Characterization of the minimal DNA binding domain of the human papillomavirus E1 helicase: Fluorescence anisotropy studies and characterization of a dimerization-defective mutant protein

Journal of Virology

Volumn 77, Issue 9, 2003, Pages 5178-5191

  Titolo, S ^a   Brault, K ^a   Majewski, J ^a   White, P W ^a   Archambault, J ^a  

^a BOEHRINGER INGELHEIM CANADA LTD   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; DNA; HELICASE; MUTANT PROTEIN; VIRUS ENZYME;

ANIMAL CELL; ANISOTROPY; ARTICLE; BINDING AFFINITY; BINDING SITE; DIMERIZATION; DNA BINDING; ENZYME ACTIVITY; FLUORESCENCE; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; QUANTITATIVE ANALYSIS; WART VIRUS; WILD TYPE;

BASE SEQUENCE; DIMERIZATION; DNA HELICASES; DNA, VIRAL; DNA-BINDING PROTEINS; FLUORESCENCE POLARIZATION; HUMANS; MOLECULAR SEQUENCE DATA; MUTATION; PAPILLOMAVIRIDAE; VIRAL PROTEINS;

EID: 0037405823     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.77.9.5178-5191.2003     Document Type: Article

References (68)

1. Alexander, K. A., and W. C. Phelps. 1996. A fluorescence anisotropy study of DNA binding by HPV-11 E2C: a hierarchy of E2-binding sites. Biochemistry 35:9864-9872.
2. Amin, A. A., S. Titolo, A. Pelletier, D. Fink, M. G. Cordingley, and J. Archambault. 2000. Identification of domains of the HPV11 E1 protein required for DNA replication in vitro. Virology 272:137-150.
3. Barbaro, B. A., K. R. Sreekumar, D. R. Winters, A. E. Prack, and P. A. Bullock. 2000. Phosphorylation of simian virus 40 T antigen on Thr 124 selectively promotes double-hexamer formation on subfragments of the viral core origin. J. Virol. 74:8601-8613.
4. Benson, J. D., and P. M. Howley. 1995. Amino-terminal domains of the bovine papillomavirus type 1 E1 and E2 proteins participate in complex formation. J. Virol. 69:4364-4372.
5. Berg, M., and A. Stenlund. 1997. Functional interactions between papillomavirus E1 and E2 proteins. J. Virol. 71:3853-3863.
6. Blitz, I. L., and L. A. Laimins. 1991. The 68-kilodalton E1 protein of bovine papillomavirus is a DNA binding phosphoprotein which associates with the E2 transcriptional activator in vitro. J. Virol. 65:649-656.
7. Bonne-Andrea, C., F. Tillier, G. D. McShan, V. G. Wilson, and P. Clertant. 1997. Bovine papillomavirus type 1 DNA replication: the transcriptional activator E2 acts in vitro as a specificity factor. J. Virol. 71:6805-6815.
8. Chao, S. F., W. J. Rocque, S. Daniel, L. E. Czyzyk, W. C. Phelps, and K. A. Alexander. 1999. Subunit affinities and stoichiometries of the human papillomavirus type 11 E1:E2:DNA complex. Biochemistry 38:4586-4594.
9. Chen, G., and A. Stenlund. 2001. The E1 initiator recognizes multiple overlapping sites in the papillomavirus origin of DNA replication. J. Virol. 75:292-302.
10. Chen, G., and A. Stenlund. 2000. Two patches of amino acids on the E2 DNA binding domain define the surface for interaction with E1. J. Virol. 74:1506-1512.
11. Chen, G., and A. Stenlund. 1998. Characterization of the DNA-binding domain of the bovine papillomavirus replication initiator E1. J. Virol. 72:2567-2576.
12. Chow, L. T., and T. R. Broker. 1994. Papillomavirus DNA replication. Intervirology 37:150-158.
13. Chow, L. T., and T. R. Broker. 1997. Small DNA tumor viruses, p. 267-301. In N. Nathanson (ed.), Viral pathogenesis. Lippincott-Raven, Philadelphia, Pa.
14. Clertant, P., and I. Seif. 1984. A common function for polyoma virus large-T and papillomavirus E1 proteins? Nature 311:276-279.
15. Conger, K. L., J.-S. Liu, S.-R. Kuo, L. T. Chow, and T. S.-F. Wang. 1999. Human Papillomavirus DNA Replication: Interactions between the viral E1 protein and two subunits of human polymerase α primase. J. Biol. Chem. 274:2696-2705.
16. Cueille, N., R. Nougarede, F. Mechali, M. Philippe, and C. Bonne-Andrea. 1998. Functional interaction between the bovine papillomavirus virus type 1 replicative helicase E1 and cyclin E-Cdk2. J. Virol. 72:7255-7262.
17. Dixon, E. P., G. L. Pahel, W. J. Rocque, J. A. Barnes, D. C. Lobe, M. H. Hanlon, K. A. Alexander, S. F. Chao, K. Lindley, and W. C. Phelps. 2000. The E1 helicase of human papillomavirus type 11 binds to the origin of replication with low sequence specificity. Virology 270:345-357.
18. Enemark, E. J., G. Chen, D. E. Vaughn, A. Stenlund, and L. Joshua-Tor. 2000. Crystal structure of the DNA binding domain of the replication initiation protein E1 from papillomavirus. Mol. Cell 6:149-158.
19. Enemark, E. J., A. Stenlund, and L. Joshua-Tor. 2002. Crystal structures of two intermediates in the assembly of the papillomavirus replication initiation complex. EMBO J. 21:1487-1496.
20. Fouts, E. T., E. H. Egelman, and M. R. Botchan. 1999. Biochemical and electron microscopic image analysis of the hexameric E1 helicase. J. Biol. Chem. 274:4447-4458.
21. Frattini, M. G., and L. A. Laimins. 1994. Binding of the human papillomavirus E1 origin-recognition protein is regulated through complex formation with the E2 enhancer-binding protein. Proc. Natl. Acad. Sci. USA 91:12398-12402.
22. Gillette, T. G., M. Lusky, and J. A. Borowiec. 1994. Induction of structural changes in the bovine papillomavirus type 1 origin of replication by the viral E1 and E2 proteins. Proc. Natl. Acad. Sci. USA 91:8846-8850.
23. Gillitzer, E., G. Chen, G., and A. Stenlund. 2000. Separate domains in E1 and E2 proteins serve architectural and productive roles for cooperative DNA binding. EMBO J. 19:3069-3079.
24. Gonzalez, A., C. Bazaldua-Hernandez, M. West, K. Woytek, and V. G. Wilson. 2000. Identification of a short, hydrophilic amino acid sequence critical for origin recognition by the bovine papillomavirus E1 protein. J. Virol. 74:245-253.
25. Gorbalenya, A. E., E. V. Koonin, and Y. I. Wolf. 1990. A new superfamily of putative NTP-binding domains encoded by genomes of small DNA and RNA viruses. FEBS Lett. 262:145-148.
26. Heyduk, T., Y. Ma, H. Tang, and R. H. Ebright. 1996. Fluorescence anisotropy: rapid, quantitative assay for protein-DNA and protein-protein interaction. Methods Enzymol. 274:492-503.
27. Holt, S. E., and V. G. Wilson. 1995. Mutational analysis of the 18-base-pair inverted repeat element at the bovine papillomavirus origin of replication: identification of critical sequences for E1 binding and in vivo replication. J. Virol. 69:6525-6532.
28. Howley, P. M. 1996. Papillomavirinae: the viruses and their replication, p. 2045-2076. In B. N. Fields and D. M. Knipe (ed.), Fields virology, 3rd ed. Raven Press, New York, N.Y.
29. Leng, X., J. H. Ludes-Meyer, and V. G. Wilson. 1997. Isolation of an aminoterminal region of bovine papillomavirus type 1 E1 protein that retains origin binding and E2 interaction capacity. J. Virol. 71:848-852.
30. Liu, J.-S, S.-R. Kuo, A. M. Makov, D. M. Cyr, J. D. Griffith, T. R. Broker, and L. T. Chow. 1998. Human Hsp70 and Hsp40 chaperone proteins facilitate human papillomavirus-11 E1 protein binding to the origin and stimulate cell-free DNA replication. J. Biol. Chem. 273:30704-30712.
31. Liu, J.-S., S.-R. Kuo, T. R. Broker, and L. T. Chow. 1995. The functions of human papillomavirus type 11 E1, E2, and E2C proteins in cell-free DNA replication. J. Biol. Chem. 270:27283-27291.
32. Lundbald, J. R., M. Laurence, and R. H. Goodman. 1996. Fluorescence polarization analysis of protein-DNA and protein-protein interactions. Mol. Endocrinol. 10:607-612.
33. Lusky, M., J. Hurwitz, and Y.-S. Seo. 1993. Cooperative assembly of the bovine papilloma virus E1 and E2 proteins on the replication origin requires an intact E2 binding site. J. Biol. Chem. 268:15795-15803.
34. Lusky, M., J. Hurwitz, and Y.-S. Seo. 1994. The bovine papillomavirus E2 protein modulates the assembly of but is not stably maintained in a replication-competent multimeric E1-replication origin complex. Proc. Natl. Acad. Sci. USA 91:8895-8899.
35. Ma, T., N. Zou, B. Y. Lin, L. T. Chow, and J. W. Harper. 1999. Interaction between cyclin-dependent kinases and human papillomavirus replicationinitiation protein E1 is required for efficient viral replication. Proc. Natl. Acad. Sci. USA 96:382-387.
36. Mansky, K. C., A. Batiza, and P. F. Lambert. 1997. Bovine papillomavirus type 1 E1 and simian virus 40 large T-antigen share regions of sequence similarity required for multiple functions. J. Virol. 71:7600-7608.
37. Masterson, P. J., M. A. Stanley, A. P. Lewis, and M. A. Romanos. 1998. A C-terminal helicase domain of the human papillomavirus E1 protein binds E2 and the DNA polymerase alpha-primase p68 subunit. J. Virol. 72:7407-7419.
38. McBride, A., and G. Myers. 1997. The E2 proteins, p. 54-73. In G. Myers, C. Baker, K. Münger, F. Sverdrup, A. McBride, and H.-U. Bernard (ed.), Human papillomaviruses 1997. Theoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, N.Mex.
39. Mendoza, R., L. Gandhi, and M. R. Botchan. 1995. E1 recognition sequences in the bovine papillomavirus type 1 origin of DNA replication: interaction between half sites of the inverted repeats. J. Virol. 69:3789-3798.
40. Mohr, I. J., R. Clark, S. Sun, E. J. Androphy, P. MacPherson, and M. R. Botchan. 1990. Targeting the E1 replication protein to the papillomavirus origin of replication by complex formation with the E2 transactivator. Science 250:1694-1699.
41. Moscufo., N., F. Sverdrup, D. E. Breiding, and E. J. Androphy. 1999. Two distincts regions of the BPV1 E1 replication protein interact with the activation domain of E2. Virus Res. 65:141-154.
42. Rocque, W. J., D. J. T. Porter, J. A. Barnes, E. P. Dixon, D. C. Lobe, J. L. Su, D. H. Willard, R. Gaillard, J. P. Condreay, W. C. Clay, C. R. Hoffman, L. K. Overton, G. Pahel, T. A. Kost, and W. C. Phelps. 2000. Replication-associated activities of purified human papillomavirus type 11 E1 helicase. Protein Express. Purif. 18:148-159.
43. Sanders, C. M., and A. Stenlund. 2001. Mechanism and requirements for bovine papillomavirus, type 1, E1 initiator complex assembly promoted by the E2 transcription factor bound to distal sites. J. Biol. Chem. 276:23689-23699.
44. Sanders, C. M., and A. Stenlund. 1998. Recruitment and loading of the E1 initiator protein: an ATP-dependent process catalysed by a transcription factor. EMBO J. 17:7044-7055.
45. Sarafi, T. R., and A. A. McBride. 1995. Domains of the BPV-1 E1 replication protein required for origin-specific DNA binding and interaction with the E2 transactivator. Virology 211:385-396.
46. Sedman, J., and A. Stenlund. 1995. Co-operative interaction between the initiator E1 and the transcriptional activator E2 is required for replicator specific DNA replication of bovine papillomavirus in vivo and in vitro. EMBO J. 14:6218-6228.
47. Sedman, J., and A. Stenlund. 1998. The papillomavirus E1 protein forms a DNA-dependent hexameric complex with ATPase and DNA helicase activities. J. Virol. 72:6893-6897.
48. Sedman, T., J. Sedman, and A. Stenlund. 1997. Binding of the E1 and E2 proteins to the origin of replication of bovine papillomavirus. J. Virol. 71:2887-2896.
49. Seo, Y.-S., F. Muller, M. Lusky, and J. Hurwitz. 1993. Bovine papillomavirus (BPV)-encoded E1 protein contains multiple activities required for BPV DNA replication. Proc. Natl. Acad. Sci. USA 90:702-706.
50. Seo, Y.-S., F. Müller, M. Lusky, E. Gibbs, H.-Y. Kim, B. Phillips, and J. Hurwitz. 1993. Bovine papilloma virus (BPV)-encoded E2 protein enhances binding of E1 to the BPV replication origin. Proc. Natl. Acad. Sci. USA 90:2865-2869.
51. Shah, K. V., and P. M. Howley. 1996. Papillomaviruses, p. 2077-2109. In B. N. Fields and D. M. Knipe (ed.), Fields Virology, 3rd ed. Raven Press, New York, N.Y.
52. Stubenrauch, F., and L. A. Laimins. 1999. Human papillomavirus life cycle: active and latent phases. Semin. Cancer Biol. 9:379-386.
53. Sun, Y.-N., J. Z.-J. Lu, and D. J. McCance. 1996. Mapping of HPV-11 E1 binding site and determination of other important cis elements for replication of the origin. Virology 216:219-222.
54. Sun, Y., H. Han, and D. J. McCance. 1998. Active domains of human papillomavirus type 11 E1 protein for origin replication. J. Gen. Virol. 79:1651-1658.
55. Sverdrup, F., and S. A. Khan. 1995. Two E2 binding sites alone are sufficient to function as the minimal origin of replication of human papillomavirus type 18 DNA. J. Virol. 69:1319-1323.
56. Sverdrup., F., and G. Myers. 1997. The E1 proteins, p. 37-53. In G. Myers, C. Baker, K. Münger, F. Sverdrup, A. McBride, and H.-U. Bernard (ed.), Human papillomaviruses 1997. Los Alamos National Laboratory, Los Alamos, N.Mex.
57. Thorner, L. K., D. A. Lim, and M. R. Botchan. 1993. DNA-binding domain of bovine papillomavirus type 1 E1 helicase: structural and functional aspects. J. Virol. 67:6000-6014.
58. Titolo, S., A. Pelletier, A. M. Pulichino, K. Brault, E. Wardrop, P. W. White, M. G. Cordingley, and J. Archambault. 2000. Identification of domains of the human papillomavirus type 11 E1 helicase involved in oligomerization and binding to the viral origin. J. Virol. 74:7349-73461.
59. Titolo, S., A. Pelletier, F. Sauve, K. Brault, E. Wardrop, P. W. White, A. Amin, M. G. Cordingley, and J. Archambault. 1999. Role of the ATPbinding domain of the human papilloma virus type 11 helicase in E2-dependent binding to the origin. J. Virol. 73:5282-5293.
60. Weber, K., and M. Osborn. 1969. The reliability of molecular weight determinations by dodecyl sulfate-polyacrylamide gel electrophoresis. J. Biol. Chem. 244:4406-4412.
61. Weisshart, K., P. Taneja, A. Jenne, U. Herbig, D. T. Simmons, and E. Fanning. 1999. Two regions of simian virus 40 T antigen determine cooperativity of double-hexamer assembly on the viral origin of DNA replication and promote hexamer interactions during bidirectional origin DNA unwinding. J. Virol. 73:2201-2211.
62. West, M., D. Flanery, K. Woytek, D. Rangasamy, and V. G. Wilson. 2001. Functional mapping of the DNA binding domain of bovine papillomavirus E1 protein. J. Virol. 75:11948-11960.
63. White, P. W., A. Pelletier, K. Brault, S. Titolo, E. Welchner, L. Thauvette, M. Fazekas, M. G. Cordingley, and J. Archambault. 2001. Characterization of recombinant HPV6 and 11 E1 helicases: effect of ATP on the interaction of E1 with E2 and mapping of a minimal helicase domain. J. Biol. Chem. 276:22426-22438.
64. Woytek, K. J., D. Rangasamy, C. Bazaldua-Hernandez, M. West, and V. G. Wilson. 2001. Effects of mutations within two hydrophilic regions of the bovine papillomavirus type 1 E1 DNA-binding domain on E1-E2 interaction. J. Gen. Virol. 82:2341-2351.
65. Yang, L., R. Li, I. Mohr, R. Clark, and M. R. Botchan. 1991. Activation of BPV-1 replication in vitro by the transcription factor E2. Nature 353:628-633.
66. Yasugi, T., J. D. Benson, H. Sakai, M. Vidal, and P. M. Howley. 1997. Mapping and characterization of the interaction domains of human papillomavirus type 16 E1 and E2 proteins. J. Virol. 71:891-899.
67. Zou, N., J.-S. Liu, S.-R. Kuo, T. R. Broker, and L. T. Chow. 1998. The carboxyl-terminal region of the human papillomavirus type 16 E1 protein determines E2 protein specificity during DNA replication. J. Virol. 72:3436-3441.
68. Zur Hausen, H., and E. M. de Villiers. 1994. Human papillomaviruses. Annu. Rev. Microbiol. 48:427-447.