HEK293 in cell biology and cancer research: Phenotype, karyotype, tumorigenicity, and stress-induced genome-phenotype evolution

Gene

Volumn 569, Issue 2, 2015, Pages 182-190

  Stepanenko, A A ^a   Dmitrenko, V V ^a  

^a INSTITUTE OF MOLECULAR BIOLOGY AND GENETICS   (Ukraine)

Author keywords

Aneuploidy; Chromosome instability; Genome theory; Heterogeneity; Oncogenes; Tumor evolution

Indexed keywords

PLASMID DNA;

ADRENAL GLAND; ANEUPLOIDY; CANCER RESEARCH; CARCINOGENICITY; CELL STRESS; CHROMOSOMAL INSTABILITY; CHROMOSOME ABERRATION; CHROMOSOME NUMBER; CYTOLOGY; DNA TRANSFECTION; GENE OVEREXPRESSION; GENOMIC INSTABILITY; HEK293 CELL LINE; HUMAN; HUMAN GENOME; KARYOTYPE; KIDNEY; ONCOGENE; PHENOTYPE; PRIORITY JOURNAL; REVIEW; TUMOR GENE; GENETICS; NEOPLASM; PHYSIOLOGY;

ADRENAL GLANDS; CHROMOSOME ABERRATIONS; GENOMIC INSTABILITY; HEK293 CELLS; HUMANS; KARYOTYPE; KIDNEY; NEOPLASMS;

EID: 84937975217     PISSN: 03781119     EISSN: 18790038     Source Type: Journal    
DOI: 10.1016/j.gene.2015.05.065     Document Type: Review

References (154)

1. Abasolo I., Yang L., Haleem R., Xiao W., Pio R., Cuttitta F., Montuenga L.M., Kozlowski J.M., Calvo A., Wang Z. Overexpression of adrenomedullin gene markedly inhibits proliferation of PC3 prostate cancer cells in vitro and in vivo. Mol. Cell. Endocrinol. 2003, 199:179-187.
2. Abdallah B.Y., Horne S.D., Stevens J.B., Liu G., Ying A.Y., Vanderhyden B., Krawetz S.A., Gorelick R., Heng H.H.Q. Why unstable genomes are incompatible with average profiles single cell heterogeneity 2013, 12:3640-3649.
3. Adey A., Burton J.N., Kitzman J.O., Hiatt J.B., Lewis A.P., Martin B.K., Qiu R., Lee C., Shendure J. The haplotype-resolved genome and epigenome of the aneuploid HeLa cancer cell line. Nature 2013, 500:207-211. 10.1038/nature12064.
4. Akli S., Zheng P.-J., Multani A.S., Wingate H.F., Pathak S., Zhang N., Tucker S.L., Chang S., Keyomarsi K. Tumor-specific low molecular weight forms of cyclin E induce genomic instability and resistance to p21, p27, and antiestrogens in breast cancer. Cancer Res. 2004, 64:3198-3208.
5. al-Mulla F., Bitar M.S., Taqi Z., Rath O., Kolch W. RAF kinase inhibitory protein (RKIP) modulates cell cycle kinetics and motility. Mol. Biosyst. 2011, 7:928-941. 10.1039/c0mb00208a.
6. Arlt M.F., Wilson T.E., Glover T.W. Replication stress and mechanisms of CNV formation. Curr. Opin. Genet. Dev. 2012, 22:204-210. 10.1016/j.gde.2012.01.009.
7. Arnhold S., Post C., Glüer S., Hoopmann M., Wenisch S., Volpers C., Addicks K. Neuronal characteristics of amniotic fluid derived cells after adenoviral transformation. Cell Biol. Int. 2008, 32:1559-1566. 10.1016/j.cellbi.2008.09.002.
8. Arrick B.A., Lopez A.R., Elfman F., Ebner R., Damsky C.H., Derynck R. Altered metabolic and adhesive properties and increased tumorigenesis associated with increased expression of transforming growth factor beta 1. J. Cell Biol. 1992, 118:715-726.
9. Ashokkumar B., Vaziri N.D., Said H.M. Thiamin uptake by the human-derived renal epithelial (HEK-293) cells: cellular and molecular mechanisms. Am. J. Physiol. Ren. Physiol. 2006, 291:F796-F805. 10.1152/ajprenal.00078.2006.
10. Bardwell L. The mutagenic and carcinogenic effects of gene transfer. Mutagenesis 1989, 4:245-253.
11. Barlow J.H., Faryabi R.B., Callén E., Wong N., Malhowski A., Chen H.T., Gutierrez-Cruz G., Sun H.-W., McKinnon P., Wright G., Casellas R., Robbiani D.F., Staudt L., Fernandez-Capetillo O., Nussenzweig A. Identification of early replicating fragile sites that contribute to genome instability. Cell 2013, 152:620-632. 10.1016/j.cell.2013.01.006.
12. Bester A.C., Roniger M., Oren Y.S., Im M.M., Sarni D., Chaoat M., Bensimon A., Zamir G., Shewach D.S., Kerem B. Nucleotide deficiency promotes genomic instability in early stages of cancer development. Cell 2011, 145:435-446. 10.1016/j.cell.2011.03.044.
13. Biederer T., Scheiffele P. Mixed-culture assays for analyzing neuronal synapse formation. Nat. Protoc. 2007, 2:670-676. 10.1038/nprot.2007.92.
14. Braun G.S., Huber S.M. Development of renal function. Zoology (Jena) 2002, 105:341-354. 10.1078/0944-2006-00073.
15. Bryan T.M., Englezou A., Dunham M.A., Reddel R.R. Telomere length dynamics in telomerase-positive immortal human cell populations. Exp. Cell Res. 1998, 239:370-378. 10.1006/excr.1997.3907.
16. 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.
17. Campbell S.A., Lin J., Dobrikova E.Y., Gromeier M. Genetic determinants of cell type-specific poliovirus propagation in HEK 293 cells. J. Virol. 2005, 79:6281-6290. 10.1128/JVI.79.10.6281-6290.2005.
18. Canis M., Lechner A., Mack B., Zengel P., Laubender R.P., Koehler U., Heissmeyer V., Gires O. CD133 induces tumour-initiating properties in HEK293 cells. Tumour Biol. 2013, 34:437-443. 10.1007/s13277-012-0568-z.
19. Capper R., Britt-Compton B., Tankimanova M., Rowson J., Letsolo B., Man S., Haughton M., Baird D.M. The nature of telomere fusion and a definition of the critical telomere length in human cells. Genes Dev. 2007, 21:2495-2508. 10.1101/gad.439107.
20. Carr A.M., Lambert S. Replication stress-induced genome instability: the dark side of replication maintenance by homologous recombination. J. Mol. Biol. 2013, 425:4733-4744. 10.1016/j.jmb.2013.04.023.
21. Castiglioni F., Tagliabue E., Campiglio M., Pupa S.M., Balsari A., Ménard S. Role of exon-16-deleted HER2 in breast carcinomas. Endocr. Relat. Cancer 2006, 13:221-232. 10.1677/erc.1.01047.
22. Chang Y.-H., Lee C.-P., Su M.-T., Wang J.-T., Chen J.-Y., Lin S.-F., Tsai C.-H., Hsieh M.-J., Takada K., Chen M.-R. Epstein-Barr virus BGLF4 kinase retards cellular S-phase progression and induces chromosomal abnormality. PLoS One 2012, 7:e39217. 10.1371/journal.pone.0039217.
23. Chao C., Goluszko E., Lee Y.-T., Kolokoltsov A.A., Davey R.A., Uchida T., Townsend C.M., Hellmich M.R. Constitutively active CCK2 receptor splice variant increases Src-dependent HIF-1 alpha expression and tumor growth. Oncogene 2007, 26:1013-1019. 10.1038/sj.onc.1209862.
24. Cheng J.D., Dunbrack R.L., Valianou M., Rogatko A., Alpaugh R.K., Weiner L.M. Promotion of tumor growth by murine fibroblast activation protein, a serine protease, in an animal model. Cancer Res. 2002, 62:4767-4772.
25. Cheng J.D., Valianou M., Canutescu A.A., Jaffe E.K., Lee H.-O., Wang H., Lai J.H., Bachovchin W.W., Weiner L.M. Abrogation of fibroblast activation protein enzymatic activity attenuates tumor growth. Mol. Cancer Ther. 2005, 4:351-360. 10.1158/1535-7163.MCT-04-0269.
26. Cooper J.K., Schilling G., Peters M.F., Herring W.J., Sharp A.H., Kaminsky Z., Masone J., Khan F.A., Delanoy M., Borchelt D.R., Dawson V.L., Dawson T.M., Ross C.A. Truncated N-terminal fragments of huntingtin with expanded glutamine repeats form nuclear and cytoplasmic aggregates in cell culture. Hum. Mol. Genet. 1998, 7:783-790.
27. Corcos D. Unbalanced replication as a major source of genetic instability in cancer cells. Am. J. Blood Res. 2012, 2:160-169.
28. Crasta K., Ganem N.J., Dagher R., Lantermann A.B., Ivanova E.V., Pan Y., Nezi L., Protopopov A., Chowdhury D., Pellman D. DNA breaks and chromosome pulverization from errors in mitosis. Nature 2012, 482:53-58. 10.1038/nature10802.
29. Cusick J.K., Mustian A., Goldberg K., Reyland M.E. RELT induces cellular death in HEK 293 epithelial cells. Cell. Immunol. 2010, 261:1-8. 10.1016/j.cellimm.2009.10.013.
30. 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.
31. Depontieu F., Grigoriu B.-D., Scherpereel A., Adam E., Delehedde M., Gosset P., Lassalle P. Loss of endocan tumorigenic properties after alternative splicing of exon 2. BMC Cancer 2008, 8:14. 10.1186/1471-2407-8-14.
32. Dereli-Öz A., Versini G., Halazonetis T.D. Studies of genomic copy number changes in human cancers reveal signatures of DNA replication stress. Mol. Oncol. 2011, 5:308-314. 10.1016/j.molonc.2011.05.002.
33. 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.
34. Duesberg P., McCormack A. Immortality of cancers: a consequence of inherent karyotypic variations and selections for autonomy. Cell Cycle 2013, 12:783-802. 10.4161/cc.23720.
35. Duesberg P., Li R., Fabarius A., Hehlmann R. The chromosomal basis of cancer. Cell. Oncol. 2005, 27:293-318.
36. 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.
37. Duesberg P., Mandrioli D., McCormack A., Nicholson J.M. Is carcinogenesis a form of speciation?. Cell Cycle 2011, 10:2100-2114.
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. Foudah D., Redondo J., Caldara C., Carini F., Tredici G., Miloso M. Human mesenchymal stem cells express neuronal markers after osteogenic and adipogenic differentiation. Cell. Mol. Biol. Lett. 2013, 18:163-186. 10.2478/s11658-013-0083-2.
40. Foudah D., Monfrini M., Donzelli E., Niada S., Brini A.T., Orciani M., Tredici G., Miloso M. Expression of neural markers by undifferentiated mesenchymal-like stem cells from different sources. J. Immunol. Res. 2014, 2014:987678. 10.1155/2014/987678.
41. Frias C., Pampalona J., Genesca A., Tusell L. Telomere dysfunction and genome instability. Front. Biosci. 2012, 17:2181-2196.
42. Fu Z., Washbourne P., Ortinski P., Vicini S. Functional excitatory synapses in HEK293 cells expressing neuroligin and glutamate receptors. J. Neurophysiol. 2003, 90:3950-3957. 10.1152/jn.00647.2003.
43. Ganem N.J., Godinho S.A., Pellman D. A mechanism linking extra centrosomes to chromosomal instability. Nature 2009, 460:278-282. 10.1038/nature08136.
44. Gao C., Furge K., Koeman J., Dykema K., Su Y., Cutler M.Lou, Werts A., Haak P., Vande Woude G.F. 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.
45. Geisse S., Fux C. Recombinant protein production by transient gene transfer into mammalian cells. Methods Enzymol. 2009, 463:223-238. 10.1016/S0076-6879(09)63015-9.
46. Genescà A., Pampalona J., Frías C., Domínguez D., Tusell L. Role of telomere dysfunction in genetic intratumor diversity. Adv. Cancer Res. 2011, 10.1016/B978-0-12-387688-1.00002-8.
47. Gilbert S.L., Pehrson J.R., Sharp P.A. XIST RNA associates with specific regions of the inactive X chromatin. J. Biol. Chem. 2000, 275:36491-36494. 10.1074/jbc.C000409200.
48. Gisselsson D., Håkanson U., Stoller P., Marti D., Jin Y., Rosengren A.H., Stewénius 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:e1871. 10.1371/journal.pone.0001871.
49. Gisselsson D., Jin Y., Lindgren D., Persson J., Gisselsson L., Hanks S., Sehic D., Mengelbier L.H., Øra I., Rahman N., Mertens F., Mitelman F., Mandahl N. Generation of trisomies in cancer cells by multipolar mitosis and incomplete cytokinesis. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:20489-20493. 10.1073/pnas.1006829107.
50. Gourley C., Paige A.J.W., Taylor K.J., Ward C., Kuske B., Zhang J., Sun M., Janczar S., Harrison D.J., Muir M., Smyth J.F., Gabra H. 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.
51. Graham F.L., Smiley J., Russell W.C., Nairn R. Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J. Gen. Virol. 1977, 36:59-74.
52. Green R.A., Kaplan K.B. Chromosome instability in colorectal tumor cells is associated with defects in microtubule plus-end attachments caused by a dominant mutation in APC. J. Cell Biol. 2003, 163:949-961. 10.1083/jcb.200307070.
53. Guan L.S., Li G.C., Chen C.C., Liu L.Q., Wang Z.Y. Rb-associated protein 46 (RbAp46) suppresses the tumorigenicity of adenovirus-transformed human embryonic kidney 293 cells. Int. J. Cancer 2001, 93:333-338.
54. 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.
55. Ha S.-A., Kim H.K., Yoo J., Kim S., Shin S.M., Lee Y.S., Hur S.Y., Kim Y.W., Kim T.E., Chung Y.J., Jeun S.S., Kim D.W., Park Y.G., Kim J., Shin S.Y., Lee Y.H., Kim J.W. Transdifferentiation-inducing HCCR-1 oncogene. BMC Cell Biol. 2010, 11:49. 10.1186/1471-2121-11-49.
56. Hamid T., Malik M.T., Kakar S.S. Ectopic expression of PTTG1/securin promotes tumorigenesis in human embryonic kidney cells. Mol. Cancer 2005, 4:3. 10.1186/1476-4598-4-3.
57. He B., Soderlund D.M. Human embryonic kidney (HEK293) cells express endogenous voltage-gated sodium currents and Na v 1.7 sodium channels. Neurosci. Lett. 2010, 469:268-272. 10.1016/j.neulet.2009.12.012.
58. Heng H.H. The genome-centric concept: resynthesis of evolutionary theory. Bioessays 2009, 31:512-525. 10.1002/bies.200800182.
59. 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.
60. 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.
61. Heng H.H., Stevens J.B., Bremer S.W., Liu G., Abdallah B.Y., Ye C.J. Evolutionary mechanisms and diversity in cancer. Adv. Cancer Res. 2011, 112:217-253. 10.1016/B978-0-12-387688-1.00008-9.
62. Heng H.H., Bremer S.W., Stevens J.B., Horne S.D., Liu G., Abdallah B.Y., Ye K.J., Ye C.J. 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.
63. Hong S.-H., Goh S.-H., Lee S.J., Hwang J.-A., Lee J., Choi I.-J., Seo H., Park J.-H., Suzuki H., Yamamoto E., Kim I.-H., Jeong J.S., Ju M.H., Lee D.-H., Lee Y.-S. Upregulation of adenylate cyclase 3 (ADCY3) increases the tumorigenic potential of cells by activating the CREB pathway. Oncotarget 2013, 4:1791-1803.
64. Horne S.D., Stevens J.B., Abdallah B.Y., Liu G., Bremer S.W., Ye C.J., Heng H.H. Why imatinib remains an exception of cancer research. J. Cell. Physiol. 2013, 228:665-670. 10.1002/jcp.24233.
65. Jahan N., Wimmer E., Mueller S. A host-specific, temperature-sensitive translation defect determines the attenuation phenotype of a human rhinovirus/poliovirus chimera, PV1(RIPO). J. Virol. 2011, 85:7225-7235. 10.1128/JVI.01804-09.
66. Jeon B.N., Kim M.K., Choi W.I., Koh D.I., Hong S.Y., Kim K.S., Kim M., Yun C.O., Yoon J., Choi K.Y., Lee K.R., Nephew K.P., Hur M.W. KR-POK interacts with p53 and represses its ability to activate transcription of p21WAF1/CDKN1A. Cancer Res. 2012, 72:1137-1148. 10.1158/0008-5472.CAN-11-2433.
67. Jiang W.G., Grimshaw D., Lane J., Martin T.A., Abounader R., Laterra J., Mansel R.E., Abounder R. 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.
68. Jin J., Woodgett J.R. Chronic activation of protein kinase Bbeta/Akt2 leads to multinucleation and cell fusion in human epithelial kidney cells: events associated with tumorigenesis. Oncogene 2005, 24:5459-5470. 10.1038/sj.onc.1208704.
69. Jin G., Kawsar H.I., Hirsch S.A., Zeng C., Jia X., Feng Z., Ghosh S.K., Zheng Q.Y., Zhou A., McIntyre T.M., Weinberg A. An antimicrobial peptide regulates tumor-associated macrophage trafficking via the chemokine receptor CCR2, a model for tumorigenesis. PLoS One 2010, 5:e10993. 10.1371/journal.pone.0010993.
70. Jo M., Takimoto S., Montel V., Gonias S.L. The urokinase receptor promotes cancer metastasis independently of urokinase-type plasminogen activator in mice. Am. J. Pathol. 2009, 175:190-200. 10.2353/ajpath.2009.081053.
71. Kavsan V.M., Iershov A.V., Balynska O.V. Immortalized cells and one oncogene in malignant transformation: old insights on new explanation. BMC Cell Biol. 2011, 12:23. 10.1186/1471-2121-12-23.
72. Kessler O., Shraga-Heled N., Lange T., Gutmann-Raviv N., Sabo E., Baruch L., Machluf M., Neufeld G. Semaphorin-3F is an inhibitor of tumor angiogenesis. Cancer Res. 2004, 64:1008-1015.
73. Kim S., Burette A., Chung H.S., Kwon S.-K., Woo J., Lee H.W., Kim K., Kim H., Weinberg R.J., Kim E. NGL family PSD-95-interacting adhesion molecules regulate excitatory synapse formation. Nat. Neurosci. 2006, 9:1294-1301. 10.1038/nn1763.
74. Kishore A.H., Batta K., Das C., Agarwal S., Kundu T.K. p53 regulates its own activator: transcriptional co-activator PC4, a new p53-responsive gene. Biochem. J. 2007, 406:437-444.
75. Klein A., Li N., Nicholson J.M., McCormack A.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.
76. Komorek J., Kuppuswamy M., Subramanian T., Vijayalingam S., Lomonosova E., Zhao L.-J., Mymryk J.S., Schmitt K., Chinnadurai G. Adenovirus type 5 E1A and E6 proteins of low-risk cutaneous beta-human papillomaviruses suppress cell transformation through interaction with FOXK1/K2 transcription factors. J. Virol. 2010, 84:2719-2731. 10.1128/JVI.02119-09.
77. Kovesdi I., Hedley S.J. Adenoviral producer cells. Viruses 2010, 2:1681-1703. 10.3390/v2081681.
78. Landry J.J.M., Pyl P.T., Rausch T., Zichner T., Tekkedil M.M., Stütz A.M., Jauch A., Aiyar R.S., Pau G., Delhomme N., Gagneur J., Korbel J.O., Huber W., Steinmetz L.M. The genomic and transcriptomic landscape of a HeLa cell line. G3 (Bethesda) 2013, 3:1213-1224. 10.1534/g3.113.005777.
79. Lee M.-C., Hsieh C.-H., Wei S.-C., Shen S.-C., Chen C.-N., Wu V.-C., Chuang L.-Y., Hsieh F.-J., Wu C.H.H., Tsai-Wu J.-J. Ectopic EBP2 expression enhances cyclin E1 expression and induces chromosome instability in HEK293 stable clones. BMB Rep. 2008, 41:716-721.
80. Leonard J.M., Ye H., Wetmore C., Karnitz L.M. Sonic Hedgehog signaling impairs ionizing radiation-induced checkpoint activation and induces genomic instability. J. Cell Biol. 2008, 183:385-391. 10.1083/jcb.200804042.
81. Letsolo B.T., Rowson J., Baird D.M. Fusion of short telomeres in human cells is characterized by extensive deletion and microhomology, and can result in complex rearrangements. Nucleic Acids Res. 2010, 38:1841-1852. 10.1093/nar/gkp1183.
82. Li A., Zhang X.-S., Jiang J.-H., Wang H.-H., Liu X.-Q., Pan Z.-G., Zeng Y.-X. Transcriptional expression of RPMS1 in nasopharyngeal carcinoma and its oncogenic potential. Cell Cycle 2005, 4:304-309.
83. Li G.-D., Zhang X., Li R., Wang Y.-D., Wang Y.-L., Han K.-J., Qian X.-P., Yang C.-G., Liu P., Wei Q., Chen W.-F., Zhang J., Zhang Y. CHP2 activates the calcineurin/nuclear factor of activated T cells signaling pathway and enhances the oncogenic potential of HEK293 cells. J. Biol. Chem. 2008, 283:32660-32668. 10.1074/jbc.M806684200.
84. Li L., McCormack A.a, Nicholson J.M., Fabarius A., Hehlmann R., Sachs R.K., Duesberg P.H. 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.
85. Lin Y.-C., Boone M., Meuris L., Lemmens I., Van Roy N., Soete A., Reumers J., Moisse M., Plaisance S., Drmanac R., Chen J., Speleman F., Lambrechts D., Van de Peer Y., Tavernier J., Callewaert N. Genome dynamics of the human embryonic kidney 293 lineage in response to cell biology manipulations. Nat. Commun. 2014, 5:4767. 10.1038/ncomms5767.
86. Liu Y.-H., Lin C.-Y., Lin W.-C., Tang S.-W., Lai M.-K., Lin J.-Y. Up-regulation of vascular endothelial growth factor-D expression in clear cell renal cell carcinoma by CD74: a critical role in cancer cell tumorigenesis. J. Immunol. 2008, 181:6584-6594.
87. Liu S.-H., Patel S., Gingras M.-C., Nemunaitis J., Zhou G., Chen C., Li M., Fisher W., Gibbs R., Brunicardi F.C. PDX-1: demonstration of oncogenic properties in pancreatic cancer. Cancer 2011, 117:723-733. 10.1002/cncr.25629.
88. Liu G., Stevens J.B., Horne S.D., Abdallah B.Y., Ye K.J., Bremer S.W., Ye C.J., Chen D.J., Heng H.H. Genome chaos: survival strategy during crisis. Cell Cycle 2014, 13:528-537. 10.4161/cc.27378.
89. Löber C., Lenz-Stöppler C., Dobbelstein M. Adenovirus E1-transformed cells grow despite the continuous presence of transcriptionally active p53. J. Gen. Virol. 2002, 83:2047-2057.
90. Louis N., Evelegh C., Graham F.L. Cloning and sequencing of the cellular-viral junctions from the human adenovirus type 5 transformed 293 cell line. Virology 1997, 233:423-429. 10.1006/viro.1997.8597.
91. Machida K., Liu J.-C., McNamara G., Levine A., Duan L., Lai M.M.C. Hepatitis C virus causes uncoupling of mitotic checkpoint and chromosomal polyploidy through the Rb pathway. J. Virol. 2009, 83:12590-12600. 10.1128/JVI.02643-08.
92. Macias-Perez I.M., Zent R., Carmosino M., Breyer M.D., Breyer R.M., Pozzi A. Mouse EP3 alpha, beta, and gamma receptor variants reduce tumor cell proliferation and tumorigenesis in vivo. J. Biol. Chem. 2008, 283:12538-12545. 10.1074/jbc.M800105200.
93. Macville M., Schröck E., Padilla-nash H., Schro E., Keck C., Ghadimi B.M., Zimonjic D., Popescu N., Ried T. Comprehensive and Definitive Molecular Cytogenetic Characterization of HeLa Cells by Spectral Karyotyping 141-150 1999.
94. Madhusudana S.N., Sundaramoorthy S., Ullas P.T. Utility of human embryonic kidney cell line HEK-293 for rapid isolation of fixed and street rabies viruses: comparison with Neuro-2a and BHK-21 cell lines. Int. J. Infect. Dis. 2010, 14:e1067-e1071. 10.1016/j.ijid.2010.07.004.
95. Maetzel D., Denzel S., Mack B., Canis M., Went P., Benk M., Kieu C., Papior P., Baeuerle P.A., Munz M., Gires O. Nuclear signalling by tumour-associated antigen EpCAM. Nat. Cell Biol. 2009, 11:162-171. 10.1038/ncb1824.
96. Mah W., Ko J., Nam J., Han K., Chung W.S., Kim E. Selected SALM (synaptic adhesion-like molecule) family proteins regulate synapse formation. J. Neurosci. 2010, 30:5559-5568. 10.1523/JNEUROSCI.4839-09.2010.
97. Marthiens V., Piel M., Basto R. Never tear us apart-the importance of centrosome clustering. J. Cell Sci. 2012, 125:3281-3292. 10.1242/jcs.094797.
98. 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.
99. Medendorp K., van Groningen J.J.M., Vreede L., Hetterschijt L., van den Hurk W.H., de Bruijn D.R.H., Brugmans L., van Kessel A.G. The mitotic arrest deficient protein MAD2B interacts with the small GTPase RAN throughout the cell cycle. PLoS One 2009, 4:e7020. 10.1371/journal.pone.0007020.
100. Medendorp K., Vreede L., van Groningen J.J.M., Hetterschijt L., Brugmans L., Jansen P.A.M., van den Hurk W.H., de Bruijn D.R.H., van Kessel A.G. The mitotic arrest deficient protein MAD2B interacts with the clathrin light chain A during mitosis. PLoS One 2010, 5:e15128. 10.1371/journal.pone.0015128.
101. Meir Y.-J.J., Weirauch M.T., Yang H.-S., Chung P.-C., Yu R.K., Wu S.C.-Y. Genome-wide target profiling of piggyBac and Tol2 in HEK 293: pros and cons for gene discovery and gene therapy. BMC Biotechnol. 2011, 11:28. 10.1186/1472-6750-11-28.
102. Mineur P., Colige A.C., Deroanne C.F., Dubail J., Kesteloot F., Habraken Y., Noël A., Vöö S., Waltenberger J., Lapière C.M., Nusgens B.V., Lambert C.A. Newly identified biologically active and proteolysis-resistant VEGF-A isoform VEGF111 is induced by genotoxic agents. J. Cell Biol. 2007, 179:1261-1273. 10.1083/jcb.200703052.
103. Moore J.M., Wimberly H., Thornton P.C., Rosenberg S.M., Hastings P.J. Gross chromosomal rearrangement mediated by DNA replication in stressed cells: evidence from Escherichia coli. Ann. N. Y. Acad. Sci. 2012, 1267:103-109. 10.1111/j.1749-6632.2012.06587.x.
104. Mortusewicz O., Herr P., Helleday T. Early replication fragile sites: where replication-transcription collisions cause genetic instability. EMBO J. 2013, 32:493-495. 10.1038/emboj.2013.20.
105. Mrasek K., Schoder C., Teichmann A.-C., Behr K., Franze B., Wilhelm K., Blaurock N., Claussen U., Liehr T., Weise A. Global screening and extended nomenclature for 230 aphidicolin-inducible fragile sites, including 61 yet unreported ones. Int. J. Oncol. 2010, 36:929-940.
106. Neelsen K.J., Zanini I.M.Y., Herrador R., Lopes M. Oncogenes induce genotoxic stress by mitotic processing of unusual replication intermediates. J. Cell Biol. 2013, 200:699-708. 10.1083/jcb.201212058.
107. 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.
108. Ozeri-Galai E., Bester A.C., Kerem B. The complex basis underlying common fragile site instability in cancer. Trends Genet. 2012, 28:295-302. 10.1016/j.tig.2012.02.006.
109. Perner S., Brüderlein S., Hasel C., Waibel I., Holdenried A., Ciloglu N., Chopurian H., Nielsen K.V., Plesch A., Högel J., Möller P. Quantifying telomere lengths of human individual chromosome arms by centromere-calibrated fluorescence in situ hybridization and digital imaging. Am. J. Pathol. 2003, 163:1751-1756. 10.1016/S0002-9440(10)63534-1.
110. Péterfia B., Füle T., Baghy K., Szabadkai K., Fullár A., Dobos K., Zong F., Dobra K., Hollósi P., Jeney A., Paku S., Kovalszky I. 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.
111. Pirazzoli V., Ferraris G.M.S., Sidenius N. Direct evidence of the importance of vitronectin and its interaction with the urokinase receptor in tumor growth. Blood 2013, 121:2316-2323. 10.1182/blood-2012-08-451187.
112. Pradhan A., Singh T.R., Ali A.M., Wahengbam K., Meetei A.R. Monopolar spindle 1 (MPS1) protein-dependent phosphorylation of RecQ-mediated genome instability protein 2 (RMI2) at serine 112 is essential for BLM-Topo III α-RMI1-RMI2 (BTR) protein complex function upon spindle assembly checkpoint (SAC) activation during mitosis. J. Biol. Chem. 2013, 288:33500-33508. 10.1074/jbc.M113.470823.
113. Quiñones A., Rainov N.G. Identification of genotoxic stress in human cells by fluorescent monitoring of p53 expression. Mutat. Res. 2001, 494:73-85.
114. 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.
115. Roschke A.V., Stover K., Tonon G., Schäffer A.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.
116. Sakakura H., Murakumo Y., Mii S., Hagiwara S., Kato T., Asai M., Hoshino A., Yamamoto N., Sobue S., Ichihara M., Ueda M., Takahashi M. Detection of a soluble form of CD109 in serum of CD109 transgenic and tumor xenografted mice. PLoS One 2014, 9:e83385. 10.1371/journal.pone.0083385.
117. Saldivar J.C., Miuma S., Bene J., Hosseini S.A., Shibata H., Sun J., Wheeler L.J., Mathews C.K., Huebner K. Initiation of genome instability and preneoplastic processes through loss of Fhit expression. PLoS Genet. 2012, 8:e1003077. 10.1371/journal.pgen.1003077.
118. Salsi V., Ferrari S., Gorello P., Fantini S., Chiavolelli F., Mecucci C., Zappavigna V. NUP98 fusion oncoproteins promote aneuploidy by attenuating the mitotic spindle checkpoint. Cancer Res. 2014, 74:1079-1090. 10.1158/0008-5472.CAN-13-0912.
119. Sansregret L., Vadnais C., Livingstone J., Kwiatkowski N., Awan A., Cadieux C., Leduy L., Hallett M.T., Nepveu A. Cut homeobox 1 causes chromosomal instability by promoting bipolar division after cytokinesis failure. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:1949-1954. 10.1073/pnas.1008403108.
120. Sarkar S., Kantara C., Ortiz I., Swiercz R., Kuo J., Davey R., Escobar K., Ullrich R., Singh P. Progastrin overexpression imparts tumorigenic/metastatic potential to embryonic epithelial cells: phenotypic differences between transformed and nontransformed stem cells. Int. J. Cancer 2012, 131:E1088-E1099. 10.1002/ijc.27615.
121. Scherpereel A., Gentina T., Grigoriu B., Sénéchal S., Janin A., Tsicopoulos A., Plénat F., Béchard D., Tonnel A.-B., Lassalle P. Overexpression of endocan induces tumor formation. Cancer Res. 2003, 63:6084-6089.
122. Shaw G., Morse S., Ararat M., Graham F.L. Preferential transformation of human neuronal cells by human adenoviruses and the origin of HEK 293 cells. FASEB J. 2002, 16:869-871. 10.1096/fj.01-0995fje.
123. Shen C., Gu M., Song C., Miao L., Hu L., Liang D., Zheng C. The tumorigenicity diversification in human embryonic kidney 293 cell line cultured in vitro. Biologicals 2008, 36:263-268. 10.1016/j.biologicals.2008.02.002.
124. Silkworth W.T., Cimini D. Transient defects of mitotic spindle geometry and chromosome segregation errors. Cell Div. 2012, 7:19. 10.1186/1747-1028-7-19.
125. Singhmar P., Kumar A. Angelman syndrome protein UBE3A interacts with primary microcephaly protein ASPM, localizes to centrosomes and regulates chromosome segregation. PLoS One 2011, 6:e20397. 10.1371/journal.pone.0020397.
126. Skoog T., Elomaa O., Pasonen-Seppänen S.M., Forsberg S., Ahokas K., Jeskanen L., Pärssinen J., Tiala I., Rollman O., Lohi J., Saarialho-Kere U. 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.
127. Stavropoulou V., Xie J., Henriksson M., Tomkinson B., Imreh S., Masucci M.G. Mitotic infidelity and centrosome duplication errors in cells overexpressing tripeptidyl-peptidase II. Cancer Res. 2005, 65:1361-1368. 10.1158/0008-5472.CAN-04-2085.
128. Stepanenko, Kavsan V.M. Immortalization and malignant transformation of eukaryotic cells. Cytol. Genet. 2012, 46:96-129. 10.3103/S0095452712020041.
129. Stepanenko A.A., Kavsan V.M. Cancer Genes and Chromosome Instability. Oncogene and Cancer - From Bench to Clinic 2013, 151-182. InTech Publisher.
130. 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.
131. 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.
132. Stepanenko A., Andreieva S., Korets K., Mykytenko D., Huleyuk N., Vassetzky Y., Kavsan V. Step-wise and punctuated genome evolution drive phenotype changes of tumor cells. Mutat. Res. Fundam. Mol. Mech. Mutagen. 2015, 771:56-69. 10.1016/j.mrfmmm.2014.12.006.
133. 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.
134. Stevens J.B., Liu G., Abdallah B.Y., Horne S.D., Ye K.J., Bremer S.W., Ye C.J., Krawetz S.A., Heng H.H. Unstable genomes elevate transcriptome dynamics. Int. J. Cancer 2014, 134:2074-2087. 10.1002/ijc.28531.
135. Stewénius Y., Gorunova L., Jonson T., Larsson N., Höglund M., Mandahl N., Mertens F., Mitelman F., 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. 2005, 102:5541-5546. 10.1073/pnas.0408454102.
136. Su G., Zhao Y., Wei J., Han J., Chen L., Xiao Z., Chen B., Dai J. The effect of forced growth of cells into 3D spheres using low attachment surfaces on the acquisition of stemness properties. Biomaterials 2013, 34:3215-3222. 10.1016/j.biomaterials.2013.01.044.
137. Suzuki H., Akiyama N., Tsuji M., Ohashi T., Saito S., Eto Y. Human Shugoshin mediates kinetochore-driven formation of kinetochore microtubules. Cell Cycle 2006, 5:1094-1101.
138. Ter Elst A., Hiemstra B.E., van der Vlies P., Kamminga W., van der Veen A.Y., Davelaar I., Terpstra P., te Meerman G.J., Gerbens F., Kok K., Buys C.H.C.M. Functional analysis of lung tumor suppressor activity at 3p21.3. Genes Chromosom. Cancer 2006, 45:1077-1093. 10.1002/gcc.20367.
139. Thomas P., Smart T.G. HEK293 cell line: a vehicle for the expression of recombinant proteins. J. Pharmacol. Toxicol. Methods 2005, 51:187-200. 10.1016/j.vascn.2004.08.014.
140. Torban E., Goodyer P.R. Effects of PAX2 expression in a human fetal kidney (HEK293) cell line. Biochim. Biophys. Acta 1998, 1401:53-62.
141. Tse H.T.K., Weaver W.M., Di Carlo D. Increased asymmetric and multi-daughter cell division in mechanically confined microenvironments. PLoS One 2012, 7:e38986. 10.1371/journal.pone.0038986.
142. Ueno T., Elmberger G., Weaver T.E., Toi M., Linder S. The aspartic protease napsin A suppresses tumor growth independent of its catalytic activity. Lab. Invest. 2008, 88:256-263. 10.1038/labinvest.3700718.
143. Varghese A., Tenbroek E.M., Coles J., Sigg D.C. Endogenous channels in HEK cells and potential roles in HCN ionic current measurements. Prog. Biophys. Mol. Biol. 2006, 90:26-37. 10.1016/j.pbiomolbio.2005.05.002.
144. Vetter I., Lewis R.J. Characterization of endogenous calcium responses in neuronal cell lines. Biochem. Pharmacol. 2010, 79:908-920. 10.1016/j.bcp.2009.10.020.
145. Wang Y.-L., Wang Y., Tong L., Wei Q. Overexpression of calcineurin B subunit (CnB) enhances the oncogenic potential of HEK293 cells. Cancer Sci. 2008, 99:1100-1108. 10.1111/j.1349-7006.2008.00799.x.
146. 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.
147. Woo J., Kwon S.-K., Choi S., Kim S., Lee J.-R., Dunah A.W., Sheng M., Kim E. Trans-synaptic adhesion between NGL-3 and LAR regulates the formation of excitatory synapses. Nat. Neurosci. 2009, 12:428-437. 10.1038/nn.2279.
148. Wu Q., Sahasrabudhe R.M., Luo L.Z., Lewis D.W., Gollin S.M., Saunders W.S. Deficiency in myosin light-chain phosphorylation causes cytokinesis failure and multipolarity in cancer cells. Oncogene 2010, 29:4183-4193. 10.1038/onc.2010.165.
149. Xiao H., Yu Z., Wu Y., Nan J., Merry D.E., Sekiguchi J.M., Ferguson D.O., Lieberman A.P., Dressler G.R. A polyglutamine expansion disease protein sequesters PTIP to attenuate DNA repair and increase genomic instability. Hum. Mol. Genet. 2012, 21:4225-4236. 10.1093/hmg/dds246.
150. Yang C., Shi X., Huang Y., Zhang Z., Cooke H.J., Wang M., Shi Q. Rapid proliferation of daughter cells lacking particular chromosomes due to multipolar mitosis promotes clonal evolution in colorectal cancer cells. Cell Cycle 2012, 11:2650-2659. 10.4161/cc.20976.
151. Yung L.Y., Lam W.S., Ho M.K.C., Hu Y., Ip F.C.F., Pang H., Chin A.C., Harley C.B., Ip N.Y., Wong Y.H. Astragaloside IV and cycloastragenol stimulate the phosphorylation of extracellular signal-regulated protein kinase in multiple cell types. Planta Med. 2012, 78:115-121. 10.1055/s-0031-1280346.
152. Zhang Q., Fan H., Shen J., Hoffman R.M., Xing H.R. Human breast cancer cell lines co-express neuronal, epithelial, and melanocytic differentiation markers in vitro and in vivo. PLoS One 2010, 5:e9712. 10.1371/journal.pone.0009712.
153. Zhang L., Wu H., Lu D., Li G., Sun C., Song H., Li J., Zhai T., Huang L., Hou C., Wang W., Zhou B., Chen S., Lu B., Zhang X. The costimulatory molecule B7-H4 promote tumor progression and cell proliferation through translocating into nucleus. Oncogene 2013, 32:5347-5358. 10.1038/onc.2012.600.
154. Zhou W.-J., Geng Z.H., Chi S., Zhang W., Niu X.-F., Lan S.-J., Ma L., Yang X., Wang L.-J., Ding Y.-Q., Geng J.-G. Slit-Robo signaling induces malignant transformation through Hakai-mediated E-cadherin degradation during colorectal epithelial cell carcinogenesis. Cell Res. 2011, 21:609-626. 10.1038/cr.2011.17.