Inflammatory monocytes mediate control of acute alphavirus infection in mice

Chikungunya virus (CHIKV) and Ross River virus (RRV) are mosquito-transmitted alphaviruses that cause debilitating acute and chronic musculoskeletal disease. Monocytes are implicated in the pathogenesis of these infections; however, their specific roles are not well defined. To investigate the role...

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Published inPLoS pathogens Vol. 13; no. 12; p. e1006748
Main Authors Haist, Kelsey C., Burrack, Kristina S., Davenport, Bennett J., Morrison, Thomas E.
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 15.12.2017
Public Library of Science (PLoS)
Subjects
Adaptive immunity
Alphavirus
Aquatic insects
Biology and Life Sciences
Bone marrow
CCR2 protein
Cell culture
Cell cycle
Chikungunya virus
Depletion
Development and progression
Epidemics
Funding
Gene expression
Health services
Immunity
Immunology
Infections
Infectious diseases
Inflammation
Interferon
Interferon regulatory factor 3
Interferon regulatory factor 7
Killer cells
Leukocytes (neutrophilic)
Macrophages
Medicine
Medicine and Health Sciences
Mice
Monocyte chemoattractant protein 1
Monocytes
Mosquitoes
Muscles
Musculoskeletal diseases
Mutation
Neutrophils
Pathogenesis
Physiological aspects
Proteins
Public health
RAG1 protein
Research and Analysis Methods
Ribonucleic acid
RNA
RNA virus infections
Toxins
Transgenic mice
Vector-borne diseases
Viral infections
Virology
Virulence
Viruses
United States
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Abstract Chikungunya virus (CHIKV) and Ross River virus (RRV) are mosquito-transmitted alphaviruses that cause debilitating acute and chronic musculoskeletal disease. Monocytes are implicated in the pathogenesis of these infections; however, their specific roles are not well defined. To investigate the role of inflammatory Ly6ChiCCR2+ monocytes in alphavirus pathogenesis, we used CCR2-DTR transgenic mice, enabling depletion of these cells by administration of diptheria toxin (DT). DT-treated CCR2-DTR mice displayed more severe disease following CHIKV and RRV infection and had fewer Ly6Chi monocytes and NK cells in circulation and muscle tissue compared with DT-treated WT mice. Furthermore, depletion of CCR2+ or Gr1+ cells, but not NK cells or neutrophils alone, restored virulence and increased viral loads in mice infected with an RRV strain encoding attenuating mutations in nsP1 to levels detected in monocyte-depleted mice infected with fully virulent RRV. Disease severity and viral loads also were increased in DT-treated CCR2-DTR+;Rag1-/- mice infected with the nsP1 mutant virus, confirming that these effects are independent of adaptive immunity. Monocytes and macrophages sorted from muscle tissue of RRV-infected mice were viral RNA positive and had elevated expression of Irf7, and co-culture of Ly6Chi monocytes with RRV-infected cells resulted in induction of type I IFN gene expression in monocytes that was Irf3;Irf7 and Mavs-dependent. Consistent with these data, viral loads of the attenuated nsP1 mutant virus were equivalent to those of WT RRV in Mavs-/- mice. Finally, reconstitution of Irf3-/-;Irf7-/- mice with CCR2-DTR bone marrow rescued mice from severe infection, and this effect was reversed by depletion of CCR2+ cells, indicating that CCR2+ hematopoietic cells are capable of inducing an antiviral response. Collectively, these data suggest that MAVS-dependent production of type I IFN by monocytes is critical for control of acute alphavirus infection and that determinants in nsP1, the viral RNA capping protein, counteract this response.
AbstractList Chikungunya virus (CHIKV) and Ross River virus (RRV) are mosquito-transmitted alphaviruses that cause debilitating acute and chronic musculoskeletal disease. Monocytes are implicated in the pathogenesis of these infections; however, their specific roles are not well defined. To investigate the role of inflammatory Ly6C.sup.hi CCR2.sup.+ monocytes in alphavirus pathogenesis, we used CCR2-DTR transgenic mice, enabling depletion of these cells by administration of diptheria toxin (DT). DT-treated CCR2-DTR mice displayed more severe disease following CHIKV and RRV infection and had fewer Ly6C.sup.hi monocytes and NK cells in circulation and muscle tissue compared with DT-treated WT mice. Furthermore, depletion of CCR2.sup.+ or Gr1.sup.+ cells, but not NK cells or neutrophils alone, restored virulence and increased viral loads in mice infected with an RRV strain encoding attenuating mutations in nsP1 to levels detected in monocyte-depleted mice infected with fully virulent RRV. Disease severity and viral loads also were increased in DT-treated CCR2-DTR.sup.+ ;Rag1.sup.-/- mice infected with the nsP1 mutant virus, confirming that these effects are independent of adaptive immunity. Monocytes and macrophages sorted from muscle tissue of RRV-infected mice were viral RNA positive and had elevated expression of Irf7, and co-culture of Ly6C.sup.hi monocytes with RRV-infected cells resulted in induction of type I IFN gene expression in monocytes that was Irf3;Irf7 and Mavs-dependent. Consistent with these data, viral loads of the attenuated nsP1 mutant virus were equivalent to those of WT RRV in Mavs.sup.-/- mice. Finally, reconstitution of Irf3.sup.-/- ;Irf7.sup.-/- mice with CCR2-DTR bone marrow rescued mice from severe infection, and this effect was reversed by depletion of CCR2.sup.+ cells, indicating that CCR2.sup.+ hematopoietic cells are capable of inducing an antiviral response. Collectively, these data suggest that MAVS-dependent production of type I IFN by monocytes is critical for control of acute alphavirus infection and that determinants in nsP1, the viral RNA capping protein, counteract this response.
Chikungunya virus (CHIKV) and Ross River virus (RRV) are mosquito-transmitted alphaviruses that cause debilitating acute and chronic musculoskeletal disease. Monocytes are implicated in the pathogenesis of these infections; however, their specific roles are not well defined. To investigate the role of inflammatory Ly6ChiCCR2+ monocytes in alphavirus pathogenesis, we used CCR2-DTR transgenic mice, enabling depletion of these cells by administration of diptheria toxin (DT). DT-treated CCR2-DTR mice displayed more severe disease following CHIKV and RRV infection and had fewer Ly6Chi monocytes and NK cells in circulation and muscle tissue compared with DT-treated WT mice. Furthermore, depletion of CCR2+ or Gr1+ cells, but not NK cells or neutrophils alone, restored virulence and increased viral loads in mice infected with an RRV strain encoding attenuating mutations in nsP1 to levels detected in monocyte-depleted mice infected with fully virulent RRV. Disease severity and viral loads also were increased in DT-treated CCR2-DTR+;Rag1-/- mice infected with the nsP1 mutant virus, confirming that these effects are independent of adaptive immunity. Monocytes and macrophages sorted from muscle tissue of RRV-infected mice were viral RNA positive and had elevated expression of Irf7, and co-culture of Ly6Chi monocytes with RRV-infected cells resulted in induction of type I IFN gene expression in monocytes that was Irf3;Irf7 and Mavs-dependent. Consistent with these data, viral loads of the attenuated nsP1 mutant virus were equivalent to those of WT RRV in Mavs-/- mice. Finally, reconstitution of Irf3-/-;Irf7-/- mice with CCR2-DTR bone marrow rescued mice from severe infection, and this effect was reversed by depletion of CCR2+ cells, indicating that CCR2+ hematopoietic cells are capable of inducing an antiviral response. Collectively, these data suggest that MAVS-dependent production of type I IFN by monocytes is critical for control of acute alphavirus infection and that determinants in nsP1, the viral RNA capping protein, counteract this response.
Chikungunya virus (CHIKV) and Ross River virus (RRV) are mosquito-transmitted alphaviruses that cause debilitating acute and chronic musculoskeletal disease. Monocytes are implicated in the pathogenesis of these infections; however, their specific roles are not well defined. To investigate the role of inflammatory Ly6ChiCCR2+ monocytes in alphavirus pathogenesis, we used CCR2-DTR transgenic mice, enabling depletion of these cells by administration of diptheria toxin (DT). DT-treated CCR2-DTR mice displayed more severe disease following CHIKV and RRV infection and had fewer Ly6Chi monocytes and NK cells in circulation and muscle tissue compared with DT-treated WT mice. Furthermore, depletion of CCR2+ or Gr1+ cells, but not NK cells or neutrophils alone, restored virulence and increased viral loads in mice infected with an RRV strain encoding attenuating mutations in nsP1 to levels detected in monocyte-depleted mice infected with fully virulent RRV. Disease severity and viral loads also were increased in DT-treated CCR2-DTR+;Rag1-/- mice infected with the nsP1 mutant virus, confirming that these effects are independent of adaptive immunity. Monocytes and macrophages sorted from muscle tissue of RRV-infected mice were viral RNA positive and had elevated expression of Irf7, and co-culture of Ly6Chi monocytes with RRV-infected cells resulted in induction of type I IFN gene expression in monocytes that was Irf3;Irf7 and Mavs-dependent. Consistent with these data, viral loads of the attenuated nsP1 mutant virus were equivalent to those of WT RRV in Mavs-/- mice. Finally, reconstitution of Irf3-/-;Irf7-/- mice with CCR2-DTR bone marrow rescued mice from severe infection, and this effect was reversed by depletion of CCR2+ cells, indicating that CCR2+ hematopoietic cells are capable of inducing an antiviral response. Collectively, these data suggest that MAVS-dependent production of type I IFN by monocytes is critical for control of acute alphavirus infection and that determinants in nsP1, the viral RNA capping protein, counteract this response.Chikungunya virus (CHIKV) and Ross River virus (RRV) are mosquito-transmitted alphaviruses that cause debilitating acute and chronic musculoskeletal disease. Monocytes are implicated in the pathogenesis of these infections; however, their specific roles are not well defined. To investigate the role of inflammatory Ly6ChiCCR2+ monocytes in alphavirus pathogenesis, we used CCR2-DTR transgenic mice, enabling depletion of these cells by administration of diptheria toxin (DT). DT-treated CCR2-DTR mice displayed more severe disease following CHIKV and RRV infection and had fewer Ly6Chi monocytes and NK cells in circulation and muscle tissue compared with DT-treated WT mice. Furthermore, depletion of CCR2+ or Gr1+ cells, but not NK cells or neutrophils alone, restored virulence and increased viral loads in mice infected with an RRV strain encoding attenuating mutations in nsP1 to levels detected in monocyte-depleted mice infected with fully virulent RRV. Disease severity and viral loads also were increased in DT-treated CCR2-DTR+;Rag1-/- mice infected with the nsP1 mutant virus, confirming that these effects are independent of adaptive immunity. Monocytes and macrophages sorted from muscle tissue of RRV-infected mice were viral RNA positive and had elevated expression of Irf7, and co-culture of Ly6Chi monocytes with RRV-infected cells resulted in induction of type I IFN gene expression in monocytes that was Irf3;Irf7 and Mavs-dependent. Consistent with these data, viral loads of the attenuated nsP1 mutant virus were equivalent to those of WT RRV in Mavs-/- mice. Finally, reconstitution of Irf3-/-;Irf7-/- mice with CCR2-DTR bone marrow rescued mice from severe infection, and this effect was reversed by depletion of CCR2+ cells, indicating that CCR2+ hematopoietic cells are capable of inducing an antiviral response. Collectively, these data suggest that MAVS-dependent production of type I IFN by monocytes is critical for control of acute alphavirus infection and that determinants in nsP1, the viral RNA capping protein, counteract this response.
Chikungunya virus (CHIKV) and Ross River virus (RRV) are mosquito-transmitted alphaviruses that cause debilitating acute and chronic musculoskeletal disease. Monocytes are implicated in the pathogenesis of these infections; however, their specific roles are not well defined. To investigate the role of inflammatory Ly6C hi CCR2 + monocytes in alphavirus pathogenesis, we used CCR2-DTR transgenic mice, enabling depletion of these cells by administration of diptheria toxin (DT). DT-treated CCR2-DTR mice displayed more severe disease following CHIKV and RRV infection and had fewer Ly6C hi monocytes and NK cells in circulation and muscle tissue compared with DT-treated WT mice. Furthermore, depletion of CCR2 + or Gr1 + cells, but not NK cells or neutrophils alone, restored virulence and increased viral loads in mice infected with an RRV strain encoding attenuating mutations in nsP1 to levels detected in monocyte-depleted mice infected with fully virulent RRV. Disease severity and viral loads also were increased in DT-treated CCR2-DTR + ; Rag1 -/- mice infected with the nsP1 mutant virus, confirming that these effects are independent of adaptive immunity. Monocytes and macrophages sorted from muscle tissue of RRV-infected mice were viral RNA positive and had elevated expression of Irf7 , and co-culture of Ly6C hi monocytes with RRV-infected cells resulted in induction of type I IFN gene expression in monocytes that was Irf3 ; Irf7 and Mavs -dependent. Consistent with these data, viral loads of the attenuated nsP1 mutant virus were equivalent to those of WT RRV in Mavs -/- mice. Finally, reconstitution of Irf3 -/- ; Irf7 -/- mice with CCR2-DTR bone marrow rescued mice from severe infection, and this effect was reversed by depletion of CCR2 + cells, indicating that CCR2 + hematopoietic cells are capable of inducing an antiviral response. Collectively, these data suggest that MAVS-dependent production of type I IFN by monocytes is critical for control of acute alphavirus infection and that determinants in nsP1, the viral RNA capping protein, counteract this response. Mosquito-transmitted arthritogenic alphaviruses, such as chikungunya virus (CHIKV), Mayaro virus, and Ross River virus (RRV), cause large disease outbreaks. Infection with these viruses results in severe pain and inflammation in joints, tendons, and muscles, likely due to direct viral infection of these tissues, that can persist for years. Monocytes and macrophages have been implicated in the damaging effects of the inflammation, however, the role of these cell types in control of alphaviral infection are poorly understood. Using mouse models and an attenuated RRV with mutations in the nsP1 gene, we found that monocytes are critical to control acute infection and to reduce disease severity. Furthermore, we found that monocytes respond to virus-infected cells by increasing expression levels of type I interferon, a critical antiviral defense system. The induction of type I interferon in monocytes was dependent on MAVS, a signaling protein downstream of cytosolic viral RNA sensor proteins. Similar to monocytes, MAVS was required to control infection with the nsP1 mutant RRV. These studies suggest that monocytes control acute alphavirus infection and that determinants in nsP1, the viral RNA capping protein, counteract this response. Thus, therapeutic strategies targeting these cells for the treatment of these viral inflammatory diseases should do so without compromising their role in innate immunity.
Audience Academic
Author Haist, Kelsey C.
Morrison, Thomas E.
Davenport, Bennett J.
Burrack, Kristina S.
AuthorAffiliation Department of Immunology and Microbiology, University of Colorado School of Medicine, Aurora, Colorado, United States of America
University of Pennsylvania School of Medicine, UNITED STATES
AuthorAffiliation_xml – name: Department of Immunology and Microbiology, University of Colorado School of Medicine, Aurora, Colorado, United States of America
– name: University of Pennsylvania School of Medicine, UNITED STATES
Author_xml – sequence: 1
  givenname: Kelsey C.
  surname: Haist
  fullname: Haist, Kelsey C.
– sequence: 2
  givenname: Kristina S.
  surname: Burrack
  fullname: Burrack, Kristina S.
– sequence: 3
  givenname: Bennett J.
  surname: Davenport
  fullname: Davenport, Bennett J.
– sequence: 4
  givenname: Thomas E.
  orcidid: 0000-0002-1811-2938
  surname: Morrison
  fullname: Morrison, Thomas E.
BackLink https://www.ncbi.nlm.nih.gov/pubmed/29244871$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright COPYRIGHT 2017 Public Library of Science
2017 Public Library of Science. 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: Haist KC, Burrack KS, Davenport BJ, Morrison TE (2017) Inflammatory monocytes mediate control of acute alphavirus infection in mice. PLoS Pathog 13(12): e1006748. https://doi.org/10.1371/journal.ppat.1006748
2017 Haist et al 2017 Haist et al
2017 Public Library of Science. 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: Haist KC, Burrack KS, Davenport BJ, Morrison TE (2017) Inflammatory monocytes mediate control of acute alphavirus infection in mice. PLoS Pathog 13(12): e1006748. https://doi.org/10.1371/journal.ppat.1006748
Copyright_xml – notice: COPYRIGHT 2017 Public Library of Science
– notice: 2017 Public Library of Science. 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: Haist KC, Burrack KS, Davenport BJ, Morrison TE (2017) Inflammatory monocytes mediate control of acute alphavirus infection in mice. PLoS Pathog 13(12): e1006748. https://doi.org/10.1371/journal.ppat.1006748
– notice: 2017 Haist et al 2017 Haist et al
– notice: 2017 Public Library of Science. 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: Haist KC, Burrack KS, Davenport BJ, Morrison TE (2017) Inflammatory monocytes mediate control of acute alphavirus infection in mice. PLoS Pathog 13(12): e1006748. https://doi.org/10.1371/journal.ppat.1006748
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Current address: Center for Immunology, Department of Laboratory Medicine and Pathology, University of Minnesota, Minneapolis, Minnesota, United States of America
The authors have declared that no competing interests exist.
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Snippet Chikungunya virus (CHIKV) and Ross River virus (RRV) are mosquito-transmitted alphaviruses that cause debilitating acute and chronic musculoskeletal disease....
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SubjectTerms Adaptive immunity
Alphavirus
Aquatic insects
Biology and Life Sciences
Bone marrow
CCR2 protein
Cell culture
Cell cycle
Chikungunya virus
Depletion
Development and progression
Epidemics
Funding
Gene expression
Health services
Immunity
Immunology
Infections
Infectious diseases
Inflammation
Interferon
Interferon regulatory factor 3
Interferon regulatory factor 7
Killer cells
Leukocytes (neutrophilic)
Macrophages
Medicine
Medicine and Health Sciences
Mice
Monocyte chemoattractant protein 1
Monocytes
Mosquitoes
Muscles
Musculoskeletal diseases
Mutation
Neutrophils
Pathogenesis
Physiological aspects
Proteins
Public health
RAG1 protein
Research and Analysis Methods
Ribonucleic acid
RNA
RNA virus infections
Toxins
Transgenic mice
Vector-borne diseases
Viral infections
Virology
Virulence
Viruses
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Title Inflammatory monocytes mediate control of acute alphavirus infection in mice
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https://doaj.org/article/83a6c1451f0d41e89b69fe8e6b02ea98
http://dx.doi.org/10.1371/journal.ppat.1006748
Volume 13
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