HPV16 E6 augments Wnt signaling in an E6AP-dependent manner

Virology

Volumn 396, Issue 1, 2010, Pages 47-58

  Lichtig, Hava ^a   Gilboa, Daniella Avital ^a   Jackman, Anna ^a   Gonen, Pinhas ^a   Levav Cohen, Yaara ^b   Haupt, Ygal ^b   Sherman, Levana ^a  

^a TEL AVIV UNIVERSITY   (Israel)

^b HEBREW UNIVERSITY   (Israel)

Author keywords

Catenin; E6; E6AP; GSK3 ; HPV; TCF; Wnt signaling

Indexed keywords

APC PROTEIN; AXIN; BETA CATENIN; GLYCOGEN SYNTHASE KINASE 3BETA; LUCIFERASE; MUTANT PROTEIN; PDZ PROTEIN; PROTEIN E6; PROTEIN E6AP; PROTEIN P53; T CELL FACTOR PROTEIN; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; WNT PROTEIN;

ANIMAL CELL; ARTICLE; CELL FRACTIONATION; CELLULAR DISTRIBUTION; CONCENTRATION RESPONSE; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVITY; ENZYME ASSAY; EPISTASIS; FEMALE; HALF LIFE TIME; HUMAN; HUMAN CELL; HUMAN PAPILLOMAVIRUS TYPE 16; IMMUNOFLUORESCENCE TEST; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STABILITY; PROTEIN TARGETING; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; VIRUS CARCINOGENESIS;

BETA CATENIN; CELLS, CULTURED; GLYCOGEN SYNTHASE KINASE 3; HUMANS; ONCOGENE PROTEINS, VIRAL; PROTEASOME ENDOPEPTIDASE COMPLEX; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; TCF TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEIN P53; UBIQUITIN-PROTEIN LIGASES; WNT PROTEINS;

HUMAN PAPILLOMAVIRUS;

EID: 70649099054     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2009.10.011     Document Type: Article

References (63)

1. Alfandari J., Shnitman Magal S., Jackman A., Schlegel R., Gonen P., and Sherman L. HPV16 E6 oncoprotein inhibits apoptosis induced during serum-calcium differentiation of foreskin human keratinocytes. Virology 257 (1999) 383-396
2. Bachar-Dahan L., Goltzmann J., Yaniv A., and Gazit A. Engrailed-1 negatively regulates β-catenin transcriptional activity by destabilizing β-catenin via a glycogen synthase kinase-3β-independent pathway. Mol. Biol. Cell 17 (2006) 2572-2580
3. Beaudenon S., and Huibregtse J.M. HPV E6, E6AP and cervical cancer. BMC Biochem 9 suppl 1 (2008) S4
4. Carreras R., Alameda F., Mancebo G., García-Moreno P., Mariñoso M.L.M., Costa C., Fusté P., Baró T., and Serrano S. A study of Ki-67, c-erbB2 and cyclin D-1 expression in CIN-I, CIN-III and squamous cell carcinoma of the cervix. Histol. Histopathol. 22 (2007) 587-592
5. Clevers H. Wnt/β-catenin signaling in development and disease. Cell 127 (2006) 469-480
6. Dignam J.D., Lebovitz R.M., and Roeder R.G. Accurate transcription by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Proc. Natl. Acad. Sci. U. S. A. 11 (1983) 1475-1489
7. Gan D.-D., and Khalili K. Interaction between JCV large T-antigen and β-catenin. Oncogene 23 (2004) 483-490
8. Gazit A., Yaniv A., Bafico A., Pramila T., Igarashi M., Kitajewski J., and Aaronson S. Human frizzed 1 interacts with transforming Wnts to transduce a TCF dependent transcriptional response. Oncogene 18 (1999) 5959-5966
9. Gewin L., Meyers H., Kiyono T., and Galloway D.A. Identification of a novel telomerase repressor that interacts with the human papillomavirus type-16 E6/E6-AP complex. Genes Dev. 18 (2004) 2269-2282
10. Giles R.H., van Es J.H., and Clevers H. Caught up in a Wnt Storm: Wnt signaling in cancer. Biochim. Biophys. Acta 1653 (2003) 1-24
11. Golan T., Yaniv A., Bafico A., Liu G., and Gazit A. The human frizzled 6 (HFz6) acts as a negative regulator of the canonical Wnt-β-catenin signaling cascade. J. Biol. Chem. 279 (2004) 14879-14888
12. Hart M., Concordat J., Lassot I., Albert I., de los Santos R., Durand H., Perret C., Rubinfeld B., Margottin F., Benarous R., and Polakis P. The F-box protein TrCP associates with phosphorylated beta-catenin and regulates its activity in the cell. Curr. Biol. 9 (1999) 207-210
13. Hayward S.D., Liu J., and Fujimuro M. Notch and Wnt signaling: mimicry and manipulation by gamma hepesviruses. Sci. STKE re4 (2006)
14. Hendriksen J., Fagotto F., Velde H., Schie M., Noordermeer J., and Fornerod M. RanBP3 enhances nuclear export of active β-catenin independently of CRM1. J. Cell Biol. 171 (2005) 785-797
15. Howie H.L., Katzenellenbogen R.A., and Galloway D.A. Papillomavirus E6 proteins. Virology 384 (2009) 324-334
16. Imura J., Ichikaa K., Takeda J., and Fujimori T. Beta-catenin expression as a prognostic indicator in cervical adenocarcinoma. Int. J. Mol. Med. 8 (2001) 353-358
17. Ishidate T., Matsumine A., Toyoshima K., and Akiyama T. The APC-hDLG complex negatively regulates cell cycle progression from the G0/G1 to S phase. Oncogene 19 (2000) 365-372
18. James M.A., Lee J.H., and Klingelhutz A.J. HPV16-E6 associated hTERT promoter acetylation is E6AP dependent, increased in later passage cells and enhanced by loss of p300. Int. J. Cancer 119 (2006) 1878-1885
19. Kelley M.L., Keiger K.E., Lee C.J., and Huibregtse J.M. The global transcriptional effects of the human papillomavirus E6 protein in cervical carcinoma cell lines are mediated by the E6AP ubiquitin ligase. J. Virol. 79 (2005) 3737-3747
20. Kikuchi A. Tumor formation by genetic mutations in the components of the Wnt signaling pathway. Cancer Sci. 94 (2003) 225-229
21. Korinek V., Barker N., Morin P.J., van Wichen D., de Weger R., Kinzler K.W., Vogelstein B., and Clevers H. Constitutive transcriptional activation by a beta-catenin-Tcf complex in APC-/- colon carcinoma. Science 275 (1997) 1784-1787
22. Levrero M. Viral hepatitis and liver cancer: the case of hepatitis C. Oncogene 25 (2006) 3834-3847
23. Li J., Sutter C., Parker D.S., Blauwakakmp T., Fang M., and Cardigan K.M. CBP/p300 are bimodal regulators of Wnt signaling. EMBO J. 26 (2007) 2284-2294
24. Lichig H., Algrisi M., Edri Botzer L., Abadi T., Verbitzky Y., Jackman A., Tommasino M., Zehbe I., and Sherman L. HPV16 E6 natural variants exhibit different activities in functional assays relevant to the carcinogenic potential of E6. Virology 350 (2006) 216-227
25. Liu Y., Chen J.J., Gao Q., Dalal S., Hong Y., Mansur C.P., Band V., and Androphy E.J. Multiple functions of human papillomavirus type 16 E6 contribute to the immortalization of mammary epithelial cells. J. Virol. 73 (1999) 7297-7307
26. Liu J., Stevens J., Rote C.A., Yost H.J., Hu Y., Neufeld K.L., White R.L., and Matsunami N. Siah-1 mediates a novel β-catenin degradation pathway linking p53 to adenometous polyposis coli protein. Mol. Cell 7 (2001) 927-936
27. Liu X., Yuan H., Fu B., Disbrow G.L., Apolinario T., Tomaic V., Kelley M.L., Baker C.C., Huibregtse J., and Schlegel R. The E6AP ubiquitin ligase is required for transactivation of the hTERT promoter by the human papillomavirus E6 oncoprotein. J. Biol. Chem. 280 (2005) 10807-10816
28. Louria-Hayon I., Alsheich-Bartok O., Levav-Cohen Y., Silberman I., Berger M., Grossman T., Matentzoglu K., Jiang Y., Muller S., Scheffner M., Haupt S., and Haupt Y. E6AP promotes the degradation of the PML tumour suppressor. Cell Death Differ. 16 (2009) 1156-1166
29. Lustig B., and Behrens J. The Wnt signaling pathway and its role in tumor development. J. Cancer Res. Clin. Oncol. 129 (2003) 199-221
30. Mammas I.N., Sourvinos G., Giannoudis A., and Spandidos D.A. Human papilloma virus (HPV) and host cellular interactions. Pathol. Oncol. Res. 10 (2008) 9056-9060
31. Massimi P., Narayan N., Cuenda A., and Banks L. Phosphorylation of the discs large tumour suppressor protein controls its membrane localization and enhances its susceptibility to HPV E6-indued degradation. Oncogene 25 (2006) 4276-4285
32. Matsumine A., Ogai A., Senda T., Okumura N., Satoh K., Baeg G.H., Kawahara T., Kobayashi S., Okada M., Toyoshima K., and Akiyama T. Binding of APC to the human homolog of the Drosophila discs large tumor suppressor protein. Science 272 (1996) 1020-1023
33. Matthews K., Leong C.M., Baxter L., Inglkis E., Yun K., Backstrom B.T., Doorbar J., and Hibma M. Depletion of Langerhans cells in human papillomavirus type 16-infected skin is associated with E6-mediated down regulation of E-cadherin. J. Virol. 77 (2003) 8378-8385
34. Matsuzawa S.-I., and Reed J. Siah-1, SIP and Ebi collaborate in a novel pathway for beta-catenin degradation linked to p53 responses. Mol. Cell 7 (2001) 915-926
35. McLaughlin-Drubin M.E., and Munger K. The human papillomavirus E7 oncoprotein. Virology 384 (2009) 335-344
36. Morin P., Sparks A., Korinek V., Barker N., Clevers H., Vogelstein B., and Kinzler K. Activation of beta-catenin-Tcf sigaling in colon cancer by mutations in beta-catenin or APC. Science 275 (1997) 1787-1790
37. Mosimann C., Hausmann G., and Basler K. β-Catenin hits chromatin: regulation of Wnt target gene activation. Nat. Rev. Mol. Cell Biol. 10 (2009) 276-286
38. Munemitsu S., Albert I., Souza B., Rubinfeld B., and Polakis P. Regulation of intracellular beta-catenin levels by the adenomatous polyposis coli (APC) tumor-suppressor protein. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 3046-3050
39. Narisawa-Saito M., and Kiyono T. Basic mechanisms of high-risk human Papillomavirus induced carcinogenesis: roles of E6 and E7 proteins. Cancer Sci. 98 (2007) 1505-1511
40. Nastasi T., Bongiovanni A., Campos Y., Mann L., Toy J.N., Bostrom J., Rottier R., Hahn C., Conaway J.W., Harris A.J., and d'Azzo A. Ozz-E3, a muscle-specific ubiquitin ligase, regulates beta-catenin degradation during myogenesis. Dev. Cell 6 (2004) 269-282
41. Pereira-Suarez A.L., Meraz M.A., Lizano M., Estrada-Chavez C., Hernandez F., Olivera P., Perez E., Padilla P., Yaniv M., Thierry F., and Garcia-Carranca A. Frequent alterations of the β-catenin protein in cancer of the uterine cervix. Tumour Biol. 23 (2002) 45-53
42. Perez-Pereira C., Vazquez-Ortiz G., Lopez-Romero R., Pina-Sanchez P., Moreno J., and Salcedo M. Genome wide expression analysis in HPV cervical cancer: identification of altered metabolic pathways. Infect. Agent Cancer 2 (2007) 16-26
43. Polakis P. Wnt signaling and cancer. Genes Dev. 14 (2000) 1837-1851
44. Rodriguez-Sastre M.A., Gonzalez-Maya L., Delgado R., Lizano M., Tubaki G., Mohar A., and Garcia-Caranca A. Abnormal distribution of E-cadherin and β-catenin in different histologic types of cancer of the uterine cervix. Gyneocol. Oncol. 97 (2005) 330-336
45. Rosin-Arbesfeld R., Adam Cliffe A., Brabletz T., and Bienz M. Nuclear export of the APC tumour suppressor controls b-catenin function in transcription. EMBO J. 22 (2003) 1101-1113
46. Sadot E., Geiger B., Oren M., and Ben-Zeev A. Down regulation of beta-catenin by activated p53. Mol. Cell. Biol. 21 (2001) 6768-6781
47. Sekaric P., Cherry J.J., and Androphy E.J. Binding of human papillomavirus Type 16 E6 to E6AP is not required for activation of hTERT. J. Virol. 82 (2008) 71-76
48. Sharma C., Pradeep A., Wong L., Rana A., and Rana B. PPARγ activation can regulate β-catenin levels via a proteasome mediated and APC independent pathway. J. Biol. Chem. 279 (2004) 35583-35594
49. Sherman L., and Schlegel R. Serum- and calcium-induced differentiation of human keratinocytes is inhibited by HPV16 E6 oncoprotein. J. Virol. 70 (1996) 3269-3279
50. Sherman L., Itzhaki H., Jackman A., Chen J.J., Koval D., and Schlegel R. Inhibition of serum- and calcium-induced terminal differentiation of human keratinocytes by HPV 16 E6: study of the association with p53 degradation, inhibition of p53 transactivation, and binding to E6BP. Virology 292 (2002) 309-320
51. Shim C., Zhang W., Rhee C.H., and Lee J.H. Profiling of differentially expressed genes in human primary cervical cancer by complementary DNA expression array. Clin. Cancer Res. 4 (1998) 3045-3050
52. Shinohara A., Yokoyama Y., Wan X., Takahashi Y., Mori Y., Takami T., Simokawa K., and Tamaya T. Cytoplasmic/nuclear expression without mutation of exon 3 of the β-catenin gene is frequent in the development of the neoplasm of the uterine cervix. Gynecol. Oncol. 72 (2001) 450-455
53. Shtutman M., Zhurinsky J., Simcha I., Albanese C., D'Amico M., Pestell R., and Ben-Ze'ev A. The cyclin D1 gene is a target of the beta-catenin/LEF-1 pathway. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 5522-5527
54. Su T.H., Chang J.G., Yeh K.T., Lin T.H., Lee T.P., Chen J.C., and Lin C.C. Mutation analysis of CTNNB1 (beta-catenin) and AXIN1, the components of Wnt pathway, in cervical carcinomas. Oncol. Rep. 10 (2003) 1195-1200
55. Takizawa S., Nagasaka K., Nakagawa S., Yano T., Nakagawa K., Yasugi T., Takeuchi T., Kanda T., Huibregste J.M., Akiyama T., and Taketani Y. Human scribble, a novel tumor suppressor identified as a target of high-risk HPV E6 for ubiquitin-mediated degradation, interacts with adenomatous polyposis coli. Genes Cells 11 (2006) 453-464
56. Ueda M., Gemmill R.M., West J., Winn R., Sugita M., Tanaka N., Ueki M., and Drabkin H.A. Mutations of the beta- and gamma-catenin genes are uncommon in human lung, breast, kidney, cervical and ovarian carcinomas. Br. J. Cancer 85 (2001) 64-68
57. Uren A., Fallen S., Yuan H., Usubutun A., Kucukali T., Schlegel R., and Toretsky J.A. Activation of the Canonical Wnt pathway during genital keratinocyte transformation: a model for cervical cancer progression. Cancer Res. 65 (2005) 6199-6206
58. Veeman M.T., Slusarski D.C., Kaykas A., Louie S.H., and Moon R.T. Zebrafish Prickle, a modulator of noncanonical Wnt/Fz signaling, regulates gastrulation movements. Curr. Biol. 13 (2003) 680-685
59. Willert K., and Jones K.A. Wnt signaling: is the party in the nucleus?. Genes Dev. 20 (2006) 1394-1404
60. Xiao J.H., Ghosn C., Hinchman F., Forbes C., Wang J., Snider N., Cordrey A., Zhao Y., and Chandraratna R.A.S. Adenomatous polyposis coli (APC)-independent regulation of beta-catenin degradation via a retinoid × receptor-mediated pathway. J. Biol. Chem. 278 (2003) 29954-29962
61. Xu M., Luo W., Elzi D.J., Grandori C., and Galloway A. NFX1 interacts with mSin3A/histone deacetylase to repress hTERT transcription in keratinocytes. Mol. Cell. Biol. 28 (2008) 4819-4828
62. Zur-Hausen H. Papillomavirus infection - a major cause of human cancers. Biochim. Biophys. Acta 1288 (1996) F55-F78
63. Zur-Hausen H. Papillomaviruses and cancer from basic studies to clinical applications. Nat. Rev. Cancer 2 (2002) 342-350