Chromosome mis-segregation and cytokinesis failure in trisomic human cells

eLife

Volumn 4, Issue MAY, 2015, Pages

  Nicholson, Joshua M ^a,b   Macedo, Joana C ^c,d,e   Mattingly, Aaron J ^a,g   Wangsa, Darawalee ^f   Camps, Jordi ^f,h   Lima, Vera ^e   Gomes, Ana M ^c   Dória, Sofia ^e   Ried, Thomas ^f   Logarinho, Elsa ^c,d,e   Cimini, Daniela ^a,b  

^a VIRGINIA POLYTECHNIC INSTITUTE AND STATE UNIVERSITY   (United States)

^b VIRGINIA BIOINFORMATICS INSTITUTE   (United States)

^c UNIVERSITY OF PORTO   (Portugal)

^d UNIVERSITY OF PORTO   (Portugal)

^e UNIVERSITY OF PORTO   (Portugal)

^f NATIONAL CANCER INSTITUTE   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

^h HOSPITAL CLÍNIC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

PEPTIDES AND PROTEINS; SPASTIN; PROTEIN; SPG20 PROTEIN, HUMAN;

ANEUPLOIDY; ARTICLE; CHROMOSOME 13; CHROMOSOME 7; CHROMOSOME SEGREGATION; COLORECTAL CANCER; CONFOCAL MICROSCOPY; CONTROLLED STUDY; COPY NUMBER VARIATION; CYTOKINESIS; FLUORESCENCE IMAGING; FLUORESCENCE IN SITU HYBRIDIZATION; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; METAPHASE; PHENOTYPE; PROTEIN LOCALIZATION; TIME-LAPSE VIDEO MICROSCOPY; TRISOMY; UPREGULATION; WESTERN BLOTTING; AMNION FLUID; CHEMISTRY; CHROMOSOMAL INSTABILITY; CHROMOSOME DISORDER; COLON; CYTOLOGY; EPITHELIUM CELL; FEMALE; FETUS; GENE EXPRESSION REGULATION; GENETICS; KARYOTYPING; METABOLISM; PATHOLOGY; PREGNANCY; PRIMARY CELL CULTURE; TUMOR CELL LINE;

AMNIOTIC FLUID; CELL LINE, TUMOR; CHROMOSOMAL INSTABILITY; CHROMOSOME DISORDERS; CHROMOSOME SEGREGATION; CHROMOSOMES, HUMAN, PAIR 13; CHROMOSOMES, HUMAN, PAIR 7; COLON; CYTOKINESIS; EPITHELIAL CELLS; FEMALE; FETUS; GENE EXPRESSION REGULATION; HUMANS; KARYOTYPING; PHENOTYPE; PREGNANCY; PRIMARY CELL CULTURE; PROTEINS; TRISOMY;

EID: 84930649727     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.05068     Document Type: Article

References (77)

1. Andreassen PR, Lohez OD, Lacroix FB, Margolis RL. 2001. Tetraploid state induces p53-dependent arrest of nontransformed mammalian cells in G1. Molecular Biology of the Cell 12:1315-1328. doi: 10.1091/mbc.12.5. 1315.
2. Bajorek M, Morita E, Skalicky JJ, Morham SG, Babst M, Sundquist WI. 2009. Biochemical analyses of human IST1 and its function in cytokinesis. Molecular Biology of the Cell 20:1360-1373. doi: 10.1091/mbc.E08-05-0475.
3. Bakhoum SF, Silkworth WT, Nardi IK, Nicholson JM, Compton DA, Cimini D. 2014. The mitotic origin of chromosomal instability. Current Biology 24:R148-R149. doi: 10.1016/j.cub.2014.01.019.
4. Bardi G, Fenger C, Johansson B, Mitelman F, Heim S. 2004. Tumor karyotype predicts clinical outcome in colorectal cancer patients. Journal of Clinical Oncology 22:2623-2634. doi: 10.1200/JCO.2004.11.014.
5. Biesecker LG, Spinner NB. 2013. A genomic view of mosaicism and human disease. Nature Reviews Genetics 14: 307-320. doi: 10.1038/nrg3424.
6. Biron-Shental T, Liberman M, Sharvit M, Sukenik-Halevy R, Amiel A. 2015. Amniocytes from aneuploidy embryos have enhanced random aneuploidy and signs of senescence - can these findings be related to medical problems? Gene 562:232-235. doi: 10.1016/j.gene.2015.02.075.
7. Boveri T. 1914. Zur frage der entstehung maligner tumoren. Jena, Germany: Gustav Fischer Verlag.
8. Boveri T. 2008. Concerning the origin of malignant tumours by Theodor Boveri. Translated and annotated by Henry Harris. Journal of Cell Science 121(Suppl 1):1-84. doi: 10.1242/jcs.025742.
9. Carere A, Antoccia A, Cimini D, Crebelli R, Degrassi F, Leopardi P, Marcon F, Sgura A, Tanzarella C, Zijno A. 1999. Analysis of chromosome loss and non-disjunction in cytokinesis-blocked lymphocytes of 24 male subjects. Mutagenesis 14:491-496. doi: 10.1093/mutage/14.5.491.
10. Carter SL, Eklund AC, Kohane IS, Harris LN, Szallasi Z. 2006. A signature of chromosomal instability inferred from gene expression profiles predicts clinical outcome in multiple human cancers. Nature Genetics 38:1043-1048. doi: 10.1038/ng1861.
11. Chen G, Mulla WA, Kucharavy A, Tsai HJ, Rubinstein B, Conkright J, McCroskey S, Bradford WD, Weems L, Haug JS, Seidel CW, Berman J, Li R. 2015. Targeting the adaptability of heterogeneous aneuploids. Cell 160:771-784. doi: 10.1016/j.cell.2015.01.026.
12. Cimini D, Howell B, Maddox P, Khodjakov A, Degrassi F, Salmon ED. 2001. Merotelic kinetochore orientation is a major mechanism of aneuploidy in mitotic mammalian tissue cells. The Journal of Cell Biology 153:517-527. doi: 10.1083/jcb.153.3.517.
13. Cremer M, Grasser F, Lanctot C, Muller S, Neusser M, Zinner R, Solovei I, Cremer T. 2008. Multicolor 3D fluorescence in situ hybridization for imaging interphase chromosomes. Methods in Molecular Biology 463: 205-239. doi: 10.1007/978-1-59745-406-3_15.
14. Dewhurst SM, McGranahan N, Burrell RA, Rowan AJ, Grönroos E, Endesfelder D, Joshi T, Mouradov D, Gibbs P Ward RL, Hawkins NJ, Szallasi Z, Sieber OM, Swanton C. 2014. Tolerance of whole-genome doubling propagates chromosomal instability and accelerates cancer genome evolution. Cancer Discovery 4:175-185. doi: 10.1158/ 2159-8290.CD-13-0285.
15. Duelli D, Lazebnik Y. 2003. Cell fusion: a hidden enemy? Cancer Cell 3:445-448. doi: 10.1016/S1535-6108(03)00114-4.
16. Duelli DM, Padilla-Nash HM, Berman D, Murphy KM, Ried T, Lazebnik Y. 2007. A virus causes cancer by inducing massive chromosomal instability through cell fusion. Current Biology 17:431-437. doi: 10.1016/j. cub.2007.01.049.
17. Duesberg P, Rausch C, Rasnick D, Hehlmann R. 1998. Genetic instability of cancer cells is proportional to their degree of aneuploidy. Proceedings of the National Academy of Sciences of USA 95:13692-13697. doi: 10.1073/ pnas.95.23.13692.
18. Duesberg PH. 2014. Does aneuploidy destabilize karyotypes automatically? Proceedings of the National Academy of Sciences of USA 111:E974. doi: 10.1073/pnas.1401413111.
19. Fenech M. 1993. The cytokinesis-block micronucleus technique: a detailed description of the method and its application to genotoxicity studies in human populations. Mutation Research 285:35-44. doi: 10.1016/0027-5107(93)90049-L.
20. Foijer F, Draviam VM, Sorger PK. 2008. Studying chromosome instability in the mouse. Biochimica et Biophysica Acta 1786:73-82. doi: 10.1016/j.bbcan.2008.07.004.
21. 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. doi: 10.1038/nature04217.
22. Ganem NJ, Godinho SA, Pellman D. 2009. A mechanism linking extra centrosomes to chromosomal instability. Nature 460:278-282. doi: 10.1038/nature08136.
23. Gao C, Furge K, Koeman J, Dykema K, Su Y, Cutler ML, Werts A, Haak P, Vande Woude GF. 2007. Chromosome instability, chromosome transcriptome, and clonal evolution of tumor cell populations. Proceedings of the National Academy of Sciences of USA 104:8995-9000. doi: 10.1073/pnas.0700631104.
24. Gemoll T, Habermann JK, Becker S, Szymczak S, Upender MB, Bruch HP, Hellman U, Ried T, Auer G, Jornvall H Roblick UJ. 2013. Chromosomal aneuploidy affects the global proteome equilibrium of colorectal cancer cells. Analytical Cellular Pathology 36:149-161. doi: 10.1155/2013/249054.
25. Gisselsson D. 2011. Intratumor diversity and clonal evolution in cancer-a skeptical standpoint. Advances in Cancer Research 112:1-9. doi: 10.1016/B978-0-12-387688-1.00001-6.
26. Godinho SA, Picone R, Burute M, Dagher R, Su Y, Leung CT, Polyak K, Brugge JS, Thery M, Pellman D. 2014. Oncogene-like induction of cellular invasion from centrosome amplification. Nature 510:167-171. doi: 10.1038/ nature13277.
27. Gordon DJ, Resio B, Pellman D. 2012. Causes and consequences of aneuploidy in cancer. Nature Reviews Genetics 13:189-203. doi: 10.1038/nrg3123.
28. Grinberg-Rashi H, Cytron S, Gelman-Kohan Z, Litmanovitch T, Avivi L. 2010. Replication timing aberrations and aneuploidy in peripheral blood lymphocytes of breast cancer patients. Neoplasia 12:668-674. doi: 10.1593/neo.10568.
29. Heng HH. 2014. Distinguishing constitutional and acquired nonclonal aneuploidy. Proceedings of the National Academy of Sciences of USA 111:E972. doi: 10.1073/pnas.1323636111.
30. Kost-Alimova M, Fedorova L, Yang Y, Klein G, Imreh S. 2004. Microcell-mediated chromosome transfer provides evidence that polysomy promotes structural instability in tumor cell chromosomes through asynchronous replication and breakage within late-replicating regions. Genes, Chromosomes & Cancer 40:316-324. doi: 10. 1002/gcc.20054.
31. Krzywicka-Racka A, Sluder G. 2011. Repeated cleavage failure does not establish centrosome amplification in untransformed human cells. The Journal of Cell Biology 194:199-207. doi: 10.1083/jcb.201101073
32. Lee AJ, Endesfelder D, Rowan AJ, Walther A, Birkbak NJ, Futreal PA, Downward J, Szallasi Z, Tomlinson IP, Howell M, Kschischo M, Swanton C. 2011. Chromosomal instability confers intrinsic Multidrug resistance. Cancer Research 71:1858-1870. doi: 10.1158/0008-5472.CAN-10-3604.
33. Lengauer C, Kinzler KW, Vogelstein B. 1997. Genetic instability in colorectal cancers. Nature 386:623-627. doi: 10. 1038/386623a0.
34. Leopardi P, Marcon F, Dobrowolny G, Zijno A, Crebelli R. 2002. Influence of donor age on vinblastine-induced chromosome malsegregation in cultured peripheral lymphocytes. Mutagenesis 17:83-88. doi: 10.1093/mutage/ 17.1.83.
35. Lind GE, Raiborg C, Danielsen SA, Rognum TO, Thiis-Evensen E, Hoff G, Nesbakken A, Stenmark H, Lothe RA. 2011. SPG20, a novel biomarker for early detection of colorectal cancer, encodes a regulator of cytokinesis. Oncogene 30:3967-3978. doi: 10.1038/onc.2011.109.
36. Mitelman F, Johansson B, Mertens F. 2014. Mitelman database of chromosome aberrations and gene fusions in cancer. http://cgap.nci.nih.gov/Chromosomes/Mitelman.
37. Miyazaki M, Furuya T, Shiraki A, Sato T, Oga A, Sasaki K. 1999. The relationship of DNA ploidy to chromosomal instability in primary human colorectal cancers. Cancer Research 59:5283-5285.
38. Nagaoka SI, Hassold TJ, Hunt PA. 2012. Human aneuploidy: mechanisms and new insights into an age-old problem. Nature Reviews Genetics 13:493-504. doi: 10.1038/nrg3245.
39. Nicholson JM, Cimini D. 2011. How mitotic errors contribute to karyotypic diversity in cancer. Advances in Cancer Research 112:43-75. doi: 10.1016/B978-0-12-387688-1.00003-X.
40. Nicholson JM, Cimini D. 2013. Cancer karyotypes: survival of the fittest. Frontiers in Oncology 3:148. doi: 10.3389/ fonc.2013.00148.
41. Nicholson JM, Cimini D. 2015. Link between aneuploidy and chromosome instability. International Review of Cell and Molecular Biology 315:299-317. doi: 10.1016/bs.ircmb.2014.11.002.
42. Nicholson JM, Duesberg P. 2009. On the karyotypic origin and evolution of cancer cells. Cancer Genetics and Cytogenetics 194:96-110. doi: 10.1016/j.cancergencyto.2009.06.008.
43. Normand G, King RW. 2010. Understanding cytokinesis failure. Advances in Experimental Medicine and Biology 676:27-55. doi: 10.1007/978-1-4419-6199-0_3.
44. Nowinski GP, Van Dyke DL, Tilley BC, Jacobsen G, Babu VR, Worsham MJ, Wilson GN, Weiss L. 1990. The frequency of aneuploidy in cultured lymphocytes is correlated with age and gender but not with reproductive history. American Journal of Human Genetics 46:1101-1111.
45. Panopoulos A, Pacios-Bras C, Choi J, Yenjerla M, Sussman MA, Fotedar R, Margolis RL. 2014. Failure of cell cleavage induces senescence in tetraploid primary cells. Molecular Biology of the Cell 25:3105-3118. doi: 10. 1091/mbc.E14-03-0844.
46. Pavelka N, Rancati G, Li R. 2010a. Dr Jekyll and Mr Hyde: role of aneuploidy in cellular adaptation and cancer. Current Opinion in Cell Biology 22:809-815. doi: 10.1016/j.ceb.2010.06.003.
47. Pavelka N, Rancati G, Zhu J, Bradford WD, Saraf A, Florens L, Sanderson BW, Hattem GL, Li R. 2010b. Aneuploidy confers quantitative proteome changes and phenotypic variation in budding yeast. Nature 468:321-325. doi: 10. 1038/nature09529.
48. Pollack JR, Sorlie T, Perou CM, Rees CA, Jeffrey SS, Lonning PE, Tibshirani R, Botstein D, Borresen-Dale AL, Brown PO. 2002. Microarray analysis reveals a major direct role of DNA copy number alteration in the transcriptional program of human breast tumors. Proceedings of the National Academy of Sciences of USA 99:12963-12968. doi: 10.1073/pnas.162471999.
49. Reish O, Brosh N, Gobazov R, Rosenblat M, Libman V, Mashevich M. 2006. Sporadic aneuploidy in PHAstimulated lymphocytes of Turner's syndrome patients. Chromosome Research 14:527-534. doi: 10.1007/ s10577-006-1050-9.
50. Reish O, Regev M, Kanesky A, Girafi S, Mashevich M. 2011. Sporadic aneuploidy in PHA-stimulated lymphocytes of trisomies 21, 18, and 13. Cytogenetic and Genome Research 133:184-189. doi: 10.1159/ 000323504.
51. Renvoise B, Parker RL, Yang D, Bakowska JC, Hurley JH, Blackstone C. 2010. SPG20 protein spartin is recruited to midbodies by ESCRT-III protein Ist1 and participates in cytokinesis. Molecular Biology of the Cell 21:3293-3303. doi: 10.1091/mbc.E09-10-0879.
52. Ried T, Hu Y, Difilippantonio MJ, Ghadimi BM, Grade M, Camps J. 2012. The consequences of chromosomal aneuploidy on the transcriptome of cancer cells. Biochimica et Biophysica Acta 1819:784-793. doi: 10.1016/j. bbagrm.2012.02.020.
53. Ried T, Knutzen R, Steinbeck R, Blegen H, Schrock E, Heselmeyer K, du Manoir S, Auer G. 1996. Comparative genomic hybridization reveals a specific pattern of chromosomal gains and losses during the genesis of colorectal tumors. Genes, Chromosomes & Cancer 15:234-245. doi: 10.1002/(SICI)1098-2264(199604)15:43.0. CO;2-2.
54. Rieder CL, Maiato H. 2004. Stuck in division or passing through; what happens when cells cannot satisfy the spindle assembly checkpoint. Developmental Cell 7:637-651. doi: 10.1016/j.devcel.2004.09.002.
55. Selmecki A, Forche A, Berman J. 2006. Aneuploidy and isochromosome formation in drug-resistant Candida albicans. Science 313:367-370. doi: 10.1126/science.1128242.
56. Selmecki AM, Dulmage K, Cowen LE, Anderson JB, Berman J. 2009. Acquisition of aneuploidy provides increased fitness during the evolution of antifungal drug resistance. PLOS Genetics 5:e1000705. doi: 10.1371/journal.pgen. 1000705.
57. Sheffer M, Bacolod MD, Zuk O, Giardina SF, Pincas H, Barany F, Paty PB, Gerald WL, Notterman DA, Domany E. 2009. Association of survival and disease progression with chromosomal instability: a genomic exploration of colorectal cancer. Proceedings of the National Academy of Sciences of USA 106:7131-7136. doi: 10.1073/pnas. 0902232106.
58. Sheltzer JM, Blank HM, Pfau SJ, Tange Y, George BM, Humpton TJ, Brito IL, Hiraoka Y, Niwa O, Amon A. 2011. Aneuploidy drives genomic instability in yeast. Science 333:1026-1030. doi: 10.1126/science.1206412.
59. Sheltzer JM, Torres EM, Dunham MJ, Amon A. 2012. Transcriptional consequences of aneuploidy. Proceedings of the National Academy of Sciences of USA 109:12644-12649. doi: 10.1073/pnas.1209227109.
60. Silkworth WT, Cimini D. 2012. Transient defects of mitotic spindle geometry and chromosome segregation errors. Cell Division 7:19. doi: 10.1186/1747-1028-7-19.
61. Silkworth WT, Nardi IK, Scholl LM, Cimini D. 2009. Multipolar spindle pole coalescence is a major source of kinetochore mis-attachment and chromosome mis-segregation in cancer cells. PLOS ONE 4:e6564. doi: 10.1371/ journal.pone.0006564.
62. Stingele S, Stoehr G, Peplowska K, Cox J, Mann M, Storchova Z. 2012. Global analysis of genome, transcriptome and proteome reveals the response to aneuploidy in human cells. Molecular Systems Biology 8:608. doi: 10.1038/ msb.2012.40.
63. Storchova Z, Pellman D. 2004. From polyploidy to aneuploidy, genome instability and cancer. Nature Reviews Molecular Cell Biology 5:45-54. doi: 10.1038/nrm1276.
64. Stukenberg PT. 2004. Triggering p53 after cytokinesis failure. The Journal of Cell Biology 165:607-608. doi: 10. 1083/jcb.200405089.
65. Suetake T, Hayashi F, Yokoyama S. 2009. Chain A, solution structure of the MIT domain from human Spartin. http:// www.ncbi.nlm.nih.gov/protein/159164182.
66. Thompson SL, Compton DA. 2008. Examining the link between chromosomal instability and aneuploidy in human cells. The Journal of Cell Biology 180:665-672. doi: 10.1083/jcb.200712029.
67. 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. doi: 10.1126/science. 1142210.
68. Uetake Y, Sluder G. 2004. Cell cycle progression after cleavage failure: mammalian somatic cells do not possess a 'tetraploidy checkpoint'. The Journal of Cell Biology 165:609-615. doi: 10.1083/jcb.200403014.
69. Upender MB, Habermann JK, McShane LM, Korn EL, Barrett JC, Difilippantonio MJ, Ried T. 2004. Chromosome transfer induced aneuploidy results in complex dysregulation of the cellular transcriptome in immortalized and cancer cells. Cancer Research 64:6941-6949. doi: 10.1158/0008-5472.CAN-04-0474.
70. Valind A, Gisselsson D. 2014a. Reply to Duesberg: stability of peritriploid and triploid states in neoplastic and nonneoplastic cells. Proceedings of the National Academy of Sciences of USA 111:E975. doi: 10.1073/pnas. 1402008111.
71. Valind A, Gisselsson D. 2014b. Reply to Heng: inborn aneuploidy and chromosomal instability. Proceedings of the National Academy of Sciences of USA 111:E973. doi: 10.1073/pnas.1323978111.
72. Valind A, Jin Y, Baldetorp B, Gisselsson D. 2013. Whole chromosome gain does not in itself confer cancer-like chromosomal instability. Proceedings of the National Academy of Sciences of USA 110:21119-21123. doi: 10. 1073/pnas.1311163110.
73. Walther A, Houlston R, Tomlinson I. 2008. Association between chromosomal instability and prognosis in colorectal cancer: a meta-analysis. Gut 57:941-950. doi: 10.1136/gut.2007.135004.
74. 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. doi: 10.1126/science. 1160058.
75. Wong C, Stearns T. 2005. Mammalian cells lack checkpoints for tetraploidy, aberrant centrosome number, and cytokinesis failure. BMC Cell Biology 6:6. doi: 10.1186/1471-2121-6-6.
76. Yang D, Rismanchi N, Renvoise B, Lippincott-Schwartz J, Blackstone C, Hurley JH. 2008. Structural basis for midbody targeting of spastin by the ESCRT-III protein CHMP1B. Nature Structural & Molecular Biology 15: 1278-1286. doi: 10.1038/nsmb.1512.
77. Zhu J, Pavelka N, Bradford WD, Rancati G, Li R. 2012. Karyotypic determinants of chromosome instability in aneuploid budding yeast. PLOS Genetics 8:e1002719. doi: 10.1371/journal.pgen.1002719.