Mutation of the CH1 domain in the histone acetyltransferase CREBBP results in autism-relevant behaviors in mice

PLoS ONE

Volumn 11, Issue 1, 2016, Pages

  Zheng, Fei ^a   Kasper, Lawryn H ^a   Bedford, David C ^a   Lerach, Stephanie ^a   Teubner, Brett J W ^a   Brindle, Paul K ^a  

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; E1A ASSOCIATED P300 PROTEIN; CREBBP PROTEIN, MOUSE; HISTONE ACETYLTRANSFERASE;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTISM; BEHAVIOR CHANGE; CH1 GENE; COGNITION; CONTROLLED STUDY; GENE; GENE DELETION; GENE MUTATION; HYPERACTIVITY; MALE; MEMORY DISORDER; MOTOR DYSFUNCTION; MOTOR PERFORMANCE; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PATHOGENESIS; PHENOTYPE; PROTEIN DOMAIN; PROTEIN FUNCTION; RUBINSTEIN SYNDROME; SOCIAL BEHAVIOR; SOCIAL INTERACTION; 129 MOUSE; ANALYSIS OF VARIANCE; ANIMAL; BINDING SITE; C57BL MOUSE; CRANIOFACIAL MALFORMATION; ENZYMOLOGY; GENETICS; HIPPOCAMPUS; HUMAN; KNOCKOUT MOUSE; LONG TERM POTENTIATION; MAZE TEST; METABOLISM; MOTOR ACTIVITY; MUTATION; PATHOPHYSIOLOGY; PHYSIOLOGY;

ANALYSIS OF VARIANCE; ANIMALS; AUTISTIC DISORDER; BINDING SITES; CRANIOFACIAL ABNORMALITIES; CREB-BINDING PROTEIN; HIPPOCAMPUS; HISTONE ACETYLTRANSFERASES; HUMANS; LONG-TERM POTENTIATION; MAZE LEARNING; MEMORY DISORDERS; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; MOTOR ACTIVITY; MUTATION; PHENOTYPE; RUBINSTEIN-TAYBI SYNDROME; SOCIAL BEHAVIOR;

EID: 84954165453     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0146366     Document Type: Article

References (59)

1. Lichtenstein P, Carlstrom E, Rastam M, Gillberg C, Anckarsater H. The genetics of autism spectrum disorders and related neuropsychiatric disorders in childhood. Am J Psychiatry. 2010; 167(11):1357-63. Epub 2010/08/06. doi: 10.1176/appi.ajp.2010.10020223 PMID: 20686188.
2. Silverman JL, Yang M, Lord C, Crawley JN. Behavioural phenotyping assays for mouse models of autism. Nat Rev Neurosci. 2010; 11(7):490-502. Epub 2010/06/19. doi: 10.1038/nrn2851 PMID: 20559336; PubMed Central PMCID: PMC3087436.
3. Kim YS, Leventhal BL, Koh YJ, Fombonne E, Laska E, Lim EC, et al. Prevalence of autism spectrum disorders in a total population sample. Am J Psychiatry. 2011; 168(9):904-12. Epub 2011/05/12. doi: 10.1176/appi.ajp.2011.10101532 PMID: 21558103.
4. Huguet G, Ey E, Bourgeron T. The genetic landscapes of autism spectrum disorders. Annual review of genomics and human genetics. 2013; 14:191-213. Epub 2013/07/24. doi: 10.1146/annurev-genom- 091212-153431 PMID: 23875794.
5. Schaaf CP, Zoghbi HY. Solving the autism puzzle a few pieces at a time. Neuron. 2011; 70(5):806-8. Epub 2011/06/11. doi: 10.1016/j.neuron.2011.05.025 PMID: 21658575.
6. De Rubeis S, He X, Goldberg AP, Poultney CS, Samocha K, Cicek AE, et al. Synaptic, transcriptional and chromatin genes disrupted in autism. Nature. 2014; 515(7526):209-15. doi: 10.1038/nature13772 PMID: 25363760.
7. Basu SN, Kollu R, Banerjee-Basu S. AutDB: a gene reference resource for autism research. Nucleic Acids Res. 2009; 37(Database issue):D832-6. Epub 2008/11/19. doi: 10.1093/nar/gkn835 PMID: 19015121; PubMed Central PMCID: PMC2686502.
8. Allis CD, Berger SL, Cote J, Dent S, Jenuwien T, Kouzarides T, et al. New nomenclature for chromatinmodifying enzymes. Cell. 2007; 131(4):633-6. Epub 2007/11/21. doi: 10.1016/j.cell.2007.10.039 PMID: 18022353.
9. Bedford DC, Kasper LH, Fukuyama T, Brindle PK. Target gene context influences the transcriptional requirement for the KAT3 family of CBP and p300 histone acetyltransferases. Epigenetics. 2010; 5 (1):9-15. Epub 2010/01/30. PMID: 20110770; PubMed Central PMCID: PMC2829352.
10. Kasper LH, Boussouar F, Boyd K, Xu W, Biesen M, Rehg J, et al. Two transactivation mechanisms cooperate for the bulk of HIF-1-responsive gene expression. Embo J. 2005; 24(22):3846-58. Epub 2005/10/21. doi: 10.1038/sj.emboj.7600846 PMID: 16237459; PubMed Central PMCID: PMC1283945.
11. Dames SA, Martinez-Yamout M, De Guzman RN, Dyson HJ, Wright PE. Structural basis for Hif-1 alpha/CBP recognition in the cellular hypoxic response. Proc Natl Acad Sci U S A. 2002; 99(8):5271-6. Epub 2002/04/18. doi: 10.1073/pnas.082121399 PMID: 11959977; PubMed Central PMCID: PMC122759.
12. Freedman SJ, Sun ZY, Kung AL, France DS, Wagner G, Eck MJ. Structural basis for negative regulation of hypoxia-inducible factor-1alpha by CITED2. Nat Struct Biol. 2003; 10(7):504-12. Epub 2003/06/05. doi: 10.1038/nsb936 PMID: 12778114.
13. Freedman SJ, Sun ZY, Poy F, Kung AL, Livingston DM, Wagner G, et al. Structural basis for recruitment of CBP/p300 by hypoxia-inducible factor-1 alpha. Proc Natl Acad Sci U S A. 2002; 99(8):5367-72. Epub 2002/04/18. doi: 10.1073/pnas.082117899 PMID: 11959990; PubMed Central PMCID: PMC122775.
14. Petrij F, Giles RH, Dauwerse HG, Saris JJ, Hennekam RC, Masuno M, et al. Rubinstein-Taybi syndrome caused by mutations in the transcriptional co-activator CBP. Nature. 1995; 376(6538):348-51. Epub 1995/07/27. doi: 10.1038/376348a0 PMID: 7630403.
15. Roelfsema JH, White SJ, Ariyurek Y, Bartholdi D, Niedrist D, Papadia F, et al. Genetic heterogeneity in Rubinstein-Taybi syndrome: mutations in both the CBP and EP300 genes cause disease. American journal of human genetics. 2005; 76(4):572-80. Epub 2005/02/12. doi: 10.1086/429130 PMID: 15706485; PubMed Central PMCID: PMC1199295.
16. Alarcon JM, Malleret G, Touzani K, Vronskaya S, Ishii S, Kandel ER, et al. Chromatin acetylation, memory, and LTP are impaired in CBP+/- mice: a model for the cognitive deficit in Rubinstein-Taybi syndrome and its amelioration. Neuron. 2004; 42(6):947-59. Epub 2004/06/23. doi: 10.1016/j.neuron. 2004.05.021 S0896627304003022 [pii]. PMID: 15207239.
17. Bourtchouladze R, Lidge R, Catapano R, Stanley J, Gossweiler S, Romashko D, et al. A mouse model of Rubinstein-Taybi syndrome: defective long-term memory is ameliorated by inhibitors of phosphodiesterase 4. Proc Natl Acad Sci U S A. 2003; 100(18):10518-22. Epub 2003/08/22. doi: 10.1073/pnas. 1834280100 1834280100 [pii]. PMID: 12930888; PubMed Central PMCID: PMC193593.
18. Oike Y, Hata A, Mamiya T, Kaname T, Noda Y, Suzuki M, et al. Truncated CBP protein leads to classical Rubinstein-Taybi syndrome phenotypes in mice: implications for a dominant-negative mechanism. Hum Mol Genet. 1999; 8(3):387-96. Epub 1999/02/09. ddc050 [pii]. PMID: 9949198.
19. Tanaka Y, Naruse I, Maekawa T, Masuya H, Shiroishi T, Ishii S. Abnormal skeletal patterning in embryos lacking a single Cbp allele: a partial similarity with Rubinstein-Taybi syndrome. Proc Natl Acad Sci U S A. 1997; 94(19):10215-20. Epub 1997/09/18. PMID: 9294190; PubMed Central PMCID: PMC23342.
20. Cali F, Failla P, Chiavetta V, Ragalmuto A, Ruggeri G, Schinocca P, et al. Multiplex ligation-dependent probe amplification detection of an unknown large deletion of the CREB-binding protein gene in a patient with Rubinstein-Taybi syndrome. Genetics and molecular research: GMR. 2013; 12(3):2809-15. Epub 2013/01/15. doi: 10.4238/2013. January.7.2 PMID: 23315884.
21. Galera C, Taupiac E, Fraisse S, Naudion S, Toussaint E, Rooryck-Thambo C, et al. Socio-behavioral characteristics of children with Rubinstein-Taybi syndrome. J Autism Dev Disord. 2009; 39(9):1252-60. Epub 2009/04/08. doi: 10.1007/s10803-009-0733-4 PMID: 19350377.
22. Hellings JA, Hossain S, Martin JK, Baratang RR. Psychopathology, GABA, and the Rubinstein-Taybi syndrome: a review and case study. American journal of medical genetics. 2002; 114(2):190-5. Epub 2002/02/22. PMID: 11857581.
23. Schorry EK, Keddache M, Lanphear N, Rubinstein JH, Srodulski S, Fletcher D, et al. Genotype-phenotype correlations in Rubinstein-Taybi syndrome. Am J Med Genet A. 2008; 146A(19):2512-9. Epub 2008/09/17. doi: 10.1002/ajmg.a.32424 PMID: 18792986.
24. Banerjee-Basu S, Packer A. SFARI Gene: an evolving database for the autism research community. Dis Model Mech. 2010; 3(3-4):133-5. Epub 2010/03/10.3/3-4/133 [pii] doi: 10.1242/dmm.005439 PMID: 20212079.
25. Xu LM, Li JR, Huang Y, Zhao M, Tang X, Wei L. AutismKB: an evidence-based knowledgebase of autism genetics. Nucleic Acids Res. 2012; 40(Database issue):D1016-22. Epub 2011/12/06. gkr1145 [pii] doi: 10.1093/nar/gkr1145 PMID: 22139918; PubMed Central PMCID: PMC3245106.
26. Iossifov I, O'Roak BJ, Sanders SJ, Ronemus M, Krumm N, Levy D, et al. The contribution of de novo coding mutations to autism spectrum disorder. Nature. 2014; 515(7526):216-21. Epub 2014/11/05. doi: 10.1038/nature13908 PMID: 25363768; PubMed Central PMCID: PMC4313871.
27. Chao HT, Chen H, Samaco RC, Xue M, Chahrour M, Yoo J, et al. Dysfunction in GABA signalling mediates autism-like stereotypies and Rett syndrome phenotypes. Nature. 2010; 468(7321):263-9. Epub 2010/11/12. doi: 10.1038/nature09582 PMID: 21068835; PubMed Central PMCID: PMC3057962.
28. Shahbazian M, Young J, Yuva-Paylor L, Spencer C, Antalffy B, Noebels J, et al. Mice with truncated MeCP2 recapitulate many Rett syndrome features and display hyperacetylation of histone H3. Neuron. 2002; 35(2):243-54. Epub 2002/08/06. PMID: 12160743.
29. Wood MA, Attner MA, Oliveira AM, Brindle PK, Abel T. A transcription factor-binding domain of the coactivator CBP is essential for long-term memory and the expression of specific target genes. Learn Mem. 2006; 13(5):609-17. Epub 2006/09/19. doi: 10.1101/lm.213906 PMID: 16980541; PubMed Central PMCID: PMC1783615.
30. Earls LR, Bayazitov IT, Fricke RG, Berry RB, Illingworth E, Mittleman G, et al. Dysregulation of presynaptic calcium and synaptic plasticity in a mouse model of 22q11 deletion syndrome. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2010; 30(47):15843-55. Epub 2010/11/26. doi: 10.1523/JNEUROSCI.1425-10.2010 PMID: 21106823; PubMed Central PMCID: PMC3073555.
31. Bedford DC, Kasper LH, Wang R, Chang Y, Green DR, Brindle PK. Disrupting the CH1 Domain Structure in the Acetyltransferases CBP and p300 Results in Lean Mice with Increased Metabolic Control. Cell Metab. 2011; 14(2):219-30. Epub 2011/08/02. doi: 10.1016/j.cmet.2011.06.010 PMID: 21803292.
32. Rose SA, Djukic A, Jankowski JJ, Feldman JF, Fishman I, Valicenti-McDermott M. Rett syndrome: an eye-tracking study of attention and recognition memory. Developmental medicine and child neurology. 2013; 55(4):364-71. Epub 2013/03/16. doi: 10.1111/dmcn.12085 PMID: 23488948.
33. Han K, Holder JL Jr., Schaaf CP, Lu H, Chen H, Kang H, et al. SHANK3 overexpression causes maniclike behaviour with unique pharmacogenetic properties. Nature. 2013; 503(7474):72-7. Epub 2013/10/25. doi: 10.1038/nature12630 PMID: 24153177.
34. Chung L, Bey AL, Jiang YH. Synaptic plasticity in mouse models of autism spectrum disorders. The Korean journal of physiology & pharmacology: official journal of the Korean Physiological Society and the Korean Society of Pharmacology. 2012; 16(6):369-78. Epub 2012/12/28. doi: 10.4196/kjpp.2012. 16.6.369 PMID: 23269898; PubMed Central PMCID: PMC3526740.
35. Wingate M, Kirby RS, Pettygrove S, Cunniff C, Schulz E, Ghosh T, et al. Prevalence of Autism Spectrum Disorder Among Children Aged 8 Years-Autism and Developmental Disabilities Monitoring Network, 11 Sites, United States, 2010. Mmwr Surveill Summ. 2014; 63(2). WOS:000334352600001. PMID: 24670961
36. Wiley S, Swayne S, Rubinstein JH, Lanphear NE, Stevens CA. Rubinstein-Taybi syndrome medical guidelines. Am J Med Genet A. 2003; 119A(2):101-10. Epub 2003/05/16. doi: 10.1002/ajmg.a.10009 PMID: 12749047.
37. Srivastava AK, Schwartz CE. Intellectual disability and autism spectrum disorders: Causal genes and molecular mechanisms. Neuroscience and biobehavioral reviews. 2014. doi: 10.1016/j.neubiorev. 2014.02.015 PMID: 24709068.
38. Barnby G, Abbott A, Sykes N, Morris A, Weeks DE, Mott R, et al. Candidate-gene screening and association analysis at the autism-susceptibility locus on chromosome 16p: evidence of association at GRIN2A and ABAT. American journal of human genetics. 2005; 76(6):950-66. doi: 10.1086/430454 PMID: 15830322; PubMed Central PMCID: PMC1196454.
39. 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 (5):997-1007. doi: 10.1016/j.cell.2013.10.020 PMID: 24267886; PubMed Central PMCID: PMC3995413.
40. Crider A, Thakkar R, Ahmed AO, Pillai A. Dysregulation of estrogen receptor beta (ERbeta), aromatase (CYP19A1), and ER co-activators in the middle frontal gyrus of autism spectrum disorder subjects. Molecular autism. 2014; 5(1):46. doi: 10.1186/2040-2392-5-46 PMID: 25221668; PubMed Central PMCID: PMC4161836.
41. Wood MA, Kaplan MP, Park A, Blanchard EJ, Oliveira AM, Lombardi TL, et al. Transgenic mice expressing a truncated form of CREB-binding protein (CBP) exhibit deficits in hippocampal synaptic plasticity and memory storage. Learn Mem. 2005; 12(2):111-9. doi: 10.1101/lm.86605 PMID: 15805310; PubMed Central PMCID: PMC1074328.
42. Han S, Tai C, Westenbroek RE, Yu FH, Cheah CS, Potter GB, et al. Autistic-like behaviour in Scn1a+/- mice and rescue by enhanced GABA-mediated neurotransmission. Nature. 2012; 489(7416):385-90. Epub 2012/08/24. doi: 10.1038/nature11356 PMID: 22914087; PubMed Central PMCID: PMC3448848.
43. Schmeisser MJ, Ey E, Wegener S, Bockmann J, Stempel AV, Kuebler A, et al. Autistic-like behaviours and hyperactivity in mice lacking ProSAP1/Shank2. Nature. 2012; 486(7402):256-60. Epub 2012/06/16. doi: 10.1038/nature11015 PMID: 22699619.
44. Xiong HY, Alipanahi B, Lee LJ, Bretschneider H, Merico D, Yuen RK, et al. RNA splicing. The human splicing code reveals new insights into the genetic determinants of disease. Science. 2015; 347 (6218):1254806. Epub 2014/12/20. doi: 10.1126/science.1254806 PMID: 25525159.
45. Amir RE, Van den Veyver IB, Wan M, Tran CQ, Francke U, Zoghbi HY. Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat Genet. 1999; 23(2):185-8. Epub 1999/10/03. doi: 10.1038/13810 PMID: 10508514.
46. Yasui DH, Gonzales ML, Aflatooni JO, Crary FK, Hu DJ, Gavino BJ, et al. Mice with an isoform-ablating Mecp2 exon 1 mutation recapitulate the neurologic deficits of Rett syndrome. Hum Mol Genet. 2014; 23 (9):2447-58. Epub 2013/12/20. ddt640 [pii] doi: 10.1093/hmg/ddt640 PMID: 24352790; PubMed Central PMCID: PMC3976336.
47. Neul JL. The relationship of Rett syndrome and MECP2 disorders to autism. Dialogues in clinical neuroscience. 2012; 14(3):253-62. Epub 2012/12/12. PMID: 23226951; PubMed Central PMCID: PMC3513680.
48. Chahrour M, Jung SY, Shaw C, Zhou X, Wong ST, Qin J, et al. MeCP2, a key contributor to neurological disease, activates and represses transcription. Science. 2008; 320(5880):1224-9. Epub 2008/05/31. doi: 10.1126/science.1153252 PMID: 18511691; PubMed Central PMCID: PMC2443785.
49. Zocchi L, Sassone-Corsi P. SIRT1-mediated deacetylation of MeCP2 contributes to BDNF expression. Epigenetics. 2012; 7(7):695-700. Epub 2012/06/09. 20733 [pii] doi: 10.4161/epi.20733 PMID: 22677942; PubMed Central PMCID: PMC3414390.
50. Ramocki MB, Zoghbi HY. Failure of neuronal homeostasis results in common neuropsychiatric phenotypes. Nature. 2008; 455(7215):912-8. doi: 10.1038/nature07457 PMID: 18923513; PubMed Central PMCID: PMC2696622.
51. Toro R, Konyukh M, Delorme R, Leblond C, Chaste P, Fauchereau F, et al. Key role for gene dosage and synaptic homeostasis in autism spectrum disorders. Trends in genetics: TIG. 2010; 26(8):363-72. doi: 10.1016/j.tig.2010.05.007 PMID: 20609491.
52. Collins AL, Levenson JM, Vilaythong AP, Richman R, Armstrong DL, Noebels JL, et al. Mild overexpression of MeCP2 causes a progressive neurological disorder in mice. Hum Mol Genet. 2004; 13 (21):2679-89. Epub 2004/09/08. doi: 10.1093/hmg/ddh282 PMID: 15351775.
53. Ehninger D, Han S, Shilyansky C, Zhou Y, Li W, Kwiatkowski DJ, et al. Reversal of learning deficits in a Tsc2+/- mouse model of tuberous sclerosis. Nature medicine. 2008; 14(8):843-8. Epub 2008/06/24. doi: 10.1038/nm1788 PMID: 18568033; PubMed Central PMCID: PMC2664098.
54. Rinaldi T, Kulangara K, Antoniello K, Markram H. Elevated NMDA receptor levels and enhanced postsynaptic long-term potentiation induced by prenatal exposure to valproic acid. Proc Natl Acad Sci U S A. 2007; 104(33):13501-6. Epub 2007/08/07. doi: 10.1073/pnas.0704391104 PMID: 17675408; PubMed Central PMCID: PMC1948920.
55. Kaksonen M, Pavlov I, Voikar V, Lauri SE, Hienola A, Riekki R, et al. Syndecan-3-deficient mice exhibit enhanced LTP and impaired hippocampus-dependent memory. Molecular and cellular neurosciences. 2002; 21(1):158-72. Epub 2002/10/03. PMID: 12359158.
56. Kim MH, Choi J, Yang J, Chung W, Kim JH, Paik SK, et al. Enhanced NMDA receptor-mediated synaptic transmission, enhanced long-term potentiation, and impaired learning and memory in mice lacking IRSp53. The Journal of neuroscience: the official journal of the Society for Neuroscience. 2009; 29 (5):1586-95. Epub 2009/02/06. doi: 10.1523/JNEUROSCI.4306-08.2009 PMID: 19193906.
57. Migaud M, Charlesworth P, Dempster M, Webster LC, Watabe AM, Makhinson M, et al. Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Nature. 1998; 396(6710):433-9. Epub 1998/12/16. doi: 10.1038/24790 PMID: 9853749.
58. Martin HG, Manzoni OJ. Late onset deficits in synaptic plasticity in the valproic acid rat model of autism. Frontiers in cellular neuroscience. 2014; 8:23. doi: 10.3389/fncel.2014.00023 PMID: 24550781; PubMed Central PMCID: PMC3907704.
59. Dyson HJ, Wright PE. Intrinsically unstructured proteins and their functions. Nat Rev Mol Cell Biol. 2005; 6(3):197-208. Epub 2005/03/02. nrm1589 [pii] doi: 10.1038/nrm1589 PMID: 15738986.