Directed evolution as a tool for understanding and optimizing nucleic acid polymerase function

Cellular and Molecular Life Sciences

Volumn 62, Issue 22, 2005, Pages 2634-2646

  Brakmann, S ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

Directed evolution; Fidelity; Nucleic acid; Polymerase; Thermostability; Unnatural nucletotides

Indexed keywords

DNA POLYMERASE; RNA POLYMERASE;

BIOTECHNOLOGY; CRYSTAL STRUCTURE; DNA REPLICATION; DNA SYNTHESIS; ENZYME ACTIVITY; ENZYME STRUCTURE; ESCHERICHIA COLI; HYDROGEN BOND; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN MOTIF; REVIEW; SACCHAROMYCES CEREVISIAE; STRUCTURE ACTIVITY RELATION;

DIRECTED MOLECULAR EVOLUTION; RNA NUCLEOTIDYLTRANSFERASES;

ESCHERICHIA COLI; SACCHAROMYCES CEREVISIAE;

EID: 28344443530     PISSN: 1420682X     EISSN: 15691632     Source Type: Journal    
DOI: 10.1007/s00018-005-5165-5     Document Type: Review

References (88)

1. Steitz T. A. (1998) A mechanism for all polymerases. Nature 391: 231-232
2. Sousa R. (1996) Structural and mechanistic relationships between nucleic acid polymerases. TIBS 21: 186-190
3. Patel P. H., Suzuki M., Adman E., Shinkai A. and Loeb L. A. (2001) Prokaryotic DNA polymerase I: evolution, structure and 'base flipping' mechanism for nucleotide selection. J. Mol. Biol. 308: 823-837
4. Ohmori H., Friedberg E. C., Fuchs R. P. P., Goodman M. F., Hanaoka F., Hinkle D. et al. (2001) The Y-family of DNA polymerases. Mol. Cell 8: 7-8
5. Braithwaite D. K. and Ito J. (1993) Compilation, alignment and phylogenetic relationships of DNA polymerases. Nucl. Acids Res. 21: 787-802
6. Steitz T. A. (1993) DNA- and RNA-dependent DNA polymerases. Curr. Opin. Struct. Biol. 3: 31-38
7. Smith R. A., Anderson D. J. and Preston B. D. (2004) Purifying selection masks the mutational flexibility of HIV-1 reverse transcriptase. J. Biol. Chem. 279: 26726-26734
8. Delarae M., Poch O., Tordo N., Moras D. and Argos P. (1990) An attempt to unify the structure of polymerases. Prot. Engin. 3: 461-467
9. Steitz T. A. (1999) DNA polymerases: structural diversity and common mechanisms. J. Biol. Chem. 274: 17395-17398
10. Patel P. H. and Loeb L. A. (2001) Getting a grip on how DNA polymerases function. Nature Struct. Biol. 8: 656-659
11. Reha-Krantz L. J. and Nonay R. L. (1994) Motif A of bacteriophage T4 DNA polymerase: role in primer extension and DNA replication fidelity. J. Biol. Chem. 269: 5635-5643
12. Astatke M., Grindley N. D. and Joyce C. M. (1998) How E. coli DNA polymerase I (Klenow fragment) distinguishes between deoxy- and dideoxynucleotides. J. Mol. Biol. 278: 147-165
13. Gao H. Q., Boyer P. L., Arnold E. and Hughes S. H. (1998) Effects of mutations in the polymerase domain on the polymerase, RNaseH and strand transfer activities of human immunodeficiency virus type 1 reverse transcriptase. J. Mol. Biol. 277: 559-572
14. Wrobel J. A., Chao S. F., ConradM. J., Merker J. D., Swanstrom R., Pielak G. J. et al. (1998) A genetic approach for identifying critical residues in the fingers and palm subdomains of HIV-1 reverse transcriptase. Proc. Natl. Acad. Sci. USA 95: 638-645
15. Weiss K. K., Isaacs S. J., Tran N. H., Adman E. T. and Kim B. (2000) Molecular architecture of the mutagenic active site of human immunodeficiency virus type I reverse transcriptase: roles of β8-αE-loop in fidelity, processivity and substrate interactions. Biochemistry 39: 10684-10694
16. Patel P. H. and Loeb L. A. (2000) DNA polymerase active site is highly mutable: evolutionary consequences. Proc. Natl. Acad. Sci. USA 97: 5095-5100
17. Brakmann S. (2001) Discovery of superior biocatalysts by directed molecular evolution. ChemBiochem 2: 865-871
18. Horwitz M. S. and Loeb L. A. (1986) Promoters selected from random DNA sequences. Proc. Natl. Acad. Sci. USA 83: 7405-7409
19. Leung D. W., Chen E. and Goeddel D. V. (1989) A method for random mutagenesis of a defined DNA segment using a modified polymerase chain reaction. Technique 1: 11-15
20. Cadwell R. C. and Joyce G. F. (1992) Randomization of genes by PCR mutagenesis. PCR Meth. Appl. 2: 28-33
21. Zhao H., Giver L., Shao Z., Affholter J. A. and Arnold F. H. (1998) Molecular evolution by staggered extension process (StEP) in vitro recombination. Nat. Biotechnol. 16: 258-261
22. Shao Z., Zhao H., Giver L. and Arnold F. H. (1998) Random-priming in vitro recombination: an effective tool for directed evolution. Nucl. Acids Res. 26: 681-683
23. Stemmer W. P. C. (1994) DNA shuffling by random fragmentation and reassembly: In vitro recombination for molecular evolution. Proc. Natl. Acad. Sci. USA 91: 10747-10751
24. Sweasy J. B. and Loeb L. A. (1992) Mammalian DNA polymerase beta can substitute for DNA polymerase I during DNA replication in Escherichia coli. J. Biol. Chem. 267: 1407-1410
25. Chelliserrykattil J., Cai G. and Ellington A. D. (2001) A combined in vitro/in vivo selection for polymerases with novel promoter specificities. BMC Biotechnol. 1: 13, http://www.biomedcentral.com/1472-6750/1/13
26. Brakmann S. and Grzeszik S. (2001) An error-prone T7 RNA polymerase mutant generated by directed evolution. ChemBiochem 2: 212-219
27. Chelliserrykattil J. and Ellington A. D. (2004) Evolution of a T7 RNA polymerase variant that transcribes 2′-O-methyl RNA. Nature Biotechnol. 22: 1155-1160
28. Jestin J. L., Kristensen P. and Winter G. (1999) A method for the selection of catalytic activity using phage display and proximity coupling. Angew. Chem. Int. Ed. Engl. 38: 1124-1127
29. Xia G., Chen L., Sera T., Fa M., Schultz P. G. and Romesberg F. E. (2002) Directed evolution of novel polymerase activities: mutation of a DNA polymerase into an efficient RNA polymerase. Proc. Natl. Acad. Sci. USA 99: 6567-6602
30. Ghadessy F. J., Ong J. L. and Holliger P. (2001) Directed evolution of polymerase function by compartmentalized self-replication. Proc. Natl. Acad. Sci. USA 98: 4552-4557
31. Pelletier H., Sawaya M. R., Kumar A., Wilson S. H. and Kraut J. (1994) Structures of ternary complexes of rat DNA polymerase β, a template-primer, and ddCTP. Science 264: 1891-1903
32. Doublié S., Tabor S., Long A. M., Richardson C. C. and Ellenberger T. (1998) Crystal structure of a bacteriophage T7 DNA replication complex at 2.2 Å resolution. Nature 391: 251-258
33. Huang H., Chopra R., Verdine G. L. and Harrison S. C. (1998) Structure of a covalently trapped catalytic complex of HIV-1 reverse transcriptase: implications for drug resistance. Science 282: 1669-1675
34. Li Y., Korolev S. and Waksman G. (1998) Crystal structures of open and closed forms of binary and ternary complexes of the large fragment of Thermus aquaticus DNA polymerase I: structural basis for nucleotide incorporation. EMBO J. 17: 7514-7525
35. Kim B. and Loeb L. A. (1995) Human immunodeficiency virus reverse transcriptase substitutes for DNA polymerase I in Escherichia coli. Proc. Natl. Acad. Sci. USA 92: 684-688
36. Kim B., Hathaway T. R. and Loeb L. A. (1996) Human immunodeficiency virus reverse transcriptase. Functional mutants obtained by random mutagenesis coupled with genetic selection in Escherichia coli. J. Biol. Chem. 271: 4872-4878
37. Kim B. (1997) Genetic selection in Escherichia coli for active human immunodeficiency virus reverse transcriptase mutants. Methods 12: 318-324
38. Washington S. L., Yoon M. S., Chagovetz A. M., Li S. X., Clairmont C. A., Preston B. D. et al. (1997) A genetic system to identify DNA polymerase beta mutator mutants. Proc. Natl. Acad. Sci. USA 94: 1321-1326
39. Shah A. M., Conn D. A., Li S. X., Capaldi A., Jäger J. and Sweasy J. B. (2001) A DNA polymerase beta mutator mutant with reduced nucleotide discrimination and increased protein stability. Biochemistry 40: 11372-11381
40. 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
41. Shinkai A., Patel P. H. and Loeb L. A. (2001) The conserved active site motif A of Escherichia coli DNA polymerase I is highly mutable. J. Biol. Chem. 276: 18836-18842
42. Shinkai A. and Loeb L. A. (2001) In vivo mutagenesis by Escherichia coli DNA polymerase I. J. Biol. Chem. 276: 46759-46764
43. Singhal R. K., Prasad R. and Wilson S. H. (1995) DNA polymerase β conducts the gap-filling step in uracil-initiated base excision repair in a bovine testis nuclear extract. J. Biol. Chem. 270: 949-957
44. Sobol R. W., Prasad R., Evenski A., Baker A., Yang X. P., Horton J. K. et al. (2000) The lyase activity of the DNA repair protein β-polymerase protects from DNA-damage-induced cytotoxicity. Nature 405: 807-810
45. Goodman M. F. and Tippin B. (2000) The expanding polymerase universe. Nat. Rev. Mol. Cell Biol. 1: 101-109
46. Goodman M. F. and Tippin B. (2000) Sloppier copier polymerases involved in genome repair. Curr. Op. Genet. Devel. 10: 162-168
47. McDonald J. P., Rapic-Otrin V., Epstein J. A., Broughton B. C., Wang X., Lehmann A. R. et al. (1999) Novel human and mouse homologs of Saccharomyces cerevisiae DNA polymerase η. Genomics 60: 20-30
48. Johnson R. E., Kondratick C. M., Prakash S. and Prakash L. (1999) hRAD30 mutations in the variant form of Xeroderma pigmentosum. Science 285: 263-265
49. Cleaver J. E. (1999) Stopping DNA replication in its tracks. Science 285: 212-213
50. Glick E., Vigna K. L. and Loeb L. A. (2001) Mutations in human DNA polymerase η motif II alter bypass of DNA lesions. EMBO J. 20: 7303-7312
51. Ling H., Boudsocq F., Woodgate R. and Yang W. (2001) Crystal structure of a Y-family DNA polymerase in action. A mechanism for error-prone and lesion-bypass replication. Cell 107: 91-102
52. Trincao J., Johnson R. E., Escalante C. R., Prakash S., Prakash L. and Aggarwal A. K. (2001) Structure of the catalytic core of S. cerevisiae DNA polymerase eta: Implications for translesion DNA synthesis. Mol. Cell 8: 417-426
53. Zhou B. L., Pata J. D. and Steitz T. A. (2001) Crystal structure of a DinB lesion bypass DNA polymerase catalytic fragment reveals a classic polymerase catalytic domain. Mol. Cell 8: 427-437
54. Silvian L. F., Toth E. A., Pham P., Goodman M. F. and Ellenberger T. (2001) Crystal structure of a DinB family error-prone DNA polymerase from Sulfolobus solfataricus. Nat. Struct. Biol. 8: 984-989
55. Johnson R. E., Washington M. T., Prakash S. and Prakash L. (1999) Bridging the gap: a family of novel DNA polymerases that replicate faulty DNA. Proc. Natl. Acad. Sci. USA 96: 12224-12226
56. Masutani C., Kusumoto R., Yamada A., Dohmae N., Yokoi M., Yuasa M. et al. (1999) The XPV (Xeroderma pigmentosum variant) gene encodes human DNA polymerase η. Nature 399: 700-704
57. McDonald J. P., Levine A. S. and Woodgate R. (1997) The Saccharomyces cerevisiae Rad30 gene, a homologue of Escherichia coli DinB and UmuC, is DNA damage inducible and functions in a novel error-free post-replication repair mechanism. Genetics 147: 1557-1568
58. Domingo E., Biebricher C. K., Eigen M. and Holland J. J. (eds) (2001) Quasispecies and RNA Virus Evolution: Principles and Consequences, Landes Bioscience, Georgetown, TX
59. Biebricher C. K. and Düker E.-M. (1984) Light-microscopic visualization of F and type 1 pili. J. Gen. Microbiol. 130: 941-949
60. Eigen M. (1971) Self organization of matter and the evolution of biological macromolecules. Naturwissenschaft 58: 465-523
61. Brakmann S. (1997) On the generation of information as motive power for molecular evolution. Biophys. Chem. 66: 133-144
62. Schmidt-Dannert C. and Arnold F. H. (1999) Directed evolution of industrial enzymes. Trends Biotechnol. 17: 135-136
63. Patra D., Lafer E. M. and Sousa R. (1992) Isolation and characterization of mutant bacteriophage T7 RNA polymerases. J. Mol. Biol. 224: 307-318
64. Osumi-Davis P. A., de Aguilera M. C., Woody R. W. and Woody A.-Y. M. (1992) Asp537, Asp812 are essential and Lys631, His811 are catalytically significant in bacteriophage T7 RNA polymerase activity. J. Mol. Biol. 226: 37-45
65. Ikeda R., Chang L. L. and Warshamana G. S. (1993) Selection and characterization of a mutant T7 RNA polymerase that recognizes an expanded range of T7 promoter-like sequences. Biochemistry 32: 9115-9124
66. Kostyuk D. A., Dragan S. M., Lyakhov D. L., Rechinsky V. O., Tunitskaya V. L., Chernov B. K. et al. (1995) Mutants of T7 RNA polymerase that are able to synthesize both RNA and DNA. FEBS Lett. 369: 165-168
67. Sousa R. and Padilla R. (1995) A mutant T7 RNA polymerase as a DNA polymerase. EMBO J. 14: 4609-4621
68. Padilla R. and Sousa R. (1999) Efficient synthesis of nucleic acids heavily modified with non-canonical ribose 2′-groups using a mutant T7 RNA polymerase. Nucl. Acids Res. 27: 1561-1563
69. Huang J., Brieba L. G. and Sousa R. (2000) Misincorporation by wild-type and mutant T7 RNA polymerases: identification of interactions that reduce misincorporation rates by stabilizing the catalytically incompetent open conformation. Biochemistry 39: 11571-11580
70. Sousa R., Chung Y. J., Rose J. P. and Wang B. C. (1993) Crystal structure of bacteriophage T7 RNA polymerase at 3.3 Å resolution. Nature 364: 593-599
71. Jeruzalmi D. and Steitz T. A. (1998) Structure of T7 RNA polymerase complexed to the transcriptional inhibitor T7 lysozyme. EMBO J. 17: 4101-4113.
72. Cheetham G. M. T., Jeruzalmi D. and Steitz T. A. (1999) Structural basis for initiation of transcription from an RNA polymerase-promoter complex. Nature 399: 80-83
73. Cheetham G. M. T. and Steitz T. A. (1999) Structure and function of a transcribing T7 RNA polymerase initiation complex. Science 286: 2305-2309
74. Dubendorff J. W. and Studier F. W. (1991) Creation of a T7 autogene. Cloning and expression of the gene for bacteriophage T7 RNA polymerase under the control of its cognate promoter. J. Mol. Biol. 219: 61-68
75. Raskin C. A., Diaz G., Joho K. and McAllister W. T. (1992) Substitution of a single bacteriophage T3 residue in bacteriophage T7 RNA polymerase at position 748 results in a switch in promoter specificity. J. Mol. Biol. 228: 506-515
76. Rong M., He B., McAllister W. T. and Durbin R. K. (1998) Promoter specificity determinants of T7 RNA polymerase. Proc. Natl. Acad. Sci. USA 95: 515-519
77. Imburgio D., Rong M., Ma K. and McAllister W. T. (2000) Studies of promoter recognition and start site selection by T7 RNA polymerase using a comprehensive collection of promoter variants. Biochemistry 39: 10419-10430
78. Opalinska J. B. and Gewirtz A. M. (2002) Nucleic acid therapeutics: Basic principles and recent applications. Nat. Rev. Drug Discov. 1: 503-514
79. Sullenger B. A. and Gilboa E. (2002) Emerging clinical applications of RNA. Nature 418: 252-258
80. Huang Y., Eckstein F., Padilla R. and Sousa R. (1997) Mechanism of ribose 2′-group discrimination by an RNA polymerase. Biochemistry 36: 8231-8242
81. Brieba L. G. and Sousa R. (2000) Roles of histidine 784 and tyrosine 639 in ribose discrimination by T7 RNA polymerase. Biochemistry 39: 919-923
82. Tawfik D. S. and Griffiths A. D. (1998) Man-made cell-like compartments for molecular evolution. Nat. Biotechnol. 16: 652-656
83. Perler F. B., Kumar S. and Kong H. (1996) Thermostable DNA polymerases. Adv. Prot. Chem. 48: 377-435
84. Ghadessy F. J., Ramsay N., Boudsocq F., Loakes D., Brown A., Iwai S. et al. (2004) Generic expansion of the substrate spectrum of a DNA polymerase by directed evolution. Nat. Biotechnol. 22: 755-759
85. Li Y., Mitaxov V. and Waksman G. (1999) Structure-based design of Taq DNA polymerases with improved properties of dideoxynucleotide incorporation. Proc. Natl. Acad. Sci. USA 96: 9491-9496
86. Fa M., Radeghieri A., Henry A. A. and Romesberg F. E. (2004) Expanding the substrate repertoire of a DNA polymerase by directed evolution. J. Am. Chem. Soc. 126: 1748-1754
87. 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 95: 3402-3407
88. Patel P. H. and Loeb L. A. (2000) Multiple amino acid substitutions allow DNA polymerases to synthesize RNA. J. Biol. Chem. 275: 40266-40272