A novel cell response triggered by interphase centromere structural instability

Journal of Cell Biology

Volumn 177, Issue 5, 2007, Pages 757-768

  Morency, Eric ^a,b   Sabra, Mirna ^a,b   Catez, Frédéric ^a,b   Texier, Pascale ^a,b   Lomonte, Patrick ^a,b  

^a UNIVERSITÉ LYON 1   (France)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; CENTROMERE PROTEIN B; COILIN; FIBRILLARIN; PROTEIN; SURVIVAL MOTOR NEURON PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CENTROMERE; CHROMOSOME DAMAGE; CHROMOSOME STRUCTURE; COILED BODY; CONTROLLED STUDY; EMBRYO; HERPES SIMPLEX VIRUS 1; HUMAN; HUMAN CELL; INTERPHASE; MICROTUBULE; MITOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION;

ANIMALS; CELLS, CULTURED; CENTROMERE; CENTROMERE PROTEIN B; CHROMOSOMAL PROTEINS, NON-HISTONE; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DNA BREAKS; DNA, SATELLITE; HERPESVIRUS 1, HUMAN; HUMANS; IMMEDIATE-EARLY PROTEINS; INTERPHASE; KINETOCHORES; MICE; NERVE TISSUE PROTEINS; NUCLEAR PROTEINS; RNA INTERFERENCE; RNA-BINDING PROTEINS; UBIQUITIN-PROTEIN LIGASES;

HUMAN HERPESVIRUS 1;

EID: 34249869815     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200612107     Document Type: Article

References (60)

1. Alexandrov, I.A., L.I. Medvedev, T.D. Mashkova, L.L. Kisselev, L.Y. Romanova, and Y.B. Yurov. 1993. Definition of a new alpha satellite suprachromosomal family characterized by monomeric organization. Nucleic Acids Res. 21:2209-2215.
2. Barcaroli, D., D. Dinsdale, M.H. Neale, L. Bongiorno-Borbone, M. Ranalli, E. Munarriz, A.E. Sayan, J.M. McWilliam, T.M. Smith, E. Fava, et al. 2006. FLASH is an essential component of Cajal bodies. Proc. Natl. Acad. Sci. USA. 103:14802-14807.
3. Bharadwaj, R., and H. Yu. 2004. The spindle checkpoint, aneuploidy, and cancer. Oncogene. 23:2016-2027.
4. Blower, M.D., B.A. Sullivan, and G.H. Karpen. 2002. Conserved organization of centromeric chromatin in flies and humans. Dev. Cell. 2:319-330.
5. Blower, M.D., T. Daigle, T. Kaufman, and G.H. Karpen. 2006. Drosophila CENP-A mutations cause a BubR1-dependent early mitotic delay without normal localization of kinetochore components. PLoS Genet. 2:e110.
6. Bouzinba-Segard, H., A. Guais, and C. Francastel. 2006. Accumulation of small murine minor satellite transcripts leads to impaired centromeric architecture and function. Proc. Natl. Acad. Sci. USA. 103:8709-8714.
7. Cioce, M., and A.I. Lamond. 2005. Cajal bodies: a long history of discovery. Annu. Rev. Cell Dev. Biol. 21:105-131.
8. Cioce, M., S. Boulon, A.G. Matera, and A.I. Lamond. 2006. UV-induced fragmentation of Cajal bodies. J. Cell Biol. 175:401-413.
9. Cleveland, D.W., Y. Mao, and K.F. Sullivan. 2003. Centromeres and kinetochores: from epigenetics to mitotic checkpoint signaling. Cell. 112:407-421.
10. Collier, S., A. Pendle, K. Boudonck, T. van Rij, L. Dolan, and P. Shaw. 2006. A distant coilin homologue is required for the formation of cajal bodies in Arabidopsis. Mol. Biol. Cell. 17:2942-2951.
11. Everett, R.D. 1989. Construction and characterization of herpes simplex virus type 1 mutants with defined lesions in immediate early gene 1. J. Gen. Virol. 70:1185-1202.
12. Everett, R.D., A. Cross, and A. Orr. 1993. A truncated form of herpes simplex virus type 1 immediate-early protein Vmw110 is expressed in a cell type dependent manner. Virology. 197:751-756.
13. Everett, R.D., P. Freemont, H. Saitoh, M. Dasso, A. Orr, M. Kathoria, and J. Parkinson. 1998. The disruption of ND10 during herpes simplex virus infection correlates with the Vmw110- and proteasome-dependent loss of several PML isoforms. J. Virol. 72:6581-6591.
14. Everett, R.D., W.C. Earnshaw, J. Findlay, and P. Lomonte. 1999a. Specific destruction of kinetochore protein CENP-C and disruption of cell division by herpes simplex virus immediate-early protein Vmw110. EMBO J. 18:1526-1538.
15. Everett, R.D., W.C. Earnshaw, A.F. Pluta, T. Sternsdorf, A.M. Ainsztein, M. Carmena, S. Ruchaud, W.L. Hsu, and A. Orr. 1999b. A dynamic connection between centromeres and ND10 proteins. J. Cell Sci. 112:3443-3454.
16. Foltz, D.R., L.E. Jansen, B.E. Black, A.O. Bailey, J.R. Yates III, and D.W. Cleveland. 2006. The human CENP-A centromeric nucleosome-associated complex. Nat. Cell Biol. 8:458-469.
17. Fukagawa, T., M. Nogami, M. Yoshikawa, M. Ikeno, T. Okazaki, Y. Takami, T. Nakayama, and M. Oshimura. 2004. Dicer is essential for formation of the heterochromatin structure in vertebrate cells. Nat. Cell Biol. 6:784-791.
18. Gall, J.G. 2001. A role for Cajal bodies in assembly of the nuclear transcription machinery. FEBS Lett. 498:164-167.
19. Gall, J.G. 2003. The centennial of the Cajal body. Nat. Rev. Mol. Cell Biol. 4:975-980.
20. Guenatri, M., D. Bailly, C. Maison, and G. Almouzni. 2004. Mouse centric and pericentric satellite repeats form distinct functional heterochromatin. J. Cell Biol. 166:493-505.
21. Hagglund, R., and B. Roizman. 2004. Role of ICP0 in the strategy of conquest of the host cell by herpes simplex virus 1. J. Virol. 78:2169-2178.
22. Hebert, M.D., and A.G. Matera. 2000. Self-association of coilin reveals a common theme in nuclear body localization. Mol. Biol. Cell. 11:4159-4171.
23. Hudson, D.F., K.J. Fowler, E. Earle, R. Saffery, P. Kalitsis, H. Trowell, J. Hill, N.G. Wreford, D.M. de Kretser, M.R. Cancilla, et al. 1998. Centromere protein B null mice are mitotically and meiotically normal but have lower body and testis weights. J. Cell Biol. 141:309-319.
24. Jallepalli, P.V., and C. Lengauer. 2001. Chromosome segregation and cancer: cutting through the mystery. Nat. Rev. Cancer. 1:109-117.
25. Kapoor, M., R. Montes de Oca Luna, G. Liu, G. Lozano, C. Cummings, M. Mancini, I. Ouspenski, B.R. Brinkley, and G.S. May. 1998. The cenpB gene is not essential in mice. Chromosoma. 107:570-576.
26. Lefebvre, S., L. Burglen, S. Reboullet, O. Clermont, P. Burlet, L. Viollet, B. Benichou, C. Cruaud, P. Millasseau, M. Zeviani, et al. 1995. Identification and characterization of a spinal muscular atrophy-determining gene. Cell. 80:155-165.
27. Liu, Q., and G. Dreyfuss. 1996. A novel nuclear structure containing the survival of motor neurons protein. EMBO J. 15:3555-3565.
28. Lomonte, P., and R.D. Everett. 1999. Herpes simplex virus type 1 immediate-early protein Vmw110 inhibits progression of cells through mitosis and from G(1) into S phase of the cell cycle. J. Virol. 73:9456-9467.
29. Lomonte, P., and E. Morency. 2007. Centromeric protein CENP-B proteasomal degradation induced by the viral protein ICP0. FEBS Lett. 581:658-662.
30. Lomonte, P., K.F. Sullivan, and R.D. Everett. 2001. Degradation of nucleosome-associated centromeric histone H3-like protein CENP-A induced by herpes simplex virus type 1 protein ICP0. J. Biol. Chem. 276:5829-5835.
31. Lomonte, P., J. Thomas, P. Texier, C. Caron, S. Khochbin, and A.L. Epstein. 2004. Functional interaction between class II histone deacetylases and ICP0 of herpes simplex virus type1. J. Virol. 78:6744-6757.
32. Luciani, J.J., D. Depetris, Y. Usson, C. Metzler-Guillemain, C. Mignon-Ravix, M.J. Mitchell, A. Megarbane, P. Sarda, H. Sirma, A. Moncla, et al. 2006. PML nuclear bodies are highly organised DNA-protein structures with a function in heterochromatin remodelling at the G2 phase. J. Cell Sci. 119:2518-2531.
33. Maison, C., D. Bailly, A.H. Peters, J.P. Quivy, D. Roche, A. Taddei, M. Lachner, T. Jenuwein, and G. Almouzni. 2002. Higher-order structure in pericentric heterochromatin involves a distinct pattern of histone modification and an RNA component. Nat. Genet. 30:329-334.
34. Matera, A.G., and M.R. Frey. 1998. Coiled bodies and gems: Janus or gemini? Am. J. Hum. Genet. 63:317-321.
35. Matera, A.G., and K.B. Shpargel. 2006. Pumping RNA: nuclear bodybuilding along the RNP pipeline. Curr. Opin. Cell Biol. 18:317-324.
36. Morency, E., Y. Coute, J. Thomas, P. Texier, and P. Lomonte. 2005. The protein ICP0 of herpes simplex virus type 1 is targeted to nucleoli of infected cells. Brief report. Arch. Virol. 150:2387-2395.
37. Newton, K., E. Petfalski, D. Tollervey, and J.F. Caceres. 2003. Fibrillarin is essential for early development and required for accumulation of an intron-encoded small nucleolar RNA in the mouse. Mol. Cell. Biol. 23:8519-8527.
38. Ohzeki, J., M. Nakano, T. Okada, and H. Masumoto. 2002. CENP-B box is required for de novo centromere chromatin assembly on human alphoid DNA. J. Cell Biol. 159:765-775.
39. Okada, M., I.M. Cheeseman, T. Hori, K. Okawa, I.X. McLeod, J.R. Yates III, A. Desai, and T. Fukagawa. 2006. The CENP-H-I complex is required for the efficient incorporation of newly synthesized CENP-A into centromeres. Nat. Cell Biol. 8:446-457.
40. Omer, A.D., S. Ziesche, H. Ebhardt, and P.P. Dennis. 2002. In vitro reconstitution and activity of a C/D box methylation guide ribonucleoprotein complex. Proc. Natl. Acad. Sci. USA. 99:5289-5294.
41. Parkinson, J., S.P. Lees-Miller, and R.D. Everett. 1999. Herpes simplex virus type 1 immediate-early protein vmw110 induces the proteasome-dependent degradation of the catalytic subunit of DNA-dependent protein kinase. J. Virol. 73:650-657.
42. Perez-Castro, A.V., F.L. Shamanski, J.J. Meneses, T.L. Lovato, K.G. Vogel, R.K. Moyzis, and R. Pedersen. 1998. Centromeric protein B null mice are viable with no apparent abnormalities. Dev. Biol. 201:135-143.
43. Pidoux, A.L., and R.C. Allshire. 2005. The role of heterochromatin in centromere function. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 360:569-579.
44. Pietras, D.F., K.L. Bennett, L.D. Siracusa, M. Woodworth-Gutai, V.M. Chapman, K.W. Gross, C. Kane-Haas, and N.D. Hastie. 1983. Construction of a small Mus musculus repetitive DNA library: identification of a new satellite sequence in Mus musculus. Nucleic Acids Res. 11:6965-6983.
45. Raska, I., L.E. Andrade, R.L. Ochs, E.K. Chan, C.M. Chang, G. Roos, and E.M. Tan. 1991. Immunological and ultrastructural studies of the nuclear coiled body with autoimmune antibodies. Exp. Cell Res. 195:27-37.
46. Rieder, C.L., and H. Maiato. 2004. Stuck in division or passing through: what happens when cells cannot satisfy the spindle assembly checkpoint. Dev. Cell. 7:637-651.
47. Saffery, R., H. Sumer, S. Hassan, L.H. Wong, J.M. Craig, K. Todokoro, M. Anderson, A. Stafford, and K.H. Choo. 2003. Transcription within a functional human centromere. Mol. Cell. 12:509-516.
48. Schueler, M.G., and B.A. Sullivan. 2006. Structural and functional dynamics of human centromeric chromatin. Annu. Rev. Genomics Hum. Genet. 7:301-313.
49. Shpargel, K.B., J.K. Ospina, K.E. Tucker, A.G. Matera, and M.D. Hebert. 2003. Control of Cajal body number is mediated by the coilin C-terminus. J. Cell Sci. 116:303-312.
50. Solovei, I., A. Cavallo, L. Schermelleh, F. Jaunin, C. Scasselati, D. Cmarko, C. Cremer, S. Fakan, and T. Cremer. 2002. Spatial preservation of nuclear chromatin architecture during three-dimensional fluorescence in situ hybridization (3D-FISH). Exp. Cell Res. 276:10-23.
51. Stow, N.D., and E.C. Stow. 1986. Isolation and characterization of a herpes simplex virus type 1 mutant containing a deletion within the gene encoding the immediate early polypeptide Vmw110. J. Gen. Virol. 67:2571-2585.
52. Tanaka, Y., H. Tachiwana, K. Yoda, H. Masumoto, T. Okazaki, H. Kurumizaka, and S. Yokoyama. 2005. Human centromere protein B induces translational positioning of nucleosomes on alpha-satellite sequences. J. Biol. Chem. 280:41609-41618.
53. Topp, C.N., C.X. Zhong, and R.K. Dawe. 2004. Centromere-encoded RNAs are integral components of the maize kinetochore. Proc. Natl. Acad. Sci. USA. 101:15986-15991.
54. Tucker, K.E., L.K. Massello, L. Gao, T.J. Barber, M.D. Hebert, E.K. Chan, and A.G. Matera. 2000. Structure and characterization of the murine p80 coilin gene, Coil. J. Struct. Biol. 129:269-277.
55. Tucker, K.E., M.T. Berciano, E.Y. Jacobs, D.F. LePage, K.B. Shpargel, J.J. Rossire, E.K. Chan, M. Lafarga, R.A. Conlon, and A.G. Matera. 2001. Residual Cajal bodies in coilin knockout mice fail to recruit Sm snRNPs and SMN, the spinal muscular atrophy gene product. J. Cell Biol. 154:293-307.
56. Tuma, R.S., J.A. Stolk, and M.B. Roth. 1993. Identification and characterization of a sphere organelle protein. J. Cell Biol. 122:767-773.
57. Verdel, A., and D. Moazed. 2005. RNAi-directed assembly of heterochromatin in fission yeast. FEBS Lett. 579:5872-5878.
58. Wilk, S., W.E. Chen, and R.P. Magnusson. 2000. Properties of the nuclear proteasome activator PA28gamma (REGgamma). Arch. Biochem. Biophys. 383:265-271.
59. Yoda, K., S. Ando, A. Okuda, A. Kikuchi, and T. Okazaki. 1998. In vitro assembly of the CENP-B/alpha-satellite DNA/core histone complex: CENP-B causes nucleosome positioning. Genes Cells. 3:533-548.
60. Zhang, W., C. Yi, W. Bao, B. Liu, J. Cui, H. Yu, X. Cao, M. Gu, M. Liu, and Z. Cheng. 2005. The transcribed 165-bp CentO satellite is the major functional centromeric element in the wild rice species Oryza punctata. Plant Physiol. 139:306-315.