Microglia priming by interleukin-6 signaling is enhanced in aged mice
During peripheral infection, excessive production of pro-inflammatory cytokines in the aged brain from primed microglia induces exaggerated behavioral pathologies. While the pro-inflammatory cytokine IL-6 increases in the brain with age, its role in microglia priming is not known. This study examine...
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| Published in | Journal of neuroimmunology Vol. 324; pp. 90 - 99 |
|---|---|
| Main Authors | , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Netherlands
Elsevier B.V
15.11.2018
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| Subjects | |
| Online Access | Get full text |
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| Abstract | During peripheral infection, excessive production of pro-inflammatory cytokines in the aged brain from primed microglia induces exaggerated behavioral pathologies. While the pro-inflammatory cytokine IL-6 increases in the brain with age, its role in microglia priming is not known. This study examined the functional role of IL-6 signaling on microglia priming. Our hypothesis is that IL-6 signaling mediates primed states of microglia in the aged. An initial study assessed age-related alteration in IL-6 signaling molecules; sIL-6R and sgp130 were measured in cerebrospinal fluid of young and aged wild-type animals. Subsequent studies of isolated microglia from C57BL6/J (IL-6+/+) and IL-6 knock-out (IL-6−/−) mice showed significantly less MHC-II expression in aged IL-6−/− compared to IL-6+/+ counterparts. Additionally, adult and aged IL-6+/+ and IL-6−/− animals were administered lipopolysaccharide (LPS) to simulate a peripheral infection; sickness behaviors and hippocampal cytokine gene expression were measured over a 24 h period. Aged IL-6−/− animals were resilient to LPS-induced sickness behaviors and recovered more quickly than IL-6+/+ animals. The age-associated baseline increase of IL-1β gene expression was ablated in aged IL-6−/− mice, suggesting IL-6 is a key driver of cytokine activity from primed microglia in the aged brain. We employed in vitro studies to understand molecular mechanisms in priming factors. MHC-II and pro-inflammatory gene expression (IL-1β, IL-10, IL-6) were measured after treating BV.2 microglia with sIL-6R and IL-6 or IL-6 alone. sIL-6R enhanced expression of both pro-inflammatory genes and MHC-II. Taken together, these data suggest IL-6 expression throughout life is involved in microglia priming and increased amounts of IL-6 following peripheral LPS challenge are involved in exaggerated sickness behaviors in the aged.
[Display omitted]
•IL-6 trans-signaling is involved in microglia priming.•Microglia in aged mice are more susceptible to IL-6-induced priming.•Ablation of IL-6 signaling significantly reduces exaggerated LPS-induced sickness behaviors in aged animals. |
|---|---|
| AbstractList | During peripheral infection, excessive production of pro-inflammatory cytokines in the aged brain from primed microglia induces exaggerated behavioral pathologies. While the pro-inflammatory cytokine IL-6 increases in the brain with age, its role in microglia priming is not known. This study examined the functional role of IL-6 signaling on microglia priming. Our hypothesis is that IL-6 signaling mediates primed states of microglia in the aged. An initial study assessed age-related alteration in IL-6 signaling molecules; sIL-6R and sgp130 were measured in cerebrospinal fluid of young and aged wild-type animals. Subsequent studies of isolated microglia from C57BL6/J (IL-6
+/+
) and IL-6 knock-out (IL-6
−/−
) mice showed significantly less MHC-II expression in aged IL-6
−/−
compared to IL-6
+/+
counterparts. Additionally, adult and aged IL-6
+/+
and IL-6
−/−
animals were administered lipopolysaccharide (LPS) to simulate a peripheral infection; sickness behaviors and hippocampal cytokine gene expression were measured over a 24 h period. Aged IL-6
−/−
animals were resilient to LPS-induced sickness behaviors and recovered more quickly than IL-6
+/+
animals. The age-associated baseline increase of IL-1β gene expression was ablated in aged IL-6
−/−
mice, suggesting IL-6 is a key driver of cytokine activity from primed microglia in the aged brain. We employed
in vitro
studies to understand molecular mechanisms in priming factors. MHC-II and pro-inflammatory gene expression (IL-1β, IL-10, IL-6) were measured after treating BV.2 microglia with sIL-6R and IL-6 or IL-6 alone. sIL-6R enhanced expression of both pro-inflammatory genes and MHC-II. Taken together, these data suggest IL-6 expression throughout life is involved in microglia priming and increased amounts of IL-6 following peripheral LPS challenge are involved in exaggerated sickness behaviors in the aged. During peripheral infection, excessive production of pro-inflammatory cytokines in the aged brain from primed microglia induces exaggerated behavioral pathologies. While the pro-inflammatory cytokine IL-6 increases in the brain with age, its role in microglia priming is not known. This study examined the functional role of IL-6 signaling on microglia priming. Our hypothesis is that IL-6 signaling mediates primed states of microglia in the aged. An initial study assessed age-related alteration in IL-6 signaling molecules; sIL-6R and sgp130 were measured in cerebrospinal fluid of young and aged wild-type animals. Subsequent studies of isolated microglia from C57BL6/J (IL-6+/+) and IL-6 knock-out (IL-6−/−) mice showed significantly less MHC-II expression in aged IL-6−/− compared to IL-6+/+ counterparts. Additionally, adult and aged IL-6+/+ and IL-6−/− animals were administered lipopolysaccharide (LPS) to simulate a peripheral infection; sickness behaviors and hippocampal cytokine gene expression were measured over a 24 h period. Aged IL-6−/− animals were resilient to LPS-induced sickness behaviors and recovered more quickly than IL-6+/+ animals. The age-associated baseline increase of IL-1β gene expression was ablated in aged IL-6−/− mice, suggesting IL-6 is a key driver of cytokine activity from primed microglia in the aged brain. We employed in vitro studies to understand molecular mechanisms in priming factors. MHC-II and pro-inflammatory gene expression (IL-1β, IL-10, IL-6) were measured after treating BV.2 microglia with sIL-6R and IL-6 or IL-6 alone. sIL-6R enhanced expression of both pro-inflammatory genes and MHC-II. Taken together, these data suggest IL-6 expression throughout life is involved in microglia priming and increased amounts of IL-6 following peripheral LPS challenge are involved in exaggerated sickness behaviors in the aged. [Display omitted] •IL-6 trans-signaling is involved in microglia priming.•Microglia in aged mice are more susceptible to IL-6-induced priming.•Ablation of IL-6 signaling significantly reduces exaggerated LPS-induced sickness behaviors in aged animals. During peripheral infection, excessive production of pro-inflammatory cytokines in the aged brain from primed microglia induces exaggerated behavioral pathologies. While the pro-inflammatory cytokine IL-6 increases in the brain with age, its role in microglia priming is not known. This study examined the functional role of IL-6 signaling on microglia priming. Our hypothesis is that IL-6 signaling mediates primed states of microglia in the aged. An initial study assessed age-related alteration in IL-6 signaling molecules; sIL-6R and sgp130 were measured in cerebrospinal fluid of young and aged wild-type animals. Subsequent studies of isolated microglia from C57BL6/J (IL-6+/+) and IL-6 knock-out (IL-6-/-) mice showed significantly less MHC-II expression in aged IL-6-/- compared to IL-6+/+ counterparts. Additionally, adult and aged IL-6+/+ and IL-6-/- animals were administered lipopolysaccharide (LPS) to simulate a peripheral infection; sickness behaviors and hippocampal cytokine gene expression were measured over a 24 h period. Aged IL-6-/- animals were resilient to LPS-induced sickness behaviors and recovered more quickly than IL-6+/+ animals. The age-associated baseline increase of IL-1β gene expression was ablated in aged IL-6-/- mice, suggesting IL-6 is a key driver of cytokine activity from primed microglia in the aged brain. We employed in vitro studies to understand molecular mechanisms in priming factors. MHC-II and pro-inflammatory gene expression (IL-1β, IL-10, IL-6) were measured after treating BV.2 microglia with sIL-6R and IL-6 or IL-6 alone. sIL-6R enhanced expression of both pro-inflammatory genes and MHC-II. Taken together, these data suggest IL-6 expression throughout life is involved in microglia priming and increased amounts of IL-6 following peripheral LPS challenge are involved in exaggerated sickness behaviors in the aged.During peripheral infection, excessive production of pro-inflammatory cytokines in the aged brain from primed microglia induces exaggerated behavioral pathologies. While the pro-inflammatory cytokine IL-6 increases in the brain with age, its role in microglia priming is not known. This study examined the functional role of IL-6 signaling on microglia priming. Our hypothesis is that IL-6 signaling mediates primed states of microglia in the aged. An initial study assessed age-related alteration in IL-6 signaling molecules; sIL-6R and sgp130 were measured in cerebrospinal fluid of young and aged wild-type animals. Subsequent studies of isolated microglia from C57BL6/J (IL-6+/+) and IL-6 knock-out (IL-6-/-) mice showed significantly less MHC-II expression in aged IL-6-/- compared to IL-6+/+ counterparts. Additionally, adult and aged IL-6+/+ and IL-6-/- animals were administered lipopolysaccharide (LPS) to simulate a peripheral infection; sickness behaviors and hippocampal cytokine gene expression were measured over a 24 h period. Aged IL-6-/- animals were resilient to LPS-induced sickness behaviors and recovered more quickly than IL-6+/+ animals. The age-associated baseline increase of IL-1β gene expression was ablated in aged IL-6-/- mice, suggesting IL-6 is a key driver of cytokine activity from primed microglia in the aged brain. We employed in vitro studies to understand molecular mechanisms in priming factors. MHC-II and pro-inflammatory gene expression (IL-1β, IL-10, IL-6) were measured after treating BV.2 microglia with sIL-6R and IL-6 or IL-6 alone. sIL-6R enhanced expression of both pro-inflammatory genes and MHC-II. Taken together, these data suggest IL-6 expression throughout life is involved in microglia priming and increased amounts of IL-6 following peripheral LPS challenge are involved in exaggerated sickness behaviors in the aged. During peripheral infection, excessive production of pro-inflammatory cytokines in the aged brain from primed microglia induces exaggerated behavioral pathologies. While the pro-inflammatory cytokine IL-6 increases in the brain with age, its role in microglia priming is not known. This study examined the functional role of IL-6 signaling on microglia priming. Our hypothesis is that IL-6 signaling mediates primed states of microglia in the aged. An initial study assessed age-related alteration in IL-6 signaling molecules; sIL-6R and sgp130 were measured in cerebrospinal fluid of young and aged wild-type animals. Subsequent studies of isolated microglia from C57BL6/J (IL-6 ) and IL-6 knock-out (IL-6 ) mice showed significantly less MHC-II expression in aged IL-6 compared to IL-6 counterparts. Additionally, adult and aged IL-6 and IL-6 animals were administered lipopolysaccharide (LPS) to simulate a peripheral infection; sickness behaviors and hippocampal cytokine gene expression were measured over a 24 h period. Aged IL-6 animals were resilient to LPS-induced sickness behaviors and recovered more quickly than IL-6 animals. The age-associated baseline increase of IL-1β gene expression was ablated in aged IL-6 mice, suggesting IL-6 is a key driver of cytokine activity from primed microglia in the aged brain. We employed in vitro studies to understand molecular mechanisms in priming factors. MHC-II and pro-inflammatory gene expression (IL-1β, IL-10, IL-6) were measured after treating BV.2 microglia with sIL-6R and IL-6 or IL-6 alone. sIL-6R enhanced expression of both pro-inflammatory genes and MHC-II. Taken together, these data suggest IL-6 expression throughout life is involved in microglia priming and increased amounts of IL-6 following peripheral LPS challenge are involved in exaggerated sickness behaviors in the aged. |
| Author | Johnson, Rodney W. Scarlett, Emily J. Burton, Michael D. Garner, Katherine M. Amin, Ravi |
| AuthorAffiliation | 3 Laboratory of Integrative Immunology and Behavior, Animal Science Department, University of Illinois at Urbana-Champaign, Urbana, 7 Animal Sciences Lab 1207 W. Gregory Dr., Urbana, IL 61801, USA 2 Center for Advanced Pain Studies, University of Texas at Dallas, Richardson, TX 75080 1 Laboratory of Neuroimmunolgy and Behavior, School of Behavioral and Brain Sciences, University of Texas at Dallas 800 W. Campbell Road, Richardson, TX 75080, United States |
| AuthorAffiliation_xml | – name: 2 Center for Advanced Pain Studies, University of Texas at Dallas, Richardson, TX 75080 – name: 3 Laboratory of Integrative Immunology and Behavior, Animal Science Department, University of Illinois at Urbana-Champaign, Urbana, 7 Animal Sciences Lab 1207 W. Gregory Dr., Urbana, IL 61801, USA – name: 1 Laboratory of Neuroimmunolgy and Behavior, School of Behavioral and Brain Sciences, University of Texas at Dallas 800 W. Campbell Road, Richardson, TX 75080, United States |
| Author_xml | – sequence: 1 givenname: Katherine M. surname: Garner fullname: Garner, Katherine M. organization: Laboratory of Neuroimmunolgy and Behavior, School of Behavioral and Brain Sciences and Center for Advanced Pain Studies, University of Texas at Dallas, 800 W. Campbell Road, Richardson, TX 75080, United States – sequence: 2 givenname: Ravi surname: Amin fullname: Amin, Ravi organization: Laboratory of Integrative Immunology and Behavior, Animal Science Department, University of Illinois at Urbana-Champaign, 7 Animal Sciences Lab 1207 W. Gregory Dr., Urbana, IL 61801, USA – sequence: 3 givenname: Rodney W. surname: Johnson fullname: Johnson, Rodney W. organization: Laboratory of Neuroimmunolgy and Behavior, School of Behavioral and Brain Sciences and Center for Advanced Pain Studies, University of Texas at Dallas, 800 W. Campbell Road, Richardson, TX 75080, United States – sequence: 4 givenname: Emily J. surname: Scarlett fullname: Scarlett, Emily J. organization: Laboratory of Neuroimmunolgy and Behavior, School of Behavioral and Brain Sciences and Center for Advanced Pain Studies, University of Texas at Dallas, 800 W. Campbell Road, Richardson, TX 75080, United States – sequence: 5 givenname: Michael D. orcidid: 0000-0002-0628-824X surname: Burton fullname: Burton, Michael D. email: michael.burton@utdallas.edu organization: Laboratory of Neuroimmunolgy and Behavior, School of Behavioral and Brain Sciences and Center for Advanced Pain Studies, University of Texas at Dallas, 800 W. Campbell Road, Richardson, TX 75080, United States |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30261355$$D View this record in MEDLINE/PubMed |
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| Keywords | STAT3 Inflammation IL-6 LPS sgp130 IL-6 trans signaling TNF-α sIL-6R gp130 Neuroimmunology IL-1B CD68 CD45 MHC-II |
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| SubjectTerms | Aging - drug effects Aging - immunology Aging - metabolism Animals Cell Line IL-6 trans signaling Inflammation Interleukin-6 - biosynthesis Interleukin-6 - genetics Interleukin-6 - immunology Lipopolysaccharides - toxicity Male MHC-II Mice Mice, Inbred C57BL Mice, Knockout Microglia - drug effects Microglia - immunology Microglia - metabolism Neuroimmunology Signal Transduction - physiology |
| Title | Microglia priming by interleukin-6 signaling is enhanced in aged mice |
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