Characterization of the DNA- and dNTP-binding activities of the human cytomegalovirus DNA polymerase catalytic subunit UL54

Biochemical Journal

Volumn 407, Issue 3, 2007, Pages 331-341

  Picard Jean, Frédéric ^a   Bougie, Isabelle ^a   Bisaillon, Martin ^a  

^a UNIVERSITY OF SHERBROOKE   (Canada)

Author keywords

Binding kinetics; Cytomegalovirus; Deoxynucleotide; DNA binding activity; Fluorescence spectroscopy; Thermodynamics

Indexed keywords

CATALYST ACTIVITY; ENZYMES; FLUORESCENCE SPECTROSCOPY; LIGANDS; POLYMERS; VIRUSES;

BINDING KINETICS; CYTOMEGALOVIRUS; DEOXYNUCLEOTIDE; DNA-BINDING ACTIVITY; HUMAN CYTOMEGALOVIRUS;

DNA;

DNA POLYMERASE; DEOXYRIBONUCLEOTIDE; DNA BINDING PROTEIN; DNA DIRECTED DNA POLYMERASE; UL54 PROTEIN, HUMAN HERPESVIRUS 5; UNCLASSIFIED DRUG; VIRUS DNA; VIRUS PROTEIN;

ARTICLE; CATALYSIS; CYTOMEGALOVIRUS; DNA BINDING; ENTROPY; ENZYME KINETICS; FLUORESCENCE SPECTROSCOPY; LIGAND BINDING; NONHUMAN; POLYMERIZATION; PRIORITY JOURNAL; THERMODYNAMICS; CHEMISTRY; ENZYME ACTIVE SITE; ESCHERICHIA COLI; GENETICS; HUMAN; ISOLATION AND PURIFICATION; METABOLISM; PHYSIOLOGY; PROTEIN BINDING;

CYTOMEGALOVIRUS; HUMAN HERPESVIRUS 5;

CATALYTIC DOMAIN; CYTOMEGALOVIRUS; DEOXYRIBONUCLEOTIDES; DNA, VIRAL; DNA-BINDING PROTEINS; DNA-DIRECTED DNA POLYMERASE; ESCHERICHIA COLI; HUMANS; PROTEIN BINDING; VIRAL PROTEINS;

EID: 35748986175     PISSN: 02646021     EISSN: None     Source Type: Journal    
DOI: 10.1042/BJ20070853     Document Type: Article

References (43)

1. Britt, W. J. and Alford, C. A. (1996) Fields Virology, Lippincott-Raven Publishers, Philadelphia
2. Trincado, D. E., Scott, G. M., White, P. A., Hunt, C., Rasmussen, L. and Rawlinson, W. D. (2000) Human cytomegalovirus strains associated with congenital and perinatal infections. J. Med. Virol. 61, 481-487
3. Chou, S. W. (2001) Cytomegalovirus drug resistance and clinical implications. Transplant. Infect. Dis. 3, 20-24
4. Gilbert, C. and Boivin, G. (2005) Human cytomegalovirus resistance to antiviral drugs. Antimicrob. Agents Chemother. 49, 873-883
5. Springer, K. L. and Weinberg, A. (2004) Cytomegalovirus infection in the era of HAART: fewer reactivations and more immunity. J. Antimicrob. Chemother. 54, 582-586
6. Weinberg, A., Jabs, D. A., Chou, S., Martin, B. K., Lurain, N. S., Forman, M. S. and Crumpacker, C. (2003) Mutations conferring foscarnet resistance in a cohort of patients with acquired immunodeficiency syndrome and cytomegalovirus retinitis. J. Infect. Dis. 187, 777-784
7. Ertl, P. F. and Powell, K. L. (1992) Physical and functional interaction of human cytomegalovirus DNA polymerase and its accessory protein (ICP36) expressed in insect cells. J. Virol. 66, 4126-4133
8. Heilbronn, R., Jahn, G., Burkle, A., Freese, U. K., Fleckenstein, B. and zur Hausen, H. (1987) Genomic localization, sequence analysis, and transcription of the putative human cytomegalovirus DNA polymerase gene. J. Virol. 61, 119-124
9. Ye, L. B. and Huang, E. S. (1993) In vitro expression of the human cytomegalovirus DNA polymerase gene: effects of sequence alterations on enzyme activity. J. Virol. 67, 6339-6347
10. Mar, E. C., Patel, P. C. and Huang, E. S. (1981) Human cytomegalovirus-associated DNA polymerase and protein kinase activities. J. Gen. Virol. 57, 149-156
11. Weiland, K. L., Oien, N. L., Homa, F. and Wathen, M. W. (1994) Functional analysis of human cytomegalovirus polymerase accessory protein. Virus Res. 34, 191-206
12. Loregian, A., Rigatti, R., Murphy, M., Schievano, E., Palu, G. and Marsden, H. S. (2003) Inhibition of human cytomegalovirus DNA polymerase by C-terminal peptides from the UL54 subunit. J. Virol. 77, 8336-8344
13. Crumpacker, C. S. (1992) Mechanism of action of foscarnet against viral polymerases. Am. J. Med. 92, 3S-7S
14. Xiong, X., Smith, J. L., Kim, C., Huang, E. S. and Chen, M. S. (1996) Kinetic analysis of the interaction of cidofovir diphosphate with human cytomegalovirus DNA polymerase. Biochem. Pharmacol. 51, 1563-1567
15. Xiong, X., Smith, J. L. and Chen, M. S. (1997) Effect of incorporation of cidofovir into DNA by human cytomegalovirus DNA polymerase on DNA elongation. Antimicrob. Agents Chemother. 41, 594-599
16. Eriksson, B., Oberg, B. and Wahren, B. (1982) Pyrophosphate analogues as inhibitors of DNA polymerases of cytomegalovirus, herpes simplex virus and cellular origin. Biochim. Biophys. Acta 696, 115-123
17. Derse, D., Bastow, K. F. and Cheng, Y. (1982) Characterization of the DNA polymerases induced by a group of herpes simplex virus type I variants selected for growth in the presence of phosphonoformic acid. J. Biol. Chem. 257, 10251-10260
18. Griffiths, P. D. (2001) Cytomegalovirus therapy: current constraints and future opportunities. Curr. Opin. Infect. Dis. 14, 765-768
19. Chou, S., Lurain, N. S., Thompson, K. D., Miner, R. C. and Drew, W. L. (2003) Viral DNA polymerase mutations associated with drug resistance in human cytomegalovirus. J. Infect. Dis. 188, 32-39
20. Cihlar, T., Fuller, M. D. and Cherrington, J. M. (1998) Characterization of drug resistance-associated mutations in the human cytomegalovirus DNA polymerase gene by using recombinant mutant viruses generated from overlapping DNA fragments. J. Virol. 72, 5927-5936
21. Smith, I. L., Cherrington, J. M., Jiles, R. E., Fuller, M. D., Freeman, W. R. and Spector, S. A. (1997) High-level resistance of cytomegalovirus to ganciclovir is associated with alterations in both the UL97 and DNA polymerase genes. J. Infect. Dis. 176, 69-77
22. Tchesnokov, E. P., Gilbert, C., Boivin, G. and Gotte, M. (2006) Role of helix P of the human cytomegalovirus DNA polymerase in resistance and hypersusceptibility to the antiviral drug foscarnet. J. Virol. 80, 1440-1450
23. Cihlar, T., Fuller, M. D. and Cherrington, J. M. (1997) Expression of the catalytic subunit UL54 and the accessory protein UL44 of human cytomegalovirus DNA polymerase in a coupled in vitro transcription/translation system. Protein Expression Purif. 11, 209-218
24. Loregian, A., Appleton, B. A., Hogle, J. M. and Coen, D. M. (2004) Residues of human cytomegalovirus DNA polymerase catalytic subunit UL54 that are necessary and sufficient for interaction with the accessory protein UL44. J. Virol. 78, 158-167
25. Ito, J. and Brathwaite, D. K. (1991) Compilation and alignment of DNA polymerase sequences. Nucleic Acids Res. 19, 4045-4057
26. Bougie, I. and Bisaillon, M. (2003) Initial binding of the broad spectrum antiviral nucleoside ribavirin to the hepatitis C virus RNA polymerase. J. Biol. Chem. 278, 52471-52478
27. Bougie, I., Charpentier, S. and Bisaillon, M. (2003) Characterization of the metal ion binding properties of the hepatitis C virus RNA polymerase. J. Biol. Chem. 278, 3868-3875
28. Bougie, I., Parent, A. and Bisaillon, M. (2004) Thermodynamics of ligand binding by the yeast mRNA-capping enzyme reveals different modes of binding. Biochem. J. 384, 411-420
29. Flowers, S., Biswas, E. E. and Biswas, S. B. (2003) Conformational dynamics of DnaB helicase upon DNA and nucleotide binding: analysis by intrinsic tryptophan fluorescence quenching. Biochemistry 42, 1910-1921
30. Painter, G. R., Wright, L. L., Hopkins, S. and Furman, P. A. (1991) Initial binding of 2′-deoxynucleoside 5′-triphosphates to human immunodeficiency virus type 1 reverse transcriptase. J. Biol. Chem. 266, 19362-19368
31. Pan, J. Y., Sanford, J. C. and Wessling-Resnick, M. (1995) Effect of guanine nucleotide binding on the intrinsic tryptophan fluorescence properties of Rab5. J. Biol. Chem. 270, 24204-24208
32. Zhou, T. and Rosen, B. P. (1997) Tryptophan fluorescence reports nucleotide-induced conformational changes in a domain of the ArsA ATPase. J. Biol. Chem. 272, 19731-19737
33. Eftink, M. R. and Ghiron, C. A. (1976) Exposure of tryptophanyl residues in proteins: quantitative determination by fluorescence quenching studies. Biochemistry 15, 672-680
34. Shi, R., Azzi, A., Gilbert, C., Boivin, G. and Lin, S. X. (2006) Three-dimensional modeling of cytomegalovirus DNA polymerase and preliminary analysis of drug resistance. Proteins 64, 301-307
35. Labowicz, J. R. (1999) Principles of Fluorescence Spectroscopy, 2nd Edn, Kluwer/Plenum, New York
36. Beaudette, N. V. and Langerman, N. (1980) The thermodynamics of nucleotide binding to proteins. Crit. Rev. Biochem. 9, 145-169
37. Tame, J. R. H., O'Brien, R. and Ladbury, J. E. (1998) Biocalorimetry: Applications of Calorimetry in Biological Sciences, John Wiley and Sons, London
38. Franklin, M. C., Wang, J. and Steitz, T. A. (2001) Structure of the replicating complex of a polα family DNA polymerase. Cell 105, 657-667
39. Brautigam, C. A. and Steitz, T. A. (1998) Structural and functional insights provided by crystal structures of DNA polymerases and their substrate complexes. Curr. Opin. Struct. Biol. 8, 54-63
40. Delarue, M., Poch, O., Tordo, N., Moras, D. and Argos, P. (1990) An attempt to unify the structure of polymerases. Protein Eng. 6, 461-467
41. Ollis, D. L., Brick, P., Hamlin, R., Xuong, N. G. and Steitz, T. A. (1985) Structure of large fragment of Escherichia coli DNA polymerase I complexed with dTMP. Nature 313, 762-766
42. Savino, C., Federici, L., Johnson, K. A., Vallone, B., Nastopoulos, V., Rossi, M., Pisani, F. M. and Tsernoglou, D. (2004) Insights into DNA replication: the crystal structure of DNA polymerase B1 from the archaeon Sulfolobus solfataricus. Structure 12, 2001-2008
43. Wang, T. S., Wong, S. W. and Korn, D. (1989) Human DNA polymerase α: predicted functional domains and relationships with viral DNA polymerases. FASEB J. 3, 14-21