Effect of amikacin on cell wall glycopeptidolipid synthesis in Mycobacterium abscessus
- 140 Downloads
- 2 Citations
Abstract
Cultivation of the smooth colony Mycobacterium abscessus at the sub-minimum inhibitory concentration (MIC) of amikacin changed its growth pattern including its colony morphology (smooth to rough) and cell arrangement (dispersed to cord formation). In addition, reduced sliding motility and biofilm formation were observed. The amount of glycogpetidolipid (GPL) and mRNA expression of key genes involved in GPL synthesis were decreased in the amikacin-treated M. abscessus strain. An in vitro infection assay revealed that the amikacin-treated smooth M. abscessus strain induced more pro-inflammatory cytokines (TNF-α, IL-1β, IL-6) than that of the smooth strain in murine macrophage cells. These results suggest that long-term exposure to a low concentration of amikacin causes a physical change in the cell wall which may increase its virulence.
Keywords
Mycobacterium abscessus glycopeptidolipid (GPL) amikacin biofilmPreview
Unable to display preview. Download preview PDF.
Supplementary material
References
- Belisle, J.T. and Brennan, P.J. 1989. Chemical basis of rough and smooth variation in mycobacteria. J. Bacteriol. 171, 3465–3470.CrossRefPubMedPubMedCentralGoogle Scholar
- Brennan, P.J. and Goren, M.B. 1979. Structural studies on the typespecific antigens and lipids of the Mycobacterium avium.Mycobacterium intracellulare.Mycobacterium scrofulaceum serocomplex.Mycobacterium intracellulare serotype 9. J. Biol. Chem. 254, 4205–4211.PubMedGoogle Scholar
- Brown-Elliott, B.A. and Wallace, R.J. Jr. 2002. Clinical and taxonomic status of pathogenic nonpigmented or late-pigmenting rapidly growing mycobacteria. Clin. Microbiol. Rev. 15, 716–746.CrossRefPubMedPubMedCentralGoogle Scholar
- Carter, G., Wu, M., Drummond, D.C., and Bermudez, L.E. 2003. Characterization of biofilm formation by clinical isolates of Mycobacterium avium. J. Med. Microbiol. 52, 747–752.CrossRefPubMedGoogle Scholar
- Ceri, H., Olson, M.E., Stremick, C., Read, R.R., Morck, D., and Buret, A. 1999. The calgary biofilm device: New technology for rapid determination of antibiotic susceptibilities of bacterial biofilms. J. Clin. Microbiol. 37, 1771–1776.PubMedPubMedCentralGoogle Scholar
- Cheung, A.L., Eberhardt, K.J., and Fischetti, V.A. 1994. A method to isolate RNA from gram-positive bacteria and mycobacteria. Anal. Biochem. 222, 511–514.CrossRefPubMedGoogle Scholar
- Collins, F.M. and Cunningham, D.S. 1981. Systemic Mycobacterium kansasii infection and regulation of the alloantigenic response. Infect. Immun. 32, 614–624.PubMedPubMedCentralGoogle Scholar
- Colombo, R.E. and Olivier, K.N. 2008. Diagnosis and treatment of infections caused by rapidly growing mycobacteria. Semin. Respir. Crit. Care Med. 29, 577–588.CrossRefPubMedGoogle Scholar
- Dailloux, M., Abalain, M.L., Laurain, C., Lebrun, L., Loos-Ayav, C., Lozniewski, A., and Maugein, J. 2006. Respiratory infections associated with nontuberculous mycobacteria in non-hiv patients. Eur. Respir. J. 28, 1211–1215.CrossRefPubMedGoogle Scholar
- Daley, C.L. and Griffith, D.E. 2002. Pulmonary disease caused by rapidly growing mycobacteria. Clin. Chest Med. 23, 623–632, vii.CrossRefPubMedGoogle Scholar
- Davidson, L.B., Neßsar, R., Kempaiah, P., Perkins, D.J., and Byrd, T.F. 2011. Mycobacterium abscessus glycopeptidolipid prevents respiratory epithelial TLR2 signaling as measured by HßD2 gene expression and IL-8 release. PLoS One 6, e29148.CrossRefGoogle Scholar
- Ebert, D.L. and Olivier, K.N. 2002. Nontuberculous mycobacteria in the setting of cystic fibrosis. Clin. Chest Med. 23, 655–663.CrossRefPubMedGoogle Scholar
- Eckstein, T.M., Inamine, J.M., Lambert, M.L., and Belisle, J.T. 2000. A genetic mechanism for deletion of the ser2 gene cluster and formation of rough morphological variants of Mycobacterium avium. J. Bacteriol. 182, 6177–6182.CrossRefPubMedPubMedCentralGoogle Scholar
- Fregnan, G.B. and Smith, D.W. 1962. Description of various colony forms of mycobacteria. J. Bacteriol. 83, 819–827.PubMedPubMedCentralGoogle Scholar
- Griffith, D.E. 2003. Emergence of nontuberculous mycobacteria as pathogens in cystic fibrosis. Am. J. Respir. Crit. Care Med. 167, 810–812.CrossRefPubMedGoogle Scholar
- Griffith, D.E., Aksamit, T., Brown-Elliott, B.A., Catanzaro, A., Daley, C., Gordin, F., Holland, S.M., Horsburgh, R., Huitt, G., Iademarco, M.F., et al. 2007. An official ats/idsa statement: Diagnosis, treatment, and prevention of nontuberculous mycobacterial diseases. Am. J. Respir. Crit. Care Med. 175, 367–416.CrossRefPubMedGoogle Scholar
- Griffith, D.E., Girard, W.M., and Wallace, R.J.Jr. 1993. Clinical features of pulmonary disease caused by rapidly growing mycobacteria. An analysis of 154 patients. Am. Rev. Respir. Dis. 147, 1271–1278.CrossRefPubMedGoogle Scholar
- He, Z. and De Buck, J. 2010. Cell wall proteome analysis of Mycobacterium smegmatis strain MC2 155. BMC Microbiol. 10, 121.CrossRefPubMedPubMedCentralGoogle Scholar
- Howard, S.T., Rhoades, E., Recht, J., Pang, X., Alsup, A., Kolter, R., Lyons, C.R., and Byrd, T.F. 2006. Spontaneous reversion of Mycobacterium abscessus from a smooth to a rough morphotype is associated with reduced expression of glycopeptidolipid and reacquisition of an invasive phenotype. Microbiology 152, 1581–1590.CrossRefPubMedGoogle Scholar
- Ingram, C.W., Tanner, D.C., Durack, D.T., Kernodle, G.W., and Corey, G.R. 1993. Disseminated infection with rapidly growing mycobacteria. Clin. Infect. Dis. 16, 463–471.CrossRefPubMedGoogle Scholar
- Jeon, K., Kwon, O.J., Lee, N.Y., Kim, B.J., Kook, Y.H., Lee, S.H., Park, Y.K., Kim, C.K., and Koh, W.J. 2009. Antibiotic treatment of Mycobacterium abscessus lung disease: A retrospective analysis of 65 patients. Am. J. Respir. Crit. Care Med. 180, 896–902.CrossRefPubMedGoogle Scholar
- Kim, H.Y., Kim, B.J., Kook, Y., Yun, Y.J., Shin, J.H., Kim, B.J., and Kook, Y.H. 2010. Mycobacterium massiliense is differentiated from Mycobacterium abscessus and Mycobacterium bolletii by erythromycin ribosome methyltransferase gene (erm) and clarithromycin susceptibility patterns. Microbiol. Immunol. 54, 347–353.CrossRefPubMedGoogle Scholar
- Kim, H.Y., Yun, Y.J., Park, C.G., Lee, D.H., Cho, Y.K., Park, B.J., Joo, S.I., Kim, E.C., Hur, Y.J., Kim, B.J., et al. 2007. Outbreak of Mycobacterium massiliense infection associated with intramuscular injections. J. Clin. Microbiol. 45, 3127–3130.CrossRefPubMedPubMedCentralGoogle Scholar
- Koh, W.J., Jeon, K., Lee, N.Y., Kim, B.J., Kook, Y.H., Lee, S.H., Park, Y.K., Kim, C.K., Shin, S.J., Huitt, G.A., et al. 2011. Clinical significance of differentiation of Mycobacterium massiliense from Mycobacterium abscessus. Am. J. Respir. Crit. Care Med. 183, 405–410.CrossRefPubMedGoogle Scholar
- Koh, S.J., Song, T., Kang, Y.A., Choi, J.W., Chang, K.J., Chu, C.S., Jeong, J.G., Lee, J.Y., Song, M.K., Sung, H.Y., et al. 2010. An outbreak of skin and soft tissue infection caused by Mycobacterium abscessus following acupuncture. Clin. Microbiol. Infect. 16, 895–901.CrossRefPubMedGoogle Scholar
- Ma, C., Li, Y., Zeng, J., Wu, X., Liu, X., and Wang, Y. 2014. Mycobacterium bovis BCG triggered Myd88 induces miR-124 feedback negatively regulates immune response in alveolar epithelial cells. PLoS One 9, e92419.CrossRefGoogle Scholar
- Martin, C., Timm, J., Rauzier, J., Gomez-Lus, R., Davies, J., and Gicquel, B. 1990. Transposition of an antibiotic resistance element in mycobacteria. Nature 345, 739–743.CrossRefPubMedGoogle Scholar
- Mcneil, M., Chatterjee, D., Hunter, S.W., and Brennan, P.J. 1989. Mycobacterial glycolipids -isolation, structures, antigenicity, and synthesis of neoantigens. Methods Enzymol. 179, 215–242.CrossRefPubMedGoogle Scholar
- Mukherjee, R., Gomez, M., Jayaraman, N., Smith, I., and Chatterji, D. 2005. Hyperglycosylation of glycopeptidolipid of Mycobacterium smegmatis under nutrient starvation: Structural studies. Microbiology 151, 2385–2392.CrossRefPubMedGoogle Scholar
- Nash, K.A., Brown-Elliott, B.A., and Wallace, R.J.Jr. 2009. A novel gene, erm(41), confers inducible macrolide resistance to clinical isolates of Mycobacterium abscessus but is absent from Mycobacterium chelonae. Antimicrob. Agents Chemother. 53, 1367–1376.CrossRefPubMedPubMedCentralGoogle Scholar
- Petrini, B. 2006. Mycobacterium abscessus: An emerging rapid-growing potential pathogen. APMIS 114, 319–328.CrossRefPubMedGoogle Scholar
- Pierre-Audigier, C., Ferroni, A., Sermet-Gaudelus, I., Le Bourgeois, M., Offredo, C., Vu-Thien, H., Fauroux, B., Mariani, P., Munck, A., Bingen, E., et al. 2005. Age-related prevalence and distribution of nontuberculous mycobacterial species among patients with cystic fibrosis. J. Clin. Microbiol. 43, 3467–3470.CrossRefPubMedPubMedCentralGoogle Scholar
- Recht, J. and Kolter, R. 2001. Glycopeptidolipid acetylation affects sliding motility and biofilm formation in Mycobacterium smegmatis. J. Bacteriol. 183, 5718–5724.CrossRefPubMedPubMedCentralGoogle Scholar
- Rhoades, E., Hsu, F., Torrelles, J.B., Turk, J., Chatterjee, D., and Russell, D.G. 2003. Identification and macrophage-activating activity of glycolipids released from intracellular Mycobacterium bovis BCG. Mol. Microbiol. 48, 875–888.CrossRefPubMedGoogle Scholar
- Rhoades, E.R., Archambault, A.S., Greendyke, R., Hsu, F.F., Streeter, C., and Byrd, T. F. 2009. Mycobacterium abscessus glycopeptidolipids mask underlying cell wall phosphatidyl-myo-inositol mannosides blocking induction of human macrophage TNFalpha by preventing interaction with TLR2. J. Immunol. 183, 1997–2007.CrossRefPubMedGoogle Scholar
- Ripoll, F., Deshayes, C., Pasek, S., Laval, F., Beretti, J.L., Biet, F., Risler, J.L., Daffe, M., Etienne, G., Gaillard, J.L., et al. 2007. Genomics of glycopeptidolipid biosynthesis in Mycobacterium abscessus and M. chelonae. BMC Genomics 8, 114.CrossRefPubMedPubMedCentralGoogle Scholar
- Sanguinetti, M., Ardito, F., Fiscarelli, E., La Sorda, M., D’Argenio, P., Ricciotti, G., and Fadda, G. 2001. Fatal pulmonary infection due to multidrug-resistant Mycobacterium abscessus in a patient with cystic fibrosis. J. Clini. Microbiol. 39, 816–819.CrossRefGoogle Scholar
- Schaefer, W.B., Davis, C.L., and Cohn, M.L. 1970. Pathogenicity of transparent, opaque, and rough variants of Mycobacterium avium in chickens and mice. Am. Rev. Respir. Dis. 102, 499–506.PubMedGoogle Scholar
- Via, L.E., Fratti, R.A., McFalone, M., Pagan-Ramos, E., Deretic, D., and Deretic, V. 1998. Effects of cytokines on mycobacterial phagosome maturation. J. Cell Sci. 111, 897–905.PubMedGoogle Scholar
- Villeneuve, C., Etienne, G., Abadie, V., Montrozier, H., Bordier, C., Laval, F., Daffe, M., Maridonneau-Parini, I., and Astarie-Dequeker, C. 2003. Surface-exposed glycopeptidolipids of Mycobacterium smegmatis specifically inhibit the phagocytosis of mycobacteria by human macrophages. Identification of a novel family of glycopeptidolipids. J. Biol. Chem. 278, 51291–51300.PubMedGoogle Scholar