High-risk human papillomavirus E6 oncoproteins interact with 14-3-3ζ in a PDZ binding motif-dependent manner

Journal of Virology

Volumn 87, Issue 3, 2013, Pages 1586-1595

  Boon, Siaw Shi ^a   Banks, Lawrence ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP DEPENDENT PROTEIN KINASE; PROTEIN 14 3 3; PROTEIN 14 3 3 ZETA; PROTEIN E6; PROTEIN KINASE B; UNCLASSIFIED DRUG;

ARTICLE; CARCINOGENESIS; CELL LEVEL; CONTROLLED STUDY; DOWN REGULATION; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN PAPILLOMAVIRUS TYPE 18; HUMAN PAPILLOMAVIRUS TYPE 31; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PDZ DOMAIN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN PURIFICATION; STEADY STATE; UTERINE CERVIX CANCER; WART VIRUS;

14-3-3 PROTEINS; CYCLIC AMP-DEPENDENT PROTEIN KINASES; DNA-BINDING PROTEINS; HELA CELLS; HOST-PATHOGEN INTERACTIONS; HUMANS; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRIDAE; PDZ DOMAINS; PHOSPHORYLATION; PROTEIN BINDING; PROTEIN INTERACTION MAPPING; PROTO-ONCOGENE PROTEINS C-AKT; REPRESSOR PROTEINS;

EID: 84873024989     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02074-12     Document Type: Article

References (49)

1. zur Hausen H. 2009. Papillomaviruses in the causation of human cancers: a brief historical account. Virology 384:260-265.
2. Bouvard V, Baan R, Straif K, Grosse Y, Secretan B, El Ghissassi F, Benbrahim-Tallaa L, Guha N, Freeman C, Galichet L, Cogliano V, WHO International Agency for Research on Cancer Monograph Working Group. 2009. A review of human carcinogens, part B: biological agents. Lancet Oncol. 10:321-322.
3. Androphy EJ, Hubbert NL, Schiller JT, Lowy DR. 1987. Identification of the HPV-16 E6 protein from transformed mouse cells and human cervical carcinoma cell lines. EMBO J. 6:989-992.
4. Banks L, Spence P, Androphy E, Hubbert N, Matlashewski G, Murray A, Crawford L. 1987. Identification of human papillomavirus type 18 E6 polypeptide in cells derived from human cervical carcinomas. J. Gen. Virol. 68:1351-1359.
5. Smotkin D, Wettstein FO. 1986. Transcription of human papillomavirus type 16 early genes in a cervical cancer and a cancer-derived cell line and identification of the E7 protein. Proc. Natl. Acad. Sci. U. S. A. 83:4680-4684.
6. Alvarez-Salas LM, Cullinan AE, Siwkowski A, Hampel A, DiPaolo JA. 1998. Inhibition of HPV-16 E6/E7 immortalization of normal keratinocytes by hairpin ribozymes. Proc. Natl. Acad. Sci. U. S. A. 95:1189-1194.
7. Goodwin EC, DiMaio D. 2000. Repression of human papillomavirus oncogenes in HeLa cervical carcinoma cells causes the orderly reactivation of dormant tumor suppressor pathways. Proc. Natl. Acad. Sci. U. S. A. 97:12513-12518.
8. Yoshinouchi M, Yamada T, Kizaki M, Fen J, Koseki T, Ikeda Y, Nishihara T, Yamato K. 2003. In vitro and in vivo growth suppression of human papillomavirus 16-positive cervical cancer cells by E6 siRNA. Mol. Ther. 8:762-768.
9. Mantovani F, Banks L. 2001. The human papillomavirus E6 protein and its contribution to malignant progression. Oncogene 20:7874-7887.
10. Münger K, Basile JR, Duensing S, Eichten A, Gonzalez SL, Grace M, Zacny VL. 2001. Biological activities and molecular targets of the human papillomavirus E7 oncoprotein. Oncogene 20:7888-7898.
11. Berezutskaya E, Yu B, Morozov A, Raychaudhuri P, Bagchi S. 1997. Differential regulation of the pocket domains of the retinoblastoma family proteins by the HPV16 E7 oncoprotein. Cell Growth Differ. 8:1277-1286.
12. Boyer SN, Wazer DE, Band V. 1996. E7 protein of human papilloma virus-16 induces degradation of retinoblastoma protein through the ubiquitin- proteasome pathway. Cancer Res. 56:4620-4624.
13. Cheng S, Schmidt-Grimminger DC, Murant T, Broker TR, Chow LT. 1995. Differentiation-dependent up-regulation of the human papillomavirus E7 gene reactivates cellular DNA replication in suprabasal differentiated keratinocytes. Genes Dev. 9:2335-2349.
14. Duensing S, Münger K. 2002. The human papillomavirus type 16 E6 and E7 oncoproteins independently induce numerical and structural chromosome instability. Cancer Res. 62:7075-7082.
15. Demers GW, Foster SA, Halbert CL, Galloway DA. 1994. Growth arrest by induction of p53 in DNA damaged keratinocytes is bypassed by human papillomavirus 16 E7. Proc. Natl. Acad. Sci. U. S. A. 91:4382-4386.
16. Slebos RJ, Lee MH, Plunkett BS, Kessis TD, Williams BO, Jacks T, Hedrick L, Kastan MB, Cho KR. 1994. p53-dependent G1 arrest involves pRB-related proteins and is disrupted by the human papillomavirus 16 E7 oncoprotein. Proc. Natl. Acad. Sci. U. S. A. 91:5320-5324. 17. Scheffner M, Huibregtse JM, Vierstra RD, Howley PM. 1993. The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell 75:495-505.
17. Scheffner M, Huibregtse JM, Vierstra RD, Howley PM. 1993. The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell 75:495-505
18. Kiyono T, Hiraiwa A, Fujita M, Hayashi Y, Akiyama T, Ishibashi M. 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. U. S. A. 94:11612-11616.
19. Lee SS, Weiss RS, Javier RT. 1997. Binding of human virus oncoproteins to hDlg/SAP97, a mammalian homolog of the Drosophila discs large tumor suppressor protein. Proc. Natl. Acad. Sci. U. S. A. 94:6670-6675.
20. Thomas M, Narayan N, Pim D, Tomaic V, Massimi P, Nagasaka K, Kranjec C, Gommah N, Banks L. 2008. Human papillomaviruses, cervical cancer and cell polarity. Oncogene 27:7018-7030.
21. Spanos WC, Geiger J, Anderson ME, Harris GF, Bossler AD, Smith RB, Klingelhutz AJ, Lee JH. 2008. Deletion of the PDZ motif of HPV16 E6 preventing immortalization and anchorage-independent growth in human tonsil epithelial cells. Head Neck 30:139-147.
22. Spanos WC, Hoover A, Harris GF, Wu S, Strand GL, Anderson ME, Klingelhutz AJ, Hendriks W, Bossler AD, Lee JH. 2008. 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. J. Virol. 82:2493-2500.
23. Watson RA, Thomas M, Banks L, Roberts S. 2003. Activity of the human papillomavirus E6 PDZ-binding motif correlates with an enhanced morphological transformation of immortalized human keratinocytes. J. Cell Sci. 116:4925-4934.
24. Nguyen ML, Nguyen MM, Lee D, Griep AE, Lambert PF. 2003. 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. 77: 6957-6964.
25. Shai A, Brake T, Somoza C, Lambert PF. 2007. The human papillomavirus E6 oncogene dysregulates the cell cycle and contributes to cervical carcinogenesis through two independent activities. Cancer Res. 67:1626-1635.
26. Lee C, Laimins LA. 2004. Role of the PDZ domain-binding motif of the oncoprotein E6 in the pathogenesis of human papillomavirus type 31. J. Virol. 78:12366-12377.
27. Nicolaides L, Davy C, Raj K, Kranjec C, Banks L, Doorbar J. 2011. Stabilization of HPV16 E6 protein by PDZ proteins, and potential implications for genome maintenance. Virology 414:137-145.
28. Kühne C, Gardiol D, Guarnaccia C, Amenitsch H, Banks L. 2000. Differential regulation of human papillomavirus E6 by protein kinase A: conditional degradation of human discs large protein by oncogenic E6. Oncogene 19:5884-5891.
29. Zhang Y, Dasgupta J, Ma RZ, Banks L, Thomas M, Chen XS. 2007. Structures of a human papillomavirus (HPV) E6 polypeptide bound to MAGUK proteins: mechanisms of targeting tumor suppressors by a highrisk HPV oncoprotein. J. Virol. 81:3618-3626.
30. Muslin AJ, Tanner JW, Allen PM, Shaw AS. 1996. Interaction of 14-3-3 with signaling proteins is mediated by the recognition of phosphoserine. Cell 84:889-897.
31. Hong HY, Jeon WK, Bae EJ, Kim ST, Lee HJ, Kim SJ, Kim BC. 2010. 14-3-3 sigma and 14-3-3 zeta plays an opposite role in cell growth inhibition mediated by transforming growth factor-beta 1. Mol. Cells 3:305-309.
32. Neal CL, Yu D. 2010. 14-3-3 as a prognostic marker and therapeutic target for cancer. Expert Opin. Ther. Targets 14:1343-1354.
33. Howie HL, Koop JI, Weese J, Robinson K, Wipf G, Kim L, Galloway DA. 2011. Beta-HPV 5 and 8 E6 promote p300 degradation by blocking AKT/p300 association. PLoS Pathog. 7:e1002211. doi:10.1371/journal. ppat.1002211.
34. Keshamouni VG, Michailidis G, Grasso CS, Anthwal S, Strahler JR, Walker A, Arenberg DA, Reddy RC, Akulapalli S, Thannickal VJ, Standiford TJ, Andrews PC, Omenn GS. 2006. Differential protein expression profiling by iTRAQ-2DLC-MS/MS of lung cancer cells undergoing epithelial-mesenchymal transition reveals a migratory/invasive phenotype. J. Proteome Res. 5:1143-1154.
35. Shen J, Person MD, Zhu J, Abbruzzese JL, Li D. 2004. Protein expression profiles in pancreatic adenocarcinoma compared with normal pancreatic tissue and tissue affected by pancreatitis as detected by twodimensional gel electrophoresis and mass spectrometry. Cancer Res. 64: 9018-9026.
36. Jang JS, Cho HY, Lee YJ, Ha WS, Kim HW. 2004. The differential proteome profile of stomach cancer: identification of the biomarker candidates. Oncol. Res. 14:491-499.
37. Thomas M, Massimi P, Banks L. 1996. HPV-18 E6 inhibits p53 DNA binding activity regardless of the oligomeric state of p53 or the exact p53 recognition sequence. Oncogene 13:471-480.
38. Pim D, Thomas M, Javier R, Gardiol D, Banks L. 2000. HPV E6 targeted degradation of the discs large protein: evidence for the involvement of a novel ubiquitin ligase. Oncogene 19:719-725.
39. Nagasaka K, Pim D, Massimi P, Thomas M, Tomaic V, Subbaiah VK, Kranjec C, Nakagawa S, Yano T, Taketani Y, Myers M, Banks L. 2010. The cell polarity regulator hScrib controls ERK activation through a KIM site-dependent interaction. Oncogene 29:5311-5321.
40. Massimi P, Narayan N, Thomas M, Gammoh N, Strand S, Strand D, Banks L. 2008. Regulation of the hDlg/hScrib/Hugl-1 tumour suppressor complex. Exp. Cell Res. 314:3306-3317.
41. Olsen JV, Vermeulen M, Santamaria A, Kumar C, Miller ML, Jensen LJ, Gnad F, Cox J, Jensen TS, Nigg EA, Brunak S, Mann M. 2010. Quantitative phosphoproteomics reveals widespread full phosphorylation site occupancy during mitosis. Sci. Signal. 3:ra3. doi:10.1126/scisignal. 2000475.
42. Matta A, Bahadur S, Duggal R, Gupta SD, Ralhan R. 2007. Overexpression of 14-3-3zeta is an early event in oral cancer. BMC Cancer 7:169.
43. Fan T, Li R, Todd NW, Qiu Q, Fang HB, Wang HJ, Shen JJ, Zhao RY, Caraway NP, Katz RL, Stass SA, Jiang F. 2007. Up-regulation of 14-3-3 in lung cancer and its implication as prognostic and therapeutic target. Cancer Res. 67:7901-7906.
44. Higareda-Almaraz JC, Enríquez-Gasca MR, Hernández-Ortiz M, Resendis- Antonio O, Encarnación-Guevara S. 2011. Proteomic patterns of cervical cancer cell lines, a network perspective. BMC Syst Biol. 5:96.
45. Reference deleted.
46. Reference deleted.
47. Pearson RB, Kemp BE. 1991. Protein kinase phosphorylation site sequences and consensus specificity motifs: tabulations. Methods Enzymol. 200:62-81.
48. Songyang Z, Fanning AS, Fu C, Xu J, Marfatia SM, Chishti AH, Crompton A, Chan AC, Anderson JM, Cantley LC. 1997. Recognition of unique carboxyl-terminal motifs by distinct PDZ domains. Science 275: 73-77.
49. Obata T, Yaffe MB, Leparc GG, Piro ET, Maegawa H, Kashiwagi A, Kikkawa R, Cantley LC. 2000. Peptide and protein library screening defines optimal substrate motifs for AKT/PKB. J. Biol. Chem. 275:36108-36115.