Table of Contents Author Guidelines Submit a Manuscript
Mediators of Inflammation
Volume 2015, Article ID 852574, 17 pages
http://dx.doi.org/10.1155/2015/852574
Research Article

Lipoxin Inhibits Fungal Uptake by Macrophages and Reduces the Severity of Acute Pulmonary Infection Caused by Paracoccidioides brasiliensis

1Departamento de Imunologia, Instituto de Ciências Biomédicas, Universidade de São Paulo, Avenida Professor Lineu Prestes 1730, 05508-900 São Paulo, SP, Brazil
2Department of Microbiology and Immunology, Indiana University School of Medicine, Indianapolis, IN 46202, USA

Received 30 June 2015; Accepted 20 September 2015

Academic Editor: Vera L. Petricevich

Copyright © 2015 Laura R. R. Ribeiro 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. J. G. McEwen, V. Bedoya, M. M. Patiño, M. E. Salazar, and A. Restrepo, “Experimental murine paracoccidiodomycosis induced by the inhalation of conidia,” Journal of Medical and Veterinary Mycology, vol. 25, no. 3, pp. 165–175, 1987. View at Publisher · View at Google Scholar · View at Scopus
  2. A. Restrepo, G. Benard, C. C. de Castro, C. A. Agudelo, and A. M. Tobón, “Pulmonary paracoccidioidomycosis,” Seminars in Respiratory and Critical Care Medicine, vol. 29, no. 2, pp. 182–197, 2008. View at Publisher · View at Google Scholar · View at Scopus
  3. V. L. G. Calich, L. M. Singer-Vermes, A. M. Siqueira, and E. Burger, “Susceptibility and resistance of inbred mice to Paracoccidioides brasiliensis,” British Journal of Experimental Pathology, vol. 66, no. 5, pp. 585–594, 1985. View at Google Scholar · View at Scopus
  4. L. M. Singer-Vermes, E. Burger, M. Russo, C. A. C. Vaz, and V. L. G. Calich, “Advances in experimental paracoccidioidomycosis using an isogenic murine model,” Archives of Medical Research, vol. 24, no. 3, pp. 239–245, 1993. View at Google Scholar · View at Scopus
  5. L. E. Cano, S. S. Kashino, C. Arruda, D. André, and C. F. Xidieh, “Protective role of interferon-gamma in experimental pulmonary paracoccidioidomycosis,” Infection and Immunity, vol. 66, no. 2, pp. 800–806, 1998. View at Google Scholar
  6. A. Pina, S. Bernardino, and V. L. G. Calich, “Alveolar macrophages from susceptible mice are more competent than those of resistant mice to control initial Paracoccidioides brasiliensis infection,” Journal of Leukocyte Biology, vol. 83, no. 5, pp. 1088–1099, 2008. View at Publisher · View at Google Scholar · View at Scopus
  7. C. Feriotti, F. V. Loures, E. Frank de Araújo, T. A. da Costa, and V. L. G. Calich, “Mannosyl-recognizing receptors induce an M1-like phenotype in macrophages of susceptible mice but an M2-like phenotype in mice resistant to a fungal infection,” PLoS ONE, vol. 8, no. 1, Article ID e54845, 17 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  8. A. Pina, E. F. de Araujo, M. Felonato et al., “Myeloid dendritic cells (DCs) of mice susceptible to paracoccidioidomycosis suppress T cell responses whereas myeloid and plasmacytoid DCs from resistant mice induce effector and regulatory T cells,” Infection and Immunity, vol. 81, no. 4, pp. 1064–1077, 2013. View at Publisher · View at Google Scholar · View at Scopus
  9. V. L. G. Calich, A. Pina, M. Felonato, S. Bernardino, T. A. Costa, and F. V. Loures, “Toll-like receptors and fungal infections: the role of TLR2, TLR4 and MyD88 in paracoccidioidomycosis,” FEMS Immunology and Medical Microbiology, vol. 53, no. 1, pp. 1–7, 2008. View at Publisher · View at Google Scholar · View at Scopus
  10. M. Peters-Golden and W. R. Henderson Jr., “Leukotrienes,” The New England Journal of Medicine, vol. 357, pp. 1841–1854, 2007. View at Publisher · View at Google Scholar
  11. C. N. Serhan, “Resolution phase of inflammation: novel endogenous anti-inflammatory and proresolving lipid mediators and pathways,” Annual Review of Immunology, vol. 25, pp. 101–137, 2007. View at Publisher · View at Google Scholar · View at Scopus
  12. M. J. Stables and D. W. Gilroy, “Old and new generation lipid mediators in acute inflammation and resolution,” Progress in Lipid Research, vol. 50, no. 1, pp. 35–51, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. N. Chiang, M. Arita, and C. N. Serhan, “Anti-inflammatory circuitry: lipoxin, aspirin-triggered lipoxins and their receptor ALX,” Prostaglandins Leukotrienes and Essential Fatty Acids, vol. 73, no. 3-4, pp. 163–177, 2005. View at Publisher · View at Google Scholar · View at Scopus
  14. Y. Kanaoka and J. A. Boyce, “Cysteinyl leukotrienes and their receptors: cellular distribution and function in immune and inflammatory responses,” The Journal of Immunology, vol. 173, no. 3, pp. 1503–1510, 2004. View at Publisher · View at Google Scholar · View at Scopus
  15. A. M. Tager and A. D. Luster, “BLT1 and BLT2: The leukotriene B(4) receptors,” Prostaglandins Leukotrienes and Essential Fatty Acids, vol. 69, no. 2-3, pp. 123–134, 2003. View at Publisher · View at Google Scholar · View at Scopus
  16. B. McMahon, S. Mitchell, H. R. Brady, and C. Godson, “Lipoxins: revelations on resolution,” Trends in Pharmacological Sciences, vol. 22, no. 8, pp. 391–395, 2001. View at Publisher · View at Google Scholar · View at Scopus
  17. M. B. Bailie, T. J. Standiford, L. L. Laichalk, M. J. Coffey, R. Strieter, and M. Peters-Golden, “Leukotriene-deficient mice manifest enhanced lethality from Klebsiella pneumonia in association with decreased alveolar macrophage phagocytic and bactericidal activities,” Journal of Immunology, vol. 157, no. 12, pp. 5221–5224, 1996. View at Google Scholar · View at Scopus
  18. M. Peters-Golden, C. Canetti, P. Mancuso, and M. J. Coffey, “Leukotrienes: underappreciated mediators of innate immune responses,” The Journal of Immunology, vol. 174, no. 2, pp. 589–594, 2005. View at Publisher · View at Google Scholar · View at Scopus
  19. Ü. S. Gürer, S. Büyüköztürk, Ş. Palandüz, B. Gürbüz, and A. Çevikbaş, “Effect of montelukast on polymorphonuclear leukocyte functions in asthmatic patients,” International Immunopharmacology, vol. 3, no. 9, pp. 1257–1260, 2003. View at Publisher · View at Google Scholar · View at Scopus
  20. N. Chen, A. Restivo, and C. S. Reiss, “Leukotrienes play protective roles early during experimental VSV encephalitis,” Journal of Neuroimmunology, vol. 120, no. 1-2, pp. 94–102, 2001. View at Publisher · View at Google Scholar · View at Scopus
  21. C. H. Serezani, J. H. Perrela, M. Russo, M. Peters-Golden, and S. Jancar, “Leukotrienes are essential for the control of Leishmania amazonensis infection and contribute to strain variation in susceptibility,” The Journal of Immunology, vol. 177, no. 5, pp. 3201–3208, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. J. J. Wirth and F. Kierszenbaum, “Stimulatory effects of leukotriene B4 on macrophage association with and intracellular destruction of Trypanosoma cruzi,” The Journal of Immunology, vol. 134, no. 3, pp. 1989–1993, 1985. View at Google Scholar · View at Scopus
  23. E. C. Yong, E. Y. Chi, and W. R. Henderson Jr., “Toxoplasma gondii alters eicosanoid release by human mononuclear phagocytes: role of leukotrienes in interferon γ-induced antitoxoplasma activity,” Journal of Experimental Medicine, vol. 180, no. 5, pp. 1637–1648, 1994. View at Publisher · View at Google Scholar · View at Scopus
  24. J. Aliberti, C. Serhan, and A. Sher, “Parasite-induced lipoxin A4 is an endogenous regulator of IL-12 production and immunopathology in Toxoplasma gondii infection,” The Journal of Experimental Medicine, vol. 196, no. 9, pp. 1253–1262, 2002. View at Publisher · View at Google Scholar · View at Scopus
  25. A. Bafica, C. A. Scanga, C. Serhan et al., “Host control of Mycobacterium tuberculosis is regulated by 5-lipoxygenase-dependent lipoxin production,” Journal of Clinical Investigation, vol. 115, no. 6, pp. 1601–1606, 2005. View at Publisher · View at Google Scholar · View at Scopus
  26. A. I. Medeiros, A. Sá-Nunes, E. G. Soares, C. M. Peres, C. L. Silva, and L. H. Faccioli, “Blockade of endogenous leukotrienes exacerbates pulmonary histoplasmosis,” Infection and Immunity, vol. 72, no. 3, pp. 1637–1644, 2004. View at Publisher · View at Google Scholar · View at Scopus
  27. A. I. Medeiros, A. Sá-Nunes, W. M. Turato et al., “Leukotrienes are potent adjuvant during fungal infection: effects on memory T cells,” Journal of Immunology, vol. 181, no. 12, pp. 8544–8551, 2008. View at Publisher · View at Google Scholar · View at Scopus
  28. A. M. V. C. Soares, S. A. Calvi, M. T. S. Peraçoli, A. C. Fernandez, L. A. Dias, and A. R. Dos Anjos, “Modulatory effect of prostaglandins on human monocyte activation for killing of high- and low-virulence strains of Paracoccidioides brasiliensis,” Immunology, vol. 102, no. 4, pp. 480–485, 2001. View at Publisher · View at Google Scholar · View at Scopus
  29. A. P. Bordon, L. A. Dias-Melicio, M. J. Acorci, S. A. Calvi, M. T. Serrão Peraçoli, and A. M. Victoriano de Campos Soares, “Prostaglandin E2 inhibits Paracoccidioides brasiliensis killing by human monocytes,” Microbes and Infection, vol. 9, no. 6, pp. 744–747, 2007. View at Publisher · View at Google Scholar · View at Scopus
  30. M. A. Michelin, F. Figueiredo, and F. Q. Cunha, “Involvement of prostaglandins in the immunosuppression occurring during experimental infection by Paracoccidioides brasiliensis,” Experimental Parasitology, vol. 102, no. 3-4, pp. 170–177, 2002. View at Publisher · View at Google Scholar · View at Scopus
  31. A. P. Bordon, L. A. Dias-Melicio, M. J. Acorci et al., “Prostaglandin E2 production by high and low virulent strains of Paracoccidioides brasiliensis,” Mycopathologia, vol. 163, no. 3, pp. 129–135, 2007. View at Publisher · View at Google Scholar · View at Scopus
  32. G. A. Biondo, L. A. Dias-Melicio, A. P. Bordon-Graciani, M. J. Acorci-Valério, and A. M. V. C. Soares, “Paracoccidioides brasiliensis uses endogenous and exogenous arachidonic acid for PGEx production,” Mycopathologia, vol. 170, no. 2, pp. 123–130, 2010. View at Publisher · View at Google Scholar · View at Scopus
  33. G. A. Biondo, L. A. Dias-Melicio, A. P. Bordon-Graciani, C. S. Kurokawa, and A. M. V. de Campos Soares, “Production of leukotriene B4 by Paracoccidioides brasiliensis,” Yeast, vol. 29, no. 6, pp. 201–208, 2012. View at Publisher · View at Google Scholar · View at Scopus
  34. F. S. M. Tristão, F. A. Rocha, A. P. Moreira, F. Q. Cunha, M. A. Rossi, and J. S. Silvaa, “5-Lipoxygenase activity increases susceptibility to experimental Paracoccidioides brasiliensis infection,” Infection and Immunity, vol. 81, no. 4, pp. 1256–1266, 2013. View at Publisher · View at Google Scholar · View at Scopus
  35. H. A. Balderramas, O. G. Ribeiro, Â. M. V. C. Soares, and S. L. Oliveira, “The role of leukotriene B4 in early stages of experimental paracoccidioidomycosis induced in phenotypically selected mouse strains,” Medical Mycology, vol. 51, no. 6, pp. 625–634, 2013. View at Publisher · View at Google Scholar · View at Scopus
  36. P. C. Santos, D. A. Santos, L. S. Ribeiro et al., “The pivotal role of 5-lipoxygenase-derived LTB4 in controlling pulmonary paracoccidioidomycosis,” PLoS Neglected Tropical Diseases, vol. 7, no. 8, Article ID e2390, 2013. View at Publisher · View at Google Scholar · View at Scopus
  37. F. V. Loures, A. Pina, M. Felonato, and V. L. G. Calich, “TLR2 is a negative regulator of Th17 cells and tissue pathology in a pulmonary model of fungal infection,” The Journal of Immunology, vol. 183, no. 2, pp. 1279–1290, 2009. View at Publisher · View at Google Scholar · View at Scopus
  38. F. V. Loures, A. Pina, M. Felonato, E. F. Araújo, K. R. M. Leite, and V. L. G. Calich, “Toll-like receptor 4 signaling leads to severe fungal infection associated with enhanced proinflammatory immunity and impaired expansion of regulatory T cells,” Infection and Immunity, vol. 78, no. 3, pp. 1078–1088, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. M. Felonato, A. Pina, E. F. de Araujo et al., “Anti-CD25 treatment depletes Treg cells and decreases disease severity in susceptible and resistant mice infected with Paracoccidioides brasiliensis,” PLoS ONE, vol. 7, no. 11, Article ID e51071, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. S. Bernardino, A. Pina, M. Felonato et al., “TNF-α and CD8+ T cells mediate the beneficial effects of nitric oxide synthase-2 deficiency in pulmonary paracoccidioidomycosis,” PLoS Neglected Tropical Diseases, vol. 7, no. 8, article e2325, 2013. View at Publisher · View at Google Scholar · View at Scopus
  41. S. S. Kashino, L. M. Singer-Vermes, V. L. G. Calich, and E. Burger, “Alterations in the pathogenicity of one Paracoccidioides brasiliensis isolate do not correlate with its in vitro growth,” Mycopathologia, vol. 111, no. 3, pp. 173–180, 1990. View at Publisher · View at Google Scholar · View at Scopus
  42. C. Fava Netto, V. S. Vegas, I. M. Sciannaméa, and E. D. B. Guarnieri, “Antígeno polissacarídico do Paracoccidioides brasiliensis. Estudo do tempo de cultivo do P. brasiliensis necessário ao preparo do antígeno,” Revista do Instituto de Medicina Tropical de São Paulo, vol. 11, no. 3, pp. 177–181, 1969. View at Google Scholar
  43. L. E. Cano, L. M. Singer-Vermes, C. A. C. Vaz, M. Russo, and V. L. G. Calich, “Pulmonary paracoccidioidomycosis in resistant and susceptible mice: relationship among progression of infection, bronchoalveolar cell activation, cellular immune response, and specific isotype patterns,” Infection and Immunity, vol. 63, no. 5, pp. 1777–1783, 1995. View at Google Scholar · View at Scopus
  44. T. R. Jones, M. Labelle, M. Belley et al., “Pharmacology of montelukast sodium (Singulair), a potent and selective leukotriene D4 receptor antagonist,” Canadian Journal of Physiology and Pharmacology, vol. 73, no. 2, pp. 191–201, 1995. View at Publisher · View at Google Scholar · View at Scopus
  45. L. M. Singer-Vermes, M. C. Ciavaglia, S. S. Kashino, E. Burger, and V. L. G. Calich, “The source of the growth-promoting factor(s) affects the plating efficiency of Paracoccidioides brasiliensis,” Medical Mycology, vol. 30, no. 3, pp. 261–264, 1992. View at Publisher · View at Google Scholar · View at Scopus
  46. A. H. Ding, C. F. Nathan, and D. J. Stuehr, “Release of reactive nitrogen intermediates and reactive oxygen intermediates from mouse peritoneal macrophages: comparison of activating cytokines and evidence for independent production,” The Journal of Immunology, vol. 141, no. 7, pp. 2407–2412, 1988. View at Google Scholar · View at Scopus
  47. A. Pina, P. H. N. Saldiva, L. E. C. Restrepo, and V. L. G. Calich, “Neutrophil role in pulmonary paracoccidioidomycosis depends on the resistance pattern of hosts,” Journal of Leukocyte Biology, vol. 79, no. 6, pp. 1202–1213, 2006. View at Publisher · View at Google Scholar · View at Scopus
  48. E. Börgeson, J. Lönn, I. Bergström et al., “Lipoxin A4 inhibits Porphyromonas gingivalis-induced aggregation and reactive oxygen species production by modulating neutrophil-platelet interaction and CD11b expression,” Infection and Immunity, vol. 79, no. 4, pp. 1489–1497, 2011. View at Publisher · View at Google Scholar · View at Scopus
  49. F. R. F. Nascimento, V. L. G. Calich, D. Rodríguez, and M. Russo, “Dual role for nitric oxide in paracoccidioidomycosis: essential for resistance, but overproduction associated with susceptibility,” The Journal of Immunology, vol. 168, no. 9, pp. 4593–4600, 2002. View at Publisher · View at Google Scholar · View at Scopus
  50. M. C. Livonesi, M. A. Rossi, J. T. de Souto et al., “Inducible nitric oxide synthase-deficient mice show exacerbated inflammatory process and high production of both Th1 and Th2 cytokines during paracoccidioidomycosis,” Microbes and Infection, vol. 11, no. 1, pp. 123–132, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. C. Magnusson, M. Mezhybovska, E. Lörinc, E. Fernebro, M. Nilbert, and A. Sjölander, “Low expression of CysLT1R and high expression of CysLT2R mediate good prognosis in colorectal cancer,” European Journal of Cancer, vol. 46, no. 4, pp. 826–835, 2010. View at Publisher · View at Google Scholar · View at Scopus
  52. E. R. Machado, M. T. Ueta, E. V. Lourenço et al., “Leukotrienes play a role in the control of parasite burden in murine strongyloidiasis,” The Journal of Immunology, vol. 175, no. 6, pp. 3892–3899, 2005. View at Publisher · View at Google Scholar · View at Scopus
  53. T. M. Laidlaw and J. A. Boyce, “Cysteinyl leukotriene receptors, old and new implications for asthma,” Clinical and Experimental Allergy, vol. 42, no. 9, pp. 1313–1320, 2012. View at Publisher · View at Google Scholar · View at Scopus
  54. S. Abdelmoaty, G. Wigerblad, D. B. Bas et al., “Spinal actions of Lipoxin A4 and 17(R)-Resolvin D1 attenuate inflammation-induced mechanical hypersensitivity and spinal TNF release,” PLoS ONE, vol. 8, no. 9, Article ID e75543, 2013. View at Publisher · View at Google Scholar · View at Scopus
  55. B. Wu, J. A. Walker, D. Temmermand et al., “Lipoxin A4 promotes more complete inflammation resolution in sepsis compared to stable lipoxin A4 analog,” Prostaglandins Leukotrienes and Essential Fatty Acids, vol. 89, no. 1, pp. 47–53, 2013. View at Publisher · View at Google Scholar · View at Scopus
  56. J. T. Souto, F. Figueiredo, A. Furlanetto, K. Pfeffer, M. A. Rossi, and J. S. Silva, “Interferon-γ and tumor necrosis factor-α determine resistance to Paracoccidioides brasiliensis infection in mice,” American Journal of Pathology, vol. 156, no. 5, pp. 1811–1820, 2000. View at Publisher · View at Google Scholar · View at Scopus
  57. T. A. Costa, S. B. Bazan, C. Feriotti et al., “In pulmonary paracoccidioidomycosis IL-10 deficiency leads to increased immunity and regressive infection without enhancing tissue pathology,” PLoS Neglected Tropical Diseases, vol. 7, no. 10, article e2512, 2013. View at Publisher · View at Google Scholar · View at Scopus
  58. C. C. Romano, M. J. S. Mendes-Giannini, A. J. S. Duarte, and G. Benard, “IL-12 and neutralization of endogenous IL-10 revert the in vitro antigen-specific cellular immunosuppression of paracoccidioidomycosis patients,” Cytokine, vol. 18, no. 3, pp. 149–157, 2002. View at Publisher · View at Google Scholar · View at Scopus
  59. C. L. Karp, L. M. Flick, K. W. Park et al., “Defective lipoxin-mediated anti-inflammatory activity in the cystic fibrosis airway,” Nature Immunology, vol. 5, no. 4, pp. 388–392, 2004. View at Publisher · View at Google Scholar · View at Scopus
  60. V. Verrière, G. Higgins, M. Al-Alawi et al., “Lipoxin a4 stimulates calcium-activated chloride currents and increases airway surface liquid height in normal and Cystic Fibrosis airway epithelia,” PLoS ONE, vol. 7, no. 5, Article ID e37746, 2012. View at Publisher · View at Google Scholar · View at Scopus
  61. G. Canny, O. Levy, G. T. Furuta et al., “Lipid mediator-induced expression of bactericidal/permeability-increasing protein (BPI) in human mucosal epithelia,” Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 6, pp. 3902–3907, 2002. View at Publisher · View at Google Scholar · View at Scopus
  62. J. G. Filep, C. Zouki, N. A. Petasis, M. Hachicha, and C. N. Serhan, “Anti-inflammatory actions of lipoxin A4 stable analogs are demonstrable in human whole blood: modulation of leukocyte adhesion molecules and inhibition of neutrophil-endothelial interactions,” Blood, vol. 94, no. 12, pp. 4132–4142, 1999. View at Google Scholar · View at Scopus
  63. V. Patcha, J. Wigren, M. E. Winberg, B. Rasmusson, J. Li, and E. Särndahl, “Differential inside-out activation of β2-integrins by leukotriene B4 and fMLP in human neutrophils,” Experimental Cell Research, vol. 300, no. 2, pp. 308–319, 2004. View at Publisher · View at Google Scholar · View at Scopus
  64. N. Shryock, C. McBerry, R. M. Salazar Gonzalez, S. Janes, F. T. M. Costa, and J. Aliberti, “Lipoxin A4 and 15-epi-lipoxin A4 protect against experimental cerebral malaria by inhibiting IL-12/IFN-γ in the brain,” PLoS ONE, vol. 8, no. 4, Article ID e61882, 2013. View at Publisher · View at Google Scholar · View at Scopus
  65. G. Benard, A. F. Campos, L. C. Netto et al., “Treatment of severe forms of paracoccidioidomycosis: is there a role for corticosteroids?” Medical Mycology, vol. 50, no. 6, pp. 641–648, 2012. View at Publisher · View at Google Scholar · View at Scopus
  66. R. C. B. Gryschek, R. M. Pereira, A. Kono et al., “Paradoxical reaction to treatment in 2 patients with severe acute paracoccidioidomycosis: a previously unreported complication and its management with corticosteroids,” Clinical Infectious Diseases, vol. 50, no. 10, pp. e56–e58, 2010. View at Publisher · View at Google Scholar · View at Scopus