Ankrd11 is a chromatin regulator involved in autism that is essential for neural development

Developmental Cell

Volumn 32, Issue 1, 2015, Pages 31-42

  Gallagher, Denis ^a,b   Voronova, Anastassia ^a   Zander, Mark A ^a   Cancino, Gonzalo I ^a   Bramall, Alexa ^a   Krause, Matthew P ^a   Abad, Clemer ^c   Tekin, Mustafa ^c   Neilsen, Paul M ^d   Callen, David F ^e   Scherer, Stephen W ^a,f   Keller, Gordon M ^b,f   Kaplan, David R ^a,f   Walz, Katherina ^c   Miller, Freda D ^a,b,f  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY HEALTH NETWORK   (Canada)

^c UNIVERSITY OF MIAMI MILLER SCHOOL OF MEDICINE   (United States)

^d SWINBURNE UNIVERSITY OF TECHNOLOGY   (Malaysia)

^e UNIVERSITY OF ADELAIDE   (Australia)

^f UNIVERSITY OF TORONTO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANKYRIN; ANKYRIN REPEAT DOMAIN CONTAINING PROTEIN 11; HISTONE ACETYLTRANSFERASE; HISTONE DEACETYLASE 3; UNCLASSIFIED DRUG; ANKRD11 PROTEIN, MOUSE; BIOLOGICAL MARKER; CHROMATIN; DNA BINDING PROTEIN; HISTONE; HISTONE DEACETYLASE; MESSENGER RNA; SMALL INTERFERING RNA;

ANIMAL CELL; ARTICLE; AUTISM; BRAIN CELL CULTURE; CELL PROLIFERATION; CHROMATIN; ENZYME ACTIVITY; GENE TARGETING; HISTONE ACETYLATION; HUMAN; HUMAN CELL; MOUSE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; ACETYLATION; ANIMAL; ANIMAL BEHAVIOR; CELL CULTURE; CELL DIFFERENTIATION; CHEMISTRY; CHROMATIN IMMUNOPRECIPITATION; DNA MICROARRAY; FEMALE; GENE EXPRESSION PROFILING; GENETICS; IMMUNOPRECIPITATION; METABOLISM; PATHOLOGY; PHYSIOLOGY; PROTEIN PROCESSING; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

MURINAE; MUS;

ACETYLATION; ANIMALS; AUTISTIC DISORDER; BEHAVIOR, ANIMAL; BIOLOGICAL MARKERS; BLOTTING, WESTERN; CELL DIFFERENTIATION; CELL PROLIFERATION; CELLS, CULTURED; CHROMATIN; CHROMATIN IMMUNOPRECIPITATION; DNA-BINDING PROTEINS; FEMALE; GENE EXPRESSION PROFILING; HISTONE DEACETYLASES; HISTONES; IMMUNOPRECIPITATION; MICE; NEUROGENESIS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTEIN PROCESSING, POST-TRANSLATIONAL; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; RNA, SMALL INTERFERING;

EID: 84922343890     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2014.11.031     Document Type: Article

References (39)

1. Barbaric I., Perry M.J., Dear T.N., Rodrigues Da Costa A., Salopek D., Marusic A., Hough T., Wells S., Hunter A.J., Cheeseman M., Brown S.D.M. An ENU-induced mutation in the Ankrd11 gene results in an osteopenia-like phenotype in the mouse mutant Yoda. Physiol. Genomics 2008, 32:311-321.
2. Barnabé-Heider F., Wasylnka J.A., Fernandes K.J., Porsche C., Sendtner M., Kaplan D.R., Miller F.D. Evidence that embryonic neurons regulate the onset of cortical gliogenesis via cardiotrophin-1. Neuron 2005, 48:253-265.
3. Bowers E.M., Yan G., Mukherjee C., Orry A., Wang L., Holbert M.A., Crump N.T., Hazzalin C.A., Liszczak G., Yuan H., et al. Virtual ligand screening of the p300/CBP histone acetyltransferase: identification of a selective small molecule inhibitor. Chem. Biol. 2010, 17:471-482.
4. Cancino G.I., Yiu A.P., Fatt M.P., Dugani C.B., Flores E.R., Frankland P.W., Josselyn S.A., Miller F.D., Kaplan D.R. p63 Regulates adult neural precursor and newly born neuron survival to control hippocampal-dependent behavior. J.Neurosci. 2013, 33:12569-12585.
5. Carter M.D., Shah C.R., Muller C.L., Crawley J.N., Carneiro A.M., Veenstra-VanderWeele J. Absence of preference for social novelty and increased grooming in integrin β3 knockout mice: initial studies and future directions. Autism Res. 2011, 4:57-67.
6. Castelo-Branco G., Lilja T., Wallenborg K., Falcão A.M., Marques S.C., Gracias A., Solum D., Paap R., Walfridsson J., Teixeira A.I., et al. Neural stem cell differentiation is dictated by distinct actions of nuclear receptor corepressors and histone deacetylases. Stem Cell Rep. 2014, 3:502-515.
7. Coles-Takabe B.L., Brain I., Purpura K.A., Karpowicz P., Zandstra P.W., Morshead C.M., van der Kooy D. Don't look: growing clonal versus nonclonal neural stem cell colonies. Stem Cells 2008, 26:2938-2944.
8. Crawley J.N., Chen T., Puri A., Washburn R., Sullivan T.L., Hill J.M., Young N.B., Nadler J.J., Moy S.S., Young L.J., et al. Social approach behaviors in oxytocin knockout mice: comparison of two independent lines tested in different laboratory environments. Neuropeptides 2007, 41:145-163.
9. Devlin B., Scherer S.W. Genetic architecture in autism spectrum disorder. Curr. Opin. Genet. Dev. 2012, 22:229-237.
10. Gallagher D., Norman A.A., Woodard C.L., Yang G., Gauthier-Fisher A., Fujitani M., Vessey J.P., Cancino G.I., Sachewsky N., Woltjen K., et al. Transient maternal IL-6 mediates long-lasting changes in neural stem cell pools by deregulating an endogenous self-renewal pathway. Cell Stem Cell 2013, 13:564-576.
11. Iossifov I., O'Roak B.J., Sanders S.J., Ronemus M., Krumm N., Levy D., Stessman H.A., Witherspoon K.T., Vives L., Patterson K.E., et al. The contribution of de novo coding mutations to autism spectrum disorder. Nature 2014, 515:216-221. 10.1038/nature13908.
12. Jamain S., Radyushkin K., Hammerschmidt K., Granon S., Boretius S., Varoqueaux F., Ramanantsoa N., Gallego J., Ronnenberg A., Winter D., et al. Reduced social interaction and ultrasonic communication in amouse model of monogenic heritable autism. Proc. Natl. Acad. Sci. USA 2008, 105:1710-1715.
13. Li C.W., Dinh G.K., Zhang A., Chen J.D. Ankyrin repeats-containing cofactors interact with ADA3 and modulate its co-activator function. Biochem. J. 2008, 413:349-357.
14. Lilja T., Heldring N., Hermanson O. Like a rolling histone: epigenetic regulation of neural stem cells and brain development by factors controlling histone acetylation and methylation. Biochim. Biophys. Acta 2013, 1830:2354-2360.
15. Lo-Castro A., Brancati F., Digilio M.C., Garaci F.G., Bollero P., Alfieri P., Curatolo P. Neurobehavioral phenotype observed in KBG syndrome caused by ANKRD11 mutations. Am. J. Med. Genet. B. Neuropsychiatr. Genet. 2013, 162B:17-23.
16. Marshall C.R., Noor A., Vincent J.B., Lionel A.C., Feuk L., Skaug J., Shago M., Moessner R., Pinto D., Ren Y., et al. Structural variation of chromosomes in autism spectrum disorder. Am. J. Hum. Genet. 2008, 82:477-488.
17. McCarthy S.E., Gillis J., Kramer M., Lihm J., Yoon S., Berstein Y., Mistry M., Pavlidis P., Solomon R., Ghiban E., et al. De novo mutations in schizophrenia implicate chromatin remodeling and support a genetic overlap with autism and intellectual disability. Mol. Psychiatry 2014, 19:652-658.
18. McQuown S.C., Barrett R.M., Matheos D.P., Post R.J., Rogge G.A., Alenghat T., Mullican S.E., Jones S., Rusche J.R., Lazar M.A., Wood M.A. HDAC3 is a critical negative regulator of long-term memory formation. J.Neurosci. 2011, 31:764-774.
19. Molina J., Carmona-Mora P., Chrast J., Krall P.M., Canales C.P., Lupski J.R., Reymond A., Walz K. Abnormal social behaviors and altered gene expression rates in a mouse model for Potocki-Lupski syndrome. Hum. Mol. Genet. 2008, 17:2486-2495.
20. Moy S.S., Nadler J.J., Perez A., Barbaro R.P., Johns J.M., Magnuson T.R., Piven J., Crawley J.N. Sociability and preference for social novelty in five inbred strains: an approach to assess autistic-like behavior in mice. Genes Brain Behav. 2004, 3:287-302.
21. Mullin A.P., Gokhale A., Moreno-De-Luca A., Sanyal S., Waddington J.L., Faundez V. Neurodevelopmental disorders: mechanisms and boundary definitions from genomes, interactomes and proteomes. Transl. Psychiatr. 2013, 3:e329.
22. Neilsen P.M., Cheney K.M., Li C.W., Chen J.D., Cawrse J.E., Schulz R.B., Powell J.A., Kumar R., Callen D.F. Identification of ANKRD11 as a p53 coactivator. J.Cell Sci. 2008, 121:3541-3552.
23. Pinto D., Delaby E., Merico D., Barbosa M., Merikangas A., Klei L., Thiruvahindrapuram B., Xu X., Ziman R., Wang Z., et al. Convergence of genes and cellular pathways dysregulated in autism spectrum disorders. Am. J. Hum. Genet. 2014, 94:677-694.
24. Rosenbloom K.R., Sloan C.A., Malladi V.S., Dreszer T.R., Learned K., Kirkup V.M., Wong M.C., Maddren M., Fang R., Heitner S.G., et al. ENCODE data in the UCSC Genome Browser: year 5 update. Nucleic Acids Res. 2013, 41:D56-D63.
25. Rudenko A., Tsai L.H. Epigenetic modifications in the nervous system and their impact upon cognitive impairments. Neuropharmacology 2014, 80:70-82.
26. Savage J., Conley A.J., Blais A., Skerjanc I.S. SOX15 and SOX7 differentially regulate the myogenic program in P19 cells. Stem Cells 2009, 27:1231-1243.
27. Sirmaci A., Spiliopoulos M., Brancati F., Powell E., Duman D., Abrams A., Bademci G., Agolini E., Guo S., Konuk B., et al. Mutations in ANKRD11 cause KBG syndrome, characterized by intellectual disability, skeletal malformations, and macrodontia. Am. J. Hum. Genet. 2011, 89:289-294.
28. Söderberg O., Gullberg M., Jarvius M., Ridderstråle K., Leuchowius K.J., Jarvius J., Wester K., Hydbring P., Bahram F., Larsson L.G., Landegren U. Direct observation of individual endogenous protein complexes insitu by proximity ligation. Nat. Methods 2006, 3:995-1000.
29. Stoner R., Chow M.L., Boyle M.P., Sunkin S.M., Mouton P.R., Roy S., Wynshaw-Boris A., Colamarino S.A., Lein E.S., Courchesne E. Patches of disorganization in the neocortex of children with autism. N.Engl. J. Med. 2014, 370:1209-1219.
30. Sun G., Yu R.T., Evans R.M., Shi Y. Orphan nuclear receptor TLX recruits histone deacetylases to repress transcription and regulate neural stem cell proliferation. Proc. Natl. Acad. Sci. USA 2007, 104:15282-15287.
31. Tsui D., Vessey J.P., Tomita H., Kaplan D.R., Miller F.D. FoxP2 regulates neurogenesis during embryonic cortical development. J.Neurosci. 2013, 33:244-258.
32. Wang J., Weaver I.C., Gauthier-Fisher A., Wang H., He L., Yeomans J., Wondisford F., Kaplan D.R., Miller F.D. CBP histone acetyltransferase activity regulates embryonic neural differentiation in the normal and Rubinstein-Taybi syndrome brain. Dev. Cell 2010, 18:114-125.
33. Wang J., Gallagher D., DeVito L.M., Cancino G.I., Tsui D., He L., Keller G.M., Frankland P.W., Kaplan D.R., Miller F.D. Metformin activates an atypical PKC-CBP pathway to promote neurogenesis and enhance spatial memory formation. Cell Stem Cell 2012, 11:23-35.
34. Willemsen M.H., Fernandez B.A., Bacino C.A., Gerkes E., de Brouwer A.P., Pfundt R., Sikkema-Raddatz B., Scherer S.W., Marshall C.R., Potocki L., et al. Identification of ANKRD11 and ZNF778 as candidate genes for autism and variable cognitive impairment in the novel 16q24.3 microdeletion syndrome. Eur. J. Hum. Genet. 2010, 18:429-435.
35. Yang G., Smibert C.A., Kaplan D.R., Miller F.D. An eIF4E/4E-T complex determines the genesis of neurons from precursors by translationally repressing a proneurogenic transcription program. Neuron 2014, 84:723-739.
36. Zander M.A., Burns S.E., Yang G., Kaplan D.R., Miller F.D. Snail coordinately regulates downstream pathways to control multiple aspects of mammalian neural precursor development. J.Neurosci. 2014, 34:5164-5175.
37. Zhang A., Yeung P.L., Li C.-W., Tsai S.-C., Dinh G.K., Wu X., Li H., Chen J.D. Identification of a novel family of ankyrin repeats containing cofactors for p160 nuclear receptor coactivators. J.Biol. Chem. 2004, 279:33799-33805.
38. Zhang A., Li C.-W., Chen J.D. Characterization of transcriptional regulatory domains of ankyrin repeat cofactor-1. Biochem. Biophys. Res. Commun. 2007, 358:1034-1040.
39. Zhang A., Li C.W., Tsai S.C., Chen J.D. Subcellular localization of ankyrin repeats cofactor-1 regulates its corepressor activity. J.Cell. Biochem. 2007, 101:1301-1315.