Condensin II mutation causes T-cell lymphoma through tissue-specific genome instability

Genes and Development

Volumn 30, Issue 19, 2016, Pages 2173-2186

  Woodward, Jessica ^a   Taylor, Gillian C ^a   Soares, Dinesh C ^a,b   Boyle, Shelagh ^a   Sie, Daoud ^c   Read, David ^a   Chathoth, Keerthi ^a   Vukovic, Milica ^d   Tarrats, Nuria ^b   Jamieson, David ^e   Campbell, Kirsteen J ^f   Blyth, Karen ^f   Acosta, Juan Carlos ^b   Ylstra, Bauke ^c   Arends, Mark J ^b   Kranc, Kamil R ^b,d   Jackson, Andrew P ^a   Bickmore, Wendy A ^a   Wood, Andrew J ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c VU UNIVERSITY MEDICAL CENTER   (Netherlands)

^d UNIVERSITY OF EDINBURGH   (United Kingdom)

^e NEWCASTLE UNIVERSITY   (United Kingdom)

^f BEATSON INSTITUTE FOR CANCER RESEARCH   (United Kingdom)

Author keywords

Chromosome structure; Condensin; Genome instability; Lymphoma; Mitosis

Indexed keywords

CONDENSIN; CONDENSIN II; PROTEIN P53; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATASE; DNA BINDING PROTEIN; MULTIPROTEIN COMPLEX;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL MUTANT; CELLS BY BODY ANATOMY; CHROMOSOME CONDENSATION; CHROMOSOME SEGREGATION; CHROMOSOME STRUCTURE; CONTROLLED STUDY; DAUGHTER CELL; DIPLOIDY; DNA DAMAGE; GENE DELETION; GENE REARRANGEMENT; GENE SEQUENCE; GENOMIC INSTABILITY; HEMATOPOIETIC CELL; MISSENSE MUTATION; MOUSE; NONHUMAN; PLOIDY; PRIORITY JOURNAL; T CELL LYMPHOMA; TISSUE SPECIFICITY; TUMOR SUPPRESSOR GENE; YOUNG ADULT; ANAPHASE; ANIMAL; CELL CULTURE; FEMALE; GENETICS; MALE; METABOLISM; METAPHASE; PATHOLOGY; PATHOPHYSIOLOGY; THYMOCYTE; THYMOMA;

ADENOSINE TRIPHOSPHATASES; ANAPHASE; ANIMALS; CELLS, CULTURED; CHROMOSOME STRUCTURES; DNA-BINDING PROTEINS; FEMALE; GENOMIC INSTABILITY; LYMPHOMA, T-CELL; MALE; METAPHASE; MICE; MULTIPROTEIN COMPLEXES; MUTATION, MISSENSE; THYMOCYTES; THYMUS NEOPLASMS;

EID: 84992146705     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.284562.116     Document Type: Article

References (61)

1. Ahmad S, Gromiha M, Fawareh H, Sarai A. 2004. ASAView: database and tool for solvent accessibility representation in proteins. BMC Bioinformatics 5: 51.
2. Boyle S, Rodesch MJ, Halvensleben HA, Jeddeloh JA, Bickmore WA. 2011. Fluorescence in situ hybridization with high-complexity repeat-free oligonucleotide probes generated by massively parallel synthesis. Chromosome Res 19: 901–909.
3. Brekelmans P, van Soest P, Voerman J, Platenburg PP, Leenen PJM, van Ewijk W. 1994. Transferrin receptor expression as a marker of immature cycling thymocytes in the mouse. Cell Immunol 159: 331–339.
4. Bürmann F, Shin H-C, Basquin J, Soh Y-M, Giménez-Oya V, Kim Y-G, Oh B-H, Gruber S. 2013. An asymmetric SMC–kleisin bridge in prokaryotic condensin. Nat Struct Mol Biol 20: 371–379.
5. Carlson CS, Emerson RO, Sherwood AM, Desmarais C, Chung M-W, Parsons JM, Steen MS, LaMadrid-Herrmannsfeldt MA, Williamson DW, Livingston RJ, et al. 2013. Using synthetic templates to design an unbiased multiplex PCR assay. Nat Commun 4: 2680.
6. Combet C. 2000. NPS@: network protein sequence analysis. Trends Biochem Sci 25: 147–150.
7. Coschi CH, Martens AL, Ritchie K, Francis SM, Chakrabarti S, Berube NG, Dick FA. 2010. Mitotic chromosome condensation mediated by the retinoblastoma protein is tumor-suppressive. Genes Dev 24: 1351–1363.
8. Coschi CH, Ishak CA, Gallo D, Marshall A, Talluri S, Wang J, Cecchini MJ, Martens AL, Percy V, Welch I, et al. 2014. Haploinsufficiency of an RB–E2F1–condensin II complex leads to aberrant replication and aneuploidy. Cancer Discov 4: 840–853.
9. Cuylen S, Metz J, Haering CH. 2011. Condensin structures chromosomal DNA through topological links. Nat Struct Mol Biol 18: 894–901.
10. de Pooter R, Zúñiga-Pflücker JC. 2007. T-cell potential and development in vitro: the OP9-DL1 approach. Curr Opin Immunol 19: 163–168.
11. Derrien T, Estellé J, Marco Sola S, Knowles DG, Raineri E, Guigo R, Ribeca P. 2012. Fast computation and applications of genome mappability. PLoS One 7: e30377.
12. Donehower LA, Harvey M, Slagle BL, McArthur MJ, Montgomery CA, Butel JS, Bradley A. 1992. Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours. Nature 356: 215–221.
13. Dudgeon C, Chan C, Kang W, Sun Y, Emerson R, Robins H, Levine AJ. 2014. The evolution of thymic lymphomas in p53 knockout mice. Genes Dev 28: 2613–2620.
14. Eskeland R, Leeb M, Grimes GR, Kress C, Boyle S, Sproul D, Gilbert N, Fan Y, Skoultchi AI, Wutz A. 2010. Ring1B compacts chromatin structure and represses gene expression independent of histone ubiquitination. Mol Cell 38: 452–464.
15. Fujiwara T, Bandi M, Nitta M, Ivanova EV, Bronson RT, Pellman D. 2005. Cytokinesis failure generating tetraploids promotes tumorigenesis in p53-null cells. Nature 437: 1043–1047.
16. Gnerre S, Maccallum I, Przybylski D, Ribeiro FJ, Burton JN, Walker BJ, Sharpe T, Hall G, Shea TP, Sykes S, et al. 2011. High-quality draft assemblies of mammalian genomes from massively parallel sequence data. Proc Natl Acad Sci 108: 1513–1518.
17. Gosling KM, Makaroff LE, Theodoratos A, Kim Y-H, Whittle B, Rui L, Wu H, Hong NA, Kennedy GC, Fritz J-A, et al. 2007. A mutation in a chromosome condensin II subunit, kleisin β, specifically disrupts T cell development. Proc Natl Acad Sci 104: 12445–12450.
18. Gouet P, Robert X, Courcelle E. 2003. ESPript/ENDscript: extracting and rendering sequence and 3D information from atomic structures of proteins. Nucleic Acids Res 31: 3320–3323.
19. Green LC, Kalitsis P, Chang TM, Cipetic M, Kim JH, Marshall O, Turnbull L, Whitchurch CB, Vagnarelli P, Samejima K, et al. 2012. Contrasting roles of condensin I and condensin II in mitotic chromosome formation. J Cell Sci 125: 1591–1604.
20. Gruber S, Haering CH, Nasmyth K. 2003. Chromosomal cohesin forms a ring. Cell 112: 765–777.
21. Gutierrez A, Kentsis A, Sanda T, Holmfeldt L, Chen S-C, Zhang J, Protopopov A, Chin L, Dahlberg SE, Neuberg DS, et al. 2011. The BCL11B tumor suppressor is mutated across the major molecular subtypes of T-cell acute lymphoblastic leukemia. Blood 118: 4169–4173.
22. Ham MF, Takakuwa T, Rahadiani N, Tresnasari K, Nakajima H, Aozasa K. 2007. Condensin mutations and abnormal chromosomal structures in pyothorax-associated lymphoma. Cancer Sci 98: 1041–1047.
23. Hardy RR, Carmack CE, Shinton SA, Kemp JD, Hayakawa K. 1991. Resolution and characterization of pro-B and pre-pro-B cell stages in normal mouse bone marrow. J Exp Med 173: 1213–1225.
24. Hirano T. 2012. Condensins: universal organizers of chromosomes with diverse functions. Genes Dev 26: 1659–1678.
25. Hirota T, Gerlich D, Koch B, Ellenberg J, Peters J-M. 2004. Distinct functions of condensin I and II in mitotic chromosome assembly. J Cell Sci 117: 6435–6445.
26. Houlard M, Godwin J, Metson J, Lee J, Hirano T, Nasmyth K. 2015. Condensin confers the longitudinal rigidity of chromosomes. Nat Cell Biol 17: 771–781.
27. Jacks T, Remington L, Williams BO, Schmitt EM, Halachmi S, Bronson RT, Weinberg RA. 1994. Tumor spectrum analysis in p53-mutant mice. Curr Biol 4: 1–7.
28. Kamada K, Miyata M, Hirano T. 2013. Molecular basis of SMC ATPase activation: role of internal structural changes of the regulatory subcomplex ScpAB. Structure 21: 581–594.
29. Kastan MB, Onyekwere O, Sidransky D, Vogelstein B, Craig RW. 1991. Participation of p53 protein in the cellular response to DNA damage. Cancer Res 51: 6304–6311.
30. Kataoka K, Nagata Y, Kitanaka A, Shiraishi Y, Shimamura T, Yasunaga J-I, Totoki Y, Chiba K, Sato-Otsubo A, Nagae G, et al. 2015. Integrated molecular analysis of adult T cell leukemia/lymphoma. Nat Genet 47: 1304–1315.
31. Leiserson MDM, Vandin F, Wu H-T, Dobson JR, Eldridge JV, Thomas JL, Papoutsaki A, Kim Y, Niu B, McLellan M, et al. 2015. Pan-cancer network analysis identifies combinations of rare somatic mutations across pathways and protein complexes. Nat Genet 47: 106–114.
32. Longworth MS, Herr A, Ji JY, Dyson NJ. 2008. RBF1 promotes chromatin condensation through a conserved interaction with the Condensin II protein dCAP-D3. Genes Dev 22: 1011–1024.
33. Losada A, Hirano T. 2005. Dynamic molecular linkers of the genome: the first decade of SMC proteins. Genes Dev 19: 1269–1287.
34. Lowe SW, Schmitt EM, Smith SW, Osborne BA, Jacks T. 1993. p53 is required for radiation-induced apoptosis in mouse thymocytes. Nature:: 362: 847–849.
35. Manning AL, Longworth MS, Dyson NJ. 2010. Loss of pRB causes centromere dysfunction and chromosomal instability. Genes Dev 24: 1364–1376.
36. Martin C-A, Murray JE, Carroll P, Leitch A, Mackenzie KJ, Halachev M, Fetit AE, Keith C, Bicknell LS, Fluteau A, et al. 2016. Mutations in genes encoding condensin complex proteins cause microcephaly through decatenation failure at mitosis. Genes Dev (this issue). doi: 10.1101/gad.286351.116.
37. Nasmyth K, Haering CH. 2005. The structure and function of SMC and kleisin complexes. Annu Rev Biochem 74: 595–648.
38. Nasmyth K, Oliveira RA. 2010. Splitting the nucleus what’s wrong with the tripartite ring model? Cold Spring Harb Symp Quant Biol 75: 375–388.
39. Nelms KA, Goodnow CC. 2001. Genome-wide ENU mutagenesis to reveal immune regulators. Immunity 15: 409–418.
40. Neumann B, Walter T, Hériché J-K, Bulkescher J, Erfle H, Conrad C, Rogers P, Poser I, Held M, Liebel U, et al. 2010. Phenotypic profiling of the human genome by time-lapse microscopy reveals cell division genes. Nature 464: 721–727.
41. Nishide K, Hirano T. 2014. Overlapping and non-overlapping functions of condensins I and II in neural stem cell divisions. PLoS Genet 10: e1004847.
42. Onn I, Aono N, Hirano M, Hirano T. 2007. Reconstitution and subunit geometry of human condensin complexes. EMBO J 26: 1024–1034.
43. Ono T, Losada A, Hirano M, Myers MP, Neuwald AF, Hirano T. 2003. Differential contributions of condensin I and condensin II to mitotic chromosome architecture in vertebrate cells. Cell 115: 109–121.
44. Ono T, Fang Y, Spector DL, Hirano T. 2004. Spatial and temporal regulation of condensins I and II in mitotic chromosome assembly in human cells. Mol Biol Cell 15: 3296–3308.
45. Parris CN, Adam Zahir S, Al-Ali H, Bourton EC, Plowman C, Plowman PN. 2015. Enhanced γ-H2AX DNA damage foci detection using multimagnification and extended depth of field in imaging flow cytometry. Cytometry A 87: 717–723.
46. Piazza I, Rutkowska A, Ori A, Walczak M, Metz J, Pelechano V, Beck M, Haering CH. 2014. Association of condensin with chromosomes depends on DNA binding by its HEAT-repeat subunits. Nat Struct Mol Biol 21: 560–568.
47. Rawlings JS, Gatzka M, Thomas PG, Ihle JN. 2010. Chromatin condensation via the condensin II complex is required for peripheral T-cell quiescence. EMBO J 30: 263–276.
48. Scheinin I, Sie D, Bengtsson H, van de Wiel MA, Olshen AB, van Thuijl HF, van Essen HF, Eijk PP, Rustenburg F, Meijer GA, et al. 2014. DNA copy number analysis of fresh and formalin-fixed specimens by shallow whole-genome sequencing with identification and exclusion of problematic regions in the genome assembly. Genome Res 24: 2022–2032.
49. Sheltzer JM, Torres EM, Dunham MJ, Amon A. 2012. Transcriptional consequences of aneuploidy. Proc Natl Acad Sci 109: 12644–12649.
50. Shintomi K, Hirano T. 2011. The relative ratio of condensin I to II determines chromosome shapes. Genes Dev 25: 1464–1469.
51. Smith ED, Xu Y, Tomson BN, Leung CG, Fujiwara Y, Orkin SH, Crispino JD. 2004. More than blood, a novel gene required for mammalian postimplantation development. Mol Cell Biol 24: 1168–1173.
52. Söding J, Biegert A, Lupas AN. 2005. The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res 33: W244–W248.
53. Swedlow JR, Hirano T. 2003. The making of the mitotic chromosome: modern insights into classical questions. Mol Cell 11: 557–569.
54. Thompson SL, Compton DA. 2010. Proliferation of aneuploid human cells is limited by a p53-dependent mechanism. J Cell Biol 188: 369–381.
55. Tina KG, Bhadra R, Srinivasan N. 2007. PIC: protein interactions calculator. Nucleic Acids Res 35: W473–W476.
56. Torres EM, Sokolsky T, Tucker CM, Chan LY, Boselli M, Dunham MJ, Amon A. 2007. Effects of aneuploidy on cellular physiology and cell division in haploid yeast. Science 317: 916–924.
57. van Thuijl HF, Scheinin I, Sie D, Alentorn A, van Essen HF, Cordes M, Fleischeuer R, Gijtenbeek AM, Beute G, van den Brink WA, et al. 2014. Spatial and temporal evolution of distal 10q deletion, a prognostically unfavorable event in diffuse low-grade gliomas. Genome Biol 15: 471.
58. Venkatraman ES, Olshen AB. 2007. A faster circular binary segmentation algorithm for the analysis of array CGH data. Bioinformatics 23: 657–663.
59. Williams BR, Prabhu VR, Hunter KE, Glazier CM, Whittaker CA, Housman DE, Amon A. 2008. Aneuploidy affects proliferation and spontaneous immortalization in mammalian cells. Science 322: 703–709.
60. Wood AJ, Severson AF, Meyer BJ. 2010. Condensin and cohesin complexity: the expanding repertoire of functions. Nat Rev Genet 11: 391–404.
61. Zhang J, Ding L, Holmfeldt L, Wu G, Heatley SL, Payne-Turner D, Easton J, Chen X, Wang J, Rusch M, et al. 2012. The genetic basis of early T-cell precursor acute lymphoblastic leukaemia. Nature 481: 157–163.