The cysteine regulatory complex from plants and microbes: What was old is new again

Current Opinion in Structural Biology

Volumn 23, Issue 2, 2013, Pages 302-310

  Jez, Joseph M ^a   Dey, Sanghamitra ^a  

^a WASHINGTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYSTEINE; CYSTEINE REGULATORY COMPLEX; CYSTEINE SYNTHASE; MULTIENZYME COMPLEX; SERINE ACETYLTRANSFERASE; SULFUR; UNCLASSIFIED DRUG;

AMINO ACID SYNTHESIS; BIOPHYSICS; BIOTECHNOLOGY; CATALYSIS; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME CHEMISTRY; ENZYME KINETICS; ENZYME MODIFICATION; ENZYME REGULATION; ENZYME SPECIFICITY; ENZYME STRUCTURE; MACROMOLECULE; MICROBIAL METABOLISM; NONHUMAN; NUTRIENT AVAILABILITY; PLANT METABOLISM; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FAMILY; REVIEW;

BACTERIA; CYSTEINE; CYSTEINE SYNTHASE; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; PLANTS; PROTEIN BINDING; PROTEIN CONFORMATION; SERINE O-ACETYLTRANSFERASE;

EID: 84878606886     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2013.02.011     Document Type: Review

References (72)

1. Winkel B.S. Metabolic channeling in plants. Annu Rev Plant Biol 2004, 55:85-107.
2. Sun M., Leyh T.S. Channeling in sulfate activating complexes. Biochemistry 2006, 45:11304-11311.
3. Zhang Y., Li S.Z., Li J., Pan X., Cahoon R.E., Jaworski J.G., Wang X., Jez J.M., Chen F., Yu O. Using unnatural protein fusions to engineer resveratrol biosynthesis in yeast and mammalian cells. J Am Chem Soc 2006, 128:13030-13031.
4. Dueber J.E., Wu G.C., Malmirchegini G.R., Moon T.S., Petzold C.J., Ullal A.V., Prather K.L., Keasling J.D. Synthetic protein scaffolds provide modular control over metabolic flux. Nat Biotech 2009, 27:753-759.
5. Moon T.S., Dueber J.E., Shiue E., Prather K.L. Use of modular, synthetic scaffolds for improved production of glucaric acid in engineered E. coli. Metab Eng 2010, 12:298-305.
6. Wang Y., Yi H., Wang M., Yu O., Jez J.M. Structural and kinetic analysis of the unnatural fusion protein 4-coumaroyl-CoA ligase::stilbene synthase. J Am Chem Soc 2011, 133:20684-20687.
7. Kredich N.M., Becker M.A., Tomkins G.M. Purification and characterization of cysteine synthetase, a bifunctional protein complex, from Salmonella typhimurium. J Biol Chem 1969, 244:2428-2439.
8. Becker M.A., Tomkins G.M. Pleiotrophy in a cysteine-requiring mutant of Salmonella typhimurium resulting from altered protein-protein interaction. J Biol Chem 1969, 244:6023-6030.
9. Cook P.F., Wedding R.T. Initial kinetic characterization of the multienzyme complex, cysteine synthetase. Arch Biochem Biophys 1977, 178:293-302.
10. Yi H., Galant A., Ravilious G.E., Preuss M.L., Jez J.M. Sensing sulfur conditions: simple to complex biochemical regulatory mechanisms in plant thiol metabolism. Mol Plant 2010, 3:269-279.
11. Yi H., Ravilious G.E., Galant A., Krishnan H.B., Jez J.M. Thiol metabolism in soybean: sulfur to homoglutathione. Amino Acids 2010, 39:963-978.
12. Olsen L.R., Huang B., Vetting M.W., Roderick S.L. Structure of serine acetyltransferase in complexes with CoA and its cysteine feedback inhibitor. Biochemistry 2004, 43:6013-6019.
13. Pye V.E., Tingey A.P., Robson R.L., Moody P.C. The structure and mechanism of serine acetyltransferase from Escherichia coli. J Biol Chem 2004, 279:40729-40736.
14. Gorman J., Shapiro L. Structure of serine acetyltransferase from Haemophilus influenzae Rd. Acta Crystallogr D 2004, 60:1600-1605.
15. Kumar S., Raj I., Nagpal I., Subbarao N., Gourinath S. Structural and biochemical studies of serine acetyltransferase reveal why the parasite Entamoeba histolytica cannot form a cysteine synthase complex. J Biol Chem 2011, 286:12533-12541.
16. Guan R., Roderick S.L., Huang B., Cook P.F. Roles of histidines 154 and 189 and aspartate 139 in the active site of serine acetyltransferase from Haemophilus influenzae. Biochemistry 2008, 47:6322-6328.
17. Rabeh W.M., Cook P.F. Structure and mechanism of O-acetylserine sulfhydrylase. J Biol Chem 2004, 279:26803-26806.
18. Burkhard P., Rao G.S., Hohenester E., Schnackerz K.D., Cook P.F., Jansonius J.N. Three-dimensional structure of O-acetylserine sulfhydrylase from Salmonella typhimurium. J Mol Biol 1998, 283:121-133.
19. Burkhard P., Tai C.H., Ristroph C.M., Cook P.F., Jansonius J.N. Ligand binding induces a large conformational change in O-acetylserine sulfhydrylase from Salmonella typhimurium. J Mol Biol 1999, 291:941-953.
20. Bonner E.R., Cahoon R.E., Knapke S.M., Jez J.M. Molecular basis of cysteine biosynthesis in plants: structural and functional analysis of O-acetylserine sulfhydrylase from Arabidopsis thaliana. J Biol Chem 2005, 280:38803-38813.
21. Banerjee S., Ekka M.K., Kumaran S. Comparative thermodynamic studies on substrate and product binding of O-acetylserine sulfhydrylase reveals two different ligand recognition modes. BMC Biochem 2011, 12:31.
22. Claus M.T., Zocher G.E., Maier T.H., Schulz G.E. Structure of the O-acetylserine sulfhydrylase isoenzyme CysM from Escherichia coli. Biochemistry 2005, 44:8620-8626.
23. Zocher G., Wiesand U., Schulz G.E. High resolution structure and catalysis of O-acetylserine sulfhydrylase isozyme B from Escherichia coli. FEBS J 2007, 274:5382-5389.
24. Chattopadhyay A., Meier M., Ivaninskii S., Burkhard P., Speroni F., Campanini B., Bettati S., Mozzarelli A., Rabeh W.M., Li L., Cook P.F. Structure, mechanism, and conformational dynamics of O-acetylserine sulfhydrylase from Salmonella typhimurium: comparison of A and B isozymes. Biochemistry 2007, 46:8315-8330.
25. Schnell R., Oehlmann W., Singh M., Schneider G. Structural insights into catalysis and inhibition of O-acetylserine sulfhydrylase from Mycobacterium tuberculosis: crystal structures of the enzyme alpha-aminoacrylate intermediate and an enzyme-inhibitor complex. J Biol Chem 2007, 282:23473-23481.
26. Watanabe M., Kusano M., Oikawa A., Fukushima A., Noji M., Saito K. Physiological roles of the beta-substituted alanine synthase gene family in Arabidopsis. Plant Physiol 2008, 146:310-320.
27. Yi H., Jez J.M. Assessing functional diversity in the soybean β-substituted alanine synthase enzyme family. Phytochemistry 2012, 83:15-24.
28. Yi H., Juergens M., Jez J.M. Structure of soybean β-cyanoalanine synthase and the molecular basis for cyanide detoxification in plants. Plant Cell 2012, 24:2696-2706.
29. Alvarez C., Calo L., Romero L.C., García I., Gotor C. An O-acetylserine(thiol)lyase homolog with l-cysteine desulfhydrase activity regulates cysteine homeostasis in Arabidopsis. Plant Physiol 2010, 152:656-669.
30. Bermúdez M.A., Páez-Ochoa M.A., Gotor C., Romero L.C. Arabidopsis S-sulfocysteine synthase activity is essential for chloroplast function and long-day light-dependent redox control. Plant Cell 2010, 22:403-416.
31. Mino K., Ishikawa K. A novel O-phospho-l-serine sulfhydrylation reaction catalyzed by O-acetylserine sulfhydrylase from Aeropyrum pernix K1. FEBS Lett 2003, 551:133-138.
32. Oda Y., Mino K., Ishikawa K., Ataka M. Three-dimensional structure of a new enzyme, O-phosphoserine sulfhydrylase, involved in I-cysteine biosynthesis by a hyperthermophilic archaeon, Aeropyrum pernix K1, at 2.0Å resolution. J Mol Biol 2005, 351:334-344.
33. Nakamura T., Kawai Y., Kunimoto K., Iwasaki Y., Nishii K., Kataoka M., Ishikawa K. Structural analysis of the substrate recognition mechanism in O-phosphoserine sulfhydrylase from the hyperthermophilic archaeon Aeropyrum pernix K1. J Mol Biol 2012, 422:33-44.
34. Agren D., Schnell R., Oehlmann W., Singh M., Schneider G. Cysteine synthase (CysM) of Mycobacterium tuberculosis is an O-phosphoserine sulfhydrylase: evidence for an alternative cysteine biosynthesis pathway in mycobacteria. J Biol Chem 2008, 283:31567-31574.
35. Droux M., Ruffet M.L., Douce R., Job D. Interactions between serine acetyltransferase and O-acetylserine (thiol) lyase in higher plants-structural and kinetic properties of the free and bound enzymes. Eur J Biochem 1998, 255:235-245.
36. Mino K., Yamanoue T., Sakiyama T., Eisaki N., Matsuyama A., Nakanishi K. Effects of bienzyme complex formation of cysteine synthetase from Escherichia coli on some properties and kinetics. Biosci Biotechnol Biochem 2000, 64:1628-1640.
37. Mino K., Imamura K., Sakiyama T., Eisaki N., Matsuyama A., Nakanishi K. Increase in the stability of serine acetyltransferase from Escherichia coli against cold inactivation and proteolysis by forming a bienzyme complex. Biosci Biotechnol Biochem 2001, 65:865-874.
38. Bogdanova N., Hell R. Cysteine synthesis in plants: protein-protein interactions of serine acetyltransferase from Arabidopsis thaliana. Plant J 1997, 11:251-262.
39. Wirtz M., Berkowitz O., Droux M., Hell R. The cysteine synthase complex from plants-mitochondrial serine acetyltransferase from Arabidopsis thaliana carries a bifunctional domain for catalysis and protein-protein interaction. Eur J Biochem 2001, 268:686-693.
40. Liszewska F., Lewandowska M., Płochocka D., Sirko A. Mutational analysis of O-acetylserine (thiol) lyase conducted in yeast two-hybrid system. Biochim Biophys Acta 2007, 1774:450-455.
41. Campanini B., Speroni F., Salsi E., Cook P.F., Roderick S.L., Huang B., Bettati S., Mozzarelli A. Interaction of serine acetyltransferase with O-acetylserine sulfhydrylase active site: evidence from fluorescence spectroscopy. Protein Sci 2005, 14:2115-2124.
42. Berkowitz O., Wirtz M., Wolf A., Kuhlmann J., Hell R. Use of biomolecular interaction analysis to elucidate the regulatory mechanism of the cysteine synthase complex from Arabidopsis thaliana. J Biol Chem 2002, 277:30629-30634.
43. Francois J.A., Kumaran S., Jez J.M. Structural basis for interaction of O-acetylserine sulfhydrylase and serine acetyltransferase in the Arabidopsis cysteine synthase complex. Plant Cell 2006, 18:3647-3655.
44. Kumaran S., Jez J.M. Thermodynamics of the interaction between O-acetylserine sulfhydrylase and the C-terminus of serine acetyltransferase. Biochemistry 2007, 46:5586-5594.
45. Kumaran S., Yi H., Krishnan H.B., Jez J.M. Assembly of the cysteine synthase complex and the regulatory role of protein-protein interactions. J Biol Chem 2009, 284:10268-10275.
46. Wirtz M., Birke H., Heeg C., Müller C., Hosp F., Throm C., König S., Feldman-Salit A., Rippe K., Petersen G., Wade R.C., Rybin V., Scheffzek K., Hell R. Structure and function of the hetero-oligomeric cysteine synthase complex in plants. J Biol Chem 2010, 285:32810-32817.
47. Huang B., Vetting M.W., Roderick S.L. The active site of O-acetylserine sulfhydrylase is the anchor point for bienzyme complex formation with serine acetyltransferase. J Bacteriol 2005, 187:3201-3205.
48. Salsi E., Campanini B., Bettati S., Raboni S., Roderick S.L., Cook P.F., Mozzarelli A. A two-step process controls the formation of the bienzyme cysteine synthase complex. J Biol Chem 2010, 285:12813-12822.
49. Wang T., Leyh T.S. Three-stage assembly of the cysteine synthase complex from Escherichia coli. J Biol Chem 2012, 287:4360-4367.
50. Feldman-Salit A., Wirtz M., Hell R., Wade R.C. A mechanistic model of the cysteine synthase complex. J Mol Biol 2009, 386:37-59.
51. Feldman-Salit A., Wirtz M., Lenherr E.D., Throm C., Hothorn M., Scheffzek K., Hell R., Wade R.C. Allosterically gated enzyme dynamics in the cysteine synthase complex regulate cysteine biosynthesis in Arabidopsis thaliana. Structure 2012, 20:292-302.
52. Hell R., Hillebrand H. Plant concepts for mineral acquisition and allocation. Curr Opin Biotechnol 2001, 12:161-168.
53. Hirai M.Y., Fujiwara T., Awazuhara M., Kimura T., Noji M., Saito K. Global expression profiling of sulfur-starved Arabidopsis by DNA macroarray reveals the role of O-acetyl-l-serine as a general regulator of gene expression in response to sulfur nutrition. Plant J 2003, 33:651-663.
54. Hopkins L., Parmar S., Blaszczyk A., Hesse H., Hoefgen R., Hawkesford M.J. O-acetylserine and the regulation of expression of genes encoding components for sulfate uptake and assimilation in potato. Plant Physiol 2005, 138:433-440.
55. Maruyama-Nakashita A., Nakamura Y., Tohge T., Saito K., Takahashi H. Arabidopsis SLIM1 is a central transcriptional regulator of plant sulfur response and metabolism. Plant Cell 2006, 18:3235-3251.
56. Wirtz M., Hell R. Dominant-negative modification reveals the regulatory function of the multimeric cysteine synthase protein complex in transgenic tobacco. Plant Cell 2007, 19:625-639.
57. Haas F.H., Heeg C., Queiroz R., Bauer A., Wirtz M., Hell R. Mitochondrial serine acetyltransferase functions as a pacemaker of cysteine synthesis in plant cells. Plant Physiol 2008, 148:1055-1067.
58. Krueger S., Niehl A., Lopez Martin M.C., Steinhauser D., Donath A., Hildebrandt T., Romero L.C., Hoefgen R., Gotor C., Hesse H. Analysis of cytosolic and plastidic serine acetyltransferase mutants and subcellular metabolite distributions suggests interplay of the cellular compartments for cysteine biosynthesis in Arabidopsis. Plant Cell Environ 2009, 32:349-367.
59. Wirtz M., Beard K.F., Lee C.P., Boltz A., Schwarzländer M., Fuchs C., Meyer A.J., Heeg C., Sweetlove L.J., Ratcliffe R.G., Hell R. Mitochondrial cysteine synthase complex regulates O-acetylserine biosynthesis in plants. J Biol Chem 2012, 287:27941-27947.
60. Hindson V.J., Moody P.C., Rowe A.J., Shaw W.C. Serine acetyltransferase from Eschericia coli is a dimer of trimers. J Biol Chem 2000, 275:461-466.
61. Jonic S., Vénien-Bryan C. Protein structure determination by electron cryo-microscopy. Curr Opin Pharm 2009, 9:636-642.
62. Mertens H.D., Svergun D.I. Structural characterization of proteins and complexes using small-angle X-ray solution scattering. J Struct Biol 2010, 172:128-141.
63. Jurgenson C.T., Burns K.E., Begley T.P., Ealick S.E. Crystal structure of a sulfur carrier protein complex found in the cysteine biosynthetic pathway of Mycobacterium tuberculosis. Biochemistry 2008, 47:10354-10364.
64. Wei J., Tang Q.X., Varlamova O., Roche C., Lee R., Leyh T.S. Cysteine biosynthetic enzymes are the pieces of a metabolic energy pump. Biochemistry 2002, 41:8493-8498.
65. Rausch T., Wachter A. Sulfur metabolism-a versatile platform for launching defence operations. Trends Plant Sci 2005, 10:503-509.
66. Kim W.S., Chronis D., Juergens M., Schroeder A.C., Hyun S.W., Jez J.M., Krishnan H.B. Transgenic soybean plants overexpressing O-acetylserine sulfhydrylase accumulate enhanced levels of cysteine and Bowman-Birk protease inhibitor in seeds. Planta 2012, 235:13-23.
67. Nguyen H.C., Hoefgen R., Hesse H. Improving the nutritive value of rice seeds-elevation of cysteine and methionine contents in rice plants by ectopic expression of a bacterial serine acetyltransferase. J Exp Bot 2012, 63:5991-6001.
68. Raj I., Kumar S., Gourinath S. The narrow active-site cleft of O-acetylserine sulfhydrylase from Leishmania donovani allows complex formation with serine acetyltransferases with a range of C-terminal sequences. Acta Crystallogr D 2012, 68:909-919.
69. Fyfe P.K., Westrop G.D., Ramos T., Müller S., Coombs G.H., Hunter W.N. Structure of Leishmania major cysteine synthase. Acta Crystallogr F 2012, 68:738-743.
70. Chinthalapudi K., Kumar M., Kumar S., Jain S., Alam N., Gourinath S. Crystal structure of native O-acetyl-serine sulfhydrylase from Entamoeba histolytica and its complex with cysteine: structural evidence for cysteine binding and lack of interactions with serine acetyl transferase. Proteins 2008, 72:1222-1232.
71. Salsi E., Bayden A.S., Spyrakis F., Amadasi A., Campanini B., Bettati S., Dodatko T., Cozzini P., Kellogg G.E., Cook P.F., Roderick S.L., Mozzarelli A. Design of O-acetylserine sulfhydrylase inhibitors by mimicking nature. J Med Chem 2010, 53:345-356.
72. Spyrakis F., Felici P., Bayden A.S., Salsi E., Miggiano R., Kellogg G.E., Cozzini P., Cook P.F., Mozzarelli A., Campanini B. Fine tuning of the active site modulates specificity in the interaction of O-acetylserine sulfhydrylase isozymes with serine acetyltransferase. Biochim Biophys Acta 2013, 1834:169-181.