Advertisement

Cytology and Genetics

, Volume 48, Issue 3, pp 180–188 | Cite as

Chromosomal damage as prognosis marker in cervical carcinogenesis

  • E. I. Cortés-GutiérrezEmail author
  • M. I. Dávila-Rodríguez
  • R. M. Cerda-Flores
Article

Abstract

Cancer of the uterine cervix is the third most common cancer in women worldwide and the most common cancer among Mexican and Latin American women. Risk factors that have been associated with the development of cervical intraepithelial neoplasia suggest that Human Papillomavirus (HPV) types 16, 18, 31, and 33 entail a high risk of developing a malignancy of this type. The accumulation of genetic alterations allows the growth of neoplastic cells; chromosomal instability is an event that occurs in the precancerous stages. The candidate cancer risk biomarkers include cytogenetic endpoints, such as chromosomal aberrations, sister chromatid exchange, micronuclei, and the outcomes of comet assay and DNA breakage detection-fluorescence in situ hybridization. The patterns identified in these cytogenetic studies indicate that chromosomal instability is a transient and chromosomally unstable intermediate in the development of cervical lesions. In this context, the mechanisms that may underlie the progressive increase in genetic instability in these patients seem to be related directly to HPV infection. The studies discussed in this paper show that chromosomal instability may serve as a biomarker by predicting the progression of cervical intraepithelial neoplasia. Nevertheless, these results should be validated in larger, prospective studies.

Keywords

chromosomal instability cervical cancer biomarker 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Mohar, A. and FrÍas-MendÍvil, M., Epidemiology of cervical cancer, Cancer Invest., 2000, vol. 18, no. 6, pp. 584–590.PubMedCrossRefGoogle Scholar
  2. 2.
    Solomo, D., Schiffman, M., and Tarone, R., Comparison of three management strategies of patients with atypical squamous cell of undertermined significance: baseline results from a randomized trial, J. Natl. Cancer Inst., 2001, vol. 93, no. 4, pp. 293–299.CrossRefGoogle Scholar
  3. 3.
    Patten, S.F., Diagnostic Cytology of the Uterine Cervix, Baser: Karger, 1978, vol. 3.Google Scholar
  4. 4.
    Herrington, C.S., Human papillomavirus and cervical neoplasia. I. Classification, virology, pathology, and epidemiology, J. Clin. Pathol., 1994, vol. 4, no. 12, pp. 1066–1072.CrossRefGoogle Scholar
  5. 5.
    Hsu, T.C., Cherry, L.M., and Saaman, N.A., Differential mutagen susceptibility in cultured lymphocytes of normal individuals and cancer patients, Cancer Genet. Cytogenet., 1985, vol. 17, no. 4, pp. 307–313.PubMedCrossRefGoogle Scholar
  6. 6.
    McKenna, D.J., McKeown, S.R., and McKelvery-Martin, V.J., Potential use of the comet assay in the clinical management of cancer, Mutagenesis, 2008, vol. 23, no. 3, pp. 183–190.PubMedCrossRefGoogle Scholar
  7. 7.
    Valverde, M. and Rojas, E., Environmental and occupational biomonitoring using the comet assay, Mutat. Res., 2009, vol. 681, no. 1, pp. 93–109.PubMedCrossRefGoogle Scholar
  8. 8.
    Jianlin, I., Jiliang, H., Lifen, J., and Hongping, D., Measuring the genetic damage in cancer patients during radiotherapy with three genetic end-points, Mutagenesis, 2004, vol. 19, no. 6, pp. 457–464.PubMedCrossRefGoogle Scholar
  9. 9.
    Heim, S., Alimena, G., Billstrom, R., and Mitelman, F., Tetraploid karyotype (92, XXYY) in two patients with acute lymphoblastic leukaemia, Cancer Genet. Cytogenet., 1987, vol. 29, no. 1, pp. 129–133.PubMedCrossRefGoogle Scholar
  10. 10.
    Singh, M., Mehrotra, S., Kalra, N., and Shukla, Y., Correlation of DNA ploidy with progression of cervical cancer, J. Cancer Epidemiol., 2008, vol. 2008, pp. 298–495.CrossRefGoogle Scholar
  11. 11.
    Olaharski, A.J., Sotelo, R., Solorza-Luna, G., and Eastmond, D.A., Tetraploidy and chromosomal instability are early events during cervical carcinogenesis, Carcinogenesis, 2006, vol. 27, no. 2, pp. 337–343.PubMedCrossRefGoogle Scholar
  12. 12.
    Atkin, N.B., Cytogenetics of carcinoma of the cervix uterine: a review, Cancer Genet. Cytogenet., 1997, vol. 95, no. 1, pp. 33–39.PubMedCrossRefGoogle Scholar
  13. 13.
    Cortés-Gutiérrez, E.I., Dávila-Rodríguez, M.I., Muraira-Rodríguez, M., and Cerda-Flores, R.M., Association between the stages of cervical cancer and chromosome 1 aneusomy, Cancer Genet. Cytogenet., 2005, vol. 159, no. 1, pp. 44–47.PubMedCrossRefGoogle Scholar
  14. 14.
    Wang, X., Zheng, B., Zhang, R.R., and Liu, H., Automated analysis of fluorescent in situ hybridization (FISH) labeled genetic biomarkers in assisting cervical cancer diagnosis, Technol. Cancer Res. Treat., 2010, vol. 9, no. 3, pp. 231–242.PubMedCentralPubMedGoogle Scholar
  15. 15.
    Cheung, T.H., Chung, T.K., Poon, C.S., and Wong, Y.F., Allelic loss on chromosome 1 is associated with tumor progression of cervical carcinoma, Cancer, 1999, vol. 86, no. 7, pp. 1294–1298.PubMedCrossRefGoogle Scholar
  16. 16.
    Segers, P., Haesen, S., Castelain, P., and Kirsch-Volders, M., Study of numerical aberrations of chromosome 1 by fluorescent in situ hybridization and DNA content by densitometric analysis on (pre)-malignant cervical lesions, Histochem. J, 1995, vol. 27, no. 1, pp. 24–34.PubMedCrossRefGoogle Scholar
  17. 17.
    Segers, P., Haesen, S., Amy, J.J., and Kirsch-Volders, M., Detection of premalignant stages in cervical smears with a biotinylated probe for chromosome 1, Cancer Genet. Cytogenet., 1994, vol. 75, no. 2, pp. 120–129.PubMedCrossRefGoogle Scholar
  18. 18.
    Kurtycz, D., Nucez, M., Bauman, C., and Meisner, L., Use of fluorescent in situ hybridization to detect aneuploidy in cervical dysplasia, Diagn. Cytopathol., 1996, vol. 15, no. 1, pp. 46–51.PubMedCrossRefGoogle Scholar
  19. 19.
    Mian, C., Bancher, D., Kohlberger, P., et al., Fluorescence in situ hybridization in cervical smears: detection of numerical aberrations of chromosomes 7, 3, and X and relationship to HPV infection, Gynecol. Oncol., 1999, vol. 75, no. 1, pp. 41–46.PubMedCrossRefGoogle Scholar
  20. 20.
    Southern, S.A. and Herrington, C.S., Interphase karyotypic analysis of chromosomes 11, 17 and X in invasive squamous-cell carcinoma of the cervix: morphological correlation with HPV infection, Int. J. Cancer, 1997, vol. 70, no. 5, pp. 502–507.PubMedCrossRefGoogle Scholar
  21. 21.
    Hariu, H. and Matsuta, M., Cervical cytology by means of fluorescence in situ hybridization with a set of chromosome-specific DNA probes, J. Obstet. Checat. Res., 1996, vol. 22, no. 2, pp. 163–170.CrossRefGoogle Scholar
  22. 22.
    Le, B.M., Molecular biology of cancer cytogenetics, in Cancer: Principles and Practice of Oncology, De, V.T., Hellman, S., and Rosenberg, S.A., Eds., Lippincott-Raven Publ., 1997, vol. 1, pp. 103–119.Google Scholar
  23. 23.
    Murty, V.V., Mitra, A.B., and Luthra, U.K., Spontaneous chromosomal aberrations in patients with precancerous and cancerous lesions of the cervix uteri, Cancer Genet. Cytogenet., 1985, vol. 1, no. 4, pp. 347–353.CrossRefGoogle Scholar
  24. 24.
    Cooke, D., Allen, J., Clare, M.G., and Hederson, L., Statistical methods for sister chromatid exchange experiments, in Statistical Evaluation of Mutagenicity Test Data, Kirkland, D.J., Ed., Cambridge: Univ. Press, 1989, vol. 1, pp. 155–183.Google Scholar
  25. 25.
    Carrano, A.V., Thompson, L.H., Lindl, P.A., and Minkler, J.L., Sister chromatid exchange as an indicator of mutagenesis, Nature, 1978, vol. 271, no. 5645, pp. 551–553.PubMedCrossRefGoogle Scholar
  26. 26.
    Skolnick, M., Livingston, G.K., Fineman, R.M., et al., Genetics of breast cancer: genealogical clusters, major genes, linkage and sister chromatid exchange as a preclinical marker, Am. J. Hum. Genet., 1980, vol. 32, no. 1, p. A151.Google Scholar
  27. 27.
    Nordenson, I., Beckman, L., Liden, S., and Stjernber, N., Chromosomal aberrations and cancer risk, Hum. Hered., 1984, vol. 34, no. 2, pp. 76–81.PubMedCrossRefGoogle Scholar
  28. 28.
    Mitra, A.B., Murty, V.V., and Luthra, U.K., Sister chromatid exchange in leukocytes of patients with cancer of cervix uteri, Hum. Genet., 1982, vol. 60, no. 3, pp. 214–215.PubMedCrossRefGoogle Scholar
  29. 29.
    Murty, V.V., Mitra, A.B., Luthra, U.K., and Sing, I.P., Sister chromatid exchanges in patients with precancerous and cancerous lesions of cervix uteri, Hum. Genet., 1986, vol. 72, no. 1, pp. 37–42.PubMedCrossRefGoogle Scholar
  30. 30.
    Lukovic, L. and Milassin, J., Sister chromatid exchanges in patients with carcinoma in situ of cervix uteri, Cancer Genet. Cytogenet., 1992, vol. 59, no. 1, pp. 84–85.PubMedCrossRefGoogle Scholar
  31. 31.
    Dhillon, V.S., Kler, R.S., and Dhillon, I.K., Chromosome instability and sister chromatid exchange (SCE) studies in patients with carcinoma of cervix uteri, Cancer Genet. Cytogenet., 1996, vol. 86, no. 1, pp. 54–57.PubMedCrossRefGoogle Scholar
  32. 32.
    Yokota, K., Ueda, K., and Fujiwara, A., Increased spontaneous and mitomicin C-induced sister chromatid exchanges in patients with cancer of the cervix uteri, with special reference to stage of cancer, Cancer Genet. Cytogenet., 1989, vol. 43, no. 1, pp. 79–97.PubMedCrossRefGoogle Scholar
  33. 33.
    Capalash, N. and Sobti, R.C., Spontaneous genomic fragility and cell cycle progression in lymphocytes of patients with cervical carcinoma, Cancer Genet. Cytogenet., 1996, vol. 88, no. 1, pp. 30–44.PubMedCrossRefGoogle Scholar
  34. 34.
    Cortés-Gutiérrez, E.I., Cerda-Flores, R.M., and Leal-Garza, C.H., Sister chromatid exchanges in peripheral lymphocytes from women with carcinoma of the uterine cervix, Cancer Genet. Cytogenet., 2000, vol. 122, no. 2, pp. 121–123.PubMedCrossRefGoogle Scholar
  35. 35.
    Adhvaryu, S.G., Vyas, R.C., Dave, B.J., and Parkh, B.N., Spontaneous and induced sister chromatic exchange frequencies and cell cycle progression in lymphocytes of patients with carcinoma of the uterine cervix, Cancer Genet. Cytogenet., 1985, vol. 14, nos. 1/2, pp. 67–72.PubMedCrossRefGoogle Scholar
  36. 36.
    Holland, N., Bolognesi, C., Kirsch-Volders, M., et al., The micronucleus assay in human buccal cells as a tool for biomonitoring DNA damage: the HUMN project perspective on current status and knowledge gaps, Mutat. Res., 2008, vol. 659, nos. 1/2, pp. 93–108.PubMedCrossRefGoogle Scholar
  37. 37.
    Delfino, V., Casartelli, G., Garzoglio, B., et al., Micronuclei and p53 accumulation in preneoplastic and malignant lesions in the head and neck, Mutagenesis, 2002, vol. 17, no. 1, pp. 73–77.PubMedCrossRefGoogle Scholar
  38. 38.
    Casartelli, G., Bonatti, S., De Ferrari, M., et al., Micronucleus frequencies in exfoliated buccal cells in normal mucosa, precancerous lesions and squamous cell carcinoma, Anal. Quant. Cytol. Histol., 2000, vol. 22, no. 6, pp. 486–492.PubMedGoogle Scholar
  39. 39.
    Desai, S.S., Ghaisas, S.D., Jakhi, S.D., and Bhide, S.V., Cytogenetic damage in exfoliated oral mucosal cells and circulating lymphocytes of patients suffering from precancerous oral lesions, Cancer Lett., 1996, vol. 109, nos. 1/2, pp. 9–14.CrossRefGoogle Scholar
  40. 40.
    Rajeswari, N., Ahuja, Y.R., Malini, U., et al., Risk assessment in first degree female relatives of breast cancer patients using the alkaline comet assay, Carcinogenesis, 2000, vol. 21, no. 4, pp. 557–561.PubMedCrossRefGoogle Scholar
  41. 41.
    Saran, R., Tiwari, R.K., Reddy, P.P., and Ahuja, Y.R., Risk assessment of oral cancer in patients with pre-cancerous states of the oral cavity using micronucleus test and challenge assay, Oral. Oncol., 2008, vol. 44, no. 7, pp. 354–360.PubMedCrossRefGoogle Scholar
  42. 42.
    Larmarcovai, G., Ceppi, M., Botta, A., and Bonassi, S., Micronuclei frequency in peripheral blood lymphocytes of cancer patients: a meta-analysis, Mutat. Res., 2008, vol. 659, no. 3, pp. 274–283.CrossRefGoogle Scholar
  43. 43.
    Fenech, M. and Morley, A.A., Cytokinesis-block micronucleus method in human lymphocytes: effect of in vivo ageing and low-dose X-irradiation, Mutat. Res., 1986, vol. 161, no. 2, pp. 193–198.PubMedCrossRefGoogle Scholar
  44. 44.
    Tolbert, P.E., Shy, C.M., and Allen, J.W., Micronuclei and other nuclear anomalies in buccal smears: methods development, Mutat. Res., 1992, vol. 271, no. 1, pp. 69–77.PubMedCrossRefGoogle Scholar
  45. 45.
    Nersesyan, A.K., Possible role of the micronucleus assay in diagnostics and secondary prevention of cervix cancer: a minireview, Cytol. Genet., 2007, vol. 41, no. 5, pp. 317–318.CrossRefGoogle Scholar
  46. 46.
    Guzman, P., Sotelo-Regil, R.C., Mohar, A., and Gonsebat, M.E., Positive correlation between the frequency of micronucleated cells and dysplasia in Papanicolaou smears, Environ. Mol. Mutagen., 2003, vol. 41, no. 5, pp. 339–343.PubMedCrossRefGoogle Scholar
  47. 47.
    Leal-Garza, C.H., Cerda-Flores, R.M., Leal-Garza, C.H., and Cortés-Gutiérrez, E.I., Micronuclei in cervical smears and peripheral blood lymphocytes from women with and without cervical uterine cancer, Mutat. Res., 2002, vol. 25, nos. 1/2, pp. 57–62.CrossRefGoogle Scholar
  48. 48.
    Bonassi, S., Zhaor, A., Ceppi, M., et al., An increased micronucleus frequency in peripheral blood lymphocytes predicts the risk of cancer in humans, Carcinogenesis, 2007, vol. 28, no. 3, pp. 625–631.PubMedCrossRefGoogle Scholar
  49. 49.
    Norppa, H., Bonassi, S., Hansteen, I.L., et al., Chromosomal aberrations and SCEs as biomarkers of cancer risk, Mutat. Res., 2006, vol. 600, nos. 1/2, pp. 37–45.PubMedCrossRefGoogle Scholar
  50. 50.
    Chakrabarti, R.N. and Dutta, K., Micronuclei test in routine smears from uterine cervix, Eur. J. Gynaecol. Oncol., 1988, vol. 9, no. 5, pp. 370–372.PubMedGoogle Scholar
  51. 51.
    Cerqueira, E.M., Santoro, C.L., Donozo, N.F., and Machado-Santelli, G.M., Genetic damage in exfoliated cells of the uterine cervix. Association and interaction between cigarette smoking and progression to malignant transformation, Acta Cytol., 1998, vol. 42, no. 3, pp. 639–649.PubMedCrossRefGoogle Scholar
  52. 52.
    Campos, L.M.R., Dias, F.L., Antunes, L.M., and Murta, E.F., Prevalence of micronuclei in exfoliated uterine cervical cells from patients with risk factors for cervical cancer, Sao Paulo Med. J., 2008, vol. 126, no. 6, pp. 323–328.Google Scholar
  53. 53.
    Aires, G.M., Meireles, J.R., Oliveira, P.C., et al., Micronuclei as biomarkers for evaluating the risk of malignant transformation in the uterine cervix, Genet. Mol. Res., 2011, vol. 10, no. 3, pp. 1558–1564.PubMedCrossRefGoogle Scholar
  54. 54.
    Samanta, S., Dey, P., and Nijhawan, R., Micronucleus in cervical intraepithelial lesions and carcinoma, Acta Cytol., 2011, vol. 55, no. 1, pp. 42–47.PubMedCrossRefGoogle Scholar
  55. 55.
    Samanta, S., Dey, P., Gupta, N., and Nijhawan, R., Micronucleus in atypical squamous cell of undetermined significance, Diagn. Cytopathol., 2010, vol. 39, no. 4, pp. 242–244.CrossRefGoogle Scholar
  56. 56.
    Murgia, E., Ballardin, M., Bonassi, S., and Barale, R., Validation of micronuclei frequency in peripheral blood lymphocytes as early cancer risk biomarker in a nested case-control study, Mutat. Res., 2008, vol. 639, nos. 1/2, pp. 27–34.CrossRefGoogle Scholar
  57. 57.
    Bonassi, S., Ugolini, D., Kirsch-Volders, M., et al., Human population studies with cytogenetic biomarkers: review of the literature and future prospectives, Environ. Mol. Mutagen., 2005, vol. 45, nos. 2/3, pp. 258–270.CrossRefGoogle Scholar
  58. 58.
    Udumudi, A., Jaiswal, M., Rajeswari, N., et al., Risk assessment in cervical dysplasia patients by single cell gel electrophoresis assay: a study of DNA damage and repair, Mutat. Res., 1998, vol. 30, no. 2, pp. 195–205.CrossRefGoogle Scholar
  59. 59.
    Cortés-Gutiérrez, E.I., Dávila-RodrÍguez, M.I., Zamudio-González, E.A., et al., DNA damage in Mexican women with cervical dysplasia evaluated by comet assay, Anal. Quant. Cytol. Histol., 2010, vol. 32, no. 4, pp. 207–213.PubMedGoogle Scholar
  60. 60.
    Fernández, J.L., Goyanes, V., Ramiro-Diaz, J., and Gosálvez, J., Application of fish for in situ detection and quantification of DNA breakage, Cytogenet. Cell Genet., 1998, vol. 82, nos. 3/4, pp. 251–256.PubMedGoogle Scholar
  61. 61.
    Fernández, J.L., Vázquez, G.F., Rivero, M.T., et al., DBD-FISH on neutral comets: simultaneous analysis of DNA single- and double-strand breaks in individual cells, Exp. Cell Res., 2001, vol. 270, no. 1, pp. 102–109.PubMedCrossRefGoogle Scholar
  62. 62.
    Fernández, J.L. and Gosálvez, J., Application of FISH to detect DNA damage: DNA breakage detection FISH (DBD-FISH), Meth. Mol. Biol., 2002, vol. 203, no. 1, pp. 203–216.Google Scholar
  63. 63.
    Cortés-Gutiérrez, E.I., Dávila-RodrÍguez, M.I., López-Fernández, C., et al., Alkali-labile sites in sperm cells from Sus and Ovis species, Int. J. Androl., 2008, vol. 31, no. 3, pp. 354–363.PubMedCrossRefGoogle Scholar
  64. 64.
    Darzynkiewicz, Z., Huang, X., and Okafuji, M., Detection of DNA strand breaks by flow and laser scanning cytometry in studies of apoptosis and cell proliferation (DNA replication), Meth. Mol. Biol., 2006, vol. 314, no. 1, pp. 81–93.CrossRefGoogle Scholar
  65. 65.
    Gore, J., Bryant, Z., Nollmann, M., et al., DNA overwinds when stretched, Nature, 2006, vol. 442, no. 7104, pp. 836–839.PubMedCrossRefGoogle Scholar
  66. 66.
    Fernández, J.L., Vazquez, G.F., Rivero, M.T., et al., Evidence of abundant constitutive alkali-labile sites in human 5 bp classical satellite DNA loci by DBD-FISH, Mutat. Res., 2001, vol. 473, no. 2, pp. 163–168.PubMedCrossRefGoogle Scholar
  67. 67.
    Rivero, M.T., Vazquez-GundÍn, F., Goyanes, V., et al., High frequency of constitutive alkali-labile sites in mouse major satellite DNA, detected by DNA breakage detection-fluorescence in situ hybridization, Mutat. Res., 2001, vol. 483, nos. 1/2, pp. 43–50.PubMedCrossRefGoogle Scholar
  68. 68.
    Rivero, M.T., Mosquera, A., Goyanes, V., and Fernández, J.L., Differences in repair profiles of interstitial telomeric sites between normal and DNA doublestrand ALS in mammalian sperm break repair deficient Chinese hamster cells, Exp. Cell Res., 2004, vol. 295, no. 1, pp. 161–172.PubMedCrossRefGoogle Scholar
  69. 69.
    López-Fernández, C., Arroyo, F., Fernández, J.L., and Gosálvez, J., Interstitial telomeric sequence blocks in constitutive pericentromeric heterochromatin from Pyrgomorpha conica (Orthoptera) are enriched in constitutive alkali-labile sites, Mutat. Res., 2006, vol. 599, nos. 1/2, pp. 36–44.CrossRefGoogle Scholar
  70. 70.
    Cortés-Gutiérrez, E.I., Dávila-Rodríguez, E.I., Fernández, J.L., and Gosálvez, J., DNA damage in women with cervical neoplasia evaluated by DNA breakage detection-fluorescence in situ hybridization, Anal. Quant. Cytol. Histol., 2001, vol. 33, no. 3, pp. 175–181.Google Scholar
  71. 71.
    Fenech, M. and Rinaldi, J., The relationship between micronuclei in human lymphocytes and plasma levels of vitamin C, vitamin E, vitamin B12 and folic acid, Carcinogenesis, 1994, vol. 15, no. 7, pp. 1405–1411.PubMedCrossRefGoogle Scholar
  72. 72.
    Titenko, H.N., Jacob, R.A., Shang, N., and Smith, M.T., Micronuclei in lymphocytes and exfoliated buccal cells of postmenopausal women with dietary changes in folate, Mutat. Res., 1998, vol. 417, nos. 2/3, pp. 101–114.CrossRefGoogle Scholar
  73. 73.
    Chen, Y.C. and Hunter, D.J., Molecular epidemiology of cancer, Cancer J. Clin., 2005, vol. 55, no. 1, pp. 45–54.CrossRefGoogle Scholar
  74. 74.
    Alvarez, R.R., Rodriguez, A.J., Arboleda-Moreno, Y.Y., et al., Chromosome aberrations in peripheral blood lymphocytes of high-risk HPV-infected women with HGSIL, Environ. Mol. Mutagen., 2008, vol. 49, no. 9, pp. 688–694.CrossRefGoogle Scholar
  75. 75.
    Cortés-Gutiérrez, E.I., Dávila-RodrÍguez, M.I., Vargas-Villarreal, J., and Cerda-Flores, R.M., Association between human papilloma virus-type infections with micronuclei frequencies, Prague. Med. Rep., 2010, vol. 111, no. 1, pp. 35–41.PubMedGoogle Scholar
  76. 76.
    Bierkens, M., Wilting, S.M., Wieringen, V., et al., Chromosomal profiles of high-grade cervical intraepithelian neoplasia relate to duration of preceding high-risk human papillomavirus infection, Int. J. Cancer, 2011, vol. 131, no. 4, pp. E579–585.PubMedCrossRefGoogle Scholar
  77. 77.
    Duensing, S. and Münger, K., Mechanisms of genomic instability in human cancer, insights from studies with human papillomavirus oncoproteins, Int. J. Cancer, 2004, vol. 109, no. 2, pp. 157–162.PubMedCrossRefGoogle Scholar
  78. 78.
    Pett, M. and Coleman, N., Integration of high-risk human papillomavirus: a key event in cervical carcinogenesis, J. Pathol., 2007, vol. 212, no. 4, pp. 356–367.PubMedCrossRefGoogle Scholar
  79. 79.
    Korzeniewski, N., Spardy, N., Duensing, A., and Duensing, S., Genomic instability and cancer: lessons learned from human papillomaviruses, Cancer Lett., 2011, vol. 305, no. 2, pp. 113–122.PubMedCentralPubMedCrossRefGoogle Scholar
  80. 80.
    Popescu, N.C., Zimonjic, D., and Dipaolo, J.A., Viral integration, fragile sites and proto-oncogenes in human neoplasia, Hum. Genet., 1990, vol. 84, no. 5, pp. 383–386.PubMedCrossRefGoogle Scholar
  81. 81.
    Wilczynski, S.P., Walker, J., Liao, S.Y., and Berman, M., Adenocarcinoma of the cervix associated with human papillomavirus, Cancer, 1988, vol. 62, no. 7, pp. 1331–1336.PubMedCrossRefGoogle Scholar
  82. 82.
    Ozkal, P., Ilgin-Ruhi, H., Akdogan, M., and Sasmaz, N., The genotoxic effects of hepatitis B virus to host DNA, Mutagenesis, 2005, vol. 20, no. 2, pp. 147–150.PubMedCrossRefGoogle Scholar
  83. 83.
    Pan, H., Zhou, F., and Gao, S.J., Kaposi’s sarcoma-associated herpesvirus induction of chromosome instability in primary human endothelial cells, Cancer Res., 2004, vol. 64, no. 12, pp. 4064–4068.PubMedCrossRefGoogle Scholar
  84. 84.
    Majone, F., Luisetto, R., Zamboni, D., et al., Ku protein as a potential human T-cell leukemia virus type 1 (HTLV-1) Tax target in clastogenic chromosomal instability of mammalian cells, Retrovirology, 2005, vol. 2, no. 1, p. 45.PubMedCentralPubMedCrossRefGoogle Scholar
  85. 85.
    Van Wijnen, A.J., Bidwell, J.P., Fey, E.G., et al., Nuclear matrix association of multiple sequence-specific DNA binding activities related to SP-1, ATF, CCAAT, C/EBP, OCT-1, and AP-1, Biochemistry, 1993, vol. 32, no. 33, pp. 8397–8402.PubMedCrossRefGoogle Scholar
  86. 86.
    Lee, K.A., Shim, J.H., Kho, C.W., et al., Protein profiling and identification of modulators regulated by the nE7 oncogene in the c33a cell line by proteomics and genomics, Proteomics, 2004, vol. 4, no. 3, pp. 839–848.PubMedCrossRefGoogle Scholar

Copyright information

© Allerton Press, Inc. 2014

Authors and Affiliations

  • E. I. Cortés-Gutiérrez
    • 1
    Email author
  • M. I. Dávila-Rodríguez
    • 1
  • R. M. Cerda-Flores
    • 2
  1. 1.Department of Genetics, Centro de Investigación Biomédica del NoresteInstituto Mexicano del Seguro SocialMonterreyMéxico
  2. 2.Facultad de EnfermeríaUniversidad Autónoma de Nuevo LeónMonterreyMéxico

Personalised recommendations