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Clinical and Developmental Immunology
Volume 2011 (2011), Article ID 686597, 9 pages
http://dx.doi.org/10.1155/2011/686597
Review Article

IL-12 and Related Cytokines: Function and Regulatory Implications in Candida albicans Infection

1The School of Dentistry, University of Queensland School of Dentistry, 200 Turbot Street, Brisbane, QLD 4000, Australia
2The National Centre for Adult Stem Cell Research, Eskitis Institute for Cell and Molecular Therapies, Griffith University, Brisbane, QLD 4111, Australia

Received 15 June 2010; Revised 1 August 2010; Accepted 21 September 2010

Academic Editor: David Williams

Copyright © 2011 Robert B. Ashman et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. P. E. Charles, F. Dalle, and F. Dalle, “Candida spp. colonization significance in critically ill medical patients: a prospective study,” Intensive Care Medicine, vol. 31, no. 3, pp. 393–400, 2005. View at Google Scholar · View at Scopus
  2. D. Pittet and R. P. Wenzel, “Nosocomial bloodstream infections: secular trends in rates, mortality, and contribution to total hospital deaths,” Archives of Internal Medicine, vol. 155, no. 11, pp. 1177–1184, 1995. View at Google Scholar · View at Scopus
  3. P. L. Fidel Jr. and G. B. Huffnagle, Eds., Fungal Immunology. From an Organ Perspective, Springer, New York, NY, USA, 2005.
  4. A. O'Garra and K. M. Murphy, “From IL-10 to IL-12: how pathogens and their products stimulate APCs to induce TH1 development,” Nature Immunology, vol. 10, no. 9, pp. 929–932, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  5. B. Oppmann, R. Lesley, and R. Lesley, “Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12,” Immunity, vol. 13, no. 5, pp. 715–725, 2000. View at Google Scholar · View at Scopus
  6. C. Parham, M. Chirica, and M. Chirica, “A receptor for the heterodimeric cytokine IL-23 is composed of IL-12Rβ1 and a novel cytokine receptor subunit, IL-23R,” Journal of Immunology, vol. 168, no. 11, pp. 5699–5708, 2002. View at Google Scholar · View at Scopus
  7. L. E. Harrington, R. D. Hatton, P. R. Mangan, H. Turner, T. L. Murphy, K. M. Murphy, and C. T. Weaver, “Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages,” Nature Immunology, vol. 6, no. 11, pp. 1123–1132, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  8. Z. Y. Tan, K. W. Bealgey, Y. Fang, Y. M. Gong, and S. Bao, “Interleukin-23: immunological roles and clinical implications,” International Journal of Biochemistry and Cell Biology, vol. 41, no. 4, pp. 733–735, 2009. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  9. J. L. Langowski, X. Zhang, and X. Zhang, “IL-23 promotes tumour incidence and growth,” Nature, vol. 442, no. 7101, pp. 461–465, 2006. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  10. L. de Repentigny, “Animal models in the analysis of Candida host-pathogen interactions,” Current Opinion in Microbiology, vol. 7, no. 4, pp. 324–329, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  11. R. B. Ashman, C. S. Farah, S. Wanasaengsakul, Y. Hu, G. Pang, and R. L. Clancy, “Innate versus adaptive immunity in Candida albicans infection,” Immunology and Cell Biology, vol. 82, no. 2, pp. 196–204, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  12. L. Romani, “Immunity to Candida albicans: Th1, Th2 cells and beyond,” Current Opinion in Microbiology, vol. 2, no. 4, pp. 363–367, 1999. View at Publisher · View at Google Scholar · View at Scopus
  13. R. F. Hector, J. E. Domer, and E. W. Carrow, “Immune responses to Candida albicans in genetically distinct mice,” Infection and Immunity, vol. 38, no. 3, pp. 1020–1028, 1982. View at Google Scholar · View at Scopus
  14. F. L. Lyon, R. F. Hector, and J. E. Domer, “Innate and acquired immune responses against Candida albicans in congenic B10.D2 mice with deficiency of the C5 complement component,” Journal of Medical and Veterinary Mycology, vol. 24, no. 5, pp. 359–367, 1986. View at Google Scholar · View at Scopus
  15. R. B. Ashman, J. M. Papadimitriou, A. Fulurija, K. E. Drysdale, C. S. Farah, O. Naidoo, and T. Gotjamanos, “Role of complement C5 and T lymphocytes in pathogenesis of disseminated and mucosal candidiasis in susceptible DBA/2 mice,” Microbial Pathogenesis, vol. 34, no. 2, pp. 103–113, 2003. View at Publisher · View at Google Scholar · View at Scopus
  16. J. E. Cutler, “Acute systemic candidiasis in normal and congenitally thymic deficient (nude) mice,” RES Journal of the Reticuloendothelial Society, vol. 19, no. 2, pp. 121–124, 1976. View at Google Scholar · View at Scopus
  17. S. Mahanty, R. A. Greenfield, W. A. Joyce, and P. W. Kincade, “Inoculation candidiasis in a murine model of severe combined immunodeficiency syndrome,” Infection and Immunity, vol. 56, no. 12, pp. 3162–3166, 1988. View at Google Scholar · View at Scopus
  18. J. Jones-Carson, A. Vazquez-Torres, T. Warner, and E. Balish, “Disparate requirement for T cells in resistance to mucosal and acute systemic candidiasis,” Infection and Immunity, vol. 68, no. 4, pp. 2363–2365, 2000. View at Publisher · View at Google Scholar · View at Scopus
  19. H. S. Kim, E. H. Choi, and E. H. Choi, “Expression of genes encoding innate host defense molecules in normal human monocytes in response to Candida albicans,” Infection and Immunity, vol. 73, no. 6, pp. 3714–3724, 2005. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  20. P. N. Lalli, M. G. Strainic, F. Lin, M. E. Medof, and P. S. Heeger, “Decay accelerating factor can control T cell differentiation into IFN-γ-producing effector cells via regulating local C5a-induced IL-12 production,” Journal of Immunology, vol. 179, no. 9, pp. 5793–5802, 2007. View at Google Scholar · View at Scopus
  21. L. Romani, A. Mencacci, and A. Mencacci, “Interleukin-12 but not interferon-γ production correlates with induction of T helper type-1 phenotype in murine candidiasis,” European Journal of Immunology, vol. 24, no. 4, pp. 909–915, 1994. View at Google Scholar · View at Scopus
  22. L. Romani, E. Cenci, A. Mencacci, R. Spaccapelo, U. Grohmann, P. Puccetti, and F. Bistoni, “Gamma interferon modifies CD4+ subset expression in murine candidiasis,” Infection and Immunity, vol. 60, no. 11, pp. 4950–4952, 1992. View at Google Scholar · View at Scopus
  23. L. Romani, A. Mencacci, U. Grohmann, S. Mocci, P. Mosci, P. Puccetti, and F. Bistoni, “Neutralizing antibody to interleukin 4 induces systemic protection and T helper type 1-associated immunity in murine candidiasis,” Journal of Experimental Medicine, vol. 176, no. 1, pp. 19–25, 1992. View at Publisher · View at Google Scholar · View at Scopus
  24. L. Romani, A. Mencacci, and A. Mencacci, “IL-12 is both required and prognostic in vivo for T helper type 1 differentiation in murine candidiasis,” Journal of Immunology, vol. 153, no. 11, pp. 5167–5175, 1994. View at Google Scholar · View at Scopus
  25. A. Mencacci, E. Cenci, R. Spaccapelo, L. Tonnetti, L. Romani, P. Puccetti, and F. Bistoni, “Rationale for cytokine and anti-cytokine therapy of Candida albicans infection,” Journal de Mycologie Medicale, vol. 5, no. 1, pp. 25–30, 1995. View at Google Scholar · View at Scopus
  26. E. Cenci, A. Mencacci, and A. Mencacci, “IFN-γ is required for IL-12 responsiveness in mice with Candida albicans infection,” Journal of Immunology, vol. 161, no. 7, pp. 3543–3550, 1998. View at Google Scholar · View at Scopus
  27. A. Mencacci, G. Del Sero, and G. Del Sero, “Endogenous interleukin 4 is required for development of protective CD4+ T helper type 1 cell responses to Candida albicans,” Journal of Experimental Medicine, vol. 187, no. 3, pp. 307–317, 1998. View at Publisher · View at Google Scholar · View at Scopus
  28. R. B. Ashman, “Genetic determination of susceptibility and resistance in the pathogenesis of Candida albicans infection,” FEMS Immunology and Medical Microbiology, vol. 19, no. 3, pp. 183–189, 1997. View at Publisher · View at Google Scholar · View at Scopus
  29. R. B. Ashman, “Murine candidiasis: cell-mediated immune responses correlate directly with susceptibility and resistance to infection,” Immunology and Cell Biology, vol. 68, no. 1, pp. 15–20, 1990. View at Google Scholar · View at Scopus
  30. R. B. Ashman, A. Fulurija, and J. M. Papadimitriou, “Both CD4+ and CD8+ lymphocytes reduce the severity of tissue lesions in murine systemic candidiasis, and CD4+ cells also demonstrate strain-specific immunopathological effects,” Microbiology, vol. 145, no. 7, pp. 1631–1640, 1999. View at Google Scholar · View at Scopus
  31. L. M. Lavigne, L. R. Schopf, C. L. Chung, R. Maylor, and J. P. Sypek, “The role of recombinant murine IL-12 and IFN-γ in the pathogenesis of a murine systemic Candida albicans infection,” Journal of Immunology, vol. 160, no. 1, pp. 284–292, 1998. View at Google Scholar · View at Scopus
  32. Q. Qian and J. E. Cutler, “Gamma interferon is not essential in host defense against disseminated candidiasis in mice,” Infection and Immunity, vol. 65, no. 5, pp. 1748–1753, 1997. View at Google Scholar · View at Scopus
  33. E. Balish, R. D. Wagner, A. Vázquez-Torres, C. Pierson, and T. Warner, “Candidiasis in interferon-γ knockout (IFN-γ(-/-)) mice,” Journal of Infectious Diseases, vol. 178, no. 2, pp. 478–487, 1998. View at Google Scholar · View at Scopus
  34. R. Káposzta, P. Tree, L. Maródi, and S. Gordon, “Characteristics of invasive candidiasis in gamma interferon- and interleukin-4-deficient mice: role of macrophages in host defense against Candida albicans,” Infection and Immunity, vol. 66, no. 4, pp. 1708–1717, 1998. View at Google Scholar · View at Scopus
  35. M. G. Netea, A. G. Vonk, and A. G. Vonk, “Differential role of IL-18 and IL-12 in the host defense against disseminated Candida albicans infection,” European Journal of Immunology, vol. 33, no. 12, pp. 3409–3417, 2003. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  36. C. S. Farah, Y. Hu, S. Riminton, and R. B. Ashman, “Distinct roles for interleukin-12p40 and tumour necrosis factor in resistance to oral candidiasis defined by gene-targeting,” Oral Microbiology and Immunology, vol. 21, no. 4, pp. 252–255, 2006. View at Publisher · View at Google Scholar · View at PubMed
  37. A. Mencacci, E. Cenci, and E. Cenci, “IL-10 is required for development of protective Th1 responses in IL-12-deficient mice upon Candida albicans infection,” Journal of Immunology, vol. 161, no. 11, pp. 6228–6237, 1998. View at Google Scholar
  38. H. R. Conti, F. Shen, and F. Shen, “Th17 cells and IL-17 receptor signaling are essential for mucosal host defense against oral candidiasis,” Journal of Experimental Medicine, vol. 206, no. 2, pp. 299–311, 2009. View at Publisher · View at Google Scholar · View at PubMed
  39. J. Brieland, D. Essig, and D. Essig, “Comparison of pathogenesis and host immune responses to Candida glabrata and Candida albicans in systemically infected immunocompetent mice,” Infection and Immunity, vol. 69, no. 8, pp. 5046–5055, 2001. View at Publisher · View at Google Scholar · View at PubMed
  40. S. Ito, J. Pedras-Vasconcelos, and D. M. Klinman, “CpG oligodeoxynucleotides increase the susceptibility of normal mice to infection by Candida albicans,” Infection and Immunity, vol. 73, no. 9, pp. 6154–6156, 2005. View at Publisher · View at Google Scholar · View at PubMed
  41. J.-H. Choi, H.-M. Ko, S. J. Park, K.-J. Kim, S.-H. Kim, and S.-Y. Im, “CpG oligodeoxynucleotides protect mice from lethal challenge with Candida albicans via a pathway involving tumor necrosis factor-α-dependent interleukin-12 induction,” FEMS Immunology and Medical Microbiology, vol. 51, no. 1, pp. 155–162, 2007. View at Publisher · View at Google Scholar · View at PubMed
  42. A. Mencacci, E. Cenci, and E. Cenci, “Defective co-stimulation and impaired Th1 development in tumor necrosis factor/lymphotoxin-α double-deficient mice infected with Candida albicans,” International Immunology, vol. 10, no. 1, pp. 37–48, 1998. View at Publisher · View at Google Scholar
  43. C. F. d'Ostiani, G. D. Del Sero, and G. D. Del Sero, “Dendritic cells discriminate between yeasts and hyphae of the fungus Candida albicans: implications for initiation of T helper cell immunity in vitro and in vivo,” Journal of Experimental Medicine, vol. 191, no. 10, pp. 1661–1673, 2000. View at Publisher · View at Google Scholar
  44. A. Torosantucci, G. Romagnoli, and G. Romagnoli, “Candida albicans yeast and germ tube forms interfere differently with human monocyte differentiation into dendritic cells: a novel dimorphism-dependent mechanism to escape the host's immune response,” Infection and Immunity, vol. 72, no. 2, pp. 833–843, 2004. View at Publisher · View at Google Scholar
  45. O. Kurzai, C. Schmitt, E.-B. Bröcker, M. Frosch, and A. Kolb-Mäurer, “Polymorphism of Candida albicans is a major factor in the interaction with human dendritic cells,” International Journal of Medical Microbiology, vol. 295, no. 2, pp. 121–127, 2005. View at Publisher · View at Google Scholar
  46. T. Zelante, A. De Luca, and A. De Luca, “IL-23 and the Th17 pathway promote inflammation and impair antifungal immune resistance,” European Journal of Immunology, vol. 37, no. 10, pp. 2695–2706, 2007. View at Publisher · View at Google Scholar · View at PubMed
  47. W. Huang, L. Na, P. L. Fidel, and P. Schwarzenberger, “Requirement of interleukin-17A for systemic anti-Candida albicans host defense in mice,” Journal of Infectious Diseases, vol. 190, no. 3, pp. 624–631, 2004. View at Publisher · View at Google Scholar · View at PubMed
  48. L. Rizzetto, M. Kuka, and M. Kuka, “Differential IL-17 production and mannan recognition contribute to fungal pathogenicity and commensalism,” Journal of Immunology, vol. 184, no. 8, pp. 4258–4268, 2010. View at Publisher · View at Google Scholar · View at PubMed
  49. S. LeibundGut-Landmann, O. Groß, and O. Groß, “Syk- and CARD9-dependent coupling of innate immunity to the induction of T helper cells that produce interleukin 17,” Nature Immunology, vol. 8, no. 6, pp. 630–638, 2007. View at Publisher · View at Google Scholar · View at PubMed
  50. S. Saijo, S. Ikeda, and S. Ikeda, “Dectin-2 recognition of α-mannans and induction of Th17 cell differentiation is essential for host defense against Candida albicans,” Immunity, vol. 32, no. 5, pp. 681–691, 2010. View at Publisher · View at Google Scholar · View at PubMed
  51. L. Liu, K. Kang, M. Takahara, K. D. Cooper, and M. A. Ghannoum, “Hyphae and yeasts of Candida albicans differentially regulate interleukin-12 production by human blood monocytes: inhibitory role of C. albicans germination,” Infection and Immunity, vol. 69, no. 7, pp. 4695–4697, 2001. View at Publisher · View at Google Scholar · View at PubMed
  52. N. Tang, L. Liu, and L. Liu, “Inhibition of monocytic interleukin-12 production by Candida albicans via selective activation of ERK mitogen-activated protein kinase,” Infection and Immunity, vol. 72, no. 5, pp. 2513–2520, 2004. View at Publisher · View at Google Scholar
  53. C. S. Farah, S. Elahi, and S. Elahi, “Primary role for CD4+ T lymphocytes in recovery from oropharyngeal candidiasis,” Infection and Immunity, vol. 70, no. 2, pp. 724–731, 2002. View at Publisher · View at Google Scholar
  54. E. Balish, H. Filutowicz, and T. D. Oberley, “Correlates of cell-mediated immunity in Candida albicans-colonized gnotobiotic mice,” Infection and Immunity, vol. 58, no. 1, pp. 107–113, 1990. View at Google Scholar
  55. M. T. Cantorna and E. Balish, “Role of CD4+ lymphocytes in resistance to mucosal candidiasis,” Infection and Immunity, vol. 59, no. 7, pp. 2447–2455, 1991. View at Google Scholar
  56. R. Narayanan, W. A. Joyce, and R. A. Greenfield, “Gastrointestinal candidiasis in a murine model of severe combined immunodeficiency syndrome,” Infection and Immunity, vol. 59, no. 6, pp. 2116–2119, 1991. View at Google Scholar
  57. J. Jones-Carson, A. Vazquez-Torres, H. C. van der Heyde, T. Warner, R. D. Wagner, and E. Balish, “γδ T cell-induced nitric oxide production enhances resistance to mucosal candidiasis,” Nature Medicine, vol. 1, no. 6, pp. 552–557, 1995. View at Google Scholar
  58. L. Romani, A. Mencacci, E. Cenci, R. Spaccapelo, P. Mosci, P. Puccetti, and F. Bistoni, “CD4+ subset expression in murine candidiasis: Th responses correlate directly with genetically determined susceptibility or vaccine-induced resistance,” Journal of Immunology, vol. 150, no. 3, pp. 925–931, 1993. View at Google Scholar
  59. E. Cenci, A. Mencacci, and A. Mencacci, “T helper cell type 1 (Th1)- and Th2-like responses are present in mice with gastric candidiasis but protective immunity is associated with Th1 development,” Journal of Infectious Diseases, vol. 171, no. 5, pp. 1279–1288, 1995. View at Google Scholar
  60. F. Bistoni, E. Cenci, A. Mencacci, E. Schiaffella, P. Mosci, P. Puccetti, and L. Romani, “Mucosal and systemic T helper cell function after intragastric colonization of adult mice with Candida albicans,” Journal of Infectious Diseases, vol. 168, no. 6, pp. 1449–1457, 1993. View at Google Scholar
  61. P. Puccetti, A. Mencacci, and A. Mencacci, “Cure of murine candidiasis by recombinant soluble interleukin-4 receptor,” Journal of Infectious Diseases, vol. 169, no. 6, pp. 1325–1331, 1994. View at Google Scholar
  62. G. Del Sero, A. Mencacci, and A. Mencacci, “Antifungal type 1 responses are upregulated in IL-10-deficient mice,” Microbes and Infection, vol. 1, no. 14, pp. 1169–1180, 1999. View at Publisher · View at Google Scholar
  63. A. Vazquez-Torres, J. Jones-Carson, R. D. Wagner, T. Warner, and E. Balish, “Early resistance of interleukin-10 knockout mice to acute systemic candidiasis,” Infection and Immunity, vol. 67, no. 2, pp. 670–674, 1999. View at Google Scholar
  64. D. A. Schofield, C. Westwater, and E. Balish, “Divergent chemokine, cytokine and β-defensin responses to gastric candidiasis in immunocompetent C57BL/6 and BALB/c mice,” Journal of Medical Microbiology, vol. 54, no. 1, pp. 87–92, 2005. View at Publisher · View at Google Scholar
  65. J. Chakir, L. Cote, C. Coulombe, and N. Deslauriers, “Differential pattern of infection and immune response during experimental oral candidiasis in BALB/c and DBA/2 (H-2d) mice,” Oral Microbiology and Immunology, vol. 9, no. 2, pp. 88–94, 1994. View at Google Scholar
  66. N. Deslauriers, C. Coulombe, B. Carre, and J.-P. Goulet, “Topical application of a corticosteroid destabilizes the host-parasite relationship in an experimental model of the oral carrier state of Candida albicans,” FEMS Immunology and Medical Microbiology, vol. 11, no. 1, pp. 45–56, 1995. View at Publisher · View at Google Scholar
  67. S. Elahi, G. Pang, R. Clancy, and R. B. Ashman, “Cellular and cytokine correlates of mucosal protection in murine model of oral candidiasis,” Infection and Immunity, vol. 68, no. 10, pp. 5771–5777, 2000. View at Publisher · View at Google Scholar
  68. S. Elahi, G. Pang, R. B. Ashman, and R. Clancy, “Nitric oxide-enhanced resistance to oral candidiasis,” Immunology, vol. 104, no. 4, pp. 447–454, 2001. View at Publisher · View at Google Scholar
  69. C. S. Farah, S. Elahi, G. Pang, T. Gotjamanos, G. J. Seymour, R. L. Clancy, and R. B. Ashman, “T cells augment monocyte and neutrophil function in host resistance against oropharyngeal candidiasis,” Infection and Immunity, vol. 69, no. 10, pp. 6110–6118, 2001. View at Publisher · View at Google Scholar · View at PubMed
  70. C. S. Farah, T. Gotjamanos, G. J. Seymour, and R. B. Ashman, “Cytokines in the oral mucosa of mice infected with Candida albicans,” Oral Microbiology and Immunology, vol. 17, no. 6, pp. 375–378, 2002. View at Publisher · View at Google Scholar · View at Scopus
  71. J. M. Saunus, A. Kazoullis, and C. S. Farah, “Cellular and molecular mechanisms of resistance to oral Candida albicans infections,” Frontiers in Bioscience, vol. 13, pp. 5345–5358, 2008. View at Google Scholar · View at Scopus
  72. H. Birkedal-Hansen, W. G. I. Moore, M. K. Bodden, L. J. Windsor, B. Birkedal-Hansen, A. DeCarlo, and J. A. Engler, “Matrix metalloproteinases: a review,” Critical Reviews in Oral Biology and Medicine, vol. 4, no. 2, pp. 197–250, 1993. View at Google Scholar · View at Scopus
  73. I. Claveau, Y. Mostefaoui, and M. Rouabhia, “Basement membrane protein and matrix metalloproteinase deregulation in engineered human oral mucosa following infection with Candida albicans,” Matrix Biology, vol. 23, no. 7, pp. 477–486, 2004. View at Publisher · View at Google Scholar · View at PubMed · View at Scopus
  74. M. Abraham, S. Shapiro, N. Lahat, and A. Miller, “The role of IL-18 and IL-12 in the modulation of matrix metalloproteinases and their tissue inhibitors in monocytic cells,” International Immunology, vol. 14, no. 12, pp. 1449–1457, 2002. View at Publisher · View at Google Scholar · View at Scopus
  75. S. Mitola, M. Strasly, M. Prato, P. Ghia, and F. Bussolino, “IL-12 regulates an endothelial cell-lymphocyte network: effect on metalloproteinase-9 production,” Journal of Immunology, vol. 171, no. 7, pp. 3725–3733, 2003. View at Google Scholar · View at Scopus