Mutations in CDC45, Encoding an Essential Component of the Pre-initiation Complex, Cause Meier-Gorlin Syndrome and Craniosynostosis

American Journal of Human Genetics

Volumn 99, Issue 1, 2016, Pages 125-138

  Fenwick, Aimee L ^a   Kliszczak, Maciej ^a   Cooper, Fay ^b   Murray, Jennie ^b   Sanchez Pulido, Luis ^b   Twigg, Stephen R F ^a   Goriely, Anne ^a   McGowan, Simon J ^a   Miller, Kerry A ^a   Taylor, Indira B ^a   Logan, Clare ^b   Bozdogan, Sevcan ^c   Danda, Sumita ^d   Dixon, Joanne ^e   Elsayed, Solaf M ^f   Elsobky, Ezzat ^f   Gardham, Alice ^g   Hoffer, Mariette J V ^h   Koopmans, Marije ^h   McDonald McGinn, Donna M ⁱ   Santen, Gijs W E ^h   Savarirayan, Ravi ^j   de Silva, Deepthi ^k   Vanakker, Olivier ^l   Wall, Steven A ^m   Wilson, Louise C ^g   Yuregir, Ozge Ozalp ⁿ   Zackai, Elaine H ⁱ   Ponting, Chris P ^b   Jackson, Andrew P ^b   Wilkie, Andrew O M ^a,m   Niedzwiedz, Wojciech ^a   Bicknell, Louise S ^b,o   more..

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c MERSIN UNIVERSITY   (Turkey)

^d CHRISTIAN MEDICAL COLLEGE   (India)

^e CHRISTCHURCH HOSPITAL   (New Zealand)

^f Ain Shams University   (Egypt)

^g GREAT ORMOND STREET HOSPITAL   (United Kingdom)

^h LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

ⁱ CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^j UNIVERSITY OF MELBOURNE   (Australia)

^k UNIVERSITY OF KELANIYA   (Sri Lanka)

^l GHENT UNIVERSITY HOSPITAL   (Belgium)

^m JOHN RADCLIFFE HOSPITAL   (United Kingdom)

ⁿ Numune Training and Research Hospital   (Turkey)

^o UNIVERSITY OF OTAGO   (New Zealand)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ORIGIN RECOGNITION COMPLEX; CDC45 PROTEIN, HUMAN; CELL CYCLE PROTEIN;

ADOLESCENT; ADULT; ALLELE; AMINO ACID SUBSTITUTION; ARTICLE; CDC45 GENE; CELL CYCLE S PHASE; CELL PROLIFERATION; CHILD; CHONDROGENESIS; CLINICAL ARTICLE; CLINICAL FEATURE; COHORT ANALYSIS; COMPLEX FORMATION; CRANIAL SUTURE; CRANIOFACIAL SYNOSTOSIS; DNA REPLICATION; DNA SYNTHESIS; DWARFISM; FEMALE; GENE; GENE FREQUENCY; GENE MUTATION; GENE SEQUENCE; GENETIC DISORDER; GENOME; GROWTH DISORDER; HUMAN; HUMAN CELL; INFANT; LOSS OF FUNCTION MUTATION; MALE; MEIER GORLIN SYNDROME; PHENOTYPE; PRESCHOOL CHILD; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA SPLICING; SCHOOL CHILD; SHORT STATURE; TRANSCRIPTION PREINITIATION COMPLEX; YOUNG ADULT; ABNORMALITIES; ALTERNATIVE RNA SPLICING; AMINO ACID SEQUENCE; AMNION; CELL CULTURE; CELL LINE; CHEMISTRY; CYTOLOGY; DEFICIENCY; DNA MUTATIONAL ANALYSIS; EXOME; EXON; GENETIC ASSOCIATION STUDY; GENETICS; METABOLISM; MICROGNATHIA; MICROTIA; MOLECULAR MODEL; MUTATION; PATELLA; PROTEIN CONFORMATION; SYNDROME;

ADOLESCENT; ADULT; ALLELES; ALTERNATIVE SPLICING; AMINO ACID SEQUENCE; AMNION; CELL CYCLE PROTEINS; CELL LINE; CELLS, CULTURED; CHILD; CHILD, PRESCHOOL; CONGENITAL MICROTIA; CRANIOSYNOSTOSES; DNA MUTATIONAL ANALYSIS; DNA REPLICATION; EXOME; EXONS; FEMALE; GENETIC ASSOCIATION STUDIES; GROWTH DISORDERS; HUMANS; MALE; MICROGNATHISM; MODELS, MOLECULAR; MUTATION; PATELLA; PROTEIN CONFORMATION; SYNDROME; YOUNG ADULT;

EID: 84978524915     PISSN: 00029297     EISSN: 15376605     Source Type: Journal    
DOI: 10.1016/j.ajhg.2016.05.019     Document Type: Article

References (57)

1. 1 Bell, S.P., Stillman, B., ATP-dependent recognition of eukaryotic origins of DNA replication by a multiprotein complex. Nature 357 (1992), 128–134.
2. 2 Tanaka, S., Diffley, J.F., Interdependent nuclear accumulation of budding yeast Cdt1 and Mcm2-7 during G1 phase. Nat. Cell Biol. 4 (2002), 198–207.
3. 3 Tanaka, S., Araki, H., Helicase activation and establishment of replication forks at chromosomal origins of replication. Cold Spring Harb. Perspect. Biol., 5, 2013, a010371.
4. 4 Costa, A., Renault, L., Swuec, P., Petojevic, T., Pesavento, J.J., Ilves, I., MacLellan-Gibson, K., Fleck, R.A., Botchan, M.R., Berger, J.M., DNA binding polarity, dimerization, and ATPase ring remodeling in the CMG helicase of the eukaryotic replisome. eLife, 3, 2014, e03273.
5. 5 Ilves, I., Petojevic, T., Pesavento, J.J., Botchan, M.R., Activation of the MCM2-7 helicase by association with Cdc45 and GINS proteins. Mol. Cell 37 (2010), 247–258.
6. 6 Li, N., Zhai, Y., Zhang, Y., Li, W., Yang, M., Lei, J., Tye, B.K., Gao, N., Structure of the eukaryotic MCM complex at 3.8 Å. Nature 524 (2015), 186–191.
7. 7 Moyer, S.E., Lewis, P.W., Botchan, M.R., Isolation of the Cdc45/Mcm2-7/GINS (CMG) complex, a candidate for the eukaryotic DNA replication fork helicase. Proc. Natl. Acad. Sci. USA 103 (2006), 10236–10241.
8. 8 Pacek, M., Tutter, A.V., Kubota, Y., Takisawa, H., Walter, J.C., Localization of MCM2-7, Cdc45, and GINS to the site of DNA unwinding during eukaryotic DNA replication. Mol. Cell 21 (2006), 581–587.
9. 9 Szambowska, A., Tessmer, I., Kursula, P., Usskilat, C., Prus, P., Pospiech, H., Grosse, F., DNA binding properties of human Cdc45 suggest a function as molecular wedge for DNA unwinding. Nucleic Acids Res. 42 (2014), 2308–2319.
10. 10 Hopwood, B., Dalton, S., Cdc45p assembles into a complex with Cdc46p/Mcm5p, is required for minichromosome maintenance, and is essential for chromosomal DNA replication. Proc. Natl. Acad. Sci. USA 93 (1996), 12309–12314.
11. 11 Mimura, S., Takisawa, H., Xenopus Cdc45-dependent loading of DNA polymerase alpha onto chromatin under the control of S-phase Cdk. EMBO J. 17 (1998), 5699–5707.
12. 12 Miyake, S., Yamashita, S., Identification of sna41 gene, which is the suppressor of nda4 mutation and is involved in DNA replication in Schizosaccharomyces pombe. Genes Cells 3 (1998), 157–166.
13. 13 Yoshida, K., Kuo, F., George, E.L., Sharpe, A.H., Dutta, A., Requirement of CDC45 for postimplantation mouse development. Mol. Cell. Biol. 21 (2001), 4598–4603.
14. 14 Zou, L., Mitchell, J., Stillman, B., CDC45, a novel yeast gene that functions with the origin recognition complex and Mcm proteins in initiation of DNA replication. Mol. Cell. Biol. 17 (1997), 553–563.
15. 15 Heller, R.C., Kang, S., Lam, W.M., Chen, S., Chan, C.S., Bell, S.P., Eukaryotic origin-dependent DNA replication in vitro reveals sequential action of DDK and S-CDK kinases. Cell 146 (2011), 80–91.
16. 16 On, K.F., Beuron, F., Frith, D., Snijders, A.P., Morris, E.P., Diffley, J.F., Prereplicative complexes assembled in vitro support origin-dependent and independent DNA replication. EMBO J. 33 (2014), 605–620.
17. 17 Yeeles, J.T., Deegan, T.D., Janska, A., Early, A., Diffley, J.F., Regulated eukaryotic DNA replication origin firing with purified proteins. Nature 519 (2015), 431–435.
18. 18 Bongers, E.M., Opitz, J.M., Fryer, A., Sarda, P., Hennekam, R.C., Hall, B.D., Superneau, D.W., Harbison, M., Poss, A., van Bokhoven, H., et al. Meier-Gorlin syndrome: report of eight additional cases and review. Am. J. Med. Genet. 102 (2001), 115–124.
19. 19 Bicknell, L.S., Bongers, E.M., Leitch, A., Brown, S., Schoots, J., Harley, M.E., Aftimos, S., Al-Aama, J.Y., Bober, M., Brown, P.A., et al. Mutations in the pre-replication complex cause Meier-Gorlin syndrome. Nat. Genet. 43 (2011), 356–359.
20. 20 Bicknell, L.S., Walker, S., Klingseisen, A., Stiff, T., Leitch, A., Kerzendorfer, C., Martin, C.A., Yeyati, P., Al Sanna, N., Bober, M., et al. Mutations in ORC1, encoding the largest subunit of the origin recognition complex, cause microcephalic primordial dwarfism resembling Meier-Gorlin syndrome. Nat. Genet. 43 (2011), 350–355.
21. 21 Guernsey, D.L., Matsuoka, M., Jiang, H., Evans, S., Macgillivray, C., Nightingale, M., Perry, S., Ferguson, M., LeBlanc, M., Paquette, J., et al. Mutations in origin recognition complex gene ORC4 cause Meier-Gorlin syndrome. Nat. Genet. 43 (2011), 360–364.
22. 22 de Munnik, S.A., Hoefsloot, E.H., Roukema, J., Schoots, J., Knoers, N.V., Brunner, H.G., Jackson, A.P., Bongers, E.M., Meier-Gorlin syndrome. Orphanet J. Rare Dis., 10, 2015, 114.
23. 23 Burrage, L.C., Charng, W.L., Eldomery, M.K., Willer, J.R., Davis, E.E., Lugtenberg, D., Zhu, W., Leduc, M.S., Akdemir, Z.C., Azamian, M., et al. De novo GMNN mutations cause autosomal-dominant primordial dwarfism associated with Meier-Gorlin syndrome. Am. J. Hum. Genet. 97 (2015), 904–913.
24. 24 Yoshida, K., Oyaizu, N., Dutta, A., Inoue, I., The destruction box of human Geminin is critical for proliferation and tumor growth in human colon cancer cells. Oncogene 23 (2004), 58–70.
25. 25 Sievers, F., Wilm, A., Dineen, D., Gibson, T.J., Karplus, K., Li, W., Lopez, R., McWilliam, H., Remmert, M., Söding, J., et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol. Syst. Biol., 7, 2011, 539.
26. 26 Yuan, Z., Bai, L., Sun, J., Georgescu, R., Liu, J., O'Donnell, M.E., Li, H., Structure of the eukaryotic replicative CMG helicase suggests a pumpjack motion for translocation. Nat. Struct. Mol. Biol. 23 (2016), 217–224.
27. 27 Sali, A., Blundell, T.L., Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol. 234 (1993), 779–815.
28. 28 Taylor, J.C., Martin, H.C., Lise, S., Broxholme, J., Cazier, J.B., Rimmer, A., Kanapin, A., Lunter, G., Fiddy, S., Allan, C., et al. Factors influencing success of clinical genome sequencing across a broad spectrum of disorders. Nat. Genet. 47 (2015), 717–726.
29. 29 Robinson, J.T., Thorvaldsdóttir, H., Winckler, W., Guttman, M., Lander, E.S., Getz, G., Mesirov, J.P., Integrative genomics viewer. Nat. Biotechnol. 29 (2011), 24–26.
30. 30 Abid Ali, F., Renault, L., Gannon, J., Gahlon, H.L., Kotecha, A., Zhou, J.C., Rueda, D., Costa, A., Cryo-EM structures of the eukaryotic replicative helicase bound to a translocation substrate. Nat. Commun., 7, 2016, 10708.
31. 31 Krastanova, I., Sannino, V., Amenitsch, H., Gileadi, O., Pisani, F.M., Onesti, S., Structural and functional insights into the DNA replication factor Cdc45 reveal an evolutionary relationship to the DHH family of phosphoesterases. J. Biol. Chem. 287 (2012), 4121–4128.
32. 32 Sanchez-Pulido, L., Ponting, C.P., Cdc45: the missing RecJ ortholog in eukaryotes?. Bioinformatics 27 (2011), 1885–1888.
33. 33 He, Q., Wang, F., Liu, S., Zhu, D., Cong, H., Gao, F., Li, B., Wang, H., Lin, Z., Liao, J., Gu, L., Structural and biochemical insight into the mechanism of Rv2837c from Mycobacterium tuberculosis as a c-di-NMP phosphodiesterase. J. Biol. Chem. 291 (2016), 3668–3681.
34. 34 Wakamatsu, T., Kim, K., Uemura, Y., Nakagawa, N., Kuramitsu, S., Masui, R., Role of RecJ-like protein with 5′-3′ exonuclease activity in oligo(deoxy)nucleotide degradation. J. Biol. Chem. 286 (2011), 2807–2816.
35. 35 Yamagata, A., Kakuta, Y., Masui, R., Fukuyama, K., The crystal structure of exonuclease RecJ bound to Mn2+ ion suggests how its characteristic motifs are involved in exonuclease activity. Proc. Natl. Acad. Sci. USA 99 (2002), 5908–5912.
36. 36 Kukimoto, I., Igaki, H., Kanda, T., Human CDC45 protein binds to minichromosome maintenance 7 protein and the p70 subunit of DNA polymerase alpha. Eur. J. Biochem. 265 (1999), 936–943.
37. 37 Desmet, F.O., Hamroun, D., Lalande, M., Collod-Béroud, G., Claustres, M., Béroud, C., Human Splicing Finder: an online bioinformatics tool to predict splicing signals. Nucleic Acids Res., 37, 2009, e67.
38. 38 Schwartz, S., Hall, E., Ast, G., SROOGLE: webserver for integrative, user-friendly visualization of splicing signals. Nucleic Acids Res. 37 (2009), W189–W192.
39. 39 Delio, M., Guo, T., McDonald-McGinn, D.M., Zackai, E., Herman, S., Kaminetzky, M., Higgins, A.M., Coleman, K., Chow, C., Jalbrzikowski, M., et al. Enhanced maternal origin of the 22q11.2 deletion in velocardiofacial and DiGeorge syndromes. Am. J. Hum. Genet. 92 (2013), 439–447.
40. 40 Casey, J.P., Nobbs, M., McGettigan, P., Lynch, S., Ennis, S., Recessive mutations in MCM4/PRKDC cause a novel syndrome involving a primary immunodeficiency and a disorder of DNA repair. J. Med. Genet. 49 (2012), 242–245.
41. 41 Gineau, L., Cognet, C., Kara, N., Lach, F.P., Dunne, J., Veturi, U., Picard, C., Trouillet, C., Eidenschenk, C., Aoufouchi, S., et al. Partial MCM4 deficiency in patients with growth retardation, adrenal insufficiency, and natural killer cell deficiency. J. Clin. Invest. 122 (2012), 821–832.
42. 42 Hughes, C.R., Guasti, L., Meimaridou, E., Chuang, C.H., Schimenti, J.C., King, P.J., Costigan, C., Clark, A.J., Metherell, L.A., MCM4 mutation causes adrenal failure, short stature, and natural killer cell deficiency in humans. J. Clin. Invest. 122 (2012), 814–820.
43. 43 Im, J.S., Ki, S.H., Farina, A., Jung, D.S., Hurwitz, J., Lee, J.K., Assembly of the Cdc45-Mcm2-7-GINS complex in human cells requires the Ctf4/And-1, RecQL4, and Mcm10 proteins. Proc. Natl. Acad. Sci. USA 106 (2009), 15628–15632.
44. 44 Sangrithi, M.N., Bernal, J.A., Madine, M., Philpott, A., Lee, J., Dunphy, W.G., Venkitaraman, A.R., Initiation of DNA replication requires the RECQL4 protein mutated in Rothmund-Thomson syndrome. Cell 121 (2005), 887–898.
45. 45 Siitonen, H.A., Sotkasiira, J., Biervliet, M., Benmansour, A., Capri, Y., Cormier-Daire, V., Crandall, B., Hannula-Jouppi, K., Hennekam, R., Herzog, D., et al. The mutation spectrum in RECQL4 diseases. Eur. J. Hum. Genet. 17 (2009), 151–158.
46. 46 Hossain, M., Stillman, B., Meier-Gorlin syndrome mutations disrupt an Orc1 CDK inhibitory domain and cause centrosome reduplication. Genes Dev. 26 (2012), 1797–1810.
47. 47 Stiff, T., Alagoz, M., Alcantara, D., Outwin, E., Brunner, H.G., Bongers, E.M., O'Driscoll, M., Jeggo, P.A., Deficiency in origin licensing proteins impairs cilia formation: implications for the aetiology of Meier-Gorlin syndrome. PLoS Genet., 9, 2013, e1003360.
48. 48 Schmidt, U., Wollmann, Y., Franke, C., Grosse, F., Saluz, H.P., Hänel, F., Characterization of the interaction between the human DNA topoisomerase IIbeta-binding protein 1 (TopBP1) and the cell division cycle 45 (Cdc45) protein. Biochem. J. 409 (2008), 169–177.
49. 49 Di Perna, R., Aria, V., De Falco, M., Sannino, V., Okorokov, A.L., Pisani, F.M., De Felice, M., The physical interaction of Mcm10 with Cdc45 modulates their DNA-binding properties. Biochem. J. 454 (2013), 333–343.
50. 50 Klingseisen, A., Jackson, A.P., Mechanisms and pathways of growth failure in primordial dwarfism. Genes Dev. 25 (2011), 2011–2024.
51. 51 de Munnik, S.A., Bicknell, L.S., Aftimos, S., Al-Aama, J.Y., van Bever, Y., Bober, M.B., Clayton-Smith, J., Edrees, A.Y., Feingold, M., Fryer, A., et al. Meier-Gorlin syndrome genotype-phenotype studies: 35 individuals with pre-replication complex gene mutations and 10 without molecular diagnosis. Eur. J. Hum. Genet. 20 (2012), 598–606.
52. 52 Twigg, S.R.F., Wilkie, A.O.M., A genetic-pathophysiological framework for craniosynostosis. Am. J. Hum. Genet. 97 (2015), 359–377.
53. 53 Newell, N.E., Mapping side chain interactions at protein helix termini. BMC Bioinformatics, 16, 2015, 231.
54. 54 Berti, M., Vindigni, A., Replication stress: getting back on track. Nat. Struct. Mol. Biol. 23 (2016), 103–109.
55. 55 Aravind, L., Koonin, E.V., The HD domain defines a new superfamily of metal-dependent phosphohydrolases. Trends Biochem. Sci. 23 (1998), 469–472.
56. 56 Cole, T.J., Freeman, J.V., Preece, M.A., British 1990 growth reference centiles for weight, height, body mass index and head circumference fitted by maximum penalized likelihood. Stat. Med. 17 (1998), 407–429.
57. 57 Fenton, T.R., Kim, J.H., A systematic review and meta-analysis to revise the Fenton growth chart for preterm infants. BMC Pediatr., 13, 2013, 59.