Skip to main content
SpringerLink
Log in

Regulation of mast cell-mediated innate immunity during early response to bacterial infection

  • Published:
Clinical Reviews in Allergy & Immunology Aims and scope Submit manuscript

Summary

Although the area of research on the role of MCs in innate immunity is relatively new, a number of studies that are reviewed here provide substantial evidence that MCs play a critical role in host immune defense against gram-negative bacteria. The studies show that mast cells have the ability to recognize and engulf bacteria and they release a number of inflammatory mediators including interleukin (IL)-4, IL-6, IL-10, TNFα, and leukotrienes in response to bacterial challenge. MC-derived TNFα and leukotrienes are shown to be important for bacterial clearance and early recruitment of phagocytic help at the site of infection. Studies directed at elucidating the molecular mechanisms associated with mast cell recognition of bacteria and subsequent events leading to mast cell mediator release revealed that GPI anchored CD48 molecule present on the cell surface of mast cells serves as a receptor for the bacterial adhesion molecule, FimH. The ligation of CD48 receptor by FimH-expresing bacteria results in bacterial uptake into caveolar chambers. This distinct mechanism of bacterial uptake promot es bacteral survival inside the cytosol of the mast cells. Although the exact mechanism(s) of how MC-dependent inflammatory responses are regulated is currently not known, recent studies have shown that complement, CD11β/CD18 (Mac-1) and protein tyrosine kinase JAK3, and TLR4 are important for the full expression of MC-dependent innate immunity in mice.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Rodewald, H. R., Dessing, M., Dvorak, A. M., and Galli, S. J. (1996), Science 271,818–822.

    Article  PubMed  CAS  Google Scholar 

  2. Galli, S. J., Gordon, J. R., and Wershil, B. K. (1993), Agents Actions Suppl. 43, 209–220.

    PubMed  CAS  Google Scholar 

  3. Galli, S. J. (1993), N. Engl. J. Med. 328,257–265.

    Article  PubMed  CAS  Google Scholar 

  4. Galli, S. J. and Wershil, B. K. (1996), Nature 381,21–22.

    Article  PubMed  CAS  Google Scholar 

  5. Galli, S. J. (1997), Int. Arch. Allergy Immunol. 113,14–22.

    Article  PubMed  CAS  Google Scholar 

  6. Malaviya, R., Ikeda, T., Ross, E., and Abraham, S. N. (1996), Nature 381, 77–80.

    Article  PubMed  CAS  Google Scholar 

  7. Echtenacher, B., Hultner, L., and Mannel, D. N. (1995), J. Inflamm. 47,85–89.

    PubMed  CAS  Google Scholar 

  8. Malaviya, R. and Abraham, S. N. (2000), J. Leukoc. Biol. 67,841–846.

    PubMed  CAS  Google Scholar 

  9. Malaviya, R., Navara, C., and Uckun, F. M. (2001), Immunity 15,313–321.

    Article  PubMed  CAS  Google Scholar 

  10. Shin, J. S., Gao, Z., and Abraham, S. N. (2000), Science 289,785–788.

    Article  PubMed  CAS  Google Scholar 

  11. Prodeus, A. P., Zhou, X., Maurer, M., Galli, S. J., and Carroll, M. C. (1997), Nature 390, 172–175.

    Article  PubMed  CAS  Google Scholar 

  12. Maurer, M., Echtenacher, B., Hultner, L., Kollias, G., Mannel, D. N., Langley, K. E., and Galli, S. J. (1998), J. Exp. Med. 188, 2343–2348.

    Article  PubMed  CAS  Google Scholar 

  13. Supajatura, V., Ushio, H., Nakao, A., Okumura, K., Ra, C., and Ogawa, H. (2001), J. Immunol. 167, 2250–2256.

    PubMed  CAS  Google Scholar 

  14. Padawer, J. (1968), Proc. Soc. Exp. Biol. Med. 129, 905–907.

    PubMed  CAS  Google Scholar 

  15. Padawer, J. and Fruhman, G. J. (1968), Experientia 24, 471–472.

    Article  PubMed  CAS  Google Scholar 

  16. Padawer, J. (1971), Lab. Invest. 25, 320–330.

    PubMed  CAS  Google Scholar 

  17. Malaviya, R. and Abraham, S. N. (1998), J. Mol. Med. 76, 617–623.

    Article  PubMed  CAS  Google Scholar 

  18. Arock, M., Ross, E., Lai-Kuen, R., Averlant, G., Gao, Z., and Abraham, S. N. (1998), Infect. Immun. 66, 6030–6034.

    PubMed  CAS  Google Scholar 

  19. Mielcarek, N., Hornquist, E. H., Johansson, B. R., Locht, C., Abraham, S. N., and Holmgren, J. (2001), Cell Microbiol. 3, 181–188.

    Article  PubMed  CAS  Google Scholar 

  20. Leal-Berumen, I., O'Byrne, P., Gupta, A., Richards, C. D., and Marshall, J. S. (1995), J. Immunol. 154, 4759–4767.

    PubMed  CAS  Google Scholar 

  21. Leal-Berumen, I., Snider, D. P., Barajas-Lopez, C., and Marshall, J. S., (1996), J. Immunol. 156, 316–321.

    PubMed  CAS  Google Scholar 

  22. Sher, A., Hein, A., Moser, G., and Caulfield, J. P. (1979), Lab. Invest. 41, 490–499.

    PubMed  CAS  Google Scholar 

  23. Malaviya, R., Twesten, N. J., Ross, E. A., Abraham, S. N., and Pfeifer, J. D. (1996), J. Immunol. 156, 1490–1496.

    PubMed  CAS  Google Scholar 

  24. Malaviya, R., Ross, E. A., MacGregor, J. I., Ikeda, T., Little, J. R., Jakschik, B. A., and Abraham, S. N. (1994), J. Immunol. 152, 1907–1914.

    PubMed  CAS  Google Scholar 

  25. Arock, M., Ross, E., Lai-Kuen, R., Averlant, G., Gao, Z., and Abraham, S. N. (1998), Infect. Immun. 66, 6030–6034.

    PubMed  CAS  Google Scholar 

  26. Malaviya, R. and Abraham, S. N. (2001), Immunological Reviews 179, 16–24.

    Article  PubMed  CAS  Google Scholar 

  27. Malaviya, R., Gao, Z., Thankavel, K., van der Merwe, P. A., and Abraham, S. N. (1999), Proc. Natl. Acad. Sci. USA 96, 8110–8115.

    Article  PubMed  CAS  Google Scholar 

  28. Fenton, M. J. and Golenbock, D. T. (1998), LPS-binding proteins and receptors. J. Leukoc. Biol. 64, 25–32.

    PubMed  CAS  Google Scholar 

  29. Clarkson, N. A., Kaufman, R., Lublin, D. M., Ward, T., Pipkin, P. A., Minor, P. D., et al. (1995), J. Virol. 69, 5497–5501.

    PubMed  CAS  Google Scholar 

  30. Ward, T., Pipkin, P. A., Clarkson, N. A., Stone, D. M., Minor, P. D., and Almond, J. W. (1994), EMBO J. 13, 5070–5074.

    PubMed  CAS  Google Scholar 

  31. Haziot, A., Katz, I., Rong, G. W., Lin, X. Y., Silver, J., and Goyert, S. M. (1997), Scand. J. Immunol. 46, 242–245.

    Article  PubMed  CAS  Google Scholar 

  32. Mayor, S., Rothberg, K. G., and Maxfield, F. R. (1994), Science 264, 1948–1951.

    Article  PubMed  CAS  Google Scholar 

  33. Smart, E. J., Ying, Y. S., Mineo, C., and Anderson, R. G. (1995), Proc. Natl. Acad. Sci. USA 92, 10,104–10,108.

    Article  CAS  Google Scholar 

  34. Bucci, M., Gratton, J. P., Rudic, R. D., Acevedo, L., Roviezzo, F., Cirino, G., and Sessa, W. C. (2000), Nat. Med. 6, 1362–1367.

    Article  PubMed  CAS  Google Scholar 

  35. Smart, E. J., Ying, Y. S., and Anderson, R. G. (1995), J. Cell Biol. 131, 929–938.

    Article  PubMed  CAS  Google Scholar 

  36. Okamoto, T., Schlegel, A., Scherer, P. E., and Lisanti, M. P. (1998), J. Biol. Chem. 273, 5419–5422.

    Article  PubMed  CAS  Google Scholar 

  37. Chapman, H. A., Wei, Y., Simon, D. I., and Waltz, D. A. (1999), Thromb. Haemost. 82, 291–297.

    PubMed  CAS  Google Scholar 

  38. Ju, H., Venema, V. J., Liang, H., Harris, M. B., Zou, R., and Venema, R. C. (2000), Biochem. J. 351, 257–264.

    Article  PubMed  CAS  Google Scholar 

  39. Wooldridge, K. G., Williams, P. H., and Ketley, J. M. (1996), Microb. Pathog. 21, 299–305.

    Article  PubMed  CAS  Google Scholar 

  40. Shin, J. S. and Abraham, S. N. (2001), FEMS Microbiol. Lett. 197, 131–138.

    Article  PubMed  CAS  Google Scholar 

  41. Schilling, J. D., Mulvey, M. A., Vincent, C. D., Lorenz, R. G., and Hultgren, S. J. (2001), J. Immunol. 166, 1148–1155.

    PubMed  CAS  Google Scholar 

  42. Funfstuck, R., Franke, S., Hellberg, M., Ott, U., Knofel, B., Straube, E., et al. (2001), Int. J. Antimicrob. Agents 17, 253–258.

    Article  PubMed  CAS  Google Scholar 

  43. Brauner, A., Soderhall, M., Jacobson, S. H., Lundahl, J., Andersson, U., and Andersson, J. (2001), Clin. Exp. Immunol. 124, 423–428.

    Article  PubMed  CAS  Google Scholar 

  44. Ferrante, A. (1989), Infect. Immun. 57, 2115–2122.

    PubMed  CAS  Google Scholar 

  45. Kenny, P. A., McDonald, P. J., and Finlay-Jones, J. J. (1993), FEMS Immunol. Med. Microbiol. 7, 271–279.

    Article  PubMed  CAS  Google Scholar 

  46. Koenig, A., Yakisan, E., Reuter, M., Huang, M., Sykora, K. W., Corbacioglu, S., and Welte, K. (1994), Blood 83, 2836–2843.

    PubMed  CAS  Google Scholar 

  47. Klimpel, G. R., Langley, K. E., Wypych, J., Abrams, J. S., Chopra, A. K., and Niesel, D. W. (1996), J. Exp. Med. 184, 271–276.

    Article  PubMed  CAS  Google Scholar 

  48. Klimpel, G. R., Chopra, A. K., Langley, K. E., Wypych, J., Annable, C. A., Kaiserlian, D., et al. (1995), J. Exp. Med. 182, 1931–1942.

    Article  PubMed  CAS  Google Scholar 

  49. Malaviya, R., Ross, E., Jakschik, B. A., Abraham, S. N. (1994), J. Clin. Invest. 93, 1645–1653.

    PubMed  CAS  Google Scholar 

  50. Galli, S. J. and Kitamura, Y. (1987), Am. J. Pathol. 127, 191–198.

    PubMed  CAS  Google Scholar 

  51. Nakano, T., Sonoda, T., Hayashi, C., Yamatodani, A., Kanayama, Y., Yamamura, T., et al. (1985), J. Exp. Med. 162, 1025–1043.

    Article  PubMed  CAS  Google Scholar 

  52. Zhang, Y., Ramos, B. F., and Jakschik, B. A. (1992), Science 258, 1957–1959.

    Article  PubMed  CAS  Google Scholar 

  53. Galli, S. J., Tsai, M., Gordon, J. R., Geissler, E. N., and Wershil, B. K. (1992), Ann. NY Acad. Sci. 664, 69–88.

    Article  PubMed  CAS  Google Scholar 

  54. Echtenacher, B., Mannel, D. N., and Hultner, L. (1996), Nature 381, 75–77.

    Article  PubMed  CAS  Google Scholar 

  55. Wershil, B. K., Wang, Z. S., Gordon, J. R., and Galli, S. J. (1991), J. Clin. Invest. 87, 446–453.

    Article  PubMed  CAS  Google Scholar 

  56. Ramos, B. F., Zhang, Y., and Jakschik, B. A. (1994), J. Immunol. 152, 1380–1384.

    PubMed  CAS  Google Scholar 

  57. Malaviya, R. and Jakschik, B. A. (1993), J. Biol. Chem. 268, 4939–4944.

    PubMed  CAS  Google Scholar 

  58. Ramos, B. F., Zhang, Y., Qureshi, R., and Jakschik, B. A. (1991), J. Immunol. 147, 1636–1641.

    PubMed  CAS  Google Scholar 

  59. Bailie, M. B., Standiford, T. J., Laichalk, L. L., Coffey, M. J., Strieter, R., and Peters-Golden, M. (1996), J. Immunol. 157, 5221–5224.

    PubMed  CAS  Google Scholar 

  60. Rosenkranz, A. R., Coxon, A., Maurer, M., Gurish, M. F., Austen, K. F., Friend, D. S., et al. (1998), J. Immunol. 161, 6463–6467.

    PubMed  CAS  Google Scholar 

  61. Suzuki, K., Nakajima, H., Watanabe, N., Kagami, S., Suto, A., Saito, Y., et al. (2000), Blood 96, 2172–2180.

    PubMed  CAS  Google Scholar 

  62. Malaviya, R., Chen, C. L., Navara, C., Liu, X. P., Keenan, M., Waurzyniak, B., and Uckun, F. M. (2000), J. Pharmacol. Exp. Ther. 295, 912–926.

    PubMed  CAS  Google Scholar 

  63. Malaviya, R., Zhu, D., Dibirdik, I., and Uckun, F. M. (1999), J. Biol. Chem. 274, 27,028–27,038.

    Article  CAS  Google Scholar 

  64. Ihle, J. N. and Kerr, I. M. (1995), Trends Genet. 11, 69–74.

    Article  PubMed  CAS  Google Scholar 

  65. Ihle, J. N. (1995), Nature 377, 591–594.

    Article  PubMed  CAS  Google Scholar 

  66. Witthuhn, B. A., Silvennoinen, O., Miura, O., Lai, K. S., Cwik, C., Liu, E. T., and Ihle, J. N. (1994), Nature 370, 153–157.

    Article  PubMed  CAS  Google Scholar 

  67. Marrero, M. B., Schieffer, B., Paxton, W. G., Heerdt, L., Berk, B. C., Delafontaine, P., and Bernstein, K. E. (1995), Nature 375, 247–250.

    Article  PubMed  CAS  Google Scholar 

  68. Dostal, D. E., Hunt, R. A., Kule, C. E., Bhat, G. J., Karoor, V., McWhinney, C. D., and Baker, K. M. (1997), J. Mol. Cell Cardiol. 29, 2893–2902.

    Article  PubMed  CAS  Google Scholar 

  69. Rodriguez-Linares, B. and Watson, S. P. (1994), FEBS Lett. 352, 335–338.

    Article  PubMed  CAS  Google Scholar 

  70. Bhat, G. J., Abraham, S. T., Singer, H. A., and Baker, K. M. (1997), Hypertension 29, 356–360.

    PubMed  CAS  Google Scholar 

  71. Guillet-Deniau, I., Burnol, A. F., and Girard, J. (1997), J. Biol. Chem. 272, 14,825–14,829.

    Article  CAS  Google Scholar 

  72. Peeler, T. C., Conrad, K. M., and Baker, K. M. (1996), Biochem. Biophys. Res. Commun. 221, 62–66.

    Article  PubMed  CAS  Google Scholar 

  73. Malaviya, R. and Uckun, F. M. (1999), Biochem. Biophys. Res. Commun. 257, 807–813.

    Article  PubMed  CAS  Google Scholar 

  74. Nosaka, T., van Deursen, J. M., Tripp, R. A., Thierfelder, W. E., Witthuhn, B. A., McMickle, A. P., et al. (1995), Science 270, 800–802.

    Article  PubMed  CAS  Google Scholar 

  75. Thomis, D. C., Lee, W., and Berg, L. J. (1997), J. Immunol. 159, 4708–4719.

    PubMed  CAS  Google Scholar 

  76. Thomis, D. C., Gurniak, C. B., Tivol, E., Sharpe, A. H., and Berg, L. J. (1995), Science 270, 794–797.

    Article  PubMed  CAS  Google Scholar 

  77. Tsai, M., Wedemeyer, J., Ganiatsas, S., Tam, S. Y., Zon, L. I., and Galli, S. J. (2000), Proc. Natl. Acad. Sci. USA 97, 9186–9190.

    Article  PubMed  CAS  Google Scholar 

  78. Qureshi, S. T., Lariviere, L., Leveque, G., Clermont, S., Moore, K. J., Gros, P., and Malo, D. (1999), J. Exp. Med. 189, 615–625.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Allergy and Inflammatory Diseases, Parker Hughes Institute, 55 113, St. Paul, MN

    Ravi Malaviya & Amara Georges

Authors
  1. Ravi Malaviya
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Amara Georges
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Malaviya, R., Georges, A. Regulation of mast cell-mediated innate immunity during early response to bacterial infection. Clinic Rev Allerg Immunol 22, 189–204 (2002). https://doi.org/10.1385/CRIAI:22:2:189

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1385/CRIAI:22:2:189

Keywords

Search

Navigation