet, C.C., LaMantia, A.S., Goldman-Rakic, P., Rakic, P., and Greengard, P. 1992. Immunocytochemical localization of DARPP-32, a dopamine and cyclic-AMP-regulated phosphoprotein, in the primate brain. J. Comp. Neurol. 323:209-218.
12. Ouimet, C.C., et al. 1984. DARPP-32, a dopamine-and adenosine 3′:5′-monophosphate-regulated phosphoprotein enriched in dopamine-innervated brain regions. III. Immunocytochemical localization. J. Neurosci. 4:111-124.
13. Alexander, G.E., DeLong, M.R., and Strick, P.L. 1986. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu. Rev. Neurosci. 9:357-381.
14. Graybiel, A.M. 2005. The basal ganglia: learning new tricks and loving it. Curr. Opin. Neurobiol. 15:638-644.
15. Haber, S.N. 2003. The primate basal ganglia: parallel and integrative networks. J. Chem. Neuroanat. 26:317-330.
16. Swerdlow, N.R., Geyer, M.A., and Braff, D.L. 2001. Neural circuit regulation of prepulse inhibition of startle in the rat: current knowledge and future challenges. Psychopharmacology (Berl.). 156:194-215.
17. Dunnett, S.B., Meldrum, A., and Muir, J.L. 2005. Frontal-striatal disconnection disrupts cognitive performance of the frontal-type in the rat. Neuroscience. 135:1055-1065.
18. Pantelis, C., et al. 1997. Frontal-striatal cognitive deficits in patients with chronic schizophrenia. Brain. 120:1823-1843.
19. Albert, K.A., et al. 2002. Evidence for decreased DARPP-32 in the prefrontal cortex of patients with schizophrenia. Arch. Gen. Psychiatry. 59:705-712.
20. Baracskay, K.L., Haroutunian, V., and Meador-Woodruff, J.H. 2006. Dopamine receptor signaling molecules are altered in elderly schizophrenic cortex. Synapse. 60:271-279.
21. Meyer-Lindenberg, A., and Weinberger, D.R. 2006. Intermediate phenotypes and genetic mechanisms of psychiatric disorders. Nat. Rev. Neurosci. 7:818-827.
22. Harrison, P.J., and Weinberger, D.R. 2005. Schizophrenia genes, gene expression, and neuropathology: on the matter of their convergence. Mol. Psychiatry. 10:40-68.
23. Egan, M.F., et al. 2001. Effect of COMT Val108/158 Met genotype on frontal lobe function and risk for schizophrenia. Proc. Natl. Acad. Sci. U. S. A. 98:6917-6922.
24. Meyer-Lindenberg, A., et al. 2006. Impact of complex genetic variation in COMT on human brain function. Mol. Psychiatry. 11:867-877.
25. Tunbridge, E.M., Bannerman, D.M., Sharp, T., and Harrison, P.J. 2004. Catechol-o-methyltransferase inhibition improves set-shifting performance and elevates stimulated dopamine release in the rat prefrontal cortex. J. Neurosci. 24:5331-5335.
26. Gogos, J.A., et al. 1998. Catechol-O-methyltransferase-deficient mice exhibit sexually dimorphic changes in catecholamine levels and behavior. Proc. Natl. Acad. Sci. U. S. A. 95:9991-9996.
27. Meyer-Lindenberg, A., et al. 2002. Reduced prefrontal activity predicts exaggerated striatal dopaminergic function in schizophrenia. Nat. Neurosci. 5:267-271.
28. Kellendonk, C., et al. 2006. Transient and selective overexpression of dopamine D2 receptors in the striatum causes persistent abnormalities in prefrontal cortex functioning. Neuron. 49:603-615.
29. Gabriel, S.B., et al. 2002. The structure of haplotype blocks in the human genome. Science. 296:2225-2229.
30. Egan, M.F., et al. 2001. Relative risk for cognitive impairments in siblings of patients with schizophrenia. Biol. Psychiatry. 50:98-107.
31. El-Rifai, W., et al. 2002. Gastric cancers overexpress DARPP-32 and a novel isoform, t-DARPP. Cancer Res. 62:4061-4064.
32. Pezawas, L., et al. 2005. 5-HTTLPR polymorphism impacts human cingulate-amygdala interactions: a genetic susceptibility mechanism for depression. Nat. Neurosci. 8:828-834.
33. Callicott, J.H., et al. 2000. Physiological dysfunction of the dorsolateral prefrontal cortex in schizophrenia revisited. Cereb. Cortex. 10:1078-1092.
34. Meyer-Lindenberg, A., et al. 2005. Neural correlates of genetically abnormal social cognition in Williams syndrome. Nat. Neurosci. 8:991-993.
35. Li, C.H., Liao, H.M., Hung, T.W., and Chen, C.H. 2006. Mutation analysis of DARPP-32 as a candidate gene for schizophrenia. Schizophr. Res. 87:1-5.
36. Law, A.J., et al. 2006. Neuregulin 1 transcripts are differentially expressed in schizophrenia and regulated by 5? SNPs associated with the disease. Proc. Natl. Acad. Sci. U. S. A. 103:6747-6752.
37. Partiot, A., et al. 1996. Delayed response tasks in basal ganglia lesions in man: further evidence for a striato-frontal cooperation in behavioral adaptation. Neuropsychologia. 34:709-721.
38. Mechelli, A., Friston, K.J., Frackowiak, R.S., and Price, C.J. 2005. Structural covariance in the human cortex. J. Neurosci. 25:8303-8310.
39. Raz, N., et al. 2005. Regional brain changes in aging healthy adults: general trends, individual differences and modifiers. Cereb. Cortex. 15:1676-1689.
40. Raz, N., et al. 2004. Aging, sexual dimorphism, and hemispheric asymmetry of the cerebral cortex: replicability of regional differences in volume. Neurobiol. Aging. 25:377-396.
41. Raz, N., et al. 1997. Selective aging of the human cerebral cortex observed in vivo: differential vulnerability of the prefrontal gray matter. Cereb. Cortex. 7:268-282.
42. Woodruff, P.W., et al. 1997. Structural brain abnormalities in male schizophrenics reflect fronto-temporal dissociation. Psychol. Med. 27:1257-1266.
43. Andrews, T.J., Halpern, S.D., and Purves, D. 1997. Correlated size variations in human visual cortex, lateral geniculate nucleus, and optic tract. J. Neurosci. 17:2859-2868.
44. Gray, J.R., Chabris, C.F., and Braver, T.S. 2003. Neural mechanisms of general fluid intelligence. Nat. Neurosci. 6:316-322.
45. Lynch, D.R., et al. 2003. Lack of effect of polymorphisms in dopamine metabolism related genes on imaging of TRODAT-1 in striatum of asymptomatic volunteers and patients with Parkinson's disease. Mov. Disord. 18:804-812.
46. Lewis, C.M., et al. 2003. Genome scan meta-analysis of schizophrenia and bipolar disorder, part II: Schizophrenia. Am. J. Hum. Genet. 73:34-48.
47. Keshavan, M.S., Rosenberg, D., Sweeney, J.A., and Pettegrew, J.W. 1998. Decreased caudate volume in neuroleptic-naive psychotic patients. Am. J. Psychiatry. 155:774-778.
48. Chakos, M.H., et al. 1994. Increase in caudate nuclei volumes of first-episode schizophrenic patients taking antipsychotic drugs. Am. J. Psychiatry. 151:1430-1436.
49. Meyer-Lindenberg, A.S., et al. 2005. Regionally specific disturbance of dorsolateral prefrontal-hippocampal functional connectivity in schizophrenia. Arch. Gen. Psychiatry. 62:379-386.
50. Schneider, J.S. 1984. Basal ganglia role in behavior: importance of sensory gating and its relevance to psychiatry. Biol. Psychiatry. 19:1693-1710.
51. Miller, E.K., and Cohen, J.D. 2001. An integrative theory of prefrontal cortex function. Annu. Rev. Neurosci. 24:167-202.
52. Valjent, E., et al. 2005. Regulation of a protein phosphatase cascade allows convergent dopamine and glutamate signals to activate ERK in the striatum. Proc. Natl. Acad. Sci. U. S. A. 102:491-496.
53. Cloninger, C.R., et al. 1998. Genome-wide search for schizophrenia susceptibility loci: the NIMH Genetics Initiative and Millennium Consortium. Am. J. Med. Genet. 81:275-281.
54. Abecasis, G.R., and Cookson, W.O. 2000. GOLD - graphical overview of linkage disequilibrium. Bioinformatics. 16:182-183.
55. Stephens, M., Smith, N.J., and Donnelly, P. 2001. A new statistical method for haplotype reconstruction from population from population data. Am. J. Hum. Genet. 68:978-989.
56. Jastak, S., Wilkinson, G.S., and Jastak, J. 1984. Wide range achievement test - revised. Jastak Associates. Wilmington, Delaware, USA.
57. Lipska, B.K., et al. 2006. Critical factors in gene expression in postmortem human brain: focus on studies in schizophrenia. Biol. Psychiatry. 60:650-658.
58. Hariri, A.R., Tessitore, A., Mattay, V.S., Fera, F., and Weinberger, D.R. 2002. The amygdala response to emotional stimuli: a comparison of faces and scenes. Neuroimage. 17:317-323.
59. Hariri, A.R., et al. 2005. A susceptibility gene for affective disorders and the response of the human amygdala. Arch. Gen. Psychiatry. 62:146-152.
60. Pezawas, L., et al. 2004. The brain-derived neurotrophic factor val66met polymorphism and variation in human cortical morphology. J. Neurosci. 24:10099-10102.
61. Augood, S.J., Westmore, K., and Emson, P.C. 1997. Phenotypic characterization of neurotensin messenger RNA-expressing cells in the neuroleptic-treated rat striatum: a detailed cellular co-expression study. Neuroscience. 76:763-774.
62. Ashburner, J., and Friston, K.J. 2000. Voxel-based morphometry - the methods. Neuroimage. 11:805-821.
63. Friston, K.J., et al. 1995. Statistical parametric maps in functional imaging: a general linear approach. Hum. Brain Mapp. 2:189-210.
64. Meyer-Lindenberg, A., et al. 2001. Evidence for abnormal cortical functional connectivity during working memory in schizophrenia. Am. J. Psychiatry. 158:1809-1817.
65. Worsley, K.J., et al. 1996. A unified statistical approach for determining significant signals in images of cerebral activation. Hum. Brain Mapp. 4:58-73.
66. Genovese, C.R., Lazar, N.A., and Nichols, T. 2002. Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage. 15:870-878.