Srgap3-/- mice present a neurodevelopmental disorder with schizophrenia-related intermediate phenotypes

FASEB Journal

Volumn 26, Issue 11, 2012, Pages 4418-4428

  Waltereit, Robert ^a,b   Leimer, Uwe ^a   Von Bohlen Und Halbach, Oliver ^c   Panke, Jutta ^a   Hölter, Sabine M ^d   Garrett, Lillian ^d   Wittig, Karola ^a   Schneider, Miriam ^a   Schmitt, Camie ^a   Calzada Wack, Julia ^e   Neff, Frauke ^e   Becker, Lore ^e,f   Prehn, Cornelia ^e   Kutscherjawy, Sergej ^a   Endris, Volker ^a   Bacon, Claire ^a   Fuchs, Helmut ^e   Gailus Durner, Valérie ^e   Berger, Stefan ^a   Schönig, Kai ^a   Adamski, Jerzy ^e   Klopstock, Thomas ^f   Esposito, Irene ^e,g   Wurst, Wolfgang ^h,i,j   De Angelis, Martin Hrabě ^e,g   Rappold, Gudrun ^a   Wieland, Thomas ^a   Bartsch, Dusan ^a   more..

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b Department of Psychiatry ^*  (Germany)

^c UNIVERSITY OF GREIFSWALD   (Germany)

^d Institute of Developmental Genetics   (Germany)

^e INSTITUTE OF EPIDEMIOLOGY   (Germany)

^f LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^g TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^h MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

ⁱ GERMAN CENTER FOR NEURODEGENERATIVE DISEASES DZNE   (Germany)

^j Lehrstuhl für Entwicklungsgenetik   (Germany)

more..

Author keywords

Hydrocephalus; Intellectual disability; Knockout mouse; Polygenetic disease; RHO proteins

Indexed keywords

RAC1 PROTEIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; SRGAP3 PROTEIN; UNCLASSIFIED DRUG;

ADULTHOOD; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN DEVELOPMENT; BRAIN VENTRICLE; BRAIN VENTRICLE DILATATION; CONTROLLED STUDY; DENDRITIC SPINE; DEVELOPMENTAL DISORDER; DISEASE ASSOCIATION; FEMALE; GENE EXPRESSION; GENE MUTATION; HISTOPATHOLOGY; HYDROCEPHALUS; IMMUNOHISTOCHEMISTRY; LOCOMOTION; LONG TERM MEMORY; MALE; MOTOR DYSFUNCTION; MOUSE; NERVE TRACT; NEUROANATOMY; NEURODEVELOPMENTAL DISORDER; NEUROLOGIC DISEASE; NEUROPATHOLOGY; NONHUMAN; OPEN FIELD TEST; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RISK FACTOR; SCHIZOPHRENIA; SOCIAL BEHAVIOR; SURVIVAL RATE; TIC; WESTERN BLOTTING; WHITE MATTER;

ANIMALS; BEHAVIOR, ANIMAL; BRAIN; FEMALE; GTPASE-ACTIVATING PROTEINS; HYDROCEPHALUS; MALE; MICE; MICE, KNOCKOUT; NEUROPEPTIDES; RAC GTP-BINDING PROTEINS; RAC1 GTP-BINDING PROTEIN; SCHIZOPHRENIA; SOCIAL BEHAVIOR;

ANIMALIA; MUS;

EID: 84868275867     PISSN: None     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.11-202317     Document Type: Article

References (68)

1. Govek, E. E., Newey, S. E., and Van Aelst, L. (2005) The role of the Rho GTPases in neuronal development. Genes Dev. 19, 1-49
2. Van Aelst, L., and Cline, H. T. (2004) Rho GTPases and activity-dependent dendrite development. Curr. Opin. Neurobiol. 14, 297-304
3. Carlisle, H. J., and Kennedy, M. B. (2005) Spine architecture and synaptic plasticity. Trends Neurosci. 28, 182-187
4. Fischer, M., Kaech, S., Knutti, D., and Matus, A. (1998) Rapid actin-based plasticity in dendritic spines. Neuron 20, 847-854
5. Luo, L. (2000) Rho GTPases in neuronal morphogenesis. Nat. Rev. Neurosci. 1, 173-180
6. Ramakers, G. J. (2000) Rho proteins and the cellular mechanisms of mental retardation. Am. J. Med. Genet. 94, 367-371
7. Threadgill, R., Bobb, K., and Ghosh, A. (1997) Regulation of dendritic growth and remodeling by Rho, Rac, and Cdc42. Neuron 19, 625-634
8. Allen, K. M., Gleeson, J. G., Bagrodia, S., Partington, M. W., MacMillan, J. C., Cerione, R. A., Mulley, J. C., and Walsh, C. A. (1998) PAK3 mutation in nonsyndromic X-linked mental retardation. Nat. Genet. 20, 25-30
9. Attree, O., Olivos, I. M., Okabe, I., Bailey, L. C., Nelson, D. L., Lewis, R. A., McInnes, R. R., and Nussbaum, R. L. (1992) The Lowe's oculocerebrorenal syndrome gene encodes a protein highly homologous to inositol polyphosphate-5-phosphatase. Nature 358, 239-242
10. Billuart, P., Bienvenu, T., Ronce, N., des Portes, V., Vinet, M. C., Zemni, R., Roest Crollius, H., Carrie, A., Fauchereau, F., Cherry, M., Briault, S., Hamel, B., Fryns, J. P., Beldjord, C., Kahn, A., Moraine, C., and Chelly, J. (1998) Oligophrenin-1 encodes a rhoGAP protein involved in X-linked mental retardation. Nature 392, 923-926
11. Frangiskakis, J. M., Ewart, A. K., Morris, C. A., Mervis, C. B., Bertrand, J., Robinson, B. F., Klein, B. P., Ensing, G. J., Everett, L. A., Green, E. D., Proschel, C., Gutowski, N. J., Noble, M., Atkinson, D. L., Odelberg, S. J., and Keating, M. T. (1996) LIM-kinase1 hemizygosity implicated in impaired visuospatial constructive cognition. Cell 86, 59-69
12. Kutsche, K., Yntema, H., Brandt, A., Jantke, I., Nothwang, H. G., Orth, U., Boavida, M. G., David, D., Chelly, J., Fryns, J. P., Moraine, C., Ropers, H. H., Hamel, B. C., van Bokhoven, H., and Gal, A. (2000) Mutations in ARHGEF6, encoding a guanine nucleotide exchange factor for Rho GTPases, in patients with X-linked mental retardation. Nat. Genet. 26, 247-250
13. Pieretti, M., Zhang, F. P., Fu, Y. H., Warren, S. T., Oostra, B. A., Caskey, C. T., and Nelson, D. L. (1991) Absence of expression of the FMR-1 gene in fragile X syndrome. Cell 66, 817-822
14. Mowrey, P. N., Chorney, M. J., Venditti, C. P., Latif, F., Modi, W. S., Lerman, M. I., Zbar, B., Robins, D. B., Rogan, P. K., and Ladda, R. L. (1993) Clinical and molecular analyses of deletion 3p25-pter syndrome. Am. J. Med. Genet. 46, 623-629
15. Bacon, C., Endris, V., and Rappold, G. (2009) Dynamic expression of the Slit-Robo GTPase activating protein genes during development of the murine nervous system. J. Comp. Neurol. 513, 224-236
16. Waltereit, R., Kautt, S., and Bartsch, D. (2008) Expression of MEGAP mRNA during embryonic development. Gene Expr. Patterns 8, 307-310
17. Endris, V., Wogatzky, B., Leimer, U., Bartsch, D., Zatyka, M., Latif, F., Maher, E. R., Tariverdian, G., Kirsch, S., Karch, D., and Rappold, G. A. (2002) The novel Rho-GTPase activating gene MEGAP/srGAP3 has a putative role in severe mental retardation. Proc. Natl. Acad. Sci. U. S. A. 99, 11754-11759
18. Soderling, S. H., Binns, K. L., Wayman, G. A., Davee, S. M., Ong, S. H., Pawson, T., and Scott, J. D. (2002) The WRP component of the WAVE-1 complex attenuates Rac-mediated signalling. Nat. Cell Biol. 4, 970-975
19. Yang, Y., Marcello, M., Endris, V., Saffrich, R., Fischer, R., Trendelenburg, M. F., Sprengel, R., and Rappold, G. (2006) MEGAP impedes cell migration via regulating actin and microtubule dynamics and focal complex formation. Exp. Cell Res. 312, 2379-2393
20. Hamdan, F. F., Gauthier, J., Pellerin, S., Dobrzeniecka, S., Marineau, C., Fombonne, E., Mottron, L., Lafreniere, R. G., Drapeau, P., Lacaille, J. C., Rouleau, G. A., and Michaud, J. L. (2009) No association between SRGAP3/MEGAP haploinsufficiency and mental retardation. Arch. Neurol. 66, 675-676
21. Cook, E. H., Jr., and Scherer, S. W. (2008) Copy-number variations associated with neuropsychiatric conditions. Nature 455, 919-923
22. Guilmatre, A., Dubourg, C., Mosca, A. L., Legallic, S., Goldenberg, A., Drouin-Garraud, V., Layet, V., Rosier, A., Briault, S., Bonnet-Brilhault, F., Laumonnier, F., Odent, S., Le Vacon, G., Joly-Helas, G., David, V., Bendavid, C., Pinoit, J. M., Henry, C., Impallomeni, C., Germano, E., Tortorella, G., Di Rosa, G., Barthelemy, C., Andres, C., Faivre, L., Frebourg, T., Saugier Veber, P., and Campion, D. (2009) Recurrent rearrangements in synaptic and neurodevelopmental genes and shared biologic pathways in schizophrenia, autism, and mental retardation. Arch. Gen. Psychiatry 66, 947-956
23. Mitchell, K. J. (2010) The genetics of neurodevelopmental disease. Curr. Opin. Neurobiol. 21, 1-7
24. Morrow, E. M. (2010) Genomic copy number variation in disorders of cognitive development. J. Am. Acad. Child Adolesc. Psychiatry 49, 1091-1104
25. Sebat, J., Levy, D. L., and McCarthy, S. E. (2009) Rare structural variants in schizophrenia: one disorder, multiple mutations; one mutation, multiple disorders. Trends Genet. 25, 528-535
26. Lewis, C. M., Levinson, D. F., Wise, L. H., DeLisi, L. E., Straub, R. E., Hovatta, I., Williams, N. M., Schwab, S. G., Pulver, A. E., Faraone, S. V., Brzustowicz, L. M., Kaufmann, C. A., Garver, D. L., Gurling, H. M., Lindholm, E., Coon, H., Moises, H. W., Byerley, W., Shaw, S. H., Mesen, A., Sherrington, R., O'Neill, F. A., Walsh, D., Kendler, K. S., Ekelund, J., Paunio, T., Lonnqvist, J., Peltonen, L., O'Donovan, M. C., Owen, M. J., Wildenauer, D. B., Maier, W., Nestadt, G., Blouin, J. L., Antonarakis, S. E., Mowry, B. J., Silverman, J. M., Crowe, R. R., Cloninger, C. R., Tsuang, M. T., Malaspina, D., Harkavy-Friedman, J. M., Svrakic, D. M., Bassett, A. S., Holcomb, J., Kalsi, G., McQuillin, A., Brynjolfson, J., Sigmundsson, T., Petursson, H., Jazin, E., Zoega, T., and Helgason, T. (2003) Genome scan meta-Analysis of schizophrenia and bipolar disorder. Part II: schizophrenia. Am. J. Hum. Genet. 73, 34-48
27. Addington, A. M., and Rapoport, J. L. (2009) The genetics of childhood-onset schizophrenia: when madness strikes the prepubescent. Curr. Psychiatry Rep. 11, 156-161
28. Stefansson, H., Rujescu, D., Cichon, S., Pietilainen, O. P., Ingason, A., Steinberg, S., Fossdal, R., Sigurdsson, E., Sigmundsson, T., Buizer-Voskamp, J. E., Hansen, T., Jakobsen, K. D., Muglia, P., Francks, C., Matthews, P. M., Gylfason, A., Halldorsson, B. V., Gudbjartsson, D., Thorgeirsson, T. E., Sigurdsson, A., Jonasdottir, A., Jonasdottir, A., Bjornsson, A., Mattiasdottir, S., Blondal, T., Haraldsson, M., Magnusdottir, B. B., Giegling, I., Moller, H. J., Hartmann, A., Shianna, K. V., Ge, D., Need, A. C., Crombie, C., Fraser, G., Walker, N., Lonnqvist, J., Suvisaari, J., Tuulio-Henriksson, A., Paunio, T., Toulopoulou, T., Bramon, E., Di Forti, M., Murray, R., Ruggeri, M., Vassos, E., Tosato, S., Walshe, M., Li, T., Vasilescu, C., Muhleisen, T. W., Wang, A. G., Ullum, H., Djurovic, S., Melle, I., Olesen, J., Kiemeney, L. A., Franke, B., Sabatti, C., Freimer, N. B., Gulcher, J. R., Thorsteinsdottir, U., Kong, A., Andreassen, O. A., Ophoff, R. A., Georgi, A., Rietschel, M., Werge, T., Petursson, H., Goldstein, D. B., Nothen, M. M., Peltonen, L., Collier, D. A., St Clair, D., and Stefansson, K. (2008) Large recurrent microdeletions associated with schizophrenia. Nature 455, 232-236
29. Hayashi-Takagi, A., Takaki, M., Graziane, N., Seshadri, S., Murdoch, H., Dunlop, A. J., Makino, Y., Seshadri, A. J., Ishizuka, K., Srivastava, D. P., Xie, Z., Baraban, J. M., Houslay, M. D., Tomoda, T., Brandon, N. J., Kamiya, A., Yan, Z., Penzes, P., and Sawa, A. (2010) Disrupted-in-schizophrenia 1 (DISC1) regulates spines of the glutamate synapse via Rac1. Nat. Neurosci. 13, 327-332
30. Gailus-Durner, V., Fuchs, H., Becker, L., Bolle, I., Brielmeier, M., Calzada-Wack, J., Elvert, R., Ehrhardt, N., Dalke, C., Franz, T. J., Grundner-Culemann, E., Hammelbacher, S., Holter, S. M., Holzlwimmer, G., Horsch, M., Javaheri, A., Kalaydjiev, S. V., Klempt, M., Kling, E., Kunder, S., Lengger, C., Lisse, T., Mijalski, T., Naton, B., Pedersen, V., Prehn, C., Przemeck, G., Racz, I., Reinhard, C., Reitmeir, P., Schneider, I., Schrewe, A., Steinkamp, R., Zybill, C., Adamski, J., Beckers, J., Behrendt, H., Favor, J., Graw, J., Heldmaier, G., Hofler, H., Ivandic, B., Katus, H., Kirchhof, P., Klingenspor, M., Klopstock, T., Lengeling, A., Muller, W., Ohl, F., Ollert, M., Quintanilla-Martinez, L., Schmidt, J., Schulz, H., Wolf, E., Wurst, W., Zimmer, A., Busch, D. H., and de Angelis, M. H. (2005) Introducing the German Mouse Clinic: open access platform for standardized phenotyping. Nat. Methods 2, 403-404
31. Nagy, A., Rossant, J., Nagy, R., Abramow-Newerly, W., and Roder, J. C. (1993) Derivation of completely cell culture-derived mice from early-passage embryonic stem cells. Proc. Natl. Acad. Sci. U. S. A. 90, 8424-8428
32. Ramon-Moliner, E. (1970) The Golgi-Cox Technique, Springer, New York
33. Von Bohlen und Halbach, O., Zacher, C., Gass, P., and Unsicker, K. (2006) Age-related alterations in hippocampal spines and deficiencies in spatial memory in mice. J. Neurosci. Res. 83, 525-531
34. Von Bohlen und Halbach, O., Minichiello, L., and Unsicker, K. (2008) TrkB but not trkC receptors are necessary for postnatal maintenance of hippocampal spines. Neurobiol. Aging 29, 1247-1255
35. Gailus-Durner, V., Fuchs, H., Adler, T., Aguilar Pimentel, A., Becker, L., Bolle, I., Calzada-Wack, J., Dalke, C., Ehrhardt, N., Ferwagner, B., Hans, W., Holter, S. M., Holzlwimmer, G., Horsch, M., Javaheri, A., Kallnik, M., Kling, E., Lengger, C., Morth, C., Mossbrugger, I., Naton, B., Prehn, C., Puk, O., Rathkolb, B., Rozman, J., Schrewe, A., Thiele, F., Adamski, J., Aigner, B., Behrendt, H., Busch, D. H., Favor, J., Graw, J., Heldmaier, G., Ivandic, B., Katus, H., Klingenspor, M., Klopstock, T., Kremmer, E., Ollert, M., Quintanilla-Martinez, L., Schulz, H., Wolf, E., Wurst, W., and de Angelis, M. H. (2009) Systemic first-line phenotyping. Methods Mol. Biol. 530, 463-509
36. Waltereit, R., Welzl, H., Dichgans, J., Lipp, H. P., Schmidt, W. J., and Weller, M. (2006) Enhanced episodic-like memory and kindling epilepsy in a rat model of tuberous sclerosis. J. Neurochem. 96, 407-413
37. Joyner, A. L. (2000) Gene Targeting: A Practical Approach, Oxford University Press, Oxford, UK
38. Benard, V., and Bokoch, G. M. (2002) Assay of Cdc42, Rac, and Rho GTPase activation by affinity methods. Methods Enzymol. 345, 349-359
39. Mohl, M., Winkler, S., Wieland, T., and Lutz, S. (2006) Gef10-the third member of a Rho-specific guanine nucleotide exchange factor subfamily with unusual protein architecture. Naunyn Schmiedebergs Arch. Pharmacol., 373, 333-341
40. Schneider, I., Tirsch, W. S., Faus-Kessler, T., Becker, L., Kling, E., Busse, R. L., Bender, A., Feddersen, B., Tritschler, J., Fuchs, H., Gailus-Durner, V., Englmeier, K. H., de Angelis, M. H., and Klopstock, T. (2006) Systematic, standardized and comprehensive neurological phenotyping of inbred mice strains in the German Mouse Clinic. J. Neurosci. Methods 157, 82-90
41. Rogers, D. C., Fisher, E. M., Brown, S. D., Peters, J., Hunter, A. J., and Martin, J. E. (1997) Behavioral and functional analysis of mouse phenotype: SHIRPA, a proposed protocol for comprehensive phenotype assessment. Mamm. Genome 8, 711-713
42. Deussing, J. M., Breu, J., Kuhne, C., Kallnik, M., Bunck, M., Glasl, L., Yen, Y. C., Schmidt, M. V., Zurmuhlen, R., Vogl, A. M., Gailus-Durner, V., Fuchs, H., Holter, S. M., Wotjak, C. T., Landgraf, R., de Angelis, M. H., Holsboer, F., and Wurst, W. (2010) Urocortin 3 modulates social discrimination abilities via corticotropin-releasing hormone receptor type 2. J. Neurosci. 30, 9103-9116
43. Schneider, M., Spanagel, R., Zhang, S. J., Bading, H., and Klugmann, M. (2007) Adeno-Associated virus (AAV)-mediated suppression of Ca2-/calmodulin kinase IV activity in the nucleus accumbens modulates emotional behaviour in mice. BMC Neurosci. 8, 105
44. Schwartz, M. (2004) Rho signalling at a glance. J. Cell Sci. 117, 5457-5458
45. Schurr, P. H., McLaurin, R. L., and Ingraham, F. D. (1953) Experimental studies on the circulation of the cerebrospinal fluid and methods of producing communicating hydrocephalus in the dog. J. Neurosurg. 10, 515-525
46. Zhang, J., Williams, M. A., and Rigamonti, D. (2006) Genetics of human hydrocephalus. J. Neurol. 253, 1255-1266
47. Steen, R. G., Mull, C., McClure, R., Hamer, R. M., and Lieberman, J. A. (2006) Brain volume in first-episode schizophrenia: systematic review and meta-Analysis of magnetic resonance imaging studies. Br. J. Psychiatry 188, 510-518
48. Chen, Y. J., Johnson, M. A., Lieberman, M. D., Goodchild, R. E., Schobel, S., Lewandowski, N., Rosoklija, G., Liu, R. C., Gingrich, J. A., Small, S., Moore, H., Dwork, A. J., Talmage, D. A., and Role, L. W. (2008) Type III neuregulin-1 is required for normal sensorimotor gating, memory-related behaviors, and corticostriatal circuit components. J. Neurosci. 28, 6872-6883
49. Mata, I., Perez-Iglesias, R., Roiz-Santianez, R., Tordesillas-Gutierrez, D., Gonzalez-Mandly, A., Vazquez-Barquero, J. L., and Crespo-Facorro, B. (2009) A neuregulin 1 variant is associated with increased lateral ventricle volume in patients with firstepisode schizophrenia. Biol. Psychiatry 65, 535-540
50. Shen, S., Lang, B., Nakamoto, C., Zhang, F., Pu, J., Kuan, S. L., Chatzi, C., He, S., Mackie, I., Brandon, N. J., Marquis, K. L., Day, M., Hurko, O., McCaig, C. D., Riedel, G., and St Clair, D. (2008) Schizophrenia-related neural and behavioral phenotypes in transgenic mice expressing truncated Disc1. J. Neurosci. 28, 10893-10904
51. Chen, L., Liao, G., Waclaw, R. R., Burns, K. A., Linquist, D., Campbell, K., Zheng, Y., and Kuan, C. Y. (2007) Rac1 controls the formation of midline commissures and the competency of tangential migration in ventral telencephalic neurons. J. Neurosci. 27, 3884-3893
52. Kassai, H., Terashima, T., Fukaya, M., Nakao, K., Sakahara, M., Watanabe, M., and Aiba, A. (2008) Rac1 in cortical projection neurons is selectively required for midline crossing of commissural axonal formation. Eur. J. Neurosci. 28, 257-267
53. Blanpied, T. A., and Ehlers, M. D. (2004) Microanatomy of dendritic spines: emerging principles of synaptic pathology in psychiatric and neurological disease. Biol. Psychiatry 55, 1121-1127
54. Halpain, S., Spencer, K., and Graber, S. (2005) Dynamics and pathology of dendritic spines. Prog. Brain Res. 147, 29-37
55. Ramakers, G. J. (2002) Rho proteins, mental retardation and the cellular basis of cognition. Trends Neurosci. 25, 191-199
56. van Spronsen, M., and Hoogenraad, C. C. (2010) Synapse pathology in psychiatric and neurologic disease. Curr. Neurol. Neurosci. Rep. 10, 207-214
57. Calabrese, B., Wilson, M. S., and Halpain, S. (2006) Development and regulation of dendritic spine synapses. Physiology 21, 38-47
58. Penzes, P., Beeser, A., Chernoff, J., Schiller, M. R., Eipper, B. A., Mains, R. E., and Huganir, R. L. (2003) Rapid induction of dendritic spine morphogenesis by trans-synaptic ephrinB-EphB receptor activation of the Rho-GEF kalirin. Neuron 37, 263-274
59. Oh, D., Han, S., Seo, J., Lee, J. R., Choi, J., Groffen, J., Kim, K., Cho, Y. S., Choi, H. S., Shin, H., Woo, J., Won, H., Park, S. K., Kim, S. Y., Jo, J., Whitcomb, D. J., Cho, K., Kim, H., Bae, Y. C., Heisterkamp, N., Choi, S. Y., and Kim, E. (2010) Regulation of synaptic Rac1 activity, long-term potentiation maintenance, and learning and memory by BCR and ABR Rac GTPase-Activating proteins. J. Neurosci. 30, 14134-14144
60. Sweatt, J. D. (2003) Mechanisms of Memory, Academic Press, San Diego, CA, USA
61. Arguello, P. A., and Gogos, J. A. (2010) Cognition in mouse models of schizophrenia susceptibility genes. Schizophr. Bull. 36, 289-300
62. Nestler, E. J., and Hyman, S. E. (2010) Animal models of neuropsychiatric disorders. Nat. Neurosci. 13, 1161-1169
63. O'Tuathaigh, C. M., Kirby, B. P., Moran, P. M., and Waddington, J. L. (2010) Mutant mouse models: genotype-phenotype relationships to negative symptoms in schizophrenia. Schizophr. Bull. 36, 271-288
64. Van den Buuse, M. (2010) Modeling the positive symptoms of schizophrenia in genetically modified mice: pharmacology and methodology aspects. Schizophr. Bull. 36, 246-270
65. Shprecher, D., and Kurlan, R. (2009) The management of tics. Mov. Disord. 24, 15-24
66. Ko, Y. H., Jung, S. W., Joe, S. H., Lee, C. H., Jung, H. G., Jung, I. K., Kim, S. H., and Lee, M. S. (2007) Association between serum testosterone levels and the severity of negative symptoms in male patients with chronic schizophrenia. Psychoneuroendocrinology 32, 385-391
67. Carlson, B. R., Lloyd, K. E., Kruszewski, A., Kim, I. H., Rodriguiz, R. M., Heindel, C., Faytell, M., Dudek, S. M., Wetsel, W. C., and Soderling, S. H. (2011) WRP/srGAP3 facilitates the initiation of spine development by an inverse F-BAR domain, and its loss impairs long-term memory. J. Neurosci. 31, 2447-2460
68. Shuib, S., McMullan, D., Rattenberry, E., Barber, R. M., Rahman, F., Zatyka, M., Chapman, C., Macdonald, F., Latif, F., Davison, V., and Maher, E. R. (2009) Microarray based analysis of 3p25-p26 deletions (3p-syndrome). Am. J. Med. Genet. A. 149A, 2099-2105