Coccidioides endospores and spherules draw strong chemotactic, adhesive, and phagocytic responses by individual human neutrophils

Cheng Yuk Lee, George Richard Thompson, Christine J. Hastey, Gregory C. Hodge, Jennine M. Lunetta, Demosthenes Pappagianis, Volkmar Heinrich

Research output: Contribution to journalArticle

22 Citations (Scopus)

Abstract

Coccidioides spp. are dimorphic pathogenic fungi whose parasitic forms cause coccidioidomycosis (Valley fever) in mammalian hosts. We use an innovative interdisciplinary approach to analyze one-on-one encounters between human neutrophils and two forms of Coccidioides posadasii. To examine the mechanisms by which the innate immune system coordinates different stages of the host response to fungal pathogens, we dissect the immune-cell response into chemotaxis, adhesion, and phagocytosis. Our single-cell technique reveals a surprisingly strong response by initially quiescent neutrophils to close encounters with C. posadasii, both from a distance (by complement-mediated chemotaxis) as well as upon contact (by serum-dependent adhesion and phagocytosis). This response closely resembles neutrophil interactions with Candida albicans and zymosan particles, and is significantly stronger than the neutrophil responses to Cryptococcus neoformans, Aspergillus fumigatus, and Rhizopus oryzae under identical conditions. The vigorous in vitro neutrophil response suggests that C. posadasii evades in vivo recognition by neutrophils through suppression of long-range mobilization and recruitment of the immune cells. This observation elucidates an important paradigm of the recognition of microbes, i.e., that intact immunotaxis comprises an intricate spatiotemporal hierarchy of distinct chemotactic processes. Moreover, in contrast to earlier reports, human neutrophils exhibit vigorous chemotaxis toward, and frustrated phagocytosis of, the large spherules of C. posadasii under physiological-like conditions. Finally, neutrophils from healthy donors and patients with chronic coccidioidomycosis display subtle differences in their responses to antibodycoated beads, even though the patient cells appear to interact normally with C. posadasii endospores.

Original languageEnglish (US)
Article numbere0129522
JournalPLoS One
Volume10
Issue number6
DOIs
StatePublished - Jun 12 2015

Fingerprint

Coccidioides
endospores
adhesives
Adhesives
neutrophils
Neutrophils
Adhesion
Zymosan
Candida
Immune system
Aspergillus
Pathogens
coccidioidomycosis
Coccidioidomycosis
Fungi
chemotaxis
Chemotaxis
phagocytosis
Phagocytosis
adhesion

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Medicine(all)

Cite this

Coccidioides endospores and spherules draw strong chemotactic, adhesive, and phagocytic responses by individual human neutrophils. / Lee, Cheng Yuk; Thompson, George Richard; Hastey, Christine J.; Hodge, Gregory C.; Lunetta, Jennine M.; Pappagianis, Demosthenes; Heinrich, Volkmar.

In: PLoS One, Vol. 10, No. 6, e0129522, 12.06.2015.

Research output: Contribution to journalArticle

Lee, Cheng Yuk ; Thompson, George Richard ; Hastey, Christine J. ; Hodge, Gregory C. ; Lunetta, Jennine M. ; Pappagianis, Demosthenes ; Heinrich, Volkmar. / Coccidioides endospores and spherules draw strong chemotactic, adhesive, and phagocytic responses by individual human neutrophils. In: PLoS One. 2015 ; Vol. 10, No. 6.
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