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Dr. NO and Mr. Toxic – the versatile role of nitric oxide

  • Constance Porrini , Nalini Ramarao ORCID logo EMAIL logo und Seav-Ly Tran
Veröffentlicht/Copyright: 7. Dezember 2019

Abstract

Nitric oxide (NO) is present in various organisms from humans, to plants, fungus and bacteria. NO is a fundamental signaling molecule implicated in major cellular functions. The role of NO ranges from an essential molecule to a potent mediator of cellular damages. The ability of NO to react with a broad range of biomolecules allows on one hand its regulation and a gradient concentration and on the other hand to exert physiological as well as pathological functions. In humans, NO is implicated in cardiovascular homeostasis, neurotransmission and immunity. However, NO can also contribute to cardiovascular diseases (CVDs) or septic shock. For certain denitrifying bacteria, NO is part of their metabolism as a required intermediate of the nitrogen cycle. However, for other bacteria, NO is toxic and harmful. To survive, those bacteria have developed processes to resist this toxic effect and persist inside their host. NO also contributes to maintain the host/microbiota homeostasis. But little is known about the impact of NO produced during prolonged inflammation on microbiota integrity, and some pathogenic bacteria take advantage of the NO response to colonize the gut over the microbiota. Taken together, depending on the environmental context (prolonged production, gradient concentration, presence of partners for interaction, presence of oxygen, etc.), NO will exert its beneficial or detrimental function. In this review, we highlight the dual role of NO for humans, pathogenic bacteria and microbiota, and the mechanisms used by each organism to produce, use or resist NO.

Acknowledgments

We wish to thank Olivier Dussurget and Isabelle Martin Verstraete for their precious advices in the redaction of this review. This work is supported by the public grants IDI 2015 and AAP Prematuration IDEX 2016, projects funded by the IDEX Paris Saclay, ANR-11-IDEX-0003-02, Funder Id: http://dx.doi.org/10.13039/501100001665.

References

Adak, S., Aulak, K.S., and Stuehr, D.J. (2002a). Direct evidence for nitric oxide production by a nitric-oxide synthase-like protein from Bacillus subtilis. J. Biol. Chem. 277, 16167–16171.10.1074/jbc.M201136200Suche in Google Scholar PubMed

Adak, S., Bilwes, A.M., Panda, K., Hosfield, D., Aulak, K.S., McDonald, J.F., Tainer, J.A., Getzoff, E.D., Crane, B.R., and Stuehr, D.J. (2002b). Cloning, expression, and characterization of a nitric oxide synthase protein from Deinococcus radiodurans. Proc. Natl. Acad. Sci. U. S. A. 99, 107–112.10.1073/pnas.012470099Suche in Google Scholar PubMed PubMed Central

Adebali, O., Sancar, A., and Selby, C.P. (2017). Mfd translocase is necessary and sufficient for transcription-coupled repair in Escherichia coli. J. Biol. Chem. 292, 18386–18391.10.1074/jbc.C117.818807Suche in Google Scholar PubMed PubMed Central

Agapie, T., Suseno, S., Woodward, J.J., Stoll, S., Britt, R.D., and Marletta, M.A. (2009). NO formation by a catalytically self-sufficient bacterial nitric oxide synthase from Sorangium cellulosum. Proc. Natl. Acad. Sci. U. S. A. 106, 16221–16226.10.1073/pnas.0908443106Suche in Google Scholar PubMed PubMed Central

Balasiny, B., Rolfe, M.D., Vine, C., Bradley, C., Green, J., and Cole, J. (2018). Release of nitric oxide by the Escherichia coli YtfE (RIC) protein and its reduction by the hybrid cluster protein in an integrated pathway to minimize cytoplasmic nitrosative stress. Microbiology 164, 563–575.10.1099/mic.0.000629Suche in Google Scholar PubMed

Bang, I.S., Liu, L., Vazquez-Torres, A., Crouch, M.L., Stamler, J.S., and Fang, F.C. (2006). Maintenance of nitric oxide and redox homeostasis by the Salmonella flavohemoglobin hmp. J. Biol. Chem. 281, 28039–28047.10.1074/jbc.M605174200Suche in Google Scholar PubMed

Barraud, N., Kelso, M.J., Rice, S.A., and Kjelleberg, S. (2015). Nitric oxide: a key mediator of biofilm dispersal with applications in infectious diseases. Curr. Pharm. Des. 21, 31–42.10.2174/1381612820666140905112822Suche in Google Scholar PubMed

Beinert, H. and Kennedy, M.C. (1993). Aconitase, a two-faced protein: enzyme and iron regulatory factor. FASEB. J. 7, 1442–1449.10.1096/fasebj.7.15.8262329Suche in Google Scholar PubMed

Benjamin, N., O’Driscoll, F., Dougall, H., Duncan, C., Smith, L., Golden, M., and McKenzie, H. (1994). Stomach NO synthesis. Nature 368, 502.10.1038/368502a0Suche in Google Scholar PubMed

Blomberg, M.R.A. and Adelroth, P. (2017). The mechanism for oxygen reduction in cytochrome c dependent nitric oxide reductase (cNOR) as obtained from a combination of theoretical and experimental results. Biochim. Biophys. Acta Bioenerg. 1858, 884–894.10.1016/j.bbabio.2017.08.005Suche in Google Scholar PubMed

Bodenmiller, D.M. and Spiro, S. (2006). The yjeB (nsrR) gene of Escherichia coli encodes a nitric oxide-sensitive transcriptional regulator. J. Bacteriol. 188, 874–881.10.1128/JB.188.3.874-881.2006Suche in Google Scholar PubMed PubMed Central

Brenot, A., King, K.Y., Janowiak, B., Griffith, O., and Caparon, M.G. (2004). Contribution of glutathione peroxidase to the virulence of Streptococcus pyogenes. Infect. Immun. 72, 408–413.10.1128/IAI.72.1.408-413.2004Suche in Google Scholar PubMed PubMed Central

Brzostek, A., Szulc, I., Klink, M., Brzezinska, M., Sulowska, Z., and Dziadek, J. (2014). Either non-homologous ends joining or homologous recombination is required to repair double-strand breaks in the genome of macrophage-internalized Mycobacterium tuberculosis. PLoS One 9, e92799.10.1371/journal.pone.0092799Suche in Google Scholar PubMed PubMed Central

Bull, M.J. and Plummer, N.T. (2014). Part 1: The human gut microbiome in health and disease. Integr. Med. (Encinitas) 13, 17–22.Suche in Google Scholar

Burnham, P.M. and Hendrixson, D.R. (2018). Campylobacter jejuni: collective components promoting a successful enteric lifestyle. Nat. Rev. Microbiol. 16, 551–565.10.1038/s41579-018-0037-9Suche in Google Scholar PubMed

Bush, M., Ghosh, T., Tucker, N., Zhang, X., and Dixon, R. (2011). Transcriptional regulation by the dedicated nitric oxide sensor, NorR: a route towards NO detoxification. Biochem. Soc. Trans. 39, 289–293.10.1042/BST0390289Suche in Google Scholar PubMed

Butler, A.R. and Megson, I.L. (2002). Non-heme iron nitrosyls in biology. Chem. Rev. 102, 1155–1166.10.1021/cr000076dSuche in Google Scholar PubMed

Cadby, I.T., Busby, S.J., and Cole, J.A. (2011). An HcpR homologue from Desulfovibrio desulfuricans and its possible role in nitrate reduction and nitrosative stress. Biochem. Soc. Trans. 39, 224–229.10.1042/BST0390224Suche in Google Scholar PubMed

Cadby, I.T., Ibrahim, S.A., Faulkner, M., Lee, D.J., Browning, D., Busby, S.J., Lovering, A.L., Stapleton, M.R., Green, J., and Cole, J.A. (2016). Regulation, sensory domains and roles of two Desulfovibrio desulfuricans ATCC27774 Crp family transcription factors, HcpR1 and HcpR2, in response to nitrosative stress. Mol. Microbiol. 102, 1120–1137.10.1111/mmi.13540Suche in Google Scholar PubMed

Cadby, I.T., Faulkner, M., Cheneby, J., Long, J., van Helden, J., Dolla, A., and Cole, J.A. (2017). Coordinated response of the Desulfovibrio desulfuricans 27774 transcriptome to nitrate, nitrite and nitric oxide. Sci. Rep. 7, 16228.10.1038/s41598-017-16403-4Suche in Google Scholar PubMed PubMed Central

Canthaboo, C., Xing, D., Wei, X.Q., and Corbel, M.J. (2002). Investigation of role of nitric oxide in protection from Bordetella pertussis respiratory challenge. Infect. Immun. 70, 679–684.10.1128/IAI.70.2.679-684.2002Suche in Google Scholar PubMed PubMed Central

Chakravortty, D., Hansen-Wester, I., and Hensel, M. (2002). Salmonella pathogenicity island 2 mediates protection of intracellular Salmonella from reactive nitrogen intermediates. J. Exp. Med. 195, 1155–1166.10.1084/jem.20011547Suche in Google Scholar PubMed PubMed Central

Choi, W.S., Chang, M.S., Han, J.W., Hong, S.Y., and Lee, H.W. (1997). Identification of nitric oxide synthase in Staphylococcus aureus. Biochem. Biophys. Res. Commun. 237, 554–558.10.1006/bbrc.1997.7189Suche in Google Scholar PubMed

Choudhari, S.K., Chaudhary, M., Bagde, S., Gadbail, A.R., and Joshi, V. (2013). Nitric oxide and cancer: a review. World J. Surg. Oncol. 11, 118.10.1186/1477-7819-11-118Suche in Google Scholar PubMed PubMed Central

Cole, C., Thomas, S., Filak, H., Henson, P.M., and Lenz, L.L. (2012). Nitric oxide increases susceptibility of Toll-like receptor-activated macrophages to spreading Listeria monocytogenes. Immunity 36, 807–820.10.1016/j.immuni.2012.03.011Suche in Google Scholar PubMed PubMed Central

Crack, J.C., Stapleton, M.R., Green, J., Thomson, A.J., and Le Brun, N.E. (2013). Mechanism of [4Fe-4S](Cys)4 cluster nitrosylation is conserved among NO-responsive regulators. J. Biol. Chem. 288, 11492–11502.10.1074/jbc.M112.439901Suche in Google Scholar PubMed PubMed Central

Cross, R.K. and Wilson, K.T. (2003). Nitric oxide in inflammatory bowel disease. Inflamm. Bowel Dis. 9, 179–189.10.1097/00054725-200305000-00006Suche in Google Scholar PubMed

Cruz-Ramos, H., Crack, J., Wu, G., Hughes, M.N., Scott, C., Thomson, A.J., Green, J., and Poole, R.K. (2002). NO sensing by FNR: regulation of the Escherichia coli NO-detoxifying flavohaemoglobin, Hmp. EMBO. J. 21, 3235–3244.10.1093/emboj/cdf339Suche in Google Scholar PubMed PubMed Central

D’Autreaux, B., Touati, D., Bersch, B., Latour, J.M., and Michaud-Soret, I. (2002). Direct inhibition by nitric oxide of the transcriptional ferric uptake regulation protein via nitrosylation of the iron. Proc. Natl. Acad. Sci. U. S. A. 99, 16619–16624.10.1073/pnas.252591299Suche in Google Scholar PubMed PubMed Central

da Silva, S.M., Amaral, C., Neves, S.S., Santos, C., Pimentel, C., and Rodrigues-Pousada, C. (2015). An HcpR paralog of Desulfovibrio gigas provides protection against nitrosative stress. FEBS. Open Bio. 5, 594–604.10.1016/j.fob.2015.07.001Suche in Google Scholar PubMed PubMed Central

Darfeuille-Michaud, A., Boudeau, J., Bulois, P., Neut, C., Glasser, A.L., Barnich, N., Bringer, M.A., Swidsinski, A., Beaugerie, L., and Colombel, J.F. (2004). High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn’s disease. Gastroenterology 127, 412–421.10.1053/j.gastro.2004.04.061Suche in Google Scholar PubMed

Darrigo, C., Guillemet, E., Dervyn, R., and Ramarao, N. (2016). The bacterial Mfd protein prevents DNA damage induced by the host nitrogen immune response in a NER-independent but RecBC-dependent pathway. PLoS One 11, e0163321.10.1371/journal.pone.0163321Suche in Google Scholar

Darwin, K.H. and Nathan, C.F. (2005). Role for nucleotide excision repair in virulence of Mycobacterium tuberculosis. Infect. Immun. 73, 4581–4587.10.1128/IAI.73.8.4581-4587.2005Suche in Google Scholar

Darwin, K.H., Ehrt, S., Gutierrez-Ramos, J.C., Weich, N., and Nathan, C.F. (2003). The proteasome of Mycobacterium tuberculosis is required for resistance to nitric oxide. Science 302, 1963–1966.10.1126/science.1091176Suche in Google Scholar

Demple, B., Ding, H., and Jorgensen, M. (2002). Escherichia coli SoxR protein: sensor/transducer of oxidative stress and nitric oxide. Methods Enzymol. 348, 355–364.10.1016/S0076-6879(02)48654-5Suche in Google Scholar

Denkel, L.A., Horst, S.A., Rouf, S.F., Kitowski, V., Bohm, O.M., Rhen, M., Jager, T., and Bange, F.C. (2011). Methionine sulfoxide reductases are essential for virulence of Salmonella typhimurium. PLoS One 6, e26974.10.1371/journal.pone.0026974Suche in Google Scholar PubMed PubMed Central

Ding, H. and Demple, B. (2000). Direct nitric oxide signal transduction via nitrosylation of iron-sulfur centers in the SoxR transcription activator. Proc. Natl. Acad. Sci. U. S. A. 97, 5146–5150.10.1073/pnas.97.10.5146Suche in Google Scholar PubMed PubMed Central

Dong, M., Vongchampa, V., Gingipalli, L., Cloutier, J.F., Kow, Y.W., O’Connor, T., and Dedon, P.C. (2006). Development of enzymatic probes of oxidative and nitrosative DNA damage caused by reactive nitrogen species. Mutat. Res. 594, 120–134.10.1016/j.mrfmmm.2005.08.008Suche in Google Scholar PubMed

Donovan, A., Brownlie, A., Zhou, Y., Shepard, J., Pratt, S.J., Moynihan, J., Paw, B.H., Drejer, A., Barut, B., Zapata, A., et al. (2000). Positional cloning of zebrafish ferroportin1 identifies a conserved vertebrate iron exporter. Nature 403, 776–781.10.1038/35001596Suche in Google Scholar PubMed

Douglas, T., Daniel, D.S., Parida, B.K., Jagannath, C., and Dhandayuthapani, S. (2004). Methionine sulfoxide reductase A (MsrA) deficiency affects the survival of Mycobacterium smegmatis within macrophages. J. Bacteriol. 186, 3590–3598.10.1128/JB.186.11.3590-3598.2004Suche in Google Scholar PubMed PubMed Central

Duan, W., Li, J., Inks, E.S., Chou, C.J., Jia, Y., Chu, X., Li, X., Xu, W., and Zhang, Y. (2015). Design, synthesis, and antitumor evaluation of novel histone deacetylase inhibitors equipped with a phenylsulfonylfuroxan module as a nitric oxide donor. J. Med. Chem. 58, 4325–4338.10.1021/acs.jmedchem.5b00317Suche in Google Scholar PubMed PubMed Central

Elvers, K.T., Wu, G., Gilberthorpe, N.J., Poole, R.K., and Park, S.F. (2004). Role of an inducible single-domain hemoglobin in mediating resistance to nitric oxide and nitrosative stress in Campylobacter jejuni and Campylobacter coli. J. Bacteriol. 186, 5332–5341.10.1128/JB.186.16.5332-5341.2004Suche in Google Scholar PubMed PubMed Central

Ezraty, B., Aussel, L., and Barras, F. (2005). Methionine sulfoxide reductases in prokaryotes. Biochim. Biophys. Acta. 1703, 221–229.10.1016/j.bbapap.2004.08.017Suche in Google Scholar PubMed

Fabrega, A. and Vila, J. (2013). Salmonella enterica serovar Typhimurium skills to succeed in the host: virulence and regulation. Clin. Microbiol. Rev. 26, 308–341.10.1128/CMR.00066-12Suche in Google Scholar PubMed PubMed Central

Fang, F.C. and Vazquez-Torres, A. (2019). Reactive nitrogen species in host-bacterial interactions. Curr. Opin. Immunol. 60, 96–102.10.1016/j.coi.2019.05.008Suche in Google Scholar PubMed PubMed Central

Fang, F.C., Vazquez-Torres, A., and Xu, Y. (1997). The transcriptional regulator SoxS is required for resistance of Salmonella typhimurium to paraquat but not for virulence in mice. Infect. Immun. 65, 5371–5375.10.1128/iai.65.12.5371-5375.1997Suche in Google Scholar PubMed PubMed Central

Finer, N.N. and Barrington, K.J. (2006). Nitric oxide for respiratory failure in infants born at or near term. Cochrane Database Syst. Rev. CD000399.10.1002/14651858.CD000399.pub2Suche in Google Scholar PubMed

Fitzpatrick, J. and Kim, E. (2015). Synthetic modeling chemistry of iron-sulfur clusters in nitric oxide signaling. Acc. Chem. Res. 48, 2453–2461.10.1021/acs.accounts.5b00246Suche in Google Scholar PubMed

Frawley, E.R., Karlinsey, J.E., Singhal, A., Libby, S.J., Doulias, P.T., Ischiropoulos, H., and Fang, F.C. (2018). Nitric oxide disrupts zinc homeostasis in Salmonella enterica Serovar Typhimurium. MBio. 9, e01040-18.10.1128/mBio.01040-18Suche in Google Scholar PubMed PubMed Central

Gardner, P.R., Gardner, A.M., Martin, L.A., and Salzman, A.L. (1998). Nitric oxide dioxygenase: an enzymic function for flavohemoglobin. Proc. Natl. Acad. Sci. U.S.A. 95, 10378–10383.10.1073/pnas.95.18.10378Suche in Google Scholar PubMed PubMed Central

Gardner, A.M., Helmick, R.A., and Gardner, P.R. (2002). Flavorubredoxin, an inducible catalyst for nitric oxide reduction and detoxification in Escherichia coli. J. Biol. Chem. 277, 8172–8177.10.1074/jbc.M110471200Suche in Google Scholar PubMed

Gilberthorpe, N.J., Lee, M.E., Stevanin, T.M., Read, R.C., and Poole, R.K. (2007). NsrR: a key regulator circumventing Salmonella enterica serovar Typhimurium oxidative and nitrosative stress in vitro and in IFN-gamma-stimulated J774.2 macrophages. Microbiology 153, 1756–1771.10.1099/mic.0.2006/003731-0Suche in Google Scholar

Gilmore, M.S., Lebreton, F., and van Schaik, W. (2013). Genomic transition of enterococci from gut commensals to leading causes of multidrug-resistant hospital infection in the antibiotic era. Curr. Opin. Microbiol. 16, 10–16.10.1016/j.mib.2013.01.006Suche in Google Scholar

Green, J., Crack, J.C., Thomson, A.J., and LeBrun, N.E. (2009). Bacterial sensors of oxygen. Curr. Opin. Microbiol. 12, 145–151.10.1016/j.mib.2009.01.008Suche in Google Scholar

Guillemet, E., Lereec, A., Tran, S.L., Royer, C., Barbosa, I., Sansonetti, P., Lereclus, D., and Ramarao, N. (2016). The bacterial DNA repair protein Mfd confers resistance to the host nitrogen immune response. Sci. Rep. 6, 29349.10.1038/srep29349Suche in Google Scholar

Gusarov, I., Starodubtseva, M., Wang, Z.Q., McQuade, L., Lippard, S.J., Stuehr, D.J., and Nudler, E. (2008). Bacterial nitric-oxide synthases operate without a dedicated redox partner. J. Biol. Chem. 283, 13140–13147.10.1074/jbc.M710178200Suche in Google Scholar

Guthlein, C., Wanner, R.M., Sander, P., Davis, E.O., Bosshard, M., Jiricny, J., Bottger, E.C., and Springer, B. (2009). Characterization of the mycobacterial NER system reveals novel functions of the uvrD1 helicase. J. Bacteriol. 191, 555–562.10.1128/JB.00216-08Suche in Google Scholar

Gutierrez, M.G., Master, S.S., Singh, S.B., Taylor, G.A., Colombo, M.I., and Deretic, V. (2004). Autophagy is a defense mechanism inhibiting BCG and Mycobacterium tuberculosis survival in infected macrophages. Cell 119, 753–766.10.1016/j.cell.2004.11.038Suche in Google Scholar

Haine, V., Dozot, M., Dornand, J., Letesson, J.J., and De Bolle, X. (2006). NnrA is required for full virulence and regulates several Brucella melitensis denitrification genes. J. Bacteriol. 188, 1615–1619.10.1128/JB.188.4.1615-1619.2006Suche in Google Scholar

Hausladen, A., Privalle, C.T., Keng, T., DeAngelo, J., and Stamler, J.S. (1996). Nitrosative stress: activation of the transcription factor OxyR. Cell. 86, 719–729.10.1016/S0092-8674(00)80147-6Suche in Google Scholar

Henard, C.A. and Vazquez-Torres, A. (2012). DksA-dependent resistance of Salmonella enterica serovar Typhimurium against the antimicrobial activity of inducible nitric oxide synthase. Infect. Immun. 80, 1373–1380.10.1128/IAI.06316-11Suche in Google Scholar PubMed PubMed Central

Hendriks, J., Oubrie, A., Castresana, J., Urbani, A., Gemeinhardt, S., and Saraste, M. (2000). Nitric oxide reductases in bacteria. Biochim. Biophys. Acta. 1459, 266–273.10.1016/S0005-2728(00)00161-4Suche in Google Scholar

Herbst, S., Schaible, U.E., and Schneider, B.E. (2011). Interferon gamma activated macrophages kill mycobacteria by nitric oxide induced apoptosis. PLoS One 6, e19105.10.1371/journal.pone.0019105Suche in Google Scholar PubMed PubMed Central

Heylen, K., Vanparys, B., Gevers, D., Wittebolle, L., Boon, N., and De Vos, P. (2007). Nitric oxide reductase (norB) gene sequence analysis reveals discrepancies with nitrite reductase (nir) gene phylogeny in cultivated denitrifiers. Environ. Microbiol. 9, 1072–1077.10.1111/j.1462-2920.2006.01194.xSuche in Google Scholar PubMed

Hosoi, T., Goto, H., Arisawa, T., Niwa, Y., Okada, N., Ohmiya, N., and Hayakawa, T. (2001). Role of nitric oxide synthase inhibitor in experimental colitis induced by 2,4,6-trinitrobenzene sulphonic acid in rats. Clin. Exp. Pharmacol. Physiol. 28, 9–12.10.1046/j.1440-1681.2001.03388.xSuche in Google Scholar PubMed

Hotta, Y., Kataoka, T., Mori, T., and Kimura, K. (2019). Review of a potential novel approach for erectile dysfunction: light-controllable nitric oxide donors and nanoformulations. Sex Med. Rev. pii: S2050-0521(19)30057-5. doi: 10.1016/j.sxmr.2019.05.006. [Epub ahead of print].10.1016/j.sxmr.2019.05.006Suche in Google Scholar PubMed

Houghton, J., Townsend, C., Williams, A.R., Rodgers, A., Rand, L., Walker, K.B., Bottger, E.C., Springer, B., and Davis, E.O. (2012). Important role for Mycobacterium tuberculosis UvrD1 in pathogenesis and persistence apart from its function in nucleotide excision repair. J. Bacteriol. 194, 2916–2923.10.1128/JB.06654-11Suche in Google Scholar PubMed PubMed Central

Huang, P.L. (2009). eNOS, metabolic syndrome and cardiovascular disease. Trends Endocrinol. Metab. 20, 295–302.10.1016/j.tem.2009.03.005Suche in Google Scholar PubMed PubMed Central

Huang, K., Wang, D., Frederiksen, R.F., Rensing, C., Olsen, J.E., and Fresno, A.H. (2017). Investigation of the role of genes encoding zinc exporters zntA, zitB, and fieF during SalmonellaTyphimurium infection. Front Microbiol. 8, 2656.10.3389/fmicb.2017.02656Suche in Google Scholar PubMed PubMed Central

Hussain, S.P., Trivers, G.E., Hofseth, L.J., He, P., Shaikh, I., Mechanic, L.E., Doja, S., Jiang, W., Subleski, J., Shorts, L., et al. (2004). Nitric oxide, a mediator of inflammation, suppresses tumorigenesis. Cancer Res. 64, 6849–6853.10.1158/0008-5472.CAN-04-2201Suche in Google Scholar PubMed

Ichimura, K., Shimizu, T., Matsumoto, A., Hirai, S., Yokoyama, E., Takeuchi, H., Yahiro, K., and Noda, M. (2017). Nitric oxide-enhanced Shiga toxin production was regulated by Fur and RecA in enterohemorrhagic Escherichia coli O157. Microbiologyopen 6, e00461.10.1002/mbo3.461Suche in Google Scholar PubMed PubMed Central

Islam, B.U., Habib, S., Ali, S.A., Moinuddin, and Ali, A. (2017). Role of peroxynitrite-induced activation of poly(ADP-Ribose) polymerase (PARP) in circulatory shock and related pathological conditions. Cardiovasc. Toxicol. 17, 373–383.10.1007/s12012-016-9394-7Suche in Google Scholar PubMed

Ito, C., Saito, Y., Nozawa, T., Fujii, S., Sawa, T., Inoue, H., Matsunaga, T., Khan, S., Akashi, S., Hashimoto, R., et al. (2013).Endogenous nitrated nucleotide is a key mediator of autophagy and innate defense against bacteria. Mol. Cell. 52, 794–804.10.1016/j.molcel.2013.10.024Suche in Google Scholar PubMed

Jadert, C., Phillipson, M., Holm, L., Lundberg, J.O., and Borniquel, S. (2014). Preventive and therapeutic effects of nitrite supplementation in experimental inflammatory bowel disease. Redox Biol. 2, 73–81.10.1016/j.redox.2013.12.012Suche in Google Scholar PubMed PubMed Central

Jadeski, L.C., Chakraborty, C., and Lala, P.K. (2003). Nitric oxide-mediated promotion of mammary tumour cell migration requires sequential activation of nitric oxide synthase, guanylate cyclase and mitogen-activated protein kinase. Int. J. Cancer. 106, 496–504.10.1002/ijc.11268Suche in Google Scholar PubMed

Jamaati, H., Mortaz, E., Pajouhi, Z., Folkerts, G., Movassaghi, M., Moloudizargari, M., Adcock, I.M., and Garssen, J. (2017). Nitric oxide in the pathogenesis and treatment of tuberculosis. Front Microbiol. 8, 2008.10.3389/fmicb.2017.02008Suche in Google Scholar PubMed PubMed Central

Jastrab, J.B. and Darwin, K.H. (2015). Bacterial proteasomes. Annu. Rev. Microbiol. 69, 109–127.10.1146/annurev-micro-091014-104201Suche in Google Scholar PubMed PubMed Central

Jia, W., Whitehead, R.N., Griffiths, L., Dawson, C., Bai, H., Waring, R.H., Ramsden, D.B., Hunter, J.O., Cauchi, M., Bessant, C., et al. (2012). Diversity and distribution of sulphate-reducing bacteria in human faeces from healthy subjects and patients with inflammatory bowel disease. FEMS. Immunol. Med. Microbiol. 65, 55–68.10.1111/j.1574-695X.2012.00935.xSuche in Google Scholar PubMed

Jianjun, Y., Zhang, R., Lu, G., Shen, Y., Peng, L., Zhu, C., Cui, M., Wang, W., Arnaboldi, P., Tang, M., et al. (2013). T cell-derived inducible nitric oxide synthase switches off Th17 cell differentiation. J. Exp. Med. 210, 1447–1462.10.1084/jem.20122494Suche in Google Scholar PubMed PubMed Central

Justino, M.C., Vicente, J.B., Teixeira, M., and Saraiva, L.M. (2005). New genes implicated in the protection of anaerobically grown Escherichia coli against nitric oxide. J. Biol. Chem. 280, 2636–2643.10.1074/jbc.M411070200Suche in Google Scholar PubMed

Justino, M.C., Almeida, C.C., Goncalves, V.L., Teixeira, M., and Saraiva, L.M. (2006). Escherichia coli YtfE is a di-iron protein with an important function in assembly of iron-sulphur clusters. FEMS. Microbiol. Lett. 257, 278–284.10.1111/j.1574-6968.2006.00179.xSuche in Google Scholar PubMed

Kapil, V., Haydar, S.M., Pearl, V., Lundberg, J.O., Weitzberg, E., and Ahluwalia, A. (2013). Physiological role for nitrate-reducing oral bacteria in blood pressure control. Free. Radic. Biol. Med. 55, 93–100.10.1016/j.freeradbiomed.2012.11.013Suche in Google Scholar

Kim, S.O., Orii, Y., Lloyd, D., Hughes, M.N., and Poole, R.K. (1999). Anoxic function for the Escherichia coli flavohaemoglobin (Hmp): reversible binding of nitric oxide and reduction to nitrous oxide. FEBS. Lett. 445, 389–394.10.1016/S0014-5793(99)00157-XSuche in Google Scholar

Kinkel, T.L., Ramos-Montanez, S., Pando, J.M., Tadeo, D.V., Strom, E.N., Libby, S.J., and Fang, F.C. (2016). An essential role for bacterial nitric oxide synthase in Staphylococcus aureus electron transfer and colonization. Nat. Microbiol. 2, 16224.10.1038/nmicrobiol.2016.224Suche in Google Scholar

Kint, N., Janoir, C., Monot, M., Hoys, S., Soutourina, O., Dupuy, B., and Martin-Verstraete, I. (2017). The alternative sigma factor sigma(B) plays a crucial role in adaptive strategies of Clostridium difficile during gut infection. Environ. Microbiol. 19, 1933–1958.10.1111/1462-2920.13696Suche in Google Scholar

Kisker, C., Kuper, J., and Van Houten, B. (2013). Prokaryotic nucleotide excision repair. Cold Spring Harb. Perspect. Biol. 5, a012591.10.1101/cshperspect.a012591Suche in Google Scholar

Kisley, L.R., Barrett, B.S., Bauer, A.K., Dwyer-Nield, L.D., Barthel, B., Meyer, A.M., Thompson, D.C., and Malkinson, A.M. (2002). Genetic ablation of inducible nitric oxide synthase decreases mouse lung tumorigenesis. Cancer Res. 62, 6850–6856.Suche in Google Scholar

Kolios, G., Valatas, V., and Ward, S.G. (2004). Nitric oxide in inflammatory bowel disease: a universal messenger in an unsolved puzzle. Immunology 113, 427–437.10.1111/j.1365-2567.2004.01984.xSuche in Google Scholar

Korner, H., Sofia, H.J., and Zumft, W.G. (2003). Phylogeny of the bacterial superfamily of Crp-Fnr transcription regulators: exploiting the metabolic spectrum by controlling alternative gene programs. FEMS. Microbiol. Rev. 27, 559–592.10.1016/S0168-6445(03)00066-4Suche in Google Scholar

Le, N.T. and Richardson, D.R. (2002). Ferroportin1: a new iron export molecule? Int. J. Biochem. Cell Biol. 34, 103–108.10.1016/S1357-2725(01)00104-2Suche in Google Scholar

Lee, W.L., Gold, B., Darby, C., Brot, N., Jiang, X., de Carvalho, L.P., Wellner, D., St John, G., Jacobs, W.R., Jr., and Nathan, C. (2009). Mycobacterium tuberculosis expresses methionine sulphoxide reductases A and B that protect from killing by nitrite and hypochlorite. Mol. Microbiol. 71, 583–593.10.1111/j.1365-2958.2008.06548.xSuche in Google Scholar PubMed PubMed Central

Martinez-Medina, M., Aldeguer, X., Lopez-Siles, M., Gonzalez-Huix, F., Lopez-Oliu, C., Dahbi, G., Blanco, J.E., Blanco, J., Garcia-Gil, L.J., and Darfeuille-Michaud, A. (2009). Molecular diversity of Escherichia coli in the human gut: new ecological evidence supporting the role of adherent-invasive E. coli (AIEC) in Crohn’s disease. Inflamm. Bowel Dis. 15, 872–882.10.1002/ibd.20860Suche in Google Scholar PubMed

Masip, L., Veeravalli, K., and Georgiou, G. (2006). The many faces of glutathione in bacteria. Antioxid. Redox Signal. 8, 753–762.10.1089/ars.2006.8.753Suche in Google Scholar PubMed

Mason, K.L., Stepien, T.A., Blum, J.E., Holt, J.F., Labbe, N.H., Rush, J.S., Raffa, K.F., and Handelsman, J. (2011). From commensal to pathogen: translocation of Enterococcus faecalis from the midgut to the hemocoel of Manduca sexta. MBio. 2, e00065–e00011.10.1128/mBio.00065-11Suche in Google Scholar PubMed PubMed Central

Matziouridou, C., Rocha, S.D.C., Haabeth, O.A., Rudi, K., Carlsen, H., and Kielland, A. (2018). iNOS- and NOX1-dependent ROS production maintains bacterial homeostasis in the ileum of mice. Mucosal. Immunol. 11, 774–784.10.1038/mi.2017.106Suche in Google Scholar PubMed

McFarland, A.P., Burke, T.P., Carletti, A.A., Glover, R.C., Tabakh, H., Welch, M.D., and Woodward, J.J. (2018). RECON-dependent inflammation in hepatocytes enhances Listeria monocytogenes cell-to-cell spread. MBio. 9, e00526-18.10.1128/mBio.00526-18Suche in Google Scholar PubMed PubMed Central

Mercanoglu, G., Safran, N., Ahishali, B.B., Uzun, H., Yalcin, A., and Mercanoglu, F. (2015). Nitric oxide mediated effects of nebivolol in myocardial infarction: the source of nitric oxide. Eur. Rev. Med. Pharmacol. Sci. 19, 4872–4889.Suche in Google Scholar

Mills, P.C., Rowley, G., Spiro, S., Hinton, J.C., and Richardson, D.J. (2008). A combination of cytochrome c nitrite reductase (NrfA) and flavorubredoxin (NorV) protects Salmonella enterica serovar Typhimurium against killing by NO in anoxic environments. Microbiology 154, 1218–1228.10.1099/mic.0.2007/014290-0Suche in Google Scholar PubMed

Miquel, S., Martin, R., Rossi, O., Bermudez-Humaran, L.G., Chatel, J.M., Sokol, H., Thomas, M., Wells, J.M., and Langella, P. (2013). Faecalibacterium prausnitzii and human intestinal health. Curr. Opin. Microbiol. 16, 255–261.10.1016/j.mib.2013.06.003Suche in Google Scholar PubMed

Mirnejad, R., Jazi, F.M., Mostafaei, S., and Sedighi, M. (2017). Molecular investigation of virulence factors of Brucella melitensis and Brucella abortus strains isolated from clinical and non-clinical samples. Microb. Pathog. 109, 8–14.10.1016/j.micpath.2017.05.019Suche in Google Scholar PubMed

Mitchell, J.G. and Kogure, K. (2006). Bacterial motility: links to the environment and a driving force for microbial physics. FEMS. Microbiol. Ecol. 55, 3–16.10.1111/j.1574-6941.2005.00003.xSuche in Google Scholar PubMed

Miyoshi, T., Li, Y., Shih, D.M., Wang, X., Laubach, V.E., Matsumoto, A.H., Helm, G.A., Lusis, A.J., and Shi, W. (2006). Deficiency of inducible NO synthase reduces advanced but not early atherosclerosis in apolipoprotein E-deficient mice. Life Sci. 79, 525–531.10.1016/j.lfs.2006.01.043Suche in Google Scholar PubMed

Montfort, W.R., Wales, J.A., and Weichsel, A. (2017). Structure and activation of soluble guanylyl cyclase, the nitric oxide sensor. Antioxid. Redox Signal. 26, 107–121.10.1089/ars.2016.6693Suche in Google Scholar PubMed PubMed Central

Montgomery, H.J., Dupont, A.L., Leivo, H.E., and Guillemette, J.G. (2010). Cloning, expression, and purification of a nitric oxide synthase-like protein from Bacillus cereus. Biochem. Res. Int. 2010, 489892.10.1155/2010/489892Suche in Google Scholar PubMed PubMed Central

Moore, C.M., Nakano, M.M., Wang, T., Ye, R.W., and Helmann, J.D. (2004). Response of Bacillus subtilis to nitric oxide and the nitrosating agent sodium nitroprusside. J. Bacteriol. 186, 4655–4664.10.1128/JB.186.14.4655-4664.2004Suche in Google Scholar PubMed PubMed Central

Morbidelli, L., Donnini, S., and Ziche, M. (2003). Role of nitric oxide in the modulation of angiogenesis. Curr. Pharm. Des. 9, 521–530.10.2174/1381612033391405Suche in Google Scholar PubMed

Mukhopadhyay, P., Zheng, M., Bedzyk, L.A., LaRossa, R.A., and Storz, G. (2004). Prominent roles of the NorR and Fur regulators in the Escherichia coli transcriptional response to reactive nitrogen species. Proc. Natl. Acad. Sci. U. S. A. 101, 745–750.10.1073/pnas.0307741100Suche in Google Scholar PubMed PubMed Central

Murrell, W. (1879). Nitro-glycerine as a remedy for angina pectoris. MRCP. 113, 80–81.10.1016/S0140-6736(02)46032-1Suche in Google Scholar

Nairz, M., Schleicher, U., Schroll, A., Sonnweber, T., Theurl, I., Ludwiczek, S., Talasz, H., Brandacher, G., Moser, P.L., Muckenthaler, M.U., et al. (2013). Nitric oxide-mediated regulation of ferroportin-1 controls macrophage iron homeostasis and immune function in Salmonella infection. J. Exp. Med. 210, 855–873.10.1084/jem.20121946Suche in Google Scholar PubMed PubMed Central

Nairz, M., Dichtl, S., Schroll, A., Haschka, D., Tymoszuk, P., Theurl, I., and Weiss, G. (2018). Iron and innate antimicrobial immunity-Depriving the pathogen, defending the host. J. Trace Elem. Med. Biol. 48, 118–133.10.1016/j.jtemb.2018.03.007Suche in Google Scholar PubMed

Nakagawa, I., Amano, A., Mizushima, N., Yamamoto, A., Yamaguchi, H., Kamimoto, T., Nara, A., Funao, J., Nakata, M., Tsuda, K., et al. (2004). Autophagy defends cells against invading group A Streptococcus. Science 306, 1037–1040.10.1126/science.1103966Suche in Google Scholar PubMed

Nakano, M.M., Geng, H., Nakano, S., and Kobayashi, K. (2006). The nitric oxide-responsive regulator NsrR controls ResDE-dependent gene expression. J. Bacteriol. 188, 5878–5887.10.1128/JB.00486-06Suche in Google Scholar PubMed PubMed Central

Negroni, A., Costanzo, M., Vitali, R., Superti, F., Bertuccini, L., Tinari, A., Minelli, F., Di Nardo, G., Nuti, F., Pierdomenico, M., et al. (2012). Characterization of adherent-invasive Escherichia coli isolated from pediatric patients with inflammatory bowel disease. Inflamm. Bowel Dis. 18, 913–924.10.1002/ibd.21899Suche in Google Scholar PubMed

Nishino, K., Nishida, A., Inoue, R., Kawada, Y., Ohno, M., Sakai, S., Inatomi, O., Bamba, S., Sugimoto, M., Kawahara, M., et al. (2018). Analysis of endoscopic brush samples identified mucosa-associated dysbiosis in inflammatory bowel disease. J. Gastroenterol. 53, 95–106.10.1007/s00535-017-1384-4Suche in Google Scholar PubMed

Nunoshiba, T., DeRojas-Walker, T., Tannenbaum, S.R., and Demple, B. (1995). Roles of nitric oxide in inducible resistance of Escherichia coli to activated murine macrophages. Infect. Immun. 63, 794–798.10.1128/iai.63.3.794-798.1995Suche in Google Scholar PubMed PubMed Central

Overton, T.W., Justino, M.C., Li, Y., Baptista, J.M., Melo, A.M., Cole, J.A., and Saraiva, L.M. (2008). Widespread distribution in pathogenic bacteria of di-iron proteins that repair oxidative and nitrosative damage to iron-sulfur centers. J. Bacteriol. 190, 2004–2013.10.1128/JB.01733-07Suche in Google Scholar PubMed PubMed Central

Pacher, P., Beckman, J.S., and Liaudet, L. (2007). Nitric oxide and peroxynitrite in health and disease. Physiol. Rev. 87, 315–424.10.1152/physrev.00029.2006Suche in Google Scholar PubMed PubMed Central

Pathania, R., Navani, N.K., Gardner, A.M., Gardner, P.R., and Dikshit, K.L. (2002). Nitric oxide scavenging and detoxification by the Mycobacterium tuberculosis haemoglobin, HbN in Escherichia coli. Mol. Microbiol. 45, 1303–1314.10.1046/j.1365-2958.2002.03095.xSuche in Google Scholar PubMed

Paul, B.J., Berkmen, M.B., and Gourse, R.L. (2005). DksA potentiates direct activation of amino acid promoters by ppGpp. Proc. Natl. Acad. Sci. U. S. A. 102, 7823–7828.10.1073/pnas.0501170102Suche in Google Scholar PubMed PubMed Central

Pawaria, S., Rajamohan, G., Gambhir, V., Lama, A., Varshney, G.C., and Dikshit, K.L. (2007). Intracellular growth and survival of Salmonella enterica serovar Typhimurium carrying truncated hemoglobins of Mycobacterium tuberculosis. Microb. Pathog. 42, 119–128.10.1016/j.micpath.2006.12.001Suche in Google Scholar PubMed

Penarando, J., Lopez-Sanchez, L.M., Mena, R., Guil-Luna, S., Conde, F., Hernandez, V., Toledano, M., Gudino, V., Raponi, M., Billard, C., et al. (2018). A role for endothelial nitric oxide synthase in intestinal stem cell proliferation and mesenchymal colorectal cancer. BMC. Biol. 16, 3.10.1186/s12915-017-0472-5Suche in Google Scholar PubMed PubMed Central

Pittman, M.S., Elvers, K.T., Lee, L., Jones, M.A., Poole, R.K., Park, S.F., and Kelly, D.J. (2007). Growth of Campylobacter jejuni on nitrate and nitrite: electron transport to NapA and NrfA via NrfH and distinct roles for NrfA and the globin Cgb in protection against nitrosative stress. Mol. Microbiol. 63, 575–590.10.1111/j.1365-2958.2006.05532.xSuche in Google Scholar PubMed

Poole, R.K. and Hughes, M.N. (2000). New functions for the ancient globin family: bacterial responses to nitric oxide and nitrosative stress. Mol. Microbiol. 36, 775–783.10.1046/j.1365-2958.2000.01889.xSuche in Google Scholar PubMed

Reinders, C.I., Hellstrom, P.M., Bjork, J., Weitzberg, E., and Lundberg, J.O. (2004). Effect of intravenous L-NMMA on nitric oxide production in collagenous colitis. Scand. J. Gastroenterol. 39, 32–36.10.1080/00365520310007611Suche in Google Scholar PubMed

Richardson, A.R., Dunman, P.M., and Fang, F.C. (2006). The nitrosative stress response of Staphylococcus aureus is required for resistance to innate immunity. Mol. Microbiol. 61, 927–939.10.1111/j.1365-2958.2006.05290.xSuche in Google Scholar

Richardson, A.R., Soliven, K.C., Castor, M.E., Barnes, P.D., Libby, S.J., and Fang, F.C. (2009). The base excision repair system of Salmonella enterica serovar typhimurium counteracts DNA damage by host nitric oxide. PLoS Pathog. 5, e1000451.10.1371/journal.ppat.1000451Suche in Google Scholar

Rivero, A. (2006). Nitric oxide: an antiparasitic molecule of invertebrates. Trends Parasitol. 22, 219–225.10.1016/j.pt.2006.02.014Suche in Google Scholar

Rodionov, D.A., Dubchak, I.L., Arkin, A.P., Alm, E.J., and Gelfand, M.S. (2005). Dissimilatory metabolism of nitrogen oxides in bacteria: comparative reconstruction of transcriptional networks. PLoS Comput. Biol. 1, e55.10.1371/journal.pcbi.0010055Suche in Google Scholar

Saleh, M., Bartual, S.G., Abdullah, M.R., Jensch, I., Asmat, T.M., Petruschka, L., Pribyl, T., Gellert, M., Lillig, C.H., Antelmann, H., et al. (2013). Molecular architecture of Streptococcus pneumoniae surface thioredoxin-fold lipoproteins crucial for extracellular oxidative stress resistance and maintenance of virulence. EMBO. Mol. Med. 5, 1852–1870.10.1002/emmm.201202435Suche in Google Scholar

Samanovic, M.I., Tu, S., Novak, O., Iyer, L.M., McAllister, F.E., Aravind, L., Gygi, S.P., Hubbard, S.R., Strnad, M., and Darwin, K.H. (2015). Proteasomal control of cytokinin synthesis protects Mycobacterium tuberculosis against nitric oxide. Mol. Cell 57, 984–994.10.1016/j.molcel.2015.01.024Suche in Google Scholar

Sapp, A.M., Mogen, A.B., Almand, E.A., Rivera, F.E., Shaw, L.N., Richardson, A.R., and Rice, K.C. (2014). Contribution of the nos-pdt operon to virulence phenotypes in methicillin-sensitive Staphylococcus aureus. PLoS One 9, e108868.10.1371/journal.pone.0108868Suche in Google Scholar

Savidge, T.C., Urvil, P., Oezguen, N., Ali, K., Choudhury, A., Acharya, V., Pinchuk, I., Torres, A.G., English, R.D., Wiktorowicz, J.E., et al. (2011). Host S-nitrosylation inhibits clostridial small molecule-activated glucosylating toxins. Nat. Med. 17, 1136–1141.10.1038/nm.2405Suche in Google Scholar

Schapiro, J.M., Libby, S.J., and Fang, F.C. (2003). Inhibition of bacterial DNA replication by zinc mobilization during nitrosative stress. Proc. Natl. Acad. Sci. U. S. A. 100, 8496–8501.10.1073/pnas.1033133100Suche in Google Scholar

Scorza, G., Pietraforte, D., and Minetti, M. (1997). Role of ascorbate and protein thiols in the release of nitric oxide from S-nitroso-albumin and S-nitroso-glutathione in human plasma. Free Radic. Biol. Med. 22, 633–642.10.1016/S0891-5849(96)00378-4Suche in Google Scholar

Selby, C.P. (2017). Mfd protein and transcription-repair coupling in Escherichia coli. Photochem. Photobiol. 93, 280–295.10.1111/php.12675Suche in Google Scholar PubMed PubMed Central

Selby, C.P., Witkin, E.M., and Sancar, A. (1991). Escherichia colimfd mutant deficient in “mutation frequency decline” lacks strand-specific repair: in vitro complementation with purified coupling factor. Proc. Natl. Acad. Sci. U. S. A. 88, 11574–11578.10.1073/pnas.88.24.11574Suche in Google Scholar PubMed PubMed Central

Sennequier, N. and Goff, S.V.-L. (1998). Biosynthèse du monoxyde d’azote (NO): mécanisme, régulation et contrôle [Biosynthesis of NO: mechanism, regulation and control]. Médecine/science 14, 1185–1195.10.4267/10608/936Suche in Google Scholar

Shatalin, K., Gusarov, I., Avetissova, E., Shatalina, Y., McQuade, L.E., Lippard, S.J., and Nudler, E. (2008). Bacillus anthracis-derived nitric oxide is essential for pathogen virulence and survival in macrophages. Proc. Natl. Acad. Sci. U. S. A. 105, 1009–1013.10.1073/pnas.0710950105Suche in Google Scholar PubMed PubMed Central

Shimizu, T., Hirai, S., Yokoyama, E., Ichimura, K., and Noda, M. (2015). An evolutionary analysis of nitric oxide reductase gene norV in enterohemorrhagic Escherichia coli O157. Infect. Genet. Evol. 33, 176–181.10.1016/j.meegid.2015.04.027Suche in Google Scholar PubMed

Singer, M., Deutschman, C.S., Seymour, C.W., Shankar-Hari, M., Annane, D., Bauer, M., Bellomo, R., Bernard, G.R., Chiche, J.D., Coopersmith, C.M., et al. (2016). The third international consensus definitions for sepsis and septic shock (Sepsis-3). J. Am. Med. Assoc. 315, 801–810.10.1001/jama.2016.0287Suche in Google Scholar PubMed PubMed Central

Singh, V.K., Vaish, M., Johansson, T.R., Baum, K.R., Ring, R.P., Singh, S., Shukla, S.K., and Moskovitz, J. (2015). Significance of four methionine sulfoxide reductases in Staphylococcus aureus. PLoS One 10, e0117594.10.1371/journal.pone.0117594Suche in Google Scholar PubMed PubMed Central

Sobko, T., Reinders, C.I., Jansson, E., Norin, E., Midtvedt, T., and Lundberg, J.O. (2005). Gastrointestinal bacteria generate nitric oxide from nitrate and nitrite. Nitric Oxide. 13, 272–278.10.1016/j.niox.2005.08.002Suche in Google Scholar PubMed

Sobko, T., Huang, L., Midtvedt, T., Norin, E., Gustafsson, L.E., Norman, M., Jansson, E.A., and Lundberg, J.O. (2006). Generation of NO by probiotic bacteria in the gastrointestinal tract. Free Radic. Biol. Med. 41, 985–991.10.1016/j.freeradbiomed.2006.06.020Suche in Google Scholar PubMed

Sokol, H., Pigneur, B., Watterlot, L., Lakhdari, O., Bermudez-Humaran, L.G., Gratadoux, J.J., Blugeon, S., Bridonneau, C., Furet, J.P., Corthier, G., et al. (2008). Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc. Natl. Acad. Sci. U. S. A. 105, 16731–16736.10.1073/pnas.0804812105Suche in Google Scholar PubMed PubMed Central

Spek, E.J., Wright, T.L., Stitt, M.S., Taghizadeh, N.R., Tannenbaum, S.R., Marinus, M.G., and Engelward, B.P. (2001). Recombinational repair is critical for survival of Escherichia coli exposed to nitric oxide. J. Bacteriol. 183, 131–138.10.1128/JB.183.1.131-138.2001Suche in Google Scholar

Spiro, S. (2007). Regulators of bacterial responses to nitric oxide. FEMS. Microbiol. Rev. 31, 193–211.10.1111/j.1574-6976.2006.00061.xSuche in Google Scholar

St John, G., Brot, N., Ruan, J., Erdjument-Bromage, H., Tempst, P., Weissbach, H., and Nathan, C. (2001). Peptide methionine sulfoxide reductase from Escherichia coli and Mycobacterium tuberculosis protects bacteria against oxidative damage from reactive nitrogen intermediates. Proc. Natl. Acad. Sci. U. S. A. 98, 9901–9906.10.1073/pnas.161295398Suche in Google Scholar

Stamler, J.S., Lamas, S., and Fang, F.C. (2001). Nitrosylation. The prototypic redox-based signaling mechanism. Cell 106, 675–683.10.1016/S0092-8674(01)00495-0Suche in Google Scholar

Stern, A.M., Liu, B., Bakken, L.R., Shapleigh, J.P., and Zhu, J. (2013). A novel protein protects bacterial iron-dependent metabolism from nitric oxide. J. Bacteriol. 195, 4702–4708.10.1128/JB.00836-13Suche in Google Scholar PubMed PubMed Central

Stevanin, T.M., Read, R.C., and Poole, R.K. (2007). The hmp gene encoding the NO-inducible flavohaemoglobin in Escherichia coli confers a protective advantage in resisting killing within macrophages, but not in vitro: links with swarming motility. Gene 398, 62–68.10.1016/j.gene.2007.03.021Suche in Google Scholar PubMed

Stryer, L. (1995). Biochemistry, 4th edition. (New York, NY, USA: W. H Freeman and Company), p. 732.Suche in Google Scholar

Sudhamsu, J. and Crane, B.R. (2009). Bacterial nitric oxide synthases: what are they good for? Trends Microbiol. 17, 212–218.10.1016/j.tim.2009.02.003Suche in Google Scholar PubMed

Suharti, Strampraad, M.J., Schroder, I., and de Vries, S. (2001). A novel copper A containing menaquinol NO reductase from Bacillus azotoformans. Biochemistry 40, 2632–2639.10.1021/bi0020067Suche in Google Scholar PubMed

Suvarnapunya, A.E., Lagasse, H.A., and Stein, M.A. (2003). The role of DNA base excision repair in the pathogenesis of Salmonella enterica serovar Typhimurium. Mol. Microbiol. 48, 549–559.10.1046/j.1365-2958.2003.03460.xSuche in Google Scholar PubMed

Svensson, L., Poljakovic, M., Save, S., Gilberthorpe, N., Schon, T., Strid, S., Corker, H., Poole, R.K., and Persson, K. (2010). Role of flavohemoglobin in combating nitrosative stress in uropathogenic Escherichia coli – implications for urinary tract infection. Microb. Pathog. 49, 59–66.10.1016/j.micpath.2010.04.001Suche in Google Scholar PubMed

Swiatczak, B. and Cohen, I.R. (2015). Gut feelings of safety: tolerance to the microbiota mediated by innate immune receptors. Microbiol. Immunol. 59, 573–585.10.1111/1348-0421.12318Suche in Google Scholar PubMed

Tarantino, M., Dionisi, A.M., Pistoia, C., Petrucci, P., Luzzi, I., and Pasquali, P. (2009). Involvement of nitric oxide in the control of a mouse model of Campylobacter jejuni infection. FEMS. Immunol. Med. Microbiol. 56, 98–101.10.1111/j.1574-695X.2009.00547.xSuche in Google Scholar PubMed

Tharmalingam, S., Alhasawi, A., Appanna, V.P., Lemire, J., and Appanna, V.D. (2017). Reactive nitrogen species (RNS)-resistant microbes: adaptation and medical implications. Biol. Chem. 398, 1193–1208.10.1515/hsz-2017-0152Suche in Google Scholar PubMed

Thursby, E. and Juge, N. (2017). Introduction to the human gut microbiota. Biochem. J. 474, 1823–1836.10.1042/BCJ20160510Suche in Google Scholar PubMed PubMed Central

Tiso, M. and Schechter, A.N. (2015). Nitrate reduction to nitrite, nitric oxide and ammonia by gut bacteria under physiological conditions. PLoS One 10, e0119712.10.1371/journal.pone.0119712Suche in Google Scholar PubMed PubMed Central

Tricoire, L. and Vitalis, T. (2012). Neuronal nitric oxide synthase expressing neurons: a journey from birth to neuronal circuits. Front Neural. Circuits 6, 82.10.3389/fncir.2012.00082Suche in Google Scholar PubMed PubMed Central

Tucker, N.P., Le Brun, N.E., Dixon, R., and Hutchings, M.I. (2010). There’s NO stopping NsrR, a global regulator of the bacterial NO stress response. Trends Microbiol. 18, 149–156.10.1016/j.tim.2009.12.009Suche in Google Scholar PubMed

Umezawa, K., Akaike, T., Fujii, S., Suga, M., Setoguchi, K., Ozawa, A., and Maeda, H. (1997). Induction of nitric oxide synthesis and xanthine oxidase and their roles in the antimicrobial mechanism against Salmonella typhimurium infection in mice. Infect. Immun. 65, 2932–2940.10.1128/iai.65.7.2932-2940.1997Suche in Google Scholar PubMed PubMed Central

Vaish, M. and Singh, V.K. (2013). Antioxidant functions of nitric oxide synthase in a methicillin sensitive Staphylococcus aureus. Int. J. Microbiol. 2013, 312146.10.1155/2013/312146Suche in Google Scholar PubMed PubMed Central

van Sorge, N.M., Beasley, F.C., Gusarov, I., Gonzalez, D.J., von Kockritz-Blickwede, M., Anik, S., Borkowski, A.W., Dorrestein, P.C., Nudler, E., and Nizet, V. (2013). Methicillin-resistant Staphylococcus aureus bacterial nitric-oxide synthase affects antibiotic sensitivity and skin abscess development. J. Biol. Chem. 288, 6417–6426.10.1074/jbc.M112.448738Suche in Google Scholar PubMed PubMed Central

Vareille, M., de Sablet, T., Hindre, T., Martin, C., and Gobert, A.P. (2007). Nitric oxide inhibits Shiga-toxin synthesis by enterohemorrhagic Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 104, 10199–10204.10.1073/pnas.0702589104Suche in Google Scholar PubMed PubMed Central

Vasudevan, S.G., Armarego, W.L., Shaw, D.C., Lilley, P.E., Dixon, N.E., and Poole, R.K. (1991). Isolation and nucleotide sequence of the hmp gene that encodes a haemoglobin-like protein in Escherichia coli K-12. Mol. Gen. Genet. 226, 49–58.10.1007/BF00273586Suche in Google Scholar PubMed

Vazquez-Torres, A. and Baumler, A.J. (2016). Nitrate, nitrite and nitric oxide reductases: from the last universal common ancestor to modern bacterial pathogens. Curr. Opin. Microbiol. 29, 1–8.10.1016/j.mib.2015.09.002Suche in Google Scholar PubMed PubMed Central

Vergne, I., Singh, S., Roberts, E., Kyei, G., Master, S., Harris, J., de Haro, S., Naylor, J., Davis, A., Delgado, M., and Deretic, V. (2006). Autophagy in immune defense against Mycobacterium tuberculosis. Autophagy 2, 175–178.10.4161/auto.2830Suche in Google Scholar PubMed

Vermeiren, J., Van de Wiele, T., Verstraete, W., Boeckx, P., and Boon, N. (2009). Nitric oxide production by the human intestinal microbiota by dissimilatory nitrate reduction to ammonium. J. Biomed. Biotechnol. 2009, 284718.10.1155/2009/284718Suche in Google Scholar PubMed PubMed Central

Vincent, S.R. (2010). Nitric oxide neurons and neurotransmission. Prog. Neurobiol. 90, 246–255.10.1016/j.pneurobio.2009.10.007Suche in Google Scholar PubMed

Vine, C.E., Justino, M.C., Saraiva, L.M., and Cole, J. (2010). Detection by whole genome microarrays of a spontaneous 126-gene deletion during construction of a ytfE mutant: confirmation that a ytfE mutation results in loss of repair of iron-sulfur centres in proteins damaged by oxidative or nitrosative stress. J. Microbiol. Methods. 81, 77–79.10.1016/j.mimet.2010.01.023Suche in Google Scholar PubMed

Volbeda, A., Dodd, E.L., Darnault, C., Crack, J.C., Renoux, O., Hutchings, M.I., Le Brun, N.E., and Fontecilla-Camps, J.C. (2017). Crystal structures of the NO sensor NsrR reveal how its iron-sulfur cluster modulates DNA binding. Nat. Commun. 8, 15052.10.1038/ncomms15052Suche in Google Scholar PubMed PubMed Central

Walter, U., Eigenthaler, M., Geiger, J., and Reinhard, M. (1993). Role of cyclic nucleotide-dependent protein kinases and their common substrate VASP in the regulation of human platelets. Adv. Exp. Med. Biol. 344, 237–249.10.1007/978-1-4615-2994-1_19Suche in Google Scholar PubMed

Wang, J., Vine, C.E., Balasiny, B.K., Rizk, J., Bradley, C.L., Tinajero-Trejo, M., Poole, R.K., Bergaust, L.L., Bakken, L.R., and Cole, J.A. (2016). The roles of the hybrid cluster protein, Hcp and its reductase, Hcr, in high affinity nitric oxide reduction that protects anaerobic cultures of Escherichia coli against nitrosative stress. Mol. Microbiol. 100, 877–892.10.1111/mmi.13356Suche in Google Scholar PubMed

Weiner, H.L., da Cunha, A.P., Quintana, F., and Wu, H. (2011). Oral tolerance. Immunol. Rev. 241, 241–259.10.1111/j.1600-065X.2011.01017.xSuche in Google Scholar PubMed PubMed Central

Wink, D.A., Kasprzak, K.S., Maragos, C.M., Elespuru, R.K., Misra, M., Dunams, T.M., Cebula, T.A., Koch, W.H., Andrews, A.W., Allen, J.S., et al. (1991). DNA deaminating ability and genotoxicity of nitric oxide and its progenitors. Science 254, 1001–1003.10.1126/science.1948068Suche in Google Scholar PubMed

Winter, S.E. and Baumler, A.J. (2014). Dysbiosis in the inflamed intestine: chance favors the prepared microbe. Gut Microbes. 5, 71–73.10.4161/gmic.27129Suche in Google Scholar PubMed PubMed Central

Winter, S.E., Winter, M.G., Xavier, M.N., Thiennimitr, P., Poon, V., Keestra, A.M., Laughlin, R.C., Gomez, G., Wu, J., Lawhon, S.D., et al. (2013). Host-derived nitrate boosts growth of E. coli in the inflamed gut. Science 339, 708–711.10.1126/science.1232467Suche in Google Scholar PubMed PubMed Central

Wu, G., Cruz-Ramos, H., Hill, S., Green, J., Sawers, G., and Poole, R.K. (2000). Regulation of cytochrome bd expression in the obligate aerobe Azotobacter vinelandii by CydR (Fnr). Sensitivity to oxygen, reactive oxygen species, and nitric oxide. J. Biol. Chem. 275, 4679–4686.10.1074/jbc.275.7.4679Suche in Google Scholar PubMed

Yang, C.S., Yuk, J.M., and Jo, E.K. (2009). The role of nitric oxide in mycobacterial infections. Immune Netw. 9, 46–52.10.4110/in.2009.9.2.46Suche in Google Scholar PubMed PubMed Central

Zhang, Y.H., Jin, C.Z., Jang, J.H., and Wang, Y. (2014). Molecular mechanisms of neuronal nitric oxide synthase in cardiac function and pathophysiology. J. Physiol. 592, 3189–3200.10.1113/jphysiol.2013.270306Suche in Google Scholar PubMed PubMed Central

Zhao, C., Hartke, A., La Sorda, M., Posteraro, B., Laplace, J.M., Auffray, Y., and Sanguinetti, M. (2010). Role of methionine sulfoxide reductases A and B of Enterococcus faecalis in oxidative stress and virulence. Infect Immun. 78, 3889–3897.10.1128/IAI.00165-10Suche in Google Scholar PubMed PubMed Central

Zhao, C., Zhou, Z., Zhang, T., Liu, F., Zhang, C.Y., Zen, K., and Gu, H. (2017). Salmonella small RNA fragment Sal-1 facilitates bacterial survival in infected cells via suppressing iNOS induction in a microRNA manner. Sci. Rep. 7, 16979.10.1038/s41598-017-17205-4Suche in Google Scholar PubMed PubMed Central

Zingarelli, B., O’Connor, M., Wong, H., Salzman, A.L., and Szabo, C. (1996). Peroxynitrite-mediated DNA strand breakage activates poly-adenosine diphosphate ribosyl synthetase and causes cellular energy depletion in macrophages stimulated with bacterial lipopolysaccharide. J. Immunol. 156, 350–358.10.4049/jimmunol.156.1.350Suche in Google Scholar

Zumft, W.G. (2005). Nitric oxide reductases of prokaryotes with emphasis on the respiratory, heme-copper oxidase type. J. Inorg. Biochem. 99, 194–215.10.1016/j.jinorgbio.2004.09.024Suche in Google Scholar PubMed

Received: 2019-09-13
Accepted: 2019-12-04
Published Online: 2019-12-07
Published in Print: 2020-04-28

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