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Dual transcriptome of the immediate neutrophil and Candida albicans interplay

Niemiec, Maria J. ; Grumaz, Christian ; Ermert, David LU ; Desel, Christiane ; Shankar, Madhu ; Lopes, José Pedro ; Mills, Ian G. ; Stevens, Philip ; Sohn, Kai and Urban, Constantin F. (2017) In BMC Genomics 18(1).
Abstract

Background: Neutrophils are traditionally considered transcriptionally inactive. Compared to other immune cells, little is known about their transcriptional profile during interaction with pathogens. Methods: We analyzed the meta-transcriptome of the neutrophil-Candida albicans interplay and the transcriptome of C. albicans challenged with neutrophil extracellular traps (NETs) by RNA-Seq, considering yeast and hypha individually in each approach. Results: The neutrophil response to C. albicans yeast and hyphae was dominated by a morphotype-independent core response. However, 11% of all differentially expressed genes were regulated in a specific manner when neutrophils encountered the hyphal form of C. albicans. While involving genes for... (More)

Background: Neutrophils are traditionally considered transcriptionally inactive. Compared to other immune cells, little is known about their transcriptional profile during interaction with pathogens. Methods: We analyzed the meta-transcriptome of the neutrophil-Candida albicans interplay and the transcriptome of C. albicans challenged with neutrophil extracellular traps (NETs) by RNA-Seq, considering yeast and hypha individually in each approach. Results: The neutrophil response to C. albicans yeast and hyphae was dominated by a morphotype-independent core response. However, 11% of all differentially expressed genes were regulated in a specific manner when neutrophils encountered the hyphal form of C. albicans. While involving genes for transcriptional regulators, receptors, and cytokines, the neutrophil core response lacked typical antimicrobial effectors genes. Genes of the NOD-like receptor pathway, including NLRP3, were enriched. Neutrophil- and NET-provoked responses in C. albicans differed. At the same time, the Candida transcriptome upon neutrophil encounter and upon NET challenge included genes from various metabolic processes and indicate a mutual role of the regulators Tup1p, Efg1p, Hap43p, and Cap1p. Upon challenge with neutrophils and NETs, the overall Candida response was partially morphotype-specific. Yet again, actual oppositional regulation in yeasts and hyphae was only detected for the arginine metabolism in neutrophil-infecting C. albicans. Conclusions: Taken together, our study provides a comprehensive and quantitative transcript profile of the neutrophil-C. albicans interaction. By considering the two major appearances of both, neutrophils and C. albicans, our study reveals yet undescribed insights into this medically relevant encounter. Hence, our findings will facilitate future research and potentially inspire novel therapy developments.

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author
; ; ; ; ; ; ; ; and
organization
publishing date
type
Contribution to journal
publication status
published
subject
keywords
Candida, Dual transcriptome, Extracellular traps, Morphotype, Neutrophils, NOD-like receptor pathway, Nutritional immunity
in
BMC Genomics
volume
18
issue
1
article number
696
publisher
BioMed Central (BMC)
external identifiers
  • pmid:28874114
  • wos:000409208200002
  • scopus:85028808388
ISSN
1471-2164
DOI
10.1186/s12864-017-4097-4
language
English
LU publication?
yes
id
daff1333-f078-4716-bcb5-92ce36f25131
date added to LUP
2017-11-28 14:11:17
date last changed
2024-04-14 22:54:52
@article{daff1333-f078-4716-bcb5-92ce36f25131,
  abstract     = {{<p>Background: Neutrophils are traditionally considered transcriptionally inactive. Compared to other immune cells, little is known about their transcriptional profile during interaction with pathogens. Methods: We analyzed the meta-transcriptome of the neutrophil-Candida albicans interplay and the transcriptome of C. albicans challenged with neutrophil extracellular traps (NETs) by RNA-Seq, considering yeast and hypha individually in each approach. Results: The neutrophil response to C. albicans yeast and hyphae was dominated by a morphotype-independent core response. However, 11% of all differentially expressed genes were regulated in a specific manner when neutrophils encountered the hyphal form of C. albicans. While involving genes for transcriptional regulators, receptors, and cytokines, the neutrophil core response lacked typical antimicrobial effectors genes. Genes of the NOD-like receptor pathway, including NLRP3, were enriched. Neutrophil- and NET-provoked responses in C. albicans differed. At the same time, the Candida transcriptome upon neutrophil encounter and upon NET challenge included genes from various metabolic processes and indicate a mutual role of the regulators Tup1p, Efg1p, Hap43p, and Cap1p. Upon challenge with neutrophils and NETs, the overall Candida response was partially morphotype-specific. Yet again, actual oppositional regulation in yeasts and hyphae was only detected for the arginine metabolism in neutrophil-infecting C. albicans. Conclusions: Taken together, our study provides a comprehensive and quantitative transcript profile of the neutrophil-C. albicans interaction. By considering the two major appearances of both, neutrophils and C. albicans, our study reveals yet undescribed insights into this medically relevant encounter. Hence, our findings will facilitate future research and potentially inspire novel therapy developments.</p>}},
  author       = {{Niemiec, Maria J. and Grumaz, Christian and Ermert, David and Desel, Christiane and Shankar, Madhu and Lopes, José Pedro and Mills, Ian G. and Stevens, Philip and Sohn, Kai and Urban, Constantin F.}},
  issn         = {{1471-2164}},
  keywords     = {{Candida; Dual transcriptome; Extracellular traps; Morphotype; Neutrophils; NOD-like receptor pathway; Nutritional immunity}},
  language     = {{eng}},
  month        = {{09}},
  number       = {{1}},
  publisher    = {{BioMed Central (BMC)}},
  series       = {{BMC Genomics}},
  title        = {{Dual transcriptome of the immediate neutrophil and Candida albicans interplay}},
  url          = {{http://dx.doi.org/10.1186/s12864-017-4097-4}},
  doi          = {{10.1186/s12864-017-4097-4}},
  volume       = {{18}},
  year         = {{2017}},
}