Rapid incorporation kinetics and improved fidelity of a novel class of 3'-OH unblocked reversible terminators

Nucleic Acids Research

Volumn 40, Issue 15, 2012, Pages 7404-7415

  Gardner, Andrew F ^a   Wang, Jinchun ^b   Wu, Weidong ^b   Karouby, Jennifer ^a,e   Li, Hong ^b   Stupi, Brian P ^b   Jack, William E ^a   Hersh, Megan N ^b   Metzker, Michael L ^b,c,d  

^a NEW ENGLAND BIOLABS   (United States)

^b LaserGen Inc   (United States)

^c Human Genome Sequencing Center   (United States)

^d BAYLOR COLLEGE OF MEDICINE   (United States)

^e Zone industrielle de Montaudran   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA POLYMERASE; LIGHTNING TERMINATOR; NITROBENZENE DERIVATIVE; NUCLEIC ACID BASE; NUCLEOTIDE; THYMIDINE DERIVATIVE; UNCLASSIFIED DRUG;

ARTICLE; CHEMICAL MODIFICATION; CONTROLLED STUDY; CYCLIC REVERSIBLE TERMINATION; ENZYME ACTIVITY; GENETIC PROCEDURES; IC 50; KINETICS; METABOLISM; METHYLATION; MOLECULAR TUNING; NEXT GENERATION SEQUENCING; NONHUMAN; NUCLEIC ACID PROBE; NUCLEOTIDE MODIFICATION; PHOTODEGRADATION; PRIORITY JOURNAL; REGULATOR GENE; STEADY STATE; STRUCTURE ACTIVITY RELATION; THERMOCOCCUS;

DEOXYURACIL NUCLEOTIDES; DNA; DNA-DIRECTED DNA POLYMERASE; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; KINETICS; NITROBENZENES; NUCLEOTIDES; SEQUENCE ANALYSIS, DNA;

EID: 84867300971     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gks330     Document Type: Article

References (73)

1. Goodman, M. F. and Tippin, B. (2000) The expanding polymerase universe. Nat. Rev. Mol. Cell Biol., 1, 101-109.
2. Ramadan, K., Shevelev, I. and Hübscher, U. (2004) The DNA-polymerase-X family: controllers of DNA quality? Nature Rev. Mol. Cell Biol., 5, 1038-1043.
3. Berdis, A. J. (2008) DNA polymerases as therapeutic targets. Biochemistry, 47, 8253-8260.
4. Johnson, K. A. (2010) The kinetic and chemical mechanism of high-fidelity DNA polymerases. Biochim. Biophys. Acta, 1804, 1041-1048.
5. Hastings, P. J., Hersh, M. N., Thornton, P. C., Fonville, N. C., Slack, A., Frisch, R. L., Ray, M. P., Harris, R. S., Leal, S. M. and Rosenberg, S. M. (2010) Competition of Escherichia coli DNA Polymerases I, II and III with DNA Pol IV in Stressed Cells. PLoS one, 5, e10862.
6. Joyce, C. M. (1997) Choosing the right sugar: how polymerases select a nucleotide substrate. Proc. Natl Acad. Sci. USA, 94, 1619-1622.
7. Steitz, T. A. (1999) DNA polymerases: structural diversity and common mechanisms. J. Biol. Chem., 274, 17395-17398.
8. Delarue, M., Poch, O., Tordo, N., Moras, D. and Argos, P. (1990) An attempt to unify the structure of polymerases. Protein Eng., 3, 461-467.
9. Gao, G., Orlova, M., Georgiadis, M. M., Hendrickson, W. A. and Goff, S. P. (1997) Conferring RNA polymerase activity to a DNA polymerase: A single residue in reverse transcriptase controls substrate selection. Proc. Natl Acad. Sci. USA, 94, 407-411.
10. Astatke, M., Ng, K., Grindley, N. D. F. and Joyce, C. M. (1998) A single side chain prevents Escherichia coli DNA polymerase I (Klenow fragment) from incorporating ribonucleotides. Proc. Natl Acad. Sci. USA, 85, 3402-3407.
11. Bonnin, A., Lázaro, J. M., Blanco, L. and Salas, M. (1999) A single tyrosine prevents insertion of ribonucleotides in the eukaryotic-type ψ29 DNA polymerase. J. Mol. Biol., 290, 241-251.
12. Gardner, A. F. and Jack, W. E. (1999) Determinants of nucleotide sugar recognition in an archaeon DNA polymerase. Nucleic Acids Res., 27, 2545-2553.
13. Cases-González, C. E., Gutiérrez-Rivas, M. and Menéndez-Arias, L. (2000) Coupling ribose selection to fidelity of DNA synthesis: The role of Tyr-115 of human immunodeficiency virus type 1 reverse transcriptase. J. Biol. Chem., 275, 19759-19767.
14. Patel, P. H. and Loeb, L. A. (2000) Multiple amino acid substitutions allow DNA polymerases to synthesize RNA. J. Biol. Chem., 275, 40266-40272.
15. Yang, G., Franklin, M., Li, J., Lin, T. C. and Konigsberg, W. (2002) A conserved Tyr residue is required for sugar selectivity in a pol α DNA polymerase. Biochemistry, 41, 10256-10261.
16. Reha-Krantz, L. J. and Nonay, R. L. (1994) Motif A of bacteriophage T4 DNA polymerase: role in primer extension and DNA replication fidelity. Isolation of new antimutator and mutator DNA polymerases. J. Biol. Chem., 269, 5635-5643.
17. Martín-Hernández, A. M., Domingo, E. and Menéndez-Arias, L. (1996) Human immunodeficiency virus type 1 reverse transcriptase: role of Tyr115 in deoxynucleotide binding and misinsertion fidelity of DNA synthesis. EMBO J., 15, 4434-4442.
18. Patel, P. H., Kawate, H., Adman, E., Ashbach, M. and Loeb, L. A. (2001) A single highly mutable catalytic site amino acid is critical for DNA polymerase fidelity. J. Biol. Chem., 276, 5044-5051.
19. Minnick, D. T., Liu, L., Grindley, N. D. F., Kunkel, T. A. and Joyce, C. M. (2002) Discrimination against purine-pyrimidine mispairs in the polymerase active site of DNA polymerase I: A structural explanation. Proc. Natl Acad. Sci. USA, 99, 1194-1199.
20. Martín-Hernández, A. M., Gutiérrez-Rivas, M., Domingo, E. and Menéndez-Arias, L. (1997) Mispair extension fidelity of Human Immunodeficiency Virus Type 1 reverse transcriptases with amino acid substitutions affecting Tyr115. Nucleic Acids Res., 25, 1383-1389.
21. Echols, H. and Goodman, M. F. (1991) Fidelity mechanisms in DNA replication. Ann. Rev. Biochem., 60, 477-511.
22. Doublié, S., Sawaya, M. R. and Ellenberger, T. (1999) An open and closed case for all polymerases. Structure, 7, R31-R35.
23. Kunkel, T. A. (2004) DNA replication fidelity. J. Biol. Chem., 279, 16895-16898.
24. Joyce, C. M. and Benkovic, S. J. (2004) DNA polymerase fidelity: Kinetics, structure, and checkpoints. Biochemistry, 43, 14317-14324.
25. Astatke, M., Grindley, N. D. F. and Joyce, C. M. (1998) How E. coli DNA polymerase I (Klenow fragment) distinguishes between deoxy-and dideoxynucleotides. J. Mol. Biol., 278, 147-165.
26. Sanger, F., Nicklen, S. and Coulson, A. R. (1977) DNA sequencing with chain-terminating inhibitors. Proc. Natl Acad. Sci. USA, 74, 5463-5467.
27. Metzker, M. L., Raghavachari, R., Richards, S., Jacutin, S. E., Civitello, A., Burgess, K. and Gibbs, R. A. (1994) Termination of DNA synthesis by novel 3'-modified deoxyribonucleoside triphosphates. Nucleic Acids Res., 22, 4259-4267.
28. Canard, B. and Sarfati, R. (1994) DNA polymerase fluorescent substrates with reversible 3'-tags. Gene, 148, 1-6.
29. Metzker, M. L. (2005) Emerging technologies in DNA sequencing. Genome Res., 15, 1767-1776.
30. Metzker, M. L. (2010) Sequencing technologies - the next generation. Nat. Rev. Genet., 11, 31-46.
31. Chen, F., Gaucher, E. A., Leal, N. A., Hutter, D., Havemann, S. A., Govindarajan, S., Ortlund, E. A. and Benner, S. A. (2010) Reconstructed evolutionary adaptive paths give polymerases accepting reversible terminators for sequencing and SNP detection. Proc. Natl Acad. Sci. USA, 107, 1948-1953.
32. Hutter, D., Kim, M.-J., Karalkar, N., Leal, N. A., Chen, F., Guggenheim, E., Visalakshi, V., Olejnik, J., Gordon, S. and Benner, S. A. (2010) Labeled nucleoside triphosphates with reversibly terminating aminoalkoxyl groups. Nucleosides Nucleotides Nucleic Acids, 29, 879-895.
33. Guo, J., Xu, N., Li, Z., Zhang, S., Wu, J., Kim, D. H., Sano Marma, M., Meng, Q., Cao, H., Li, X. et al. (2008) Four-color DNA sequencing with 3'-O-modified nucleotide reversible terminators and chemically cleavable fluorescent dideoxynucleotides. Proc. Natl Acad. Sci. USA, 105, 9145-9150.
34. Bentley, D. R., Balasubramanian, S., Swerdlow, H. P., Smith, G. P., Milton, J., Brown, C. G., Hall, K. P., Evers, D. J., Barnes, C. L., Bignell, H. R. et al. (2008) Accurate whole human genome sequencing using reversible terminator chemistry. Nature, 456, 53-59.
35. Ju, J., Kim, D. H., Bi, L., Meng, Q., Bai, X., Li, Z., Li, X., Marma, M. S., Shi, S., Wu, J. et al. (2006) Four-color DNA sequencing by synthesis using cleavable fluorescent nucleotide reversible terminators. Proc. Natl Acad. Sci. USA, 103, 19635-19640.
36. Wu, J., Zhang, S., Meng, Q., Cao, H., Li, Z., Li, X., Shi, S., Kim, D. H., Bi, L., Turro, N. J. et al. (2007) 3'-O-modified nucleotides as reversible terminators for pyrosequencing. Proc. Natl Acad. Sci. USA, 104, 16462-16467.
37. Wu, W., Stupi, B. P., Litosh, V. A., Mansouri, D., Farley, D., Morris, S., Metzker, S. and Metzker, M. L. (2007) Termination of DNA synthesis by N6-alkylated, not 3'-O-alkylated, photocleavable 2'-deoxyadenosine triphosphates. Nucleic Acid Res., 35, 6339-6349.
38. Litosh, V. A., Wu, W., Stupi, B. P., Wang, J., Morris, S. E., Hersh, M. N. and Metzker, M. L. (2011) Improved nucleotide selectivity and termination of 3'-OH unblocked reversible terminators by molecular tuning of 2-nitrobenzyl alkylated HOMedU triphosphates. Nucleic Acid Res., 39, e39.
39. Stupi, B. P., Li, H., Wang, J., Wu, W., Morris, S. E., Litosh, V. A., Muniz, J., Hersh, M. N. and Metzker, M. L. (2012) Stereochemistry of benzylic carbon substitution coupled with ring modification of 2-nitrobenzyl groups as key determinants for fast-cleaving reversible terminators. Angew. Chem. Int. Ed., 51, 1724-1727.
40. Southworth, M. W., Kong, H., Kucera, R. B., Jannasch, H. W. and Perler, F. B. (1996) Cloning of thermostable DNA polymerases from hyperthermophilic marine Archaea with emphasis on Thermococcus sp. 9 degrees N-7 and mutations affecting 3'-5' exonuclease activity. Proc. Natl Acad. Sci. USA, 93, 5281-5285.
41. Gardner, A. F. and Jack, W. E. (2002) Acyclic and dideoxy terminator preferences denote divergent sugar recognition by archaeon and Taq DNA polymerase. Nucleic Acid Res., 30, 605-613.
42. Zavgorodny, S., Polianski, M., Besidsky, E., Kriukov, V., Sanin, A., Pokrovskaya, M., Gurskaya, G., Lönnberg, H. and Azhayev, A. (1991) 1-Alkylthioalkylation of nucleoside hydroxyl functions and its synthetic applications: a new versatile method in nucleoside chemistry. Tetrahedron Lett., 32, 7593-7596.
43. Metzker, M. L., Raghavachari, R., Burgess, K. and Gibbs, R. A. (1998) Elimination of residual natural nucleotides from 3'-OmodifieddNTP syntheses by enzymatic Mop-Up. BioTechniques, 25, 814-817.
44. Benner, S. A., Hutter, D., Leal, N. A. and Chen, F. (2011), U. S. patent application 12/383, 306.
45. Gardner, A. F., Joyce, C. M. and Jack, W. E. (2004) Comparative kinetics of nucleotide analog incorporation by Vent DNA polymerase. J. Biol. Chem., 279, 11834-11842.
46. Johnson, K. A. (1992) In: Sigman, D. S. (ed.), The Enzymes, Vol. XX, 3rd edn. Academic Press, Inc., New York, pp. 1-61.
47. Johnson, K. A. (1993) Conformational coupling in DNA polymerase fidelity. Annu. Rev. Biochem., 62, 685-713.
48. Metzker, M. L., Lu, J. and Gibbs, R. A. (1996) Electrophoretically uniform fluorescent dyes for automated DNA sequencing. Science, 271, 1420-1422.
49. Chen, J. J., Tsai, C.-H., Cai, X., Horhota, A. T., McLaughlin, L. W. and Szostak, J. W. (2009) Enzymatic primer-extension with glycerol-nucleoside triphosphates on DNA templates. PLoS One, 4, e4949.
50. Ichida, J. K., Horhota, A., Zou, K., McLaughlin, L. W. and Szostak, J. W. (2005) High fidelity TNA synthesis by Therminator polymerase. Nucleic Acids Res., 33, 5219-5225.
51. Kataoka, M., Kouda, Y., Sato, K., Minakawa, N. and Matsuda, A. (2011) Highly efficient enzymatic synthesis of 3'-deoxyapionucleic acid (apioNA) having the four natural nucleobases. Chem. Commun., 47, 8700-8702.
52. Kuchta, R. D., Mizrahi, V., Benkovic, P. A., Johnson, K. A. and Benkovic, S. J. (1987) Kinetic mechanism of DNA polymerase I (Klenow). Biochemistry, 26, 8410-8417.
53. Brandis, J. W., Edwards, S. G. and Johnson, K. A. (1996) Slow rate of phosphodiester bond formation accounts for the strong bias that Taq DNA polymerase shows against 2', 3'-dideoxynucleotide terminators. Biochemistry, 35, 2189-2200.
54. Yang, G., Franklin, M., Li, J., Lin, T. C. and Konigsberg, W. (2002) Correlation of the kinetics of finger domain mutants in RB69 DNA polymerase with its structure. Biochemistry, 41, 2526-2534.
55. Brown, J. A. and Suo, Z. (2009) Elucidating the kinetic mechanism of DNA polymerization catalyzed by Sulfolobus solfataricus P2 DNA polymerase B1. Biochemistry, 48, 7502-7511.
56. Kennedy, E. M., Hergott, C., Dewhurst, S. and Kim, B. (2009) The mechanistic architecture of thermostable Pyrococcus furiosus family B DNA polymerase motif A and its interaction with the dNTP substrate. Biochemistry, 48, 11161-11168.
57. Bowers, J., Mitchell, J., Beer, E., Buzby, P. R., Causey, M., Efcavitch, J. W., Jarosz, M., Krzymanska-Olejnik, E., Kung, L., Lipson, D. et al. (2009) Virtual terminator nucleotides for next-generation DNA sequencing. Nat. Methods, 6, 593-595.
58. Rodriguez, A. C., Park, H.-W., Mao, C. and Beese, L. S. (2000) Crystal structure of a pol α family DNA polymerase from the hyperthermophilic archaeon Thermococcus sp. 9°N-7. J. Mol. Biol., 299, 447-462.
59. Zhao, Y., Jeruzalmi, D., Moarefi, I., Leighton, L., Lasken, R. and Kuriyan, J. (1999) Crystal structure of an archaebacterial DNA polymerase. Structure, 7, 1189-1199.
60. Hashimoto, H., Nishioka, M., Fujiwara, S., Takagi, M., Imanaka, T., Inoue, T. and Kai, Y. (2001) Crystal structure of DNA polymerase from hyperthermophilic archaeon Pyrococcus kodakaraensis KOD1. J. Mol. Biol., 306, 469-477.
61. Kim, S. W., Kim, D.-U., Kim, J. K., Kang, L.-W. and Cho, H.-S. (2008) Crystal structure of Pfu, the high fidelity DNA polymerase from Pyrococcus furiosus. Int. J. Biol. Macromol., 42, 356-361.
62. Wang, J., Sattar, A. K. M. A., Wang, C. C., Karam, J. D., Konigsberg, W. H. and Steitz, T. A. (1997) Crystal structure of a pol α family replication DNA polymerase from bacteriophage RB69. Cell, 89, 1087-1099.
63. 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.
64. Hopfner, K.-P., Eichinger, A., Engh, R. A., Laue, F., Ankenbauer, W., Huber, R. and Angerer, B. (1999) Crystral structure of a thermostable type B DNA polymerase from Thermococcus gorgonaritus. Proc. Natl Acad. Sci. USA, 96, 3600-3605.
65. Franklin, M. C., Wang, J. and Steitz, T. A. (2001) Structure of the replicating complex of a Pol α family DNA polymerase. Cell, 105, 657-667.
66. Michailidis, E., Marchand, B., Kodama, E. N., Singh, K., Matsuoka, M., Kirby, K. A., Ryan, E. M., Sawani, A. M., Nagy, E., Ashida, N. et al. (2009) Mechanism of inhibition of HIV-1 reverse transcriptase by 4'-ethynyl-2-fluoro- 2'-deoxyadenosine triphosphate, a translocation-defective reverse transcriptase inhibitor. J Biol Chem, 284, 35681-35691.
67. Korlach, J., Bibillo, A., Wegener, J., Peluso, P., Pham, T. T., Park, I., Clark, S., Otto, G. A. and Turner, S. W. (2008) Long, processive enzymatic DNA synthesis using 100% dye-labeled terminal phosphate-linked nucleotides. Nucleosides Nucleotides Nucleic Acids, 27, 1072-1082.
68. Eid, J., Fehr, A., Gray, J., Luong, K., Lyle, J., Otto, G., Peluso, P., Rank, D., Baybayan, P., Bettman, B. et al. (2009) Real-time DNA sequencing from single polymerase molecules. Science, 323, 133-138.
69. Metzker, M. L. (2009) Sequencing in real time. Nat. Biotechnol., 27, 150-151.
70. Nakamura, K., Oshima, T., Morimoto, T., Ikeda, S., Yoshikawa, H., Shiwa, Y., Ishikawa, S., Linak, M. C., Hirai, A., Takahashi, H. et al. (2011) Sequence-specific error profile of Illumina sequencers. Nucleic Acids Res., 39, e90.
71. Drmanac, R., Sparks, A. B., Callow, M. J., Halpern, A. L., Burns, N. L., Kermani, B. G., Carnevali, P., Nazarenko, I., Nilsen, G. B., Yeung, G. et al. (2010) Human genome sequencing using unchained base reads on self-assembling DNA nanoarrays. Science, 327, 78-81.
72. Lam, H. Y. K., Clark, M. J., Chen, R., Chen, R., Natsoulis, G., O'Huallachain, M., Dewey, F. E., Habegger, L., Ashley, E. A., Gerstein, M. B. et al. (2012) Performance comparison of whole-genome sequencing platforms. Nat. Biotechnol., 30, 78-82.
73. Hertzog, D., Hersh, M. N. and Metzker, M. L. (2011) A high-performance, low-cost approach to next-generation sequencing. BioOptics World, Issue Nov/Dec. 2011.