Disrupted in schizophrenia 1 modulates medial prefrontal cortex pyramidal neuron activity through cAMP regulation of transient receptor potential c and small-conductance k+ channels

Biological Psychiatry

Volumn 76, Issue 6, 2014, Pages 476-485

  El Hassar, Lynda ^a   Simen, Arthur A ^a   Duque, Alvaro ^a   Patel, Kiran D ^a   Kaczmarek, Leonard K ^a   Arnsten, Amy F T ^a   Yeckel, Mark F ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

DISC1; IP3; mGluR5; persistent activity; prefrontal cortex

Indexed keywords

CYCLIC AMP; DISRUPTED IN SCHIZOPHRENIA 1 PROTEIN; FORSKOLIN; GUANFACINE; METABOTROPIC RECEPTOR; SHORT HAIRPIN RNA; SMALL CONDUCTANCE CALCIUM ACTIVATED POTASSIUM CHANNEL; TRANSIENT RECEPTOR POTENTIAL CHANNEL C; DISC1 PROTEIN, RAT; NERVE PROTEIN; TRANSIENT RECEPTOR POTENTIAL CATION CHANNEL, SUBFAMILY C, MEMBER 1;

ADULT; ANIMAL EXPERIMENT; ARTICLE; CALCIUM CELL LEVEL; CONTROLLED STUDY; DEPOLARIZATION; DIALYSIS; ENZYME REGULATION; HUMAN; HUMAN CELL; HYPERPOLARIZATION; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR SIGNALING; ION CURRENT; MALE; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN FUNCTION; PYRAMIDAL NERVE CELL; RAT; ANIMAL; CALCIUM SIGNALING; GENETICS; KNOCKOUT MOUSE; MEMBRANE POTENTIAL; METABOLISM; NERVE CELL; PHYSIOLOGY; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT;

ANIMALS; CALCIUM SIGNALING; CYCLIC AMP; MALE; MEMBRANE POTENTIALS; MICE, KNOCKOUT; NERVE TISSUE PROTEINS; NEURONS; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, METABOTROPIC GLUTAMATE; SIGNAL TRANSDUCTION; SMALL-CONDUCTANCE CALCIUM-ACTIVATED POTASSIUM CHANNELS; TRPC CATION CHANNELS;

EID: 84907598135     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2013.12.019     Document Type: Article

References (71)

1. P.S. Goldman-Rakic Cellular basis of working memory Neuron 14 1995 477 485
2. T.D. Cannon, W. Hennah, T.G. van Erp, P.M. Thompson, J. Lonnqvist, and M. Huttunen et al. Association of DISC1/TRAX haplotypes with schizophrenia, reduced prefrontal gray matter, and impaired short- and long-term memory Arch Gen Psychiatry 62 2005 1205 1213
3. T.L. Gasperoni, J. Ekelund, M. Huttunen, C.G. Palmer, A. Tuulio-Henriksson, and J. Lonnqvist et al. Genetic linkage and association between chromosome 1q and working memory function in schizophrenia Am J Med Genet B Neuropsychiatr Genet 116B 2003 8 16
4. H.Y. Tan, Q. Chen, S. Sust, J.W. Buckholtz, J.D. Meyers, and M.F. Egan et al. Epistasis between catechol-O-methyltransferase and type II metabotropic glutamate receptor 3 genes on working memory brain function Proc Natl Acad Sci U S A 104 2007 12536 12541
5. J. Wedenoja, A. Tuulio-Henriksson, J. Suvisaari, A. Loukola, T. Paunio, and T. Partonen et al. Replication of association between working memory and Reelin, a potential modifier gene in schizophrenia Biol Psychiatry 67 2010 983 991
6. T. Sigurdsson, K.L. Stark, M. Karayiorgou, J.A. Gogos, and J.A. Gordon Impaired hippocampal-prefrontal synchrony in a genetic mouse model of schizophrenia Nature 464 2010 763 767
7. L.A. Glantz, and D.A. Lewis Decreased dendritic spine density on prefrontal cortical pyramidal neurons in schizophrenia Arch Gen Psychiatry 57 2000 65 73
8. K. Broadbelt, W. Byne, and L.B. Jones Evidence for a decrease in basilar dendrites of pyramidal cells in schizophrenic medial prefrontal cortex Schizophr Res 58 2002 75 81
9. M. Bleich-Cohen, M. Kupchik, M. Gruberger, M. Kotler, and T. Hendler Never resting region - mPFC in schizophrenia Schizophr Res 140 2012 155 158
10. A.F. Arnsten, M.J. Wang, and C.D. Paspalas Neuromodulation of thought: Flexibilities and vulnerabilities in prefrontal cortical network synapses Neuron 76 2012 223 239
11. C.D. Paspalas, M. Wang, and A.F. Arnsten Constellation of HCN channels and cAMP regulating proteins in dendritic spines of the primate prefrontal cortex: Potential substrate for working memory deficits in schizophrenia Cereb Cortex 23 2013 1643 1654
12. A. Hayashi-Takagi, M. Takaki, N. Graziane, S. Seshadri, H. Murdoch, and A.J. Dunlop et al. Disrupted-in-Schizophrenia 1 (DISC1) regulates spines of the glutamate synapse via Rac1 Nat Neurosci 13 2010 327 332
13. Q. Wang, E.I. Charych, V.L. Pulito, J.B. Lee, N.M. Graziane, and R.A. Crozier et al. The psychiatric disease risk factors DISC1 and TNIK interact to regulate synapse composition and function Mol Psychiatry 16 2011 1006 1023
14. J. Wei, N.M. Graziane, H. Wang, P. Zhong, Q. Wang, and W. Liu et al. Regulation of N-Methyl-D-Aspartate receptors by Disrupted-in-Schizophrenia-1 [published online ahead of print July 29] Biol Psychiatry 2013
15. A.M. Hagenston, J.S. Fitzpatrick, and M.F. Yeckel MGluR-mediated calcium waves that invade the soma regulate firing in layer V medial prefrontal cortical pyramidal neurons Cereb Cortex 18 2008 407 423
16. L.D. Partridge, D. Swandulla, and T.H. Muller Modulation of calcium-activated non-specific cation currents by cyclic AMP-dependent phosphorylation in neurones of Helix J Physiol 429 1990 131 145
17. 2+ wave-dependent activation of SK and TRPC channels J Physiol 589 2011 3211 3229
18. A.M. Hagenston, N.D. Rudnick, C.E. Boone, and M.F. Yeckel 2-Aminoethoxydiphenyl-borate (2-APB) increases excitability in pyramidal neurons Cell Calcium 45 2009 310 317
19. N.J. Gamo, A. Duque, C.D. Paspalas, A. Kata, R. Fine, and L. Boven et al. Role of disrupted in schizophrenia 1 (DISC1) in stress-induced prefrontal cognitive dysfunction Transl Psychiatry 3 2013 e328
20. J.C. Magee Dendritic hyperpolarization-activated currents modify the integrative properties of hippocampal CA1 pyramidal neurons J Neurosci 18 1998 7613 7624
21. N.P. Poolos, M. Migliore, and D. Johnston Pharmacological upregulation of h-channels reduces the excitability of pyramidal neuron dendrites Nat Neurosci 5 2002 767 774
22. J.K. Millar, B.S. Pickard, S. Mackie, R. James, S. Christie, and S.R. Buchanan et al. DISC1 and PDE4B are interacting genetic factors in schizophrenia that regulate cAMP signaling Science 310 2005 1187 1191
23. H. Murdoch, S. Mackie, D.M. Collins, E.V. Hill, G.B. Bolger, and E. Klussmann et al. Isoform-selective susceptibility of DISC1/phosphodiesterase-4 complexes to dissociation by elevated intracellular cAMP levels J Neurosci 27 2007 9513 9524
24. T. Soda, C. Frank, K. Ishizuka, A. Baccarella, Y.U. Park, and Z. Flood et al. DISC1-ATF4 transcriptional repression complex: Dual regulation of the cAMP-PDE4 cascade by DISC1 Mol Psychiatry 18 2013 898 908
25. Y. Ren, L.F. Barnwell, J.C. Alexander, F.D. Lubin, J.P. Adelman, and P.J. Pfaffinger et al. Regulation of surface localization of the small conductance Ca2+-activated potassium channel, Sk2, through direct phosphorylation by cAMP-dependent protein kinase J Biol Chem 281 2006 11769 11779
26. P. Pedarzani, and J.F. Storm PKA mediates the effects of monoamine transmitters on the K+ current underlying the slow spike frequency adaptation in hippocampal neurons Neuron 11 1993 1023 1035
27. J.K. Millar, J.C. Wilson-Annan, S. Anderson, S. Christie, M.S. Taylor, and C.A. Semple et al. Disruption of two novel genes by a translocation co-segregating with schizophrenia Hum Mol Genet 9 2000 1415 1423
28. K. Ishizuka, M. Paek, A. Kamiya, and A. Sawa A review of Disrupted-In-Schizophrenia-1 (DISC1): Neurodevelopment, cognition, and mental conditions Biol Psychiatry 59 2006 1189 1197
29. T. Cash-Padgett, and H. Jaaro-Peled DISC1 mouse models as a tool to decipher gene-environment interactions in psychiatric disorders Front Behav Neurosci 7 2013 113
30. B.J. Duff, K.A. Macritchie, T.W. Moorhead, S.M. Lawrie, and D.H. Blackwood Human brain imaging studies of DISC1 in schizophrenia, bipolar disorder and depression: A systematic review Schizophr Res 147 2013 1 13
31. T. Hikida, N.J. Gamo, and A. Sawa DISC1 as a therapeutic target for mental illnesses Expert Opin Ther Targets 16 2012 1151 1160
32. J.E. Chubb, N.J. Bradshaw, D.C. Soares, D.J. Porteous, and J.K. Millar The DISC locus in psychiatric illness Mol Psychiatry 13 2008 36 64
33. R. Hashimoto, T. Numakawa, T. Ohnishi, E. Kumamaru, Y. Yagasaki, and T. Ishimoto et al. Impact of the DISC1 Ser704Cys polymorphism on risk for major depression, brain morphology and ERK signaling Hum Mol Genet 15 2006 3024 3033
34. H. Kilpinen, T. Ylisaukko-Oja, W. Hennah, O.M. Palo, T. Varilo, and R. Vanhala et al. Association of DISC1 with autism and Asperger syndrome Mol Psychiatry 13 2008 187 196
35. C.P. Austin, B. Ky, L. Ma, J.A. Morris, and P.J. Shughrue Expression of Disrupted-In-Schizophrenia-1, a schizophrenia-associated gene, is prominent in the mouse hippocampus throughout brain development Neuroscience 124 2004 3 10
36. A. Kamiya, K. Kubo, T. Tomoda, M. Takaki, R. Youn, and Y. Ozeki et al. A schizophrenia-associated mutation of DISC1 perturbs cerebral cortex development Nat Cell Biol 7 2005 1167 1178
37. B. Kirkpatrick, L. Xu, N. Cascella, Y. Ozeki, A. Sawa, and R.C. Roberts DISC1 immunoreactivity at the light and ultrastructural level in the human neocortex J Comp Neurol 497 2006 436 450
38. K. Miyoshi, A. Honda, K. Baba, M. Taniguchi, K. Oono, and T. Fujita et al. Disrupted-In-Schizophrenia 1, a candidate gene for schizophrenia, participates in neurite outgrowth Mol Psychiatry 8 2003 685 694
39. R.L. Faulkner, M.H. Jang, X.B. Liu, X. Duan, K.A. Sailor, and J.Y. Kim et al. Development of hippocampal mossy fiber synaptic outputs by new neurons in the adult brain Proc Natl Acad Sci U S A 105 2008 14157 14162
40. J.K. Millar, S. Mackie, S.J. Clapcote, H. Murdoch, B.S. Pickard, and S. Christie et al. Disrupted in schizophrenia 1 and phosphodiesterase 4B: Towards an understanding of psychiatric illness J Physiol 584 2007 401 405
41. M. Wang, B.P. Ramos, C.D. Paspalas, Y. Shu, A. Simen, and A. Duque et al. Alpha2A-adrenoceptors strengthen working memory networks by inhibiting cAMP-HCN channel signaling in prefrontal cortex Cell 129 2007 397 410
42. MF SA Yeckel, J.S. Fitzpatrick, D. Hertle, A.M. Hagenston, and R.T. Garner Intracellular calcium waves transmit synaptic information to the nucleus in hippocampal pyramidal neurons S.M. Dudek, Transcriptional Regulation By Neuronal Activity 2008 Springer Science Publishing New York 73 89
43. J. Tegner, A. Compte, and X.J. Wang The dynamical stability of reverberatory neural circuits Biol Cybern 87 2002 471 481
44. X.J. Wang Synaptic reverberation underlying mnemonic persistent activity Trends Neurosci 24 2001 455 463
45. J.J. Gargus, E. Fantino, and G.A. Gutman A piece in the puzzle: An ion channel candidate gene for schizophrenia Mol Med Today 4 1998 518 524
46. O. Wittekindt, A. Jauch, E. Burgert, L. Scharer, H. Holtgreve-Grez, and G. Yvert et al. The human small conductance calcium-regulated potassium channel gene (hSKCa3) contains two CAG repeats in exon 1, is on chromosome 1q21.3, and shows a possible association with schizophrenia Neurogenetics 1 1998 259 265
47. K.G. Chandy, E. Fantino, O. Wittekindt, K. Kalman, L.L. Tong, and T.H. Ho et al. Isolation of a novel potassium channel gene hSKCa3 containing a polymorphic CAG repeat: A candidate for schizophrenia and bipolar disorder? Mol Psychiatry 3 1998 32 37
48. A.G. Cardno, T. Bowen, C.A. Guy, L.A. Jones, G. McCarthy, and N.M. Williams et al. CAG repeat length in the hKCa3 gene and symptom dimensions in schizophrenia Biol Psychiatry 45 1999 1592 1596
49. I.S. Yoon, P.P. Li, K.P. Siu, J.L. Kennedy, F. Macciardi, and R.G. Cooke et al. Altered TRPC7 gene expression in bipolar-I disorder Biol Psychiatry 50 2001 620 626
50. M. Stocker, K. Hirzel, D. D'Hoedt, and P. Pedarzani Matching molecules to function: Neuronal Ca2+-activated K+ channels and afterhyperpolarizations Toxicon 43 2004 933 949
51. S. Andreopoulos, M. Wasserman, K. Woo, P.P. Li, and J.J. Warsh Chronic lithium treatment of B lymphoblasts from bipolar disorder patients reduces transient receptor potential channel 3 levels Pharmacogenomics J 4 2004 365 373
52. D.V. Madison, and R.A. Nicoll Cyclic adenosine 3',5'-monophosphate mediates beta-receptor actions of noradrenaline in rat hippocampal pyramidal cells J Physiol 372 1986 245 259
53. J.F. Storm, P. Pedarzani, T. Haug, and T. Winther Modulation of K+ channels in hippocampal neurons: Transmitters acting via cyclic AMP enhance the excitability of hippocampal neurons through kinase-dependent and -independent modulation of AHP- and h-channels K. Kuba, H. Higashida, D.A. Brown, T. Yoshioka, Slow Synaptic Responses and Modulation 2000 Springer-Verlag Tokyo 78 92
54. N. DeSouza, S. Reiken, K. Ondrias, Y.M. Yang, S. Matkovich, and A.R. Marks Protein kinase A and two phosphatases are components of the inositol 1,4,5-trisphosphate receptor macromolecular signaling complex J Biol Chem 277 2002 39397 39400
55. J.K. Foskett, C. White, K.H. Cheung, and D.O. Mak Inositol trisphosphate receptor Ca2+ release channels Physiol Rev 87 2007 593 658
56. J.S. Fitzpatrick, A.M. Hagenston, D.N. Hertle, K.E. Gipson, L. Bertetto-D'Angelo, and M.F. Yeckel Inositol-1,4,5-trisphosphate receptor-mediated Ca2+ waves in pyramidal neuron dendrites propagate through hot spots and cold spots J Physiol 587 2009 1439 1459
57. P. Congar, R. Khazipov, and Y. Ben-Ari Direct demonstration of functional disconnection by anoxia of inhibitory interneurons from excitatory inputs in rat hippocampus J Neurophysiol 73 1995 421 426
58. T.J. Jentsch Neuronal KCNQ potassium channels: Physiology and role in disease Nat Rev Neurosci 1 2000 21 30
59. J.R. Taylor, S. Birnbaum, R. Ubriani, and A.F. Arnsten Activation of cAMP-dependent protein kinase A in prefrontal cortex impairs working memory performance J Neurosci 19 1999 RC23
60. B.P. Ramos, D. Stark, L. Verduzco, C.H. van Dyck, and A.F. Arnsten Alpha2A-adrenoceptor stimulation improves prefrontal cortical regulation of behavior through inhibition of cAMP signaling in aging animals Learn Mem 13 2006 770 776
61. A.F. Arnsten Stress signalling pathways that impair prefrontal cortex structure and function Nat Rev Neurosci 10 2009 410 422
62. J.S. Franowicz, and A.F. Arnsten Actions of alpha-2 noradrenergic agonists on spatial working memory and blood pressure in rhesus monkeys appear to be mediated by the same receptor subtype Psychopharmacology (Berl) 162 2002 304 312
63. J.S. Franowicz, and A.F. Arnsten The alpha-2a noradrenergic agonist, guanfacine, improves delayed response performance in young adult rhesus monkeys Psychopharmacology (Berl) 136 1998 8 14
64. J.S. Franowicz, and A.F. Arnsten Treatment with the noradrenergic alpha-2 agonist clonidine, but not diazepam, improves spatial working memory in normal young rhesus monkeys Neuropsychopharmacology 21 1999 611 621
65. A.F. Arnsten, and A.G. Dudley Methylphenidate improves prefrontal cortical cognitive function through alpha2 adrenoceptor and dopamine D1 receptor actions: Relevance to therapeutic effects in attention deficit hyperactivity disorder Behav Brain Funct 1 2005 2
66. A.F. Arnsten, J.X. Cai, and P.S. Goldman-Rakic The alpha-2 adrenergic agonist guanfacine improves memory in aged monkeys without sedative or hypotensive side effects: Evidence for alpha-2 receptor subtypes J Neurosci 8 1988 4287 4298
67. D. Kolar, A. Keller, M. Golfinopoulos, L. Cumyn, C. Syer, and L. Hechtman Treatment of adults with attention-deficit/hyperactivity disorder Neuropsychiatr Dis Treat 4 2008 389 403
68. P. Jerie Clinical experience with guanfacine in long-term treatment of hypertension. Part II: Adverse reactions to guanfacine Br J Clin Pharmacol 10 suppl 1 1980 157S 164S
69. D. Kaminer, S. Seedat, and D.J. Stein Post-traumatic stress disorder in children World Psychiatry 4 2005 121 125
70. J.R. Kiechel Pharmacokinetics and metabolism of guanfacine in man: A review Br J Clin Pharmacol 10 suppl 1 1980 25S 32S
71. H. Koike, P.A. Arguello, M. Kvajo, M. Karayiorgou, and J.A. Gogos Disc1 is mutated in the 129S6/SvEv strain and modulates working memory in mice Proc Natl Acad Sci U S A 103 2006 3693 3697