Targeted deletion of the C-terminus of the mouse adenomatous polyposis coli tumor suppressor results in neurologic phenotypes related to schizophrenia

Molecular Brain

Volumn 7, Issue 1, 2014, Pages

  Onouchi, Takanori ^a   Kobayashi, Katsunori ^b,c   Sakai, Kazuyoshi ^d   Shimomura, Atsushi ^a   Smits, Ron ^e   Sumi Ichinose, Chiho ^a   Kurosumi, Masafumi ^f   Takao, Keizo ^c,d,g,h   Nomura, Ryuji ^a   Iizuka Kogo, Akiko ^a,k   Suzuki, Hidenori ^b,c   Kondo, Kazunao ^a   Akiyama, Tetsu ⁱ   Miyakawa, Tsuyoshi ^c,d,g,h   Fodde, Riccardo ^j   Senda, Takao ^a,l  

^a FUJITA HEALTH UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b NIPPON MEDICAL SCHOOL   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^d FUJITA HEALTH UNIVERSITY   (Japan)

^e ERASMUS MEDICAL CENTER   (Netherlands)

^f SAITAMA CANCER CENTER   (Japan)

^g NATIONAL INSTITUTE FOR PHYSIOLOGICAL SCIENCES   (Japan)

^h KYOTO UNIVERSITY   (Japan)

ⁱ UNIVERSITY OF TOKYO   (Japan)

^j JOSEPHINE NEFKENS INSTITUTE   (Netherlands)

^k GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^l GIFU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

more..

Author keywords

Adenomatous polyposis coli (Apc); Hippocampus; Locomotor activity; Schizophrenia; Working memory

Indexed keywords

APC PROTEIN; SEROTONIN; WNT PROTEIN;

AMNESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANXIETY; ARTICLE; CARBOXY TERMINAL SEQUENCE; CENTRAL NERVOUS SYSTEM; COGNITION; COLON POLYPOSIS; CONTROLLED STUDY; DENDRITIC SPINE; ENDOPHENOTYPE; GENE DELETION; HIPPOCAMPAL CA1 REGION; LEARNING DISORDER; LOCOMOTION; LONG TERM POTENTIATION; MALE; MAZE TEST; MEMORY DISORDER; MOUSE; NEUROPSYCHIATRY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; ROTAROD TEST; SCHIZOPHRENIA; SOCIAL INTERACTION; SYNAPTIC TRANSMISSION; WNT SIGNALING PATHWAY; WORKING MEMORY;

ADENOMATOUS POLYPOSIS COLI PROTEIN; ANIMALS; ANXIETY; CA1 REGION, HIPPOCAMPAL; DEPRESSION; DOPAMINE; EXPLORATORY BEHAVIOR; GENE TARGETING; MEMORY; MICE; MICE, INBRED C57BL; MICE, NEUROLOGIC MUTANTS; MOTOR ACTIVITY; PHENOTYPE; SCHIZOPHRENIA; SEQUENCE DELETION; SEROTONIN; SOCIAL BEHAVIOR; STRUCTURE-ACTIVITY RELATIONSHIP; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 84898427404     PISSN: None     EISSN: 17566606     Source Type: Journal    
DOI: 10.1186/1756-6606-7-21     Document Type: Article

References (37)

1. APC, signal transduction and genetic instability in colorectal cancer. Fodde R, Smits R, Clevers H, Nat Rev Cancer 2001 1 55 67 10.1038/35094067 11900252 (Pubitemid 33741881)
2. High levels of expression of the tumor suppressor gene APC during development of the rat central nervous system. Bhat RV, Baraban JM, Johnson RC, Eipper BA, Mains RE, J Neurosci 1994 14 3059 3071 8182459 (Pubitemid 24138993)
3. The molecular basis of Turcot's syndrome. Hamilton SR, Liu B, Parsons RE, Papadopoulos N, Jen J, Powell SM, Krush AJ, Berk T, Cohen Z, Tetu B, Burger PC, Wood PA, Taqi F, Booker SV, Petersen GM, Offerhaus GJA, Tersmette AC, Giardiello FM, Vogelstein B, Kinzler KW, N Engl J Med 1995 332 839 847 10.1056/NEJM199503303321302 7661930
4. Adenomatous polyposis coli (APC) plays multiple roles in the intestinal and colorectal epithelia. Senda T, Iizuka-Kogo A, Onouchi T, Shimomura A, Med Mol Morphol 2007 40 68 81 10.1007/s00795-006-0352-5 17572842 (Pubitemid 47305230)
5. The multiple functions of tumour suppressors: it's all in APC. Fodde R, Nat Cell Biol 2003 5 190 192 10.1038/ncb0303-190 12646874 (Pubitemid 36322244)
6. Association of APC and REEP5 gene polymorphisms with major depression disorder and treatment response to antidepressants in a Han Chinese population. Yang Z, Ma X, Wang Y, Wang J, Xiang B, Wu J, Deng W, Li M, Wang Q, Li T, Gen Hosp Psychiatry 2012 34 571 577 10.1016/j.genhosppsych.2012.05.015 22795047
7. The tumor suppressor adenomatous polyposis coli gene is associated with susceptibility to schizophrenia. Cui DH, Jiang KD, Jiang SD, Xu YF, Yao H, Mol Psychiatry 2005 10 669 677 10.1038/sj.mp.4001653 15768050 (Pubitemid 40961737)
8. Disease model: familial adenomatous polyposis. Fodde R, Smits R, Trends Mol Med 2001 7 369 373 10.1016/S1471-4914(01)02050-0 11516998 (Pubitemid 32735023)
9. Adenomatous polyposis coli heterozygous knockout mice display hypoactivity and age-dependent working memory deficits. Koshimizu H, Fukui Y, Takao K, Ohira K, Tanda K, Nakanishi K, Toyama K, Oshima M, Taketo MM, Miyakawa T, Front Behav Neurosci 2011 5 85 22347851
10. Apc1638T: a mouse model delineating critical domains of the adenomatous polyposis coli protein involved in tumorigenesis and development. Smits R, Kielman MF, Breukel C, Zurcher C, Neufeld K, Jagmohan-Changur S, Hofland N, van Dijk J, White R, Edelmann W, Kucherlapati R, Khan PM, Fodde R, Genes Dev 1999 13 1309 1321 10.1101/gad.13.10.1309 10346819 (Pubitemid 29250198)
11. Neural population-level memory traces in the mouse hippocampus. Chen G, Wang LP, Tsien JZ, PLoS One 2009 4 8256 10.1371/journal.pone.0008256 20016843
12. Alterations of dopamine and serotonin transmission in schizophrenia. Remington G, Prog Brain Res 2008 172 117 140 18772030
13. Neonatal phencyclidine treatment in mice induces behavioral, histological and neurochemical abnormalities in adulthood. Nakatani-Pawlak A, Yamaguchi K, Tatsumi Y, Mizoguchi H, Yoneda Y, Biol Pharm Bull 2009 32 1576 1583 10.1248/bpb.32.1576 19721235
14. Generation and characterization of conditional heparin-binding EGF-like growth factor knockout mice. Oyagi A, Oida Y, Kakefuda K, Shimazawa M, Shioda N, Moriguchi S, Kitaichi K, Nanba D, Yamaguchi K, Furuta Y, Fukunaga K, Higashiyama S, Hara H, PLoS One 2009 4 7461 10.1371/journal.pone.0007461 19829704
15. Deficiency of schnurri-2, an MHC enhancer binding protein, induces mild chronic inflammation in the brain and confers molecular, neuronal, and behavioral phenotypes related to schizophrenia. Takao K, Kobayashi K, Hagihara H, Ohira K, Shoji H, Hattori S, Koshimizu H, Umemori J, Toyama K, Nakamura HK, Kuroiwa M, Maeda J, Atsuzawa K, Esaki K, Yamaguchi S, Furuya S, Takagi T, Walton NM, Hayashi N, Suzuki H, Higuchi M, Usuda N, Suhara T, Nishi A, Matsumoto M, Ishii S, Miyakawa T, Neuropsychopharmacology 2013 38 1409 1425 10.1038/npp.2013.38 23389689
16. Impact of brain-behavior phenotypying of genetically-engineered mice on research of neuropsychiatric disorders. Takao K, Yamasaki N, Miyakawa T, Neurosci Res 2007 58 124 132 10.1016/j.neures.2007.02.009 17524507 (Pubitemid 46843324)
17. Alteration of BACE1-dependent NRG1/ErbB4 signaling and schizophrenia-like phenotypes in BACE1-null mice. Savonenko AV, Melnikova T, Laird FM, Stewart KA, Price DL, Wong PC, Proc Natl Acad Sci U S A 2008 105 5585 5590 10.1073/pnas.0710373105 18385378 (Pubitemid 351753906)
18. Mice lacking the AMPA GluR1 receptor exhibit striatal hyperdopaminergia and 'schizophrenia-related' behaviors. Wiedholz LM, Owens WA, Horton RE, Feyder M, Karlsson RM, Hefner K, Sprengel R, Celikel T, Daws LC, Holmes A, Mol Psychiatry 2008 13 631 640 10.1038/sj.mp.4002056 17684498 (Pubitemid 351704934)
19. Alpha-CaMKII deficiency causes immature dentate gyrus, a novel candidate endophenotype of psychiatric disorders. Yamasaki N, Maekawa M, Kobayashi K, Kajii Y, Maeda J, Soma M, Takao K, Tanda K, Ohira K, Toyama K, Kanzaki K, Fukunaga K, Sudo Y, Ichinose H, Ikeda M, Iwata N, Ozaki N, Suzuki H, Higuchi M, Suhara T, Yuasa S, Miyakawa T, Mol Brain 2008 1 6 10.1186/1756-6606-1-6 18803808
20. Modeling cognitive endophenotypes of schizophrenia in mice. Kellendonk C, Simpson EH, Kandel ER, Trends Neurosci 2009 32 347 358 10.1016/j.tins.2009.02. 003 19409625
21. Neuroplasticity of neocortical circuits in schizophrenia. Lewis DA, Gonzalez-Burgos G, Neuropsychopharmacology 2008 33 141 165 10.1038/sj.npp. 1301563 17805309 (Pubitemid 350191315)
22. Impaired maturation of dendritic spines without disorganization of cortical cell layers in mice lacking NRG1/ErbB signaling in the central nervous system. Barros CS, Calabrese B, Chamero P, Roberts AJ, Korzus E, Lloyd K, Stowers L, Mayford M, Halpain S, Muller U, Proc Natl Acad Sci U S A 2009 106 4507 4512 10.1073/pnas.0900355106 19240213
23. Type III neuregulin-1 is required for normal sensorimotor gating, memory-related behaviors, and corticostriatal circuit components. Chen YJ, Johnson MA, Lieberman MD, Goodchild RE, Schobel S, Lewandowski N, Rosoklija G, Liu RC, Gingrich JA, Small S, Moore H, Dwork AJ, Talmage DA, Role LW, J Neurosci 2008 28 6872 6883 10.1523/JNEUROSCI.1815-08.2008 18596162
24. Neuroligins and neurexins link synaptic function to cognitive disease. Sudhof TC, Nature 2008 455 903 911 10.1038/nature07456 18923512
25. The role of actin in the regulation of dendritic spine morphology and bidirectional synaptic plasticity. Chen Y, Bourne J, Pieribone VA, Fitzsimonds RM, Neuroreport 2004 15 829 832 10.1097/00001756-200404090-00018 15073524 (Pubitemid 38453467)
26. Storage of spatial information by the maintenance mechanism of LTP. Pastalkova E, Serrano P, Pinkhasova D, Wallace E, Fenton AA, Sacktor TC, Science 2006 313 1141 1144 10.1126/science.1128657 16931766 (Pubitemid 44300243)
27. The hippocampal formation in schizophrenia. Tamminga CA, Stan AD, Wagner AD, Am J Psychiatr 2010 167 1178 1193 10.1176/appi.ajp.2010.09081187 20810471
28. Regionally specific disturbance of dorsolateral prefrontal-hippocampal functional connectivity in schizophrenia. Meyer-Lindenberg AS, Olsen RK, Kohn PD, Brown T, Egan MF, Weinberger DR, Berman KF, Arch Gen Psychiatry 2005 62 379 386 10.1001/archpsyc.62.4.379 15809405 (Pubitemid 40471687)
29. A systematic fMRI investigation of the brain systems subserving different working memory components in schizophrenia. Henseler I, Falkai P, Gruber O, Eur J Neurosci 2009 30 693 702 10.1111/j.1460-9568.2009.06850.x 19686473
30. Brain-derived neurotrophic factor (BDNF) Val(66)Met polymorphism differentially predicts hippocampal function in medication-free patients with schizophrenia. Eisenberg DP, Ianni AM, Wei SM, Kohn PD, Kolachana B, Apud J, Weinberger DR, Berman KF, Mol Psychiatry 2013 18 713 720 10.1038/mp.2012.187 23319002
31. Prefrontal cortex dysfunction during working memory performance in schizophrenia: reconciling discrepant findings. Manoach DS, Schizophr Res 2003 60 285 298 12591590 (Pubitemid 36184716)
32. NMDA hypofunction as a convergence point for progression and symptoms of schizophrenia. Snyder MA, Gao WJ, Front Cell Neurosci 2013 7 31 23543703
33. Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Kornau HC, Schenker LT, Kennedy MB, Seeburg PH, Science 1995 269 1737 1740 10.1126/science.7569905 7569905
34. Requirement of the tumour suppressor APC for the clustering of PSD-95 and AMPA receptors in hippocampal neurons. Shimomura A, Ohkuma M, Iizuka-Kogo A, Kohu K, Nomura R, Miyachi E, Akiyama T, Senda T, Eur J Neurosci 2007 26 903 912 10.1111/j.1460-9568.2007.05723.x 17714185 (Pubitemid 47274618)
35. Conditional calcineurin knockout mice exhibit multiple abnormal behaviors related to schizophrenia. Miyakawa T, Leiter LM, Gerber DJ, Gainetdinov RR, Sotnikova TD, Zeng H, Caron MG, Tonegawa S, Proc Natl Acad Sci U S A 2003 100 8987 8992 10.1073/pnas.1432926100 12851457 (Pubitemid 36899210)
36. Characterization of substance P- and [Met]enkephalin-immunoreactive neurons in the caudate nucleus of cat and ferret by a single section Golgi procedure. Izzo PN, Graybiel AM, Bolam JP, Neuroscience 1987 20 577 587 10.1016/0306-4522(87)90111-4 2438593 (Pubitemid 17048714)
37. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Bradford MM, Anal Biochem 1976 72 248 254 10.1016/0003-2697(76)90527-3 942051