Mutation in PHC1 implicates chromatin remodeling in primary microcephaly pathogenesis

Human Molecular Genetics

Volumn 22, Issue 11, 2013, Pages 2200-2213

  Awad, Salma ^a   Al Dosari, Mohammed S ^a,b   Al Yacoub, Nadya ^a   Colak, Dilek ^a   Salih, Mustafa A ^c   Alkuraya, Fowzan S ^a,d   Poizat, Coralie ^a  

^a KING FAISAL SPECIALIST HOSPITAL AND RESEARCH CENTER   (Saudi Arabia)

^b KING SAUD UNIVERSITY   (Saudi Arabia)

^c KING KHALID UNIVERSITY HOSPITAL   (Saudi Arabia)

^d ALFAISAL UNIVERSITY   (Saudi Arabia)

Author keywords

[No Author keywords available]

Indexed keywords

CELL DNA; GEMININ; HISTONE H2A; PHC1 PROTEIN; POLYCOMB GROUP PROTEIN; UNCLASSIFIED DRUG;

ADOLESCENT; ARTICLE; CASE REPORT; CHILD; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; DNA REPAIR; EXOME; FEMALE; GENE OVEREXPRESSION; GENE SEQUENCE; GENETIC VARIABILITY; GENOME ANALYSIS; HUMAN; HUMAN CELL; INFRARED RADIATION; MALE; MICROCEPHALY; MISSENSE MUTATION; MOLECULAR PATHOLOGY; PRESCHOOL CHILD; PRIMARY MICROCEPHALY; PRIORITY JOURNAL; PROTEIN CONTENT; PROTEIN EXPRESSION; SEQUENCE ANALYSIS; UBIQUITINATION; WILD TYPE;

ADOLESCENT; CELL CYCLE; CHILD; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONSANGUINITY; DNA DAMAGE; DNA REPAIR; EXOME; FEMALE; GEMININ; GENE EXPRESSION; GENETIC LINKAGE; GENETIC LOCI; HISTONES; HUMANS; MALE; MICROCEPHALY; MODELS, BIOLOGICAL; MUTATION; PEDIGREE; POLYCOMB REPRESSIVE COMPLEX 1; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEOLYSIS; SEQUENCE ANALYSIS, DNA; UBIQUITINATION;

EID: 84877904456     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt072     Document Type: Article

References (45)

1. Thornton, G.K. and Woods, C.G. (2009) Primary microcephaly: do all roads lead to Rome? Trends Genet., 25, 501-510.
2. Mahmood, S., Ahmad, W. and Hassan, M.J. (2011) Autosomal recessive primary microcephaly (MCPH): clinical manifestations, genetic heterogeneity and mutation continuum. Orphanet. J. Rare. Dis., 6, 39.
3. Lin, S.Y., Rai, R., Li, K., Xu, Z.X. and Elledge, S.J. (2005) BRIT1/ MCPH1 is a DNA damage responsive protein that regulates the Brca1-Chk1 pathway, implicating checkpoint dysfunction in microcephaly. Proc. Natl Acad. Sci. USA, 102, 15105-15109.
4. Tang, B.L. (2006) Molecular genetic determinants of human brain size. Biochem Biophys Res. Commun., 345, 911-916.
5. Hussain, M.S., Baig, S.M., Neumann, S., Nurnberg, G., Farooq, M., Ahmad, I., Alef, T., Hennies, H.C., Technau, M., Altmuller, J. et al. (2012) A truncating mutation of CEP135 causes primary microcephaly and disturbed centrosomal function. Am. J. Hum. Genet., 90, 871-878.
6. Gruber, R., Zhou, Z., Sukchev, M., Joerss, T., Frappart, P.O. and Wang, Z.Q. (2011) MCPH1 regulates the neuroprogenitor division mode by coupling the centrosomal cycle with mitotic entry through the Chk1-Cdc25 pathway. Nat. Cell. Biol., 13, 1325-1334.
7. Fish, J.L., Kosodo, Y., Enard, W., Paabo, S. and Huttner, W.B. (2006) Aspm specifically maintains symmetric proliferative divisions of neuroepithelial cells. Proc. Natl Acad. Sci. USA, 103, 10438-10443.
8. Klingseisen, A. and Jackson, A.P. (2011) Mechanisms and pathways of growth failure in primordial dwarfism. Genes. Dev., 25, 2011-2024.
9. Al-Dosari, M.S., Shaheen, R., Colak, D. and Alkuraya, F.S. (2010) Novel CENPJ mutation causes Seckel syndrome. J. Med. Genet., 47, 411-414.
10. Waltes, R., Kalb, R., Gatei, M., Kijas, A.W., Stumm, M., Sobeck, A., Wieland, B., Varon, R., Lerenthal, Y., Lavin, M.F. et al. (2009) Human RAD50 deficiency in a Nijmegen breakage syndrome-like disorder. Am. J. Hum. Genet., 84, 605-616.
11. O'Driscoll, M. and Jeggo, P.A. (2008) The role of the DNA damage response pathways in brain development and microcephaly: insight from human disorders. DNA Repair (Amst), 7, 1039-1050.
12. Demuth, I. and Digweed, M. (2007) The clinical manifestation of a defective response to DNA double-strand breaks as exemplified by Nijmegen breakage syndrome. Oncogene, 26, 7792-7798.
13. McKinnon, P.J. and Caldecott, K.W. (2007) DNA strand break repair and human genetic disease. Annu. Rev. Genomics Hum. Genet., 8, 37-55.
14. Sparmann, A. and van Lohuizen, M. (2006) Polycomb silencers control cell fate, development and cancer. Nat. Rev. Cancer, 6, 846-856.
15. Cao, R., Tsukada, Y. and Zhang, Y. (2005) Role of Bmi-1 and Ring1A in H2A ubiquitylation and Hox gene silencing. Mol. Cell, 20, 845-854.
16. Margueron, R. and Reinberg, D. (2011) The Polycomb complex PRC2 and its mark in life. Nature, 469, 343-349.
17. Wang, H., Wang, L., Erdjument-Bromage, H., Vidal, M., Tempst, P., Jones, R.S. and Zhang, Y. (2004) Role of histone H2A ubiquitination in Polycomb silencing. Nature, 431, 873-878.
18. Ohno, Y., Yasunaga, S., Ohtsubo, M., Mori, S., Tsumura, M., Okada, S., Ohta, T., Ohtani, K., Kobayashi, M. and Takihara, Y. (2010) Hoxb4 transduction down-regulates Geminin protein, providing hematopoietic stem and progenitor cells with proliferation potential. Proc. Natl Acad. Sci. USA, 107, 21529-21534.
19. Alkema, M.J., Bronk, M., Verhoeven, E., Otte, A., van't Veer, L.J., Berns, A. and van Lohuizen, M. (1997) Identification of Bmi1-interacting proteins as constituents of a multimeric mammalian polycomb complex. Genes Dev., 11, 226-240.
20. Cmarko, D., Verschure, P.J., Otte, A.P., van Driel, R. and Fakan, S. (2003) Polycomb group gene silencing proteins are concentrated in the perichromatin compartment of the mammalian nucleus. J. Cell Sci., 116, 335-343.
21. Hashimoto, N., Brock, H.W., Nomura, M., Kyba, M., Hodgson, J., Fujita, Y., Takihara, Y., Shimada, K. and Higashinakagawa, T. (1998) RAE28, BMI1, and M33 are members of heterogeneous multimeric mammalian Polycomb group complexes. Biochem. Biophys. Res. Commun., 245, 356-365.
22. Chou, D.M., Adamson, B., Dephoure, N.E., Tan, X., Nottke, A.C., Hurov, K.E., Gygi, S.P., Colaiacovo, M.P. and Elledge, S.J. (2010) A chromatin localization screen reveals poly (ADP ribose)-regulated recruitment of the repressive polycomb and NuRD complexes to sites of DNA damage. Proc. Natl Acad. Sci. USA, 107, 18475-18480.
23. Gieni, R.S., Ismail, I.H., Campbell, S. and Hendzel, M.J. (2011) Polycomb group proteins in the DNA damage response: a link between radiation resistance and 'stemness'. Cell Cycle, 10, 883-894.
24. Liang, Y., Gao, H., Lin, S.Y., Peng, G., Huang, X., Zhang, P., Goss, J.A., Brunicardi, F.C., Multani, A.S., Chang, S. et al. (2010) BRIT1/MCPH1 is essential for mitotic and meiotic recombination DNA repair and maintaining genomic stability in mice. PLoS Genet., 6, e1000826.
25. Ismail, I.H., Andrin, C., McDonald, D. and Hendzel, M.J. (2010) BMI1-mediated histone ubiquitylation promotes DNA double-strand break repair. J. Cell. Biol., 191, 45-60.
26. Zhou, W., Wang, X. and Rosenfeld, M.G. (2009) Histone H2A ubiquitination in transcriptional regulation and DNA damage repair. Int. J. Biochem. Cell. Biol., 41, 12-15.
27. Tang, C.J., Lin, S.Y., Hsu, W.B., Lin, Y.N., Wu, C.T., Lin, Y.C., Chang, C.W., Wu, K.S. and Tang, T.K. (2011) The human microcephaly protein STIL interacts with CPAP and is required for procentriole formation. EMBO J., 30, 4790-4804.
28. Higgins, J., Midgley, C., Bergh, A.M., Bell, S.M., Askham, J.M., Roberts, E., Binns, R.K., Sharif, S.M., Bennett, C., Glover, D.M. et al. (2010) Human ASPM participates in spindle organisation, spindle orientation and cytokinesis. BMC Cell. Biol., 11, 85.
29. Paro, R. (1995) Propagating memory of transcriptional states. Trends Genet., 11, 295-297.
30. Simon, J. (1995) Locking in stable states of gene expression: transcriptional control during Drosophila development. Curr. Opin. Cell Biol., 7, 376-385.
31. Krumlauf, R. (1994) Hox genes in vertebrate development. Cell, 78, 191-201.
32. Tomotsune, D., Takihara, Y., Berger, J., Duhl, D., Joo, S., Kyba, M., Shirai, M., Ohta, H., Matsuda, Y., Honda, B.M. et al. (1999) A novel member of murine Polycomb-group proteins, Sex comb on midleg homolog protein, is highly conserved, and interacts with RAE28/mph1 in vitro. Differentiation, 65, 229-239.
33. Luo, L. and Kessel, M. (2004) Geminin coordinates cell cycle and developmental control. Cell Cycle, 3, 711-714.
34. McGarry, T.J. and Kirschner, M.W. (1998) Geminin, an inhibitor of DNA replication, is degraded during mitosis. Cell, 93, 1043-1053.
35. Shen, J., Gilmore, E.C., Marshall, C.A., Haddadin, M., Reynolds, J.J., Eyaid, W., Bodell, A., Barry, B., Gleason, D., Allen, K. et al. (2010) Mutations in PNKP cause microcephaly, seizures and defects in DNA repair. Nat. Genet., 42, 245-249.
36. Qiao, F. and Bowie, J.U. (2005) The many faces of SAM. Sci. STKE, 2005, re7.
37. Ohta, H., Tokimasa, S., Zou, Z., Funaki, S., Kurahashi, H., Takahashi, Y., Kimura, M., Matsuoka, R., Horie, M., Hara, J. et al. (2000) Structure and chromosomal localization of the RAE28/HPH1 gene, a human homologue of the polyhomeotic gene. DNA Seq., 11, 61-73.
38. Nomura, M., Takihara, Y. and Shimada, K. (1994) Isolation and characterization of retinoic acid-inducible cDNA clones in F9 cells: one of the early inducible clones encodes a novel protein sharing several highly homologous regions with a Drosophila polyhomeotic protein. Differentiation, 57, 39-50.
39. Tokimasa, S., Ohta, H., Sawada, A., Matsuda, Y., Kim, J.Y., Nishiguchi, S., Hara, J. and Takihara, Y. (2001) Lack of the Polycomb-group gene rae28 causes maturation arrest at the early B-cell developmental stage. Exp. Hematol., 29, 93-103.
40. Takihara, Y., Tomotsune, D., Shirai, M., Katoh-Fukui, Y., Nishii, K., Motaleb, M.A., Nomura, M., Tsuchiya, R., Fujita, Y., Shibata, Y. et al. (1997) Targeted disruption of the mouse homologue of the Drosophila polyhomeotic gene leads to altered anteroposterior patterning and neural crest defects. Development, 124, 3673-3682.
41. Ohta, H., Sawada, A., Kim, J.Y., Tokimasa, S., Nishiguchi, S., Humphries, R.K., Hara, J. and Takihara, Y. (2002) Polycomb group gene rae28 is required for sustaining activity of hematopoietic stem cells. J. Exp. Med., 195, 759-770.
42. Hoffmann, K. and Lindner, T.H. (2005) easyLINKAGE-Plus-automated linkage analyses using large-scale SNP data. Bioinformatics, 21, 3565-3567.
43. Carr, I.M., Flintoff, K.J., Taylor, G.R., Markham, A.F. and Bonthron, D.T. (2006) Interactive visual analysis of SNP data for rapid autozygosity mapping in consanguineous families. Hum. Mutat., 27, 1041-1046.
44. Singh, N.P., McCoy, M.T., Tice, R.R. and Schneider, E.L. (1988) A simple technique for quantitation of low levels of DNA damage in individual cells. Exp. Cell Res., 175, 184-191.
45. Nicoletti, I., Migliorati, G., Pagliacci, M.C., Grignani, F. and Riccardi, C. (1991) A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J. Immunol. Methods, 139, 271-279.