Crystal structure of a molybdopterin synthase-precursor Z complex: Insight into its sulfur transfer mechanism and its role in molybdenum cofactor deficiency

Biochemistry

Volumn 47, Issue 2, 2008, Pages 615-626

  Daniels, Juma N ^a   Wuebbens, Margot M ^b   Rajagopalan, K V ^b   Schindelin, Hermann ^a,c  

^a STONY BROOK UNIVERSITY   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

^c UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BIOSYNTHESIS; CRYSTAL STRUCTURE; ENZYME ACTIVITY; MOLYBDENUM; SULFUR;

MOLYBDENUM COFACTOR DEFICIENCY; MOLYBDOPTERIN;

PROTEINS;

CARBOXYLIC ACID DERIVATIVE; DIMER; GLYCINE; METAL; MOLYBDENUM; MOLYBDENUM COFACTOR; MOLYBDOPTERIN SYNTHASE; PTERIN; SULFUR; SYNTHETASE; TETRAMER; THIOL DERIVATIVE; TUNGSTEN; UNCLASSIFIED DRUG;

ARTICLE; BIOSYNTHESIS; CARBOXY TERMINAL SEQUENCE; COMPLEX FORMATION; CRYSTAL STRUCTURE; ENZYME MECHANISM; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN STRUCTURE; REACTION ANALYSIS; STAPHYLOCOCCUS AUREUS;

STAPHYLOCOCCUS AUREUS;

EID: 38849106821     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi701734g     Document Type: Article

References (47)

1. Rajagopalan, K. (1996) Escherichia coli and Salmonella typhimurium, Vol. 1, American Society for Microbiology, Washington, DC.
2. Hille, R. (1996) The Mononuclear Molybdenum Enzymes, Chem. Rev. 96, 2757-2816.
3. Johnson, J. L., and Wadman, S. K. (1989) The metabolic basis of inherited disease, McGraw-Hill, New York.
4. Johnson, J. L., Rajagopalan, K. V., Mukund, S., and Adams, M. W. (1993) Identification of molybdopterin as the organic component of the tungsten cofactor in four enzymes from hyperthermophilic Archaea, J. Biol. Chem. 268, 4848-4852.
5. Koshiba, T., Saito, E., Ono, N., Yamamoto, N., and Sato, M. (1996) Purification and properties of flavin- and molybdenum-containing aldehyde oxidase from coleoptiles of maize, Plant Physiol. 110, 781-789.
6. Lin, J. T., and Stewart, V. (1998) Nitrate assimilation by bacteria, Adv. Microb. Physiol. 39, 1-30, 379.
7. Campbell, W. H. (1996) Nitrate reductase biochemistry comes of age, Plant Physiol. 111, 355-361.
8. Menendez, C., Siebert, D., and Brandsch, R. (1996) MoaA of Arthrobacter nicotinovorans pAO1 involved in Mo-pterin cofactor synthesis is an Fe-S protein, FEBS Lett. 391, 101-103.
9. Hanzelmann, P., and Schindelin, H. (2004) Crystal structure of the S-adenosylmethionine-dependent enzyme MoaA and its implications for molybdenum cofactor deficiency in humans, Proc. Natl. Acad. Sci. U.S.A. 101, 12870-12875.
10. Wuebbens, M. M., Liu, M. T., Rajagopalan, K., and Schindelin, H. (2000) Insights into molybdenum cofactor deficiency provided by the crystal structure of the molybdenum cofactor biosynthesis protein MoaC, Struct. Folding Des. 8, 709-718.
11. Rudolph, M. J., Wuebbens, M. M., Rajagopalan, K. V., and Schindelin, H. (2001) Crystal structure of molybdopterin synthase and its evolutionary relationship to ubiquitin activation, Nat. Struct. Biol. 8, 42-46.
12. Pitterle, D. M., Johnson, J. L., and Rajagopalan, K. V. (1993) In vitro synthesis of molybdopterin from precursor Z using purified converting factor. Role of protein-bound sulfur in formation of the dithiolene, J. Biol. Chem. 268, 13506-13509.
13. Pitterle, D. M., and Rajagopalan, K. V. (1993) The biosynthesis of molybdopterin in Escherichia coli. Purification and characterization of the converting factor, J. Biol. Chem. 268, 13499-13505.
14. Rudolph, M. J., Wuebbens, M. M., Turque, O., Rajagopalan, K. V., and Schindelin, H. (2003) Structural studies of molybdopterin synthase provide insights into its catalytic mechanism, J. Biol. Chem. 278, 14514-14522.
15. Lake, M. W., Wuebbens, M. M., Rajagopalan, K. V., and Schindelin, H. (2001) Mechanism of ubiquitin activation revealed by the structure of a bacterial MoeB-MoaD complex, Nature 414, 325-329.
16. Leimkuhler, S., Wuebbens, M. M., and Rajagopalan, K. V. (2001) Characterization of Escherichia coli MoeB and its involvement in the activation of molybdopterin synthase for the biosynthesis of the molybdenum cofactor, J. Biol. Chem. 276, 34695-34701.
17. Xiang, S., Nichols, J., Rajagopalan, K. V., and Schindelin, H. (2001) The crystal structure of Escherichia coli MoeA and its relationship to the multifunctional protein gephyrin, Structure 9, 299-310.
18. Sandu, C., and Brandsch, R. (2002) Evidence for MoeA-dependent formation of the molybdenum cofactor from molybdate and molybdopterin in Escherichia coli, Arch. Microbiol. 178, 465-470.
19. Liu, M. T., Wuebbens, M. M., Rajagopalan, K. V., and Schindelin, H. (2000) Crystal structure of the gephyrin-related molybdenum cofactor biosynthesis protein MogA from Escherichia coli, J. Biol. Chem. 275, 1814-1822.
20. Schwarz, G., Schrader, N., Mendel, R. R., Hecht, H. J., and Schindelin, H. (2001) Crystal structures of human gephyrin and plant Cnx1 G domains: Comparative analysis and functional implications, J. Mol. Biol. 312, 405-418.
21. Llamas, A., Otte, T., Multhaup, G., Mendel, R. R., and Schwarz, G. (2006) The mechanism of nucleotide-assisted molybdenum insertion into molybdopterin. A novel route toward metal cofactor assembly, J. Biol. Chem. 281, 18343-18350.
22. Johnson, J. L., Indermaur, L. W., and Rajagopalan, K. V. (1991) Molybdenum cofactor biosynthesis in Escherichia coli. Requirement of the chlB gene product for the formation of molybdopterin guanine dinucleotide, J. Biol. Chem. 266, 12140-12145.
23. Johnson, J. L., Bastian, N. R., and Rajagopalan, K. V. (1990) Molybdopterin guanine dinucleotide: A modified form of molybdopterin identified in the molybdenum cofactor of dimethyl sulfoxide reductase from Rhodobacter sphaeroides forma specialis denitrificans, Proc. Natl. Acad. Sci. U.S.A. 87, 3190-3194.
24. Vergnes, A., Pommier, J., Toci, R., Blasco, F., Giordano, G., and Magalon, A. (2006) NarJ chaperone binds on two distinct sites of the aponitrate reductase of Escherichia coli to coordinate molybdenum cofactor insertion and assembly, J. Biol. Chem. 281, 2170-2176.
25. Neumann, M., Stocklein, W., and Leimkuhler, S. (2007) Transfer of the molybdenum cofactor synthesized by Rhodobacter capsulars MoeA to XdhC and MobA, J. Biol. Chem. 282, 28493-28500.
26. Reiss, J. (2000) Genetics of molybdenum cofactor deficiency, Hum. Genet. 106, 157-163.
27. Reiss, J., and Johnson, J. L. (2003) Mutations in the molybdenum cofactor biosynthetic genes MOCS1, MOCS2, and GEPH, Hum. Mutat. 21, 569-576.
28. Reiss, J., Dorche, C., Stallmeyer, B., Mendel, R. R., Cohen, N., and Zabot, M. T. (1999) Human molybdopterin synthase gene: Genomic structure and mutations in molybdenum cofactor deficiency type B, Am. J. Hum. Genet. 64, 706-711.
29. Leimkuhler, S., Charcosset, M., Latour, P., Dorche, C., Kleppe, S., Scaglia, F., Szymczak, I., Schupp, P., Hahnewald, R., and Reiss, J. (2005) Ten novel mutations in the molybdenum cofactor genes MOCS1 and MOCS2 and in vitro characterization of a MOCS2 mutation that abolishes the binding ability of molybdopterin synthase, Hum. Genet. 117, 565-570.
30. Wuebbens, M. M., and Rajagopalan, K. V. (2003) Mechanistic and mutational studies of Escherichia coli molybdopterin synthase clarify the final step of molybdopterin biosynthesis, J. Biol. Chem. 278, 14523-14532.
31. Wuebbens, M. M., and Rajagopalan, K. V. (1993) Structural characterization of a molybdopterin precursor, J. Biol. Chem. 268, 13493-13498.
32. Otwinowski, A., and Minor, W. (1997) Methods in Enzymology, Macromolecular Crystallography, Vol. 276A, Academic Press, San Diego.
33. Vagin, A. A., and Isupov, M. N. (2001) Spherically averaged phased translation function and its application to the search for molecules and fragments in electron-density maps, Acta Crystallogr. D57, 1451-1456.
34. Vagin, A., and Teplyakov, A. (2000) An approach to multi-copy search in molecular replacement, Acta Crystallogr. D56, 1622-1624.
35. Murshudov, G. N., Vagin, A. A., and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method, Acta Crystallogr. D53, 240-255.
36. Winn, M. D., Isupov, M. N., and Murshudov, G. N. (2001) Use of TLS parameters to model anisotropic displacements in macromolecular refinement, Acta Crystallogr. D57, 122-133.
37. Winn, M. D., Murshudov, G. N., and Papiz, M. Z. (2003) Macromolecular TLS refinement in REFMAC at moderate resolutions, Methods Enzymol. 374, 300-321.
38. Jones, T. A., Zou, J. Y., Cowan, S. W., and Kjeldgaard, M. (1991) Improved methods for building protein models in electron density maps and the location of errors in these models, Acta Crystallogr. A47 (Part 2), 110-119.
39. Bailey, S. (1994) The CCP4 suite: Programs for protein crystallography, Acta Crystallogr. D50, 760-763.
40. Perrakis, A., Morris, R., and Lamzin, V. S. (1999) Automated protein model building combined with iterative structure refinement, Nat. Struct. Biol. 6, 458-463.
41. Johnson, J. L., and Rajagopalan, K. V. (1982) Structural and metabolic relationship between the molybdenum cofactor and urothione, Proc. Natl. Acad. Sci. U.S.A. 79, 6856-6860.
42. Johnson, J. L., Hainline, B. E., Rajagopalan, K. V., and Arison, B. H. (1984) The pterin component of the molybdenum cofactor. Structural characterization of two fluorescent derivatives, J. Biol. Chem. 259, 5414-5422.
43. Lovell, S. C., Davis, I. W., Arendall, W. B., III, de Bakker, P. I., Word, J. M., Prisant, M. G., Richardson, J. S., and Richardson, D. C. (2003) Structure validation by Cα geometry: φ,ψ and Cβ deviation, Proteins 50, 437-450.
44. Johnson, J. L., Wuebbens, M. M., and Rajagopalan, K. V. (1989) The structure of a molybdopterin precursor. Characterization of a stable, oxidized derivative, J. Biol. Chem. 264, 13440-13447.
45. Santamaria-Araujo, J. A., Fischer, B., Otte, T., Nimtz, M., Mendel, R. R., Wray, V., and Schwarz, G. (2004) The tetrahydropyranopterin structure of the sulfur-free and metal-free molybdenum cofactor precursor, J. Biol. Chem. 279, 15994-15999.
46. Vander Horn, P. B., Backstrom, A. D., Stewart, V., and Begley, T. P. (1993) Structural genes for thiamine biosynthetic enzymes (thiCEFGH) in Escherichia coli K-12, J. Bacteriol. 175, 982-992.
47. Schmitz, J., Wuebbens, M. M., Rajagopalan, K. V., and Leimkuhler, S. (2007) Role of the C-terminal Gly-Gly motif of Escherichia coli MoaD, a molybdenum cofactor biosynthesis protein with a ubiquitin fold, Biochemistry 46, 909-916.