Meier-Gorlin syndrome mutations disrupt an Orc1 CDK inhibitory domain and cause centrosome reduplication

Genes and Development

Volumn 26, Issue 16, 2012, Pages 1797-1810

  Hossain, Manzar ^a   Stillman, Bruce ^a  

^a Cold Spring Harbor Laboratory ^*  (United States)

Author keywords

Centriole; Centrosome; Cyclin dependent protein kinase; Meier Gorlin syndrome; Origin recognition complex

Indexed keywords

CYCLIN A; CYCLIN E; ORIGIN RECOGNITION COMPLEX; ORIGIN RECOGNITION COMPLEX 1; UNCLASSIFIED DRUG;

ARTICLE; CENTROSOME; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; DNA REPLICATION; ENZYME ACTIVITY; ENZYME INHIBITION; GENE DOSAGE; GENE MUTATION; HUMAN; MEIER GORLIN SYNDROME; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

AMINO ACID SEQUENCE; CELL LINE, TUMOR; CENTRIOLES; CENTROSOME; CYCLIN-DEPENDENT KINASES; EAR; GROWTH DISORDERS; HEK293 CELLS; HUMANS; MICROGNATHISM; MOLECULAR SEQUENCE DATA; MUTATION; ORIGIN RECOGNITION COMPLEX; PATELLA; PROTEIN STRUCTURE, TERTIARY; RNA-BINDING PROTEINS; SEQUENCE ALIGNMENT;

EID: 84865092757     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.197178.112     Document Type: Article

References (46)

1. Armache KJ, Garlick JD, Canzio D, Narlikar GJ, Kingston RE. 2011. Structural basis of silencing: Sir3 BAH domain in complex with a nucleosome at 3.0 A resolution. Science 334: 977-982
2. Bartke T, Vermeulen M, Xhemalce B, Robson SC, Mann M Kouzarides T. 2010. Nucleosome-interacting proteins regulated by DNA and histone methylation. Cell 143: 470-484
3. Bicknell LS, Bongers EM, Leitch A, Brown S, Schoots J, Harley ME, Aftimos S, Al-Aama JY, Bober M, Brown PA, et al. 2011a. Mutations in the pre-replication complex cause Meier-Gorlin syndrome. Nat Genet 43: 356-359
4. Bicknell LS, Walker S, Klingseisen A, Stiff T, Leitch A, Kerzendorfer C, Martin CA, Yeyati P, Al Sanna N, Bober M, et al. 2011b. Mutations in ORC1, encoding the largest subunit of the origin recognition complex, cause microcephalic primordial dwarfism resembling Meier-Gorlin syndrome. Nat Genet 43: 350-355.
5. Brustel J, Tardat M, Kirsh O, Grimaud C, Julien E. 2011. Coupling mitosis to DNA replication: The emerging role of the histone H4-lysine 20 methyltransferase PR-Set7. Trends Cell Biol 21: 452-460.
6. Coverley D, Laman H, Laskey RA. 2002. Distinct roles for cyclins E and A during DNA replication complex assembly and activation. Nat Cell Biol 4: 523-528
7. de Munnik SA, Bicknell LS, Aftimos S, Al-Aama JY, van Bever Y, Bober MB, Clayton-Smith J, Edrees AY, Feingold M, Fryer A, et al. 2012. Meier-Gorlin syndrome genotype-phenotype studies: 35 individuals with pre-replication complex gene mutations and 10 without molecular diagnosis. Eur J Hum Genet 20: 598-606.
8. Doxsey SJ, Stein P, Evans L, Calarco PD, Kirschner M. 1994. Pericentrin, a highly conserved centrosome protein involved in microtubule organization. Cell 76: 639-650.
9. Ferguson RL, Maller JL. 2008. Cyclin E-dependent localization of MCM5 regulates centrosome duplication. J Cell Sci 121: 3224-3232.
10. Ferguson RL, Pascreau G, Maller JL. 2010. The cyclin A centrosomal localization sequence recruits MCM5 and Orc1 to regulate centrosome reduplication. J Cell Sci 123: 2743-2749.
11. Gillingham AK, Munro S. 2000. The PACT domain, a conserved centrosomal targeting motif in the coiled-coil proteins AKAP450 and pericentrin. EMBO Rep 1: 524-529
12. Guarguaglini G, Duncan PI, Stierhof YD, HolmstromT, Duensing S, Nigg EA. 2005. The forkhead-associated domain protein Cep170 interacts with Polo-like kinase 1 and serves as a marker for mature centrioles. Mol Biol Cell 16: 1095-1107.
13. Guernsey DL, Matsuoka M, Jiang H, Evans S, Macgillivray C, Nightingale M, Perry S, Ferguson M, LeBlanc M, Paquette J, et al. 2011. Mutations in origin recognition complex gene ORC4 cause Meier-Gorlin syndrome. Nat Genet 43: 360-364.
14. Hemerly AS, Prasanth SG, Siddiqui K, Stillman B. 2009. Orc1 controls centriole and centrosome copy number in human cells. Science 323: 789-793.
15. Hinchcliffe EH, Li C, Thompson EA, Maller JL, Sluder G. 1999. Requirement of Cdk2-cyclin E activity for repeated centrosome reproduction in Xenopus egg extracts. Science 283: 851-854.
16. Huang Z, Zang K, Reichardt LF. 2005. The origin recognition core complex regulates dendrite and spine development in postmitotic neurons. J Cell Biol 170: 527-535
17. Kitagawa D, Kohlmaier G, Keller D, Strnad P, Balestra FR Fluckiger I, Gonczy P. 2011. Spindle positioning in human cells relies on proper centriole formation and on the microcephaly proteins CPAP and STIL. J Cell Sci 124: 3884-3893.
18. Klingseisen A, Jackson AP. 2011. Mechanisms and pathways of growth failure in primordial dwarfism. Genes Dev 25: 2011-2024.
19. Knockleby J, Lee H. 2010. Same partners, different dance: Involvement of DNA replication proteins in centrosome regulation. Cell Cycle 9: 4487-4491.
20. Kreitz S, Ritzi M, Baack M, Knippers R. 2001. The human origin recognition complex protein 1 dissociates from chromatin during S phase in HeLa cells. J Biol Chem 276: 6337-6342
21. Kuo AJ, Song J, Cheung P, Ishibe-Murakami S, Yamazoe S, Chen JK, Patel DJ, Gozani O. 2012. The BAH domain of ORC1 links H4K20me2 to DNA replication licensing and Meier-Gorlin syndrome. Nature 484: 115-119.
22. Lacey KR, Jackson PK, Stearns T. 1999. Cyclin-dependent kinase control of centrosome duplication. Proc Natl Acad Sci 96: 2817-2822
23. Malecki MJ, Sanchez-Irizarry C, Mitchell JL, Histen G, Xu ML Aster JC, Blacklow SC. 2006. Leukemia-associated mutations within the NOTCH1 heterodimerization domain fall into at least two distinct mechanistic classes. Mol Cell Biol 26: 4642-4651
24. Mendez J, Zou-Yang XH, Kim SY, Hidaka M, Tansey WP Stillman B. 2002. Human origin recognition complex large subunit is degraded by ubiquitin-mediated proteolysis after initiation of DNA replication. Mol Cell 9: 481-491
25. Miyoshi K, Kasahara K, Miyazaki I, Shimizu S, Taniguchi M Matsuzaki S, Tohyama M, Asanuma M. 2009. Pericentrin, a centrosomal protein related to microcephalic primordial dwarfism, is required for olfactory cilia assembly in mice. FASEB J 23: 3289-3297.
26. Nigg EA, Stearns T. 2011. The centrosome cycle: Centriole biogenesis, duplication and inherent asymmetries. Nat Cell Biol 13: 1154-1160.
27. Nishimura T, Takahashi M, Kim HS, Mukai H, Ono Y. 2005. Centrosome-targeting region of CG-NAP causes centrosome amplification by recruiting cyclin E-cdk2 complex. Genes Cells 10: 75-86
28. Noguchi K, Vassilev A, Ghosh S, Yates JL, DePamphilis ML. 2006. The BAH domain facilitates the ability of human Orc1 protein to activate replication origins in vivo. EMBO J 25: 5372-5382.
29. Prasanth SG, Prasanth KV, Siddiqui K, Spector DL, Stillman B. 2004. Human Orc2 localizes to centrosomes, centromeres and heterochromatin during chromosome inheritance. EMBO J 23: 2651-2663
30. Rauch A, Thiel CT, Schindler D, Wick U, Crow YJ, Ekici AB, van Essen AJ, Goecke TO, Al-Gazali L, Chrzanowska KH, et al. 2008. Mutations in the pericentrin (PCNT) gene cause primordial dwarfism. Science 319: 816-819.
31. Salisbury JL, Suino KM, Busby R, Springett M. 2002. Centrin-2 is required for centriole duplication in mammalian cells. Curr Biol 12: 1287-1292.
32. Segel IH. 1975. Enzyme kinetics: Behavior and analysis of rapid equilibrium and steady state enzyme systems. Wiley, New York.
33. Siddiqui K, Stillman B. 2007. ATP-dependent assembly of the human origin recognition complex. J Biol Chem 282: 32370-32383.
34. Sir JH, Barr AR, Nicholas AK, Carvalho OP, Khurshid M, Sossick A, Reichelt S, D'Santos C, Woods CG, Gergely F. 2011. A primary microcephaly protein complex forms a ring around parental centrioles. Nat Genet 43: 1147-1153.
35. Stearns T, Evans L, Kirschner M. 1991. g-Tubulin is a highly conserved component of the centrosome. Cell 65: 825-836.
36. Stillman B. 2005. Origin recognition and the chromosome cycle. FEBS Lett 579: 877-884
37. Stoeber K, Mills AD, Kubota Y, Krude T, Romanowski P Marheineke K, Laskey RA, Williams GH. 1998. Cdc6 protein causes premature entry into S phase in a mammalian cellfree system. EMBO J 17: 7219-7229
38. Strnad P, Leidel S, Vinogradova T, Euteneuer U, Khodjakov A Gonczy P. 2007. Regulated HsSAS-6 levels ensure formation of a single procentriole per centriole during the centrosome duplication cycle. Dev Cell 13: 203-213
39. Stuermer A, Hoehn K, Faul T, Auth T, Brand N, Kneissl M Putter V, Grummt F. 2007. Mouse pre-replicative complex proteins colocalise and interact with the centrosome. Eur J Cell Biol 86: 37-50.
40. Tachibana KE, Nigg EA. 2006. Geminin regulates multiple steps of the chromosome inheritance cycle. Cell Cycle 5: 151-154
41. Tang CJ, Lin SY, Hsu WB, Lin YN, Wu CT, Lin YC, Chang CW Wu KS, Tang TK. 2011. The human microcephaly protein STIL interacts with CPAP and is required for procentriole formation. EMBO J 30: 4790-4804.
42. Thornton GK, Woods CG. 2009. Primary microcephaly: Do all roads lead to Rome? Trends Genet 25: 501-510.
43. Tsou MF, Stearns T. 2006. Controlling centrosome number: Licenses and blocks. Curr Opin Cell Biol 18: 74-78
44. Vermeulen M, Eberl HC, Matarese F, Marks H, Denissov S, Butter F, Lee KK, Olsen JV, Hyman AA, Stunnenberg HG, et al. 2010. Quantitative interaction proteomics and genomewide profiling of epigenetic histone marks and their readers. Cell 142: 967-980.
45. Wong C, Stearns T. 2003. Centrosome number is controlled by a centrosome-intrinsic block to reduplication. Nat Cell Biol 5: 539-544.
46. Zhang Z, Hayashi MK, Merkel O, Stillman B, Xu RM. 2002. Structure and function of the BAH-containing domain of Orc1p in epigenetic silencing. EMBO J 21: 4600-4611