Investigation of the role of the N-terminal proline, the distal heme ligand in the CO sensor CooA

Biochemistry

Volumn 43, Issue 44, 2004, Pages 14149-14160

  Clark, Robert W ^a   Youn, Hwan ^a   Parks, Ryan B ^a   Cherney, Melisa M ^a   Roberts, Gary P ^a   Burstyn, Judith N ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; IRON; PROTEINS;

DISTAL COORDINATION; DISTAL HEME POCKETSI; PROLINE;

CARBON MONOXIDE;

CARBON MONOXIDE; FERROUS ION; HEME; HEMOPROTEIN; LIGAND; PROLINE;

ABSORPTION SPECTROSCOPY; AMINO TERMINAL SEQUENCE; ARTICLE; BINDING AFFINITY; BIOSENSOR; CIRCULAR DICHROISM; DNA BINDING; ELECTRON SPIN RESONANCE; LIGAND BINDING; NONHUMAN; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; WILD TYPE;

AMINO ACID SUBSTITUTION; BACTERIAL PROTEINS; CARBON MONOXIDE; CIRCULAR DICHROISM; DNA-BINDING PROTEINS; ELECTRON SPIN RESONANCE SPECTROSCOPY; ESCHERICHIA COLI PROTEINS; FERRIC COMPOUNDS; FERROUS COMPOUNDS; FIMBRIAE PROTEINS; HEME; HEMEPROTEINS; LIGANDS; OXIDATION-REDUCTION; PEPTIDE FRAGMENTS; PROLINE; PROTEIN BINDING; SPECTROPHOTOMETRY; TRANS-ACTIVATORS;

EID: 8344231645     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0487948     Document Type: Article

References (61)

1. Rodgers, K. R. (1999) Heme-based sensors in biological systems, Curr. Opin. Chem. Biol. 3, 158-167.
2. Dioum, E. M., Rutter, J., Tuckerman, J. R., Gonzalez, G., Gilles-Gonzalez, M.-A., and McKnight, S. L. (2002) NPAS2: a gas-responsive transcription factor, Science 298, 2385-2387.
3. Jain, R., and Chan, M. K. (2003) Mechanisms of ligand discrimination by heme proteins, J. Biol. Inorg. Chem. 8, 1-11.
4. Park, H., Suquet, C., Satterlee, J. D., and Kang, C. (2004) Insights into signal transduction involving PAS domain oxygen-sensing heme proteins from the X-ray crystal structure of Escherichia coli Dos heme domain (Ec DosH), Biochemistry 43, 2738-2746.
5. Igarashi, J., Sato, A., Kitagawa, T., Yoshimura, T., Yamauchi, S., Sagami, I., and Shimizu, T. (2004) Activation of heme-regulated eukaryotic initiation factor 2α kinase by nitric oxide is induced by the formation of a five-coordinate NO-heme complex: optical absorption, electron spin resonance, and resonance Raman spectral studies, J. Biol. Chem. 279, 15752-15762.
6. Kurokawa, H., Lee, D.-S., Watanabe, M., Sagami, I., Mikami, B., Raman, C. S., and Shimizu, T. (2004) A redox-controlled molecular switch revealed by the crystal structure of a bacterial heme PAS sensor, J. Biol. Chem. 279, 20186-20193.
7. Stone, J. R., and Marletta, M. A. (1996) Spectral and kinetic studies on the activation of soluble guanylate cyclase by nitric oxide, Biochemistry 35, 1093-1099.
8. Dierks, E. A., Hu, S., Vogel, K. M., Yu, A. E., Spiro, T. G., and Burstyn, J. N. (1997) Demonstration of the role of scission of the proximal histidine-iron bond in the activation of soluble guanylyl cyclase through metalloporphyrin substitution studies, J. Am. Chem. Soc. 119, 7316-7323.
9. Hobbs, A. J. (1997) Soluble guanylate cyclase: the forgotten sibling, Trends Pharmacol. Sci. 18, 484-491.
10. Gilles-Gonzalez, M. A., Ditta, G. S., and Helinski, D. R. (1991) A hemoprotein with kinase activity encoded by the oxygen sensor of Rhizobium meliloti, Nature 350, 170-172.
11. Gilles-Gonzalez, M. A., Gonzalez, G., and Perutz, M. F. (1995) Kinase activity of oxygen sensor FixL depends on the spin state of its heme iron, Biochemistry 34, 232-236.
12. He, Y., Shelver, D., Kerby, R. L., and Roberts, G. P. (1996) Characterization of a CO-responsive transcriptional activator from Rhodospirillum rubrum, J. Biol. Chem. 271, 120-123.
13. Shelver, D., Kerby, R. L., He, Y., and Roberts, G. P. (1997) CooA, a CO-sensing transcription factor from Rhodospirillum rubrum, is a CO-binding heme protein, Proc. Natl. Acad. Sci. U.S.A. 94, 11216-11220.
14. Kerby, R. L., Ludden, P. W., and Roberts, G. P. (1995) Carbon monoxide-dependent growth of Rhodospirillum rubrum, J. Bacteriol. 177, 2241-2244.
15. Aono, S., Nakajima, H., Saito, K., and Okada, M. (1996) A novel heme protein that acts as a carbon monoxide-dependent transcriptional activator in Rhodospirillum rubrum, Biochem. Biophys. Res. Commun. 228, 752-756.
16. Shelver, D., Kerby, R. L., He, Y., and Roberts, G. P. (1995) Carbon monoxide-induced activation of gene expression in Rhodospirillum rubrum requires the product of cooA, a member of the cyclic AMP receptor protein family of transcriptional regulators, J. Bacteriol. 177, 2157-2163.
17. Shelver, D., Thorsteinsson, M. V., Kerby, R. L., Chung, S.-Y., Roberts, G. P., Reynolds, M. F., Parks, R. B., and Burstyn, J. N. (1999) Identification of two important heme site residues (cysteine 75 and histidine 77) in CooA, the CO-sensing transcription factor of Rhodospirillum rubrum, Biochemistry 38, 2669-2678.
18. Lanzilotta, W. N., Schuller, D. J., Thorsteinsson, M. V., Kerby, R. L., Roberts, G. P., and Poulos, T. L. (2000) Structure of the CO sensing transcription activator CooA, Nat. Struct. Biol. 7, 876-880.
19. Kerby, R. L., Youn, H., Thorsteinsson, M. V., and Roberts, G. P. (2003) Repositioning about the dimer interface of the transcription regulator CooA: a major signal transduction pathway between the effector and DNA-binding domains, J. Mol. Biol. 325, 809-823.
20. Aono, S., Ohkubo, K., Matsuo, T., and Nakajima, H. (1998) Redox-controlled ligand exchange of the heme in the CO-sensing transcriptional activator CooA, J. Biol. Chem. 273, 25757-25764.
21. Reynolds, M. F., Shelver, D., Kerby, R. L., Parks, R. B., Roberts, G. P., and Burstyn, J. N. (1998) EPR and electronic absorption spectroscopies of the CO-sensing CooA protein reveal a cysteine-ligated low-spin ferric heme, J. Am. Chem. Soc. 120, 9080-9081.
22. Dhawan, I. K., Shelver, D., Thorsteinsson, M. V., Roberts, G. P., and Johnson, M. K. (1999) Probing the heme axial ligation in the CO-sensing CooA protein with magnetic circular dichroism spectroscopy, Biochemistry 38, 12805-12813.
23. 1H NMR spectroscopic studies, J. Biol. Chem. 276, 11473-11476.
24. Martinez, S. E., Huang, D., Szczepaniak, A., Cramer, W. A., and Smith, J. L. (1994) Crystal structure of chloroplast cytochrome f reveals a novel cytochrome fold and unexpected heme ligation, Structure 2, 95-105.
25. Martell, A. E., and Smith, R. M. (1974) Critical Stability Constants, p 37, Plenum Press, New York.
26. Radonovich, L. J., Bloom, A., and Hoard, J. L. (1972) Stereochemistry of low-spin iron porphyrins. II. Bis(piperidine)-α,β,γ,δ- tetraphenylporphinatoiron(II), J. Am. Chem. Soc. 94, 2073-2078.
27. Scheldt, W. R., Brinegar, A. C., Ferro, E. B., and Kirner, J. F. (1977) Nitrosylmetalloporphyrins. 4. Molecular stereochemistry of two crystalline forms of nitrosyl-α,β,γ,δ-tetraphenylporphinato-(4- methylpiperidine)iron(II). A structural correlation with ν(NO), J. Am. Chem. Soc. 99, 7315-7322.
28. Wyllie, G. R. A., Schulz, C. E., and Scheidt, W. R. (2003) Five-to six-coordination in (nitrosyl)iron(II) porphyrinates: effects of binding the sixth ligand, Inorg. Chem. 42, 5722-5734.
29. Thorsteinsson, M. V., Kerby, R. L., Conrad, M., Youn, H., Staples, C. R., Lanzilotta, W. N., Poulos, T. J., Serate, J., and Roberts, G. P. (2000) Characterization of variants altered at the N-terminal proline, a novel heme-axial ligand in CooA, the CO-sensing transcriptional activator, J. Biol. Chem. 275, 39332-39338.
30. Nakajima, H., Honma, Y., Tawara, T., Kato, T., Park, S. Y., Miyatake, H., Shiro, Y., and Aono, S. (2001) Redox properties and coordination structure of the heme in the CO-sensing transcriptional activator CooA, J. Biol. Chem. 276, 7055-7061.
31. Youn, H., Kerby, R. L., Thorsteinsson, M. V., Clark, R. W., Burstyn, J. N., and Roberts, G. P. (2002) Analysis of the L116K variant of CooA, the heme-containing CO sensor, suggests the presence of an unusual heme ligand resulting in novel activity, J. Biol. Chem. 277, 33616-33623.
32. Waterman, M. R. (1978) Spectral characterization of human hemoglobin and its derivatives, Methods Enzymol. 52, 456-463.
33. Lundblad, J. R., Laurance, M., and Goodman, R. H. (1996) Fluorescence polarization analysis of protein-DNA and protein-protein interactions, Mol. Endocrinol. 10, 607-612.
34. Lu, Y., Casimiro, D. R., Bren, K. L., Richards, J. H., and Gray, H. B. (1993) Structurally engineered cytochromes with unusual ligand-binding properties: expression of Saccharomyces cerevisiae Met-80→Ala iso-1-cytochrome c, Proc. Natl. Acad. Sci. U.S.A. 90, 11456-11459.
35. Sono, M., Dawson, J. H., Hall, K., and Hager, L. P. (1986) Ligand and halide binding properties of chloroperoxidase: peroxidase-type active site heme environment with cytochrome P-450 type endogenous axial ligand and spectroscopic properties, Biochemistry 25, 347-356.
36. Sigman, J. A., Pond, A. E., Dawson, J. H., and Lu, Y. (1999) Engineering cytochrome c peroxidase into cytochrome P450: a proximal effect on heme-thiolate ligation, Biochemistry 38, 11122-11129.
37. cam. I. Crystallization and properties, J. Biol. Chem. 249, 94-101.
38. Hollenberg, P. F., and Hager, L. P. (1973) The P-450 nature of the carbon monoxide complex of ferrous chloroperoxidase, J. Biol. Chem. 248, 2630-2633.
39. Roach, M. P., Pond, A. E., Thomas, M. R., Boxer, S. G., and Dawson, J. H. (1999) The role of the distal and proximal protein environments in controlling the ferric spin state and in stabilizing thiolate ligation in heme systems: thiolate adducts of the myoglobin H93G cavity mutant. J. Am. Chem. Soc. 121, 12088-12093.
40. cam, Biochemistry 19, 3590-3599.
41. Dawson, J. H., Andersson, L. A., and Sono, M. (1982) Spectroscopic investigations of ferric cytochrome P-450-CAM ligand complexes. Identification of the ligand trans to cysteinate in the native enzyme, J. Biol. Chem. 257, 3606-3617.
42. Sono, M., Hager, L. P., and Dawson, J. H. (1991) Electron paramagnetic resonance investigations of exogenous ligand complexes of low-spin ferric chloroperoxidase: further support for endogenous thiolate ligation to the heme iron, Biochim. Biophys. Acta 1078, 351-359.
43. Wuttke, D. S. (1993) Preparation, characterization and intramolecular electron-transfer studies of ruthenium-modified cytochromes c, Ph.D. Thesis, pp 408-413, California Institute of Technology, Pasadena, CA.
44. Blumberg, W. E., and Peisach, J. (1971) Unified theory for low spin forms of all ferric heme proteins as studied by EPR, in Probes and Structure and Function of Macromolecules and Membranes (Chance, B., Yonetani, T., and Mildvan, A. S., Eds.) Vol. 2, pp 215-29, Academic Press, New York.
45. 117 is crucial for proper heme ligation and activity of CooA, J. Biol. Chem. 276, 41603-41610.
46. Hollenberg, P. F., Hager, L. P., Blumberg, W. E., and Peisach, J. (1980) An electron paramagnetic resonance study of the high and low spin forms of chloroperoxidase, J. Biol. Chem. 255, 4801-4807.
47. Tsai, A.-L., Berka, V., Chen, P.-F., and Palmer, G. (1996) Characterization of endothelial nitric-oxide synthase and its reaction with ligand by electron paramagnetic resonance, J. Biol. Chem. 271, 32563-32571.
48. Tang, S. C., Koch, S., Papaefthymiou, G. C., Foner, S., Frankel, R. B., Ibers, J. A., and Holm, R. H. (1976) Axial ligation modes in iron(III) porphyrins. Models for the oxidized reaction states of cytochrome P-450 enzymes and the molecular structure of iron-(III) protoporphyrin IX dimethyl ester p-nitrobenzenethiolate, J. Am. Chem. Soc. 98, 2414-2434.
49. Dawson, J. H., Trudell, J. R., Barth, G., Linder, R. E., Bunnenberg, E., Djerassi, C., Chiang, R., and Hager, L. P. (1976) Chloroperoxidase. Evidence for P-450 type heme environment from magnetic circular dichroism spectroscopy, J. Am. Chem. Soc. 98, 3709-3710.
50. Sono, M., Stuehr, D. J., Ikeda-Saito, M., and Dawson, J. H. (1995) Identification of nitric oxide synthase as a thiolate-ligated heme protein using magnetic circular dichroism spectroscopy. Comparison with cytochrome P-450-CAM and chloroperoxidase, J. Biol. Chem. 270, 19943-19948.
51. cam, Biochim. Biophys. Acta 386, 87-98.
52. Bracete, A. M., Sono, M., and Dawson, J. H. (1991) Effects of cyanogen bromide modification of the distal histidine on the spectroscopic and ligand binding properties of myoglobin: magnetic circular dichroism spectroscopy as a probe of distal water ligation in ferric high-spin histidine-bound heme proteins, Biochim. Biophys. Acta 1080, 264-270.
53. Sawai, H., Kawada, N., Yoshizato, K., Nakajima, H., Aono, S., and Shiro, Y. (2003) Characterization of the heme environmental structure of cytoglobin, a fourth globin in humans, Biochemistry 42, 5133-5142.
54. Yamashita, T., Hoashi, Y., Watanabe, K., Tomisugi, Y., Ishikawa, Y., and Uno, T. (2004) Roles of heme axial ligands in the regulation of CO binding to CooA, J. Biol. Chem. 279, 21394-21400.
55. Youn, H., Kerby, R. L., Conrad, M., and Roberts, G. P. (2004) Functionally critical elements of CooA-related CO sensors, J. Bacteriol. 186, 1320-1329.
56. Sugar, S. G., Egeberg, K. D., Sage, J. T., Morikis, D., and Champion, P. M. (1987) Alteration of heme axial ligands by site-directed mutagenesis: a cytochrome becomes a catalytic demethylase, J. Am. Chem. Soc. 109, 7896-7897.
57. 5 at acidic pH, Biochem. Biophys. Res. Commun. 282, 351-355.
58. Reynolds, M. F., Parks, R. B., Burstyn, J. N., Shelver, D., Thorsteinsson, M. V., Kerby, R. L., Roberts, G. P., Vogel, K. M., and Spiro, T. G. (2000) Electronic absorption, EPR, and resonance Roman spectroscopy of CooA, a CO-sensing transcription activator from R. rubrum, reveals a five-coordinate NO-heme, Biochemistry 39, 388-396,
59. Youn, H., Kerby Robert, L., and Roberts, G. P. (2003) The role of the hydrophobic distal heme pocket of CooA in ligand sensing and response, J. Biol. Chem. 278, 2333-2340.
60. Coyle, C. M., Puranik, M., Youn, H., Nielsen, S. B., Williams, R. D., Kerby, R. L., Roberts, G. P., and Spiro, T. G. (2003) Activation mechanism of the CO sensor CooA: mutational and resonance Raman spectroscopic studies, J. Biol. Chem. 278, 35384-35393.
61. Puranik, M., Nielsen, S. B., Youn, H., Hvitved, A. N., Bourassa, J. L., Case, M. A., Tengroth, C., Balakrishnan, G., Thorsteinsson, M. V., Groves, J. T., McLendon, G. L., Roberts, G. P., Olson, J. S., and Spiro, T. G. (2004) Dynamics of carbon monoxide binding to CooA, J. Biol. Chem. 279, 21096-21108.