Human papillomavirus (HPV)-18 E6 oncoprotein interferes with the epithelial cell polarity Par3 protein

Molecular Oncology

Volumn 8, Issue 3, 2014, Pages 533-543

  Facciuto, Florencia ^a   Bugnon Valdano, Marina ^a   Marziali, Federico ^a   Massimi, Paola ^b   Banks, Lawrence ^b   Cavatorta, Ana Laura ^a   Gardiol, Daniela ^a  

^a UNIVERSIDAD NACIONAL DE ROSARIO   (Argentina)

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

Author keywords

Cell polarity; E6 protein; HPV; Par3; PDZ

Indexed keywords

CALCIUM; PARTITIONING DEFECTIVE 3 PROTEIN; PDZ PROTEIN; PROTEIN E6; UNCLASSIFIED DRUG; CELL CYCLE PROTEIN; DNA BINDING PROTEIN; E6 PROTEIN, HUMAN PAPILLOMAVIRUS TYPE 18; MEMBRANE PROTEIN; ONCOPROTEIN; PARD3 PROTEIN, HUMAN; PROTEASOME; PROTEIN BINDING;

ARTICLE; CELL CONTACT; CELL JUNCTION; CELL POLARITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EPITHELIUM CELL; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN PAPILLOMAVIRUS TYPE 18; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; IN VIVO STUDY; MICROSCOPY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TIGHT JUNCTION; WESTERN BLOTTING; CELL LINE; CYTOLOGY; HOST PATHOGEN INTERACTION; METABOLISM; PAPILLOMAVIRUS INFECTION; PATHOLOGY; PHYSIOLOGY; VIROLOGY;

HUMAN PAPILLOMAVIRUS; HUMAN PAPILLOMAVIRUS - 18;

CELL CYCLE PROTEINS; CELL LINE; CELL POLARITY; DNA-BINDING PROTEINS; EPITHELIAL CELLS; HOST-PATHOGEN INTERACTIONS; HUMAN PAPILLOMAVIRUS 18; HUMANS; MEMBRANE PROTEINS; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRUS INFECTIONS; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; TIGHT JUNCTIONS;

EID: 84899493013     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1016/j.molonc.2014.01.002     Document Type: Article

References (45)

1. Aono S., Hirai Y. Phosphorylation of claudin-4 is required for tight junction formation in a human keratinocyte cell line. Exp. Cell. Res. 2008, 314:3326-3339.
2. Aranda V., Nolan M.E., Muthuswamy S.K. Par complex in cancer: a regulator of normal cell polarity joins the dark side. Oncogene 2008, 27:6878-6887.
3. Assemat E., Bazellieres E., Pallesi-Pocachard E., Le Bivic A., Massey-Harroche D. Polarity complex proteins. Biochim. Biophys. Acta 2008, 1778:614-630.
4. Banks L., Pim D., Thomas M. Human tumour viruses and the deregulation of cell polarity in cancer. Nat. Rev. Cancer 2012, 12:877-886.
5. Cavatorta A.L., Fumero G., Chouhy D., Aguirre R., Nocito A.L., Giri A.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.
6. Coureuil M., Mikaty G., Miller F., Lecuyer H., Bernard C., Bourdoulous S., Dumenil G., Mege R.M., Weksler B.B., Romero I.A., Couraud P.O., Nassif X. Meningococcal type IV pili recruit the polarity complex to cross the brain endothelium. Science 2009, 325:83-87.
7. Chen J., Zhang M. The Par3/Par6/aPKC complex and epithelial cell polarity. Exp. Cell Res. 2013, 319:1357-1364.
8. Debnath J., Muthuswamy S.K., Brugge J.S. Morphogenesis and oncogenesis of MCF-10A mammary epithelial acini grown in three-dimensional basement membrane cultures. Methods 2003, 30:256-268.
9. Facciuto F., Cavatorta A.L., Valdano M.B., Marziali F., Gardiol D. Differential expression of PDZ domain-containing proteins in human diseases - challenging topics and novel issues. Febs. J. 2012, 279:3538-3548.
10. Fang L., Wang Y., Du D., Yang G., Tak Kwok T., Kai Kong S., Chen B., Chen D.J., Chen Z. Cell polarity protein Par3 complexes with DNA-PK via Ku70 and regulates DNA double-strand break repair. Cell Res. 2007, 17:100-116.
11. Feng W., Wu H., Chan L.N., Zhang M. The Par-3 NTD adopts a PB1-like structure required for Par-3 oligomerization and membrane localization. Embo. J. 2007, 26:2786-2796.
12. 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.
13. Goldstein B., Macara I.G. The PAR proteins: fundamental players in animal cell polarization. Dev. Cell 2007, 13:609-622.
14. Guccione E., Pim D., Banks L. HPV-18 E6*I modulates HPV-18 full-length E6 functions in a cell cycle dependent manner. Int. J. Cancer 2004, 110:928-933.
15. Hernandez-Monge J., Garay E., Raya-Sandino A., Vargas-Sierra O., Diaz-Chavez J., Popoca-Cuaya M., Lambert P.F., Gonzalez-Mariscal L., Gariglio P. Papillomavirus E6 oncoprotein up-regulates occludin and ZO-2 expression in ovariectomized mice epidermis. Exp. Cell Res. 2013, 319:2588-2603.
16. Horikoshi Y., Suzuki A., Yamanaka T., Sasaki K., Mizuno K., Sawada H., Yonemura S., Ohno S. Interaction between PAR-3 and the aPKC-PAR-6 complex is indispensable for apical domain development of epithelial cells. J.Cell Sci. 2009, 122:1595-1606.
17. Humbert P., Russell S., Richardson H. Dlg, Scribble and Lgl in cell polarity, cell proliferation and cancer. Bioessays 2003, 25:542-553.
18. Humbert P.O., Grzeschik N.A., Brumby A.M., Galea R., Elsum I., Richardson H.E. Control of tumourigenesis by the Scribble/Dlg/Lgl polarity module. Oncogene 2008, 27:6888-6907.
19. Iden S., van Riel W.E., Schafer R., Song J.Y., Hirose T., Ohno S., Collard J.G. Tumor type-dependent function of the par3 polarity protein in skin tumorigenesis. Cancer Cell 2012, 22:389-403.
20. Joberty G., Petersen C., Gao L., Macara I.G. The cell-polarity protein Par6 links Par3 and atypical protein kinase C to Cdc42. Nat. Cell Biol. 2000, 2:531-539.
21. Jonson A.L., Rogers L.M., Ramakrishnan S., Downs L.S. Gene silencing with siRNA targeting E6/E7 as a therapeutic intervention in a mouse model of cervical cancer. Gynecol. Oncol. 2008, 111:356-364.
22. Kranjec C., Banks L. A systematic analysis of human papillomavirus (HPV) E6 PDZ substrates identifies MAGI-1 as a major target of HPV type 16 (HPV-16) and HPV-18 whose loss accompanies disruption of tight junctions. J.Virol. 2011, 85:1757-1764.
23. Lace M.J., Anson J.R., Klingelhutz A.J., Lee J.H., Bossler A.D., Haugen T.H., Turek L.P. Human papillomavirus (HPV) type 18 induces extended growth in primary human cervical, tonsillar, or foreskin keratinocytes more effectively than other high-risk mucosal HPVs. J.Virol. 2009, 83:11784-11794.
24. Lowy D.R., Schiller J.T. Reducing HPV-associated cancer globally. Cancer Prev. Res. (Phila) 2012, 5:18-23.
25. Massimi P., Gardiol D., Roberts S., Banks L. Redistribution of the discs large tumor suppressor protein during mitosis. Exp. Cell Res. 2003, 290:265-274.
26. 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.
27. Matlashewski G., Schneider J., Banks L., Jones N., Murray A., Crawford L. Human papillomavirus type 16 DNA cooperates with activated ras in transforming primary cells. Embo. J. 1987, 6:1741-1746.
28. McCaffrey L.M., Montalbano J., Mihai C., Macara I.G. Loss of the Par3 polarity protein promotes breast tumorigenesis and metastasis. Cancer Cell 2012, 22:601-614.
29. Mesplede T., Gagnon D., Bergeron-Labrecque F., Azar I., Senechal H., Coutlee F., Archambault J. p53 degradation activity, expression, and subcellular localization of E6 proteins from 29 human papillomavirus genotypes. J.Virol. 2012, 86:94-107.
30. Nakagawa S., Huibregtse J.M. 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. 2000, 20:8244-8253.
31. Nakagawa S., Yano T., Nakagawa K., Takizawa S., Suzuki Y., Yasugi T., Huibregtse J.M., Taketani Y. Analysis of the expression and localisation of a LAP protein, human scribble, in the normal and neoplastic epithelium of uterine cervix. Br. J. Cancer 2004, 90:194-199.
32. Pieczynski J., Margolis B. Protein complexes that control renal epithelial polarity. Am. J. Physiol. Renal. Physiol. 2011, 300:F589-F601.
33. 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.
34. Runkle E.A., Mu D. Tight junction proteins: from barrier to tumorigenesis. Cancer Lett. 2013, 337:41-48.
35. Scheffner M., Huibregtse J.M., Vierstra R.D., Howley P.M. The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell 1993, 75:495-505.
36. Storrs C.H., Silverstein S.J. PATJ, a tight junction-associated PDZ protein, is a novel degradation target of high-risk human papillomavirus E6 and the alternatively spliced isoform 18 E6. J.Virol. 2007, 81:4080-4090.
37. Thomas M., Narayan N., Pim D., Tomaic V., Massimi P., Nagasaka K., Kranjec C., Gammoh N., Banks L. Human papillomaviruses, cervical cancer and cell polarity. Oncogene 2008, 27:7018-7030.
38. Tomaic V., Gardiol D., Massimi P., Ozbun M., Myers M., Banks L. Human and primate tumour viruses use PDZ binding as an evolutionarily conserved mechanism of targeting cell polarity regulators. Oncogene 2008, 28:1-8.
39. Walker J., Bloss J.D., Liao S.Y., Berman M., Bergen S., Wilczynski S.P. Human papillomavirus genotype as a prognostic indicator in carcinoma of the uterine cervix. Obstet. Gynecol. 1989, 74:781-785.
40. Xue B., Krishnamurthy K., Allred D.C., Muthuswamy S.K. Loss of Par3 promotes breast cancer metastasis by compromising cell-cell cohesion. Nat. Cell Biol. 2012, 15:189-200.
41. Yoshinouchi M., Yamada T., Kizaki M., Fen J., Koseki T., Ikeda Y., Nishihara T., Yamato K. Invitro and invivo growth suppression of human papillomavirus 16-positive cervical cancer cells by E6 siRNA. Mol. Ther. 2003, 8:762-768.
42. Zen K., Yasui K., Gen Y., Dohi O., Wakabayashi N., Mitsufuji S., Itoh Y., Zen Y., Nakanuma Y., Taniwaki M., Okanoue T., Yoshikawa T. Defective expression of polarity protein PAR-3 gene (PARD3) in esophageal squamous cell carcinoma. Oncogene 2009, 28:2910-2918.
43. Zhang J., Rose B.R., Thompson C.H., Jarrett C., Russell P., Houghton R.S., Cossart Y.E. Associations between oncogenic human papillomaviruses and local invasive patterns in cervical cancer. Gynecol. Oncol. 1995, 57:170-177.
44. Zhang Y., Dasgupta J., Ma R.Z., Banks L., Thomas M., Chen X.S. Structures of a human papillomavirus (HPV) E6 polypeptide bound to MAGUK proteins: mechanisms of targeting tumor suppressors by a high-risk HPV oncoprotein. J.Virol. 2007, 81:3618-3626.
45. zur Hausen H. Papillomaviruses and cancer: from basic studies to clinical application. Nat. Rev. Cancer 2002, 2:342-350.