Redox regulation and reaction mechanism of human cystathionine-β- synthase: A PLP-dependent hemesensor protein

Archives of Biochemistry and Biophysics

Volumn 433, Issue 1, 2005, Pages 144-156

  Banerjee, Ruma ^a   Zou, Cheng Gang ^a  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

Cystathionine beta synthase; Heme; Homocysteine; Pyridoxal 5 phosphate; Reactive oxygen species

Indexed keywords

CYSTATHIONINE BETA SYNTHASE; HEMOPROTEIN;

CATALYSIS; CATALYST; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME MECHANISM; ENZYME REGULATION; HOMEOSTASIS; HUMAN; HYPERHOMOCYSTEINEMIA; MUTATION; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN MOTIF; SHORT SURVEY;

ALANINE; ALLOSTERIC REGULATION; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ANIMALS; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; CYSTATHIONINE BETA-SYNTHASE; DNA MUTATIONAL ANALYSIS; ENZYME ACTIVATION; HEME; HEMEPROTEINS; HUMANS; KINETICS; MODELS, CHEMICAL; MODELS, MOLECULAR; MODELS, STRUCTURAL; MOLECULAR SEQUENCE DATA; MOLECULAR STRUCTURE; MOLECULAR WEIGHT; OXIDATION-REDUCTION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; PYRIDOXAL PHOSPHATE; SEQUENCE HOMOLOGY, AMINO ACID; SUBSTRATE SPECIFICITY; THREONINE;

ANIMALIA; MAMMALIA;

EID: 9744276776     PISSN: 00039861     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.abb.2004.08.037     Document Type: Short Survey

References (69)

1. R. Banerjee, R. Evande, O. Kabil, S. Ojha, and S. Taoka Reaction mechanism and regulation of cystathionine beta-synthase Biochim. Biophys. Acta 1647 2003 30 35
2. E.W. Miles, and J.P. Kraus Cystathionine {beta}-synthase: structure, function, regulation, and location of homocystinuria-causing mutations J. Biol. Chem. 279 2004 29871 29874
3. J.D. Finkelstein, W.E. Kyle, J.J. Martin, and A.-M. Pick Activation of cystathionine β-synthase by adenosylmethionine and adenosylethionine Biochem. Biophys. Res. Commun. 66 1975 81 87
4. M.H. Stipanuk Sulfur amino acid metabolism: pathways for production and removal of homocysteine and cysteine Annu. Rev. Nutr. 24 2004 539 577
5. S.H. Mudd, H.L. Levy, and F. Skovby The Metabolic and Molecular Basis of Inherited Diseases 1995 McGraw-Hill New York
6. J.P. Kraus, M. Janosik, V. Kozich, R. Mandell, V. Shih, M.P. Sperandeo, G. Sebastio, R. de Franchis, G. Andria, L.A. Kluijtmans, H. Blom, G.H. Boers, R.B. Gordon, P. Kamoun, M.Y. Tsai, W.D. Kruger, H.G. Koch, T. Ohura, and M. Gaustadnes Cystathionine beta-synthase mutations in homocystinuria Hum. Mutat. 13 1999 362 375
7. J.P. Kraus, C.L. Williamson, F.A. Firgaira, T.L. Yang-Feng, M. Münke, U. Francke, G. Bukovska, and L.E. Rosenberg Cloning and sequencing nanogram amounts of immunopurified mRNA's: cDNA cloning and chromosomal mappingof cystathionine β-synthase and the β subunit of propionyl CoA carboxylase Proc. Natl. Acad. Sci. USA 83 1986 2047 2051
8. S. Taoka, L. Widjaja, and R. Banerjee Assignment of enzymatic functions to specific regions of the PLP-dependent hemeprotein cystathionine β-synthase Biochemistry 38 1999 13155 13161
9. X. Shan, and W.D. Kruger Correction of disease causing CBS mutations in yeast Nat. Genet. 19 1998 91 93
10. V. Kery, L. Poneleit, and J. Kraus Trypsin cleavage of human cystathionine beta-synthase into an evolutionarily conserved active core: structural and functional consequences Arch. Biochem. Biophys. 355 1998 222 232
11. F.W. Alexander, E. Sandmeier, P.K. Mehta, and P. Christen Evolutionary relationships among pyridoxal-5′-phosphate-dependent enzymes. Regio-specific alpha, beta and gamma families Eur. J. Biochem. 219 1994 953 960
12. N.V. Grishin, M.A. Phillips, and E.J. Goldsmith Modeling of the spatial structure of eukaryotic ornithine decarboxylases Protein Sci. 4 1995 1291 1304
13. V. Kery, G. Bukovska, and J.P. Kraus Transsulfuration depends on heme in addition to pyridoxal 5′-phosphate. Cystathionine β-synthase is a heme protein J. Biol. Chem. 269 1994 25283 25288
14. K.H. Jhee, P. McPhie, and E.W. Miles Yeast cystathionine beta-synthase is a pyridoxal phosphate enzyme but, unlike the human enzyme, is not a heme protein J. Biol. Chem. 275 2000 11541 11544
15. T. Nozaki, Y. Shigeta, Y. Saito-Nakano, M. Imada, and W.D. Kruger Characterization of transsulfuration and cysteine biosynthetic pathways in the protozoan hemoflagellate, Trypanosoma cruzi. Isolation and molecular characterization of cystathionine beta-synthase and serine acetyltransferase from Trypanosoma J. Biol. Chem. 276 2001 6516 6523
16. R. Evande, S. Ojha, and R. Banerjee Visualization of PLP-bound intermediates in hemeless variants of human cystathionine beta-synthase: evidence that lysine 119 is a general base Arch. Biochem. Biophys. 427 2004 188 196
17. A. Bateman The structure of a domain common to archaebacteria and the homocystinuria disease protein Trends Biochem. Sci. 22 1997 12 13
18. J.W. Scott, S.A. Hawley, K.A. Green, M. Anis, G. Stewart, G.A. Scullion, D.G. Norman, and D.G. Hardie CBS domains form energy-sensing modules whose binding of adenosine ligands is disrupted by disease mutations J. Clin. Invest. 113 2004 274 284
19. X. Shan, R.L. Dunbrack Jr., S.A. Christopher, and W.D. Kruger Mutations in the regulatory domain of cystathionine beta synthase can functionally suppress patient-derived mutations in cis Hum. Mol. Genet. 10 2001 635 643
20. M. Meier, M. Janosik, V. Kery, J.P. Kraus, and P. Burkhard Structure of human cystathionine beta-synthase: a unique pyridoxal 5′-phosphate- dependent heme protein EMBO J. 20 2001 3910 3916
21. S. Taoka, B.W. Lepore, Kabil, Ö., S. Ojha, D. Ringe, and R. Banerjee Human cystathionine beta-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 2002 10454 10461
22. V. Kery, L. Poneleit, J.D. Meyer, M.C. Manning, and J.P. Kraus Binding of pyridoxal 5-'phosphate to the heme protein human cystathionine beta synthase Biochemistry 38 1999 2710 2724
23. K.H. Jhee, P. McPhie, and E.W. Miles Domain architecture of the heme-independent yeast cystathionine beta-synthase provides insights into mechanisms of catalysis and regulation Biochemistry 39 2000 10548 10556
24. 31P NMR and pulsed EPR spectroscopy that the heme and the PLP cofactors are not proximal in the human enzyme J. Biol. Chem. 276 2001 19350 19355
25. S. Taoka, S. Ohja, X. Shan, W.D. Kruger, and R. Banerjee Evidence for heme-mediated redox regulation of human cystathionine β-synthase activity J. Biol. Chem. 273 1998 25179 25184
26. S. Ojha, J. Hwang, O. Kabil, J.E. Penner-Hahn, and R. Banerjee Characterization of the heme in human cystathionine beta-synthase by X- ray absorption and electron paramagnetic resonance spectroscopies Biochemistry 39 2000 10542 10547
27. S. Taoka, E.L. Green, T.M. Loehr, and R. Banerjee Mercuric chloride-induced spin or ligation state changes in ferric or ferrous human cystathionine b-synthase inhibit enzyme activity J. Inorg. Bioc. 87 2001 253 259
28. E.L. Green, S. Taoka, R. Banerjee, and T.M. Loehr Resonance Raman characterization of the heme cofactor in cystathionine beta-synthase. identification of the Fe-S(Cys) vibration in the six- coordinate low-spin heme Biochemistry 40 2001 459 463
29. S. Taoka, M. West, and R. Banerjee Characterization of the heme and pyridoxal phosphate cofactors of human cystathionine beta synthase reveals nonequivalent active sites Biochemistry 38 1999 2738 2744
30. E.M. Dioum, J. Rutter, J.R. Tuckerman, G. Gonzalez, M.A. Gilles-Gonzalez, and S.L. McKnight NPAS2: a gas-responsive transcription factor Science 298 2002 2385 2387
31. T. Ingi, G. Chiang, and G.V. Ronnett The regulation of heme turnover and carbon monoxide biosynthesis in cultured primary rat olfactory receptor neurons J. Neurosci. 16 1996 5621 5628
32. M. Puranik, S.B. Nielsen, H. Youn, A.N. Hvitved, J.L. Bourassa, M.A. Case, C. Tengroth, G. Balakrishnan, M.V. Thorsteinsson, J.T. Groves, G.L. McLendon, G.P. Roberts, J.S. Olson, and T.G. Spiro Dynamics of carbon monoxide binding to CooA J. Biol. Chem. 279 2004 21096 21108
33. S. Taoka, and R. Banerjee Activity of human cystathionine beta synthase is regulated by CO and NO: possible role for the hemeprotein in CO sensing J. Inorg. Bioc. 87 2001 245 251
34. S. Vadon-Le Goff, M. Delaforge, J.L. Boucher, M. Janosik, J.P. Kraus, and D. Mansuy Coordination chemistry of the heme in cystathionine beta-synthase: formation of iron(II)-isonitrile complexes Biochem. Biophys. Res. Commun. 283 2001 487 492
35. S. Ojha, J. Wu, R. LoBrutto, and R. Banerjee Effects of heme ligand mutations including a pathogenic variant, H65R, on the properties of human cystathionine beta syntase Biochemistry 41 2002 4649 4654
36. J. Oliveriusova, V. Kery, K.N. Maclean, and J.P. Kraus Deletion mutagenesis of human cystathionine beta-synthase. Impact on activity, oligomeric status, and S-adenosylmethionine regulation J. Biol. Chem. 277 2002 48386 48394
37. S. Daum, C.H. Tai, and P.F. Cook Characterization of the S272A,D site-directed mutations of O-acetylserine sulfhydrylase: involvement of the pyridine ring in the alpha,beta-elimination reaction Biochemistry 42 2003 106 113
38. K.H. Jhee, P. McPhie, H.S. Ro, and E.W. Miles Tryptophan synthase mutations that alter cofactor chemistry lead to mechanism-based inactivation Biochemistry 37 1998 14591 14604
39. K.H. Jhee, L.H. Yang, S.A. Ahmed, P. McPhie, R. Rowlett, and E.W. Miles Mutation of an active site residue of tryptophan synthase (beta-serine 377) alters cofactor chemistry J. Biol. Chem. 273 1998 11417 11422
40. K.H. Jhee, D. Niks, P. McPhie, M.F. Dunn, and E.W. Miles The reaction of yeast cystathionine beta-synthase is rate-limited by the conversion of aminoacrylate to cystathionine Biochemistry 40 2001 10873 10880
41. S. Taoka, and R. Banerjee Stopped-flow kinetic analysis of the reaction catalyzed by the full length yeast cystathionine beta synthase J. Biol. Chem. 277 2002 22421 22425
42. E. Borcsok, and R.H. Abeles Mechanism of action of cystathionine synthase Arch. Biochem. Biophys. 213 1982 695 707
43. M.V. Martinov, V.M. Vitvitsky, E.V. Mosharov, R. Banerjee, and F.I. Ataullakhanov A substrate switch: A new mode of regulation in the methionine metabolic pathway J. Theor. Biol. 204 2000 521 532
44. J.D. Finkelstein, and J.J. Martin Methionine metabolism in mammals. Distribution of homocysteine between competing pathways J. Biol. Chem. 259 1984 9508 9513
45. W.M. Rabeh, and P.F. Cook Structure and mechanism of O-acetylserine sulfhydrylase J. Biol. Chem. 279 2004 26803 26806
46. P. Burkhard, C.H. Tai, C.M. Ristroph, P.F. Cook, and J.N. Jansonius Ligand binding induces a large conformational change in O-acetylserine sulfhydrylase from Salmonella typhimurium J Mol Biol 291 1999 941 953
47. S.M. Aitken, and J.F. Kirsch Role of active-site residues Thr81, Ser82, Thr85, Gln157, and Tyr158 in yeast cystathionine beta-synthase catalysis and reaction specificity Biochemistry 43 2004 1963 1971
48. S. Bruno, F. Schiaretti, P. Burkhard, J.P. Kraus, M. Janosik, and A. Mozzarelli Functional properties of the active core of human cystathionine beta-synthase crystals J. Biol. Chem. 276 2001 16 19
49. S.M. Aitken, and J.F. Kirsch Kinetics of the yeast cystathionine beta-synthase forward and reverse reactions: continuous assays and the equilibrium constant for the reaction Biochemistry 42 2003 571 578
50. K.H. Jhee, D. Niks, P. McPhie, M.F. Dunn, and E.W. Miles Yeast cystathionine beta-synthase reacts with l-allothreonine, a non-natural substrate, and l-homocysteine to form a new amino acid, 3-methyl-l-cystathionine Biochemistry 41 2002 1828 1835
51. H. Kimura Hydrogen sulfide as a neuromodulator Mol. Neurobiol. 26 2002 13 19
52. K. Eto, and H. Kimura A novel enhancing mechanism for hydrogen sulfide-producing activity of cystathionine beta-synthase J. Biol. Chem. 277 2002 42680 42685
53. M.D. Sintchak, M.A. Fleming, O. Futer, S.A. Raybuck, S.P. Chambers, P.R. Caron, M.A. Murcko, and K.P. Wilson Structure and mechanism of inosine monophosphate dehydrogenase in complex with the immunosuppressant mycophenolic acid Cell 85 1996 921 930
54. R. Evande, G.H.J. Boers, H.J. Blom, and R. Banerjee Alleviation of intrasteric inhibition by the pathogenic activation domain mutation, D444N, in human cystathionine beta-synthase Biochemistry 41 2002 11832 11837
55. O. Kabil, and R. Banerjee Deletion of the regulatory domain in the pyridoxal phosphate-dependent heme protein cystathionine beta-synthase alleviates the defect observed in a catalytic site mutant J. Biol. Chem. 274 1999 31256 31260
56. M. Janosik, V. Kery, M. Gaustadnes, K.N. Maclean, and J.P. Kraus Regulation of human cystathionine beta-synthase by S-adenosyl-l-methionine: evidence for two catalytically active conformations involving an autoinhibitory domain in the C-terminal region Biochemistry 40 2001 10625 10633
57. M. Janosik, J. Oliveriusova, B. Janosikova, J. Sokolova, E. Kraus, J.P. Kraus, and V. Kozich Impaired heme binding and aggregation of mutant cystathionine beta-synthase subunits in homocystinuria Am. J. Hum. Genet. 68 2001 1506 1513
58. Kluitjmans L.A.J., G.H.J. Boers., E.M.B. Stevens, E.M.B. Renie, W.O. Kraus, J.P. Trijbels, F.J.M. Heuvel, L.P.W.J. v. d., and Blom H.J. Defective cystathionine beta-synthase regulation by S-adenosylmethionine in a partially pyridoxine responsive homocystinuria J. Clin. Invest. 98 1996 285 289
59. A. Prudova, M.V. Martinov, V. Vitvitsky, F. Ataullakhanov, R. Banerjee, Analysis of pathological defects in methionine metabolism using a simple mathematical model (submitted for publication)
60. C.-K. Lee, R.G. Klopp, R. Weindruch, and T.A. Prolla Gene expression profile of aging and its retardation by caloric restriction Science 285 1999 1390 1393
61. E. Mosharov, M.R. Cranford, and R. Banerjee The quantitatively important relationship between homocysteine metabolism and glutathione synthesis by the transsulfuration pathway and its regulation by redox changes Biochemistry 39 2000 13005 13011
62. Zou, C.-G. and, and R. Banerjee Tumor necrosis factor-a-induced targeted proteolysis of cystathionine beta-synthase modulates redox homeostasis J. Biol. Chem. 278 2003 16802 16808
63. V. Vitvitsky, E. Mosharov, M. Tritt, F. Ataullakhanov, and R. Banerjee Redox regulation of homocysteine-dependent glutathione synthesis Redox Rep. 8 2003 56 63
64. V. Vitvitsky, S. Dayal, S. Stabler, Y. Zhou, H. Wang, S.R. Lentz, R. Banerjee, Perturbations in homocysteine-linked redox homeostasis in a murine model for hyperhomocysteinemia, Am. J. Physiol. Regul. Integr. Comp. Physiol. 287, R39-46
65. A. Meister Metabolism and Transport of Glutathione and Other γ-Glutamyl Compounds 1983 Raven Press New York
66. A. Meister Glutathione metabolism Methods Enzymol. 251 1995 3 7
67. P.W. Beatty, and D.J. Reed Involvement of the cystathionine pathway in the biosynthesis of glutathione by isolated rat hepatocytes Arch. Biochem. Biophys. 204 1980 80 87
68. S.C. Lu, Y. Bao, Z.Z. Huang, V.P. Sarthy, and R. Kannan Regulation of gamma-glutamylcysteine synthetase subunit gene expression in retinal Muller cells by oxidative stress Invest. Ophthalmol. Vis. Sci. 40 1999 1776 1782
69. S.C. Lu Regulation of glutathione synthesis Curr. Top. Cell Regul. 36 2000 95 116