Type 1 interferon mediates chronic stress-induced neuroinflammation and behavioral deficits via complement component 3-dependent pathway

Chronic stress is a major risk factor in the pathophysiology of many neuropsychiatric disorders. Further, chronic stress conditions can promote neuroinflammation and inflammatory responses in both humans and animal models. Type I interferons (IFN-I) are critical mediators of the inflammatory respons...

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Vydáno v:Molecular psychiatry Ročník 26; číslo 7; s. 3043 - 3059
Hlavní autoři: Tripathi, Ashutosh, Whitehead, Carl, Surrao, Katelyn, Pillai, Ananya, Madeshiya, Amit, Li, Yong, Khodadadi, Hesam, Ahmed, Anthony O, Turecki, Gustavo, Baban, Babak, Pillai, Anilkumar
Médium: Journal Article
Jazyk:angličtina
Vydáno: England Nature Publishing Group 01.07.2021
Témata:
Animal models
Animals
Behavior
Complement C3
Complement component C3
Gene expression
Inflammation
Interferon Type I
Macrophages
Mental disorders
Mice
Mice, Inbred C57BL
Neuroinflammatory Diseases - immunology
Prefrontal cortex
Risk factors
Stress, Psychological
Suicide
β-Interferon
ISSN:1359-4184, 1476-5578, 1476-5578
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Abstract Chronic stress is a major risk factor in the pathophysiology of many neuropsychiatric disorders. Further, chronic stress conditions can promote neuroinflammation and inflammatory responses in both humans and animal models. Type I interferons (IFN-I) are critical mediators of the inflammatory response in the periphery and responsible for the altered mood and behavior. However, the underlying mechanisms are not well understood. In the present study, we investigated the role of IFN-I signaling in chronic stress-induced changes in neuroinflammation and behavior. Using the chronic restraint stress model, we found that chronic stress induces a significant increase in serum IFNβ levels in mice, and systemic blockade of IFN-I signaling attenuated chronic stress-induced infiltration of macrophages into prefrontal cortex and behavioral abnormalities. Furthermore, complement component 3 (C3) mediates systemic IFNβ-induced changes in neuroinflammation and behavior. Also, we found significant increases in the mRNA expression levels of IFN-I stimulated genes in the prefrontal cortex of depressed suicide subjects and significant correlation with C3 and inflammatory markers. Together, these findings from animal and human postmortem brain studies identify a crucial role of C3 in IFN-I-mediated changes in neuroinflammation and behavior under chronic stress conditions.
AbstractList Chronic stress is a major risk factor in the pathophysiology of many neuropsychiatric disorders. Further, chronic stress conditions can promote neuroinflammation and inflammatory responses in both humans and animal models. Type I interferons (IFN-I) are critical mediators of the inflammatory response in the periphery and responsible for the altered mood and behavior. However, the underlying mechanisms are not well understood. In the present study, we investigated the role of IFN-I signaling in chronic stress-induced changes in neuroinflammation and behavior. Using the chronic restraint stress model, we found that chronic stress induces a significant increase in serum IFNβ levels in mice, and systemic blockade of IFN-I signaling attenuated chronic stress-induced infiltration of macrophages into prefrontal cortex and behavioral abnormalities. Furthermore, complement component 3 (C3) mediates systemic IFNβ-induced changes in neuroinflammation and behavior. Also, we found significant increases in the mRNA expression levels of IFN-I stimulated genes in the prefrontal cortex of depressed suicide subjects and significant correlation with C3 and inflammatory markers. Together, these findings from animal and human postmortem brain studies identify a crucial role of C3 in IFN-I-mediated changes in neuroinflammation and behavior under chronic stress conditions.Chronic stress is a major risk factor in the pathophysiology of many neuropsychiatric disorders. Further, chronic stress conditions can promote neuroinflammation and inflammatory responses in both humans and animal models. Type I interferons (IFN-I) are critical mediators of the inflammatory response in the periphery and responsible for the altered mood and behavior. However, the underlying mechanisms are not well understood. In the present study, we investigated the role of IFN-I signaling in chronic stress-induced changes in neuroinflammation and behavior. Using the chronic restraint stress model, we found that chronic stress induces a significant increase in serum IFNβ levels in mice, and systemic blockade of IFN-I signaling attenuated chronic stress-induced infiltration of macrophages into prefrontal cortex and behavioral abnormalities. Furthermore, complement component 3 (C3) mediates systemic IFNβ-induced changes in neuroinflammation and behavior. Also, we found significant increases in the mRNA expression levels of IFN-I stimulated genes in the prefrontal cortex of depressed suicide subjects and significant correlation with C3 and inflammatory markers. Together, these findings from animal and human postmortem brain studies identify a crucial role of C3 in IFN-I-mediated changes in neuroinflammation and behavior under chronic stress conditions.
Chronic stress is a major risk factor in the pathophysiology of many neuropsychiatric disorders. Further, chronic stress conditions can promote neuroinflammation and inflammatory responses in both humans and animal models. Type I interferons (IFN-I) are critical mediators of the inflammatory response in the periphery and responsible for the altered mood and behavior. However, the underlying mechanisms are not well understood. In the present study, we investigated the role of IFN-I signaling in chronic stress-induced changes in neuroinflammation and behavior. Using the chronic restraint stress model, we found that chronic stress induces a significant increase in serum IFNβ levels in mice, and systemic blockade of IFN-I signaling attenuated chronic stress-induced infiltration of macrophages into prefrontal cortex and behavioral abnormalities. Furthermore, complement component 3 (C3) mediates systemic IFNβ-induced changes in neuroinflammation and behavior. Also, we found significant increases in the mRNA expression levels of IFN-I stimulated genes in the prefrontal cortex of depressed suicide subjects and significant correlation with C3 and inflammatory markers. Together, these findings from animal and human postmortem brain studies identify a crucial role of C3 in IFN-I-mediated changes in neuroinflammation and behavior under chronic stress conditions.
Author Madeshiya, Amit
Whitehead, Carl
Baban, Babak
Ahmed, Anthony O
Pillai, Ananya
Khodadadi, Hesam
Tripathi, Ashutosh
Li, Yong
Turecki, Gustavo
Surrao, Katelyn
Pillai, Anilkumar
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  surname: Tripathi
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  organization: Department of Psychiatry and Behavioral Sciences, McGovern Medical School, The University of Texas Health Science Center at Houston, Houston, TX, USA
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  surname: Whitehead
  fullname: Whitehead, Carl
  organization: Department of Psychiatry and Health Behavior, Medical College of Georgia, Augusta University, Augusta, GA, USA
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  givenname: Katelyn
  surname: Surrao
  fullname: Surrao, Katelyn
  organization: Department of Psychiatry and Health Behavior, Medical College of Georgia, Augusta University, Augusta, GA, USA
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  givenname: Ananya
  surname: Pillai
  fullname: Pillai, Ananya
  organization: Department of Psychiatry and Health Behavior, Medical College of Georgia, Augusta University, Augusta, GA, USA
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  givenname: Amit
  surname: Madeshiya
  fullname: Madeshiya, Amit
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  surname: Ahmed
  fullname: Ahmed, Anthony O
  organization: Department of Psychiatry, Weill Cornell Medical College, 1300 York Ave, New York, NY, USA
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  orcidid: 0000-0003-4075-2736
  surname: Turecki
  fullname: Turecki, Gustavo
  organization: McGill Group for Suicide Studies, Depressive Disorders Program, Douglas Mental Health University Institute, McGill University, Montreal, Quebec, Canada
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  surname: Baban
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  organization: Department of Oral Biology, Dental College of Georgia, Department of Neurology, Augusta University, Augusta, GA, USA
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  givenname: Anilkumar
  orcidid: 0000-0002-1952-8556
  surname: Pillai
  fullname: Pillai, Anilkumar
  email: anilkumar.r.pillai@uth.tmc.edu, anilkumar.r.pillai@uth.tmc.edu, anilkumar.r.pillai@uth.tmc.edu
  organization: Research and Development, Charlie Norwood VA Medical Center, Augusta, GA, USA. anilkumar.r.pillai@uth.tmc.edu
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ContentType Journal Article
Copyright 2021. This is a U.S. government work and not under copyright protection in the U.S.; foreign copyright protection may apply.
This is a U.S. government work and not under copyright protection in the U.S.; foreign copyright protection may apply 2021.
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Snippet Chronic stress is a major risk factor in the pathophysiology of many neuropsychiatric disorders. Further, chronic stress conditions can promote...
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SubjectTerms Animal models
Animals
Behavior
Complement C3
Complement component C3
Gene expression
Inflammation
Interferon Type I
Macrophages
Mental disorders
Mice
Mice, Inbred C57BL
Neuroinflammatory Diseases - immunology
Prefrontal cortex
Risk factors
Stress, Psychological
Suicide
β-Interferon
Title Type 1 interferon mediates chronic stress-induced neuroinflammation and behavioral deficits via complement component 3-dependent pathway
URI https://www.ncbi.nlm.nih.gov/pubmed/33833372
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