A Mg2+-induced conformational switch rendering a competent DNA polymerase catalytic complex

Proteins: Structure, Function and Genetics

Volumn 71, Issue 2, 2008, Pages 565-574

  Mendieta, Jesús ^a   Cases González, Clara E ^a   Matamoros, Tania ^a   Ramírez, Galo ^a   Menéndez Arias, Luis ^a  

^a CSIC   (Spain)

Author keywords

Beryllium; Catalytic ions; HIV; Magnesium; Molecular dynamics; Pre steady state kinetics; Reverse transcriptase

Indexed keywords

BERYLLIUM; DNA POLYMERASE; MAGNESIUM; METAL; NUCLEOTIDE; PHOSPHORUS; RNA DIRECTED DNA POLYMERASE; REVERSE TRANSCRIPTASE, HUMAN IMMUNODEFICIENCY VIRUS 1;

ARTICLE; CATALYSIS; CONCENTRATION (PARAMETERS); DNA REPLICATION; ENZYME CONFORMATION; KINETICS; MOLECULAR BIOLOGY; MOLECULAR MODEL; POLYMERIZATION; PRIORITY JOURNAL; SIMULATION; STEADY STATE; VALIDATION PROCESS; CHEMICAL STRUCTURE; CHEMISTRY; COMPUTER SIMULATION; DRUG EFFECT; ENZYME ACTIVE SITE; PROTEIN BINDING; PROTEIN CONFORMATION;

HUMAN IMMUNODEFICIENCY VIRUS 1;

BERYLLIUM; CATALYTIC DOMAIN; COMPUTER SIMULATION; HIV REVERSE TRANSCRIPTASE; KINETICS; MAGNESIUM; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN CONFORMATION;

EID: 41149104094     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.21711     Document Type: Article

References (33)

1. Patel PH, Loeb LA. Getting a grip on how DNA polymerases function. Nature Struct Biol 2001;8:656-659.
2. Bebenek K, Kunkel TA. Functions of DNA polymerases. Adv Prot Chem 2004;69:137-165.
3. Ollis DL, Brick P, Hamlin R, Xuong NG, Steitz TA. Structure of large fragment of Escherichia coli DNA polymerase I complexed with dTMP. Nature 1985;313:762-766.
4. Kohlstaedt LA, Wang J, Friedman JM, Rice PA, Steitz TA. Crystal structure at 3.5 Å resolution of HIV-1 reverse transcriptase complexed with an inhibitor. Science 1992;256:1783-1790.
5. Beese LS, Steitz TA. Structural basis for the 3′-5′ exonuclease activity of Escherichia coli DNA polymerase I: a two metal ion mechanism. EMBO J 1991;10:25-33.
6. Steitz TA, Smerdon SJ, Jäger J, Joyce CM. A unified polymerase mechanism for nonhomologous DNA and RNA polymerases. Science 1994;266:2022-2025.
7. Sirover MA, Loeb LA. Infidelity of DNA synthesis in vitro: screening for potential metal mutagens or carcinogens. Science 1976; 194:1434-1436.
8. Beckman RA, Mildvan AS, Loeb LA. On the fidelity of DNA replication: Manganese mutagenesis in vitro. Biochemistry 1985;24: 5810-5817.
9. Snow ET, Xu LS, Kinney PL. Effects of nickel ions on polymerase activity and fidelity during DNA replication in vitro. Chem-Biol Interact 1993;88:155-173.
10. Cases-González CE, Gutiérrez-Rivas M, Menéndez-Arias L. Coupling ribose selection to fidelity of DNA synthesis-the role of Tyr-115 of human immunodeficiency virus reverse transcriptase. J Biol Chem 2000;275:19759-19767.
11. Batra VK, Beard WA, Shock DD, Krahn JM, Pedersen LC, Wilson SH. Magnesium-induced assembly of a complete DNA polymerase catalytic complex. Structure 2006;14:757-766.
12. Showalter AK, Tsai M-D. A reexamination of the nucleotide incorporation fidelity of DNA polymerases. Biochemistry 2002;41:10571-10576.
13. Joyce CM, Benkovic SJ. DNA polymerase fidelity: kinetics, structure and checkpoints. Biochemistry 2004;43:14317-14324.
14. Bakhtina M, Lee S, Wang Y, Dunlap C, Lamarche B, Tsai M-D. Use of viscogens, dNTPαS, and rhodium(III) as probes in stopped-flow experiments to obtain new evidence for the mechanism of catalysis by DNA polymerase β. Biochemistry 2005;44: 5177-5187.
15. Huang H, Chopra R, Verdine GL, Harrison SC. Structure of a covalently trapped catalytic complex of HIV-1 reverse transcriptase: implications for drug resistance. Science 1998;282:1669-1675.
16. Sirover MA, Loeb LA. Metal-induced infidelity during DNA synthesis. Proc Natl Acad Sci USA 1976;73:2331-2335.
17. Boretto J, Longhi S, Navarro J-M, Selmi B, Sire J, Canard B. An integrated system to study multiply substituted human immunodeficiency virus type 1 reverse transcriptase. Anal Biochem 2001;292: 139-147.
18. Matamoros T, Deval J, Guerreiro C, Mulard L, Canard B, Menéndez-Arias L. Suppression of multidrug-resistant HIV-1 reverse transcriptase primer unblocking activity by a-phosphate-modified thymidine analogues. J Mol Biol 2005;349:451-463.
19. Kati WM, Johnson KA, Jerva LF, Anderson KS. Mechanism and fidelity of HIV reverse transcriptase. J Biol Chem 1992;267:25988-25997.
20. Menéndez-Arias L. Studies on the effects of truncating α-helix E' of p66 human immunodeficiency virus type 1 reverse transcriptase on template-primer binding and fidelity of DNA synthesis. Biochemistry 1998;37:16636-16644.
21. Case DA, Darden T, Cheatham TE, III, Simmerling CL, Wang J, Duke RE, Luo R, Merz KM, Wang B, Pearlman DA, Crowley M, Brozell S, Tsui V, Gohlke H, Mongan J, Hornak V, Cui G, Beroza P, Schafmeister C, Caldwell JW, Ross WS, Kollman PA. AMBER 8. San Francisco, California: University of California; 2004.
22. Cieplak P, Cornell WD, Bayly CY, Kollman PA. Application of the multimolecule and multiconformational RESP methodology to biopolymers: charge derivation for DNA, RNA and proteins. J Comput Chem 1995;16:1357-1377.
23. Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Montgomery JA, Jr, Vreven T, Kudin KN, Burant JC, Millam JM, Iyengar SS, Tomasi J, Barone V, Mennucci B, Cossi M, Scalmani G, Rega N, Petersson GA, Nakatsuji H, Hada M, Ehara M, Toyota K, Fukuda R, Hasegawa J, Ishida M, Nakajima T, Honda Y, Kitao O, Nakai H, Klene M, Li X, Knox JE, Hratchian HP, Cross JB, Bakken V, Adamo C, Jaramillo J, Gomperts R, Stratmann RE, Yazyev O, Austin AJ, Cammi R, Pomelli C, Ochterski JW, Ayala PY, Morokuma K, Voth GA, Salvador P, Dannenberg JJ, Zakrzewski VG, Dapprich S, Daniels AD, Strain MC, Farkas O, Malick DK, Rabuck AD, Raghavachari K, Foresman JB, Ortiz JV, Cui Q, Baboul AG, Clifford S, Cioslowski J, Stefanov BB, Liu G, Liashenko A, Piskorz P, Komaromi I, Martin RL, Fox DJ, Keith T, Al-Laham MA, Peng CY, Nanayakkara A, Challacombe M, Gill PMW, Johnson B, Chen M, Wong W, Gonzalez C, Pople JA. Gaussian 03. Wallingford, CT, USA: Gaussian; 2004.
24. Pavlov M, Siegbhan PEM, Sandström M. Hydration of beryllium, magnesium, calcium and zinc ions using density functional theory. J Phys Chem A 1998;102:219-228.
25. Ding J, Das K, Hsiou Y, Sarafianos SG, Clark AD, Jr, Jacobo-Molina A, Tantillo C, Hughes SH, Arnold E. Structural and functional implications of the polymerase active site region in a complex of HIV-1 RT with a double-stranded DNA template-primer and an antibody Fab fragment at 2.8 Å resolution. J Mol Biol 1998;284: 1095-1111.
26. Yang L, Arora K, Beard WA, Wilson SH, Schlick T. Critical role of magnesium ions in DNA polymerase β's closing and active site assembly. J Am Chem Soc 2004;126:8441-8453.
27. Shanbhag SM, Choppin GR. Thermodynamics of Mg and Ca complexation with AMP, ADP, ATP. Inorg Chim Acta 1987;138:187-192.
28. 2+ dependency of HIV-1 reverse transcription, inhibition by nucleoside analogues and resistance. Nucleic Acids Res 2006;34:42-52.
29. Sabbioni E, Blanch N, Baricevic K, Serra M-A. Effects of trace metal compounds on HIV-1 reverse transcriptase. An in vitro study. Biol Trace Elem Res 1999;68:107-119.
30. Boukhalfa H, Lewis JG, Crumbliss AL. Beryllium(II) binding to ATP and ADP: Potentiometrie determination of the thermodynamic constants and implications for in vivo toxicity. BioMetals 2004; 17:105-109.
31. 2+-ion catalysis and substrate specificity. Mol Cell 2006; 22:5-13.
32. Arora K, Schlick T. In silico evidence for DNA polymerase-β's substrate-induced conformational change. Biophys J 2004;87:3088-3099.
33. Cases-González CE, Franco S, Martínez MA, Menéndez-Arias L. Mutational patterns associated with the 69 insertion complex of multi-drug-resistant HIV-1 reverse transcriptase that confer increased excision activity and high-level resistance to zidovudine. J Mol Biol 2007;365:298-309.