Structural reevaluation of Streptococcus pneumoniae lipoteichoic acid and new insights into its immunostimulatory potency

Journal of Biological Chemistry

Volumn 288, Issue 22, 2013, Pages 15654-15667

  Gisch, Nicolas ^a   Kohler, Thomas ^b   Ulmer, Artur J ^a   Muẗhing, Johannes ^c   Pribyl, Thomas ^b   Fischer, Kathleen ^a   Lindner, Buko ^a   Hammerschmidt, Sven ^b   Zaḧringer, Ulrich ^a  

^a RESEARCH CENTER BORSTEL   (Germany)

^b UNIVERSITY OF GREIFSWALD   (Germany)

^c UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CROSS-REACTIVITY; HUMAN MONONUCLEAR CELLS; HUMAN PATHOGENS; LIPOTEICHOIC ACIDS; PHOSPHORYLCHOLINE; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS PNEUMONIAE; STRUCTURAL MODELS;

BACTERIA; ELECTROSPRAY IONIZATION; MODEL STRUCTURES; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

BIOMATERIALS;

FORSSMAN ANTIGEN; HYDRAZINE; INTERLEUKIN 6; LIPOTEICHOIC ACID; TOLL LIKE RECEPTOR 2;

ANTIBODY DETECTION; ARTICLE; BACTERIAL STRAIN; BACTERIUM MUTANT; CONTROLLED STUDY; CROSS REACTION; CYTOKINE RELEASE; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; INFLAMMATION; MONONUCLEAR CELL; NONHUMAN; PRIORITY JOURNAL; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS PNEUMONIAE; STRUCTURE ANALYSIS;

ANALYTICAL CHEMISTRY; FORSSMAN ANTIGEN; IMMUNOSTIMULATORY POTENCY; INNATE IMMUNITY; LIPOTEICHOIC ACID; MASS SPECTROMETRY (MS); NMR; STREPTOCOCCUS PNEUMONIAE; STRUCTURAL BIOLOGY;

ADJUVANTS, IMMUNOLOGIC; ANTIBODIES, BACTERIAL; ANTIBODIES, HETEROPHILE; HUMANS; INTERLEUKIN-6; LEUKOCYTES, MONONUCLEAR; LIPOPOLYSACCHARIDES; MALE; MODELS, MOLECULAR; MUTATION; SPECIES SPECIFICITY; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS PNEUMONIAE; TEICHOIC ACIDS; TOLL-LIKE RECEPTOR 2;

POSIBACTERIA; STAPHYLOCOCCUS AUREUS; STREPTOCOCCUS PNEUMONIAE;

EID: 84878405643     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.446963     Document Type: Article

References (51)

1. Weidenmaier, C., and Peschel, A. (2008) Teichoic acids and related cell-wall glycopolymers in Gram-positive physiology and host interactions. Nat. Rev. Microbiol. 6, 276-287 (Pubitemid 351404772)
2. López, R. ( 2004) Streptococcus pneumoniae and its bacteriophages. One long argument. Int. Microbiol. 7, 163-171
3. Kadioglu, A., Weiser, J. N., Paton, J. C., and Andrew, P. W. (2008) The role of Streptococcus pneumoniae virulence factors in host respiratory colonization and disease. Nat. Rev. Microbiol. 6, 288-301 (Pubitemid 351404773)
4. Schmidt, R. R., Pedersen, C. M., Qiao, Y., and Zähringer, U. ( 2011) Chemical synthesis of bacterial lipoteichoic acids. An insight on its biological significance. Org. Biomol. Chem. 9, 2040-2052
5. Fischer, W., Behr, T., Hartmann, R., Peter-Katalinić, J., and Egge, H. ( 1993) Teichoic acid and lipoteichoic acid of Streptococcus pneumoniae possess identical chain structures. Eur. J. Biochem. 215, 851-857
6. Fischer, W. ( 1997) Pneumococcal lipoteichoic and teichoic acid. Microb. Drug Resist. 3, 309-325
7. Bergmann, S., and Hammerschmidt, S. (2006) Versatility of pneumococcal surface proteins. Microbiology 152, 295-303 (Pubitemid 43210660)
8. Gamez, G., and Hammerschmidt, S. ( 2012) Combat pneumococcal infections. Adhesins as candidates for protein-based vaccine developement. Curr. Drug Targets 13, 323-337
9. Voss, S., Gámez, G., and Hammerschmidt, S. ( 2012) Impact of pneumococcal microbial surface components recognizing adhesive matrix molecules on colonization. Mol. Oral Microbiol. 27, 246-256
10. Cundell, D. R., Gerard, N. P., Gerard, C., Idanpaan-Heikkila, I., and Tuomanen, E. I. ( 1995) Streptococcus pneumoniae anchor to activate human cells by the receptor for platelet-activating factor. Nature 377, 435- 438
11. Radin, J. N., Orihuela, C. J., Murti, G., Guglielmo, C., Murray, P. J., and Tuomanen, E. I. (2005) β-Arrestin 1 participates in platelet-activating factor receptor-mediated endocytosis of Streptococcus pneumoniae. Infect. Immun. 73, 7827-7835 (Pubitemid 41740265)
12. Behr, T., Fischer, W., Peter-Katalinić, J., and Egge, H. ( 1992) The structure of pneumococcal lipoteichoic acid. Eur. J. Biochem. 207, 1063-1075
13. Seo, H. S., Cartee, R. T., Pritchard, D. G., and Nahm, M. H. (2008) A new model of pneumococcal lipoteichoic acid structure resolves biochemical, biosynthetic, and serologic inconsistencies of the current model. J. Bacteriol. 190, 2379-2387 (Pubitemid 351466333)
14. Fischer, W. ( 2000) Pneumococcal lipoteichoic and teichoic acids. in Streptococcus pneumoniae: Molecular Biology and Mechanisms of Disease, pp. 155-177, Mary Ann Liebert, Inc., New York
15. Kinjo, Y., Illarionov, P., Vela, J. L., Pei, B., Girardi, E., Li, X., Li, Y., Imamura, M., Kaneko, Y., Okawara, A., Miyazaki, Y., Gómez-Velasco, A., Rogers, P., Dahesh, S., Uchiyama, S., Khurana, A., Kawahara, K., Yesilkaya, H., Andrew, P. W., Wong, C.-H., Kawakami, K., Nizet, V., Besra, G. S., Tsuji, M., Zajonc, D. M., and Kronenberg, M. ( 2011) Invariant natural killer T cells recognize glycolipids from pathogenic Gram-positive bacteria. Nat. Immunol. 12, 966-974
16. Heissigerova, H., Breton, C., Moravcova, J., and Imberty, A. (2003) Molecular modeling of glycosyltransferases involved in the biosynthesis of blood group A, blood group B, Forssman, and iGb3 antigens and their interaction with substrates. Glycobiology 13, 377-386 (Pubitemid 36592325)
17. Draing, C., Pfitzenmaier, M., Zummo, S., Mancuso, G., Geyer, A., Hartung, T., and von Aulock, S. (2006) Comparision of lipoteichoic acid from different serotypes of Streptococcus pneumoniae. J. Biol. Chem. 281, 33849-33859 (Pubitemid 46036597)
18. Courtney, H. S., Simpson, W. A., and Beachey, E. H. (1986) Relationship of critical micelle concentrations of bacterial lipoteichoic acids to biological activities. Infect. Immun. 51, 414-418 (Pubitemid 16212114)
19. Morath, S., Geyer, A., and Hartung, T. (2001) Structure-function relationship of cytokine induction by lipoteichoic acid from Staphylococcus aureus. J. Exp. Med. 193, 393-397 (Pubitemid 32524522)
20. Denapaite, D., Brückner, R., Hakenbeck, R., and Vollmer, W. ( 2012) Biosynthesis of teichoic acids in Streptococcus pneumoniae and closely related species. Lessons from genomes. Microb. Drug Resist. 18, 344-358
21. Zähringer, U., Lindner, B., Inamura, S., Heine, H., and Alexander, C. ( 2008) TLR2. Promiscuous or specific? A critical re-evaluation of a receptor expressing apparent broad specificity. Immunobiology 213, 205-224
22. Henneke, P., Morath, S., Uematsu, S., Weichert, S., Pfitzenmaier, M., Takeuchi, O., Müller, A., Poyart, C., Akira, S., Berner, R., Teti, G., Geyer, A., Hartung, T., Trieu-Cuot, P., Kasper, D. L., and Golenbock, D. T. (2005) Role of lipoteichoic acid in the phagocyte response to group B Streptococcus. J. Immunol. 174, 6449-6455 (Pubitemid 40663839)
23. Stoll, H., Dengjel, J., Nerz, C., and Götz, F. (2005) Staphylococcus aureus deficient in lipidation of prelipoproteins is attenuated in growth and immune activation. Infect. Immun. 73, 2411-2423 (Pubitemid 40470844)
24. Hashimoto, M., Tawaratsumida, K., Kariya, H., Kiyohara, A., Suda, Y., Krikae, F., Kirikae, T., and Götz, F. (2006) Not lipoteichoic acid but lipoproteins appear to be the dominant immunobiologically active compounds in Staphylococcus aureus. J. Immunol. 177, 3162-3169 (Pubitemid 44277834)
25. Jin, M. S., Kim, S. E., Heo, J. Y., Lee, M. E., Paik, S.-G., Lee, H., and Lee, J.-O. (2007) Crystal structure of the TLR1-TLR2 heterodimer induced by binding of a tri-acylated lipopeptide. Cell 130, 1071-1082 (Pubitemid 47410281)
26. Kang, J. Y., Nan, X., Jin, M. S., Youn, S.-J., Ryu, Y. H., Mah, S., Han, S. H., Lee, H., Paik, S.-G., and Lee, J.-O. ( 2009) Recognition of lipopeptide patterns by toll-like receptor 2-toll-like receptor 6 heterodimer. Immunity 31, 873-884
27. Farhat, K., Riekenberg, S., Heine, H., Debarry, J., Lang, R., Mages, J., Buwitt-Beckmann, U., Röschmann, K., Jung, G., Wiesmüller, K.-H., and Ulmer, A. J. ( 2008) Heterodimerization of TLR2 with TLR1 or TLR6 expands the ligand spectrum but does not lead to differential signaling. J. Leukoc. Biol. 83, 692-700
28. Rennemeier, C., Hammerschmidt, S., Niemann, S., Inamura, S., Zähringer, U., and Kehrel, B. E. (2007) Thrombospondin-1 promotes cellular adherence of Gram-positive pathogens via recognition of peptidoglycan. FASEB J. 21, 3118-3132 (Pubitemid 47565532)
29. Petit, C. M., Brown, J. R., Ingraham, K., Bryant, A. P., and Holmes, D. J. (2001) Lipid modification of prelipoproteins is dispensable for growth in vitro but essential for virulence in Streptococcus pneumoniae. FEMS Microbiol. Lett. 200, 229-233 (Pubitemid 32566367)
30. Hávarstein, L. S., Coomaraswamy, G., and Morrison, D. A. ( 1995) An unmodified heptadecapeptide pheromone induces competence for genetic transformation in Streptococcus pneumoniae. Proc. Natl. Acad. Sci. U.S.A. 92, 11140-11144
31. Fischer, W., Koch, H. U., and Haas, R. ( 1983) Improved preparation of lipoteichoic acids. Eur. J. Biochem. 133, 523-530
32. Lowry, O. H., Roberts, N. R., Leiner, K. Y., Wu, M. L., and Farr, A. L. ( 1954) The quantitative histochemistry of brain. I. Chemical methods. J. Biol. Chem. 207, 1-17
33. Morr, M., Takeuchi, O., Akira, S., Simon, M. M., and Mühlradt, P. F. (2002) Differential recognition of structural details of bacterial lipopeptides by toll-like receptors. Eur. J. Immunol. 32, 3337-3347 (Pubitemid 36024371)
34. Elling, L., Zervosen, A., Gutiérrez Gallego, R., Nieder, V., Malissard, M., Berger, E. G., Vliegenthart, J. F., and Kamerling, J. P. (1999) UDP-N-acetyl-α-D-glucosamine as acceptor substrate of β-1,4- galactosyltransferase. Enzymatic synthesis of UDP-N-acetyllactosamine. Glycoconjugate J. 16, 327-336 (Pubitemid 29535140)
35. Böyum, A. ( 1968) Isolation of mononuclear cells and granulocytes from human blood. Isolation of monuclear cells by one centrifugation, and of granulocytes by combining centrifugation and sedimentation at 1 g. Scand. J. Clin. Lab. Invest. Suppl. 97, 77-89
36. Debarry, J., Garn, H., Hanuszkiewicz, A., Dickgreber, N., Blümer, N., von Mutius, E., Bufe, A., Gatermann, S., Renz, H., and Holst, O. (2007) Acinetobacter lwoffii and Lactococcus lactis strains isolated from farm cowsheds possess strong allergy-protective properties. J. Allergy Clin. Immunol. 119, 1514-1521 (Pubitemid 46863371)
37. Saito, T., and Hakomori, S. I. ( 1971) Quantitative isolation of total glycosphingolipids from animal cells. J. Lipid Res. 12, 257-259
38. Kundu, S. K., and Roy, S. K. (1978)Arapid and quantitative method for the isolation of gangliosides and neutral glycosphingolipids by DEAE-silica gel chromatography. J. Lipid Res. 19, 390-395 (Pubitemid 8301839)
39. Ueno, K., Ando, S., and Yu, R. K. (1978) Gangliosides of human, cat, and rabbit spinal cords and cord myelin. J. Lipid Res. 19, 863-871 (Pubitemid 9028240)
40. Ledeen, R. W., and Yu, R. K. ( 1982) Gangliosides. Structure, isolation, and analysis. Methods Enzymol. 83, 139-191
41. Bethke, U., Kniep, B., and Mühlradt, P. F. (1987) Forssman glycolipid, an antigenic marker for a major subpopulation of macrophages from murine spleen and peripheral lymph nodes. J. Immunol. 138, 4329-4335 (Pubitemid 17090407)
42. Bethke, U., Müthing, J., Schauder, B., Conradt, P., and Mühlradt, P. F. (1986) An improved semi-quantitative enzyme immunostaining procedure for glycosphingolipid antigens on high performance thin layer chromatograms. J. Immunol. Methods 89, 111-116 (Pubitemid 16079587)
43. Müthing, J., Meisen, I., Zhang, W., Bielaszewska, M., Mormann, M., Bauerfeind, R., Schmidt, M. A., Friedrich, A. W., and Karch, H. ( 2012) Promiscuous Shiga toxin 2e and its intimate relationship to Forssman. Glycobiology 22, 849-862
44. Houliston, R. S., Bernatchez, S., Karwaski, M.-F., Mandrell, R. E., Jarrell, H. C., Wakarchuk, W. W., and Gilbert, M. ( 2009) Complete chemoenzymatic synthesis of the Forssman antigen using novel glycosyltransferases identified in Campylobacter jejuni and Pasteurella multocida. Glycobiology 19, 153-159
45. Pedersen, C. M., Figueroa-Perez, I., Lindner, B., Ulmer, A. J., Zähringer, U., and Schmidt, R. R. ( 2010) Total synthesis of lipoteichoic acid of Streptococcus pneumoniae. Angew. Chem. Int. Ed. Engl. 49, 2585-2590
46. Morath, S., Stadelmaier, A., Geyer, A., Schmidt, R. R., and Hartung, T. (2002) Synthetic lipoteichoic acid from Staphylococcus aureus is a potent stimulus of cytokine release. J. Exp. Med. 195, 1635-1640 (Pubitemid 34666076)
47. Dehus, O., Pfitzenmaier, M., Stuebs, G., Fischer, N., Schwaeble, W., Morath, S., Hartung, T., Geyer, A., and Hermann, C. ( 2011) Growth temperature-dependent expression of structural variants of Listeria monocytogenes lipoteichoic acid. Immunobiology 216, 24-31
48. Bui, N. K., Eberhardt, A., Vollmer, D., Kern, T., Bougault, C., Tomasz, A., Simorre, J.-P., and Vollmer, W. ( 2012) Isolation and analysis of cell wall components from Streptococcus pneumoniae. Anal. Biochem. 421, 657-666
49. Hummell, D. S., Swift, A. J., Tomasz, A., and Winkelstein, J. A. (1985) Activation of the alternative complement pathway by pneumococcal lipoteichoic acid. Infect. Immun. 47, 384-387 (Pubitemid 15169835)
50. Loos, M., Clas, F., and Fischer, W. (1986) Interaction of purified lipoteichoic acid with the classical complement pathway. Infect. Immun. 53, 595-599 (Pubitemid 16053181)
51. Lynch, N. J., Roscher, S., Hartung, T., Morath, S., Matsushita, M., Maennel, D. N., Kuraya, M., Fujita, T., and Schwaeble, W. J. (2004) L-Ficolin specifically binds to lipoteichoic acid, a cell wall constituent of Grampositive bacteria, and activates the lectin pathway of complement. J. Immunol. 172, 1198-1202 (Pubitemid 38113782)