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
2020-03-28
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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 Immun2:576–586 [CrossRef][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 Immunol127:1243–1252e7 [CrossRef][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. Science303:1532–1535 [CrossRef][PubMed]
    [Google Scholar]
  4. Brummer E., Castaneda E., Restrepo A.. 1993; Paracoccidioidomycosis: an update. Clin Microbiol Rev6:89–117[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 Pathog6:e1000873 [CrossRef][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 Immunol190:4136–4148 [CrossRef][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 Res4:409–429[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 Mycol49:785–798[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 Res112:747–756 [CrossRef][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. Microbiology160:385–395 [CrossRef][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 Mycol42:349–353 [CrossRef][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 Microanal10:215–223 [CrossRef][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 Mycol46:241–249 [CrossRef][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 Biol176:231–241 [CrossRef][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 [CrossRef][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 Mycol41:391–399 [CrossRef][PubMed]
    [Google Scholar]
  17. González A., Restrepo A., Cano L. E.. 2008; Pulmonary immune responses induced in BALB/c mice by Paracoccidioides brasiliensis conidia. Mycopathologia165:313–330 [CrossRef][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 A106:6748–6753 [CrossRef][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 Microbe13:169–180 [CrossRef][PubMed]
    [Google Scholar]
  20. Kanetsuna F., Carbonell L. M.. 1970; Cell wall glucans of the yeast and mycelial forms of Paracoccidioides brasiliensis. J Bacteriol101:675–680[PubMed]
    [Google Scholar]
  21. Kanetsuna F., Carbonell L. M., Azuma I., Yamamura Y.. 1972; Biochemical studies on the thermal dimorphism of Paracoccidioides brasiliensis. J Bacteriol110:208–218[PubMed]
    [Google Scholar]
  22. Kurita N., Biswas S. K., Oarada M., Sano A., Nishimura K., Miyaji M.. 1999;a). Fungistatic and fungicidal activities of murine polymorphonuclear leucocytes against yeast cells of Paracoccidioides brasiliensis. Med Mycol37:19–24 [CrossRef][PubMed]
    [Google Scholar]
  23. Kurita N., Oarada M., Ito E., Miyaji M.. 1999;b). Antifungal activity of human polymorphonuclear leucocytes against yeast cells of Paracoccidioides brasiliensis. Med Mycol37:261–267 [CrossRef][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 Mycol38:177–182 [CrossRef][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 Microbiol89:433–449 [CrossRef][PubMed]
    [Google Scholar]
  26. Londero A. T., Melo I. S.. 1983; Paracoccidioidomycosis in childhood. Mycopathologia82:49–55 [CrossRef][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 Dis5:e1232 [CrossRef][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 Biol47:179–189 [CrossRef][PubMed]
    [Google Scholar]
  29. Marques S. A.. 2013; Paracoccidioidomycosis: epidemiological, clinical, diagnostic and treatment up-dating. An Bras Dermatol88:700–711 [CrossRef][PubMed]
    [Google Scholar]
  30. Medina E.. 2009; Neutrophil extracellular traps: a strategic tactic to defeat pathogens with potential consequences for the host. J Innate Immun1:176–180 [CrossRef][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 Immunol4:56 [CrossRef][PubMed]
    [Google Scholar]
  32. Negroni R.. 1993; Paracoccidioidomycosis (South American blastomycosis, Lutz’s mycosis). Int J Dermatol32:847–859 [CrossRef][PubMed]
    [Google Scholar]
  33. Papayannopoulos V., Zychlinsky A.. 2009; NETs: a new strategy for using old weapons. Trends Immunol30:513–521 [CrossRef][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 Immunol185:7413–7425 [CrossRef][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 Biol79:1202–1213 [CrossRef][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 A104:1366–1370 [CrossRef][PubMed]
    [Google Scholar]
  37. Restrepo A., Jiménez B. E.. 1980; Growth of Paracoccidioides brasiliensis yeast phase in a chemically defined culture medium. J Clin Microbiol12:279–281[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 Mycol24:247–250 [CrossRef][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 Med29:182–197 [CrossRef][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 Mycol45:27–33 [CrossRef][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 Dis5:e1353 [CrossRef][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 Microbe12:109–116 [CrossRef][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 Immun82:364–370 [CrossRef][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 ONE5:e10978 [CrossRef][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. Cytokine41:48–53 [CrossRef][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 Biol114:809–816 [CrossRef][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 Microbiol8:668–676 [CrossRef][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 Pathog5:e1000639 [CrossRef][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. Blood113:6419–6427 [CrossRef][PubMed]
    [Google Scholar]
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