PqqD is a novel peptide chaperone that forms a ternary complex with the radical S-adenosylmethionine protein PqqE in the pyrroloquinoline quinone biosynthetic pathway

Journal of Biological Chemistry

Volumn 290, Issue 20, 2015, Pages 12908-12918

  Latham, John A ^a,b   Iavarone, Anthony T ^a,b   Barr, Ian ^a,b   Juthani, Prerak V ^a,b   Klinman, Judith P ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; BACTERIA; BIOINFORMATICS; CARBON; MASS SPECTROMETRY; PEPTIDES; STOICHIOMETRY; SURFACE PLASMON RESONANCE;

BIOINFORMATIC ANALYSIS; BIOSYNTHETIC PATHWAY; ISOTHERMAL CALORIMETRY; KLEBSIELLA PNEUMONIAE; MODIFICATION PATHWAY; NATIVE MASS SPECTROMETRIES; PYRROLOQUINOLINE QUINONE; SURFACE PLASMON RESONANCE SPECTROSCOPY;

PROTEINS;

CHAPERONE; MYCOFACTOCIN; PROTEIN; PYRROLOQUINOLINEQUINONE; S ADENOSYLMETHIONINE; SUBTILOSIN; SULFATASE; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; MULTIPROTEIN COMPLEX; PQQD PROTEIN, METHYLOBACTERIUM EXTORQUENS; PQQE PROTEIN, METHYLOBACTERIUM EXTORQUENS; PROTEINASE;

ARTICLE; BIOSYNTHESIS; CONTROLLED STUDY; ISOTHERMAL TITRATION CALORIMETRY; MASS SPECTROMETRY; METHYLOBACTERIUM EXTORQUENS; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN MODIFICATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; STOICHIOMETRY; SURFACE PLASMON RESONANCE; CHEMISTRY; GENETICS; METABOLISM;

KLEBSIELLA PNEUMONIAE; METHYLOBACTERIUM EXTORQUENS;

BACTERIAL PROTEINS; ENDOPEPTIDASES; MASS SPECTROMETRY; METHYLOBACTERIUM EXTORQUENS; MOLECULAR CHAPERONES; MULTIPROTEIN COMPLEXES; SURFACE PLASMON RESONANCE;

EID: 84929340856     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M115.646521     Document Type: Article

References (40)

1. Babasaki, K., Takao, T., Shimonishi, Y., and Kurahashi, K. (1985) Subtilosin A, a new antibiotic peptide produced by Bacillus subtilis 168: isolation, structural analysis, and biogenesis. J. Biochem. 98, 585-603
2. Duquesne, S., and Destoumieux-Garzón, D. (2007) Microcins, gene-encoded antibacterial peptides from enterobacteria. Nat. Prod. Rep. 24, 708-734
3. Willey, J. M., and van der Donk, W. A. (2007) Lantibiotics: peptides of diverse structure and function. Annu. Rev. Microbiol. 61, 477-501
4. Bacon Schneider, K., Palmer, T. M., and Grossman, A. D. (2002) Characterization of comQ and comX, two genes required for production of ComX pheromone in Bacillus subtilis. J. Bacteriol. 184, 410-419
5. Okada, M., Sato, I., Cho, S. J., Iwata, H., Nishio, T., Dubnau, D., and Sakagami, Y. (2005) Structure of the Bacillus subtilis quorum-sensing peptide pheromone ComX. Nat. Chem. Biol. 1, 23-24
6. Behling, L. A., Hartsel, S. C., Lewis, D. E., DiSpirito, A. A., Choi, D. W., Masterson, L. R., Veglia, G., and Gallagher, W. H. (2008) NMR, mass spectrometry and chemical evidence reveal a different chemical structure for methanobactin that contains oxazolone rings. J. Am. Chem. Soc. 130, 12604-12605
7. Anthony, C. (1998) The pyrroloquinoline quinone (PQQ)-containing quinoprotein dehydrogenases. Biochem. Soc. Trans. 26, 413-417
8. Toyama, H., Chistoserdova, L., and Lidstrom, M. E. (1997) Sequence analysis of pqq genes required for biosynthesis of pyrroloquinoline quinone in Methylobacterium extorquens AM1 and the purification of a biosynthetic intermediate. Microbiology 143, 595-602
9. Goosen, N., Huinen, R. G., and van de Putte, P. (1992) A 24-amino-acid polypeptide is essential for the biosynthesis of the coenzyme pyrroloquinoline-quinone. J. Bacteriol. 174, 1426-1427
10. Grell, T. A., Goldman, P. J., and Drennan, C. L. (2015) SPASM and twitch domains in AdoMet radical enzyme structures. J. Biol. Chem. 290, 3964-3971
11. Haft, D. H., and Basu, M. K. (2011) Biological systems discovery in silico: radical S-adenosylmethionine protein families and their target peptides for posttranslational modification. J. Bacteriol. 193, 2745-2755
12. Goodwin, P. M., and Anthony, C. (1998) The biochemistry, physiology and genetics of PQQ and PQQ-containing enzymes. Adv. Microb. Physiol. 40, 1-80
13. Anthony, C. (2001) Pyrroloquinoline quinone (PQQ) and quinoprotein enzymes. Antioxidants Redox. Signal. 3, 757-774
14. Gliese, N., Khodaverdi, V., and Görisch, H. (2010) The PQQ biosynthetic operons and their transcriptional regulation in Pseudomonas aeruginosa. Arch. Microbiol. 192, 1-14
15. Shen, Y.-Q., Bonnot, F., Imsand, E. M., RoseFigura, J. M., Sjölander, K., and Klinman, J. P. (2012) Distribution and properties of the genes encoding the biosynthesis of the bacterial cofactor, pyrroloquinoline quinone. Biochemistry 51, 2265-2275
16. Velterop, J. S., Sellink, E., Meulenberg, J. J., David, S., Bulder, I., and Postma, P. W. (1995) Synthesis of pyrroloquinoline quinone in vivo and in vitro and detection of an intermediate in the biosynthetic pathway: synthesis of pyrroloquinoline quinone in vivo and in vitro and detection of an intermediate in the biosynthetic pathway. J. Bacteriol. 177, 5088-5098
17. Bonnot, F., Iavarone, A. T., and Klinman, J. P. (2013) Multistep, eightelectron oxidation catalyzed by the cofactorless oxidase, PqqC: identification of chemical intermediates and their dependence on molecular oxygen. Biochemistry 52, 4667-4675
18. Magnusson, O. T., Toyama, H., Saeki, M., Rojas, A., Reed, J. C., Liddington, R. C., Klinman, J. P., and Schwarzenbacher, R. (2004) Quinone biogenesis: structure and mechanism of PqqC, the final catalyst in the production of pyrroloquinoline quinone. Proc. Natl. Acad. Sci. U.S.A. 101, 7913-7918
19. Wecksler, S. R., Stoll, S., Tran, H., Magnusson, O. T., Wu, S.-P., King, D., Britt, R. D., and Klinman, J. P. (2009) Pyrroloquinoline quinone biogenesis: demonstration that PqqE from Klebsiella pneumoniae is a radical S-adenosyl-L-methionine enzyme. Biochemistry 48, 10151-10161
20. Tsai, T. Y., Yang, C. Y., Shih, H. L., Wang, A. H. J., and Chou, S. H. (2009) Xanthomonas campestris PqqD in the pyrroloquinoline quinone biosynthesis operon adopts a novel saddle-like fold that possibly serves as a PQQ carrier. Proteins Struct. Funct. Bioinforma. 76, 1042-1048
21. Wecksler, S. R., Stoll, S., Iavarone, A. T., Imsand, E. M., Tran, H., Britt, R. D., and Klinman, J. P. (2010) Interaction of PqqE and PqqD in the pyrroloquinoline quinone (PQQ) biosynthetic pathway links PqqD to the radical SAM superfamily. Chem. Commun. 46, 7031-7033
22. Beeson, W. T., 4th, Iavarone, A. T., Hausmann, C. D., Cate, J. H., and Marletta, M. A. (2011) Extracellular aldonolactonase from Myceliophthora thermophila. Appl. Environ. Microbiol. 77, 650-656
23. Konarev, P. V., Volkov, V. V., Sokolova, A. V., Koch, H. J., and Svergun, D. I. (2003) PRIMUS: a Windows PC-based system for small-angle scattering data analysis. J. Appl. Crystallogr. 36, 1277-1282
24. Svergun, D. I. (1992) Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Crystallogr. 25, 495-503
25. Franke, D., and Svergun, D. I. (2009) DAMMIF, a program for rapid ab initio shape determination in small-angle scattering. J. Appl. Crystallogr. 42, 342-346
26. Wriggers, W. (2010) Using Situs for the integration of multi-resolution structures. Biophys. Rev. 2, 21-27
27. Schneidman-Duhovny, D., Hammel, M., and Sali, A. (2010) FoXS: a web server for rapid computation and fitting of SAXS profiles. Nucleic Acids Res. 38, W540-W544
28. Pettersen, E. F., Goddard, T. D., Huang, C. C., Couch, G. S., Greenblatt, D. M., Meng, E. C., and Ferrin, T. E. (2004) UCSF Chimera: a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605-1612
29. Fischer, H., de Oliveira Neto, M., Napolitano, H. B., Polikarpov, I., and Craievich, A. F. (2009) Determination of the molecular weight of proteins in solution from a single small-angle x-ray scattering measurement on a relative scale. J. Appl. Crystallogr. 43, 101-109
30. Atkinson, H. J., Morris, J. H., Ferrin, T. E., and Babbitt, P. C. (2009) Using sequence similarity networks for visualization of relationships across diverse protein superfamilies. PLoS One 4, e4345
31. Barber, A. E., 2nd, and Babbitt, P. C. (2012) Pythoscape: a framework for generation of large protein similarity networks. Bioinformatics 28, 2845-2846
32. Shannon, P., Markiel, A., Ozier, O., Baliga, N. S., Wang, J. T., Ramage, D., Amin, N., Schwikowski, B., and Ideker, T. (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498-2504
33. Fu, L., Niu, B., Zhu, Z., Wu, S., and Li, W. (2012) CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics 28, 3150-3152
34. Putnam, C. D., Hammel, M., Hura, G. L., and Tainer, J. A. (2007) X-ray solution scattering (SAXS) combined with crystallography and computation: defining accurate macromolecular structures, conformations and assemblies in solution. Q. Rev. Biophys. 40, 191-285
35. Lobanov, M. I., Bogatyreva, N. S., and Galzitskaia, O. V. (2008) Radius of gyration is indicator of compactness of protein structure. Mol. Biol. (Mosk) 42, 701-706
36. Zhang, Y., Kolinski, A., and Skolnick, J. (2003) TOUCHSTONE II: a new approach to ab initio protein structure prediction. Biophys. J. 85, 1145-1164
37. Svergun, D., Barberato, C., and Koch, M. H. J. (1995) CRYSOL: a program to evaluate x-ray solution scattering of biological macromolecules from atomic coordinates. J. Appl. Crystallogr. 28, 768-773
38. Mylonas, E., and Svergun, D. (2007) Accuracy of molecular mass determination of proteins in solution by small-angle x-ray scattering. J. Appl. Crystallogr. 40, s245-s249
39. Ozbabacan, S. E., Engin, H. B., Gursoy, A., and Keskin, O. (2011) Transient protein-protein interactions. Protein Eng. Des. Sel. 24, 635-648
40. Flühe, L., Knappe, T. A., Gattner, M. J., Schäfer, A., Burghaus, O., Linne, U., and Marahiel, M. A. (2012) The radical S-adenosylmethionine enzyme AlbA catalyzes thioether bond formation in subtilosin A. Nat. Chem. Biol. 8, 350-357