Inhibition of papillomavirus protein function in cervical cancer cells by intrabody targeting

Journal of Molecular Biology

Volumn 355, Issue 3, 2006, Pages 360-378

  Griffin, Heather ^a,b   Elston, Robert ^a   Jackson, Deborah ^a   Ansell, Keith ^b   Coleman, Michael ^a   Winter, Greg ^b   Doorbar, John ^a  

^a NATIONAL INSTITUTE FOR MEDICAL RESEARCH   (United Kingdom)

^b MEDICAL RESEARCH COUNCIL   (United Kingdom)

Author keywords

Apoptosis; Cervical cancer; E6; Intrabodies; Papillomavirus

Indexed keywords

PROTEIN P53;

APOPTOSIS; ARTICLE; BINDING AFFINITY; CANCER CELL; CANCER GROWTH; CELL LINE; CELL PROLIFERATION; CELL STRUCTURE; GENE EXPRESSION; GENE LIBRARY; MAMMAL CELL; NONHUMAN; ONCOGENE; PAPILLOMA VIRUS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; SIMIAN VIRUS; UTERINE CERVIX CANCER;

MAMMALIA; PAPILLOMAVIRIDAE; SIMIAN VIRUS; SIMIAN VIRUS 40;

EID: 28944438180     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.10.077     Document Type: Article

References (91)

1. M.N. Lobato, and T.H. Rabbitts Intracellular antibodies and challenges facing their use as therapeutic agents Trends Mol. Med. 9 2003 390 396
2. T. Tanaka, and T.H. Rabbitts Intrabodies based on intracellular capture frameworks that bind the RAS protein with high affinity and impair oncogenic transformation EMBO J. 22 2003 1025 1035
3. P.A. Cohen, J.C. Mani, and D.P. Lane Characterization of a new intrabody directed against the N-terminal region of human p53 Oncogene 17 1998 2445 2456
4. J.M. Lecerf, T.L. Shirley, Q. Zhu, A. Kazantsev, P. Amersdorfer, and D.E. Housman Human single-chain Fv intrabodies counteract in situ huntingtin aggregation in cellular models of Huntington's disease Proc. Natl Acad. Sci. USA 98 2001 4764 4769
5. W.A. Marasco, J. LaVecchio, and A. Winkler Human anti-HIV-1 tat sFv intrabodies for gene therapy of advanced HIV-1-infection and AIDS J. Immunol. Methods 231 1999 223 238
6. A.M. Mhashilkar, D.K. Biswas, J. LaVecchio, A.B. Pardee, and W.A. Marasco Inhibition of human immunodeficiency virus type 1 replication in vitro by a novel combination of anti-Tat single-chain intrabodies and NF-kappa B antagonists J. Virol. 71 1997 6486 6494
7. A.M. Mhashilkar, J. Bagley, S.Y. Chen, A.M. Szilvay, D.G. Helland, and W.A. Marasco Inhibition of HIV-1 Tat-mediated LTR transactivation and HIV-1 infection by anti-Tat single chain intrabodies EMBO J. 14 1995 1542 1551
8. J.P. Maciejewski, F.F. Weichold, N.S. Young, A. Cara, D. Zella, M.S. Reitz Jr, and R.C. Gallo Intracellular expression of antibody fragments directed against HIV reverse transcriptase prevents HIV infection in vitro Nature Med. 1 1995 667 673
9. P. Levy-Mintz, L. Duan, H. Zhang, B. Hu, G. Dornadula, and M. Zhu Intracellular expression of single-chain variable fragments to inhibit early stages of the viral life cycle by targeting human immunodeficiency virus type 1 integrase J. Virol. 70 1996 8821 8832
10. C.J. Lacey Therapy for genital human papillomavirus-related disease J. Clin. Virol. 32 2005 S82 S90
11. N. Munoz, F.X. Bosch, S. de Sanjose, R. Herrero, X. Castellsague, and K.V. Shah Epidemiologic classification of human papillomavirus types associated with cervical cancer New Engl. J. Med. 348 2003 518 527
12. J. Walboomers, M. Jacobs, M.M. Manos, F. Bosch, J. Kummer, and K. Shah Human papillomavirus is a necessary cause of invasive cervical cancer worldwide J. Pathol. 189 1999 12 19
13. M.S. Longworth, R. Wilson, and L.A. Laimins HPV31 E7 facilitates replication by activating E2F2 transcription through its interaction with HDACs EMBO J. 24 2005 1821 1830
14. D.L. Jones, D.A. Thompson, E. Suh-Burgmann, M. Grace, and K. Munger Expression of the HPV E7 oncoprotein mimics but does not evoke a p53-dependent cellular DNA damage response pathway Virology 258 1999 406 414
15. D.L. Jones, R.M. Alani, and K. Munger The human papillomavirus E7 oncoprotein can uncouple cellular differentiation and proliferation in human keratinocytes by abrogating p21CIP1 mediated inhibition of cdk2 Genes Dev. 11 1997 2101 2111
16. J.O. Funk, S. Waga, J.B. Harry, E. Espling, B. Stillman, and D.A. Galloway Inhibition of CDK activity and PCNA-dependent DNA replication by p21 is blocked by interaction with the HPV16 E7 oncoprotein Genes Dev. 11 1997 2090 2100
17. J.M. Huibregtse, M. Scheffner, and P.M. Howley A cellular protein mediates association of p53 with the E6 oncoprotein of human papillomavirus types 16 or 18 EMBO J. 10 1991 4129 4135
18. A.L. Talis, J.M. Huibregtse, and P.M. Howley The role of E6AP in the regulation of p53 protein levels in human papillomavirus (HPV)-positive and HPV-negative cells J. Biol. Chem. 273 1998 6439 6445
19. S. Li, S. Labrecque, M.C. Gauzzi, A.R. Cuddihy, A.H. Wong, and S. Pellegrini The human papilloma virus (HPV)-18 E6 oncoprotein physically associates with Tyk2 and impairs Jak-STAT activation by interferon-alpha Oncogene 18 1999 5727 5737
20. K. Matthews, C.M. Leong, L. Baxter, E. Inglis, K. Yun, and B.T. Backstrom 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
21. E.C. Goodwin, and D. DiMaio Induced senescence in HeLa cervical carcinoma cells containing elevated telomerase activity and extended telomeres Cell Growth Differ. 12 2001 525 534
22. E.C. Goodwin, and D. DiMaio Repression of human papillomavirus oncogenes in HeLa cervical carcinoma cells causes the orderly reactivation of dormant tumor suppressor pathways Proc. Natl Acad. Sci. USA 97 2000 12513 12518
23. S.I. Wells, D.A. Francis, A.Y. Karpova, J.J. Dowhanick, J.D. Benson, and P.M. Howley Papillomavirus E2 induces senescence in HPV-positive cells via pRB- and p21(CIP)-dependent pathways EMBO J. 19 2000 5762 5771
24. A. Nishimura, T. Ono, A. Ishimoto, J.J. Dowhanick, M.A. Frizzell, P.M. Howley, and H. Sakai Mechanisms of human papillomavirus E2-mediated repression of viral oncogene expression and cervical cancer cell growth inhibition J. Virol. 74 2000 3752 3760
25. D.A. Francis, S.I. Schmid, and P.M. Howley Repression of the integrated papillomavirus E6/E7 promoter is required for growth suppression of cervical cancer cells J. Virol. 74 2000 2679 2686
26. K. Butz, T. Ristriani, A. Hengstermann, C. Denk, M. Scheffner, and F. Hoppe-Seyler siRNA targeting of the viral E6 oncogene efficiently kills human papillomavirus-positive cancer cells Oncogene 22 2003 5938 5945
27. B. Abdulkarim, S. Sabri, E. Deutsch, H. Chagraoui, L. Maggiorella, and J. Thierry Antiviral agent Cidofovir restores p53 function and enhances the radiosensitivity in HPV-associated cancers Oncogene 21 2002 2334 2346
28. C.W. Cho, H. Poo, Y.S. Cho, M.C. Cho, K.A. Lee, and S.J. Lee HPV E6 antisense induces apoptosis in CaSki cells via suppression of E6 splicing Expt. Mol. Med. 34 2002 159 166
29. S. Hietanen, S. Lain, E. Krausz, C. Blattner, and D.P. Lane Activation of p53 in cervical carcinoma cells by small molecules Proc. Natl Acad. Sci. USA 97 2000 8501 8506
30. M.C. Kamradt, N. Mohideen, and A.T. Vaughan RU486 increases radiosensitivity and restores apoptosis through modulation of HPV E6/E7 in dexamethasone-treated cervical carcinoma cells Gynecol. Oncol. 77 2000 177 182
31. K. Butz, C. Denk, A. Ullmann, M. Scheffner, and F. Hoppe-Seyler Induction of apoptosis in human papillomavirus positive cancer cells by peptide aptamers targeting the viral E6 oncoprotein Proc. Natl Acad. Sci. USA 97 2000 6693 6697
32. W. Beerheide, M.M. Sim, Y.J. Tan, H.U. Bernard, and A.E. Ting Inactivation of the human papillomavirus-16 E6 oncoprotein by organic disulfides Bioorg. Med. Chem. 8 2000 2549 2560
33. Y. Liu, Z. Liu, E. Androphy, J. Chen, and J.D. Baleja Design and characterization of helical peptides that inhibit the E6 protein of papillomavirus Biochemistry 43 2004 7421 7731
34. S.E. Grossberg Perspectives on the neutralization of interferons by antibody Neurology 61 2003 S21 S23
35. J.R. Mascola Defining the protective antibody response for HIV-1 Curr. Mol. Med. 3 2003 209 216
36. W. Magliani, S. Conti, A. Salati, S. Arseni, L. Ravanetti, R. Frazzi, and L. Polonelli Biotechnological approaches to the production of idiotypic vaccines and antiidiotypic antibiotics Curr. Pharm. Biotechnol. 4 2003 91 97
37. R. Elston, S. Napthine, and J. Doorbar The identification of a conserved binding motif within human papillomavirus type 16 E6 binding peptides, E6AP and E6BP J. Gen.Virol. 79 1998 371 374
38. H. Sterlinko, M. Weber, R. Elston, P. McIntosh, H. Griffin, L. Banks, and J. Doorbar Inhibition of E6-induced degradation of its cellular substrates by novel blocking peptides J.Mol. Biol. 335 2004 971 985
39. A.D. Griffiths, S.C. Williams, O. Hartley, I. Tomlinson, P. Waterhouse, and W.L. Crosby Isolation of high affinity human antibodies directly from large synthetic repertoires EMBO J. 13 1994 3245 3260
40. J. Doorbar, C. Foo, N. Coleman, E. Medcalf, O. Hartley, and T. Prospero Characterisation of events during the late stages of HPV16 infection in vivo using high affinity synthetic Fabs to E4 Virology 238 1997 40 52
41. L. Banks, P. Spence, E. Androphy, N. Hubbert, G. Matlashewski, A. Murray, and L. Crawford Identification of human papillomavirus type 18 E6 polypeptide in cells derived from human cervical carcinomas J. Gen. Virol. 68 1987 1351 1359
42. J. Doorbar, R. Elston, S. Napthine, K. Raj, E. Medcalf, and D. Jackson The E1 E4 protein of human papillomavirus type 16 associates with a putative RNA helicase through sequences in its C terminus J. Virol. 74 2000 10081 10095
43. D. Pim, P. Massimi, and L. Banks Alternatively spliced HPV-18 E6* protein inhibits E6 mediated degradation of p53 and suppresses transformed cell growth Oncogene 15 1997 257 264
44. D. Pim, and L. Banks HPV-18 E6*I protein modulates the E6-directed degradation of p53 by binding to full-length HPV-18 E6 Oncogene 18 1999 7403 7408
45. S.A. Sedman, M.S. Barbosa, W.C. Vass, N.L. Hubbert, J.A. Haas, D.R. Lowy, and J.T. Schiller The full-length E6 protein of human papillomavirus type 16 has transforming and trans-activating activities and cooperates with E7 to immortalize keratinocytes in culture J. Virol. 65 1991 4860 4866
46. K. Munger, W.C. Phelps, V. Bubb, P.M. Howley, and R. Schlegel The E6 and E7 genes of the human papillomavirus type 16 together are necessary and sufficient for transformation of primary human keratinocytes J. Virol. 63 1989 4417 4421
47. H. Romanczuk, L.L. Villa, R. Schlegel, and P.M. Howley The viral transcriptional regulatory region upstream of the E6 and E7 genes is a major determinant of the differential immortalization activities of human papillomavirus types 16 and 18 J. Virol. 65 1991 2739 2744
48. M. Reinman, J. Jantti, K. Alfthan, S. Keranen, H. Soderlund, and K. Takkinen Functional inactivation of the conserved Sem1p in yeast by intrabodies Yeast 20 2003 1071 1084
49. E. Tse, and T.H. Rabbitts Intracellular antibody-caspase-mediated cell killing: an approach for application in cancer therapy Proc. Natl Acad. Sci. USA 97 2000 12266 12271
50. N. Jendreyko, M. Popkov, R.R. Beerli, J. Chung, D.B. McGavern, C. Rader, and C.F. Barbas 3rd Intradiabodies, bispecific, tetravalent antibodies for the simultaneous functional knockout of two cell surface receptors J. Biol. Chem. 278 2003 47812 47819
51. O. Perisic, P.A. Webb, P. Holliger, G. Winter, and R.L. Williams Crystal structure of a diabody, a bivalent antibody fragment Structure 2 1994 1217 1226
52. X.Y. Pei, P. Holliger, A.G. Murzin, and R.L. Williams The 2.0-Å resolution crystal structure of a trimeric antibody fragment with noncognate VH-VL domain pairs shows a rearrangement of VH CDR3 Proc. Natl Acad. Sci. USA 94 1997 9637 9642
53. M.K. El Awady, J.B. Kaplan, S.J. O'Brien, and R.D. Burk Molecular analysis of integrated human papillomavirus16 sequences in the cervical cancer cell line SiHa Virology 159 1987 389 398
54. F. Friedl, I. Kimura, T. Osato, and Y. Ito Studies on a new human cell line (SiHa) derived from carcinoma of the uterus Proc. Soc. Expt. Biol. Med. 135 1970 543 545
55. H. von Boehmer Unique features of the pre-T-cell receptor alpha-chain: not just a surrogate Nature Rev. Immunol. 5 2005 571 577
56. Z. Darzynkiewicz, E. Bedner, F. Traganos, and T. Murakami Critical aspects in the analysis of apoptosis and necrosis Hum. Cell 11 1998 3 12
57. R. Sgonc, and J. Gruber Apoptosis detection: an overview Expt. Gerontol. 33 1998 525 533
58. Y. Otsuki, Z. Li, and M.A. Shibata Apoptotic detection methods - from morphology to gene Prog. Histochem. Cytochem. 38 2003 275 339
59. V.M. Heatwole TUNEL assay for apoptotic cells Methods Mol. Biol. 115 1999 141 148
60. Z. Darzynkiewicz, E. Bedner, and F. Traganos Difficulties and pitfalls in analysis of apoptosis Methods Cell Biol. 63 2001 527 546
61. C. Caulin, G.S. Salvesen, and R.G. Oshima Caspase cleavage of keratin 18 and reorganization of intermediate filaments during epithelial cell apoptosis J. Cell Biol. 138 1997 1379 1394
62. M.P. Leers, W. Kolgen, V. Bjorklund, T. Bergman, G. Tribbick, and B. Persson Immunocytochemical detection and mapping of a cytokeratin 18 neo-epitope exposed during early apoptosis J. Pathol. 187 1999 567 572
63. M. Jiang, and J. Milner Selective silencing of viral gene expression in HPV-positive human cervical carcinoma cells treated with siRNA, a primer of RNA interference Oncogene 21 2002 6041 6048
64. T. Tan, and R.C.Y. Tring The in vitro and in vivo inhibition of human papillomavirus type 16 E6 and E7 genes Cancer Res. 55 1995 4599 4605
65. K. Munger, A. Baldwin, K.M. Edwards, H. Hayakawa, C.L. Nguyen, and M. Owens Mechanisms of human papillomavirus-induced oncogenesis J. Virol. 78 2004 11451 11460
66. F. Venturini, J. Braspenning, M. Homann, L. Gissmann, and G. Sczakiel Kinetic selection of HPV 16 E6/E7-directed antisense nucleic acids: anti-proliferative effects on HPV 16-transformed cells Nucl. Acids Res. 27 1999 1585 1592
67. C. Giovane, G. Trav, A. Briones, Y. Lutz, B. Wasylyk, and E. Weiss Targetting of the N-terminal domain of the human papillomavirus type 16 E6 oncoprotein with monomeric ScFvs blocks the E6-mediated degradation of cellular p53 J. Mol. Recognit. 12 1999 141 152
68. M. Lagrange, S. Charbonnier, G. Orfanoudakis, P. Robinson, K. Zanier, and M. Masson Binding of human papillomavirus 16 E6 to p53 and E6AP is impaired by monoclonal antibodies directed against the second zinc-binding domain of E6 J. Gen. Virol. 86 2005 1001 1007
69. Y. Wu, L. Duan, M. Zhu, B. Hu, S. Kubota, O. Bagasra, and R.J. Pomerantz Binding of intracellular anti-Rev single chain variable fragments to different epitopes of human immunodeficiency virus type 1 rev: variations in viral inhibition J. Virol. 70 1996 3290 3297
70. J. Deshane, G.P. Siegal, R.D. Alvarez, M.H. Wang, M. Feng, and G. Cabrera Targeted tumor killing via an intracellular antibody against erbB-2 J. Clin. Invest. 96 1995 2980 2989
71. C.B. Jannot, R.R. Beerli, S. Mason, W.J. Gullick, and N.E. Hynes Intracellular expression of a single-chain antibody directed to the EGFR leads to growth inhibition of tumor cells Oncogene 13 1996 275 282
72. O. Cochet, M. Kenigsberg, I. Delumeau, A. Virone-Oddos, M.C. Multon, and W.H. Fridman Intracellular expression of an antibody fragment-neutralizing p21 ras promotes tumor regression Cancer Res. 58 1998 1170 1176
73. F. Wang-Johanning, G.Y. Gillespie, J. Grim, C. Rancourt, R.D. Alvarez, G.P. Siegal, and D.T. Curiel Intracellular expression of a single-chain antibody directed against human papillomavirus type 16 E7 oncoprotein achieves targeted antineoplastic effects Cancer Res. 58 1998 1893 1900
74. S. Biocca, F. Ruberti, M. Tafani, P. Pierandrei-Amaldi, and A. Cattaneo Redox state of single chain Fv fragments targeted to the endoplasmic reticulum, cytosol and mitochondria Biotechnology (NY) 13 1995 1110 1115
75. A. Cattaneo, and S. Biocca The selection of intracellular antibodies Trends Biotechnol. 17 1999 115 121
76. K. Tsumoto, Y. Nishimiya, N. Kasai, H. Ueda, T. Nagamune, and K. Ogasahara Novel selection method for engineered antibodies using the mechanism of Fv fragment stabilization in the presence of antigen Protein Eng. 10 1997 1311 1318
77. R. Finnern, E. Pedrollo, I. Fisch, J. Wieslander, J.D. Marks, C.M. Lockwood, and W.H. Ouwehand Human autoimmune anti-proteinase 3 scFv from a phage display library Clin. Expt. Immunol. 107 1997 269 281
78. A. Nissim, H.R. Hoogenboom, I.M. Tomlinson, G. Flynn, C. Midgley, D. Lane, and G. Winter Antibody fragments from a "single pot" phage display library as immunochemical reagents EMBO J. 13 1994 692 698
79. W.J. Dower, J.F. Miller, and C.W. Ragsdale High efficiency transformation of E. coli by high voltage electroporation Nucl. Acids Res. 16 1988 6127 6145
80. J.F. Gibson, R.K. Poole, M.N. Hughes, and J.F. Rees Filamentous growth of Escherichia coli K12 elicited by dimeric, mixed-valence complexes of ruthenium Arch. Microbiol. 139 1984 265 271
81. T. Clackson, H.R. Hoogenboom, A.D. Griffiths, and G. Winter Making antibody fragments using phage display libraries Nature 352 1991 624 628
82. P. Kristensen, and G. Winter Proteolytic selection for protein folding using filamentous bacteriophages Fold. Des. 3 1998 321 328
83. J.D. Marks, H.R. Hoogenboom, T.P. Bonnert, J. McCafferty, A.D. Griffiths, and G. Winter By-passing immunization. Human antibodies from V-gene libraries displayed on phage J. Mol. Biol. 222 1991 581 597
84. Elston, R. C. (1996). Identification of cellular proteins which interact with the human papillomavirus E6 proteins. PhD, University of Cambridge.
85. R.M. de Wildt, C.R. Mundy, B.D. Gorick, and I.M. Tomlinson Antibody arrays for high-throughput screening of antibody-antigen interactions Nature Biotechnol. 18 2000 989 994
86. Laemmli, (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
87. J. Sambrook, and D.W. Russell Molecular Cloning: A Laboratory Manual 2001 Cold Spring Harbor Laboratory Press Cold Spring Harbor, NY
88. N.L. Hubbert, S.A. Sedman, and J.T. Schiller Human papillomavirus type 16 E6 increases the degradation rate of p53 in human keratinocytes J. Virol. 66 1992 6237 6241
89. P. Holliger, O. Manzke, M. Span, R. Hawkins, B. Fleischmann, and L. Qinghua Carcinoembryonic antigen (CEA)-specific T-cell activation in colon carcinoma induced by anti-CD3 x anti-CEA bispecific diabodies and B7 x anti-CEA bispecific fusion proteins Cancer Res. 59 1999 2909 2916
90. P. Holliger, and G. Winter Diabodies: small bispecific antibody fragments Cancer Immunol. Immunother. 45 1997 128 130
91. I. Tomlinson, and P. Holliger Methods for generating multivalent and bispecific antibody fragments Methods Enzymol. 326 2000 461 479