Structural and thermodynamic basis for the enhanced transcriptional control by the human papillomavirus strain-16 E2 protein

Biochemistry

Volumn 45, Issue 21, 2006, Pages 6551-6560

  Cicero, Daniel O ^a   Nadra, Alejandro D ^a   Eliseo, Tommaso ^a   Dellarole, Mariano ^a   Paci, Maurizio ^a   De Prat Gay, Gonzalo ^a  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; CALORIMETRY; CARCINOGENS; DNA; MUTAGENESIS; THERMODYNAMICS; TUMORS; VIRUSES;

BINDING AFFINITY; CARCINOGENESIS; DNA DUPLEX; TRANSCRIPTIONAL CONTROL;

PROTEINS;

CARBON 13; NITROGEN 15; VIRUS DNA; VIRUS PROTEIN;

ARTICLE; BINDING AFFINITY; BINDING SITE; CARBON NUCLEAR MAGNETIC RESONANCE; DNA BINDING; DNA PROTEIN COMPLEX; DNA VIRUS; ENTHALPY; GENETIC TRANSCRIPTION; HUMAN PAPILLOMAVIRUS TYPE 16; ISOTOPE LABELING; NITROGEN NUCLEAR MAGNETIC RESONANCE; NONHUMAN; PRIORITY JOURNAL; PROTON NUCLEAR MAGNETIC RESONANCE; THERMODYNAMICS; TRANSCRIPTION REGULATION; VIRUS TYPING; WART VIRUS;

AMINO ACID SEQUENCE; BASE SEQUENCE; DNA-BINDING PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; OLIGONUCLEOTIDES; ONCOGENE PROTEINS, VIRAL; PROTEIN CONFORMATION; SEQUENCE HOMOLOGY, AMINO ACID; THERMODYNAMICS; TRANSCRIPTION, GENETIC;

HUMAN PAPILLOMAVIRUS;

EID: 33744795425     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi060123h     Document Type: Article

References (42)

1. Howley, P. M. (1996) Papillomaviridae: The viruses and their replication, in Fields Virology (Fields, B. N., Knipe, D. M., and Howley, P. M., Eds.) 3rd ed., Vol. 65, pp 2045-2076, Lippincott-Raven Publishers, Philadelphia, PA.
2. Cohen, J. (2005) Public health. High hopes and dilemmas for a cervical cancer vaccine, Science 308, 618-621.
3. Munoz, N., Bosch, F. X., de Sanjose, S., Herrero, R., Castellsague, X., Shah, K. V., Snijders, P. J., and Meijer, C. J. (2003) Epidemiologic classification of human papillomavirus types associated with cervical cancer, N. Engl. J. Med. 348, 518-527.
4. zur Hausen, H. (2000) Papillomaviruses causing cancer: evasion from host-cell control in early events in carcinogenesis, J. Natl. Cancer Inst. 92, 690-698.
5. Dell, G., and Gaston, K. (2001) Human papillomaviruses and their role in cervical cancer, Cell Mol. Life Sci. 58, 1923-1942.
6. Munoz, N. (2000) Human papillomavirus and cancer: the epidemiological evidence, J. Clin. Virol. 19, 1-5.
7. Steger, G., and Corbach, S. (1997) Dose-dependent regulation of the early promoter of human papillomavirus type 18 by the viral E2 protein, J. Virol. 71, 50-58.
8. Piirsoo, M., Ustav, E., Mandel, T., A., S., and Ustav, M. (1996) Cis and trans requirements for stable episomal maintenance of the BPV-1 replicator, EMBO J. 15, 1-11.
9. Bastien, N., and McBride, A. A. (2000) Interaction of the papillomavirus E2 protein with mitotic chromosomes, Virology 270, 124-34.
10. Hegde, R. S. (2002) The papillomavirus E2 proteins: structure, function, and biology, Annu. Rev. Biophys. Biomol. Struct 31, 343-60.
11. Hines, C. S., Meghoo, C., Shetty, S., Biburger, M., Brenowitz, M., and Hegde, R. S. (1998) DNA structure and flexibility in the sequence-specific binding of papillomavirus E2 proteins, J. Mol. Biol. 276, 809-818.
12. Thain, A., Webster, K., Emery, D., Clarke, A. R., and Gaston, K. (1997) DNA binding and bending by the human papillomavirus type 16 E2 protein. Recognition of an extended binding site, J. Biol. Chem. 272, 8236-8242.
13. Hegde, R. S., Grossman, S. R., Laimins, L. A., and Sigler, P. B. (1992) Crystal structure at 1.7 A of the bovine papillomavirus-1 E2 DNA-binding domain bound to its DNA target, Nature 359, 505-12.
14. Dell, G., Wilkinson, K. W., Tranter, R., Parish, J., Leo Brady, R., and Gaston, K. (2003) Comparison of the structure and DNA-binding properties of the E2 proteins from an oncogenic and a non-oncogenic human papillomavirus, J. Mol. Biol. 334, 979-991.
15. Hegde, R. S., and Androphy, E. J. (1998) Crystal structure of the E2 DNA-binding domain from human papillomavirus type 16: implications for its DNA binding-site selection mechanism, J. Mol. Biol. 284, 1479-1489.
16. Liang, H., Petros, A. M., Meadows, R. P., Yoon, H. S., Egan, D. A., Walter, K., Holzman, T. F., Robins, T., and Fesik, S. W. (1996) Solution structure of the DNA-binding domain of a human papillomavirus E2 protein: evidence for flexible DNA-binding regions, Biochemistry 35, 2095-2103.
17. Kim, S., Tam, J., Wang, A., and Hegde, R. (2000) The structural basis of DNA target discrimination by papillomavirus E2 proteins, J. Biol. Chem. 275, 31245-31254.
18. de Prat-Gay, G., Nadra, A. D., Corrales-Izquierdo, F. J., Alonso, L. G., Ferreiro, D. U., and Mok, Y. K. (2005) The folding mechanism of a dimeric beta-barrel domain, J. Mol. Biol. 351, 672-682.
19. Mok, Y. K., Bycroft, M., and de Prat-Gay, G. (1996) The dimeric DNA binding domain of the human papillomavirus E2 protein folds through a monomeric intermediate which cannot be native-like, Nat. Struct. Biol. 3, 711-717.
20. Mok, Y. K., de Prat Gay, G., Butler, P. J., and Bycroft, M. (1996) Equilibrium dissociation and unfolding of the dimeric human papillomavirus strain-16 E2 DNA-binding domain, Protein Sci. 5, 310-319.
21. Mok, Y. K., Alonso, L. G., Lima, L. M., Bycroft, M., and de Prat-Gay, G. (2000) Folding of a dimeric beta-barrel: residual structure in the urea denatured state of the human papillomavirus E2 DNA binding domain, Protein Sci. 9, 799-811.
22. Ferreiro, D. U., Lima, L. M., Nadra, A. D., Alonso, L. G., Goldbaum, F. A., and de Prat-Gay, G. (2000) Distinctive cognate sequence discrimination, bound DNA conformation, and binding modes in the E2 C-terminal domains from prototype human and bovine papillomaviruses, Biochemistry 39, 14692-14701.
23. Ferreiro, D. U., and de Prat-Gay, G. (2003) A protein-DNA binding mechanism proceeds through multi-state or two-state parallel pathways, J. Mol. Biol. 331, 89-99.
24. Ferreiro, D. U., Dellarole, M., Nadra, A. D., and de Prat-Gay, G. (2005) Free energy contributions to direct readout of a DNA sequence, J. Biol. Chem. 280, 32480-32484.
25. Nadra, A. D., Eliseo, T., Mok, Y. K., Almeida, C. L., Bycroft, M., Paci, M., de Prat-Gay, G., and Cicero, D. O. (2004) Solution structure of the HPV-16 E2 DNA binding domain, a transcriptional regulator with a dimeric beta-barrel fold, J. Biomol. NMR 30, 211-214.
26. Hou, S. Y., Wu, S. Y., and Chiang, C. M. (2002) Transcriptional activity among high and low risk human papillomavirus E2 proteins correlates with E2 DNA binding, J. Biol. Chem. 277, 45619-45629.
27. Clackson, T., Detlef, G., and Jones, P. (1991) in PCR, a Practical Approach (McPherson, M., Quirke, P., and Taylor, G., Eds.) pp 202, IRL Press, Oxford, U.K.
28. Bax, A., Kontaxis, G., and Tjandra, N. (2001) Dipolar couplings in macromolecular structure determination, Methods Enzymol. 339, 127-174.
29. Chou, J. J., Li, S., and Bax, A. (2000) Study of conformational rearrangement and refinement of structural homology models by the use of heteronuclear dipolar couplings, J. Biomol. NMR 18, 211-221.
30. O'Donoghue, S. I., King, G. F., and Nilges, M. (1996) Calculation of symmetric multimer structures from NMR data using a priori knowledge of the monomer structure, co-monomer restraints, and interface mapping: The case of leucine zippers, J. Biomol. NMR 8, 193-206.
31. Wishart, D. S., and Sykes, B. D. (1994) Chemical shifts as a tool for structure determination, Methods Enzymol. 239, 363-392.
32. Cornilescu, G., Marquardt, J. L., Ottiger, M., and Bax, A. (1998) Validation of Protein Structure from Anisotropic Carbonyl Chemical Shifts in a Dilute Liquid Crystalline Phase, J. Am. Chem. Soc. 120, 6836-6837.
33. Bonvin, A. M., Boelens, R., and Kaptein, R. (2005) NMR analysis of protein interactions, Curr. Opin. Chem. Biol. 9, 501-508.
34. Williams, D. C., Jr., Cai, M., and Clore, G. M. (2004) Molecular basis for synergistic transcriptional activation by Oct1 and Sox2 revealed from the solution structure of the 42-kDa Oct1.Sox2.Hoxb1-DNA ternary transcription factor complex, J. Biol. Chem. 279, 1449-1457.
35. Kalodimos, C. G., Biris, N., Bonvin, A. M., Levandoski, M. M., Guennuegues, M., Boelens, R., and Kaptein, R. (2004) Structure and flexibility adaptation in nonspecific and specific protein-DNA complexes, Science 305, 386-389.
36. Hegde, R. S., Wang, A. F., Kim, S. S., and Schapira, M. (1998) Subunit rearrangement accompanies sequence-specific DNA binding by the bovine papillomavirus-1 E2 protein, J. Mol. Biol. 276, 797-808.
37. Zimmerman, J. M., and Maher, L. J., III. (2003) Solution measurement of DNA curvature in papillomavirus E2 binding sites, Nucleic Acids Res. 31, 5134-5139.
38. Zhang, Y., Xi, Z., Hegde, R. S., Shakked, Z., and Crothers, D. M. (2004) Predicting indirect readout effects in protein-DNA interactions, Proc. Natl. Acad. Sci. U.S.A. 101, 8337-8341.
39. Rohs, R., Sklenar, H., and Shakked, Z. (2005) Structural and energetic origins of sequence-specific DNA bending: Monte Carlo simulations of papillomavirus E2-DNA binding sites, Structure 13, 1499-1509.
40. Hawley-Nelson, P., Androphy, E. J., Lowy, D. R., and Schiller, J. T. (1988) The specific DNA recognition sequence of the bovine papillomavirus E2 protein is an E2-dependent enhancer, EMBO J. 7, 525-531.
41. Turnbull, W. B., and Daranas, A. H. (2003) On the value of c: can low affinity systems be studied by isothermal titration calorimetry? J. Am. Chem. Soc. 125, 14859-14866.
42. Poirot, O., Suhre, K., Abergel, C., O'Toole, E., and Notredame, C. (2004) 3DCoffee@igs: a web server for combining sequences and structures into a multiple sequence alignment, Nucleic Acids Res. 32, W37-40.