Herpesvirus latency confers symbiotic protection from bacterial infection

All humans become infected with multiple herpesviruses during childhood. After clearance of acute infection, herpesviruses enter a dormant state known as latency. Latency persists for the life of the host and is presumed to be parasitic, as it leaves the individual at risk for subsequent viral react...

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Published inNature Vol. 447; no. 7142; pp. 326 - 329
Main Authors Virgin, Herbert W, Barton, Erik S, White, Douglas W, Cathelyn, Jason S, Brett-McClellan, Kelly A, Engle, Michael, Diamond, Michael S, Miller, Virginia L
Format Journal Article
LanguageEnglish
Published London Nature Publishing 17.05.2007
Nature Publishing Group
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Abstract All humans become infected with multiple herpesviruses during childhood. After clearance of acute infection, herpesviruses enter a dormant state known as latency. Latency persists for the life of the host and is presumed to be parasitic, as it leaves the individual at risk for subsequent viral reactivation and disease. Here we show that herpesvirus latency also confers a surprising benefit to the host. Mice latently infected with either murine gammaherpesvirus 68 or murine cytomegalovirus, which are genetically highly similar to the human pathogens Epstein-Barr virus and human cytomegalovirus, respectively, are resistant to infection with the bacterial pathogens Listeria monocytogenes and Yersinia pestis. Latency-induced protection is not antigen specific but involves prolonged production of the antiviral cytokine interferon- and systemic activation of macrophages. Latency thereby upregulates the basal activation state of innate immunity against subsequent infections. We speculate that herpesvirus latency may also sculpt the immune response to self and environmental antigens through establishment of a polarized cytokine environment. Thus, whereas the immune evasion capabilities and lifelong persistence of herpesviruses are commonly viewed as solely pathogenic, our data suggest that latency is a symbiotic relationship with immune benefits for the host.
AbstractList All humans become infected with multiple herpesviruses during childhood. After clearance of acute infection, herpesviruses enter a dormant state known as latency. Latency persists for the life of the host and is presumed to be parasitic, as it leaves the individual at risk for subsequent viral reactivation and disease. Here we show that herpesvirus latency also confers a surprising benefit to the host. Mice latently infected with either murine gammaherpesvirus 68 or murine cytomegalovirus, which are genetically highly similar to the human pathogens Epstein-Barr virus and human cytomegalovirus, respectively, are resistant to infection with the bacterial pathogens Listeria monocytogenes and Yersinia pestis. Latency-induced protection is not antigen specific but involves prolonged production of the antiviral cytokine interferon-[greek letter gamma] and systemic activation of macrophages. Latency thereby upregulates the basal activation state of innate immunity against subsequent infections. We speculate that herpesvirus latency may also sculpt the immune response to self and environmental antigens through establishment of a polarized cytokine environment. Thus, whereas the immune evasion capabilities and lifelong persistence of herpesviruses are commonly viewed as solely pathogenic, our data suggest that latency is a symbiotic relationship with immune benefits for the host.
All humans become infected with multiple herpesviruses during childhood. After clearance of acute infection, herpesviruses enter a dormant state known as latency. Latency persists for the life of the host and is presumed to be parasitic, as it leaves the individual at risk for subsequent viral reactivation and disease. Here we show that herpesvirus latency also confers a surprising benefit to the host. Mice latently infected with either murine gammaherpesvirus 68 or murine cytomegalovirus, which are genetically highly similar to the human pathogens Epstein-Barr virus and human cytomegalovirus, respectively, are resistant to infection with the bacterial pathogens Listeria monocytogenes and Yersinia pestis. Latency-induced protection is not antigen specific but involves prolonged production of the antiviral cytokine interferon- gamma and systemic activation of macrophages. Latency thereby upregulates the basal activation state of innate immunity against subsequent infections. We speculate that herpesvirus latency may also sculpt the immune response to self and environmental antigens through establishment of a polarized cytokine environment. Thus, whereas the immune evasion capabilities and lifelong persistence of herpesviruses are commonly viewed as solely pathogenic, our data suggest that latency is a symbiotic relationship with immune benefits for the host.
All humans become infected with multiple herpesviruses during childhood. After clearance of acute infection, herpesviruses enter a dormant state known as latency. Latency persists for the life of the host and is presumed to be parasitic, as it leaves the individual at risk for subsequent viral reactivation and disease. Here we show that herpesvirus latency also confers a surprising benefit to the host. Mice latently infected with either murine gammaherpesvirus 68 or murine cytomegalovirus, which are genetically highly similar to the human pathogens Epstein-Barr virus and human cytomegalovirus, respectively, are resistant to infection with the bacterial pathogens Listeria monocytogenes and Yersinia pestis. Latency-induced protection is not antigen specific but involves prolonged production of the antiviral cytokine interferon- and systemic activation of macrophages. Latency thereby upregulates the basal activation state of innate immunity against subsequent infections. We speculate that herpesvirus latency may also sculpt the immune response to self and environmental antigens through establishment of a polarized cytokine environment. Thus, whereas the immune evasion capabilities and lifelong persistence of herpesviruses are commonly viewed as solely pathogenic, our data suggest that latency is a symbiotic relationship with immune benefits for the host.
All humans become infected with multiple herpesviruses during childhood. After clearance of acute infection, herpesviruses enter a dormant state known as latency. Latency persists for the life of the host and is presumed to be parasitic, as it leaves the individual at risk for subsequent viral reactivation and disease. Here we show that herpesvirus latency also confers a surprising benefit to the host. Mice latently infected with either murine gammaherpesvirus 68 or murine cytomegalovirus, which are genetically highly similar to the human pathogens Epstein-Barr virus and human cytomegalovirus, respectively, are resistant to infection with the bacterial pathogens Listeria monocytogenes and Yersinia pestis. Latency-induced protection is not antigen specific but involves prolonged production of the antiviral cytokine interferon and systemic activation of macrophages. Latency thereby upregulates the basal activation state of innate immunity against subsequent infections. We speculate that herpesvirus latency may also sculpt the immune response to self and environmental antigens through establishment of a polarized cytokine environment. Thus, whereas the immune evasion capabilities and lifelong persistence of herpesviruses are commonly viewed as solely pathogenic, our data suggest that latency is a symbiotic relationship with immune benefits for the host. [PUBLICATION ABSTRACT]
Audience Academic
Author White, Douglas W
Virgin, Herbert W
Brett-McClellan, Kelly A
Cathelyn, Jason S
Barton, Erik S
Engle, Michael
Diamond, Michael S
Miller, Virginia L
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  surname: Virgin
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  surname: Barton
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– sequence: 3
  givenname: Douglas W
  surname: White
  fullname: White, Douglas W
– sequence: 4
  givenname: Jason S
  surname: Cathelyn
  fullname: Cathelyn, Jason S
– sequence: 5
  givenname: Kelly A
  surname: Brett-McClellan
  fullname: Brett-McClellan, Kelly A
– sequence: 6
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  surname: Diamond
  fullname: Diamond, Michael S
– sequence: 8
  givenname: Virginia L
  surname: Miller
  fullname: Miller, Virginia L
BackLink http://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=18733442$$DView record in Pascal Francis
https://www.ncbi.nlm.nih.gov/pubmed/17507983$$D View this record in MEDLINE/PubMed
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IsPeerReviewed true
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Issue 7142
Keywords Infection
Virus
Symbiotic relation
Herpesviridae
Bacteriosis
Bacteria
Protection
Latency
Language English
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E Amyes (BFnature05762_CR20) 2003; 198
C Nilsson (BFnature05762_CR26) 2005; 116
K Takeuchi (BFnature05762_CR25) 2006; 56
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Snippet All humans become infected with multiple herpesviruses during childhood. After clearance of acute infection, herpesviruses enter a dormant state known as...
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SubjectTerms Animals
Bacteria
Bacterial diseases
Bacterial Infections - complications
Bacterial Infections - immunology
Bacterial Infections - microbiology
Bacterial Infections - prevention & control
Biological and medical sciences
Cytokines
Epstein-Barr virus
General aspects
Herpes viruses
Herpesviridae - physiology
Herpesviridae Infections - complications
Herpesviridae Infections - immunology
Herpesviridae Infections - virology
Human cytomegalovirus
Immune response
Immune system
Immunity, Innate - immunology
Infectious diseases
Listeria monocytogenes
Listeria monocytogenes - immunology
Listeria monocytogenes - physiology
Listeriosis - complications
Listeriosis - immunology
Listeriosis - prevention & control
Macrophage Activation
Macrophages - immunology
Medical sciences
Mice
Mice, Inbred C57BL
Murine cytomegalovirus
Murine gammaherpesvirus 68
Muromegalovirus - immunology
Muromegalovirus - physiology
Pathogens
Plague - complications
Plague - immunology
Plague - prevention & control
Rodents
Symbiosis
Virus Latency - physiology
West Nile Fever - complications
West Nile virus - physiology
Yersinia pestis
Yersinia pestis - immunology
Yersinia pestis - physiology
Title Herpesvirus latency confers symbiotic protection from bacterial infection
URI http://dx.doi.org/10.1038/nature05762
https://www.ncbi.nlm.nih.gov/pubmed/17507983
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Volume 447
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