Induction of Krüppel-Like Factor 4 Mediates Polymorphonuclear Neutrophil Activation in Streptococcus pneumoniae Infection
The recruitment and activation of polymorphonuclear neutrophils (PMNs) are of central importance for the elimination of pathogens in bacterial infections. We investigated the Streptococcus pneumoniae -dependent induction of the transcription factor Krüppel-like factor (KLF) 4 in PMNs as a potential...
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| Published in | Frontiers in microbiology Vol. 11; p. 582070 |
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| Main Authors | , , , , , , , |
| Format | Journal Article |
| Language | English |
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03.02.2021
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| Abstract | The recruitment and activation of polymorphonuclear neutrophils (PMNs) are of central importance for the elimination of pathogens in bacterial infections. We investigated the
Streptococcus pneumoniae
-dependent induction of the transcription factor Krüppel-like factor (KLF) 4 in PMNs as a potential regulator of PMN activation. We found that KLF4 expression is induced in human blood-derived PMNs in a time- and dose-dependent manner by wild-type
S. pneumoniae
and capsule knockout mutants. Unencapsulated knockout mutants induced stronger KLF4 expression than encapsulated wild types. The presence of autolysin LytA-competent (thus viable) pneumococci and LytA-mediated bacterial autolysis were required for KLF4 induction in human and murine PMNs. LyzMcre-mediated knockdown of KLF4 in murine blood-derived PMNs revealed that KLF4 influences pneumococci killing and increases the release of the proinflammatory cytokines tumor necrosis factor α and keratinocyte chemoattractant and decreases the release of the anti-inflammatory cytokine interleukin-10. Thus,
S. pneumoniae
induces KLF4 expression in PMNs, which contributes to PMN activation in
S. pneumoniae
infection. |
|---|---|
| AbstractList | The recruitment and activation of polymorphonuclear neutrophils (PMNs) are of central importance for the elimination of pathogens in bacterial infections. We investigated the
-dependent induction of the transcription factor Krüppel-like factor (KLF) 4 in PMNs as a potential regulator of PMN activation. We found that KLF4 expression is induced in human blood-derived PMNs in a time- and dose-dependent manner by wild-type
and capsule knockout mutants. Unencapsulated knockout mutants induced stronger KLF4 expression than encapsulated wild types. The presence of autolysin LytA-competent (thus viable) pneumococci and LytA-mediated bacterial autolysis were required for KLF4 induction in human and murine PMNs. LyzMcre-mediated knockdown of KLF4 in murine blood-derived PMNs revealed that KLF4 influences pneumococci killing and increases the release of the proinflammatory cytokines tumor necrosis factor α and keratinocyte chemoattractant and decreases the release of the anti-inflammatory cytokine interleukin-10. Thus,
induces KLF4 expression in PMNs, which contributes to PMN activation in
infection. The recruitment and activation of polymorphonuclear neutrophils (PMNs) are of central importance for the elimination of pathogens in bacterial infections. We investigated the Streptococcus pneumoniae-dependent induction of the transcription factor Krüppel-like factor (KLF) 4 in PMNs as a potential regulator of PMN activation. We found that KLF4 expression is induced in human blood-derived PMNs in a time- and dose-dependent manner by wild-type S. pneumoniae and capsule knockout mutants. Unencapsulated knockout mutants induced stronger KLF4 expression than encapsulated wild types. The presence of autolysin LytA-competent (thus viable) pneumococci and LytA-mediated bacterial autolysis were required for KLF4 induction in human and murine PMNs. LyzMcre-mediated knockdown of KLF4 in murine blood-derived PMNs revealed that KLF4 influences pneumococci killing and increases the release of the proinflammatory cytokines tumor necrosis factor α and keratinocyte chemoattractant and decreases the release of the anti-inflammatory cytokine interleukin-10. Thus, S. pneumoniae induces KLF4 expression in PMNs, which contributes to PMN activation in S. pneumoniae infection. The recruitment and activation of polymorphonuclear neutrophils (PMNs) are of central importance for the elimination of pathogens in bacterial infections. We investigated the Streptococcus pneumoniae-dependent induction of the transcription factor Krüppel-like factor (KLF) 4 in PMNs as a potential regulator of PMN activation. We found that KLF4 expression is induced in human blood-derived PMNs in a time- and dose-dependent manner by wild-type S. pneumoniae and capsule knockout mutants. Unencapsulated knockout mutants induced stronger KLF4 expression than encapsulated wild types. The presence of autolysin LytA-competent (thus viable) pneumococci and LytA-mediated bacterial autolysis were required for KLF4 induction in human and murine PMNs. LyzMcre-mediated knockdown of KLF4 in murine blood-derived PMNs revealed that KLF4 influences pneumococci killing and increases the release of the proinflammatory cytokines tumor necrosis factor α and keratinocyte chemoattractant and decreases the release of the anti-inflammatory cytokine interleukin-10. Thus, S. pneumoniae induces KLF4 expression in PMNs, which contributes to PMN activation in S. pneumoniae infection.The recruitment and activation of polymorphonuclear neutrophils (PMNs) are of central importance for the elimination of pathogens in bacterial infections. We investigated the Streptococcus pneumoniae-dependent induction of the transcription factor Krüppel-like factor (KLF) 4 in PMNs as a potential regulator of PMN activation. We found that KLF4 expression is induced in human blood-derived PMNs in a time- and dose-dependent manner by wild-type S. pneumoniae and capsule knockout mutants. Unencapsulated knockout mutants induced stronger KLF4 expression than encapsulated wild types. The presence of autolysin LytA-competent (thus viable) pneumococci and LytA-mediated bacterial autolysis were required for KLF4 induction in human and murine PMNs. LyzMcre-mediated knockdown of KLF4 in murine blood-derived PMNs revealed that KLF4 influences pneumococci killing and increases the release of the proinflammatory cytokines tumor necrosis factor α and keratinocyte chemoattractant and decreases the release of the anti-inflammatory cytokine interleukin-10. Thus, S. pneumoniae induces KLF4 expression in PMNs, which contributes to PMN activation in S. pneumoniae infection. The recruitment and activation of polymorphonuclear neutrophils (PMNs) are of central importance for the elimination of pathogens in bacterial infections. We investigated the Streptococcus pneumoniae -dependent induction of the transcription factor Krüppel-like factor (KLF) 4 in PMNs as a potential regulator of PMN activation. We found that KLF4 expression is induced in human blood-derived PMNs in a time- and dose-dependent manner by wild-type S. pneumoniae and capsule knockout mutants. Unencapsulated knockout mutants induced stronger KLF4 expression than encapsulated wild types. The presence of autolysin LytA-competent (thus viable) pneumococci and LytA-mediated bacterial autolysis were required for KLF4 induction in human and murine PMNs. LyzMcre-mediated knockdown of KLF4 in murine blood-derived PMNs revealed that KLF4 influences pneumococci killing and increases the release of the proinflammatory cytokines tumor necrosis factor α and keratinocyte chemoattractant and decreases the release of the anti-inflammatory cytokine interleukin-10. Thus, S. pneumoniae induces KLF4 expression in PMNs, which contributes to PMN activation in S. pneumoniae infection. |
| Author | Bhattacharyya, Aritra Conrad, Claudia Herta, Toni Frey, Doris Zahlten, Janine Hippenstiel, Stefan Suttorp, Norbert García, Pedro |
| AuthorAffiliation | 2 Departamento de Biotecnología Microbiana y de Plantas, Centro de Investigaciones Biológicas Margarita Salas, Consejo Superior de Investigaciones Científicas , Madrid , Spain 3 CIBER de Enfermedades Respiratorias , Madrid , Spain 1 Department of Infectious Diseases and Respiratory Medicine, Charité – Universitätsmedizin Berlin , Berlin , Germany |
| AuthorAffiliation_xml | – name: 1 Department of Infectious Diseases and Respiratory Medicine, Charité – Universitätsmedizin Berlin , Berlin , Germany – name: 3 CIBER de Enfermedades Respiratorias , Madrid , Spain – name: 2 Departamento de Biotecnología Microbiana y de Plantas, Centro de Investigaciones Biológicas Margarita Salas, Consejo Superior de Investigaciones Científicas , Madrid , Spain |
| Author_xml | – sequence: 1 givenname: Aritra surname: Bhattacharyya fullname: Bhattacharyya, Aritra – sequence: 2 givenname: Toni surname: Herta fullname: Herta, Toni – sequence: 3 givenname: Claudia surname: Conrad fullname: Conrad, Claudia – sequence: 4 givenname: Doris surname: Frey fullname: Frey, Doris – sequence: 5 givenname: Pedro surname: García fullname: García, Pedro – sequence: 6 givenname: Norbert surname: Suttorp fullname: Suttorp, Norbert – sequence: 7 givenname: Stefan surname: Hippenstiel fullname: Hippenstiel, Stefan – sequence: 8 givenname: Janine surname: Zahlten fullname: Zahlten, Janine |
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| CitedBy_id | crossref_primary_10_1016_j_phrs_2024_107345 crossref_primary_10_3389_fimmu_2021_745854 crossref_primary_10_1093_jleuko_qiad070 crossref_primary_10_3389_fimmu_2021_726135 |
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| Copyright | Copyright © 2021 Bhattacharyya, Herta, Conrad, Frey, García, Suttorp, Hippenstiel and Zahlten. Copyright © 2021 Bhattacharyya, Herta, Conrad, Frey, García, Suttorp, Hippenstiel and Zahlten. 2021 Bhattacharyya, Herta, Conrad, Frey, García, Suttorp, Hippenstiel and Zahlten |
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| Keywords | S. pneumoniae innate immunity neutrophils infectious diseases Krüppel-like factor 4 |
| Language | English |
| License | Copyright © 2021 Bhattacharyya, Herta, Conrad, Frey, García, Suttorp, Hippenstiel and Zahlten. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Reviewed by: Ganjana Lertmemongkolchai, Khon Kaen University, Thailand; Jeremy Brown, University College London, United Kingdom This article was submitted to Microbial Immunology, a section of the journal Frontiers in Microbiology Edited by: Tamás Laskay, University of Lübeck, Germany |
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| SubjectTerms | infectious diseases innate immunity Krüppel-like factor 4 Microbiology neutrophils S. pneumoniae |
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| Title | Induction of Krüppel-Like Factor 4 Mediates Polymorphonuclear Neutrophil Activation in Streptococcus pneumoniae Infection |
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