The role of meiotic cohesin REC8 in chromosome segregation in γ irradiation-induced endopolyploid tumour cells

Experimental Cell Research

Volumn 315, Issue 15, 2009, Pages 2593-2603

  Erenpreisa, Jekaterina ^a   S Cragg, Mark ^b   Salmina, Kristine ^a   Hausmann, Michael ^c   Scherthan, Harry ^d,e  

^a LATVIAN BIOMEDICAL RESEARCH AND STUDY CENTRE   (Latvia)

^b UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d UNIVERSITY OF ULM   (Germany)

^e MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

Author keywords

Chromosome segregation; Endopolyploidy; Irradiation; REC8; SGOL1; SGOL2; Tumour cells

Indexed keywords

BINDING PROTEIN; COHESIN; MICROTUBULE ASSOCIATED PROTEIN; NUCLEAR MITOTIC APPARATUS PROTEIN; PROTEIN P53; PROTEIN REC8; SHUGOSHIN LIKE 1 PROTEIN; SHUGOSHIN LIKE 2 PROTEIN; UNCLASSIFIED DRUG;

ANAPHASE; ARTICLE; CANCER CELL CULTURE; CELLULAR DISTRIBUTION; CENTROMERE; CENTROSOME; CHROMOSOME SEGREGATION; CONTROLLED STUDY; ENDOREDUPLICATION; GAMMA IRRADIATION; HELA CELL; HUMAN; HUMAN CELL; INTERPHASE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RADIATION CARCINOGENESIS;

EID: 67651020778     PISSN: 00144827     EISSN: 10902422     Source Type: Journal    
DOI: 10.1016/j.yexcr.2009.05.011     Document Type: Article

References (61)

1. Illidge T.M., Cragg M.S., Fringes B., Olive P., and Erenpreisa J.A. Polyploid giant cells provide a survival mechanism for p53 mutant cells after DNA damage. Cell Biol. Int. 24 (2000) 621-633
2. Vakifahmetoglu H., Olsson M., and Zhivotovsky B. Death through a tragedy: mitotic catastrophe. Cell Death Differ. 15 (2008) 1153-1162
3. Erenpreisa J., and Cragg M.S. Mitotic death: a mechanism of survival? A review. Cancer Cell Int. 1 (2001) 1
4. Rajaraman R., Guernsey D.L., Rajaraman M.M., and Rajaraman S.R. Stem cells, senescence, neosis and self-renewal in cancer. Cancer Cell Int. 6 (2006) 25
5. Puig P.E., Guilly M.N., Bouchot A., Droin N., Cathelin D., Bouyer F., Favier L., Ghiringhelli F., Kroemer G., Solary E., Martin F., and Chauffert B. Tumor cells can escape DNA-damaging cisplatin through DNA endoreduplication and reversible polyploidy. Cell Biol. Int. 32 (2008) 1031-1043
6. de la Hoz C., and Baroja A. Proliferative behaviour of high-ploidy cells in two murine tumour lines. J. Cell. Sci. 104 Pt 1 (1993) 31-36
7. Ianzini F., and Mackey M.A. Development of the large scale digital cell analysis system. Radiat. Prot. Dosimetry 99 (2002) 289-293
8. Ianzini F., Kosmacek E.A., Nelson E.S., Napoli E., Erenpreisa J., Kalejs M., and Mackey M.A. Activation of meiosis-specific genes is associated with depolyploidization of human tumor cells following radiation-induced mitotic catastrophe. Cancer Res. 69 (2009) 2296-2304
9. Prieur-Carrillo G., Chu K., Lindqvist J., and Dewey W.C. Computerized video time-lapse (CVTL) analysis of the fate of giant cells produced by X-irradiating EJ30 human bladder carcinoma cells. Radiat. Res. 159 (2003) 705-712
10. Sundaram M., Guernsey D.L., Rajaraman M.M., and Rajaraman R. Neosis: a novel type of cell division in cancer. Cancer Biol. Ther. 3 (2004) 207-218
11. Stewenius Y., Gorunova L., Jonson T., Larsson N., Hoglund M., Mandahl N., Mertens F., Mitelman F., and Gisselsson D. Structural and numerical chromosome changes in colon cancer develop through telomere-mediated anaphase bridges, not through mitotic multipolarity. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 5541-5546
12. C.A. Berger, Multiplication and reduction of somatic chromosome groups as a regular developmental process in the mosquito, Culex pipiens Carnegie. Institute. of. Washington. Publication. 496 (1938) 209-232.
13. Huskins C.L. Segregation and reduction in somatic tissues. J. Hered. 39 (1948) 311-325
14. Nagl W. Endopolyploidy in Differentiation and Evolution (1978), North-Holland, Amsterdam, New York
15. Afon'kin S.Y. Induced and spontaneous polyploidisation in large amebas. Int. Rev. Cytol. 115 (1989) 231-266
16. Storchova Z., and Pellman D. From polyploidy to aneuploidy, genome instability and cancer. Nat. Rev. Mol. Cell. Biol. 5 (2004) 45-54
17. Erenpreisa J., Kalejs M., and Cragg M.S. Mitotic catastrophe and endomitosis in tumour cells: an evolutionary key to a molecular solution. Cell Biol. Int. 29 (2005) 1012-1018
18. Wheatley D. Growing evidence of the repopulation of regressed tumours by the division of giant cells. Cell Biol. Int. 32 (2008) 1029-1030
19. Martin F., Puig P.E., Ghiringhelli F., and Chauffert B. DNA-damaged polyploid cancer cells can reverse to diploidy: an ordered, but little understood, process of genomic reduction [with reference to the previous comments of Forer (2008) and Wheatley (2008a and b)]. Cell Biol. Int. 33 (2009) 702-703
20. Erenpreisa J., and Cragg M.S. Cancer: a matter of life cycle?. Cell Biol. Int. 31 (2007) 1507-1510
21. Forer A. Ploidy and division in cancer and mosquito hind-gut cells. Cell Biol. Int. 33 253 (2009)
22. Comai L. The advantages and disadvantages of being polyploid. Nat. Rev. Genet. 6 (2005) 836-846
23. Cleveland L.R. The origin and evolution of meiosis. Science 105 (1947) 287-289
24. Mogie M. On the relationship between asexual reproduction and polyploidy. J. Theoret. Biol. 122 (1986) 493-496
25. Kondrashov A.S. The asexual ploidy cycle and the origin of sex. Nature 370 (1994) 213-216
26. Kalejs M., Ivanov A., Plakhins G., Cragg M.S., Emzinsh D., Illidge T.M., and Erenpreisa J. Upregulation of meiosis-specific genes in lymphoma cell lines following genotoxic insult and induction of mitotic catastrophe. BMC Cancer 6 (2006) 6
27. Nasmyth K. Disseminating the genome: joining, resolving, and separating sister chromatids during mitosis and meiosis. Annu. Rev. Genet. 35 (2001) 673-745
28. Eijpe M., Offenberg H., Jessberger R., Revenkova E., and Heyting C. Meiotic cohesin REC8 marks the axial elements of rat synaptonemal complexes before cohesins SMC1beta and SMC3. J. Cell Biol. 160 (2003) 657-670
29. Parisi S., McKay M.J., Molnar M., Thompson M.A., van der Spek P.J., van Drunen-Schoenmaker E., Kanaar R., Lehmann E., Hoeijmakers J.H., and Kohli J. Rec8p, a meiotic recombination and sister chromatid cohesion phosphoprotein of the Rad21p family conserved from fission yeast to humans. Mol. Cell. Biol. 19 (1999) 3515-3528
30. Klein F., Mahr P., Galova M., Buonomo S.B., Michaelis C., Nairz K., and Nasmyth K. A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis. Cell 98 (1999) 91-103
31. Watanabe Y., and Nurse P. Cohesin Rec8 is required for reductional chromosome segregation at meiosis. Nature 400 (1999) 461-464
32. Watanabe Y., and Kitajima T.S. Shugoshin protects cohesin complexes at centromeres. Philos. Trans. R. Soc. Lond., B. Biol. Sci. 360 (2005) 515-521
33. Xu H., Beasley M.D., Warren W.D., van der Horst G.T., and McKay M.J. Absence of mouse REC8 cohesin promotes synapsis of sister chromatids in meiosis. Dev. Cell. 8 (2005) 949-961
34. Kitajima T.S., Miyazaki Y., Yamamoto M., and Watanabe Y. Rec8 cleavage by separase is required for meiotic nuclear divisions in fission yeast. EMBO J. 22 (2003) 5643-5653
35. Brar G.A., Kiburz B.M., Zhang Y., Kim J.E., White F., and Amon A. Rec8 phosphorylation and recombination promote the step-wise loss of cohesins in meiosis. Nature 441 (2006) 532-536
36. Kitajima T.S., Sakuno T., Ishiguro K., Iemura S., Natsume T., Kawashima S.A., and Watanabe Y. Shugoshin collaborates with protein phosphatase 2A to protect cohesin. Nature 441 (2006) 46-52
37. Kiburz B.M., Reynolds D.B., Megee P.C., Marston A.L., Lee B.H., Lee T.I., Levine S.S., Young R.A., and Amon A. The core centromere and Sgo1 establish a 50-kb cohesin-protected domain around centromeres during meiosis I. Genes Dev. 19 (2005) 3017-3030
38. Lichten M. Meiotic recombination: breaking the genome to save it. Curr. Biol. 11 (2001) R253-R256
39. Sehorn M.G., and Sung P. Meiotic recombination: an affair of two recombinases. Cell Cycle 3 (2004) 1375-1377
40. Keeney S. Mechanism and control of meiotic recombination initiation. Curr. Top Dev. Biol. 52 (2001) 1-53
41. Erenpreisa J., Ivanov A., Wheatley S.P., Kosmacek E.A., Ianzini F., Anisimov A.P., Mackey M., Davis P.J., Plakhins G., and Illidge T.M. Endopolyploidy in irradiated p53-deficient tumour cell lines: persistence of cell division activity in giant cells expressing Aurora-B kinase. Cell Biol. Int. 32 (2008) 1044-1056
42. Erenpreisa J., Kalejs M., Ianzini F., Kosmacek E.A., Mackey M.A., Emzinsh D., Cragg M.S., Ivanov A., and Illidge T.M. Segregation of genomes in polyploid tumour cells following mitotic catastrophe. Cell Biol. Int. 29 (2005) 1005-1011
43. Ivanov A., Cragg M.S., Erenpreisa J., Emzinsh D., Lukman H., and Illidge T.M. Endopolyploid cells produced after severe genotoxic damage have the potential to repair DNA double strand breaks. J. Cell Sci. 116 (2003) 4095-4106
44. Tachibana K., Tanaka D., Isobe T., and Kishimoto T. c-Mos forces the mitotic cell cycle to undergo meiosis II to produce haploid gametes. Proc. Natl. Acad. Sci. U. S. A. 97 (2000) 14301-14306
45. Resnick T.D., Satinover D.L., MacIsaac F., Stukenberg P.T., Earnshaw W.C., Orr-Weaver T.L., and Carmena M. INCENP and Aurora B promote meiotic sister chromatid cohesion through localization of the Shugoshin MEI-S332 in Drosophila. Dev. Cell. 11 (2006) 57-68
46. Hauf S., Biswas A., Langegger M., Kawashima S.A., Tsukahara T., and Watanabe Y. Aurora controls sister kinetochore mono-orientation and homolog bi-orientation in meiosis-I. EMBO J. 26 (2007) 4475-4486
47. Kaitna S., Pasierbek P., Jantsch M., Loidl J., and Glotzer M. The aurora B kinase AIR-2 regulates kinetochores during mitosis and is required for separation of homologous chromosomes during meiosis. Curr. Biol. 12 (2002) 798-812
48. Petronczki M., Siomos M.F., and Nasmyth K. Un menage a quatre: the molecular biology of chromosome segregation in meiosis. Cell 112 (2003) 423-440
49. O'Connor P.M., Jackman J., Jondle D., Bhatia K., Magrath I., and Kohn K.W. Role of the p53 tumor suppressor gene in cell cycle arrest and radiosensitivity of Burkitt's lymphoma cell lines. Cancer Res. 53 (1993) 4776-4780
50. Amundson S.A., Xia F., Wolfson K., and Liber H.L. Different cytotoxic and mutagenic responses induced by X-rays in two human lymphoblastoid cell lines derived from a single donor. Mutat. Res. 286 (1993) 233-241
51. Gaglio T., Saredi A., and Compton D.A. NuMA is required for the organization of microtubules into aster-like mitotic arrays. J. Cell Biol. 131 (1995) 693-708
52. Kimura K., Wakamatsu A., Suzuki Y., Ota T., Nishikawa T., Yamashita R., Yamamoto J., Sekine M., Tsuritani K., Wakaguri H., Ishii S., Sugiyama T., Saito K., Isono Y., Irie R., Kushida N., Yoneyama T., Otsuka R., Kanda K., Yokoi T., Kondo H., Wagatsuma M., Murakawa K., Ishida S., Ishibashi T., Takahashi-Fujii A., Tanase T., Nagai K., Kikuchi H., Nakai K., Isogai T., and Sugano S. Diversification of transcriptional modulation: large-scale identification and characterization of putative alternative promoters of human genes. Genome Res. 16 (2006) 55-65
53. Ianzini F., and Mackey M.A. Delayed DNA damage associated with mitotic catastrophe following X-irradiation of HeLa S3 cells. Mutagenesis 13 (1998) 337-344
54. Selig S., Okumura K., Ward D.C., and Cedar H. Delineation of DNA replication time zones by fluorescence in situ hybridization. EMBO J. 11 (1992) 1217-1225
55. Carrier F., Smith M.L., Bae I., Kilpatrick K.E., Lansing T.J., Chen C.Y., Engelstein M., Friend S.H., Henner W.D., Gilmer M.B.T., Kastan M.B., and Fornace A.J.J. Characterization of human Gadd45, a p53-regulated protein. Proc. Natl. Acad. Sci. U. S. A. 269 (1994) 32672-32677
56. Walen K.H. Bipolar genome reductional division of human near-senescent, polyploid fibroblast cells. Cancer Genet. Cytogenet. 173 (2007) 43-50
57. Gregson H.C., Schmiesing J.A., Kim J.S., Kobayashi T., Zhou S., and Yokomori K. A potential role for human cohesin in mitotic spindle aster assembly. J. Biol. Chem. 276 (2001) 47575-47582
58. Wong R.W., and Blobel G. Cohesin subunit SMC1 associates with mitotic microtubules at the spindle pole. Proc. Natl. Acad. Sci. U. S. A. 105 (2008) 15441-15445
59. Wong R.W., Blobel G., and Coutavas E. Rae1 interaction with NuMA is required for bipolar spindle formation. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 19783-19787
60. Rogakou E.P., Boon C., Redon C., and Bonner W.M. Megabase chromatin domains involved in DNA double-strand breaks in vivo. J. Cell Biol. 146 (1999) 905-916
61. Monajembashi S., Rapp A., Schmitt E., Dittmar H., Greulich K.O., and Hausmann M. Spatial association of homologous pericentric regions in human lymphocyte nuclei during repair. Biophys. J. 88 (2005) 2309-2322