Increased stability and DNA site discrimination of "single chain" variants of the dimeric β-barrel DNA binding domain of the human papillomavirus e2 transcriptional regulator

Biochemistry

Volumn 46, Issue 43, 2007, Pages 12441-12450

  Dellarole, Mariano ^a   Sánchez, Ignacio E ^a   Freire, Eleonora ^a   De Prat Gay, Gonzalo ^a  

^a FUNDACIÓN INSTITUTO LELOIR   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

MONOMERIZATION; RESIDUE LINKERS; SITE DISCRIMINATION; TRANSCRIPTIONAL REGULATORS;

CRYSTALLOGRAPHY; PROTEINS; TRANSCRIPTION; TUMORS; VIRUSES;

DNA;

DIMER; MONOMER; PROTEIN E2; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CRYSTALLOGRAPHY; DIMERIZATION; GENE EXPRESSION REGULATION; ISOTHERMAL TITRATION CALORIMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PURIFICATION; PROTEIN QUATERNARY STRUCTURE; TIME; WART VIRUS;

BASE SEQUENCE; CRYSTALLOGRAPHY, X-RAY; DIMERIZATION; DNA PRIMERS; DNA, VIRAL; DNA-BINDING PROTEINS; PAPILLOMAVIRIDAE; TRANSCRIPTION FACTORS; VIRAL PROTEINS;

HUMAN PAPILLOMAVIRUS;

EID: 35648930349     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi701104q     Document Type: Article

References (58)

1. Bosch, F. X., Sanjosé, S., Castellsagué, X., Moreno, V., and Muñoz, N. (2006) Epimediology of Human Papillomavirus Infections and Associations with Cervical Cancer: New Opportunities for Prevention, in Papillomavirus Research: From Natural History to Vaccines and Beyond (Saveria Campo, M., Ed.) pp 19-40, Caisreir Academic Press, Wymondham.
2. Howley, P. M. (1996) Papillomaviridae: The viruses and their replication (Fields, B. N., Knipe, D. M., Howley, P. M., Eds.) pp 2045-2076, Lippincott-Raven Press, Philadelphia.
3. Kalantari, M., and Bernard, H.-U. (2006) Gene Expression of Papillomaviruses, in Papillomavirus Research: From Natural History to Vaccines and Beyond (Saveria Campo, M., Ed.) pp 41-52, Caisreir Academic Press, Wymondham.
4. Chow, L. T., and Broker, T. R. (2006) Mechanisms and Regulation of Papillomavirus DNA Replication, in Papillomavirus Research: From Natural History to Vaccines and Beyond (Saveria Campo, M., Ed.) pp 53-71, Caisreir Academic Press, Wymondham.
5. Hegde, R. S. (2002) The papillomavirus E2 proteins: structure, function, and biology, Annu. Rev. Biophys. Biomol. Struct. 31, 343-360.
6. Dell, G., and Gaston, K. (2001) Human papillomaviruses and their role in cervical cancer, Cell. Mol. Life Sci. 58, 1923-1942.
7. Giri, I., and Yaniv, M. (1988) Structural and mutational analysis of E2 trans-activating proteins of papillomaviruses reveals three distinct functional domains, EMBO J. 7, 2823-2829.
8. Cruickshank, J., Shire, K., Davidson, A. R., Edwards, A. M., and Frappier, L. (2000) Two domains of the Epstein-Barr virus origin DNA-binding protein, EBNA1, orchestrate sequence-specific DNA binding, J. Biol. Chem. 275, 22273-22277.
9. 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, 505-512.
10. Nadra, A. D., Eliseo, T., Mok, Y. K., Almeida, C. L., Bycroft, M., Paci, M., Prat-Gay, G. d., 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.
11. 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.
12. 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.
13. Mok, Y. K., Prat-Gay, G. d., 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.
14. 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.
15. Mok, Y. K., Bycroft, M., and Prat-Gay, G. d. (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.
16. 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.
17. Ferreiro, D. U., Lima, L. M., Nadra, A. D., Alonso, L. G., Goldbaum, F. A., and Prat-Gay, G. d. (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.
18. Ferreiro, D. U., and Prat-Gay, G. d. (2003) A protein-DNA binding mechanism proceeds through multi-state or two-state parallel pathways, J. Mol. Biol. 331, 89-99.
19. 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.
20. Cicero, D. O., Nadra, A. D., Eliseo, T., Dellarole, M., Paci, M., and Prat-Gay, G. d. (2006) Structural and thermodynamic basis for the enhanced transcriptional control by the human papillomavirus strain-16 E2 protein, Biochemistry 45, 6551-6560.
21. Beckett, D. (2001) Regulated assembly of transcription factors and control of transcription initiation, J. Mol. Biol. 314, 335-352.
22. Jana, R., Hazbun, T. R., Fields, J. D., and Mossing, M. C. (1998) Single-chain lambda Cro repressors confirm high intrinsic dimer-DNA affinity, Biochemistry 37, 6446-6455.
23. Moran, L. B., Schneider, J. P., Kentsis, A., Reddy, G. A., and Sosnick, T. R. (1999) Transition state heterogeneity in GCN4 coiled coil folding studied by using multisite mutations and crosslinking, Proc. Natl. Acad. Sci. U.S.A. 96, 10699-10704.
24. Liang, H., Sandberg, W. S., and Terwilliger, T. C. (1993) Genetic fusion of subunits of a dimeric protein substantially enhances its stability and rate of folding, Proc. Natl. Acad. Sci. U.S.A. 90, 7010-7014.
25. Robinson, C. R., and Sauer, R. T. (1996) Covalent attachment of Arc repressor subunits by a peptide linker enhances affinity for operator DNA, Biochemistry 35, 109-116.
26. Robinson, C. R., and Sauer, R. T. (1996) Equilibrium stability and sub-millisecond refolding of a designed single-chain Arc repressor, Biochemistry 35, 13878-13884.
27. Sieber, M., and Allemann, R. K. (1998) Single chain dimers of MASH-1 bind DNA with enhanced affinity, Nucleic Acids Res. 26, 1408-1413.
28. Walton, R. I., Millange, F., Loiseau, T., O'Hare, D., and Ferey, G. (2000) Crystallization of a Large-Pore Three-Dimensional Gallium Fluorophosphate under Mild Conditions, Angew. Chem., Int. Ed. 39, 4552-4555.
29. Navaza, J. (2001) Implementation of molecular replacement in AMoRe, Acta Crystallogr., Sect. D: Biol. Crystallogr. 57, 1367-1372.
30. Jones, T. A., Zou, J. Y., Cowan, S. W., and Kjeldgaard, M. (1991) Improved methods for building protein models in electron density maps and the location of errors in these models, Acta Crystallogr. A 47 (Part 2), 110-119.
31. Brunger, A. T., Adams, P. D., Core, G. M., DeLano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Kuszewski, J., Nilges, M., Pannu, N. S., Read, R. J., Rice, L. M., Simonson, T., and Warren, G. L. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination, Acta Crystallogr., Sect. D: Biol. Crystallogr. 54, 905-921.
32. Santoro, M. M., and Bolen, D. W. (1988) Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl alpha-chymotrypsin using different denaturants, Biochemistry 27, 8063-8068.
33. Sanchez, I. E., and Kiefhaber, T. (2003) Evidence for sequential barriers and obligatory intermediates in apparent two-state protein folding, J. Mol. Biol. 325, 367-376.
34. Falconi, M., Santolamazza, A., Eliseo, T., de Prat-Gay, G., Cicero, D. O., and Desideri, A. (2007) Molecular dynamics of the DNA-binding domain of the papillomavirus E2 transcriptional regulator uncover differential properties for DNA target accommodation, FEBS J. 274, 2385-2395.
35. Myers, J. K., Pace, C. N., and Scholtz, J. M. (1995) Denaturant m values and heat capacity changes: relation to changes in accessible surface areas of protein unfolding, Protein Sci. 4, 2138-2148.
36. Zhou, H. X. (2001) Single-chain versus dimeric protein folding: thermodynamic and kinetic consequences of covalent linkage, J. Am. Chem. Soc. 123, 6730-6731.
37. Zhou, H. X. (2004) Loops, linkages, rings, catenanes, cages, and crowders: entropy-based strategies for stabilizing proteins, Acc. Chem. Res. 37, 123-130.
38. Bachmann, A., Segel, D., and Kiefhaber, T. (2002) Test for cooperativity in the early kinetic intermediate in lysozyme folding, Biophys. Chem. 96, 141-151.
39. Record, M. T., Jr., Ha, J. H., and Fisher, M. A. (1991) Analysis of equilibrium and kinetic measurements to determine thermodynamic origins of stability and specificity and mechanism of formation of site-specific complexes between proteins and helical DNA, Methods Enzymol. 208, 291-343.
40. von Hippel, P., and Berg, O. (1986) On the specificity of DNA-protein interactions, Proc. Natl. Acad. Sci. U.S.A. 83, 1608-1612.
41. Ghaemmaghami, S., Huh, W. K., Bower, K., Howson, R. W., Belle, A., Dephoure, N., O'Shea, E. K., and Weissman, J. S. (2003) Global analysis of protein expression in yeast, Nature 425, 737-741.
42. Prat-Gay, G. d. (1996) Association of complementary fragments and the elucidation of protein folding pathways, Protein Eng. 9, 843-847.
43. Jonsson, T., Waldburger, C. D., and Sauer, R. T. (1996) Nonlinear free energy relationships in Arc repressor unfolding imply the existence of unstable, native-like folding intermediates, Biochemistry 35, 4795-4802.
44. Mohana-Borges, R., Silva, J. L., Ruiz-Sanz, J., and Prat-Gay, G. d. (1999) Folding of a pressure-denatured model protein. Proc. Natl. Acad. Sci. U.S.A. 96, 7888-7893.
45. Robinson, C. R., Rentzeperis, D., Silva, J. L., and Sauer, R. T. (1997) Formation of a denatured dimer limits the thermal stability of Arc repressor, J. Mol. Biol. 273, 692-700.
46. Freire, E., Oddo, C., Frappier, L., and de Prat-Gay, G. (2007) Kinetically driven refolding of the hyperstable EBNA1 origin DNA-binding dimeric beta-barrel domain into amyloid-like spherical oligomers, Proteins, submitted.
47. Ruiz-Sanz, J., Prat-Gay, G. d., Otzen, D. E., and Fersht, A. R. (1995) Protein fragments as models for events in protein folding pathways: protein engineering analysis of the association of two complementary fragments of the barley chymotrypsin inhibitor 2 (CI-2), Biochemistry 34, 1695-1701.
48. Topping, T. B., Hoch, D. A., and Gloss, L. M. (2004) Folding mechanism of FIS, the intertwined, dimeric factor for inversion stimulation, J. Mol. Biol. 335, 1065-1081.
49. Gloss, L. M., Simler, B. R., and Matthews, C. R. (2001) Rough energy landscapes in protein folding: dimeric E. coli Trp repressor folds through three parallel channels, J. Mol. Biol. 312, 1121-1134.
50. Lee, B. C., Pandit, A., Croonquist, P. A., and Hoff, W. D. (2001) Folding and signaling share the same pathway in a photoreceptor, Proc. Natl. Acad. Sci. U.S.A. 98, 9062-9067.
51. Wetzler, D. E., Castano, E. M., and de Prat-Gay, G. (2007) A quasi-spontaneous amyloid route in a DNA binding gene regulatory domain: The papillomavirus HPV16 E2 protein, Protein Sci. 16, 744-754.
52. Lima, L. M., and Prat-Gay, G. d. (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.
53. 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.
54. Ladbury, J. E., and Williams, M. A. (2004) The extended interface: measuring non-local effects in biomolecular interactions, Curr. Opin. Struct. Biol. 14, 562-569.
55. Kurg, R., Tekkel, H., Abroi, A., and Ustav, M. (2006) Characterization of the functional activities of the bovine papillomavirus type 1 E2 protein single-chain heterodimers, J. Virol. 80, 11218-11225.
56. Zhou, H. X. (2001) The affinity-enhancing roles of flexible linkers in two-domain DNA-binding proteins, Biochemistry 40, 15069-15073.
57. Fiser, A., Do, R. K., and Sali, A. (2000) Modeling of loops in protein structures. Protein Sci. 9, 1753-1773.
58. Koradi, R., Billeter, M., and Wuthrich, K. (1996) MOLMOL: a program for display and analysis of macromolecular structures, J. Mol. Graphics 14, 51-55, 29-32.