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Complement Attack against Aspergillus and Corresponding Evasion Mechanisms

DOI: 10.1155/2012/463794

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Abstract:

Invasive aspergillosis shows a high mortality rate particularly in immunocompromised patients. Perpetually increasing numbers of affected patients highlight the importance of a clearer understanding of interactions between innate immunity and fungi. Innate immunity is considered to be the most significant host defence against invasive fungal infections. Complement represents a crucial part of this first line defence and comprises direct effects against invading pathogens as well as bridging functions to other parts of the immune network. However, despite the potency of complement to attack foreign pathogens, the prevalence of invasive fungal infections is increasing. Two possible reasons may explain that phenomenon: First, complement activation might be insufficient for an effective antifungal defence in risk patients (due to, e.g., low complement levels, poor recognition of fungal surface, or missing interplay with other immune elements in immunocompromised patients). On the other hand, fungi may have developed evasion strategies to avoid recognition and/or eradication by complement. In this review, we summarize the most important interactions between Aspergillus and the complement system. We describe the various ways of complement activation by Aspergillus and the antifungal effects of the system, and also show proven and probable mechanisms of Aspergillus for complement evasion. 1. Aspergillus Evokes Invasive Infections in Immunocompromised Individuals Aspergillus species are ascomycetes that are classified in the form subdivision Deuteromycotina, as many of them do not show a sexual reproductive phase [1]. Generally, they are common ubiquitous saprophytes in soil and on dead organic substrates. Being classic opportunistic pathogens, invasive infections by Aspergillus species almost exclusively develop in immunocompromised patients, while localized infections and allergic bronchopulmonary aspergillosis occur in individuals without immunosuppression. Generally, the species Aspergillus fumigatus represents the most common inducer of invasive and allergic manifestations, followed by A. terreus, A. flavus, and A. niger [1, 2]. Invasive aspergillosis (IA) considerably contributes to the morbidity and mortality among immunocompromised individuals, including patients with haematological malignancies, recipients of haematological stem cell and solid organ transplants, AIDS patients, and patients treated with immunosuppressive regimens due to autoimmune diseases [3]. The most important single risk factor is prolonged and profound neutropenia (<500

References

[1]  D. W. Denning, “Invasive aspergillosis,” Clinical Infectious Diseases, vol. 26, no. 4, pp. 781–803, 1998.
[2]  C. Speth, G. Rambach, R. Würzner, and C. Lass-Fl?rl, “Complement and fungal pathogens: an update,” Mycoses, vol. 51, no. 6, pp. 477–496, 2008.
[3]  M. Ellis, “Invasive fungal infections: evolving challenges for diagnosis and therapeutics,” Molecular Immunology, vol. 38, no. 12-13, pp. 947–957, 2002.
[4]  M. J. G. T. Rüping, J. J. Vehreschild, and O. A. Cornely, “Patients at high risk of invasive fungal infections: when and how to treat,” Drugs, vol. 68, no. 14, pp. 1941–1962, 2008.
[5]  V. Balloy, M. Huerre, J. P. Latgé, and M. Chignard, “Differences in patterns of infection and inflammation for corticosteroid treatment and chemotherapy in experimental invasive pulmonary aspergillosis,” Infection and Immunity, vol. 73, no. 1, pp. 494–503, 2005.
[6]  M. Ruhnke, G. Kofla, K. Otto, and S. Schwartz, “CNS aspergillosis: recognition, diagnosis and management,” CNS Drugs, vol. 21, no. 8, pp. 659–676, 2007.
[7]  D. W. Denning, “Invasive aspergillosis in AIDS-an overview,” Journal of Medical Mycology, vol. 2, supplement 1, pp. 34–41, 1998.
[8]  A. N. Malani and C. A. Kauffman, “Changing epidemiology of rare mould infections: implications for therapy,” Drugs, vol. 67, no. 13, pp. 1803–1812, 2007.
[9]  M. A. Pfaller, P. G. Pappas, and J. R. Wingard, “Invasive fungal pathogens: current epidemiological trends,” Clinical Infectious Diseases, vol. 43, supplement 1, pp. S3–S14, 2006.
[10]  H. F. Tsai, R. G. Washburn, Y. C. Chang, and K. J. Kwon-Chung, “Aspergillus fumigatus arp1 modulates conidial pigmentation and complement deposition,” Molecular Microbiology, vol. 26, no. 1, pp. 175–183, 1997.
[11]  H. F. Tsai, Y. C. Chang, R. G. Washburn, M. H. Wheeler, and K. J. Kwon-Chung, “The developmentally regulated alb1 gene of Aspergillus fumigatus: its role in modulation of conidial morphology and virulence,” Journal of Bacteriology, vol. 180, no. 12, pp. 3031–3038, 1998.
[12]  A. A. Brakhage, S. Bruns, A. Thywissen, P. F. Zipfel, and J. Behnsen, “Interaction of phagocytes with filamentous fungi,” Current Opinion in Microbiology, vol. 13, no. 4, pp. 409–415, 2010.
[13]  A. Thywissen, T. Heinekamp, H. M. Dahse, et al., “Conidial dihydroxynaphthalene melanin of the human pathogenic fungus Aspergillus fumigatus interferes with the host endocytosis pathway,” Frontiers in Microbiology, vol. 2, p. 96, 2011.
[14]  B. Jahn, F. Boukhallouk, J. Lotz, K. Langfelder, G. Wanner, and A. A. Brakhage, “Interaction of human phagocytes with pigmentless Aspergillus conidia,” Infection and Immunity, vol. 68, no. 6, pp. 3736–3739, 2000.
[15]  J. Behnsen, F. Lessing, S. Schindler et al., “Secreted Aspergillus fumigatus protease Alp1 degrades human complement proteins C3, C4, and C5,” Infection and Immunity, vol. 78, no. 8, pp. 3585–3594, 2010.
[16]  M. Monod, S. Capoccia, B. Léchenne, C. Zaugg, M. Holdom, and O. Jousson, “Secreted proteases from pathogenic fungi,” International Journal of Medical Microbiology, vol. 292, no. 5-6, pp. 405–419, 2002.
[17]  G. Rambach, D. Dum, I. Mohsenipour et al., “Secretion of a fungal protease represents a complement evasion mechanism in cerebral aspergillosis,” Molecular Immunology, vol. 47, no. 7-8, pp. 1438–1449, 2010.
[18]  S. Spikes, R. Xu, C. K. Nguyen et al., “Gliotoxin production in Aspergillus fumigatus contributes to host-specific differences in virulence,” Journal of Infectious Diseases, vol. 197, no. 3, pp. 479–486, 2008.
[19]  P. Sutton, N. R. Newcombe, P. Waring, and A. Mullbacher, “In vivo immunosuppressive activity of gliotoxin, a metabolite produced by human pathogenic fungi,” Infection and Immunity, vol. 62, no. 4, pp. 1192–1198, 1994.
[20]  C. Speth, C. Kupfahl, K. Pfaller et al., “Gliotoxin as putative virulence factor and immunotherapeutic target in a cell culture model of cerebral aspergillosis,” Molecular Immunology, vol. 48, no. 15-16, pp. 2122–2129, 2011.
[21]  J. Sturtevant and J. P. Latge, “Participation of complement in the phagocytosis of the conidia of Aspergillus fumigatus by human polymorphonuclear cells,” Journal of Infectious Diseases, vol. 166, no. 3, pp. 580–586, 1992.
[22]  M. Hasenberg, J. Behnsen, S. Krappmann, A. Brakhage, and M. Gunzer, “Phagocyte responses towards Aspergillus fumigatus,” International Journal of Medical Microbiology, vol. 301, no. 5, pp. 436–444, 2011.
[23]  W. W. Hope, T. J. Walsh, and D. W. Denning, “The invasive and saprophytic syndromes due to Aspergillus spp,” Medical Mycology, vol. 43, pp. S207–S238, 2005.
[24]  B. K. Kleinschmidt-DeMasters, “Central nervous system aspergillosis: a 20-year retrospective series,” Human Pathology, vol. 33, no. 1, pp. 116–124, 2002.
[25]  T. J. Walsh, D. B. Hier, and L. R. Caplan, “Fungal infections of the central nervous system: comparative analysis of risk factors and clinical signs in 57 patients,” Neurology, vol. 35, no. 11, pp. 1654–1657, 1985.
[26]  S. J. Lin, J. Schranz, and S. M. Teutsch, “Aspergillosis case-fatality rate: systematic review of the literature,” Clinical Infectious Diseases, vol. 32, no. 3, pp. 358–366, 2001.
[27]  C. Speth, W. Prodinger, R. Wurzner, H. Stoiber, and M. P. Dierich, “Complement,” in Fundamental Immunology, W. E. Paul, Ed., pp. 1047–1078, Lippincott Williams & Wilkins, Philadelphia, Pa, USA, 2008.
[28]  M. G. Strainic, J. Liu, D. Huang et al., “Locally produced complement fragments C5a and C3a provide both costimulatory and survival signals to naive CD4+ T cells,” Immunity, vol. 28, no. 3, pp. 425–435, 2008.
[29]  J. Lu, X. Wu, and B. K. Teh, “The regulatory roles of C1q,” Immunobiology, vol. 212, no. 4-5, pp. 245–252, 2007.
[30]  F. R. Toapanta and T. M. Ross, “Complement-mediated activation of the adaptive immune responses: role of C3d in linking the innate and adaptive immunity,” Immunologic Research, vol. 36, no. 1–3, pp. 197–210, 2006.
[31]  P. Gasque, “Complement: a unique innate immune sensor for danger signals,” Molecular Immunology, vol. 41, no. 11, pp. 1089–1098, 2004.
[32]  F. Moalli, A. Doni, L. Deban et al., “Role of complement and Fcγ receptors in the protective activity of the long pentraxin PTX3 against Aspergillus fumigatus,” Blood, vol. 116, no. 24, pp. 5170–5180, 2010.
[33]  R. C. Duncan, L. C. Wijeyewickrema, and R. N. Pike, “The initiating proteases of the complement system: controlling the cleavage,” Biochimie, vol. 90, no. 2, pp. 387–395, 2008.
[34]  Y. J. Ma, A. Doni, T. Hummelsh?j et al., “Synergy between ficolin-2 and pentraxin 3 boosts innate immune recognition and complement deposition,” Journal of Biological Chemistry, vol. 284, no. 41, pp. 28263–28275, 2009.
[35]  C. Dumestre-Pérard, B. Lamy, D. Aldebert et al., “Aspergillus conidia activate the complement by the mannan-binding lectin C2 bypass mechanism,” Journal of Immunology, vol. 181, no. 10, pp. 7100–7105, 2008.
[36]  S. D. Fleming and G. C. Tsokos, “Complement, natural antibodies, autoantibodies and tissue injury,” Autoimmunity Reviews, vol. 5, no. 2, pp. 89–92, 2006.
[37]  J. Van Beek, K. Elward, and P. Gasque, “Activation of complement in the central nervous system: roles in neurodegeneration and neuroprotection,” Annals of the New York Academy of Sciences, vol. 992, pp. 56–71, 2003.
[38]  G. Raivich, M. Bohatschek, C. U. A. Kloss, A. Werner, L. L. Jones, and G. W. Kreutzberg, “Neuroglial activation repertoire in the injured brain: graded response, molecular mechanisms and cues to physiological function,” Brain Research Reviews, vol. 30, no. 1, pp. 77–105, 1999.
[39]  Z. Chen, S. B. Koralov, and G. Kelsoe, “Regulation of humoral immune responses by CD21/CD35,” Immunological Reviews, vol. 176, pp. 194–204, 2000.
[40]  J. K?hl, “Anaphylatoxins and infectious and non-infectious inflammatory diseases,” Molecular Immunology, vol. 38, no. 2-3, pp. 175–187, 2001.
[41]  M. M. Markiewski and J. D. Lambris, “The role of complement in inflammatory diseases from behind the scenes into the spotlight,” American Journal of Pathology, vol. 171, no. 3, pp. 715–727, 2007.
[42]  J. A. Ember and T. E. Hugli, “Complement factors and their receptors,” Immunopharmacology, vol. 38, no. 1-2, pp. 3–15, 1997.
[43]  D. D. Kim and W. C. Song, “Membrane complement regulatory proteins,” Clinical Immunology, vol. 118, no. 2-3, pp. 127–136, 2006.
[44]  J. M. Thurman and B. Renner, “Dynamic control of the complement system by modulated expression of regulatory proteins,” Laboratory Investigation, vol. 91, no. 1, pp. 4–11, 2011.
[45]  M. V. Carroll and R. B. Sim, “Complement in health and disease,” Advanced Drug Delivery Reviews, vol. 63, no. 12, pp. 965–975, 2011.
[46]  T. R. Kozel, M. A. Wilson, T. P. Farrell, and S. M. Levitz, “Activation of C3 and binding to Aspergillus fumigatus conidia and hyphae,” Infection and Immunity, vol. 57, no. 11, pp. 3412–3417, 1989.
[47]  J. E. Sturtevant and J. P. Latge, “Interactions between conidia of Aspergillus fumigatus and human complement component C3,” Infection and Immunity, vol. 60, no. 5, pp. 1913–1918, 1992.
[48]  O. Neth, D. L. Jack, A. W. Dodds, H. Holzel, N. J. Klein, and M. W. Turner, “Mannose-binding lectin binds to a range of clinically relevant microorganisms and promotes complement deposition,” Infection and Immunity, vol. 68, no. 2, pp. 688–693, 2000.
[49]  W. K. Eddie Ip, K. Takahashi, R. Alan Ezekowitz, and L. M. Stuart, “Mannose-binding lectin and innate immunity,” Immunological Reviews, vol. 230, no. 1, pp. 9–21, 2009.
[50]  E. C. Van Asbeck, A. I. M. Hoepelman, J. Scharringa, B. L. Herpers, and J. Verhoef, “Mannose binding lectin plays a crucial role in innate immunity against yeast by enhanced complement activation and enhanced uptake of polymorphonuclear cells,” BMC Microbiology, vol. 8, article 229, 2008.
[51]  M. W. Turner, “The role of mannose-binding lectin in health and disease,” Molecular Immunology, vol. 40, no. 7, pp. 423–429, 2003.
[52]  D. J. Crosdale, K. V. Poulton, W. E. Ollier, W. Thomson, and D. W. Denning, “Mannose-binding lectin gene polymorphisms as a susceptibility factor for chronic necrotizing pulmonary aspergillosis,” Journal of Infectious Diseases, vol. 184, no. 5, pp. 653–656, 2001.
[53]  S. Kaur, V. K. Gupta, S. Thiel, P. U. Sarma, and T. Madan, “Protective role of mannan-binding lectin in a murine model of invasive pulmonary aspergillosis,” Clinical and Experimental Immunology, vol. 148, no. 2, pp. 382–389, 2007.
[54]  R. F. Hector, E. Yee, and M. S. Collins, “Use of DBA/2N mice in models of systemic candidiasis and pulmonary and systemic aspergillosis,” Infection and Immunity, vol. 58, no. 5, pp. 1476–1478, 1990.
[55]  S. Henwick, S. V. Hetherington, and C. C. Patrick, “Complement binding to Aspergillus conidia correlates with pathogenicity,” Journal of Laboratory and Clinical Medicine, vol. 122, no. 1, pp. 27–35, 1993.
[56]  T. R. Kozel, “Activation of the complement system by pathogenic fungi,” Clinical Microbiology Reviews, vol. 9, no. 1, pp. 34–46, 1996.
[57]  J. Sturtevant and J. P. Latge, “Participation of complement in the phagocytosis of the conidia of Aspergillus fumigatus by human polymorphonuclear cells,” Journal of Infectious Diseases, vol. 166, no. 3, pp. 580–586, 1992.
[58]  G. Rambach, M. Hagleitner, I. Mohsenipour et al., “Antifungal activity of the local complement system in cerebral aspergillosis,” Microbes and Infection, vol. 7, no. 13, pp. 1285–1295, 2005.
[59]  A. R. Waldorf and R. D. Diamond, “Neutrophil chemotactic responses induced by fresh and swollen Rhizopus oryzae spores and Aspergillus fumigatus conidia,” Infection and Immunity, vol. 48, no. 2, pp. 458–463, 1985.
[60]  E. V. Svirshchevskaya, M. A. Shevchenko, D. Huet et al., “Susceptibility of mice to invasive aspergillosis correlates with delayed cell influx into the lungs,” International Journal of Immunogenetics, vol. 36, no. 5, pp. 289–299, 2009.
[61]  N. P. Gerard and C. Gerard, “The chemotactic receptor for human C5a anaphylatoxin,” Nature, vol. 349, no. 6310, pp. 614–617, 1991.
[62]  L. Kacani, Z. Bánki, J. Zwirner et al., “C5a and enhance the susceptibility of monocyte-derived macrophages to HIV infection,” Journal of Immunology, vol. 166, no. 5, pp. 3410–3415, 2001.
[63]  R. H. Daniels, W. A. J. Houston, M. M. Petersen, J. D. Williams, B. D. Williams, and B. P. Morgan, “Stimulation of human rheumatoid synovial cells by non-lethal complement membrane attack,” Immunology, vol. 69, no. 2, pp. 237–242, 1990.
[64]  M. Schonermark, R. Deppisch, G. Riedasch, K. Rother, and G. M. Hansch, “Induction of mediator release from human glomerular mesangial cells by the terminal complement components c5b-9,” International Archives of Allergy and Applied Immunology, vol. 96, no. 4, pp. 331–337, 1991.
[65]  P. Kalinski, “Regulation of immune responses by prostaglandin E2,” The Journal of Immunology, vol. 188, no. 1, pp. 21–28, 2012.
[66]  S. M. Dashiell, H. Rus, and C. L. Koski, “Terminal complement complexes concomitantly stimulate proliferation and rescue of Schwann cells from apoptosis,” Glia, vol. 30, no. 2, pp. 187–198, 2000.
[67]  L. Soane, H. Rus, F. Niculescu, and M. L. Shin, “Inhibition of oligodendrocyte apoptosis by sublytic C5b-9 is associated with enhanced synthesis of Bcl-2 and mediated by inhibition of caspase-3 activation,” Journal of Immunology, vol. 163, no. 11, pp. 6132–6138, 1999.
[68]  R. Würzner, “Complement and infectious diseases,” Contributions to Microbiology, vol. 10, pp. 1–17, 2003.
[69]  G. Rambach, H. Maier, G. Vago et al., “Complement induction and complement evasion in patients with cerebral aspergillosis,” Microbes and Infection, vol. 10, no. 14-15, pp. 1567–1576, 2008.
[70]  G. Vogl, I. Lesiak, D. B. Jensen et al., “Immune evasion by acquisition of complement inhibitors: the mould Aspergillus binds both factor H and C4b binding protein,” Molecular Immunology, vol. 45, no. 5, pp. 1485–1493, 2008.
[71]  J. Behnsen, A. Hartmann, J. Schmaler, A. Gehrke, A. A. Brakhage, and P. F. Zipfel, “The opportunistic human pathogenic fungus Aspergillus fumigatus evades the host complement system,” Infection and Immunity, vol. 76, no. 2, pp. 820–827, 2008.
[72]  R. G. Washburn, C. H. Hammer, and J. E. Bennett, “Inhibition of complement by culture supernatants of Aspergillus fumigatus,” Journal of Infectious Diseases, vol. 154, no. 6, pp. 944–951, 1986.
[73]  R. G. Washburn, D. J. DeHart, D. E. Agwu, B. J. Bryant-Varela, and N. C. Julian, “Aspergillus fumigatus complement inhibitor: production, characterization, and purification by hydrophobic interaction and thin-layer chromatography,” Infection and Immunity, vol. 58, no. 11, pp. 3508–3515, 1990.
[74]  J. F. C. Tomee and H. F. Kauffman, “Putative virulence factors of Aspergillus fumigatus,” Clinical and Experimental Allergy, vol. 30, no. 4, pp. 476–484, 2000.
[75]  E. P. Scully, L. R. Baden, and J. T. Katz, “Fungal brain infections,” Current Opinion in Neurology, vol. 21, no. 3, pp. 347–352, 2008.
[76]  K. Langfelder, B. Jahn, H. Gehringer, A. Schmidt, G. Wanner, and A. A. Brakhage, “Identification of a polyketide synthase gene (pksP) of Aspergillus fumigatus involved in conidial pigment biosynthesis and virulence,” Medical Microbiology and Immunology, vol. 187, no. 2, pp. 79–89, 1998.
[77]  K. Langfelder, M. Streibel, B. Jahn, G. Haase, and A. A. Brakhage, “Biosynthesis of fungal melanins and their importance for human pathogenic fungi,” Fungal Genetics and Biology, vol. 38, no. 2, pp. 143–158, 2003.
[78]  I. Lesiak-Markowicz, G. Vogl, T. Schwarzmuller, et al., “Candida albicans Hgt1p, a multifunctional evasion molecule: complement inhibitor, CR3 analogue, and human immunodeficiency virus-binding molecule,” Journal of Infectious Diseases, vol. 204, no. 5, pp. 802–809, 2011.
[79]  S. Luo, A. M. Blom, S. Rupp et al., “The pH-regulated antigen 1 of Candida albicans binds the human complement inhibitor C4b-binding protein and mediates fungal complement evasion,” Journal of Biological Chemistry, vol. 286, no. 10, pp. 8021–8029, 2011.

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