Spinal cord transection-induced allodynia in rats--behavioral, physiopathological and pharmacological characterization
In humans, spinal cord lesions induce not only major motor and neurovegetative deficits but also severe neuropathic pain which is mostly resistant to classical analgesics. Better treatments can be expected from precise characterization of underlying physiopathological mechanisms. This led us to thor...
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| Veröffentlicht in: | PloS one 2014-07, Vol.9 (7), p.e102027 |
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| description | In humans, spinal cord lesions induce not only major motor and neurovegetative deficits but also severe neuropathic pain which is mostly resistant to classical analgesics. Better treatments can be expected from precise characterization of underlying physiopathological mechanisms. This led us to thoroughly investigate (i) mechanical and thermal sensory alterations, (ii) responses to acute treatments with drugs having patent or potential anti-allodynic properties and (iii) the spinal/ganglion expression of transcripts encoding markers of neuronal injury, microglia and astrocyte activation in rats that underwent complete spinal cord transection (SCT). SCT was performed at thoracic T8-T9 level under deep isoflurane anaesthesia, and SCT rats were examined for up to two months post surgery. SCT induced a marked hyper-reflexia at hindpaws and strong mechanical and cold allodynia in a limited (6 cm2) cutaneous territory just rostral to the lesion site. At this level, pressure threshold value to trigger nocifensive reactions to locally applied von Frey filaments was 100-fold lower in SCT- versus sham-operated rats. A marked up-regulation of mRNAs encoding ATF3 (neuronal injury) and glial activation markers (OX-42, GFAP, P2×4, P2×7, TLR4) was observed in spinal cord and/or dorsal root ganglia at T6-T11 levels from day 2 up to day 60 post surgery. Transcripts encoding the proinflammatory cytokines IL-1β, IL-6 and TNF-α were also markedly but differentially up-regulated at T6-T11 levels in SCT rats. Acute treatment with ketamine (50 mg/kg i.p.), morphine (3-10 mg/kg s.c.) and tapentadol (10-20 mg/kg i.p.) significantly increased pressure threshold to trigger nocifensive reaction in the von Frey filaments test, whereas amitriptyline, pregabalin, gabapentin and clonazepam were ineffective. Because all SCT rats developed long lasting, reproducible and stable allodynia, which could be alleviated by drugs effective in humans, thoracic cord transection might be a reliable model for testing innovative therapies aimed at reducing spinal cord lesion-induced central neuropathic pain. |
| doi_str_mv | 10.1371/journal.pone.0102027 |
| format | Article |
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Better treatments can be expected from precise characterization of underlying physiopathological mechanisms. This led us to thoroughly investigate (i) mechanical and thermal sensory alterations, (ii) responses to acute treatments with drugs having patent or potential anti-allodynic properties and (iii) the spinal/ganglion expression of transcripts encoding markers of neuronal injury, microglia and astrocyte activation in rats that underwent complete spinal cord transection (SCT). SCT was performed at thoracic T8-T9 level under deep isoflurane anaesthesia, and SCT rats were examined for up to two months post surgery. SCT induced a marked hyper-reflexia at hindpaws and strong mechanical and cold allodynia in a limited (6 cm2) cutaneous territory just rostral to the lesion site. At this level, pressure threshold value to trigger nocifensive reactions to locally applied von Frey filaments was 100-fold lower in SCT- versus sham-operated rats. A marked up-regulation of mRNAs encoding ATF3 (neuronal injury) and glial activation markers (OX-42, GFAP, P2×4, P2×7, TLR4) was observed in spinal cord and/or dorsal root ganglia at T6-T11 levels from day 2 up to day 60 post surgery. Transcripts encoding the proinflammatory cytokines IL-1β, IL-6 and TNF-α were also markedly but differentially up-regulated at T6-T11 levels in SCT rats. Acute treatment with ketamine (50 mg/kg i.p.), morphine (3-10 mg/kg s.c.) and tapentadol (10-20 mg/kg i.p.) significantly increased pressure threshold to trigger nocifensive reaction in the von Frey filaments test, whereas amitriptyline, pregabalin, gabapentin and clonazepam were ineffective. Because all SCT rats developed long lasting, reproducible and stable allodynia, which could be alleviated by drugs effective in humans, thoracic cord transection might be a reliable model for testing innovative therapies aimed at reducing spinal cord lesion-induced central neuropathic pain.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0102027</identifier><identifier>PMID: 25019623</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Activating transcription factor 3 ; Activating Transcription Factor 3 - metabolism ; Activation ; Amitriptyline ; Analgesics ; Analysis of Variance ; Anesthesia ; Animals ; Biology and Life Sciences ; Cell cycle ; Clonazepam ; Coding ; Cytokines ; Cytokines - metabolism ; Dorsal root ganglia ; Drugs ; Filaments ; Gabapentin ; Ganglia ; Ganglia, Spinal - metabolism ; Glial fibrillary acidic protein ; Hot Temperature - adverse effects ; Hyperalgesia - drug therapy ; Hyperalgesia - etiology ; Hyperalgesia - physiopathology ; Inflammation ; Interleukin 6 ; Intermediate filament proteins ; Isoflurane ; Ketamine ; Ketamine - therapeutic use ; Lesions ; Life Sciences ; Male ; Markers ; Medical innovations ; Medicine and Health Sciences ; Microglia ; Model testing ; Morphine ; Morphine - therapeutic use ; Nerve Tissue Proteins - metabolism ; Neuralgia ; Neuronal-glial interactions ; Neurons and Cognition ; Neuropathy ; Neurosciences ; Pain ; Pain Measurement ; Pain perception ; Pharmacology ; Phenols - therapeutic use ; Pressure ; Rats ; Rats, Sprague-Dawley ; Real-Time Polymerase Chain Reaction ; Research and Analysis Methods ; Reverse Transcriptase Polymerase Chain Reaction ; Rodents ; Spinal cord injuries ; Spinal Cord Injuries - complications ; Surgery ; Territory ; Thorax ; Toll-like receptors ; Transcription factors ; Tumor necrosis factor-TNF</subject><ispartof>PloS one, 2014-07, Vol.9 (7), p.e102027</ispartof><rights>COPYRIGHT 2014 Public Library of Science</rights><rights>2014 M'Dahoma et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License: http://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. 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Better treatments can be expected from precise characterization of underlying physiopathological mechanisms. This led us to thoroughly investigate (i) mechanical and thermal sensory alterations, (ii) responses to acute treatments with drugs having patent or potential anti-allodynic properties and (iii) the spinal/ganglion expression of transcripts encoding markers of neuronal injury, microglia and astrocyte activation in rats that underwent complete spinal cord transection (SCT). SCT was performed at thoracic T8-T9 level under deep isoflurane anaesthesia, and SCT rats were examined for up to two months post surgery. SCT induced a marked hyper-reflexia at hindpaws and strong mechanical and cold allodynia in a limited (6 cm2) cutaneous territory just rostral to the lesion site. At this level, pressure threshold value to trigger nocifensive reactions to locally applied von Frey filaments was 100-fold lower in SCT- versus sham-operated rats. A marked up-regulation of mRNAs encoding ATF3 (neuronal injury) and glial activation markers (OX-42, GFAP, P2×4, P2×7, TLR4) was observed in spinal cord and/or dorsal root ganglia at T6-T11 levels from day 2 up to day 60 post surgery. Transcripts encoding the proinflammatory cytokines IL-1β, IL-6 and TNF-α were also markedly but differentially up-regulated at T6-T11 levels in SCT rats. Acute treatment with ketamine (50 mg/kg i.p.), morphine (3-10 mg/kg s.c.) and tapentadol (10-20 mg/kg i.p.) significantly increased pressure threshold to trigger nocifensive reaction in the von Frey filaments test, whereas amitriptyline, pregabalin, gabapentin and clonazepam were ineffective. Because all SCT rats developed long lasting, reproducible and stable allodynia, which could be alleviated by drugs effective in humans, thoracic cord transection might be a reliable model for testing innovative therapies aimed at reducing spinal cord lesion-induced central neuropathic pain.</description><subject>Activating transcription factor 3</subject><subject>Activating Transcription Factor 3 - metabolism</subject><subject>Activation</subject><subject>Amitriptyline</subject><subject>Analgesics</subject><subject>Analysis of Variance</subject><subject>Anesthesia</subject><subject>Animals</subject><subject>Biology and Life Sciences</subject><subject>Cell cycle</subject><subject>Clonazepam</subject><subject>Coding</subject><subject>Cytokines</subject><subject>Cytokines - metabolism</subject><subject>Dorsal root ganglia</subject><subject>Drugs</subject><subject>Filaments</subject><subject>Gabapentin</subject><subject>Ganglia</subject><subject>Ganglia, Spinal - metabolism</subject><subject>Glial fibrillary acidic protein</subject><subject>Hot Temperature - adverse effects</subject><subject>Hyperalgesia - drug therapy</subject><subject>Hyperalgesia - etiology</subject><subject>Hyperalgesia - physiopathology</subject><subject>Inflammation</subject><subject>Interleukin 6</subject><subject>Intermediate filament proteins</subject><subject>Isoflurane</subject><subject>Ketamine</subject><subject>Ketamine - therapeutic use</subject><subject>Lesions</subject><subject>Life Sciences</subject><subject>Male</subject><subject>Markers</subject><subject>Medical innovations</subject><subject>Medicine and Health Sciences</subject><subject>Microglia</subject><subject>Model testing</subject><subject>Morphine</subject><subject>Morphine - therapeutic use</subject><subject>Nerve Tissue Proteins - metabolism</subject><subject>Neuralgia</subject><subject>Neuronal-glial interactions</subject><subject>Neurons and Cognition</subject><subject>Neuropathy</subject><subject>Neurosciences</subject><subject>Pain</subject><subject>Pain Measurement</subject><subject>Pain perception</subject><subject>Pharmacology</subject><subject>Phenols - 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therapeutic use</topic><topic>Nerve Tissue Proteins - metabolism</topic><topic>Neuralgia</topic><topic>Neuronal-glial interactions</topic><topic>Neurons and Cognition</topic><topic>Neuropathy</topic><topic>Neurosciences</topic><topic>Pain</topic><topic>Pain Measurement</topic><topic>Pain perception</topic><topic>Pharmacology</topic><topic>Phenols - therapeutic use</topic><topic>Pressure</topic><topic>Rats</topic><topic>Rats, Sprague-Dawley</topic><topic>Real-Time Polymerase Chain Reaction</topic><topic>Research and Analysis Methods</topic><topic>Reverse Transcriptase Polymerase Chain Reaction</topic><topic>Rodents</topic><topic>Spinal cord injuries</topic><topic>Spinal Cord Injuries - complications</topic><topic>Surgery</topic><topic>Territory</topic><topic>Thorax</topic><topic>Toll-like receptors</topic><topic>Transcription factors</topic><topic>Tumor necrosis factor-TNF</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>M'Dahoma, Saïd</creatorcontrib><creatorcontrib>Bourgoin, Sylvie</creatorcontrib><creatorcontrib>Kayser, Valérie</creatorcontrib><creatorcontrib>Barthélémy, Sandrine</creatorcontrib><creatorcontrib>Chevarin, Caroline</creatorcontrib><creatorcontrib>Chali, Farah</creatorcontrib><creatorcontrib>Orsal, Didier</creatorcontrib><creatorcontrib>Hamon, Michel</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Opposing Viewpoints</collection><collection>Gale In Context: Science</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Biotechnology Research Abstracts</collection><collection>Nursing & Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Immunology Abstracts</collection><collection>Meteorological & Geoastrophysical Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Meteorological & Geoastrophysical Abstracts - 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Better treatments can be expected from precise characterization of underlying physiopathological mechanisms. This led us to thoroughly investigate (i) mechanical and thermal sensory alterations, (ii) responses to acute treatments with drugs having patent or potential anti-allodynic properties and (iii) the spinal/ganglion expression of transcripts encoding markers of neuronal injury, microglia and astrocyte activation in rats that underwent complete spinal cord transection (SCT). SCT was performed at thoracic T8-T9 level under deep isoflurane anaesthesia, and SCT rats were examined for up to two months post surgery. SCT induced a marked hyper-reflexia at hindpaws and strong mechanical and cold allodynia in a limited (6 cm2) cutaneous territory just rostral to the lesion site. At this level, pressure threshold value to trigger nocifensive reactions to locally applied von Frey filaments was 100-fold lower in SCT- versus sham-operated rats. A marked up-regulation of mRNAs encoding ATF3 (neuronal injury) and glial activation markers (OX-42, GFAP, P2×4, P2×7, TLR4) was observed in spinal cord and/or dorsal root ganglia at T6-T11 levels from day 2 up to day 60 post surgery. Transcripts encoding the proinflammatory cytokines IL-1β, IL-6 and TNF-α were also markedly but differentially up-regulated at T6-T11 levels in SCT rats. Acute treatment with ketamine (50 mg/kg i.p.), morphine (3-10 mg/kg s.c.) and tapentadol (10-20 mg/kg i.p.) significantly increased pressure threshold to trigger nocifensive reaction in the von Frey filaments test, whereas amitriptyline, pregabalin, gabapentin and clonazepam were ineffective. Because all SCT rats developed long lasting, reproducible and stable allodynia, which could be alleviated by drugs effective in humans, thoracic cord transection might be a reliable model for testing innovative therapies aimed at reducing spinal cord lesion-induced central neuropathic pain.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25019623</pmid><doi>10.1371/journal.pone.0102027</doi><orcidid>https://orcid.org/0000-0001-7801-4398</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2014-07, Vol.9 (7), p.e102027 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1545002688 |
| source | MEDLINE; DOAJ Directory of Open Access Journals; EZB-FREE-00999 freely available EZB journals; PubMed Central; Free Full-Text Journals in Chemistry; Public Library of Science (PLoS) |
| subjects | Activating transcription factor 3 Activating Transcription Factor 3 - metabolism Activation Amitriptyline Analgesics Analysis of Variance Anesthesia Animals Biology and Life Sciences Cell cycle Clonazepam Coding Cytokines Cytokines - metabolism Dorsal root ganglia Drugs Filaments Gabapentin Ganglia Ganglia, Spinal - metabolism Glial fibrillary acidic protein Hot Temperature - adverse effects Hyperalgesia - drug therapy Hyperalgesia - etiology Hyperalgesia - physiopathology Inflammation Interleukin 6 Intermediate filament proteins Isoflurane Ketamine Ketamine - therapeutic use Lesions Life Sciences Male Markers Medical innovations Medicine and Health Sciences Microglia Model testing Morphine Morphine - therapeutic use Nerve Tissue Proteins - metabolism Neuralgia Neuronal-glial interactions Neurons and Cognition Neuropathy Neurosciences Pain Pain Measurement Pain perception Pharmacology Phenols - therapeutic use Pressure Rats Rats, Sprague-Dawley Real-Time Polymerase Chain Reaction Research and Analysis Methods Reverse Transcriptase Polymerase Chain Reaction Rodents Spinal cord injuries Spinal Cord Injuries - complications Surgery Territory Thorax Toll-like receptors Transcription factors Tumor necrosis factor-TNF |
| title | Spinal cord transection-induced allodynia in rats--behavioral, physiopathological and pharmacological characterization |
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