Cross-talk between the catalytic core and the regulatory domain in cystathionine β-synthase: Study by differential covalent labeling and computational modeling

Biochemistry

Volumn 49, Issue 49, 2010, Pages 10526-10534

  Hnízda, Aleš ^a   Spiwok, Vojtěch ^b   Jurga, Vojtěch ^b   Kožich, Viktor ^a   Kodíček, Milan ^b   Kraus, Jan P ^c  

^a Charles University in Prague and General University Hospital in Prague   (Czech Republic)

^b INSTITUTE OF CHEMICAL TECHNOLOGY   (Czech Republic)

^c Children's Hospital Colorado   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOSTERIC MECHANISMS; ALLOSTERY; ATOMIC MECHANISM; AUTOINHIBITION; CATALYTIC CORE; COMPUTATIONAL MODELING; CONFORMATIONAL CONVERSION; CONFORMATIONAL STABILITIES; CONTACT AREAS; COVALENT LABELING; FULL-LENGTH ENZYMES; HOMOCYSTEINES; MODIFICATION AGENT; MODULAR ENZYMES; REACTIVE SITE; REGULATORY DOMAIN; S ADENOSYL L METHIONINES; SIDE CHAINS; SIDE-CHAIN; SYNTHASES; THERMAL ACTIVATION; THERMOLYSIN; UREA GRADIENT;

AMINO ACIDS; CROSSTALK; CRYSTAL STRUCTURE; ENZYME ACTIVITY; ENZYMES; MASS SPECTROMETRY; UREA;

ELECTRIC CIRCUIT BREAKERS;

4 HYDROXYPHENYLGLYOXAL; ACETIC ACID; ARGININE DECARBOXYLASE; CYSTATHIONINE BETA SYNTHASE; DIETHYL PYROCARBONATE; N ACETYLIMIDAZOLE; N BROMOSUCCINIMIDE; N ETHYLMALEIMIDE; S ADENOSYLMETHIONINE; SULFO N HYDROXYSUCCINIMIDO ACETATE; UNCLASSIFIED DRUG;

ALLOSTERISM; ARTICLE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CONCENTRATION (PARAMETERS); COVALENT BOND; ENZYME ACTIVITY; MASS SPECTROMETRY; MATHEMATICAL MODEL; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN STRUCTURE; THERMAL ANALYSIS;

ALLOSTERIC SITE; CATALYTIC DOMAIN; COMPUTATIONAL BIOLOGY; CRYSTALLOGRAPHY, X-RAY; CYSTATHIONINE BETA-SYNTHASE; HUMANS; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; PROTEIN CONFORMATION; PROTEIN STRUCTURE, TERTIARY; RECEPTOR CROSS-TALK;

EID: 78650101391     PISSN: 00062960     EISSN: 15204995     Source Type: Journal    
DOI: 10.1021/bi101384m     Document Type: Article

References (54)

1. Mudd, S. H., Finkelstein, J. D., Irreverre, F., and Laster, L. (1965) Threonine dehydratase activity in humans lacking cystathionine synthase Biochem. Biophys. Res. Commun. 19, 665-670
2. Oliveriusova, J., Kery, V., Maclean, K. N., and Kraus, J. P. (2002) Deletion mutagenesis of human cystathionine beta-synthase. Impact on activity, oligomeric status, and S-adenosylmethionine regulation J. Biol. Chem. 277, 48386-48394
3. Janosik, M., Kery, V., Gaustadnes, M., Maclean, K. N., and Kraus, J. P. (2001) 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, 10625-10633
4. Kery, V., Poneleit, L., and Kraus, J. P. (1998) Trypsin cleavage of human cystathionine beta-synthase into an evolutionarily conserved active core: structural and functional consequences Arch. Biochem. Biophys. 355, 222-232
5. Frank, N., Kery, V., Maclean, K. N., and Kraus, J. P. (2006) Solvent-accessible cysteines in human cystathionine beta-synthase: crucial role of cysteine 431 in S -adenosyl- l -methionine binding Biochemistry 45, 11021-11029
6. Skovby, F., Kraus, J. P., and Rosenberg, L. E. (1984) Biosynthesis and proteolytic activation of cystathionine beta-synthase in rat liver J. Biol. Chem. 259, 588-593
7. Zou, C. G. and Banerjee, R. (2003) Tumor necrosis factor-alpha-induced targeted proteolysis of cystathionine beta-synthase modulates redox homeostasis J. Biol. Chem. 278, 16802-16808
8. Meier, M., Janosik, M., Kery, V., Kraus, J. P., and Burkhard, P. (2001) Structure of human cystathionine beta-synthase: a unique pyridoxal 5′-phosphate-dependent heme protein EMBO J. 20, 3910-3916
9. Taoka, S., Lepore, B. W., Kabil, O., Ojha, S., Ringe, D., and Banerjee, R. (2002) 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, 10454-10461
10. Sen, S., Yu, J., Yamanishi, M., Schellhorn, D., and Banerjee, R. (2005) Mapping peptides correlated with transmission of intrasteric inhibition and allosteric activation in human cystathionine beta-synthase Biochemistry 44, 14210-14216
11. Suckau, D., Mak, M., and Przybylski, M. (1992) Protein surface topology-probing by selective chemical modification and mass spectrometric peptide mapping Proc. Natl. Acad. Sci. U.S.A. 89, 5630-5634
12. Mendoza, V. L. and Vachet, R. W. (2009) Probing protein structure by amino acid-specific covalent labeling and mass spectrometry Mass Spectrom. Rev. 28, 785-815
13. 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 beta-synthase: an enzyme involved in vascular disease Acta Crystallogr., Sect. D: Biol. Crystallogr. 57, 289-291
14. Frank, N., Kent, J. O., Meier, M., and Kraus, J. P. (2008) Purification and characterization of the wild type and truncated human cystathionine beta-synthase enzymes expressed in E. coli Arch. Biochem. Biophys. 470, 64-72
15. Park, C. and Marqusee, S. (2005) Pulse proteolysis: a simple method for quantitative determination of protein stability and ligand binding Nat. Methods 2, 207-212
16. Prudova, A., Bauman, Z., Braun, A., Vitvitsky, V., Lu, S. C., and Banerjee, R. (2006) S-adenosylmethionine stabilizes cystathionine beta-synthase and modulates redox capacity Proc. Natl. Acad. Sci. U.S.A. 103, 6489-6494
17. Park, C. and Marqusee, S. (2004) Probing the high energy states in proteins by proteolysis J. Mol. Biol. 343, 1467-1476
18. Hnizda, A., Santrucek, J., Sanda, M., Strohalm, M., and Kodicek, M. (2008) Reactivity of histidine and lysine side-chains with diethylpyrocarbonate- a method to identify surface exposed residues in proteins J. Biochem. Biophys. Methods 70, 1091-1097
19. + oxidoreductase Arch. Biochem. Biophys. 320, 280-288
20. Hubalek, F., Pohl, J., and Edmondson, D. E. (2003) Structural comparison of human monoamine oxidases A and B: mass spectrometry monitoring of cysteine reactivities J. Biol. Chem. 278, 28612-28618
21. Wells, I. and Marnett, L. J. (1992) Acetylation of prostaglandin endoperoxide synthase by N -acetylimidazole: comparison to acetylation by aspirin Biochemistry 31, 9520-9525
22. Gabant, G., Augier, J., and Armengaud, J. (2008) Assessment of solvent residues accessibility using three sulfo-NHS-biotin reagents in parallel: application to footprint changes of a methyltransferase upon binding its substrate J. Mass Spectrom. 43, 360-370
23. Carven, G. J. and Stern, L. J. (2005) Probing the ligand-induced conformational change in HLA-DR1 by selective chemical modification and mass spectrometric mapping Biochemistry 44, 13625-13637
24. Kozich, V. and Kraus, J. P. (1992) Screening for mutations by expressing patient cDNA segments in E. coli: homocystinuria due to cystathionine beta-synthase deficiency Hum. Mutat. 1, 113-123
25. Biringer, R. G., Amato, H., Harrington, M. G., Fonteh, A. N., Riggins, J. N., and Huhmer, A. F. (2006) Enhanced sequence coverage of proteins in human cerebrospinal fluid using multiple enzymatic digestion and linear ion trap LC-MS/MS Briefings Funct. Genomics Proteomics 5, 144-153
26. Strohalm, M., Hassman, M., Kosata, B., and Kodicek, M. (2008) mMass data miner: an open source alternative for mass spectrometric data analysis Rapid Commun. Mass Spectrom. 22, 905-908
27. Turner, B. T., Jr., Sabo, T. M., Wilding, D., and Maurer, M. C. (2004) Mapping of factor XIII solvent accessibility as a function of activation state using chemical modification methods Biochemistry 43, 9755-9765
28. Perdivara, I., Deterding, L. J., Przybylski, M., and Tomer, K. B. (2010) Mass spectrometric identification of oxidative modifications of tryptophan residues in proteins: chemical artifact or post-translational modification? J. Am. Soc. Mass Spectrom. 21, 1114-1117
29. Sharp, J. S., Becker, J. M., and Hettich, R. L. (2004) Analysis of protein solvent accessible surfaces by photochemical oxidation and mass spectrometry Anal. Chem. 76, 672-683
30. Sali, A. and Blundell, T. L. (1993) Comparative protein modelling by satisfaction of spatial restraints J. Mol. Biol. 234, 779-815
31. Lucas, M., Encinar, J. A., Arribas, E. A., Oyenarte, I., Garcia, I. G., Kortazar, D., Fernandez, J. A., Mato, J. M., Martinez-Chantar, M. L., and Martinez-Cruz, L. A. (2010) Binding of S-methyl-5′-thioadenosine and S-adenosyl- l -methionine to protein MJ0100 triggers an open-to-closed conformational change in its CBS motif pair J. Mol. Biol. 396, 800-820
32. Kelley, L. A. and Sternberg, M. J. (2009) Protein structure prediction on the Web: a case study using the Phyre server Nat. Protoc. 4, 363-371
33. Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W., and Lipman, D. J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Nucleic Acids Res. 25, 3389-3402
34. Sippl, M. J. (1993) Recognition of errors in three-dimensional structures of proteins Proteins 17, 355-362
35. Halabi, N., Rivoire, O., Leibler, S., and Ranganathan, R. (2009) Protein sectors: evolutionary units of three-dimensional structure Cell 138, 774-786
36. Finn, R. D., Mistry, J., Tate, J., Coggill, P., Heger, A., Pollington, J. E., Gavin, O. L., Gunasekaran, P., Ceric, G., Forslund, K., Holm, L., Sonnhammer, E. L., Eddy, S. R., and Bateman, A. (2010) The Pfam protein families database Nucleic Acids Res. 38, D211-D222
37. Chen, R., Li, L., and Weng, Z. (2003) ZDOCK: an initial-stage protein-docking algorithm Proteins 52, 80-87
38. Evande, R., Blom, H., Boers, G. H., and Banerjee, R. (2002) Alleviation of intrasteric inhibition by the pathogenic activation domain mutation, D444N, in human cystathionine beta-synthase Biochemistry 41, 11832-11837
39. Mendoza, V. L. and Vachet, R. W. (2008) Protein surface mapping using diethylpyrocarbonate with mass spectrometric detection Anal. Chem. 80, 2895-2904
40. Kvaratskhelia, M., Miller, J. T., Budihas, S. R., Pannell, L. K., and Le Grice, S. F. (2002) Identification of specific HIV-1 reverse transcriptase contacts to the viral RNA:tRNA complex by mass spectrometry and a primary amine selective reagent Proc. Natl. Acad. Sci. U.S.A. 99, 15988-15993
41. Blair, L. P., Tackett, A. J., and Raney, K. D. (2009) Development and evaluation of a structural model for SF1B helicase Dda Biochemistry 48, 2321-2329
42. Leitner, A. and Lindner, W. (2005) Effect of an arginine-selective tagging procedure on the fragmentation behavior of peptides studied by electrospray ionization tandem mass spectrometry (ESI-MS/MS) Anal. Chim. Acta 528, 165-173
43. Ignoul, S. and Eggermont, J. (2005) CBS domains: structure, function, and pathology in human proteins Am. J. Physiol. 289, C1369-C1378
44. Meier, M., Oliveriusova, J., Kraus, J. P., and Burkhard, P. (2003) Structural insights into mutations of cystathionine beta-synthase Biochim. Biophys. Acta 1647, 206-213
45. Urreizti, R., Asteggiano, C., Cozar, M., Frank, N., Vilaseca, M. A., Grinberg, D., and Balcells, S. (2006) Functional assays testing pathogenicity of 14 cystathionine-beta synthase mutations Hum. Mutat. 27, 211
46. Majtan, T., Liu, L., Carpenter, J. F., and Kraus, J. P. (2010) Rescue of cystathionine beta-synthase (CBS) mutants with chemical chaperones: purification and characterization of eight CBS mutant enzymes J. Biol. Chem. 21, 15866-15873
47. Kozich, V., Sokolova, J., Klatovska, V., Krijt, J., Janosik, M., Jelinek, K., and Kraus, J. P. (2010) Cystathionine beta-synthase mutations: effect of mutation topology on folding and activity Hum. Mutat. 7, 809-819
48. Sen, S. and Banerjee, R. (2007) A pathogenic linked mutation in the catalytic core of human cystathionine beta-synthase disrupts allosteric regulation and allows kinetic characterization of a full-length dimer Biochemistry 46, 4110-4116
49. Tsai, C. J., del Sol, A., and Nussinov, R. (2008) Allostery: absence of a change in shape does not imply that allostery is not at play J. Mol. Biol. 378, 1-11
50. Kern, D. and Zuiderweg, E. R. (2003) The role of dynamics in allosteric regulation Curr. Opin. Struct. Biol. 13, 748-757
51. Laskowski, R. A., Gerick, F., and Thornton, J. M. (2009) The structural basis of allosteric regulation in proteins FEBS Lett. 583, 1692-1698
52. Goodey, N. M. and Benkovic, S. J. (2008) Allosteric regulation and catalysis emerge via a common route Nat. Chem. Biol. 4, 474-482
53. Singh, S., Madzelan, P., and Banerjee, R. (2007) Properties of an unusual heme cofactor in PLP-dependent cystathionine beta-synthase Nat. Prod. Rep. 24, 631-639
54. Yamanishi, M., Kabil, O., Sen, S., and Banerjee, R. (2006) Structural insights into pathogenic mutations in heme-dependent cystathionine-beta-synthase J. Inorg. Biochem. 100, 1988-1995