Adaptation of Listeria monocytogenes to oxidative and nitrosative stress in IFN-γ-activated macrophages

International Journal of Medical Microbiology

Volumn 301, Issue 7, 2011, Pages 547-555

  Mraheil, Mobarak Abu ^a   Billion, André ^a   Mohamed, Walid ^a   Rawool, Deepak ^a   Hain, Torsten ^a   Chakraborty, Trinad ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

HPF; IFN ; Listeria monocytogenes; Macrophages; ROS

Indexed keywords

GAMMA INTERFERON; TRANSCRIPTOME;

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; HOST CELL; LISTERIA MONOCYTOGENES; MACROPHAGE; NITROSATIVE STRESS; OXIDATION; OXIDATIVE STRESS;

ADAPTATION, PHYSIOLOGICAL; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; INTERFERON-GAMMA; LISTERIA MONOCYTOGENES; MACROPHAGES; MICROARRAY ANALYSIS; MICROBIAL VIABILITY; OXIDATIVE STRESS; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN SPECIES; STRESS, PHYSIOLOGICAL;

EID: 80052698780     PISSN: 14384221     EISSN: 16180607     Source Type: Journal    
DOI: 10.1016/j.ijmm.2011.05.001     Document Type: Article

References (51)

1. Beissbarth T., Fellenberg K., Brors B., Arribas-Prat R., Boer J., Hauser N.C., Scheideler M., Hoheisel J.D., Schütz G., Poustka A., Vingron M. Processing and quality control of DNA array hybridization data. Bioinformatics 2000, 16:1014-1022.
2. Bogdan C., Röllinghoff M., Diefenbach A. The role of nitric oxide in innate immunity. Immunol. Rev. 2000, 173:17-26.
3. Bower J.M., Mulvey M.A. Polyamine-mediated resistance of uropathogenic Escherichia coli to nitrosative stress. J. Bacteriol. 2006, 188:928-933.
4. Chatterjee S.S., Hossain H., Otten S., Kuenne C., Kuchmina K., Machata S., Domann E., Chakraborty T., Hain T. Intracellular gene expression profile of Listeria monocytogenes. Infect. Immun. 2006, 74:1323-1338.
5. Crimmins G.T., Herskovits A.A., Rehder K., Sivick K.E., Lauer P., Dubensky T.W., Portnoy D.A. Listeria monocytogenes multidrug resistance transporters activate a cytosolic surveillance pathway of innate immunity. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:10191-10196.
6. Decker T., Stockinger S., Karaghiosoff M., Müller M., Kovarik P. IFNs and STATs in innate immunity to microorganisms. J. Clin. Invest. 2002, 109:1271-1277.
7. Freestone P., Nyström T., Trinei M., Norris V. The universal stress protein, UspA, of Escherichia coli is phosphorylated in response to stasis. J. Mol. Biol. 1997, 274:318-324.
8. Gaballa A., Helmann J.D. A peroxide-induced zinc uptake system plays an important role in protection against oxidative stress in Bacillus subtilis. Mol. Microbiol. 2002, 45:997-1005.
9. Glaser P., Frangeul L., Buchrieser C., Rusniok C., Amend A., Baquero F., Berche P., Bloecker H., Brandt P., Chakraborty T., Charbit A., Chetouani F., Couvé E., de Daruvar A., Dehoux P., Domann E., Domínguez-Bernal G., Duchaud E., Durant L., Dussurget O., Entian K.D., Fsihi H., García-del Portillo F., Garrido P., Gautier L., Goebel W., Gómez-López N., Hain T., Hauf J., Jackson D., Jones L.M., Kaerst U., Kreft J., Kuhn M., Kunst F., Kurapkat G., Madueno E., Maitournam A., Vicente J.M., Ng E., Nedjari H., Nordsiek G., Novella S., de Pablos B., Pérez-Diaz J.C., Purcell R., Remmel B., Rose M., Schlueter T., Simoes N., Tierrez A., Vázquez-Boland J.A., Voss H., Wehland J., Cossart P. Comparative genomics of Listeria species. Science 2001, 294:849-852.
10. Hain T., Steinweg C., Kuenne C.T., Billion A., Ghai R., Chatterjee S.S., Domann E., Kärst U., Goesmann A., Bekel T., Bartels D., Kaiser O., Meyer F., Pühler A., Weisshaar B., Wehland J., Liang C., Dandekar T., Lampidis R., Kreft J., Goebel W., Chakraborty T. Whole-genome sequence of Listeria welshimeri reveals common steps in genome reduction with Listeria innocua as compared to Listeria monocytogenes. J. Bacteriol. 2006, 188:7405-7415.
11. Havell E.A. Production of tumor necrosis factor during murine listeriosis. J. Immunol. 1987, 139:4225-42231.
12. Herskovits A.A., Auerbuch V., Portnoy D.A. Bacterial ligands generated in a phagosome are targets of the cytosolic innate immune system. PLoS Pathog. 2007, 3:e51.
13. Hsieh C.S., Macatonia S.E., Tripp C.S., Wolf S.F., O'Garra A., Murphy K.M. Development of TH1 CD4+ T cells through IL-12 produced by Listeria-induced macrophages. Science 1993, 260:547-549.
14. Huda M.N., Morita Y., Kuroda T., Mizushima T., Tsuchiya T. Na+-driven multidrug efflux pump VcmA from Vibrio cholerae non-O1, a non-halophilic bacterium. FEMS Microbiol. Lett. 2001, 203:235-239.
15. Igarashi K., Kashiwagi K. Polyamines: mysterious modulators of cellular functions. Biochem. Biophys. Res. Commun. 2000, 271:559-564.
16. Imlay J.A., Chin S.M., Linn S. Toxic DNA damage by hydrogen peroxide through the Fenton reaction in vivo and in vitro. Science 1988, 240:640-642.
17. Joseph B., Przybilla K., Stühler C., Schauer K., Slaghuis J., Fuchs T.M., Goebel W. Identification of Listeria monocytogenes genes contributing to intracellular replication by expression profiling and mutant screening. J. Bacteriol. 2006, 188:556-568.
18. Jung I.L., Oh T.J., Kim I.G. Abnormal growth of polyamine-deficient Escherichia coli mutant is partially caused by oxidative stress-induced damage. Arch. Biochem. Biophys. 2003, 418:125-132.
19. Kocks C., Gouin E., Tabouret M., Berche P., Ohayon H., Cossart P. L. monocytogenes-induced actin assembly requires the actA gene product, a surface protein. Cell 1992, 68:521-531.
20. Kolosova N., Sherman D., Karlson D., Dudareva N. Cellular and subcellular localization of S-adenosyl-l-methionine:benzoic acid carboxyl methyltransferase, the enzyme responsible for biosynthesis of the volatile ester methylbenzoate in snapdragon flowers. Plant Physiol. 2001, 126:956-964.
21. Kramer G.F., Ames B.N. Mechanisms of mutagenicity and toxicity of sodium selenite (Na2SeO3) in Salmonella typhimurium. Mutat. Res. 1988, 201:169-180.
22. Langermans J.A., van der Hulst M.E., Nibbering P.H., van der Meide P.H., van Furth R. Intravenous injection of interferon-gamma inhibits the proliferation of Listeria monocytogenes in the liver but not in the spleen and peritoneal cavity. Immunolog. 1992, 77:354-361.
23. Ledgham F., Quest B., Vallaeys T., Mergeay M., Covès J. A probable link between the DedA protein and resistance to selenite. Res. Microbiol. 2005, 156:367-374.
24. Makino M., Kawai M., Kawamura I., Fujita M., Gejo F., Mitsuyama M. Involvement of reactive oxygen intermediate in the enhanced expression of virulence-associated genes of Listeria monocytogenes inside activated macrophages. Microbiol. Immunol. 2005, 49:805-811.
25. Martin J.H., Edwards S.W. Interferon-gamma enhances monocyte cytotoxicity via enhanced reactive oxygen intermediate production. Absence of an effect on macrophage cytotoxicity is due to failure to enhance reactive nitrogen intermediate production. Immunolog. 1994, 81:592-597.
26. Morita Y., Kataoka A., Shiota S., Mizushima T., Tsuchiya T. NorM of Vibrio parahaemolyticus is an Na(+)-driven multidrug efflux pump. J. Bacteriol. 2000, 182:6694-6697.
27. Nachin L., Nannmark U., Nyström T. Differential roles of the universal stress proteins of Escherichia coli in oxidative stress resistance, adhesion, and motility. J. Bacteriol. 2005, 187:6265-6272.
28. Nathan C.F., Murray H.W., Wiebe M.E., Rubin B.Y. Identification of interferon-gamma as the lymphokine that activates human macrophage oxidative metabolism and antimicrobial activity. J. Exp. Med. 1983, 158:670-689.
29. Nathan C.F., Hibbs J.B. Role of nitric oxide synthesis in macrophage antimicrobial activity. Curr. Opin. Immunol. 1991, 3:65-70.
30. Nyström T., Neidhardt F.C. Expression and role of the universal stress protein, UspA, of Escherichia coli during growth arrest. Mol. Microbiol. 1994, 11:537-544.
31. Oh T.J., Kim I.G. The SOS induction of umu'-'lacZ fusion gene by oxidative damage is influenced by polyamines in Escherichia coli. Cell Biol. Toxicol. 1999, 15:291-297.
32. Oh T.J., Kim I.G. The expression of Escherichia coli SOS genes recA and uvrA is inducible by polyamines. Biochem. Biophys. Res. Commun. 1999, 264:584-589.
33. Pamer E.G. Immune responses to Listeria monocytogenes. Nat. Rev. Immunol. 2004, 4:812-823.
34. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001, 29:e45.
35. Pistor S., Chakraborty T., Niebuhr K., Domann E., Wehland J. The ActA protein of Listeria monocytogenes acts as a nucleator inducing reorganization of the actin cytoskeleton. EMBO J. 1994, 13:758-763.
36. Popov A., Abdullah Z., Wickenhauser C., Saric T., Driesen J., Hanisch F.G., Domann E., Raven E.L., Dehus O., Hermann C., Eggle D., Debey S., Chakraborty T., Krönke M., Utermöhlen O., Schultze J.L. Indoleamine 2,3-dioxygenase-expressing dendritic cells form suppurative granulomas following Listeria monocytogenes infection. J. Clin. Invest. 2006, 116:3160-3170.
37. Rando R.R. Chemical biology of isoprenylation/methylation. Biochem. Soc. Trans. 1996, 24:682-687.
38. Rea R.B., Gahan C.G., Hill C. Disruption of putative regulatory loci in Listeria monocytogenes demonstrates a significant role for Fur and PerR in virulence. Infect. Immun. 2004, 72:717-727.
39. Schapiro J.M., Libby S.J., Fang F.C. Inhibition of bacterial DNA replication by zinc mobilization during nitrosative stress. Proc. Natl. Acad. Sci. U. S. A. 2003, 100:8496-8501.
40. Schuchat A., Swaminathan B., Broome C.V. Epidemiology of human listeriosis. Clin. Microbiol. Rev. 1991, 4:169-183.
41. Setsukinai K., Urano Y., Kakinuma K., Majima H.J., Nagano T. Development of novel fluorescence probes that can reliably detect reactive oxygen species and distinguish specific species. J. Biol. Chem. 2003, 278:3170-3175.
42. Stritzker J., Janda J., Schoen C., Taupp M., Pilgrim S., Gentschev I., Schreier P., Geginat G., Goebel W. Growth, virulence, and immunogenicity of Listeria monocytogenes aro mutants. Infect. Immun. 2004, 72:5622-5629.
43. Swaminathan B., Gerner-Smidt P. The epidemiology of human listeriosis. Microbes Infect. 2007, 9:1236-1243.
44. Tasara T., Stephan R. Evaluation of housekeeping genes in Listeria monocytogenes as potential internal control references for normalizing mRNA expression levels in stress adaptation models using real-time PCR. FEMS Microbiol. Lett. 2007, 269:265-272.
45. Tripp C.S., Wolf S.F., Unanue E.R. Interleukin 12 and tumor necrosis factor alpha are costimulators of interferon gamma production by natural killer cells in severe combined immunodeficiency mice with listeriosis, and interleukin 10 is a physiologic antagonist. Proc. Natl. Acad. Sci. U. S. A. 1993, 90:3725-3729.
46. Tusher V.G., Tibshirani R., Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:5116-5121.
47. Urnov F.D. Methylation and the genome: the power of a small amendment. J. Nutr. 2002, 132:2450S-2456S.
48. van Dissel J.T., Stikkelbroeck J.J., Michel B.C., van den Barselaar M.T., Leijh P.C., van Furth R. Inability of recombinant interferon-gamma to activate the antibacterial activity of mouse peritoneal macrophages against Listeria monocytogenes and Salmonella typhimurium. J. Immunol. 1987, 139:1673-1678.
49. Vázquez-Boland J.A., Kuhn M., Berche P., Chakraborty T., Domínguez-Bernal G., Goebel W., González-Zorn B., Wehland J., Kreft J. Listeria pathogenesis and molecular virulence determinants. Clin. Microbiol. Rev. 2001, 14:584-640.
50. Xu S., Cooper A., Sturgill-Koszycki S., van Heyningen T., Chatterjee D., Orme I., Allen P., Russell D.G. Intracellular trafficking in Mycobacterium tuberculosis and Mycobacterium avium-infected macrophages. J. Immunol. 1994, 153:2568-2578.
51. Yoshikawa Y., Ogawa M., Hain T., Yoshida M., Fukumatsu M., Kim M., Mimuro H., Nakagawa I., Yanagawa T., Ishii T., Kakizuka A., Sztul E., Chakraborty T., Sasakawa C. Listeria monocytogenes ActA-mediated escape from autophagic recognition. Nat. Cell Biol. 2009, 11:1233-1240.