DNA damage response in microcephaly development of MCPH1 mouse model

DNA Repair

Volumn 12, Issue 8, 2013, Pages 645-655

  Zhou, Zhong Wei ^a   Tapias, Alicia ^a   Bruhn, Christopher ^a   Gruber, Ralph ^a   Sukchev, Mikhail ^a   Wang, Zhao Qi ^a,b  

^a FRITZ LIPMANN INSTITUTE   (Germany)

^b FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

Author keywords

DNA damage response; MCPH1; Microcephaly; Neurogenesis

Indexed keywords

APOPTOSIS; ARTICLE; BRAIN CORTEX; CELL MIGRATION; CENTROSOME; CONTROLLED STUDY; DNA DAMAGE; GAMMA IRRADIATION; GENE; GENE DELETION; GENOMIC INSTABILITY; GROWTH RETARDATION; IONIZING RADIATION; MICROCEPHALIN 1 GENE; MICROCEPHALY; MOUSE; NEOCORTEX; NERVE CELL; NEURONAL MIGRATION DISORDER; NONHUMAN; PRIORITY JOURNAL;

CORTICAL PLATE; CP; DDR; DNA DAMAGE RESPONSE; DNA DOUBLE-STRAND BREAKS; DNA SINGLE-STRAND BREAKS; DSB; EGL; EXTERNAL GRANULE LAYER; HOMOLOGOUS RECOMBINATION; HR; INTERMEDIATE ZONE; IONIZING RADIATION; IR; IZ; MCPH1; MEF; MICROCEPHALY; MICRONUCLEI; MN; MOUSE EMBRYONIC FIBROBLAST; NEUROGENESIS; SSB; SUBVENTRICULAR ZONE; SVZ; VENTRICULAR ZONE; VZ;

ANIMALS; APOPTOSIS; CELL DIFFERENTIATION; CENTROSOME; CHROMOSOMAL PROTEINS, NON-HISTONE; DISEASE MODELS, ANIMAL; DNA DAMAGE; DNA REPAIR; GENE DELETION; GENE KNOCKOUT TECHNIQUES; GENOMIC INSTABILITY; MICE; MICROCEPHALY; NEOCORTEX; NEURONS; RADIATION, IONIZING; RECOMBINATION, GENETIC;

MUS;

EID: 84880643551     PISSN: 15687864     EISSN: 15687856     Source Type: Journal    
DOI: 10.1016/j.dnarep.2013.04.017     Document Type: Article

References (49)

1. Branzei D., Foiani M. Maintaining genome stability at the replication fork. Nat. Rev. Mol. Cell. Biol. 2010, 11:208-219.
2. Mavrou A., Tsangaris G.T., Roma E., Kolialexi A. The ATM gene and ataxia telangiectasia. Anticancer Res. 2008, 28:401-405.
3. Shiloh Y. ATM and related protein kinases: safeguarding genome integrity. Nat. Rev. Cancer 2003, 3:155-168.
4. Jackson S.P., Bartek J. The DNA-damage response in human biology and disease. Nature 2009, 461:1071-1078.
5. Digweed M., Sperling K. Nijmegen breakage syndrome: clinical manifestation of defective response to DNA double-strand breaks. DNA Repair (Amst) 2004, 3:1207-1217.
6. Lavin M.F. Ataxia-telangiectasia: from a rare disorder to a paradigm for cell signalling and cancer. Nat. Rev. Mol. Cell. Biol. 2008, 9:759-769.
7. Stracker T.H., Petrini J.H. The MRE11 complex: starting from the ends. Nat. Rev. Mol. Cell. Biol. 2011, 12:90-103.
8. McKinnon P.J. DNA repair deficiency and neurological disease. Nat. Rev. Neurosci. 2009, 10:100-112.
9. Barzilai A., Biton S., Shiloh Y. The role of the DNA damage response in neuronal development, organization and maintenance. DNA Repair (Amst) 2008, 7:1010-1027.
10. O'Driscoll M., Jeggo P.A. The role of the DNA damage response pathways in brain development and microcephaly: insight from human disorders. DNA Repair (Amst) 2008, 7:1039-1050.
11. Manzini M.C., Walsh C.A. What disorders of cortical development tell us about the cortex: one plus one does not always make two. Curr. Opin. Genet. Dev. 2011, 21:333-339.
12. Barkovich A.J., Guerrini R., Kuzniecky R.I., Jackson G.D., Dobyns W.B. A developmental and genetic classification for malformations of cortical development: update 2012. Brain 2012, 135:1348-1369.
13. Woods C.G., Bond J., Enard W. Autosomal recessive primary microcephaly (MCPH): a review of clinical, molecular, and evolutionary findings. Am. J. Hum. Genet. 2005, 76:717-728.
14. Thornton G.K., Woods C.G. Primary microcephaly: do all roads lead to Rome?. Trends Genet. 2009, 25:501-510.
15. Trimborn M., Bell S.M., Felix C., Rashid Y., Jafri H., Griffiths P.D., Neumann L.M., Krebs A., Reis A., Sperling K., Neitzel H., Jackson A.P. Mutations in microcephalin cause aberrant regulation of chromosome condensation. Am. J. Hum. Genet. 2004, 75:261-266.
16. Kaindl A.M., Passemard S., Kumar P., Kraemer N., Issa L., Zwirner A., Gerard B., Verloes A., Mani S., Gressens P. Many roads lead to primary autosomal recessive microcephaly. Prog. Neurobiol. 2010, 90:363-383.
17. Abuelo D. Microcephaly syndromes. Semin. Pediatr. Neurol. 2007, 14:118-127.
18. Guernsey D.L., Jiang H., Hussin J., Arnold M., Bouyakdan K., Perry S., Babineau-Sturk T., Beis J., Dumas N., Evans S.C., Ferguson M., Matsuoka M., Macgillivray C., Nightingale M., Patry L., Rideout A.L., Thomas A., Orr A., Hoffmann I., Michaud J.L., Awadalla P., Meek D.C., Ludman M., Samuels M.E. Mutations in centrosomal protein CEP152 in primary microcephaly families linked to MCPH4. Am. J. Hum. Genet. 2010, 87:40-51.
19. Nicholas A.K., Khurshid M., Desir J., Carvalho O.P., Cox J.J., Thornton G., Kausar R., Ansar M., Ahmad W., Verloes A., Passemard S., Misson J.P., Lindsay S., Gergely F., Dobyns W.B., Roberts E., Abramowicz M., Woods C.G. WDR62 is associated with the spindle pole and is mutated in human microcephaly. Nat. Genet. 2010, 42:1010-1014.
20. Yu T.W., Mochida G.H., Tischfield D.J., Sgaier S.K., Flores-Sarnat L., Sergi C.M., Topcu M., McDonald M.T., Barry B.J., Felie J.M., Sunu C., Dobyns W.B., Folkerth R.D., Barkovich A.J., Walsh C.A. Mutations in WDR62, encoding a centrosome-associated protein, cause microcephaly with simplified gyri and abnormal cortical architecture. Nat. Genet. 2010, 42:1015-1020.
21. Mahmood S., Ahmad W., Hassan M.J. Autosomal Recessive Primary Microcephaly (MCPH): clinical manifestations, genetic heterogeneity and mutation continuum. Orphanet. J. Rare Dis. 2011, 6:39.
22. Megraw T.L., Sharkey J.T., Nowakowski R.S. Cdk5rap2 exposes the centrosomal root of microcephaly syndromes. Trends Cell Biol. 2011, 21:470-480.
23. Jackson A.P., Eastwood H., Bell S.M., Adu J., Toomes C., Carr I.M., Roberts E., Hampshire D.J., Crow Y.J., Mighell A.J., Karbani G., Jafri H., Rashid Y., Mueller R.F., Markham A.F., Woods C.G. Identification of microcephalin, a protein implicated in determining the size of the human brain. Am. J. Hum. Genet. 2002, 71:136-142.
24. Jackson A.P., McHale D.P., Campbell D.A., Jafri H., Rashid Y., Mannan J., Karbani G., Corry P., Levene M.I., Mueller R.F., Markham A.F., Lench N.J., Woods C.G. Primary autosomal recessive microcephaly (MCPH1) maps to chromosome 8p22-pter. Am. J. Hum. Genet. 1998, 63:541-546.
25. Bork P., Hofmann K., Bucher P., Neuwald A.F., Altschul S.F., Koonin E.V. A superfamily of conserved domains in DNA damage-responsive cell cycle checkpoint proteins. FASEB J. 1997, 11:68-76.
26. Yu X., Chini C.C., He M., Mer G., Chen J. The BRCT domain is a phospho-protein binding domain. Science 2003, 302:639-642.
27. Lin S.Y., Liang Y., Li K. Multiple roles of BRIT1/MCPH1 in DNA damage response, DNA repair, and cancer suppression. Yonsei Med. J. 2010, 51:295-301.
28. Lin S.Y., Rai R., Li K., Xu Z.X., Elledge S.J. BRIT1/MCPH1 is a DNA damage responsive protein that regulates the Brca1-Chk1 pathway, implicating checkpoint dysfunction in microcephaly. Proc. Natl. Acad. Sci. U.S.A. 2005, 102:15105-15109.
29. Rai R., Dai H., Multani A.S., Li K., Chin K., Gray J., Lahad J.P., Liang J., Mills G.B., Meric-Bernstam F., Lin S.Y. BRIT1 regulates early DNA damage response, chromosomal integrity, and cancer. Cancer Cell 2006, 10:145-157.
30. Alderton G.K., Galbiati L., Griffith E., Surinya K.H., Neitzel H., Jackson A.P., Jeggo P.A., O'Driscoll M. Regulation of mitotic entry by microcephalin and its overlap with ATR signalling. Nat. Cell Biol. 2006, 8:725-733.
31. Xu X., Lee J., Stern D.F. Microcephalin is a DNA damage response protein involved in regulation of CHK1 and BRCA1. J. Biol. Chem. 2004, 279:34091-34094.
32. Wood J.L., Liang Y., Li K., Chen J. Microcephalin/MCPH1 associates with the Condensin II complex to function in homologous recombination repair. J. Biol. Chem. 2008, 283:29586-29592.
33. Peng G., Yim E.K., Dai H., Jackson A.P., Burgt I., Pan M.R., Hu R., Li K., Lin S.Y. BRIT1/MCPH1 links chromatin remodelling to DNA damage response. Nat. Cell Biol. 2009, 11:865-872.
34. Yang S.Z., Lin F.T., Lin W.C. MCPH1/BRIT1 cooperates with E2F1 in the activation of checkpoint, DNA repair and apoptosis. EMBO Rep. 2008, 9:907-915.
35. Liang Y., Gao H., Lin S.Y., Peng G., Huang X., Zhang P., Goss J.A., Brunicardi F.C., Multani A.S., Chang S., Li K. BRIT1/MCPH1 is essential for mitotic and meiotic recombination DNA repair and maintaining genomic stability in mice. PLoS Genet. 2010, 6:e1000826.
36. Trimborn M., Ghani M., Walther D.J., Dopatka M., Dutrannoy V., Busche A., Meyer F., Nowak S., Nowak J., Zabel C., Klose J., Esquitino V., Garshasbi M., Kuss A.W., Ropers H.H., Mueller S., Poehlmann C., Gavvovidis I., Schindler D., Sperling K., Neitzel H. Establishment of a mouse model with misregulated chromosome condensation due to defective Mcph1 function. PLoS ONE 2010, 5:e9242.
37. Gruber R., Zhou Z., Sukchev M., Joerss T., Frappart P.O., Wang Z.Q. MCPH1 regulates the neuroprogenitor division mode by coupling the centrosomal cycle with mitotic entry through the Chk1-Cdc25 pathway. Nat. Cell Biol. 2011, 13:1325-1334.
38. Molyneaux B.J., Arlotta P., Menezes J.R., Macklis J.D. Neuronal subtype specification in the cerebral cortex. Nat. Rev. Neurosci. 2007, 8:427-437.
39. Yang Y.G., Saidi A., Frappart P.O., Min W., Barrucand C., Dumon-Jones V., Michelon J., Herceg Z., Wang Z.Q. Conditional deletion of Nbs1 in murine cells reveals its role in branching repair pathways of DNA double-strand breaks. EMBO J. 2006, 25:5527-5538.
40. Higginbotham H.R., Gleeson J.G. The centrosome in neuronal development. Trends Neurosci. 2007, 30:276-283.
41. Wu X., Mondal G., Wang X., Wu J., Yang L., Pankratz V.S., Rowley M., Couch F.J. Microcephalin regulates BRCA2 and Rad51-associated DNA double-strand break repair. Cancer Res. 2009, 69:5531-5536.
42. Jeffers L.J., Coull B.J., Stack S.J., Morrison C.G. Distinct BRCT domains in Mcph1/Brit1 mediate ionizing radiation-induced focus formation and centrosomal localization. Oncogene 2008, 27:139-144.
43. Wood J.L., Singh N., Mer G., Chen J. MCPH1 functions in an H2AX-dependent but MDC1-independent pathway in response to DNA damage. J. Biol. Chem. 2007, 282:35416-35423.
44. Tibelius A., Marhold J., Zentgraf H., Heilig C.E., Neitzel H., Ducommun B., Rauch A., Ho A.D., Bartek J., Kramer A. Microcephalin and pericentrin regulate mitotic entry via centrosome-associated Chk1. J. Cell Biol. 2009, 185:1149-1157.
45. Zhou Z., Bruhn C., Wang Z.Q. Differential function of NBS1 and ATR in neurogenesis. DNA Repair (Amst) 2012, 11:210-221.
46. Frappart P.O., Lee Y., Lamont J., McKinnon P.J. BRCA2 is required for neurogenesis and suppression of medulloblastoma. EMBO J. 2007, 26:2732-2742.
47. Li R., Yang Y.G., Gao Y., Wang Z.Q., Tong W.M. A distinct response to endogenous DNA damage in the development of Nbs1-deficient cortical neurons. Cell Res. 2012, 22:859-872.
48. Dumon-Jones V., Frappart P.O., Tong W.M., Sajithlal G., Hulla W., Schmid G., Herceg Z., Digweed M., Wang Z.Q. Nbn heterozygosity renders mice susceptible to tumor formation and ionizing radiation-induced tumorigenesis. Cancer Res. 2003, 63:7263-7269.
49. Pierce A.J., Johnson R.D., Thompson L.H., Jasin M. XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. Genes Dev. 1999, 13:2633-2638.