X-ray crystal structures elucidate the nucleotidyl transfer reaction of transcript initiation using two nucleotides

Proceedings of the National Academy of Sciences of the United States of America

Volumn 108, Issue 9, 2011, Pages 3566-3571

  Gleghorn, Michael L ^a,c   Davydova, Elena K ^b   Basu, Ritwika ^a   Rothman Denes, Lucia B ^b   Murakami, Katsuhiko S ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BASE; ESTER; GUANOSINE TRIPHOSPHATE; NUCLEOTIDE; RNA POLYMERASE;

ARTICLE; BACTERIOPHAGE; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME BINDING; ENZYME CONFORMATION; ENZYME KINETICS; ENZYME STRUCTURE; METAL BINDING; PRIORITY JOURNAL; TRANSCRIPTION INITIATION; X RAY CRYSTALLOGRAPHY;

AMINO ACIDS; BACTERIOPHAGE N4; BINDING SITES; BIOCATALYSIS; CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; DNA, VIRAL; DNA-DIRECTED RNA POLYMERASES; GUANOSINE DIPHOSPHATE; GUANOSINE TRIPHOSPHATE; METALS; MODELS, MOLECULAR; NUCLEOTIDES; PROTEIN CONFORMATION; RNA, MESSENGER; SUBSTRATE SPECIFICITY; TRANSCRIPTION, GENETIC; VIRION;

EID: 79952758726     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1016691108     Document Type: Article

References (36)

1. Vassylyev DG, et al. (2007) Structural basis for substrate loading in bacterial RNA polymerase. Nature 448:163-168. (Pubitemid 47067369)
2. Yin YW, Steitz TA (2004) The structural mechanism of translocation and helicase activity in T7 RNA polymerase. Cell 116:393-404. (Pubitemid 38366316)
3. Steitz TA, Steitz JA (1993) A general two-metal-ion mechanism for catalytic RNA. Proc Natl Acad Sci USA 90:6498-6502. (Pubitemid 23207240)
4. 2+-ion catalysis and substrate specificity. Mol Cell 22:5-13.
5. Temiakov D, et al. (2004) Structural basis for substrate selection by T7 RNA polymerase. Cell 116:381-391. (Pubitemid 38366315)
6. Doublie S, Tabor S, Long AM, Richardson CC, Ellenberger T (1998) Crystal structure of a bacteriophage T7 DNA replication complex at 2.2 Å resolution. Nature 391:251-258. (Pubitemid 28099004)
7. Johnson SJ, Taylor JS, Beese LS (2003) Processive DNA synthesis observed in a polymerase crystal suggests a mechanism for the prevention of frameshift mutations. Proc Natl Acad Sci USA 100:3895-3900. (Pubitemid 36418128)
8. Kennedy WP, Momand JR, Yin YW (2007) Mechanism for de novo RNA synthesis and initiating nucleotide specificity by T7 RNA polymerase. J Mol Biol 370:256-268. (Pubitemid 46829207)
9. Gleghorn ML, Davydova EK, Rothman-Denes LB, Murakami KS (2008) Structural basis for DNA-hairpin promoter recognition by the bacteriophage N4 virion RNA polymerase. Mol Cell 32:707-717.
10. Kazmierczak KM, Davydova EK, Mustaev AA, Rothman-Denes LB (2002) The phage N4 virion RNA polymerase catalytic domain is related to single-subunit RNA polymerases. EMBO J 21:5815-5823. (Pubitemid 35315279)
11. Davydova EK, Santangelo TJ, Rothman-Denes LB (2007) Bacteriophage N4 virion RNA polymerase interaction with its promoter DNA hairpin. Proc Natl Acad Sci USA 104:7033-7038. (Pubitemid 47186004)
12. Glucksmann MA, Markiewicz P, Malone C, Rothman-Denes LB (1992) Specific sequences and a hairpin structure in the template strand are required for N4 virion RNA polymerase promoter recognition. Cell 70:491-500.
13. Haynes LL, Rothman-Denes LB (1985) N4 virion RNA polymerase sites of transcription initiation. Cell 41:597-605. (Pubitemid 16219429)
14. Santoso Y, et al. (2009) Conformational transitions in DNA polymerase I revealed by single-molecule FRET. Proc Natl Acad Sci USA 107:715-720.
15. Furia TE (1972) Sequestrants in foods. CRC Handbook of Food Additives, ed TE Furia (CRC, Boca Raton, FL), 2nd Ed, Vol 1,, pp 271-294.
16. Garcia-Diaz M, Bebenek K, Krahn JM, Pedersen LC, Kunkel TA (2007) Role of the catalytic metal during polymerization by DNA polymerase lambda. DNA Repair 6:1333-1340. (Pubitemid 47243717)
17. Tomita K, Ishitani R, Fukai S, Nureki O (2006) Complete crystallographic analysis of the dynamics of CCA sequence addition. Nature 443:956-960. (Pubitemid 44646167)
18. Shultzaberger RK, Chen Z, Lewis KA, Schneider TD (2007) Anatomy of Escherichia coli sigma70 promoters. Nucleic Acids Res 35:771-788. (Pubitemid 46344705)
19. Suzuki M, Avicola AK, Hood L, Loeb LA (1997) Low fidelity mutants in the O-helix of Thermus aquaticusDNA polymerase I. J Biol Chem 272:11228-11235. (Pubitemid 27184120)
20. Batra VK, et al. (2006) Magnesium-induced assembly of a complete DNA polymerase catalytic complex. Structure 14:757-766.
21. Yang W, Woodgate R (2007) What a difference a decade makes: Insights into translesion DNA synthesis. Proc Natl Acad Sci USA 104:15591-15598. (Pubitemid 350035345)
22. Harding M (2001) Geometry of metal-ligand interactions in proteins. Acta Crystallogr, Sect D: Biol Crystallogr 57:401-411.
23. Woody AY, Eaton SS, Osumi-Davis PA, Woody RW (1996) Asp537 and Asp812 in bacteriophage T7 RNA polymerase as metal ion-binding sites studied by EPR, flow-dialysis, and transcription. Biochemistry 35:144-152. (Pubitemid 26036417)
24. Burgers PM, Eckstein F (1979) A study of the mechanism of DNA polymerase I from Escherichia coli with diastereomeric phosphorothioate analogs of deoxyadenosine triphosphate. J Biol Chem 254:6889-6893. (Pubitemid 9243543)
25. Saenger W (1983) Principles of Nucleic Acid Structure (Springer, New York), pp 108-110.
26. Martin CT, Coleman JE (1989) T7 RNA polymerase does not interact with the 5′-phosphate of the initiating nucleotide. Biochemistry 28:2760-2762.
27. Murakami KS, Davydova EK, Rothman-Denes LB (2008) X-ray crystal structure of the polymerase domain of the bacteriophage N4 virion RNA polymerase. Proc Natl Acad Sci USA 105:5046-5051. (Pubitemid 351738507)
28. 2+ and deoxynucleoside monophosphate incorporation into transcripts. Biochemistry 36:13718-13728.
29. Brieba LG, Padilla R, Sousa R (2002) Role of T7 RNA polymerase His784 in start site selection and initial transcription. Biochemistry 41:5144-5149. (Pubitemid 34411668)
30. Wang D, Bushnell DA, Westover KD, Kaplan CD, Kornberg RD (2006) Structural basis of transcription: Role of the trigger loop in substrate specificity and catalysis. Cell 127:941-954. (Pubitemid 44792264)
31. Zhang G, et al. (1999) Crystal structure of Thermus aquaticuscore RNA polymerase at 3.3 Å resolution. Cell 98:811-824.
32. McClure WR, Cech CL, Johnston DE (1978) A steady state assay for the RNA polymerase initiation reaction. J Biol Chem 253:8941-8948. (Pubitemid 9117004)
33. Hirata A, Klein BJ, Murakami KS (2008) The X-ray crystal structure of RNA polymerase from Archaea. Nature 451:851-854. (Pubitemid 351253162)
34. Cramer P, et al. (2000) Architecture of RNA polymerase II and implications for the transcription mechanism. Science 288:640-649. (Pubitemid 30241562)
35. Conaway RC, Kong SE, Conaway JW (2003) TFIIS and GreB: Two like-minded transcription elongation factors with sticky fingers. Cell 114:272-274. (Pubitemid 36962924)
36. Bermek O, Grindley ND, Joyce CM (2011) Distinct roles of the active-site Mg2 ligands, Asp882 and Asp705, of DNA polymerase I (Klenow fragment) during the prechemistry conformational transitions. J Biol Chem 286:3755-3766.