Two enzymes with redundant fructose bisphosphatase activity sustain gluconeogenesis and virulence in Mycobacterium tuberculosis

Nature Communications

Volumn 6, Issue , 2015, Pages

  Ganapathy, Uday ^a   Marrero, Joeli ^a   Calhoun, Susannah ^a   Eoh, Hyungjin ^a   De Carvalho, Luiz Pedro Sorio ^b   Rhee, Kyu ^a   Ehrt, Sabine ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b THE FRANCIS CRICK INSTITUTE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; FRUCTOSE BISPHOSPHATASE; GLPX PROTEIN; GPM2 PROTEIN; UNCLASSIFIED DRUG; LITHIUM;

BACTERIAL DISEASE; BACTERIUM; CATALYSIS; ENZYME ACTIVITY; FATTY ACID; GENE EXPRESSION; METABOLISM; MUTATION; PATHOGEN; RODENT; VIRULENCE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; BACTERIAL VIRULENCE; BACTERIUM MUTANT; CARBON SOURCE; CONTROLLED STUDY; ENZYME ACTIVITY; FEMALE; GENE DELETION; GENE DISRUPTION; GLUCONEOGENESIS; MICROBIAL ATTENUATION; MOUSE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; TUBERCULOSIS; ENZYMOLOGY; METABOLISM; PATHOGENICITY; VIRULENCE;

MYCOBACTERIUM TUBERCULOSIS;

FRUCTOSE-BISPHOSPHATASE; GLUCONEOGENESIS; LITHIUM; MYCOBACTERIUM TUBERCULOSIS; VIRULENCE;

EID: 84938922889     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms8912     Document Type: Article

References (54)

1. Bloch, H. and Segal, W. Biochemical differentiation of Mycobacterium tuberculosis grown in vivo and in vitro. J. Bacteriol. 72, 132-141 (1956
2. Segal, W. and Bloch, H. Pathogenic and immunogenic differentiation of Mycobacterium tuberculosis grown in vitro and in vivo. Am. Rev. Tuberc. 75, 495-500 (1957
3. Ehrt, S. and Rhee, K. Mycobacterium tuberculosis metabolism and host interaction: mysteries and paradoxes. Curr. Top. Microbiol. Immunol. 374, 163-188 (2013
4. Munoz-Elias, E. J. and McKinney, J. D. Mycobacterium tuberculosis isocitrate lyases 1 and 2 are jointly required for in vivo growth and virulence. Nat. Med. 11, 638-644 (2005
5. Gould, T. A., van de Langemheen, H., Munoz-Elias, E. J., McKinney, J. D. and Sacchettini, J. C. Dual role of isocitrate lyase 1 in the glyoxylate and methylcitrate cycles in Mycobacterium tuberculosis. Mol. Microbiol. 61, 940-947 (2006
6. Eoh, H. and Rhee, K. Y. Methylcitrate cycle defines the bactericidal essentiality of isocitrate lyase for survival of Mycobacterium tuberculosis on fatty acids. Proc. Natl Acad. Sci. USA 111, 4976-4981 (2014
7. Marrero, J., Rhee, K. Y., Schnappinger, D., Pethe, K. and Ehrt, S. Gluconeogenic carbon flow of tricarboxylic acid cycle intermediates is critical for Mycobacterium tuberculosis to establish and maintain infection. Proc. Natl Acad. Sci. USA 107, 9819-9824 (2010
8. Beste, D. J. et al. (1)(3)C metabolic flux analysis identifies an unusual route for pyruvate dissimilation in mycobacteria which requires isocitrate lyase and carbon dioxide fixation. PLoS Pathog. 7, e1002091 (2011
9. Puckett, S. et al. Inactivation of fructose-1,6-bisphosphate aldolase prevents optimal co-catabolism of glycolytic and gluconeogenic carbon substrates in Mycobacterium tuberculosis. PLoS Pathog. 10, e1004144 (2014
10. Trujillo, C. et al. Triosephosphate isomerase is dispensable in vitro yet essential for Mycobacterium tuberculosis to establish infection. MBio 5, e00085 (2014
11. Fujita, Y. et al. Identification and expression of the Bacillus subtilis fructose-1, 6-bisphosphatase gene (fbp). J. Bacteriol. 180, 4309-4313 (1998
12. Donahue, J. L., Bownas, J. L., Niehaus, W. G. and Larson, T. J. Purification and characterization of glpX-encoded fructose 1, 6-bisphosphatase, a new enzyme of the glycerol 3-phosphate regulon of Escherichia coli. J. Bacteriol. 182, 5624-5627 (2000
13. Hines, J. K., Fromm, H. J. and Honzatko, R. B. Novel allosteric activation site in Escherichia coli fructose-1,6-bisphosphatase. J. Biol. Chem. 281, 18386-18393 (2006
14. Sedivy, J. M., Daldal, F. and Fraenkel, D. G. Fructose bisphosphatase of Escherichia coli: cloning of the structural gene (fbp) and preparation of a chromosomal deletion. J. Bacteriol. 158, 1048-1053 (1984
15. Stec, B., Yang, H., Johnson, K. A., Chen, L. and Roberts, M. F. MJ0109 is an enzyme that is both an inositol monophosphatase and the missing archaeal fructose-1,6-bisphosphatase. Nat. Struct. Biol. 7, 1046-1050 (2000
16. Fushinobu, S., Nishimasu, H., Hattori, D., Song, H. J. and Wakagi, T. Structural basis for the bifunctionality of fructose-1,6-bisphosphate aldolase/phosphatase. Nature 478, 538-541 (2011
17. Rashid, N. et al. A novel candidate for the true fructose-1,6-bisphosphatase in archaea. J. Biol. Chem. 277, 30649-30655 (2002
18. Sato, T. et al. Genetic evidence identifying the true gluconeogenic fructose-1,6- bisphosphatase in Thermococcus kodakaraensis and other hyperthermophiles. J. Bacteriol. 186, 5799-5807 (2004
19. Say, R. F. and Fuchs, G. Fructose 1,6-bisphosphate aldolase/phosphatase may be an ancestral gluconeogenic enzyme. Nature 464, 1077-1081 (2010
20. Du, J., Say, R. F., Lu, W., Fuchs, G. and Einsle, O. Active-site remodelling in the bifunctional fructose-1,6-bisphosphate aldolase/phosphatase. Nature 478, 534-537 (2011
21. York, J. D., Ponder, J. W. and Majerus, P. W. Definition of a metal-dependent/ Li(+)-inhibited phosphomonoesterase protein family based upon a conserved three-dimensional core structure. Proc. Natl Acad. Sci. USA 92, 5149-5153 (1995
22. Movahedzadeh, F. et al. The Mycobacterium tuberculosis Rv1099c gene encodes a GlpX-like class II fructose 1,6-bisphosphatase. Microbiology 150, 3499-3505 (2004
23. Gutka, H. J., Rukseree, K., Wheeler, P. R., Franzblau, S. G. and Movahedzadeh, F. glpX gene of Mycobacterium tuberculosis: heterologous expression, purification, and enzymatic characterization of the encoded fructose 1,6-bisphosphatase II. Appl. Biochem. Biotechnol. 164, 1376-1389 (2011
24. Beste, D. J. et al. The genetic requirements for fast and slow growth in mycobacteria. PLoS ONE 4, e5349 (2009
25. DeJesus, M. A. and Ioerger, T. R. A Hidden Markov Model for identifying essential and growth-defect regions in bacterial genomes from transposon insertion sequencing data. BMC Bioinformatics 14, 303 (2013
26. Watkins, H. A. and Baker, E. N. Structural and functional analysis of Rv3214 from Mycobacterium tuberculosis, a protein with conflicting functional annotations, leads to its characterization as a phosphatase. J. Bacteriol. 188, 3589-3599 (2006
27. Leech, A. P., Baker, G. R., Shute, J. K., Cohen, M. A. and Gani, D. Chemical and kinetic mechanism of the inositol monophosphatase reaction and its inhibition by Li+. Eur. J. Biochem. 212, 693-704 (1993
28. Kuznetsova, E. et al. Structure and activity of the metal-independent fructose- 1,6-bisphosphatase YK23 from Saccharomyces cerevisiae. J. Biol. Chem. 285, 21049-21059 (2010
29. Clasquin, M. F. et al. Riboneogenesis in yeast. Cell 145, 969-980 (2011
30. de Carvalho, L. P. et al. Metabolomics of Mycobacterium tuberculosis reveals compartmentalized co-catabolism of carbon substrates. Chem. Biol. 17, 1122-1131 (2010
31. Gu, X. et al. Rv2131c gene product: an unconventional enzyme that is both inositol monophosphatase and fructose-1,6-bisphosphatase. Biochem. Biophys. Res. Commun. 339, 897-904 (2006
32. Hatzios, S. K., Iavarone, A. T. and Bertozzi, C. R. Rv2131c from Mycobacterium tuberculosis is a CysQ 3-phosphoadenosine-5-phosphatase. Biochemistry 47, 5823-5831 (2008
33. Jules, M., Le Chat, L., Aymerich, S. and Le Coq, D. The Bacillus subtilis ywjI (glpX) gene encodes a class II fructose-1,6-bisphosphatase, functionally equivalent to the class III Fbp enzyme. J. Bacteriol. 191, 3168-3171 (2009
34. Derman, A. I., Prinz, W. A., Belin, D. and Beckwith, J. Mutations that allow disulfide bond formation in the cytoplasm of Escherichia coli. Science 262, 1744-1747 (1993
35. Jardon, R., Gancedo, C. and Flores, C. L. The gluconeogenic enzyme fructose-1,6- bisphosphatase is dispensable for growth of the yeast Yarrowia lipolytica in gluconeogenic substrates. Eukaryot. Cell 7, 1742-1749 (2008
36. Watkins, H. A., Yu, M. and Baker, E. N. Cloning, expression, purification and preliminary crystallographic data for Rv3214 (EntD), a predicted cofactordependent phosphoglycerate mutase from Mycobacterium tuberculosis. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 61, 753-755 (2005
37. Rifat, D., Bishai, W. R. and Karakousis, P. C. Phosphate depletion: a novel trigger for Mycobacterium tuberculosis persistence. J. Infect. Dis. 200, 1126-1135 (2009
38. Nakahigashi, K. et al. Systematic phenome analysis of Escherichia coli multipleknockout mutants reveals hidden reactions in central carbon metabolism. Mol. Syst. Biol. 5, 306 (2009
39. Bennett, B. D. et al. Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli. Nat. Chem. Biol. 5, 593-599 (2009
40. Singh, K. D., Schmalisch, M. H., Stulke, J. and Gorke, B. Carbon catabolite repression in Bacillus subtilis: quantitative analysis of repression exerted by different carbon sources. J. Bacteriol. 190, 7275-7284 (2008
41. Marrero, J., Trujillo, C., Rhee, K. Y. and Ehrt, S. Glucose phosphorylation is required for Mycobacterium tuberculosis persistence in mice. PLoS Pathog. 9, e1003116 (2013
42. Bock, A. and Neidhardt, F. C. Isolation of a mutant of Escherichia coli with a temperature-sensitive fructose-1,6-diphosphate aldolase activity. J. Bacteriol. 92, 464-469 (1966
43. Bock, A. and Neidhardt, F. C. Properties of a mutant of Escherichia coli with a temperature-sensitive fructose-1,6-diphosphate aldolase. J. Bacteriol. 92, 470-476 (1966
44. de la Paz Santangelo, M. et al. Glycolytic and non-glycolytic functions of Mycobacterium tuberculosis fructose-1,6-bisphosphate aldolase, an essential enzyme produced by replicating and non-replicating bacilli. J. Biol. Chem. 286, 40219-40231 (2011
45. Brown, G. et al. Structural and biochemical characterization of the type II fructose-1,6-bisphosphatase GlpX from Escherichia coli. J. Biol. Chem. 284, 3784-3792 (2009
46. Rigden, D. J. The histidine phosphatase superfamily: structure and function. Biochem. J. 409, 333-348 (2008
47. Eoh, H. and Rhee, K. Y. Multifunctional essentiality of succinate metabolism in adaptation to hypoxia in Mycobacterium tuberculosis. Proc. Natl Acad. Sci. USA 110, 6554-6559 (2013
48. Bardarov, S. et al. Conditionally replicating mycobacteriophages: a system for transposon delivery to Mycobacterium tuberculosis. Proc. Natl Acad. Sci. USA 94, 10961-10966 (1997
49. Glickman, M. S., Cox, J. S. and Jacobs, Jr W. R. A novel mycolic acid cyclopropane synthetase is required for cording, persistence, and virulence of Mycobacterium tuberculosis. Mol. Cell 5, 717-727 (2000
50. Gee, C. L. et al. A phosphorylated pseudokinase complex controls cell wall synthesis in mycobacteria. Sci. Signal. 5, ra7 (2012
51. Rittmann, D., Schaffer, S., Wendisch, V. F. and Sahm, H. Fructose-1,6- bisphosphatase from Corynebacterium glutamicum: expression and deletion of the fbp gene and biochemical characterization of the enzyme. Arch. Microbiol. 180, 285-292 (2003
52. Lin, G. et al. Mycobacterium tuberculosis prcBA genes encode a gated proteasome with broad oligopeptide specificity. Mol. Microbiol. 59, 1405-1416 (2006
53. Shevchenko, A., Wilm, M., Vorm, O. and Mann, M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858 (1996
54. Kall, L., Canterbury, J. D., Weston, J., Noble, W. S. and MacCoss, M. J. Semi-supervised learning for peptide identification from shotgun proteomics datasets. Nat. Methods 4, 923-925 (2007