Impact of ROS-Induced Damage of TCA Cycle Enzymes on Metabolism and Virulence of Salmonella enterica serovar Typhimurium

Noster J, Persicke M, Chao T-C, Krone L, Heppner B, Hensel M, Hansmeier N (2019)
FRONTIERS IN MICROBIOLOGY 10: 762.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
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Autor*in
Noster, Janina; Persicke, MarcusUniBi; Chao, Tzu-Chiao; Krone, Lena; Heppner, Bianca; Hensel, Michael; Hansmeier, Nicole
Abstract / Bemerkung
Salmonella enterica serovar Typhimurium (STM) is exposed to reactive oxygen species (ROS) originating from aerobic respiration, antibiotic treatment, and the oxidative burst occurring inside the Salmonella-containing vacuole (SCV) within host cells. ROS damage cellular compounds, thereby impairing bacterial viability and inducing cell death. Proteins containing iron-sulfur (Fe-S) clusters are particularly sensitive and become non-functional upon oxidation. Comprising five enzymes with Fe-S clusters, the TCA cycle is a pathway most sensitive toward ROS. To test the impact of ROS-mediated metabolic perturbations on bacterial physiology, we analyzed the proteomic and metabolic profile of STM deficient in both cytosolic superoxide dismutases (Delta sodAB). Incapable of detoxifying superoxide anions (SOA), endogenously generated SOA accumulate during growth. Delta sodAB showed reduced abundance of aconitases, leading to a metabolic profile similar to that of an aconitase-deficient strain (Delta acnAB). Furthermore, we determined a decreased expression of acnA in STM Delta sodAB. While intracellular proliferation in RAW264.7 macrophages and survival of methyl viologen treatment were not reduced for STM Delta acnAB, proteomic profiling revealed enhanced stress response. We conclude that ROS-mediated reduced expression and damage of aconitase does not impair bacterial viability or virulence, but might increase ROS amounts in STM, which reinforces the bactericidal effects of antibiotic treatment and immune responses of the host.
Stichworte
metabolomics; oxidative stress; iron-sulfur cluster damage; aconitase; superoxide dismutase
Erscheinungsjahr
2019
Zeitschriftentitel
FRONTIERS IN MICROBIOLOGY
Band
10
Art.-Nr.
762
ISSN
1664-302X
Page URI
https://pub.uni-bielefeld.de/record/2935582

Zitieren

Noster J, Persicke M, Chao T-C, et al. Impact of ROS-Induced Damage of TCA Cycle Enzymes on Metabolism and Virulence of Salmonella enterica serovar Typhimurium. FRONTIERS IN MICROBIOLOGY. 2019;10: 762.
Noster, J., Persicke, M., Chao, T. - C., Krone, L., Heppner, B., Hensel, M., & Hansmeier, N. (2019). Impact of ROS-Induced Damage of TCA Cycle Enzymes on Metabolism and Virulence of Salmonella enterica serovar Typhimurium. FRONTIERS IN MICROBIOLOGY, 10, 762. doi:10.3389/fmicb.2019.00762
Noster, J., Persicke, M., Chao, T. - C., Krone, L., Heppner, B., Hensel, M., and Hansmeier, N. (2019). Impact of ROS-Induced Damage of TCA Cycle Enzymes on Metabolism and Virulence of Salmonella enterica serovar Typhimurium. FRONTIERS IN MICROBIOLOGY 10:762.
Noster, J., et al., 2019. Impact of ROS-Induced Damage of TCA Cycle Enzymes on Metabolism and Virulence of Salmonella enterica serovar Typhimurium. FRONTIERS IN MICROBIOLOGY, 10: 762.
J. Noster, et al., “Impact of ROS-Induced Damage of TCA Cycle Enzymes on Metabolism and Virulence of Salmonella enterica serovar Typhimurium”, FRONTIERS IN MICROBIOLOGY, vol. 10, 2019, : 762.
Noster, J., Persicke, M., Chao, T.-C., Krone, L., Heppner, B., Hensel, M., Hansmeier, N.: Impact of ROS-Induced Damage of TCA Cycle Enzymes on Metabolism and Virulence of Salmonella enterica serovar Typhimurium. FRONTIERS IN MICROBIOLOGY. 10, : 762 (2019).
Noster, Janina, Persicke, Marcus, Chao, Tzu-Chiao, Krone, Lena, Heppner, Bianca, Hensel, Michael, and Hansmeier, Nicole. “Impact of ROS-Induced Damage of TCA Cycle Enzymes on Metabolism and Virulence of Salmonella enterica serovar Typhimurium”. FRONTIERS IN MICROBIOLOGY 10 (2019): 762.

71 References

Daten bereitgestellt von Europe PubMed Central.

Regulatory and structural differences in the Cu,Zn-superoxide dismutases of Salmonella enterica and their significance for virulence.
Ammendola S, Pasquali P, Pacello F, Rotilio G, Castor M, Libby SJ, Figueroa-Bossi N, Bossi L, Fang FC, Battistoni A., J. Biol. Chem. 283(20), 2008
PMID: 18362154
Gene ontology: tool for the unification of biology. The Gene Ontology Consortium.
Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G., Nat. Genet. 25(1), 2000
PMID: 10802651
Salmonella detoxifying enzymes are sufficient to cope with the host oxidative burst.
Aussel L, Zhao W, Hebrard M, Guilhon AA, Viala JP, Henri S, Chasson L, Gorvel JP, Barras F, Meresse S., Mol. Microbiol. 80(3), 2011
PMID: 21362067
Characterization of Salmonella enterica serovar Typhimurium aconitase A.
Baothman OA, Rolfe MD, Green J., Microbiology (Reading, Engl.) 159(Pt 6), 2013
PMID: 23637460
Bactericidal Antibiotics Induce Toxic Metabolic Perturbations that Lead to Cellular Damage.
Belenky P, Ye JD, Porter CB, Cohen NR, Lobritz MA, Ferrante T, Jain S, Korry BJ, Schwarz EG, Walker GC, Collins JJ., Cell Rep 13(5), 2015
PMID: 26565910
An incomplete TCA cycle increases survival of Salmonella Typhimurium during infection of resting and activated murine macrophages.
Bowden SD, Ramachandran VK, Knudsen GM, Hinton JC, Thompson A., PLoS ONE 5(11), 2010
PMID: 21079785
The iron-sulfur clusters in Escherichia coli succinate dehydrogenase direct electron flow.
Cheng VW, Ma E, Zhao Z, Rothery RA, Weiner JH., J. Biol. Chem. 281(37), 2006
PMID: 16864590
Reserve Flux Capacity in the Pentose Phosphate Pathway Enables Escherichia coli's Rapid Response to Oxidative Stress.
Christodoulou D, Link H, Fuhrer T, Kochanowski K, Gerosa L, Sauer U., Cell Syst 6(5), 2018
PMID: 29753645
One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products.
Datsenko KA, Wanner BL., Proc. Natl. Acad. Sci. U.S.A. 97(12), 2000
PMID: 10829079
Periplasmic superoxide dismutase protects Salmonella from products of phagocyte NADPH-oxidase and nitric oxide synthase.
De Groote MA, Ochsner UA, Shiloh MU, Nathan C, McCord JM, Dinauer MC, Libby SJ, Vazquez-Torres A, Xu Y, Fang FC., Proc. Natl. Acad. Sci. U.S.A. 94(25), 1997
PMID: 9391141
Metabolic Response of Escherichia coli upon Treatment with Hypochlorite at Sub-Lethal Concentrations.
Drazic A, Kutzner E, Winter J, Eisenreich W., PLoS ONE 10(5), 2015
PMID: 25932918
The inactivation of Fe-S cluster containing hydro-lyases by superoxide.
Flint DH, Tuminello JF, Emptage MH., J. Biol. Chem. 268(30), 1993
PMID: 8226748
Balance between endogenous superoxide stress and antioxidant defenses.
Gort AS, Imlay JA., J. Bacteriol. 180(6), 1998
PMID: 9515906
Two genetically-distinct and differentially-regulated aconitases (AcnA and AcnB) in Escherichia coli.
Gruer MJ, Guest JR., Microbiology (Reading, Engl.) 140 ( Pt 10)(), 1994
PMID: 8000525
Identification of Mature Atherosclerotic Plaque Proteome Signatures Using Data-Independent Acquisition Mass Spectrometry.
Hansmeier N, Buttigieg J, Kumar P, Pelle S, Choi KY, Kopriva D, Chao TC., J. Proteome Res. 17(1), 2017
PMID: 29129081
Redundant hydrogen peroxide scavengers contribute to Salmonella virulence and oxidative stress resistance.
Hebrard M, Viala JP, Meresse S, Barras F, Aussel L., J. Bacteriol. 191(14), 2009
PMID: 19447905
Functional analysis of ssaJ and the ssaK/U operon, 13 genes encoding components of the type III secretion apparatus of Salmonella Pathogenicity Island 2.
Hensel M, Shea JE, Raupach B, Monack D, Falkow S, Gleeson C, Kubo T, Holden DW., Mol. Microbiol. 24(1), 1997
PMID: 9140973
C-terminal domain swapping of SSB changes the size of the ssDNA binding site.
Huang YH, Huang CY., Biomed Res Int 2014(), 2014
PMID: 25162017
Citrate--new functions for an old metabolite.
Iacobazzi V, Infantino V., Biol. Chem. 395(4), 2014
PMID: 24445237
Biochemical and spectroscopic characterization of Escherichia coli aconitases (AcnA and AcnB).
Jordan PA, Tang Y, Bradbury AJ, Thomson AJ, Guest JR., Biochem. J. 344 Pt 3(), 1999
PMID: 10585860
Cecum lymph node dendritic cells harbor slow-growing bacteria phenotypically tolerant to antibiotic treatment.
Kaiser P, Regoes RR, Dolowschiak T, Wotzka SY, Lengefeld J, Slack E, Grant AJ, Ackermann M, Hardt WD., PLoS Biol. 12(2), 2014
PMID: 24558351
SHIP-1 increases early oxidative burst and regulates phagosome maturation in macrophages.
Kamen LA, Levinsohn J, Cadwallader A, Tridandapani S, Swanson JA., J. Immunol. 180(11), 2008
PMID: 18490750
Bactericidal effect of hydroxyl radicals generated from a low concentration hydrogen peroxide with ultrasound in endodontic treatment.
Kobayashi Y, Hayashi M, Yoshino F, Tamura M, Yoshida A, Ibi H, Lee MC, Ochiai K, Ogiso B., J Clin Biochem Nutr 54(3), 2014
PMID: 24895478
A common mechanism of cellular death induced by bactericidal antibiotics.
Kohanski MA, Dwyer DJ, Hayete B, Lawrence CA, Collins JJ., Cell 130(5), 2007
PMID: 17803904
Fumarase C, the stable fumarase of Escherichia coli, is controlled by the soxRS regulon.
Liochev SI, Fridovich I., Proc. Natl. Acad. Sci. U.S.A. 89(13), 1992
PMID: 1631070
Salmonella typhimurium LT2 possesses three distinct 23S rRNA intervening sequences.
Mattatall NR, Sanderson KE., J. Bacteriol. 178(8), 1996
PMID: 8636028
Evidence for a superoxide permeability pathway in endosomal membranes.
Mumbengegwi DR, Li Q, Li C, Bear CE, Engelhardt JF., Mol. Cell. Biol. 28(11), 2008
PMID: 18378695
Antimicrobial activity of sodium citrate against Streptococcus pneumoniae and several oral bacteria.
Nagaoka S, Murata S, Kimura K, Mori T, Hojo K., Lett. Appl. Microbiol. 51(5), 2010
PMID: 20849395
Identification of SoxS-regulated genes in Salmonella enterica serovar typhimurium.
Pomposiello PJ, Demple B., J. Bacteriol. 182(1), 2000
PMID: 10613858
Redox-operated genetic switches: the SoxR and OxyR transcription factors.
Pomposiello PJ, Demple B., Trends Biotechnol. 19(3), 2001
PMID: 11179804
Role of host cell-derived amino acids in nutrition of intracellular Salmonella enterica.
Popp J, Noster J, Busch K, Kehl A, Zur Hellen G, Hensel M., Infect. Immun. 83(12), 2015
PMID: 26351287
A systematic investigation of Escherichia coli central carbon metabolism in response to superoxide stress.
Rui B, Shen T, Zhou H, Liu J, Chen J, Pan X, Liu H, Wu J, Zheng H, Shi Y., BMC Syst Biol 4(), 2010
PMID: 20809933
Parallel exploitation of diverse host nutrients enhances Salmonella virulence.
Steeb B, Claudi B, Burton NA, Tienz P, Schmidt A, Farhan H, Maze A, Bumann D., PLoS Pathog. 9(4), 2013
PMID: 23633950
Escherichia coli aconitases and oxidative stress: post-transcriptional regulation of sodA expression.
Tang Y, Quail MA, Artymiuk PJ, Guest JR, Green J., Microbiology (Reading, Engl.) 148(Pt 4), 2002
PMID: 11932448
Role of gluconeogenesis and the tricarboxylic acid cycle in the virulence of Salmonella enterica serovar Typhimurium in BALB/c mice.
Tchawa Yimga M, Leatham MP, Allen JH, Laux DC, Conway T, Cohen PS., Infect. Immun. 74(2), 2006
PMID: 16428761
Expansion of the Gene Ontology knowledgebase and resources.
The Gene Ontology Consortium., Nucleic Acids Res. 45(D1), 2016
PMID: 27899567
Polyamines reduce oxidative stress in Escherichia coli cells exposed to bactericidal antibiotics.
Tkachenko AG, Akhova AV, Shumkov MS, Nesterova LY., Res. Microbiol. 163(2), 2011
PMID: 22138596
Oxygen- and growth rate-dependent regulation of Escherichia coli fumarase (FumA, FumB, and FumC) activity.
Tseng CP, Yu CC, Lin HH, Chang CY, Kuo JT., J. Bacteriol. 183(2), 2001
PMID: 11133938
Elevated citrate levels in non-alcoholic fatty liver disease: the potential of citrate to promote radical production.
van de Wier B, Balk JM, Haenen GR, Giamouridis D, Bakker JA, Bast BC, den Hartog GJ, Koek GH, Bast A., FEBS Lett. 587(15), 2013
PMID: 23792160
Direct measurement of oxidative and nitrosative stress dynamics in Salmonella inside macrophages.
van der Heijden J, Bosman ES, Reynolds LA, Finlay BB., Proc. Natl. Acad. Sci. U.S.A. 112(2), 2014
PMID: 25548165
Transcriptomic response of Escherichia coli O157:H7 to oxidative stress.
Wang S, Deng K, Zaremba S, Deng X, Lin C, Wang Q, Tortorello ML, Zhang W., Appl. Environ. Microbiol. 75(19), 2009
PMID: 19666735
Oxidative metabolism enables Salmonella evasion of the NLRP3 inflammasome.
Wynosky-Dolfi MA, Snyder AG, Philip NH, Doonan PJ, Poffenberger MC, Avizonis D, Zwack EE, Riblett AM, Hu B, Strowig T, Flavell RA, Jones RG, Freedman BD, Brodsky IE., J. Exp. Med. 211(4), 2014
PMID: 24638169
Activation of the OxyR transcription factor by reversible disulfide bond formation.
Zheng M, Aslund F, Storz G., Science 279(5357), 1998
PMID: 9497290
OxyR and SoxRS regulation of fur.
Zheng M, Doan B, Schneider TD, Storz G., J. Bacteriol. 181(15), 1999
PMID: 10419964

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