Attention-deficit/hyperactivity phenotype in mice lacking the cyclin-dependent kinase 5 cofactor p35

Biological Psychiatry

Volumn 68, Issue 12, 2010, Pages 1163-1171

  Drerup, Justin M ^a   Hayashi, Kanehiro ^a   Cui, Huxing ^a   Mettlach, Gabriel L ^a   Long, Michael A ^b   Marvin, Marian ^b   Sun, Xiankai ^a   Goldberg, Matthew S ^b   Lutter, Michael ^a   Bibb, James A ^a,c  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c UNIVERSITY OF TEXAS AT DALLAS   (United States)

Author keywords

Attention deficit hyperactivity disorder (ADHD); Cdk5; dopamine; methylphenidate; p35; prefrontal cortex

Indexed keywords

CYCLIN DEPENDENT KINASE 5; FLUORODEOXYGLUCOSE F 18; GLUCOSE; METHYLPHENIDATE; NEUROTRANSMITTER; PROTEIN P35; TYROSINE 3 MONOOXYGENASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATTENTION DEFICIT DISORDER; BRAIN CORTEX; CONTROLLED STUDY; DRUG EXPOSURE; GLUCOSE METABOLISM; IN VIVO STUDY; KNOCKOUT MOUSE; LIMBIC SYSTEM; LONG TERM EXPOSURE; MALE; MOUSE; NONHUMAN; PHENOTYPE; POSITRON EMISSION TOMOGRAPHY; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; STRIATE CORTEX;

ANIMALS; ATROPHY; ATTENTION DEFICIT DISORDER WITH HYPERACTIVITY; BRAIN; DISEASE MODELS, ANIMAL; DOPAMINE; DOPAMINE AND CAMP-REGULATED PHOSPHOPROTEIN 32; FLUORODEOXYGLUCOSE F18; MALE; METHYLPHENIDATE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MOTOR ACTIVITY; NEURAL PATHWAYS; PHENOTYPE; PHOSPHOTRANSFERASES; POSITRON-EMISSION TOMOGRAPHY; PREFRONTAL CORTEX; RECEPTORS, AMPA; SEROTONIN; SYNAPTIC TRANSMISSION;

EID: 78649831025     PISSN: 00063223     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biopsych.2010.07.016     Document Type: Article

References (66)

1. American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders 4th ed. 2000 American Psychiatric Press Washington, DC
2. A.J. Zametkin, T.E. Nordahl, M. Gross, A.C. King, W.E. Semple, and J. Rumsey Cerebral glucose metabolism in adults with hyperactivity of childhood onset N Engl J Med 323 1990 1361 1366
3. J.N. Giedd, F.X. Castellanos, B.J. Casey, P. Kozuch, A.C. King, S.D. Hamburger, and J.L. Rapoport Quantitative morphology of the corpus callosum in attention deficit hyperactivity disorder Am J Psychiatry 151 1994 665 669
4. B.J. Casey, F.X. Castellanos, J.N. Giedd, W.L. Marsh, S.D. Hamburger, and A.B. Schubert Implication of right fronto-striatal circuitry in response inhibition and attention-deficit/hyperactivity disorder J Am Acad Child Adolesc Psychiatry 36 1997 374 383
5. D.G. Amen, and B.D. Carmichael High-resolution brain SPECT imaging in ADHD Ann Clin Psychiatry 9 1997 81 86
6. F.X. Castellanos, P.P. Lee, W. Sharp, N.O. Jeffries, D.K. Greenstein, and L.S. Clasen Developmental trajectories of brain volume abnormalities in children and adolescents with attention-deficit/hyperactivity disorder JAMA 288 2002 1740 1748
7. A. Qiu, D. Crocetti, M. Adler, E.M. Mahone, M.B. Denckla, M.I. Miller, and S.H. Mostofsky Basal ganglia volume and shape in children with attention deficit hyperactivity disorder Am J Psychiatry 166 2009 74 82
8. P. Shaw, K. Eckstrand, W. Sharp, J. Blumenthal, J.P. Lerch, and D. Greenstein Attention-deficit/hyperactivity disorder is characterized by a delay in cortical maturation Proc Natl Acad Sci U S A 104 2007 19649 19654
9. G. Tripp, and J. Wickens Neurobiology of ADHD Neuropharmacology 57 2009 579 589
10. D. Pan, S.J. Gatley, S.L. Dewey, R. Chen, D.A. Alexoff, Y.S. Ding, and J.S. Fowler Binding of bromine-substituted analogs of methylphenidate to monoamine transporters Eur J Pharmacol 264 1994 177 182
11. Y.S. Ding, J.S. Fowler, N.D. Volkow, J. Logan, S.J. Gatley, and Y. Sugano Carbon-11-d-threo-methylphenidate binding to dopamine transporter in baboon brain J Nucl Med 36 1995 2298 2305
12. S. Vijayraghavan, M. Wang, S.G. Birnbaum, G.V. Williams, and A.F. Arnsten Inverted-U dopamine D1 receptor actions on prefrontal neurons engaged in working memory Nat Neurosci 10 2007 376 384
13. S. Granon, F. Passetti, K.L. Thomas, J.W. Dalley, B.J. Everitt, and T.W. Robbins Enhanced and impaired attentional performance after infusion of D1 dopaminergic receptor agents into rat prefrontal cortex J Neurosci 20 2000 1208 1215
14. Y. Chudasama, and T.W. Robbins Dopaminergic modulation of visual attention and working memory in the rodent prefrontal cortex Neuropsychopharmacology 29 2004 1628 1636
15. C.W. Berridge, D.M. Devilbiss, M.E. Andrzejewski, A.F.T. Arnsten, A.E. Kelley, and B. Schmeichel Methylphenidate preferentially increases catecholamine neurotransmission within the prefrontal cortex at low doses that enhance cognitive function Biol Psychiatry 60 2006 1111 1120
16. T.P. Zahn, J.L. Rapoport, and C.L. Thompson Autonomic and behavioral effects of dextroamphetamine and placebo in normal and hyperactive prepubertal boys J Abnorm Child Psychol 8 1980 145 160
17. T.J. Spencer, J. Biederman, B.K. Madras, D.D. Dougherty, A.A. Bonab, and E. Livni Further evidence of dopamine transporter dysregulation in ADHD: A controlled PET imaging study using altropane Biol Psychiatry 62 2007 1059 1061
18. A. Jucaite, E. Fernell, C. Halldin, H. Forssberg, and L. Farde Reduced midbrain dopamine transporter binding in male adolescents with attention-deficit/hyperactivity disorder: association between striatal dopamine markers and motor hyperactivity Biol Psychiatry 57 2005 229 238
19. M.I. Seaman, J.B. Fisher, F. Chang, and K.K. Kidd Tandem duplication polymorphism upstream of the dopamine D4 receptor gene (DRD4) Am J Med Genet 88 1999 705 709
20. J.T. McCracken, S.L. Smalley, J.J. McGough, L. Crawford, M. Del'Homme, and R.M. Cantor Evidence for linkage of a tandem duplication polymorphism upstream of the dopamine D4 receptor gene (DRD4) with attention deficit hyperactivity disorder (ADHD) Mol Psychiatry 5 2000 531 536
21. V. Kustanovich, J. Ishii, L. Crawford, M. Yang, J.J. McGough, and J.T. McCracken Transmission disequilibrium testing of dopamine-related candidate gene polymorphisms in ADHD: confirmation of association with DRD4 and DRD5 Mol Psychiatry 9 2004 711 717
22. C. Kieling, T. Roman, A.E. Doyle, M.H. Hutz, and L.A. Rohde Association between DRD4 gene and performance of children with ADHD in a test of sustained attention Biol Psychiatry 60 2006 1163 1165
23. B. Kim, M.S. Koo, J.Y. Jun, I.H. Park, D.Y. Oh, and K.A. Cheon Association between dopamine D4 receptor gene polymorphism and scores on a continuous performance test in Korean children with attention deficit hyperactivity disorder Psychiatry Investig 6 2009 216 221
24. L.H. Tsai, I. Delalle, V.S. Caviness, T. Chae, and E. Harlow p35 is a neural-specific regulatory subunit of cyclin-dependent kinase 5 Nature 371 1994 419 423
25. J. Lew, Q.Q. Huang, Z. Qi, R.V. Winkfein, R. Aebersold, T. Hunt, and J.H. Wang A brain-specific activator of cyclin-dependent kinase 5 Nature 371 1994 423 426
26. X.H. Cai, K. Tomizawa, D. Tang, Y.F. Lu, A. Moriwaki, and M. Tokuda Changes in the expression of novel Cdk5 activator messenger RNA (p39nck5ai mRNA) during rat brain development Neurosci Res 28 1997 355 360
27. E.C. Gilmore, T. Ohshima, A.M. Goffinet, A.B. Kulkarni, and K. Herrup Cyclin-dependent kinase 5-deficient mice demonstrate novel developmental arrest in cerebral cortex J Neurosci 18 1998 6370 6377
28. T. Ohshima, J.M. Ward, C.G. Huh, G. Longenecker, Veeranna, and H.C. Pant Targeted disruption of the cyclin-dependent kinase 5 gene results in abnormal corticogenesis, neuronal pathology and perinatal death Proc Natl Acad Sci U S A 93 1996 11173 11178
29. T. Chae, Y.T. Kwon, R. Bronson, P. Dikkes, E. Li, and L.H. Tsai Mice lacking p35, a neuronal specific activator of Cdk5, display cortical lamination defects, siezures, and adult lethality Neuron 18 1997 29 42
30. Y.T. Kwon, and L.H. Tsai A novel disruption of cortical development in p35 (-/-) mice distinct from reeler J Comp Neurol 395 1998 510 522
31. M. Nikolic, H. Dudek, Y.T. Kwon, Y.F. Ramos, and L.H. Tsai The cdk5/p35 kinase is essential for neurite outgrowth during neuronal differentiation Genes Dev 10 1996 816 825
32. H.J. Wenzel, C.T. Tamse, and P.A. Schwartzkroin Dentate development in organotypic hippocampal slice cultures from p35 knockout mice Dev Neurosci 29 2007 99 112
33. J.A. Bibb, G. Snyder, A. Nishi, Z. Yan, L. Meijer, and A.A. Fienberg Phosphorylation of DARPP-32 by Cdk5 modulates dopamine signalling in neurons Nature 402 1999 669 671
34. J.A. Bibb, J. Chen, J.R. Taylor, P. Svenningsson, A. Nishi, and G.L. Snyder Effects of chronic exposure to cocaine are regulated by the neuronal protein cdk5 Nature 410 2001 376 380
35. D.R. Benavides, J.J. Quinn, P. Zhong, A.H. Hawasli, R.J. DiLeone, and J.W. Kansy Cdk5 modulates cocaine reward, motivation, and striatal neuron excitability J Neurosci 27 2007 12967 12976
36. J.R. Taylor, W.J. Lynch, H. Sanchez, P. Olausson, E.J. Nestler, and J.A. Bibb Inhibition of Cdk5 in the nucleus accumbens enhances the locomotor-activating and incentive-motivational effects of cocaine Proc Natl Acad Sci U S A 104 2007 4147 4152
37. M. Lindskog, P. Svenningsson, L. Pozzi, Y. Kim, A.A. Feinberg, and J.A. Bibb Involvement of DARPP-32 phosphorylation in the stimulant action of caffeine Nature 418 2002 774 778
38. S.K. Mani, A. Feinberg, J.P. O'Callaghan, G.L. Snyder, P.B. Allen, and P.K. Dash Requirement for DARPP-32 in progesterone-facilitated sexual receptivity in female rats and mice Science 287 2000 1053 1056
39. K. Chergui, P. Svenningsson, and P. Greengard Cyclin-dependent kinase 5 regulates dopaminergic and glutamatergic transmission in the striatum Proc Natl Acad Sci U S A 101 2004 2191 2196
40. L.Y. Moy, and L.H. Tsai Cyclin-dependent kinase 5 phosphorylates serine-31 of tyrosine hydroxylase and regulates its stability J Biol Chem 279 2004 54487 54493
41. J.W. Kansy, S.C. Daubner, A. Nishi, N. Sotogaku, M.D. Lloyd, and C. Nguyen Identification of tyrosine hydroxylase as a physiological substrate for Cdk5 J Neurochem 91 2004 374 384
42. T.C. Frank-Cannon, T. Tran, K.A. Ruhn, T.N. Martinez, J. Hong, and M. Marvin Parkin deficiency increases vulnerability to inflammation-related nigral degeneration J Neurosci 28 2008 10825 10834
43. B. Sahin, A. Hawasli, R.W. Greene, J.D. Molkentin, and J.A. Bibb Negative regulation of cyclin-dependent kinase 5 targets by protein kinase C Eur J Pharmacol 581 2008 270 275
44. L.C. Schmued, and J.H. Fallon Fluoro-Gold: A fluorescent retrograde axonal tracer with numerous unique properties Brain Res 377 1986 147 154
45. K.W. Roche, R. O'Brien, A.L. Mammen, J. Bernhardt, and R.L. Huganir Characterization of multiple phosphorylation sites on the AMPA receptor GluR1 subunit Neuron 16 1996 1179 1188
46. H.C. Hemmings, P. Greengard, H.Y.L. Tung, and P. Cohen DARPP-32, a dopamine-regulated neuronal phosphoprotein, is a potent inhibitor of protein phosphatase-1 Nature 310 1984 503 505
47. S.R. Sesack, and B.S. Bunney Pharmacological characterization of the receptor mediating electrophysiological responses to dopamine in the rat medial prefrontal cortex: A microiontophoretic study J Pharmacol Exp Ther 248 1989 1323 1333
48. D. Law-Tho, J.C. Hirsch, and F. Crepel Dopamine modulation of synaptic transmission in rat prefrontal cortex: An in vitro electrophysiological study Neurosci Res 21 1994 151 160
49. A.C. Grobin, and A.Y. Deutch Dopaminergic regulation of extracellular y-aminobutyric acid levels in the prefrontal cortex of the rat J Pharmacol Exp Ther 285 1998 350 357
50. P.W. Kalivas, and J. Stewart Dopamine transmission in the initiation and expression of drug- and stress-induced sensitization motor activity Brain Res Rev 16 1991 223 244
51. B.A. Sorg, N. Li, and W. Wu Dopamine D1 receptor activation in the medial prefrontal cortex prevents the expression of cocaine sensitization J Pharmacol Exp Ther 297 2001 501 508
52. K.E. Banks, and A. Gratton Possible involvement of medial prefrontal cortex in amphetamine-induced sensitization of mesolimbic dopamine function Eur J Pharmacol 282 1995 157 167
53. C.E. Beyer, and J. Steketee Cocaine sensitization: Modulation by dopamine D2 receptors Cereb Cortex 12 2002 526 535
54. F.A. Krapacher, E.C. Miewski, S. Ferreras, V. Pisano, M. Paolorossi, C. Hansen, and G. Paglini Mice lacking p35 display hyperactivity and paradoxical response to psychostimulants J Neurochemistry 113 2010 203 214
55. B.U. Keller, M. Hollman, S. Heinemann, and A. Konnerth Calcium influx through subunits GluR1/GluR3 of kainate/AMPA receptor channels is regulated by cAMP dependent protein kinase EMBO J 11 1992 891 896
56. T.G. Banke, D. Bowie, H. Lee, R.L. Huganir, A. Schousboe, and S.F. Traynelis Control of GluR1 AMPA receptor function by cAMP-dependent protein kinase J Neurosci 20 2000 89 102
57. R. Fukui, P. Svenningsson, T. Matsuishi, H. Higashi, A.C. Nairn, P. Greengard, and A. Nishi Effect of methylphenidate on dopamine/DARPP signalling in adult, but not young, mice J Neurochem 87 2003 1391 1401
58. M. Zhou, H. Rebholz, C. Brocia, J.L. Warner-Schmidt, A.A. Fienberg, and A.C. Nairn Forebrain overexpression of CK1delta leads to down-regulation of dopamine receptors and altered locomotor activity reminiscent of ADHD Proc Natl Acad Sci U S A 107 2010 4401 4406
59. A.J. Zametkin, T.E. Nordahl, M. Gross, A.C. King, W.E. Semple, and J. Rumsey Cerebral glucose metabolism in adults with hyperactivity of childhood onset N Engl J Med 323 1990 1361 1366
60. A.J. Zametkin, L.L. Liebenauer, G.A. Fitzgerald, A.C. King, D.V. Minkunas, and P. Herscovitch Brain metabolism in teenagers with attention-deficit hyperactivity disorder Arch Gen Psychiatry 50 1993 333 340
61. M. Ernst, L.L. Liebenauer, A.C. King, G.A. Fitzgerald, R.M. Cohen, and A.J. Zametkin Reduced brain metabolism in hyperactive girls J Am Acad Child Adolesc Psychiatry 33 1994 858 868
62. A.H. Hawasli, D. Benavides, C. Nguyen, J. Kansy, K. Hayashi, and P. Chambon Cyclin-dependent kinase 5 governs learning and synaptic plasticity via control of NMDAR degradation Nat Neurosci 10 2007 880 886
63. A.H. Hawasli, D. Koovakkattu, K. Hayashi, A.E. Anderson, C.M. Powell, and C.M. Sinton Regulation of hippocampal and behavioral excitability by cyclin-dependent kinase 5 PLoS ONE 4 2009 e5808
64. M.T. Alkire, R.J. Haier, N.K. Shah, and C.T. Anderson Positron emission tomography study of regional cerebral metabolism in humans during isoflurane anesthesia Anesthesiology 86 1997 549 557
65. Y.P. Wang, D.L. Mou, J.F. Song, Z.R. Rao, D. Li, and G. Ju Aberrant activation of CDK5 is involved in the pathogenesis of OPIDN J Neurochem 99 2006 186 197
66. M.F. Bouchard, D.C. Bellinger, R.O. Wright, and M.G. Weisskopf Attention-deficit/hyperactivity disorder and urinary metabolites of organophosphate pesticides Pediatrics 125 2010 e1270 e1277