Transcellular delivery of vesicular SOCS proteins from macrophages to epithelial cells blunts inflammatory signaling

JAK-STAT signaling mediates the actions of numerous cytokines and growth factors, and its endogenous brake is the family of SOCS proteins. Consistent with their intracellular roles, SOCS proteins have never been identified in the extracellular space. Here we report that alveolar macrophages can secr...

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Published inThe Journal of experimental medicine Vol. 212; no. 5; pp. 729 - 742
Main Authors Bourdonnay, Emilie, Zasłona, Zbigniew, Penke, Loka Raghu Kumar, Speth, Jennifer M., Schneider, Daniel J., Przybranowski, Sally, Swanson, Joel A., Mancuso, Peter, Freeman, Christine M., Curtis, Jeffrey L., Peters-Golden, Marc
Format Journal Article
LanguageEnglish
Published United States The Rockefeller University Press 04.05.2015
Subjects
Animals
Cell Line, Transformed
Cell-Derived Microparticles - immunology
Cell-Derived Microparticles - pathology
Epithelial Cells - immunology
Epithelial Cells - pathology
Female
Humans
Inflammation - immunology
Inflammation - pathology
Janus Kinases - immunology
Macrophages - immunology
Male
Mice
Pulmonary Alveoli - immunology
Pulmonary Alveoli - pathology
Rats
Rats, Wistar
Signal Transduction - immunology
STAT Transcription Factors - immunology
Suppressor of Cytokine Signaling Proteins - immunology
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Abstract JAK-STAT signaling mediates the actions of numerous cytokines and growth factors, and its endogenous brake is the family of SOCS proteins. Consistent with their intracellular roles, SOCS proteins have never been identified in the extracellular space. Here we report that alveolar macrophages can secrete SOCS1 and -3 in exosomes and microparticles, respectively, for uptake by alveolar epithelial cells and subsequent inhibition of STAT activation. Secretion is tunable and occurs both in vitro and in vivo. SOCS secretion into lung lining fluid was diminished by cigarette smoking in humans and mice. Secretion and transcellular delivery of vesicular SOCS proteins thus represent a new model for the control of inflammatory signaling, which is subject to dysregulation during states of inflammation.
AbstractList JAK-STAT signaling mediates the actions of numerous cytokines and growth factors, and its endogenous brake is the family of SOCS proteins. Consistent with their intracellular roles, SOCS proteins have never been identified in the extracellular space. Here we report that alveolar macrophages can secrete SOCS1 and -3 in exosomes and microparticles, respectively, for uptake by alveolar epithelial cells and subsequent inhibition of STAT activation. Secretion is tunable and occurs both in vitro and in vivo. SOCS secretion into lung lining fluid was diminished by cigarette smoking in humans and mice. Secretion and transcellular delivery of vesicular SOCS proteins thus represent a new model for the control of inflammatory signaling, which is subject to dysregulation during states of inflammation.
SOCS1 and -3 proteins are released by alveolar macrophages into exosomes and microparticles, respectively, which are then taken up by alveolar epithelial cells, resulting in inhibition of STAT signaling. This process was dampened by exposure to cigarette smoke and may thus be important in suppressing airway inflammation. JAK-STAT signaling mediates the actions of numerous cytokines and growth factors, and its endogenous brake is the family of SOCS proteins. Consistent with their intracellular roles, SOCS proteins have never been identified in the extracellular space. Here we report that alveolar macrophages can secrete SOCS1 and -3 in exosomes and microparticles, respectively, for uptake by alveolar epithelial cells and subsequent inhibition of STAT activation. Secretion is tunable and occurs both in vitro and in vivo. SOCS secretion into lung lining fluid was diminished by cigarette smoking in humans and mice. Secretion and transcellular delivery of vesicular SOCS proteins thus represent a new model for the control of inflammatory signaling, which is subject to dysregulation during states of inflammation.
SOCS1 and -3 proteins are released by alveolar macrophages into exosomes and microparticles, respectively, which are then taken up by alveolar epithelial cells, resulting in inhibition of STAT signaling. This process was dampened by exposure to cigarette smoke and may thus be important in suppressing airway inflammation. JAK-STAT signaling mediates the actions of numerous cytokines and growth factors, and its endogenous brake is the family of SOCS proteins. Consistent with their intracellular roles, SOCS proteins have never been identified in the extracellular space. Here we report that alveolar macrophages can secrete SOCS1 and -3 in exosomes and microparticles, respectively, for uptake by alveolar epithelial cells and subsequent inhibition of STAT activation. Secretion is tunable and occurs both in vitro and in vivo. SOCS secretion into lung lining fluid was diminished by cigarette smoking in humans and mice. Secretion and transcellular delivery of vesicular SOCS proteins thus represent a new model for the control of inflammatory signaling, which is subject to dysregulation during states of inflammation.
JAK-STAT signaling mediates the actions of numerous cytokines and growth factors, and its endogenous brake is the family of SOCS proteins. Consistent with their intracellular roles, SOCS proteins have never been identified in the extracellular space. Here we report that alveolar macrophages can secrete SOCS1 and -3 in exosomes and microparticles, respectively, for uptake by alveolar epithelial cells and subsequent inhibition of STAT activation. Secretion is tunable and occurs both in vitro and in vivo. SOCS secretion into lung lining fluid was diminished by cigarette smoking in humans and mice. Secretion and transcellular delivery of vesicular SOCS proteins thus represent a new model for the control of inflammatory signaling, which is subject to dysregulation during states of inflammation.JAK-STAT signaling mediates the actions of numerous cytokines and growth factors, and its endogenous brake is the family of SOCS proteins. Consistent with their intracellular roles, SOCS proteins have never been identified in the extracellular space. Here we report that alveolar macrophages can secrete SOCS1 and -3 in exosomes and microparticles, respectively, for uptake by alveolar epithelial cells and subsequent inhibition of STAT activation. Secretion is tunable and occurs both in vitro and in vivo. SOCS secretion into lung lining fluid was diminished by cigarette smoking in humans and mice. Secretion and transcellular delivery of vesicular SOCS proteins thus represent a new model for the control of inflammatory signaling, which is subject to dysregulation during states of inflammation.
Author Penke, Loka Raghu Kumar
Zasłona, Zbigniew
Speth, Jennifer M.
Przybranowski, Sally
Mancuso, Peter
Curtis, Jeffrey L.
Swanson, Joel A.
Schneider, Daniel J.
Freeman, Christine M.
Bourdonnay, Emilie
Peters-Golden, Marc
AuthorAffiliation 4 Research Services and 5 Medical Services, Department of Veterans Affairs Health Care System, Ann Arbor, MI 48105
1 Division of Pulmonary and Critical Care Medicine, Department of Internal Medicine and 2 Department of Microbiology and Immunology, University of Michigan Medical School ; and 3 Department of Environmental Health Sciences, School of Public Health; University of Michigan, Ann Arbor, MI 48109
AuthorAffiliation_xml – name: 1 Division of Pulmonary and Critical Care Medicine, Department of Internal Medicine and 2 Department of Microbiology and Immunology, University of Michigan Medical School ; and 3 Department of Environmental Health Sciences, School of Public Health; University of Michigan, Ann Arbor, MI 48109
– name: 4 Research Services and 5 Medical Services, Department of Veterans Affairs Health Care System, Ann Arbor, MI 48105
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  surname: Bourdonnay
  fullname: Bourdonnay, Emilie
– sequence: 2
  givenname: Zbigniew
  surname: Zasłona
  fullname: Zasłona, Zbigniew
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PublicationTitle The Journal of experimental medicine
PublicationTitleAlternate J Exp Med
PublicationYear 2015
Publisher The Rockefeller University Press
Publisher_xml – name: The Rockefeller University Press
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Snippet JAK-STAT signaling mediates the actions of numerous cytokines and growth factors, and its endogenous brake is the family of SOCS proteins. Consistent with...
SOCS1 and -3 proteins are released by alveolar macrophages into exosomes and microparticles, respectively, which are then taken up by alveolar epithelial...
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SubjectTerms Animals
Cell Line, Transformed
Cell-Derived Microparticles - immunology
Cell-Derived Microparticles - pathology
Epithelial Cells - immunology
Epithelial Cells - pathology
Female
Humans
Inflammation - immunology
Inflammation - pathology
Janus Kinases - immunology
Macrophages - immunology
Male
Mice
Pulmonary Alveoli - immunology
Pulmonary Alveoli - pathology
Rats
Rats, Wistar
Signal Transduction - immunology
STAT Transcription Factors - immunology
Suppressor of Cytokine Signaling Proteins - immunology
Title Transcellular delivery of vesicular SOCS proteins from macrophages to epithelial cells blunts inflammatory signaling
URI https://www.ncbi.nlm.nih.gov/pubmed/25847945
https://www.proquest.com/docview/1680184002
https://www.proquest.com/docview/1808662839
https://pubmed.ncbi.nlm.nih.gov/PMC4419346
Volume 212
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