Capsular polysaccharides from Cryptococcus neoformans modulate production of neutrophil extracellular traps (NETs) by human neutrophils

Scientific Reports

Volumn 5, Issue , 2015, Pages 8008-

  Rocha, Juliana D B ^a   Nascimento, Michelle T C ^a   Decote Ricardo, Debora ^b   Côrte Real, Suzana ^c   Morrot, Alexandre ^a   Heise, Norton ^a   Nunes, Marise P ^c   Previato, José Osvaldo ^a   Mendonça Previato, Lucia ^a   Dosreis, George A ^a   Saraiva, Elvira M ^a   Freire De Lima, Célio G ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b FEDERAL RURAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^c INSTITUTO OSWALDO CRUZ   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL POLYSACCHARIDE; GALACTAN; GLUCURONOXYLOMANNAN; POLYSACCHARIDE; REACTIVE OXYGEN METABOLITE;

CHEMISTRY; CRYPTOCOCCUS NEOFORMANS; DRUG EFFECTS; EXTRACELLULAR TRAP; HUMAN; METABOLISM; NEUTROPHIL; PATHOGENICITY;

CRYPTOCOCCUS NEOFORMANS; EXTRACELLULAR TRAPS; FUNGAL POLYSACCHARIDES; GALACTANS; HUMANS; NEUTROPHILS; POLYSACCHARIDES; REACTIVE OXYGEN SPECIES;

EID: 84922998533     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep08008     Document Type: Article

References (50)

1. Buchanan, K. L. & Murphy, J. W. What makes Cryptococcus neoformans a pathogen? Emerg Infect Dis 4, 71-83 (1998).
2. McClelland, E. E., Bernhardt, P. & Casadevall, A. Estimating the relative contributions of virulence factors for pathogenic microbes. Infect Immun 74, 1500-1504 (2006).
3. Chang, Y. C. & Kwon-Chung, K. J. Complementation of a capsule-deficient mutation of Cryptococcus neoformans restores its virulence. Mol Cell Biol 14, 4912-4919 (1994).
4. Fromtling, R. A., Shadomy, H. J. & Jacobson, E. S. Decreased virulence in stable, acapsular mutants of cryptococcus neoformans. Mycopathologia 79, 23-29 (1982).
5. Cherniak, R., Jones, R. G. & Reiss, E. Structure determination of Cryptococcus neoformans serotype A-variant glucuronoxylomannan by 13C-n.m.r. spectroscopy. Carbohydr Res 172, 113-138 (1988).
6. Cherniak, R., Valafar, H., Morris, L. C. & Valafar, F. Cryptococcus neoformans chemotyping by quantitative analysis of 1H nuclear magnetic resonance spectra of glucuronoxylomannans with a computer-simulated artificial neural network. Clin Diagn Lab Immunol 5, 146-159 (1998).
7. Monari, C. et al. Differences in outcome of the interaction between Cryptococcus neoformans glucuronoxylomannan and human monocytes and neutrophils. Eur J Immunol 33, 1041-1051 (2003).
8. Dong, Z. M. & Murphy, J. W. Cryptococcal polysaccharides induce L-selectin shedding and tumor necrosis factor receptor loss from the surface of human neutrophils. J Clin Invest 97, 689-698 (1996).
9. Monari, C., Kozel, T. R., Bistoni, F. & Vecchiarelli, A. Modulation of C5aR expression on human neutrophils by encapsulated and acapsular Cryptococcus neoformans. Infect Immun 70, 3363-3370 (2002).
10. Heiss, C., Klutts, J. S., Wang, Z., Doering, T. L. & Azadi, P. The structure of Cryptococcus neoformans galactoxylomannan contains beta-D-glucuronic acid. Carbohydr Res 344, 915-920 (2009).
11. Villena, S. N. et al Capsular polysaccharides galactoxylomannan and glucuronoxylomannan from Cryptococcus neoformans induce macrophage apoptosis mediated by Fas ligand. Cell Microbiol 10, 1274-1285 (2008).
12. Chaturvedi, V., Wong, B. & Newman, S. L. Oxidative killing of Cryptococcus neoformans by human neutrophils. Evidence that fungal mannitol protects by scavenging reactive oxygen intermediates. J Immunol 156, 3836-3840 (1996).
13. Diamond, R. D., Root, R. K. & Bennett, J. E. Factors influencing killing of Cryptococcus neoformans by human leukocytes in vitro. J Infect Dis 125, 367-376 (1972).
14. Papayannopoulos, V., Metzler, K. D., Hakkim, A. & Zychlinsky, A. Neutrophil elastase and myeloperoxidase regulate the formation of neutrophil extracellular traps. J Cell Biol 191, 677-691 (2010).
15. Brinkmann, V. et al. Neutrophil extracellular traps kill bacteria. Science 303, 1532-1535 (2004).
16. Guimaraes-Costa, A. B. et al. Leishmania amazonensis promastigotes induce and are killed by neutrophil extracellular traps. Proc Natl Acad Sci USA 106, 6748-6753 (2009).
17. Saitoh, T. et al. Neutrophil extracellular traps mediate a host defense response to human immunodeficiency virus-1. Cell Host Microbe 12, 109-116 (2012).
18. Urban, C. F. et al. Neutrophil extracellular traps contain calprotectin, a cytosolic protein complex involved in host defense against Candida albicans. PLoS Pathog 5 (2009).
19. Bianchi, M. et al. Restoration of NET formation by gene therapy in CGD controls aspergillosis. Blood 114, 2619-2622 (2009).
20. Bruns, S. et al. 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 (2010).
21. Springer, D. J. et al. Extracellular fibrils of pathogenic yeast Cryptococcus gattii are important for ecological niche, murine virulence and human neutrophil interactions. PLoS One 5, e10978 (2010).
22. Urban, C. F., Reichard, U., Brinkmann, V. & Zychlinsky, A. Neutrophil extracellular traps capture and kill Candida albicans yeast and hyphal forms. Cell Microbiol 8, 668-676 (2006).
23. Wang, Y. et al. Human PAD4 regulates histone arginine methylation levels via demethylimination. Science 306, 279-283 (2004).
24. Pilsczek, F. H. et al. A novel mechanism of rapid nuclear neutrophil extracellular trap formation in response to Staphylococcus aureus. J Immunol 185, 7413-7425 (2010).
25. Hemmers, S., Teijaro, J. R., Arandjelovic, S. & Mowen, K. A. PAD4-mediated neutrophil extracellular trap formation is not required for immunity against influenza infection. PLoS One 6, e22043 (2011).
26. Graybill, J. R., Bocanegra, R., Lambros, C. & Luther, M. F. Granulocyte colony stimulating factor therapy of experimental cryptococcal meningitis. J Med Vet Mycol 35, 243-247 (1997).
27. Mednick, A. J., Feldmesser, M., Rivera, J. & Casadevall, A. Neutropenia alters lung cytokine production in mice and reduces their susceptibility to pulmonary cryptococcosis. Eur J Immunol 33, 1744-1753 (2003).
28. Segal, B. H. et al. Aspergillus nidulans infection in chronic granulomatous disease. Medicine (Baltimore) 77, 345-354 (1998).
29. Segal, B. H. & Romani, L. R. Invasive aspergillosis in chronic granulomatous disease. Med Mycol 47 Suppl 1, S282-290 (2009).
30. Branzk, N. & Papayannopoulos, V. Molecular mechanisms regulating NETosis in infection and disease. Semin Immunopathol 35, 513-530 (2013).
31. Kirchner, T. et al. The impact of various reactive oxygen species on the formation of neutrophil extracellular traps. Mediators Inflamm 2012, 849136 (2012).
32. Wartha, F. & Henriques-Normark, B. ETosis: a novel cell death pathway. Sci Signal 1, pe25 (2008).
33. Li, P. et al. PAD4 is essential for antibacterial innate immunity mediated by neutrophil extracellular traps. The Journal of experimental medicine 207, 1853-1862 (2010).
34. Gabriel, C., McMaster, W. R., Girard, D. & Descoteaux, A. Leishmania donovani promastigotes evade the antimicrobial activity of neutrophil extracellular traps. J Immunol 185, 4319-4327 (2010).
35. Chen, K. et al. Endocytosis of soluble immune complexes leads to their clearance by FcgammaRIIIB but induces neutrophil extracellular traps via FcgammaRIIA in vivo. Blood 120, 4421-4431 (2012).
36. Byrd, A. S., O'Brien, X. M., Johnson, C. M., Lavigne, L. M. & Reichner, J. S. An extracellular matrix-based mechanism of rapid neutrophil extracellular trap formation in response to Candida albicans. J Immunol 190, 4136-4148 (2013).
37. Sumby, P. et al. Extracellular deoxyribonuclease made by group A Streptococcus assists pathogenesis by enhancing evasion of the innate immune response. Proc Natl Acad Sci U S A 102, 1679-1684 (2005).
38. Walker, M. J. et al. DNase Sda1 provides selection pressure for a switch to invasive group A streptococcal infection. Nat Med 13, 981-985 (2007).
39. Beiter, K. et al. An endonuclease allows Streptococcus pneumoniae to escape from neutrophil extracellular traps. Curr Biol 16, 401-407 (2006).
40. Buchanan, J. T. et al. DNase expression allows the pathogen group A Streptococcus to escape killing in neutrophil extracellular traps. Curr Biol 16, 396-400 (2006).
41. Zinkernagel, A. S. et al. The IL-8 protease SpyCEP/ScpC of group A Streptococcus promotes resistance to neutrophil killing. Cell Host Microbe 4, 170-178 (2008).
42. Monari, C. et al. A microbial polysaccharide reduces the severity of rheumatoid arthritis by influencing Th17 differentiation and proinflammatory cytokines production. J Immunol 183, 191-200 (2009).
43. Kaplan, M. J. Neutrophils in the pathogenesis and manifestations of SLE. Nat Rev Rheumatol 7, 691-699 (2011).
44. Kessenbrock, K. et al. Netting neutrophils in autoimmune small-vessel vasculitis. Nat Med 15, 623-625 (2009).
45. Vaishnav, V. V., Bacon, B. E., O'Neill, M. & Cherniak, R. Structural characterization of the galactoxylomannan of Cryptococcus neoformans Cap67. Carbohydr. Res 306, 315-330 (1998).
46. Nimrichter, L. et al. Self-aggregation of Cryptococcus neoformans capsular glucuronoxylomannan is dependent on divalent cations. Eukaryot Cell 6, 1400-1410 (2007).
47. Cherniak, R., Morris, L. C., Anderson, B. C. & Meyer, S. A. Facilitated isolation, purification, and analysis of glucuronoxylomannan of Cryptococcus neoformans. Infect Immun 59, 59-64 (1991).
48. Cherniak, R., Reiss, E., Slodki, M. E., Plattner, R. D. & Blumer, S. O. Structure and antigenic activity of the capsular polysaccharide of Cryptococcus neoformans serotype A. Mol Immunol 17, 1025-1032 (1980).
49. Dubois, M., Gilles, K., Hamilton, J. K., Rebers, P. A. & Smith, F. A colorimetric method for the determination of sugars. Nature 168, 167 (1951).
50. Guimaraes-Costa, A. B. et al. 3'-nucleotidase/nuclease activity allows Leishmania parasites to escape killing by neutrophil extracellular traps. Infect Immun 82, 1732-1740 (2014).