This Article
Right arrow Full Text
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Services
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Download to citation manager
Right arrowReprints and Permissions
Right arrow Copyright Information
Right arrow Books from ASM Press
Right arrow MicrobeWorld
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Google Scholar
Right arrow Articles by Stoll, H.
Right arrow Articles by Götz, F.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Stoll, H.
Right arrow Articles by Götz, F.

 Previous Article  |  Next Article 

Infection and Immunity, April 2005, p. 2411-2423, Vol. 73, No. 4
0019-9567/05/$08.00+0     doi:10.1128/IAI.73.4.2411-2423.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.

Staphylococcus aureus Deficient in Lipidation of Prelipoproteins Is Attenuated in Growth and Immune Activation

Hartmut Stoll,1 Jörn Dengjel,2 Christiane Nerz,1 and Friedrich Götz1*

Mikrobielle Genetik,1 Institute of Cell Biology, Department of Immunology, Universität Tübingen, Tübingen, Germany2

Received 20 August 2004/ Returned for modification 24 August 2004/ Accepted 6 December 2004

A lipoprotein diacylglyceryl transferase (lgt) deletion mutant of Staphylococcus aureus SA113 was constructed. The lipoprotein and prelipoprotein expression, the growth behavior, and the ability of the mutant to elicit an immune response in various host cells were studied. In the wild type, the majority of [14C]palmitate-labeled lipoproteins were located in the membrane fraction, although some lipoproteins were also present on the cell surface and in the culture supernatant. The lgt mutant completely lacked palmitate-labeled lipoproteins and released high amounts of some unmodified prelipoproteins, e.g., the oligopeptide-binding protein OppA, the peptidyl-prolyl cis-trans isomerase PrsA, and the staphylococcal iron transporter SitC, into the culture supernatant. The growth of the lgt mutant was hardly affected in rich medium but was retarded under nutrient limitation. The lgt mutant and its crude lysate induced much fewer proinflammatory cytokines and chemokines in human monocytic (MonoMac6), epithelial (pulmonary A549), and endothelial (human umbilical vein endothelial) cells than the wild type. However, in whole blood samples, the culture supernatant of the lgt mutant was equal or even superior to the wild-type supernatant in tumor necrosis factor alpha induction. Lipoprotein fractionation experiments provided evidence that a small proportion of the mature lipoproteins are released by the S. aureus wild type despite the lipid anchor and are trapped in part by the cell wall, thereby exposing the immune-activating lipid structure on the cell surface. Bacterial lipoproteins appear to be essential for a complete immune stimulation by gram-positive bacteria.

* Corresponding author. Mailing address: Mikrobielle Genetik, Universität Tübingen, Auf der Morgenstelle 28, D-72076 Tübingen, Germany. Phone: (49) 7071 29746-36 or (49) 7071 29746-35. Fax: (49) 7071 295039. E-mail: friedrich.goetz{at}uni-tuebingen.de.

Editor: J. B. Bliska

Infection and Immunity, April 2005, p. 2411-2423, Vol. 73, No. 4
0019-9567/05/$08.00+0     doi:10.1128/IAI.73.4.2411-2423.2005
Copyright © 2005, American Society for Microbiology. All Rights Reserved.



This article has been cited by other articles:

  • Munoz-Planillo, R., Franchi, L., Miller, L. S., Nunez, G. (2009). A Critical Role for Hemolysins and Bacterial Lipoproteins in Staphylococcus aureus-Induced Activation of the Nlrp3 Inflammasome. J. Immunol. 183: 3942-3948 [Abstract] [Full Text]  
  • Schmaler, M., Jann, N. J., Ferracin, F., Landolt, L. Z., Biswas, L., Gotz, F., Landmann, R. (2009). Lipoproteins in Staphylococcus aureus Mediate Inflammation by TLR2 and Iron-Dependent Growth In Vivo. J. Immunol. 182: 7110-7118 [Abstract] [Full Text]  
  • Bray, B. A., Sutcliffe, I. C., Harrington, D. J. (2009). Impact of lgt mutation on lipoprotein biosynthesis and in vitro phenotypes of Streptococcus agalactiae. Microbiology 155: 1451-1458 [Abstract] [Full Text]  
  • Tawaratsumida, K., Furuyashiki, M., Katsumoto, M., Fujimoto, Y., Fukase, K., Suda, Y., Hashimoto, M. (2009). Characterization of N-terminal Structure of TLR2-activating Lipoprotein in Staphylococcus aureus. J. Biol. Chem. 284: 9147-9152 [Abstract] [Full Text]  
  • 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. (2009). 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. 284: 8406-8411 [Abstract] [Full Text]  
  • Denham, E. L., Ward, P. N., Leigh, J. A. (2009). In the absence of Lgt, lipoproteins are shed from Streptococcus uberis independently of Lsp. Microbiology 155: 134-141 [Abstract] [Full Text]  
  • Wurfel, M. M., Gordon, A. C., Holden, T. D., Radella, F., Strout, J., Kajikawa, O., Ruzinski, J. T., Rona, G., Black, R. A., Stratton, S., Jarvik, G. P., Hajjar, A. M., Nickerson, D. A., Rieder, M., Sevransky, J., Maloney, J. P., Moss, M., Martin, G., Shanholtz, C., Garcia, J. G. N., Gao, L., Brower, R., Barnes, K. C., Walley, K. R., Russell, J. A., Martin, T. R. (2008). Toll-like Receptor 1 Polymorphisms Affect Innate Immune Responses and Outcomes in Sepsis. Am. J. Respir. Crit. Care Med. 178: 710-720 [Abstract] [Full Text]  
  • Parcina, M., Wendt, C., Goetz, F., Zawatzky, R., Zahringer, U., Heeg, K., Bekeredjian-Ding, I. (2008). Staphylococcus aureus-Induced Plasmacytoid Dendritic Cell Activation Is Based on an IgG-Mediated Memory Response. J. Immunol. 181: 3823-3833 [Abstract] [Full Text]  
  • Machata, S., Tchatalbachev, S., Mohamed, W., Jansch, L., Hain, T., Chakraborty, T. (2008). Lipoproteins of Listeria monocytogenes Are Critical for Virulence and TLR2-Mediated Immune Activation. J. Immunol. 181: 2028-2035 [Abstract] [Full Text]  
  • Henneke, P., Dramsi, S., Mancuso, G., Chraibi, K., Pellegrini, E., Theilacker, C., Hubner, J., Santos-Sierra, S., Teti, G., Golenbock, D. T., Poyart, C., Trieu-Cuot, P. (2008). Lipoproteins Are Critical TLR2 Activating Toxins in Group B Streptococcal Sepsis. J. Immunol. 180: 6149-6158 [Abstract] [Full Text]  
  • Seo, H. S., Michalek, S. M., Nahm, M. H. (2008). Lipoteichoic Acid Is Important in Innate Immune Responses to Gram-Positive Bacteria. Infect. Immun. 76: 206-213 [Abstract] [Full Text]  
  • Gust, A. A., Biswas, R., Lenz, H. D., Rauhut, T., Ranf, S., Kemmerling, B., Gotz, F., Glawischnig, E., Lee, J., Felix, G., Nurnberger, T. (2007). Bacteria-derived Peptidoglycans Constitute Pathogen-associated Molecular Patterns Triggering Innate Immunity in Arabidopsis. J. Biol. Chem. 282: 32338-32348 [Abstract] [Full Text]  
  • Hermann, C. (2007). Review: Variability of host pathogen interaction. Innate Immunity 13: 199-218 [Abstract]  
  • Neff, L., Daher, S., Muzzin, P., Spenato, U., Gulacar, F., Gabay, C., Bas, S. (2007). Molecular Characterization and Subcellular Localization of Macrophage Infectivity Potentiator, a Chlamydia trachomatis Lipoprotein. J. Bacteriol. 189: 4739-4748 [Abstract] [Full Text]  
  • Kraus, D., Kalbacher, H., Buschmann, J., Berger-Bachi, B., Gotz, F., Peschel, A. (2007). Muropeptide Modification-Amidation of Peptidoglycan D-Glutamate Does Not Affect the Proinflammatory Activity of Staphylococcus aureus. Infect. Immun. 75: 2084-2087 [Abstract] [Full Text]  
  • Hashimoto, M., Furuyashiki, M., Kaseya, R., Fukada, Y., Akimaru, M., Aoyama, K., Okuno, T., Tamura, T., Kirikae, T., Kirikae, F., Eiraku, N., Morioka, H., Fujimoto, Y., Fukase, K., Takashige, K., Moriya, Y., Kusumoto, S., Suda, Y. (2007). Evidence of Immunostimulating Lipoprotein Existing in the Natural Lipoteichoic Acid Fraction. Infect. Immun. 75: 1926-1932 [Abstract] [Full Text]  
  • Bekeredjian-Ding, I., Inamura, S., Giese, T., Moll, H., Endres, S., Sing, A., Zahringer, U., Hartmann, G. (2007). Staphylococcus aureus Protein A Triggers T Cell-Independent B Cell Proliferation by Sensitizing B Cells for TLR2 Ligands. J. Immunol. 178: 2803-2812 [Abstract] [Full Text]  
  • Baumgartner, M., Karst, U., Gerstel, B., Loessner, M., Wehland, J., Jansch, L. (2007). Inactivation of Lgt Allows Systematic Characterization of Lipoproteins from Listeria monocytogenes. J. Bacteriol. 189: 313-324 [Abstract] [Full Text]  
  • Garcia-del Portillo, F., Cossart, P. (2007). An Important Step in Listeria Lipoprotein Research. J. Bacteriol. 189: 294-297 [Full Text]  
  • Rahman, M. S., Ceraul, S. M., Dreher-Lesnick, S. M., Beier, M. S., Azad, A. F. (2007). The lspA Gene, Encoding the Type II Signal Peptidase of Rickettsia typhi: Transcriptional and Functional Analysis. J. Bacteriol. 189: 336-341 [Abstract] [Full Text]  
  • Hamilton, A., Robinson, C., Sutcliffe, I. C., Slater, J., Maskell, D. J., Davis-Poynter, N., Smith, K., Waller, A., Harrington, D. J. (2006). Mutation of the Maturase Lipoprotein Attenuates the Virulence of Streptococcus equi to a Greater Extent than Does Loss of General Lipoprotein Lipidation. Infect. Immun. 74: 6907-6919 [Abstract] [Full Text]  
  • Bubeck Wardenburg, J., Williams, W. A., Missiakas, D. (2006). Host defenses against Staphylococcus aureus infection require recognition of bacterial lipoproteins. Proc. Natl. Acad. Sci. USA 103: 13831-13836 [Abstract] [Full Text]  
  • Sibbald, M. J. J. B., Ziebandt, A. K., Engelmann, S., Hecker, M., de Jong, A., Harmsen, H. J. M., Raangs, G. C., Stokroos, I., Arends, J. P., Dubois, J. Y. F., van Dijl, J. M. (2006). Mapping the Pathways to Staphylococcal Pathogenesis by Comparative Secretomics. Microbiol. Mol. Biol. Rev. 70: 755-788 [Abstract] [Full Text]  
  • Hashimoto, M., Tawaratsumida, K., Kariya, H., Kiyohara, A., Suda, Y., Krikae, F., Kirikae, T., Gotz, F. (2006). Not Lipoteichoic Acid but Lipoproteins Appear to Be the Dominant Immunobiologically Active Compounds in Staphylococcus aureus.. J. Immunol. 177: 3162-3169 [Abstract] [Full Text]  
  • Grundling, A., Schneewind, O. (2006). Cross-Linked Peptidoglycan Mediates Lysostaphin Binding to the Cell Wall Envelope of Staphylococcus aureus.. J. Bacteriol. 188: 2463-2472 [Abstract] [Full Text]  
  • Hashimoto, M., Tawaratsumida, K., Kariya, H., Aoyama, K., Tamura, T., Suda, Y. (2006). Lipoprotein is a predominant Toll-like receptor 2 ligand in Staphylococcus aureus cell wall components. Int Immunol 18: 355-362 [Abstract] [Full Text]  


Copyright © 2009 by the American Society for Microbiology.   For an alternate route to Journals.ASM.org, visit: http://intl-journals.asm.org | More Info»