It takes two to Tango: Defining an essential second active site in pyridoxal 5′-phosphate synthase

PLoS ONE

Volumn 6, Issue 1, 2011, Pages

  Moccand, Cyril ^a   Kaufmann, Markus ^a   Fitzpatrick, Teresa B ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTAMINASE; GLYCERALDEHYDE 3 PHOSPHATE; PYRIDOXAL 5 PHOSPHATE; RIBOSE 5 PHOSPHATE; TRANSCRIPTION FACTOR PDX 1; AMINOTRANSFERASE; MULTIENZYME COMPLEX; PYRIDOXINE; RIBOSE PHOSPHATE; RIBOSE-5-PHOSPHATE;

ARTICLE; BACILLUS SUBTILIS; BINDING AFFINITY; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CATALYSIS; CHROMATOPHORE; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME KINETICS; MUTAGENESIS; NONHUMAN; PROTEIN BINDING; SITE DIRECTED MUTAGENESIS; ANIMAL; BIOSYNTHESIS; CHEMISTRY; HUMAN; METABOLISM;

ANIMALS; CATALYTIC DOMAIN; GLUTAMINASE; GLYCERALDEHYDE 3-PHOSPHATE; HUMANS; METABOLIC NETWORKS AND PATHWAYS; MULTIENZYME COMPLEXES; PROTEIN BINDING; PYRIDOXAL PHOSPHATE; RIBOSEMONOPHOSPHATES; TRANSAMINASES; VITAMIN B 6;

EID: 79251636885     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0016042     Document Type: Article

References (44)

1. Bender D (1989) Vitamin B6 requirements and recommendations. Eur J Clin Nutri 43: 289-309.
2. Matxain JM, Padro D, Ristilal M, Strid A, Eriksson LA (2009) Evidence of high OH radical quenching efficiency by vitamin B6. J Phys Chem B 113: 9629-9632.
3. Ehrenshaft M, Bilski P, Li MY, Chignell CF, Daub ME (1999) A highly conserved sequence is a novel gene involved in de novo vitamin B6 biosynthesis. Proc Natl Acad Sci USA 96: 9374-9378.
4. Ehrenshaft M, Jenns AE, Chung KR, Daub ME (1998) SOR1, a gene required for photosensitizer and singlet oxygen resistance in Cercospora fungi, is highly conserved in divergent organisms. Mol Cell 1: 603-609.
5. Komatsu S, Yanaka N, Matsubara K, Kato N (2003) Antitumor effect of vitamin B6 and its mechanisms. Biochim Biophys Acta 1647: 127-130.
6. John R (1995) Pyridoxal phosphate-dependent enyzmes. Biochim Biophys Acta 1248: 81-96.
7. Fitzpatrick TB, Amrhein N, Kappes B, Macheroux P, Tews I, et al. (2007) Two independent routes of de novo vitamin B6 biosynthesis: not that different after all. Biochem J 407: 1-13.
8. Tambasco-Studart M, Titiz O, Raschle T, Forster G, Amrhein N, et al. (2005) Vitamin B6 biosynthesis in higher plants. Proc Natl Acad Sci USA 102: 13687-13692.
9. Cane DE, Du S, Robinson JK, Hsiung Y, Spenser ID (1999) Biosynthesis of vitamin B6: Enzymatic conversion of 1-deoxy-d-xylulose-5-phosphate to pyridoxol phosphate. J Am Chem Soc 121: 7722-7723.
10. Laber B, Maurer W, Scharf S, Stepusin K, Schmidt FS (1999) Vitamin B6 biosynthesis: formation of pyridoxine 5′-phosphate from 4-(phosphohydroxy)- threonine and 1-deoxy-xylulose-5-phosphate by PdxA and PdxJ protein. FEBS Lett 449: 45-48.
11. Tazuya K, Adachi Y, Masuda K, Yamada K, Kumaoka H (1995) Origin of the nitrogen atom of pyridoxine in Saccharomyces cerevisiae. Biochim Biophys Acta 1244: 113-6.
12. Ehrenshaft M, Daub ME (2001) Isolation of PDX2, a second novel gene in the pyridoxine biosynthesis pathway of eukaryotes, archaebacteria, and a subset of eubacteria. J Bacteriol 183: 3383-3390.
13. Osmani AH, May GS, Osmani SA (1999) The extremely conserved pyroA gene of Aspergillus nidulans is required for pyridoxine synthesis and is required indirectly for resistance to photosensitizers. J Biol Chem 274: 23565-23569.
14. Sakai A, Kita M, Katsuragi T, Ogasawata N, Tani Y (2002) YaaD and YaaE are involved in vitamin B6 biosynthesis in Bacillus subtilis. J Biosci Bioeng 93: 309-312.
15. Raschle T, Amrhein N, Fitzpatrick TB (2005) On the two components of pyridoxal 5′-phosphate synthase from Bacillus subtilis. J Biol Chem 280: 32291-32300.
16. Burns KE, Xiang Y, Kinsland CL, McLafferty FW, Begley TP (2005) Reconstitution and biochemical characterization of a new pyridoxal-5′- phosphate biosynthetic pathway. J Am Chem Soc 127: 3682-3683.
17. Strohmeier M, Raschle T, Mazurkiewicz J, Rippe K, Sinning I, et al. (2006) Structure of a bacterial pyridoxal 59-phosphate synthase complex. Proc Natl Acad Sci USA 103: 19284-19289.
18. Zein F, Zhang Y, Kang Y-N, Burns K, Begley TP, et al. (2006) Structural insights into the mechanism of the PLP synthase holoenzyme from Thermotoga maritima. Biochemistry 45: 14609-14620.
19. Zhu J, Burgner JW, Harms E, Belitsky BR, Smith JL (2005) A new arrangement of (β/α)8 barrels in the synthase subunit of PLP synthase. J Biol Chem 280: 27914-27923.
20. Neuwirth M, Strohmeier M, Windeisin V, Wallner S, Deller S, et al. (2009) Xray crystal structure of Saccharomyces cerevisiae Pdx1 provides insights into the oligomeric nature of PLP synthases. FEBS Lett 583: 2179-2186.
21. Raschle T, Speziga D, Kress W, Moccand C, Gehrig P, et al. (2009) Intersubunit cross-talk in pyridoxal 5′-phosphate synthase, coordinated by the C Terminus of the synthase subunit. J Biol Chem 284: 7706-7718.
22. Raschle T, Arigoni D, Brunisholz R, Rechsteiner H, Amrhein N, et al. (2007) Reaction mechanism of pyridoxal 59-phosphate synthase: Detection of an enzyme-bound chromophoric intermediate. J Biol Chem 282: 6098-6105.
23. Müller IB, Knöckel J, Groves MR, Jordanova R, Ealick SE, et al. (2008) The assembly of the plasmodial PLP synthase complex follows a defined course. PLoS ONE 3: e1815.
24. te Biesebeke R, Krab IM, Parmeggiani A (2001) The arginine finger loop of yeast and human GAP is a determinant for the specificity toward Ras GTPase. Biochemistry 40: 7474-7479.
25. Zhang B, Zhang Y, Collins CC, Johnson DI, Zheng Y (1999) A built-in arginine finger triggers the self-stimulatory GTPase-activating activity of Rho family GTPases. J Biol Chem 274: 2609-2612.
26. Crampton DJ, Guo S, Johnson DE, Richardson CC (2004) The arginine finger of bacteriophage T7 gene 4 helicase: Role in energy coupling. Proc Natl Acad Sci USA 101: 4373-4378.
27. Fitzpatrick TB, Moccand C, Roux C (2010) Vitamin B6 biosynthesis: charting the mechanistic landscape. ChemBioChem 11: 1185-1193.
28. Mozzarelli A, Bettati S (2006) Exploring the pyridoxal 5′-phosphate-dependent enzymes. Chem Rec 6: 275-287.
29. Vacca R, Giannattasio S, Capitani G, Marra E, Christen P (2008) Molecular evolution of B6 enzymes: Binding of pyridoxal-5′-phosphate and Lys41Arg substitution turn ribonuclease A into a model B6 protoenzyme. BMC Biochem 9: 17.
30. +-ATPase. J Biol Chem 269: 7419-7422.
31. 13C NMR snapshots of the complex reaction coordinate of pyridoxal phosphate synthase. Nat Chem Biol 4: 425-430.
32. 6. Yeast 19: 1261-1276.
33. Titiz O, Tambasco-Studart M, Warzych E, Apel K, Amrhein N, et al. (2006) PDX1 is essential for vitamin B6 biosynthesis, development and stress tolerance in Arabidopsis. Plant J 48: 933-946.
34. Dick T, Manjunatha U, Kappes B, Gengenbacher M (2010) Vitamin B6 biosynthesis is essential for survival and virulence of Mycobacterium tuberculosis. Mol Microbiol, in press. doi:10.1111/j.1365-2958.2010.07381.x.
35. Hanes JW, Burns KE, Hilmey DG, Chatterjee A, Dorrestein PC, et al. (2008) Mechanistic studies on pyridoxal phosphate synthase: The reaction pathway leading to a chromophoric intermediate. J Am Chem Soc 130: 3043-3052.
36. Hanes JW, Keresztes I, Begley TP (2008) Trapping of a chromophoric intermediate in the Pdx1-catalyzed biosynthesis of pyridoxal 5′-phosphate. Angew Chem 120: 2132-2135.
37. Guillén Schlippe YV, Hedstrom L (2005) A twisted base? The role of arginine in enzyme-catalyzed proton abstractions. Arch Biochem Biophys 433: 266-278.
38. a values. Proteins 61: 704-721.
39. Middleton SA, Kantrowitz ER (1988) Function of arginine-234 and aspartic acid-271 in domain closure, cooperativity, and catalysis in Escherichia coli aspartate transcarbamylase. Biochemistry 27: 8653-8660.
40. Yang ES, Schirch V (2000) Tight binding of pyridoxal 5′-phosphate to recombinant Escherichia coli pyridoxine 5′-phosphate oxidase. Arch Biochem Biophys 377: 109-114.
41. Hill RE, Himmeldirk K, Kennedy IA, Pauloski RM, Sayer BG, et al. (1996) The biogenetic anatomy of vitamin B6. J Biol Chem 271: 30426-30435.
42. Zhang X, Teng Y-B, Liu J-P, He Y-X, Zhou K, et al. (2010) Structural insights into the catalytic mechanism of the yeast pyridoxal 5-phosphate synthase Snz1. Biochem J in press. doi: 10.1042/BJ20101241.
43. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 7: 248-54.
44. Mahon MM, Graber R, Christen P, Malthouse JPG (1999) The aspartate aminotransferase-catalysed exchange of the a-protons of aspartate and glutamate: the effects of the R386A and R292V mutations on this exchange reaction. Biochim Biophys Acta 1434: 191-201.