Crystal structure of the E2 DNA-binding domain from human papillomavirus type 16: Implications for its DNA binding-site selection mechanism

Journal of Molecular Biology

Volumn 284, Issue 5, 1998, Pages 1479-1489

  Hegde, Rashmi S ^a   Androphy, Elliot J ^b  

^a NEW YORK UNIVERSITY MEDICAL CENTER   (United States)

^b TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

DNA binding; E2; Papillomavirus; X ray crystallography; barrel

Indexed keywords

CURVED DNA; PHOSPHATE; VIRUS DNA; VIRUS PROTEIN;

ARTICLE; BINDING SITE; CRYSTAL STRUCTURE; NONHUMAN; PAPILLOMA VIRUS; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN FOLDING; STEREOCHEMISTRY; WART VIRUS;

BOVINAE; BOVINE PAPILLOMAVIRUS; BOVINE PAPILLOMAVIRUS TYPE 1; DNA VIRUSES; HUMAN PAPILLOMAVIRUS; HUMAN PAPILLOMAVIRUS TYPE 16; HUMAN PAPILLOMAVIRUS TYPES; PAPILLOMAVIRUS;

EID: 0032545160     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1006/jmbi.1998.2260     Document Type: Article

References (59)

1. Abagyan, R. A., Totrov, M. M. & Kuznetsov, D. N. (1994). ICM-a new method for protein modelling and design. Applications to docking and structure prediction form the distorted native conformation. J. Comput. Chem. 15, 488-506.
2. Androphy, E. J., Lowy, D. R. & Schiller, J. T. (1987). Bovine papillomavirus E2 trans-acting gene product binds to specific sites in papillomavirus DNA. Nature, 325, 70-73.
3. Bedrosian, C. L. & Bastia, D. (1990). The DNA-binding domain of HPV-16 E2 protein interaction with the viral enhancer: protein-induced DNA bending and role of the nonconserved core sequence in binding site affinity. Virology, 174, 557-575.
4. Benson, J. D. & Howley, P. M. (1995). Amino-terminal domains of the bovine papillomavirus type I E1 and E2 proteins participate in complex formation. J. Virol. 69, 4364-4372.
5. Berg, M. & Stenlund, A. (1997). Functional interactions between papillomavirus E1 and E2 proteins. J. Virol. 71, 3853-3863.
6. Bochkarev, A., Barwell, J., Pfuetzner, R., Furey, W. J., Edwards, A. M. & Frappier, L. D. (1995). Crystal Structure of the, DNA-binding and Dimerization domain of the Epstein-Barr origin-binding protein EBNA1. Cell, 83, 39-46.
7. Bochkarev, A., Barwell, J. A., Pfuetzner, R. A., Bochkareva, E., Frappier, L. & Edwards, A. M. (1996). Crystal structure of the DNA-binding domain of the Epstein-Barr virus origin-binding protein, EBNA1, bound to DNA. Cell, 84, 791-800.
8. Bonne-Andrea, C., Tillier, F., McShan, G. D., Wilson, V. G. & Clertant, P. (1997). Bovine papillomavirus type 1 DNA replication: the transcriptional activator E2 acts in vitro as a specificity factor. J. Virol. 71, 6805-6815.
9. Breiding, D. E., Sverdup, F., Grossel, M. J., Moscufo, N., Boonchai, W. & Androphy, E. J. (1997). Functional interaction of a novel cellular protein with the papillomavirus E2 transactivation domain. Mol. Cell. Biol. 17, 7208-7219.
10. Brunger, A. (1992). X-PLOR, 3.1 edit., Yale University Press, New Haven, CT..
11. Brunger, A. T. (1997). X-ray crystallography and NMR reveal complementary views of structure and dynamics. Nature Struct. Biol. 4, 862-865.
12. Chen, G. & Stenlund, A. (1998). Characterization of the DNA-binding domain of the bovine papillomavirus replication initiator E1. J. Virol. 72, 2567-2576.
13. Chiang, C.-M., Ustav, M., Stenlund, A., Ho, T. F., Broker, T. R. & Chow, L. T. (1992). Viral E1 and E2 proteins support replication of homologous and het-erologous papillomavirus origins. Proc. Natl Acad. Sci. USA, 89, 5799-5803.
14. Del, Vecchio A. M., Romaczuk, H., Howley, P. M. & Baker, C. C. (1992). Transient replication of human papillomavirus DNAs. J. Virol. 66, 5949-5958.
15. DePamphilis, M. L. (1993). How transcription factors regulate origins of DNA replication in eukaryotic cells. Trends Cell Biol. 3, 161-167.
16. Foguel, D., Silva, J. L. & de Prat-Gay, G. (1998). Characterization of a partially folded monomer of the DNA-binding domain of human papillomavirus E2 protein obtained at high pressure. J. Biol. Chem. 273, 9050-9057.
17. Giri, I. & Yaniv, M. (1988). Structural and mutational analysis of E2 trans-activating proteins of papillomaviruses reveals three distinct functional domains. EMBO J. 7, 2823-2829.
18. Hegde, R. S., Grossman, S. R., Laimins, L. A. & Sigler, P. B. (1992). Crystal structure at 1.7 Å of the bovine papillomavirus-1 E2 DNA-binding domain bound to its DNA target. Nature, 359, 505-512.
19. Hegde, R. S., Wang, A.-F., Kim, S.-S. & Schapira, M. (1998). Subunit Rearrangement accompanies sequence-specific DNA-binding by the bovine papillomavirus-1 E2 protein. J. Mol. Biol. 276, 797-808.
20. Hines, C. S., Meghoo, C., Shetty, S., Biburger, M., Brenowitz, M. & Hegde, R. S. (1998). DNA structure and flexibility in the sequence-specific binding of papillomavirus E2 proteins. J. Mol. Biol. 276, 809-818.
21. Howley, P. M. (1996). In Papillomaviridae: The Viruses and Their Replication (Fields, B. N., Knipe, D. M. & Howley, P. M., eds), 3rd edit., pp. 2045-2076, Lippincott-Raven Publishers, Philadelphia.
22. Hwang, E.-S., Riese, D. J., Settleman, J., Nilson, L. A., Honig, J., Flynn, S. & DiMaio, D. (1993). Inhibition of cervical carcinoma cell line proliferation by the introduction of a Bovine Papillomavirus regulatory gene. J. Virol. 67, 3720-3729.
23. Jones, T. A., Zou, J.-Y., Cowan, S. W. & Kjeldgaard, M. (1991). Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A, 47, 110-119.
24. Laskowski, R. A., MacArthur, M. W., Moss, D. S. & Thornton, J. M. (1993). PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Crystallog. 26, 283-291.
25. Leng, X., Ludes-Meyer, J. H. & Wilson, V. G. (1997). Isolation of an amino-terminal region of bovine papillomavirus type 1 E1 protein that retains origin binding and E2 interaction capacity. J. Virol. 71, 848-852.
26. Li, R. & Botchan, M. R. (1993). The acidic transcriptional activation domains of VP16 and p53 bind the cellular replication protein A and stimulate in vitro BPV-1 DNA replication. Cell, 73, 1207-1221.
27. Li, R. & Botchan, M. R. (1994). Acidic transcription factors alleviate nucleosome-mediated repression of DNA replication of bovine papillomavirus type 1. Proc. Natl. Acad. Sci. USA, 91, 7051-7055.
28. Li, R., Knight, J., Bream, G., Stenlund, A. & Botchan, M. (1989). Specific recognition nucleotides and their DNA context determine the affinity of E2 protein for 17 binding sites in the BPV-1 genome. Genes Dev. 3, 510-526.
29. Li, R., Knight, J. D., Jackson, S. P., Tjian, R. & Botchan, M. (1991). Direct interaction between Sp1 and the BPV enhancer E2 protein mediates synergisitic activation of transcription. Cell, 65, 493-505.
30. Liang, H., Petros, A. M., Meadows, R. P., Yoon, H. S., Egan, D. A., Walter, K., Holzman, T. E., Robins, T. & Fesk, S. W. (1996). Solution structure of the DNA-binding domain of a human papillomavirus E2 protein: evidence for flexible DNA-binding regions. Biochemistry, 35, 2095-103.
31. Lima, L. M. & de Prat-Gay, G. (1997). Conformational changes and stabilization induced by ligand binding in the DNA-binding domain of the E2 protein from Human papillomavirus. J. Biol. Chem. 272, 19295-19303.
32. Metallo, S. J., Paolella, D. N. & Schepartz, A. (1997). The role of a basic amino acid cluster in target site selection and non-specific binding of bZIP peptides to DNA. Nucl. Acids Res. 25, 2967-2972.
33. Mohr, I. J., Clark, R., Sun, S., Androphy, E. J., MacPherson, P. & Botchan, M. R. (1990). Targeting the E1 replication protein to the papillomavirus origin of replication by complex formation with the E2 transactivator. Science, 250, 1694-699.
34. Mok, Y.-K., Bycroft, M. & de Prat-Gay, G. (1996a). The dimeric DNA binding domain of the human papillomavirus E2 protein folds through a monomeric intermediate which cannot be native-like. Nature Struct. Biol. 3, 711-717.
35. Mok, Y.-K., de Prat-Gay, G., Jonathan, B. P. & Bycroft, M. (1996b). Equilibrium dissociation and unfolding of the dimeric human papillomavirus strain-16 E2 DNA-binding domain. Protein Sci. 5, 310-319.
36. Moskaluk, C. & Bastia, D. (1988). Interaction of the Bovine Papillomavirus type 1 E2 transcriptional control protein with the viral enhancer: purification of the DNA-binding domain and analysis of its contact points with DNA. J. Virol. 62, 1925-1931.
37. Nagai, K., Oubridge, C., Jessen, T. H., Li, J. & Evans, P. R. (1990). Crystal structure of the RNA-binding domain of the U1 small nuclear ribonucleoprotein A. Nature, 346, 515-520.
38. Navaza, J. (1994). AMORE: an automated package for molecular replacement. Acta Crystallog. sect. A, 50, 157-163.
39. Nicholls, A., Sharp, K. A. & Honig, B. (1991). Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins: Struct. Funct. Genet. 11, 281-296.
40. Otwinowski, Z. (1993). In Data Collection and Processing (Sawyer, L., Isaacs, N. & Bailey, S., eds), pp. 56-62, SERC Daresbury Laboratory, Warrington, UK.
41. Oubridge, C., Ito, N., Evans, P. R., Teo, C.-H. & Nagai, K. (1994). Crystal structure at 1.92 Å resolution of the RNA-binding domain of the U1A spliceosomal protein complexed with an RNA hairpin. Nature, 372, 432-438.
42. Paolella, D. N., Liu, Y., Fabian, M. A. & Schepartz, A. (1997). Electrostatic mechanism for DNA bending by bZIP proteins. Biochemistry, 36, 10033-10038.
43. Rank, N. M. & Lambert, P. F. (1995). Bovine papillomavirus type 1 E2 transcriptional regulators directly bind two cellular transcription factors, TFIID and TFIIB. J. Virol. 69, 6323-6334.
44. Romanczuk, H. & Howley, P. M. (1992). Disruption of either the E1 or E2 regulatory gene of human papillomavirus type 16 increases viral immortalization capacity. Proc. Natl Acad. Sci. 89, 3159-3163.
45. Romanczuk, H., Thierry, F. & Howley, P. M. (1990). Mutational analysis of cis-elements involved in E2 modulation of human papillomavirus type 16 P97 and type 18 P105 promoters. J. Virol. 64, 2849-2859.
46. Sedman, T., Sedman, J. & Stenlund, A. (1997). Binding of the E1 and E2 proteins to the origin of replication of bovine papillomavirus. J. Virol. 71, 2887-2896.
47. Spalholz, B. A., Vande, Pol S. B. & Howley, P. M. (1991). Characterization of the as elements involved in the basal and E2 transactivated expression of the bovine papillomavirus P2443 promoter. J. Virol. 65, 743-753.
48. Steger, G., Ham, J., Lefebvre, O. & Yaniv, M. (1995). The bovine papillomavirus-1 E2 protein contains two activation domains: one that interacts with TBP and another that functions after TBP binding. EMBO J. 14, 329-340.
49. Strauss, J. K. & Maher, L. J. (1994). DNA Bending by Asymmetric Phosphate Neutralization. Science, 266, 1829-1834.
50. Strauss-Soukup, J. K. & Maher, L. J., III (1997). Role of asymmetric phosphate neutralization in DNA bending by PU.1. J. Biol. Chem. 272, 31570-31575.
51. Strauss-Soukup, J. K. & Maher, L. J., III (1998). Electrostatic effects in DNA bending by GCN4 mutants. Biochemistry, 37, 1060-1066.
52. Strauss-Soukup, J. K., Vaghefi, M. M., Hogrefe, R. I. & Maher, L. J., III (1997). Effects of neutralization pattern and stereochemistry on DNA bending by methylphosphonate substitutions. Biochemistry, 36, 8692-8698.
53. Totrov, M. M. & Abagyan, R. A. (1995). The contour-buildup algorithm to calculate the analytical molecular surface. J. Struct. Biol. 115, 1-6.
54. Ustav, M. & Stenlund, A. (1991). Transient replication of BPV-1 requires two viral polypeptides encoded by the E1 and E2 open reading frames. EMBO J. 10, 449-457.
55. Villa, L. L. (1997). Human papillomaviruses and cervical cancer. Advan. Cancer Res. 71, 321-341.
56. Vousden, K. (1993). Interactions of human papillomavirus transforming proteins with the products of tumor suppressor genes. FASEB J. 7, 872-879.
57. Yang, L., Li, R., Mohr, I. J., Clark, R. & Botchan, M. R. (1991). Activation of BPV-1 replication in vitro by the transcription factor E2. Nature, 353, 628-632.
58. Yao, J.-M., Breiding, D. E. & Androphy, E. J. (1998). Functional interaction of the bovine papillomavirus E2 transactivation domain with TFIIB. J. Virol. 72, 1013-1019.
59. zur Hausen, H. (1996). Papillomavirus infections-a major cause of human cancers. Biochim. Biophys. Acta Rev. Cancer, 1288, F55-F78.