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Role of oxidative stress in oxaliplatin‐induced enteric neuropathy and colonic dysmotility in mice

Background and Purpose Oxaliplatin is a platinum‐based chemotherapeutic drug used as a first‐line therapy for colorectal cancer. However, its use is associated with severe gastrointestinal side‐effects resulting in dose limitations and/or cessation of treatment. In this study, we tested whether oxid...

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Published in:British journal of pharmacology 2016-12, Vol.173 (24), p.3502-3521
Main Authors: McQuade, Rachel M, Carbone, Simona E, Stojanovska, Vanesa, Rahman, Ahmed, Gwynne, Rachel M, Robinson, Ainsley M, Goodman, Craig A, Bornstein, Joel C, Nurgali, Kulmira
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container_issue 24
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container_title British journal of pharmacology
container_volume 173
creator McQuade, Rachel M
Carbone, Simona E
Stojanovska, Vanesa
Rahman, Ahmed
Gwynne, Rachel M
Robinson, Ainsley M
Goodman, Craig A
Bornstein, Joel C
Nurgali, Kulmira
description Background and Purpose Oxaliplatin is a platinum‐based chemotherapeutic drug used as a first‐line therapy for colorectal cancer. However, its use is associated with severe gastrointestinal side‐effects resulting in dose limitations and/or cessation of treatment. In this study, we tested whether oxidative stress, caused by chronic oxaliplatin treatment, induces enteric neuronal damage and colonic dysmotility. Experimental Approach Oxaliplatin (3 mg·kg−1 per day) was administered in vivo to Balb/c mice intraperitoneally three times a week. The distal colon was collected at day 14 of treatment. Immunohistochemistry was performed in wholemount preparations of submucosal and myenteric ganglia. Neuromuscular transmission was studied by intracellular electrophysiology. Circular muscle tone was studied by force transducers. Colon propulsive activity studied in organ bath experiments and faeces were collected to measure water content. Key Results Chronic in vivo oxaliplatin treatment resulted in increased formation of reactive oxygen species (O2ˉ), nitration of proteins, mitochondrial membrane depolarisation resulting in the release of cytochrome c, loss of neurons, increased inducible NOS expression and apoptosis in both the submucosal and myenteric plexuses of the colon. Oxaliplatin treatment enhanced NO‐mediated inhibitory junction potentials and altered the response of circular muscles to the NO donor, sodium nitroprusside. It also reduced the frequency of colonic migrating motor complexes and decreased circular muscle tone, effects reversed by the NO synthase inhibitor, Nω‐Nitro‐L‐arginine. Conclusion and Implications Our study is the first to provide evidence that oxidative stress is a key player in enteric neuropathy and colonic dysmotility leading to symptoms of chronic constipation observed in oxaliplatin‐treated mice.
doi_str_mv 10.1111/bph.13646
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However, its use is associated with severe gastrointestinal side‐effects resulting in dose limitations and/or cessation of treatment. In this study, we tested whether oxidative stress, caused by chronic oxaliplatin treatment, induces enteric neuronal damage and colonic dysmotility. Experimental Approach Oxaliplatin (3 mg·kg−1 per day) was administered in vivo to Balb/c mice intraperitoneally three times a week. The distal colon was collected at day 14 of treatment. Immunohistochemistry was performed in wholemount preparations of submucosal and myenteric ganglia. Neuromuscular transmission was studied by intracellular electrophysiology. Circular muscle tone was studied by force transducers. Colon propulsive activity studied in organ bath experiments and faeces were collected to measure water content. Key Results Chronic in vivo oxaliplatin treatment resulted in increased formation of reactive oxygen species (O2ˉ), nitration of proteins, mitochondrial membrane depolarisation resulting in the release of cytochrome c, loss of neurons, increased inducible NOS expression and apoptosis in both the submucosal and myenteric plexuses of the colon. Oxaliplatin treatment enhanced NO‐mediated inhibitory junction potentials and altered the response of circular muscles to the NO donor, sodium nitroprusside. It also reduced the frequency of colonic migrating motor complexes and decreased circular muscle tone, effects reversed by the NO synthase inhibitor, Nω‐Nitro‐L‐arginine. Conclusion and Implications Our study is the first to provide evidence that oxidative stress is a key player in enteric neuropathy and colonic dysmotility leading to symptoms of chronic constipation observed in oxaliplatin‐treated mice.</description><identifier>ISSN: 0007-1188</identifier><identifier>EISSN: 1476-5381</identifier><identifier>DOI: 10.1111/bph.13646</identifier><identifier>PMID: 27714760</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Animals ; Antineoplastic Agents - administration &amp; dosage ; Antineoplastic Agents - pharmacology ; Apoptosis ; Arginine ; Colon ; Colon - drug effects ; Colon - metabolism ; Colon - pathology ; Colorectal carcinoma ; Constipation ; Cytochrome c ; Electrophysiology ; Enteric nervous system ; Ganglia ; Immunohistochemistry ; Intestinal Pseudo-Obstruction - chemically induced ; Intestinal Pseudo-Obstruction - pathology ; Male ; Membrane Potential, Mitochondrial - drug effects ; Mice ; Mice, Inbred BALB C ; Mitochondria ; Mitochondria - drug effects ; Mitochondria - metabolism ; Muscles ; Myenteric plexus ; Neuromuscular junctions ; Neuromuscular transmission ; Neuropathy ; Nitration ; Nitric-oxide synthase ; Organoplatinum Compounds - administration &amp; dosage ; Organoplatinum Compounds - pharmacology ; Oxaliplatin ; Oxidative stress ; Oxidative Stress - drug effects ; Platinum ; Proteins ; Reactive oxygen species ; Research Paper ; Research Papers ; Rodents ; Sodium ; Sodium nitroprusside ; Superoxides - metabolism ; Transducers ; Water content</subject><ispartof>British journal of pharmacology, 2016-12, Vol.173 (24), p.3502-3521</ispartof><rights>2016 The Authors. 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However, its use is associated with severe gastrointestinal side‐effects resulting in dose limitations and/or cessation of treatment. In this study, we tested whether oxidative stress, caused by chronic oxaliplatin treatment, induces enteric neuronal damage and colonic dysmotility. Experimental Approach Oxaliplatin (3 mg·kg−1 per day) was administered in vivo to Balb/c mice intraperitoneally three times a week. The distal colon was collected at day 14 of treatment. Immunohistochemistry was performed in wholemount preparations of submucosal and myenteric ganglia. Neuromuscular transmission was studied by intracellular electrophysiology. Circular muscle tone was studied by force transducers. Colon propulsive activity studied in organ bath experiments and faeces were collected to measure water content. Key Results Chronic in vivo oxaliplatin treatment resulted in increased formation of reactive oxygen species (O2ˉ), nitration of proteins, mitochondrial membrane depolarisation resulting in the release of cytochrome c, loss of neurons, increased inducible NOS expression and apoptosis in both the submucosal and myenteric plexuses of the colon. Oxaliplatin treatment enhanced NO‐mediated inhibitory junction potentials and altered the response of circular muscles to the NO donor, sodium nitroprusside. It also reduced the frequency of colonic migrating motor complexes and decreased circular muscle tone, effects reversed by the NO synthase inhibitor, Nω‐Nitro‐L‐arginine. 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However, its use is associated with severe gastrointestinal side‐effects resulting in dose limitations and/or cessation of treatment. In this study, we tested whether oxidative stress, caused by chronic oxaliplatin treatment, induces enteric neuronal damage and colonic dysmotility. Experimental Approach Oxaliplatin (3 mg·kg−1 per day) was administered in vivo to Balb/c mice intraperitoneally three times a week. The distal colon was collected at day 14 of treatment. Immunohistochemistry was performed in wholemount preparations of submucosal and myenteric ganglia. Neuromuscular transmission was studied by intracellular electrophysiology. Circular muscle tone was studied by force transducers. Colon propulsive activity studied in organ bath experiments and faeces were collected to measure water content. Key Results Chronic in vivo oxaliplatin treatment resulted in increased formation of reactive oxygen species (O2ˉ), nitration of proteins, mitochondrial membrane depolarisation resulting in the release of cytochrome c, loss of neurons, increased inducible NOS expression and apoptosis in both the submucosal and myenteric plexuses of the colon. Oxaliplatin treatment enhanced NO‐mediated inhibitory junction potentials and altered the response of circular muscles to the NO donor, sodium nitroprusside. It also reduced the frequency of colonic migrating motor complexes and decreased circular muscle tone, effects reversed by the NO synthase inhibitor, Nω‐Nitro‐L‐arginine. Conclusion and Implications Our study is the first to provide evidence that oxidative stress is a key player in enteric neuropathy and colonic dysmotility leading to symptoms of chronic constipation observed in oxaliplatin‐treated mice.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>27714760</pmid><doi>10.1111/bph.13646</doi><tpages>20</tpages><oa>free_for_read</oa></addata></record>
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source Wiley; PubMed Central
subjects Animals
Antineoplastic Agents - administration & dosage
Antineoplastic Agents - pharmacology
Apoptosis
Arginine
Colon
Colon - drug effects
Colon - metabolism
Colon - pathology
Colorectal carcinoma
Constipation
Cytochrome c
Electrophysiology
Enteric nervous system
Ganglia
Immunohistochemistry
Intestinal Pseudo-Obstruction - chemically induced
Intestinal Pseudo-Obstruction - pathology
Male
Membrane Potential, Mitochondrial - drug effects
Mice
Mice, Inbred BALB C
Mitochondria
Mitochondria - drug effects
Mitochondria - metabolism
Muscles
Myenteric plexus
Neuromuscular junctions
Neuromuscular transmission
Neuropathy
Nitration
Nitric-oxide synthase
Organoplatinum Compounds - administration & dosage
Organoplatinum Compounds - pharmacology
Oxaliplatin
Oxidative stress
Oxidative Stress - drug effects
Platinum
Proteins
Reactive oxygen species
Research Paper
Research Papers
Rodents
Sodium
Sodium nitroprusside
Superoxides - metabolism
Transducers
Water content
title Role of oxidative stress in oxaliplatin‐induced enteric neuropathy and colonic dysmotility in mice
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