Dual transcriptome of the immediate neutrophil and Candida albicans interplay

Maria J. Niemiec, Christian Grumaz, David Ermert, Christiane Desel, Madhu Shankar, José Pedro Lopes, Ian G. Mills, Philip Stevens, Kai Sohn, Constantin F. Urban

Research output: Contribution to journalArticleResearchpeer-review

9 Citations (Scopus)

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 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.

Original languageEnglish
Article number696
Number of pages21
JournalBMC Genomics
Volume18
Issue number1
DOIs
Publication statusPublished - 6 Sep 2017
Externally publishedYes

Keywords

  • Candida
  • Dual transcriptome
  • Extracellular traps
  • Morphotype
  • Neutrophils
  • NOD-like receptor pathway
  • Nutritional immunity

Cite this

Niemiec, M. J., Grumaz, C., Ermert, D., Desel, C., Shankar, M., Lopes, J. P., ... Urban, C. F. (2017). Dual transcriptome of the immediate neutrophil and Candida albicans interplay. BMC Genomics, 18(1), [696]. https://doi.org/10.1186/s12864-017-4097-4
Niemiec, Maria J. ; Grumaz, Christian ; Ermert, David ; Desel, Christiane ; Shankar, Madhu ; Lopes, José Pedro ; Mills, Ian G. ; Stevens, Philip ; Sohn, Kai ; Urban, Constantin F. / Dual transcriptome of the immediate neutrophil and Candida albicans interplay. In: BMC Genomics. 2017 ; Vol. 18, No. 1.
@article{732535c3624c4b83b71fb444553b5d6c,
title = "Dual transcriptome of the immediate neutrophil and Candida albicans interplay",
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 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.",
keywords = "Candida, Dual transcriptome, Extracellular traps, Morphotype, Neutrophils, NOD-like receptor pathway, Nutritional immunity",
author = "Niemiec, {Maria J.} and Christian Grumaz and David Ermert and Christiane Desel and Madhu Shankar and Lopes, {Jos{\'e} Pedro} and Mills, {Ian G.} and Philip Stevens and Kai Sohn and Urban, {Constantin F.}",
year = "2017",
month = "9",
day = "6",
doi = "10.1186/s12864-017-4097-4",
language = "English",
volume = "18",
journal = "BMC Genomics",
issn = "1471-2164",
publisher = "BioMed Central",
number = "1",

}

Niemiec, MJ, Grumaz, C, Ermert, D, Desel, C, Shankar, M, Lopes, JP, Mills, IG, Stevens, P, Sohn, K & Urban, CF 2017, 'Dual transcriptome of the immediate neutrophil and Candida albicans interplay', BMC Genomics, vol. 18, no. 1, 696. https://doi.org/10.1186/s12864-017-4097-4

Dual transcriptome of the immediate neutrophil and Candida albicans interplay. / Niemiec, Maria J.; Grumaz, Christian; Ermert, David; Desel, Christiane; Shankar, Madhu; Lopes, José Pedro; Mills, Ian G.; Stevens, Philip; Sohn, Kai; Urban, Constantin F.

In: BMC Genomics, Vol. 18, No. 1, 696, 06.09.2017.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Dual transcriptome of the immediate neutrophil and Candida albicans interplay

AU - Niemiec, Maria J.

AU - Grumaz, Christian

AU - Ermert, David

AU - Desel, Christiane

AU - Shankar, Madhu

AU - Lopes, José Pedro

AU - Mills, Ian G.

AU - Stevens, Philip

AU - Sohn, Kai

AU - Urban, Constantin F.

PY - 2017/9/6

Y1 - 2017/9/6

N2 - 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.

AB - 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.

KW - Candida

KW - Dual transcriptome

KW - Extracellular traps

KW - Morphotype

KW - Neutrophils

KW - NOD-like receptor pathway

KW - Nutritional immunity

UR - http://www.scopus.com/inward/record.url?scp=85028808388&partnerID=8YFLogxK

U2 - 10.1186/s12864-017-4097-4

DO - 10.1186/s12864-017-4097-4

M3 - Article

VL - 18

JO - BMC Genomics

JF - BMC Genomics

SN - 1471-2164

IS - 1

M1 - 696

ER -