The solution structure of the recombinant hemoglobin from the cyanobacterium Synechocystis sp. PCC 6803 in its hemichrome state

Journal of Molecular Biology

Volumn 324, Issue 5, 2002, Pages 1015-1029

  Falzone, Christopher J ^a   Vu, B Christie ^a   Scott, Nancy L ^a   Lecomte, Juliette T J ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

Author keywords

Bis histidine; GlbN; NMR; Paramagnetic; Truncated hemoglobin

Indexed keywords

BACTERIAL PROTEIN; HISTIDINE; IRON; LIGAND; RECOMBINANT HEMOGLOBIN; VINYL DERIVATIVE; HEME; HEMOGLOBIN; PORPHYRIN; RECOMBINANT PROTEIN;

ARTICLE; CHLAMYDOMONAS; CHLAMYDOMONAS EUGAMETOS; CROSS LINKING; CYANOBACTERIUM; GREEN ALGA; LIGAND BINDING; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN STRUCTURE; SYNECHOCYSTIS; AMINO ACID SEQUENCE; ANIMAL; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; ELECTRICITY; METABOLISM; MOLECULAR GENETICS; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; SOLUTION AND SOLUBILITY;

BACTERIA (MICROORGANISMS); CHLAMYDOMONAS; CHLAMYDOMONAS EUGAMETOS; CHLOROPHYTA; CYANOBACTERIA; SYNECHOCYSTIS; SYNECHOCYSTIS SP.; SYNECHOCYSTIS SP. PCC 6803;

AMINO ACID SEQUENCE; ANIMALS; BACTERIAL PROTEINS; BINDING SITES; CHLAMYDOMONAS; CYANOBACTERIA; ELECTROSTATICS; HEME; HEMOGLOBINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PORPHYRINS; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECOMBINANT PROTEINS; SOLUTIONS;

EID: 0037073478     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0022-2836(02)01093-8     Document Type: Article

References (68)

1. Wittenberg, J. B., Bolognesi, M., Wittenberg, B. A. & Guertin, M. (2002). Truncated hemoglobins: a new family of hemoglobins widely distributed in bacteria, unicellular eukaryotes and plants. J. Biol. Chem. 277, 871-874.
2. Perutz, M. F., Kendrew, J. C. & Watson, H. C. (1965). Structure and function of haemoglobin. II. Some relations between polypeptide chain configuration and amino acid sequence. J. Mol. Biol. 13, 669-678.
3. Pesce, A., Couture, M., Dewilde, S., Guertin, M., Yamauchi, K., Ascenzi, P. et al. (2000). A novel two-over-two alpha-helical sandwich fold is characteristic of the truncated hemoglobin family. EMBO J. 19, 2424-2434.
4. Milani, M., Pesce, A., Ouellet, Y., Ascenzi, P., Guertin, M. & Bolognesi, M. (2001). Mycobacterium tuberculosis hemoglobin N displays a protein tunnel suited for O2 diffusion to the heme. EMBO J. 20, 3902-3909.
5. Kaneko, T., Sato, S., Kotani, H., Tanaka, A., Asamizu, E., Nakamura, Y. et al. (1996). Sequence analysis of the genome of the unicellular cyanobacterium Synechocystis sp. strain PCC6803. II. Sequence determination of the entire genome and assignment of potential protein-coding regions. DNA Res. 3, 109-136.
6. Scott, N. L., Falzone, C. J., Vuletich, D. A., Zhao, J., Bryant, D. A. & Lecomte, J. T. J. (2002). The hemoglobin of the cyanobacterium Synechococcus sp. PCC 7002: evidence for hexacoordination and covalent adduct formation in the ferric recombinant protein. Biochemistry, 41, 6902-6910.
7. Scott, N. L. & Lecomte, J. T. J. (2000). Cloning, expression, purification, and preliminary characterization of a putative hemoglobin from the cyanobacterium Synechocystis sp. PCC 6803. Protein Sci. 9, 587-597.
8. Lecomte, J. T. J., Scott, N. L., Vu, B. C. & Falzone, C. J. (2001). Binding of ferric heme by the recombinant globin from the cyanobacterium Synechocystis sp. PCC 6803. Biochemistry, 40, 6541-6552.
9. Couture, M., Das, T. K., Savard, P. Y., Ouellet, Y., Wittenberg, J. B., Wittenberg, B. A. et al. (2000). Structural investigations of the hemoglobin of the cyanobacterium Synechocystis PCC6803 reveal a unique distal heme pocket. Eur. J. Biochem. 267, 4770-4780.
10. Hvitved, A. N., Trent, J. T., III, Premer, S. A. & Hargrove, M. S. (2001). Ligand binding and hexacoordination in Synechocystis hemoglobin. J. Biol. Chem. 276, 34714-34721.
11. Vu, B. C., Jones, A. D. & Lecomte, J. T. J. (2002). Novel histidine-heme covalent linkage in a hemoglobin. J. Am. Chem. Soc. 124, 8544-8545.
12. Shulz, H., Hennecke, H. & Thoeny-Meyer, L. (1998). Prototype of a heme chaperone essential for cytochrome c maturation. Science, 281, 1197-1200.
13. La Mar, G. N., Satterlee, J. D. & de Ropp, J. S. (2000). Nuclear magnetic resonance of hemoproteins. In The Porphyrins Handbook (Smith, K. M., Kadish, K. & Guilard, R., eds), vol. 5, pp. 185-298, Academic Press, Burlington, MA.
14. Emerson, S. D. & La Mar, G. N. (1990). Solution structural characterization of cyanometmyoglobin: resonance assignment of heme cavity residues by two-dimensional NMR. Biochemistry, 29, 1545-1555.
15. Emerson, S. D. & La Mar, G. N. (1990). NMR determination of the orientation of the magnetic susceptibility tensor of cyano metmyoglobin: a new probe of steric tilt of bound ligand. Biochemistry, 29, 1556-1566.
16. 15N signals of Synechocystis sp. PCC 6803 methemoglobin. J. Biomol. NMR, 23, 71-72.
17. Lyons, T. A., Ratnaswamy, G. & Pochapsky, T. C. (1996). Redox-dependent dynamics of putidaredoxin characterized by amide proton exchange. Protein Sci. 5, 627-639.
18. Bai, Y., Milne, J. S., Mayne, L. & Englander, S. W. (1993). Primary structure effects on peptide group hydrogen exchange. Proteins, 17, 75-86.
19. 1H]-COSY experiments. J. Biomol. NMR, 2, 257-274.
20. Neri, D., Billeter, M. & Wüthrich, K. (1992). Determination of the nuclear magnetic resonance solution structure of the DNA-binding domain (residues 1 to 69) of the 434 repressor and comparison with the X-ray crystal structure. J. Mol. Biol. 223, 743-767.
21. Cornilescu, G., Delaglio, F. & Bax, A. (1999). Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR, 13, 289-302.
22. Powers, R., Garrett, D. S., March, C. J., Frieden, E. A., Gronenborn, A. M. & Clore, G. M. (1993). The high-resolution, three-dimensional solution structure of human interleukin-4 determined by multi-dimensional heteronuclear magnetic resonance spectroscopy. Biochemistry, 32, 6744-6762.
23. Kuszewski, J., Gronenborn, A. M. & Clore, G. M. (1997). Improvements and extensions in the conformational database potential for the refinement of NMR and X-ray structures of proteins and nucleic acids. J. Magn. Reson. 125, 171-177.
24. Kuszewski, J. & Clore, G. M. (2000). Sources of and solutions to problems in the refinement of protein NMR structures against torsion angle potentials of mean force. J. Magn. Reson. 146, 249-254.
25. Vriend, G. (1990). WHAT IF: a molecular modeling and drug design program. J. Mol. Graph. 8, 52-56.
26. Hooft, R. W., Vriend, G., Sander, C. & Abola, E. E. (1996). Errors in protein structures. Nature, 381, 272.
27. Laskowski, R. A., Rullmannn, J. A., MacArthur, M. W., Kaptein, R. & Thornton, J. M. (1996). AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR, 8, 477-486.
28. Kabsch, W. & Sander, C. (1983). Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers, 22, 2577-2637.
29. Aurora, R. & Rose, G. D. (1998). Helix capping. Protein Sci. 7, 21-38.
30. 13C-NMR. The effect of the axial ligands. Eur. J. Biochem. 227, 829-837.
31. 13C isotropic shifts of horse heart ferricytochrome c: explanation of Curie and anti-Curie temperature dependence and nonlinear pseudocontact shifts in a common two-level framework. J. Am. Chem. Soc. 120, 8472-8479.
32. Shokhirev, N. V. & Walker, F. A. (1998). The effect of axial ligand plane orientation on the contact and pseudocontact shifts of low-spin ferriheme proteins. J. Biol. Inorg. Chem. 3, 581-594.
33. Shokhirev, N. V. & Walker, F. A. (1998). Co- and counterrotation of magnetic axes and axial ligands in low-spin ferriheme systems. J. Am. Chem. Soc. 120, 981-990.
34. 1H chemical shifts as structural parameters in some low-spin ferriheme proteins. J. Biol. Inorg. Chem. 4, 515-519.
35. Holm, L. & Sander, C. (1993). Protein structure comparison by alignment of distance matrices. J. Mol. Biol. 233, 123-138.
36. Bolognesi, M., Bordo, D., Rizzi, M., Tarricone, C. & Ascenzi, P. (1997). Nonvertebrate hemoglobins: structural bases for reactivity. Prog. Biophys. Mol. Biol. 68, 29-68.
37. 1H NMR study of the heme cavity and folding topology of the abbreviated chain 118-residue globin from the cyanobacterium Nostoc commune. Biochemistry, 39, 1389-1399.
38. Tarricone, C., Galizzi, A., Coda, A., Ascenzi, P. & Bolognesi, M. (1997). Unusual structure of the oxygen-binding site in the dimeric bacterial hemoglobin from Vitreoscilla sp. Structure, 5, 497-507.
39. Mitchell, D. T., Kitto, G. B. & Hackert, M. L. (1995). Structural analysis of monomeric hemichrome and dimeric cyanomet hemoglobins from Caudina arenicola. J. Mol. Biol. 251, 421-431.
40. Hargrove, M. S., Brucker, E. A., Stec, B., Sarath, G., Arredondo-Peter, R., Klucas, R. V. et al. (2000). Crystal structure of a nonsymbiotic plant hemoglobin. Struct. Fold. Des. 8, 1005-1014.
41. Ptitsyn, O. B. & Ting, K. L. (1999). Non-functional conserved residues in globins and their possible role as a folding nucleus. J. Mol. Biol. 291, 671-682.
42. Lecomte, J. T. J., Sukits, S. F., Bhattacharya, S. & Falzone, C. J. (1999). Conformational properties of native sperm whale apomyoglobin in solution. Protein Sci. 8, 1484-1491.
43. Weber, R. E. & Vinogradov, S. N. (2001). Non-vertebrate hemoglobins: functions and molecular adaptations. Physiol. Rev. 81, 569-628.
44. Rifkind, J. M., Abugo, O., Levy, A. & Heim, J. (1994). Detection, formation, and relevance of hemichromes and hemochromes. Methods Enzymol. 231, 449-480.
45. Couture, M., Das, T. K., Lee, H. C., Peisach, J., Rousseau, D. L., Wittenberg, B. A. et al. (1999). Chlamydomonas chloroplast ferrous hemoglobin. Heme pocket structure and reactions with ligands. J. Biol. Chem. 274, 6898-6910.
46. Das, T. K., Lee, H. C., Duff, S. M., Hill, R. D., Peisach, J., Rousseau, D. L. et al. (1999). The heme environment in barley hemoglobin. J. Biol. Chem. 274, 4207-4212.
47. Burmester, T., Weich, B., Reinhardt, S. & Hankeln, T. (2000). A vertebrate globin expressed in the brain. Nature, 407, 520-523.
48. Trent, J. T., III, Watts, R. A. & Hargrove, M. S. (2001). Human neuroglobin, a hexacoordinate hemoglobin that reversibly binds oxygen. J. Biol. Chem. 276, 30106-30110.
49. Couture, M., Burmester, T, Hankeln, T. & Rousseau, D. L. (2001). The heme environment of mouse neuroglobin. Evidence for the presence of two conformations of the heme pocket. J. Biol. Chem. 276, 36377-36382.
50. Trent, J. T., III & Hargrove, M. S. (2002). A ubiquitously expressed human hexacoordinate hemoglobin. J. Biol. Chem. 277, 19538-19545.
51. Trent, J. T., Hvitved, A. & Hargrove, M. S. (2001). A model for ligand binding to hexacoordinate hemoglobins. Biochemistry, 40, 6155-6163.
52. Delaglio, F., Grzesiek, S., Vuister, G. W., Zhu, G., Pfeifer, J. & Bax, A. (1995). NMRPipe: a multi-dimensional spectral processing system based on UNIX pipes. J. Biomol. NMR, 6, 277-293.
53. 1H NMR spectra of proteins via double quantum filtering. Biochem. Biophys. Res. Commun. 117, 479-485.
54. Kumar, A., Ernst, R. R. & Wüthrich, K. (1980). A 2D NOE experiment for the elucidation of complete proton-proton cross-relaxation networks in biological macromolecules. Biochem. Biophys. Res. Commun. 95, 1-6.
55. Braunschweiler, L. & Ernst, R. R. (1983). Coherence transfer by isotropic mixing: application to proton correlation spectroscopy. J. Magn. Reson. 53, 521-528.
56. Shaka, A. J., Lee, C. & Pines, A. (1988). Iterative schemes for bilinear operators; application to spin decoupling. J. Magn. Reson. 77, 274-293.
57. Piotto, M., Saudek, V. & Sklenár, V. (1992). Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol. NMR, 2, 661-665.
58. 15N HSQC experiments optimized to retain full sensitivity. J. Magn. Reson. 102, 241-245.
59. Bodenhausen, G. & Ruben, D. G. (1980). Natural abundance nitrogen-15 NMR by enhanced heteronuclear spectroscopy. Chem. Phys. Letters, 69, 185-189.
60. Forsen, S. & Huffman, R. A. (1963). Study of moderately rapid chemical exchange reactions by means of nuclear magnetic double resonance. J. Chem. Phys. 39, 2892-2901.
61. 5. Biochemistry, 40, 4879-4891.
62. 1H nuclear magnetic resonance determination of the distal pocket structure of cyanomet complexes of genetically engineered sperm whale myoglobin His64 (E7) → Val, Thr67 (E10) → Arg. The role of distal hydrogen bonding by Arg67 (E10) in modulating ligand tilt. Biophys. J. 65, 2178-2190.
63. 1H NMR study of the solution molecular and electronic structure of engineered distal myoglobin His64(E7) Val/Val68(E11) His double mutant. Coordination of His64(E11) at the sixth position in both low-spin and high-spin states. J. Biol. Chem. 269, 1083-1090.
64. Dou, Y., Admiraal, S. J., Ikeda-Saito, M., Krzywda, S., Wilkinson, A. J., Li, T. et al. (1995). Alteration of axial coordination by protein engineering in myoglobin. Bisimidazole ligation in the His64 → Val/ Val68 → His double mutant. J. Biol. Chem. 270, 15993-16001.
65. Nilges, M., Clore, G. M. & Gronenborn, A. M. (1988). Determination of three-dimensional structures of proteins from interproton distance data by hybrid distance geometry-dynamical simulated annealing calculations. FEBS Letters, 229, 317-324.
66. Chothia, C., Levitt, M. & Richardson, D. (1981). Helix to helix packing in proteins. J. Mol. Biol. 145, 215-250.
67. Xia, Z., Nguyen, B. D. & La Mar, G. N. (2000). The use of chemical shift temperature gradients to establish the paramagnetic susceptibility tensor orientation: implication for structure determination/ refinement in paramagnetic metalloproteins. J. Biomol. NMR, 17, 167-174.
68. Kraulis, P. (1991). MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallog. 24, 946-950.