Hydrogen bonds in rubredoxins from mesophilic and hyperthermophilic organisms

Biochemistry

Volumn 42, Issue 15, 2003, Pages 4357-4372

  Bougault, Catherine M ^a   Eidsness, Marly K ^a   Prestegard, James H ^a  

^a UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; HYDROGEN BONDS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; SOLUTIONS;

METAL BINDING;

BIOCHEMISTRY;

ALANINE; BACTERIAL PROTEIN; CARBON; HYDROGEN; NITROGEN; OXYGEN; RUBREDOXIN;

ANALYTIC METHOD; ARTICLE; BETA SHEET; BINDING SITE; CARBON NUCLEAR MAGNETIC RESONANCE; CLOSTRIDIUM PASTEURIANUM; CONTROLLED STUDY; COVALENT BOND; HYDROGEN BOND; METAL BINDING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; PYROCOCCUS FURIOSUS; SEQUENCE HOMOLOGY; STRUCTURE ANALYSIS; TEMPERATURE DEPENDENCE; THERMOPHILIC BACTERIUM;

CLOSTRIDIUM; HYDROGEN BONDING; MAGNETIC RESONANCE SPECTROSCOPY; PROTEIN STRUCTURE, TERTIARY; PYROCOCCUS FURIOSUS; RUBREDOXINS; TEMPERATURE;

BACTERIA (MICROORGANISMS); CLOSTRIDIUM PASTEURIANUM; PYROCOCCUS FURIOSUS;

EID: 0344490342     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi027264d     Document Type: Article

References (97)

1. Vieille, C., and Zeikus, G. J. (2001) Hyperthermophilic enzymes: Sources, uses, and molecular mechanisms for thermostability, Microbiol. Mol. Biol. Rev. 65, 1-43.
2. Sterner, R., and Liebl, W. (2001) Thermophilic adaptation of proteins, Crit. Rev. Biochem. Mol. Biol. 36, 39-106.
3. Szilagyi, A., and Zavodszky, P. (2000) Structural differences between mesophilic, moderately thermophilic and extremely thermophilic protein subunits: results of a comprehensive survey, Struct. Folding Des. 8, 493-504.
4. Kumar, S., Tsai, C. J., and Nussinov, R. (2000) Factors enhancing protein thermostability, Protein Eng. 13, 179-191.
5. Vogt, G., Woell, S., and Argos, P. (1997) Protein thermal stability, hydrogen bonds, and ion pairs, J. Mol. Biol. 269, 631-643.
6. Jenney, F. E., and Adams, M. W. W. (2001) Rubredoxin from Pyrococcus furiosus, Methods Enzymol. 334, 45-55.
7. Fiala, G., and Stetter, K. O. (1986) Pyrococcus furiosus represents a novel genus of marine heterotrophic archaebacteria growing optimally at 100 degrees C, Arch. Microbiol. 145, 56-61.
8. Blake, P. R., Park, J. B., Bryant, F. O., Aono, S., Magnuson, J. K., Eccleston, E., Howard, J. B., Summers, M. F., and Adams, M. W. W. (1991) Determinants of protein hyperthermostability - Purification and amino-acid-sequence of rubredoxin from the hyperthermophilic archaebacterium Pyrococcus furiosus and secondary structure of the zinc adduct by NMR, Biochemistry 30, 10885-10895.
9. Frey, M., Sieker, L., Payan, F., Haser, R., Bruschi, M., Pepe, G., and Legall, J. (1987) Rubredoxin from Desulfovibrio gigas - a molecular model of the oxidized form at 1.4 Å resolution, J. Mol. Biol. 197, 525-541.
10. Dauter, Z., Sieker, L. C., and Wilson, K. S. (1992) Refinement of rubredoxin from Desulfovibrio vulgaris at 1.0 Å with and without restraints, Acta Crystallogr., Sect. B: Struct. Commun. 48, 42-59.
11. Watenpaugh, K. D., Sieker, L. C., and Jensen, L. H. (1980) Crystallographic refinement of rubredoxin at 1.2 Å resolution, J. Mol. Biol. 138, 615-633.
12. Desulfovibrio desulfuricans rubredoxin was omitted due to its shorter amino acid sequence (45 instead of 53-54 residues).
13. Cavagnero, S., Zhou, Z. H., Adams, M. W. W., and Chan, S. I. (1995) Response of rubredoxin from Pyrococcus furiosus to environmental changes - Implications for the origin of hyperthermostability, Biochemistry 34, 9865-9873.
14. Papavassiliou, P., and Hatchikian, E. C. (1985) Isolation and characterization of a rubredoxin and a 2-(4Fe-4S) Ferredoxin from Thermodesulfobacterium commune, Biochim. Biophys. Acta 810, 1-11.
15. Eidsness, M. K., Richie, K. A., Burden, A. E., Kurtz, D. M., and Scott, R. A. (1997) Dissecting contributions to the thermostability of Pyrococcus furiosus rubredoxin: beta-sheet chimeras, Biochemistry 36, 10406-10413.
16. Cavagnero, S., Debe, D. A., Zhou, Z. H., Adams, M. W. W., and Chan, S. I. (1998) Kinetic role of electrostatic interactions in the unfolding of hyperthermophilic and mesophilic rubredoxins, Biochemistry 37, 3369-3376.
17. Hiller, R., Zhou, Z. H., Adams, M. W. W., and Englander, S. W. (1997) Stability and dynamics in a hyperthermophilic protein with melting temperature close to 200 degrees C, Proc. Natl. Acad. Sci. U.S.A. 94, 11329-11332.
18. Bonomi, F., Fessas, D., Iametti, S., Kurtz, D. M., and Mazzini, S. (2000) Thermal stability of Clostridium pasteurianum rubredoxin: Deconvoluting the contributions of the metal site and the protein, Protein Sci. 9, 2413-2426.
19. Cavagnero, S., Zhou, Z. H., Adams, M. W. W., and Chan, S. I. (1998) Unfolding mechanism of rubredoxin from Pyrococcus furiosus, Biochemistry 37, 3377-3385.
20. Day, M. W., Hsu, B. T., Joshuator, L., Park, J. B., Zhou, Z. H., Adams, M. W. W., and Rees, D. C. (1992) X-ray crystal-structures of the oxidized and reduced forms of the rubredoxin from the marine hyperthermophilic archaebacterium Pyrococcus furiosus, Protein Sci. 1, 1494-1507.
21. Blake, P. R., Park, J. B., Adams, M. W. W., and Summers, M. F. (1992) Novel observation of NH⋯S(Cys) hydrogen-bond-mediated scalar coupling in Cd-113-substituted rubredoxin from Pyrococcus furiosus, J. Am. Chem. Soc. 114, 4931-4933.
22. Blake, P. R., Lee, B., Summers, M. F., Adams, M. W. W., Park, J. B., Zhou, Z. H., and Bax, A. (1992) Quantitative measurement of small through-hydrogen-bond and through-space H-1-Cd-113 and H-1-Hg-199 J-couplings in metal-substituted rubredoxin from Pyrococcus furiosus, J. Biomol. NMR 2, 527-533.
23. Ayhan, M., Xiao, Z. G., Lavery, M. J., Hamer, A. M., Nugent, K. W., Scrofani, S. D. B., Guss, M., and Wedd, A. G. (1996) The rubredoxin from Clostridium pasteurianum: Mutation of the conserved glycine residues 10 and 43 to alanine and valine, Inorg. Chem. 35, 5902-5911.
24. Blake, P. R., Lee, B., Summers, M. F., Park, J. B., Zhi, H. Z., and Adams, M. W. W. (1994) Heteronuclear Magnetic-Resonance Studies of Zn, Cd-113, and Hg-199 substituted P. furiosus rubredoxin - Implications for biological electron-transfer, New J. Chem. 18, 387-395.
25. Xiao, Z. G., Maher, M. J., Cross, M., Bond, C. S., Guss, J. M., and Wedd, A. G. (2000) Mutation of the surface valine residues 8 and 44 in the rubredoxin from Clostridium pasteurianum: solvent access versus structural changes as determinants of reversible potential, J. Biol. Inorg. Chem. 5, 75-84.
26. Eidsness, M. K., Burden, A. E., Richie, K. A., Kurtz, D. M., Scott, R. A., Smith, E. T., Ichiye, T., Beard, B., Min, T. P., and Kang, C. H. (1999) Modulation of the redox potential of the [Fe(SCys)-(4)] site in rubredoxin by the orientation of a peptide dipole, Biochemistry 38, 14803-14809.
27. Strop, P., and Mayo, S. L. (2000) Contribution of surface salt bridges to protein stability, Biochemistry 39, 1251-1255.
28. Zartler, E. R., Jenney, F. E., Terrell, M., Eidsness, M. K., Adams, M. W. W., and Prestegard, J. H. (2001) Structural basis for thermostability in aporubredoxins from Pyrococcus furiosus and Clostridium pasteurianum, Biochemistry 40, 7279-7290.
29. Bradley, E. A., Stewart, D. E., Adams, M. W. W., and Wampler, J. E. (1993) Investigations of the thermostability of rubredoxin models using molecular-dynamics simulations, Protein Sci. 2, 650-665.
30. Jung, D. H., Kang, N. S., and Jhon, M. S. (1997) Site-directed mutation study on hyperthermostability of rubredoxin from Pyrococcus furiosus using molecular dynamics simulations in solution, J. Phys. Chem. A 101, 466-471.
31. Blake, P. R., Day, M. W., Hsu, B. T., Joshuator, L., Park, J. B., Hare, D. R., Adams, M. W. W., Rees, D. C., and Summers, M. F. (1992) Comparison of the X-ray structure of native rubredoxin from Pyrococcus furiosus with the NMR structure of the zinc-substituted protein, Protein Sci. 1, 1522-1525.
32. Bau, R., Rees, D. C., Kurtz, D. M., Scott, R. A., Huang, H. S., Adams, M. W. W., and Eidsness, M. K. (1998) Crystal structure of rubredoxin from Pyrococcus furiosus at 0.95 angstrom resolution, and the structures of N-terminal methionine and formylmethionine variants of PfRd. Contributions of N-terminal interactions to thermostability, J. Biol. lnorg. Chem. 3, 484-493.
33. Richie, K. A., Teng, Q., Elkin, C. J., and Kurtz, D. M. (1996) 2D H-1 and 3D H-1-N-15 NMR of zinc-rubredoxins: Contributions of the beta-sheet to thermostability, Protein Sci. 5, 883-894.
34. Dingley, A. J., Cordier, F., and Grzesiek, S. (2001) An introduction to hydrogen bond scalar coupling, Concepts Magn. Reson. 13, 103-127.
35. Grzesiek, S., Cordier, F., and Dingley, A. J. (2001) Scalar couplings across hydrogen bonds, Methods Enzymol. 338, 111-133.
36. NC′ scalar couplings, J. Am. Chem. Soc. 121, 1601-1602.
37. Cornilescu, G., Hu, J.-S., and Bax, A. (1999) Identification of the hydrogen bonding network in a protein by scalar couplings, J. Am. Chem. Soc. 121, 2949-2950.
38. NC′ connectivities across hydrogen bonds in a 30 kDa protein, J. Biomol. NMR 14, 181-184.
39. Meissner, A., and Sørensen, O. W. (2000) New techniques for the measurement of C′-N and C ′H-N J coupling constants across hydrogen bonds in proteins, J. Magn. Reson. 143, 387-390.
40. Liu, A., Hu, W. D., Qamar, S., and Majumdar, A. (2000) Sensitivity enhanced NMR spectroscopy by quenching scalar coupling mediated relaxation: Application to the direct observation of hydrogen bonds in C-13/N-15-labeled proteins, J. Biomol. NMR 17, 55-61.
41. Liu, A. Z., Hu, W. D., Majumdar, A., Rosen, M. K., and Patel, D. J. (2000) Detection of very weak side chain-main chain hydrogen bonding interactions in medium-size C-13/N-15-labeled proteins by sensitivity-enhanced NMR spectroscopy, J. Biomol. NMR 17, 79-82.
42. NC′ and hydrogen bond length in proteins, J. Am. Chem. Soc. 121, 6275-6279.
43. Liu, A. Z., Hu, W. D., Majumdar, A., Rosen, M. K., and Patel, D. J. (2000) NMR detection of side chain-side chain hydrogen bonding interactions in C-13/N-15-labeled proteins, J. Biomol. NMR 77, 305-310.
44. Hennig, M., and Geierstanger, B. H. (1999) Direct detection of a histidine-histidine side chain hydrogen bond important for folding of apomyoglobin, J. Am. Chem. Soc. 121, 5123-5126.
45. Alexandrescu, A. T., Snyder, D. R., and Abildgaard, F. (2001) NMR of hydrogen bonding in cold-shock protein A and an analysis of the influence of crystallographic resolution on comparisons of hydrogen bond lengths, Protein Sci. 10, 1856-1868.
46. Scheurer, C., and Bruschweiler, R. (1999) Quantum-chemical characterization of nuclear spin-spin couplings across hydrogen bonds, J. Am. Chem. Soc. 121, 8661-8662.
47. Pecul, M., Leszczynski, J., and Sadlej, J. (2000) The shielding constants and scalar couplings in N-H⋯O=C and N-H⋯N= C hydrogen bonded systems: An ab initio MO study, J. Phys. Chem. A 104, 8105-8113.
48. Arnold, W. D., and Oldfield, E. (2000) The chemical nature of hydrogen bonding in proteins via NMR: J-couplings, chemical shifts, and AIM theory, J. Am. Chem. Soc. 122, 12835-12841.
49. Bagno, A. (2000) Quantum chemical modeling of through-' hydrogen bond spin-spin coupling in amides and ubiquitin, Chem.-Eur. J. 6, 2925-2930.
50. Barfield, M. (2002) Structural dependencies of interresidue scalar coupling (h3)J(NC), and donor H-1 chemical shifts in the hydrogen bonding regions of proteins, J. Am. Chem. Soc. 124, 4158-4168.
51. Cordier, F., and Grzesiek, S. (2002) Temperature-dependence properties as studied by of protein hydrogen bond high-resolution NMR, J. Mol. Biol. 317, 739-752.
52. Li, H., Yamada, H., Akasaka, K., and Gronenborn, A. M. (2000) Pressure alters electronic orbital overlap in hydrogen bonds, J. Biomol. NMR 18, 207-216.
53. Cordier, F., Wang, C. Y., Grzesiek, S., and Nicholson, L. K. (2000) Ligand-induced strain in hydrogen bonds of the c-Src-SH3 domain detected by NMR, J. Mol. Biol. 304, 497-505.
54. Jaravine, V. A., Alexandrescu, A. T., and Grzesiek, S. (2001) Observation of the closing of individual hydrogen bonds during TFE-induced helix formation in a peptide, Protein Sci. 10, 943-950.
55. Chemical shifts are for the most part insensitive to pH changes between 6 and 8.
56. -1. Electrospray ionization mass spectra were collected on a Micromass Q-Tof-II spectrometer, after sample desalting. Experimental molecular weights agree, within 0.03%, with the Rd masses predicted for the fully labeled demetalated species.
57. Kay, L. E., Keifer, P., and Saarinen, T. (1992) Pure absorption gradient enhanced heteronuclear single quantum correlation spectroscopy with improved sensitivity, J. Am. Chem. Soc. 114, 10663-10665.
58. 2O saturation, J. Magn. Reson., Ser. A 109, 129-133.
59. Grzesiek, S., and Bax, A. (1993) The origin and removal of artifacts in 3D-HCACO spectra of proteins uniformly enriched with C-13, J. Magn. Reson., Ser. B 102, 103-106.
60. Olejniczak, E. T., and Fesik, S. W. (1994) 2-Dimensional nuclear-magnetic-resonance method for identifying the H-alpha/C-alpha signals of amino acid-residues preceding proline, J. Am. Chem. Soc. 116, 2215-2216.
61. Marion, D., Ikura, M., Tschudin, R., and Bax, A. (1989) Rapid recording of 2D NMR-spectra without phase cycling - Application to the study of hydrogen-exchange in proteins, J. Magn. Reson. 85, 393-399.
62. Schleucher, J., Sattler, M., and Griesinger, C. (1993) Coherence selection by gradients without signal attenuation - Application to the 3-Dimensional HNCO experiment, Angew. Chem., Int. Ed. Engl. 32, 1489-1491.
63. 2O samples of proteins, J. Magn. Reson., Ser. B 101, 333-337.
64. Yamazaki, T., Formankay, J. D., and Kay, L. E. (1993) 2-Dimensional NMR experiments for correlating C-13-beta and H-1-delta/epsilon chemical-shifts of aromatic residues in C-13-labeled proteins via scalar couplings, J. Am. Chem. Soc. 115, 11054-11055.
65. 2O, J. Magn. Reson., Ser. B 102, 317-321.
66. Löhr, F., and Rüterjans, H. (1996) Novel pulse sequences for the resonance assignment of aromatic side chains in C-13-labeled proteins, J. Magn. Reson., Ser. B 112, 259-268.
67. Yamazaki, T., Yoshida, M., and Nagayama, K. (1993) Complete assignments of magnetic resonances of Ribonuclease-H from Escherichia coli by double-resonance and triple-resonance 2D and 3D NMR spectroscopies, Biochemistry 32, 5656-5669.
68. Wishart, D. S., Bigam, C. G., Yao, J., Abildgaard, F., Dyson, H. J., Oldfield, E., Markley, J. L., and Sykes, B. D. (1995) H-1, C-13 and N-15 chemical-shift referencing in biomolecular NMR, J. Biomol. NMR 6, 135-140.
69. Reported assignments refer to the major species present in the CpRdZn and PfRdZn samples, i.e., the fMet forms in both cases. Backbone-only assignments are reported for MetCpRdZn and do not significantly differ from the fMet form. Specific backbone assignments could not be pursued for the wt-PfRdZn and Met-PfRdZn species due to their lower percentage in the sample and resonance overlap with the major fMet-PfRdZn component.
70. Cavanagh, J., Fairbrother, W. J., Palmer, A. G., III, and Skelton, N. J. (1996) Protein NMR spectroscopy Principles and Practice, Academic Press, San Diego.
71. Schwarzinger, S., Kroon, G. J. A., Foss, T. R., Wright, P. E., and Dyson, H. J. (2000) Random coil chemical shifts in acidic 8 M urea: Implementation of random coil shift data in NMRView, J. Biomol. NMR 18, 43-48.
72. Schwarzinger, S., Kroon, G. J. A., Foss, T. R., Chung, J., Wright, P. E., and Dyson, H. J. (2001) Sequence-dependent correction of random coil NMR chemical shifts, J. Am. Chem. Soc. 123, 2970-2978.
73. Case, D. A. (1995) Calibration of ring-current effects in proteins and nucleic acids, J. Biomol. NMR 6, 341-346.
74. No significant difference in the ring current shifts was noted when lower resolution structures were used.
75. Bodenhausen, G., and Ruben, D. J. (1980) Natural abundance N-15 NMR by enhanced heteronuclear spectroscopy, Chem. Phys. Lett. 69, 185-189.
76. Ottiger, M., Delaglio, F., and Bax, A. (1998) Measurement of J and dipolar couplings from simplified two-dimensional NMR spectra, J. Magn. Reson. 131, 373-378.
77. Tolman, J. R., and Prestegard, J. H. (1996) A quantitative J-correlation experiment for the accurate measurement of one-bond amide N-15-H-1 couplings in proteins, J. Magn. Reson., Ser. B 112, 245-252.
78. Prantner, A. M., Volkman, B. F., Wilkens, S. J., Xia, B., and Markley, J. L. (1997) Assignment of 1H, 13C and 15N signals of reduced Clostridium pasteurianum rubredoxin: Oxidation state-dependent changes in chemical shifts and relaxation rates, J. Biomol. NMR 10, 411-412.
79. Bertini, I., Kurtz, D. M., Eidsness, M. K., Liu, G., Luchinat, C., Antonio, R., and Scott, R. A. (1998) Solution structure of reduced Clostridium pasteurianum rubredoxin, J. Biol. Inorg. Chem. 3, 401-410.
80. 15N signals of oxidized Clostridium pasteurianum rubredoxin, J. Biomol. NMR 10, 409-410.
81. Blake, P. R., Park, J. B., Zhou, Z. H., Hare, D. R., Adams, M. W. W., and Summers, M. F. (1992) Solution-State Structure by NMR of zinc-substituted rubredoxin from the marine hyper-thermophilic archaebacterium Pyrococcus furiosus, Protein Sci. 1, 1508-1521.
82. Dijkstra, K., Kroon, G. J. A., Vannuland, N. A. J., and Scheek, R. M. (1994) The COCAH experiment to correlate intraresidue Carbonyl, C-alpha, and H-alpha resonances in proteins, J. Magn. Reson., Ser. A 107, 102-105.
83. Huang, C. C., Couch, G. S., Pettersen, E. F., and Ferrin, T. E. (1996) Chimera: An extensible molecular modeling application constructed using standard components, Pac. Symp. Biocomput. 1, 724.
84. Hernandez, G., and LeMaster, D. M. (2001) Reduced temperature dependence of collective conformational opening in a hyperthermophile rubredoxin, Biochemistry 40, 14384-14391.
85. Del Bene, J. E., Perera, S. A., and Bartlett, R. J. (2000) Predicted NMR coupling constants across hydrogen bonds: A fingerprint for specifying hydrogen bond type? J. Am. Chem. Soc. 122, 3560-3561.
86. Wagner, G., Pardi, A., and Wuthrich, K. (1983) Hydrogen-bond length and H-1-NMR chemical-shifts in proteins, J. Am. Chem. Soc. 105, 5948-5949.
87. Tessari, M., Vis, H., Boelens, R., Kaptein, R., and Vuister, G. W. (1997) Quantitative measurement of relaxation interference effects between H-1(N)-CSA and H-1-N-15 dipolar interaction: Correlation with secondary structure, J. Am. Chem. Soc. 119, 8985-8990.
88. Tjandra, N., and Bax, A. (1997) Solution NMR measurement of amide proton chemical shift anisotropy in N-15-enriched proteins. Correlation with hydrogen bond length, J. Am. Chem. Soc. 119, 8076-8082.
89. NC′ coupling-constant, J. Am. Chem. Soc. 117, 405-410.
90. NC′ coupling constants in the hydrogen-bonding network of human ubiquitin, J. Am. Chem. Soc. 123, 4099-4100.
91. Andersen, N. H., Neidigh, J. W., Harris, S. M., Lee, G. M., Liu, Z. H., and Tong, H. (1997) Extracting information from the temperature gradients of polypeptide NH chemical shifts. 1. The importance of conformational averaging, J. Am. Chem. Soc. 119, 8547-8561.
92. Walling, A. E., Pargas, R. E., and deDios, A. C. (1997) Chemical shift tensors in peptides: A quantum mechanical study, J. Phys. Chem. A 101, 7299-7303.
93. Bonomi, F., Burden, A. E., Eidsness, M. K., Fessas, D., Iametti, S., Kurtz, D. M., Mazzini, S., Scott, R. A., and Zeng, Q. D. (2002) Thermal stability of the [Fe(SCys)(4)] site in Clostridium pasteurianum rubredoxin: contributions of the local environment and Cys ligand protonation, J. Biol. Inorg. Chem. 7, 427-436.
94. Strop, P., and Mayo, S. L. (1999) Rubredoxin variant folds without iron, J. Am. Chem. Soc. 121, 2341-2345.
95. Koradi, R., Billeter, M., and Wuthrich, K. (1996) MolMol: a program for display and analysis of macromolecular structures, J. Mol. Graphics 14, 51-55.
96. Dyson, H. J., and Wright, P. E. (1996) Insights into protein folding from NMR, Annu. Rev. Phys. Chem. 47, 369-395.
97. Van Nuland, N. A. J., Forge V., Balbach J., and Dobson C. M. (1998) Real-time NMR studies of protein folding, Acc. Chem. Res. 31, 773-780.