Assembly of the eukaryotic PLP-synthase complex from Plasmodium and activation of the Pdx1 enzyme

Structure

Volumn 20, Issue 1, 2012, Pages 172-184

  Guédez, Gabriela ^a   Hipp, Katharina ^b   Windeisen, Volker ^a   Derrer, Bianca ^c   Gengenbacher, Martin ^c   Böttcher, Bettina ^b   Sinning, Irmgard ^a   Kappes, Barbara ^c   Tews, Ivo ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMMONIA; BACTERIAL ENZYME; ENZYME VARIANT; GLUTAMINASE; METHIONINE; PROTEIN PDX2; PROTOZOAL PROTEIN; PYRIDOXAL 5' PHOSPHATE SYNTHASE; RECOMBINANT ENZYME; SCHIFF BASE; SYNTHETASE; TRANSCRIPTION FACTOR PDX 1; UNCLASSIFIED DRUG;

ALPHA HELIX; ARTICLE; BIOSYNTHESIS; COMPLEX FORMATION; COVALENT BOND; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; ELECTRON MICROSCOPY; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME CONFORMATION; ENZYME KINETICS; ENZYME STRUCTURE; ENZYME SUBSTRATE COMPLEX; ENZYME SUBUNIT; ENZYME SYNTHESIS; MUTAGENESIS; ORTHOLOGY; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN ASSEMBLY; SPECIES DIFFERENCE;

AMMONIA; CATALYTIC DOMAIN; CRYSTALLOGRAPHY; ENZYME ACTIVATION; GLUTAMINASE; METHIONINE; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; PLASMODIUM FALCIPARUM; PROTEIN CONFORMATION; PYRIDOXAL PHOSPHATE;

BACTERIA (MICROORGANISMS); EUKARYOTA; PLASMODIUM (APICOMPLEXA); PLASMODIUM FALCIPARUM;

EID: 84855771820     PISSN: 09692126     EISSN: 18784186     Source Type: Journal    
DOI: 10.1016/j.str.2011.11.015     Document Type: Article

References (57)

1. K.E. Burns, Y. Xiang, C.L. Kinsland, F.W. McLafferty, and T.P. Begley Reconstitution and biochemical characterization of a new pyridoxal-5′- phosphate biosynthetic pathway J. Am. Chem. Soc. 127 2005 3682 3683 (Pubitemid 40411393)
2. J.N. Burrows, K. Chibale, and T.N. Wells The state of the art in anti-malarial drug discovery and development Curr. Top. Med. Chem. 11 2011 1226 1254
3. C. Bustamante, C.N. Batista, and M. Zalis Molecular and biological aspects of antimalarial resistance in Plasmodium falciparum and Plasmodium vivax Curr. Drug Targets 10 2009 279 290
4. Collaborative Computational Project, Number 4 The CCP4 suite: programs for protein crystallography Acta Crystallogr. D Biol. Crystallogr. 50 1994 760 763
5. W.L. DeLano The PyMOL Molecular Graphics System 2002 DeLano Scientific San Carlos, CA
6. B. Derrer, V. Windeisen, G. Guédez Rodríguez, J. Seidler, M. Gengenbacher, W.D. Lehmann, K. Rippe, I. Sinning, I. Tews, and B. Kappes Defining the structural requirements for ribose 5-phosphate-binding and intersubunit cross-talk of the malarial pyridoxal 5-phosphate synthase FEBS Lett. 584 2010 4169 4174
7. T. Dick, U. Manjunatha, B. Kappes, and M. Gengenbacher Vitamin B6 biosynthesis is essential for survival and virulence of Mycobacterium tuberculosis Mol. Microbiol. 78 2010 980 988
8. M. Diepholz, D. Venzke, S. Prinz, C. Batisse, B. Flörchinger, M. Rössle, D.I. Svergun, B. Böttcher, and J. Féthire A different conformation for EGC stator subcomplex in solution and in the assembled yeast V-ATPase: possible implications for regulatory disassembly Structure 16 2008 1789 1798
9. A.A. Divo, T.G. Geary, N.L. Davis, and J.B. Jensen Nutritional requirements of Plasmodium falciparum in culture. I. Exogenously supplied dialyzable components necessary for continuous growth J. Protozool. 32 1985 59 64 (Pubitemid 15107964)
10. M. Ehrenshaft, P. Bilski, M.Y. Li, C.F. Chignell, and M.E. Daub A highly conserved sequence is a novel gene involved in de novo vitamin B6 biosynthesis Proc. Natl. Acad. Sci. USA 96 1999 9374 9378 (Pubitemid 29374762)
11. A.C. Eliot, and J.F. Kirsch Pyridoxal phosphate enzymes: mechanistic, structural, and evolutionary considerations Annu. Rev. Biochem. 73 2004 383 415 (Pubitemid 39050374)
12. T.B. Fitzpatrick, N. Amrhein, B. Kappes, P. Macheroux, I. Tews, and T. Raschle Two independent routes of de novo vitamin B6 biosynthesis: not that different after all Biochem. J. 407 2007 1 13 (Pubitemid 47535575)
13. T.B. Fitzpatrick, C. Moccand, and C. Roux Vitamin B6 biosynthesis: charting the mechanistic landscape ChemBioChem 11 2010 1185 1193
14. K. Flicker, M. Neuwirth, M. Strohmeier, B. Kappes, I. Tews, and P. Macheroux Structural and thermodynamic insights into the assembly of the heteromeric pyridoxal phosphate synthase from Plasmodium falciparum J. Mol. Biol. 374 2007 732 748 (Pubitemid 350018765)
15. M. Gengenbacher, T.B. Fitzpatrick, T. Raschle, K. Flicker, I. Sinning, S. Müller, P. Macheroux, I. Tews, and B. Kappes Vitamin B6 biosynthesis by the malaria parasite Plasmodium falciparum: biochemical and structural insights J. Biol. Chem. 281 2006 3633 3641 (Pubitemid 43845981)
16. J.W. Hanes, K.E. Burns, D.G. Hilmey, A. Chatterjee, P.C. Dorrestein, and T.P. Begley Mechanistic studies on pyridoxal phosphate synthase: the reaction pathway leading to a chromophoric intermediate J. Am. Chem. Soc. 130 2008 3043 3052 (Pubitemid 351455975)
17. J.W. Hanes, I. Keresztes, and T.P. Begley 13C NMR snapshots of the complex reaction coordinate of pyridoxal phosphate synthase Nat. Chem. Biol. 4 2008 425 430 (Pubitemid 351860550)
18. J.W. Hanes, I. Keresztes, and T.P. Begley Trapping of a chromophoric intermediate in the Pdx1-catalyzed biosynthesis of pyridoxal 5′-phosphate Angew. Chem. Int. Ed. Engl. 47 2008 2102 2105
19. G. Hansen, A. Heitmann, T. Witt, H. Li, H. Jiang, X. Shen, V.T. Heussler, A. Rennenberg, and R. Hilgenfeld Structural basis for the regulation of cysteine-protease activity by a new class of protease inhibitors in Plasmodium Structure 19 2011 919 929
20. C. Hartmann, M. Chami, U. Zachariae, B.L. de Groot, A. Engel, and M.G. Grütter Vacuolar protein sorting: two different functional states of the AAA-ATPase Vps4p J. Mol. Biol. 377 2008 352 363
21. B. Kappes, I. Tews, A. Binter, and P. Macheroux PLP-dependent enzymes as potential drug targets for protozoan diseases Biochim. Biophys. Acta 1814 2011 1567 1576
22. J. Knöckel, I.B. Müller, B. Bergmann, R.D. Walter, and C. Wrenger The apicomplexan parasite Toxoplasma gondii generates pyridoxal phosphate de novo Mol. Biochem. Parasitol. 152 2007 108 111 (Pubitemid 46107705)
23. J. Knöckel, R. Jordanova, I.B. Müller, C. Wrenger, and M.R. Groves Mobility of the conserved glycine 155 is required for formation of the active plasmodial Pdx1 dodecamer Biochim. Biophys. Acta 1790 2009 347 350
24. V. Lakshmanan, K.Y. Rhee, and J.P. Daily Metabolomics and malaria biology Mol. Biochem. Parasitol. 175 2011 104 111
25. S.J. Ludtke, P.R. Baldwin, and W. Chiu EMAN: semiautomated software for high-resolution single-particle reconstructions J. Struct. Biol. 128 1999 82 97 (Pubitemid 30013436)
26. C. Mehlin Structure-based drug discovery for Plasmodium falciparum Comb. Chem. High Throughput Screen. 8 2005 5 14 (Pubitemid 40164018)
27. C. Mehlin, E. Boni, F.S. Buckner, L. Engel, T. Feist, M.H. Gelb, L. Haji, D. Kim, C. Liu, and N. Mueller Heterologous expression of proteins from Plasmodium falciparum: results from 1000 genes Mol. Biochem. Parasitol. 148 2006 144 160 (Pubitemid 43964865)
28. G. Mittenhuber Phylogenetic analyses and comparative genomics of vitamin B6 (pyridoxine) and pyridoxal phosphate biosynthesis pathways J. Mol. Microbiol. Biotechnol. 3 2001 1 20 (Pubitemid 32094166)
29. C. Moccand, M. Kaufmann, and T.B. Fitzpatrick It takes two to tango: defining an essential second active site in pyridoxal 5′-phosphate synthase PLoS One 6 2011 e16042
30. S. Mooney, and H. Hellmann Vitamin B6: killing two birds with one stone? Phytochemistry 71 2010 495 501
31. T. Mukherjee, J. Hanes, I. Tews, S.E. Ealick, and T.P. Begley Pyridoxal phosphate: biosynthesis and catabolism Biochim. Biophys. Acta 1814 2011 1585 1596
32. I.B. Müller, J. Knöckel, M.R. Groves, R. Jordanova, S.E. Ealick, R.D. Walter, and C. Wrenger The assembly of the plasmodial PLP synthase complex follows a defined course PLoS One 3 2008 e1815
33. S. Müller Redox and antioxidant systems of the malaria parasite Plasmodium falciparum Mol. Microbiol. 53 2004 1291 1305 (Pubitemid 39209105)
34. S. Müller, and B. Kappes Vitamin and cofactor biosynthesis pathways in Plasmodium and other apicomplexan parasites Trends Parasitol. 23 2007 112 121 (Pubitemid 46274506)
35. I.B. Müller, J.E. Hyde, and C. Wrenger Vitamin B metabolism in Plasmodium falciparum as a source of drug targets Trends Parasitol. 26 2010 35 43
36. M. Neuwirth, K. Flicker, M. Strohmeier, I. Tews, and P. Macheroux Thermodynamic characterization of the protein-protein interaction in the heteromeric Bacillus subtilis pyridoxalphosphate synthase Biochemistry 46 2007 5131 5139 (Pubitemid 46683011)
37. M. Neuwirth, M. Strohmeier, V. Windeisen, S. Wallner, S. Deller, K. Rippe, I. Sinning, P. Macheroux, and I. Tews X-ray crystal structure of Saccharomyces cerevisiae Pdx1 provides insights into the oligomeric nature of PLP synthases FEBS Lett. 583 2009 2179 2186
38. R. Percudani, and A. Peracchi A genomic overview of pyridoxal-phosphate- dependent enzymes EMBO Rep. 4 2003 850 854 (Pubitemid 37304400)
39. I. Petersen, R. Eastman, and M. Lanzer Drug-resistant malaria: molecular mechanisms and implications for public health FEBS Lett. 585 2011 1551 1562
40. T. Raschle, N. Amrhein, and T.B. Fitzpatrick On the two components of pyridoxal 5′-phosphate synthase from Bacillus subtilis J. Biol. Chem. 280 2005 32291 32300 (Pubitemid 41361838)
41. T. Raschle, D. Arigoni, R. Brunisholz, H. Rechsteiner, N. Amrhein, and T.B. Fitzpatrick Reaction mechanism of pyridoxal 5′-phosphate synthase. Detection of an enzyme-bound chromophoric intermediate J. Biol. Chem. 282 2007 6098 6105 (Pubitemid 47100844)
42. T. Raschle, D. Speziga, W. Kress, C. Moccand, P. Gehrig, N. Amrhein, E. Weber-Ban, and T.B. Fitzpatrick Intersubunit cross-talk in pyridoxal 5′-phosphate synthase, coordinated by the C terminus of the synthase subunit J. Biol. Chem. 284 2009 7706 7718
43. M. Strohmeier, T. Raschle, J. Mazurkiewicz, K. Rippe, I. Sinning, T.B. Fitzpatrick, and I. Tews Structure of a bacterial pyridoxal 5′-phosphate synthase complex Proc. Natl. Acad. Sci. USA 103 2006 19284 19289 (Pubitemid 46028495)
44. M. Tambasco-Studart, I. Tews, N. Amrhein, and T.B. Fitzpatrick Functional analysis of PDX2 from Arabidopsis, a glutaminase involved in vitamin B6 biosynthesis Plant Physiol. 144 2007 915 925 (Pubitemid 46944754)
45. K. Tanaka, K. Tazuya, K. Yamada, and H. Kumaoka Biosynthesis of pyridoxine: origin of the nitrogen atom of pyridoxine in microorganisms J. Nutr. Sci. Vitaminol. (Tokyo) 46 2000 55 57 (Pubitemid 30397396)
46. K. Tazuya, Y. Adachi, K. Masuda, K. Yamada, and H. Kumaoka Origin of the nitrogen atom of pyridoxine in Saccharomyces cerevisiae Biochim. Biophys. Acta 1244 1995 113 116
47. J.J. Tesmer, R.K. Sunahara, A.G. Gilman, and S.R. Sprang Crystal structure of the catalytic domains of adenylyl cyclase in a complex with Gsalpha.GTPgammaS Science 278 1997 1907 1916 (Pubitemid 28013225)
48. M.A. Travassos, and M.K. Laufer Resistance to antimalarial drugs: molecular, pharmacologic, and clinical considerations Pediatr. Res. 65 2009 64R 70R
49. M. van Heel, G. Harauz, E.V. Orlova, R. Schmidt, and M. Schatz A new generation of the IMAGIC image processing system J. Struct. Biol. 116 1996 17 24 (Pubitemid 26093118)
50. S. Wallner, M. Neuwirth, K. Flicker, I. Tews, and P. Macheroux Dissection of contributions from invariant amino acids to complex formation and catalysis in the heteromeric pyridoxal 5-phosphate synthase complex from Bacillus subtilis Biochemistry 48 2009 1928 1935
51. World Health Organization Malaria Fact Sheet 94 2010 1
52. C. Wrenger, M.L. Eschbach, I.B. Müller, D. Warnecke, and R.D. Walter Analysis of the vitamin B6 biosynthesis pathway in the human malaria parasite Plasmodium falciparum J. Biol. Chem. 280 2005 5242 5248 (Pubitemid 40279996)
53. C. Wrenger, J. Knöckel, R.D. Walter, and I.B. Müller Vitamin B1 and B6 in the malaria parasite: requisite or dispensable? Braz. J. Med. Biol. Res. 41 2008 82 88 (Pubitemid 351425847)
54. H. Zalkin, and J.L. Smith Enzymes utilizing glutamine as an amide donor Adv. Enzymol. Relat. Areas Mol. Biol. 72 1998 87 144
55. F. Zein, Y. Zhang, Y.N. Kang, K. Burns, T.P. Begley, and S.E. Ealick Structural insights into the mechanism of the PLP synthase holoenzyme from Thermotoga maritima Biochemistry 45 2006 14609 14620 (Pubitemid 44906977)
56. X. Zhang, Y.B. Teng, J.P. Liu, Y.X. He, K. Zhou, Y. Chen, and C.Z. Zhou Structural insights into the catalytic mechanism of the yeast pyridoxal 5-phosphate synthase Snz1 Biochem. J. 432 2010 445 450
57. J. Zhu, J.W. Burgner, E. Harms, B.R. Belitsky, and J.L. Smith A new arrangement of (beta/alpha)8 barrels in the synthase subunit of PLP synthase J. Biol. Chem. 280 2005 27914 27923 (Pubitemid 41076909)