Thermodynamics of cooperative DNA recognition at a replication origin and transcription regulatory site

Biochemistry

Volumn 49, Issue 48, 2010, Pages 10277-10286

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

^a FUNDACIÓN INSTITUTO LELOIR   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

[No Author keywords available]

Indexed keywords

COOPERATIVITY; DNA BINDING; DNA RECOGNITION; DNA STRUCTURE; GLOBAL DYNAMICS; HUMAN PAPILLOMAVIRUS; ISOTHERMAL TITRATION CALORIMETRY; PROTEIN-NUCLEIC ACIDS; REPLICATION ORIGIN; STRONG COUPLING; TRANSCRIPTIONAL REGULATOR;

BINDING SITES; NUCLEIC ACIDS; PROTEINS; THERMODYNAMICS; TRANSCRIPTION;

DNA;

DNA; GLYCOPROTEIN E2;

ARTICLE; BETA SHEET; BINDING SITE; DNA REPLICATION ORIGIN; DNA STRUCTURE; DNA TRANSCRIPTION; ENTHALPY; ENTROPY; HUMAN PAPILLOMAVIRUS TYPE 11; HUMAN PAPILLOMAVIRUS TYPE 18; MOLECULAR RECOGNITION; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN FOLDING; THERMODYNAMICS;

BASE SEQUENCE; BINDING SITES; DNA; DNA-BINDING PROTEINS; HUMAN PAPILLOMAVIRUS 16; KINETICS; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; ONCOGENE PROTEINS, VIRAL; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; REGULATORY ELEMENTS, TRANSCRIPTIONAL; REPLICATION ORIGIN; THERMODYNAMICS; TRANSCRIPTION, GENETIC;

HUMAN PAPILLOMAVIRUS TYPE 16;

EID: 78650902377     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi1014908     Document Type: Article

References (75)

1. Prado, F., and Aguilera, A. (2005) Impairment of replication forkprogression mediatesRNApol II transcription-associated recombination.EMBO J. 24, 1267-1276.
2. Liu, B., and Alberts, B. M. (1995) Head-on collision between a DNAreplication apparatus and RNA polymerase transcription complex, Science 267, 1131-1137.
3. Flint, S. J., Enquist, L. W., Racaniello, V. R., and Skalka, A. M.(2008) Transcription strategies: DNA templates. In Principles of Virology, 3rd ed., pp 240-287, ASM Press, Washington, DC.
4. Flint, S. J., Enquist, L. W., Racaniello, V. R., and Skalka, A. M.(2008) Genome replication strategies: DNA viruses. In Principles of Virology, 3rd ed., pp 288-333, ASM Press, Washington, DC.
5. Kelly, T. J. (1988) SV40 DNA replication. J. Biol. Chem. 263, 17889-17892.
6. Komatsu, T., Ballestas, M. E., Barbera, A. J., Kelley-Clarke, B., and Kaye, K. M. (2004) KSHV LANA1 binds DNA as an oligomer and residuesN-terminal to the oligomerization domain are essential for DNAbinding, replication, and episome persistence. Virology 319, 225-236.
7. Polvino-Bodnar, M., and Schaffer, P. A. (1992) DNAbinding activityis required for EBNA 1-dependent transcriptional activation and DNA replication. Virology 187, 591-603.
8. Chiang, C. M., Ustav, M., Stenlund, A., Ho, T. F., Broker, T. R., and Chow, L. T. (1992) Viral E1 and E2 proteins support replication ofhomologous and heterologous papillomaviral origins. Proc. Natl.Acad. Sci. U.S.A. 89, 5799-5803.
9. Cox, M., Ryder, K., Silver, S., and Tegtmeyer, P. (1988) The role ofoperator position in SV40 T-antigen-mediated repression. Virology167, 293-295.
10. Lim, C., Sohn, H., Gwack, Y., and Choe, J. (2000) Latency- associatednuclear antigen of Kaposi's sarcoma-associated herpesvirus (humanherpesvirus-8) binds ATF4/CREB2 and inhibits its transcriptionalactivation activity. J. Gen. Virol. 81, 2645-2652.
11. Thierry, F. (2009) Transcriptional regulation of the papillomavirusoncogenes by cellular and viral transcription factors in cervicalcarcinoma. Virology 384, 375-379.
12. Rawlins, D. R., Milman, G., Hayward, S. D., and Hayward, G. S.(1985) Sequence-specific DNA binding of the Epstein-Barr virusnuclear antigen (EBNA-1) to clustered sites in the plasmid maintenanceregion. Cell 42, 859-868.
13. Abbate, E. A., Voitenleitner, C., and Botchan, M. R. (2006) Structureof the papillomavirus DNA-tethering complex E2 :Brd4 and a peptidethat ablates HPV chromosomal association. Mol. Cell 24, 877-889.
14. Feeney, K. M., and Parish, J. L. (2009) Targeting mitotic chromosomes:A conserved mechanism to ensure viral genome persistence.Proc. Biol. Sci. 276, 1535-1544.
15. Titolo, S., Brault, K., Majewski, J., White, P. W., and Archambault, J.(2003) Characterization of the minimal DNA binding domain of thehuman papillomavirus e1 helicase: Fluorescence anisotropy studiesand characterization of a dimerization-defective mutant protein. J. Virol. 77, 5178-5191.
16. Titolo, S., Welchner, E., White, P. W., and Archambault, J. (2003) Characterization of the DNA-binding properties of the origin-bindingdomain of simian virus 40 large T antigen by fluorescenceanisotropy. J. Virol. 77, 5512-5518.
17. Wong, L. Y., and Wilson, A. C. (2005) Kaposi's sarcoma- associatedherpesvirus latency-associated nuclear antigen induces a strong bendon binding to terminal repeat DNA. J. Virol. 79, 13829-13836.
18. Sanchez, I. E., Dellarole, M., Gaston, K., and de Prat Gay, G. (2008) Comprehensive comparison of the interaction of the E2 masterregulator with its cognate target DNA sites in 73 human papillomavirustypes by sequence statistics. Nucleic Acids Res. 36, 756-769.
19. Wyman, J., and Gill, S. J. (1990) Binding and linkage: Functionalchemistry of biological macromolecules, UNSB, Mill Valley, CA.
20. Ptashne, M. (2004) A Genetic Switch-Phage Lambda Revisited, 3rded., Cold Spring Harbor Laboratory Press, Plainview, NY.
21. Tan, S., Leong, L. E., Walker, P. A., and Bernard, H. (1994) Thehuman papillomavirus type 16 E2 transacription factor binds with lowcooperativity to two flanking sites and represses the E6 promoterthrough displacement of Sp1 and TF IID. J. Virol. 68, 6411-6420.
22. Garber, A. C., Hu, J., and Renne, R. (2002) Latency-associatednuclear antigen (LANA) cooperatively binds to two sites within theterminal repeat, and both sites contribute to the ability of LANA tosuppress transcription and to facilitate DNA replication. J. Biol. Chem. 277, 27401-27411.
23. Weisshart, K., Taneja, P., Jenne, A., Herbig, U., Simmons, D. T., and Fanning, E. (1999) Two regions of simian virus 40 Tantigen determinecooperativity of double-hexamer assembly on the viral origin ofDNAreplication and promote hexamer interactions during bidirectionalorigin DNA unwinding. J. Virol. 73, 2201-2211.
24. Spalholz, B. A., Byrne, J. C., and Howley, P. M. (1988) Evidence forcooperativity between E2 binding sites in E2 trans-regulation ofbovine papillomavirus type. J. Virol. 62, 3143-3150.
25. Summers, H., Barwell, J. A., Pfuetzner, R. A., Edwards, A. M., and Frappier, L. (1996) Cooperative assembly of EBNA1 on the Epstein-Barr virus latent origin of replication. J. Virol. 70, 1228-1231.
26. 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 Vaccinesand Beyond (Saveria Campo, M., Ed.) pp 19-40, Caisreir AcademicPress, Wymondham, U.K.
27. Bernard, H. U., Burk, R. D., Chen, Z., van Doorslaer, K., Hausen, H. Z., and de Villiers, E. M. (2010) Classification of papillomaviruses(PVs) based on 189 PV types and proposal of taxonomic amendments.Virology 401, 70-79.
28. Lu, J. Z., Sun, Y. N., Rose, R. C., Bonnez, W., and McCance, D. J.(1993) Two E2 binding sites ( E2 BS) alone or one E2 BS plus an A/Trichregion are minimal requirements for the replication of the humanpapillomavirus type 11 origin. J. Virol. 67, 7131-7139.
29. Sverdrup, F., and Khan, S. A. (1995) Two E2 binding sites alone aresufficient to function as the minimal origin of replication of humanpapillomavirus type 18 DNA. J. Virol. 69, 1319-1323.
30. Thierry, F., and Howley, P. M. (1991) Functional analysis of E2 -mediated repression of the HPV18 P105 promoter. New Biol. 3, 90-100.
31. Tan, S. H., Gloss, B., and Bernard, H. U. (1992) During negativeregulation of the human papillomavirus-16 E6 promoter, the viral E2 protein can displace Sp1 from a proximal promoter element. Nucleic Acids Res. 20, 251-256.
32. Dong, G., Broker, T. R., and Chow, L. T. (1994) Human papillomavirustype 11 E2 proteins repress the homologous E6 promoter byinterfering with the binding of host transcription factors to adjacentelements. J. Virol. 68, 1115-1127.
33. Steger, G., and Corbach, S. (1997) Dose-dependent regulation of theearly promoter of human papillomavirus type 18 by the viral E2 protein. J. Virol. 71, 50-58.
34. Hernandez-Ramon, E. E., Burns, J. E., Zhang, W., Walker, H. F., Allen, S., Antson, A. A., and Maitland, N. J. (2008) Dimerization ofthe human papillomavirus type 16 E2 N terminus results in DNAlooping within the upstream regulatory region. J. Virol. 82, 4853-4861.
35. Sim, J., Ozgur, S., Lin, B. Y., Yu, J. H., Broker, T. R., Chow, L. T., and Griffith, J. (2008) Remodeling of the human papillomavirus type11 replication origin into discrete nucleoprotein particles and loopedstructures by the E2 protein. J. Mol. Biol. 375, 1165-1177.
36. de Prat Gay, G., Gaston, K., and Cicero, D. O. (2008) The papillomavirus E2 DNA binding domain. Front. Biosci. 13, 6006-6021.
37. 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 DNAbindingdomain bound to its DNA target. Nature 359, 505-512.
38. Lima, L. M., and de Prat Gay, G. (1997) Conformational changes and stabilization induced by ligand binding in the DNA-binding domainof the E2 protein from human papillomavirus. J. Biol. Chem. 272, 19295-19303.
39. Mok, Y. K., Alonso, L. G., Lima, L. M., Bycroft, M., and de PratGay, G. (2000) Folding of a dimeric β-barrel: Residual structure in theurea denatured state of the human papillomavirus E2 DNA bindingdomain. Protein Sci. 9, 799-811.
40. Hegde, R. S. (2002) The papillomavirus E2 proteins: Structure, function, and biology. Annu. Rev. Biophys. Biomol. Struct. 31, 343-360.
41. de Prat Gay, G., Nadra, A. D., Corrales-Izquierdo, F. J., Alonso, L. G., Ferreiro, D. U., and Mok, Y.K. (2005) The folding mechanismof a dimeric β-barrel domain. J. Mol. Biol. 351, 672-682.
42. Bochkarev, A., Barwell, J. A., Pfuetzner, R. A., Bochkareva, E., Frappier, L., and Edwards, A. M. (1996) Crystal structure of theDNA-binding domain of the Epstein-Barr virus origin-binding protein, EBNA1, bound to DNA. Cell 84, 791-800.
43. Oddo, C., Freire, E., Frappier, L., and de Prat Gay, G. (2006) Mechanism of DNA recognition at a viral replication origin. J. Biol. Chem. 281, 26893-26903.
44. Kim, S. S., Tam, J. K., Wang, A. F., and Hegde, R. S. (2000) Thestructural basis of DNA target discrimination by papillomavirus E2 proteins. J. Biol. Chem. 275, 31245-31254.
45. Hooley, E., Fairweather, V., Clarke, A. R., Gaston, K., and Brady, R. L. (2006) The recognition of local DNA conformation by thehuman papillomavirus type 6 E2 protein. Nucleic Acids Res. 34, 3897-3908.
46. Ferreiro, D. U., Dellarole, M., Nadra, A. D., and de Prat Gay, G.(2005) Free energy contributions to direct readout of a DNAsequence. J. Biol. Chem. 280, 32480-32484.
47. Ferreiro, D. U., and de Prat Gay, G. (2003) A protein-DNA bindingmechanism proceeds through multi-state or two-state parallel pathways. J. Mol. Biol. 331, 89-99.
48. Ferreiro, D. U., Sanchez, I. E., and de Prat Gay, G. (2008) Transitionstate for protein-DNA recognition. Proc. Natl. Acad. Sci. U.S.A. 105, 10797-10802.
49. Sanchez, I. E., Ferreiro, D. U., Dellarole, M., and de Prat Gay, G.(2010) Experimental snapshots of a protein-DNA binding landscape.Proc. Natl. Acad. Sci. U.S.A. 107, 7751-7756.
50. 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 structureof the HPV-16 E2 DNA binding domain, a transcriptional regulatorwith a dimeric β-barrel fold. J. Biomol. NMR 30, 211-214.
51. Dellarole, M., Sanchez, I. E., Freire, E., and de Prat Gay, G. (2007) Increased Stability and DNA Site Discrimination of "Single Chain"Variants of the Dimeric β-Barrel DNA Binding Domain of theHuman Papillomavirus E2 Transcriptional Regulator. Biochemistry 46, 12441-12450.
52. Eliseo, T., Sanchez, I. E., Nadra, A. D., Dellarole, M., Paci, M., de Prat Gay, G., and Cicero, D. O. (2009) Indirect DNA readout onthe protein side: Coupling between histidine protonation, globalstructural cooperativity, dynamics, and DNA binding of the humanpapillomavirus type 16 E2 C domain. J. Mol. Biol. 388, 327-344.
53. Gray, D. M., Hung, S. H., and Johnson, K. H. (1995) Absorption and circular dichroism spectroscopy of nucleic acid duplexes and triplexes.Methods Enzymol. 246, 19-34.
54. Ferreiro, D. U., Lima, L. M., Nadra, A. D., Alonso, L. G., Goldbaum, F. A., and de Prat Gay, G. (2000) Distinctive cognatesequence discrimination, bound DNA conformation, and bindingmodes in the E2 C-terminal domains from prototype human and bovine papillomaviruses. Biochemistry 39, 14692-14701.
55. Mok, Y. K., de Prat Gay, G., Butler, P. J., and Bycroft, M. (1996) Equilibrium dissociation and unfolding of the dimeric humanpapillomavirus strain-16 E2 DNA-binding domain. Protein Sci. 5, 310-319.
56. Alexander, K. A., and Phelps, W. C. (1996) A fluorescence anisotropystudy of DNA binding by HPV-11 E2 C protein: A hierarchy of E2 -binding sites. Biochemistry 35, 9864-9872.
57. Schneider, T. D., and Stephens, R. M. (1990) Sequence logos: A newway to display consensus sequences. Nucleic Acids Res. 18, 6097-6100.
58. Crooks, G. E., Hon, G., Chandonia, J. M., and Brenner, S. E. (2004) WebLogo: A sequence logo generator. Genome Res. 14, 1188-1190.
59. Büchen-Osmond, C. (2003) The Universal Virus Database ICTVdB.Comput. Sci. Eng. 5 (3) , 16-25.
60. Clamp, M., Cuff, J., Searle, S. M., and Barton, G. J. (2004) The Jalview Java alignment editor. Bioinformatics 20, 426-427.
61. Wiseman, T., Williston, S., Brandts, J. F., and Lin, L. N. (1989) Rapidmeasurement of binding constants and heats of binding using a newtitration calorimeter. Anal. BioChem. 179, 131-137.
62. Houtman, J. C., Brown, P. H., Bowden, B., Yamaguchi, H., Appella, E., Samelson, L. E., and Schuck, P. (2007) Studying multisite binaryand ternary protein interactions by global analysis of isothermaltitration calorimetry data in SEDPHAT: Application to adaptorprotein complexes in cell signaling. Protein Sci. 16, 30-42.
63. Gray, D. (1996) Circular Dichroism of Protein Nucleic Acid Interactions.In Circular Dichroism and the Conformational Analysis ofBiomolecules (Fasman, G., Ed.) Plenum Press, New York.
64. Baase, W. A., and Johnson, W. C., Jr. (1979) Circular dichroism and DNA secondary structure. Nucleic Acids Res. 6, 797-814.
65. Bains, G., and Freire, E. (1991) Calorimetric determination ofcooperative interactions in high affinity binding processes. Anal. BioChem. 192, 203-206.
66. Freire, E., Schon, A., and Velazquez-Campoy, A. (2009) Isothermaltitration calorimetry: General formalism using binding polynomials.Methods Enzymol. 455, 127-155.
67. Brown, A. (2009) Analysis of cooperativity by isothermal titrationcalorimetry. Int. J. Mol. Sci. 10, 3457-3477.
68. Schumacher, M. A., Miller, M. C., Grkovic, S., Brown, M. H., Skurray, R. A., and Brennan, R. G. (2002) Structural basis forcooperative DNA binding by two dimers of the multidrug-bindingprotein QacR. EMBO J. 21, 1210-1218.
69. Lacal, J., Guazzaroni, M. E., Gutierrez-del-Arroyo, P., Busch, A., Velez, M., Krell, T., and Ramos, J. L. (2008) Two levels of cooperativenessin the binding of TodT to the tod operon promoter. J. Mol.Biol. 384, 1037-1047.
70. Dragan, A. I., Carrillo, R., Gerasimova, T. I., and Privalov, P. L.(2008) Assembling the human IFN-β enhanceosome in solution. J. Mol. Biol. 384, 335-348.
71. Weinberg, R. L., Veprintsev, D. B., and Fersht, A. R. (2004) Cooperative binding of tetrameric p53 to DNA. J. Mol. Biol. 341, 1145-1159.
72. Thain, A., Webster, K., Emery, D., Clarke, A. R., and Gaston, K.(1997) DNA binding and bending by the human papillomavirus type16 E2 protein. Recognition of an extended binding site. J. Biol. Chem. 272, 8236-8242.
73. Johnson, B. B., Dahl, K. S., Tinoco, I., Jr., Ivanov, V. I., and Zhurkin, V. B. (1981) Correlations between deoxyribonucleic acid structuralparameters and calculated circular dichroism spectra. Biochemistry 20, 73-78.
74. Di Pietro, S. M., Centeno, J. M., Cerutti, M. L., Lodeiro, M. F., Ferreiro, D. U., Alonso, L. G., Schwarz, F. P., Goldbaum, F. A., and de Prat Gay, G. (2003) Specific antibody-DNA interaction: A novelstrategy for tight DNA recognition. Biochemistry 42, 6218-6227.
75. Alexandrov, B. S., Gelev, V., Bishop, A. R., Usheva, A., and Rasmussen, K. O. (2010) DNA Breathing Dynamics in the Presenceof a Terahertz Field. Phys. Lett. A 374, 1214.