Toll-like receptor (TLR) 2 mediates inflammatory responses to oligomerized RRGA pneumococcal pilus type 1 protein

Journal of Biological Chemistry

Volumn 288, Issue 4, 2013, Pages 2665-2675

  Basset, Alan ^a   Zhang, Fan ^a   Benes, Cyril ^b   Sayeed, Sabina ^a   Herd, Muriel ^a   Thompson, Claudette ^c   Golenbock, Douglas T ^d   Camilli, Andrew ^e   Malley, Richard ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^d UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^e TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INFLAMMATORY RESPONSE; INTRAPERITONEAL; LIPIDATION; TOLL-LIKE RECEPTORS;

AMINO ACIDS; OLIGOMERS; PROTEINS;

MAMMALS;

INTERLEUKIN 8; PROTEIN RRGA; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR AGONIST; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTEREMIA; BACTERIAL GENE; BACTERIAL VIRULENCE; BACTERIUM PILUS; CELL ACTIVATION; CLADISTICS; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE DELETION; HUMAN; HUMAN CELL; INFLAMMATION; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; MOLECULAR RECOGNITION; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN BINDING; PROTEIN DETERMINATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN POLYMERIZATION; RRGA GENE; RRGB GENE; RRGC GENE; WESTERN BLOTTING; WILD TYPE;

AMINO ACID MOTIFS; ANIMALS; CELL MEMBRANE; FEMALE; FIMBRIAE PROTEINS; FIMBRIAE, BACTERIAL; GENE DELETION; HUMANS; INFLAMMATION; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MUTATION; PROTEIN STRUCTURE, TERTIARY; STREPTOCOCCUS PNEUMONIAE; SURFACE PROPERTIES; TOLL-LIKE RECEPTOR 2; VIRULENCE; VIRULENCE FACTORS;

EID: 84873859442     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.398875     Document Type: Article

References (51)

1. O'Brien, K. L., Wolfson, L. J., Watt, J. P., Henkle, E., Deloria-Knoll, M., McCall, N., Lee, E., Mulholland, K., Levine, O. S., and Cherian, T. (2009) Burden of disease caused by Streptococcus pneumoniae in children younger than 5 years. Global estimates. Lancet 374, 893-902
2. Black, S., Shinefield, H., Fireman, B., Lewis, E., Ray, P., Hansen, J. R., Elvin, L., Ensor, K. M., Hackell, J., Siber, G., Malinoski, F., Madore, D., Chang, I., Kohberger, R., Watson, W., Austrian, R., and Edwards, K. (2000) Efficacy, safety, and immunogenicity of heptavalent pneumococcal conjugate vaccine in children. Northern California Kaiser Permanente Vaccine Study Center Group. Pediatr. Infect. Dis. J. 19, 187-195
3. Black, S. B., Shinefield, H. R., Hansen, J., Elvin, L., Laufer, D., and Malinoski, F. (2001) Postlicensure evaluation of the effectiveness of seven valent pneumococcal conjugate vaccines. Pediatr. Infect. Dis. J. 20, 1105-1107
4. Hanage, W. P. (2008) Serotype-specific problems associated with pneumococcal conjugate vaccination. Future Microbiol. 3, 23-30
5. Lipsitch, M. (2001) Interpreting results from trials of pneumococcal conjugate vaccines. A statistical test for detecting vaccine-induced increases in carriage of nonvaccine serotypes. Am. J. Epidemiol. 154, 85-92
6. Weinberger, D. M., Malley, R., and Lipsitch, M. (2011) Serotype replacement in disease after pneumococcal vaccination. Lancet 378, 1962-1973
7. Balachandran, P., Brooks-Walter, A., Virolainen-Julkunen, A., Hollingshead, S. K., and Briles, D. E. (2002) Role of pneumococcal surface protein C in nasopharyngeal carriage and pneumonia and its ability to elicit protection against carriage of Streptococcus pneumoniae. Infect. Immun. 70, 2526-2534
8. Briles, D. E., Hollingshead, S., Brooks-Walter, A., Nabors, G. S., Ferguson, L., Schilling, M., Gravenstein, S., Braun, P., King, J., and Swift, A. (2000) The potential to use PspA and other pneumococcal proteins to elicit protection against pneumococcal infection. Vaccine 18, 1707-1711
9. Ogunniyi, A. D., Folland, R. L., Briles, D. E., Hollingshead, S. K., and Paton, J. C. (2000) Immunization of mice with combinations of pneumococcal virulence proteins elicits enhanced protection against challenge with Streptococcus pneumoniae. Infect. Immun. 68, 3028-3033
10. Lu, Y. J., Leite, L., Gonçalves, V. M., Dias Wde, O., Liberman, C., Fratelli, F., Alderson, M., Tate, A., Maisonneuve, J. F., Robertson, G., Graca, R., Sayeed, S., Thompson, C. M., Anderson, P., and Malley, R. (2010) GMPgrade pneumococcal whole-cell vaccine injected subcutaneously protects mice from nasopharyngeal colonization and fatal aspiration-sepsis. Vaccine 28, 7468-7475
11. Moffitt, K. L., Gierahn, T. M., Lu, Y. J., Gouveia, P., Alderson, M., Flechtner, J. B., Higgins, D. E., and Malley, R. (2011) T(H)17-based vaccine design for prevention of Streptococcus pneumoniae colonization. Cell Host Microbe 9, 158-165
12. Moffitt, K. L., and Malley, R. (2011) Next generation pneumococcal vaccines. Curr. Opin. Immunol. 23, 407-413
13. Gianfaldoni, C., Censini, S., Hilleringmann, M., Moschioni, M., Facciotti, C., Pansegrau, W., Masignani, V., Covacci, A., Rappuoli, R., Barocchi, M. A., and Ruggiero, P. (2007) Streptococcus pneumoniae pilus subunits protect mice against lethal challenge. Infect. Immun. 75, 1059-1062
14. LeMieux, J., Hava, D. L., Basset, A., and Camilli, A. (2006) RrgA and RrgB are components of a multisubunit pilus encoded by the Streptococcus pneumoniae rlrA pathogenicity islet. Infect. Immun. 74, 2453-2456
15. Moschioni, M., De Angelis, G., Harfouche, C., Bizzarri, E., Filippini, S., Mori, E., Mancuso, G., Doro, F., Barocchi, M. A., Ruggiero, P., and Masignani, V. (2012) Immunization with the RrgB321 fusion protein protects mice against both high and low pilus-expressing Streptococcus pneumoniae populations. Vaccine 30, 1349-1356
16. Harfouche, C., Filippini, S., Gianfaldoni, C., Ruggiero, P., Moschioni, M., Maccari, S., Pancotto, L., Arcidiacono, L., Galletti, B., Censini, S., Mori, E., Giuliani, M., Facciotti, C., Cartocci, E., Savino, S., Doro, F., Pallaoro, M., Nocadello, S., Mancuso, G., Haston, M., Goldblatt, D., Barocchi, M. A., Pizza, M., Rappuoli, R., and Masignani, V. (2012) RrgB321, a fusion protein of the three variants of the pneumococcal pilus backbone RrgB, is protective in vivo and elicits opsonic antibodies. Infect. Immun. 80, 451-460
17. Nelson, A. L., Ries, J., Bagnoli, F., Dahlberg, S., Fälker, S., Rounioja, S., Tschöp, J., Morfeldt, E., Ferlenghi, I., Hilleringmann, M., Holden, D. W., Rappuoli, R., Normark, S., Barocchi, M. A., and Henriques-Normark, B. (2007) RrgA is a pilus-associated adhesin in Streptococcus pneumoniae. Mol. Microbiol. 66, 329-340
18. Bagnoli, F., Moschioni, M., Donati, C., Dimitrovska, V., Ferlenghi, I., Facciotti, C., Muzzi, A., Giusti, F., Emolo, C., Sinisi, A., Hilleringmann, M., Pansegrau, W., Censini, S., Rappuoli, R., Covacci, A., Masignani, V., and Barocchi, M. A. (2008)Asecond pilus type in Streptococcus pneumoniae is prevalent in emerging serotypes and mediates adhesion to host cells. J. Bacteriol. 190, 5480-5492
19. Barocchi, M. A., Ries, J., Zogaj, X., Hemsley, C., Albiger, B., Kanth, A., Dahlberg, S., Fernebro, J., Moschioni, M., Masignani, V., Hultenby, K., Taddei, A. R., Beiter, K., Wartha, F., von Euler, A., Covacci, A., Holden, D. W., Normark, S., Rappuoli, R., and Henriques-Normark, B. (2006) A pneumococcal pilus influences virulence and host inflammatory responses. Proc. Natl. Acad. Sci. U.S.A. 103, 2857-2862
20. Muñoz-Elías, E. J., Marcano, J., and Camilli, A. (2008) Isolation of Streptococcus pneumoniae biofilm mutants and their characterization during nasopharyngeal colonization. Infect. Immun. 76, 5049-5061
21. Basset, A., Trzcinski, K., Hermos, C., O'Brien, K. L., Reid, R., Santosham, M., McAdam, A. J., Lipsitch, M., and Malley, R. (2007) Association of the pneumococcal pilus with certain capsular serotypes but not with in-creased virulence. J. Clin. Microbiol. 45, 1684-1689
22. Regev-Yochay, G., Hanage, W. P., Trzcinski, K., Rifas-Shiman, S. L., Lee, G., Bessolo, A., Huang, S. S., Pelton, S. I., McAdam, A. J., Finkelstein, J. A., Lipsitch, M., and Malley, R. (2010) Re-emergence of the type 1 pilus among Streptococcus pneumoniae isolates in Massachusetts, USA. Vaccine 28, 4842-4846
23. Regev-Yochay, G., Lipsitch, M., Basset, A., Rubinstein, E., Dagan, R., Raz, M., and Malley, R. (2009) The pneumococcal pilus predicts the absence of Staphylococcus aureus co-colonization in pneumococcal carriers. Clin. Infect. Dis. 48, 760-763
24. Aguiar, S. I., Serrano, I., Pinto, F. R., Melo-Cristino, J., and Ramirez, M. (2008) The presence of the pilus locus is a clonal property among pneumococcal invasive isolates. BMC Microbiol. 8, 41
25. Basset, A., Turner, K. H., Boush, E., Sayeed, S., Dove, S. L., and Malley, R. (2011) Expression of the type 1 pneumococcal pilus is bistable and negatively regulated by the structural component RrgA. Infect. Immun. 79, 2974-2983
26. De Angelis, G., Moschioni, M., Muzzi, A., Pezzicoli, A., Censini, S., Delany, I., Lo Sapio, M., Sinisi, A., Donati, C., Masignani, V., and Barocchi, M. A. (2011) The Streptococcus pneumoniae pilus-1 displays a biphasic expression pattern. PLoS ONE 6, e21269
27. Basset, A., Turner, K. H., Boush, E., Sayeed, S., Dove, S. L., and Malley, R. (2012) An epigenetic switch mediates bistable expression of the type 1 pilus genes in Streptococcus pneumoniae. J. Bacteriol. 194, 1088-1091
28. Ii, M., Matsunaga, N., Hazeki, K., Nakamura, K., Takashima, K., Seya, T., Hazeki, O., Kitazaki, T., and Iizawa, Y. (2006) A novel cyclohexene derivative, ethyl (6R)-6-[N-(2-chloro-4-fluorophenyl)sulfamoyl]cyclohex-1- ene-1-carboxylate (TAK-242), selectively inhibits toll-like receptor 4-mediated cytokine production through suppression of intracellular signaling. Mol. Pharmacol. 69, 1288-1295
29. Sung, C. K., Li, H., Claverys, J. P., and Morrison, D. A. (2001) An rpsL cassette, Janus, for gene replacement through negative selection in Streptococcus pneumoniae. Appl. Environ. Microbiol. 67, 5190-5196
30. Kurt-Jones, E. A., Popova, L., Kwinn, L., Haynes, L. M., Jones, L. P., Tripp, R. A., Walsh, E. E., Freeman, M. W., Golenbock, D. T., Anderson, L. J., and Finberg, R. W. (2000) Pattern recognition receptors TLR4 and CD14 mediate response to respiratory syncytial virus. Nat. Immunol. 1, 398-401
31. Halle, A., Hornung, V., Petzold, G. C., Stewart, C. R., Monks, B. G., Reinheckel, T., Fitzgerald, K. A., Latz, E., Moore, K. J., and Golenbock, D. T. (2008) The NALP3 inflammasome is involved in the innate immune response to amyloid-β. Nat. Immunol. 9, 857-865
32. Han, S. H., Kim, J. H., Martin, M., Michalek, S. M., and Nahm, M. H. (2003) Pneumococcal lipoteichoic acid (LTA) is not as potent as staphylococcal LTA in stimulating Toll-like receptor 2. Infect. Immun. 71, 5541-5548
33. Malley, R., Henneke, P., Morse, S. C., Cieslewicz, M. J., Lipsitch, M., Thompson, C. M., Kurt-Jones, E., Paton, J. C., Wessels, M. R., and Golenbock, D. T. (2003) Recognition of pneumolysin by Toll-like receptor 4 confers resistance to pneumococcal infection. Proc. Natl. Acad. Sci. U.S.A. 100, 1966-1971
34. Albiger, B., Dahlberg, S., Sandgren, A., Wartha, F., Beiter, K., Katsuragi, H., Akira, S., Normark, S., and Henriques-Normark, B. (2007) Toll-like receptor 9 acts at an early stage in host defence against pneumococcal infection. Cell Microbiol. 9, 633-644
35. Yoshimura, A., Lien, E., Ingalls, R. R., Tuomanen, E., Dziarski, R., and Golenbock, D. (1999) Cutting edge. Recognition of Gram-positive bacterial cell wall components by the innate immune system occurs via Toll-like receptor 2. J. Immunol. 163, 1-5
36. Izoré, T., Contreras-Martel, C., El Mortaji, L., Manzano, C., Terrasse, R., Vernet, T., Di Guilmi, A. M., and Dessen, A. (2010) Structural basis of host cell recognition by the pilus adhesin from Streptococcus pneumoniae. Structure 18, 106-115
37. Berry, A. M., Alexander, J. E., Mitchell, T. J., Andrew, P. W., Hansman, D., and Paton, J. C. (1995) Effect of defined point mutations in the pneumolysin gene on the virulence of Streptococcus pneumoniae. Infect. Immun. 63, 1969-1974
38. Gilbert, R. J., Rossjohn, J., Parker, M. W., Tweten, R. K., Morgan, P. J., Mitchell, T. J., Errington, N., Rowe, A. J., Andrew, P. W., and Byron, O. (1998) Self-interaction of pneumolysin, the pore-forming protein toxin of Streptococcus pneumoniae. J. Mol. Biol. 284, 1223-1237
39. Moschioni, M., Donati, C., Muzzi, A., Masignani, V., Censini, S., Hanage, W. P., Bishop, C. J., Reis, J. N., Normark, S., Henriques-Normark, B., Covacci, A., Rappuoli, R., and Barocchi, M. A. (2008) Streptococcus pneumoniae contains 3 rlrA pilus variants that are clonally related. J. Infect. Dis. 197, 888-896
40. Hoffmann, J. A., Kafatos, F. C., Janeway, C. A., and Ezekowitz, R. A. (1999) Phylogenetic perspectives in innate immunity. Science 284, 1313-1318
41. Drennan, M. B., Nicolle, D., Quesniaux, V. J., Jacobs, M., Allie, N., Mpagi, J., Frémond, C., Wagner, H., Kirschning, C., and Ryffel, B. (2004) Toll-like receptor 2-deficient mice succumb to Mycobacterium tuberculosis infection. Am. J. Pathol. 164, 49-57
42. Ehl, S., Bischoff, R., Ostler, T., Vallbracht, S., Schulte-Mönting, J., Poltorak, A., and Freudenberg, M. (2004) The role of Toll-like receptor 4 versus interleukin-12 in immunity to respiratory syncytial virus. Eur. J. Immunol. 34, 1146-1153
43. Torres, D., Barrier, M., Bihl, F., Quesniaux, V. J., Maillet, I., Akira, S., Ryffel, B., and Erard, F. (2004) Toll-like receptor 2 is required for optimal control of Listeria monocytogenes infection. Infect. Immun. 72, 2131-2139
44. Tabeta, K., Georgel, P., Janssen, E., Du, X., Hoebe, K., Crozat, K., Mudd, S., Shamel, L., Sovath, S., Goode, J., Alexopoulou, L., Flavell, R. A., and Beutler, B. (2004) Toll-like receptors 9 and 3 as essential components of innate immune defense against mouse cytomegalovirus infection. Proc. Natl. Acad. Sci. U.S.A. 101, 3516-3521
45. Mancuso, G., Midiri, A., Beninati, C., Biondo, C., Galbo, R., Akira, S., Henneke, P., Golenbock, D., and Teti, G. (2004) Dual role of TLR2 and myeloid differentiation factor 88 in a mouse model of invasive group B streptococcal disease. J. Immunol. 172, 6324-6329
46. Takeuchi, O., Hoshino, K., and Akira, S. (2000) Cutting edge. TLR2-deficient and MyD88-deficient mice are highly susceptible to Staphylococcus aureus infection. J. Immunol. 165, 5392-5396
47. Kirschning, C. J., and Schumann, R. R. (2002) TLR2. Cellular sensor for microbial and endogenous molecular patterns. Curr. Top. Microbiol. Immunol. 270, 121-144
48. Srivastava, A., Henneke, P., Visintin, A., Morse, S. C., Martin, V., Watkins, C., Paton, J. C., Wessels, M. R., Golenbock, D. T., and Malley, R. (2005) The apoptotic response to pneumolysin is Toll-like receptor 4-dependent and protects against pneumococcal disease. Infect. Immun. 73, 6479-6487
49. Henneke, P., Takeuchi, O., Malley, R., Lien, E., Ingalls, R. R., Freeman, M. W., Mayadas, T., Nizet, V., Akira, S., Kasper, D. L., and Golenbock, D. T. (2002) Cellular activation, phagocytosis, and bactericidal activity against group B streptococcus involve parallel myeloid differentiation factor 88-dependent and independent signaling pathways. J. Immunol. 169, 3970-3977
50. Hilleringmann, M., Giusti, F., Baudner, B. C., Masignani, V., Covacci, A., Rappuoli, R., Barocchi, M. A., and Ferlenghi, I. (2008) Pneumococcal pili are composed of protofilaments exposing adhesive clusters of RrgA. PLoS Pathog. 4, e1000026
51. Goodridge, H. S., Reyes, C. N., Becker, C. A., Katsumoto, T. R., Ma, J., Wolf, A. J., Bose, N., Chan, A. S., Magee, A. S., Danielson, M. E., Weiss, A., Vasilakos, J. P., and Underhill, D. M. (2011) Activation of the innate immune receptor Dectin-1 upon formation of a "phagocytic synapse". Nature 472, 471-475