Lipoprotein in the cell wall of Staphylococcus aureus is a major inducer of nitric oxide production in murine macrophages

Molecular Immunology

Volumn 65, Issue 1, 2015, Pages 17-24

  Kim, Nam Joong ^a   Ahn, Ki Bum ^a   Jeon, Jun Ho ^b   Yun, Cheol Heui ^a   Finlay, B Brett ^c   Han, Seung Hyun ^a  

^a Seoul National University   (South Korea)

^b Korea National Institute of Health   (South Korea)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Lipoproteins; Macrophage; Nitric oxide; Staphylococcus aureus; TLR2

Indexed keywords

BETA INTERFERON; DEXTRO ALANINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; LIPOPROTEIN; LIPOTEICHOIC ACID; NITRIC OXIDE; STAT1 PROTEIN; TOLL LIKE RECEPTOR 2; BACTERIAL PROTEIN; MESSENGER RNA; PHOSPHATIDYLGLYCEROL GLYCERYL TRANSFERASE; STAT1 PROTEIN, MOUSE; TLR2 PROTEIN, MOUSE; TRANSFERASE;

ANIMAL CELL; ARTICLE; BACTERIAL CELL WALL; CONTROLLED STUDY; INNATE IMMUNITY; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; STAPHYLOCOCCUS AUREUS; TRANSIENT TRANSFECTION; WESTERN BLOTTING; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL LINE; CELL WALL; ENZYME ACTIVATION; ENZYMOLOGY; GENETICS; HEK293 CELL LINE; HUMAN; IMMUNOLOGY; KNOCKOUT MOUSE; METABOLISM; PATHOGENICITY; PHOSPHORYLATION; STAPHYLOCOCCUS INFECTION;

MURINAE; MUS; POSIBACTERIA; STAPHYLOCOCCUS AUREUS;

ANIMALS; BACTERIAL PROTEINS; CELL LINE; CELL WALL; ENZYME ACTIVATION; HEK293 CELLS; HUMANS; LIPOPROTEINS; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NF-KAPPA B; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE II; PHOSPHORYLATION; RNA, MESSENGER; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; STAT1 TRANSCRIPTION FACTOR; TOLL-LIKE RECEPTOR 2; TRANSFERASES;

EID: 84922544804     PISSN: 01615890     EISSN: 18729142     Source Type: Journal    
DOI: 10.1016/j.molimm.2014.12.016     Document Type: Article

References (48)

1. Aubry C., Corr S.C., Wienerroither S., Goulard C., Jones R., Jamieson A.M., Decker T., O'Neill L.A., Dussurget O., Cossart P. Both TLR2 and TRIF contribute to interferon-β production during Listeria infection. PloS One 2012, 7:e33299.
2. Bubeck Wardenburg J., Williams W.A., Missiakas D. Host defenses against Staphylococcus aureus infection require recognition of bacterial lipoproteins. Proc. Natl. Acad. Sci. U.S.A. 2006, 103:13831-13836.
3. Castrillo A., Joseph S.B., Marathe C., Mangelsdorf D.J., Tontonoz P. Liver X receptor-dependent repression of matrix metalloproteinase-9 expression in macrophages. J. Biol. Chem. 2003, 278:10443-10449.
4. Crosara-Alberto D.P., Darini A.L., Inoue R.Y., Silva J.S., Ferreira S.H., Cunha F.Q. Involvement of NO in the failure of neutrophil migration in sepsis induced by Staphylococcus aureus. Br. J. Pharmacol. 2002, 136:645-658.
5. De Kimpe S.J., Kengatharan M., Thiemermann C., Vane J.R. The cell wall components peptidoglycan and lipoteichoic acid from Staphylococcus aureus act in synergy to cause shock and multiple organ failure. Proc. Natl. Acad. Sci. U.S.A. 1995, 92:10359-10363.
6. Deng W.G., Wu K.K. Regulation of inducible nitric oxide synthase expression by p300 and p50 acetylation. J. Immunol. 2003, 171:6581-6588.
7. Dufour J.F., Turner T.J., Arias I.M. Nitric oxide blocks bile canalicular contraction by inhibiting inositol trisphosphate-dependent calcium mobilization. Gastroenterology 1995, 108:841-849.
8. Duran W.N., Breslin J.W., Sanchez F.A. The NO cascade, eNOS location, and microvascular permeability. Cardiovasc. Res. 2010, 87:254-261.
9. Ellingsen E., Morath S., Flo T., Schromm A., Hartung T., Thiemermann C., Espevik T., Golenbock D., Foster D., Solberg R., Aasen A., Wang J. Induction of cytokine production in human T cells and monocytes by highly purified lipoteichoic acid: involvement of Toll-like receptors and CD14. Med. Sci. Monit. 2002, 8:BR149-BR156.
10. Farges J.C., Carrouel F., Keller J.F., Baudouin C., Msika P., Bleicher F., Staquet M.J. Cytokine production by human odontoblast-like cells upon Toll-like receptor-2 engagement. Immunobiology 2011, 216:513-517.
11. Fournier B., Philpott D.J. Recognition of Staphylococcus aureus by the innate immune system. Clin. Microbiol. Rev. 2005, 18:521-540.
12. Giustarini D., Rossi R., Milzani A., Dalle-Donne I. Nitrite and nitrate measurement by Griess reagent in human plasma: evaluation of interferences and standardization. Methods Enzymol. 2008, 440:361-380.
13. Han S.H., Kim J.H., Martin M., Michalek S.M., Nahm M.H. Pneumococcal lipoteichoic acid (LTA) is not as potent as staphylococcal LTA in stimulating Toll-like receptor 2. Infect. Immunol. 2003, 71:5541-5548.
14. Han S.H., Kim J.H., Seo H.S., Martin M.H., Chung G.H., Michalek S.M., Nahm M.H. Lipoteichoic acid-induced nitric oxide production depends on the activation of platelet-activating factor receptor and Jak2. J. Immunol. 2006, 176:573-579.
15. Hashimoto M., Tawaratsumida K., Kariya H., Aoyama K., Tamura T., Suda Y. Lipoprotein is a predominant Toll-like receptor 2 ligand in Staphylococcus aureus cell wall components. Int. Immunol. 2006, 18:355-362.
16. Hong S.W., Baik J.E., Kang S.S., Yun C.H., Seo D.G., Han S.H. Lipoteichoic acid of Streptococcus mutans interacts with Toll-like receptor 2 through the lipid moiety for induction of inflammatory mediators in murine macrophages. Mol. Immunol. 2014, 57:284-291.
17. Horton R.A., Ceppi E.D., Knowles R.G., Titheradge M.A. Inhibition of hepatic gluconeogenesis by nitric oxide: a comparison with endotoxic shock. Biochem. J. 1994, 299(Pt 3):735-739.
18. Jones E., Adcock I.M., Ahmed B.Y., Punchard N.A. Modulation of LPS stimulated NF-κB mediated nitric oxide production by PKCe and JAK2 in RAW macrophages. J. Inflamm. (Lond.) 2007, 4:23.
19. Kaito C., Sekimizu K. Colony spreading in Staphylococcus aureus. J. Bacteriol. 2007, 189:2553-2557.
20. Kang H.J., Ha J.M., Kim H.S., Lee H., Kurokawa K., Lee B.L. The role of phagocytosis in IL-8 production by human monocytes in response to lipoproteins on Staphylococcus aureus. Biochem. Biophys. Res. Commun. 2011, 406:449-453.
21. Kengatharan K.M., De Kimpe S., Robson C., Foster S.J., Thiemermann C. Mechanism of Gram-positive shock: identification of peptidoglycan and lipoteichoic acid moieties essential in the induction of nitric oxide synthase, shock, and multiple organ failure. J. Exp. Med. 1998, 188:305-315.
22. Kengatharan K.M., De Kimpe S.J., Thiemermann C. Role of nitric oxide in the circulatory failure and organ injury in a rodent model of Gram-positive shock. Br. J. Pharmacol. 1996, 119:1411-1421.
23. Kim J., Yang J., Park O.J., Kang S.S., Kim W.S., Kurokawa K., Yun C.H., Kim H.H., Lee B.L., Han S.H. Lipoproteins are an important bacterial component responsible for bone destruction through the induction of osteoclast differentiation and activation. J. Bone Miner. Res. 2013, 28:2381-2391.
24. Kim K.W., Im J., Jeon J.H., Lee H.G., Yun C.H., Han S.H. Staphylococcus aureus induces IL-1β expression through the activation of MAP kinases and AP-1, CRE and NF-κB transcription factors in the bovine mammary gland epithelial cells. Comp. Immunol. Microbiol. Infect. Dis. 2011, 34:347-354.
25. Kimbrell M.R., Warshakoon H., Cromer J.R., Malladi S., Hood J.D., Balakrishna R., Scholdberg T.A., David S.A. Comparison of the immunostimulatory and proinflammatory activities of candidate Gram-positive endotoxins, lipoteichoic acid, peptidoglycan, and lipopeptides, in murine and human cells. Immunol. Lett. 2008, 118:132-141.
26. Kovacs-Simon A., Titball R.W., Michell S.L. Lipoproteins of bacterial pathogens. Infect. Immunol. 2011, 79:548-561.
27. Kroncke K.D., Fehsel K., Kolb-Bachofen V. Inducible nitric oxide synthase in human diseases. Clin. Exp. Immunol. 1998, 113:147-156.
28. Kurokawa K., Lee H., Roh K.B., Asanuma M., Kim Y.S., Nakayama H., Shiratsuchi A., Choi Y., Takeuchi O., Kang H.J., Dohmae N., Nakanishi Y., Akira S., Sekimizu K., Lee B.L. The triacylated ATP binding cluster transporter substrate-binding lipoprotein of Staphylococcus aureus functions as a native ligand for toll-like receptor 2. J. Biol. Chem. 2009, 284:8406-8411.
29. Li H., Poulos T.L. Structure-function studies on nitric oxide synthases. J. Inorg. Biochem. 2005, 99:293-305.
30. Li Q., Kumar A., Gui J.F., Yu F.S. Staphylococcus aureus lipoproteins trigger human corneal epithelial innate response through toll-like receptor-2. Microb. Pathog. 2008, 44:426-434.
31. Long E.M., Millen B., Kubes P., Robbins S.M. Lipoteichoic acid induces unique inflammatory responses when compared to other toll-like receptor 2 ligands. PloS One 2009, 4:e5601.
32. Newton K., Dixit V.M. Signaling in innate immunity and inflammation. Cold Spring Harb. Perspect. Biol. 2012, 4.
33. Ohmori Y., Hamilton T.A. Requirement for STAT1 in LPS-induced gene expression in macrophages. J. Leukoc. Biol. 2001, 69:598-604.
34. Oku Y., Kurokawa K., Matsuo M., Yamada S., Lee B.L., Sekimizu K. Pleiotropic roles of polyglycerolphosphate synthase of lipoteichoic acid in growth of Staphylococcus aureus cells. J. Bacteriol. 2009, 191:141-151.
35. Pecora N.D., Gehring A.J., Canaday D.H., Boom W.H., Harding C.V. Mycobacterium tuberculosis LprA is a lipoprotein agonist of TLR2 that regulates innate immunity and APC function. J. Immunol. 2006, 177:422-429.
36. Peunova N., Enikolopov G. Nitric oxide triggers a switch to growth arrest during differentiation of neuronal cells. Nature 1995, 375:68-73.
37. Rockel C., Hartung T., Hermann C. Different Staphylococcus aureus whole bacteria mutated in putative pro-inflammatory membrane components have similar cytokine inducing activity. Immunobiology 2011, 216:316-321.
38. Sander P., Rezwan M., Walker B., Rampini S.K., Kroppenstedt R.M., Ehlers S., Keller C., Keeble J.R., Hagemeier M., Colston M.J., Springer B., Bottger E.C. Lipoprotein processing is required for virulence of Mycobacterium tuberculosis. Mol. Microbiol. 2004, 52:1543-1552.
39. Schmaler M., Jann N.J., Ferracin F., Landolt L.Z., Biswas L., Gotz F., Landmann R. Lipoproteins in Staphylococcus aureus mediate inflammation by TLR2 and iron-dependent growth in vivo. J. Immunol. 2009, 182:7110-7118.
40. Seeley E.J., Matthay M.A., Wolters P.J. Inflection points in sepsis biology: from local defense to systemic organ injury. Am. J. Physiol. Lung Cell Mol. Physiol. 2012, 303:L355-L363.
41. Stempelj M., Kedinger M., Augenlicht L., Klampfer L. Essential role of the JAK/STAT1 signaling pathway in the expression of inducible nitric-oxide synthase in intestinal epithelial cells and its regulation by butyrate. J. Biol. Chem. 2007, 282:9797-9804.
42. Stoll H., Dengjel J., Nerz C., Gotz F. Staphylococcus aureus deficient in lipidation of prelipoproteins is attenuated in growth and immune activation. Infect. Immunol. 2005, 73:2411-2423.
43. Takeuchi O., Akira S. Pattern recognition receptors and inflammation. Cell 2010, 140:805-820.
44. Takeuchi O., Hoshino K., Akira S. Cutting edge: TLR2-deficient and MyD88-deficient mice are highly susceptible to Staphylococcus aureus infection. J. Immunol. 2000, 165:5392-5396.
45. Tidhar A., Flashner Y., Cohen S., Levi Y., Zauberman A., Gur D., Aftalion M., Elhanany E., Zvi A., Shafferman A., Mamroud E. The NlpD lipoprotein is a novel Yersinia pestis virulence factor essential for the development of plague. PloS One 2009, 4:e7023.
46. Titheradge M.A. Nitric oxide in septic shock. Biochim. Biophys. Acta 1999, 1411:437-455.
47. Xiong Y., Song C., Snyder G.A., Sundberg E.J., Medvedev A.E. R753Q polymorphism inhibits Toll-like receptor (TLR) 2 tyrosine phosphorylation, dimerization with TLR6, and recruitment of myeloid differentiation primary response protein 88. J. Biol. Chem. 2012, 287:38327-38337.
48. Yoshimura A., Lien E., Ingalls R.R., Tuomanen E., Dziarski R., Golenbock D. Cutting edge: recognition of Gram-positive bacterial cell wall components by the innate immune system occurs via Toll-like receptor 2. J. Immunol. 1999, 163:1-5.