1887

Abstract

Neutrophils play an important role as effector cells and contribute to the resistance of the host against microbial pathogens. Neutrophils are able to produce extracellular traps (NETs) in response to medically important fungi, including spp., and . However, NET production in response to has yet to be studied. We have demonstrated that human neutrophils produce NETs against both conidia and yeasts of . Although the NADPH oxidase inhibitor diphenyleneiodonium chloride (DPI) did not alter NET production against conidia, it partially suppressed NET formation against yeasts. Cytochalasin D or IFN-γ did not affect the production of NETs against the fungus. Additionally, a mutant strain of with reduced expression of an alternative oxidase induced significantly higher levels of NETs in comparison with the WT strain. Finally, c.f.u. quantification of showed no significant differences when neutrophils were treated with DPI, DNase I or cytochalasin D as compared with untreated cells. These data establish that NET formation by human neutrophils appears to be either dependent or independent of reactive oxygen species production, correlating with the fungal morphotype used for stimulation. However, this mechanism was ineffective in killing the fungus.

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2015-05-01
2024-05-07
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References

  1. Berends E. T., Horswill A. R., Haste N. M., Monestier M., Nizet V., von Köckritz-Blickwede M. 2010; Nuclease expression by Staphylococcus aureus facilitates escape from neutrophil extracellular traps. J Innate Immun 2:576–586 [View Article][PubMed]
    [Google Scholar]
  2. Bianchi M., Niemiec M. J., Siler U., Urban C. F., Reichenbach J. 2011; Restoration of anti-Aspergillus defense by neutrophil extracellular traps in human chronic granulomatous disease after gene therapy is calprotectin-dependent. J Allergy Clin Immunol 127:1243–1252e7 [View Article][PubMed]
    [Google Scholar]
  3. Brinkmann V., Reichard U., Goosmann C., Fauler B., Uhlemann Y., Weiss D. S., Weinrauch Y., Zychlinsky A. 2004; Neutrophil extracellular traps kill bacteria. Science 303:1532–1535 [View Article][PubMed]
    [Google Scholar]
  4. Brummer E., Castaneda E., Restrepo A. 1993; Paracoccidioidomycosis: an update. Clin Microbiol Rev 6:89–117[PubMed]
    [Google Scholar]
  5. Bruns S., Kniemeyer O., Hasenberg M., Aimanianda V., Nietzsche S., Thywissen A., Jeron A., Latgé J. P., Brakhage A. A., Gunzer M. 2010; Production of extracellular traps against Aspergillus fumigatus in vitro and in infected lung tissue is dependent on invading neutrophils and influenced by hydrophobin RodA. PLoS Pathog 6:e1000873 [View Article][PubMed]
    [Google Scholar]
  6. Byrd A. S., O’Brien X. M., Johnson C. M., Lavigne L. M., Reichner J. S. 2013; An extracellular matrix-based mechanism of rapid neutrophil extracellular trap formation in response to Candida albicans . J Immunol 190:4136–4148 [View Article][PubMed]
    [Google Scholar]
  7. Campos E. G., Jesuino R. S., Dantas A. S., Brígido M. M., Felipe M. S. 2005; Oxidative stress response in Paracoccidioides brasiliensis . Genet Mol Res 4:409–429[PubMed]
    [Google Scholar]
  8. Colombo A. L., Tobón A., Restrepo A., Queiroz-Telles F., Nucci M. 2011; Epidemiology of endemic systemic fungal infections in Latin America. Med Mycol 49:785–798[PubMed]
    [Google Scholar]
  9. Dantas A. S., Andrade R. V., de Carvalho M. J., Felipe M. S., Campos E. G. 2008; Oxidative stress response in Paracoccidioides brasiliensis: assessing catalase and cytochrome c peroxidase. Mycol Res 112:747–756 [View Article][PubMed]
    [Google Scholar]
  10. de Buhr N., Neumann A., Jerjomiceva N., von Köckritz-Blickwede M., Baums C. G. 2014; Streptococcus suis DNase SsnA contributes to degradation of neutrophil extracellular traps (NETs) and evasion of NET-mediated antimicrobial activity. Microbiology 160:385–395 [View Article][PubMed]
    [Google Scholar]
  11. Del M., Jiménez P., Restrepo A., García L. F., Cano L. E. 2004; Separation of Paracoccidioides brasiliensis conidia through Percoll gradients. Med Mycol 42:349–353 [View Article][PubMed]
    [Google Scholar]
  12. Dias M. F., Filgueira A. L., de Souza W. 2004; A morphological and cytochemical study of the interaction between Paracoccidiodes brasiliensis and neutrophils. Microsc Microanal 10:215–223 [View Article][PubMed]
    [Google Scholar]
  13. Dias M. F. R. G., Mesquita J., Filgueira A. L., De Souza W. 2008; Human neutrophils susceptibility to Paracoccidioides brasiliensis: an ultrastructural and cytochemical assay. Med Mycol 46:241–249 [View Article][PubMed]
    [Google Scholar]
  14. Fuchs T. A., Abed U., Goosmann C., Hurwitz R., Schulze I., Wahn V., Weinrauch Y., Brinkmann V., Zychlinsky A. 2007; Novel cell death program leads to neutrophil extracellular traps. J Cell Biol 176:231–241 [View Article][PubMed]
    [Google Scholar]
  15. Gessler N. N., Aver’yanov A. A., Belozerskaya T. A. 2007; Reactive oxygen species in regulation of fungal development. Biochemistry (Mosc) 72:1091–1109 [View Article][PubMed]
    [Google Scholar]
  16. Gonzalez A., Sahaza J. H., Ortiz B. L., Restrepo A., Cano L. E. 2003; Production of pro-inflammatory cytokines during the early stages of experimental Paracoccidioides brasiliensis infection. Med Mycol 41:391–399 [View Article][PubMed]
    [Google Scholar]
  17. González A., Restrepo A., Cano L. E. 2008; Pulmonary immune responses induced in BALB/c mice by Paracoccidioides brasiliensis conidia. Mycopathologia 165:313–330 [View Article][PubMed]
    [Google Scholar]
  18. Guimarães-Costa A. B., Nascimento M. T., Froment G. S., Soares R. P., Morgado F. N., Conceição-Silva F., Saraiva E. M. 2009; Leishmania amazonensis promastigotes induce and are killed by neutrophil extracellular traps. Proc Natl Acad Sci U S A 106:6748–6753 [View Article][PubMed]
    [Google Scholar]
  19. Jenne C. N., Wong C. H., Zemp F. J., McDonald B., Rahman M. M., Forsyth P. A., McFadden G., Kubes P. 2013; Neutrophils recruited to sites of infection protect from virus challenge by releasing neutrophil extracellular traps. Cell Host Microbe 13:169–180 [View Article][PubMed]
    [Google Scholar]
  20. Kanetsuna F., Carbonell L. M. 1970; Cell wall glucans of the yeast and mycelial forms of Paracoccidioides brasiliensis . J Bacteriol 101:675–680[PubMed]
    [Google Scholar]
  21. Kanetsuna F., Carbonell L. M., Azuma I., Yamamura Y. 1972; Biochemical studies on the thermal dimorphism of Paracoccidioides brasiliensis . J Bacteriol 110:208–218[PubMed]
    [Google Scholar]
  22. Kurita N., Biswas S. K., Oarada M., Sano A., Nishimura K., Miyaji M. 1999a). Fungistatic and fungicidal activities of murine polymorphonuclear leucocytes against yeast cells of Paracoccidioides brasiliensis . Med Mycol 37:19–24 [View Article][PubMed]
    [Google Scholar]
  23. Kurita N., Oarada M., Ito E., Miyaji M. 1999b). Antifungal activity of human polymorphonuclear leucocytes against yeast cells of Paracoccidioides brasiliensis . Med Mycol 37:261–267 [View Article][PubMed]
    [Google Scholar]
  24. Kurita N., Oarada M., Miyaji M., Ito E. 2000; Effect of cytokines on antifungal activity of human polymorphonuclear leucocytes against yeast cells of Paracoccidioides brasiliensis . Med Mycol 38:177–182 [View Article][PubMed]
    [Google Scholar]
  25. Lappann M., Danhof S., Guenther F., Olivares-Florez S., Mordhorst I. L., Vogel U. 2013; In vitro resistance mechanisms of Neisseria meningitidis against neutrophil extracellular traps. Mol Microbiol 89:433–449 [View Article][PubMed]
    [Google Scholar]
  26. Londero A. T., Melo I. S. 1983; Paracoccidioidomycosis in childhood. Mycopathologia 82:49–55 [View Article][PubMed]
    [Google Scholar]
  27. Lopera D., Naranjo T. W., Cruz O. G., Restrepo A., Cano L. E., Lenzi H. L. 2011; Structural and topographic dynamics of pulmonary histopathology and local cytokine profiles in Paracoccidioides brasiliensis conidia-infected mice. PLoS Negl Trop Dis 5:e1232 [View Article][PubMed]
    [Google Scholar]
  28. Maricato J. T., Batista W. L., Kioshima E. S., Feitosa L. S., Novaes e Brito R. R., Goldman G. H., Mariano M., Puccia R., Lopes J. D. 2010; The Paracoccidioides brasiliensis gp70 antigen is encoded by a putative member of the flavoproteins monooxygenase family. Fungal Genet Biol 47:179–189 [View Article][PubMed]
    [Google Scholar]
  29. Marques S. A. 2013; Paracoccidioidomycosis: epidemiological, clinical, diagnostic and treatment up-dating. An Bras Dermatol 88:700–711 [View Article][PubMed]
    [Google Scholar]
  30. Medina E. 2009; Neutrophil extracellular traps: a strategic tactic to defeat pathogens with potential consequences for the host. J Innate Immun 1:176–180 [View Article][PubMed]
    [Google Scholar]
  31. Narayana Moorthy A., Narasaraju T., Rai P., Perumalsamy R., Tan K. B., Wang S., Engelward B., Chow V. T. 2013; In vivo and in vitro studies on the roles of neutrophil extracellular traps during secondary pneumococcal pneumonia after primary pulmonary influenza infection. Front Immunol 4:56 [View Article][PubMed]
    [Google Scholar]
  32. Negroni R. 1993; Paracoccidioidomycosis (South American blastomycosis, Lutz’s mycosis). Int J Dermatol 32:847–859 [View Article][PubMed]
    [Google Scholar]
  33. Papayannopoulos V., Zychlinsky A. 2009; NETs: a new strategy for using old weapons. Trends Immunol 30:513–521 [View Article][PubMed]
    [Google Scholar]
  34. Pilsczek F. H., Salina D., Poon K. K., Fahey C., Yipp B. G., Sibley C. D., Robbins S. M., Green F. H., Surette M. G. et al. 2010; A novel mechanism of rapid nuclear neutrophil extracellular trap formation in response to Staphylococcus aureus . J Immunol 185:7413–7425 [View Article][PubMed]
    [Google Scholar]
  35. Pina A., Saldiva P. H., Restrepo L. E., Calich V. L. 2006; Neutrophil role in pulmonary paracoccidioidomycosis depends on the resistance pattern of hosts. J Leukoc Biol 79:1202–1213 [View Article][PubMed]
    [Google Scholar]
  36. Rappleye C. A., Eissenberg L. G., Goldman W. E. 2007; Histoplasma capsulatum α-(1,3)-glucan blocks innate immune recognition by the β-glucan receptor. Proc Natl Acad Sci U S A 104:1366–1370 [View Article][PubMed]
    [Google Scholar]
  37. Restrepo A., Jiménez B. E. 1980; Growth of Paracoccidioides brasiliensis yeast phase in a chemically defined culture medium. J Clin Microbiol 12:279–281[PubMed]
    [Google Scholar]
  38. Restrepo A., Tobon A. 2010; Paracoccidioides brasiliensis. Infectious diseases and their etiologic agents. In Principles and Practice of Infectious Disease, 7th edn. pp. 3357–3390, chapter 268. Edited by Mandel G. L., Bennett J. E., Dolin R. Philadelphia, PA: Elsevier Churchill Livingtone;
    [Google Scholar]
  39. Restrepo A., Salazar M. E., Cano L. E., Patiño M. M. 1986; A technique to collect and dislodge conidia produced by Paracoccidioides brasiliensis mycelial form. J Med Vet Mycol 24:247–250 [View Article][PubMed]
    [Google Scholar]
  40. Restrepo A., Benard G., de Castro C. C., Agudelo C. A., Tobón A. M. 2008; Pulmonary paracoccidioidomycosis. Semin Respir Crit Care Med 29:182–197 [View Article][PubMed]
    [Google Scholar]
  41. Rodrigues D. R., Dias-Melicio L. A., Calvi S. A., Peraçoli M. T., Soares A. M. 2007; Paracoccidioides brasiliensis killing by IFN-γ, TNF-α and GM-CSF activated human neutrophils: role for oxygen metabolites. Med Mycol 45:27–33 [View Article][PubMed]
    [Google Scholar]
  42. Ruiz O. H., Gonzalez A., Almeida A. J., Tamayo D., Garcia A. M., Restrepo A., McEwen J. G. 2011; Alternative oxidase mediates pathogen resistance in Paracoccidioides brasiliensis infection. PLoS Negl Trop Dis 5:e1353 [View Article][PubMed]
    [Google Scholar]
  43. Saitoh T., Komano J., Saitoh Y., Misawa T., Takahama M., Kozaki T., Uehata T., Iwasaki H., Omori H. et al. 2012; Neutrophil extracellular traps mediate a host defense response to human immunodeficiency virus-1. Cell Host Microbe 12:109–116 [View Article][PubMed]
    [Google Scholar]
  44. Short K. R., von Köckritz-Blickwede M., Langereis J. D., Chew K. Y., Job E. R., Armitage C. W., Hatcher B., Fujihashi K., Reading P. C. et al. 2014; Antibodies mediate formation of neutrophil extracellular traps in the middle ear and facilitate secondary pneumococcal otitis media. Infect Immun 82:364–370 [View Article][PubMed]
    [Google Scholar]
  45. Springer D. J., Ren P., Raina R., Dong Y., Behr M. J., McEwen B. F., Bowser S. S., Samsonoff W. A., Chaturvedi S., Chaturvedi V. 2010; Extracellular fibrils of pathogenic yeast Cryptococcus gattii are important for ecological niche, murine virulence and human neutrophil interactions. PLoS ONE 5:e10978 [View Article][PubMed]
    [Google Scholar]
  46. Tavian E. G., Dias-Melicio L. A., Acorci M. J., Graciani A. P., Peraçoli M. T., Soares A. M. 2008; Interleukin-15 increases Paracoccidioides brasiliensis killing by human neutrophils. Cytokine 41:48–53 [View Article][PubMed]
    [Google Scholar]
  47. Tomazett P. K., Félix C. R., Lenzi H. L., de Paula Faria F., de Almeida Soares C. M., Pereira M. 2010; 1,3-β-d-Glucan synthase of Paracoccidioides brasiliensis: recombinant protein, expression and cytolocalization in the yeast and mycelium phases. Fungal Biol 114:809–816 [View Article][PubMed]
    [Google Scholar]
  48. Urban C. F., Reichard U., Brinkmann V., Zychlinsky A. 2006; Neutrophil extracellular traps capture and kill Candida albicans yeast and hyphal forms. Cell Microbiol 8:668–676 [View Article][PubMed]
    [Google Scholar]
  49. Urban C. F., Ermert D., Schmid M., Abu-Abed U., Goosmann C., Nacken W., Brinkmann V., Jungblut P. R., Zychlinsky A. 2009; Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans . PLoS Pathog 5:e1000639 [View Article][PubMed]
    [Google Scholar]
  50. Yost C. C., Cody M. J., Harris E. S., Thornton N. L., McInturff A. M., Martinez M. L., Chandler N. B., Rodesch C. K., Albertine K. H. et al. 2009; Impaired neutrophil extracellular trap (NET) formation: a novel innate immune deficiency of human neonates. Blood 113:6419–6427 [View Article][PubMed]
    [Google Scholar]
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