Β-Glucan–dependent shuttling of conidia from neutrophils to macrophages occurs during fungal infection establishment

Vahid Pazhakh, Felix Ellett, Ben A. Croker, Joanne A. O’Donnell, Luke Pase, Keith E. Schulze, R.Stefan Greulich, Aakash Gupta, Constantino Carlos Reyes-Aldasoro, Alex Andrianopoulos, Graham J. Lieschke

Research output: Contribution to journalArticleResearchpeer-review

Abstract

The initial host response to fungal pathogen invasion is critical to infection establishment and outcome. However, the diversity of leukocyte–pathogen interactions is only recently being appreciated. We describe a new form of interleukocyte conidial exchange called “shuttling.” In Talaromyces marneffei and Aspergillus fumigatus zebrafish in vivo infections, live imaging demonstrated conidia initially phagocytosed by neutrophils were transferred to macrophages. Shuttling is unidirectional, not a chance event, and involves alterations of phagocyte mobility, intercellular tethering, and phagosome transfer. Shuttling kinetics were fungal-species–specific, implicating a fungal determinant. β-glucan serves as a fungal-derived signal sufficient for shuttling. Murine phagocytes also shuttled in vitro. The impact of shuttling for microbiological outcomes of in vivo infections is difficult to specifically assess experimentally, but for these two pathogens, shuttling augments initial conidial redistribution away from fungicidal neutrophils into the favorable macrophage intracellular niche. Shuttling is a frequent host–pathogen interaction contributing to fungal infection establishment patterns.

Original languageEnglish
Article numbere3000113
Number of pages33
JournalPLoS Biology
Volume17
Issue number9
DOIs
Publication statusPublished - 4 Sep 2019

Keywords

  • neutrophils
  • macrophages
  • aspergillus fumigatus
  • phagocytes
  • green fluorescent protein
  • fungal spores
  • zebrafish
  • fungal pathogens

Cite this

Pazhakh, Vahid ; Ellett, Felix ; Croker, Ben A. ; O’Donnell, Joanne A. ; Pase, Luke ; Schulze, Keith E. ; Greulich, R.Stefan ; Gupta, Aakash ; Reyes-Aldasoro, Constantino Carlos ; Andrianopoulos, Alex ; Lieschke, Graham J. / Β-Glucan–dependent shuttling of conidia from neutrophils to macrophages occurs during fungal infection establishment. In: PLoS Biology. 2019 ; Vol. 17, No. 9.
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title = "Β-Glucan–dependent shuttling of conidia from neutrophils to macrophages occurs during fungal infection establishment",
abstract = "The initial host response to fungal pathogen invasion is critical to infection establishment and outcome. However, the diversity of leukocyte–pathogen interactions is only recently being appreciated. We describe a new form of interleukocyte conidial exchange called “shuttling.” In Talaromyces marneffei and Aspergillus fumigatus zebrafish in vivo infections, live imaging demonstrated conidia initially phagocytosed by neutrophils were transferred to macrophages. Shuttling is unidirectional, not a chance event, and involves alterations of phagocyte mobility, intercellular tethering, and phagosome transfer. Shuttling kinetics were fungal-species–specific, implicating a fungal determinant. β-glucan serves as a fungal-derived signal sufficient for shuttling. Murine phagocytes also shuttled in vitro. The impact of shuttling for microbiological outcomes of in vivo infections is difficult to specifically assess experimentally, but for these two pathogens, shuttling augments initial conidial redistribution away from fungicidal neutrophils into the favorable macrophage intracellular niche. Shuttling is a frequent host–pathogen interaction contributing to fungal infection establishment patterns.",
keywords = "neutrophils, macrophages, aspergillus fumigatus, phagocytes, green fluorescent protein, fungal spores, zebrafish, fungal pathogens",
author = "Vahid Pazhakh and Felix Ellett and Croker, {Ben A.} and O’Donnell, {Joanne A.} and Luke Pase and Schulze, {Keith E.} and R.Stefan Greulich and Aakash Gupta and Reyes-Aldasoro, {Constantino Carlos} and Alex Andrianopoulos and Lieschke, {Graham J.}",
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Pazhakh, V, Ellett, F, Croker, BA, O’Donnell, JA, Pase, L, Schulze, KE, Greulich, RS, Gupta, A, Reyes-Aldasoro, CC, Andrianopoulos, A & Lieschke, GJ 2019, 'Β-Glucan–dependent shuttling of conidia from neutrophils to macrophages occurs during fungal infection establishment', PLoS Biology, vol. 17, no. 9, e3000113. https://doi.org/10.1371/journal.pbio.3000113

Β-Glucan–dependent shuttling of conidia from neutrophils to macrophages occurs during fungal infection establishment. / Pazhakh, Vahid; Ellett, Felix; Croker, Ben A.; O’Donnell, Joanne A.; Pase, Luke; Schulze, Keith E.; Greulich, R.Stefan; Gupta, Aakash; Reyes-Aldasoro, Constantino Carlos; Andrianopoulos, Alex; Lieschke, Graham J.

In: PLoS Biology, Vol. 17, No. 9, e3000113, 04.09.2019.

Research output: Contribution to journalArticleResearchpeer-review

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AU - Pase, Luke

AU - Schulze, Keith E.

AU - Greulich, R.Stefan

AU - Gupta, Aakash

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