Resolvins AT-D1 and E1 differentially impact functional outcome, post-traumatic sleep, and microglial activation following diffuse brain injury in the mouse
•Diffuse TBI resulted in motor and cognitive impairments in the mouse.•AT-RvD1, but not RvE1, facilitated functional recovery.•RvE1-treated brain-injured mice slept significantly more immediately after TBI.•RvE1, but not AT-RvD1, decreased the injury-induced activation of microglia to TBI.•AT-RvD1 &...
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| Published in | Brain, behavior, and immunity Vol. 47; pp. 131 - 140 |
|---|---|
| Main Authors | , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Netherlands
Elsevier Inc
01.07.2015
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| Subjects | |
| Online Access | Get full text |
| ISSN | 0889-1591 1090-2139 1090-2139 |
| DOI | 10.1016/j.bbi.2015.01.001 |
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| Abstract | •Diffuse TBI resulted in motor and cognitive impairments in the mouse.•AT-RvD1, but not RvE1, facilitated functional recovery.•RvE1-treated brain-injured mice slept significantly more immediately after TBI.•RvE1, but not AT-RvD1, decreased the injury-induced activation of microglia to TBI.•AT-RvD1 & RvE1 independently altered sleep, inflammation, and outcome after TBI.
Traumatic brain injury (TBI) is induced by mechanical forces which initiate a cascade of secondary injury processes, including inflammation. Therapies which resolve the inflammatory response may promote neural repair without exacerbating the primary injury. Specific derivatives of omega-3 fatty acids loosely grouped as specialized pro-resolving lipid mediators (SPMs) and termed resolvins promote the active resolution of inflammation. In the current study, we investigate the effect of two resolvin molecules, RvE1 and AT-RvD1, on post-traumatic sleep and functional outcome following diffuse TBI through modulation of the inflammatory response.
Adult, male C57BL/6 mice were injured using a midline fluid percussion injury (mFPI) model (6–10min righting reflex time for brain-injured mice). Experimental groups included mFPI administered RvE1 (100ng daily), AT-RvD1 (100ng daily), or vehicle (sterile saline) and counterbalanced with uninjured sham mice. Resolvins or saline were administered daily for seven consecutive days beginning 3days prior to TBI to evaluate proof-of-principle to improve outcome. Immediately following diffuse TBI, post-traumatic sleep was recorded for 24h post-injury. For days 1–7 post-injury, motor outcome was assessed by rotarod. Cognitive function was measured at 6days post-injury using novel object recognition (NOR). At 7days post-injury, microglial activation was quantified using immunohistochemistry for Iba-1.
In the diffuse brain-injured mouse, AT-RvD1 treatment, but not RvE1, mitigated motor and cognitive deficits. RvE1 treatment significantly increased post-traumatic sleep in brain-injured mice compared to all other groups. RvE1 treated mice displayed a higher proportion of ramified microglia and lower proportion of activated rod microglia in the cortex compared to saline or AT-RvD1 treated brain-injured mice. Thus, RvE1 treatment modulated post-traumatic sleep and the inflammatory response to TBI, albeit independently of improvement in motor and cognitive outcome as seen in AT-RvD1-treated mice. This suggests AT-RvD1 may impart functional benefit through mechanisms other than resolution of inflammation alone. |
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| AbstractList | Traumatic brain injury (TBI) is induced by mechanical forces which initiate a cascade of secondary injury processes, including inflammation. Therapies which resolve the inflammatory response may promote neural repair without exacerbating the primary injury. Specific derivatives of omega-3 fatty acids loosely grouped as specialized pro-resolving lipid mediators (SPMs) and termed resolvins promote the active resolution of inflammation. In the current study, we investigate the effect of two resolvin molecules, RvE1 and AT-RvD1, on post-traumatic sleep and functional outcome following diffuse TBI through modulation of the inflammatory response. Adult, male C57BL/6 mice were injured using a midline fluid percussion injury (mFPI) model (6-10min righting reflex time for brain-injured mice). Experimental groups included mFPI administered RvE1 (100ng daily), AT-RvD1 (100ng daily), or vehicle (sterile saline) and counterbalanced with uninjured sham mice. Resolvins or saline were administered daily for seven consecutive days beginning 3days prior to TBI to evaluate proof-of-principle to improve outcome. Immediately following diffuse TBI, post-traumatic sleep was recorded for 24h post-injury. For days 1-7 post-injury, motor outcome was assessed by rotarod. Cognitive function was measured at 6days post-injury using novel object recognition (NOR). At 7days post-injury, microglial activation was quantified using immunohistochemistry for Iba-1. In the diffuse brain-injured mouse, AT-RvD1 treatment, but not RvE1, mitigated motor and cognitive deficits. RvE1 treatment significantly increased post-traumatic sleep in brain-injured mice compared to all other groups. RvE1 treated mice displayed a higher proportion of ramified microglia and lower proportion of activated rod microglia in the cortex compared to saline or AT-RvD1 treated brain-injured mice. Thus, RvE1 treatment modulated post-traumatic sleep and the inflammatory response to TBI, albeit independently of improvement in motor and cognitive outcome as seen in AT-RvD1-treated mice. This suggests AT-RvD1 may impart functional benefit through mechanisms other than resolution of inflammation alone.Traumatic brain injury (TBI) is induced by mechanical forces which initiate a cascade of secondary injury processes, including inflammation. Therapies which resolve the inflammatory response may promote neural repair without exacerbating the primary injury. Specific derivatives of omega-3 fatty acids loosely grouped as specialized pro-resolving lipid mediators (SPMs) and termed resolvins promote the active resolution of inflammation. In the current study, we investigate the effect of two resolvin molecules, RvE1 and AT-RvD1, on post-traumatic sleep and functional outcome following diffuse TBI through modulation of the inflammatory response. Adult, male C57BL/6 mice were injured using a midline fluid percussion injury (mFPI) model (6-10min righting reflex time for brain-injured mice). Experimental groups included mFPI administered RvE1 (100ng daily), AT-RvD1 (100ng daily), or vehicle (sterile saline) and counterbalanced with uninjured sham mice. Resolvins or saline were administered daily for seven consecutive days beginning 3days prior to TBI to evaluate proof-of-principle to improve outcome. Immediately following diffuse TBI, post-traumatic sleep was recorded for 24h post-injury. For days 1-7 post-injury, motor outcome was assessed by rotarod. Cognitive function was measured at 6days post-injury using novel object recognition (NOR). At 7days post-injury, microglial activation was quantified using immunohistochemistry for Iba-1. In the diffuse brain-injured mouse, AT-RvD1 treatment, but not RvE1, mitigated motor and cognitive deficits. RvE1 treatment significantly increased post-traumatic sleep in brain-injured mice compared to all other groups. RvE1 treated mice displayed a higher proportion of ramified microglia and lower proportion of activated rod microglia in the cortex compared to saline or AT-RvD1 treated brain-injured mice. Thus, RvE1 treatment modulated post-traumatic sleep and the inflammatory response to TBI, albeit independently of improvement in motor and cognitive outcome as seen in AT-RvD1-treated mice. This suggests AT-RvD1 may impart functional benefit through mechanisms other than resolution of inflammation alone. •Diffuse TBI resulted in motor and cognitive impairments in the mouse.•AT-RvD1, but not RvE1, facilitated functional recovery.•RvE1-treated brain-injured mice slept significantly more immediately after TBI.•RvE1, but not AT-RvD1, decreased the injury-induced activation of microglia to TBI.•AT-RvD1 & RvE1 independently altered sleep, inflammation, and outcome after TBI. Traumatic brain injury (TBI) is induced by mechanical forces which initiate a cascade of secondary injury processes, including inflammation. Therapies which resolve the inflammatory response may promote neural repair without exacerbating the primary injury. Specific derivatives of omega-3 fatty acids loosely grouped as specialized pro-resolving lipid mediators (SPMs) and termed resolvins promote the active resolution of inflammation. In the current study, we investigate the effect of two resolvin molecules, RvE1 and AT-RvD1, on post-traumatic sleep and functional outcome following diffuse TBI through modulation of the inflammatory response. Adult, male C57BL/6 mice were injured using a midline fluid percussion injury (mFPI) model (6–10min righting reflex time for brain-injured mice). Experimental groups included mFPI administered RvE1 (100ng daily), AT-RvD1 (100ng daily), or vehicle (sterile saline) and counterbalanced with uninjured sham mice. Resolvins or saline were administered daily for seven consecutive days beginning 3days prior to TBI to evaluate proof-of-principle to improve outcome. Immediately following diffuse TBI, post-traumatic sleep was recorded for 24h post-injury. For days 1–7 post-injury, motor outcome was assessed by rotarod. Cognitive function was measured at 6days post-injury using novel object recognition (NOR). At 7days post-injury, microglial activation was quantified using immunohistochemistry for Iba-1. In the diffuse brain-injured mouse, AT-RvD1 treatment, but not RvE1, mitigated motor and cognitive deficits. RvE1 treatment significantly increased post-traumatic sleep in brain-injured mice compared to all other groups. RvE1 treated mice displayed a higher proportion of ramified microglia and lower proportion of activated rod microglia in the cortex compared to saline or AT-RvD1 treated brain-injured mice. Thus, RvE1 treatment modulated post-traumatic sleep and the inflammatory response to TBI, albeit independently of improvement in motor and cognitive outcome as seen in AT-RvD1-treated mice. This suggests AT-RvD1 may impart functional benefit through mechanisms other than resolution of inflammation alone. Traumatic brain injury (TBI) is induced by mechanical forces which initiate a cascade of secondary injury processes, including inflammation. Therapies which resolve the inflammatory response may promote neural repair without exacerbating the primary injury. Specific derivatives of omega-3 fatty acids loosely grouped as specialized pro-resolving lipid mediators (SPMs) and termed resolvins promote the active resolution of inflammation. In the current study, we investigate the effect of two resolvin molecules, RvE1 and AT-RvD1, on post-traumatic sleep and functional outcome following diffuse TBI through modulation of the inflammatory response. Adult, male C57BL/6 mice were injured using a midline fluid percussion injury (mFPI) model (6-10 min righting reflex time for brain-injured mice). Experimental groups included mFPI administered RvE1 (100ng daily), AT-RvD1 (100ng daily), or vehicle (sterile saline) and counterbalanced with uninjured sham mice. Resolvins or saline were administered daily for seven consecutive days beginning 3 days prior to TBI to evaluate proof-of-principle to improve outcome. Immediately following diffuse TBI, post-traumatic sleep was recorded for 24 hours post-injury. For days 1-7 post-injury, motor outcome was assessed by Rotarod. Cognitive function was measured at 6 days post-injury using Novel Object Recognition (NOR). At 7 days post-injury, microglial activation was quantified using immunohistochemistry for Iba-1. In the diffuse brain-injured mouse, AT-RvD1 treatment, but not RvE1, mitigated motor and cognitive deficits. RvE1 treatment significantly increased post-traumatic sleep in brain-injured mice compared to all other groups. RvE1 treated mice displayed a higher proportion of ramified microglia and lower proportion of activated rod microglia in the cortex compared to saline or AT-RvD1 treated brain-injured mice. Thus, RvE1 treatment modulated post-traumatic sleep and the inflammatory response to TBI, albeit independently of improvement in motor and cognitive outcome as seen in AT-RvD1-treated mice. This suggests AT-RvD1 may impart functional benefit through mechanisms other than resolution of inflammation alone. Highlights • Diffuse TBI resulted in motor and cognitive impairments in the mouse. • AT-RvD1, but not RvE1, facilitated functional recovery. • RvE1-treated brain-injured mice slept significantly more immediately after TBI. • RvE1, but not AT-RvD1, decreased the injury-induced activation of microglia to TBI. • AT-RvD1 & RvE1 independently altered sleep, inflammation, and outcome after TBI. Traumatic brain injury (TBI) is induced by mechanical forces which initiate a cascade of secondary injury processes, including inflammation. Therapies which resolve the inflammatory response may promote neural repair without exacerbating the primary injury. Specific derivatives of omega-3 fatty acids loosely grouped as specialized pro-resolving lipid mediators (SPMs) and termed resolvins promote the active resolution of inflammation. In the current study, we investigate the effect of two resolvin molecules, RvE1 and AT-RvD1, on post-traumatic sleep and functional outcome following diffuse TBI through modulation of the inflammatory response. Adult, male C57BL/6 mice were injured using a midline fluid percussion injury (mFPI) model (6-10min righting reflex time for brain-injured mice). Experimental groups included mFPI administered RvE1 (100ng daily), AT-RvD1 (100ng daily), or vehicle (sterile saline) and counterbalanced with uninjured sham mice. Resolvins or saline were administered daily for seven consecutive days beginning 3days prior to TBI to evaluate proof-of-principle to improve outcome. Immediately following diffuse TBI, post-traumatic sleep was recorded for 24h post-injury. For days 1-7 post-injury, motor outcome was assessed by rotarod. Cognitive function was measured at 6days post-injury using novel object recognition (NOR). At 7days post-injury, microglial activation was quantified using immunohistochemistry for Iba-1. In the diffuse brain-injured mouse, AT-RvD1 treatment, but not RvE1, mitigated motor and cognitive deficits. RvE1 treatment significantly increased post-traumatic sleep in brain-injured mice compared to all other groups. RvE1 treated mice displayed a higher proportion of ramified microglia and lower proportion of activated rod microglia in the cortex compared to saline or AT-RvD1 treated brain-injured mice. Thus, RvE1 treatment modulated post-traumatic sleep and the inflammatory response to TBI, albeit independently of improvement in motor and cognitive outcome as seen in AT-RvD1-treated mice. This suggests AT-RvD1 may impart functional benefit through mechanisms other than resolution of inflammation alone. |
| Author | Harrison, Jordan L. Rowe, Rachel K. Yee, Nicole S. Lifshitz, Jonathan Adelson, P. David Ellis, Timothy W. O’Hara, Bruce F. |
| AuthorAffiliation | 6 Department of Biology, University of Kentucky College of Arts and Sciences, Lexington, KY 5 College of Osteopathic Medicine, Midwestern University, Glendale, AZ 2 Department of Child Health, University of Arizona College of Medicine - Phoenix, Phoenix, AZ 4 Phoenix Veteran Affairs Healthcare System, Phoenix, AZ 7 Spinal Cord and Brain Injury Research Center, University of Kentucky College of Medicine, Lexington, KY, USA 1 BARROW Neurological Institute at Phoenix Children’s Hospital, Phoenix, AZ 3 Interdisciplinary Graduate Program in Neuroscience, Arizona State University, Tempe, AZ |
| AuthorAffiliation_xml | – name: 3 Interdisciplinary Graduate Program in Neuroscience, Arizona State University, Tempe, AZ – name: 1 BARROW Neurological Institute at Phoenix Children’s Hospital, Phoenix, AZ – name: 5 College of Osteopathic Medicine, Midwestern University, Glendale, AZ – name: 4 Phoenix Veteran Affairs Healthcare System, Phoenix, AZ – name: 7 Spinal Cord and Brain Injury Research Center, University of Kentucky College of Medicine, Lexington, KY, USA – name: 2 Department of Child Health, University of Arizona College of Medicine - Phoenix, Phoenix, AZ – name: 6 Department of Biology, University of Kentucky College of Arts and Sciences, Lexington, KY |
| Author_xml | – sequence: 1 givenname: Jordan L. surname: Harrison fullname: Harrison, Jordan L. organization: BARROW Neurological Institute at Phoenix Children’s Hospital, Phoenix, AZ, USA – sequence: 2 givenname: Rachel K. surname: Rowe fullname: Rowe, Rachel K. organization: BARROW Neurological Institute at Phoenix Children’s Hospital, Phoenix, AZ, USA – sequence: 3 givenname: Timothy W. surname: Ellis fullname: Ellis, Timothy W. organization: BARROW Neurological Institute at Phoenix Children’s Hospital, Phoenix, AZ, USA – sequence: 4 givenname: Nicole S. surname: Yee fullname: Yee, Nicole S. organization: BARROW Neurological Institute at Phoenix Children’s Hospital, Phoenix, AZ, USA – sequence: 5 givenname: Bruce F. surname: O’Hara fullname: O’Hara, Bruce F. organization: Department of Biology, University of Kentucky College of Arts and Sciences, Lexington, KY, USA – sequence: 6 givenname: P. David surname: Adelson fullname: Adelson, P. David organization: BARROW Neurological Institute at Phoenix Children’s Hospital, Phoenix, AZ, USA – sequence: 7 givenname: Jonathan surname: Lifshitz fullname: Lifshitz, Jonathan email: jlifshitz@email.arizona.edu organization: BARROW Neurological Institute at Phoenix Children’s Hospital, Phoenix, AZ, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25585137$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | 2015 Elsevier Inc. Elsevier Inc. Copyright © 2015 Elsevier Inc. All rights reserved. 2014 Elsevier Inc. All rights reserved. 2014 |
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| Snippet | •Diffuse TBI resulted in motor and cognitive impairments in the mouse.•AT-RvD1, but not RvE1, facilitated functional recovery.•RvE1-treated brain-injured mice... Highlights • Diffuse TBI resulted in motor and cognitive impairments in the mouse. • AT-RvD1, but not RvE1, facilitated functional recovery. • RvE1-treated... Traumatic brain injury (TBI) is induced by mechanical forces which initiate a cascade of secondary injury processes, including inflammation. Therapies which... |
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| SubjectTerms | Allergy and Immunology Animals Aspirin-triggered resolvin Behavior Brain Injuries - metabolism Brain Injuries - physiopathology Cognition - drug effects Cognition - physiology Docosahexaenoic Acids - pharmacology Eicosapentaenoic Acid - analogs & derivatives Eicosapentaenoic Acid - pharmacology Inflammation Inflammation - metabolism Inflammation - physiopathology Male Memory - drug effects Memory - physiology Mice Mice, Inbred C57BL Microglia - drug effects Microglia - metabolism Motor Activity - drug effects Motor Activity - physiology Mouse Protectins Psychiatry Resolvins Sleep Sleep - drug effects Sleep - physiology TBI |
| Title | Resolvins AT-D1 and E1 differentially impact functional outcome, post-traumatic sleep, and microglial activation following diffuse brain injury in the mouse |
| URI | https://www.clinicalkey.com/#!/content/1-s2.0-S0889159115000033 https://www.clinicalkey.es/playcontent/1-s2.0-S0889159115000033 https://dx.doi.org/10.1016/j.bbi.2015.01.001 https://www.ncbi.nlm.nih.gov/pubmed/25585137 https://www.proquest.com/docview/1689312252 https://www.proquest.com/docview/1701492440 https://pubmed.ncbi.nlm.nih.gov/PMC4468045 |
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