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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Published inMolecular psychiatry Vol. 26; no. 7; pp. 3043 - 3059
Main Authors Tripathi, Ashutosh, Whitehead, Carl, Surrao, Katelyn, Pillai, Ananya, Madeshiya, Amit, Li, Yong, Khodadadi, Hesam, Ahmed, Anthony O., Turecki, Gustavo, Baban, Babak, Pillai, Anilkumar
Format Journal Article
LanguageEnglish
Published London Nature Publishing Group UK 01.07.2021
Nature Publishing Group
Subjects
13/21
13/31
631/378
64/60
692/699/476/1414
Animal models
Animals
Behavior
Behavioral Sciences
Biological Psychology
Complement C3
Complement component C3
Gene expression
Health aspects
Inflammation
Interferon
Interferon Type I
Macrophages
Medicine
Medicine & Public Health
Mental disorders
Mice
Mice, Inbred C57BL
Neuroinflammatory Diseases - immunology
Neurosciences
Pharmacotherapy
Prefrontal cortex
Psychiatry
Risk factors
Stress (Psychology)
Stress, Psychological
Suicide
β-Interferon
United States
Online AccessGet full text
ISSN1359-4184
1476-5578
1476-5578
DOI10.1038/s41380-021-01065-6

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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.
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 IFN[beta] 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 IFN[beta]-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.
Audience Academic
Author Madeshiya, Amit
Whitehead, Carl
Baban, Babak
Ahmed, Anthony O.
Pillai, Ananya
Khodadadi, Hesam
Tripathi, Ashutosh
Li, Yong
Turecki, Gustavo
Surrao, Katelyn
Pillai, Anilkumar
AuthorAffiliation 5 Department of Psychiatry, Weill Cornell Medical College, 1300 York Ave, New York, NY, USA
7 Research and Development, Charlie Norwood VA Medical Center, Augusta, GA, USA
6 McGill Group for Suicide Studies, Depressive Disorders Program, Douglas Mental Health University Institute, McGill University, Montreal, Quebec, Canada
2 Department of Psychiatry and Behavioral Sciences, McGovern Medical School, The University of Texas Health Science Center at Houston, Houston, TX, USA
3 Department of Neuroscience and Regenerative Medicine, Augusta University, Augusta, GA, USA
1 Department of Psychiatry and Health Behavior, Medical College of Georgia, Augusta University, Augusta, GA, USA
4 Department of Oral Biology, Dental College of Georgia, Department of Neurology, Augusta University, Augusta, GA, USA
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/33833372$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright 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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StartPage 3043
SubjectTerms 13/21
13/31
631/378
64/60
692/699/476/1414
Animal models
Animals
Behavior
Behavioral Sciences
Biological Psychology
Complement C3
Complement component C3
Gene expression
Health aspects
Inflammation
Interferon
Interferon Type I
Macrophages
Medicine
Medicine & Public Health
Mental disorders
Mice
Mice, Inbred C57BL
Neuroinflammatory Diseases - immunology
Neurosciences
Pharmacotherapy
Prefrontal cortex
Psychiatry
Risk factors
Stress (Psychology)
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://link.springer.com/article/10.1038/s41380-021-01065-6
https://www.ncbi.nlm.nih.gov/pubmed/33833372
https://www.proquest.com/docview/2580805785
https://www.proquest.com/docview/2511247382
https://pubmed.ncbi.nlm.nih.gov/PMC8497654
Volume 26
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