Neisseria meningitidis capsular polysaccharides induce inflammatory responses via TLR2 and TLR4-MD-2

Journal of Leukocyte Biology

Volumn 89, Issue 3, 2011, Pages 469-480

  Zughaier, Susu M ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Capsule; Cytokine; E5564; Inflammation; Macrophage; Vaccine

Indexed keywords

BACTERIAL POLYSACCHARIDE; BIOLOGICAL FACTOR; CD14 ANTIGEN; DIACYLGLYCEROL; ENDOTOXIN; ERITORAN; GAMMA INTERFERON INDUCIBLE PROTEIN 10; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; INTERLEUKIN 8; MONOCLONAL ANTIBODY; MYELOID DIFFERENTIATION PROTEIN 2; POLYMER; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 6; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BACTERIAL OUTER MEMBRANE; CONTROLLED STUDY; CYTOKINE RELEASE; DOSE RESPONSE; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOSTIMULATION; INFLAMMATION; INNATE IMMUNITY; MACROPHAGE; NEISSERIA MENINGITIDIS; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

ACUTE-PHASE PROTEINS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; ANTIBODIES, BLOCKING; ANTIGENS, CD14; BACTERIAL CAPSULES; CARRIER PROTEINS; CELL LINE; HUMANS; INFLAMMATION; INTERLEUKIN-8; LYMPHOCYTE ANTIGEN 96; MACROPHAGE ACTIVATION; MACROPHAGES; MEMBRANE GLYCOPROTEINS; MICE; NEISSERIA MENINGITIDIS; RECEPTORS, INTERLEUKIN-1; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4;

MURINAE; NEISSERIA MENINGITIDIS;

EID: 79952206304     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0610369     Document Type: Article

References (62)

1. Zughaier, S. M., Tzeng, Y. L., Zimmer, S. M., Datta, A., Carlson, R. W., Stephens, D. S. (2004) Neisseria meningitidis lipooligosaccharide structure-dependent activation of the macrophage CD14/Toll-like receptor 4 pathway. Infect. Immun. 72, 371-380. (Pubitemid 38018198)
2. Zimmer, S. M., Zughaier, S. M., Tzeng, Y. L., Stephens, D. S. (2007) Human MD-2 discrimination of meningococcal lipid A structures and activation of TLR4. Glycobiology 17, 847-856. (Pubitemid 47243541)
3. Zughaier, S., Agrawal, S., Stephens, D. S., Pulendran, B. (2006) Hexaacylation and KDO(2)-glycosylation determine the specific immunostimulatory activity of Neisseria meningitidis lipid A for human monocyte derived dendritic cells. Vaccine 24, 1291-1297. (Pubitemid 43222036)
4. Stephens, D. S., Greenwood, B., Brandtzaeg, P. (2007) Epidemic meningitis, meningococcemia, and Neisseria meningitidis. Lancet 369, 2196-2210. (Pubitemid 46977462)
5. Tzeng, Y. L., Datta, A. K., Strole, C. A., Lobritz, M. A., Carlson, R. W., Stephens, D. S. (2005) Translocation and surface expression of lipidated serogroup B capsular polysaccharide in Neisseria meningitidis. Infect. Immun. 73, 1491-1505.
6. Powell, J. L., Wright, A. C., Wasserman, S. S., Hone, D. M., Morris Jr., J. G. (1997) Release of tumor necrosis factor α in response to Vibrio vulnificus capsular polysaccharide in in vivo and in vitro models. Infect. Immun. 65, 3713-3718.
7. Bush, C. A., Patel, P., Gunawardena, S., Powell, J., Joseph, A., Johnson, J. A., Morris, J. G. (1997) Classification of Vibrio vulnificus strains by the carbohydrate composition of their capsular polysaccharides. Anal. Biochem. 250, 186-195. (Pubitemid 27319096)
8. Monari, C., Pericolini, E., Bistoni, G., Casadevall, A., Kozel, T. R., Vecchiarelli, A. (2005) Cryptococcus neoformans capsular glucuronoxylomannan induces expression of fas ligand in macrophages. J. Immunol. 174, 3461-3468. (Pubitemid 40354053)
9. Shoham, S., Huang, C., Chen, J. M., Golenbock, D. T., Levitz, S. M. (2001) Toll-like receptor 4 mediates intracellular signaling without TNF-α release in response to Cryptococcus neoformans polysaccharide capsule. J. Immunol. 166, 4620-4626. (Pubitemid 32233748)
10. Harn, D. A., McDonald, J., Atochina, O., Da'dara, A. A. (2009) Modulation of host immune responses by helminth glycans. Immunol. Rev. 230, 247-257.
11. Thomas, P. G., Carter, M. R., Atochina, O., Da'Dara, A. A., Piskorska, D., McGuire, E., Harn, D. A. (2003) Maturation of dendritic cell 2 phenotype by a helminth glycan uses a Toll-like receptor 4-dependent mechanism. J. Immunol. 171, 5837-5841. (Pubitemid 37467200)
12. Tzianabos, A., Wang, J. Y., Kasper, D. L. (2003) Biological chemistry of immunomodulation by zwitterionic polysaccharides. Carbohydr. Res. 338, 2531-2538. (Pubitemid 37509952)
13. Wang, Q., McLoughlin, R. M., Cobb, B. A., Charrel-Dennis, M., Zaleski, K. J., Golenbock, D., Tzianabos, A. O., Kasper, D. L. (2006) A bacterial carbohydrate links innate and adaptive responses through Toll-like receptor 2. J. Exp. Med. 203, 2853-2863. (Pubitemid 46026163)
14. Graveline, R., Segura, M., Radzioch, D., Gottschalk, M. (2007) TLR2-dependent recognition of Streptococcus suis is modulated by the presence of capsular polysaccharide which modifies macrophage responsiveness. Int. Immunol. 19, 375-389. (Pubitemid 46523386)
15. Iwata, T., Mitani, A., Ishihara, Y., Tanaka, S., Yamamoto, G., Kikuchi, T., Naganawa, T., Matsumura, Y., Suga, T., Koide, M., Sobue, T., Suzuki, T., Noguchi, T. (2005) Actinobacillus actinomycetemcomitans Y4 capsular polysaccharide induces IL-1β mRNA expression through the JNK pathway in differentiated THP-1 cells. Clin. Exp. Immunol. 141, 261-269. (Pubitemid 41003350)
16. Hsu, H. Y., Jeyashoke, N., Yeh, C. H., Song, Y. J., Hua, K. F., Chao, L. K. (2010) Immunostimulatory bioactivity of algal polysaccharides from Chlorella pyrenoidosa activates macrophages via Toll-like receptor 4. J. Agric. Food Chem. 58, 927-936.
17. Li, X., Xu, W., Chen, J. (2010) Polysaccharide purified from Polyporus umbellatus (Per) Fr induces the activation and maturation of murine bone-derived dendritic cells via Toll-like receptor 4. Cell. Immunol. 265, 50-56.
18. Li, X., Xu, W. (2010) TLR4-mediated activation of macrophages by the polysaccharide fraction from Polyporus umbellatus(pers.) Fries. J. Ethnopharmacol., Epub ahead of print.
19. Steeghs, L., den Hartog, R., den Boer, A., Zomer, B., Roholl, P., van der Ley, P. (1998) Meningitis bacterium is viable without endotoxin. Nature 392, 449-450. (Pubitemid 28168969)
20. Plant, L., Wan, H., Jonsson, A. B. (2007) Non-lipooligosaccharide- mediated signaling via Toll-like receptor 4 causes fatal meningococcal sepsis in a mouse model. Cell. Microbiol. 9, 657-669. (Pubitemid 46231972)
21. Plant, L., Wan, H., Jonsson, A. B. (2006) MyD88-dependent signaling affects the development of meningococcal sepsis by nonlipooligosaccharide ligands. Infect. Immun. 74, 3538-3546. (Pubitemid 43794545)
22. Zarantonelli, M. L., Huerre, M., Taha, M. K., Alonso, J. M. (2006) Differential role of lipooligosaccharide of Neisseria meningitidis in virulence and inflammatory response during respiratory infection in mice. Infect. Immun. 74, 5506-5512. (Pubitemid 44484533)
23. Hellerud, B. C., Nielsen, E. W., Thorgersen, E. B., Lindstad, J. K., Pharo, A., Tonnessen, T. I., Castellheim, A., Mollnes, T. E., Brandtzaeg, P. (2010) Dissecting the effects of lipopolysaccharides from nonlipopolysaccharide molecules in experimental porcine meningococcal sepsis. Crit. Care Med. 38, 1467-1474.
24. Van der Ley, P., Steeghs, L. (2003) Lessons from an LPS-deficient Neisseria meningitidis mutant. J. Endotoxin Res. 9, 124-128.
25. Czeslick, E., Struppert, A., Simm, A., Sablotzki, A. (2006) E5564 (Eritoran) inhibits lipopolysaccharide-induced cytokine production in human blood monocytes. Inflamm. Res. 55, 511-515. (Pubitemid 44826742)
26. Rossignol, D. P., Wasan, K. M., Choo, E., Yau, E., Wong, N., Rose, J., Moran, J., Lynn, M. (2004) Safety, pharmacokinetics, pharmacodynamics, and plasma lipoprotein distribution of Eritoran (E5564) during continuous intravenous infusion into healthy volunteers. Antimicrob. Agents Chemother. 48, 3233-3240. (Pubitemid 39129312)
27. Rossignol, D. P., Lynn, M. (2002) Antagonism of in vivo and ex vivo response to endotoxin by E5564, a synthetic lipid A analogue. J. Endotoxin Res. 8, 483-488. (Pubitemid 36104606)
28. Gudlavalleti, S. K., Datta, A. K., Tzeng, Y. L., Noble, C., Carlson, R. W., Stephens, D. S. (2004) The Neisseria meningitidis serogroup A capsular polysaccharide O-3 and O-4 acetyltransferase. J. Biol. Chem. 279, 42765-42773.
29. Zughaier, S. M., Zimmer, S. M., Datta, A., Carlson, R. W., Stephens, D. S. (2005) Differential induction of the Toll-like receptor 4-MyD88-dependent and -independent signaling pathways by endotoxins. Infect. Immun. 73, 2940-2950. (Pubitemid 40575735)
30. Kim, H. M., Park, B. S., Kim, J. I., Kim, S. E., Lee, J., Oh, S. C., Enkhbayar, P., Matsushima, N., Lee, H., Yoo, O. J., Lee, J. O. (2007) Crystal structure of the TLR4-MD-2 complex with bound endotoxin antagonist Eritoran. Cell 130, 906-917. (Pubitemid 47332573)
31. Kumar, H., Kawai, T., Akira, S. (2009) Toll-like receptors and innate immunity. Biochem. Biophys. Res. Commun. 388, 621-625.
32. Sacre, S. M., Lundberg, A. M., Andreakos, E., Taylor, C., Feldmann, M., Foxwell, B. M. (2007) Selective use of TRAM in lipopolysaccharide (LPS) and lipoteichoic acid (LTA) induced NF-κB activation and cytokine production in primary human cells: TRAM is an adaptor for LPS and LTA signaling. J. Immunol. 178, 2148-2154. (Pubitemid 46233412)
33. Forsberg, L. S., Carlson, R. W. (1998) The structures of the lipopolysaccharides from Rhizobium etli strains CE358 and CE359. The complete structure of the core region of R. etli lipopolysaccharides. J. Biol. Chem. 273, 2747-2757.
34. Brandtzaeg, P., Ovsteboo, R., Kierulf, P. (1992) Compartmentalization of lipopolysaccharide production correlates with clinical presentation in meningococcal disease. J. Infect. Dis. 166, 650-652.
35. Bonnah, R. A., Hoelter, J., Steeghs, L., Enns, C. A., So, M., Muckenthaler, M. U. (2005) Lipooligosaccharide-independent alteration of cellular homeostasis in Neisseria meningitidis-infected epithelial cells. Cell. Microbiol. 7, 869-885. (Pubitemid 40740381)
36. Pridmore, A. C., Wyllie, D. H., Abdillahi, F., Steeghs, L., van der Ley, P., Dower, S. K., Read, R. C. (2001) A lipopolysaccharide-deficient mutant of Neisseria meningitidis elicits attenuated cytokine release by human macrophages and signals via Toll-like receptor (TLR) 2 but not via TLR4/MD2. J. Infect. Dis. 183, 89-96. (Pubitemid 32043045)
37. Sprong, T., Stikkelbroeck, N., van der Ley, P., Steeghs, L., van Alphen, L., Klein, N., Netea, M. G., van der Meer, J. W., van Deuren, M. (2001) Contributions of Neisseria meningitidis LPS and non-LPS to proinflammatory cytokine response. J. Leukoc. Biol. 70, 283-288. (Pubitemid 32751520)
38. Ovstebø, R., Olstad, O. K., Brusletto, B., Moller, A. S., Aase, A., Haug, K. B., Brandtzaeg, P., Kierulf, P. (2008) Identification of genes particularly sensitive to lipopolysaccharide (LPS) in human monocytes induced by wild-type versus LPS-deficient Neisseria meningitidis strains. Infect. Immun. 76, 2685-2695.
39. Steeghs, L., de Cock, H., Evers, E., Zomer, B., Tommassen, J., van der Ley, P. (2001) Outer membrane composition of a lipopolysaccharide-deficient Neisseria meningitidis mutant. EMBO J. 20, 6937-6945. (Pubitemid 34062286)
40. Bos, M. P., Tommassen, J. (2005) Viability of a capsule- and lipopolysaccharide-deficient mutant of Neisseria meningitidis. Infect. Immun. 73, 6194-6197. (Pubitemid 41193066)
41. Singleton, T. E., Massari, P., Wetzler, L. M. (2005) Neisserial porin-induced dendritic cell activation is MyD88 and TLR2 dependent. J. Immunol. 174, 3545-3550. (Pubitemid 40354063)
42. Takeuchi, A., Kamiryou, Y., Yamada, H., Eto, M., Shibata, K., Haruna, K., Naito, S., Yoshikai, Y. (2009) Oral administration of xanthan gum enhances antitumor activity through Toll-like receptor 4. Int. Immunopharmacol. 9, 1562-1567.
43. Li, W., Liu, M., Lai, S., Xu, C., Lu, F., Xiao, X., Bao, Y. (2010) Immunomodulatory effects of polysaccharopeptide (PSP) in human PBMC through regulation of TRAF6/TLR immunosignal-transduction pathways. Immunopharmacol. Immunotoxicol. 32, 576-584.
44. Mogensen, T. H., Paludan, S. R., Kilian, M., Ostergaard, L. (2006) Live Streptococcus pneumoniae, Haemophilus influenzae, and Neisseria meningitidis activate the inflammatory response through Toll-like receptors 2, 4, and 9 in species-specific patterns. J. Leukoc. Biol. 80, 267-277. (Pubitemid 44835500)
45. Cohen, N., Stolarsky-Bennun, M., Amir-Kroll, H., Margalit, R., Nussbaum, G., Cohen-Sfady, M., Pevsner-Fischer, M., Fridkin, M., Bercovier, H., Eisenbach, L., Jung, S., Cohen, I. R. (2008) Pneumococcal capsular polysaccharide is immunogenic when present on the surface of macrophages and dendritic cells: TLR4 signaling induced by a conjugate vaccine or by lipopolysaccharide is conducive. J. Immunol. 180, 2409-2418.
46. Cleary, J. A., Kelly, G. E., Husband, A. J. (1999) The effect of molecular weight and β-1,6-linkages on priming of macrophage function in mice by (1,3)-β-D-glucan. Immunol. Cell Biol. 77, 395-403. (Pubitemid 29476909)
47. Menéndez, T., Carmenate, T., Cruz-Leal, Y., Coizeau, E., Caballero, E., Bello, D., Guirola, M., Alvarez, A., Guillen, G. (2010) Purified capsular polysaccharide of Neisseria meningitidis serogroup A as immune potentiator for antibody production. Curr. Microbiol. 60, 79-84.
48. Zughaier, S., Svoboda, P., Pohl, J., Stephens, D. S., Shafer, W. M. (2010) The host defense peptide LL-37 interacts with Neisseria meningitidis capsular polysaccharides and inhibits inflammatory mediators release. PLoS ONE 5, e13627.
49. Park, B. S., Song, D. H., Kim, H. M., Choi, B. S., Lee, H., Lee, J. O. (2009) The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex. Nature 458, 1191-1195.
50. Zimmer, S. M., Liu, J., Clayton, J. L., Stephens, D. S., Snyder, J. P. (2008) Paclitaxel binding to human and murine MD-2. J. Biol. Chem. 283, 27916-27926.
51. Brodsky, I., Medzhitov, R. (2007) Two modes of ligand recognition by TLRs. Cell 130, 979-981. (Pubitemid 47410282)
52. Ohto, U., Fukase, K., Miyake, K., Satow, Y. (2007) Crystal structures of human MD-2 and its complex with antiendotoxic lipid IVa. Science 316, 1632-1634. (Pubitemid 46982039)
53. Yamada, C., Sano, H., Shimizu, T., Mitsuzawa, H., Nishitani, C., Himi, T., Kuroki, Y. (2006) Surfactant protein A directly interacts with TLR4 and MD-2 and regulates inflammatory cellular response. Importance of supratrimeric oligomerization. J. Biol. Chem. 281, 21771-21780. (Pubitemid 44181881)
54. Nie, X., Nishitani, C., Yamazoe, M., Ariki, S., Takahashi, M., Shimizu, T., Mitsuzawa, H., Sawada, K., Smith, K., Crouch, E., Nagae, H., Takahashi, H., Kuroki, Y. (2008) Pulmonary surfactant protein D binds MD-2 through the carbohydrate recognition domain. Biochemistry 47, 12878-12885.
55. Haagsman, H. P., Hogenkamp, A., van Eijk, M., Veldhuizen, E. J. (2008) Surfactant collectins and innate immunity. Neonatology 93, 288-294. (Pubitemid 351799112)
56. Sorensen, G. L., Husby, S., Holmskov, U. (2007) Surfactant protein A and surfactant protein D variation in pulmonary disease. Immunobiology 212, 381-416. (Pubitemid 46825244)
57. Takahashi, H., Sano, H., Chiba, H., Kuroki, Y. (2006) Pulmonary surfactant proteins A and D: innate immune functions and biomarkers for lung diseases. Curr. Pharm. Des. 12, 589-598.
58. Kishore, U., Greenhough, T. J., Waters, P., Shrive, A. K., Ghai, R., Kamran, M. F., Bernal, A. L., Reid, K. B., Madan, T., Chakraborty, T. (2006) Surfactant proteins SP-A and SP-D: structure, function and receptors. Mol. Immunol. 43, 1293-1315. (Pubitemid 43356370)
59. Kocabas, C., Katsenelson, N., Kanswal, S., Kennedy, M. N., Cui, X., Blake, M. S., Segal, D. M., Akkoyunlu, M. (2007) Neisseria meningitidis type C capsular polysaccharide inhibits lipooligosaccharide-induced cell activation by binding to CD14. Cell. Microbiol. 9, 1297-1310. (Pubitemid 46547145)
60. Bardotti, A., Averani, G., Berti, F., Berti, S., Galli, C., Giannini, S., Fabbri, B., Proietti, D., Ravenscroft, N., Ricci, S. (2005) Size determination of bacterial capsular oligosaccharides used to prepare conjugate vaccines against Neisseria meningitidis groups Y and W135. Vaccine 23, 1887-1899. (Pubitemid 40289059)
61. Gantner, B. N., Simmons, R. M., Canavera, S. J., Akira, S., Underhill, D. M. (2003) Collaborative induction of inflammatory responses by dectin-1 and Toll-like receptor 2. J. Exp. Med. 197, 1107-1117. (Pubitemid 36570066)
62. Stoddard, M. B., Pinto, V., Keiser, P. B., Zollinger, W. (2010) Evaluation of a whole-blood cytokine release assay for use in measuring endotoxin activity of group B Neisseria meningitidis vaccines made from lipid A acylation mutants. Clin. Vaccine Immunol. 17, 98-107.