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Biochemistry (Moscow)

, Volume 75, Issue 9, pp 1098–1114 | Cite as

Toll-like receptors and their adapter molecules

  • A. I. TukhvatulinEmail author
  • D. Yu. Logunov
  • D. N. Shcherbinin
  • M. M. Shmarov
  • B. S. Naroditsky
  • A. V. Gudkov
  • A. L. Gintsburg
Review

Abstract

Toll-like receptors (TLR) are among key receptors of the innate mammalian immune system. Receptors of this family are able to recognize specific highly conserved molecular regions (patterns) in pathogen structures, thus initiating reactions of both innate and acquired immune response finally resulting in the elimination of the pathogen. In this case every individual TLR type is able to bind a broad spectrum of molecules of microbial origin characterized by different chemical properties and structures. Recent data demonstrate the existence of a multistep mechanism of the TLR recognition of the pathogen in which, in addition to receptors proper, the involvement of different adapter molecules is necessary. However, functions of separate adapter molecules as well as the principles of formation of a multicomponent system of ligand-specific recognition are still not quite understandable. We describe all identified as well as possible (candidate) adapter TLR molecules by giving their brief characteristics, and we also propose generalized possible variants of the TLR ligand-specific recognition with involvement of adapter molecules.

Key words

Toll-like receptors adapter molecules ligand-receptor recognition 

Abbreviations

AP-1

activator protein 1

CCR6

chemokine receptor 6

DAMPs

damage-associated molecular patterns

dsRNA

double-stranded RNA

HDGF

hepatoma-derived growth factor

HMGB1

high mobility group protein 1

IFNα

interferon α

IRF

interferon regulatory transcription factor 1

LBP

LPS-binding protein

LRR

leucine rich repeats

LTA

lipoteichoic acid

MBP

mannose-binding protein

MyD88

myeloid differentiation primary response gene (88)

NALP

(NACHT-, LRR-, and PYD-containing proteins)

NF-κB

nuclear factor kappa-light-chain-enhancer of activated B cells

NK cells

natural killer cells

PAMPs

pathogen-associated molecular patterns

PGRP

peptidoglycan-recognizing protein

PRRs

pattern-recognizing receptors

RAGE

renal cell carcinoma antigen

RP105

radioprotective protein with molecular mass 105 kDa

SP-A

surfactant-associated protein A

SP-D

surfactant-associated protein D

TIR

Toll/interleukin-1 receptor homology domain

TLRs

Toll-like receptors

TNFα

tumor necrosis factor α

TNP

Tamm-Horsfall glycoprotein

TRAM

TRIF-related adaptor molecule

TRIF

TIR-domain-containing adapter-inducing interferon-β

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References

  1. 1.
    Medzhitov, R. (2001) Nat. Rev. Immunol., 1, 135–145.PubMedGoogle Scholar
  2. 2.
    Uematsu, S., and Akira, S. (2008) Handb. Exp. Pharmacol., 183, 1–20.PubMedGoogle Scholar
  3. 3.
    Bianchi, M. E. (2007) J. Leukoc. Biol., 81, 1–5.PubMedGoogle Scholar
  4. 4.
    Schroder, N. W., Opitz, B., Lamping, N., Michelsen, K. S., Zahringer, U., Gobel, U. B., and Schumann, R. R. (2000) J. Immunol., 165, 2683–2693.PubMedGoogle Scholar
  5. 5.
    Gazzinelli, R. T., and Denkers, E. Y. (2006) Nat. Rev. Immunol., 6, 895–906.PubMedGoogle Scholar
  6. 6.
    Bafica, A., Costa Santiago, H., Goldzmind, R., Ropert, C., Gazzinelli, R. T., and Sher, T. (2006) J. Immunol., 177, 3515–3519.PubMedGoogle Scholar
  7. 7.
    Van der Kleij, D., Latz, E., Brouwers, J. F. H. M., Kruize, Y. C. M., Schmitz, M., Kurt-Jones, E., Espevik, T., de Jong, E. C., Kapsenberg, M. L., Golenbock, D. T., Tielens, A. G. M., and Yazdanbakhsh, M. (2007) J. Biol. Chem., 277, 48122–48129.Google Scholar
  8. 8.
    Schroder, N. W., Morath, S., Alexander, C., Hamann, L., Hartung, T., Zahringer, U., Gobel, U. B., Weber, J. R., and Schumann, R. R. (2003) J. Biol. Chem., 278, 15587–15594.PubMedGoogle Scholar
  9. 9.
    Wang, T., Lafuse, W. P., and Zwilling, B. S. (2000) J. Immunol., 165, 6308–6313.PubMedGoogle Scholar
  10. 10.
    Means, T. K., Jones, B. W., Schromm, A. B., Shurtleff, B. A., Smith, J. A., Keane, J., Golenbock, D. T., Vogel, S. N., and Fenton, M. J. (2001) J. Immunol., 166, 4074–4082.PubMedGoogle Scholar
  11. 11.
    Quesniaux, V. J., Nicolle, D. M., Torres, D., Kremer, L., Guerardel, Y., Nigou, J., Puzo, G., Erard, F., and Ryffel, B. (2004) J. Immunol., 172, 4425–4434.PubMedGoogle Scholar
  12. 12.
    Becker, I., Salaiza, N., Aquirre, M., Delgado, J., Carillo-Carrasco, N., Kobeh, L. G., Ruiz, A., Cervantes, R., Torres, A. P., Cabrera, N., Gonzales, A., and Isibasi, A. (2003) Mol. Biochem. Parasitol., 130, 65–74.PubMedGoogle Scholar
  13. 13.
    Ouaissi, A., Guilvard, E., Delneste, Y., Caron, G., Magistrelli, G., Herbault, N., Thieblemont, N., and Jeannin, P. (2002) J. Immunol., 168, 6366–6374.PubMedGoogle Scholar
  14. 14.
    Massari, P., Henneke, P., Ho, Y., Latz, E., Golenbock, D. T., and Wetzler, L. M. (2002) J. Immunol., 168, 1533–1537.PubMedGoogle Scholar
  15. 15.
    Galdiero, M., Galdiero, M., Finamore, E., Rossano, F., Gambuzza, M., Catania, R., Teti, G., Midiri, A., and Mancuso, G. (2004) Infect. Immun., 72, 1204–1209.PubMedGoogle Scholar
  16. 16.
    Hajjar, A. M., O’Mahony, D. S., Ozinsky, A., Underhill, D. M., Aderem, A., Klebanoff, S. J., and Wilson, C. B. (2001) J. Immunol., 166, 15–19.PubMedGoogle Scholar
  17. 17.
    Sing, A., Rost, D., Tvardovskaia, N., Roggenkamp, A., Wiedemann, A., Kirschning, C. J., Aepfelbacher, M., and Heesemann, J. (2002) J. Exp. Med., 196, 1017–1024.PubMedGoogle Scholar
  18. 18.
    Soulas, C., Baussant, T., Aubry, J. P., Delneste, Y., Barillat, N., Caron, G., Renno, T., Bonnefoy, J. Y., and Jeannin, P. (2000) J. Immunol., 165, 2335–2340.PubMedGoogle Scholar
  19. 19.
    Ito, Y., Kawamura, I., Kohda, C., Tsuchiya, K., Nomura, T., and Mitsuyama, M. (2005) Int. Immunol., 17, 1597–1606.PubMedGoogle Scholar
  20. 20.
    Werts, C., Tapping, R. I., Mathison, J. C., Chuang, T.-H., Kravchenko, V. V., Saint Girons, I., Haake, D. A., Godowski, P. J., Hayashi, F., Ozinsky, A., Underhill, D. M., Kirschning, C. J., Wagner, H., Aderem, A., Tobias, P. S., and Ulevitch, R. J. (2001) Nat. Immunol., 2, 346–352.PubMedGoogle Scholar
  21. 21.
    Hirschfeld, M., Weis, J. J., Toshchakov, V., Salkowski, C. A., Cody, M. J., Ward, D. C., Qureshi, N., Michalek, S. M., and Vogel, S. N. (2001) Infect. Immun., 69, 1477–1482.PubMedGoogle Scholar
  22. 22.
    Girard, R., Pedron, T., Uematsu, S., Balloy, V., Chignard, M., Akira, S., and Chaby, R. (2003) J. Cell Sci., 116, 293–302.PubMedGoogle Scholar
  23. 23.
    Kirikae, T., Nitta, T., Kirikae, F., Suda, Y., Kusumoto, S., Qureshi, N., and Nakano, M. (1999) Infect. Immun., 67, 1736–1742.PubMedGoogle Scholar
  24. 24.
    Kirschning, C. J., Wesche, H., Ayres, T. M., and Rothe, M. (1998) J. Exp. Med., 188, 2091–2097.PubMedGoogle Scholar
  25. 25.
    Sugawara, S., Yang, S., Iki, K., Hatakeyama, J., Tamai, R., Takeuchi, O., Akashi, S., Espevik, T., Akira, S., and Takada, H. (2001) Infect. Immun., 69, 4951–4957.PubMedGoogle Scholar
  26. 26.
    Bieback, K., Lien, E., Klagge, I. M., Avota, E., Schneider-Schaulies, J., Duprex, W. P., Wagner, H., Kirschning, C. J., ter Meulen, V., and Schneider-Schaulies, S. (2002) J. Virol., 76, 8729–8736.PubMedGoogle Scholar
  27. 27.
    Dziarski, R., and Gupta, D. (2005) Infect. Immun., 73, 5212–5216.PubMedGoogle Scholar
  28. 28.
    Takeuchi, O., Kaufmann, A., Grote, K., Kawai, T., Hoshino, K., Morr, M., Muhlradt, P. F., and Akira, S. (2000) J. Immunol., 164, 554–557.PubMedGoogle Scholar
  29. 29.
    Lien, E., Sellati, T. J., Yoshimura, A., Flo, T. H., Rawadi, G., Finberg, R. W., Carroll, J. D., Espevik, T., Ingalls, R. R., Radolf, J. D., and Golenbock, D. T. (1999) J. Biol. Chem., 274, 33419–33425.PubMedGoogle Scholar
  30. 30.
    Hashimoto, M., Tawaratsumida, K., Kariya, H., Kiyohara, A., Suda, Y., Kirikae, F., Kirikae, T., and Gotz, F. (2006) J. Immunol., 177, 3162–3169.PubMedGoogle Scholar
  31. 31.
    Shimizu, T., Kida, Y., and Kuwano, K. (2005) J. Immunol., 175, 4641–4646.PubMedGoogle Scholar
  32. 32.
    Hasebe, A., Mu, H. H., Washborn, L. R., Chan, F. V., Pennock, N. D., Taylor, M. L., and Cole, B. C. (2007) Infect. Immun., 75, 1820–1826.PubMedGoogle Scholar
  33. 33.
    Hirschfeld, M., Kirschning, C. J., Schwandner, R., Wesche, H., Weis, J. H., Wooten, R. M., and Weis, J. J. (1999) J. Immunol., 163, 2382–2386.PubMedGoogle Scholar
  34. 34.
    Lopez, M., Sly, L. M., Luu, Y., Young, D., Cooper, H., and Reiner, N. E. (2003) J. Immunol., 170, 2409–2416.PubMedGoogle Scholar
  35. 35.
    Tanamoto, K.-I., Kato, H., Haishima, Y., and Azumi, S. (2001) Clin. Diagn. Lab. Immun., 8, 522–527.Google Scholar
  36. 36.
    Wyllie, D. H., Kiss-Toth, E., Visintin, A., Smith, S. C., Boussouf, S., Segal, D. M., Duff, G. W., and Dower, S. K. (2000) J. Immunol., 165, 7125–7132.PubMedGoogle Scholar
  37. 37.
    Kurt-Jones, E. A., Chan, M., Zhou, S., Wang, J., Reed, G., Bronson, R., Arnold, M. M., Knipe, D. M., and Finberg, R. W. (2004) Proc. Natl. Acad. Sci. USA, 101, 1315–1320.PubMedGoogle Scholar
  38. 38.
    Wang, J. P., Kurt-Jones, E. A., Shin, O. S., Mnachak, M. D., Levin, M. J., and Finberg, R. W. (2005) J. Virol., 79, 12658–12666.PubMedGoogle Scholar
  39. 39.
    Compton, T., Kurt-Jones, E. A., Boehme, K. W., Belko, J., Latz, E., Golenbock, D. T., and Finberg, R. W. (2003) J. Virol., 77, 4588–4596.PubMedGoogle Scholar
  40. 40.
    Frasnelli, M. E., Tarussion, D., Chobaz-Peclat, V., Busso, N., and So, A. (2005) Arthritis Res. Ther., 7, 370–379.Google Scholar
  41. 41.
    Scheibner, K. A., Lutz, M. A., Boodoo, S., Fenton, M. J., Powell, J. D., and Horton, M. R. (2006) J. Immunol., 177, 1272–1281.PubMedGoogle Scholar
  42. 42.
    Park, J. S., Svetkauskaite, D., He, Q., Kim, J. Y., Strassheim, D., Ishizaka, A., and Abraham, E. (2004) J. Biol. Chem., 279, 7370–7377.PubMedGoogle Scholar
  43. 43.
    Funderburg, N., Lederman, M. M., Feng, Z., Drage, M. G., Jadlowsky, J., Harding, C. V., Weinberg, A., and Sieg, S. F. (2007) Proc. Natl. Acad. Sci. USA, 104, 18631–18635.PubMedGoogle Scholar
  44. 44.
    Vabulas, R. M., Ahmad-Nejad, P., Ghose, S., Kirschning, C. J., Issels, R. D., and Wagner, H. (2002) J. Biol. Chem., 277, 15107–15112.PubMedGoogle Scholar
  45. 45.
    Asea, A., Rehli, M., Kabingu, E., Boch, J. A., Bare, O., Auron, P. E., Stevenson, M. A., and Calderwood, S. K. (2002) J. Biol. Chem., 277, 15028–15034.PubMedGoogle Scholar
  46. 46.
    Vabulas, R. M., Braedel, S., Hilf, N., Singh-Jasuja, H., Herter, S., Ahmad-Nejad, P., Kirschning, C. J., Da Costa, C., Rammensee, H. G., Wagner, H., and Schild, H. (2002) J. Biol. Chem., 277, 20847–20853.PubMedGoogle Scholar
  47. 47.
    Ohya, M., Nishitani, C., Sano, H., Yamada, C., Mitsuzawa, H., Shimizu, T., Saito, T., Smith, K., Crouch, E., and Kuroki, Y. (2006) Biochemistry, 45, 8657–8664.PubMedGoogle Scholar
  48. 48.
    Alexopoulou, L., Holt, A. C., Medzhitov, R., and Flavell, R. A. (2001) Nature, 413, 732–738.PubMedGoogle Scholar
  49. 49.
    Tada, H., Nemoto, E., Shimauchi, H., Watanabe, T., Mikami, T., Matsumoto, T., Ohno, N., Tamura, H., Shibata, K., Akashi, S., Miyake, K., Sugawara, S., and Takada, H. (2002) Microbiol. Immunol., 46, 503–512.PubMedGoogle Scholar
  50. 50.
    Netea, M. G., van der Graaf, C., van der Meer, J. W., and Kullberg, B. J. (2004) Eur. J. Clin. Microbiol. Infect. Dis., 23, 672–676.PubMedGoogle Scholar
  51. 51.
    Oliveira, A. C., Peixoto, J. R., de Arruda, L. B., Campos, M. A., Gazzinelli, R. T., Golenbock, D. T., Akira, S., Previato, J. O., Mendonca-Previato, L., Nobrega, A., and Bellio, M. (2004) J. Immunol., 173, 5688–5696.PubMedGoogle Scholar
  52. 52.
    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) Nat. Immunol., 1, 398–401.PubMedGoogle Scholar
  53. 53.
    Rassa, J. C., Meyers, J. L., Zhang, Y., Kudaravalli, R., and Ross, S. R. (2002) Proc. Natl. Acad. Sci. USA, 99, 2281–2286.PubMedGoogle Scholar
  54. 54.
    Chow, J. C., Young, D. W., Golenbock, D. T., Christ, W. J., and Gusovsky, F. (1999) J. Biol. Chem., 274, 10689–10692.PubMedGoogle Scholar
  55. 55.
    Yamada, C., Sano, H., Shimizu, T., Mitsuzawa, H., Nishitani, C., Himi, T., and Kuroki, Y. (2006) J. Biol. Chem., 281, 21771–21780.PubMedGoogle Scholar
  56. 56.
    Biragyn, A., Ruffini, P. A., Leifer, C. A., Klyushnenkova, E., Shakhov, A., Chertov, O., Shirakawa, A. K., Farber, J. M., Segal, D. M., Oppenheim, J. J., and Kwak, L. W. (2002) Science, 298, 1025–1029.PubMedGoogle Scholar
  57. 57.
    Yang, Y., Jiang, Y., Yin, Q., Liang, H., and She, R. (2010) Vet. Immunol. Immunopathol., 133, 59–65.PubMedGoogle Scholar
  58. 58.
    Kawasaki, K., Akashi, S., Shimazu, R., Yoshida, T., Miyake, K., and Nishijima, M. (2000) J. Biol. Chem., 275, 2251–2254.PubMedGoogle Scholar
  59. 59.
    Ohashi, K., Burkart, V., Flohe, S., and Kolb, H. (2000) J. Immunol., 164, 558–561.PubMedGoogle Scholar
  60. 60.
    Roelofs, M. F., Boelens, W. C., Joosten, L. A., Abdollahi-Roodsaz, S., Geurts, J., Wunderink, L. U., Schreurs, B. W., van den Berg, W. B., and Radstake, T. R. (2006) J. Immunol., 176, 7021–7027.PubMedGoogle Scholar
  61. 61.
    Termeer, C., Benedix, F., Sleeman, J., Fieber, C., Voith, U., Ahrens, T., Miyake, K., Freudenberg, M., Galanos, C., and Simon, J. C. (2002) J. Exp. Med., 195, 99–111.PubMedGoogle Scholar
  62. 62.
    Okamura, Y., Watari, M., Jerud, E. S., Young, D. W., Ishizaka, S. T., Rose, J., Chow, J. C., and Strauss, J. F., III. (2001) J. Biol. Chem., 276, 10229–10233.PubMedGoogle Scholar
  63. 63.
    Smiley, S. T., King, J. A., and Hancock, W. W. (2001) J. Immunol., 167, 2887–2894.PubMedGoogle Scholar
  64. 64.
    Lee, J. Y., Sohn, K. H., Rhee, S. H., and Hwang, D. (2001) J. Biol. Chem., 276, 16683–16689.PubMedGoogle Scholar
  65. 65.
    Miller, Y. I., Viriyakosol, S., Binder, C. J., Feramisco, J. R., Kirkland, T. N., and Witztum, J. L. (2003) J. Biol. Chem., 278, 1561–1568.PubMedGoogle Scholar
  66. 66.
    Gomi, K., Kawasaki, K., Kawai, Y., Shiozaki, M., and Nishijima, M. (2002) J. Immunol., 168, 2939–2943.PubMedGoogle Scholar
  67. 67.
    Lien, E., Chow, J. C., Hawkins, L. D., McGuinness, P. D., Miyake, K., Espevik, T., Gusovsky, F., and Golenbock, D. T. (2001) J. Biol. Chem., 276, 1873–1880.PubMedGoogle Scholar
  68. 68.
    Johnson, G. B., Brunn, G. J., Kodaira, Y., and Platt, J. L. (2002) J. Immunol., 168, 5233–5239.PubMedGoogle Scholar
  69. 69.
    Andersen-Nissen, E., Smith, K. D., Strobe, K. L., Barrett, S. L., Cookson, B. T., Logan, S. M., and Aderem, A. (2005) Proc. Natl. Acad. Sci. USA, 102, 9247–9252.PubMedGoogle Scholar
  70. 70.
    Diebold, S. S., Kaisho, T., Hemmi, H., Akira, S., Reis, E., and Sousa, C. (2004) Science, 303, 1529–1531.PubMedGoogle Scholar
  71. 71.
    Heil, F., Hemmi, H., Hochrein, H., Ampenberger, F., Kirschning, C., Akira, S., Lipford, G., Wagner, H., and Bauer, S. (2004) Science, 303, 1526–1529.PubMedGoogle Scholar
  72. 72.
    Akira, S., and Hemmi, H. (2003) Immunol. Lett., 85, 85–95.PubMedGoogle Scholar
  73. 73.
    Lee, J., Chuang, T. H., Redecke, V., She, L., Pitha, P. M., Carson, D. A., Raz, E., and Cottam, H. B. (2003) Proc. Natl. Acad. Sci. USA, 100, 6646–6651.PubMedGoogle Scholar
  74. 74.
    Jurk, M., Heil, F., Vollmer, J., Schetter, C., Krieg, A. M., Wagner, H., Lipford, G., and Bauer, S. (2002) Nat. Immunol., 3, 499.PubMedGoogle Scholar
  75. 75.
    Latz, E., Schoenemeyer, A., Visintin, A., Fitzgerald, K. A., Monks, B. G., Knetter, C. F., Lien, E., Nilsen, N. J., Espevik, T., and Golenbock, D. T. (2004) Nat. Immunol., 5, 190–198.PubMedGoogle Scholar
  76. 76.
    Leadbetter, E. A., Rifkin, I. R., Hohlbaum, A. M., Beaudette, B. C., Shlomchik, M. J., and Marshak-Rothstein, A. (2002) Nature, 416, 603–607.PubMedGoogle Scholar
  77. 77.
    Zhang, D., Zhang, G., Hayden, M. S., Greenblatt, M. B., Bussey, C., Flavell, R. A., and Ghosh, S. (2004) Science, 303, 1522–1526.PubMedGoogle Scholar
  78. 78.
    Yarovinsky, F., Zhang, D., Andersen, J. F., Bannenberg, G. L., Serhan, C. N., Hayden, M. S., Hieny, S., Sutterwala, F. S., Flavell, R. A., Ghosh, S., and Sher, A. (2005) Science, 308, 1626–1629.PubMedGoogle Scholar
  79. 79.
    Akashi-Takamura, S., and Miyake, K. (2008) Curr. Opin. Immunol., 20, 420–425.PubMedGoogle Scholar
  80. 80.
    Medzhitov, R., Preston-Hurlburt, P., and Janeway, C. A., Jr. (1997) Nature, 388, 394–397.PubMedGoogle Scholar
  81. 81.
    Poltorak, A., He, X., Smirnova, I., Liu, M. Y., van Huffel, C., Du, X., Birdwell, D., Alejos, E., Silva, M., Galanos, C., Freudenberg, M., Ricciardi-Castagnoli, P., Layton, B., and Beutler, B. (1998) Science, 282, 2085–2088.PubMedGoogle Scholar
  82. 82.
    Mazzoni, A., and Segal, D. M. (2004) J. Leukoc. Biol., 75, 721–730.PubMedGoogle Scholar
  83. 83.
    Aravind, L., Dixit, V. M., and Koonin, E. V. (2001) Science, 291, 1279–1284.PubMedGoogle Scholar
  84. 84.
    Jebanathirajah, J. A., Peri, S., and Pandey, A. (2002) Trends Plant. Sci., 7, 388–391.PubMedGoogle Scholar
  85. 85.
    Kawai, T., and Akira, S. (2007) Semin. Immunol., 19, 24–32.PubMedGoogle Scholar
  86. 86.
    Iwasaki, A., and Medzhitov, R. (2004) Nat. Immunol., 5, 987–995.PubMedGoogle Scholar
  87. 87.
    Kobe, B., and Deisenhofer, J. (1995) Curr. Opin. Struct. Biol., 5, 409–416.PubMedGoogle Scholar
  88. 88.
    Jin, M. S., Kim, S. E., Heo, J. Y., Lee, M. E., Kim, H. M., Paik, S. G., Lee, H., and Lee, J. O. (2007) Cell, 130, 1071–1082.PubMedGoogle Scholar
  89. 89.
    Liu, L., Botos, I., Wang, Y., Leonard, J. N., Shiloach, J., Segal, D. M., and Davies, D. R. (2008) Science, 320, 379–381.PubMedGoogle Scholar
  90. 90.
    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., and Lee, J. O. (2007) Cell, 130, 906–917.PubMedGoogle Scholar
  91. 91.
    Park, B. S., Song, D. H., Kim, H. M., Choi, B. S., Lee, H., and Lee, J. O. (2009) Nature, 458, 1191–1195.PubMedGoogle Scholar
  92. 92.
    Murakami, S., Iwaki, D., Mitsuzawa, H., Sano, H., Takahashi, H., Voelker, D. R., Akino, T., and Kuroki, Y. (2002) J. Biol. Chem., 277, 6830–6837.PubMedGoogle Scholar
  93. 93.
    Sano, H., Chiba, H., Iwaki, D., Sohma, H., Voelker, D. R., and Kuroki, Y. (2000) J. Biol. Chem., 275, 22442–22451.PubMedGoogle Scholar
  94. 94.
    Yamada, C., Sano, H., Shimizu, T., Mitsuzawa, H., Nishitani, C., Himi, T., and Kuroki, Y. (2006) J. Biol. Chem., 281, 21771–21780.PubMedGoogle Scholar
  95. 95.
    Chiba, H., Sano, H., Iwaki, D., Murakami, S., Mitsuzawa, H., Takahashi, T., Konishi, M., Takahashi, H., and Kuroki, Y. (2001) Infect. Immun., 69, 1587–1592.PubMedGoogle Scholar
  96. 96.
    Biragyn, A., Coscia, M., Nagashima, K., Sanford, M., Young, H. A., and Olkhanud, P. (2008) J. Leukoc. Biol., 83, 998–1008.PubMedGoogle Scholar
  97. 97.
    Lande, R., Gregorio, J., Facchinetti, V., Chatterjee, B., Wang, Y. H., Homey, B., Cao, W., Wang, Y. H., Su, B., Nestle, F. O., Zal, T., Mellman, I., Schroder, J. M., Liu, Y. J., and Gilliet, M. (2007) Nature, 449, 564–569.PubMedGoogle Scholar
  98. 98.
    Tian, J., Avalos, A. M., Mao, S. Y., Chen, B., Senthil, K., Wu, H., Parroche, P., Drabic, S., Golenbock, D., Sirois, C., Hua, J., An, L. L., Audoly, L., La Rosa, G., Bierhaus, A., Naworth, P., Marshak-Rothstein, A., Crow, M. K., Fitzgerald, K. A., Latz, E., Kiener, P. A., and Coyle, A. J. (2007) Nat. Immunol., 8, 487–496.PubMedGoogle Scholar
  99. 99.
    Ivanov, S., Dragoi, A. M., Wang, X., Dallacosta, C., Louten, J., Musco, G., Sitia, G., Yap, G. S., Wan, Y., Biron, C. A., Bianchi, M. E., Wang, H., and Chu, W. M. (2007) Blood, 110, 1970–1981.PubMedGoogle Scholar
  100. 100.
    Hoebe, K., Georgel, P., Rutschmann, S., Du, X., Mudd, S., Crozat, K., Sovath, S., Shamel, L., Hartung, T., Zahringer, U., and Beutler, B. (2005) Nature, 433, 523–527.PubMedGoogle Scholar
  101. 101.
    Jiang, Z., Georgel, P., Du, X., Shamel, L., Sovath, S., Mudd, S., Huber, M., Kalis, C., Keck, S., Galanos, C., Freudenberg, M., and Beutler, B. (2005) Nat. Immunol., 6, 565–570.PubMedGoogle Scholar
  102. 102.
    Lee, H. K., Dunzendorfer, S., Soldau, K., and Tobias, P. S. (2006) Immunity, 24, 153–163.PubMedGoogle Scholar
  103. 103.
    Blumenthal, A., Kobayashi, T., Pierini, L. M., Banaei, N., Ernst, J. D., Miyake, K., and Ehrt, S. (2009) Cell Host Microbe, 5, 35–46.PubMedGoogle Scholar
  104. 104.
    Schumann, R. R., Leong, S. R., Flaggs, G. W., Gray, P. W., Wright, S. D., Mathison, J. C., Tobias, P. S., and Ulevitch, R. J. (1990) Science, 249, 1429–1431.PubMedGoogle Scholar
  105. 105.
    Matsumoto, F., Saitoh, S., Fukui, R., Kobayashi, T., Tanimura, N., Konno, K., Kusumoto, Y., Akashi-Takamura, S., and Miyake, K. (2008) Biochem. Biophys. Res. Commun., 367, 693–699.PubMedGoogle Scholar
  106. 106.
    Zahringer, U., Lindner, B., Inamura, S., Heine, H., and Alexander, C. (2008) Immunobiology, 213, 205–224.PubMedGoogle Scholar
  107. 107.
    Michel, T., Reichhart, J. M., Hoffmann, J. A., and Royet, J. (2001) Nature, 414, 756–759.PubMedGoogle Scholar
  108. 108.
    Bischoff, V., Vignal, C., Boneca, I. G., Michel, T., Hoffmann, J. A., and Royet, J. (2004) Nat. Immunol., 5, 1175–1180.PubMedGoogle Scholar
  109. 109.
    Roh, K. B., Kim, C. H., Lee, H., Kwon, H. M., Park, J. W., Ryu, J. H., Kurokawa, K., Ha, N. C., Lee, W. J., Lemaitre, B., Soderhall, K., and Lee, B. L. (2009) J. Biol. Chem., 284, 19474–19481.PubMedGoogle Scholar
  110. 110.
    Crouch, E., and Wright, J. R. (2001) Annu. Rev. Physiol., 63, 521–554.PubMedGoogle Scholar
  111. 111.
    Sano, H., Sohma, H., Muta, T., Nomura, S., Voelker, D. R., and Kuroki, Y. (1999) J. Immunol., 163, 387–395.PubMedGoogle Scholar
  112. 112.
    Kuan, S.-F., Rust, K., and Crouch, E. (1992) J. Clin. Invest., 90, 97–106.PubMedGoogle Scholar
  113. 113.
    McNeely, T. B., and Coonrod, J. D. (1994) Am. J. Respir. Cell Mol. Biol., 11, 114–122.PubMedGoogle Scholar
  114. 114.
    Kabha, K., Schmegner, J., Keisari, Y., Parolis, H., Schlepper-Schaefer, J., and Ofek, I. (1997) Am. J. Physiol., 272, L344–L352.PubMedGoogle Scholar
  115. 115.
    Zimmerman, P. E., Voelker, D. R., McCormack, F. X., Paulsrud, J. R., and Martin, W. J. I. (1992) J. Clin. Invest., 89, 143–149.PubMedGoogle Scholar
  116. 116.
    Chiba, H., Pattanajitvilai, S., Evans, A. J., Harbeck, R. J., and Voelker, D. R. (2002) J. Biol. Chem., 277, 20379–20385.PubMedGoogle Scholar
  117. 117.
    Ferguson, J. S., Voelker, D. R., McCormack, F. X., and Schlesinger, L. S. (1999) J. Immunol., 163, 312–321.PubMedGoogle Scholar
  118. 118.
    Kudo, K., Sano, H., Takahashi, H., Kuronuma, K., Yokota, S., Fujii, N., Shimada, K., Yano, I., Kumazawa, Y., Voelker, D. R., Abe, S., and Kuroki, Y. (2004) J. Immunol., 172, 7592–7602.PubMedGoogle Scholar
  119. 119.
    Hartshorn, K. L., White, M. R., Voelker, D. R., Coburn, J., Zaner, K., and Crouch, E. C. (2000) Biochem. J., 351, 449–458.PubMedGoogle Scholar
  120. 120.
    Hickling, T. P., Bright, H., Wing, K., Gower, D., Martin, S. L., Sim, R. B., and Malhotra, R. (1999) Eur. J. Immunol., 29, 3478–3484.PubMedGoogle Scholar
  121. 121.
    Nadesalingam, J., Dodds, A. W., Reid, K. B., and Palaniyar, N. (2005) J. Immunol., 175, 1785–1794.PubMedGoogle Scholar
  122. 122.
    Devyatyarova-Johnson, M., Rees, I. H., Robertson, B. D., Turner, M. W., Klein, N. J., and Jack, D. L. (2000) Infect. Immun., 68, 3894–3899.PubMedGoogle Scholar
  123. 123.
    Polotsky, V. Y., Belisle, J. T., Mikusova, K., Ezekowitz, R. A., and Joiner, K. A. (1997) J. Infect. Dis., 175, 1159–1168.PubMedGoogle Scholar
  124. 124.
    Guan, R., and Mariuzza, R. A. (2007) Trends Microbiol., 15, 127–134.PubMedGoogle Scholar
  125. 125.
    Menendez, A., and Brett Finlay, B. (2007) Curr. Opin. Immunol., 19, 385–391.PubMedGoogle Scholar
  126. 126.
    Yang, D., Chertov, O., Bykovskaia, S. N., Chen, Q., Buffo, M. J., Shogan, J., Anderson, M., Schroder, J. M., Wang, J. M., Howard, O. M., and Oppenheim, J. J. (1999) Science, 286, 525–528.PubMedGoogle Scholar
  127. 127.
    Funderburg, N., Lederman, M. M., Feng, Z., Drage, M. G., Jadlowsky, J., Harding, C. V., Weinberg, A., and Sieg, S. F. (2007) Proc. Natl. Acad. Sci. USA, 104, 18631–18635.PubMedGoogle Scholar
  128. 128.
    Dietrich, D. E., Xiao, X., Dawson, D. V., Belanger, M., Xie, H., Progulske-Fox, A., and Brogden, K. A. (2008) Infect. Immun., 76, 5714–5720.PubMedGoogle Scholar
  129. 129.
    Hartshorn, K. L., White, M. R., Tecle, T., Holmskov, U., and Crouch, E. C. (2006) J. Immunol., 176, 6962–6972.PubMedGoogle Scholar
  130. 130.
    Furci, L., Sironi, F., Tolazzi, M., Vassena, L., and Lusso, P. (2007) Blood, 109, 2928–2935.PubMedGoogle Scholar
  131. 131.
    Raffi, H. S., Bates, J. M., Jr., Laszik, Z., and Kumar, S. (2005) Am. J. Nephrol., 25, 570–578.PubMedGoogle Scholar
  132. 132.
    Pak, J., Pu, Y., Zhang, Z. T., Hasty, D. L., and Wu, X. R. (2001) J. Biol. Chem., 276, 9924–9930.PubMedGoogle Scholar
  133. 133.
    Wimmer, T., Cohen, G., Saemann, M. D., and Horl, W. H. (2004) Nephrol. Dial. Transplant., 19, 2192–2197.PubMedGoogle Scholar
  134. 134.
    Saemann, M. D., Weichhart, T., Zeyda, M., Staffler, G., Schunn, M., Stuhlmeier, K. M., Sobanov, Y., Stulnig, T. M., Akira, S., von Gabain, A., von Ahsen, U., Horl, W. H., and Zlabinger, G. J. (2005) J. Clin. Invest., 115, 468–475.PubMedGoogle Scholar
  135. 135.
    Pfistershammer, K., Klauser, C., Leitner, J., Stockl, J., Majdic, O., Weichhart, T., Sobanov, Y., Bochkov, V., Saemann, M., Zlabinger, G., and Steinberger, P. (2008) J. Leukoc. Biol., 83, 131–138.PubMedGoogle Scholar
  136. 136.
    Muller, S., Ronfani, L., and Bianchi, M. E. (2004) J. Intern. Med., 255, 332–343.PubMedGoogle Scholar
  137. 137.
    Park, J. S., Arcaroli, J., Yum, H. K., Yang, H., Wang, H., Yang, K. Y., Choe, K. H., Strassheim, D., Pitts, T. M., Tracey, K. J., and Abraham, E. (2003) Am. J. Physiol. Cell Physiol., 284, 870–879.Google Scholar
  138. 138.
    Yang, D., Chen, Q., Yang, H., Tracey, K. J., Bustin, M., and Oppenheim, J. J. (2006) J. Leukoc. Biol., 81, 59–66.PubMedGoogle Scholar
  139. 139.
    Dumitriu, I. E., Baruah, P., Manfredi, A. A., Bianchi, M. E., and Rovere-Querini, P. (2005) Trends Immunol., 26, 381–387.PubMedGoogle Scholar
  140. 140.
    Degryse, B., Bonaldi, T., Scaffidi, P., Muller, S., Resnati, M., Sanvito, F., Arrigoni, G., and Bianchi, M. E. (2001) J. Cell Biol., 152, 1197–1206.PubMedGoogle Scholar
  141. 141.
    Mitola, S., Belleri, M., Urbinati, C., Coltrini, D., Sparatore, B., Pedrazzi, M., Melloni, E., and Presta, M. (2006) J. Immunol., 1, 12–15.Google Scholar
  142. 142.
    Messmer, D., Yang, H., Telusma, G., Knoll, F., Li, J., Messmer, B., Tracey, K. J., and Chiorazzi, N. (2004) J. Immunol., 173, 307–313.PubMedGoogle Scholar
  143. 143.
    Dumitriu, I. E., Baruah, P., Bianchi, M. E., Manfredi, A. A., and Rovere-Querini, P. (2005) Eur. J. Immunol., 35, 2184–2190.PubMedGoogle Scholar
  144. 144.
    Palumbo, R., Sampaolesi, M., De Marchis, F., Tonlorenzi, R., Colombetti, S., Mondino, A., Cossu, G., and Bianchi, M. E. (2004) J. Cell Biol., 164, 441–449.PubMedGoogle Scholar
  145. 145.
    Jack, R. S., Fan, X., Bernheiden, M., Rune, G., Ehlers, M., Weber, A., Kirsch, G., Mentel, R., Furll, B., Freudenberg, M., Schmitz, G., Stelter, F., and Schutt, C. (1997) Nature, 389, 742–745.PubMedGoogle Scholar
  146. 146.
    Knapp, S., de Vos, A. F., Florquin, S., Golenbock, D. T., and van der Poll, T. (2003) Infect. Immun., 71, 6747–6753.PubMedGoogle Scholar
  147. 147.
    Fan, M. H., Klein, R. D., Steinstraesser, L., Merry, A. C., Nemzek, J. A., Remick, D. G., Wang, S. C., and Su, G. L. (2002) Shock, 18, 248–254.PubMedGoogle Scholar
  148. 148.
    Tobias, P. S., Soldau, K., Gegner, J. A., Mintz, D., and Ulevitch, R. J. (1995) J. Biol. Chem., 270, 10482–10488.PubMedGoogle Scholar
  149. 149.
    Vesy, C. J., Kitchens, R. L., Wolfbauer, G., Albers, J. J., and Munford, R. S. (1999) Infect. Immun., 68, 2410–2417.Google Scholar
  150. 150.
    Yu, B., and Wright, S. D. (1996) J. Biol. Chem., 271, 4100–4105.PubMedGoogle Scholar
  151. 151.
    Wurfel, M. M., Hailman, E., and Wright, S. D. (1995) J. Exp. Med., 181, 1743–1754.PubMedGoogle Scholar
  152. 152.
    Kitchens, R. L., Thompson, P. A., Munford, R. S., and O’Keefe, G. E. (2003) J. Lipid Res., 44, 2339–2348.PubMedGoogle Scholar
  153. 153.
    Gutsmann, T., Muller, M., Carroll, S. F., MacKenzie, R. C., Wiese, A., and Seydel, U. (2001) Infect. Immun., 69, 6942–6950.PubMedGoogle Scholar
  154. 154.
    Frey, E. A., Miller, D. S., Jahr, T. G., Sundan, A., Bazil, V., Espevik, T., Finlay, B. B., and Wright, S. D. (1992) J. Exp. Med., 176, 1665–1671.PubMedGoogle Scholar
  155. 155.
    Hailman, E., Vasselon, T., Kelley, M., Busse, L. A., Hu, M. C., Lichenstein, H. S., Detmers, P. A., and Wright, S. D. (1996) J. Immunol., 156, 4384–4390.PubMedGoogle Scholar
  156. 156.
    Pugin, J., Schurer-Maly, C.-C., Leturcq, D., Moriarty, A., Ulevitch, R. J., and Tobias, P. S. (1993) Proc. Natl. Acad. Sci. USA, 90, 2744–2748.PubMedGoogle Scholar
  157. 157.
    Da Silva Correia, J., Soldau, K., Christen, U., Tobias, P. S., and Ulevitch, R. J. (2001) J. Biol. Chem., 276, 21129–21135.PubMedGoogle Scholar
  158. 158.
    Akashi, S., Saitoh, S., Wakabayashi, Y., Kikuchi, T., Takamura, N., Nagai, Y., Kusumoto, Y., Fukase, K., Kusumoto, S., Adachi, Y., Kosugi, A., and Miyake, K. (2003) J. Exp. Med., 198, 1035–1042.PubMedGoogle Scholar
  159. 159.
    Wright, S. D., Ramos, R. A., Tobias, P. S., Ulevitch, R. J., and Mathison, J. C. (1990) Science, 249, 1431–1433.PubMedGoogle Scholar
  160. 160.
    Haziot, A., Ferrero, E., Kontgen, F., Hijiya, N., Yamamoto, S., Silver, J., Stewart, C. L., and Goyert, S. M. (1996) Immunity, 4, 407–414.PubMedGoogle Scholar
  161. 161.
    Muroi, M., Ohnishi, T., and Tanamoto, K. (2002) J. Biol. Chem., 277, 42372–42379.PubMedGoogle Scholar
  162. 162.
    Juan, T. S., Hailman, E., Kelley, M. J., Wright, S. D., and Lichenstein, H. S. (1995) J. Biol. Chem., 270, 17237–17242.PubMedGoogle Scholar
  163. 163.
    Stelter, F., Loppnow, H., Menzel, R., Grunwald, U., Bernheiden, M., Jack, R. S., Ulmer, A. J., and Schutt, C. (1999) J. Immunol., 163, 6035–6044.PubMedGoogle Scholar
  164. 164.
    Viriyakosol, S., Tobias, P. S., Kitchens, R. L., and Kirkland, T. N. (2001) J. Biol. Chem., 276, 38044–38051.PubMedGoogle Scholar
  165. 165.
    Ohto, U., Fukase, K., Miyake, K., and Satow, Y. (2007) Science, 316, 1632–1634.PubMedGoogle Scholar
  166. 166.
    Nagai, Y., Akashi, S., Nagafuku, M., Ogata, M., Iwakura, Y., Akira, S., Kitamura, T., Kosugi, A., Kimoto, M., and Miyake, K. (2002) Nat. Immunol., 3, 667–672.PubMedGoogle Scholar
  167. 167.
    Mancek, M., Pristovsek, P., and Jerala, R. (2002) Biochem. Biophys. Res. Commun., 292, 880–885.PubMedGoogle Scholar
  168. 168.
    Kawasaki, K., Gomi, K., and Nishijima, M. (2001) J. Immunol., 166, 11–14.PubMedGoogle Scholar
  169. 169.
    Akashi, S., Nagai, Y., Ogata, H., Oikawa, M., Fukase, K., Kusumoto, S., Kawasaki, K., Nishijima, M., Hayashi, S., Kimoto, M., and Miyake, K. (2001) Int. Immunol., 13, 1595–1599.PubMedGoogle Scholar
  170. 170.
    Lien, E., Means, T. K., Heine, H., Yoshimura, A., Kusumoto, S., Fukase, K., Fenton, M. J., Oikawa, M., Qureshi, N., Monks, B., Finberg, R. W., Ingalls, R. R., and Golenbock, D. T. (2000) J. Clin. Invest., 105, 497–504.PubMedGoogle Scholar
  171. 171.
    Hajjar, A. M., Ernst, R. K., Tsai, J. H., Wilson, C. B., and Miller, S. I. (2002) Nat. Immunol., 3, 354–359.PubMedGoogle Scholar
  172. 172.
    Ohnishi, T., Muroi, M., and Tanamoto, K. (2003) Clin. Diagn. Lab. Immunol., 10, 405–410.PubMedGoogle Scholar
  173. 173.
    Da Silva Correia, J., and Ulevitch, R. J. (2002) J. Biol. Chem., 277, 1845–1854.PubMedGoogle Scholar
  174. 174.
    Divanovic, S., Trompette, A., Atabani, S. F., Madan, R., Golenbock, D. T., Visintin, A., Finberg, R. W., Tarakhovsky, A., Vogel, S. N., Belkaid, Y., Kurt-Jones, E. A., and Karp, C. L. (2005) Nat. Immunol., 6, 571–578.PubMedGoogle Scholar
  175. 175.
    Miyake, K., Yamashita, Y., Ogata, M., Sudo, T., and Kimoto, M. (1995) J. Immunol., 154, 3333–3340.PubMedGoogle Scholar
  176. 176.
    Kimoto, M., Nagasawa, K., and Miyake, K. (2003) Scand. J. Infect. Dis., 35, 568–572.PubMedGoogle Scholar
  177. 177.
    Blumenthal, A., Lauber, J., Hoffmann, R., Ernst, M., Keller, C., Buer, J., Ehlers, S., and Reiling, N. (2005) Infect. Immunol., 73, 3330–3341.Google Scholar
  178. 178.
    Nagai, Y., Shimazu, R., Ogata, H., Akashi, S., Sudo, K., Yamasaki, H., Hayashi, S., Iwakura, Y., Kimoto, M., and Miyake, K. (2002) Blood, 99, 1699–1705.PubMedGoogle Scholar
  179. 179.
    Ogata, H., Su, I., Miyake, K., Nagai, Y., Akashi, S., Mecklenbrauker, I., Rajewsky, K., Kimoto, M., and Tarakhovsky, A. (2000) J. Exp. Med., 192, 23–29.PubMedGoogle Scholar
  180. 180.
    Tsuneyoshi, N., Fukudome, K., Kohara, J., Tomimasu, R., Gauchat, J. F., Nakatake, H., and Kimoto, M. (2005) J. Immunol., 174, 340–344.PubMedGoogle Scholar
  181. 181.
    Murphy, J. E., Tedbury, P. R., Homer-Vanniasinkam, S., Walker, J. H., and Ponnambalam, S. (2005) Atherosclerosis, 182, 1–15.PubMedGoogle Scholar
  182. 182.
    Means, T. K., Mylonakis, E., Tampakakis, E., Colvin, R. A., Seung, E., Puckett, L., Tai, M. F., Stewart, C. R., Pukkila-Worley, R., Hickman, S. E., Moore, K. J., Calderwood, S. B., Hacohen, N., Luster, A. D., and El Khoury, J. (2009) J. Exp. Med., 206, 637–653.PubMedGoogle Scholar
  183. 183.
    Triantafilou, M., Gamper, F. G., Haston, R. M., Mouratis, M. A., Morath, S., Hartung, T., and Triantafilou, K. (2006) J. Biol. Chem., 281, 31002–31011.PubMedGoogle Scholar
  184. 184.
    Stuart, L. M., Deng, J., Silver, J. M., Takahashi, K., Tseng, A. A., Hennessy, E. J., Ezekowitz, R. A., and Moore, K. J. (2005) J. Cell Biol., 170, 477–485.PubMedGoogle Scholar
  185. 185.
    Manukyan, M., Triantafilou, K., Triantafilou, M., Mackie, A., Nilsen, N., Espevik, T., Wiesmuller, K. H., Ulmer, A. J., and Heine, H. (2005) Eur. J. Immunol., 35, 911–921.PubMedGoogle Scholar
  186. 186.
    Miyake, K. (2004) Semin. Immunol., 16, 11–16.PubMedGoogle Scholar

Copyright information

© Pleiades Publishing, Ltd. 2010

Authors and Affiliations

  • A. I. Tukhvatulin
    • 1
    Email author
  • D. Yu. Logunov
    • 1
  • D. N. Shcherbinin
    • 1
  • M. M. Shmarov
    • 1
  • B. S. Naroditsky
    • 1
  • A. V. Gudkov
    • 2
  • A. L. Gintsburg
    • 1
  1. 1.Gamaleya Institute of Epidemiology and MicrobiologyRussian Academy of Medical SciencesMoscowRussia
  2. 2.Roswell Park Cancer InstituteBuffaloUSA

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