Step-wise and punctuated genome evolution drive phenotype changes of tumor cells

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 771, Issue , 2015, Pages 56-69

  Stepanenko, Aleksei ^a   Andreieva, Svitlana ^a   Korets, Kateryna ^a   Mykytenko, Dmytro ^a   Huleyuk, Nataliya ^b   Vassetzky, Yegor ^c   Kavsan, Vadym ^a  

^a INSTITUTE OF MOLECULAR BIOLOGY AND GENETICS   (Ukraine)

^b STATE INSTITUTION NATIONAL RESEARCH CENTER FOR RADIATION MEDICINE OF THE NATIONAL ACADEMY OF MEDICAL SCIENCES OF UKRAINE   (Ukraine)

^c UMR 8126   (France)

Author keywords

Aneuploidy; Cancer gene; Chromosome instability; Tumor heterogeneity; YKL 40

Indexed keywords

TEMOZOLOMIDE; ALKYLATING AGENT; DACARBAZINE;

ARTICLE; CELL VIABILITY; CHI3L1 GENE; CHROMOSOMAL INSTABILITY; CLONAL EVOLUTION; COLONY FORMATION; COLONY FORMATION EFFICIENCY; COMPARATIVE GENOMIC HYBRIDIZATION; CONTROLLED STUDY; CYTOGENETICS; GENE; GENOME; GENOTOXICITY; HEK293 CELL LINE; HELA CELL LINE; HUMAN; HUMAN CELL; KARYOTYPE; MOLECULAR CLONING; PHENOTYPE; ANALOGS AND DERIVATIVES; CHEMISTRY; DNA DAMAGE; DRUG EFFECTS; GENE REGULATORY NETWORK; GENE VECTOR; GENETIC TRANSFECTION; GENETICS; HUMAN GENOME; MOLECULAR EVOLUTION;

ANTINEOPLASTIC AGENTS, ALKYLATING; CHROMOSOMAL INSTABILITY; DACARBAZINE; DNA DAMAGE; EVOLUTION, MOLECULAR; GENE REGULATORY NETWORKS; GENETIC VECTORS; GENOME, HUMAN; HEK293 CELLS; HELA CELLS; HUMANS; TRANSFECTION;

EID: 84921047216     PISSN: 00275107     EISSN: 18792871     Source Type: Journal    
DOI: 10.1016/j.mrfmmm.2014.12.006     Document Type: Article

References (68)

1. Duesberg P., Li R., Fabarius A., Hehlmann R. The chromosomal basis of cancer. Cell. Oncol. 2005, 27:293-318.
2. Duesberg P., Li R., Sachs R., Fabarius A., Upender M.B., Hehlmann R. Cancer drug resistance: the central role of the karyotype. Drug Resist. Updat. 2007, 10:51-58. 10.1016/j.drup.2007.02.003.
3. Duesberg P., Mandrioli D., McCormack A., Nicholson J.M. Is carcinogenesis a form of speciation?. Cell Cycle 2011, 10:2100-2114.
4. Heng H.H.Q., Liu G., Bremer S., Ye K.J., Stevens J., Ye C.J. Clonal and non-clonal chromosome aberrations and genome variation and aberration. Genome 2006, 204:195-204. 10.1139/G06-023.
5. Heng H.H.Q., Stevens J.B., Bremer S.W., Ye K.J., Liu G., Ye C.J. The evolutionary mechanism of cancer. J. Cell. Biochem. 2010, 109:1072-1084. 10.1002/jcb.22497.
6. Heng H.H., Bremer S.W., Stevens J.B., Horne S.D., Liu G., Abdallah B.Y., et al. Chromosomal instability (CIN): what it is and why it is crucial to cancer evolution. Cancer Metastasis Rev. 2013, 32:325-340. 10.1007/s10555-013-9427-7.
7. Stepanenko A.A., Kavsan V.M. Immortalization and malignant transformation of eukaryotic cells. Cytol. Genet. 2012, 46:96-129. 10.3103/S0095452712020041.
8. Stepanenko A.A., Kavsan V.M. Evolutionary karyotypic theory of cancer versus conventional cancer gene mutation theory. Biopolym. Cell 2012, 28:267-280. 10.7124/bc.000059.
9. Stepanenko A.A., Kavsan V.M. Karyotypically distinct U251, U373, and SNB19 glioma cell lines are of the same origin but have different drug treatment sensitivities. Gene 2014, 540:263-265. 10.1016/j.gene.2014.02.053.
10. Abdallah B.Y., Horne S.D., Stevens J.B., Liu G., Ying A.Y., Vanderhyden B., et al. Single cell heterogeneity: why unstable genomes are incompatible with average profiles. Cell Cycle 2013, 12:3640-3649.
11. Ye C.J., Stevens J.B., Liu G., Bremer S.W., Jaiswal A.S., Ye K.J., et al. Genome based cell population heterogeneity promotes tumorigenicity: the evolutionary mechanism of cancer. J. Cell. Physiol. 2009, 219:288-300. 10.1002/jcp.21663.
12. Ragel B.T., Couldwell W.T., Gillespie D.L., Wendland M.M., Whang K., Jensen R.L. A comparison of the cell lines used in meningioma research. Surg. Neurol. 2008, 70:295-307. discussion 307. 10.1016/j.surneu.2007.06.031.
13. Zhang D.-L., Ji L., Li L.-J., Huang G.-S. Systematically experimental investigation on carcinogenesis or tumorigenicity of VERO cell lines of different karyotypes in nude mice in vivo used for viral vaccine manufacture. Yi Chuan Xue Bao 2004, 31:647-660.
14. Bahlis N.J. Darwinian evolution and tiding clones in multiple myeloma. Blood 2012, 120:927-928. 10.1182/blood-2012-06-430645.
15. Burrell R.A., Swanton C. The evolution of the unstable cancer genome. Curr. Opin. Genet. Dev. 2014, 24:61-67. 10.1016/j.gde.2013.11.011.
16. Li L., McCormack A.A., Nicholson J.M., Fabarius A., Hehlmann R., Sachs R.K., et al. Cancer-causing karyotypes: chromosomal equilibria between destabilizing aneuploidy and stabilizing selection for oncogenic function. Cancer Genet. Cytogenet. 2009, 188:1-25. 10.1016/j.cancergencyto.2008.08.016.
17. Silk A.D., Zasadil L.M., Holland A.J., Vitre B., Cleveland D.W., Weaver B.A. Chromosome missegregation rate predicts whether aneuploidy will promote or suppress tumors. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:E4134-E4141. 10.1073/pnas.1317042110.
18. Roylance R., Endesfelder D., Gorman P., Burrell R.A., Sander J., Tomlinson I., et al. Relationship of extreme chromosomal instability with long-term survival in a retrospective analysis of primary breast cancer. Cancer Epidemiol. Biomarkers Prev. 2011, 20:2183-2194. 10.1158/1055-9965.EPI-11-0343.
19. Birkbak N.J., Eklund A.C., Li Q., McClelland S.E., Endesfelder D., Tan P., et al. Paradoxical relationship between chromosomal instability and survival outcome in cancer. Cancer Res. 2011, 71:3447-3452. 10.1158/0008-5472.CAN-10-3667.
20. Stepanenko A.A., Vassetzky Y.S., Kavsan V.M. Antagonistic functional duality of cancer genes. Gene 2013, 529:199-207. 10.1016/j.gene.2013.07.047.
21. Shao R., Hamel K., Petersen L., Cao Q.J., Arenas R.B., Bigelow C., et al. YKL-40, a secreted glycoprotein, promotes tumor angiogenesis. Oncogene 2009, 28:4456-4468. 10.1038/onc.2009.292.
22. Kawada M., Seno H., Kanda K., Nakanishi Y., Akitake R., Komekado H., et al. Chitinase 3-like 1 promotes macrophage recruitment and angiogenesis in colorectal cancer. Oncogene 2012, 31:3111-3123. 10.1038/onc.2011.498.
23. Ngernyuang N., Francescone R.A., Jearanaikoon P., Daduang J., Supoken A., Yan W., et al. Chitinase 3 like 1 is associated with tumor angiogenesis in cervical cancer. Int. J. Biochem. Cell Biol. 2014, 51:45-52. 10.1016/j.biocel.2014.03.021.
24. Salamon J., Hoffmann T., Elies E., Peldschus K., Johansen J.S., Lüers G., et al. Antibody directed against human YKL-40 increases tumor volume in a human melanoma xenograft model in scid mice. PLOS ONE 2014, 9:e95822. 10.1371/journal.pone.0095822.
25. Nakada M., Furuta T., Hayashi Y., Minamoto T., Hamada J.-I. The strategy for enhancing temozolomide against malignant glioma. Front. Oncol. 2012, 2:98. 10.3389/fonc.2012.00098.
26. Yoshimoto K., Mizoguchi M., Hata N., Murata H., Hatae R., Amano T., et al. Complex DNA repair pathways as possible therapeutic targets to overcome temozolomide resistance in glioblastoma. Front. Oncol. 2012, 2:186. 10.3389/fonc.2012.00186.
27. Spiegl-Kreinecker S., Pirker C., Marosi C., Buchroithner J., Pichler J., Silye R., et al. Dynamics of chemosensitivity and chromosomal instability in recurrent glioblastoma. Br. J. Cancer 2007, 96:960-969. 10.1038/sj.bjc.6603652.
28. Johnson B.E., Mazor T., Hong C., Barnes M., Aihara K., McLean C.Y., et al. Mutational analysis reveals the origin and therapy-driven evolution of recurrent glioma. Science 2014, 343:189-193. 10.1126/science.1239947.
29. Bylund L., Kytölä S., Lui W.-O., Larsson C., Weber G. Analysis of the cytogenetic stability of the human embryonal kidney cell line 293 by cytogenetic and STR profiling approaches. Cytogenet. Genome Res. 2004, 106:28-32. 10.1159/000078556.
30. Macville M., Schröck E., Padilla-nash H., Schro E., Keck C., Ghadimi B.M., et al. Comprehensive and definitive molecular cytogenetic characterization of HeLa cells by spectral karyotyping. Cancer Res. 1999, 141-150.
31. Roschke A.V., Stover K., Tonon G., a Schäffer A., Kirsch I.R. Stable karyotypes in epithelial cancer cell lines despite high rates of ongoing structural and numerical chromosomal instability. Neoplasia 2002, 4:19-31. 10.1038/sj/neo/7900197.
32. Liu G., Stevens J.B., Horne S.D., Abdallah B.Y., Ye K.J., Bremer S.W., et al. Genome chaos: survival strategy during crisis. Cell Cycle 2014, 13:528-537. 10.4161/cc.27378.
33. Stepanenko A., Kavsan V. Cancer genes and chromosome instability. Oncogene and Cancer - From Bench to Clinic 2013, 151-182. InTech Publisher, Rijeka, Croatia. Y. Siregar (Ed.).
34. Winnard P., Glackin C., Raman V. Stable integration of an empty vector in MCF-7 cells greatly alters the karyotype. Cancer Genet. Cytogenet. 2006, 164:174-176. 10.1016/j.cancergencyto.2005.07.021.
35. Bardwell L. The mutagenic and carcinogenic effects of gene transfer. Mutagenesis 1989, 4:245-253.
36. Baum C., Kustikova O., Modlich U., Li Z., Fehse B. Mutagenesis and oncogenesis by chromosomal insertion of gene transfer vectors. Hum. Gene Ther. 2006, 17:253-263. 10.1089/hum.2006.17.253.
37. Doerfler W. Impact of foreign DNA integration on tumor biology and on evolution via epigenetic alterations. Epigenomics 2012, 4:41-49. 10.2217/epi.11.111.
38. Duesberg P., Iacobuzio-donahue C., Brosnan J., Mccormack A., Mandrioli D., Chen L. Origin of metastases: subspecies of cancers generated by intrinsic karyotypic variations. Cell Cycle 2012, 11:1151-1166. 10.4161/cc.11.6.19580.
39. McCormack A., Fan J.L., Duesberg M., Bloomfield M., Fiala C., Duesberg P. Individual karyotypes at the origins of cervical carcinomas. Mol. Cytogenet. 2013, 6(44). 10.1186/1755-8166-6-44.
40. Nicholson J.M., Duesberg P. On the karyotypic origin and evolution of cancer cells. Cancer Genet. Cytogenet. 2009, 194:96-110. 10.1016/j.cancergencyto.2009.06.008.
41. Klein A., Li N., Nicholson J.M., aMcCormack A., Graessmann A., Duesberg P. Transgenic oncogenes induce oncogene-independent cancers with individual karyotypes and phenotypes. Cancer Genet. Cytogenet. 2010, 200:79-99. 10.1016/j.cancergencyto.2010.04.008.
42. Stevens J.B., Liu G., Abdallah B.Y., Horne S.D., Ye K.J., Bremer S.W., et al. Unstable genomes elevate transcriptome dynamics. Int. J. Cancer 2014, 134:2074-2087. 10.1002/ijc.28531.
43. Gao C., Furge K., Koeman J., Dykema K., Su Y., Lou Cutler M., et al. Chromosome instability, chromosome transcriptome, and clonal evolution of tumor cell populations. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:8995-9000. 10.1073/pnas.0700631104.
44. Donnelly N., Storchová Z. Dynamic karyotype, dynamic proteome: buffering the effects of aneuploidy. Biochim. Biophys. Acta 2014, 1843:473-481. 10.1016/j.bbamcr.2013.11.017.
45. Stevens J.B., Horne S.D., Abdallah B.Y., Ye C.J., Heng H.H. Chromosomal instability and transcriptome dynamics in cancer. Cancer Metastasis Rev. 2013, 32:391-402. 10.1007/s10555-013-9428-6.
46. Ried T., Hu Y., Difilippantonio M.J., Ghadimi B.M., Grade M., Camps J. The consequences of chromosomal aneuploidy on the transcriptome of cancer cells. Biochim. Biophys. Acta 2012, 1819:784-793. 10.1016/j.bbagrm.2012.02.020.
47. Heng H.H.Q., Bremer S.W., Stevens J.B., Ye K.J., Liu G., Ye C.J. Genetic and epigenetic heterogeneity in cancer: a genome-centric perspective. J. Cell. Physiol. 2009, 220:538-547. 10.1002/jcp.21799.
48. Abasolo I., Yang L., Haleem R., Xiao W., Pio R., Cuttitta F., et al. Overexpression of adrenomedullin gene markedly inhibits proliferation of PC3 prostate cancer cells in vitro and in vivo. Mol. Cell. Endocrinol. 2003, 199:179-187.
49. Dautzenberg F.M., Higelin J., Teichert U. Functional characterization of corticotropin-releasing factor type 1 receptor endogenously expressed in human embryonic kidney 293 cells. Eur. J. Pharmacol. 2000, 390:51-59.
50. Gutiérrez-Pabello J.A., McMurray D.N., Adams L.G. Upregulation of thymosin beta-10 by Mycobacterium bovis infection of bovine macrophages is associated with apoptosis. Infect. Immun. 2002, 70:2121-2127.
51. Skoog T., Elomaa O., Pasonen-Seppänen S.M., Forsberg S., Ahokas K., Jeskanen L., et al. Matrix metalloproteinase-21 expression is associated with keratinocyte differentiation and upregulated by retinoic acid in HaCaT cells. J. Invest. Dermatol. 2009, 129:119-130. 10.1038/jid.2008.206.
52. Gourley C., Paige A.J.W., Taylor K.J., Ward C., Kuske B., Zhang J., et al. WWOX gene expression abolishes ovarian cancer tumorigenicity in vivo and decreases attachment to fibronectin via integrin alpha3. Cancer Res. 2009, 69:4835-4842. 10.1158/0008-5472.CAN-08-2974.
53. Jiang W.G., Grimshaw D., Lane J., Martin T.A., Abounader R., Laterra J., et al. A hammerhead ribozyme suppresses expression of hepatocyte growth factor/scatter factor receptor c-MET and reduces migration and invasiveness of breast cancer cells. Clin. Cancer Res. 2001, 7:2555-2562.
54. Péterfia B., Füle T., Baghy K., Szabadkai K., Fullár A., Dobos K., et al. Syndecan-1 enhances proliferation, migration and metastasis of HT-1080 cells in cooperation with syndecan-2. PLoS ONE 2012, 7:e39474. 10.1371/journal.pone.0039474.
55. Areshkov P.O., Avdieiev S.S., Balynska O.V., Leroith D., Kavsan V.M. Two closely related human members of chitinase-like family, CHI3L1 and CHI3L2, activate ERK1/2 in 293 and U373 cells but have the different influence on cell proliferation. Int. J. Biol. Sci. 2012, 8:39-48.
56. Vavouri T., Semple J.I., Garcia-Verdugo R., Lehner B. Intrinsic protein disorder and interaction promiscuity are widely associated with dosage sensitivity. Cell 2009, 138:198-208. 10.1016/j.cell.2009.04.029.
57. Lee J.M. The good oncogene: when bad genes identify good outcome in cancer. Med. Hypotheses 2011, 76:259-263. 10.1016/j.mehy.2010.10.015.
58. Sotillo R., Schvartzman J.-M., Socci N.D., Benezra R. Mad2-induced chromosome instability leads to lung tumour relapse after oncogene withdrawal. Nature 2010, 464:436-440. 10.1038/nature08803.
59. Li R., Hehlman R., Sachs R., Duesberg P. Chromosomal alterations cause the high rates and wide ranges of drug resistance in cancer cells. Cancer Genet. Cytogenet. 2005, 163:44-56. 10.1016/j.cancergencyto.2005.05.003.
60. Lee A.J.X., Endesfelder D., Rowan A.J., Walther A., Birkbak N.J., Futreal P.A., et al. Chromosomal instability confers intrinsic multidrug resistance. Cancer Res. 2011, 71:1858-1870. 10.1158/0008-5472.CAN-10-3604.
61. Horne S.D., Stevens J.B., Abdallah B.Y., Liu G., Bremer S.W., Ye C.J., et al. Why imatinib remains an exception of cancer research. J. Cell. Physiol. 2013, 228:665-670. 10.1002/jcp.24233.
62. Happold C., Roth P., Wick W., Schmidt N., Florea A.-M., Silginer M., et al. Distinct molecular mechanisms of acquired resistance to temozolomide in glioblastoma cells. J. Neurochem. 2012, 122:444-455. 10.1111/j. 1471-4159.2012.07781.x.
63. Kumar D.M., Patil V., Ramachandran B., Nila M.V., Dharmalingam K., Somasundaram K. Temozolomide-modulated glioma proteome: role of interleukin-1 receptor-associated kinase-4 (IRAK4) in chemosensitivity. Proteomics 2013, 13:2113-2124. 10.1002/pmic.201200261.
64. Lamoral-Theys D., Le Mercier M., Le Calvé B., Rynkowski M.A., Bruyère C., Decaestecker C., et al. Long-term temozolomide treatment induces marked amino metabolism modifications and an increase in TMZ sensitivity in Hs683 oligodendroglioma cells. Neoplasia 2010, 12:69-79.
65. Le Calvé B., Rynkowski M., Le Mercier M., Bruyère C., Lonez C., Gras T., et al. Long-term in vitro treatment of human glioblastoma cells with temozolomide increases resistance in vivo through up-regulation of GLUT transporter and aldo-keto reductase enzyme AKR1C expression. Neoplasia 2010, 12:727-739.
66. Anderson J.C., Duarte C.W., Welaya K., Rohrbach T.D., Bredel M., Yang E.S., et al. Kinomic exploration of temozolomide and radiation resistance in Glioblastoma multiforme xenolines. Radiother. Oncol. 2014, 10.1016/j.radonc.2014.04.010.
67. Hiddingh L., Raktoe R.S., Jeuken J., Hulleman E., Noske D.P., Kaspers G.J.L., et al. Identification of temozolomide resistance factors in glioblastoma via integrative miRNA/mRNA regulatory network analysis. Sci. Rep. 2014, 4:5260. 10.1038/srep05260.
68. Leshchenko V.V., Kuo P.-Y., Jiang Z., Thirukonda V.K., Parekh S. Integrative genomic analysis of temozolomide resistance in diffuse large B-cell lymphoma. Clin. Cancer Res. 2014, 20:382-392. 10.1158/1078-0432.CCR-13-0669.