The human papillomavirus E6 PDZ binding motif: From life cycle to malignancy

Viruses

Volumn 7, Issue 7, 2015, Pages 3530-3551

  Ganti, Ketaki ^a   Broniarczyk, Justyna ^a   Manoubi, Wiem ^a   Massimi, Paola ^a   Mittal, Suruchi ^a   Pim, David ^a   Szalmas, Anita ^a   Thatte, Jayashree ^a   Thomas, Miranda ^a   Tomaić, Vjekoslav ^a   Banks, Lawrence ^a  

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

Author keywords

14 3 3; Cell polarity; E6; HPV; PDZ

Indexed keywords

PDZ PROTEIN; PROTEIN E6; VIRUS DNA; ONCOPROTEIN;

APOPTOSIS; CARCINOGENESIS; CELL ADHESION; CELL POLARITY; CELL PROLIFERATION; DISEASE COURSE; GENE AMPLIFICATION; GENE EXPRESSION; GENE INTERACTION; GENETIC TRANSFORMATION; HUMAN; LIFE CYCLE; METABOLIC REGULATION; NEOPLASM; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; UTERINE CERVIX CANCER; VIRUS GENOME; WART VIRUS; ALPHAPAPILLOMAVIRUS; ANIMAL; CHEMISTRY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; PAPILLOMAVIRUS INFECTION; PDZ DOMAIN; PHOSPHORYLATION; VIROLOGY;

HUMAN PAPILLOMAVIRUS;

ALPHAPAPILLOMAVIRUS; ANIMALS; HUMANS; NEOPLASMS; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRUS INFECTIONS; PDZ DOMAINS; PHOSPHORYLATION;

EID: 84936980768     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v7072785     Document Type: Review

References (119)

1. Zur Hausen, H. Papilloma Viruses and cancer: From basic studies to clinical application. Nat. Rev. Cancer 2002, 2, 342–350.
2. Parkin, D.M.; Bray, F. Chapter 2: The burden of HPV-related cancers. Vaccine 2006, 24.
3. Bouvard, V.; Baan, R.; Straif, K.; Grosse, Y.; Secretan, B.; El Ghissassi, F.; Benbrahim-Tallaa, L.; Guha, N.; Freeman, C.; Galichet, L.; et al. A review of human carcinogens—Part B: Biological agents. Lancet Oncol. 2009, 10, 321–322.
4. Wakeham, K.; Kavanagh, K. The Burden of HPV-Associated Anogenital Cancers. Curr. Oncol. Rep. 2014, 16, 402.
5. Garbuglia, A.R. Human papillomavirus in head and neck cancer. Cancers 2014, 6, 1705–1726.
6. Smotkin, D.; Wettstein, F.O. 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. USA 1986, 83, 4680–4684.
7. Androphy, E.J.; Hubbert, N.L.; Schiller, J.T.; Lowy, D.R. Identification of the HPV-16 E6 protein from transformed mouse cells and human cervical carcinoma cell lines. EMBO J. 1987, 6, 989–992.
8. 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.
9. 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.
10. Magaldi, T.G.; Almstead, L.L.; Bellone, S.; Prevatt, E.G.; Santin, A.D.; DiMaio, D. Primary human cervical carcinoma cells require human papillomavirus E6 and E7 expression for ongoing proliferation. Virology 2012, 422, 114–124.
11. Jabbar, S.F.; Abrams, L.; Glick, A.; Lambert, P.F. Persistence of high-grade cervical dysplasia and cervical cancer requires the continuous expression of the human papillomavirus type 16 E7 oncogene. Cancer Res. 2009, 69, 4407–4414.
12. Goodwin, E.C.; DiMaio, D. Repression of human papillomavirus oncogenes in HeLa cervical carcinoma cells causes the orderly reactivation of dormant tumor suppressor pathways. Proc. Natl. Acad. Sci. USA 2000, 97, 12513–12518.
13. DeFilippis, R.A.; Goodwin, E.C.; Wu, L.; DiMaio, D. Endogenous human papillomavirus E6 and E7 proteins differentially regulate proliferation, senescence, and apoptosis in HeLa cervical carcinoma cells. J. Virol. 2003, 77, 1551–1563.
14. Songyang, Z.; Fanning, A.S.; Fu, C.; Xu, J.; Marfatia, S.M.; Chishti, A.H.; Crompton, A.; Chan, A.C.; Anderson, J.M.; Cantley, L.C. Recognition of unique carboxyl-terminal motifs by distinct PDZ domains. Science 1997, 275, 73–77.
15. Lee, S.S.; Weiss, R.S.; Javier, R.T. 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.
16. 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.
17. Ye, F.; Zhang, M. Structures and target recognition modes of PDZ domains: Recurring themes and emerging pictures. Biochem. J. 2013, 455, 1–14.
18. Hung, A.Y.; Sheng, M. PDZ domains: Structural modules for protein complex assembly. J. Biol. Chem. 2002, 277, 5699–5702.
19. Nourry, C.; Grant, S.G.N.; Borg, J.-P. PDZ domain proteins: Plug and play! Sci. STKE 2003, 2003, RE7.
20. Tonikian, R.; Zhang, Y.; Sazinsky, S.L.; Currell, B.; Yeh, J.-H.; Reva, B.; Held, H.A.; Appleton, B.A.; Evangelista, M.; Wu, Y.; et al. A specificity map for the PDZ domain family. PLoS Biol. 2008, 6, e239.
21. Thomas, M.; Massimi, P.; Navarro, C.; Borg, J.-P.; Banks, L. The hScrib/Dlg apico-basal control complex is differentially targeted by HPV-16 and HPV-18 E6 proteins. Oncogene 2005, 24, 6222–6230.
22. Charbonnier, S.; Nominé, Y.; Ramírez, J.; Luck, K.; Chapelle, A.; Stote, R.H.; Travé, G.; Kieffer, B.; Atkinson, R.A. The structural and dynamic response of MAGI-1 PDZ1 with noncanonical domain boundaries to the binding of human papillomavirus E6. J. Mol. Biol. 2011, 406, 745–763.
23. Fournane, S.; Charbonnier, S.; Chapelle, A.; Kieffer, B.; Orfanoudakis, G.; Travé, G.; Masson, M.; Nominé, Y. Surface plasmon resonance analysis of the binding of high-risk mucosal HPV E6 oncoproteins to the PDZ1 domain of the tight junction protein MAGI-1. J. Mol. Recognit. 2011, 24, 511–523.
24. 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.
25. Vincentelli, R.; Luck, k.; Poirson, J.; Abdat, J.; Blémont, M.; Turchetto, J.; Iv, F.; Ricquier, K.; Straub, M.-L.; et al. Quantifying domain-ligand affinities and specificities by high-throughput holdup assay. Nat. Methods 2015.
26. Belotti, E.; Polanowska, J.; Daulat, A.M.; Audebert, S.; Thomé, V.; Lissitzky, J.-C.; Lembo, F.; Blibek, K.; Omi, S.; Lenfant, N.; et al. The human PDZome: A gateway to PSD95-Disc large-zonula occludens (PDZ)-mediated functions. Mol. Cell. Proteomics 2013, 12, 2587–2603.
27. Rozenblatt-Rosen, O.; Deo, R.C.; Padi, M.; Adelmant, G.; Calderwood, M.A.; Rolland, T.; Grace, M.; Dricot, A.; Askenazi, M.; Tavares, M.; et al. Interpreting cancer genomes using systematic host network perturbations by tumour virus proteins. Nature 2012, 487, 491–495.
28. Van Doorslaer, K.; Tan, Q.; Xirasagar, S.; Bandaru, S.; Gopalan, V.; Mohamoud, Y.; Huyen, Y.; McBride, A.A. The Papillomavirus Episteme: A central resource for papillomavirus sequence data and analysis. Nucleic Acids Res. 2013, 41, D571–D578.
29. Du, M.; Fan, X.; Hanada, T.; Gao, H.; Lutchman, M.; Brandsma, J.L.; Chishti, A.H.; Chen, J.J. Association of cottontail rabbit papillomavirus E6 oncoproteins with the hDlg/SAP97 tumor suppressor. J. Cell. Biochem. 2005, 94, 1038–1045.
30. Liu, Y.; Henry, G.D.; Hegde, R.S.; Baleja, J.D. Solution structure of the hDlg/SAP97 PDZ2 domain and its mechanism of interaction with HPV-18 papillomavirus E6 protein. Biochemistry 2007, 46, 10864–10874.
31. Gardiol, D.; Galizzi, S.; Banks, L. Mutational analysis of the discs large tumour suppressor identifies domains responsible for human papillomavirus type 18 E6-mediated degradation. J. Gen. Virol. 2002, 83, 283–289.
32. Pim, D.; Thomas, M.; Banks, L. Chimaeric HPV E6 proteins allow dissection of the proteolytic pathways regulating different E6 cellular target proteins. Oncogene 2002, 21, 8140–8148.
33. Gardiol, D.; Kühne, 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.
34. Lee, C.; Laimins, L.A. 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.
35. Takizawa, S.; Nagasaka, K.; Nakagawa, S.; Yano, T.; Nakagawa, K.; Yasugi, T.; Takeuchi, T.; Kanda, T.; Huibregtse, J.M.; Akiyama, T.; et al. 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 2006, 11, 453–464.
36. 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.
37. Glaunsinger, B.A.; Lee, S.S.; Thomas, M.; Banks, L.; Javier, R. Interactions of the PDZ-protein MAGI-1 with adenovirus E4-ORF1 and high-risk papillomavirus E6 oncoproteins. Oncogene 2000, 19, 5270–5280.
38. 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.
39. Handa, K.; Yugawa, T.; Narisawa-Saito, M.; Ohno, S.-I.; Fujita, M.; Kiyono, T. E6AP-dependent degradation of DLG4/PSD95 by high-risk human papillomavirus type 18 E6 protein. J. Virol. 2007, 81, 1379–1389.
40. Favre-Bonvin, A.; Reynaud, C.; Kretz-Remy, C.; Jalinot, P. Human papillomavirus type 18 E6 protein binds the cellular PDZ protein TIP-2/GIPC, which is involved in transforming growth factor β signaling and triggers its degradation by the proteasome. J. Virol. 2005, 79, 4229–4237.
41. Accardi, R.; Rubino, R.; Scalise, M.; Gheit, T.; Shahzad, N.; Thomas, M.; Banks, L.; Indiveri, C.; Sylla, B.S.; Cardone, R.A.; et al. E6 and E7 from human papillomavirus type 16 cooperate to target the PDZ protein Na/H exchange regulatory factor 1. J. Virol. 2011, 85, 8208–8216.
42. Lee, S.S.; Glaunsinger, B.; Mantovani, F.; Banks, L.; Javier, R.T. Multi-PDZ domain protein MUPP1 is a cellular target for both adenovirus E4-ORF1 and high-risk papillomavirus type 18 E6 oncoproteins. J. Virol. 2000, 74, 9680–9693.
43. Latorre, I.J.; Roh, M.H.; Frese, K.K.; Weiss, R.S.; Margolis, B.; Javier, R.T. Viral oncoprotein-induced mislocalization of select PDZ proteins disrupts tight junctions and causes polarity defects in epithelial cells. J. Cell Sci. 2005, 118, 4283–4293.
44. 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.
45. Jing, M.; Bohl, J.; Brimer, N.; Kinter, M.; Vande Pol, S.B. Degradation of tyrosine phosphatase PTPN3 (PTPH1) by association with oncogenic human papillomavirus E6 proteins. J. Virol. 2007, 81, 2231–2239.
46. Töpffer, S.; Müller-Schiffmann, A.; Matentzoglu, K.; Scheffner, M.; Steger, G. Protein tyrosine phosphatase H1 is a target of the E6 oncoprotein of high-risk genital human papillomaviruses. J. Gen. Virol. 2007, 88, 2956–2965.
47. Spanos, W.C.; Geiger, J.; Anderson, M.E.; Harris, G.F.; Bossler, A.D.; Smith, R.B.; Klingelhutz, A.J.; Lee, J.H. Deletion of the PDZ motif of HPV16 E6 preventing immortalization and anchorage-independent growth in human tonsil epithelial cells. Head Neck 2008, 30, 139–147.
48. 48. Thomas, M.; Banks, L. PDZRN3/LNX3 is a novel target of human papillomavirus type 16
49. (HPV-16) and HPV-18 E6. J. Virol. 2015, 89, 1439–1444.
50. Boon, S.S.; Banks, L. High-Risk Human Papillomavirus E6 Oncoproteins Interact with 14-3-3 in a PDZ Binding Motif-Dependent Manner. J. Virol. 2012, 87, 1586–1595.
51. Boon, S.S.; Tomai, V.; Thomas, M.; Roberts, S.; Banks, L. Cancer-Causing Human Papillomavirus E6 Proteins Display Major Differences in the Phospho-Regulation of their PDZ Interactions. J. Virol. 2015, 89, 1579–1586.
52. Facciuto, F.; Bugnon Valdano, M.; Marziali, F.; Massimi, P.; Banks, L.; Cavatorta, A.L.; Gardiol, D. Human papillomavirus (HPV)-18 E6 oncoprotein interferes with the epithelial cell polarity Par3 protein. Mol. Oncol. 2014, 8, 533–543.
53. Vande Pol, S.B.; Klingelhutz, A.J. Papillomavirus E6 oncoproteins. Virology 2013, 445, 115–137.
54. 53 . Tomaić, V.; Pim, D.; Banks, L. The stability of the human papillomavirus E6 oncoprotein is E6AP dependent. Virology 2009, 393, 7–10.
55. Zanier, K.; Charbonnier, S.; Baltzinger, M.; Nominé, Y.; Altschuh, D.; Travé, G. Kinetic analysis of the interactions of human papillomavirus E6 oncoproteins with the ubiquitin ligase E6AP using surface plasmon resonance. J. Mol. Biol. 2005, 349, 401–412.
56. Zanier, K.; M’hamedould Sidi, A.; Boulade-Ladame, C.; Rybin, V.; Chappelle, A.; Atkinson, A.; Kieffer, B.; Travé, G. Solution structure analysis of the HPV16 E6 oncoprotein reveals a self-association mechanism required for E6-mediated degradation of p53. Structure 2012, 20, 604–617.
57. Zanier, K.; Charbonnier, S.; Sidi, A.O.; McEwen, A.G.; Ferrario, M.G.; Poussin-Courmontagne, P.; Cura, V.; Brimer, N.; Babah, K.O.; Ansari, T.; et al. Structural basis for hijacking of cellular LxxLL motifs by papillomavirus E6 oncoproteins. Science 2013, 339, 694–698.
58. Nominé, Y.; Masson, M.; Charbonnier, S.; Zanier, K.; Ristriani, T.; Deryckère, F.; Sibler, A.-P.; Desplancq, D.; Atkinson, R.A.; Weiss, E.; et al. Structural and functional analysis of E6 oncoprotein: Insights in the molecular pathways of human papillomavirus-mediated pathogenesis. Mol. Cell 2006, 21, 665–678.
59. Nguyen, M.L.; Nguyen, M.M.; Lee, D.; Griep, A.E.; Lambert, P.F. 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.
60. Shai, A.; Brake, T.; Somoza, C.; Lambert, P.F. The human papillomavirus E6 oncogene dysregulates the cell cycle and contributes to cervical carcinogenesis through two independent activities. Cancer Res. 2007, 67, 1626–1635.
61. Howley, P.M.; Lowy, D.R. Fields Virology; Wolters Kluwer: Alphen aan den Rijn, The Netherlands; Lippincott Williams & Wilkins: Philadelphia, PA, USA, 2007; pp. 2299–2354.
62. Doorbar, J. Molecular biology of human papillomavirus infection and cervical cancer. Clin. Sci. (Lond.) 2006, 110, 525–541.
63. Park, R.B.; Androphy, E.J. Genetic analysis of high-risk e6 in episomal maintenance of human papillomavirus genomes in primary human keratinocytes. J. Virol. 2002, 76, 11359–11364.
64. Thomas, J.T.; Hubert, W.G.; Ruesch, M.N.; Laimins, L.A. Human papillomavirus type 31 oncoproteins E6 and E7 are required for the maintenance of episomes during the viral life cycle in normal human keratinocytes. Proc. Natl. Acad. Sci. USA 1999, 96, 8449–8454.
65. Wang, H.-K.; Duffy, A.A.; Broker, T.R.; Chow, L.T. Robust production and passaging of infectious HPV in squamous epithelium of primary human keratinocytes. Genes Dev. 2009, 23, 181–194.
66. Delury, C.P.; Marsh, E.K.; James, C.D.; Boon, S.S.; Banks, L.; Knight, G.L.; 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.
67. 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.
68. Brimer, N.; Vande Pol, S.B. Papillomavirus E6 PDZ Interactions Can Be Replaced by Repression of p53 To Promote Episomal Human Papillomavirus Genome Maintenance. J. Virol. 2013, 88, 3027–3030.
69. Ramirez, J.; Poirson, J.; Foltz, C.; Chebaro, Y.; Schrapp, M.; Meyer, A.; Bonetta, A.; Forster, A.; Jacob, Y.; Masson, M.; et al. Targeting the Two Oncogenic Functional Sites of the HPV E6 Oncoprotein with a High-Affinity Bivalent Ligand. Angew. Chem. Int. Ed. Engl. 2015, 54, 7958–7962.
70. Van Doorslaer, K.; DeSalle, R.; Einstein, M.H.; Burk, R.D. Degradation of Human PDZ-Proteins by Human Alphapapillomaviruses Represents an Evolutionary Adaptation to a Novel Cellular Niche. PLoS Pathog. 2015, 11, e1004980.
71. Watson, R.A.; 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, 116, 4925–4934.
72. James, M.A.; Lee, J.H.; Klingelhutz, A.J. Human papillomavirus type 16 E6 activates NF-kappaB, induces cIAP-2 expression, and protects against apoptosis in a PDZ binding motif-dependent manner. J. Virol. 2006, 80, 5301–5307.
73. Sherman, L.; Itzhaki, H.; Jackman, A.; Chen, J.J.; Koval, D.; 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 2002, 292, 309–320.
74. Muench, P.; Hiller, T.; Probst, S.; Florea, A.-M.; Stubenrauch, F.; Iftner, T. Binding of PDZ proteins to HPV E6 proteins does neither correlate with epidemiological risk classification nor with the immortalization of foreskin keratinocytes. Virology 2009, 387, 380–387.
75. Riley, R.R.; Duensing, S.; Brake, T.; Mu, K.; Lambert, P.F.; Arbeit, J.M. Dissection of Human Papillomavirus E6 and E7 Function in Transgenic Mouse Models of Cervical Carcinogenesis. Cancer Res. 2003, 63, 4862–4871.
76. Song, S.; Pitot, H.C.; Lambert, P.F. The human papillomavirus type 16 E6 gene alone is sufficient to induce carcinomas in transgenic animals. J. Virol. 1999, 73, 5887–5893.
77. Jabbar, S.; Strati, K.; Shin, M.K.; Pitot, H.C.; Lambert, P.F. Human papillomavirus type 16 E6 and E7 oncoproteins act synergistically to cause head and neck cancer in mice. Virology 2010, 407, 60–67.
78. Thomas, M.K.; Pitot, H.C.; Liem, A.; Lambert, P.F. Dominant role of HPV16 E7 in anal carcinogenesis. Virology 2011, 421, 114–118.
79. Strati, K.; Lambert, P.F. Role of Rb-dependent and Rb-independent functions of papillomavirus E7 oncogene in head and neck cancer. Cancer Res. 2007, 67, 11585–11593.
80. 79. Suzuki, A.; Ohno, S. The PAR-aPKC system: Lessons in polarity. J. Cell Sci. 2006, 119, 979–987.
81. Halaoui, R.; McCaffrey, L. Rewiring cell polarity signaling in cancer. Oncogene 2014, 34, 1–12.
82. Pocha, S.M.; Knust, E. Complexities of Crumbs function and regulation in tissue morphogenesis. Curr. Biol. 2013, 23, R289–R293.
83. Laprise, P. Emerging role for epithelial polarity proteins of the Crumbs family as potential tumor suppressors. J. Biomed. Biotechnol. 2011, 2011, 868217.
84. Pim, D.; Bergant, M.; Boon, S.S.; Ganti, K.; Kranjec, C.; Massimi, P.; Subbaiah, V.K.; Thomas, M.; Tomaić, V.; Banks, L. Human papillomaviruses and the specificity of PDZ domain targeting. FEBS J. 2012, 279, 3530–3537.
85. McCaffrey, L.M.; Macara, I.G. Epithelial organization, cell polarity and tumorigenesis. Trends Cell Biol. 2011, 21, 727–735.
86. Goldenring, J.R. A central role for vesicle trafficking in epithelial neoplasia: Intracellular highways to carcinogenesis. Nat. Rev. Cancer 2013, 13, 813–820.
87. Tomaić, 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 2009, 28, 1–8.
88. 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.
89. Kamei, Y.; Kito, K.; Takeuchi, T.; Imai, Y.; Murase, R.; Ueda, N.; Kobayashi, N.; Abe, Y. Human scribble accumulates in colorectal neoplasia in association with an altered distribution of β-catenin. Hum. Pathol. 2007, 38, 1273–1281.
90. Zhan, L.; Rosenberg, A.; Bergami, K.C.; Yu, M.; Xuan, Z.; Jaffe, A.B.; Allred, C.; Muthuswamy, S.K. Deregulation of scribble promotes mammary tumorigenesis and reveals a role for cell polarity in carcinoma. Cell 2008, 135, 865–878.
91. Pearson, H.B.; Perez-Mancera, P.A.; Dow, L.E.; Ryan, A.; Tennstedt, P.; Bogani, D.; Elsum, I.; Greenfield, A.; Tuveson, D.A.; Simon, R.; et al. SCRIB expression is deregulated in human prostate cancer, and its deficiency in mice promotes prostate neoplasia. J. Clin. Investig. 2011, 121, 4257–4267.
92. Ouyang, Z.; Zhan, W.; Dan, L. hScrib, a human homolog of Drosophila neoplastic tumor suppressor, is involved in the progress of endometrial cancer. Oncol. Res. 2010, 18, 593–599.
93. 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.
94. Watson, R.A.; Rollason, T.P.; Reynolds, G.M.; Murray, P.G.; Banks, L.; 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.
95. Lin, H.-T.; Steller, M.A.; Aish, L.; Hanada, T.; Chishti, A.H. Differential expression of human Dlg in cervical intraepithelial neoplasias. Gynecol. Oncol. 2004, 93, 422–428.
96. 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.
97. Roberts, S.; Delury, C.; Marsh, E. The PDZ protein discs-large (DLG): The “Jekyll and Hyde” of the epithelial polarity proteins. FEBS J. 2012, 279, 3549–3558.
98. Anastas, J.N.; Biechele, T.L.; Robitaille, M.; Muster, J.; Allison, K.H.; Angers, S.; Moon, R.T. A protein complex of SCRIB, NOS1AP and VANGL1 regulates cell polarity and migration, and is associated with breast cancer progression. Oncogene 2012, 31, 3696–3708.
99. Frese, K.K.; Latorre, I.J.; Chung, S.-H.; Caruana, G.; Bernstein, A.; Jones, S.N.; Donehower, L.A.; Justice, M.J.; Garner, C.C.; Javier, R.T. Oncogenic function for the Dlg1 mammalian homolog of the Drosophila discs-large tumor suppressor. EMBO J. 2006, 25, 1406–1417.
100. Kong, K.; Kumar, M.; Taruishi, M.; Javier, R.T. 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.
101. Feigin, M.E.; Akshinthala, S.D.; Araki, K.; Rosenberg, A.Z.; Muthuswamy, L.B.; Martin, B.; Lehmann, B.D.; Berman, H.K.; Pietenpol, J.A.; Cardiff, R.D.; et al. Mislocalization of the cell polarity protein scribble promotes mammary tumorigenesis and is associated with basal breast cancer. Cancer Res. 2014, 74, 3180–3194.
102. Krishna Subbaiah, V.; Massimi, P.; Boon, S.S.; Myers, M.P.; 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.
103. 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.
104. 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.
105. Thomas, M.; Glaunsinger, B.; Pim, D.; Javier, R.; Banks, L. HPV E6 and MAGUK protein interactions: Determination of the molecular basis for specific protein recognition and degradation. Oncogene 2001, 20, 5431–5439.
106. Kranjec, C.; Massimi, P.; Banks, L. Restoration of MAGI-1 expression in human papillomavirus-positive tumor cells induces cell growth arrest and apoptosis. J. Virol. 2014, 88, 7155–7169.
107. Ostrow, R.S.; LaBresh, K.V; Faras, A.J. Characterization of the complete RhPV 1 genomic sequence and an integration locus from a metastatic tumor. Virology 1991, 181, 424–429.
108. De Villiers, E.-M.; Fauquet, C.; Broker, T.R.; Bernard, H.-U.; zur Hausen, H. Classification of papillomaviruses. Virology 2004, 324, 17–27.
109. Wood, C.E.; Chen, Z.; Cline, J.M.; Miller, B.E.; Burk, R.D. Characterization and experimental transmission of an oncogenic papillomavirus in female macaques. J. Virol. 2007, 81, 6339–6345.
110. Bilder, D. Epithelial polarity and proliferation control: Links from the Drosophila neoplastictumor suppressors. Genes Dev. 2004, 18, 1909–1925.
111. 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.
112. Kühne, C.; Gardiol, D.; Guarnaccia, C.; Amenitsch, H.; Banks, L. Differential regulation of human papillomavirus E6 by protein kinase A: Conditional degradation of human discs large protein by oncogenic E6. Oncogene 2000, 19, 5884–5891.
113. Ivarsson, Y. Plasticity of PDZ domains in ligand recognition and signaling. FEBS Lett. 2012, 586, 2638–2647.
114. Contreras Paredes, A.; Martínez Ramírez, I.; Dueñas González, A.; Lizano, M. E6 variants of human papillomavirus 18 differentially modulate the protein kinase B/phosphatidylinositol 3-kinase (akt/PI3K) signaling pathway. Virology 2009, 383, 78–85.
115. Rubio, M.P.; Geraghty, K.M.; Wong, B.H.C.; Wood, N.T.; Campbell, D.G.; Morrice, N.; Mackintosh, C. 14-3-3-affinity purification of over 200 human phosphoproteins reveals new links to regulation of cellular metabolism, proliferation and trafficking. Biochem. J. 2004, 379, 395–408.
116. Jin, J.; Smith, F.D.; Stark, C.; Wells, C.D.; Fawcett, J.P.; Kulkarni, S.; Metalnikov, P.; O’Donnell, P.; Taylor, P.; Taylor, L.; et al. Proteomic, Functional, and Domain-Based Analysis of In Vivo 14-3-3 Binding Proteins Involved in Cytoskeletal Regulation and Cellular Organization. Curr. Biol. 2004, 14, 1436–1450.
117. Meek, S.E.M.; Lane, W.S.; Piwnica-Worms, H. Comprehensive Proteomic Analysis of Interphase and Mitotic 14-3-3-binding Proteins. J. Biol. Chem. 2004, 279, 32046–32054.
118. Benzinger, A. Targeted Proteomic Analysis of 14-3-3, a p53 Effector Commonly Silenced in Cancer. Mol. Cell. Proteomics 2005, 4, 785–795.
119. Dougherty, M.K. Unlocking the code of 14-3-3. J. Cell Sci. 2004, 117, 1875–1884.