BCL11A Haploinsufficiency Causes an Intellectual Disability Syndrome and Dysregulates Transcription

American Journal of Human Genetics

Volumn 99, Issue 2, 2016, Pages 253-274

  Dias, Cristina ^a   Estruch, Sara B ^b   Graham, Sarah A ^b   McRae, Jeremy ^a   Sawiak, Stephen J ^c,d   Hurst, Jane A ^e   Joss, Shelagh K ^f   Holder, Susan E ^g   Morton, Jenny E V ^h   Turner, Claire ⁱ   Thevenon, Julien ^j   Mellul, Kelly ^k   Sánchez Andrade, Gabriela ^a   Ibarra Soria, Ximena ^a   Deriziotis, Pelagia ^b   Santos, Rui F ^l   Lee, Song Choon ^a,m   Faivre, Laurence ^j   Kleefstra, Tjitske ⁿ   Liu, Pentao ^a   Hurles, Mathew E ^a   Fisher, Simon E ^b,o   Logan, Darren W ^a   more..

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b MAX PLANCK INSTITUTE FOR PSYCHOLINGUISTICS   (Netherlands)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^d UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^e GREAT ORMOND STREET HOSPITAL   (United Kingdom)

^f QUEEN ELIZABETH UNIVERSITY HOSPITAL   (United Kingdom)

^g EALING HOSPITAL NHS TRUST   (United Kingdom)

^h BIRMINGHAM WOMEN S HOSPITAL   (United Kingdom)

ⁱ ROYAL DEVON AND EXETER HOSPITAL   (United Kingdom)

^j DIJON UNIVERSITY HOSPITAL   (France)

^k IMAGINE INSTITUTE   (France)

^l ROYAL MANCHESTER CHILDREN S HOSPITAL   (United Kingdom)

^m Singapore Science Centre   (Singapore)

ⁿ RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^o RADBOUD UNIVERSITY   (Netherlands)

more..

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR BCL11A; UNCLASSIFIED DRUG; BCL11A PROTEIN, HUMAN; CARRIER PROTEIN; NUCLEAR PROTEIN; STOP CODON; TRANSCRIPTOME;

ADULT; AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; BRAIN CORTEX; CLINICAL ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; DIMERIZATION; FEMALE; FRAMESHIFT MUTATION; GENE LOCATION; GENE LOCUS; GENETIC ASSOCIATION; HAPLOINSUFFICIENCY; HETEROZYGOSITY; HIPPOCAMPUS; HUMAN; HUMAN CELL; INTELLECTUAL IMPAIRMENT; LOSS OF FUNCTION MUTATION; MALE; MICROCEPHALY; MISSENSE MUTATION; MOUSE; NONHUMAN; NONSENSE MUTATION; PATHOGENESIS; PHENOTYPE; PRIORITY JOURNAL; SOCIAL BEHAVIOR; TRANSCRIPTION REGULATION; ANIMAL; CHEMISTRY; CHROMATIN ASSEMBLY AND DISASSEMBLY; GENETIC TRANSCRIPTION; GENETICS; MENTAL DISEASE; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; PSYCHOLOGY; STOP CODON; SYNDROME;

ANIMALS; CARRIER PROTEINS; CEREBRAL CORTEX; CHROMATIN ASSEMBLY AND DISASSEMBLY; CODON, NONSENSE; COGNITION DISORDERS; FRAMESHIFT MUTATION; HAPLOINSUFFICIENCY; HIPPOCAMPUS; HUMANS; INTELLECTUAL DISABILITY; MALE; MICE; MICROCEPHALY; MUTATION, MISSENSE; NEURODEVELOPMENTAL DISORDERS; NUCLEAR PROTEINS; PHENOTYPE; SOCIAL BEHAVIOR; SYNDROME; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TRANSCRIPTOME;

EID: 84994127960     PISSN: 00029297     EISSN: 15376605     Source Type: Journal    
DOI: 10.1016/j.ajhg.2016.05.030     Document Type: Article

References (89)

1. 1 Kochinke, K., Zweier, C., Nijhof, B., Fenckova, M., Cizek, P., Honti, F., Keerthikumar, S., Oortveld, M.A., Kleefstra, T., Kramer, J.M., et al. Systematic phenomics analysis deconvolutes genes mutated in intellectual disability into biologically coherent modules. Am. J. Hum. Genet. 98 (2016), 149–164.
2. 2 Vissers, L.E.L.M., Gilissen, C., Veltman, J.A., Genetic studies in intellectual disability and related disorders. Nat. Rev. Genet. 17 (2016), 9–18.
3. 3 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. 94 (2014), 677–694.
4. 4 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 19 (2014), 652–658.
5. 5 Hoyer, J., Ekici, A.B., Endele, S., Popp, B., Zweier, C., Wiesener, A., Wohlleber, E., Dufke, A., Rossier, E., Petsch, C., et al. Haploinsufficiency of ARID1B, a member of the SWI/SNF-a chromatin-remodeling complex, is a frequent cause of intellectual disability. Am. J. Hum. Genet. 90 (2012), 565–572.
6. 6 Deciphering Developmental Disorders Study. Large-scale discovery of novel genetic causes of developmental disorders. Nature 519 (2015), 223–228.
7. 7 Kadoch, C., Hargreaves, D.C., Hodges, C., Elias, L., Ho, L., Ranish, J., Crabtree, G.R., Proteomic and bioinformatic analysis of mammalian SWI/SNF complexes identifies extensive roles in human malignancy. Nat. Genet. 45 (2013), 592–601.
8. 8 Avram, D., Fields, A., Senawong, T., Topark-Ngarm, A., Leid, M., COUP-TF (chicken ovalbumin upstream promoter transcription factor)-interacting protein 1 (CTIP1) is a sequence-specific DNA binding protein. Biochem. J. 368 (2002), 555–563.
9. 9 Liu, P., Keller, J.R., Ortiz, M., Tessarollo, L., Rachel, R.A., Nakamura, T., Jenkins, N.A., Copeland, N.G., Bcl11a is essential for normal lymphoid development. Nat. Immunol. 4 (2003), 525–532.
10. 10 Satterwhite, E., Sonoki, T., Willis, T.G., Harder, L., Nowak, R., Arriola, E.L., Liu, H., Price, H.P., Gesk, S., Steinemann, D., et al. The BCL11 gene family: involvement of BCL11A in lymphoid malignancies. Blood 98 (2001), 3413–3420.
11. 11 Avram, D., Fields, A., Pretty On Top, K., Nevrivy, D.J., Ishmael, J.E., Leid, M., Isolation of a novel family of C(2)H(2) zinc finger proteins implicated in transcriptional repression mediated by chicken ovalbumin upstream promoter transcription factor (COUP-TF) orphan nuclear receptors. J. Biol. Chem. 275 (2000), 10315–10322.
12. 12 Khaled, W.T., Choon Lee, S., Stingl, J., Chen, X., Raza Ali, H., Rueda, O.M., Hadi, F., Wang, J., Yu, Y., Chin, S.-F., et al. BCL11A is a triple-negative breast cancer gene with critical functions in stem and progenitor cells. Nat. Commun., 6, 2015, 5987.
13. 13 Sankaran, V.G., Menne, T.F., Xu, J., Akie, T.E., Lettre, G., Van Handel, B., Mikkola, H.K.A., Hirschhorn, J.N., Cantor, A.B., Orkin, S.H., Human fetal hemoglobin expression is regulated by the developmental stage-specific repressor BCL11A. Science 322 (2008), 1839–1842.
14. 14 Kuo, T.-Y., Hong, C.-J., Hsueh, Y.-P., Bcl11A/CTIP1 regulates expression of DCC and MAP1b in control of axon branching and dendrite outgrowth. Mol. Cell. Neurosci. 42 (2009), 195–207.
15. 15 Kuo, T.-Y., Hsueh, Y.-P., Expression of zinc finger transcription factor Bcl11A/Evi9/CTIP1 in rat brain. J. Neurosci. Res. 85 (2007), 1628–1636.
16. 16 Wiegreffe, C., Simon, R., Peschkes, K., Kling, C., Strehle, M., Cheng, J., Srivatsa, S., Liu, P., Jenkins, N.A., Copeland, N.G., et al. Bcl11a (Ctip1) controls migration of cortical projection neurons through regulation of Sema3c. Neuron 87 (2015), 311–325.
17. 17 John, A., Brylka, H., Wiegreffe, C., Simon, R., Liu, P., Jüttner, R., Crenshaw, E.B. 3rd, Luyten, F.P., Jenkins, N.A., Copeland, N.G., et al. Bcl11a is required for neuronal morphogenesis and sensory circuit formation in dorsal spinal cord development. Development 139 (2012), 1831–1841.
18. 18 Peter, B., Matsushita, M., Oda, K., Raskind, W., De novo microdeletion of BCL11A is associated with severe speech sound disorder. Am. J. Med. Genet. A. 164A (2014), 2091–2096.
19. 19 Balci, T.B., Sawyer, S.L., Davila, J., Humphreys, P., Dyment, D.A., Brain malformations in a patient with deletion 2p16.1: A refinement of the phenotype to BCL11A. Eur. J. Med. Genet. 58 (2015), 351–354.
20. 20 De Rubeis, S., He, X., Goldberg, A.P., Poultney, C.S., Samocha, K., Cicek, A.E., Kou, Y., Liu, L., Fromer, M., Walker, S., et al. DDD Study Homozygosity Mapping Collaborative for Autism, UK10K Consortium. Synaptic, transcriptional and chromatin genes disrupted in autism. Nature 515 (2014), 209–215.
21. 21 Cánovas, J., Berndt, F.A., Sepúlveda, H., Aguilar, R., Veloso, F.A., Montecino, M., Oliva, C., Maass, J.C., Sierralta, J., Kukuljan, M., The specification of cortical subcerebral projection neurons depends on the direct repression of TBR1 by CTIP1/BCL11a. J. Neurosci. 35 (2015), 7552–7564.
22. 22 Funnell, A.P.W., Prontera, P., Ottaviani, V., Piccione, M., Giambona, A., Maggio, A., Ciaffoni, F., Stehling-Sun, S., Marra, M., Masiello, F., et al. 2p15-p16.1 microdeletions encompassing and proximal to BCL11A are associated with elevated HbF in addition to neurologic impairment. Blood 126 (2015), 89–93.
23. 23 Basak, A., Hancarova, M., Ulirsch, J.C., Balci, T.B., Trkova, M., Pelisek, M., Vlckova, M., Muzikova, K., Cermak, J., Trka, J., et al. BCL11A deletions result in fetal hemoglobin persistence and neurodevelopmental alterations. J. Clin. Invest. 125 (2015), 2363–2368.
24. 24 Henrichsen, C.N., Vinckenbosch, N., Zöllner, S., Chaignat, E., Pradervand, S., Schütz, F., Ruedi, M., Kaessmann, H., Reymond, A., Segmental copy number variation shapes tissue transcriptomes. Nat. Genet. 41 (2009), 424–429.
25. 25 de Ligt, J., Willemsen, M.H., van Bon, B.W.M., Kleefstra, T., Yntema, H.G., Kroes, T., Vulto-van Silfhout, A.T., Koolen, D.A., de Vries, P., Gilissen, C., et al. Diagnostic exome sequencing in persons with severe intellectual disability. N. Engl. J. Med. 367 (2012), 1921–1929.
26. 26 McLaren, W., Pritchard, B., Rios, D., Chen, Y., Flicek, P., Cunningham, F., Deriving the consequences of genomic variants with the Ensembl API and SNP Effect Predictor. Bioinformatics 26 (2010), 2069–2070.
27. 27 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 515 (2014), 216–221.
28. 28 Gilissen, C., Hehir-Kwa, J.Y., Thung, D.T., van de Vorst, M., van Bon, B.W.M., Willemsen, M.H., Kwint, M., Janssen, I.M., Hoischen, A., Schenck, A., et al. Genome sequencing identifies major causes of severe intellectual disability. Nature 511 (2014), 344–347.
29. 29 Fromer, M., Pocklington, A.J., Kavanagh, D.H., Williams, H.J., Dwyer, S., Gormley, P., Georgieva, L., Rees, E., Palta, P., Ruderfer, D.M., et al. De novo mutations in schizophrenia implicate synaptic networks. Nature 506 (2014), 179–184.
30. 30 Appenzeller, S., Balling, R., Barisic, N., Baulac, S., Caglayan, H., Craiu, D., De Jonghe, P., Depienne, C., Dimova, P., Djémié, T., et al. EuroEPINOMICS-RES Consortium Epilepsy Phenome/Genome Project, Epi4K Consortium. De novo mutations in synaptic transmission genes including DNM1 cause epileptic encephalopathies. Am. J. Hum. Genet. 95 (2014), 360–370.
31. 31 Zaidi, S., Choi, M., Wakimoto, H., Ma, L., Jiang, J., Overton, J.D., Romano-Adesman, A., Bjornson, R.D., Breitbart, R.E., Brown, K.K., et al. De novo mutations in histone-modifying genes in congenital heart disease. Nature 498 (2013), 220–223.
32. 32 Allen, A.S., Berkovic, S.F., Cossette, P., Delanty, N., Dlugos, D., Eichler, E.E., Epstein, M.P., Glauser, T., Goldstein, D.B., Han, Y., et al. Epi4K Consortium, Epilepsy Phenome/Genome Project. De novo mutations in epileptic encephalopathies. Nature 501 (2013), 217–221.
33. 33 Sanders, S.J., Murtha, M.T., Gupta, A.R., Murdoch, J.D., Raubeson, M.J., Willsey, A.J., Ercan-Sencicek, A.G., DiLullo, N.M., Parikshak, N.N., Stein, J.L., et al. De novo mutations revealed by whole-exome sequencing are strongly associated with autism. Nature 485 (2012), 237–241.
34. 34 Rauch, A., Wieczorek, D., Graf, E., Wieland, T., Endele, S., Schwarzmayr, T., Albrecht, B., Bartholdi, D., Beygo, J., Di Donato, N., et al. Range of genetic mutations associated with severe non-syndromic sporadic intellectual disability: an exome sequencing study. Lancet 380 (2012), 1674–1682.
35. 35 O'Roak, B.J., Vives, L., Girirajan, S., Karakoc, E., Krumm, N., Coe, B.P., Levy, R., Ko, A., Lee, C., Smith, J.D., et al. Sporadic autism exomes reveal a highly interconnected protein network of de novo mutations. Nature 485 (2012), 246–250.
36. 36 Iossifov, I., Ronemus, M., Levy, D., Wang, Z., Hakker, I., Rosenbaum, J., Yamrom, B., Lee, Y.H., Narzisi, G., Leotta, A., et al. De novo gene disruptions in children on the autistic spectrum. Neuron 74 (2012), 285–299.
37. 37 Akawi, N., McRae, J., Ansari, M., Balasubramanian, M., Blyth, M., Brady, A.F., Clayton, S., Cole, T., Deshpande, C., Fitzgerald, T.W., et al., DDD study. Discovery of four recessive developmental disorders using probabilistic genotype and phenotype matching among 4,125 families. Nat. Genet. 47 (2015), 1363–1369.
38. 38 Samocha, K.E., Robinson, E.B., Sanders, S.J., Stevens, C., Sabo, A., McGrath, L.M., Kosmicki, J.A., Rehnström, K., Mallick, S., Kirby, A., et al. A framework for the interpretation of de novo mutation in human disease. Nat. Genet. 46 (2014), 944–950.
39. 39 Deriziotis, P., O'Roak, B.J., Graham, S.A., Estruch, S.B., Dimitropoulou, D., Bernier, R.A., Gerdts, J., Shendure, J., Eichler, E.E., Fisher, S.E., De novo TBR1 mutations in sporadic autism disrupt protein functions. Nat. Commun., 5, 2014, 4954.
40. 40 Deriziotis, P., Graham, S.A., Estruch, S.B., Fisher, S.E., Investigating protein-protein interactions in live cells using bioluminescence resonance energy transfer. J. Vis. Exp., 87, 2014, e51438.
41. 41 Lee, S.-C., Liu, P., Construction of gene-targeting vectors by recombineering. Cold Spring Harb. Protoc., 2009, 2009, t5291.
42. 42 Yu, Y., Wang, J., Khaled, W., Burke, S., Li, P., Chen, X., Yang, W., Jenkins, N.A., Copeland, N.G., Zhang, S., Liu, P., Bcl11a is essential for lymphoid development and negatively regulates p53. J. Exp. Med. 209 (2012), 2467–2483.
43. 43 Sawiak, S.J., Wood, N.I., Williams, G.B., Morton, A.J., Carpenter, T.A., Voxel-based morphometry with templates and validation in a mouse model of Huntington's disease. Magn. Reson. Imaging 31 (2013), 1522–1531.
44. 44 Ashburner, J., A fast diffeomorphic image registration algorithm. Neuroimage 38 (2007), 95–113.
45. 45 deCarlos, F., Alvarez-Suárez, A., Costilla, S., Noval, I., Vega, J.A., Cobo, J., 3D-μCT Cephalometric Measurements in Mice. Saba, D.L., (eds.) Computed Tomography - Special Applications, 2011, InTech.
46. 46 McIntyre, R.E., Lakshminarasimhan Chavali, P., Ismail, O., Carragher, D.M., Sanchez-Andrade, G., Forment, J.V., Fu, B., Del Castillo Velasco-Herrera, M., Edwards, A., van der Weyden, L., et al., Sanger Mouse Genetics Project. Disruption of mouse Cenpj, a regulator of centriole biogenesis, phenocopies Seckel syndrome. PLoS Genet., 8, 2012, e1003022.
47. 47 Yang, M., Silverman, J.L., Crawley, J.N., Automated three-chambered social approach task for mice. Curr. Protoc. Neurosci., 8, 2001, 8.26.
48. 48 Dobin, A., Davis, C.A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M., Gingeras, T.R., STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29 (2013), 15–21.
49. 49 Love, M.I., Huber, W., Anders, S., Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol., 15, 2014, 550.
50. 50 Backes, C., Keller, A., Kuentzer, J., Kneissl, B., Comtesse, N., Elnakady, Y.A., Müller, R., Meese, E., Lenhof, H.-P., GeneTrail—advanced gene set enrichment analysis. Nucleic Acids Res. 35 (2007), W186–W192.
51. 51 Pawson, A.J., Sharman, J.L., Benson, H.E., Faccenda, E., Alexander, S.P.H., Buneman, O.P., Davenport, A.P., McGrath, J.C., Peters, J.A., Southan, C., et al., NC-IUPHAR. The IUPHAR/BPS Guide to PHARMACOLOGY: an expert-driven knowledgebase of drug targets and their ligands. Nucleic Acids Res. 42 (2014), D1098–D1106.
52. 52 Basu, S.N., Kollu, R., Banerjee-Basu, S., AutDB: a gene reference resource for autism research. Nucleic Acids Res. 37 (2009), D832–D836.
53. 53 Cunningham, F., Amode, M.R., Barrell, D., Beal, K., Billis, K., Brent, S., Carvalho-Silva, D., Clapham, P., Coates, G., Fitzgerald, S., et al. Ensembl 2015. Nucleic Acids Res. 43 (2015), D662–D669.
54. 54 Trapnell, C., Williams, B.A., Pertea, G., Mortazavi, A., Kwan, G., van Baren, M.J., Salzberg, S.L., Wold, B.J., Pachter, L., Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat. Biotechnol. 28 (2010), 511–515.
55. 55 Yuan, H., Meng, Z., Zhang, L., Luo, X., Liu, L., Chen, M., Li, X., Zhao, W., Liang, L., A rare de novo interstitial duplication of 15q15.3q21.2 in a boy with severe short stature, hypogonadism, global developmental delay and intellectual disability. Mol. Cytogenet., 9, 2016, 2.
56. 56 Liu, H., Ippolito, G.C., Wall, J.K., Niu, T., Probst, L., Lee, B.-S., Pulford, K., Banham, A.H., Stockwin, L., Shaffer, A.L., et al. Functional studies of BCL11A: characterization of the conserved BCL11A-XL splice variant and its interaction with BCL6 in nuclear paraspeckles of germinal center B cells. Mol. Cancer, 5, 2006, 18.
57. 57 Cismasiu, V.B., Adamo, K., Gecewicz, J., Duque, J., Lin, Q., Avram, D., BCL11B functionally associates with the NuRD complex in T lymphocytes to repress targeted promoter. Oncogene 24 (2005), 6753–6764.
58. 58 Nakamura, T., Yamazaki, Y., Saiki, Y., Moriyama, M., Largaespada, D.A., Jenkins, N.A., Copeland, N.G., Evi9 encodes a novel zinc finger protein that physically interacts with BCL6, a known human B-cell proto-oncogene product. Mol. Cell. Biol. 20 (2000), 3178–3186.
59. 59 Mircsof, D., Langouët, M., Rio, M., Moutton, S., Siquier-Pernet, K., Bole-Feysot, C., Cagnard, N., Nitschke, P., Gaspar, L., Žnidarič, M., et al., DDD Study. Mutations in NONO lead to syndromic intellectual disability and inhibitory synaptic defects. Nat. Neurosci. 18 (2015), 1731–1736.
60. 60 Kogan, J.H., Frankland, P.W., Silva, A.J., Long-term memory underlying hippocampus-dependent social recognition in mice. Hippocampus 10 (2000), 47–56.
61. 61 Silverman, J.L., Yang, M., Lord, C., Crawley, J.N., Behavioural phenotyping assays for mouse models of autism. Nat. Rev. Neurosci. 11 (2010), 490–502.
62. 62 Srivastava, A.K., Schwartz, C.E., Intellectual disability and autism spectrum disorders: causal genes and molecular mechanisms. Neurosci. Biobehav. Rev. 46 (2014), 161–174.
63. 63 Vogel-Ciernia, A., Matheos, D.P., Barrett, R.M., Kramár, E.A., Azzawi, S., Chen, Y., Magnan, C.N., Zeller, M., Sylvain, A., Haettig, J., et al. The neuron-specific chromatin regulatory subunit BAF53b is necessary for synaptic plasticity and memory. Nat. Neurosci. 16 (2013), 552–561.
64. 64 Pasterkamp, R.J., Getting neural circuits into shape with semaphorins. Nat. Rev. Neurosci. 13 (2012), 605–618.
65. 65 Bagheri, H., Badduke, C., Qiao, Y., Colnaghi, R., Abramowicz, I., Alcantara, D., Dunham, C., Wen, J., Wildin, R.S., Nowaczyk, M.J.M., et al. Identifying candidate genes for 2p15p16.1 microdeletion syndrome using clinical, genomic, and functional analysis. JCI Insight, 1, 2016, e85461.
66. 66 de Leeuw, N., Pfundt, R., Koolen, D.A., Neefs, I., Scheltinga, I., Mieloo, H., Sistermans, E.A., Nillesen, W., Smeets, D.F., de Vries, B.B.A., Knoers, N.V., A newly recognised microdeletion syndrome involving 2p15p16.1: narrowing down the critical region by adding another patient detected by genome wide tiling path array comparative genomic hybridisation analysis. J. Med. Genet. 45 (2008), 122–124.
67. 67 Hucthagowder, V., Liu, T.-C., Paciorkowski, A.R., Thio, L.L., Keller, M.S., Anderson, C.D., Herman, T., Dehner, L.P., Grange, D.K., Kulkarni, S., Chromosome 2p15p16.1 microdeletion syndrome: 2.5 Mb deletion in a patient with renal anomalies, intractable seizures and a choledochal cyst. Eur. J. Med. Genet. 55 (2012), 485–489.
68. 68 Piccione, M., Piro, E., Serraino, F., Cavani, S., Ciccone, R., Malacarne, M., Pierluigi, M., Vitaloni, M., Zuffardi, O., Corsello, G., Interstitial deletion of chromosome 2p15-16.1: report of two patients and critical review of current genotype-phenotype correlation. Eur. J. Med. Genet. 55 (2012), 238–244.
69. 69 Rajcan-Separovic, E., Harvard, C., Liu, X., McGillivray, B., Hall, J.G., Qiao, Y., Hurlburt, J., Hildebrand, J., Mickelson, E.C.R., Holden, J.J.A., Lewis, M.E., Clinical and molecular cytogenetic characterisation of a newly recognised microdeletion syndrome involving 2p15-16.1. J. Med. Genet. 44 (2007), 269–276.
70. 70 Jorgez, C.J., Rosenfeld, J.A., Wilken, N.R., Vangapandu, H.V., Sahin, A., Pham, D., Carvalho, C.M.B., Bandholz, A., Miller, A., Weaver, D.D., et al. Genitourinary defects associated with genomic deletions in 2p15 encompassing OTX1. PLoS ONE, 9, 2014, e107028.
71. 71 Florisson, J.M.G., Mathijssen, I.M.J., Dumee, B., Hoogeboom, J.A.M., Poddighe, P.J., Oostra, B.A., Frijns, J.P., Koster, L., de Klein, A., Eussen, B., et al. Complex craniosynostosis is associated with the 2p15p16.1 microdeletion syndrome. Am. J. Med. Genet. A. 161A (2013), 244–253.
72. 72 Hancarova, M., Simandlova, M., Drabova, J., Mannik, K., Kurg, A., Sedlacek, Z., A patient with de novo 0.45 Mb deletion of 2p16.1: the role of BCL11A, PAPOLG, REL, and FLJ16341 in the 2p15-p16.1 microdeletion syndrome. Am. J. Med. Genet. A. 161A (2013), 865–870.
73. 73 Félix, T.M., Petrin, A.L., Sanseverino, M.T.V., Murray, J.C., Further characterization of microdeletion syndrome involving 2p15-p16.1. Am. J. Med. Genet. A. 152A (2010), 2604–2608.
74. 74 Son, E.Y., Crabtree, G.R., The role of BAF (mSWI/SNF) complexes in mammalian neural development. Am. J. Med. Genet. C. Semin. Med. Genet. 166C (2014), 333–349.
75. 75 Alajem, A., Biran, A., Harikumar, A., Sailaja, B.S., Aaronson, Y., Livyatan, I., Nissim-Rafinia, M., Sommer, A.G., Mostoslavsky, G., Gerbasi, V.R., et al. Differential association of chromatin proteins identifies BAF60a/SMARCD1 as a regulator of embryonic stem cell differentiation. Cell Rep. 10 (2015), 2019–2031.
76. 76 Yoo, A.S., Staahl, B.T., Chen, L., Crabtree, G.R., MicroRNA-mediated switching of chromatin-remodelling complexes in neural development. Nature 460 (2009), 642–646.
77. 77 Van Battum, E.Y., Brignani, S., Pasterkamp, R.J., Axon guidance proteins in neurological disorders. Lancet Neurol. 14 (2015), 532–546.
78. 78 Sakurai, A., Doçi, C.L., Gutkind, J.S., Semaphorin signaling in angiogenesis, lymphangiogenesis and cancer. Cell Res. 22 (2012), 23–32.
79. 79 Wolman, M.A., Regnery, A.M., Becker, T., Becker, C.G., Halloran, M.C., Semaphorin3D regulates axon axon interactions by modulating levels of L1 cell adhesion molecule. J. Neurosci. 27 (2007), 9653–9663.
80. 80 Aghajanian, H., Choi, C., Ho, V.C., Gupta, M., Singh, M.K., Epstein, J.A., Semaphorin 3d and semaphorin 3e direct endothelial motility through distinct molecular signaling pathways. J. Biol. Chem. 289 (2014), 17971–17979.
81. 81 Chauvet, S., Cohen, S., Yoshida, Y., Fekrane, L., Livet, J., Gayet, O., Segu, L., Buhot, M.-C., Jessell, T.M., Henderson, C.E., Mann, F., Gating of Sema3E/PlexinD1 signaling by neuropilin-1 switches axonal repulsion to attraction during brain development. Neuron 56 (2007), 807–822.
82. 82 Wang, F., Eagleson, K.L., Levitt, P., Positive regulation of neocortical synapse formation by the Plexin-D1 receptor. Brain Res. 1616 (2015), 157–165.
83. 83 Bribián, A., Nocentini, S., Llorens, F., Gil, V., Mire, E., Reginensi, D., Yoshida, Y., Mann, F., del Río, J.A., Sema3E/PlexinD1 regulates the migration of hem-derived Cajal-Retzius cells in developing cerebral cortex. Nat. Commun., 5, 2014, 4265.
84. 84 Blockus, H., Chédotal, A., The multifaceted roles of Slits and Robos in cortical circuits: from proliferation to axon guidance and neurological diseases. Curr. Opin. Neurobiol. 27 (2014), 82–88.
85. 85 Barber, M., Di Meglio, T., Andrews, W.D., Hernández-Miranda, L.R., Murakami, F., Chédotal, A., Parnavelas, J.G., The role of Robo3 in the development of cortical interneurons. Cereb. Cortex 19:Suppl 1 (2009), i22–i31.
86. 86 Hernández-Miranda, L.R., Cariboni, A., Faux, C., Ruhrberg, C., Cho, J.H., Cloutier, J.-F., Eickholt, B.J., Parnavelas, J.G., Andrews, W.D., Robo1 regulates semaphorin signaling to guide the migration of cortical interneurons through the ventral forebrain. J. Neurosci. 31 (2011), 6174–6187.
87. 87 Graham, S.A., Fisher, S.E., Understanding language from a genomic perspective. Annu. Rev. Genet. 49 (2015), 131–160.
88. 88 Xu, J., Peng, C., Sankaran, V.G., Shao, Z., Esrick, E.B., Chong, B.G., Ippolito, G.C., Fujiwara, Y., Ebert, B.L., Tucker, P.W., Orkin, S.H., Correction of sickle cell disease in adult mice by interference with fetal hemoglobin silencing. Science 334 (2011), 993–996.
89. 89 Firth, H.V., Wright, C.F., DDD Study. The Deciphering Developmental Disorders (DDD) study. Dev. Med. Child Neurol. 53 (2011), 702–703.