Human Herpesvirus 8 (HHV8) Sequentially Shapes the NK Cell Repertoire during the Course of Asymptomatic Infection and Kaposi Sarcoma

The contribution of innate immunity to immunosurveillance of the oncogenic Human Herpes Virus 8 (HHV8) has not been studied in depth. We investigated NK cell phenotype and function in 70 HHV8-infected subjects, either asymptomatic carriers or having developed Kaposi's sarcoma (KS). Our results...

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Published inPLoS pathogens Vol. 8; no. 1; p. e1002486
Main Authors Dupuy, Stéphanie, Lambert, Marion, Zucman, David, Choukem, Siméon-Pierre, Tognarelli, Sara, Pages, Cécile, Lebbé, Céleste, Caillat-Zucman, Sophie
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.01.2012
Public Library of Science (PLoS)
Subjects
Asymptomatic Infections
Base Sequence
Biology
Cells
Cells, Cultured
Development and progression
Health aspects
Herpesviridae Infections - complications
Herpesviridae Infections - immunology
Herpesviridae Infections - virology
Herpesvirus
Herpesvirus 8, Human - immunology
Herpesvirus 8, Human - physiology
HIV Infections - complications
HIV Infections - immunology
HIV-1 - immunology
HIV-1 - physiology
Human herpesvirus 8
Humans
Immune system
Immunology
Infections
Kaposi's sarcoma
Killer cells
Killer Cells, Natural - classification
Killer Cells, Natural - immunology
Killer Cells, Natural - metabolism
Lymphocyte Activation - physiology
Medicine
Middle Aged
Molecular Sequence Data
NK Cell Lectin-Like Receptor Subfamily K - metabolism
Phenotype
Physiological aspects
Proteins
Sarcoma
Sarcoma, Kaposi - complications
Sarcoma, Kaposi - immunology
Sarcoma, Kaposi - virology
Virus Latency - genetics
Virus Latency - immunology
France
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Abstract The contribution of innate immunity to immunosurveillance of the oncogenic Human Herpes Virus 8 (HHV8) has not been studied in depth. We investigated NK cell phenotype and function in 70 HHV8-infected subjects, either asymptomatic carriers or having developed Kaposi's sarcoma (KS). Our results revealed substantial alterations of the NK cell receptor repertoire in healthy HHV8 carriers, with reduced expression of NKp30, NKp46 and CD161 receptors. In addition, down-modulation of the activating NKG2D receptor, associated with impaired NK-cell lytic capacity, was observed in patients with active KS. Resolution of KS after treatment was accompanied with restoration of NKG2D levels and NK cell activity. HHV8-latently infected endothelial cells overexpressed ligands of several NK cell receptors, including NKG2D ligands. The strong expression of NKG2D ligands by tumor cells was confirmed in situ by immunohistochemical staining of KS biopsies. However, no tumor-infiltrating NK cells were detected, suggesting a defect in NK cell homing or survival in the KS microenvironment. Among the known KS-derived immunoregulatory factors, we identified prostaglandin E2 (PGE2) as a critical element responsible for the down-modulation of NKG2D expression on resting NK cells. Moreover, PGE2 prevented up-regulation of the NKG2D and NKp30 receptors on IL-15-activated NK cells, and inhibited the IL-15-induced proliferation and survival of NK cells. Altogether, our observations are consistent with distinct immunoevasion mechanisms that allow HHV8 to escape NK cell responses stepwise, first at early stages of infection to facilitate the maintenance of viral latency, and later to promote tumor cell growth through suppression of NKG2D-mediated functions. Importantly, our results provide additional support to the use of PGE2 inhibitors as an attractive approach to treat aggressive KS, as they could restore activation and survival of tumoricidal NK cells.
AbstractList The contribution of innate immunity to immunosurveillance of the oncogenic Human Herpes Virus 8 (HHV8) has not been studied in depth. We investigated NK cell phenotype and function in 70 HHV8-infected subjects, either asymptomatic carriers or having developed Kaposi's sarcoma (KS). Our results revealed substantial alterations of the NK cell receptor repertoire in healthy HHV8 carriers, with reduced expression of NKp30, NKp46 and CD161 receptors. In addition, down-modulation of the activating NKG2D receptor, associated with impaired NK-cell lytic capacity, was observed in patients with active KS. Resolution of KS after treatment was accompanied with restoration of NKG2D levels and NK cell activity. HHV8-latently infected endothelial cells overexpressed ligands of several NK cell receptors, including NKG2D ligands. The strong expression of NKG2D ligands by tumor cells was confirmed in situ by immunohistochemical staining of KS biopsies. However, no tumor-infiltrating NK cells were detected, suggesting a defect in NK cell homing or survival in the KS microenvironment. Among the known KS-derived immunoregulatory factors, we identified prostaglandin E2 (PGE2) as a critical element responsible for the down-modulation of NKG2D expression on resting NK cells. Moreover, PGE2 prevented up-regulation of the NKG2D and NKp30 receptors on IL-15-activated NK cells, and inhibited the IL-15-induced proliferation and survival of NK cells. Altogether, our observations are consistent with distinct immunoevasion mechanisms that allow HHV8 to escape NK cell responses stepwise, first at early stages of infection to facilitate the maintenance of viral latency, and later to promote tumor cell growth through suppression of NKG2D-mediated functions. Importantly, our results provide additional support to the use of PGE2 inhibitors as an attractive approach to treat aggressive KS, as they could restore activation and survival of tumoricidal NK cells. Natural Killer (NK) cells are part of the innate immune response against virus infections and tumors. Their activation is the net result of signals emanating from a panel of inhibitory and activating receptors recognizing specific ligands on target cells. Human Herpes Virus 8 (HHV8) is an oncogenic virus responsible of Kaposi Sarcoma (KS), a multifocal angiogenic tumor. How NK cells contribute to the control of infection by HHV8 infection and development of KS, is unclear. In this paper, we show different strategies used by HHV8 to escape NK cell response. Patients with asymptomatic infection or KS have down-modulated expression of NKp30, NKp46 and CD161 receptors. In addition, patients with active KS show additional down-modulation of the NKG2D activating receptor, associated with impaired NK-cell cytotoxicity against target cells. Resolution of KS correlates with regained NKG2D expression and cytotoxic function. We present evidence that down-modulation of NKG2D is mediated by inflammatory prostaglandin E2 (PGE2), known to be released by KS cells, and show that PGE2 acts by preventing IL-15-mediated activation of NK cells. These results strongly support the use of PGE2 inhibitors as an attractive approach to treat active KS.
The contribution of innate immunity to immunosurveillance of the oncogenic Human Herpes Virus 8 (HHV8) has not been studied in depth. We investigated NK cell phenotype and function in 70 HHV8-infected subjects, either asymptomatic carriers or having developed Kaposi's sarcoma (KS). Our results revealed substantial alterations of the NK cell receptor repertoire in healthy HHV8 carriers, with reduced expression of NKp30, NKp46 and CD161 receptors. In addition, down-modulation of the activating NKG2D receptor, associated with impaired NK-cell lytic capacity, was observed in patients with active KS. Resolution of KS after treatment was accompanied with restoration of NKG2D levels and NK cell activity. HHV8-latently infected endothelial cells overexpressed ligands of several NK cell receptors, including NKG2D ligands. The strong expression of NKG2D ligands by tumor cells was confirmed in situ by immunohistochemical staining of KS biopsies. However, no tumor-infiltrating NK cells were detected, suggesting a defect in NK cell homing or survival in the KS microenvironment. Among the known KS-derived immunoregulatory factors, we identified prostaglandin E2 (PGE2) as a critical element responsible for the down-modulation of NKG2D expression on resting NK cells. Moreover, PGE2 prevented up-regulation of the NKG2D and NKp30 receptors on IL-15-activated NK cells, and inhibited the IL-15-induced proliferation and survival of NK cells. Altogether, our observations are consistent with distinct immunoevasion mechanisms that allow HHV8 to escape NK cell responses stepwise, first at early stages of infection to facilitate the maintenance of viral latency, and later to promote tumor cell growth through suppression of NKG2D-mediated functions. Importantly, our results provide additional support to the use of PGE2 inhibitors as an attractive approach to treat aggressive KS, as they could restore activation and survival of tumoricidal NK cells. Natural Killer (NK) cells are part of the innate immune response against virus infections and tumors. Their activation is the net result of signals emanating from a panel of inhibitory and activating receptors recognizing specific ligands on target cells. Human Herpes Virus 8 (HHV8) is an oncogenic virus responsible of Kaposi Sarcoma (KS), a multifocal angiogenic tumor. How NK cells contribute to the control of infection by HHV8 infection and development of KS, is unclear. In this paper, we show different strategies used by HHV8 to escape NK cell response. Patients with asymptomatic infection or KS have down-modulated expression of NKp30, NKp46 and CD161 receptors. In addition, patients with active KS show additional down-modulation of the NKG2D activating receptor, associated with impaired NK-cell cytotoxicity against target cells. Resolution of KS correlates with regained NKG2D expression and cytotoxic function. We present evidence that down-modulation of NKG2D is mediated by inflammatory prostaglandin E2 (PGE2), known to be released by KS cells, and show that PGE2 acts by preventing IL-15-mediated activation of NK cells. These results strongly support the use of PGE2 inhibitors as an attractive approach to treat active KS.
The contribution of innate immunity to immunosurveillance of the oncogenic Human Herpes Virus 8 (HHV8) has not been studied in depth. We investigated NK cell phenotype and function in 70 HHV8-infected subjects, either asymptomatic carriers or having developed Kaposi's sarcoma (KS). Our results revealed substantial alterations of the NK cell receptor repertoire in healthy HHV8 carriers, with reduced expression of NKp30, NKp46 and CD161 receptors. In addition, down-modulation of the activating NKG2D receptor, associated with impaired NK-cell lytic capacity, was observed in patients with active KS. Resolution of KS after treatment was accompanied with restoration of NKG2D levels and NK cell activity. HHV8-latently infected endothelial cells overexpressed ligands of several NK cell receptors, including NKG2D ligands. The strong expression of NKG2D ligands by tumor cells was confirmed in situ by immunohistochemical staining of KS biopsies. However, no tumor-infiltrating NK cells were detected, suggesting a defect in NK cell homing or survival in the KS microenvironment. Among the known KS-derived immunoregulatory factors, we identified prostaglandin E2 (PGE2) as a critical element responsible for the down-modulation of NKG2D expression on resting NK cells. Moreover, PGE2 prevented up-regulation of the NKG2D and NKp30 receptors on IL-15-activated NK cells, and inhibited the IL-15-induced proliferation and survival of NK cells. Altogether, our observations are consistent with distinct immunoevasion mechanisms that allow HHV8 to escape NK cell responses stepwise, first at early stages of infection to facilitate the maintenance of viral latency, and later to promote tumor cell growth through suppression of NKG2D-mediated functions. Importantly, our results provide additional support to the use of PGE2 inhibitors as an attractive approach to treat aggressive KS, as they could restore activation and survival of tumoricidal NK cells.
  The contribution of innate immunity to immunosurveillance of the oncogenic Human Herpes Virus 8 (HHV8) has not been studied in depth. We investigated NK cell phenotype and function in 70 HHV8-infected subjects, either asymptomatic carriers or having developed Kaposi's sarcoma (KS). Our results revealed substantial alterations of the NK cell receptor repertoire in healthy HHV8 carriers, with reduced expression of NKp30, NKp46 and CD161 receptors. In addition, down-modulation of the activating NKG2D receptor, associated with impaired NK-cell lytic capacity, was observed in patients with active KS. Resolution of KS after treatment was accompanied with restoration of NKG2D levels and NK cell activity. HHV8-latently infected endothelial cells overexpressed ligands of several NK cell receptors, including NKG2D ligands. The strong expression of NKG2D ligands by tumor cells was confirmed in situ by immunohistochemical staining of KS biopsies. However, no tumor-infiltrating NK cells were detected, suggesting a defect in NK cell homing or survival in the KS microenvironment. Among the known KS-derived immunoregulatory factors, we identified prostaglandin E2 (PGE2) as a critical element responsible for the down-modulation of NKG2D expression on resting NK cells. Moreover, PGE2 prevented up-regulation of the NKG2D and NKp30 receptors on IL-15-activated NK cells, and inhibited the IL-15-induced proliferation and survival of NK cells. Altogether, our observations are consistent with distinct immunoevasion mechanisms that allow HHV8 to escape NK cell responses stepwise, first at early stages of infection to facilitate the maintenance of viral latency, and later to promote tumor cell growth through suppression of NKG2D-mediated functions. Importantly, our results provide additional support to the use of PGE2 inhibitors as an attractive approach to treat aggressive KS, as they could restore activation and survival of tumoricidal NK cells.
The contribution of innate immunity to immunosurveillance of the oncogenic Human Herpes Virus 8 (HHV8) has not been studied in depth. We investigated NK cell phenotype and function in 70 HHV8-infected subjects, either asymptomatic carriers or having developed Kaposi's sarcoma (KS). Our results revealed substantial alterations of the NK cell receptor repertoire in healthy HHV8 carriers, with reduced expression of NKp30, NKp46 and CD161 receptors. In addition, down-modulation of the activating NKG2D receptor, associated with impaired NK-cell lytic capacity, was observed in patients with active KS. Resolution of KS after treatment was accompanied with restoration of NKG2D levels and NK cell activity. HHV8-latently infected endothelial cells overexpressed ligands of several NK cell receptors, including NKG2D ligands. The strong expression of NKG2D ligands by tumor cells was confirmed in situ by immunohistochemical staining of KS biopsies. However, no tumor-infiltrating NK cells were detected, suggesting a defect in NK cell homing or survival in the KS microenvironment. Among the known KS-derived immunoregulatory factors, we identified prostaglandin E2 (PGE2) as a critical element responsible for the down-modulation of NKG2D expression on resting NK cells. Moreover, PGE2 prevented up-regulation of the NKG2D and NKp30 receptors on IL-15-activated NK cells, and inhibited the IL-15-induced proliferation and survival of NK cells. Altogether, our observations are consistent with distinct immunoevasion mechanisms that allow HHV8 to escape NK cell responses stepwise, first at early stages of infection to facilitate the maintenance of viral latency, and later to promote tumor cell growth through suppression of NKG2D-mediated functions. Importantly, our results provide additional support to the use of PGE2 inhibitors as an attractive approach to treat aggressive KS, as they could restore activation and survival of tumoricidal NK cells.The contribution of innate immunity to immunosurveillance of the oncogenic Human Herpes Virus 8 (HHV8) has not been studied in depth. We investigated NK cell phenotype and function in 70 HHV8-infected subjects, either asymptomatic carriers or having developed Kaposi's sarcoma (KS). Our results revealed substantial alterations of the NK cell receptor repertoire in healthy HHV8 carriers, with reduced expression of NKp30, NKp46 and CD161 receptors. In addition, down-modulation of the activating NKG2D receptor, associated with impaired NK-cell lytic capacity, was observed in patients with active KS. Resolution of KS after treatment was accompanied with restoration of NKG2D levels and NK cell activity. HHV8-latently infected endothelial cells overexpressed ligands of several NK cell receptors, including NKG2D ligands. The strong expression of NKG2D ligands by tumor cells was confirmed in situ by immunohistochemical staining of KS biopsies. However, no tumor-infiltrating NK cells were detected, suggesting a defect in NK cell homing or survival in the KS microenvironment. Among the known KS-derived immunoregulatory factors, we identified prostaglandin E2 (PGE2) as a critical element responsible for the down-modulation of NKG2D expression on resting NK cells. Moreover, PGE2 prevented up-regulation of the NKG2D and NKp30 receptors on IL-15-activated NK cells, and inhibited the IL-15-induced proliferation and survival of NK cells. Altogether, our observations are consistent with distinct immunoevasion mechanisms that allow HHV8 to escape NK cell responses stepwise, first at early stages of infection to facilitate the maintenance of viral latency, and later to promote tumor cell growth through suppression of NKG2D-mediated functions. Importantly, our results provide additional support to the use of PGE2 inhibitors as an attractive approach to treat aggressive KS, as they could restore activation and survival of tumoricidal NK cells.
Audience Academic
Author Zucman, David
Choukem, Siméon-Pierre
Pages, Cécile
Caillat-Zucman, Sophie
Lebbé, Céleste
Dupuy, Stéphanie
Tognarelli, Sara
Lambert, Marion
AuthorAffiliation University of North Carolina at Chapel Hill, United States of America
2 Hôpital Foch, Service de Médecine Interne, Suresnes, France
1 Institut National de la Santé et de la Recherche Médicale (INSERM), U986, Hôpital St-Vincent de Paul; Université Paris Descartes, Faculté de Médecine, Paris, France
4 AP-HP, Hôpital Saint-Louis, Service de Dermatologie; Université Paris Diderot, INSERM U976 Skin Research Center, Paris, France
3 AP-HP, Hôpital Saint-Louis, Service d'Endocrinologie; Université Paris Diderot, Faculté de Médecine, Paris, France
AuthorAffiliation_xml – name: 4 AP-HP, Hôpital Saint-Louis, Service de Dermatologie; Université Paris Diderot, INSERM U976 Skin Research Center, Paris, France
– name: 2 Hôpital Foch, Service de Médecine Interne, Suresnes, France
– name: 3 AP-HP, Hôpital Saint-Louis, Service d'Endocrinologie; Université Paris Diderot, Faculté de Médecine, Paris, France
– name: University of North Carolina at Chapel Hill, United States of America
– name: 1 Institut National de la Santé et de la Recherche Médicale (INSERM), U986, Hôpital St-Vincent de Paul; Université Paris Descartes, Faculté de Médecine, Paris, France
Author_xml – sequence: 1
  givenname: Stéphanie
  surname: Dupuy
  fullname: Dupuy, Stéphanie
– sequence: 2
  givenname: Marion
  surname: Lambert
  fullname: Lambert, Marion
– sequence: 3
  givenname: David
  surname: Zucman
  fullname: Zucman, David
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  givenname: Siméon-Pierre
  surname: Choukem
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  surname: Tognarelli
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– sequence: 6
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  surname: Pages
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/22253598$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright COPYRIGHT 2012 Public Library of Science
2012 Dupuy et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Dupuy S, Lambert M, Zucman D, Choukem S-P, Tognarelli S, et al. (2012) Human Herpesvirus 8 (HHV8) Sequentially Shapes the NK Cell Repertoire during the Course of Asymptomatic Infection and Kaposi Sarcoma. PLoS Pathog 8(1): e1002486. doi:10.1371/journal.ppat.1002486
Dupuy et al. 2012
Copyright_xml – notice: COPYRIGHT 2012 Public Library of Science
– notice: 2012 Dupuy et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Dupuy S, Lambert M, Zucman D, Choukem S-P, Tognarelli S, et al. (2012) Human Herpesvirus 8 (HHV8) Sequentially Shapes the NK Cell Repertoire during the Course of Asymptomatic Infection and Kaposi Sarcoma. PLoS Pathog 8(1): e1002486. doi:10.1371/journal.ppat.1002486
– notice: Dupuy et al. 2012
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DocumentTitleAlternate How HHV8 Evades Host NK Cell Response
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Current address: Department of Medicine, Douala General Hospital, Douala, Cameroon; Faculty of Health Sciences, University of Buea, Buea, Cameroon
Conceived and designed the experiments: SD, ML, ST, SCZ. Performed the experiments: SD, ML, ST. Analyzed the data: SD, ML, DZ, ST, SPC, CP, CL, SCZ. Contributed reagents/materials/analysis tools: DZ, SPC, CP, CL. Wrote the paper: SD, CL, SCZ.
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SSID ssj0041316
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Snippet The contribution of innate immunity to immunosurveillance of the oncogenic Human Herpes Virus 8 (HHV8) has not been studied in depth. We investigated NK cell...
  The contribution of innate immunity to immunosurveillance of the oncogenic Human Herpes Virus 8 (HHV8) has not been studied in depth. We investigated NK cell...
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SourceType Open Website
Open Access Repository
Aggregation Database
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StartPage e1002486
SubjectTerms Asymptomatic Infections
Base Sequence
Biology
Cells
Cells, Cultured
Development and progression
Health aspects
Herpesviridae Infections - complications
Herpesviridae Infections - immunology
Herpesviridae Infections - virology
Herpesvirus
Herpesvirus 8, Human - immunology
Herpesvirus 8, Human - physiology
HIV Infections - complications
HIV Infections - immunology
HIV-1 - immunology
HIV-1 - physiology
Human herpesvirus 8
Humans
Immune system
Immunology
Infections
Kaposi's sarcoma
Killer cells
Killer Cells, Natural - classification
Killer Cells, Natural - immunology
Killer Cells, Natural - metabolism
Lymphocyte Activation - physiology
Medicine
Middle Aged
Molecular Sequence Data
NK Cell Lectin-Like Receptor Subfamily K - metabolism
Phenotype
Physiological aspects
Proteins
Sarcoma
Sarcoma, Kaposi - complications
Sarcoma, Kaposi - immunology
Sarcoma, Kaposi - virology
Virus Latency - genetics
Virus Latency - immunology
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Title Human Herpesvirus 8 (HHV8) Sequentially Shapes the NK Cell Repertoire during the Course of Asymptomatic Infection and Kaposi Sarcoma
URI https://www.ncbi.nlm.nih.gov/pubmed/22253598
https://www.proquest.com/docview/1289105608
https://www.proquest.com/docview/916849044
https://www.proquest.com/docview/954639992
https://pubmed.ncbi.nlm.nih.gov/PMC3257307
https://doaj.org/article/2850ba062cde4bb2920887b55ac8a325
http://dx.doi.org/10.1371/journal.ppat.1002486
Volume 8
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