Altered neocortical gene expression, brain overgrowth and functional over-connectivity in chd8 haploinsufficient mice

Cerebral Cortex

Volumn 28, Issue 6, 2018, Pages 2192-2206

  Suetterlin, Philipp ^a   Hurley, Shaun ^a   Mohan, Conor ^a   Riegman, Kimberley L H ^a   Pagani, Marco ^b   Caruso, Angela ^c   Ellegood, Jacob ^d   Galbusera, Alberto ^b   Crespo Enriquez, Ivan ^a   Michetti, Caterina ^e   Yee, Yohan ^d   Ellingford, Robert ^a   Brock, Olivier ^a   Delogu, Alessio ^a   Francis West, Philippa ^a   Lerch, Jason P ^d   Scattoni, Maria Luisa ^c   Gozzi, Alessandro ^b   Fernandes, Cathy ^a   Basson, M Albert ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

^b Center for Neuroscience and Cognitive Systems UniTn   (Italy)

^c ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^d HOSPITAL FOR SICK CHILDREN   (Canada)

^e ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AXON GUIDANCE; BRAIN GROWTH; BRAIN SIZE; CELL ADHESION; CONTROLLED STUDY; DOWN REGULATION; FEMALE; FUNCTIONAL CONNECTIVITY; GENE EXPRESSION; GENETIC TRANSCRIPTION; HAPLOINSUFFICIENCY; HIPPOCAMPUS; HYPERTELORISM; HYPOACTIVITY; MALE; MOTOR DYSFUNCTION; MOUSE; NEOCORTEX; NONHUMAN; PERINATAL PERIOD; PHENOTYPE; PRIORITY JOURNAL; SOCIAL ASPECT; ANIMAL; AUTISM; BRAIN; DISEASE MODEL; GENE EXPRESSION REGULATION; GENETICS; KNOCKOUT MOUSE; METABOLISM; NERVE TRACT; PATHOPHYSIOLOGY;

DNA BINDING PROTEIN; DUPLIN PROTEIN, MOUSE; TRANSCRIPTOME;

ANIMALS; AUTISM SPECTRUM DISORDER; BRAIN; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HAPLOINSUFFICIENCY; MICE; MICE, KNOCKOUT; NEOCORTEX; NEURAL PATHWAYS; TRANSCRIPTOME;

EID: 85047735670     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhy058     Document Type: Article

References (71)

1. Andrews S. 2010. FASTQC. A quality control tool for high throughput sequence data. Available from. http://www. bioinformatics.babraham.ac.uk/projects/fastqc/
2. APA. 2013. Diagnostic and statistical manual of mental disorders. Arlington, VA: American Psychiatric Publishing.
3. Avants BB, Tustison NJ, Song G, Gee JC. 2009. ANTS: Advanced Open-Source Normalization Tools for Neuroanatomy. Penn Image Computing and Science Laboratory.
4. Barnard RA, Pomaville MB, O?Roak BJ. 2015. Mutations and modeling of the chromatin remodeler chd8 define an emerging autism etiology. Front Neurosci. 9:477.
5. Bedford R, Pickles A, Lord C. 2016. Early gross motor skills predict the subsequent development of language in children with autism spectrum disorder. Autism Res. 9(9):993-1001.
6. Belmonte MK, Allen G, Beckel-Mitchener A, Boulanger LM, Carper RA, Webb SJ. 2004. Autism and abnormal development of brain connectivity. J Neurosci Nurs. 24(42):9228-9231.
7. Bernier R, Golzio C, Xiong B, Stessman HA, Coe BP, Penn O, Witherspoon K, Gerdts J, Baker C, Vulto-van Silfhout AT, et al. 2014. Disruptive chd8 mutations define a subtype of autism early in development. Cell. 158(2):263-276.
8. Blatt GJ. 2012. The neuropathology of autism. Scientifica (Cairo). 2012:703675.
9. Bourgeron T. 2015. From the genetic architecture to synaptic plasticity in autism spectrum disorder. Nat Rev Neurosci. 16 (9):551-563.
10. Bruneau N, Dourneau MC, Garreau B, Pourcelot L, Lelord G. 1992. Blood flow response to auditory stimulations in normal, mentally retarded, and autistic children: A preliminary transcranial doppler ultrasonographic study of the middle cerebral arteries. Biol Psychiatry. 32(8):691-699.
11. Cao R, Zhang Y. 2004. Suz12 is required for both the histone methyltransferase activity and the silencing function of the eed-ezh2 complex. Mol Cell. 15(1):57-67.
12. Cerliani L, Mennes M, Thomas RM, Di Martino A, Thioux M, Keysers C. 2015. Increased functional connectivity between subcortical and cortical resting-state networks in autism spectrum disorder. JAMA Psychiatry. 72(8):767-777.
13. Chakravarty MM, Steadman P, van Eede MC, Calcott RD, Gu V, Shaw P, Raznahan A, Collins DL, Lerch JP. 2013. Performing label-fusion-based segmentation using multiple automatically generated templates. Human Brain Mapping. 34(10): 2635-2654.
14. Chen EY, Tan CM, Kou Y, Duan Q, Wang Z, Meirelles GV, Clark NR, Ma?ayan A. 2013. Enrichr: interactive and collaborative html5 gene list enrichment analysis tool. BMC Bioinf. 14:128.
15. Cherkassky VL, Kana RK, Keller TA, Just MA. 2006. Functional connectivity in a baseline resting-state network in autism. NeuroReport. 17(16):1687-1690.
16. Chinello A, Di Gangi V, Valenza E. 2016. Persistent primary reflexes affect motor acts: potential implications for autism spectrum disorder. Research in Developmental Disabilities.
17. Constantino JN, Charman T. 2016. Diagnosis of autism spectrum disorder: reconciling the syndrome, its diverse origins, and variation in expression. Lancet Neurol. 15(3):279-291.
18. Cotney J, Muhle RA, Sanders SJ, Liu L, Willsey AJ, Niu W, Liu W, Klei L, Lei J, Yin J, et al. 2015. The autism-Associated chromatin modifier chd8 regulates other autism risk genes during human neurodevelopment. Nat Commun. 6:6404.
19. Croen LA, Zerbo O, Qian Y, Massolo ML, Rich S, Sidney S, Kripke C. 2015. The health status of adults on the autism spectrum. Autism. 19(7):814-823.
20. Di Martino A, Yan CG, Li Q, Denio E, Castellanos FX, Alaerts K, Anderson JS, Assaf M, Bookheimer SY, Dapretto M, et al. 2014. The autism brain imaging data exchange: Towards a large-scale evaluation of the intrinsic brain architecture in autism. Mol Psychiatry. 19(6):659-667.
21. Donovan AP, Basson MA. 2017. The neuroanatomy of autism-A developmental perspective. J Anat. 230(1):4-15.
22. Durak O, Gao F, Kaeser-Woo YJ, Rueda R, Martorell AJ, Nott A, Liu CY, Watson LA, Tsai LH. 2016. Chd8 mediates cortical neurogenesis via transcriptional regulation of cell cycle and wnt signaling. Nat Neurosci. 19(11):1477.
23. Ecker C. 2016. The neuroanatomy of autism spectrum disorder: An overview of structural neuroimaging findings and their translatability to the clinical setting. Autism. 21(1): 18-208.
24. Eden E, Navon R, Steinfeld I, Lipson D, Yakhini Z. 2009. Gorilla: A tool for discovery and visualization of enriched go terms in ranked gene lists. BMC Bioinf. 10:48.
25. Edgar JC, Fisk Iv CL, Berman JI, Chudnovskaya D, Liu S, Pandey J, Herrington JD, Port RG, Schultz RT, Roberts TP. 2015. Auditory encoding abnormalities in children with autism spectrum disorder suggest delayed development of auditory cortex. Molecular Autism. 6:69.
26. Ferrari L, Turrini G, Crestan V, Bertani S, Cristofori P, Bifone A, Gozzi A. 2012. A robust experimental protocol for pharmacological fMRI in rats and mice. J Neurosci Methods. 204(1): 9-18.
27. French L, Pavlidis P. 2011. Relationships between gene expression and brain wiring in the adult rodent brain. PLoS Comput Biol. 7(1):e1001049.
28. Friedel M, van Eede MC, Pipitone J, Chakravarty MM, Lerch JP. 2014. Pydpiper: A flexible toolkit for constructing novel registration pipelines. Front Neuroinform. 8:67.
29. Gompers AL, Su-Feher L, Ellegood J, Copping NA, Riyadh MA, Stradleigh TW, Pride MC, Schaffler MD, Wade AA, Catta-Preta R, et al. 2017. Germline chd8 haploinsufficiency alters brain development in mouse. Nat Neurosci. 20(8):1062.
30. Hill CA, Sussan TE, Reeves RH, Richtsmeier JT. 2009. Complex contributions of ets2 to craniofacial and thymus phenotypes of trisomic "down syndrome" mice. Am J Med Genet A. 149A (10):2158-2165.
31. Huang DW, Sherman BT, Lempicki RA. 2009. Systematic and integrative analysis of large gene lists using david bioinformatics resources. Nat Protoc. 4(1):44-57.
32. Iossifov I, O?Roak BJ, Sanders SJ, Ronemus M, Krumm N, Levy D, Stessman HA, Witherspoon KT, Vives L, Patterson KE, et al. 2014. The contribution of de novo coding mutations to autism spectrum disorder. Nature. 515(7526):216-221.
33. Jeste SS, Tuchman R. 2015. Autism spectrum disorder and epilepsy: Two sides of the same coin? J Child Neurol. 30(14): 1963-1971.
34. Just MA, Cherkassky VL, Keller TA, Minshew NJ. 2004. Cortical activation and synchronization during sentence comprehension in high-functioning autism: evidence of underconnectivity. Brain. 127(Pt 8):1811-1821.
35. Katayama Y, Nishiyama M, Shoji H, Ohkawa Y, Kawamura A, Sato T, Suyama M, Takumi T, Miyakawa T, Nakayama KI. 2016. Chd8 haploinsufficiency results in autistic-like phenotypes in mice. Nature. 537(7622):675-679.
36. Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL. 2013. Tophat2: Accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14(4):R36.
37. Krueger F. 2012. Trim Galore! Available from: http://www. bioinformatics.babraham.ac.uk/projects/trim-galore/
38. Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A, Bernard A, Boe AF, Boguski MS, Brockway KS, Byrnes EJ, et al. 2007. Genome-wide atlas of gene expression in the adult mouse brain. Nature. 445(7124):168-176.
39. Lewandoski M, Martin GR. 1997. Cre-mediated chromosome loss in mice. Nat Genet. 17(2):223-225.
40. Liao Y, Smyth GK, Shi W. 2014. Featurecounts: An efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics. 30(7):923-930.
41. Liska A, Bertero A, Gomolka R, Sabbioni M, Galbusera A, Barsotti N, Panzeri S, Scattoni ML, Pasqualetti M, Gozzi A. 2017. Homozygous loss of autism-risk gene cntnap2 results in reduced local and long-range prefrontal functional connectivity. Cereb Cortex. 10:1-13.
42. Liska A, Galbusera A, Schwarz AJ, Gozzi A. 2015. Functional connectivity hubs of the mouse brain. NeuroImage. 115: 281-291.
43. Liska A, Gozzi A. 2016. Can mouse imaging studies bring order to autism connectivity chaos? Front Neurosci. 10:484.
44. Liu X, Zhu XH, Zhang Y, Chen W. 2011. Neural origin of spontaneous hemodynamic fluctuations in rats under burstsuppression anesthesia condition. Cereb Cortex. 21(2): 374-384.
45. Love MI, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for rna-seq data with deseq2. Genome Biol. 15(12):550.
46. Marco EJ, Hinkley LB, Hill SS, Nagarajan SS. 2011. Sensory processing in autism: A review of neurophysiologic findings. Pediatr Res. 69(5 Pt 2):48R-54R.
47. Merner N, Forgeot d?Arc B, Bell SC, Maussion G, Peng H, Gauthier J, Crapper L, Hamdan FF, Michaud JL, Mottron L, et al. 2016. A de novo frameshift mutation in chromodomain helicase DNA-binding domain 8 (chd8): A case report and literature review. Am J Med Genet A. 170(5):1225-1235.
48. Neale BM, Kou Y, Liu L, Ma?ayan A, Samocha KE, Sabo A, Lin CF, Stevens C, Wang LS, Makarov V, et al. 2012. Patterns and rates of exonic de novo mutations in autism spectrum disorders. Nature. 485(7397):242-245.
49. Ng L, Bernard A, Lau C, Overly CC, Dong HW, Kuan C, Pathak S, Sunkin SM, Dang C, Bohland JW, et al. 2009. An anatomic gene expression atlas of the adult mouse brain. Nat Neurosci. 12(3):356-362.
50. Orefice LL, Zimmerman AL, Chirila AM, Sleboda SJ, Head JP, Ginty DD. 2016. Peripheral mechanosensory neuron dysfunction underlies tactile and behavioral deficits in mouse models of asds. Cell. 166(2):299-313.
51. O?Roak BJ, Stessman HA, Boyle EA, Witherspoon KT, Martin B, Lee C, Vives L, Baker C, Hiatt JB, Nickerson DA, et al. 2014. Recurrent de novo mutations implicate novel genes underlying simplex autism risk. Nat Commun. 5:5595.
52. O?Roak BJ, Vives L, Fu W, Egertson JD, Stanaway IB, Phelps IG, Carvill G, Kumar A, Lee C, Ankenman K, et al. 2012a. Multiplex targeted sequencing identifies recurrently mutated genes in autism spectrum disorders. Science. 338 (6114):1619-1622.
53. O?Roak BJ, Vives L, Girirajan S, Karakoc E, Krumm N, Coe BP, Levy R, Ko A, Lee C, Smith JD, et al. 2012b. Sporadic autism exomes reveal a highly interconnected protein network of de novo mutations. Nature. 485(7397):246-250.
54. Picci G, Gotts SJ, Scherf KS. 2016. A theoretical rut: revisiting and critically evaluating the generalized under/over-connectivity hypothesis of autism. Dev Sci. 19(4):524-549.
55. Platt RJ, Zhou Y, Slaymaker IM, Shetty AS, Weisbach NR, Kim JA, Sharma J, Desai M, Sood S, Kempton HR, et al. 2017. Chd8 mutation leads to autistic-like behaviors and impaired striatal circuits. Cell Rep. 19(2):335-350.
56. Scott-Van Zeeland AA, Abrahams BS, Alvarez Retuerto AI, Sonnenblick LI, Rudie JD, Ghahremani D, Mumford JA, Poldrack RA, Dapretto M, Geschwind DH, et al. 2010. Altered functional connectivity in frontal lobe circuits is associated with variation in the autism risk gene cntnap2. Sci Transl Med. 2(56):56-80.
57. Sforazzini F, Bertero A, Dodero L, David G, Galbusera A, Scattoni ML, Pasqualetti M, Gozzi A. 2016. Altered functional connectivity networks in acallosal and socially impaired btbr mice. Brain Struct Funct. 221(2):941-954.
58. Sforazzini F, Schwarz AJ, Galbusera A, Bifone A, Gozzi A. 2014. Distributed bold and cbv-weighted resting-state networks in the mouse brain. NeuroImage. 87:403-415.
59. Sinclair D, Oranje B, Razak KA, Siegel SJ, Schmid S. 2017. Sensory processing in autism spectrum disorders and fragile x syndrome-from the clinic to animal models. Neurosci Biobehav Rev. 76(Pt B):235-253.
60. Steffey MA, Brosnan RJ, Steffey EP. 2003. Assessment of halothane and sevoflurane anesthesia in spontaneously breathing rats. Am J Vet Res. 64(4):470-474.
61. Stessman HA, Xiong B, Coe BP, Wang T, Hoekzema K, Fenckova M, Kvarnung M, Gerdts J, Trinh S, Cosemans N, et al. 2017. Targeted sequencing identifies 91 neurodevelopmentaldisorder risk genes with autism and developmentaldisability biases. Nat Genet. 49(4):515-526.
62. Stolerman ES, Smith B, Chaubey A, Jones JR. 2016. Chd8 intragenic deletion associated with autism spectrum disorder. Eur J Med Genet. 59(4):189-194.
63. Sugathan A, Biagioli M, Golzio C, Erdin S, Blumenthal I, Manavalan P, Ragavendran A, Brand H, Lucente D, Miles J, et al. 2014. Chd8 regulates neurodevelopmental pathways associated with autism spectrum disorder in neural progenitors. Proc Natl Acad Sci USA. 111(42):E4468-E4477.
64. Talkowski ME, Rosenfeld JA, Blumenthal I, Pillalamarri V, Chiang C, Heilbut A, Ernst C, Hanscom C, Rossin E, Lindgren AM, et al. 2012. Sequencing chromosomal abnormalities reveals neurodevelopmental loci that confer risk across diagnostic boundaries. Cell. 149(3):525-537.
65. Tavassoli T, Miller LJ, Schoen SA, Nielsen DM, Baron-Cohen S. 2014. Sensory over-responsivity in adults with autism spectrum conditions. Autism. 18(4):428-432.
66. Thompson BA, Tremblay V, Lin G, Bochar DA. 2008. Chd8 is an atp-dependent chromatin remodeling factor that regulates beta-catenin target genes. Mol Cell Biol. 28(12): 3894-3904.
67. Truett GE, Heeger P, Mynatt RL, Truett AA, Walker JA, Warman ML. 2000. Preparation of pcr-quality mouse genomic DNA with hot sodium hydroxide and tris (hotshot). Biotechniques. 29(1):52-54.
68. Whittaker DE, Riegman KL, Kasah S, Mohan C, Yu T, Sala BP, Hebaishi H, Caruso A, Marques AC, Michetti C, et al. 2017a. The chromatin remodeling factor CHD7 controls cerebellar development by regulating reelin expression. J Clin Invest. 127:874-887.
69. Whittaker DE, Kasah S, Donovan APA, Ellegood J, Riegman KLH, Volk HA, McGonnell I, Lerch JP, Basson MA. 2017b. Distinct cerebellar foliation anomalies in a chd7 haploinsufficient mouse model of charge syndrome. Am J Med Genet C Semin Med Genet. 175(4). 10.1002/ajmg.c.31595.
70. Yuan CC, Zhao X, Florens L, Swanson SK, Washburn MP, Hernandez N. 2007. Chd8 associates with human staf and contributes to efficient u6 RNA polymerase iii transcription. Mol Cell Biol. 27(24):8729-8738.
71. Zhan Y, Paolicelli RC, Sforazzini F, Weinhard L, Bolasco G, Pagani F, Vyssotski AL, Bifone A, Gozzi A, Ragozzino D, et al. 2014. Deficient neuron-microglia signaling results in impaired functional brain connectivity and social behavior. Nat Neurosci. 17(3):400-406.