Neurodegenerative evidence in mice brains with cecal ligation and puncture-induced sepsis: preventive effect of the free radical scavenger edaravone
Sepsis is a major clinical challenge and septic encephalopathy is its nasty complication. The pathogenesis and underlying mechanisms of septic encephalopathy are not well understood. This study sought to fully characterize sepsis-associated biochemical and histopathological changes in brains of mice...
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Published in | PloS one Vol. 7; no. 12; p. e51539 |
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Main Authors | , , , , , , , |
Format | Journal Article |
Language | English |
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Public Library of Science
07.12.2012
Public Library of Science (PLoS) |
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Abstract | Sepsis is a major clinical challenge and septic encephalopathy is its nasty complication. The pathogenesis and underlying mechanisms of septic encephalopathy are not well understood. This study sought to fully characterize sepsis-associated biochemical and histopathological changes in brains of mice after cecal ligation and puncture, regarded as a highly clinically relevant animal model of polymicrobial sepsis. Real-time PCR analysis showed that gene expression levels of proinflammatory cytokines, including tumor necrosis factor-α and interleukin-1β, were significantly up-regulated in brain tissues from septic mice, but to a much lesser extent when compared with those in peripheral tissues such as lungs. Blood-brain barrier (BBB) permeability was significantly increased in septic mice, as determined by the measurement of sodium fluorescein and Evans blue content. Sepsis resulted in increases in NADPH oxidase activity and expression of p47(phox) and p67(phox) and up-regulation of inducible nitric oxide (NO) synthase in brains, indicating that superoxide, produced by NADPH oxidase, reacts with NO to form peroxynitrite, that maybe lead to the loss of BBB integrity. Light and electron microscopic examination of septic mouse brain showed serious neuronal degeneration, as indicated by hyperchromatic, shrunken, pyknotic, and electron-dense neurons. These histopathological changes were prevented by treatment with the free radical scavenger edaravone. Together, these results suggest that sepsis can lead to rapid neurodegenerative changes in brains via free radical species production and possibly subsequent injury to the BBB. We may also provide a potentially useful therapeutic tool for treating septic encephalopathy. |
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AbstractList | Sepsis is a major clinical challenge and septic encephalopathy is its nasty complication. The pathogenesis and underlying mechanisms of septic encephalopathy are not well understood. This study sought to fully characterize sepsis-associated biochemical and histopathological changes in brains of mice after cecal ligation and puncture, regarded as a highly clinically relevant animal model of polymicrobial sepsis. Real-time PCR analysis showed that gene expression levels of proinflammatory cytokines, including tumor necrosis factor-α and interleukin-1β, were significantly up-regulated in brain tissues from septic mice, but to a much lesser extent when compared with those in peripheral tissues such as lungs. Blood-brain barrier (BBB) permeability was significantly increased in septic mice, as determined by the measurement of sodium fluorescein and Evans blue content. Sepsis resulted in increases in NADPH oxidase activity and expression of p47(phox) and p67(phox) and up-regulation of inducible nitric oxide (NO) synthase in brains, indicating that superoxide, produced by NADPH oxidase, reacts with NO to form peroxynitrite, that maybe lead to the loss of BBB integrity. Light and electron microscopic examination of septic mouse brain showed serious neuronal degeneration, as indicated by hyperchromatic, shrunken, pyknotic, and electron-dense neurons. These histopathological changes were prevented by treatment with the free radical scavenger edaravone. Together, these results suggest that sepsis can lead to rapid neurodegenerative changes in brains via free radical species production and possibly subsequent injury to the BBB. We may also provide a potentially useful therapeutic tool for treating septic encephalopathy. Sepsis is a major clinical challenge and septic encephalopathy is its nasty complication. The pathogenesis and underlying mechanisms of septic encephalopathy are not well understood. This study sought to fully characterize sepsis-associated biochemical and histopathological changes in brains of mice after cecal ligation and puncture, regarded as a highly clinically relevant animal model of polymicrobial sepsis. Real-time PCR analysis showed that gene expression levels of proinflammatory cytokines, including tumor necrosis factor-α and interleukin-1β, were significantly up-regulated in brain tissues from septic mice, but to a much lesser extent when compared with those in peripheral tissues such as lungs. Blood-brain barrier (BBB) permeability was significantly increased in septic mice, as determined by the measurement of sodium fluorescein and Evans blue content. Sepsis resulted in increases in NADPH oxidase activity and expression of p47phox and p67phox and up-regulation of inducible nitric oxide (NO) synthase in brains, indicating that superoxide, produced by NADPH oxidase, reacts with NO to form peroxynitrite, that maybe lead to the loss of BBB integrity. Light and electron microscopic examination of septic mouse brain showed serious neuronal degeneration, as indicated by hyperchromatic, shrunken, pyknotic, and electron-dense neurons. These histopathogical changes were prevented by treatment with the free radical scavenger edaravone. Together, these results suggest that sepsis can lead to rapid neurodegenerative changes in brains via free radical species production and possibly subsequent injury to the BBB. We may also provide a potentially useful therapeutic tool for treating septic encephalopathy. Sepsis is a major clinical challenge and septic encephalopathy is its nasty complication. The pathogenesis and underlying mechanisms of septic encephalopathy are not well understood. This study sought to fully characterize sepsis-associated biochemical and histopathological changes in brains of mice after cecal ligation and puncture, regarded as a highly clinically relevant animal model of polymicrobial sepsis. Real-time PCR analysis showed that gene expression levels of proinflammatory cytokines, including tumor necrosis factor-α and interleukin-1β, were significantly up-regulated in brain tissues from septic mice, but to a much lesser extent when compared with those in peripheral tissues such as lungs. Blood-brain barrier (BBB) permeability was significantly increased in septic mice, as determined by the measurement of sodium fluorescein and Evans blue content. Sepsis resulted in increases in NADPH oxidase activity and expression of p47 phox and p67 phox and up-regulation of inducible nitric oxide (NO) synthase in brains, indicating that superoxide, produced by NADPH oxidase, reacts with NO to form peroxynitrite, that maybe lead to the loss of BBB integrity. Light and electron microscopic examination of septic mouse brain showed serious neuronal degeneration, as indicated by hyperchromatic, shrunken, pyknotic, and electron-dense neurons. These histopathogical changes were prevented by treatment with the free radical scavenger edaravone. Together, these results suggest that sepsis can lead to rapid neurodegenerative changes in brains via free radical species production and possibly subsequent injury to the BBB. We may also provide a potentially useful therapeutic tool for treating septic encephalopathy. Sepsis is a major clinical challenge and septic encephalopathy is its nasty complication. The pathogenesis and underlying mechanisms of septic encephalopathy are not well understood. This study sought to fully characterize sepsis-associated biochemical and histopathological changes in brains of mice after cecal ligation and puncture, regarded as a highly clinically relevant animal model of polymicrobial sepsis. Real-time PCR analysis showed that gene expression levels of proinflammatory cytokines, including tumor necrosis factor-[alpha] and interleukin-1[beta], were significantly up-regulated in brain tissues from septic mice, but to a much lesser extent when compared with those in peripheral tissues such as lungs. Blood-brain barrier (BBB) permeability was significantly increased in septic mice, as determined by the measurement of sodium fluorescein and Evans blue content. Sepsis resulted in increases in NADPH oxidase activity and expression of p47.sup.phox and p67.sup.phox and up-regulation of inducible nitric oxide (NO) synthase in brains, indicating that superoxide, produced by NADPH oxidase, reacts with NO to form peroxynitrite, that maybe lead to the loss of BBB integrity. Light and electron microscopic examination of septic mouse brain showed serious neuronal degeneration, as indicated by hyperchromatic, shrunken, pyknotic, and electron-dense neurons. These histopathogical changes were prevented by treatment with the free radical scavenger edaravone. Together, these results suggest that sepsis can lead to rapid neurodegenerative changes in brains via free radical species production and possibly subsequent injury to the BBB. We may also provide a potentially useful therapeutic tool for treating septic encephalopathy. |
Audience | Academic |
Author | Hattori, Yuichi Yokoo, Hiroki Tomita, Kengo Chiba, Seiichi Yagisita, Saburo Sagara, Hiroshi Takano, Yasuo Takashina, Michinori |
AuthorAffiliation | 5 Kanagawa Cancer Research Institute, Yokohama, Japan 1 Department of Molecular and Medical Pharmacology, Graduate School of Medicine and Pharmaceutical Sciences, University of Toyama, Toyama, Japan 2 Department of Internal Medicine, Faculty of Medicine, Oita University, Yufu, Japan University of São Paulo, Brazil 3 Medical Proteomics Laboratory, Institute of Medical Science, University of Tokyo, Tokyo, Japan 4 Section of Pathology, Kanagawa Rehabilitation Center, Atsugi, Japan |
AuthorAffiliation_xml | – name: 3 Medical Proteomics Laboratory, Institute of Medical Science, University of Tokyo, Tokyo, Japan – name: University of São Paulo, Brazil – name: 5 Kanagawa Cancer Research Institute, Yokohama, Japan – name: 2 Department of Internal Medicine, Faculty of Medicine, Oita University, Yufu, Japan – name: 4 Section of Pathology, Kanagawa Rehabilitation Center, Atsugi, Japan – name: 1 Department of Molecular and Medical Pharmacology, Graduate School of Medicine and Pharmaceutical Sciences, University of Toyama, Toyama, Japan |
Author_xml | – sequence: 1 givenname: Hiroki surname: Yokoo fullname: Yokoo, Hiroki email: hyokoo@med.u-toyama.ac.jp organization: Department of Molecular and Medical Pharmacology, Graduate School of Medicine and Pharmaceutical Sciences, University of Toyama, Toyama, Japan. hyokoo@med.u-toyama.ac.jp – sequence: 2 givenname: Seiichi surname: Chiba fullname: Chiba, Seiichi – sequence: 3 givenname: Kengo surname: Tomita fullname: Tomita, Kengo – sequence: 4 givenname: Michinori surname: Takashina fullname: Takashina, Michinori – sequence: 5 givenname: Hiroshi surname: Sagara fullname: Sagara, Hiroshi – sequence: 6 givenname: Saburo surname: Yagisita fullname: Yagisita, Saburo – sequence: 7 givenname: Yasuo surname: Takano fullname: Takano, Yasuo – sequence: 8 givenname: Yuichi surname: Hattori fullname: Hattori, Yuichi |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/23236515$$D View this record in MEDLINE/PubMed |
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Copyright | COPYRIGHT 2012 Public Library of Science 2012 Yokoo et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: https://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2012 Yokoo et al 2012 Yokoo et al |
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Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Conceived and designed the experiments: HY YH. Performed the experiments: HY SC KT MT HS. Analyzed the data: HY SY YT YH. Contributed reagents/materials/analysis tools: HY SC KT MT SY YT. Wrote the paper: HY SY YH. Competing Interests: The authors have declared that no competing interests exist. |
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Snippet | Sepsis is a major clinical challenge and septic encephalopathy is its nasty complication. The pathogenesis and underlying mechanisms of septic encephalopathy... |
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SubjectTerms | Abdomen Analysis Animal tissues Animals Antipyrine - analogs & derivatives Antipyrine - therapeutic use Biology Blood-brain barrier Blood-Brain Barrier - metabolism Brain Cecum Cecum - injuries Cytokines Cytokines - metabolism Degeneration Encephalopathy Evans Blue Fluorescein Free Radical Scavengers - therapeutic use Free radicals Gene expression Gene Expression Regulation - immunology Health aspects Hypoxia Infection Inflammation Intensive care Interleukins Ischemia Kinases Laboratory animals Ligation Lungs Medicine Membrane permeability Mice Microscopy, Electron Multiple sclerosis NAD(P)H oxidase NADPH Oxidases - metabolism Neurodegeneration Neurodegenerative Diseases - etiology Neurodegenerative Diseases - pathology Neurodegenerative Diseases - prevention & control Neurons Nitric oxide Nitric Oxide Synthase Type II - biosynthesis Oxidase Oxidases Pathogenesis Permeability Peroxynitrite Pharmaceutical sciences Pharmacology Phosphoproteins - metabolism Real-Time Polymerase Chain Reaction Rodents Sepsis Sepsis - complications Sepsis - etiology Sodium Stroke Superoxide Superoxides Tumor necrosis factor Tumor necrosis factor-TNF Tumor necrosis factor-α Uric acid |
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Title | Neurodegenerative evidence in mice brains with cecal ligation and puncture-induced sepsis: preventive effect of the free radical scavenger edaravone |
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