Genetic and structural validation of Aspergillus fumigatus N-acetylphosphoglucosamine mutase as an antifungal target

Bioscience Reports

Volumn 33, Issue 5, 2013, Pages 689-699

  Fang, Wenxia ^a   Du, Ting ^b   Raimi, Olawale G ^a,c   Hurtado Guerrero, Ramón ^a,d   Mariño, Karina ^a,e   Ibrahim, Adel F M ^a   Albarbarawi, Osama ^a,f   Ferguson, Michael A J ^a   Jin, Cheng ^b   Van Aalten, Daan M F ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b INSTITUTE OF MICROBIOLOGY   (China)

^c LAGOS STATE UNIVERSITY   (Nigeria)

^d UNIVERSITY OF ZARAGOZA   (Spain)

^e Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^f TAIBAH UNIVERSITY   (Saudi Arabia)

Author keywords

Cell wall; Drug target; Enzyme; Inhibitor; Nucleotide sugar; Protein structure

Indexed keywords

1,5 DIAMINO 4,8 DIHYDROXYANTHRAQUINONE; 2 CHLORO 1,5 DIAMINO 4,8 DIHYDROXYANTHRAQUINONE; 6 HYDROXY DOPA; ANTIFUNGAL AGENT; CHITIN; ENZYME INHIBITOR; FUNGAL ENZYME; MUTASE; N ACETYLGLUCOSAMINE; N ACETYLPHOSPHOGLUCOSAMINE MUTASE; N ACETYLPHOSPHOGLUCOSAMINE MUTASE INHIBITOR; TRISODIUM 4 [(2Z) 2 [4 FORMYL 6 METYL 5 OXO 3 (PHOSPHONATOOXYMETYL)PYRIDIN 2 YLIDENE] HYDRAZINYL] BENZOATE; UNCLASSIFIED DRUG; URIDINE DIPHOSPHATE; FUNGAL PROTEIN; MAGNESIUM;

ANTIFUNGAL ACTIVITY; ARTICLE; ASPERGILLUS FUMIGATUS; BIOSYNTHESIS; CELL COMPOSITION; CELL GROWTH; CELL ULTRASTRUCTURE; CELL VIABILITY; CONTROLLED STUDY; CRYSTAL STRUCTURE; DRUG STRUCTURE; DRUG TARGETING; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME STRUCTURE; FUNGAL CELL WALL; GENE EXPRESSION REGULATION; GROWTH REGULATION; HIGH THROUGHPUT SCREENING; IC 50; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; CELL WALL; CHEMICAL STRUCTURE; CHEMISTRY; DRUG ANTAGONISM; ENZYMOLOGY; GENETICS; HUMAN; KINETICS; MICROBIAL SENSITIVITY TEST; MICROBIAL VIABILITY; PROTEIN SECONDARY STRUCTURE; ULTRASTRUCTURE; X RAY CRYSTALLOGRAPHY;

ANTIFUNGAL AGENTS; ASPERGILLUS FUMIGATUS; CATALYTIC DOMAIN; CELL WALL; CRYSTALLOGRAPHY, X-RAY; FUNGAL PROTEINS; HUMANS; INHIBITORY CONCENTRATION 50; KINETICS; MAGNESIUM; MICROBIAL SENSITIVITY TESTS; MICROBIAL VIABILITY; MODELS, MOLECULAR; PHOSPHOTRANSFERASES (PHOSPHOMUTASES); PROTEIN STRUCTURE, SECONDARY;

EID: 84884846272     PISSN: 01448463     EISSN: 15734935     Source Type: Journal    
DOI: 10.1042/BSR20130053     Document Type: Article

References (50)

1. Latge,J.P. (2001) The pathobiology of Aspergillus fumigatus. Trends Microbiol. 9, 382-389
2. Latge,J.P. (1999) Aspergillus fumigatus and aspergillosis. Clin. Microbiol. Rev. 12, 310-350
3. Zmeili, O. S. and Soubani, A. O. (2007) Pulmonary aspergillosis: a clinical update. Q. J. Med. 100, 317-334 (Pubitemid 47073808)
4. Brown, G. D., Denning, D. W., Gow, N. A., Levitz, S. M., Netea, M. G. and White, T. C. (2012) Hidden killers: human fungal infections. Sci. Transl. Med. 4, 165rv113
5. Walsh, T. J., Anaissie, E. J., Denning, D. W., Herbrecht, R., Kontoyiannis, D. P., Marr, K. A., Morrison, V. A., Segal, B. H., Steinbach, W. J., Stevens, D. A. et al. (2008) Treatment of aspergillosis: clinical practice guidelines of the Infectious Diseases Society of America. Clin. Infect. Dis. 46, 327-360 (Pubitemid 351265310)
6. Anderson, J. B. (2005) Evolution of antifungal-drug resistance: mechanisms and pathogen fitness. Nat. Rev. Microbiol. 3, 547-556 (Pubitemid 40903878)
7. Spanakis, E. K., Aperis, G. and Mylonakis, E. (2006) New agents for the treatment of fungal infections: clinical efficacy and gaps in coverage. Clin. Infect. Dis. 43, 1060-1068 (Pubitemid 44631109)
8. Latge,J.P., Mouyna, I., Tekaia, F., Beauvais, A., Debeaupuis, J. P. and Nierman, W. (2005) Specific molecular features in the organization and biosynthesis of the cell wall of Aspergillus fumigatus. Med. Mycol. 43 (Suppl. 1), S15-S22 (Pubitemid 41038543)
9. Latge,J.P. (2007) The cell wall: a carbohydrate armour for the fungal cell. Mol. Microbiol. 66, 279-290
10. Tiede, A., Bastisch, I., Schubert, J., Orlean, P. and Schmidt, R. E. (1999) Biosynthesis of glycosylphosphatidylinositols in mammals and unicellular microbes. Biol. Chem. 380, 503-523 (Pubitemid 29248439)
11. Herscovics, A. and Orlean, P. (1993) Glycoprotein biosynthesis in yeast. FASEB J. 7, 540-550 (Pubitemid 23120901)
12. Niimi, K. and Niimi, M. (2009) The mechanisms of resistance to echinocandin class of antifungal drugs. Nihon Ishinkin Gakkai Zasshi 50, 57-66
13. Milewski, S., Gabriel, I. and Olchowy, J. (2006) Enzymes of UDP-GlcNAc biosynthesis in yeast. Yeast 23, 1-14 (Pubitemid 43230969)
14. Nishitani, Y., Maruyama, D., Nonaka, T., Kita, A., Fukami, T. A., Mio, T., Yamada-Okabe, H., Yamada-Okabe, T. and Miki, K. (2006) Crystal structures of N-acetylglucosamine-phosphate mutase, a member of the alpha-D-phosphohexomutase superfamily, and its substrate and product complexes. J. Biol. Chem. 281, 19740-19747 (Pubitemid 44035476)
15. Mio, T., Yamada-Okabe, T., Arisawa, M. and Yamada-Okabe, H. (2000) Functional cloning and mutational analysis of the human cDNA for phosphoacetylglucosamine mutase: identification of the amino acid residues essential for the catalysis. Biochim. Biophys. Acta 1492, 369-376 (Pubitemid 30427348)
16. Pang, H., Koda, Y., Soejima, M. and Kimura, H. (2002) Identification of human phosphoglucomutase 3 (PGM3) as N-acetylglucosamine-phosphate mutase (AGM1). Ann. Hum. Genet. 66, 139-144
17. Horfmann, M., Boles, E. and Zimmermann, F. K. (1994) Characterization of the essential yeast gene encoding N-acetylglucosamine-phosphate mutase. Eur. J. Biochem. 221, 741-747 (Pubitemid 24128043)
18. Nishitani, Y., Maruyama, D., Nonaka, T., Kita, A., Fukami, T. A., Mio, T., Yamada-Okabe, H., Yamada-Okabe, T. and Miki, K. (2006) Purification, crystallization and preliminary X-ray diffraction studies of N-acetylglucosamine-phosphate mutase from Candida albicans. Acta Crystallogr. F Struct. Biol. Cryst. Commun. 62, 419-421
19. Fernandez-Sorensen, A. and Carlson, D. M. (1971) Purification and properties of phosphoacetylglucosamine mutase. J. Biol. Chem. 246, 3485-3493
20. Cheng, P. W. and Carlson, D. M. (1979) Mechanism of phosphoacetylglucosamine mutase. J. Biol. Chem. 254, 8353-8357
21. Jolly, L., Pompeo, F., van Heijenoort, J., Fassy, F. and Mengin-Lecreulx, D. (2000) Autophosphorylation of phosphoglucosamine mutase from Escherichia coli. J. Bacteriol. 182, 1280-1285 (Pubitemid 30104404)
22. Jolly, L., Ferrari, P., Blanot, D., Van Heijenoort, J., Fassy, F. and Mengin-Lecreulx, D. (1999) Reaction mechanism of phosphoglucosamine mutase from Escherichia coli. Eur. J. Biochem. 262, 202-210 (Pubitemid 29242627)
23. Mengin-Lecreulx, D. and van Heijenoort, J. (1996) Characterization of the essential gene glmM encoding phosphoglucosamine mutase in Escherichia coli. J. Biol. Chem. 271, 32-39 (Pubitemid 26027279)
24. Regni, C., Schramm, A. M. and Beamer, L. J. (2006) The reaction of phosphohexomutase from Pseudomonas aeruginosa: structural insights into a simple processive enzyme. J. Biol. Chem. 281, 15564-15571 (Pubitemid 43855149)
25. Greig, K. T., Antonchuk, J., Metcalf, D., Morgan, P. O., Krebs, D. L., Zhang, J. G., Hacking, D. F., Bode, L., Robb, L., Kranz, C. et al. (2007) Agm1/Pgm3-mediated sugar nucleotide synthesis is essential for hematopoiesis and development. Mol. Cell. Biol. 27, 5849-5859 (Pubitemid 47257838)
26. Marino, K., Guther, M. L., Wernimont, A. K., Amani, M., Hui, R. and Ferguson, M. A. Identification, subcellular localization, biochemical properties, and high-resolution crystal structure of Trypanosoma brucei UDP-glucose pyrophosphorylase. Glycobiology 20, 1619-1630
27. da Silva Ferreira, M. E., Kress, M. R., Savoldi, M., Goldman, M. H., Hartl, A., Heinekamp, T., Brakhage, A. A. and Goldman, G. H. (2006) The akuB(KU80) mutant deficient for nonhomologous end joining is a powerful tool for analyzing pathogenicity in Aspergillus fumigatus. Eukaryot. Cell 5, 207-211 (Pubitemid 43113467)
28. Armitt, S., McCullough, W. and Roberts, C. F. (1976) Analysis of acetate non-utilizing (acu) mutants in Aspergillus nidulans. J. Gen. Microbiol. 92, 263-282
29. Cove, D. J. (1966) The induction and repression of nitrate reductase in the fungus Aspergillus nidulans. Biochim. Biophys. Acta 113, 51-56
30. Waring, R. B., May, G. S. and Morris, N. R. (1989) Characterization of an inducible expression system in Aspergillus nidulans using alcA and tubulin-coding genes. Gene 79, 119-130 (Pubitemid 19160739)
31. Langfelder, K., Gattung, S. and Brakhage, A. A. (2002) A novel method used to delete a new Aspergillus fumigatus ABC transporter-encoding gene. Curr. Genet. 41, 268-274 (Pubitemid 36075978)
32. Bustin, S. A. (2000) Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays. J. Mol. Endocrinol. 25, 169-193
33. Bustin, S. A. (2002) Quantification of mRNA using real-time reverse transcription PCR (RT-PCR): trends and problems. J. Mol. Endocrinol. 29, 23-39 (Pubitemid 34965744)
34. Larionov, A., Krause, A. and Miller, W. (2005) A standard curve based method for relative real time PCR data processing. BMC Bioinformatics 6, 62
35. Li, H., Zhou, H., Luo, Y., Ouyang, H., Hu, H. and Jin, C. (2007) Glycosylphosphatidylinositol (GPI) anchor is required in Aspergillus fumigatus for morphogenesis and virulence. Mol. Microbiol. 64, 1014-1027 (Pubitemid 46743963)
36. Fang, W., Yu, X., Wang, B., Zhou, H., Ouyang, H., Ming, J. and Jin, C. (2009) Characterization of the Aspergillus fumigatus phosphomannose isomerase Pmi1 and its impact on cell wall synthesis and morphogenesis. Microbiology 155, 3281-3293
37. Otwinowski, Z. and Minor, A. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (Pubitemid 27085611)
38. Vagin, A. and Teplyakov, A. (1997) MOLREP: an automated program for molecular replacement. J. Appl. Cryst. 30, 1022-1025 (Pubitemid 127485985)
39. Murshudov, G. N., Vagin, A. A. and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53, 240-255 (Pubitemid 27235885)
40. Emsley, P. and Cowtan, K. (2004) Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126-2132 (Pubitemid 41742764)
41. DeLano, W. L. (2004) Use of PYMOL as a communication tool for molecular science. Am. Chem. Soc. 228, Abstract 030-CHED
42. Liu, H.-Y., Wang, Z., Regni, C., Zou, X. and Tipton, P. A. (2004) Detailed kinetic studies of an aggregating inhibitor; inhibition of phosphomannomutase/phosphoglucomutase by Disperse Blue 56. Biochemistry 43, 8662-8669 (Pubitemid 38880036)
43. Mok, M. T. and Edwards, M. R. (2005) Critical sources of error in colorimetric assay for UDP-N-acetylglucosamine pyrophosphorylase. Anal. Biochem. 343, 341-343 (Pubitemid 41074050)
44. Zhou, Q., Kyazike, J., Edmunds, T. and Higgins, E. (2002) Mannose 6-phosphate quantitation in glycoproteins using high-pH anion-exchange chromatography with pulsed amperometric detection. Anal. Biochem. 306, 163-170 (Pubitemid 34791484)
45. Bensadoun, A. and Weinstein, D. (1976) Assay of proteins in the presence of interfering materials. Anal. Biochem. 70, 241-250
46. Naught, L. E., Regni, C., Beamer, L. J. and Tipton, P. A. (2003) Roles of active site residues in Pseudomonas aeruginosa phosphomannomutase/ phosphoglucomutase. Biochemistry 42, 9946-9951 (Pubitemid 37012870)
47. Romero, B., Turner, G., Olivas, I., Laborda, F. and De Lucas, J. R. (2003) The Aspergillus nidulans alcA promoter drives tightly regulated conditional gene expression in Aspergillus fumigatus permitting validation of essential genes in this human pathogen. Fungal Genet. Biol. 40, 103-114 (Pubitemid 37152531)
48. Levin, D. E. Regulation of cell wall biogenesis in Saccharomyces cerevisiae: the cell wall integrity signaling pathway. Genetics 189, 1145-1175
49. Levin, D. E. (2005) Cell wall integrity signaling in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 69, 262-291 (Pubitemid 40847940)
50. Tavares, I. M., Jolly, L., Pompeo, F., Leitao, J. H., Fialho, A. M., Sa-Correia, I. and Mengin-Lecreulx, D. (2000) Identification of the Pseudomonas aeruginosa glmM gene, encoding phosphoglucosamine mutase. J. Bacteriol. 182, 4453-4457 (Pubitemid 30599808)