Inactivation of Fructose-1,6-Bisphosphate Aldolase Prevents Optimal Co-catabolism of Glycolytic and Gluconeogenic Carbon Substrates in Mycobacterium tuberculosis

PLoS Pathogens

Volumn 10, Issue 5, 2014, Pages

  Puckett, Susan ^a   Trujillo, Carolina ^a   Eoh, Hyungjin ^a   Marrero, Joeli ^a   Spencer, John ^b   Jackson, Mary ^b   Schnappinger, Dirk ^a   Rhee, Kyu ^a   Ehrt, Sabine ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b Department of Environmental and Radiological Health Sciences   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BUTYRIC ACID DERIVATIVE; FRUCTOSE BISPHOSPHATE ALDOLASE;

ANIMAL; C57BL MOUSE; CARBOHYDRATE METABOLISM; FEMALE; GENE DELETION; GENETICS; GLUCONEOGENESIS; GLYCOLYSIS; METABOLISM; METABOLOME; MOUSE; MYCOBACTERIUM TUBERCULOSIS; TRANSGENIC ORGANISM;

ANIMALS; BUTYRATES; CARBOHYDRATE METABOLISM; FEMALE; FRUCTOSE-BISPHOSPHATE ALDOLASE; GENE DELETION; GLUCONEOGENESIS; GLYCOLYSIS; METABOLISM; METABOLOME; MICE; MICE, INBRED C57BL; MYCOBACTERIUM TUBERCULOSIS; ORGANISMS, GENETICALLY MODIFIED;

EID: 84901654908     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004144     Document Type: Article

References (44)

1. Ehrt S, Rhee K, (2013) Mycobacterium tuberculosis metabolism and host interaction: mysteries and paradoxes. Curr Top Microbiol Immunol 374: 163-188 doi:__10.1007/82_2012_299.
2. Lin PL, Rodgers M, Smith L, Bigbee M, Myers A, et al. (2009) Quantitative comparison of active and latent tuberculosis in the cynomolgus macaque model. Infect Immun 77: 4631-4642 doi:10.1128/IAI.00592-09.
3. Barry CE, Boshoff HI, Dartois V, Dick T, Ehrt S, et al. (2009) The spectrum of latent tuberculosis: rethinking the biology and intervention strategies. Nat Rev Micro 7: 845-855 doi:10.1038/nrmicro2236.
4. de Carvalho LPS, Fischer SM, Marrero J, Nathan C, Ehrt S, et al. (2010) Metabolomics of Mycobacterium tuberculosis reveals compartmentalized co-catabolism of carbon substrates. Chemistry & Biology 17: 1122-1131 doi:10.1016/j.chembiol.2010.08.009.
5. Beste DJV, Bonde B, Hawkins N, Ward JL, Beale MH, et al. (2011) 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 doi:10.1371/journal.ppat.1002091.
6. Beste DJV, Nöh K, Niedenführ S, Mendum TA, Hawkins ND, et al. (2013) 13C-Flux Spectral Analysis of Host-Pathogen Metabolism Reveals a Mixed Diet for Intracellular Mycobacterium tuberculosis. Chemistry & Biology 20: 1012-1021 doi:10.1016/j.chembiol.2013.06.012.
7. Bloch H, Segal W, (1956) Biochemical differentiation of Mycobacterium tuberculosis grown in vivo and in vitro. J Bacteriol 72: 132-141.
8. Muñoz-Elías E, McKinney J, (2005) Mycobacterium tuberculosis isocitrate lyases 1 and 2 are jointly required for in vivo growth and virulence. Nat Med 11: 638-644.
9. Pandey AK, Sassetti CM, (2008) Mycobacterial persistence requires the utilization of host cholesterol. Proc Natl Acad Sci USA 105: 4376-4380 doi:10.1073/pnas.0711159105.
10. Marrero J, Rhee KY, Schnappinger D, Pethe K, Ehrt S, (2010) 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 doi:10.1073/pnas.1000715107.
11. Marrero J, Trujillo C, Rhee KY, Ehrt S, (2013) Glucose Phosphorylation Is Required for Mycobacterium tuberculosis Persistence in Mice. PLoS Pathog 9: e1003116 doi:10.1371/journal.ppat.1003116.s006.
12. Kalscheuer R, Weinrick B, Veeraraghavan U, Besra GS, Jacobs WR, (2010) Trehalose-recycling ABC transporter LpqY-SugA-SugB-SugC is essential for virulence of Mycobacterium tuberculosis. Proc Natl Acad Sci USA 107: 21761-21766 doi:10.1073/pnas.1014642108.
13. Watanabe S, Zimmermann M, Goodwin MB, Sauer U, Barry CE, et al. (2011) Fumarate reductase activity maintains an energized membrane in anaerobic Mycobacterium tuberculosis. PLoS Pathog 7: e1002287 doi:10.1371/journal.ppat.1002287.
14. McKinney J, zu Bentrup K, Muñoz-Elías E, Miczak A, Chen B, et al. (2000) Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature 406: 735-738.
15. Blumenthal A, Trujillo C, Ehrt S, Schnappinger D, (2010) Simultaneous analysis of multiple Mycobacterium tuberculosis knockdown mutants in vitro and in vivo. PLoS ONE 5: e15667 doi:10.1371/journal.pone.0015667.
16. Kalscheuer R, Syson K, Veeraraghavan U, Weinrick B, Biermann KE, et al. (2010) Self-poisoning of Mycobacterium tuberculosis by targeting GlgE in an alpha-glucan pathway. Nat Chem Biol 6: 376-384 doi:10.1038/nchembio.340.
17. Venugopal A, Bryk R, Shi S, Rhee K, Rath P, et al. (2011) Virulence of Mycobacterium tuberculosis depends on lipoamide dehydrogenase, a member of three multienzyme complexes. Cell Host Microbe 9: 21-31 doi:10.1016/j.chom.2010.12.004.
18. Pegan S, Rukseree K, Franzblau S, Mesecar A, (2009) Structural basis for catalysis of a tetrameric class IIa fructose 1, 6-bisphosphate aldolase from Mycobacterium tuberculosis. J Mol Biol 386: 1038-1053.
19. la Paz Santangelo de M, Gest PM, Guerin ME, Coinçon M, Pham H, et al. (2011) 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 doi:10.1074/jbc.M111.259440.
20. Labbé G, Krismanich AP, de Groot S, Rasmusson T, Shang M, et al. (2012) Development of metal-chelating inhibitors for the Class II fructose 1,6-bisphosphate (FBP) aldolase. J Inorg Biochem 112: 49-58 doi:10.1016/j.jinorgbio.2012.02.032.
21. Pegan SD, Rukseree K, Capodagli GC, Baker EA, Krasnykh O, et al. (2013) Active Site Loop Dynamics of a Class IIa Fructose 1,6-Bisphosphate Aldolase from Mycobacterium tuberculosis. Biochemistry 52: 912-925 doi:10.1021/bi300928u.
22. Capodagli GC, Sedhom WG, Jackson M, Ahrendt KA, Pegan SD, (2014) A Noncompetitive Inhibitor for Mycobacterium tuberculosis's Class IIa Fructose 1,6-Bisphosphate Aldolase. Biochemistry 53: 202-213 doi:10.1021/bi401022b.
23. Griffin JE, Gawronski JD, Dejesus MA, Ioerger TR, Akerley BJ, et al. (2011) High-resolution phenotypic profiling defines genes essential for mycobacterial growth and cholesterol catabolism. PLoS Pathog 7: e1002251 doi:10.1371/journal.ppat.1002251.
24. Rosenkrands I, Slayden R, Crawford J, Aagaard C, Barry C III, et al. (2002) Hypoxic response of Mycobacterium tuberculosis studied by metabolic labeling and proteome analysis of cellular and extracellular proteins. J Bacteriol 184: 3485.
25. Ramsaywak PC, Labbé G, Siemann S, Dmitrienko GI, Guillemette JG, (2004) Molecular cloning, expression, purification, and characterization of fructose 1,6-bisphosphate aldolase from Mycobacterium tuberculosis-a novel Class II A tetramer. Protein Expr Purif 37: 220-228 doi:10.1016/j.pep.2004.05.011.
26. Cole ST, Brosch R, Parkhill J, Garnier T, Churcher C, et al. (1998) Deciphering the biology of Mycobacterium tuberculosis from the complete genome sequence. Nature 393: 537-544.
27. Bai NJ, Pai MR, Murthy PS, Venkitasubramanian TA, (1974) Effect of oxygen tension on the aldolases of Mycobacterium tuberculosis H37Rv. FEBS Lett 45: 68-70.
28. Bai N, Pai M, Murthy P, Venkitasubramanian T, (1982) Fructose-bisphosphate aldolases from mycobacteria. Methods Enzymol 90: 241-250.
29. Daher R, Therisod M, (2010) Highly Selective Inhibitors of Class II Microbial Fructose Bis-phosphate Aldolases. ACS Medicinal Chemistry Letters 1: 101-104 doi:10.1021/ml100017c.
30. Daher R, Coinçon M, Fonvielle M, Gest PM, Guerin ME, et al. (2010) Rational design, synthesis, and evaluation of new selective inhibitors of microbial class II (zinc dependent) fructose bis-phosphate aldolases. J Med Chem 53: 7836-7842 doi:10.1021/jm1009814.
31. Kim J-H, O'Brien KM, Sharma R, Boshoff HIM, Rehren G, et al. (2013) A genetic strategy to identify targets for the development of drugs that prevent bacterial persistence. Proc Natl Acad Sci USA 110: 19095-19100 doi:10.1073/pnas.1315860110.
32. Ehrt S, Guo XV, Hickey CM, Ryou M, Monteleone M, et al. (2005) Controlling gene expression in mycobacteria with anhydrotetracycline and Tet repressor. Nucleic Acids Res 33: e21 doi:10.1093/nar/gni013.
33. Griffin JE, Pandey AK, Gilmore SA, Mizrahi V, Mckinney JD, et al. (2012) Cholesterol Catabolism by Mycobacterium tuberculosis Requires Transcriptional and Metabolic Adaptations. Chemistry & Biology 19: 218-227 doi:10.1016/j.chembiol.2011.12.016.
34. Kovárová-Kovar K, Egli T, (1998) Growth kinetics of suspended microbial cells: from single-substrate-controlled growth to mixed-substrate kinetics. Microbiol Mol Biol Rev 62: 646-666.
35. Görke B, Stülke J, (2008) Carbon catabolite repression in bacteria: many ways to make the most out of nutrients. Nat Rev Micro 6: 613-624 doi:10.1038/nrmicro1932.
36. Böck A, Neidhardt FC, (1966) Isolation of a Mutant of Escherichia coli with a Temperature-sensitive Fructose-1,6-Diphosphate Aldolase Activity. J Bacteriol 92: 464-469.
37. Böck A, Neidhardt FC, (1966) Properties of a Mutant of Escherichia coli with a Temperature-sensitive Fructose-1,6-Diphosphate Aldolase. J Bacteriol 92: 470-476.
38. Schreyer R, Böck A, (1973) Phenotypic suppression of a fructose-1,6-diphosphate aldolase mutation in Escherichia coli. J Bacteriol 115: 268-276.
39. Wei J-R, Krishnamoorthy V, Murphy K, Kim J-H, Schnappinger D, et al. (2011) Depletion of antibiotic targets has widely varying effects on growth. Proc Natl Acad Sci USA 108: 4176-4181 doi:10.1073/pnas.1018301108.
40. Dartois V (2010) Immunopathology of tuberculosis disease across species. In: Leong FJ, Dartois V, Dick T, editors. A Color Atlas of Comparative Pathology of Pulmonary Tuberculosis. CRC Press.
41. Peyron P, Vaubourgeix J, Poquet Y, Levillain F, Botanch C, et al. (2008) Foamy Macrophages from Tuberculous Patients' Granulomas Constitute a Nutrient-Rich Reservoir for M. tuberculosis Persistence. PLoS Pathog 4: e1000204 doi:10.1371/journal.ppat.1000204.t003.
42. Kim M-J, Wainwright HC, Locketz M, Bekker L-G, Walther GB, et al. (2010) Caseation of human tuberculosis granulomas correlates with elevated host lipid metabolism. EMBO Mol Med 2: 258-274 doi:10.1002/emmm.201000079.
43. Eoh H, Rhee KY, (2013) Multifunctional essentiality of succinate metabolism in adaptation to hypoxia in Mycobacterium tuberculosis. Proc Natl Acad Sci USA 110: 6554-6559 doi:10.1073/pnas.1219375110.
44. Vandal OH, Pierini LM, Schnappinger D, Nathan CF, Ehrt S, (2008) A membrane protein preserves intrabacterial pH in intraphagosomal Mycobacterium tuberculosis. Nat Med 14: 849-854 doi:10.1038/nm.1795.