Altered Expression of CDC42 Signaling Pathway Components in Cortical Layer 3 Pyramidal Cells in Schizophrenia

Biological Psychiatry

Volumn 78, Issue 11, 2015, Pages 775-785

  Datta, Dibyadeep ^a   Arion, Dominique ^a   Corradi, John P ^b   Lewis, David A ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b BRISTOL MYERS SQUIBB   (United States)

Author keywords

Actin cytoskeleton; CDC42; Dendritic spine; mRNA; Prefrontal cortex; Schizophrenia

Indexed keywords

MESSENGER RNA; NEUROLEPTIC AGENT; P21 ACTIVATED KINASE; P21 ACTIVATED KINASE 3; PROTEIN CDC42; PROTEIN SERINE THREONINE KINASE; ARHGDIA PROTEIN, HUMAN; BENZODIAZEPINE DERIVATIVE; CDC42EP4 PROTEIN, HUMAN; GUANINE NUCLEOTIDE BINDING PROTEIN; HALOPERIDOL; LIM KINASE; LIMK1 PROTEIN, HUMAN; LIMK2 PROTEIN, HUMAN; OLANZAPINE; PAK3 PROTEIN, HUMAN; RHO GUANINE NUCLEOTIDE DISSOCIATION INHIBITOR 1;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CORTEX LAYER III; DORSOLATERAL PREFRONTAL CORTEX; DOWN REGULATION; FEMALE; GENETIC TRANSCRIPTION; HAPLORHINI; HUMAN; HUMAN TISSUE; LASER MICRODISSECTION; MAJOR CLINICAL STUDY; MALE; MICROARRAY ANALYSIS; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; QUANTITATIVE ANALYSIS; SCHIZOPHRENIA; SIGNAL TRANSDUCTION; ANIMAL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; LASER CAPTURE MICRODISSECTION; MACACA FASCICULARIS; METABOLISM; MIDDLE AGED; PATHOLOGY; PHYSIOLOGY; PREFRONTAL CORTEX;

ADULT; ANIMALS; ANTIPSYCHOTIC AGENTS; BENZODIAZEPINES; CDC42 GTP-BINDING PROTEIN; FEMALE; GENE EXPRESSION REGULATION; GTP-BINDING PROTEIN REGULATORS; HALOPERIDOL; HUMANS; LASER CAPTURE MICRODISSECTION; LIM KINASES; MACACA FASCICULARIS; MALE; MIDDLE AGED; P21-ACTIVATED KINASES; PREFRONTAL CORTEX; RHO GUANINE NUCLEOTIDE DISSOCIATION INHIBITOR ALPHA; SCHIZOPHRENIA; SIGNAL TRANSDUCTION;

EID: 84960799274     PISSN: 00063223     EISSN: 18732402     Source Type: Journal    
DOI: 10.1016/j.biopsych.2015.03.030     Document Type: Article

References (79)

1. R.S. Kahn, and R.S. Keefe Schizophrenia is a cognitive illness: Time for a change in focus JAMA Psychiatry 70 2013 1107 1112
2. D.R. Weinberger Implications of normal brain development for the pathogenesis of schizophrenia Arch Gen Psychiatry 44 1987 660 669
3. L.V. Kristiansen, I. Huerta, M. Beneyto, and J.H. Meador-Woodruff NMDA receptors and schizophrenia Curr Opin Pharmacol 7 2007 48 55
4. K. Merritt, P. McGuire, and A. Egerton Relationship between glutamate dysfunction and symptoms and cognitive function in psychosis Front Psychiatry 4 2013 151
5. D.C. Javitt, and S.R. Zukin Recent advances in the phencyclidine model of schizophrenia Am J Psychiatry 148 1991 1301 1308
6. J.T. Coyle The GABA-glutamate connection in schizophrenia: Which is the proximate cause? Biochem Pharmacol 68 2004 1507 1514
7. C. Konradi, and S. Heckers Molecular aspects of glutamate dysregulation: Implications for schizophrenia and its treatment Pharmacol Ther 97 2003 153 179
8. B. Moghaddam Targeting metabotropic glutamate receptors for treatment of the cognitive symptoms of schizophrenia Psychopharmacology (Berl) 174 2004 39 44
9. L.J. Garey, W.Y. Ong, T.S. Patel, M. Kanani, A. Davis, A.M. Mortimer, and et al. Reduced dendritic spine density on cerebral cortical pyramidal neurons in schizophrenia J Neurol Neurosurg Psychiatry 65 1998 446 453
10. 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
11. G.T. Konopaske, N. Lange, J.T. Coyle, and F.M. Benes Prefrontal cortical dendritic spine pathology in schizophrenia and bipolar disorder JAMA Psychiatry 71 2014 1323 1331
12. R.A. Sweet, R.A. Henteleff, W. Zhang, A.R. Sampson, and D.A. Lewis Reduced dendritic spine density in auditory cortex of subjects with schizophrenia Neuropsychopharmacology 34 2009 374 389
13. S.E. Arnold, B.R. Franz, R.C. Gur, R.E. Gur, R.M. Shapiro, P.J. Moberg, and et al. Smaller neuron size in schizophrenia in hippocampal subfields that mediate cortical-hippocampal interactions Am J Psychiatry 152 1995 738 748
14. J.N. Pierri, C.L. Volk, S. Auh, A. Sampson, and D.A. Lewis Decreased somal size of deep layer 3 pyramidal neurons in the prefrontal cortex of subjects with schizophrenia Arch Gen Psychiatry 58 2001 466 473
15. G. Rajkowska, L.D. Selemon, and P.S. Goldman-Rakic Neuronal and glial somal size in the prefrontal cortex: A postmortem morphometric study of schizophrenia and Huntington disease Arch Gen Psychiatry 55 1998 215 224
16. R.A. Sweet, J.N. Pierri, S. Auh, A.R. Sampson, and D.A. Lewis Reduced pyramidal cell somal volume in auditory association cortex of subjects with schizophrenia Neuropsychopharmacology 28 2003 599 609
17. N. Kolluri, Z. Sun, A.R. Sampson, and D.A. Lewis Lamina-specific reductions in dendritic spine density in the prefrontal cortex of subjects with schizophrenia Am J Psychiatry 162 2005 1200 1202
18. R.A. Sweet, S.E. Bergen, Z. Sun, A.R. Sampson, J.N. Pierri, and D.A. Lewis Pyramidal cell size reduction in schizophrenia: Evidence for involvement of auditory feedforward circuits Biol Psychiatry 55 2004 1128 1137
19. J.R. Glausier, and D.A. Lewis Dendritic spine pathology in schizophrenia Neuroscience 251 2013 90 107
20. J.J. Hill, T. Hashimoto, and D.A. Lewis Molecular mechanisms contributing to dendritic spine alterations in the prefrontal cortex of subjects with schizophrenia Mol Psychiatry 11 2006 557 566
21. M. Ide, and D.A. Lewis Altered cortical CDC42 signaling pathways in schizophrenia: Implications for dendritic spine deficits Biol Psychiatry 68 2010 25 32
22. T. Bonhoeffer, and R. Yuste Spine motility. Phenomenology, mechanisms, and function Neuron 35 2002 1019 1027
23. A.J. Koleske Molecular mechanisms of dendrite stability Nat Rev Neurosci 14 2013 536 550
24. M. Negishi, and H. Katoh Rho family GTPases and dendrite plasticity Neuroscientist 11 2005 187 191
25. T. Tada, and M. Sheng Molecular mechanisms of dendritic spine morphogenesis Curr Opin Neurobiol 16 2006 95 101
26. D. Arion, T. Unger, D.A. Lewis, and K. Mirnics Molecular markers distinguishing supragranular and infragranular layers in the human prefrontal cortex Eur J Neurosci 25 2007 1843 1854
27. G. Joberty, R.R. Perlungher, P.J. Sheffield, M. Kinoshita, M. Noda, T. Haystead, and et al. Borg proteins control septin organization and are negatively regulated by Cdc42 Nat Cell Biol 3 2001 861 866
28. D.C. Edwards, L.C. Sanders, G.M. Bokoch, and G.N. Gill Activation of LIM-kinase by Pak1 couples Rac/Cdc42 GTPase signalling to actin cytoskeletal dynamics Nat Cell Biol 1 1999 253 259
29. P. Hotulainen, and C.C. Hoogenraad Actin in dendritic spines: Connecting dynamics to function J Cell Biol 189 2010 619 629
30. E. Manser, T. Leung, H. Salihuddin, Z.S. Zhao, and L. Lim A brain serine/threonine protein kinase activated by Cdc42 and Rac1 Nature 367 1994 40 46
31. M.C. Parrini, M. Lei, S.C. Harrison, and B.J. Mayer Pak1 kinase homodimers are autoinhibited in trans and dissociated upon activation by Cdc42 and Rac1 Mol Cell 9 2002 73 83
32. T.J. Chen, S. Gehler, A.E. Shaw, J.R. Bamburg, and P.C. Letourneau Cdc42 participates in the regulation of ADF/cofilin and retinal growth cone filopodia by brain derived neurotrophic factor J Neurobiol 66 2006 103 114
33. P. Hotulainen, E. Paunola, M.K. Vartiainen, and P. Lappalainen Actin-depolymerizing factor and cofilin-1 play overlapping roles in promoting rapid F-actin depolymerization in mammalian nonmuscle cells Mol Biol Cell 16 2005 649 664
34. T. Sumi, K. Matsumoto, and T. Nakamura Specific activation of LIM kinase 2 via phosphorylation of threonine 505 by ROCK, a Rho-dependent protein kinase J Biol Chem 276 2001 670 676
35. S.E. Newey, V. Velamoor, E.E. Govek, and L. Van Aelst Rho GTPases, dendritic structure, and mental retardation J Neurobiol 64 2005 58 74
36. American Psychiatric Association Diagnostic and Statistical Manual of Mental Disorders 4th ed. 1994 American Psychiatric Press Washington, DC
37. D.W. Volk, S.M. Eggan, and D.A. Lewis Alterations in metabotropic glutamate receptor 1alpha and regulator of G protein signaling 4 in the prefrontal cortex in schizophrenia Am J Psychiatry 167 2010 1489 1498
38. A.A. Curley, D. Arion, D.W. Volk, J.K. Asafu-Adjei, A.R. Sampson, K.N. Fish, and et al. Cortical deficits of glutamic acid decarboxylase 67 expression in schizophrenia: Clinical, protein, and cell type-specific features Am J Psychiatry 168 2011 921 929
39. S.M. Eggan, M.S. Lazarus, S.R. Stoyak, D.W. Volk, J.R. Glausier, Z.J. Huang, and et al. Cortical glutamic acid decarboxylase 67 deficiency results in lower cannabinoid 1 receptor messenger RNA expression: Implications for schizophrenia Biol Psychiatry 71 2012 114 119
40. S. Kimoto, H.H. Bazmi, and D.A. Lewis Lower expression of glutamic acid decarboxylase 67 in the prefrontal cortex in schizophrenia: Contribution of altered regulation by Zif268 Am J Psychiatry 171 2014 969 978
41. T. Hashimoto, H.H. Bazmi, K. Mirnics, Q. Wu, A.R. Sampson, and D.A. Lewis Conserved regional patterns of GABA-related transcript expression in the neocortex of subjects with schizophrenia Am J Psychiatry 165 2008 479 489
42. T. Hashimoto, D.W. Volk, S.M. Eggan, K. Mirnics, J.N. Pierri, Z. Sun, and et al. Gene expression deficits in a subclass of GABA neurons in the prefrontal cortex of subjects with schizophrenia J Neurosci 23 2003 6315 6326
43. D.W. Volk, M.C. Austin, J.N. Pierri, A.R. Sampson, and D.A. Lewis Decreased glutamic acid decarboxylase67 messenger RNA expression in a subset of prefrontal cortical gamma-aminobutyric acid neurons in subjects with schizophrenia Arch Gen Psychiatry 57 2000 237 245
44. D. Arion, J.P. Corradi, T. Shaowu, D. Datta, F. Boothe, A. He, and et al. Distinctive transcriptome alterations of prefrontal pyramidal neurons in schizophrenia and schizoaffective disorder [published online ahead of print Jan 6] Mol Psychiatry. 2015
45. D.W. Volk, A. Chitrapu, J.R. Edelson, and D.A. Lewis Chemokine receptors and cortical interneuron dysfunction in schizophrenia [published online ahead of print Nov 11] Schizophr Res. 2014
46. K.A. Dorph-Petersen, J.N. Pierri, J.M. Perel, Z. Sun, A.R. Sampson, and D.A. Lewis The influence of chronic exposure to antipsychotic medications on brain size before and after tissue fixation: A comparison of haloperidol and olanzapine in macaque monkeys Neuropsychopharmacology 30 2005 1649 1661
47. D.W. Volk, T. Matsubara, S. Li, E.J. Sengupta, D. Georgiev, Y. Minabe, and et al. Deficits in transcriptional regulators of cortical parvalbumin neurons in schizophrenia Am J Psychiatry 169 2012 1082 1091
48. T. Hashimoto, D. Arion, T. Unger, J.G. Maldonado-Aviles, H.M. Morris, D.W. Volk, and et al. Alterations in GABA-related transcriptome in the dorsolateral prefrontal cortex of subjects with schizophrenia Mol Psychiatry 13 2008 147 161
49. D. Datta, D. Arion, and D.A. Lewis Developmental expression patterns of GABAA receptor subunits in layer 3 and 5 pyramidal cells of monkey prefrontal cortex [published online ahead of print Mar 7] Cereb Cortex. 2014
50. X. Wang, Y. Lin, C. Song, E. Sibille, and G.C. Tseng Detecting disease-associated genes with confounding variable adjustment and the impact on genomic meta-analysis: With application to major depressive disorder BMC Bioinformatics 13 2012 52
51. J. Li, and G.C. Tseng An adaptively weighted statistic for detecting differential gene expression when combining multiple transcriptomic studies Ann Appl Stat 5 2011 994 1019
52. Y. Benjamini, and Y. Hochberg Controlling the false discovery rate - a practical and powerful approach to multiple testing J R Stat Soc Series B Stat Methodol 57 1995 289 300
53. G.D. Hoftman, D.W. Volk, H.H. Bazmi, S. Li, A.R. Sampson, and D.A. Lewis Altered cortical expression of GABA-related genes in schizophrenia: Illness progression vs developmental disturbance Schizophr Bull 41 2015 180 191
54. J.R. Glausier, and D.A. Lewis Selective pyramidal cell reduction of GABA(A) receptor alpha1 subunit messenger RNA expression in schizophrenia Neuropsychopharmacology 36 2011 2103 2110
55. M.S. Sodhi, M. Simmons, R. McCullumsmith, V. Haroutunian, and J.H. Meador-Woodruff Glutamatergic gene expression is specifically reduced in thalamocortical projecting relay neurons in schizophrenia Biol Psychiatry 70 2011 646 654
56. L. Luo Rho GTPases in neuronal morphogenesis Nat Rev Neurosci 1 2000 173 180
57. J.P. Gorvel, T.C. Chang, J. Boretto, T. Azuma, and P. Chavrier Differential properties of D4/LyGDI versus RhoGDI: Phosphorylation and rho GTPase selectivity FEBS Lett 422 1998 269 273
58. G.R. Hoffman, N. Nassar, and R.A. Cerione Structure of the Rho family GTP-binding protein Cdc42 in complex with the multifunctional regulator RhoGDI Cell 100 2000 345 356
59. P.H. Chia, P. Li, and K. Shen Cell biology in neuroscience: Cellular and molecular mechanisms underlying presynapse formation J Cell Biol 203 2013 11 22
60. Y. Ouyang, M. Wong, F. Capani, N. Rensing, C.S. Lee, Q. Liu, and et al. Transient decrease in F-actin may be necessary for translocation of proteins into dendritic spines Eur J Neurosci 22 2005 2995 3005
61. R.W. Scott, and M.F. Olson LIM kinases: Function, regulation and association with human disease J Mol Med (Berl) 85 2007 555 568
62. T. Sumi, K. Matsumoto, Y. Takai, and T. Nakamura Cofilin phosphorylation and actin cytoskeletal dynamics regulated by rho- and Cdc42-activated LIM-kinase 2 J Cell Biol 147 1999 1519 1532
63. H. Murakoshi, H. Wang, and R. Yasuda Local, persistent activation of Rho GTPases during plasticity of single dendritic spines Nature 472 2011 100 104
64. K. Hayashi, T. Ohshima, M. Hashimoto, and K. Mikoshiba Pak1 regulates dendritic branching and spine formation Dev Neurobiol 67 2007 655 669
65. H. Zhang, D.J. Webb, H. Asmussen, S. Niu, and A.F. Horwitz A GIT1/PIX/Rac/PAK signaling module regulates spine morphogenesis and synapse formation through MLC J Neurosci 25 2005 3379 3388
66. A. Hayashi-Takagi, Y. Araki, M. Nakamura, B. Vollrath, S.G. Duron, Z. Yan, and et al. PAKs inhibitors ameliorate schizophrenia-associated dendritic spine deterioration in vitro and in vivo during late adolescence Proc Natl Acad Sci U S A 111 2014 6461 6466
67. D.A. Lewis, A.A. Curley, J.R. Glausier, and D.W. Volk Cortical parvalbumin interneurons and cognitive dysfunction in schizophrenia Trends Neurosci 35 2012 57 67
68. Z. Zhao, J. Xu, J. Chen, S. Kim, M. Reimers, S.A. Bacanu, and et al. Transcriptome sequencing and genome-wide association analyses reveal lysosomal function and actin cytoskeleton remodeling in schizophrenia and bipolar disorder Mol Psychiatry 20 2015 536 572
69. M. Fromer, A.J. Pocklington, D.H. Kavanagh, H.J. Williams, S. Dwyer, P. Gormley, and et al. De novo mutations in schizophrenia implicate synaptic networks Nature 506 2014 179 184
70. M. Pathania, E.C. Davenport, J. Muir, D.F. Sheehan, G. Lopez-Domenech, and J.T. Kittler The autism and schizophrenia associated gene CYFIP1 is critical for the maintenance of dendritic complexity and the stabilization of mature spines Transl Psychiatry 4 2014 e374
71. K.J. Yoon, H.N. Nguyen, G. Ursini, F. Zhang, N.S. Kim, Z. Wen, and et al. Modeling a genetic risk for schizophrenia in iPSCs and mice reveals neural stem cell deficits associated with adherens junctions and polarity Cell Stem Cell 15 2014 79 91
72. M.D. Rubio, V. Haroutunian, and J.H. Meador-Woodruff Abnormalities of the Duo/Ras-related C3 botulinum toxin substrate 1/p21-activated kinase 1 pathway drive myosin light chain phosphorylation in frontal cortex in schizophrenia Biol Psychiatry 71 2012 906 914
73. B.K. Lipska, S.N. Mitkus, S.V. Mathew, R. Fatula, T.M. Hyde, D.R. Weinberger, and et al. Functional genomics in postmortem human brain: Abnormalities in a DISC1 molecular pathway in schizophrenia Dialogues Clin Neurosci 8 2006 353 357
74. B.K. Lipska, T. Peters, T.M. Hyde, N. Halim, C. Horowitz, S. Mitkus, and et al. Expression of DISC1 binding partners is reduced in schizophrenia and associated with DISC1 SNPs Hum Mol Genet 15 2006 1245 1258
75. 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
76. N.J. Brandon, and A. Sawa Linking neurodevelopmental and synaptic theories of mental illness through DISC1 Nat Rev Neurosci 12 2011 707 722
77. H.A. Erdely, C.A. Tamminga, R.C. Roberts, and M.W. Vogel Regional alterations in RGS4 protein in schizophrenia Synapse 59 2006 472 479
78. A.L. Guillozet-Bongaarts, T.M. Hyde, R.A. Dalley, M.J. Hawrylycz, A. Henry, P.R. Hof, and et al. Altered gene expression in the dorsolateral prefrontal cortex of individuals with schizophrenia Mol Psychiatry 19 2014 478 485
79. K. Mirnics, F.A. Middleton, G.D. Stanwood, D.A. Lewis, and P. Levitt Disease-specific changes in regulator of G-protein signaling 4 (RGS4) expression in schizophrenia Mol Psychiatry 6 2001 293 301