The high-risk HPV E6 target scribble (hScrib) is required for HPV E6 expression in cervical tumour-derived cell lines

Papillomavirus Research

Volumn 2, Issue , 2016, Pages 70-77

  Kranjec, Christian ^a   Tomaić, Vjekoslav ^b   Massimi, Paola ^b   Nicolaides, Lietta ^a   Doorbar, John ^a   Banks, Lawrence ^b  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

Author keywords

HPV E6; HScrib; Protein translation; S6 kinase

Indexed keywords

CELL PROTEIN; PROTEIN E6; PROTEIN HDLG; S6 KINASE; SCRIBBLE PROTEIN; UNCLASSIFIED DRUG; DNA BINDING PROTEIN; E6 PROTEIN, HUMAN PAPILLOMAVIRUS TYPE 18; MEMBRANE PROTEIN; ONCOPROTEIN; SCRIB PROTEIN, HUMAN; TUMOR SUPPRESSOR PROTEIN;

ARTICLE; CELL POLARITY; CONTROLLED STUDY; FEMALE; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; MALIGNANT TRANSFORMATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STABILITY; PROTEIN TARGETING; SIGNAL TRANSDUCTION; TRANSLATION REGULATION; UTERINE CERVIX CANCER; VIRUS CELL INTERACTION; WART VIRUS; BIOSYNTHESIS; GENE EXPRESSION REGULATION; HELA CELL LINE; HOST PATHOGEN INTERACTION; HUMAN PAPILLOMAVIRUS TYPE 18; METABOLISM; PHYSIOLOGY;

DNA-BINDING PROTEINS; GENE EXPRESSION REGULATION; HELA CELLS; HOST-PATHOGEN INTERACTIONS; HUMAN PAPILLOMAVIRUS 18; HUMANS; MEMBRANE PROTEINS; ONCOGENE PROTEINS, VIRAL; RIBOSOMAL PROTEIN S6 KINASES; SIGNAL TRANSDUCTION; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEINS;

EID: 84963599545     PISSN: None     EISSN: 24058521     Source Type: Journal    
DOI: 10.1016/j.pvr.2016.04.001     Document Type: Article

References (44)

1. zur Hausen H. Papillomaviruses in the causation of human cancer - a brief historical account. Virology 2009, 384:26-265.
2. Hartwig S., Baldauf J.-J., Dominiak-Felden G., Simondon F., Alemany L., de Sanjose S., Castellsague X. Estimation of the epidemiological burden of HPV-related anogenital cancers, precancerous lesions and gential warts in women and men in Europe: potential additional benefits of nine-valent second generation HPV vaccine compared to first generation HPV vaccines. Papillomavirus Res. 2015, 1:90-100.
3. Yoshinouchi M., Yamada T., Kizaki M., Fen J., Koseki T., Ikeda Y., Nishihara T., Yamato K. In vitro and in vivo growth suppression of human papillomavirus 16-positive cervical cancer cells by E6 siRNA. Mol Ther. 2003, 8:762-768.
4. Butz K., Ristriani T., Hengstermann A., Denk C., Scheffner M., Hoppe-Seyler F. siRNA targeting of the viral E6 oncogene efficiently kills human papillomavirus-positive cancer cells. Oncogene 2003, 22:5938-5945.
5. Dyson N., Howley P., Munger K., Harlow E. The human papillomavirus- 16 E7 oncoprotein is able to bind to the retinoblastoma gene product. Science 1989, 243:934-937.
6. Werness B., Levine A., Howley P. Association of human papillomavirus type 16 and 18 E6 proteins with p53. Science 1990, 248:76-79.
7. Kiyono T., Hiraiwa A., Fujita M., Hayashi Y., Akiyama T., Ishibashi M. 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 1997, 94:11612-11616.
8. Lee S.S., Weiss R., Javier R. Binding of human virus oncoproteins to hDlg/SAP97, a mammalian homolog of the Drosophila discs large tumor suppressor protein. Proc. Natl. Acad. Sci USA 1997, 94:6670-6675.
9. Watson R., Thomas M., Banks L., Roberts S. Activity of the human papillomavirus E6 PDZ-binding motif correlates with an enhanced morphological transformation of immortalized human keratinocytes. J. Cell Sci 2003, 115:4925-4934.
10. Nguyen M.L., Nguyen M.M., Lee D., Griep A., Lambert P. The PDZ ligand domain of the human papillomavirus type 16 E6 protein is required for E6's induction of epithelial hyperplasia in vivo. J. Virol 2003, 77:6957-6964.
11. Shai A., Brake T., Somoza C., Lambert P. The human papillomavirus E6 oncogene dysregulates the cell cycle and contributes to cervical carcinogenesis through two independent activities. Cancer Res. 2007, 67:1626-1635.
12. Pim D., Bergant M., Boon S.S., Ganti K., Kranjec C., Massimi P., Subbaiah V.K., Thomas M., Tomaic V., Banks L. Human papillomaviruses and the specificity of PDZ domain targeting. FEBS J. 2012, 279:3530-3537.
13. Vincentelli R., Luck K., Poirson J., Polanowska J., Abdat J., Blemont M., Turchetto J., Iv F., Ricquier K., Straub M., Forster A., Cassonnet P., Borg J.P., Jacob Y., Masson M., Nomine Y., Reboul J., Wolff N., Charbonnier S., Trave G. Quantifying domain-ligand affinities and specificities by high-throughput holdup assay. Nat. Methods 2015, 12:787-793.
14. Gardiol D., Kuhne C., Glaunsinger B., Lee S.S., Javier R., Banks L. Oncogenic human papillomavirus E6 proteins target the discs large tumour suppressor for proteasome-mediated degradation. Oncogene 1999, 18:5487-5496.
15. Nakagawa S., Huibregtse J. Human scribble (Vartul) is targeted for ubiquitin-mediated degradation by the high-risk papillomaviruses E6 proteins and the E6AP ubiquitn-protein ligase. Mol. Cell Biol. 2000, 20:8244-8253.
16. Thomas M., Laura R., Hepner K., Guccione E., Sawyers C., Lasky L., Banks L. Oncogenic human papillomavirus E6 proteins target the MAGI-2 and MAGI-3 proteins for degradation. Oncogene 2002, 21:5088-5096.
17. Banks L., Pim D., Thomas M. Human tumour viruses and the deregulation of cell polarity in cancer. Nat. Rev. Cancer 2012, 12:877-886.
18. Watson R., Rollason T., Reynolds G., Murray P., Roberts S. Changes in expression of the human homologue of the Drosophila discs large tumour suppressor protein in high-grade premalignant cervical neoplasias. Carcinogenesis 2002, 23:1791-1796.
19. Cavatorta A., Fumero G., Chouhy D., Aguirre R., Nocito A., Giri A., Banks L., Gardiol D. Differential expression of the human homologue of drosophila discs large oncosuppressor in histologic samples from human papillomavirus-associated lesions as a marker for progression to malignancy. Int. J. Cancer 2004, 111:373-380.
20. Massimi P., Zori P., Roberts S., Banks L. Differential regulation of cell-cell contact, invasion and anoikis by hScrib and hDlg in keratinocytes. PLoS One 2012, 7:e40279.
21. Subbaiah V., Massimi P., Boon S.S., Myers M., Sharek L., Garcia-Mata R., Banks L. The invasive capacity of HPV transformed cells requires the hDlg-dependent enhancement of SGEF/RhoG activity. PLoS Pathog. 2012, 8:e1002543.
22. Zhan L., Rosenberg A., Bergami K., Yu M., Xuan Z., Jaffe A., Allred C., Muthuswamy S. Deregulation of Scribble promotes mammary tumnourigenesis and reveals a role for cell polarity in carcinoma. Cell 2008, 135:865-878.
23. Elsum I., Martin C., Humbert P. Scribble regulates an EMT polarity pathway through modulation of MAPK-ERK signaling to mediate junction formation. J. Cell Sci. 2013, 126:3990-3999.
24. Feigin M., Akshinthala D., Araki K., Rosenberg A., Muthuswamy L., Martin B., Lehmann B., Berman H., Pietenpol J., Cardiff R., Muthuswamy S. Mislocalization of the cell polarity protein Scribble promotes mammary tumourigensis and is associated with basal breast cancer. Cancer Res. 2014, 74:3180-3194.
25. Hampson L., Li C., Oliver A., Kitchener H., Hampson I. The PDZ protein Tip-1 is a gain of function target of the HPV16 E6 oncoprotein. Int. J. Oncol. 2004, 25:1249-1256.
26. Oliver A., He X., Borthwick K., Donne A., Hampson L., Hampson I. The HPV16 E6 binding protein Tip-1 interacts with ARHGEF16, which activates Cdc42. British J. Cancer 2011, 104:324-331.
27. Lee C., Laimins L. Role of the PDZ domain-binding motif of the oncoprotein E6 in the pathogenesis of human papillomavirus type 31. J. Virol. 2004, 78:12366-12377.
28. Nicolaides L., Davy C., Raj K., Kranjec C., Banks L., Doorbar J. Stabilization of HPV16 E6 protein by PDZ proteins, and potential implications for genome maintenance. Virology 2011, 414:137-145.
29. Delury C., Marsh E., James C., Boon S.S., Banks L., Knight G., Roberts S. The role of protein kinase A regulation of the E6 PDZ-binding domain during the differentiation-dependent life cycle of human papillomavirus type 18. J. Virol. 2013, 87:9463-9472.
30. Tomaic V., Pim D., Banks.L. The stability of the human papillomavirus E6 oncoprotein is E6AP dependent. Virology 2009, 393:7-10.
31. Grossman S., Mora R., Laimins L. Intracellular localization and DNA-binding properties of human papillomavirus type 18 E6 protein expressed with a baculovirus vector. J. Virol. 1989, 63:366-374.
32. Guccione E., Massimi P., Bernat A., Banks L. Comparative analysis of the intracellular location of the high- and low-risk human papillomavirus oncoproteins. Virology 2002, 293:20-25.
33. Schneider-Gadicke A., Schwarz E. Different human cervical carcinoma cell lines show similar transcription patterns of human papillomavirus 18 early genes. EMBO J. 1986, 5:2285-2292.
34. Smotkin D., Wettstein F. Transcription of human papillomavirus type 16 early genes in a cervical cancer and a cancer-derived cell line cell line and identification of the E7 protein. Proc. Natl. Acad. Sci. USA 1986, 83:4680-4684.
35. Boyer S., Wazer D., Band V. E7 protein of human papillomavirus-16 induces degradation of retinoblastoma protein through the ubiquitin-proteasome pathway. Cancer Res. 1996, 56:4620-4624.
36. S. Tang, M. Tao, J. McCoy, ZM Zheng. The E7 oncoprotein is translated from spliced E6*I transcripts in high-risk human papillomavirus type 16-or type 18-positive cervical cancer cell lines via translation reinitiation. J. Virol. 80 (2006) 4249-4263.
37. Stacey S., Jordan D., Williamson A., Brown M., Coote J., Arrand J. Leaky scanning is the predominant mechanism for translation of human papillomavirus type 16 E7 oncoprotein from E6/E7 bicistronic mRNA. J. Virol. 2000, 74:7284-7297.
38. Ma X., Blenis J. Molecular mechanisms of mTOR-mediated translational control. Nat. Rev. Mol. Cell. Biol. 2009, 10:307-318.
39. Spangle J., Munger K. The human papillomavirus type 16 E6 oncoprotein activates mTORC1 signaling and increases protein synthesis. J. Virol. 2010, 84:9398-9407.
40. Spangle J., Ghosh-Choudhury N., Munger K. Activation of cap-dependent translation by mucosal human papillomavirus E6 proteins is dependent on the integrity of the LXXLL binding motif. J. Virol. 2012, 86:7466-7472.
41. Kumar M., Kong K., Javier R. Hijacking Dlg1 for oncogenic phosphatidylinositol 3-kinase activation in human epithelial cells is a conserved mechanism of human adenovirus E4-ORF1 proteins. J. Virol. 2014, 88:14268-14277.
42. Kong K., Kumar M., Taruishi M., Javier R. The human adenovirus E4-ORF1 protein subverts discs large 1 to mediate membrane recruitment and dysregulation of phosphatidylinositol 3-kinase. PLoS Pathog. 2014, 10:e1004102.
43. Popowski M., Ferguson H., Sion A., Koller E., Knudsen E., Van Den Berg C. Stress and IGF-1 differently control cell fate through mammalian target of rapamycin (mTOR) and retinoblastoma protein (pRB). J. Biol. Chem. 2008, 283:28265-28273.
44. Ray P., Grover R., Das S. Two internal ribosome entry sites mediate the translation of p53 isoforms. EMBO Rep. 2006, 7:404-410.