Identification of the ligands to the ferric heme of chlamydomonas chloroplast hemoglobin: Evidence for ligation of tyrosine-63 (B10) to the heme

Biochemistry

Volumn 38, Issue 46, 1999, Pages 15360-15368

  Das, Tapan Kanti ^a   Couture, Manon ^b   Lee, H Caroline ^a   Peisach, Jack ^a   Rousseau, Denis L ^a   Wittenberg, Beatrice A ^a   Wittenberg, Jonathan B ^a   Guertin, Michel ^b  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

CYTOCHROME C; HEME DERIVATIVE; HEMOGLOBIN; LIGAND; TYROSINE;

ARTICLE; CHEMICAL BOND; CHEMICAL INTERACTION; CHLAMYDOMONAS; CHLOROPLAST; MUTATION; NONHUMAN; PH; PHOTOSYNTHESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; SPECTRAL SENSITIVITY;

AMINO ACID SUBSTITUTION; ANIMALS; CHLAMYDOMONAS; CHLOROPLASTS; ELECTRON SPIN RESONANCE SPECTROSCOPY; FERRIC COMPOUNDS; HEME; HEMOGLOBINS; HYDROGEN-ION CONCENTRATION; LIGANDS; MUTAGENESIS, SITE-DIRECTED; SPECTRUM ANALYSIS, RAMAN; TYROSINE;

ALGAE; CHLAMYDOMONAS; EUKARYOTA; MAMMALIA; PROTOZOA;

EID: 0033576249     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi991237e     Document Type: Article

References (55)

1. Couture, M., Chamberland, H., St-Pierre, B., Lafontaine, J., and Guertin, M. (1994) Nuclear genes encoding chloroplast hemoglobins in the unicellular green alga Chlamydomonas eugametos, Mol. Gen. Genet, 243, 185-197.
2. Gagne, G., and Guertin, M. (1992) The early genetic response to light in the green unicellular alga Chlamydomonas eugametos grown under light/dark cycles involves genes that represent direct responses to light and photosynthesis, Plant Mol. Biol. 18, 429-445.
3. Couture, M., Das, T. K., Lee, H. C., Peisach, J., Rousseau, D. L., Wittenberg, B. A., Wittenberg, J. B., and Guertin, M. (1999) Chlamydomonas chloroplast ferrous hemoglobin. Heme pocket structure and reactions with ligands, J. Biol. Chem. 274, 6898-6910.
4. Antonini, E., and Brunori, M. (1971) in Hemoglobin and Myoglobin in Their Reactions with Ligands (Neuberger, A., and Tatum, E. L., Eds.) pp 1-436, North-Holland Publishing, Amsterdam.
5. Couture, M., and Guertin, M. (1996) Purification and spectroscopic characterization of a recombinant chloroplastic hemoglobin from the green unicellular alga Chlamydomonas eugametos, Eur. J. Biochem. 242, 779-787.
6. Wang, J., Caughey, W. S., and Rousseau, D. L. (1996) Resonance Raman scattering: a probe of heme protein-bound nitric oxide, in Methods in Nitric Oxide Research (Feelisch, M., and Stamler, J. S., Eds.) pp 427-454, John Wiley & Sons, New York.
7. Duff, S. M. G., Wittenberg, J. B., and Hill, R. D. (1997) Expression, purification, and properties of recombinant barley (Hordeum sp.) hemoglobin. Optical spectra and reactions with gaseous ligands, J. Biol. Chem. 272, 16746-16752.
8. Boffi, A., Takahashi, S., Spagnuolo, C., Rousseau, D. L., and Chiancone, E. (1994) Structural characterization of oxidized dimeric Scapharca inaequivalvis hemoglobin by resonance Raman spectroscopy, J. Biol. Chem. 269, 20437-20440.
9. Arredondo-Peter, R., Hargrove, M. S., Sarath, G., Moran, J. F., Lohrman, J., Olson, J. S., and Klucas, R. V. (1997) Rice hemoglobins. Gene cloning, analysis, and O2-binding kinetics of a recombinant protein synthesized in Escherichia coli, Plant Physiol. 115, 1259-1266.
10. Rousseau, D. L., Ching, Y.-C., Brunori, M., and Giacometti, G. M. (1989) Axial coordination of ferric Aplysia myoglobin, J. Biol. Chem. 264, 7878-7881.
11. Hanania, G. I., Yeghiayan, A., and Cameron, B. F. (1966) Absorption spectra of sperm-whale ferrimyoglobin, Biochem. J. 98. 189-192.
12. Wittenberg, J. B., Wittenberg, B. A., Peisach, J., and Blumberg, W. E. (1970) On the state of the iron and the nature of the ligand in oxyhemoglobin, Proc. Natl. Acad. Sci. U.S.A. 67, 1846-1853.
13. Feis, A., Marzocchi, M. P., Paoli, M., and Smulevich, G. (1994) Spin state and axial ligand bonding in the hydroxide complexes of metmyoglobin, methemoglobin, and horseradish peroxidase at room and low temperatures, Biochemistry 33, 4577-4583.
14. Hu, S., Smith, K. M., and Spiro, T. G. (1996) Assignment of protoheme resonance Raman spectrum by heme labeling in myoglobin, J. Am. Chem. Soc. 118, 12638-12646.
15. Das, T. K., Lee, H. C., Duff, S. M. G., Hill, R. D., Peisach, J., Rousseau, D. L., Wittenberg, B. A., and Wittenberg, J. B. (1999) The heme environment in barley hemoglobin, J. Biol. Chem. 274, 4207-4212.
16. Das, T. K., Boffi, A., Chiancone, E., and Rousseau, D. L. (1999) Hydroxide rather than histidine is coordinated to the heme in five-coordinate ferric Scapharca inaequivalvis hemoglobin, J. Biol Chem. 274, 2916-2919.
17. Das, T. K., Franzen, S., Pond, A., Dawson, J. H., and Rousseau, D. L. (1999) Formation of a five-coordinate hydroxide-bound heme in the His93Gly mutant of sperm whale myoglobin, Inorg. Chem. 38, 1952-1953.
18. Schlechter, E., and Saludjian, P. (1967) Conformation of ferricytochrome c. IV. Relationship between optical absorption and protein conformation, Biopolymers 5, 788-790.
19. Das, T. K., Mazumdar, S., and Mitra, S. (1998) Characterization of a partially unfolded structure of cytochrome c induced by sodium dodecyl sulphate and the kinetics of its refolding, Eur. J. Biochem. 254, 662-670.
20. Blumberg, W. E., and Peisach, J. (1971) A unified theory for low spin forms of all ferric heme proteins as studied by EPR, in Probes of Structure and Function of Macromolecules and Membranes. Vol. II. Probes of Enzymes and Hemoproteins (Chance, B., Yonetani, T., and Mildvan, A. S., Eds.) pp 215-229, Academic Press, New York.
21. Peisach, J. (1998) EPR of metalloproteins: Truth tables revisited, in Foundations of Modern EPR (Eaton, G. R., Eaton, S. S., and Salikhov, K. M., Eds.) pp 346-360, World Scientific Press, River Edge, NJ.
22. Brautigan, D. L., Feinberg, B. A., Hoffman, B. M., Margoliash, E., Peisach, J., and Blumberg, W. E. (1977) Multiple low spin forms of the cytochrome c ferrihemochrome. EPR spectra of various eukaryotic and prokaryotic cytochromes c, J. Biol. Chem. 252, 574-582.
23. Watari, H., Hayashi, A., Morimoto, H., and Kotani, M. (1968) in Recent Developments of Magnetic Resonance in Biological Systems (Fujiwara, S., and Piette, L. H., Eds.) pp 128-134, Hirokawa Publishing, Tokyo.
24. Peisach, J., Blumberg, W. E., Ogawa, S., Rachmilewitz, E. A., and Oltzik, R. (1971) The effects of protein conformation on the heme symmetry in high spin ferric heme proteins as studied by electron paramagnetic resonance, J. Biol. Chem. 246, 3342-3355.
25. Peisach, J., and Gersonde, K. (1977) Binding of CO to mutant a chains of hemoglobin M Iwate: evidence for distal imidazole ligation, Biochemistry 16, 2539-2545.
26. Kraus, D. W., Wittenberg, J. B., Lu, J. F., and Peisach, J. (1990) Hemoglobins of the Lucina pectinata/bacteria symbiosis. II. An electron paramagnetic resonance and optical spectral study of the ferric proteins, J. Biol. Chem. 265, 16054-16059.
27. Ikeda-Saito, M., Hori, H., Andersson, L. A., Prince, R. C., Pickering, I. J., George, G. N., Sanders, C. R., II, Lutz, R. S., McKelvey, E. J., and Mattera, R. (1992) Coordination structure of the ferric heme iron in engineered distal histidine myoglobin mutants, J. Biol. Chem. 267, 22843-22852.
28. Pyrz, J. W., Roe, A. L., Stern, L. J., and Que, L., Jr. (1985) Model studies of iron-tyrosinate proteins, J. Am. Chem. Soc. 107, 614-620.
29. Nagai, M., Yoneyama, Y., and Kitagawa, T. (1989) Characteristics in tyrosine coordinations of four hemoglobins M probed by resonance Raman spectroscopy, Biochemistry 28, 2418-2422.
30. Nagai, K., Kagimoto, T., Hayashi, A., Taketa, F., and Kitagawa, T. (1983) Resonance Raman studies of hemoglobins M: evidence for iron-tyrosine charge-transfer interactions in the abnormal subunits of Hb M Boston and Hb M Iwate, Biochemistry 22, 1305-1311.
31. Egeberg, K. D., Springer, B. A., Martinis, S. A., Sligar, S. G., Morikis, D., and Champion, P. M. (1990) Alteration of sperm whale myoglobin heme axial ligation by site-directed mutagenesis, Biochemistry 29, 9783-9791.
32. Adachi, S., Nagano, S., Ishimori, K., Watanabe, Y., Morishima, I., Egawa, T., Kitagawa, T., and Makino, R. (1993) Roles of proximal ligand in heme proteins: replacement of proximal histidine of human myoglobin with cysteine and tyrosine by site-directed mutagenesis as models for P-450, chloroperoxidase, and catalase, Biochemistry 32, 241-252.
33. Antanaitis, B. C., Strekas, T., and Aisen, P. (1982) Characterization of pink and purple uteroferrin by resonance Raman and CD spectroscopy, J. Biol. Chem. 257, 3766-3770.
34. Averill, B. A., Davis, J. C., Burman, S., Zirino, T., Sanders-Loehr, J., Loehr, T. M., Sage, T., and Debrunner, P. G. (1987) Spectroscopic and magnetic studies of the purple acid phosphatase from bovine spleen, J. Am. Chem. Soc. 109, 3760-3767.
35. Chuang, W. J., Johnson, S., and Van Wan, H. E. (1988) Resonance Raman spectra of bovine liver catalase: enhancement of proximal tyrosinate vibrations, J. Inorg. Biochem. 34, 201-219.
36. Sharma, K. D., Andersson, L. A., Loehr, T. M., Terner, J., and Goff, H. M. (1989) Comparative spectral analysis of mammalian, fungal, and bacterial catalases. Resonance Raman evidence for iron-tyrosinate coordination, J. Biol. Chem. 264, 12772-12779.
37. Yoshikawa, S., Shinzawa-Itoh, K., Nakashima, R., Yaono, R., Yamashita, E., Inoue, N., Yao, M., Fei, M. J., Libeu, C. P., Mizushima, T., Yamaguchi, H., Tomizaki, T., and Tsukihara, T. (1998) Redox-coupled crystal structural changes in bovine heart cytochrome c oxidase, Science 280, 1723-1729.
38. Das, T. K., Pecoraro, C., Tomson, F. L., Gennis, R. B., and Rousseau, D. L. (1998) The post-translational modification in cytochrome c oxidase is required to establish a functional environment of the catalytic site, Biochemistry 37, 14471-14476.
39. Bravo, J., Fita, I., Ferrer, J. C., Ens, W., Hillar, A., Switala, J., and Loewen, P. C. (1997) Identification of a novel bond between a histidine and the essential tyrosine in catalase HPII of Escherichia coli, Protein Sci. 6, 1016-1023.
40. Liu, Y., Thoden, J. B., Kim, J., Berger, E., Gulick, A. M., Ruzicka, F. J., Holden, H. M., and Frey, P. A. (1997) Mechanistic roles of tyrosine 149 and serine 124 in UDP-galactose 4-epimerase from Escherichia coli, Biochemistry 36, 10675-10684.
41. Appleby, C. A. (1984) Leghemoglobin and Rhizobium respiration, Annu. Rev. Plant Physiol. 35, 443-478.
42. Rashid, A. K., Van Hauwaert, M. L., Haque, M., Siddiqi, A. H., Lasters, I., De Maeyer, M., Griffon, N., Marden, M. C., Dewilde, S., Clauwaert, J., Vinogradov, S. N., and Moens, L. (1997) Trematode myoglobins, functional molecules with a distal tyrosine, J. Biol. Chem. 272, 2992-2999.
43. Blaxter, M. L., Ingram, L., and Tweedie, S. (1994) Sequence, expression and evolution of the globins of the parasitic nematode Nippostrongylus brasiliensis, Mol. Biochem. Parasitol 68, 1-14.
44. Moens, L., Vanfleteren, J., Van de Peer, Y., Peeters, K., Kapp, O., Czeluzniak, J., Goodman, M., Blaxter, M., and Vinogradov, S. (1996) Globins in nonvertebrate species: dispersal by horizontal gene transfer and evolution of the structure-function relationships, Mol. Biol. Evol. 13, 324-333.
45. Bolognesi, M., Bordo, D., Rizzi, M., Tarricone, C., and Ascenzi, P. (1997) Nonvertebrate hemoglobins: structural bases for reactivity, Prog. Biophys. Mol. Biol. 68, 29-68.
46. Hardison, R. (1998) Hemoglobins from bacteria to man: evolution of different patterns of gene expression, J. Exp. Biol. 201, 1099-1117.
47. Appleby, C. A., Bradbury, J. H., Morris, R. J., Wittenberg, B. A., Wittenberg, J. B., and Wright, P. E. (1983) Leghemoglobin. Kinetic, nuclear magnetic resonance, and optical studies of pH dependence of oxygen and carbon monoxide binding, J. Biol. Chem. 258, 2254-2259.
48. Thorsteinsson, M. V., Bevan, D. R., Potts, M., Dou, Y., Eich, R. F., Hargrove, M. S., Gibson, Q. H., and Olson, J. S. (1999) A cyanobacterial hemoglobin with unusual ligand binding kinetics and stability properties, Biochemistry 38, 2117-2126.
49. Kloek, A. P., Yang, J., Mathews, F. S., Frieden, C., and Goldberg, D. E. (1994) The tyrosine B10 hydroxyl is crucial for oxygen avidity of Ascaris hemoglobin, J. Biol. Chem. 269, 2377-2379.
50. De Baere, I., Perutz, M. F., Kiger, L., Marden, M. C., and Poyart, C. (1994) Formation of two hydrogen bonds from the globin to the heme-linked oxygen molecule in Ascaris hemoglobin, Proc. Natl. Acad. Sci. U.S.A. 91, 1594-1597.
51. Peterson, E. S., Huang, S. C., Wang, J. Q., Miller, L. M., Vidugiris, G., Kloek, A. P., Goldberg, D. E., Chance, M. R., Wittenberg, J. B., and Friedman, J. M. (1997) A comparison of functional and structural consequences of the tyrosine B10 and glutamine E7 motifs in two invertebrate hemoglobins (Ascaris suum and Lucina pectinata), Biochemistry 36, 13110-13121.
52. Palaniappan, V., and Bocian, D. F. (1994) Acid-induced transformations of myoglobin. Characterization of a new equilibrium heme-pocket intermediate, Biochemistry 33, 14264-14274.
53. Palmer, G. (1985) The electron paramagnetic resonance of metalloproteins, Biochem. Soc. Trans. 13, 548-560.
54. 1, from Pseudomonas stutzeri and Thiosphaera pantotropha, Biochemistry 36, 16267-16276.
55. Appleby, C. A., Blumberg, W. E., Peisach, J., Wittenberg, B. A., and Wittenberg, J. B. (1976) Leghemoglobin. An electron paramagnetic resonance and optical spectral study of the free protein and its complexes with nicotinate and acetate, J. Biol. Chem. 251, 6090-6096.