Adenomatous polyposis coli protein deletion leads to cognitive and autism-like disabilities

Molecular Psychiatry

Volumn 19, Issue 10, 2014, Pages 1133-1142

  Mohn, J L ^a   Alexander, J ^a   Pirone, A ^a   Palka, C D ^a   Lee, S Y ^a   Mebane, L ^a   Haydon, P G ^a   Jacob, M H ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APC PROTEIN; BETA CATENIN; NERVE CELL ADHESION MOLECULE; PRESENILIN 1; WNT PROTEIN; CADHERIN; CDH2 PROTEIN, MOUSE; CTNNB1 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APC GENE; ARTICLE; AUTISM; BRAIN REGION; COGNITIVE DEFECT; COMPULSION; CONTROLLED STUDY; FOREBRAIN; GENE; GENE EXPRESSION; GENE INACTIVATION; GENE MUTATION; HIPPOCAMPUS; LEARNING DISORDER; LONG TERM POTENTIATION; MALE; MEMORY DISORDER; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SOCIAL INTERACTION; SYNAPSE; ANIMAL; DENDRITIC SPINE; DISEASE MODEL; EXCITATORY POSTSYNAPTIC POTENTIAL; GENETICS; KNOCKOUT MOUSE; MAZE TEST; METABOLISM; MINIATURE ENDPLATE POTENTIAL; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PYRAMIDAL NERVE CELL; SOCIAL BEHAVIOR; SPATIAL MEMORY; STEREOTYPY; WNT SIGNALING PATHWAY;

ADENOMATOUS POLYPOSIS COLI PROTEIN; ANIMALS; AUTISTIC DISORDER; BETA CATENIN; CADHERINS; COGNITION DISORDERS; DENDRITIC SPINES; DISEASE MODELS, ANIMAL; EXCITATORY POSTSYNAPTIC POTENTIALS; HIPPOCAMPUS; LONG-TERM POTENTIATION; MALE; MAZE LEARNING; MICE, KNOCKOUT; MINIATURE POSTSYNAPTIC POTENTIALS; PYRAMIDAL CELLS; SOCIAL BEHAVIOR; SPATIAL MEMORY; STEREOTYPED BEHAVIOR; SYNAPSES; WNT SIGNALING PATHWAY;

EID: 84902234785     PISSN: 13594184     EISSN: 14765578     Source Type: Journal    
DOI: 10.1038/mp.2014.61     Document Type: Article

References (75)

1. Gilman SR, Iossifov I, Levy D, Ronemus M, Wigler M, Vitkup D. Rare de novo variants associated with autism implicate a large functional network of genes involved in formation and function of synapses. Neuron 2011; 70: 898-907.
2. Zoghbi HY, Bear MF. Synaptic dysfunction in neurodevelopmental disorders associated with autism and intellectual disabilities. Cold Spring Harb Perspect Biol 2012; 4: pii: a009886.
3. Stamos JL, Weis WI. The beta-catenin destruction complex. Cold Spring Harb Perspect Biol 2013; 5: a007898.
4. Hodgson SV, Coonar AS, Hanson PJ, Cottrell S, Scriven PN, Jones T et al. Two cases of 5q deletions in patients with familial adenomatous polyposis: possible link with Caroli's disease. J Med Genet 1993; 30: 369-375.
5. Herrera L, Kakati S, Gibas L, Pietrzak E, Sandberg AA. Gardner syndrome in a man with an interstitial deletion of 5q. Am J Med Genet 1986; 25: 473-476.
6. Hockey KA, Mulcahy MT, Montgomery P, Levitt S. Deletion of chromosome 5q and familial adenomatous polyposis. J Med Genet 1989; 26: 61-62.
7. Kobayashi T, Narahara K, Yokoyama Y, Ueyama S, Mohri O, Fujii T et al. Gardner syndrome in a boy with interstitial deletion of the long arm of chromosome 5. Am J Med Genet 1991; 41: 460-463.
8. Cross I, Delhanty J, Chapman P, Bowles LV, Griffin D, Wolstenholme J et al. An intrachromosomal insertion causing 5q22 deletion and familial adenomatous polyposis coli in two generations. J Med Genet 1992; 29: 175-179.
9. Lindgren V, Bryke CR, Ozcelik T, Yang-Feng TL, Francke U. Phenotypic, cytogenetic, and molecular studies of three patients with constitutional deletions of chromosome 5 in the region of the gene for familial adenomatous polyposis. Am J Hum Genet 1992; 50: 988-997.
10. Heald B, Moran R, Milas M, Burke C, Eng C. Familial adenomatous polyposis in a patient with unexplained mental retardation. Nat Clin Pract Neurol 2007; 3: 694-700.
11. Barber JC, Ellis KH, Bowles LV, Delhanty JD, Ede RF, Male BM et al. Adenomatous polyposis coli and a cytogenetic deletion of chromosome 5 resulting from a maternal intrachromosomal insertion. J Med Genet 1994; 31: 312-316.
12. Finch R, Moore HG, Lindor N, Jalal SM, Markowitz A, Suresh J et al. Familial adenomatous polyposis and mental retardation caused by a de novo chromosomal deletion at 5q15-q22: report of a case. Dis Colon Rectum 2005; 48: 2148-2152.
13. Raedle J, Friedl W, Engels H, Koenig R, Trojan J, Zeuzem S. A de novo deletion of chromosome 5q causing familial adenomatous polyposis, dysmorphic features, and mild mental retardation. Am J Gastroenterol 2001; 96: 3016-3020.
14. Zhou XL, Giacobini M, Anderlid BM, Anckarsäter H, Omrani D, Gillberg C et al. Association of adenomatous polyposis coli (APC) gene polymorphisms with autism spectrum disorder (ASD). Am J Med Genet B Neuropsychiatr Genet 2007; 144B: 351-354.
15. O'Roak BJ, Vives L, Fu W, Egertson JD, Stanaway IB, Phelps IG et al. Multiplex targeted sequencing identifies recurrently mutated genes in autism spectrum disorders. Science 2012; 338: 1619-1622.
16. Iossifov I, Ronemus M, Levy D, Wang Z, Hakker I, Rosenbaum J et al. De novo gene disruptions in children on the autistic spectrum. Neuron 2012; 74: 285-299.
17. Neale BM, Kou Y, Liu L, Ma'ayan A, Samocha KE, Sabo A et al. Patterns and rates of exonic de novo mutations in autism spectrum disorders. Nature 2012; 485: 242-245.
18. Sanders SJ, Ercan-Sencicek AG, Hus V, Luo R, Murtha MT, Moreno-De-Luca D et al. Multiple recurrent de novo CNVs, including duplications of the 7q11.23 Williams syndrome region, are strongly associated with autism. Neuron 2011; 70:863-885.
19. Talkowski ME, Rosenfeld JA, Blumenthal I, Pillalamarri V, Chiang C, Heilbut A et al. Sequencing chromosomal abnormalities reveals neurodevelopmental loci that confer risk across diagnostic boundaries. Cell 2012; 149: 525-537.
20. Willsey AJ, Sanders SJ, Li M, Dong S, Tebbenkamp AT, Muhle RA et al. Coexpression networks implicate human midfetal deep cortical projection neurons in the pathogenesis of autism. Cell 2013; 155: 997-1007.
21. Levy D, Ronemus M, Yamrom B, Lee YH, Leotta A, Kendall J et al. Rare de novo and transmitted copy-number variation in autistic spectrum disorders. Neuron 2011; 70: 886-897.
22. Chow ML, Pramparo T, Winn ME, Barnes CC, Li HR, Weiss L et al. Age-dependent brain gene expression and copy number anomalies in autism suggest distinct pathological processes at young versus mature ages. PLoS Genet 2012; 8: e1002592.
23. Martin PM, Yang X, Robin N, Lam E, Rabinowitz JS, Erdman CA et al. A rare WNT1 missense variant overrepresented in ASD leads to increased Wnt signal pathway activation. Transl Psychiatry 2013; 3: e301.
24. de Ligt J, Willemsen MH, van Bon BW, Kleefstra T, Yntema HG, Kroes T et al. Diagnostic exome sequencing in persons with severe intellectual disability. N Engl J Med 2012; 367: 1921-1929.
25. Krumm N, O'Roak BJ, Shendure J, Eichler EE. A de novo convergence of autism genetics and molecular neuroscience. Trends Neurosci 2014; 37: 95-105.
26. Temburni MK, Rosenberg M.M, Pathak N, McConnell R, Jacob MH. Neuronal nicotinic synapse assembly requires the adenomatous polyposis coli tumor suppressor protein. J Neurosci 2004; 24: 6776-6784.
27. Rosenberg MM, Yang F, Mohn JL, Storer EK, Jacob MH. The postsynaptic adenomatous polyposis coli (APC) multiprotein complex is required for localizing neuroligin and neurexin to neuronal nicotinic synapses in vivo. JNeurosci2010; 30: 11073-11085.
28. Rosenberg MM, Yang F, Giovanni M, Mohn JL, Temburni MK, Jacob MH. Adenomatous polyposis coli plays a key role, in vivo, in coordinating assembly of the neuronal nicotinic postsynaptic complex. Mol Cell Neurosci 2008; 38: 138-152.
29. Shimomura A, Ohkuma M, Iizuka-Kogo A, Kohu K, Nomura R, Miyachi E et al. Requirement of the tumour suppressor APC for the clustering of PSD-95 and AMPA receptors in hippocampal neurons. Eur J Neurosci 2007; 26: 903-912.
30. Yanai H, Satoh K, Matsumine A, Akiyama T. The colorectal tumour suppressor APC is present in the NMDA-receptor-PSD-95 complex in the brain. Genes Cells 2000; 5: 815-822.
31. Gounari F, Chang R, Cowan J, Guo Z, Dose M, Gounaris E et al. Loss of adenomatous polyposis coli gene function disrupts thymic development. Nat Immunol 2005; 6: 800-809.
32. Rios M, Fan G, Fekete C, Kelly J, Bates B, Kuehn R et al. Conditional deletion of brain-derived neurotrophic factor in the postnatal brain leads to obesity and hyperactivity. Mol Endocrinol 2001; 15: 1748-1757.
33. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, Wallace M et al. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 2000; 28: 41-51.
34. Murphy JA, Jensen ON, Walikonis RS. BRAG1, a Sec7 domain-containing protein, is a component of the postsynaptic density of excitatory synapses. Brain Res 2006; 1120: 35-45.
35. Barnes CA. Memory deficits associated with senescence: a neurophysiological and behavioral study in the rat. J Comp Physiol Psychol 1979; 93: 74-104.
36. Hughes RN. The value of spontaneous alternation behavior (SAB) as a test of retention in pharmacological investigations of memory. Neurosci Biobehav Rev 2004; 28: 497-505.
37. Pearson BL, Pobbe RL, Defensor EB, Oasay L, Bolivar VJ, Blanchard DC et al. Motor and cognitive stereotypies in the BTBR T+tf/J mouse model of autism. Genes Brain Behav 2011; 10: 228-235.
38. Silverman JL, Yang M, Lord C, Crawley JN. Behavioural phenotyping assays for mouse models of autism. Nat Rev Neurosci 2010; 11: 490-502.
39. Parikshak NN, Luo R, Zhang A, Won H, Lowe JK, Chandran V et al. Integrative functional genomic analyses implicate specific molecular pathways and circuits in autism. Cell 2013; 155: 1008-1021.
40. Moser AR, Shoemaker AR, Connelly CS, Clipson L, Gould KA, Luongo C et al. Homozygosity for the Min allele of Apc results in disruption of mouse development prior to gastrulation. Dev Dyn 1995; 203: 422-433.
41. Yokota Y, Kim WY, Chen Y, Wang X, Stanco A, Komuro Y et al. The adenomatous polyposis coli protein is an essential regulator of radial glial polarity and construction of the cerebral cortex. Neuron 2009; 61: 42-56.
42. Ivaniutsin U, Chen Y, Mason JO, Price DJ, Pratt T. Adenomatous polyposis coli is required for early events in the normal growth and differentiation of the developing cerebral cortex. Neural Dev 2009; 4: 3.
43. Novak G, Seeman P. Hyperactive mice show elevated D2(High) receptors, a model for schizophrenia: Calcium/calmodulin-dependent kinase II alpha knockouts. Synapse 2010; 64: 794-800.
44. Ng J, Rashid AJ, So CH, O'Dowd BF, George SR. Activation of calcium/calmodulin-dependent protein kinase IIalpha in the striatum by the heteromeric D1-D2 dopamine receptor complex. Neuroscience 2010; 165: 535-541.
45. Koshimizu H, Fukui Y, Takao K, Ohira K, Tanda K, Nakanishi K et al. Adenomatous polyposis coli heterozygous knockout mice display hypoactivity and age-dependent working memory deficits. Front Behav Neurosci 2011; 5: 85.
46. Thomas A, Burant A, Bui N, Graham D, Yuva-Paylor LA, Paylor R. Marble burying reflects a repetitive and perseverative behavior more than novelty-induced anxiety. Psychopharmacology (Berl) 2009; 204: 361-373.
47. Fujimura N, Vacik T, Machon O, Vlcek C, Scalabrin S, Speth M et al. Wnt-mediated down-regulation of Sp1 target genes by a transcriptional repressor Sp5. J Biol Chem 2007; 282: 1225-1237.
48. Hirabayashi Y, Itoh Y, Tabata H, Nakajima K, Akiyama T, Masuyama N et al. The Wnt/beta-catenin pathway directs neuronal differentiation of cortical neural precursor cells. Development 2004; 131: 2791-2801.
49. Luo Y, Shan G, Guo W, Smrt RD, Johnson EB, Li X et al. Fragile X Mental Retardation Protein Regulates Proliferation and Differentiation of Adult Neural Stem/Progenitor Cells. PLoS Genet 2010; 6: e1000898.
50. Gitler D, Takagishi Y, Feng J, Ren Y, Rodriguiz RM, Wetsel WC et al. Different presynaptic roles of synapsins at excitatory and inhibitory synapses. J Neurosci 2004; 24: 11368-11380.
51. Hodar C, Assar R, Colombres M, Aravena A, Pavez L, González M et al. Genomewide identification of new Wnt/beta-catenin target genes in the human genome using CART method. BMC Genomics 2010; 11: 348.
52. Diep DB, Hoen N, Backman M, Machon O, Krauss S. Characterisation of the Wnt antagonists and their response to conditionally activated Wnt signalling in the developing mouse forebrain. Brain Res Dev Brain Res 2004; 153: 261-270.
53. Marambaud P, Wen PH, Dutt A, Shioi J, Takashima A, Siman R et al. A CBP binding transcriptional repressor produced by the PS1/epsilon-cleavage of N-cadherin is inhibited by PS1 FAD mutations. Cell 2003; 114: 635-645.
54. Yu H, Saura CA, Choi SY, Sun LD, Yang X, Handler M et al. APP processing and synaptic plasticity in presenilin-1 conditional knockout mice. Neuron 2001; 31: 713-726.
55. Kundel M, Jones KJ, Shin CY, Wells DG. Cytoplasmic polyadenylation elementbinding protein regulates neurotrophin-3-dependent beta-catenin mRNA translation in developing hippocampal neurons. J Neurosci 2009; 29: 13630-13639.
56. Yu X, Malenka RC. Multiple functions for the cadherin/catenin complex during neuronal development. Neuropharmacology 2004; 47: 779-786.
57. Murase S, Mosser E, Schuman EM. Depolarization drives beta-Catenin into neuronal spines promoting changes in synaptic structure and function. Neuron 2002; 35: 91-105.
58. Liu SJ, Savtchouk I. Ca(2+) permeable AMPA receptors switch allegiances: mechanisms and consequences. J Physiol 2012; 590: 13-20.
59. Chen J, Park CS, Tang SJ. Activity-dependent synaptic Wnt release regulates hippocampal long term potentiation. J Biol Chem 2006; 281: 11910-11916.
60. Cerpa W, Gambrill A, Inestrosa NC, Barria A. Regulation of NMDA-receptor synaptic transmission by Wnt signaling. J Neurosci 2011; 31: 9466-9471.
61. Salinas PC. Wnt signaling in the vertebrate central nervous system: from axon guidance to synaptic function. Cold Spring Harb Perspect Biol 2012; 4.
62. Park M, Shen K. WNTs in synapse formation and neuronal circuitry. EMBO J 2012; 31: 2697-2704.
63. Rosso SB, Inestrosa NC. WNT signaling in neuronal maturation and synaptogenesis. Front Cell Neurosci 2013; 7: 103.
64. Brigidi GS, Bamji SX. Cadherin-catenin adhesion complexes at the synapse. Curr Opin Neurobiol 2011; 21: 208-214.
65. Shimogori T, VanSant J, Paik E, Grove EA. Members of the Wnt, Fz, and Frp gene families expressed in postnatal mouse cerebral cortex. J Comp Neurol 2004; 473: 496-510.
66. Cerpa W, Godoy JA, Alfaro I, Farías GG, Metcalfe MJ, Fuentealba R et al. Wnt-7a modulates the synaptic vesicle cycle and synaptic transmission in hippocampal neurons. J Biol Chem 2008; 283: 5918-5927.
67. Avila ME, Sepúlveda FJ, Burgos CF, Moraga-Cid G, Parodi J, Moon RT et al. Canonical Wnt3a modulates intracellular calcium and enhances excitatory neurotransmission in hippocampal neurons. J Biol Chem 2010; 285: 18939-18947.
68. Bamji SX, Shimazu K, Kimes N, Huelsken J, Birchmeier W, Lu B et al. Role of betacatenin in synaptic vesicle localization and presynaptic assembly. Neuron 2003; 40: 719-731.
69. Maguschak KA, Ressler KJ. Wnt signaling in amygdala-dependent learning and memory. J Neurosci 2011; 31: 13057-13067.
70. Fortress AM, Schram SL, Tuscher JJ, Frick KM. Canonical Wnt signaling is necessary for object recognition memory consolidation. J Neurosci 2013; 33: 12619-12626.
71. Jensen M, Hoerndli FJ, Brockie PJ, Wang R, Johnson E, Maxfield D et al. Wnt signaling regulates acetylcholine receptor translocation and synaptic plasticity in the adult nervous system. Cell 2012; 149: 173-187.
72. Maguschak KA, Ressler KJ. A role for WNT/beta-catenin signaling in the neural mechanisms of behavior. J Neuroimmune Pharmacol 2012; 7: 763-773.
73. De Ferrari GV, Moon RT. The ups and downs of Wnt signaling in prevalent neurological disorders. Oncogene 2006; 25: 7545-7553.
74. Inestrosa NC, Varela-Nallar L. Wnt signaling in the nervous system and in Alzheimer's disease. J Mol Cell Biol 2014; 6: 64-74.
75. Seib DR, Corsini NS, Ellwanger K, Plaas C, Mateos A, Pitzer C et al. Loss of Dickkopf-1 restores neurogenesis in old age and counteracts cognitive decline. Cell Stem Cell 2013; 12: 204-214.