Glycolytic dependency of high-level nitric oxide resistance and virulence in staphylococcus aureus

mBio

Volumn 6, Issue 2, 2015, Pages

  Vitko, Nicholas P ^a   Spahich, Nicole A ^a   Richardson, Anthony R ^a  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CASAMINO ACID; GLUCONIC ACID; GLUCOSE; GLYCEROL; HEXOSE; LACTIC ACID; MANNITOL; MANNOSE; NITRIC OXIDE; PYRUVIC ACID; RIBOSE; SORBITOL;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BACTERIAL GROWTH; BACTERIAL VIRULENCE; CARBOHYDRATE METABOLISM; CARBON SOURCE; CONTROLLED STUDY; FEMALE; GLYCOLYSIS; INNATE IMMUNITY; MACROPHAGE; MOUSE; NONHUMAN; OXIDATION REDUCTION REACTION; PHAGOCYTOSIS; PRIORITY JOURNAL; SEPSIS; SKIN INFECTION; SOFT TISSUE INFECTION; STAPHYLOCOCCUS AUREUS; ANIMAL; C57BL MOUSE; DISEASE MODEL; DRUG EFFECTS; DRUG TOLERANCE; FERMENTATION; GROWTH, DEVELOPMENT AND AGING; IMMUNOLOGY; METABOLISM; MICROBIAL VIABILITY; MICROBIOLOGY; PHAGOCYTE; PHYSIOLOGY; STAPHYLOCOCCUS INFECTION; VIRULENCE;

BACTERIA (MICROORGANISMS); STAPHYLOCOCCUS AUREUS;

ANIMALS; DISEASE MODELS, ANIMAL; DRUG TOLERANCE; FEMALE; FERMENTATION; GLYCOLYSIS; LACTIC ACID; MICE, INBRED C57BL; MICROBIAL VIABILITY; NITRIC OXIDE; PHAGOCYTES; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; VIRULENCE;

EID: 84929494191     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00045-15     Document Type: Article

References (47)

1. Livermore DM. 2000. Antibiotic resistance in staphylococci. Int J Antimicrob Agents 16:3–10. http://dx.doi.org/10.1016/S0924-8579(00)00299-5.
2. Kong HH. 2011. Skin microbiome: genomics-based insights into the diversity and role of skin microbes. Trends Mol Med 17:320–328. http://dx.doi.org/10.1016/j.molmed.2011.01.013.
3. Archer GL. 1998. Staphylococcus aureus: a well-armed pathogen. Clin Infect Dis 26:1179–1181. http://dx.doi.org/10.1086/520289.
4. Xie QW, Cho HJ, Calaycay J, Mumford RA, Swiderek KM, Lee TD, Ding A, Troso T, Nathan C. 1992. Cloning and characterization of inducible nitric oxide synthase from mouse macrophages. Science 256: 225–228. http://dx.doi.org/10.1126/science.1373522.
5. Fang FC. 2004. Antimicrobial reactive oxygen and nitrogen species: concepts and controversies. Nat Rev Microbiol 2:820–832. http://dx.doi.org/10.1038/nrmicro1004.
6. Wink DA, Mitchell JB. 1998. Chemical biology of nitric oxide: insights into regulatory, cytotoxic, and cytoprotective mechanisms of nitric oxide. Free Radic Biol Med 25:434-456. http://dx.doi.org/10.1016/S0891-5849(98)00092-6.
7. Clementi E, Brown GC, Feelisch M, Moncada S. 1998. Persistent inhibition of cell respiration by nitric oxide: crucial role of S-nitrosylation of mitochondrial complex I and protective action of glutathione. Proc Natl Acad Sci U S A 95:7631–7636. http://dx.doi.org/10.1073/pnas.95.13.7631.
8. Richardson AR, Libby SJ, Fang FC. 2008. A nitric oxide-inducible lactate dehydrogenase enables Staphylococcus aureus to resist innate immunity. Science 319:1672–1676. http://dx.doi.org/10.1126/science.1155207.
9. Laurent M, Lepoivre M, Tenu JP. 1996. Kinetic modelling of the nitric oxide gradient generated in vitro by adherent cells expressing inducible nitric oxide synthase. Biochem J 314:109–113.
10. Lewis RS, Tamir S, Tannenbaum SR, Deen WM. 1995. Kinetic analysis of the fate of nitric oxide synthesized by macrophages in vitro. J Biol Chem 270:29350–29355. http://dx.doi.org/10.1074/jbc.270.49.29350.
11. Richardson AR, Dunman PM, Fang FC. 2006. The nitrosative stress response of Staphylococcus aureus is required for resistance to innate immunity. Mol Microbiol 61:927–939. http://dx.doi.org/10.1111/j.1365-2958.2006.05290.x.
12. Crooke AK, Fuller JR, Obrist MW, Tomkovich SE, Vitko NP, Richardson AR. 2013. CcpA-independent glucose regulation of lactate dehydrogenase 1 in Staphylococcus aureus. PLoS One 8:e54293. http://dx.doi.org/10.1371/journal.pone.0054293.
13. Thurlow LR, Joshi GS, Clark JR, Spontak JS, Neely CJ, Maile R, Richardson AR. 2013. Functional modularity of the arginine catabolic mobile element contributes to the success of USA300 methicillin-resistant Staphylococcus aureus. Cell Host Microbe 13:100–107. http://dx.doi.org/10.1016/j.chom.2012.11.012.
14. Abbe K, Takahashi S, Yamada T. 1982. Involvement of oxygen-sensitive pyruvate formate-lyase in mixed-acid fermentation by Streptococcus mutans under strictly anaerobic conditions. J Bacteriol 152:175–182.
15. Birkenstock T, Liebeke M, Winstel V, Krismer B, Gekeler C, Niemiec MJ, Bisswanger H, Lalk M, Peschel A. 2012. Exometabolome analysis identifies pyruvate dehydrogenase as a target for the antibiotic triphenylbismuthdichloride in multiresistant bacterial pathogens. J Biol Chem 287: 2887–2895. http://dx.doi.org/10.1074/jbc.M111.288894.
16. Vodovotz Y, Russell D, Xie QW, Bogdan C, Nathan C. 1995. Vesicle membrane association of nitric oxide synthase in primary mouse macrophages. J Immunol 154:2914–2925.
17. Bae T, Banger AK, Wallace A, Glass EM, Aslund F, Schneewind O, MissiakasDM. 2004. Staphylococcus aureus virulence genes identified by bursa aurealis mutagenesis and nematode killing. Proc Natl Acad SciUSA 101:12312–12317. http://dx.doi.org/10.1073/pnas.0404728101.
18. Coulter SN, Schwan WR, Ng EY, Langhorne MH, Ritchie HD, Westbrock-Wadman S, Hufnagle WO, Folger KR, Bayer AS, Stover CK. 1998. Staphylococcus aureus genetic loci impacting growth and survival in multiple infection environments. Mol Microbiol 30:393-404. http://dx.doi.org/10.1046/j.1365-2958.1998.01075.x.
19. Mei JM, Nourbakhsh F, Ford CW, Holden DW. 1997. Identification of Staphylococcus aureus virulence genes in a murine model of bacteraemia using signature-tagged mutagenesis. Mol Microbiol 26:399–407. http://dx.doi.org/10.1046/j.1365-2958.1997.5911966.x.
20. Purves J, Cockayne A, Moody PCE, Morrissey JA. 2010. Comparison of the regulation, metabolic functions, and roles in virulence of the glyceraldehyde-3-phosphate dehydrogenase homologues gapA and gapB in Staphylococcus aureus. Infect Immun 78:5223–5232. http://dx.doi.org/10.1128/IAI.00762-10.
21. Novick RP, Richmond MH. 1965. Nature and interactions of the genetic elements governing penicillinase synthesis in Staphylococcus aureus. J Bacteriol 90:467–480.
22. Herbert S, Ziebandt AK, Ohlsen K, Schäfer T, Hecker M, Albrecht D, Novick R, Götz F. 2010. Repair of global regulators in Staphylococcus aureus 8325 and comparative analysis with other clinical isolates. Infect Immun 78:2877–2889. http://dx.doi.org/10.1128/IAI.00088-10.
23. Theodore TS, Schade AL. 1965. Carbohydrate metabolism of iron-rich and iron-poor Staphylococcus aureus. J Gen Microbiol 40:385–395. http://dx.doi.org/10.1099/00221287-40-3-385.
24. Friedman DB, Stauff DL, Pishchany G, Whitwell CW, Torres VJ, Skaar EP. 2006. Staphylococcus aureus redirects central metabolism to increase iron availability. PLoS Pathog 2:e87. http://dx.doi.org/10.1371/journal.ppat.0020087.
25. Hammer ND, Reniere ML, Cassat JE, Zhang Y, Hirsch AO, Indriati Hood M, Skaar EP. 2013. Two heme-dependent terminal oxidases power Staphylococcus aureus organ-specific colonization of the vertebrate host. MBio 4(4):e00241-13. http://dx.doi.org/10.1128/mBio.00241-13.
26. Kutyshenko VP, Molchanov M, Beskaravayny P, Uversky VN, Timchenko MA. 2011. Analyzing and mapping sweat metabolomics by highresolution NMR spectroscopy. PLoS One 6:e28824. http://dx.doi.org/10.1371/journal.pone.0028824.
27. Harvey CJ, LeBouf RF, Stefaniak AB. 2010. Formulation and stability of a novel artificial human sweat under conditions of storage and use. Toxicol In Vitro 24:1790–1796. http://dx.doi.org/10.1016/j.tiv.2010.06.016.
28. Psychogios N, Hau DD, Peng J, Guo AC, Mandal R, Bouatra S, Sinelnikov I, Krishnamurthy R, Eisner R, Gautam B, Young N, Xia J, Knox C, Dong E, Huang P, Hollander Z, Pedersen TL, Smith SR, Bamforth F, Greiner R, McManus B, Newman JW, Goodfriend T, Wishart DS. 2011. The human serum metabolome. PLoS One 6:e16957. http://dx.doi.org/10.1371/journal.pone.0016957.
29. Fuller JR, Vitko NP, Perkowski EF, Scott E, Khatri D, Spontak JS, Thurlow LR, Richardson AR. 2011. Identification of a lactate-quinone oxidoreductase in Staphylococcus aureus that is essential for virulence. Front Cell Infect Microbiol 1:19. http://dx.doi.org/10.3389/fcimb.2011.00019.
30. Fuchs TM, Eisenreich W, Heesemann J, Goebel W. 2012. Metabolic adaptation of human pathogenic and related nonpathogenic bacteria to extra- and intracellular habitats. FEMS Microbiol Rev 36:435–462. http://dx.doi.org/10.1111/j.1574-6976.2011.00301.x.
31. Myint KT, Uehara T, Aoshima K, Oda Y. 2009. Polar anionic metabolome analysis by nano-LC/MS with a metal chelating agent. Anal Chem 81:7766–7772. http://dx.doi.org/10.1021/ac901269h.
32. McKinney JD, Höner zu Bentrup K, Muñoz-Elías EJ, Miczak A, Chen B, Chan WT, Swenson D, Sacchettini JC, Jacobs WR, Jr, Russell DG. 2014. Persistence of Mycobacterium tuberculosis in macrophages and mice requires the glyoxylate shunt enzyme isocitrate lyase. Nature 406: 735–738.
33. 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 U S A 107:9819-9824. http://dx.doi.org/10.1073/pnas.1000715107.
34. Eylert E, Schär J, Mertins S, Stoll R, Bacher A, Goebel W, Eisenreich W. 2008. Carbon metabolism of Listeria monocytogenes growing inside macrophages. Mol Microbiol 69:1008–1017. http://dx.doi.org/10.1111/j.1365-2958.2008.06337.x.
35. Fonseca MV, Swanson MS. 2014. Nutrient salvaging and metabolism by the intracellular pathogen Legionella pneumophila. Front Cell Microb Biol 4:12. http://dx.doi.org/10.3389/fcimb.2014.00012.
36. Lipsky BA, Tabak YP, Johannes RS, Vo L, Hyde L, Weigelt JA. 2010. Skin and soft tissue infections in hospitalised patients with diabetes: culture isolates and risk factors associated with mortality, length of stay and cost. Diabetologia 53:914-923. http://dx.doi.org/10.1007/s00125-010-1672-5.
37. Fowler VG, Jr, Miro JM, Hoen B, Cabell CH, Abrutyn E, Rubinstein E, Corey GR, Spelman D, Bradley SF, Barsic B, Pappas PA, Anstrom KJ, Wray D, Fortes CQ, Anguera I, Athan E, Jones P, van der Meer JTM, Elliott TSJ, Levine DP, Bayer AS, ICE Investigators. 2005. Staphylococcus aureus endocarditis: a consequence of medical progress. JAMA 293: 3012–3021. http://dx.doi.org/10.1001/jama.293.24.3012.
38. Kourany WM, Miro JM, Moreno A, Corey GR, Pappas PA, Abrutyn E, Hoen B, Habib G, Fowler VG, Jr, Sexton DJ, Olaison L, Cabell CH, ICE MD Investigators. 2006. Influence of diabetes mellitus on the clinical manifestations and prognosis of infective endocarditis: a report from the International Collaboration on Endocarditis-Merged Database. Scand J Infect Dis 38:613–619. http://dx.doi.org/10.1080/00365540600617017.
39. Geerlings SE, Hoepelman AI. 1999. Immune dysfunction in patients with diabetes mellitus (DM). FEMS Immunol Med Microbiol 26:259-265. http://dx.doi.org/10.1111/j.1574-695X.1999.tb01397.x.
40. King JT, Goulet JL, Perkal MF, Rosenthal RA. 2011. Glycemic control and infections in patients with diabetes undergoing noncardiac surgery. Ann Surg 253:158–165. http://dx.doi.org/10.1097/SLA.0b013e3181f9bb3a.
41. Kornum JB, Thomsen RW, Riis A, Lervang HH, Schønheyder HC, Sørensen HT. 2008. Diabetes, glycemic control, and risk of hospitalization with pneumonia: a population-based case-control study. Diabetes Care 31:1541–1545. http://dx.doi.org/10.2337/dc08-0138.
42. Dronge AS, Perkal MF, Kancir S, Concato J, Aslan M, Rosenthal RA. 2006. Long-term glycemic control and postoperative infectious complications. Arch Surg 141:375–380. http://dx.doi.org/10.1001/archsurg.141.4.375.
43. Zoraghi R, See RH, Axerio-Cilies P, Kumar NS, Gong H, Moreau A, Hsing M, Kaur S, Swayze RD, Worrall L, Amandoron E, Lian T, Jackson L, Jiang J, Thorson L, Labriere C, Foster L, Brunham RC, McMaster WR, Finlay BB, Strynadka NC, Cherkasov A, Young RN, Reiner NE. 2011. Identification of pyruvate kinase in methicillin-resistant Staphylococcus aureus as a novel antimicrobial drug target. Antimicrob Agents Chemother 55:2042–2053. http://dx.doi.org/10.1128/AAC.01250-10.
44. Zoraghi R, Worrall L, See RH, Strangman W, Popplewell WL, Gong H, Samaai T, Swayze RD, Kaur S, Vuckovic M, Finlay BB, Brunham RC, McMaster WR, Davies-Coleman MT, Strynadka NC, Andersen RJ, Reiner NE. 2011. Methicillin-resistant Staphylococcus aureus (MRSA) pyruvate kinase as a target for bis-indole alkaloids with antibacterial activities. J Biol Chem 286:44716-44725. http://dx.doi.org/10.1074/jbc.M111.289033.
45. Kumar NS, Dullaghan EM, Finlay BB, Gong H, Reiner NE, Selvam JJP, Thorson LM, Campbell S, Vitko N, Richardson AR, Zoraghi R, Young RN. 2014. Discovery and optimization of a new class of pyruvate kinase inhibitors as potential therapeutics for the treatment of methicillinresistant Staphylococcus aureus infections. Bioorg Med Chem 22: 1708–1725. http://dx.doi.org/10.1016/j.bmc.2014.01.020.
46. McNamara PJ, Proctor RA. 2000. Staphylococcus aureus small colony variants, electron transport and persistent infections. Int J Antimicrob Agents 14:117–122. http://dx.doi.org/10.1016/S0924-8579(99)00170-3.
47. Vitko NP, Richardson AR. 2005. Laboratory maintenance of methicillinresistant Staphylococcus aureus (MRSA). John Wiley & Sons, Hoboken, NJ. http://dx.doi.org/10.1002/9780471729259.mc09c02s28.