Three steps to the immortality of cancer cells: Senescence, polyploidy and self-renewal

Cancer Cell International

Volumn 13, Issue 1, 2013, Pages

  Erenpreisa, Jekaterina ^a   Cragg, Mark S ^b  

^a LATVIAN BIOMEDICAL RESEARCH AND STUDY CENTRE   (Latvia)

^b UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

DNA damage; Polyploidy; Reprogramming; Resistance; Self renewal; Senescence; Totipotency; Tumour cells

Indexed keywords

AURORA B KINASE; CYCLIN B1; RAD51 PROTEIN; RAD52 PROTEIN; SURVIVIN;

AUTOPHAGY; CANCER CELL; CELL CYCLE; CELL FATE; CELL RENEWAL; CELL SURFACE; CHROMATIN; DNA DAMAGE; DNA DAMAGE CHECKPOINT; DNA REPAIR; EMBRYO DEVELOPMENT; G2 PHASE CELL CYCLE CHECKPOINT; GAMETOGENESIS; GENE ACTIVATION; GLYCOLYSIS; HUMAN; IMMUNOGENICITY; LIFE CYCLE; MACROAUTOPHAGY; MACRONUCLEUS; MEIOSIS; MITOSIS; ONCOGENE C MYC; PHENOTYPE; POLYPLOIDY; REVIEW; SENESCENCE; TETRAHYMENA; TETRAPLOIDY; TUMOR CELL;

EID: 84883635815     PISSN: None     EISSN: 14752867     Source Type: Journal    
DOI: 10.1186/1475-2867-13-92     Document Type: Review

References (152)

1. Roninson IB. Tumor cell senescence in cancer treatment. Cancer Res 2003, 63(11):2705-2715.
2. Serrano M, Lin AW, McCurrach ME, Beach D, Lowe SW. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 1997, 88(5):593-602. 10.1016/S0092-8674(00)81902-9, 9054499.
3. Finkel E. Telomeres: keys to senescence and cancer. Lancet 1998, 351(9110):1186. 10.1016/S0140-6736(05)79136-4, 9643705.
4. Kuilman T, Michaloglou C, Mooi WJ, Peeper DS. The essence of senescence. Genes Dev 2010, 24(22):2463-2479. 10.1101/gad.1971610, 2975923, 21078816.
5. Hasty P, Sharp ZD, Curiel TJ, Campisi J. mTORC1 and p53: clash of the gods?. Cell Cycle 2013, 12(1):20-25. 10.4161/cc.22912, 3570511, 23255104.
6. Lopez-Otin C, Blasco MA, Partridge L, Serrano M, Kroemer G. The hallmarks of aging. Cell 2013, 153(6):1194-1217. 10.1016/j.cell.2013.05.039, 23746838.
7. Campisi J, d'Adda di Fagagna F. Cellular senescence: when bad things happen to good cells. Nat Rev Mol Cell Biol 2007, 8(9):729-740. 10.1038/nrm2233, 17667954.
8. Wu PC, Wang Q, Grobman L, Chu E, Wu DY. Accelerated cellular senescence in solid tumor therapy. Exp Oncol 2012, 34(3):298-305.
9. Kang TW, Yevsa T, Woller N, Hoenicke L, Wuestefeld T, Dauch D, Hohmeyer A, Gereke M, Rudalska R, Potapova A, et al. Senescence surveillance of pre-malignant hepatocytes limits liver cancer development. Nature 2011, 479(7374):547-551. 10.1038/nature10599, 22080947.
10. Hoenicke L, Zender L. Immune surveillance of senescent cells-biological significance in cancer- and non-cancer pathologies. Carcinogenesis 2012, 33(6):1123-1126. 10.1093/carcin/bgs124, 22470164.
11. Serrano M. Cancer: final act of senescence. Nature 2011, 479(7374):481-482. 10.1038/479481a, 22113687.
12. Rajaraman R, Guernsey DL, Rajaraman MM, Rajaraman SR. Stem cells, senescence, neosis and self-renewal in cancer. Cancer Cell Int 2006, 6:25. 10.1186/1475-2867-6-25, 1664585, 17092342.
13. Wheatley D. Growing evidence of the repopulation of regressed tumours by the division of giant cells. Cell Biol Int 2008, 32(9):1029-1030. 10.1016/j.cellbi.2008.06.001, 18598775.
14. Lee HO, Davidson JM, Duronio RJ. Endoreplication: polyploidy with purpose. Genes Dev 2009, 23(21):2461-2477. 10.1101/gad.1829209, 2779750, 19884253.
15. Ianzini F, Mackey MA. Development of the large scale digital cell analysis system. Radiat Prot Dosimetry 2002, 99(1-4):289-293.
16. Prieur-Carrillo G, Chu K, Lindqvist J, Dewey WC. Computerized video time-lapse (CVTL) analysis of the fate of giant cells produced by X-irradiating EJ30 human bladder carcinoma cells. Radiat Res 2003, 159(6):705-712. 10.1667/RR3009, 12751952.
17. Sundaram M, Guernsey DL, Rajaraman MM, Rajaraman R. Neosis: a novel type of cell division in cancer. Cancer Biol Ther 2004, 3(2):207-218.
18. Chu K, Teele N, Dewey MW, Albright N, Dewey WC. Computerized video time lapse study of cell cycle delay and arrest, mitotic catastrophe, apoptosis and clonogenic survival in irradiated 14-3-3sigma and CDKN1A (p21) knockout cell lines. Radiat Res 2004, 162(3):270-286. 10.1667/RR3221, 15332997.
19. Illidge TM, Cragg MS, Fringes B, Olive P, Erenpreisa JA. Polyploid giant cells provide a survival mechanism for p53 mutant cells after DNA damage. Cell Biol Int 2000, 24(9):621-633. 10.1006/cbir.2000.0557, 10964452.
20. Puig PE, Guilly MN, Bouchot A, Droin N, Cathelin D, Bouyer F, Favier L, Ghiringhelli F, Kroemer G, Solary E, et al. Tumor cells can escape DNA-damaging cisplatin through DNA endoreduplication and reversible polyploidy. Cell Biol Int 2008, 32(9):1031-1043. 10.1016/j.cellbi.2008.04.021, 18550395.
21. Vitale I, Senovilla L, Jemaa M, Michaud M, Galluzzi L, Kepp O, Nanty L, Criollo A, Rello-Varona S, Manic G, et al. Multipolar mitosis of tetraploid cells: inhibition by p53 and dependency on Mos. EMBO J 2010, 29(7):1272-1284. 10.1038/emboj.2010.11, 2857458, 20186124.
22. Erenpreisa J, Ivanov A, Wheatley SP, Kosmacek EA, Ianzini F, Anisimov AP, Mackey M, Davis PJ, Plakhins G, Illidge TM. Endopolyploidy in irradiated p53-deficient tumour cell lines: persistence of cell division activity in giant cells expressing Aurora-B kinase. Cell Biol Int 2008, 32(9):1044-1056. 10.1016/j.cellbi.2008.06.003, 2570184, 18602486.
23. Ianzini F, Kosmacek EA, Nelson ES, Napoli E, Erenpreisa J, Kalejs M, Mackey MA. Activation of meiosis-specific genes is associated with depolyploidization of human tumor cells following radiation-induced mitotic catastrophe. Cancer Res 2009, 69(6):2296-2304. 10.1158/0008-5472.CAN-08-3364, 2657811, 19258501.
24. Nagl W. Endopolyploidy and polyteny in differentiation and evolution 1978, Amsterdam-New York: North-Holland: Publ. Comp.
25. Davoli T, de Lange T. The causes and consequences of polyploidy in normal development and cancer. Annu Rev Cell Dev Biol 2011, 27:585-610. 10.1146/annurev-cellbio-092910-154234, 21801013.
26. Zybina TG, Zybina EV. Cell cycle modification in trophoblast cell populations in the course of placenta formation. A review. DNA replication and related cellular processes 2011, 227-258. Rijeka: Croatia: InTech, Kusic-Tisma J.
27. Beermann W. Control of differentiation at the chromosomal level. J Exp Zool 1964, 157:49-62. 10.1002/jez.1401570110, 14220214.
28. Zybina E. Cytophotometric estimation of the amount of DNA in the nuclei of the giant cells of the trophoblast. DoklAkadNauk SSSR 1963, 153:1428-1431.
29. Rivello HG, Meckert PC, Vigliano C, Favaloro R, Laguens RP. Cardiac myocyte nuclear size and ploidy status decrease after mechanical support. Cardiovasc Pathol 2001, 10(2):53-57. 10.1016/S1054-8807(01)00068-0, 11425598.
30. Duncan AW, Taylor MH, Hickey RD, Hanlon Newell AE, Lenzi ML, Olson SB, Finegold MJ, Grompe M. The ploidy conveyor of mature hepatocytes as a source of genetic variation. Nature 2010, 467(7316):707-710. 10.1038/nature09414, 2967727, 20861837.
31. Erenpreisa JA, Cragg MS, Fringes B, Sharakhov I, Illidge TM. Release of mitotic descendants by giant cells from irradiated Burkitt's lymphoma cell line. Cell Biol Int 2000, 24(9):635-648. 10.1006/cbir.2000.0558, 10964453.
32. Ivanov A, Cragg MS, Erenpreisa J, Emzinsh D, Lukman H, Illidge TM. Endopolyploid cells produced after severe genotoxic damage have the potential to repair DNA double strand breaks. J Cell Sci 2003, 116(Pt 20):4095-4106.
33. Erenpreisa J, Cragg MS, Anisimov AP, Illidge TM. Tumor cell embryonality and the ploidy number 32n: is it a developmental checkpoint?. Cell Cycle 2011, 10(11):1873-1874. 10.4161/cc.10.11.15755, 21519193.
34. Vitale I, Galluzzi L, Senovilla L, Criollo A, Jemaa M, Castedo M, Kroemer G. Illicit survival of cancer cells during polyploidization and depolyploidization. Cell Death Differ 2011, 18(9):1403-1413. 10.1038/cdd.2010.145, 3178421, 21072053.
35. Vakifahmetoglu H, Olsson M, Zhivotovsky B. Death through a tragedy: mitotic catastrophe. Cell Death Differ 2008, 15(7):1153-1162. 10.1038/cdd.2008.47, 18404154.
36. Lu X, Kang Y. Cell fusion as a hidden force in tumor progression. Cancer Res 2009, 69(22):8536-8539. 10.1158/0008-5472.CAN-09-2159, 2783941, 19887616.
37. Gisselsson D, Hakanson U, Stoller P, Marti D, Jin Y, Rosengren AH, Stewenius Y, Kahl F, Panagopoulos I. When the genome plays dice: circumvention of the spindle assembly checkpoint and near-random chromosome segregation in multipolar cancer cell mitoses. PLoS One 2008, 3(4):e1871. 10.1371/journal.pone.0001871, 2289843, 18392149.
38. Zasadil LM, Britigan EM, Weaver BA. 2n or not 2n: Aneuploidy, polyploidy and chromosomal instability in primary and tumor cells. Semin Cell Dev Biol 2013, 24(4):370-379. 10.1016/j.semcdb.2013.02.001, 23416057.
39. Erenpreisa J, Kalejs M, Ianzini F, Kosmacek EA, Mackey MA, Emzinsh D, Cragg MS, Ivanov A, Illidge TM. Segregation of genomes in polyploid tumour cells following mitotic catastrophe. Cell Biol Int 2005, 29(12):1005-1011. 10.1016/j.cellbi.2005.10.008, 16314119.
40. Walen KH. Meiotic-like division to a aneuploidy: chromosomal instability (CIN), cell-senescence and cancer. Cell Oncol 2008, 30(5):451-452.
41. Walen KH. Genetic stability of senescence reverted cells: genome reduction division of polyploidy cells, aneuploidy and neoplasia. Cell Cycle 2008, 7(11):1623-1629. 10.4161/cc.7.11.5964, 18469530.
42. Walen KH. Mitosis is not the only distributor of mutated cells: non-mitotic endopolyploid cells produce reproductive genome-reduced cells. Cell Biol Int 2010, 34(8):867-872. 10.1042/CBI20090502, 20441563.
43. Erenpreisa J, Cragg MS, Salmina K, Hausmann M, Scherthan H. The role of meiotic cohesin REC8 in chromosome segregation in gamma irradiation-induced endopolyploid tumour cells. Exp Cell Res 2009, 315(15):2593-2603. 10.1016/j.yexcr.2009.05.011, 19463812.
44. Davoli T, Denchi EL, de Lange T. Persistent telomere damage induces bypass of mitosis and tetraploidy. Cell 2010, 141(1):81-93. 10.1016/j.cell.2010.01.031, 2854042, 20371347.
45. Erenpreisa J, Salmina K, Huna A, Kosmacek EA, Cragg M, Ianzini F, Anisimov A. Polyploid tumour cells elicit para-diploid progeny through de-polyploidising divisions and regulated autophagic degradation. Cell Biol Int 2011, 35(7):687-695. 10.1042/CBI20100762, 21250945.
46. Erenpreisa J, Huna A, Salmina K, Jackson TR, Cragg MS. Macroautophagy-aided elimination of chromatin: sorting of waste, sorting of fate?. Autophagy 2012, 8(12):1877-1881. 10.4161/auto.21610, 3541312, 22935563.
47. Zhang S, Mercado-Uribe I, Xing Z, Sun B, Kuang J, Liu J. Generation of cancer stem-like cells through the formation of polyploid giant cancer cells. Oncogene 2013, 1-13.
48. Marxer M, Foucar CE, Man WY, Chen Y, Ma HT, Poon RY. Tetraploidization increases sensitivity to Aurora B kinase inhibition. Cell Cycle 2012, 11(13):2567-2577. 10.4161/cc.20947, 22722494.
49. Tam WL, Ang YS, Lim B. The molecular basis of ageing in stem cells. Mech Ageing Dev 2007, 128(1):137-148. 10.1016/j.mad.2006.11.020, 17134742.
50. Sabisz M, Skladanowski A. Cancer stem cells and escape from drug-induced premature senescence in human lung tumor cells: implications for drug resistance and in vitro drug screening models. Cell Cycle 2009, 8(19):3208-3217. 10.4161/cc.8.19.9758, 19738435.
51. Sliwinska MA, Mosieniak G, Wolanin K, Babik A, Piwocka K, Magalska A, Szczepanowska J, Fronk J, Sikora E. Induction of senescence with doxorubicin leads to increased genomic instability of HCT116 cells. Mech Ageing Dev 2009, 130(1-2):24-32.
52. Mosieniak G, Sikora E. Polyploidy: the link between senescence and cancer. Curr Pharm Des 2010, 16(6):734-740. 10.2174/138161210790883714, 20388083.
53. Roberson RS, Kussick SJ, Vallieres E, Chen SY, Wu DY. Escape from therapy-induced accelerated cellular senescence in p53-null lung cancer cells and in human lung cancers. Cancer Res 2005, 65(7):2795-2803. 10.1158/0008-5472.CAN-04-1270, 15805280.
54. Wang Q, Wu PC, Roberson RS, Luk BV, Ivanova I, Chu E, Wu DY. Survivin and escaping in therapy-induced cellular senescence. Int J Cancer 2011, 128(7):1546-1558. 10.1002/ijc.25482, 3000873, 20503268.
55. Wang Q, Wu PC, Dong DZ, Ivanova I, Chu E, Zeliadt S, Vesselle H, Wu DY. Polyploidy road to therapy-induced cellular senescence and escape. Int J Cancer 2013, 132(7):1505-1515. 10.1002/ijc.27810, 22945332.
56. Bolton MA, Lan W, Powers SE, McCleland ML, Kuang J, Stukenberg PT. Aurora B kinase exists in a complex with survivin and INCENP and its kinase activity is stimulated by survivin binding and phosphorylation. Mol Biol Cell 2002, 13(9):3064-3077. 10.1091/mbc.E02-02-0092, 124143, 12221116.
57. Bernstein H, Hopf FA, Michod RE. The molecular basis of the evolution of sex. Adv Genet 1987, 24:323-370.
58. Kondrashov AS. The asexual ploidy cycle and the origin of sex. Nature 1994, 370(6486):213-216. 10.1038/370213a0, 8028667.
59. Nebreda AR, Ferby I. Regulation of the meiotic cell cycle in oocytes. Curr Opin Cell Biol 2000, 12(6):666-675. 10.1016/S0955-0674(00)00150-2, 11063930.
60. Dernburg AF, McDonald K, Moulder G, Barstead R, Dresser M, Villeneuve AM. Meiotic recombination in C. elegans initiates by a conserved mechanism and is dispensable for homologous chromosome synapsis. Cell 1998, 94(3):387-398. 10.1016/S0092-8674(00)81481-6, 9708740.
61. Erenpreisa J, Kalejs M, Cragg MS. Mitotic catastrophe and endomitosis in tumour cells: an evolutionary key to a molecular solution. Cell Biol Int 2005, 29(12):1012-1018. 10.1016/j.cellbi.2005.10.005, 16310380.
62. Erenpreisa J, Cragg MS. Cancer: a matter of life cycle?. Cell Biol Int 2007, 31(12):1507-1510. 10.1016/j.cellbi.2007.08.013, 17936649.
63. Erenpreisa J, Cragg MS. MOS, aneuploidy and the ploidy cycle of cancer cells. Oncogene 2010, 29(40):5447-5451. 10.1038/onc.2010.310, 20676137.
64. Kalejs M, Ivanov A, Plakhins G, Cragg MS, Emzinsh D, Illidge TM, Erenpreisa J. Upregulation of meiosis-specific genes in lymphoma cell lines following genotoxic insult and induction of mitotic catastrophe. BMC Cancer 2006, 6:6. 10.1186/1471-2407-6-6, 1351196, 16401344.
65. Gorgoulis VG, Zacharatos P, Mariatos G, Liloglou T, Kokotas S, Kastrinakis N, Kotsinas A, Athanasiou A, Foukas P, Zoumpourlis V, et al. Deregulated expression of c-mos in non-small cell lung carcinomas: relationship with p53 status, genomic instability, and tumor kinetics. Cancer Research 2001, 61(2):538-549.
66. Rosa AM, Dabas N, Byrnes DM, Eller MS, Grichnik JM. Germ cell proteins in melanoma: prognosis, diagnosis, treatment, and theories on expression. J Skin Cancer 2012, 2012:621968. 3503391, 23209909.
67. Nasmyth K. Disseminating the genome: joining, resolving, and separating sister chromatids during mitosis and meiosis. Annu Rev Genet 2001, 35:673-745. 10.1146/annurev.genet.35.102401.091334, 11700297.
68. Dupre A, Haccard O, Jessus C. Mos in the oocyte: how to use MAPK independently of growth factors and transcription to control meiotic divisions. J Signal Transduct 2011, 2011:350412. 3101788, 21637374.
69. Dupre A, Suziedelis K, Valuckaite R, de Gunzburg J, Ozon R, Jessus C, Haccard O. Xenopus H-RasV12 promotes entry into meiotic M phase and cdc2 activation independently of Mos and p42(MAPK). Oncogene 2002, 21(42):6425-6433. 10.1038/sj.onc.1205827, 12226746.
70. Fukasawa K, Murakami MS, Blair DG, Kuriyama R, Hunt T, Fischinger P, Vande Woude GF. Similarities between somatic cells overexpressing the mos oncogene and oocytes during meiotic interphase. Cell Growth Differ 1994, 5(10):1093-1103.
71. Erenpreiss J. Current concepts of malignant growth 1993, 191. Riga: Part A. From a normal cell to cancer Zvaigzne Publishers.
72. Mallette FA, Gaumont-Leclerc MF, Ferbeyre G. The DNA damage signaling pathway is a critical mediator of oncogene-induced senescence. Genes & Development 2007, 21(1):43-48. 10.1101/gad.1487307, 1759898, 17210786.
73. Hasan AKMMT, Kihira M, Yoshida J, Sato K-I. Phospho-Signaling at Oocyte Maturation and Fertilization: Set Up for Embryogenesis and Beyond Part I. Protein Kinases, Embryogenesis 2012, Sato K-I, InTech. DOI: 10.5772/39369. http://www.intechopen.com/books/embryogenesis/phospho-signaling-at-oocyte-maturation-and-fertilization-set-up-for-embryogenesis-and-beyond-part-ii.
74. Johnson AD, Cork RJ, Williams MA, Robinson KR, Smith LD. H-ras(val12) induces cytoplasmic but not nuclear events of the cell cycle in small Xenopus oocytes. Cell Regul 1990, 1(7):543-554. 361572, 2098115.
75. Back JH, Kim AL. The expanding relevance of nuclear mTOR in carcinogenesis. Cell Cycle 2011, 10(22):3849-3852. 10.4161/cc.10.22.18329, 3356804, 22067472.
76. Laplante M, Sabatini DM. mTOR signaling in growth control and disease. Cell 2012, 149(2):274-293. 10.1016/j.cell.2012.03.017, 3331679, 22500797.
77. Birchmeier C, Broek D, Wigler M. Ras proteins can induce meiosis in Xenopus oocytes. Cell 1985, 43(3 Pt 2):615-621.
78. Dean M, Fojo T, Bates S. Tumour stem cells and drug resistance. Nat Rev Cancer 2005, 5(4):275-284. 10.1038/nrc1590, 15803154.
79. Jordan CT, Guzman ML, Noble M. Cancer stem cells. N Engl J Med 2006, 355(12):1253-1261. 10.1056/NEJMra061808, 16990388.
80. Ben-Porath I, Thomson MW, Carey VJ, Ge R, Bell GW, Regev A, Weinberg RA. An embryonic stem cell-like gene expression signature in poorly differentiated aggressive human tumors. Nat Genet 2008, 40(5):499-507. 10.1038/ng.127, 2912221, 18443585.
81. Saigusa S, Tanaka K, Toiyama Y, Yokoe T, Okugawa Y, Ioue Y, Miki C, Kusunoki M. Correlation of CD133, OCT4, and SOX2 in rectal cancer and their association with distant recurrence after chemoradiotherapy. Ann Surg Oncol 2009, 16(12):3488-3498. 10.1245/s10434-009-0617-z, 19657699.
82. Ge N, Lin HX, Xiao XS, Guo L, Xu HM, Wang X, Jin T, Cai XY, Liang Y, Hu WH, et al. Prognostic significance of Oct4 and Sox2 expression in hypopharyngeal squamous cell carcinoma. J Transl Med 2010, 8:94. 10.1186/1479-5876-8-94, 2958910, 20937145.
83. Xiang R, Liao D, Cheng T, Zhou H, Shi Q, Chuang TS, Markowitz D, Reisfeld RA, Luo Y. Downregulation of transcription factor SOX2 in cancer stem cells suppresses growth and metastasis of lung cancer. Br J Cancer 2011, 104(9):1410-1417. 10.1038/bjc.2011.94, 3101944, 21468047.
84. Baumann M, Krause M, Hill R. Exploring the role of cancer stem cells in radioresistance. Nat Rev Cancer 2008, 8(7):545-554.
85. Blagosklonny MV. Target for cancer therapy: proliferating cells or stem cells. Leukemia 2006, 20(3):385-391. 10.1038/sj.leu.2404075, 16357832.
86. Salmina K, Jankevics E, Huna A, Perminov D, Radovica I, Klymenko T, Ivanov A, Jascenko E, Scherthan H, Cragg M, et al. Up-regulation of the embryonic self-renewal network through reversible polyploidy in irradiated p53-mutant tumour cells. Exp Cell Res 2010, 316(13):2099-2112. 10.1016/j.yexcr.2010.04.030, 20457152.
87. Lee GY, Shim JS, Cho B, Jung JY, Lee DS, Oh IH. Stochastic acquisition of a stem cell-like state and drug tolerance in leukemia cells stressed by radiation. Int J Hematol 2011, 93(1):27-35. 10.1007/s12185-010-0734-2, 21170617.
88. Ghisolfi L, Keates AC, Hu X, Lee DK, Li CJ. Ionizing radiation induces stemness in cancer cells. PLoS One 2012, 7(8):e43628. 10.1371/journal.pone.0043628, 3424153, 22928007.
89. Lagadec C, Vlashi E, Della Donna L, Dekmezian C, Pajonk F. Radiation-induced reprogramming of breast cancer cells. Stem Cells 2012, 30(5):833-844. 10.1002/stem.1058, 3413333, 22489015.
90. Chuang YS, Huang WH, Park SW, Persaud SD, Hung CH, Ho PC, Wei LN. Promyelocytic leukemia protein in retinoic acid-induced chromatin remodeling of Oct4 gene promoter. Stem Cells 2011, 29(4):660-669. 10.1002/stem.623, 3321229, 21360626.
91. Bartova E, Sustackova G, Stixova L, Kozubek S, Legartova S, Foltankova V. Recruitment of Oct4 protein to UV-damaged chromatin in embryonic stem cells. PLoS One 2011, 6(12):e27281. 10.1371/journal.pone.0027281, 3229488, 22164208.
92. Guo Y, Mantel C, Hromas RA, Broxmeyer HE. Oct-4 is critical for survival/antiapoptosis of murine embryonic stem cells subjected to stress: effects associated with Stat3/survivin. Stem Cells 2008, 26(1):30-34. 10.1634/stemcells.2007-0401, 2818886, 17932422.
93. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006, 126(4):663-676. 10.1016/j.cell.2006.07.024, 16904174.
94. Banito A, Rashid ST, Acosta JC, Li S, Pereira CF, Geti I, Pinho S, Silva JC, Azuara V, Walsh M, et al. Senescence impairs successful reprogramming to pluripotent stem cells. Genes Dev 2009, 23(18):2134-2139. 10.1101/gad.1811609, 2751980, 19696146.
95. Li H, Collado M, Villasante A, Strati K, Ortega S, Canamero M, Blasco MA, Serrano M. The Ink4/Arf locus is a barrier for iPS cell reprogramming. Nature 2009, 460(7259):1136-1139. 10.1038/nature08290, 3578184, 19668188.
96. Menendez JA, Vellon L, Oliveras-Ferraros C, Cufi S, Vazquez-Martin A. mTOR-regulated senescence and autophagy during reprogramming of somatic cells to pluripotency: a roadmap from energy metabolism to stem cell renewal and aging. Cell Cycle 2011, 10(21):3658-3677. 10.4161/cc.10.21.18128, 22052357.
97. Huna A, Salmina K, Jascenko E, Duburs G, Inashkina I, Erenpreisa J. Self-Renewal Signalling in Presenescent Tetraploid IMR90 Cells. J Aging Res 2011, 2011:103253. 3100543, 21629737.
98. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 1998, 273(10):5858-5868. 10.1074/jbc.273.10.5858, 9488723.
99. Boheler KR. Stem cell pluripotency: a cellular trait that depends on transcription factors, chromatin state and a checkpoint deficient cell cycle. J Cell Physiol 2009, 221(1):10-17. 10.1002/jcp.21866, 3326661, 19562686.
100. Mantel C, Guo Y, Lee MR, Kim MK, Han MK, Shibayama H, Fukuda S, Yoder MC, Pelus LM, Kim KS, et al. Checkpoint-apoptosis uncoupling in human and mouse embryonic stem cells: a source of karyotpic instability. Blood 2007, 109(10):4518-4527. 10.1182/blood-2006-10-054247, 1885509, 17289813.
101. Mantel C, Guo Y, Lee MR, Han MK, Rhorabough S, Kim KS, Broxmeyer HE. Cells enter a unique intermediate 4N stage, not 4N-G1, after aborted mitosis. Cell Cycle 2008, 7(4):484-492. 10.4161/cc.7.4.5316, 18235235.
102. Conant GC, Wolfe KH. Increased glycolytic flux as an outcome of whole-genome duplication in yeast. Mol Syst Biol 2007, 3:129. 1943425, 17667951.
103. Anatskaya OV, Vinogradov AE. Genome multiplication as adaptation to tissue survival: evidence from gene expression in mammalian heart and liver. Genomics 2007, 89(1):70-80. 10.1016/j.ygeno.2006.08.014, 17029690.
104. Ward PS, Thompson CB. Metabolic reprogramming: a cancer hallmark even Warburg did not anticipate. Cancer Cell 2012, 21(3):297-308. 10.1016/j.ccr.2012.02.014, 3311998, 22439925.
105. Hu J, Locasale JW, Bielas JH, O'Sullivan J, Sheahan K, Cantley LC, Heiden MGV, Vitkup D. Heterogeneity of tumor-induced gene expression changes in the human metabolic network. Nat Biotech 2013, 31(6):522-529.
106. Jiang J, Tang YL, Liang XH. EMT: a new vision of hypoxia promoting cancer progression. Cancer Biol Ther 2011, 11(8):714-723. 10.4161/cbt.11.8.15274, 21389772.
107. Miller DM, Thomas SD, Islam A, Muench D, Sedoris K. c-Myc and cancer metabolism. Clin Cancer Res 2012, 18(20):5546-5553. 10.1158/1078-0432.CCR-12-0977, 3505847, 23071356.
108. Sun Q, Chen X, Ma J, Peng H, Wang F, Zha X, Wang Y, Jing Y, Yang H, Chen R, et al. Mammalian target of rapamycin up-regulation of pyruvate kinase isoenzyme type M2 is critical for aerobic glycolysis and tumor growth. Proc Natl Acad Sci U S A 2011, 108(10):4129-4134. 10.1073/pnas.1014769108, 3054028, 21325052.
109. Wong DJ, Liu H, Ridky TW, Cassarino D, Segal E, Chang HY. Module map of stem cell genes guides creation of epithelial cancer stem cells. Cell Stem Cell 2008, 2(4):333-344. 10.1016/j.stem.2008.02.009, 2628721, 18397753.
110. Dominguez-Sola D, Ying CY, Grandori C, Ruggiero L, Chen B, Li M, Galloway DA, Gu W, Gautier J, Dalla-Favera R. Non-transcriptional control of DNA replication by c-Myc. Nature 2007, 448(7152):445-451. 10.1038/nature05953, 17597761.
111. Li Q, Dang CV. c-Myc overexpression uncouples DNA replication from mitosis. Mol Cell Biol 1999, 19(8):5339-5351. 84377, 10409725.
112. Conner EA, Lemmer ER, Sanchez A, Factor VM, Thorgeirsson SS. E2F1 blocks and c-Myc accelerates hepatic ploidy in transgenic mouse models. Biochem Biophys Res Commun 2003, 302(1):114-120. 10.1016/S0006-291X(03)00125-6, 12593856.
113. den Hollander J, Rimpi S, Doherty JR, Rudelius M, Buck A, Hoellein A, Kremer M, Graf N, Scheerer M, Hall MA, et al. Aurora kinases A and B are up-regulated by Myc and are essential for maintenance of the malignant state. Blood 2010, 116(9):1498-1505. 10.1182/blood-2009-11-251074, 2938839, 20519624.
114. Gusse M, Ghysdael J, Evan G, Soussi T, Mechali M. Translocation of a store of maternal cytoplasmic c-myc protein into nuclei during early development. Mol Cell Biol 1989, 9(12):5395-5403. 363707, 2685563.
115. Gordon DJ, Resio B, Pellman D. Causes and consequences of aneuploidy in cancer. Nat Rev Genet 2012, 13(3):189-203.
116. Jackson TR, Salmina K, Huna A, Inashkina I, Jankevics E, Riekstina U, Kalnina Z, Ivanov A, Townsend PA, Cragg MS, et al. DNA damage causes TP53-dependent coupling of self-renewal and senescence pathways in embryonal carcinoma cells. Cell Cycle 2013, 12(3):430-441. 10.4161/cc.23285, 3587444, 23287532.
117. Sherman MY, Meng L, Stampfer M, Gabai VL, Yaglom JA. Oncogenes induce senescence with incomplete growth arrest and suppress the DNA damage response in immortalized cells. Aging Cell 2011, 10(6):949-961. 10.1111/j.1474-9726.2011.00736.x, 3433764, 21824272.
118. Zybina TG, Stein GI, Zybina EV. Endopolyploid and proliferating trophoblast cells express different patterns of intracellular cytokeratin and glycogen localization in the rat placenta. Cell Biol Int 2011, 35(7):649-655. 10.1042/CBI20100278, 21299496.
119. Lee J, Go Y, Kang I, Han YM, Kim J. Oct-4 controls cell-cycle progression of embryonic stem cells. Biochem J 2010, 426(2):171-181. 10.1042/BJ20091439, 2825734, 19968627.
120. Raderschall E, Bazarov A, Cao J, Lurz R, Smith A, Mann W, Ropers HH, Sedivy JM, Golub EI, Fritz E, et al. Formation of higher-order nuclear Rad51 structures is functionally linked to p21 expression and protection from DNA damage-induced apoptosis. J Cell Sci 2002, 115(Pt 1):153-164.
121. Zheng L, Dai H, Zhou M, Li X, Liu C, Guo Z, Wu X, Wu J, Wang C, Zhong J, et al. Polyploid cells rewire DNA damage response networks to overcome replication stress-induced barriers for tumour progression. Nat Commun 2012, 3:815. 3517178, 22569363.
122. Huang S. Reprogramming cell fates: reconciling rarity with robustness. Bioessays 2009, 31(5):546-560. 10.1002/bies.200800189, 19319911.
123. Huang S. Non-genetic heterogeneity of cells in development: more than just noise. Dev 2009, 136(23):3853-3862.
124. Rajaraman R, Guernsey DL, Rajaraman MM, Rajaraman SR. Neosis - A parasexual somatic reduction division in cancer. Int J Hum Genet 2007, 7(1):29-48.
125. Weihua Z, Lin Q, Ramoth AJ, Fan D, Fidler IJ. Formation of solid tumors by a single multinucleated cancer cell. Cancer 2011, 117(17):4092-4099. 10.1002/cncr.26021, 3136613, 21365635.
126. Young AR, Narita M. Connecting autophagy to senescence in pathophysiology. Curr Opin Cell Biol 2010, 22(2):234-240. 10.1016/j.ceb.2009.12.005, 20045302.
127. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011, 144(5):646-674. 10.1016/j.cell.2011.02.013, 21376230.
128. Dunn GP, Old LJ, Schreiber RD. The three Es of cancer immunoediting. Annu Rev Immunol 2004, 22:329-360. 10.1146/annurev.immunol.22.012703.104803, 15032581.
129. Simpson AJ, Caballero OL, Jungbluth A, Chen YT, Old LJ. Cancer/testis antigens, gametogenesis and cancer. Nat Rev Cancer 2005, 5(8):615-625. 10.1038/nrc1669, 16034368.
130. Fratta E, Coral S, Covre A, Parisi G, Colizzi F, Danielli R, Nicolay HJ, Sigalotti L, Maio M. The biology of cancer testis antigens: putative function, regulation and therapeutic potential. Mol Oncol 2011, 5(2):164-182. 10.1016/j.molonc.2011.02.001, 21376678.
131. Lindsey SF, Byrnes DM, Eller MS, Rosa AM, Dabas N, Escandon J, Grichnik JM. Potential role of meiosis proteins in melanoma chromosomal instability. J Skin Cancer 2013, 2013:1-9. http://dx.doi.org/10.1155/2013/1901099.
132. Zayakin P, Ancans G, Silina K, Meistere I, Kalnina Z, Andrejeva D, Endzelins E, Ivanova L, Pismennaja A, Ruskule A, et al. Tumor-associated autoantibody signature for the early detection of gastric cancer. Int J Cancer 2013, 132(1):137-147. 10.1002/ijc.27667, 22684876.
133. Boileve A, Senovilla L, Vitale I, Lissa D, Martins I, Metivier D, van den Brink S, Clevers H, Galluzzi L, Castedo M, et al. Immunosurveillance against tetraploidization-induced colon tumorigenesis. Cell Cycle 2013, 12(3):473-479. 10.4161/cc.23369, 23324343.
134. Senovilla L, Vitale I, Martins I, Tailler M, Pailleret C, Michaud M, Galluzzi L, Adjemian S, Kepp O, Niso-Santano M, et al. An immunosurveillance mechanism controls cancer cell ploidy. Science 2012, 337(6102):1678-1684. 10.1126/science.1224922, 23019653.
135. Cufi S, Vazquez-Martin A, Oliveras-Ferraros C, Martin-Castillo B, Vellon L, Menendez JA. Autophagy positively regulates the CD44(+) CD24(-/low) breast cancer stem-like phenotype. Cell Cycle 2011, 10(22):3871-3885. 10.4161/cc.10.22.17976, 22127234.
136. Akalay I, Janji B, Hasmim M, Noman MZ, Andre F, De Cremoux P, Bertheau P, Badoual C, Vielh P, Larsen AK, et al. Epithelial-to-mesenchymal transition and autophagy induction in breast carcinoma promote escape from T-cell-mediated lysis. Cancer Res 2013, 73(8):2418-2427. 10.1158/0008-5472.CAN-12-2432, 23436798.
137. Wells D, Hillier SG. Polar bodies: their biological mystery and clinical meaning. Mol Hum Reprod 2011, 17(5):273-274. 10.1093/molehr/gar028, 23443970.
138. Lu E, Wolfe J. Lysosomal enzymes in the macronucleus of Tetrahymena during its apoptosis-like degradation. Cell Death Differ 2001, 8(3):289-297. 10.1038/sj.cdd.4400807, 11319612.
139. Raikov IB. The protozoan nucleus - morphology and evolution 1982, Wien u.a: Springer, 1983.
140. Marsh TC, Cole ES, Stuart KR, Campbell C, Romero DP. RAD51 is required for propagation of the germinal nucleus in Tetrahymena thermophila. Genetics 2000, 154(4):1587-1596. 1461009, 10747055.
141. Erenpreisa J, Cragg MS. Life-cycle features of tumour cells 2008, 61-71. Germany: Springer-Verlag Berlin, Evolutionary biology from concept to application.
142. Mintz B, Illmensee K. Normal genetically mosaic mice produced from malignant teratocarcinoma cells. Proc Natl Acad Sci U S A 1975, 72(9):3585-3589. 10.1073/pnas.72.9.3585, 433040, 1059147.
143. Yeom YI, Fuhrmann G, Ovitt CE, Brehm A, Ohbo K, Gross M, Hubner K, Scholer HR. Germline regulatory element of Oct-4 specific for the totipotent cycle of embryonal cells. Dev 1996, 122(3):881-894.
144. Zuccotti M, Merico V, Belli M, Mulas F, Sacchi L, Zupan B, Redi CA, Prigione A, Adjaye J, Bellazzi R, et al. OCT4 and the acquisition of oocyte developmental competence during folliculogenesis. Int J Dev Biol 2012, 56(10-12):853-858.
145. Wang X, Dai J. Concise review: isoforms of OCT4 contribute to the confusing diversity in stem cell biology. Stem Cells 2010, 28(5):885-893. 2962909, 20333750.
146. Hubner K, Fuhrmann G, Christenson LK, Kehler J, Reinbold R, De La Fuente R, Wood J, Strauss JF, Boiani M, Scholer HR. Derivation of oocytes from mouse embryonic stem cells. Science 2003, 300(5623):1251-1256. 10.1126/science.1083452, 12730498.
147. Huang S, Ernberg I, Kauffman S. Cancer attractors: a systems view of tumors from a gene network dynamics and developmental perspective. Semin Cell Dev Biol 2009, 20(7):869-876. 10.1016/j.semcdb.2009.07.003, 2754594, 19595782.
148. Huang S. On the intrinsic inevitability of cancer: from foetal to fatal attraction. Semin Cancer Biol 2011, 21(3):183-199. 10.1016/j.semcancer.2011.05.003, 21640825.
149. Lipkin G. Plasticity of the cancer cell: implications for epigenetic control of melanoma and other malignancies. J Invest Dermatol 2008, 128(9):2152-2155. 10.1038/jid.2008.69, 18401428.
150. Baylin SB, Jones PA. A decade of exploring the cancer epigenome - biological and translational implications. Nat Rev Cancer 2011, 11(10):726-734. 10.1038/nrc3130, 3307543, 21941284.
151. Tsai HC, Baylin SB. Cancer epigenetics: linking basic biology to clinical medicine. Cell Res 2011, 21(3):502-517. 10.1038/cr.2011.24, 3193419, 21321605.
152. Bissell M. Q&A: Mina Bissell on tumors as organs. Cancer Discov 2013, 3(1):7.