Gain-of-Function Mutations in ZIC1 Are Associated with Coronal Craniosynostosis and Learning Disability

American Journal of Human Genetics

Volumn 97, Issue 3, 2015, Pages 378-388

  Twigg, Stephen R F ^a   Forecki, Jennifer ^b   Goos, Jacqueline A C ^c   Richardson, Ivy C A ^d   Hoogeboom, A Jeannette M ^c   Van Den Ouweland, Ans M W ^c   Swagemakers, Sigrid M A ^c   Lequin, Maarten H ^c   Van antwerp, Daniel ^b   McGowan, Simon J ^a   Westbury, Isabelle ^a   Miller, Kerry A ^a   Wall, Steven A ^e   Van Der Spek, Peter J ^c   Mathijssen, Irene M J ^c   Pauws, Erwin ^d   Merzdorf, Christa S ^b   Wilkie, Andrew O M ^a,e  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b MONTANA STATE UNIVERSITY   (United States)

^c ERASMUS MEDICAL CENTER   (Netherlands)

^d UNIVERSITY COLLEGE LONDON   (United Kingdom)

^e JOHN RADCLIFFE HOSPITAL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADOLESCENT; ADULT; ANIMAL TISSUE; ARTICLE; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; CRANIAL SUTURE; CRANIOFACIAL SYNOSTOSIS; EMBRYO; ENGRAILED 1 GENE; ENGRAILED 2 GENE; EXOME; EXON; FAMILY; GAIN OF FUNCTION MUTATION; GENE; GENE EXPRESSION; GENETIC ASSOCIATION; GENETIC SCREENING; HETEROZYGOTE; HUMAN; HUMAN TISSUE; INFANT; LEARNING DISORDER; MALE; MISSENSE MUTATION; MOUSE; MOUSE EMBRYO; MUTATIONAL ANALYSIS; NONHUMAN; NONSENSE MEDIATED MRNA DECAY; NONSENSE MUTATION; PHENOTYPE; PRIORITY JOURNAL; SCHOOL CHILD; SINGLE NUCLEOTIDE POLYMORPHISM; XENOPUS; YOUNG ADULT; ZINC FINGER PROTEIN OF CEREBELLUM 1 GENE; ANIMAL; CASE REPORT; DNA SEQUENCE; FEMALE; GENE EXPRESSION REGULATION; GENETICS; IN SITU HYBRIDIZATION; KARYOTYPING; METABOLISM; MOLECULAR CLONING; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PEDIGREE; STOP CODON; XENOPUS LAEVIS;

ENGRAILED 2 PROTEIN; HOMEODOMAIN PROTEIN; NERVE PROTEIN; STOP CODON; TRANSCRIPTION FACTOR; ZIC1 PROTEIN, HUMAN;

ANIMALS; BASE SEQUENCE; CLONING, MOLECULAR; CODON, NONSENSE; CRANIOSYNOSTOSES; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; HUMANS; IN SITU HYBRIDIZATION; KARYOTYPING; LEARNING DISORDERS; MALE; MICE; MOLECULAR SEQUENCE DATA; MUTATION, MISSENSE; NERVE TISSUE PROTEINS; PEDIGREE; PHENOTYPE; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION FACTORS; XENOPUS LAEVIS;

EID: 84940973303     PISSN: 00029297     EISSN: 15376605     Source Type: Journal    
DOI: 10.1016/j.ajhg.2015.07.007     Document Type: Article

References (51)

1. A.O.M. Wilkie, J.C. Byren, J.A. Hurst, J. Jayamohan, D. Johnson, S.J.L. Knight, T. Lester, P.G. Richards, S.R.F. Twigg, and S.A. Wall Prevalence and complications of single-gene and chromosomal disorders in craniosynostosis Pediatrics 126 2010 e391 e400
2. E. Lajeunie, M. Le Merrer, C. Bonaïti-Pellie, D. Marchac, and D. Renier Genetic study of nonsyndromic coronal craniosynostosis Am. J. Med. Genet. 55 1995 500 504
3. D. Johnson, and A.O.M. Wilkie Craniosynostosis Eur. J. Hum. Genet. 19 2011 369 376
4. V.P. Sharma, A.L. Fenwick, M.S. Brockop, S.J. McGowan, J.A. Goos, A.J. Hoogeboom, A.F. Brady, N.O. Jeelani, S.A. Lynch, J.B. Mulliken, et al. 500 Whole-Genome Sequences (WGS500) Consortium Mutations in TCF12, encoding a basic helix-loop-helix partner of TWIST1, are a frequent cause of coronal craniosynostosis Nat. Genet. 45 2013 304 307
5. X. Jiang, S. Iseki, R.E. Maxson, H.M. Sucov, and G.M. Morriss-Kay Tissue origins and interactions in the mammalian skull vault Dev. Biol. 241 2002 106 116
6. T. Yoshida, P. Vivatbutsiri, G. Morriss-Kay, Y. Saga, and S. Iseki Cell lineage in mammalian craniofacial mesenchyme Mech. Dev. 125 2008 797 808
7. S.R.F. Twigg, and A.O.M. Wilkie A genetic-pathophysiological framework for craniosynostosis Am. J. Hum. Genet. 97 2015 359 377 this issue
8. A.E. Merrill, E.G. Bochukova, S.M. Brugger, M. Ishii, D.T. Pilz, S.A. Wall, K.M. Lyons, A.O.M. Wilkie, and R.E. Maxson Jr. Cell mixing at a neural crest-mesoderm boundary and deficient ephrin-Eph signaling in the pathogenesis of craniosynostosis Hum. Mol. Genet. 15 2006 1319 1328
9. M.K. Hajihosseini, R. Duarte, J. Pegrum, A. Donjacour, E. Lana-Elola, D.P. Rice, J. Sharpe, and C. Dickson Evidence that Fgf10 contributes to the skeletal and visceral defects of an Apert syndrome mouse model Dev. Dyn. 238 2009 376 385
10. G. Holmes, G. Rothschild, U.B. Roy, C.X. Deng, A. Mansukhani, and C. Basilico Early onset of craniosynostosis in an Apert mouse model reveals critical features of this pathology Dev. Biol. 328 2009 273 284
11. R.A. Deckelbaum, G. Holmes, Z. Zhao, C. Tong, C. Basilico, and C.A. Loomis Regulation of cranial morphogenesis and cell fate at the neural crest-mesoderm boundary by engrailed 1 Development 139 2012 1346 1358
12. M.C. Ting, N.L. Wu, P.G. Roybal, J. Sun, L. Liu, Y. Yen, and R.E. Maxson Jr. EphA4 as an effector of Twist1 in the guidance of osteogenic precursor cells during calvarial bone growth and in craniosynostosis Development 136 2009 855 864
13. R.A. Deckelbaum, A. Majithia, T. Booker, J.E. Henderson, and C.A. Loomis The homeoprotein engrailed 1 has pleiotropic functions in calvarial intramembranous bone formation and remodeling Development 133 2006 63 74
14. R.G. Ali, H.M. Bellchambers, and R.M. Arkell Zinc fingers of the cerebellum (Zic): transcription factors and co-factors Int. J. Biochem. Cell Biol. 44 2012 2065 2068
15. M.J. Benedyk, J.R. Mullen, and S. DiNardo odd-paired: a zinc finger pair-rule protein required for the timely activation of engrailed and wingless in Drosophila embryos Genes Dev. 8 1994 105 117
16. J. Aruga, A. Kamiya, H. Takahashi, T.J. Fujimi, Y. Shimizu, K. Ohkawa, S. Yazawa, Y. Umesono, H. Noguchi, T. Shimizu, and et al. A wide-range phylogenetic analysis of Zic proteins: implications for correlations between protein structure conservation and body plan complexity Genomics 87 2006 783 792
17. C.S. Merzdorf Emerging roles for zic genes in early development Dev. Dyn. 236 2007 922 940
18. I. Grinberg, H. Northrup, H. Ardinger, C. Prasad, W.B. Dobyns, and K.J. Millen Heterozygous deletion of the linked genes ZIC1 and ZIC4 is involved in Dandy-Walker malformation Nat. Genet. 36 2004 1053 1055
19. J. Aruga, O. Minowa, H. Yaginuma, J. Kuno, T. Nagai, T. Noda, and K. Mikoshiba Mouse Zic1 is involved in cerebellar development J. Neurosci. 18 1998 284 293
20. M.C. Blank, I. Grinberg, E. Aryee, C. Laliberte, V.V. Chizhikov, R.M. Henkelman, and K.J. Millen Multiple developmental programs are altered by loss of Zic1 and Zic4 to cause Dandy-Walker malformation cerebellar pathogenesis Development 138 2011 1207 1216
21. K.A. Eley, D. Johnson, A.O.M. Wilkie, J. Jayamohan, P. Richards, and S.A. Wall Raised intracranial pressure is frequent in untreated nonsyndromic unicoronal synostosis and does not correlate with severity of phenotypic features Plast. Reconstr. Surg. 130 2012 690e 697e
22. J.C. Taylor, H.C. Martin, S. Lise, J. Broxholme, J.-B. Cazier, A. Rimmer, A. Kanapin, G. Lunter, S. Fiddy, C. Allan, and et al. Factors influencing success of clinical genome sequencing across a broad spectrum of disorders Nat. Genet. 47 2015 717 726
23. A. Rimmer, H. Phan, I. Mathieson, Z. Iqbal, S.R.F. Twigg, A.O.M. Wilkie, G. McVean, G. Lunter WGS500 Consortium Integrating mapping-, assembly- and haplotype-based approaches for calling variants in clinical sequencing applications Nat. Genet. 46 2014 912 918
24. G. Lunter, and M. Goodson Stampy: a statistical algorithm for sensitive and fast mapping of Illumina sequence reads Genome Res. 21 2011 936 939
25. R. Drmanac, A.B. Sparks, M.J. Callow, A.L. Halpern, N.L. Burns, B.G. Kermani, P. Carnevali, I. Nazarenko, G.B. Nilsen, G. Yeung, and et al. Human genome sequencing using unchained base reads on self-assembling DNA nanoarrays Science 327 2010 78 81
26. P. Carnevali, J. Baccash, A.L. Halpern, I. Nazarenko, G.B. Nilsen, K.P. Pant, J.C. Ebert, A. Brownley, M. Morenzoni, V. Karpinchyk, and et al. Computational techniques for human genome resequencing using mated gapped reads J. Comput. Biol. 19 2012 279 292
27. C.S. Merzdorf, and H.L. Sive The zic1 gene is an activator of Wnt signaling Int. J. Dev. Biol. 50 2006 611 617
28. H.L. Sive, K. Hattori, and H. Weintraub Progressive determination during formation of the anteroposterior axis in Xenopus laevis Cell 58 1989 171 180
29. P.D. Nieuwkoop, and J. Faber Normal Table of Xenopus laevis (daudin) 1967 North-Holland Publishing Co Amsterdam
30. P.J. Kolm, and H.L. Sive Regulation of the Xenopus labial homeodomain genes, HoxA1 and HoxD1: activation by retinoids and peptide growth factors Dev. Biol. 167 1995 34 49
31. R.M. Harland In situ hybridization: an improved whole-mount method for Xenopus embryos Methods Cell Biol. 36 1991 685 695
32. A.H. Brivanlou, and R.M. Harland Expression of an engrailed-related protein is induced in the anterior neural ectoderm of early Xenopus embryos Development 106 1989 611 617
33. D.G. Wilkinson In situ Hybridization: A Practical Approach 1998 Oxford University Press Oxford, New York
34. C. Gaston-Massuet, D.J. Henderson, N.D. Greene, and A.J. Copp Zic4, a zinc-finger transcription factor, is expressed in the developing mouse nervous system Dev. Dyn. 233 2005 1110 1115
35. W. Wurst, A.B. Auerbach, and A.L. Joyner Multiple developmental defects in Engrailed-1 mutant mice: an early mid-hindbrain deletion and patterning defects in forelimbs and sternum Development 120 1994 2065 2075
36. A. Ferraris, L. Bernardini, V. Sabolic Avramovska, G. Zanni, S. Loddo, E. Sukarova-Angelovska, V. Parisi, A. Capalbo, S. Tumini, L. Travaglini, et al. Italian CBCD Study Group Dandy-Walker malformation and Wisconsin syndrome: novel cases add further insight into the genotype-phenotype correlations of 3q23q25 deletions Orphanet J. Rare Dis. 8 2013 75
37. M. Khajavi, K. Inoue, and J.R. Lupski Nonsense-mediated mRNA decay modulates clinical outcome of genetic disease Eur. J. Hum. Genet. 14 2006 1074 1081
38. J.S. Kuo, M. Patel, J. Gamse, C. Merzdorf, X. Liu, V. Apekin, and H. Sive Opl: a zinc finger protein that regulates neural determination and patterning in Xenopus Development 125 1998 2867 2882
39. S. Li, Y. Shin, K.W. Cho, and C.S. Merzdorf The Xfeb gene is directly upregulated by Zic1 during early neural development Dev. Dyn. 235 2006 2817 2827
40. C. Milet, F. Maczkowiak, D.D. Roche, and A.H. Monsoro-Burq Pax3 and Zic1 drive induction and differentiation of multipotent, migratory, and functional neural crest in Xenopus embryos Proc. Natl. Acad. Sci. USA 110 2013 5528 5533
41. T. Nagai, J. Aruga, S. Takada, T. Günther, R. Spörle, K. Schughart, and K. Mikoshiba The expression of the mouse Zic1, Zic2, and Zic3 gene suggests an essential role for Zic genes in body pattern formation Dev. Biol. 182 1997 299 313
42. S.A. Brown, D. Warburton, L.Y. Brown, C.Y. Yu, E.R. Roeder, S. Stengel-Rutkowski, R.C.M. Hennekam, and M. Muenke Holoprosencephaly due to mutations in ZIC2, a homologue of Drosophila odd-paired Nat. Genet. 20 1998 180 183
43. M. Gebbia, G.B. Ferrero, G. Pilia, M.T. Bassi, A. Aylsworth, M. Penman-Splitt, L.M. Bird, J.S. Bamforth, J. Burn, D. Schlessinger, and et al. X-linked situs abnormalities result from mutations in ZIC3 Nat. Genet. 17 1997 305 308
44. J. Aruga, K. Mizugishi, H. Koseki, K. Imai, R. Balling, T. Noda, and K. Mikoshiba Zic1 regulates the patterning of vertebral arches in cooperation with Gli3 Mech. Dev. 89 1999 141 150
45. S.R. Braddock, K.L. Jones, D.W. Superneau, and M.C. Jones Sagittal craniosynostosis, Dandy-Walker malformation, and hydrocephalus: a unique multiple malformation syndrome Am. J. Med. Genet. 47 1993 640 643 discussion 644
46. S. DiNardo, and P.H. O'Farrell Establishment and refinement of segmental pattern in the Drosophila embryo: spatial control of engrailed expression by pair-rule genes Genes Dev. 1 1987 1212 1225
47. J.L. Plouhinec, D.D. Roche, C. Pegoraro, A.L. Figueiredo, F. Maczkowiak, L.J. Brunet, C. Milet, J.P. Vert, N. Pollet, R.M. Harland, and A.H. Monsoro-Burq Pax3 and Zic1 trigger the early neural crest gene regulatory network by the direct activation of multiple key neural crest specifiers Dev. Biol. 386 2014 461 472
48. H. Chen, D. Ovchinnikov, C.L. Pressman, A. Aulehla, Y. Lun, and R.L. Johnson Multiple calvarial defects in lmx1b mutant mice Dev. Genet. 22 1998 314 320
49. S.D. Dreyer, G. Zhou, A. Baldini, A. Winterpacht, B. Zabel, W. Cole, R.L. Johnson, and B. Lee Mutations in LMX1B cause abnormal skeletal patterning and renal dysplasia in nail patella syndrome Nat. Genet. 19 1998 47 50
50. L. Brown, M. Paraso, R. Arkell, and S. Brown In vitro analysis of partial loss-of-function ZIC2 mutations in holoprosencephaly: alanine tract expansion modulates DNA binding and transactivation Hum. Mol. Genet. 14 2005 411 420
51. J. Cowan, M. Tariq, and S.M. Ware Genetic and functional analyses of ZIC3 variants in congenital heart disease Hum. Mutat. 35 2014 66 75