Crystal structure of a thermostable Bacillus DNA polymerase I large fragment at 2.1 Å resolution

Structure

Volumn 5, Issue 1, 1997, Pages 95-108

  Kiefer, James R ^a   Mao, Chen ^a   Hansen, Connie J ^b   Basehore, Scott L ^b   Hogrefe, Holly H ^b   Braman, Jeffrey C ^b   Beese, Lorena S ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b Stratagene   (United States)

Author keywords

Bacillus stearothermophilus; DNA replication; Klenow fragment; thermostability; X ray crystallography

Indexed keywords

GEOBACILLUS STEAROTHERMOPHILUS;

EID: 0031568308     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0969-2126(97)00169-X     Document Type: Article

References (71)

1. Kornberg, A. (1960). Biologic synthesis of deoxyribonucleic acid. Science 131, 1503-1508.
2. Klenow, H. & Henningson, I. (1970). Selective elimination of the exonuclease activity of the DNA polymerase from E. coli by limited proteolysis. Proc. Natl. Acad. Sci. USA 65, 168-175.
3. Ollis, D.L., Brick, P., Hamlin, R., Xuong, N.G. & Steitz, T.A. (1985). Structure of large fragment of Escherichia coli DNA polymerase I complexed with dTMP. Nature 313, 762-766.
4. Beese, L.S. & Steitz, T.A. (1991). Structural basis for the 3′-5′ exonuclease activity of Escherichia coli DNA polymerase I: a two metal mechanism. EMBO J. 10, 25-33.
5. Polesky, A.H., Steitz, T.A., Grindley, N.D.F. & Joyce, C.M. (1990). Identification of residues critical for the polymerase activity of the Klenow Fragment of DNA polymerase I of Escherichia coli. J. Biol. Chem. 265, 14579-14591.
6. Polesky, A.H., Dahlberg, M.E., Benkovic, S.J., Grindley, N.D.F. & Joyce, C.M. (1992). Sidechains involved in catalysis of the polymerase reaction of DNA polymerase I of Escherichia coli. J. Biol. Chem. 267, 8417-8428.
7. Mizrahi, V., Henrie, R.N., Marier, J.F., Johnson, K.A. & Benkovic, S.J. (1985). Rate-limiting steps in the DNA polymerase I reaction pathway. Biochemistry 24, 4010-4018.
8. Kuchta, R.D., Mizrahi, V., Benkovic, P.A., Johnson, K.A. & Benkovic, S.J. (1987). The kinetic mechanism of DNA polymerase I. Biochemistry 26, 8410-8417.
9. Patel, S.S., Wong, I. & Johnson, K.A. (1991) Presteady-state kinetic analysis of processive DNA replication including complete characterization of an exonuclease deficient mutant. Biochemistry 30, 511-525.
10. Beese, L.S., Friedman, J.M. & Steitz, T.A. (1993) Crystal structures of the Klenow Fragment of DNA polymerase I complexed with deoxynucleotide triphosphate and pyrophosphate. Biochemistry 32, 14095-14101.
11. Beese, L.S., Derbyshire, V. & Steitz, T.A. (1993). Structure of DNA polymerase I Klenow Fragment bound to duplex DNA. Science 260, 352-355.
12. Derbyshire, V., Grindley, N.D.F. & Joyce, C.M. (1991). The 3′-5′ exonuclease of DNA polymerase I of Escherichia coli: contribution of each amino acid at the active site of the reaction. EMBO J. 10, 17-24.
13. Delarue, M., Poch, O., Tordo, N., Moras, D. & Argos, P. (1990). An attempt to unify the structure of polymerases. Protein Eng. 3, 461-467.
14. Kohlstaedt, L.A., Wang, J., Friedman, J.M., Rice, P.A. & Steitz, T.A. (1992). Crystal structure at 3.5 Å resolution of HIV-1 reverse transcriptase complexed with an inhibitor. Science 256, 1783-1790.
15. Jacobo-Molina, A., et al., & Arnold, E. (1993). Crystal structure of Human Immunodeficiency Virus Type 1 reverse transcriptase complexed with double-stranded DNA at 3.0 Å resolution shows bent DNA. Proc. Natl. Acad. Sci. USA 90, 6320-6324.
16. Georgiadis, M.M., Jessen, S.M., Ogata, C.M., Telesnitsky, A., Goff, S.P. & Hendrickson, W.A. (1995). Mechanistic implications from the structure of a catalytic fragment of Moloney murine leukemia virus reverse transcriptase. Structure 3, 879-892.
17. Lawyer, F.C., Stoffel, S., Saiki, R.K., Myambo, K., Drummond, R. & Gelfand, D.H. (1989). Isolation, characterization, and expression in Escherichia coli of DNA polymerase the gene from Thermus aquaticus. J. Biol. Chem. 264, 6427-6437.
18. Kim, Y., Eom, S.H., Wang, J., Lee, D.-S., Suh, S.W. & Steitz, T.A. (1995). Crystal structure of Thermus aquaticus DNA polymerase. Nature 376, 612-616.
19. Korolev, S., Nayal, M., Barnes, W.M., Di Cera, E. & Waksman, G. (1995). Crystal structure of the large fragment of Thermus aquaticus DNA polymerase I at 2.5 Å resolution: structural basis for thermostability. Proc. Natl. Acad. Sci. USA 92, 9264-9268.
20. Phang, S.-M., Teo, C.-Y., Lo, E. & Wong, V.W.T. (1995). Cloning and complete sequence of the DNA polymerase-encoding gene (Bstpoll) and characterization of the Klenow-like fragment from Bacillus stearothermophilus. Gene 163, 65-68.
21. Kong, H., Kucera, R.B. & Jack, W.E. (1993). Characterization of a DNA polymerase from the hyperthermophile Archaea Thermococcus litoralis. J. Biol. Chem. 268, 1965-1975.
22. Joyce, C.M. & Grindley, N.D.F. (1982). Identification of two genes immediately downstream from the polA gene of Escherichia coli. J. Biol. Chem. 257, 1958-1964.
23. Lasergene Biocomputing Software for the Macintosh. (1994). DNASTAR user's guide: a manual for the Lasergene system. Madison, WI, USA.
24. Hein, J. (1990). Unified approach to alignment and phylogenies. Methods Enzymol. 183, 626-645.
25. Laskowski, R.A., MacArthur, M.W., Moss, D.S. & Thornton, J.M. (1993). PROCHECK: a program to check the stereochemical quality of protein structures. J. Appl. Cryst. 26, 283-291.
26. Kabsch, W. & Sander, C. (1983). Dictionary of protein secondary structures: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22, 2577-2637.
27. Derbyshire, V., et al., & Steitz, T.A. (1988). Genetic and crystallographic studies of the 3′-5′ exonucleolytic site of DNA polymerase I. Science 240, 199-201.
28. Kaboev, O.K., Luchkina, L.A., Akhmedov, A.T. & Bekker, M.L. (1981). Purification and properties of deoxyribonucleic acid polymerase from Bacillus stearothermophilus. J. Bacteriol. 145, 21-26.
29. Uemori, T., Ishino, Y., Toh, H., Asada, K. & Kato, I. (1993). Cloning of the DNA polymerase gene from Bacillus caldotenax and characterization of the gene product. J. Biochem. (Tokyo) 113, 401-410.
30. Sousa, R., Chung, Y.J., Rose, J.P. & Wang, B.C. (1993). Crystal structure of bacteriophage T7 RNA polymerase at 3.3 Å resolution. Nature 364, 593-599.
31. Rodgers, D.W., et al., & Harrison, S.C. (1995). The structure of unliganded reverse transcriptase from the human immunodeficiency virus type 1. Proc. Nat. Acad. Sci. USA 92, 1222-1226.
32. Hsiou, Y., Ding, J., Das, K., Clark, A.D. Jr., Hughes, S.J., Arnold, E. (1996). Structure of unliganded HIV-1 reverse transcriptase at 2.7 Å resolution: implications of conformational changes for polymerization and inhibition mechanisms. Structure 4, 853-860.
33. Ren, J., et al., & Stammers, D. (1995). High-resolution structures of HIV-1 RT from four RT-inhibitor complexes. Nat. Struct. Biol. 2, 293-302.
34. Ding, J., et al., & Arnold, E. (1995). Structure of HIV-1 reverse transcriptase in a complex with the non-nucleoside inhibitor alpha-APA R 95845 at 2.8 Å resolution. Structure 3, 365-379.
35. Boyer, P.L., et al., & Hughes, S.H. (1994). Mutational analysis of the fingers and palm subdomains of Human Immunodeficiency Virus type-1 (HIV-1) reverse transcriptase. J. Mol. Biol. 243, 472-483.
36. Sousa, R., Rose, J. & Wang, B.C. (1994). The thumb's knuckle: flexibility in the thumb subdomain of T7 RNA polymerase is revealed by the structure of a chimeric T7/T3 RNA polymerase. J. Mol. Biol. 244, 6-12.
37. Patel, P.H., et al., & Arnold, E. (1995). Insights into DNA polymerization mechanisms from structure and function analysis of HIV-1 reverse transcriptase. Biochemistry 34, 5351-5363.
38. Tabor, S. & Richardson, C.C. (1995). A single residue in DNA polymerases of the Escherichia coli DNA polymerase I family is critical for distinguishing between deoxy- and dideoxyribonucleotides. Proc. Natl. Acad. Sci. USA 92, 6339-6343.
39. Alber, T. (1989). Mutational effects on protein stability. Annu. Rev. Biochem. 58, 765-798.
40. Dill, K.A. (1990). Dominant forces in protein folding. Biochemistry 29, 7133-7155.
41. Goldman, A. (1995). How to make my blood boil. Structure 3, 1277-1279.
42. Raidt, H. & Perutz, M.F. (1975). Stereochemical basis of heat stability in bacterial ferredoxins and in hemoglobin A2. Nature 255, 256-259.
43. Perutz, M.F. (1978). Electrostatic effects in proteins. Science 201, 1187-1191.
44. Day, M., et al., & Rees, D.C. (1992). X-ray crystal structures of the oxidized and reduced forms of the rubredoxin from the marine hyperthermophilic archaebactezrium Pyrococcus furiosus. Protein Sci. 1, 1494-1507.
45. Korndorfer, I., Steipe, B., Huber, R., Tomschy, A. & Jaenicke, R. (1995). The crystal structure of holo-glyceraldehyde-3-phosphate dehydrogenase from the hyperthermophilic bacterium Thermotoga maritima at 2.5 Å resolution. J. Mol. Biol. 246, 511-521.
46. Yip, K.S.P., et al., & Rice, D.W. (1995). The structure of Pyrococcus furiosus glutamate dehydrogenase reveals a key role for ion-pair networks in maintaining enzyme stability at extreme temperatures. Structure 3, 1147-1158.
47. Hennig, M., Darimont, B., Sterner, R., Kirschner, K. & Jansonius, J.N. (1995). 2.0 Å structure of indole-3-glycerolphosphate synthase from the hyperthermophile Sulfolobus solfataricus: possible determinants of protein stability. Structure 3, 1295-1306.
48. Chan, M.K., Mukund, S., Kietzin, A., Adams, M.W.W. & Rees, D.C. (1995) Structure of a hyperthermophilic tungstopterin enzyme, aldehyde ferredoxin oxidoreductase. Science 267, 1463-1469.
49. Argos, P., Rossman, M.G., Grau, U.M., Zuber, H., Frank, G. & Tratshin, J.D. (1979). Thermal stability and protein structure. Biochemistry 18, 5698-5703.
50. Matthews, B.W., Nicholson, H. & Becktel, W.J. (1987). Enhanced protein thermostability from site-directed mutations that decrease the entropy of unfolding. Proc. Natl. Acad. Sci. USA 84, 6663-6667.
51. Herning, T., Yutani, K., Inaka, K., Kuroki, R., Matsushima, M. & Kikuchi, M. (1992). Role of proline residues in human lysozyme stability: a scanning calorimetric study combined with X-ray structure analysis of proline mutants. Biochemistry 31, 7077-7085.
52. Russell, R.J.M., Hough, D.W. & Danson, M.J. (1994). The crystal structure of citrate synthase from the thermophilic Archaeon, Thermoplasma acidophilum. Structure 2, 1157-1167.
53. Stiles, W.E., Meeker, A.K. & Shortle, M.D. (1994). Evidence for strained interactions between sidechains and the polypeptide backbone. J. Mol. Biol. 235, 27-32.
54. Kelly, S. & Post, F.J. (1989). Basic Microbiological Technique, 3rd Edition. Star Publishing, Belmont, CA.
55. Larsen, N., et al., & Woese, C.R. (1993). The Ribosomal Database Project. Nuc. Acids Res. 21S, 3021-3023.
56. Marmur, J. (1961). A procedure for the isolation of deoxyribonucleic acid from microorganisms. J. Mol. Biol. 3, 208-218.
57. Short, J.M., Fernandez, J.M., Sorge, J.A. & Huse, W.D. (1988). λ Zap: a bacteriophage vector with in vivo excision properties. Nuc. Acids Res. 16, 7583-7600.
58. Sagner, G., Ruger, R. & Kessler, C. (1991). Rapid filter assay for the detection of DNA polymerase activity: direct identification of the gene for the DNA polymerase from Thermus aquaticus. Gene 97, 119-123.
59. Lundberg, K.S., Shoemaker, D.D., Adams, M.W.W., Short, J.M., Sorge, J.A. & Mathur, E.J. (1991). High-fidelity amplification using a thermostable DNA polymerase isolated from Pyrococcus furiosus. Gene 108, 1-6.
60. Tabor, S., Huber, H.E. & Richardson, C.C. (1987). Escherichia coli thioredoxin confers processivity on the DNA polymerase activity of the gene 5 protein of bacteriophage T7. J. Biol. Chem. 262, 16212-16223.
61. Ricchetti, M. & Buc, H. (1993). E. coli DNA polymerase I as a reverse transcriptase. EMBO J. 12, 387-396.
62. Jones, T.A. & Kjeldgaard, M. (1993). O Version 5.9, The Manual. Uppsala University, Uppsala, Sweden.
63. Matthews, B.W. (1968). Solvent content of protein crystals. J. Mol. Biol. 33, 491-497.
64. Otwinowski, Z. & Minor, W. (1996). HKL Program Suite. Methods Enzmol., in press.
65. Furey, W. & Swaminathan, S. (1996). PHASES: a program package for the processing and analysis of diffraction data from macromolecules. Methods Enzymol., in press.
66. Navaza, J. (1994). AMoRe: an automated package for molecular replacement. Acta Cryst. D 50, 157-163.
67. Brünger, A.T. (1992). X-PLOR, Version 3.1: A System for X-Ray Crystallography and NMR. Yale University Press, New Haven, CT, USA.
68. Read, R.J. (1986). Improved Fourier coeffecients for maps using phases from partial structures with errors. Acta. Cryst. A 42, 140-149.
69. Cowtan, K. (1994). 'DM': an automated procedure for phase improvement by density modification. Joint CCP4 and ESF-EACBM Newsletter on Protein Crystallography 31, 34-38.
70. Kraulis, P.J. (1991). MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Cryst. 24, 946-950.
71. Carson, M. (1987). Ribbon models of macromolecules. J. Mol. Graphics 5, 103-106.