The PDZ binding motif of human papillomavirus type 16 E6 induces PTPN13 loss, which allows anchorage-independent growth and synergizes with ras for invasive growth

Journal of Virology

Volumn 82, Issue 5, 2008, Pages 2493-2500

  Spanos, William C ^a   Hoover, Andrew ^a   Harris, George F ^a   Wu, Shu ^a   Strand, Guinevere L ^a   Anderson, Mary E ^a   Klingelhutz, Aloysius J ^b   Hendriks, Wiljan ^c   Bossler, Aaron D ^a   Lee, John H ^a  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF IOWA   (United States)

^c RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ONCOPROTEIN; PAPILLOMAVIRUS E6 PROTEIN; PDZ PROTEIN; PROTEIN TYROSINE PHOSPHATASE; RAS PROTEIN; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COLORECTAL CARCINOMA; CONTROLLED STUDY; CORRELATION ANALYSIS; GENOME ANALYSIS; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS TYPE 16; IN VIVO STUDY; MOUSE; NONHUMAN; ONCOGENE; ONCOGENE RAS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; VIROGENESIS; VIRUS GENE;

ANIMALS; BINDING SITES; CELL ADHESION; CELL DIVISION; HUMANS; MICE; NEOPLASM INVASIVENESS; PAPILLOMAVIRIDAE; PROTEIN TYROSINE PHOSPHATASE, NON-RECEPTOR TYPE 13; PROTO-ONCOGENE PROTEINS P21(RAS);

HUMAN PAPILLOMAVIRUS; HUMAN PAPILLOMAVIRUS TYPE 16;

EID: 39749192555     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.02188-07     Document Type: Article

References (44)

1. Alonio, L. V., M. A. Picconi, D. Dalbert, J. Mural, O. Bartt, G. Bazan, M. Dominguez, and A. R. Teyssie. 2003. Ha-ras oncogene mutation associated to progression of papillomavirus induced lesions of uterine cervix. J. Clin. Virol. 27:263-269.
2. Berger, K. L., F. Barriga, M. J. Lace, L. P. Turek, G. J. Zamba, F. E. Domann, J. H. Lee, and A. J. Klingelhutz. 2006. Cervical keratinocytes containing stably replicating extrachromosomal HPV-16 are refractory to transformation by oncogenic H-Ras. Virology 356:68-78.
3. Cuppen, E., S. Nagata, B. Wieringa, and W. Hendriks. 1997. No evidence for involvement of mouse protein-tyrosine phosphatase-BAS-like Fas-associated phosphatase-1 in Fas-mediated apoptosis. J. Biol. Chem. 272:30215-30220.
4. Cuppen, E., M. Wijers, J. Schepens, J. Fransen, B. Wieringa, and W. Hendriks. 1999. A FERM domain governs apical confinement of PTP-BL in epithelial cells. J. Cell Sci. 112(Pt. 19):3299-3308.
5. Dalal, S., Q. Gao, E. J. Androphy, and V. Band. 1996. Mutational analysis of human papillomavirus type 16 E6 demonstrates that p53 degradation is necessary for immortalization of mammary epithelial cells. J. Virol. 70:683-688.
6. Douma, S., T. Van Laar. J. Zevenhoven, R. Meuwissen, E. Van Garderen, and D. S. Peeper. 2004. Suppression of anoikis and induction of metastasis by the neurotrophic receptor TrkB. Nature 430:1034-1039.
7. Erdmann, K. S. 2003. The protein tyrosine phosphatase PTP-Basophil/Basophil-like. Interacting proteins and molecular functions. Eur. J. Biochem. 270:4789-4798.
8. Foster, S. A., G. W. Demers, B. G. Etscheid, and D. A. Galloway. 1994. The ability of human papillomavirus E6 proteins to target p53 for degradation in vivo correlates with their ability to abrogate actinomycin D-induced growth arrest. J. Virol. 68:5698-5705.
9. Frangioni, J. V., and B. G. Neel. 1993. Solubilization and purification of enzymatically active glutathione S-transferase (pGEX) fusion proteins. Anal. Biochem. 210:179-187.
10. Frisch, M., R. J. Biggar, and J. J. Goedert. 2000. Human papillomavirus-associated cancers in patients with human immunodeficiency virus infection and acquired immunodeficiency syndrome. J. Natl. Cancer Inst. 92:1500-1510.
11. Frisch, S. M., and R. A. Screaton. 2001. Anoikis mechanisms. Curr. Opin. Cell Biol. 13:555-562.
12. Gardiol, D., C. Kuhne, B. Glaunsinger, S. S. Lee, R. Javier, and L. Banks. 1999. Oncogenic human papillomavirus E6 proteins target the discs large tumour suppressor for proteasome-mediated degradation. Oncogene 18:5487-5496.
13. Glaunsinger, B. A., S. S. Lee, M. Thomas, L. Banks, and R. Javier. 2000. Interactions of the PDZ-protein MAGI-1 with adenovirus E4-ORF1 and high-risk papillomavirus E6 oncoproteins. Oncogene 19:5270-5280.
14. Halbert, C. L., G. W. Demers, and D. A. Galloway. 1991. The E7 gene of human papillomavirus type 16 is sufficient for immortalization of human epithelial cells. J. Virol. 65:473-478.
15. Hendriks, W., J. Schepens, D. Bachner, J. Rijss, P. Zeeuwen, U. Zechner, H. Hameister, and B. Wieringa. 1995. Molecular cloning of a mouse epithelial protein-tyrosine phosphatase with similarities to submembranous proteins. J. Cell. Biochem. 59:418-430.
16. Higgins, G. D., D. M. Uzelin, G. E. Phillips, and C. J. Burrell. 1991. Presence and distribution of human papillomavirus sense and antisense RNA transcripts in genital cancers. J. Gen. Virol. 72(Pt. 4):885-895.
17. Higgins, G. D., D. M. Uzelin, G. E. Phillips, P. McEvoy, R. Marin, and C. J. Burrell. 1992. Transcription patterns of human papillomavirus type 16 in genital intraepithelial neoplasia: evidence for promoter usage within the E7 open reading frame during epithelial differentiation. J. Gen. Virol. 73(Pt. 8):2047-2057.
18. Hoffman, H. T., L. H. Karnell, G. F. Funk, R. A. Robinson, and H. R. Menck. 1998. The National Cancer Data Base report on cancer of the head and neck. Arch. Otolaryngol. Head Neck Surg. 124:951-962.
19. Hoover, A. C., W. C. Spanos, G. F. Harris, M. E. Anderson, A. J. Klingelhutz, and J. H. Lee. 2007. The role of human papillomavirus 16 E6 in anchorage-independent and invasive growth of mouse tonsil epithelium. Arch. Otolaryngol. Head Neck Surg. 133:495-502.
20. Ioka, A., H. Tsukuma, W. Ajiki, and A. Oshima. 2005. Trends in head and neck cancer incidence in Japan during 1965-1999. Jpn. J. Clin. Oncol. 35:45-47.
21. Ivanov, V. N., Z. Ronai, and T. K. Hei. 2006. Opposite roles of FAP-1 and dynamin in the regulation of Fas (CD95) translocation to the cell surface and susceptibility to Fas ligand-mediated apoptosis. J. Biol. Chem. 281:1840-1852.
22. Jing, M., J. Bohl, N. Brimer, M. Kinter, and S. B. Vande Pol. 2007. Degradation of tyrosine phosphatase PTPN3 (PTPH1) by association with oncogenic human papillomavirus E6 proteins. J. Virol. 81:2231-2239.
23. Kalyankrishna, S., and J. R. Grandis. 2006. Epidermal growth factor receptor biology in head and neck cancer. J. Clin. Oncol. 24:2666-2672.
24. Khan, A. J., B. L. King, B. D. Smith, G. L. Smith, M. P. DiGiovanna, D. Carter, and B. G. Haffty. 2002. Characterization of the HER-2/neu oncogene by immunohistochemical and fluorescence in situ hybridization analysis in oral and oropharyngeal squamous cell carcinoma. Clin. Cancer Res. 8:540-548.
25. Kiyono, T., A. Hiraiwa, M. Fujita, Y. Hayashi, T. Akiyama, and M. Ishibashi. 1997. Binding of high-risk human papillomavirus E6 oncoproteins to the human homologue of the Drosophila discs large tumor suppressor protein. Proc. Natl. Acad. Sci. USA 94:11612-11616.
26. Klingelhutz, A. J., S. A. Foster, and J. K. McDougall. 1996. Telomerase activation by the E6 gene product of human papillomavirus type 16. Nature 380:79-82.
27. Kreimer, A. R., G. M. Clifford, P. Boyle, and S. Franceschi. 2005. Human papillomavirus types in head and neck squamous cell carcinomas worldwide: a systematic review. Cancer Epidemiol. Biomarkers Prev. 14:467-475.
28. Lanham, S., A. Herbert, and P. Watt. 2001. HPV detection and measurement of HPV-16, telomerase, and survivin transcripts in colposcopy clinic patients. J. Clin. Pathol. 54:304-308.
29. Lee, J. H., S. M. Yi, M. E. Anderson, K. L. Berger, M. J. Welsh, A. J. Klingelhutz, and M. A. Ozbun. 2004. Propagation of infectious human papillomavirus type 16 by using an adenovirus and Cre/LoxP mechanism. Proc. Natl. Acad. Sci. USA 101:2094-2099.
30. Lee, S. S., B. Glaunsinger, F. Mantovani, L. Banks, and R. T. Javier. 2000. Multi-PDZ domain protein MUPP1 is a cellular target for both adenovirus E4-ORF1 and high-risk papillomavirus type 18 E6 oncoproteins. J. Virol. 74:9680-9693.
31. Lorber, B., W. J. Hendriks, C. E. Van der Zee, M. Berry, and A. Logan. 2005. Effects of LAR and PTP-BL phosphatase deficiency on adult mouse retinal cells activated by lens injury. Eur. J. Neurosci. 21:2375-2383.
32. Lu, S. L., H. Herrington, D. Reh, S. Weber, S. Bornstein, D. Wang, A. G. Li, C. F. Tang, Y. Siddiqui, J. Nord, P. Andersen, C. L. Corless, and X. J. Wang. 2006. Loss of transforming growth factor-beta type II receptor promotes metastatic head-and-neck squamous cell carcinoma. Genes Dev. 20:1331-1342.
33. Nakagawa, S., and J. M. Huibregtse. 2000. Human scribble (Vartul) is targeted for ubiquitin-mediated degradation by the high-risk papillomavirus E6 proteins and the E6AP ubiquitin-protein ligase. Mol. Cell. Biol. 20:8244-8253.
34. Ritchie, J. M., E. M. Smith, K. F. Summersgill, H. T. Hoffman, D. Wang, J. P. Klussmann, L. P. Turek, and T. H. Haugen. 2003. Human papillomavirus infection as a prognostic factor in carcinomas of the oral cavity and oropharynx. Int. J. Cancer 104:336-344.
35. Scheffner, M., J. M. Huibregtse, R. D. Vierstra, and P. M. Howley. 1993. The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell 75:495-505.
36. Schreiber, K., R. E. Cannon, T. Karrison, G. Beck-Engeser, D. Huo, R. W. Tennant, H. Jensen, W. M. Kast, T. Krausz, S. C. Meredith, L. Chen, and H. Schreiber. 2004. Strong synergy between mutant ras and HPV16 E6/E7 in the development of primary tumors. Oncogene 23:3972-3979.
37. Simonson, S. J., M. J. Difilippantonio, and P. F. Lambert. 2005. Two distinct activities contribute to human papillomavirus 16 E6's oncogenic potential. Cancer Res. 65:8266-8273.
38. Smith, E. M., J. M. Ritchie, K. F. Summersgill, J. P. Klussmann, J. H. Lee, D. Wang, T. H. Haugen, and L. P. Turek. 2004. Age, sexual behavior and human papillomavirus infection in oral cavity and oropharyngeal cancers. Int. J. Cancer 108:766-772.
39. Spanos, W. C., M. El-Deiry, and J. H. Lee. 2005. Cidofovir incorporation into human keratinocytes with episomal HPV 16 results in nonselective cytotoxicity. Ann. Otol. Rhinol. Laryngol. 114:840-846.
40. Spanos, W. C., J. Gieger, G. F. Harris, A. Bossler, R. B. Smith, A. Klingelhutz, and J. H. Lee. 2007. Deletion of the PDZ motif of HPV16 E6 preventing immortalization and anchorage-independent growth in human tonsil epithelial cells. Head Neck [Epub ahead of print.] doi:10.1002/hed.20673.
41. Thomas, M., R. Laura, K. Hepner, E. Guccione, C. Sawyers, L. Lasky, and L. Banks. 2002. Oncogenic human papillomavirus E6 proteins target the MAGI-2 and MAGI-3 proteins for degradation. Oncogene 21:5088-5096.
42. Villa, F., M. Deak, G. B. Bloomberg, D. R. Alessi, and D. M. van Aalten. 2005. Crystal structure of the PTPL1/FAP-1 human tyrosine phosphatase mutated in colorectal cancer: evidence for a second phosphotyrosine substrate recognition pocket. J. Biol. Chem. 280:8180-8187.
43. Wang, Z., D. Shen, D. W. Parsons, A. Bardelli, J. Sager, S. Szabo, J. Ptak, N. Silliman, B. A. Peters, M. S. van der Heijden, G. Parmigiani, H. Yan, T. L. Wang, G. Riggins, S. M. Powell, J. K. Willson, S. Markowitz, K. W. Kinzler, B. Vogelstein, and V. E. Velculescu. 2004. Mutational analysis of the tyrosine phosphatome in colorectal cancers. Science 304:1164-1166.
44. Wansink, D. G., W. Peters, I. Schaafsma, R. P. Sutmuller, F. Oerlemans, G. J. Adema, B. Wieringa, C. E. van der Zee, and W. Hendriks. 2004. Mild impairment of motor nerve repair in mice lacking PTP-BL tyrosine phosphatase activity. Physiol. Genomics 19:50-60.