Dissection of the NKG2C NK cell response against Puumala Orthohantavirus.

<h4>Background</h4>Infections with the Puumala orthohantavirus (PUUV) in humans may cause hemorrhagic fever with renal syndrome (HFRS), known as nephropathia epidemica (NE), which is associated with acute renal failure in severe cases. In response to PUUV-infections, a subset of potent a...

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Main Authors: Hannes Vietzen, Svenja Hartenberger, Stephan W Aberle, Elisabeth Puchhammer-Stöckl
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2021-12-01
Series:PLoS Neglected Tropical Diseases
Online Access:https://journals.plos.org/plosntds/article/file?id=10.1371/journal.pntd.0010006&type=printable
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author Hannes Vietzen
Svenja Hartenberger
Stephan W Aberle
Elisabeth Puchhammer-Stöckl
author_facet Hannes Vietzen
Svenja Hartenberger
Stephan W Aberle
Elisabeth Puchhammer-Stöckl
author_sort Hannes Vietzen
collection DOAJ
description <h4>Background</h4>Infections with the Puumala orthohantavirus (PUUV) in humans may cause hemorrhagic fever with renal syndrome (HFRS), known as nephropathia epidemica (NE), which is associated with acute renal failure in severe cases. In response to PUUV-infections, a subset of potent antiviral NKG2C+ NK cells expand, whose role in virus defence and pathogenesis of NE is unclear. NKG2C+ NK cell proliferation is mediated by binding of NKG2C/CD94 to HLA-E on infected cells. The proliferation and activation of NKG2C+ NK cells via the NKG2C/HLA-E axis is affected by different NKG2C (NKG2Cwt/del) and HLA-E (HLA-E*0101/0103) alleles, which naturally occur in the human host. Homozygous (NKG2Cdel/del) and heterozygous (NKG2Cwt/del) deletions of the NKG2C receptor results in an impaired NKG2C/CD94 mediated proliferation and activation of NKG2C+ cells. We therefore analyzed the PUUV-mediated NKG2C+ NK cell responses and the impact of different NKG2C and HLA-E alleles in NE patients.<h4>Methodology/principal findings</h4>NKG2C+ NK cell expansion and effector functions in PUUV-infected cells were investigated using flow cytometry and it was shown that PUUV-infected endothelial cells led to a NKG2C/CD94 mediated NKG2C+ NK cell activation and expansion, dependent on the HLA-G-mediated upregulation of HLA-E. Furthermore, the NKG2Cdel and HLA-E*0101/0103 alleles were determined in 130 NE patients and 130 matched controls, and it was shown that in NE patients the NKG2Cwt/del allele was significantly overrepresented, compared to the NKG2Cwt/wt variant (p = 0.01). In addition, in vitro analysis revealed that NKG2Cwt/del NK cells exhibited on overall a lower proliferation (p = 0.002) and lower IFNγ expression (p = 0.004) than NKG2Cwt/wt NK cells.<h4>Conclusions/significance</h4>Our results corroborate the substantial impact of the NKG2C/HLA-E axis on PUUV-specific NK cell responses. A weak NKG2C+ NK cell response, as reflected by NKG2Cwt/del variant, may be associated with a higher risk for a severe hantavirus infections.
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spelling doaj-art-fe4868e1fef4403d9cd55042d513802d2025-08-20T02:55:31ZengPublic Library of Science (PLoS)PLoS Neglected Tropical Diseases1935-27271935-27352021-12-011512e001000610.1371/journal.pntd.0010006Dissection of the NKG2C NK cell response against Puumala Orthohantavirus.Hannes VietzenSvenja HartenbergerStephan W AberleElisabeth Puchhammer-Stöckl<h4>Background</h4>Infections with the Puumala orthohantavirus (PUUV) in humans may cause hemorrhagic fever with renal syndrome (HFRS), known as nephropathia epidemica (NE), which is associated with acute renal failure in severe cases. In response to PUUV-infections, a subset of potent antiviral NKG2C+ NK cells expand, whose role in virus defence and pathogenesis of NE is unclear. NKG2C+ NK cell proliferation is mediated by binding of NKG2C/CD94 to HLA-E on infected cells. The proliferation and activation of NKG2C+ NK cells via the NKG2C/HLA-E axis is affected by different NKG2C (NKG2Cwt/del) and HLA-E (HLA-E*0101/0103) alleles, which naturally occur in the human host. Homozygous (NKG2Cdel/del) and heterozygous (NKG2Cwt/del) deletions of the NKG2C receptor results in an impaired NKG2C/CD94 mediated proliferation and activation of NKG2C+ cells. We therefore analyzed the PUUV-mediated NKG2C+ NK cell responses and the impact of different NKG2C and HLA-E alleles in NE patients.<h4>Methodology/principal findings</h4>NKG2C+ NK cell expansion and effector functions in PUUV-infected cells were investigated using flow cytometry and it was shown that PUUV-infected endothelial cells led to a NKG2C/CD94 mediated NKG2C+ NK cell activation and expansion, dependent on the HLA-G-mediated upregulation of HLA-E. Furthermore, the NKG2Cdel and HLA-E*0101/0103 alleles were determined in 130 NE patients and 130 matched controls, and it was shown that in NE patients the NKG2Cwt/del allele was significantly overrepresented, compared to the NKG2Cwt/wt variant (p = 0.01). In addition, in vitro analysis revealed that NKG2Cwt/del NK cells exhibited on overall a lower proliferation (p = 0.002) and lower IFNγ expression (p = 0.004) than NKG2Cwt/wt NK cells.<h4>Conclusions/significance</h4>Our results corroborate the substantial impact of the NKG2C/HLA-E axis on PUUV-specific NK cell responses. A weak NKG2C+ NK cell response, as reflected by NKG2Cwt/del variant, may be associated with a higher risk for a severe hantavirus infections.https://journals.plos.org/plosntds/article/file?id=10.1371/journal.pntd.0010006&type=printable
spellingShingle Hannes Vietzen
Svenja Hartenberger
Stephan W Aberle
Elisabeth Puchhammer-Stöckl
Dissection of the NKG2C NK cell response against Puumala Orthohantavirus.
PLoS Neglected Tropical Diseases
title Dissection of the NKG2C NK cell response against Puumala Orthohantavirus.
title_full Dissection of the NKG2C NK cell response against Puumala Orthohantavirus.
title_fullStr Dissection of the NKG2C NK cell response against Puumala Orthohantavirus.
title_full_unstemmed Dissection of the NKG2C NK cell response against Puumala Orthohantavirus.
title_short Dissection of the NKG2C NK cell response against Puumala Orthohantavirus.
title_sort dissection of the nkg2c nk cell response against puumala orthohantavirus
url https://journals.plos.org/plosntds/article/file?id=10.1371/journal.pntd.0010006&type=printable
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AT svenjahartenberger dissectionofthenkg2cnkcellresponseagainstpuumalaorthohantavirus
AT stephanwaberle dissectionofthenkg2cnkcellresponseagainstpuumalaorthohantavirus
AT elisabethpuchhammerstockl dissectionofthenkg2cnkcellresponseagainstpuumalaorthohantavirus