Papillomavirus E5: The smallest oncoprotein with many functions

Molecular Cancer

Volumn 10, Issue , 2011, Pages

  Venuti, Aldo ^a   Paolini, Francesca ^a   Nasir, Lubna ^b   Corteggio, Annunziata ^c   Roperto, Sante ^c   Campo, Maria S ^b   Borzacchiello, Giuseppe ^c  

^a REGINA ELENA NATIONAL CANCER INSTITUTE   (Italy)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

^c UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

Animal models; Cell transformation; E5 oncoprotein; Growth factor receptors; Immune escape; Oncogene; Papillomaviruses

Indexed keywords

ENDOTHELIN 1; EPIDERMAL GROWTH FACTOR RECEPTOR; KERATINOCYTE GROWTH FACTOR RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; ONCOPROTEIN; PAPILLOMAVIRUS E5 PROTEIN; PROTEIN KINASE C; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; UNCLASSIFIED DRUG; VIRUS PROTEIN; ONCOGENE PROTEIN E5, HUMAN PAPILLOMAVIRUS TYPE 16;

APOPTOSIS; BIOLOGICAL ACTIVITY; CARCINOGENESIS; CELL CYCLE; CELL FUSION; CELL INTERACTION; CELL PROLIFERATION; CELL TRANSFORMATION; CYTOTOXIC T LYMPHOCYTE; DOWN REGULATION; ENDOPLASMIC RETICULUM; ENDOPLASMIC RETICULUM STRESS; GOLGI COMPLEX; HOST CELL; HUMAN PAPILLOMAVIRUS TYPE 16; IMMUNE EVASION; MAJOR HISTOCOMPATIBILITY COMPLEX; MOLECULARLY TARGETED THERAPY; NONHUMAN; OPEN READING FRAME; PAPILLOMAVIRUS INFECTION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN STRUCTURE; REVIEW; UTERINE CERVIX CARCINOMA IN SITU; VIRUS REPLICATION; ANIMAL; CATTLE; HUMAN; METABOLISM; PAPILLOMA VIRUS; PHYSIOLOGY; VIRUS CELL TRANSFORMATION;

ANIMALIA; BOVINAE; BOVINE PARVOVIRUS; HUMAN PAPILLOMAVIRUS TYPE 16; PAPILLOMAVIRIDAE;

ANIMALS; CATTLE; CELL TRANSFORMATION, VIRAL; HUMANS; ONCOGENE PROTEINS, VIRAL; PAPILLOMAVIRIDAE;

EID: 81055131727     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-10-140     Document Type: Review

References (184)

1. IARC Working Group Human papillomaviruses. 1995, 64. Lyon, International Agency for research on cancer, IARC Working Group.
2. Walboomers JM, Jacobs MV, Manos MM, Bosch FX, Kummer JA, Shah KV, Snijders PJ, Peto J, Meijer CJ, Muñoz N. Human papillomavirus is a necessary cause of invasive cervical cancer worldwide. J Pathol 1999, 189:12-19.
3. Frazer IH. Prevention of cervical cancer through papillomavirus vaccination. Nat Rev Immunol 2004, 4:46-54.
4. Parkin DM, Bray F. Chapter 2: The burden of HPV-related cancers. Vaccine 2006, 24:11-25.
5. Syrjänen S, Lodi G, von Bültzingslöwen I, Aliko A, Arduino P, Campisi G, Challacombe S, Ficarra G, Flaitz C, Zhou HM, Maeda H, Miller C, Jontell M. Human papillomaviruses in oral carcinoma and oral potentially malignant disorders: a systematic review. Oral Dis 2011, 17:58-72.
6. Klozar J, Tachezy R, Rotnáglová E, Koslabová E, Saláková M, Hamsíková E. Human papillomavirus in head and neck tumors: epidemiological, molecular and clinical aspects. Wien Med Wochenschr 2010, 160:305-309.
7. Zafer E, Ergun MA, Alver G, Sahin FI, Yavuzer S, Ekmekci A. Detection and typing of human papillomavirus in non-small cell lung cancer. Respiration 2004, 71:88-90.
8. Gillison ML. Human papillomavirus-associated head and neck cancer is a distinct epidemiologic, clinical, and molecular entity. Semin Oncol 2004, 31:744-754.
9. Syrjänen KJ. HPV infections in benign and malignant sinonasal lesions. J Clin Pathol 2003, 56:174-181.
10. zur Hausen H. Yohei Ito Memorial Lecture: Papillomaviruses in human cancers. Leukemia 1999, 13:1-5.
11. Audeau A, Han HW, Johnston MJ, Whitehead MW, Frizelle FA. Does human papilloma virus have a role in squamous cell carcinoma of the colon and upper rectum?. Eur J Surg Oncol 2002, 28:657-660.
12. Damin AP, Karam R, Zettler CG, Caleffi M, Alexandre CO. Evidence for an association of human papillomavirus and breast carcinomas. Breast Cancer Res Treat 2004, 84:131-137.
13. Shigehara K, Sasagawa T, Kawaguchi S, Nakashima T, Shimamura M, Maeda Y, Konaka H, Mizokami A, Koh E, Namiki M. Etiologic role of human papillomavirus infection in bladder carcinoma. Cancer 2011, 117:2067-2076.
14. Martinez-Fierro ML, Leach RJ, Gomez-Guerra LS, Garza-Guajardo R, Johnson-Pais T, Beuten J, Morales-Rodriguez IB, Hernandez-Ordoñez MA, Calderon-Cardenas G, Ortiz-Lopez R, Rivas-Estilla AM, Ancer-Rodriguez J, Rojas-Martinez A. Identification of viral infections in the prostate and evaluation of their association with cancer. BMC Cancer 2010, 10:326.
15. Borzacchiello G, Roperto F, Nasir L, Campo MS. Human papillomavirus research: do we still need animal models?. Int J Cancer 2009, 125:739-740.
16. Werness BA, Levine AJ, Howley PM. Association of human papillomavirus types 16 and 18 E6 proteins with p53. Science 1990, 248:76-79.
17. Scheffner M, Werness BA, Huibregtse JM, Levine AJ, Howley PM. The E6 oncoprotein encoded by human papillomavirus types 16 and 18 promotes the degradation of p53. Cell 1990, 63:1129-1136.
18. Moody CA, Laimins LA. Human papillomavirus oncoproteins: pathways to transformation. Nat Rev Cancer 2010, 10:550-560.
19. Bernard HU, Burk RD, Chen Z, van Doorslaer K, Hausen H, de Villiers EM. Classification of papillomaviruses (PVs) based on 189 PV types and proposal of taxonomic amendments. Virology 2010, 401:70-79.
20. Muñoz N, Bosch FX, de Sanjosé S, Herrero R, Castellsagué X, Shah KV, Snijders PJ, Meijer CJ, . International Agency for Research on Cancer Multicenter Cervical Cancer Study Group Epidemiologic classification of human papillomavirus types associated with cervical cancer. N Engl J Med 2003, 348:518-527. International Agency for Research on Cancer Multicenter Cervical Cancer Study Group.
21. Nath R, Mant CA, Kell B, Cason J, Bible JM. Analyses of variant human papillomavirus type-16 E5 proteins for their ability to induce mitogenesis of murine fibroblasts. Cancer Cell Int 2006, 6:19-27.
22. Bravo IG, Alonso A. Mucosal human papillomaviruses encode four different E5 proteins whose chemistry and phylogeny correlate with malignant or benign growth. J Virol 2004, 78:13613-13626.
23. Schiffman M, Herrero R, Desalle R, Hildesheim A, Wacholder S, Rodriguez AC, Bratti MC, Sherman ME, Morales J, Guillen D, Alfaro M, Hutchinson M, Wright TC, Solomon D, Chen Z, Schussler J, Castle PE, Burk RD. The carcinogenicity of human papillomavirus types reflects viral evolution. Virology 2005, 337:76-84.
24. Garcia-Vallve S, Alonso A, Bravo IG. Papillomaviruses: different genes have different histories. Trends Microbiol 2005, 13:514-521.
25. Longworth MS, Laimins LA. Pathogenesis of human papillomaviruses in differentiating epithelia. Microbiol Mol Biol Rev 2004, 68:362-372.
26. Burnett S, Jareborg N, DiMaio D. Localization of bovine papillomavirus type 1 E5 protein to transformed basal keratinocytes and permissive differentiated cells in fibropapilloma tissue. Proc Natl Acad Sci USA 1992, 89:5665-5669.
27. Araibi EH, Marchetti B, Ashrafi GH, Campo MS. Downregulation of major histocompatibility complex class I in bovine papillomas. J Gen Virol 2004, 85:2809-2814.
28. Chang JL, Tsao YP, Liu DW, Huang SJ, Lee WH, Chen SL. The expression of HPV- 16 E5 protein in squamous neoplastic changes in the uterine cervix. J Biomed Sci 2001, 8:206-213.
29. Chen SL, Mounts P. Transforming activity of E5a protein of human papillomavirus type 6 in NIH 3T3 and C127 cells. J Virol 1990, 64:3226-3233.
30. Leechanachai P, Banks L, Moreau F, Matlashewski G. The E5 gene from human papillomavirus type 16 is an oncogene which enhances growth factor-mediated signal transduction to the nucleus. Oncogene 1992, 7:19-25.
31. Leptak C, Ramon y Cajal S, Kulke R, Horwitz BH, Riese DJ, Dotto GP, DiMaio D. Tumorigenic transformation of murine keratinocytes by the E5 genes of bovine papillomavirus type 1 and human papillomavirus type 16. J Virol 1991, 65:7078-7083.
32. Pim D, Collins M, Banks L. Human papillomavirus type 16 E5 gene stimulates the transforming activity of the epidermal growth factor receptor. Oncogene 1992, 7:27-32.
33. Bouvard V, Matlashewski G, Gu ZM, Storey A, Banks L. The human papillomavirus type 16 E5 gene cooperates with the E7 gene to stimulate proliferation of primary cells and increases viral gene expression. Virology 1994, 203:73-80.
34. Straight SW, Herman B, McCance DJ. The E5 oncoprotein of human papillomavirus type 16 inhibits the acidification of endosomes in human keratinocytes. J Virol 1995, 69:3185-3192.
35. Valle FG, Banks L. The human papillomavirus (HPV)-6 and HPV-16 E5 proteins co-operate with HPV-16 E7 in the transformation of primary rodent cells. J Gen Virol 1995, 76:1239-1245.
36. Venuti A, Salani D, Poggiali F, Manni V, Bagnato A. The E5 oncoprotein of human papillomavirus type 16 enhances endothelin-1-induced keratinocyte growth. Virology 1998, 248:1-5.
37. Ghai J, Ostrow RS, Tolar J, McGlennen RC, Lemke TD, Tobolt D, Liu Z, Faras AJ. The E5 gene product of rhesus papillomavirus is an activator of endogenous Ras and phosphatidylinositol-3'-kinase in NIH 3T3 cells. Proc Natl Acad Sci USA 1996, 93:12879-12884.
38. Rho J, de Villiers EM, Choe J. Transforming activities of human papillomavirus type 59 E5, E6 and E7 open reading frames in mouse C127 cells. Virus Res 1996, 44:57-65.
39. Conrad M, Bubb VJ, Schlegel R. The human papillomavirus type 6 and 16 E5 proteins are membrane-associated proteins which associate with the 16-kilodalton pore-forming protein. J Virol 1993, 67:6170-6178.
40. Disbrow GL, Sunitha I, Baker CC, Hanover J, Schlegel R. Codon optimization of the HPV-16 E5 gene enhances protein expression. Virology 2003, 311:105-114.
41. Hu L, Ceresa BP. Characterization of the plasma membrane localization and orientation of HPV16 E5 for cell-cell fusion. Virology 2009, 393:135-143.
42. Hu L, Plafker K, Vorozhko V. Human papillomavirus E5 induces bi-nucleated cell formation by cell-cell fusion. Virology 2009, 384:125-134.
43. Hu L, Potapova TA, Li S. Expression of HPV16 E5 produces enlarged nuclei and polyploidy through endoreplication. Virology 2010, 405:342-351.
44. Krawczyk E, Suprynowicz FA, Sudarshan SR, Schlegel R. Membrane orientation of the human papillomavirus type 16 E5 oncoprotein. J Virol 2010, 84:1696-1703.
45. Hanover JA, Schlegel R, Suprynowicz FA. Karyopherin β3: a new cellular target for the HPV-16 E5 oncoprotein. Biochem Biophys Res Commun 2008, 371:684-688.
46. Deane R, Schäfer W, Zimmermann HP, Mueller L, Goörlich D, Prehn S, Ponstingl H, Bischoff FR. Ran-binding protein 5 (RanBP5) is related to the nuclear transport factor importin-beta but interacts differently with RanBP1. Mol Cell Biol 1997, 17:5087-5096.
47. Yaseen NR, Blobel G. Cloning and characterization of human karyopherin β3. Proc Natl Acad Sci USA 1997, 94:4451-4456.
48. Burkhardt A, Willingham M, Gay C, Jeang KT, Schlegel R. The E5 oncoprotein of bovine papillomavirus is oriented asymmetrically in Golgi and plasma membranes. Virology 1989, 170:334-339.
49. Yang DH, Wildeman AG, Sharom FJ. Overexpression, purification, and structural analysis of the hydrophobic E5 protein from human papillomavirus type 16. Protein Expr Purif 2003, 30:1-10.
50. Gieswein CE, Sharom FJ, Wildeman AG. Oligomerization of the E5 protein of human papillomavirus type 16 occurs through multiple hydrophobic regions. Virology 2003, 313:415-426.
51. Gruener M, Bravo IG, Momburg F, Alonso A, Tomakidi P. The E5 protein of the human papillomavirus type 16 down-regulates HLA-I surface expression in calnexin expressing but not in calnexin-deficient cells. Virol J 2007, 4:116-130.
52. Regan JA, Laimins LA. Bap31 is a novel target of the human papillomavirus E5 protein. J Virol 2008, 82:10042-10051.
53. Cortese MS, Ashrafi GH, Campo MS. All four di-leucine motifs in the first hydrophobic domain of the E5 oncoprotein of human papillomavirus type 16 are essential for surface MHC class I downregulation activity and E5 endomembrane localization. Int J Cancer 2010, 126:1675-1682.
54. Adam JL, Briggs MW, McCance DJ. A mutagenic analysis of the E5 protein of human papillomavirus type 16 reveals that E5 binding to the vacuolar H+-ATPase is not sufficient for biological activity, using mammalian and yeast expression systems. Virology 2000, 272:315-325.
55. Rodriguez MI, Finbow ME, Alonso A. Binding of human papillomavirus 16 E5 to the 16 kDa subunit c (proteolipid) of the vacuolar H+-ATPase can be dissociated from the E5-mediated epidermal growth factor receptor overactivation. Oncogene 2000, 19:3727-3732.
56. Krawczyk E, Suprynowicz FA, Liu X, Dai Y, Hartmann DP, Hanover J, Schlegel R. Koilocytosis: a cooperative interaction between the human papillomavirus E5 and E6 oncoproteins. Am J Pathol 2008, 173:682-688.
57. Krawczyk E, Suprynowicz FA, Hebert JD, Kamonjoh CM, Schlegel R. The human papillomavirus type 16 E5 oncoprotein translocates calpactin I to the perinuclear region. J Virol 2011, 85:10968-10975.
58. Straight SW, Hinkle PM, Jewers RJ, McCance DJ. The E5 oncoprotein of human papillomavirus type 16 transforms fibroblasts and effects the downregulation of the epidermal growth factor receptor in keratinocytes. J Virol 1993, 67:4521-4532.
59. Mittal KR, Chan W, Demopoulos RL. Sensitivity and specificity of various morphological features of cervical condylomas. Arch Pathol Lab Med 1990, 114:1038-1041.
60. Prasad CJ, Sheets E, Selig AM, McArthur MC, Crum CP. The bi-nucleated squamous cell: histologic spectrum and relationship to low-grade squamous intraepithelial lesions. Mod Pathol 1993, 6:313-317.
61. Wright TC, Gatscha RM, Luff RD, Prey MU. Epithelial cell abnormalities: squamous. The Bethesda System for Reporting Cervical Cytology 2004, 89-123. New York: Springer-Verlag, Solomon D, Nayar R, 2.
62. Olaharski AJ, Sotelo R, Solorza-Luna G, Gonsebatt ME, Guzman P, Mohar A, Eastmond DA. Tetraploidy and chromosomal instability are early events during cervical carcinogenesis. Carcinogenesis 2006, 27:337-343.
63. Egawa K. Do human papillomaviruses target epidermal stem cells?. Dermatology 2003, 207:251-254.
64. McMurray HR, Nguyen D, Westbrook TF, McAnce DJ. Biology of human papillomaviruses. Int J Exp Pathol 2001, 82:15-33.
65. zur Hausen H. Papillomaviruses and cancer: from basic studies to clinical application. Nat Rev Cancer 2002, 2:342-350.
66. Fehrmann F, Laimins LA. Human papillomaviruses: targeting differentiating epithelial cells for malignant transformation. Oncogene 2003, 22:5201-5207.
67. Genther Williams SM, Disbrow GL, Schlegel R, Lee D, Threadgill DW, Lambert PF. Requirement of epidermal growth factor receptor for hyperplasia induced by E5, a high-risk human papillomavirus oncogene. Cancer Research 2005, 65:6534-6542.
68. DiMaio D, Mattoon D. Mechanism s of cell transformation by papillomavirus E5 proteins. Oncogene 2001, 20:7866-7873.
69. Thomsen P, van Deurs B, Norrild B, Kayser L. The HPV16 E5 oncogene inhibits endocytic trafficking. Oncogene 2000, 19:6023-6032.
70. Crusius K, Rodriguez I, Alonso A. The human papillomavirus type 16 E5 protein modulates ERK1/2 and p38 MAP kinase activation by an EGFR-independent process in stressed human keratinocytes. Virus Genes 2000, 20:65-69.
71. Crusius K, Auvinen E, Alonso A. Enhancement of EGF- and PMA-mediated MAP kinase activation in cells expressing the human papillomavirus type 16 E5 protein. Oncogene 1997, 15:1437-1444.
72. Gu Z, Matlashewski G. Effect of human papillomavirus type 16 oncogenes on MAP kinase activity. J Virol 1995, 69:8051-8056.
73. Chen SL, Huang CH, Tsai TC, Lu KY, Tsao YP. The regulation mechanism of c-jun and junB by human papillomavirus type 16 E5 oncoprotein. Arch Virol 1996, 141:791-800.
74. Chen SL, Lin YK, Li LY, Tsao YP, Lo HY, Wang WB, Tsai TC. E5 proteins of human papillomavirus types 11 and 16 transactivate the c-fos promoter through the NF1 binding element. J Virol 1996, 70:8558-8563.
75. Crusius K, Auvinen E, Steuer B, Gaissert H, Alonso A. The human papillomavirus type 16 E5-protein modulates ligand-dependent activation of the EGF receptor family in the human epithelial cell line HaCaT. Exp Cell Res 1998, 241:76-83.
76. Hwang ES, Nottoli T, Dimaio D. The HPV16 E5 protein: expression, detection, and stable complex formation with transmembrane proteins in COS cells. Virology 1995, 211:227-233.
77. Chen SL, Lin ST, Tsai TC, Hsiao WC, Tsao YP. ErbB4 (JM-b/CYT-1)-induced expression and phosphorylation of c-Jun is abrogated by human papillomavirus type 16 E5 protein. Oncogene 2007, 26:42-53.
78. Simeone P, Teson M, Latini A, Carducci M, Venuti A. Endothelin-1 could be one of the targets of psoriasis therapy. Br J Dermatol 2004, 151:1273-1275.
79. Bagnato A, Loizidou M, Pflug BR, Curwen J, Growcott J. Role of the endothelin axis and its antagonists in the treatment of cancer. Br J Pharmacol 2011, 163:220-233.
80. Belleudi F, Leone L, Purpura V, Cannella F, Scrofani C, Torrisi MR. HPV16 E5 affects the KGFR/FGFR2b-mediated epithelial growth through alteration of the receptor expression, signalling and endocytic traffic. Oncogene 2011,
81. Tsao YP, Li LY, Tsai TC, Chen SL. Human papillomavirus type 11 and 16 E5 represses p21(WafI/SdiI/CipI) gene expression in fibroblasts and keratinocytes. J Virol 1996, 70:7535-7539.
82. Pedroza-Saavedra A, Lam EW, Esquivel-Guadarrama F, Gutierrez-Xicotencatl L. The human papillomavirus type 16 E5 oncoprotein synergizes with EGFreceptor signalling to enhance cell cycle progression and the down-regulation of p27(Kip1). Virology 2010, 400:44-52.
83. Oelze I, Kartenbeck J, Crusius K, Alonso A. Human papillomavirus type 16 E5 protein affects cell-cell communication in an epithelial cell line. J Virol 1995, 69:4489-4494.
84. Tomakidi P, Cheng H, Kohl A, Komposch G, Alonso A. Connexin 43 expression is downregulated in raft cultures of human keratinocytes expressing the human papillomavirus type 16 E5 protein. Cell Tissue Res 2000, 301:323-327.
85. Stoler MH, Rhodes CR, Whitbeck A, Wolinsky SM, Chow LT, Broker TR. Human papillomavirus type 16 and 18 gene expression in cervical neoplasias. Hum Pathol 1992, 23:117-128.
86. Kell B, Jewers RJ, Cason J, Pakarian F, Kaye JN, Best JM. Detection of E5 oncoprotein in human papillomavirus type 16-positive cervical scrapes using antibodies raised to synthetic peptides. J Gen Virol 1994, 75:2451-2456.
87. Kabsch K, Alonso A. The human papillomavirus type 16 E5 protein impairs TRAIL- and FasL-mediated apoptosis in HaCaT cells by different mechanisms. J Virol 2002, 76:12162-12172.
88. Kabsch K, Mossadegh N, Kohl A, Komposch G, Schenkel J, Alonso A, Tomakidi P. The HPV-16 E5 protein inhibits TRAIL- and FasL-mediated apoptosis in human keratinocyte raft cultures. Intervirology 2004, 47:48-56.
89. Zhang B, Spandau DF, Roman A. E5 protein of human papillomavirus type 16 protects human foreskin keratinocytes from UV B-irradiation-induced apoptosis. J Virol 2002, 76:220-231.
90. Kabsch K, Alonso A. The human papillomavirus type 16 (HPV-16) E5 protein sensitizes human keratinocytes to apoptosis induced by osmotic stress. Oncogene 2002, 21:947-953.
91. Tardif KD, Mori K, Kaufman RJ, Siddiqui A. Hepatitis C virus suppresses the IRE1-XBP1 pathway of the unfolded protein response. J Biol Chem 2004, 279:17158-17164.
92. Schiffman M, Castle PE. The promise of global cervical-cancer prevention. N Engl J Med 2005, 353:2101-2104.
93. Condjella R, Liu X, Suprynowicz F, Yuan H, Sudarshan S, Dai Y, Schlegel R. The canine papillomavirus E5 protein signals from the endoplasmic reticulum. J Virol 2009, 83:12833-12841.
94. Wu R, Abramson AL, Shikowitz MJ, Dannenberg AJ, Steinberg BM. Epidermal growth factor-induced cyclooxygenase-2 expression is mediated through phosphatidylinositol-3 kinase, not mitogen-activated protein/extracellular signal-regulated kinase kinase, in recurrent respiratory papillomas. Clin Cancer Res 2005, 11:6155-6161.
95. Wu R, Coniglio SJ, Chan A, Symons MH, Steinberg BM. Up-regulation of Rac1 by epidermal growth factor mediates COX-2 expression in recurrent respiratory papillomas. Mol Med 2007, 13:143-150.
96. Subbaramaiah K, Dannenberg AJ. Cyclooxygenase-2 transcription is regulated by human papillomavirus 16 E6 and E7 oncoproteins: evidence of a corepressor/coactivator exchange. Cancer Res 2007, 67:3976-3985.
97. Kim SH, Oh JM, No JH, Bang YJ, Juhnn YS, Song YS. Involvement of NFkappaB and AP-1 in COX-2 upregulation by human papillomavirus 16 E5 oncoprotein. Carcinogenesis 2009, 30:753-757.
98. Sudarshan SR, Schlegel R, Liu X. The HPV-16 E5 protein represses expression of stress pathway genes XBP-1 and COX-2 in genital keratinocytes. Biochem Biophys Res Commun 2010, 399:617-622.
99. Oh JM, Lee YI, Song YS, Kim WH, Juhnn YS. Human papillomavirus E5 protein induces expression of the EP4 subtype of prostaglandin E2 receptor in cyclic AMP response element-dependent pathways in cervical cancer cells. Carcinogenesis 2009, 30:141-149.
100. Stanley MA, Pett MR, Coleman N. HPV: from infection to cancer. Biochem Soc Trans 2007, 35:1456-1460.
101. O'Brien PM, Campo MS. Evasion of host immunity directed by papillomavirus encoded proteins. Virus Res 2002, 1:103-118.
102. Ashrafi GH, Haghshenas MR, Marchetti B, O'Brien PM, Campo MS. The E5 protein of human papillomavirus type 16 selectively down-regulates surface HLA class. Int J Cancer 2005, 113:276-283.
103. Schapiro F, Sparkowski J, Adduci A, Schlegel R, Grinstein S. Golgi alkalinization by the papillomavirus E5 oncoprotein. J Cell Biol 2000, 148:305-315.
104. Ashrafi GH, Haghshenas M, Marchetti B, Campo MS. E5 protein of human papillomavirus 16 downregulates HLA class I and interacts with the heavy chain via its first hydrophobic domain. Int J Cancer 2006, 119:2105-2112.
105. Araibi EH, Marchetti B, Dornan ES, Ashrafi GH, Dobromylskyj M, Ellis SA, Campo MS. The E5 oncoprotein of BPV-4 does not interfere with the biosynthetic pathway of non-classical MHC class I. Virology 2006, 353:174-183.
106. Campo MS, Graham SV, Cortese MS, Ashrafi GH, Araibi EH, Dornan ES, Miners K, Nunes C, Man S. HPV-16 E5 down-regulates expression of surface HLA class I and reduces recognition by CD8 T cells. Virology 2010, 407:137-142.
107. Zhang B, Li P, Wang E, Brahmi Z, Dunn KW, Blum JS, Roman A. The E5 protein of human papillomavirus type 16 perturbs MHC class II antigen maturation in human foreskin keratinocytes treated with interferon-γ. Virology 2003, 310:100-108.
108. Barnard P, Payne E, McMillan N. The human papillomavirus E7 protein is able to inhibit the antiviral and anti-growth functions of interferon α. Virology 2000, 277:411-419.
109. Lee SJ, Cho YS, Cho MC, Shim JH, Lee KA, Ko KK, Choe YK, Park SN, Hoshino T, Kim S, Dinarello CA, Yoon DY. Both E6 and E7 oncoproteins of human papillomavirus 16 inhibit IL-18-induced IFN-gamma production in human peripheral blood mononuclear and NK cells. J Immunol 2001, 167:497-504.
110. Ronco LV, Karpova AY, Vidal M, Howley PM. Human papillomavirus 16 E6 oncoprotein binds to interferon regulatory factor-3 and inhibits its transcriptional activity. Genes Dev 1998, 12:2061-2072.
111. Miura S, Kawana K, Schust DJ, Fujii T, Yokoyama T, Iwasawa Y, Nagamatsu T, Adachi K, Tomio A, Tomio K, Kojima S, Yasugi T, Kozuma S, Taketani Y. CD1d, a sentinel molecule bridging innate and adaptive immunity, is downregulated by the human papillomavirus (HPV) E5 protein: a possible mechanism for immune evasion by HPV. J Virol 2010, 84:11614-11623.
112. Obalek S, Favre M, Szymanczyk J, Misiewicz J, Jablonska S, Orth G. Human papillomavirus (HPV) types specific of epidermodysplasia verruciformis detected in warts induced by HPV3 or HPV3-related types in immunosuppressed patients. J Investig Dermatol 1992, 98:936-941.
113. Orth G. Genetics of epidermodysplasia verruciformis: insights into host defense against papillomaviruses. Semin Immunol 2006, 18:362-374.
114. Ramoz N, Rueda LA, Bouadjar B, Montoya LS, Orth G, Favre M. Mutations in two adjacent novel genes are associated with epidermodysplasia verruciformis. Nat Genet 2002, 32:579-581.
115. Lazarczyk M, Pons C, Mendoza JA, Cassonnet P, Jacob Y, Favre M. Regulation of cellular zinc balance as a potential mechanism of EVER-mediated protection against pathogenesis by cutaneous oncogenic human papillomaviruses. J Exp Med 2008, 205:35-42.
116. Palmiter RD, Findley SD. Cloning and functional characterization of a mammalian zinc transporter that confers resistance to zinc. EMBO J 1995, 14:639-649.
117. Orth G. Host defenses against human papillomaviruses: lessons from epidermodysplasia verruciformis. Curr Top Microbiol Immunol 2008, 321:59-83.
118. Cordano P, Gillan V, Bratlie S, Bouvard V, Banks L, Tommasino M, Campo MS. The E6 E7 oncoproteins of cutaneous human papillomavirus type 38 interfere with the interferon pathway. Virology 2008, 377:408-418.
119. Bible JM, Mant C, Best JM, Kell B, Starkey WG, Shanti Raju K, Seed P, Biswas C, Muir P, Banatvala JE, Cason J. Cervical lesions are associated with human papillomavirus type 16 intratypic variants that have high transcriptional activity and increased usage of common mammalian codons. J Gen Virol 2000, 81:1517-1527.
120. Riley RR, Duensing S, Brake T, Münger K, Lambert PF, Arbeit JM. Dissection of human papillomavirus E6 and E7 function in transgenic mouse models of cervical carcinogenesis. Cancer Res 2003, 63:4862-4871.
121. Genther SM, Sterling S, Duensing S, Münger K, Sattler C, Lambert PF. Quantitative role of the human papillomavirus type 16 E5 gene during the productive stage of the viral life cycle. J Virol 2003, 77:2832-2842.
122. Pett MR, Herdman MT, Palmer RD, Yeo GS, Shivji MK, Stanley MA, Coleman N. Selection of cervical keratinocytes containing integrated HPV16 associates with episome loss and an endogenous antiviral response. Proc Natl Acad Sci USA 2006, 103:3822-3827.
123. Muto V, Stellacci E, Lamberti AG, Perrotti E, Carrabba A, Matera G, Sgarbanti M, Battistini A, Liberto MC, Focà A. Human papillomavirus type 16 E5 protein induces expression of beta interferon through interferon regulatory factor 1 in human keratinocytes. J Virol 2011, 85:5070-5080.
124. Schiller JT, Vass WC, Vousdan KH, Lowy DR. The E5 open reading frame of bovine papillomavirus type 1 encodes a transforming gene. J Virol 1986, 57:1-6.
125. Schlegel R, Wade-Glass M, Rabson MS, Yang YC. The E5 transforming gene of bovine papillomavirus encodes a small hydrophobic polypeptide. Science 1986, 233:464-467.
126. Burkhardt A, DiMaio D, Schlegel R. Genetic and biochemical definition of the bovine papillomavirus E5 transforming protein. EMBO J 1987, 8:2381-2385.
127. Pennie WD, Grindlay GJ, Cairney M, Campo MS. Analysis of the transforming functions of bovine papillomavirus type 4. Virology 1993, 19:614-620.
128. Marchetti B, Ashrafi GH, Tsirimonaki E, O'Brien PM, Campo MS. The bovine papillomavirus oncoprotein E5 retains MHC class I molecole in the Golgi apparatus and prevents their transport to the cell surface. Oncogene 2002, 21:7808-7816.
129. King G, Oates J, Patel D, van den Berg HA, Dixon AM. Towards a structural understanding of the smallest known oncoprotein: Investigation of the bovine papillomavirus E5 protein using solution-state NMR. Biochim Biophys Acta 2011, 1808:1943-1501.
130. Windisch D, Hoffmann S, Afonin S, Vollmer S, Benamira S, Langer B, Bürck J, Muhle-Goll C, Ulrich AS. Structural role of the conserved cysteines in the dimerization of the viral transmembrane oncoprotein E5. Biophys J 2010, 99:1764-1772.
131. Oates J, Hicks M, Dafforn TR, DiMaio D, Dixon AM. In vitro dimerization of the bovine papillomavirus E5 protein transmembrane domain. Biochemistry 2008, 47:8985-8992.
132. Campo MS, Moar MH, Jarret WFH, Laird HM. A new papillomavirus associated with alimentary cancer in cattle. Nature 1980, 286:180-182.
133. Bergman P, Ustav M, Sedman J, Moreno-Lopéz J, Vennström B, Pettersson U. The E5 gene of bovine papillomavirus type 1 is sufficient for complete oncogenic transformation of mouse fibroblasts. Oncogene 1988, 2:453-459.
134. Petti LM, Ray FA. Transformation of mortal human fibroblasts and activation of a growth inhibitory pathway by the bovine papillomavirus E5 oncoprotein. Cell growth differ 2000, 11:395-408.
135. O'Brien V, Ashrafi GH, Grindlay GJ, Anderson R, Campo MS. A Mutational Analysis of the Transforming Functions of the E8 Protein of Bovine Papillomavirus Type 4. Virology 1999, 255:385-394.
136. Tsirimonaki E, Ullah R, Marchetti B, Ashrafi GH, McGarry L, Ozanne B, Campo MS. Similarities and differences between the E5 oncoproteins of bovine papillomaviruses type 1 and type 4: cytoskeleton, motility and invasiveness in E5-transformed bovine and mouse cells. Virus Res 2006, 115:158-168.
137. Horwitz BH, Settleman J, Prakash SS, DiMaio D. Structure, activity, and regulation of the bovine papillomavirus E5 gene and its transforming protein product. Curr Top Microbiol Immunol 1989, 144:143-151.
138. Petti L, Nilson LA, DiMaio D. Activation of the platelet-derived growth factor receptor by the bovine papillomavirus E5 transforming protein. EMBO J 1991, 10:845-855.
139. Nilson LA, DiMaio D. Platelet-derived growth factor receptor can mediate tumorigenic transformation by the bovine papillomavirus E5 protein. Mol Cell Biol 1993, 13:4137-4145.
140. Goldstein DJ, Li W, Wang LM. The bovine papillomavirus type 1 E5 transforming protein specifically binds and activates the beta-type receptor for the platelet-derived growth factor but not other related tyrosine kinase-containing receptors to induce cellular transformation. J Virol 1994, 68:4432-4441.
141. Drummond-Barbosa DA, Vaillancourt RR, Kazlauskas A, DiMaio D. Ligand-independent activation of the platelet-derived growth factor beta receptor: requirements for bovine papillomavirus E5-induced mitogenic signalling. Mol Cell Biol 1995, 15:2570-2581.
142. Cohen BD, Goldstein DJ, Rutledge L, Vass WC, Lowy DR, Schlegel R, Schiller JT. Transformation-specific interaction of the bovine papillomavirus E5 oncoprotein with the platelet-derived growth factor receptor transmembrane domain and the epidermal growth factor receptor cytoplasmic domain. J Virol 1993, 67:5303-5311.
143. Petti L, DiMaio D. Stable association between the bovine papillomavirus E5 transforming protein and activated platelet-derived growth factor receptor in transformed mouse cells. Proc Natl Acad Sci USA 1992, 89:6736-6740.
144. Petti L, DiMaio D. Specific interaction between the bovine papillomavirus E5 transforming protein and the beta receptor for platelet-derived growth factor in stably transformed and acutely transfected cells. J Virol 1994, 68:3582-3592.
145. Klein O, Kegler-Ebo D, Su J, Smith S, DiMaio D. The bovine papillomavirus E5 protein requires a juxtamembrane negative charge for activation of the platelet-derived growth factor beta receptor and transformation of C127 cells. J Virol 1999, 73:3264-3272.
146. Lai CC, Edwards AP, DiMaio D. Productive interaction between transmembrane mutants of the bovine papillomavirus E5 protein and the platelet-derived growth factor beta receptor. J Virol 2005, 79:1924-1929.
147. Goldstein DJ, Andresson T, Sparkowski JJ, Schlegel R. The BPV-1 E5 protein, the 16 kDa membrane pore-forming protein and the PDGF receptor exist in a complex that is dependent on hydrophobic transmembrane interactions. EMBO J 1992, 11:4851-4859.
148. Klein O, Polack GW, Surti T, Kegler-Ebo D, Smith SO, DiMaio D. Role of glutamine 17 of the bovine papillomavirus E5 protein in platelet-derived growth factor beta receptor activation and cell transformation. J Virol 1998, 72:8921-8932.
149. Surti T, Klein O, Aschheim K, DiMaio D, Smith SO. Structural models of the bovine papillomavirus E5 protein. Proteins 1998, 33:601-612.
150. Kulke R, DiMaio D. Biological properties of the deer papillomavirus E5 gene in mouse C127 cells: growth transformation, induction of DNA synthesis, and activation of the platelet-derived growth factor receptor. J Virol 1991, 65:4943-4949.
151. Horwitz BH, Burkhardt AL, Schlegel R, DiMaio D. 44-amino-acid E5 transforming protein of bovine papillomavirus requires a hydrophobic core and specific carboxyl-terminal amino acids. Mol Cell Biol 1988, 8:4071-4078.
152. Horwitz BH, Weinstat DL, DiMaio D. Transforming activity of a 16-amino-acid segment of the bovine papillomavirus E5 protein linked to random sequences of hydrophobic amino acids. J Virol 1989, 63:4515-4519.
153. Meyer AN, Xu Y-F, Webster MK, Smith AE, Donoghue DJ. Cellular transformation by a transmembrane peptide: structural requirements for the bovine papillomavirus E5 oncoprotein. Proc Natl Acad Sci USA 1994, 91:4634-4638.
154. Kulke R, Horwitz BH, Zibello T, DiMaio D. The central hydrophobic domain of the bovine papillomavirus E5 transforming protein can be functionally replaced by many hydrophobic amino acid sequences containing a glutamine. J Virol 1992, 66:505-511.
155. Mattoon D, Gupta K, Doyon J, Loll PJ, DiMaio D. Identification of the transmembrane dimer interface of the bovine papillomavirus E5 protein. Oncogene 2001, 20:3824-3834.
156. Nappi VM, Petti LM. Multiple transmembrane amino acid requirements suggest a highly specific interaction between the bovine papillomavirus E5 oncoprotein and the platelet-derived growth factor beta receptor. J Virol 2002, 76:7976-7986.
157. Nappi VM, Schaefer JA, Petti LM. Molecular examination of the transmembrane requirements of the platelet-derived growth factor beta receptor for a productive interaction with the bovine papillomavirus E5 oncoprotein. J Biol Chem 2002, 277:47149-47159.
158. Petti LM, Reddy V, Smith SO, DiMaio D. Identification of amino acids in the transmembrane and juxtamembrane domains of the platelet-derived growth factor receptor required for productive interaction with the bovine papillomavirus E5 protein. J Virol 1997, 71:7318-7327.
159. Staebler A, Pierce JH, Brazinski S Heidaran MA, Li W, Schlegel R, Goldstein DJ. Mutational analysis of the beta-type platelet-derived growth factor receptor defines the site of interaction with the bovine papillomavirus type 1 E5 transforming protein. J Virol 1995, 69:6507-6517.
160. Corteggio A, Urraro C, Roperto S, Roperto F, Borzacchiello G. Phosphatidylinositol-3-kinase-AKT pathway, phospho-JUN and phospho-JNK expression in spontaneously arising bovine urinary bladder tumours. J Comp Pathol 2010, 143:173-178.
161. Corteggio A, Di Geronimo O, Roperto S, Roperto F, Borzacchiello G. Activated platelet-derived growth factor β receptor and Ras-mitogen-activated protein kinase pathway in natural bovine urinary bladder carcinomas. Vet J 2011,
162. Petti LM, Ricciardi EC, Page HJ, Porter KA. Transforming signals resulting from sustained activation of the PDGFbeta receptor in mortal human fibroblasts. J Cell Sci 2008, 121:1172-1182.
163. Suprynowicz FA, Baege A, Sunitha I, Schlegel R. c-Src activation by the E5 oncoprotein enables transformation independently of PDGF receptor activation. Oncogene 2002, 21:1695-1706.
164. Suprynowicz FA, Sparkowski J, Baege A, Schlegel R. E5 oncoprotein mutants activate phosphoinositide 3-kinase independently of platelet-derived growth factor receptor activation. J Biol Chem 2000, 275:5111-5119.
165. Grindlay GJ, Campo MS, O'Brien V. Transactivation of the cyclin A promoter by bovine papillomavirus type 4 E5 protein. Virus Res 2005, 108:29-38.
166. O'Brien V, Campo MS. BPV-4 E8 transforms NIH3T3 cells, up-regulates cyclin A and cyclin A-associated kinase activity and de-regulates expression of the cdk inhibitor p27Kip1. Oncogene 1998, 17:293-301.
167. O'Brien V, Grindlay GJ, Campo MS. Cell transformation by the E5/E8 protein of bovine papillomavirus type 4. p27(Kip1), Elevated through increased protein synthesis is sequestered by cyclin D1-CDK4 complexes. J Biol Chem 2001, 276:33861-33868.
168. Zago M, Campo MS, O'Brien V. Cyclin A expression and growth in suspension can be uncoupled from p27 deregulation and extracellular signal-regulated kinase activity in cells transformed by bovine papillomavirus type 4 E5. J Gen Virol 2004, 85:3585-3595.
169. Ashrafi GH, Tsirimonaki E, Marchetti B, O'Brien PM, Sibbet GJ, Andrew L, Campo MS. Down-regulation of MHC class I by bovine papillomavirus E5 oncoproteins. Oncogene 2002, 2:248-259.
170. Ashrafi GH, Brown DR, Fife KH, Campo MS. Down-regulation of MHC class I is a property common to papillomavirus E5 proteins. Virus Res 2006, 120:208-211.
171. Faccini AM, Cairney M, Ashrafi GH, Finbow ME, Campo MS, Pitts JD. The bovine papillomavirus type 4 E8 protein binds to ductin and causes loss of gap junctional intercellular communication in primary fibroblasts. J Virol 1996, 70:9041-9045.
172. Andresson T, Sparkowski J, Goldstein DJ, Schlegel R. Vacuolar H(+)-ATPase mutants transform cells and define a binding site for the papillomavirus E5 oncoprotein. J Biol Chem 1995, 270:6830-6837.
173. Ashrafi GH, Pitts JD, Faccini AM, McLean P, O'Brien V, Finbow ME, Campo S. Binding of bovine papillomavirus type 4 E8 to ductin (16K proteolipid), down-regulation of gap junction intercellular communication and full cell transformation are independent events. J Gen Virol 2000, 81:689-694.
174. Roperto S, De Tullio R, Raso C, Stifanese R, Russo V, Gaspari M, Borzacchiello G, Averna M, Paciello O, Cuda G, Roperto F. Calpain3 is espresse in a proteolitically active form in papillomavirus-associated urothelial tumours of the urinary bladder in cattle. PLos One 2010, 5:e10299.
175. Kim MK, Kim HS, Kim SH, Oh JM, Han JY, Lim JM, Juhnn YS, Song YS. Human papillomavirus type 16 E5 oncoprotein as a new target for cervical cancer treatment. Biochem Pharmacol 2010, 80:1930-1935.
176. Liu DW, Tsao YP, Hsieh CH, Hsieh JT, Kung JT, Chiang CL, Huang SJ, Chen SL. Induction of CD8 T Cells by Vaccination with Recombinant Adenovirus Expressing Human Papillomavirus Type 16 E5 Gene Reduces Tumor Growth. J Virol 2000, 74:9083-9089.
177. Chen YF, Lin CW, Tsao YP, Chen SL. Cytotoxic-T-lymphocyte human papillomavirus type 16 E5 peptide with CpG-oligodeoxynucleotide can eliminate tumor growth in C57BL/6 mice. J Virol 2004, 78:1333-1343.
178. Lorenzon L, Mazzetta F, Venuti A, Frega A, Torrisi MR, French D. In vivo HPV 16 E5 mRNA: Expression pattern in patients with squamous intra-epithelial lesions of the cervix. J Clin Virol 2011, 52:79-83.
179. Wang W, Sima N, Kong D, Luo A, Gao Q, Liao S, Liao S, Li W, Han L, Wang J, Wang S, Lu Y, Wang D, Xu G, Zhou J, Meng L, Ma D. Selective targeting ofHPV-16 E6/E7 in cervical cancer cells with a potent oncolytic adenovirus and its enhanced effect with radiotherapy in vitro and vivo. Cancer Lett 2010, 291:67-75.
180. Jonson AL, Rogers LM, Ramakrishnan S, Downs LS. Gene silencing with siRNA targeting E6/E7 as a therapeutic intervention in a mouse model of cervical cancer. Gynecol Oncol 2008, 111:356-364.
181. Raghava S, Giorda KM, Romano FB, Heuck AP, Hebert DN. The SV40 late protein VP4 is a viroporin that forms pores to disrupt membranes for viral release. PLoS Pathog 2011, 7:e1002116.
182. Maufort JP, Shai A, Pitot HC, Lambert PF. A role for HPV16 E5 in cervical carcinogenesis. Cancer Res 2010, 70:2924-2931.
183. Schwarz E, Freese UK, Gissmann L, Mayer W, Roggenbuck B, Stremlau A, zur Hausen H. Structure and transcription of human papillomavirus sequences in cervical carcinoma cells. Nature 1985, 314:111-114.
184. Borzacchiello G, Roperto F, Campo MS, Venuti A. 1st International Workshop on Papillomavirus E5 Oncogene-A report. Virology 2010, 408:135-137.