The redox behavior of the heme in cystathionine β-synthase is sensitive to pH

Biochemistry

Volumn 43, Issue 46, 2004, Pages 14684-14695

  Pazicni, Samuel ^a   Lukat Rodgers, Gudrun S ^b   Oliveriusová, Jana ^c   Rees, Katherine A ^a   Parks, Ryan B ^a   Clark, Robert W ^a   Rodgers, Kenton R ^b   Kraus, Jan P ^c   Burstyn, Judith N ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b NORTH DAKOTA STATE UNIVERSITY   (United States)

^c UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

OXIDATION; PARAMAGNETIC RESONANCE; RAMAN SPECTROSCOPY; REDOX REACTIONS; REDUCTION;

ENZYME ACTIVITY; REDOX BEHAVIOR; TRUNCATION VARIANT;

PH EFFECTS;

CYSTATHIONINE BETA SYNTHASE; DITHIONITE; FERRIC ION; FERROUS ION; HEMOPROTEIN;

ARTICLE; CIRCULAR DICHROISM; CONTROLLED STUDY; ELECTRON SPIN RESONANCE; ELECTRON TRANSPORT; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME MECHANISM; ENZYME REGULATION; NONHUMAN; OXIDATION REDUCTION STATE; PH; PH MEASUREMENT; PRIORITY JOURNAL; RAMAN SPECTROMETRY;

CIRCULAR DICHROISM; CITRIC ACID; COENZYMES; CYSTATHIONINE BETA-SYNTHASE; DITHIONITE; ELECTRON SPIN RESONANCE SPECTROSCOPY; ENZYME ACTIVATION; FERRIC COMPOUNDS; HEME; HEMEPROTEINS; HUMANS; HYDROGEN-ION CONCENTRATION; OXIDATION-REDUCTION; REDUCING AGENTS; SPECTROPHOTOMETRY; SPECTRUM ANALYSIS, RAMAN;

EID: 8744247470     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0488496     Document Type: Article

References (72)

1. Mudd, S. H., Levy, H. L., and Kraus, J. P. (2001) Disorders of transulfuration, in The Metabolic and Molecular Basis of Inherited Disease (Scriver, C. R., Beaudet, A. L., Sly, W. S., Valle, D., Childs, B., Kinzler, K. W., and Vogelstein, B., Eds.) pp 2007-2056, McGraw-Hill, New York.
2. Kraus, J. P., Janosik, M., Kozich, V., Mandell, R., Shih, V., Sperandeo, M. P., Sebastio, G., de Franchis, R., Andria, G., Kluijtmans, L. A. J., Blom, H., Boers, G. H. J., Gordon, R. B., Kamoun, P., Tsai, M. Y., Kruger, W. D., Koch, H. G., Ohura, T., and Gaustadnes, M. (1999) Cystathionine β-synthase mutations in homocystinuria, Hum. Mutat. 13, 362-375.
3. Mills, J. L., McPartlin, J. M., Kirke, P. N., Lee, Y. J., Conley, M. R., Weir, D. G., and Scott, J. M. (1995) Homocysteine metabolism in pregnancies complicated by neural-tube defects, Lancet 345, 149-151.
4. Clarke, R., Smith, A. D., Jobst, K. A., Refsum, H., Sutton, L., and Ueland, P. M. (1998) Folate, vitamin 812, and serum total homocysteine levels in confirmed Alzheimer disease, Arch. Neurol. 55, 1449-1455.
5. Kery, V., Bukovska, G., and Kraus, J. P. (1994) Transsulfuration depends on heme in addition to pyridoxal 5′-phosphate. Cystathionine β-synthase is a heme protein, J. Biol. Chem. 269, 25283-25288.
6. Janosik, M., Kery, V., Gaustadnes, M., MacLean, K. N., and Kraus, J. P. (2001) Regulation of human cystathionine β-synthase by S-adenosyl-L- methionine: evidence for two catalytically active conformations involving an autoinhibitory domain in the C-terminal region, Biochemistry 40, 10625-10633.
7. Skovby, F., Kraus, J. P., and Rosenberg, L. E. (1984) Biosynthesis and proteolytic activation of cystathionine β-synthase in rat liver, J. Biol. Chem. 259, 588-593.
8. Kery, V., Poneleit, L., and Kraus, J. P. (1998) Trypsin cleavage of human cystathionine β-synthase into an evolutionarily conserved active core: structural and functional consequences, Arch. Biochem. Biophys. 355, 222-232.
9. Oliveriusova, J., Kery, V., Maclean, K. N., and Kraus, J. P. (2002) Deletion mutagenesis of human cystathionine β-synthase. Impact on activity, oligomeric status, and S-adenosylmethionine regulation, J. Biol. Chem. 277, 48386-48394.
10. Ojha, S., Hwang, J., Kabil, O., Penner-Hahn, J. E., and Banerjee, R. (2000) Characterization of the heme in human cystathionine β-synthase by X-ray absorption and electron paramagnetic resonance spectroscopies, Biochemistry 39, 10542-10547.
11. Meier, M., Janosik, M., Kery, V., Kraus, J. P., and Burkhard, P. (2001) Structure of human cystathionine β-synthase: a unique pyridoxal 5′-phosphate-dependent heme protein, EMBO J. 20, 3910-3916.
12. Taoka, S., Green, E. L., Loehr, T. M., and Banerjee, R. (2001) Mercuric chloride-induced spin or ligation state changes in ferric or ferrous human cystathionine β-synthase inhibit enzyme activity, J. Inorg. Biochem. 87, 253-259.
13. Taoka, S., Lepore, B. W., Kabil, O., Ojha, S., Ringe, D., and Banerjee, R. (2002) Human cystathionine β-Synthase is a heme sensor protein. Evidence that the redox sensor is heme and not the vicinal cysteines in the CXXC motif seen in the crystal structure of the truncated enzyme, Biochemistry 41, 10454-10461.
14. Cheesman, M. R., Little, P. J., and Berks, B. C. (2001) Novel heme ligation in a c-type cytochrome involved in thiosulfate oxidation: EPR and MCD of SoxAX from Rhodovulum sulfidophilum, Biochemistry 40, 10562-10569.
15. Bamford, V. A., Bruno, S., Rasmussen, T., Appia-Ayme, C., Cheesman, M. R., Berks, B. C., and Hemmings, A. M. (2002) Structural basis for the oxidation of thiosulfate by a sulfur cycle enzyme, EMBO J. 21, 5599-5610.
16. Kraus, J. P., and Rosenberg, L. E. (1983) Cystathionine β-synthase from human liver: improved purification scheme and additional characterization of the enzyme in crude and pure form, Arch. Biochem. Biophys. 222, 44-52.
17. Janosik, M., Meier, M., Kery, V., Oliveriusova, J., Burkhard, P., and Kraus, J. P. (2001) Crystallization and preliminary X-ray diffraction analysis of the active core of human recombinant cystathionine β-synthase: an enzyme involved in vascular disease, Acta Crystallogr., Sect. D: Biol. Crystallogr. 57, 289-291.
18. Kim, I.-C., and Deal, W. C., Jr. (1976) Isolation and properties of a new, soluble, hemoprotein (H-450) from pig liver, Biochemistry 15, 4925-4930.
19. Hasegawa, T., Sadano, H., and Omura, T. (1984) Spectral similarities between "H-450" and cytochrome P-450, J. Biochem. (Tokyo) 96, 265-268.
20. Omura, T., Sadano, H., Hasegawa, T., Yoshida, Y., and Kominami, S. (1984) Hemoprotein H-450 identified as a form of cytochrome P-450 having an endogenous ligand at the 6th coordination position of the heme, J. Biochem. (Tokyo) 96, 1491-1500.
21. Svastits, E. W., Alberta, J. A., Kim, I.-C., and Dawson, J. H. (1989) Magnetic circular dichroism studies of the active site structure of hemoprotein H-450: comparison to cytochrome P-450 and sensitivity to pH effects, Biochem. Biophys. Res. Commun. 165, 1170-1176.
22. Kery, V., Poneleit, L., Meyer, J. D., Manning, M. C., and Kraus, J. P. (1999) Binding of pyridoxal 5′-phosphate to the heme protein human cystathionine β-synthase, Biochemistry 38, 2716-2724.
23. Evande, R., Ojha, S., and Banerjee, R. (2004) Visualization of PLP-bound intermediates in hemeless variants of human cys-tathionine β-synthase: evidence that lysine 119 is a general base, Arch. Biochem. Biophys. 427, 188-196.
24. Bruno, S., Schiaretti, F., Burkhard, P., Kraus, J. P., Janosik, M., and Mozzarelli, A. (2001) Functional properties of the active core of human cystathionine β-synthase crystals, J. Biol. Chem. 276, 16-19.
25. Jhee, K.-H., McPhie, P., and Miles, E. W. (2000) Yeast cystathionine β-synthase is a pyridoxal phosphate enzyme but, unlike the human enzyme, is not a heme protein, J. Biol. Chem. 275, 11541-11544.
26. Jhee, K.-H., McPhie, P., and Miles, E. W. (2000) Domain architecture of the heme-independent yeast cystathionine β-synthase provides insights into mechanisms of catalysis and regulation, Biochemistry 39, 10548-10556.
27. Maclean, K. N., Janosik, M., Oliveriusova, J., Kery, V., and Kraus, J. P. (2000) Transsulfuration in Saccharomyces cerevisiae is not dependent on heme: purification and characterization of recombinant yeast cystathionine β-synthase, J. Inorg. Biochem. 81, 161-171.
28. Nozaki, T., Shigeta, Y., Saito-Nakano, Y., Imada, M., and Kruger, W. D. (2001) Characterization of transsulfuration and cysteine biosynthetic pathways in the protozoan hemoflagellate, Trypanosoma cruzi. Isolation and molecular characterization of cystathionine β-synthase and serine acetyltransferase from Trypanosoma, J. Biol. Chem. 276, 6516-6523.
29. Brochu, C., and Ouellette, M. Submitted (APR-2000) to the EMBL/GenBank/DDBJ databases.
30. Zehnder, A. J. B., and Wuhrmann, K. (1976) Titanium(III) citrate as a nontoxic oxidation-reduction buffering system for the culture of obligate anaerobes, Science 194, 1165-1166.
31. Bukovska, G., Kery, V., and Kraus, J. P. (1994) Expression of human cystathionine β-synthase in Escherichia coli: purification and characterization, Protein Expression Purif. 5, 442-448.
32. Lowry, O. H., Rosebrough, N. J., Fair, A. L., and Randall, R. J. (1951) Protein measurement with the Folin phenol reagent, J. Biol. Chem. 193, 265-275.
33. Morrison, M., and Horie, S. (1965) Determination of heme a concentration in cytochrome preparations by hemochromogen method, Anal. Biochem. 12, 77-82.
34. Kraus, J. P. (1987) Cystathionine β-synthase (human), Methods Enzymol. 143, 388-394.
35. Lukat-Rodgers, G. S., and Rodgers, K. R. (1997) Characterization of ferrous FixL-nitric oxide adducts by resonance Raman spectroscopy, Biochemistry 36, 4178-4187.
36. Dawson, R. M. C., Elliott, D. C., Elliot, W. H., and Jones, K. M. (1986) Amino acids, amines, amides, peptides, and their derivatives, Data for Biochemical Research, pp 1-31, Oxford Science Publications, Oxford, U.K.
37. Martell, A. E., and Smith, R. M. (1974) Critical Stability Constants, Vol. 1, Plenum Press, New York.
38. Benesch, R. E., and Benesch, R. (1955) The acid strength of the -SH group in cysteine and related compounds, J. Am. Chem. Soc. 77, 5877-5881.
39. Bayer, E., Hill, H. A. O., Roder, A., and Williams, R. J. P. (1969) The interaction between haem-iron and thiols, Chem. Commun. 109.
40. 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.
41. 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.
42. Lu, Y., Casimiro, D., Bren, K., Richards, J., and Gray, H. (1993) Structurally engineered cytochromes with unusual ligand-binding properties: expression of Saccharomyces cerevisiae Met-80 to Ala Iso-1- cytochrome c, Proc. Natl. Acad. Sci. U.S.A. 90, 11456-11459.
43. Thomson, A. J., Cheesman, M., and George, S. J. (1993) Variable-temperature magnetic circular dichroism, Methods Enzymol. 226, 199-232.
44. Johnson, M. K. (2000) CD and MCD spectroscopy, in Physical Methods in Bioinorganic Chemistry: Spectroscopy and Magnetism (Lawrence Que, J., Ed.) pp 233-285, University Science Books, Sausalito, CA.
45. Hu, S., Morris, I. K., Singh, J. P., Smith, K. M., and Spiro, T. G. (1993) Complete assignment of cytochrome c resonance Raman spectra via enzymatic reconstitution with isotopically labeled hemes, J. Am. Chem. Soc. 115, 12446-12458.
46. Green, E. L., Taoka, S., Banerjee, R., and Loehr, T. M. (2001) Resonance Raman characterization of the heme cofactor in cystathionine β-synthase. Identification of the Fe-S(Cys) vibration in the six-coordinate low-spin heme, Biochemistry 40, 459-463.
47. Walker, F. A. (1999) Magnetic spectroscopic (EPR, ESSEM, Mössbauer, MCD, and NMR) studies of low-spin ferriheme centers and their corresponding proteins, Coord. Chem. Rev. 185-186, 471-534.
48. Sono, M., Andersson, L. A., and Dawson, J. H. (1982) Sulfur donor ligand binding to ferric cytochrome P-450-CAM and myoglobin. Ultraviolet-visible absorption, magnetic circular dichroism, and electron paramagnetic resonance spectroscopic investigation of the complexes, J. Biol. Chem. 257, 8308-8320.
49. Dawson, J. H., Andersson, L. A., and Sono, M. (1983) The diverse spectroscopic properties of ferrous cytochrome P-450-CAM ligand complexes, J. Biol. Chem. 258, 13637-13645.
50. Taoka, S., Ohja, S., Shan, X., Kruger, W. D., and Banerjee, R. (1998) Evidence for heme-mediated redox regulation of human cystathionine β-synthase activity, J. Biol. Chem. 273, 25179-25184.
51. Taoka, S., Widjaja, L., and Banerjee, R. (1999) Assignment of enzymatic functions to specific regions of the PLP-dependent heme protein cystathionine β-synthase, Biochemistry 38, 13155-13161.
52. Cheesman, M. R., Greenwood, C., and Thomson, A. J. (1991) Magnetic circular dichroism of hemoproteins, in Advances in Inorganic Chemistry (Sykes, A. G., Ed.) pp 201-255, Academic Press, Orlando, FL.
53. cam, Biochim. Biophys. Acta 386, 87-98.
54. Taoka, S., and Banerjee, R. (2001) Characterization of NO binding to human cystathionine β-synthase: possible implications of the effects of CO and NO binding to the human enzyme, J. Inorg. Biochem. 87, 245-251.
55. Kery, V., Elleder, D., and Kraus, J. P. (1995) δ-Aminolevulinate increases heme saturation and yield of human cystathionine β-synthase expressed in Escherichia coli, Arch. Biochem. Biophys. 316, 24-29.
56. Ignarro, L. J., Degnan, J. N., Baricos, W. H., Kadowitz, P. J., and Wolin, M. S. (1982) Activation of purified guanylate cyclase by nitric oxide requires heme. Comparison of heme-deficient, heme-reconstituted and heme-containing forms of soluble enzyme from bovine lung, Biochim. Biophys. Acta 718, 49-59.
57. Craven, P. A., and DeRubertis, F. R. (1983) Requirement for heme in the activation of purified guanylate cyclase by nitric oxide, Biochim. Biophys. Acta 745, 310-321.
58. Yu, A. E., Hu, S., Spiro, T. G., and Burstyn, J. N. (1994) Resonance Raman spectroscopy of soluble guanylyl cyclase reveals displacement of distal and proximal heme ligands by NO, J. Am. Chem. Soc. 116, 4117-4118.
59. 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.
60. 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.
61. 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.
62. 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.
63. Rodgers, K. R., Lukat-Rodgers, G. S., and Barron, J. A. (1996) Structural basis for ligand discrimination and response initiation in the heme-based oxygen sensor FixL, Biochemistry 35, 9539-9548.
64. Tai, C.-H., Nalabolu, S. R., Simmons, J. W., Jacobson, T. M., and Cook, P. F. (1995) Acid-base chemical mechanism of O-acetylserine sulfhydrylases-A and -B from pH studies, Biochemistry 34, 12311-12322.
65. 2 complex. Effects of pH, isotopic substitution, and allosteric ligands, J. Biol. Chem. 274, 31189-31194.
66. Smulevich, G., Bjerrum, M. J., Gray, H. B., and Spiro, T. G. (1994) Resonance Raman spectra of the active site structure of semisynthetic Met80Cys horse heart cytochrome c, Inorg. Chem. 33, 4629-4634.
67. Blanke, S. R., Martinis, S. A., Sligar, S. G., and Hager, L. P. (1996) Probing the heme iron coordination structure of alkaline chloroperoxidase, Biochemistry 35, 14537-14543.
68. 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.
69. 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.
70. Perera, R., Sono, M., Sigman, J. A., Pfister, T. D., Lu, Y., and Dawson, J. H. (2003) Neutral thiol as a proximal ligand to ferrous heme iron: implications for the heme proteins that lose cysteine thiolate ligation on reduction, Proc. Natl. Acad. Sci. U.S.A. 100, 3641-3646.
71. 6), J. Am. Chem Soc. 97, 2048-2052.
72. 6 chemistry, Bioorg. Chem. 29, 234-257.