Succinate Dehydrogenase is the Regulator of Respiration in

English version České info

This work establishes the principle that Mycobacterium tuberculosis undergoes a metabolic remodeling as oxygen concentrations fall that serves to decrease its rate of oxygen consumption and therefore oxidative phosphorylation. Furthermore, cells can be stimulated to respire, even in low oxygen conditions, by providing reducing equivalents to the respiratory chain by either genetic manipulation (deletion of succinate dehydrogenase) or by exogenous addition of reducing agents such as DTT. Thus, activation of persister cells may be accomplished by increasing their respiration rate in low oxygen conditions. These findings will inform the design of novel drug screens which should seek enhancers of cellular respiration to find compounds which will serve to shorten the duration of TB chemotherapy.

Vyšlo v časopise: Succinate Dehydrogenase is the Regulator of Respiration in. PLoS Pathog 10(11): e32767. doi:10.1371/journal.ppat.1004510
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004510

Souhrn

Zdroje

1. World Health Organization (2013) Global Tuberculosis Report 2013. 2013th ed. Geneva, Switzerland: WHO Press. Available: http://apps.who.int/iris/handle/10665/91355.

2. TufarielloJM, ChanJ, FlynnJL (2003) Latent tuberculosis: mechanisms of host and bacillus that contribute to persistent infection. Lancet Infect Dis 3: 578–590 Available: http://www.ncbi.nlm.nih.gov/pubmed/12954564

3. GengenbacherM, KaufmannSHE (2012) Mycobacterium tuberculosis: success through dormancy. FEMS Microbiol Rev 36: 514–532 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3319523&tool=pmcentrez&rendertype=abstract

4. CORPERHJ, COHNML (1951) The viability and virulence of old cultures of tubercle bacilli; studies on 30-year-old broth cultures maintained at 37 degrees C. Tubercle 32: 232–237 Available: http://www.ncbi.nlm.nih.gov/pubmed/14893467

5. WayneLG, HayesLG (1996) An in vitro model for sequential study of shiftdown of Mycobacterium tuberculosis through two stages of nonreplicating persistence. Infect Immun 64: 2062–2069 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=174037&tool=pmcentrez&rendertype=abstract

6. GengenbacherM, RaoSPS, PetheK, DickT (2010) Nutrient-starved, non-replicating Mycobacterium tuberculosis requires respiration, ATP synthase and isocitrate lyase for maintenance of ATP homeostasis and viability. Microbiology 156: 81–87 Available: http://mic.sgmjournals.org/cgi/content/abstract/156/1/81

7. WatanabeS, ZimmermannM, GoodwinMB, SauerU, BarryCE, et al. (2011) Fumarate reductase activity maintains an energized membrane in anaerobic Mycobacterium tuberculosis. PLoS Pathog 7: e1002287 Available: http://dx.plos.org/10.1371/journal.ppat.1002287

8. KoulA, VranckxL, DendougaN, BalemansW, Van den WyngaertI, et al. (2008) Diarylquinolines are bactericidal for dormant mycobacteria as a result of disturbed ATP homeostasis. J Biol Chem 283: 25273–25280 Available: http://www.ncbi.nlm.nih.gov/pubmed/18625705

9. Beste DJV, EspasaM, BondeB, KierzekAM, StewartGR, et al. (2009) The genetic requirements for fast and slow growth in mycobacteria. PLoS One 4: e5349 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2685279&tool=pmcentrez&rendertype=abstract

10. SassettiCM, RubinEJ (2003) Genetic requirements for mycobacterial survival during infection. Proc Natl Acad Sci U S A 100: 12989–12994 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=240732&tool=pmcentrez&rendertype=abstract

11. KaushalD, SchroederBG, TyagiS, YoshimatsuT, ScottC, et al. (2002) Reduced immunopathology and mortality despite tissue persistence in a Mycobacterium tuberculosis mutant lacking alternative sigma factor, SigH. Proc Natl Acad Sci U S A 99: 8330–8335 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=123067&tool=pmcentrez&rendertype=abstract

12. ZhangYJ, ReddyMC, IoergerTR, RothchildAC, DartoisV, et al. (2013) Tryptophan biosynthesis protects mycobacteria from CD4 T-cell-mediated killing. Cell 155: 1296–1308 Available: http://www.sciencedirect.com/science/article/pii/S0092867413013639

13. ZhangY, YewWW, BarerMR (2012) Targeting persisters for tuberculosis control. Antimicrob Agents Chemother 56: 2223–2230 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3346619&tool=pmcentrez&rendertype=abstract

14. BerneyM, CookGM (2010) Unique flexibility in energy metabolism allows mycobacteria to combat starvation and hypoxia. PLoS One 5: e8614 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2799521&tool=pmcentrez&rendertype=abstract

15. BardarovS, BardarovSJr, PavelkaMSJr, SambandamurthyV, LarsenM, et al. (2002) Specialized transduction: an efficient method for generating marked and unmarked targeted gene disruptions in Mycobacterium tuberculosis, M. bovis BCG and M. smegmatis. Microbiology 148: 3007–3017 Available: http://www.ncbi.nlm.nih.gov/pubmed/12368434

16. JainP, HsuT, AraiM, BiermannK, ThalerDS, et al. (2014) Specialized transduction designed for precise high-throughput unmarked deletions in Mycobacterium tuberculosis. MBio 5: e01245–14 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=4049104&tool=pmcentrez&rendertype=abstract

17. CecchiniG, SchröderI, GunsalusRP, MaklashinaE (2002) Succinate dehydrogenase and fumarate reductase from Escherichia coli. Biochim Biophys Acta 1553: 140–157 Available: http://www.ncbi.nlm.nih.gov/pubmed/11803023

18. LemosRS, FernandesAS, PereiraMM, GomesCM, TeixeiraM (2002) Quinol:fumarate oxidoreductases and succinate:quinone oxidoreductases: phylogenetic relationships, metal centres and membrane attachment. Biochim Biophys Acta 1553: 158–170 Available: http://www.ncbi.nlm.nih.gov/pubmed/11803024

19. Drancourt M, Bavesh D.Kana, Machowski EE, Schechter N, Teh J-S, et al.. (2009) Mycobacterium: Genomics and Molecular Biology. Caister Academic Press. Available: http://books.google.com/books?hl=en&lr=&id=2UFkCKT6K8sC&pgis=1.

20. BaughnAD, GarforthSJ, VilchèzeC, JacobsWR (2009) An anaerobic-type alpha-ketoglutarate ferredoxin oxidoreductase completes the oxidative tricarboxylic acid cycle of Mycobacterium tuberculosis. PLoS Pathog 5: e1000662 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2773412&tool=pmcentrez&rendertype=abstract

21. EohH, RheeKY (2013) Multifunctional essentiality of succinate metabolism in adaptation to hypoxia in Mycobacterium tuberculosis. Proc Natl Acad Sci U S A 110: 6554–6559 Available: http://www.pnas.org/content/110/16/6554.short

22. PecsiI, HardsK, EkanayakaN, BerneyM, HartmanT, et al. (2014) Essentiality of Succinate Dehydrogenase in Mycobacterium smegmatis and Its Role in the Generation of the Membrane Potential Under Hypoxia. MBio 5: e01093–14 Available: http://www.ncbi.nlm.nih.gov/pubmed/25118234

23. FelleH, PorterJS, SlaymanCL, KabackHR (1980) Quantitative measurements of membrane potential in Escherichia coli. Biochemistry 19: 3585–3590 Available: http://pubs.acs.org/doi/abs/10.1021/bi00556a026

24. MadejMG, NasiriHR, HilgendorffNS, SchwalbeH, UndenG, et al. (2006) Experimental evidence for proton motive force-dependent catalysis by the diheme-containing succinate:menaquinone oxidoreductase from the Gram-positive bacterium Bacillus licheniformis. Biochemistry 45: 15049–15055 Available: http://dx.doi.org/10.1021/bi0618161

25. SchirawskiJ, UndenG (1998) Menaquinone-dependent succinate dehydrogenase of bacteria catalyzes reversed electron transport driven by the proton potential. Eur J Biochem 257: 210–215 Available: http://www.ncbi.nlm.nih.gov/pubmed/9799121

26. Cox RA, Cook GM (2007) Growth regulation in the mycobacterial cell. Curr Mol Med: 231–245. Available: http://www.ingentaconnect.com/content/ben/cmm/2007/00000007/00000003/art00002.

27. KrögerA, KlingenbergM (1973) The kinetics of the redox reactions of ubiquinone related to the electron-transport activity in the respiratory chain. Eur J Biochem 34: 358–368 Available: http://www.ncbi.nlm.nih.gov/pubmed/4351161

28. DryIB, MooreAL, DayDA, WiskichJT (1989) Regulation of alternative pathway activity in plant mitochondria: nonlinear relationship between electron flux and the redox poise of the quinone pool. Arch Biochem Biophys 273: 148–157 Available: http://www.sciencedirect.com/science/article/pii/0003986189901732

29. LemmaE, UndenG, KrögerA (1990) Menaquinone is an obligatory component of the chain catalyzing succinate respiration in Bacillus subtilis. Arch Microbiol 155: 62–67 Available: http://link.springer.com/article/10.1007/BF00291276

30. ZhangYJ, IoergerTR, HuttenhowerC, LongJE, SassettiCM, et al. (2012) Global Assessment of Genomic Regions Required for Growth in Mycobacterium tuberculosis. PLoS Pathog 8: e1002946 Available: http://www.plospathogens.org/article/info%3Adoi%2F10.1371%2Fjournal.ppat.1002946#

31. KaufmannSH, LadelCH (1994) Role of T cell subsets in immunity against intracellular bacteria: experimental infections of knock-out mice with Listeria monocytogenes and Mycobacterium bovis BCG. Immunobiology 191: 509–519 Available: http://www.ncbi.nlm.nih.gov/pubmed/7713565

32. TsaiMC, ChakravartyS, ZhuG, XuJ, TanakaK, et al. (2006) Characterization of the tuberculous granuloma in murine and human lungs: cellular composition and relative tissue oxygen tension. Cell Microbiol 8: 218–232 Available: http://www.ncbi.nlm.nih.gov/pubmed/16441433

33. DriverER, RyanGJ, HoffDR, IrwinSM, BasarabaRJ, et al. (2012) Evaluation of a mouse model of necrotic granuloma formation using C3HeB/FeJ mice for testing of drugs against Mycobacterium tuberculosis. Antimicrob Agents Chemother 56: 3181–3195 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3370740&tool=pmcentrez&rendertype=abstract

34. WayneLG, SohaskeyCD (2001) Nonreplicating persistence of mycobacterium tuberculosis. Annu Rev Microbiol 55: 139–163 Available: http://www.annualreviews.org/doi/pdf/10.1146/annurev.micro.55.1.139

35. LoebelRO, ShorrE, RichardsonHB (1933) The Influence of Adverse Conditions upon the Respiratory Metabolism and Growth of Human Tubercle Bacilli. J Bacteriol 26: 167–200 Available: http://www.ncbi.nlm.nih.gov/pmc/articles/PMC533551/

36. WayneLG, HayesLG (1996) An in vitro model for sequential study of shiftdown of Mycobacterium tuberculosis through two stages of nonreplicating persistence. Infect Immun 64: 2062–2069 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=174037&tool=pmcentrez&rendertype=abstract

37. ElliottSJ, LégerC, PershadHR, HirstJ, HeffronK, et al. (2002) Detection and interpretation of redox potential optima in the catalytic activity of enzymes. Biochim Biophys Acta 1555: 54–59 Available: http://www.ncbi.nlm.nih.gov/pubmed/12206891

38. WangQ, ZhangY, YangC, XiongH (2010) Acetylation of metabolic enzymes coordinates carbon source utilization and metabolic flux. Science 327: 1004–1007 Available: http://stke.sciencemag.org/cgi/content/abstract/sci;327/5968/1004

39. NamT-W, ParkY-H, JeongH-J, RyuS, SeokY-J (2005) Glucose repression of the Escherichia coli sdhCDAB operon, revisited: regulation by the CRP*cAMP complex. Nucleic Acids Res 33: 6712–6722 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1297706&tool=pmcentrez&rendertype=abstract

40. ZhangZ, HuangL, ShulmeisterVM, ChiYI, KimKK, et al. (1998) Electron transfer by domain movement in cytochrome bc1. Nature 392: 677–684 Available: http://www.ncbi.nlm.nih.gov/pubmed/9565029

41. HunteC, PalsdottirH, TrumpowerBL (2003) Protonmotive pathways and mechanisms in the cytochrome bc1 complex. FEBS Lett 545: 39–46 Available: http://linkinghub.elsevier.com/retrieve/pii/S0014579303003910

42. MitchellP (1975) Protonmotive redox mechanism of the cytochrome b-c1 complex in the respiratory chain: protonmotive ubiquinone cycle. FEBS Lett 56: 1–6 Available: http://ukpmc.ac.uk/abstract/MED/239860

43. BekkerM, KramerG, HartogAF, WagnerMJ, de KosterCG, et al. (2007) Changes in the redox state and composition of the quinone pool of Escherichia coli during aerobic batch-culture growth. Microbiology 153: 1974–1980 Available: http://mic.sgmjournals.org/content/153/6/1974.full

44. VoskuilMI (2004) Mycobacterium tuberculosis gene expression during environmental conditions associated with latency. Tuberculosis (Edinb) 84: 138–143 Available: http://www.ncbi.nlm.nih.gov/pubmed/15207483

45. ShiL, SohaskeyCD, KanaBD, DawesS, NorthRJ, et al. (2005) Changes in energy metabolism of Mycobacterium tuberculosis in mouse lung and under in vitro conditions affecting aerobic respiration. Proc Natl Acad Sci U S A 102: 15629–15634 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1255738&tool=pmcentrez&rendertype=abstract

46. De SouzaN (2007) Too much of a good thing. Nat Methods 4: 386–386 Available: http://www.nature.com/nature/journal/vaop/ncurrent/full/472159a.html

47. AndreuJ, CáceresJ, PallisaE, Martinez-RodriguezM (2004) Radiological manifestations of pulmonary tuberculosis. Eur J Radiol 51: 139–149 Available: http://www.ncbi.nlm.nih.gov/pubmed/15246519

48. MitchisonDA, ChangKC (2009) Experimental models of tuberculosis: can we trust the mouse? Am J Respir Crit Care Med 180: 201–202 Available: http://www.ncbi.nlm.nih.gov/pubmed/19633155

49. YoungD (2009) Animal models of tuberculosis. Eur J Immunol 39: 2011–2014 Available: http://www.ncbi.nlm.nih.gov/pubmed/19672894

50. BarryCE, BoshoffHI, DartoisV, DickT, EhrtS, et al. (2009) The spectrum of latent tuberculosis: rethinking the biology and intervention strategies. Nat Rev Microbiol 7: 845–855 Available: http://www.ncbi.nlm.nih.gov/pubmed/19855401

51. GomezJE, McKinneyJD (2004) M. tuberculosis persistence, latency, and drug tolerance. Tuberculosis 84: 29–44 Available: http://linkinghub.elsevier.com/retrieve/pii/S1472979203000866

52. NeyrollesO, Hernández-PandoR, Pietri-RouxelF, FornèsP, TailleuxL, et al. (2006) Is adipose tissue a place for Mycobacterium tuberculosis persistence? PLoS One 1: e43 Available: http://dx.plos.org/10.1371/journal.pone.0000043

53. DasB, KashinoSS, PuluI, KalitaD, SwamiV, et al. (2013) CD271+ Bone Marrow Mesenchymal Stem Cells May Provide a Niche for Dormant Mycobacterium tuberculosis. Sci Transl Med 5: 170ra13 Available: http://www.ncbi.nlm.nih.gov/pubmed/23363977

54. FilippiniP, IonaE, PiccaroG, PeyronP, NeyrollesO, et al. (2010) Activity of drug combinations against dormant Mycobacterium tuberculosis. Antimicrob Agents Chemother 54: 2712–2715 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2876400&tool=pmcentrez&rendertype=abstract

55. De CarvalhoLPS, FischerSM, MarreroJ, NathanC, EhrtS, et al. (2010) Metabolomics of Mycobacterium tuberculosis reveals compartmentalized co-catabolism of carbon substrates. Chem Biol 17: 1122–1131 Available: http://www.ncbi.nlm.nih.gov/pubmed/21035735

56. BorisovVB, MuraliR, VerkhovskayaML, Bloch Da, HanH, et al. (2011) Aerobic respiratory chain of Escherichia coli is not allowed to work in fully uncoupled mode. Proc Natl Acad Sci U S A 108: 17320–17324 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3198357&tool=pmcentrez&rendertype=abstract

57. BaekS-H, LiAH, SassettiCM (2011) Metabolic regulation of mycobacterial growth and antibiotic sensitivity. PLoS Biol 9: e1001065 Available: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3101192&tool=pmcentrez&rendertype=abstract

58. AndriesK, VerhasseltP, GuillemontJ, GöhlmannHWH, NeefsJ-M, et al. (2005) A diarylquinoline drug active on the ATP synthase of Mycobacterium tuberculosis. Science 307: 223–227 Available: http://www.ncbi.nlm.nih.gov/pubmed/15591164

59. DiaconAH, PymA (2009) The diarylquinoline TMC207 for multidrug-resistant tuberculosis. N Engl J Med 360: 2397–2405 Available: http://www.nejm.org/doi/full/10.1056/nejmoa0808427

60. DiaconAH, DawsonR, von Groote-BidlingmaierF, SymonsG, VenterA, et al. (2012) 14-day bactericidal activity of PA-824, bedaquiline, pyrazinamide, and moxifloxacin combinations: a randomised trial. Lancet 380: 986–993 Available: http://www.ncbi.nlm.nih.gov/pubmed/22828481

61. SambandamurthyVK, WangX, ChenB, RussellRG, DerrickS, et al. (2002) A pantothenate auxotroph of Mycobacterium tuberculosis is highly attenuated and protects mice against tuberculosis. Nat Med 8: 1171–1174 Available: http://www.ncbi.nlm.nih.gov/pubmed/12219086

62. NotredameC, HigginsDG, HeringaJ (2000) T-Coffee: A novel method for fast and accurate multiple sequence alignment. J Mol Biol 302: 205–217 Available: http://www.ncbi.nlm.nih.gov/pubmed/10964570

63. PagliaG, HrafnsdóttirS, MagnúsdóttirM, FlemingRMT, ThorlaciusS, et al. (2012) Monitoring metabolites consumption and secretion in cultured cells using ultra-performance liquid chromatography quadrupole-time of flight mass spectrometry (UPLC-Q-ToF-MS). Anal Bioanal Chem 402: 1183–1198 Available: http://www.ncbi.nlm.nih.gov/pubmed/22159369