Table of Contents Author Guidelines Submit a Manuscript
Journal of Oncology
Volume 2010, Article ID 530130, 10 pages
http://dx.doi.org/10.1155/2010/530130
Research Article

Locking Src/Abl Tyrosine Kinase Activities Regulate Cell Differentiation and Invasion of Human Cervical Cancer Cells Expressing E6/E7 Oncoproteins of High-Risk HPV

1Segal Cancer Centre, Lady Davis Institute for Medical Research of the Sir Mortimer B. Davis-Jewish General Hospital, Davis-Jewish General Hospital, McGill University, 3755, Ch. de la Cote Ste-Catherine, Montreal, QC, Canada H3T 1E2
2Faculty of Pharmacy, University of Aleppo, Aleppo, Syria
3Syrian Research Cancer Center of the Syrian Society against Cancer, Aleppo, Syria
4Department of Clinical Medicine and Prevention, University of Milano-Bicocca, 20052 Monza, Italy
5Department of Mechanical Engineering, Concordia University, Montreal, QC, Canada H4B 1R2
6Department of Oncology, Faculty of Medicine, McGill University, QC, H3G1M8, Canada

Received 2 March 2010; Revised 16 June 2010; Accepted 6 July 2010

Academic Editor: Therese Deramaudt

Copyright © 2010 Amber Yasmeen et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. N. Muñoz, F. X. Bosch, X. Castellsagué et al., “Against which human papillomavirus types shall we vaccinate and screen? The international perspective,” International Journal of Cancer, vol. 111, no. 2, pp. 278–285, 2004. View at Publisher · View at Google Scholar · View at Scopus
  2. W. A. A. Tjalma, T. R. Van Waes, L. E. M. Van den Eeden, and J. J. P. M. Bogers, “Role of human papillomavirus in the carcinogenesis of squamos cell carcinoma and adenocarcinoma of the cervix,” Best Practice & Research: Clinical Obstetrics & Gynaecology, vol. 19, no. 4, pp. 469–483, 2005. View at Publisher · View at Google Scholar · View at Scopus
  3. S. de Sanjosé, M. Diaz, X. Castellsagué et al., “Worldwide prevalence and genotype distribution of cervical human papillomavirus DNA in women with normal cytology: a meta-analysis,” The Lancet Infectious Diseases, vol. 7, no. 7, pp. 453–459, 2007. View at Publisher · View at Google Scholar · View at Scopus
  4. S. M. Schwartz, J. R. Daling, K. A. Shera et al., “Human papillomavirus and prognosis of invasive cervical cancer: a population-based study,” Journal of Clinical Oncology, vol. 19, no. 7, pp. 1906–1915, 2001. View at Google Scholar · View at Scopus
  5. G. M. Clifford, J. S. Smith, M. Plummer, N. Muñoz, and S. Franceschi, “Human papillomavirus types in invasive cervical cancer worldwide: a meta-analysis,” British Journal of Cancer, vol. 88, no. 1, pp. 63–69, 2003. View at Publisher · View at Google Scholar · View at Scopus
  6. X. Castellsagué, M. Diaz, S. de Sanjosé et al., “Worldwide human papillomavirus etiology of cervical adenocarcinoma and its cofactors: implications for screening and prevention,” Journal of the National Cancer Institute, vol. 98, no. 5, pp. 303–315, 2006. View at Publisher · View at Google Scholar · View at Scopus
  7. J. S. Smith, L. Lindsay, B. Hoots et al., “Human papillomavirus type distribution in invasive cervical cancer and high-grade cervical lesions: a meta-analysis update,” International Journal of Cancer, vol. 121, no. 3, pp. 621–632, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. K. H. Vousden, “Regulation of the cell cycle by viral oncoproteins,” Seminars in Cancer Biology, vol. 6, no. 2, pp. 109–116, 1995. View at Google Scholar · View at Scopus
  9. M. Scheffner, J. M. Huibregtse, R. D. Vierstra, and P. M. Howley, “The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53,” Cell, vol. 75, no. 3, pp. 495–505, 1993. View at Publisher · View at Google Scholar · View at Scopus
  10. N. Dyson, P. M. Howley, K. Munger, and E. Harlow, “The human papilloma virus-16 E7 oncoprotein is able to bind to the retinoblastoma gene product,” Science, vol. 243, no. 4893, pp. 934–937, 1989. View at Google Scholar · View at Scopus
  11. N. Dyson, P. Guida, K. Munger, and E. Harlow, “Homologous sequences in adenovirus E1A and human papillomavirus E7 proteins mediate interaction with the same set of cellular proteins,” Journal of Virology, vol. 66, no. 12, pp. 6893–6902, 1992. View at Google Scholar · View at Scopus
  12. Y. Kang and J. Massagué, “Epithelial-mesenchymal transitions: twist in development and metastasis,” Cell, vol. 118, no. 3, pp. 277–279, 2004. View at Publisher · View at Google Scholar · View at Scopus
  13. J. P. Thiery and M. Morgan, “Breast cancer progression with a twist,” Nature Medicine, vol. 10, no. 8, pp. 777–778, 2004. View at Publisher · View at Google Scholar · View at Scopus
  14. L. Kopfstein and G. Christofori, “Metastasis: cell-autonomous mechanisms versus contributions by the tumor microenvironment,” Cellular and Molecular Life Sciences, vol. 63, no. 4, pp. 449–468, 2006. View at Publisher · View at Google Scholar · View at Scopus
  15. A. Yasmeen, T. A. Bismar, and A.-E. Al Moustafa, “ErbB receptors and epithelial-cadherin-catenin complex in human carcinomas,” Future Oncology, vol. 2, no. 6, pp. 765–781, 2006. View at Publisher · View at Google Scholar · View at Scopus
  16. A. Wodarz and I. Näthke, “Cell polarity in development and cancer,” Nature Cell Biology, vol. 9, no. 9, pp. 1016–1024, 2007. View at Publisher · View at Google Scholar · View at Scopus
  17. A.-E. Al Moustafa, A. Kassab, A. Darnel, and A. Yasmeen, “High-risk HPV/ErbB-2 interaction on E-cadherin/catenin regulation in human carcinogenesis,” Current Pharmaceutical Design, vol. 14, no. 22, pp. 2159–2172, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. A. H. Klopp, A. Jhingran, L. Ramdas et al., “Gene expression changes in cervical squamous cell carcinoma after initiation of chemoradiation and correlation with clinical outcome,” International Journal of Radiation Oncology Biology Physics, vol. 71, no. 1, pp. 226–236, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. M. C. Frame, “Src in cancer: deregulation and consequences for cell behaviour,” Biochimica et Biophysica Acta, vol. 1602, no. 2, pp. 114–130, 2002. View at Publisher · View at Google Scholar · View at Scopus
  20. Ö. Alper and E. T. Bowden, “Novel insights into c-Src,” Current Pharmaceutical Design, vol. 11, no. 9, pp. 1119–1130, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. A.-E. Al Moustafa, W. D. Foulkes, N. Benlimame et al., “E6/E7 proteins of HPV type 16 and ErbB-2 cooperate to induce neoplastic transformation of primary normal oral epithelial cells,” Oncogene, vol. 23, no. 2, pp. 350–358, 2004. View at Publisher · View at Google Scholar · View at Scopus
  22. M. Puttini, A. M. L. Coluccia, F. Boschelli et al., “In vitro and in vivo activity of SKI-606, a novel Src-Abl inhibitor, against imatinib-resistant Bcr-Abl+ neoplastic cells,” Cancer Research, vol. 66, no. 23, pp. 11314–11322, 2006. View at Publisher · View at Google Scholar · View at Scopus
  23. H. Jallal, M.-L. Valentino, G. Chen, F. Boschelli, S. Ali, and S. A. Rabbani, “A Src/Abl kinase inhibitor, SKI-606, blocks breast cancer invasion, growth, and metastasis in vitro and in vivo,” Cancer Research, vol. 67, no. 4, pp. 1580–1588, 2007. View at Publisher · View at Google Scholar · View at Scopus
  24. A. M. L. Coluccia, D. Benati, H. Dekhil, A. De Filippo, C. Lan, and C. Gambacorti-Passerini, “SKI-606 decreases growth and motility of colorectal cancer cells by preventing pp60(c-Src)-dependent tyrosine phosphorylation of β-catenin and its nuclear signaling,” Cancer Research, vol. 66, no. 4, pp. 2279–2286, 2006. View at Publisher · View at Google Scholar · View at Scopus
  25. J. Zhang, S. Kalyankrishna, M. Wislez et al., “Src-family kinases are activated in non-small cell lung cancer and promote the survival of epidermal growth factor receptor-dependent cell lines,” American Journal of Pathology, vol. 170, no. 1, pp. 366–376, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. A. Goncalves, M. Fabbro, C. Lhommé et al., “A phase II trial to evaluate gefitinib as second- or third-line treatment in patients with recurring locoregionally advanced or metastatic cervical cancer,” Gynecologic Oncology, vol. 108, no. 1, pp. 42–46, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. A. Yasmeen, T. A. Bismar, H. Dekhil et al., “ErbB-2 receptor cooperates with E6/E7 oncoproteins of HPV type 16 in breast tumorigenesis,” Cell Cycle, vol. 6, no. 23, pp. 2939–2943, 2007. View at Google Scholar · View at Scopus
  28. F. M. Johnson and G. E. Gallick, “Src family nonreceptor tyrosine kinases as molecular targets for cancer therapy,” Anti-Cancer Agents in Medicinal Chemistry, vol. 7, no. 6, pp. 651–659, 2007. View at Publisher · View at Google Scholar · View at Scopus
  29. R. Schmidmaier and P. Baumann, “ANTI-ADHESION evolves to a promising therapeutic concept in oncology,” Current Medicinal Chemistry, vol. 15, no. 10, pp. 978–990, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. M. D. Basson, “An intracellular signal pathway that regulates cancer cell adhesion in response to extracellular forces,” Cancer Research, vol. 68, no. 1, pp. 2–4, 2008. View at Publisher · View at Google Scholar · View at Scopus
  31. Z. Yang, R. Bagheri-Yarmand, R.-A. Wang et al., “The epidermal growth factor receptor tyrosine kinase inhibitor ZD1839 (Iressa) suppresses c-Src and Pak1 pathways and invasiveness of human cancer cells,” Clinical Cancer Research, vol. 10, no. 2, pp. 658–667, 2004. View at Publisher · View at Google Scholar · View at Scopus
  32. S. Rodrigues, S. Attoub, Q.-D. Nguyen et al., “Selective abrogation of the proinvasive activity of the trefoil peptides pS2 and spasmolytic polypeptide by disruption of the EGF receptor signaling pathways in kidney and colonic cancer cells,” Oncogene, vol. 22, no. 29, pp. 4488–4497, 2003. View at Publisher · View at Google Scholar · View at Scopus
  33. E. J. Lee, S. H. Who, N. K. Jeon, and J. Kim, “The epidermal growth factor receptor tyrosine kinase inhibitor ZD1839 (Iressa) suppresses proliferation and invasion of human oral squamous carcinoma cells via p53 independent and MMP, uPAR dependent mechanism,” Annals of the New York Academy of Sciences, vol. 1095, pp. 113–128, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. D. Raben, C. Bianco, V. Damiano et al., “Antitumor activity of ZD6126, a novel vascular-targeting agent, is enhanced when combined with ZD1839, an epidermal growth factor receptor tyrosine kinase inhibitor, and potentiates the effects of radiation in a human non-small cell lung cancer xenograft model,” Molecular Cancer Therapeutics, vol. 3, no. 8, pp. 977–983, 2004. View at Google Scholar · View at Scopus
  35. D. Takabatake, T. Fujita, T. Shien et al., “Tumor inhibitory effect of gefitinib (ZD1839, Iressa) and taxane combination therapy in EGFR-overexpressing breast cancer cell lines (MCF7/ADR, MDA-MB-231),” International Journal of Cancer, vol. 120, no. 1, pp. 181–188, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. A.-E. Al Moustafa, W. D. Foulkes, A. Wong et al., “Cyclin D1 is essential for neoplastic transformation induced by both E6/E7 and E6/E7/ErbB-2 cooperation in normal cells,” Oncogene, vol. 23, no. 30, pp. 5252–5256, 2004. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Yasmeen, A. N. Hosein, Q. Yu, and A.-E. Al Moustafa, “Critical role for D-type cyclins in cellular transformation induced by E6/E7 of human papillomavirus type 16 and E6/E7/ErbB-2 cooperation,” Cancer Science, vol. 98, no. 7, pp. 973–977, 2007. View at Publisher · View at Google Scholar · View at Scopus
  38. A. Vultur, R. Buettner, C. Kowolik et al., “SKI-606 (bosutinib), a novel Src kinase inhibitor, suppresses migration and invasion of human breast cancer cells,” Molecular Cancer Therapeutics, vol. 7, no. 5, pp. 1185–1194, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. M. Graflund, B. Sorbe, S. Sigurdardóttir, and M. Karlsson, “HPV-DNA, vascular space invasion, and their impact on the clinical outcome in early-stage cervical carcinomas,” International Journal of Gynecological Cancer, vol. 14, no. 5, pp. 896–902, 2004. View at Publisher · View at Google Scholar · View at Scopus
  40. R. E. Zuna, R. A. Allen, W. E. Moore, R. Mattu, and S. T. Dunn, “Comparison of human papillomavirus genotypes in high-grade squamous intraepithelial lesions and invasive cervical carcinoma: evidence for differences in biologic potential of precursor lesions,” Modern Pathology, vol. 17, no. 11, pp. 1314–1322, 2004. View at Publisher · View at Google Scholar · View at Scopus
  41. L. Sherman, A. Jackman, H. Itzhaki, M. C. Stöppler, D. Koval, and R. Schlegel, “Inhibition of serum- and calcium-induced differentiation of human keratinocytes by HPV16 E6 oncoprotein: role of p53 inactivation,” Virology, vol. 237, no. 2, pp. 296–306, 1997. View at Publisher · View at Google Scholar · View at Scopus
  42. A. Longatto Filho, A. Albergaria, J. Paredes, M. A. R. Moreira, F. Milanezi, and F. C. Schmitt, “P-cadherin expression in glandular lesions of the uterine cervix detected by liquid-based cytology,” Cytopathology, vol. 16, no. 2, pp. 88–93, 2005. View at Publisher · View at Google Scholar · View at Scopus
  43. S. Kabukcuoglu, S. S. Ozalp, U. Oner, M. F. Açikalin, O. T. Yalcin, and E. Colak, “Fascin, an actin-bundling protein expression in cervical neoplasms,” European Journal of Gynaecological Oncology, vol. 26, no. 6, pp. 636–641, 2005. View at Google Scholar · View at Scopus
  44. A. D. Darnel, D. Wang, L. Ghabreau et al., “Correlation between the presence of high-risk human papillomaviruses and Id gene expression in Syrian women with cervical cancer,” Clinical Microbiology and Infection, vol. 16, no. 3, pp. 262–266, 2010. View at Publisher · View at Google Scholar · View at Scopus
  45. K. Nakamura, A. Hongo, J. Kodama, Y. Miyagi, M. Yoshinouchi, and T. Kudo, “Down-regulation of the insulin-like growth factor I receptor by antisense RNA can reverse the transformed phenotype of human cervical cancer cell lines,” Cancer Research, vol. 60, no. 3, pp. 760–765, 2000. View at Google Scholar · View at Scopus
  46. M. Manavi, G. Hudelist, A. Fink-Retter, D. Gschwandtler-Kaulich, K. Pischinger, and K. Czerwenka, “Gene profiling in Pap-cell smears of high-risk human papillomavirus-positive squamous cervical carcinoma,” Gynecologic Oncology, vol. 105, no. 2, pp. 418–426, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. J. Zhurinsky, M. Shtutman, and A. Ben-Ze'ev, “Differential mechanisms of LEF/TCF family-dependent transcriptional activation by β-catenin and plakoglobin,” Molecular and Cellular Biology, vol. 20, no. 12, pp. 4238–4252, 2000. View at Publisher · View at Google Scholar · View at Scopus
  48. J. Lilien and J. Balsamo, “The regulation of cadherin-mediated adhesion by tyrosine phosphorylation/dephosphorylation of β-catenin,” Current Opinion in Cell Biology, vol. 17, no. 5, pp. 459–465, 2005. View at Publisher · View at Google Scholar · View at Scopus