Table of Contents Author Guidelines Submit a Manuscript
Journal of Immunology Research
Volume 2018 (2018), Article ID 5379085, 12 pages
https://doi.org/10.1155/2018/5379085
Research Article

Aspergillus fumigatus Infection-Induced Neutrophil Recruitment and Location in the Conducting Airway of Immunocompetent, Neutropenic, and Immunosuppressed Mice

1Laboratory of Cell Interactions, Department of Immunology, Shemyakin and Ovchinnikov Institute of Bioorganic Chemistry, Russian Academy of Sciences, Miklukho-Maklaya St. 16/10, Moscow 117997, Russia
2Laboratory for Advanced Studies of Membrane Proteins, Moscow Institute of Physics and Technology, 9 Institutskiy Per., Dolgoprudny 141701, Russia
3Institute of Complex Systems 4 (ICS-4: Cellular Biophysics), Forschungszentrum Jülich, 52425 Jülich, Germany
4Institute of Complex Systems 6 (ICS-6: Structural Biochemistry), Forschungszentrum Jülich, 52425 Jülich, Germany
5Université Grenoble Alpes, CEA, CNRS, IBS, 38000 Grenoble, France

Correspondence should be addressed to Marina A. Shevchenko and Valentin I. Borshchevskiy

Received 25 August 2017; Revised 5 November 2017; Accepted 22 November 2017; Published 18 January 2018

Academic Editor: Elzbieta Kolaczkowska

Copyright © 2018 Marina A. Shevchenko 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. W. Baddley, “Clinical risk factors for invasive aspergillosis,” Medical Mycology, vol. 49, no. S1, pp. S7–S12, 2011. View at Publisher · View at Google Scholar · View at Scopus
  2. J. Farrant, H. Brice, S. Fowler, and R. Niven, “Fungal sensitisation in severe asthma is associated with the identification of Aspergillus fumigatus in sputum,” Journal of Asthma, vol. 53, no. 7, pp. 732–735, 2016. View at Publisher · View at Google Scholar · View at Scopus
  3. G. D. Brown, D. W. Denning, N. A. Gow, S. M. Levitz, M. G. Netea, and T. C. White, “Hidden killers: human fungal infections,” Science Translational Medicine, vol. 4, no. 165, article 165rv13, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. M. Kousha, R. Tadi, and A. O. Soubani, “Pulmonary aspergillosis: a clinical review,” European Respiratory Review, vol. 20, no. 121, pp. 156–174, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. M. M. Mircescu, L. Lipuma, N. van Rooijen, E. G. Pamer, and T. M. Hohl, “Essential role for neutrophils but not alveolar macrophages at early time points following Aspergillus fumigatus infection,” The Journal of Infectious Diseases, vol. 200, no. 4, pp. 647–656, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. C. R. Bonnett, E. J. Cornish, A. G. Harmsen, and J. B. Burritt, “Early neutrophil recruitment and aggregation in the murine lung inhibit germination of Aspergillus fumigatus conidia,” Infection and Immunity, vol. 74, no. 12, pp. 6528–6539, 2006. View at Publisher · View at Google Scholar · View at Scopus
  7. S. Bruns, O. Kniemeyer, M. Hasenberg 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 Pathogens, vol. 6, no. 4, article e1000873, 2010. View at Publisher · View at Google Scholar
  8. S. J. Park, M. D. Burdick, W. K. Brix et al., “Neutropenia enhances lung dendritic cell recruitment in response to Aspergillus via a cytokine-to-chemokine amplification loop,” The Journal of Immunology, vol. 185, no. 10, pp. 6190–6197, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. M. A. Shevchenko, E. L. Bolkhovitina, E. A. Servuli, and A. M. Sapozhnikov, “Elimination of Aspergillus fumigatus conidia from the airways of mice with allergic airway inflammation,” Respiratory Research, vol. 14, no. 1, p. 78, 2013. View at Publisher · View at Google Scholar · View at Scopus
  10. A. Kohler, K. De Filippo, M. Hasenberg et al., “G-CSF-mediated thrombopoietin release triggers neutrophil motility and mobilization from bone marrow via induction of Cxcr2 ligands,” Blood, vol. 117, no. 16, pp. 4349–4357, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. J. J. Hoth, J. D. Wells, E. M. Hiltbold, C. E. McCall, and B. K. Yoza, “Mechanism of neutrophil recruitment to the lung after pulmonary contusion,” Shock, vol. 35, no. 6, pp. 604–609, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. C. Summers, S. M. Rankin, A. M. Condliffe, N. Singh, A. M. Peters, and E. R. Chilvers, “Neutrophil kinetics in health and disease,” Trends in Immunology, vol. 31, no. 8, pp. 318–324, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. K. Yamamoto, A. N. Ahyi, Z. A. Pepper-Cunningham et al., “Roles of lung epithelium in neutrophil recruitment during pneumococcal pneumonia,” American Journal of Respiratory Cell and Molecular Biology, vol. 50, no. 2, pp. 253–262, 2014. View at Publisher · View at Google Scholar · View at Scopus
  14. C. Silvestre-Roig, A. Hidalgo, and O. Soehnlein, “Neutrophil heterogeneity: implications for homeostasis and pathogenesis,” Blood, vol. 127, no. 18, pp. 2173–2181, 2016. View at Publisher · View at Google Scholar · View at Scopus
  15. K. E. Barletta, R. E. Cagnina, K. L. Wallace, S. I. Ramos, B. Mehrad, and J. Linden, “Leukocyte compartments in the mouse lung: distinguishing between marginated, interstitial, and alveolar cells in response to injury,” Journal of Immunological Methods, vol. 375, no. 1-2, pp. 100–110, 2012. View at Publisher · View at Google Scholar · View at Scopus
  16. B. V. Patel, K. C. Tatham, M. R. Wilson, K. P. O'Dea, and M. Takata, “In vivo compartmental analysis of leukocytes in mouse lungs,” American Journal of Physiology Lung Cellular and Molecular Physiology, vol. 309, no. 7, pp. L639–L652, 2015. View at Publisher · View at Google Scholar · View at Scopus
  17. B. E. McParland, P. T. Macklem, and P. D. Pare, “Airway wall remodeling: friend or foe?” Journal of Applied Physiology, vol. 95, no. 1, pp. 426–434, 2003. View at Publisher · View at Google Scholar
  18. C. M. Lloyd and D. S. Robinson, “Allergen-induced airway remodelling,” European Respiratory Journal, vol. 29, no. 5, pp. 1020–1032, 2007. View at Publisher · View at Google Scholar · View at Scopus
  19. S. Baraldo, G. Turato, C. Badin et al., “Neutrophilic infiltration within the airway smooth muscle in patients with COPD,” Thorax, vol. 59, no. 4, pp. 308–312, 2004. View at Publisher · View at Google Scholar · View at Scopus
  20. G. M. Gersuk, D. M. Underhill, L. Q. Zhu, and K. A. Marr, “Dectin-1 and TLRs permit macrophages to distinguish between different Aspergillus fumigatus cellular states,” The Journal of Immunology, vol. 176, no. 6, pp. 3717–3724, 2006. View at Publisher · View at Google Scholar
  21. T. Akoumianaki, I. Kyrmizi, I. Valsecchi et al., “Aspergillus cell wall melanin blocks LC3-associated phagocytosis to promote pathogenicity,” Cell Host & Microbe, vol. 19, no. 1, pp. 79–90, 2016. View at Publisher · View at Google Scholar · View at Scopus
  22. J. Lother, T. Breitschopf, S. Krappmann et al., “Human dendritic cell subsets display distinct interactions with the pathogenic mould Aspergillus fumigatus,” International Journal of Medical Microbiology, vol. 304, no. 8, pp. 1160–1168, 2014. View at Publisher · View at Google Scholar · View at Scopus
  23. K. W. Bruhn, K. Dekitani, T. B. Nielsen, P. Pantapalangkoor, and B. Spellberg, “Ly6G-mediated depletion of neutrophils is dependent on macrophages,” Results in Immunology, vol. 6, pp. 5–7, 2015. View at Publisher · View at Google Scholar · View at Scopus
  24. T. Z. Veres, S. Rochlitzer, M. Shevchenko et al., “Spatial interactions between dendritic cells and sensory nerves in allergic airway inflammation,” American Journal of Respiratory Cell and Molecular Biology, vol. 37, no. 5, pp. 553–561, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. J. P. Latgé, “The pathobiology of Aspergillus fumigatus,” Trends in Microbiology, vol. 9, no. 8, pp. 382–389, 2001. View at Publisher · View at Google Scholar · View at Scopus
  26. D. M. Dixon, A. Polak, and T. J. Walsh, “Fungus dose-dependent primary pulmonary aspergillosis in immunosuppressed mice,” Infection and Immunity, vol. 57, no. 5, pp. 1452–1456, 1989. View at Google Scholar
  27. J. M. Daley, A. A. Thomay, M. D. Connolly, J. S. Reichner, and J. E. Albina, “Use of Ly6G-specific monoclonal antibody to deplete neutrophils in mice,” Journal of Leukocyte Biology, vol. 83, no. 1, pp. 64–70, 2008. View at Publisher · View at Google Scholar · View at Scopus
  28. B. G. Yipp and P. Kubes, “Antibodies against neutrophil LY6G do not inhibit leukocyte recruitment in mice in vivo,” Blood, vol. 121, no. 1, pp. 241-242, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. J. X. Wang, A. M. Bair, S. L. King et al., “Ly6G ligation blocks recruitment of neutrophils via a β2-integrin-dependent mechanism,” Blood, vol. 120, no. 7, pp. 1489–1498, 2012. View at Publisher · View at Google Scholar · View at Scopus
  30. A. Hasenberg, M. Hasenberg, L. Mann et al., “Catchup: a mouse model for imaging-based tracking and modulation of neutrophil granulocytes,” Nature Methods, vol. 12, no. 5, pp. 445–452, 2015. View at Publisher · View at Google Scholar · View at Scopus
  31. 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. View at Publisher · View at Google Scholar · View at Scopus
  32. A. J. Hartigan, J. Westwick, G. Jarai, and C. M. Hogaboam, “CCR7 deficiency on dendritic cells enhances fungal clearance in a murine model of pulmonary invasive aspergillosis,” The Journal of Immunology, vol. 183, no. 8, pp. 5171–5179, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. E. M. O’Dea, N. Amarsaikhan, H. T. Li et al., “Eosinophils are recruited in response to chitin exposure and enhance Th2-mediated immune pathology in Aspergillus fumigatus infection,” Infection and Immunity, vol. 82, no. 8, pp. 3199–3205, 2014. View at Publisher · View at Google Scholar · View at Scopus
  34. N. Kalleda, J. Amich, B. Arslan et al., “Dynamic immune cell recruitment after murine pulmonary Aspergillus fumigatus infection under different immunosuppressive regimens,” Frontiers in Microbiology, vol. 7, p. 1107, 2016. View at Publisher · View at Google Scholar · View at Scopus
  35. L. O. Carvalho, E. N. Aquino, A. C. Neves, and W. Fontes, “The neutrophil nucleus and its role in neutrophilic function,” Journal of Cellular Biochemistry, vol. 116, no. 9, pp. 1831–1836, 2015. View at Publisher · View at Google Scholar · View at Scopus
  36. C. F. Hung, K. L. Mittelsteadt, R. Brauer et al., “Lung pericyte-like cells are functional interstitial immune sentinel cells,” American Journal of Physiology Lung Cellular and Molecular Physiology, vol. 312, no. 4, pp. L556–L567, 2017. View at Publisher · View at Google Scholar
  37. P. Baluk, K. Phillips, L. C. Yao, A. Adams, M. Nitschke, and D. M. McDonald, “Neutrophil dependence of vascular remodeling after Mycoplasma infection of mouse airways,” The American Journal of Pathology, vol. 184, no. 6, pp. 1877–1889, 2014. View at Publisher · View at Google Scholar · View at Scopus
  38. J. Pillay, I. den Braber, N. Vrisekoop et al., “In vivo labeling with 2H2O reveals a human neutrophil lifespan of 5.4 days,” Blood, vol. 116, no. 4, pp. 625–627, 2010. View at Publisher · View at Google Scholar · View at Scopus
  39. J. M. Adrover, J. A. Nicolas-Avila, and A. Hidalgo, “Aging: a temporal dimension for neutrophils,” Trends in Immunology, vol. 37, no. 5, pp. 334–345, 2014. View at Publisher · View at Google Scholar · View at Scopus
  40. G. D. Brown, “Innate antifungal immunity: the key role of phagocytes,” Annual Review of Immunology, vol. 29, no. 1, pp. 1–21, 2011. View at Publisher · View at Google Scholar · View at Scopus
  41. R. P. Gazendam, A. van de Geer, D. Roos, T. K. van den Berg, and T. W. Kuijpers, “How neutrophils kill fungi,” Immunological Reviews, vol. 273, no. 1, pp. 299–311, 2016. View at Publisher · View at Google Scholar · View at Scopus
  42. A. R. Burns, C. W. Smith, and D. C. Walker, “Unique structural features that influence neutrophil emigration into the lung,” Physiological Reviews, vol. 83, no. 2, pp. 309–336, 2003. View at Publisher · View at Google Scholar
  43. E. Kolaczkowska and P. Kubes, “Neutrophil recruitment and function in health and inflammation,” Nature Reviews Immunology, vol. 13, no. 3, pp. 159–175, 2013. View at Publisher · View at Google Scholar · View at Scopus
  44. K. Bucher, F. Schmitt, S. E. Autenrieth et al., “Fluorescent Ly6G antibodies determine macrophage phagocytosis of neutrophils and alter the retrieval of neutrophils in mice,” Journal of Leukocyte Biology, vol. 98, no. 3, pp. 365–372, 2015. View at Publisher · View at Google Scholar · View at Scopus
  45. K. Moses, J. C. Klein, L. Mann, A. Klingberg, M. Gunzer, and S. Brandau, “Survival of residual neutrophils and accelerated myelopoiesis limit the efficacy of antibody-mediated depletion of Ly-6G+ cells in tumor-bearing mice,” Journal of Leukocyte Biology, vol. 99, no. 6, pp. 811–823, 2016. View at Publisher · View at Google Scholar · View at Scopus