Ultra-low dose naloxone restores the antinociceptive effect of morphine in pertussis toxin-treated rats by reversing the coupling of μ-opioid receptors from Gs-protein to coupling to Gi-protein
Abstract Pertussis toxin (PTX) treatment results in ADP-ribosylation of Gi-protein and thus in disruption of μ-opioid receptor signal transduction and loss of the antinociceptive effect of morphine. We have previously demonstrated that pretreatment with ultra-low dose naloxone preserves the antinoci...
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| description | Abstract Pertussis toxin (PTX) treatment results in ADP-ribosylation of Gi-protein and thus in disruption of μ-opioid receptor signal transduction and loss of the antinociceptive effect of morphine. We have previously demonstrated that pretreatment with ultra-low dose naloxone preserves the antinociceptive effect of morphine in PTX-treated rats. The present study further examined the effect of ultra-low dose naloxone on μ-opioid receptor signaling in PTX-treated rats and the underlying mechanism. Male Wistar rats implanted with an intrathecal catheter received an intrathecal injection of saline or PTX (1 μg in 5 μl of saline), then, 4 days later, were pretreated by intrathecal injection with either saline or ultra-low dose naloxone (15 ng in 5 μl of saline), followed, 30 min later, by saline or morphine (10 μg in 5 μl of saline). Four days after PTX injection, thermal hyperalgesia was observed, together with increased coupling of excitatory Gs-protein to μ-opioid receptors in the spinal cord. Ultra-low dose naloxone pretreatment preserved the antinociceptive effect of morphine, and this effect was completely blocked by the μ-opioid receptor antagonist CTOP, but not by the κ-opioid receptor antagonist nor-BNI or the δ-opioid receptor antagonist naltrindole. Moreover, a co-immunoprecipitation study showed that ultra-low dose naloxone restored μ-opioid receptor/Gi-protein coupling and inhibited the PTX-induced μ-opioid receptor/Gs-protein coupling. In addition to the anti-neuroinflammatory effect and glutamate transporter modulation previously observed in PTX-treated rats, the re-establishment of μ-opioid receptor Gi/Go-protein coupling is involved in the restoration of the antinociceptive effect of morphine by ultra-low dose naloxone pretreatment by normalizing the balance between the excitatory and inhibitory signaling pathways. These results show that ultra-low dose naloxone preserves the antinociceptive effect of morphine, suppresses spinal neuroinflammation, and reduces PTX-elevated excitatory Gs-coupled opioid receptors in PTX-treated rats. We suggest that ultra-low dose naloxone might be clinically valuable in pain management. |
| doi_str_mv | 10.1016/j.neuroscience.2009.08.015 |
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We have previously demonstrated that pretreatment with ultra-low dose naloxone preserves the antinociceptive effect of morphine in PTX-treated rats. The present study further examined the effect of ultra-low dose naloxone on μ-opioid receptor signaling in PTX-treated rats and the underlying mechanism. Male Wistar rats implanted with an intrathecal catheter received an intrathecal injection of saline or PTX (1 μg in 5 μl of saline), then, 4 days later, were pretreated by intrathecal injection with either saline or ultra-low dose naloxone (15 ng in 5 μl of saline), followed, 30 min later, by saline or morphine (10 μg in 5 μl of saline). Four days after PTX injection, thermal hyperalgesia was observed, together with increased coupling of excitatory Gs-protein to μ-opioid receptors in the spinal cord. Ultra-low dose naloxone pretreatment preserved the antinociceptive effect of morphine, and this effect was completely blocked by the μ-opioid receptor antagonist CTOP, but not by the κ-opioid receptor antagonist nor-BNI or the δ-opioid receptor antagonist naltrindole. Moreover, a co-immunoprecipitation study showed that ultra-low dose naloxone restored μ-opioid receptor/Gi-protein coupling and inhibited the PTX-induced μ-opioid receptor/Gs-protein coupling. In addition to the anti-neuroinflammatory effect and glutamate transporter modulation previously observed in PTX-treated rats, the re-establishment of μ-opioid receptor Gi/Go-protein coupling is involved in the restoration of the antinociceptive effect of morphine by ultra-low dose naloxone pretreatment by normalizing the balance between the excitatory and inhibitory signaling pathways. These results show that ultra-low dose naloxone preserves the antinociceptive effect of morphine, suppresses spinal neuroinflammation, and reduces PTX-elevated excitatory Gs-coupled opioid receptors in PTX-treated rats. We suggest that ultra-low dose naloxone might be clinically valuable in pain management.</description><identifier>ISSN: 0306-4522</identifier><identifier>EISSN: 1873-7544</identifier><identifier>DOI: 10.1016/j.neuroscience.2009.08.015</identifier><identifier>PMID: 19682558</identifier><identifier>CODEN: NRSCDN</identifier><language>eng</language><publisher>Amsterdam: Elsevier Ltd</publisher><subject>ADP-ribosylate ; Analgesics ; Analgesics, Opioid - administration & dosage ; Analgesics, Opioid - pharmacology ; Animals ; Biological and medical sciences ; Drug Therapy, Combination ; Fundamental and applied biological sciences. Psychology ; G-protein ; GTP-Binding Protein alpha Subunits, Gi-Go - metabolism ; GTP-Binding Protein alpha Subunits, Gs - metabolism ; immunoprecipitation ; intrathecal injection ; Male ; Medical sciences ; Morphine - administration & dosage ; Morphine - pharmacology ; Naloxone - administration & dosage ; Naloxone - pharmacology ; Narcotic Antagonists - administration & dosage ; Narcotic Antagonists - pharmacology ; Neurology ; neuropathic pain ; Neuropharmacology ; opioid ; Pain - chemically induced ; Pain - drug therapy ; Pain - metabolism ; Pertussis Toxin ; Pharmacology. Drug treatments ; Rats ; Rats, Wistar ; Receptors, Opioid, mu - antagonists & inhibitors ; Receptors, Opioid, mu - metabolism ; Spinal Cord - drug effects ; Spinal Cord - metabolism ; Vertebrates: nervous system and sense organs</subject><ispartof>Neuroscience, 2009-12, Vol.164 (2), p.435-443</ispartof><rights>IBRO</rights><rights>2009 IBRO</rights><rights>2015 INIST-CNRS</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c464t-e1f80beb2ac9ff57e55e404f5840c7d32053e912cbc9d9909c52c8116e7e9c183</citedby><cites>FETCH-LOGICAL-c464t-e1f80beb2ac9ff57e55e404f5840c7d32053e912cbc9d9909c52c8116e7e9c183</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.neuroscience.2009.08.015$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,776,780,3536,27903,27904,45974</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=22149131$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/19682558$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Tsai, R.-Y</creatorcontrib><creatorcontrib>Tai, Y.-H</creatorcontrib><creatorcontrib>Tzeng, J.-I</creatorcontrib><creatorcontrib>Cherng, C.-H</creatorcontrib><creatorcontrib>Yeh, C.-C</creatorcontrib><creatorcontrib>Wong, C.-S</creatorcontrib><title>Ultra-low dose naloxone restores the antinociceptive effect of morphine in pertussis toxin-treated rats by reversing the coupling of μ-opioid receptors from Gs-protein to coupling to Gi-protein</title><title>Neuroscience</title><addtitle>Neuroscience</addtitle><description>Abstract Pertussis toxin (PTX) treatment results in ADP-ribosylation of Gi-protein and thus in disruption of μ-opioid receptor signal transduction and loss of the antinociceptive effect of morphine. We have previously demonstrated that pretreatment with ultra-low dose naloxone preserves the antinociceptive effect of morphine in PTX-treated rats. The present study further examined the effect of ultra-low dose naloxone on μ-opioid receptor signaling in PTX-treated rats and the underlying mechanism. Male Wistar rats implanted with an intrathecal catheter received an intrathecal injection of saline or PTX (1 μg in 5 μl of saline), then, 4 days later, were pretreated by intrathecal injection with either saline or ultra-low dose naloxone (15 ng in 5 μl of saline), followed, 30 min later, by saline or morphine (10 μg in 5 μl of saline). Four days after PTX injection, thermal hyperalgesia was observed, together with increased coupling of excitatory Gs-protein to μ-opioid receptors in the spinal cord. Ultra-low dose naloxone pretreatment preserved the antinociceptive effect of morphine, and this effect was completely blocked by the μ-opioid receptor antagonist CTOP, but not by the κ-opioid receptor antagonist nor-BNI or the δ-opioid receptor antagonist naltrindole. Moreover, a co-immunoprecipitation study showed that ultra-low dose naloxone restored μ-opioid receptor/Gi-protein coupling and inhibited the PTX-induced μ-opioid receptor/Gs-protein coupling. In addition to the anti-neuroinflammatory effect and glutamate transporter modulation previously observed in PTX-treated rats, the re-establishment of μ-opioid receptor Gi/Go-protein coupling is involved in the restoration of the antinociceptive effect of morphine by ultra-low dose naloxone pretreatment by normalizing the balance between the excitatory and inhibitory signaling pathways. These results show that ultra-low dose naloxone preserves the antinociceptive effect of morphine, suppresses spinal neuroinflammation, and reduces PTX-elevated excitatory Gs-coupled opioid receptors in PTX-treated rats. We suggest that ultra-low dose naloxone might be clinically valuable in pain management.</description><subject>ADP-ribosylate</subject><subject>Analgesics</subject><subject>Analgesics, Opioid - administration & dosage</subject><subject>Analgesics, Opioid - pharmacology</subject><subject>Animals</subject><subject>Biological and medical sciences</subject><subject>Drug Therapy, Combination</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>G-protein</subject><subject>GTP-Binding Protein alpha Subunits, Gi-Go - metabolism</subject><subject>GTP-Binding Protein alpha Subunits, Gs - metabolism</subject><subject>immunoprecipitation</subject><subject>intrathecal injection</subject><subject>Male</subject><subject>Medical sciences</subject><subject>Morphine - administration & dosage</subject><subject>Morphine - pharmacology</subject><subject>Naloxone - administration & dosage</subject><subject>Naloxone - pharmacology</subject><subject>Narcotic Antagonists - administration & dosage</subject><subject>Narcotic Antagonists - pharmacology</subject><subject>Neurology</subject><subject>neuropathic pain</subject><subject>Neuropharmacology</subject><subject>opioid</subject><subject>Pain - chemically induced</subject><subject>Pain - drug therapy</subject><subject>Pain - metabolism</subject><subject>Pertussis Toxin</subject><subject>Pharmacology. Drug treatments</subject><subject>Rats</subject><subject>Rats, Wistar</subject><subject>Receptors, Opioid, mu - antagonists & inhibitors</subject><subject>Receptors, Opioid, mu - metabolism</subject><subject>Spinal Cord - drug effects</subject><subject>Spinal Cord - metabolism</subject><subject>Vertebrates: nervous system and sense organs</subject><issn>0306-4522</issn><issn>1873-7544</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2009</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNktGO1CAUhhujcWdXX8EQE-NVR6DQghcmm3UdTTbxQveaMPTgMnagAh133s0rH8Bnkjqja7yyFxTCd_6fnP9U1VOClwST9sVm6WGKIRkH3sCSYiyXWCwx4feqBRFdU3ecsfvVAje4rRmn9KQ6TWmDy8dZ87A6IbIVlHOxqL5fDznqeghfUR8SIK-HcBs8oAgph7KgfANI--x8MM7AmN0OEFgLJqNg0TbE8cYV3nk0QsxTSq7UhFvn6xxBZ-hR1Dmh9b5I7iAm5z_90jRhGof5UFR-fKvD6IIrLMweISZkY9iiVarHGDIU9RzuSsp-5X7fPKoeWD0keHz8n1XXby4_Xrytr96v3l2cX9WGtSzXQKzAa1hTbaS1vAPOgWFmuWDYdH1DMW9AEmrWRvZSYmk4NYKQFjqQhojmrHp-0C2-X6bSHrV1ycAwaA9hSqprGBZMiKaQLw-kKSmlCFaN0W113CuC1Ryh2qi_I1RzhAoLVSIsxU-ONtN6C_1d6TGzAjw7AjoZPdiovXHpD0cpYZI0pHCvDxyUpuwcRHW0613pclZ9cP_3nlf_yJiSgSvOn2EPaROmWIYmKaISVVh9mIdunjksMaFStM1PFHbcnw</recordid><startdate>20091201</startdate><enddate>20091201</enddate><creator>Tsai, R.-Y</creator><creator>Tai, Y.-H</creator><creator>Tzeng, J.-I</creator><creator>Cherng, C.-H</creator><creator>Yeh, C.-C</creator><creator>Wong, C.-S</creator><general>Elsevier Ltd</general><general>Elsevier</general><scope>IQODW</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope></search><sort><creationdate>20091201</creationdate><title>Ultra-low dose naloxone restores the antinociceptive effect of morphine in pertussis toxin-treated rats by reversing the coupling of μ-opioid receptors from Gs-protein to coupling to Gi-protein</title><author>Tsai, R.-Y ; Tai, Y.-H ; Tzeng, J.-I ; Cherng, C.-H ; Yeh, C.-C ; Wong, C.-S</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c464t-e1f80beb2ac9ff57e55e404f5840c7d32053e912cbc9d9909c52c8116e7e9c183</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2009</creationdate><topic>ADP-ribosylate</topic><topic>Analgesics</topic><topic>Analgesics, Opioid - administration & dosage</topic><topic>Analgesics, Opioid - pharmacology</topic><topic>Animals</topic><topic>Biological and medical sciences</topic><topic>Drug Therapy, Combination</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>G-protein</topic><topic>GTP-Binding Protein alpha Subunits, Gi-Go - metabolism</topic><topic>GTP-Binding Protein alpha Subunits, Gs - metabolism</topic><topic>immunoprecipitation</topic><topic>intrathecal injection</topic><topic>Male</topic><topic>Medical sciences</topic><topic>Morphine - administration & dosage</topic><topic>Morphine - pharmacology</topic><topic>Naloxone - administration & dosage</topic><topic>Naloxone - pharmacology</topic><topic>Narcotic Antagonists - administration & dosage</topic><topic>Narcotic Antagonists - pharmacology</topic><topic>Neurology</topic><topic>neuropathic pain</topic><topic>Neuropharmacology</topic><topic>opioid</topic><topic>Pain - chemically induced</topic><topic>Pain - drug therapy</topic><topic>Pain - metabolism</topic><topic>Pertussis Toxin</topic><topic>Pharmacology. Drug treatments</topic><topic>Rats</topic><topic>Rats, Wistar</topic><topic>Receptors, Opioid, mu - antagonists & inhibitors</topic><topic>Receptors, Opioid, mu - metabolism</topic><topic>Spinal Cord - drug effects</topic><topic>Spinal Cord - metabolism</topic><topic>Vertebrates: nervous system and sense organs</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Tsai, R.-Y</creatorcontrib><creatorcontrib>Tai, Y.-H</creatorcontrib><creatorcontrib>Tzeng, J.-I</creatorcontrib><creatorcontrib>Cherng, C.-H</creatorcontrib><creatorcontrib>Yeh, C.-C</creatorcontrib><creatorcontrib>Wong, C.-S</creatorcontrib><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Tsai, R.-Y</au><au>Tai, Y.-H</au><au>Tzeng, J.-I</au><au>Cherng, C.-H</au><au>Yeh, C.-C</au><au>Wong, C.-S</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Ultra-low dose naloxone restores the antinociceptive effect of morphine in pertussis toxin-treated rats by reversing the coupling of μ-opioid receptors from Gs-protein to coupling to Gi-protein</atitle><jtitle>Neuroscience</jtitle><addtitle>Neuroscience</addtitle><date>2009-12-01</date><risdate>2009</risdate><volume>164</volume><issue>2</issue><spage>435</spage><epage>443</epage><pages>435-443</pages><issn>0306-4522</issn><eissn>1873-7544</eissn><coden>NRSCDN</coden><abstract>Abstract Pertussis toxin (PTX) treatment results in ADP-ribosylation of Gi-protein and thus in disruption of μ-opioid receptor signal transduction and loss of the antinociceptive effect of morphine. We have previously demonstrated that pretreatment with ultra-low dose naloxone preserves the antinociceptive effect of morphine in PTX-treated rats. The present study further examined the effect of ultra-low dose naloxone on μ-opioid receptor signaling in PTX-treated rats and the underlying mechanism. Male Wistar rats implanted with an intrathecal catheter received an intrathecal injection of saline or PTX (1 μg in 5 μl of saline), then, 4 days later, were pretreated by intrathecal injection with either saline or ultra-low dose naloxone (15 ng in 5 μl of saline), followed, 30 min later, by saline or morphine (10 μg in 5 μl of saline). Four days after PTX injection, thermal hyperalgesia was observed, together with increased coupling of excitatory Gs-protein to μ-opioid receptors in the spinal cord. Ultra-low dose naloxone pretreatment preserved the antinociceptive effect of morphine, and this effect was completely blocked by the μ-opioid receptor antagonist CTOP, but not by the κ-opioid receptor antagonist nor-BNI or the δ-opioid receptor antagonist naltrindole. Moreover, a co-immunoprecipitation study showed that ultra-low dose naloxone restored μ-opioid receptor/Gi-protein coupling and inhibited the PTX-induced μ-opioid receptor/Gs-protein coupling. In addition to the anti-neuroinflammatory effect and glutamate transporter modulation previously observed in PTX-treated rats, the re-establishment of μ-opioid receptor Gi/Go-protein coupling is involved in the restoration of the antinociceptive effect of morphine by ultra-low dose naloxone pretreatment by normalizing the balance between the excitatory and inhibitory signaling pathways. These results show that ultra-low dose naloxone preserves the antinociceptive effect of morphine, suppresses spinal neuroinflammation, and reduces PTX-elevated excitatory Gs-coupled opioid receptors in PTX-treated rats. We suggest that ultra-low dose naloxone might be clinically valuable in pain management.</abstract><cop>Amsterdam</cop><pub>Elsevier Ltd</pub><pmid>19682558</pmid><doi>10.1016/j.neuroscience.2009.08.015</doi><tpages>9</tpages></addata></record> |
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| ispartof | Neuroscience, 2009-12, Vol.164 (2), p.435-443 |
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| subjects | ADP-ribosylate Analgesics Analgesics, Opioid - administration & dosage Analgesics, Opioid - pharmacology Animals Biological and medical sciences Drug Therapy, Combination Fundamental and applied biological sciences. Psychology G-protein GTP-Binding Protein alpha Subunits, Gi-Go - metabolism GTP-Binding Protein alpha Subunits, Gs - metabolism immunoprecipitation intrathecal injection Male Medical sciences Morphine - administration & dosage Morphine - pharmacology Naloxone - administration & dosage Naloxone - pharmacology Narcotic Antagonists - administration & dosage Narcotic Antagonists - pharmacology Neurology neuropathic pain Neuropharmacology opioid Pain - chemically induced Pain - drug therapy Pain - metabolism Pertussis Toxin Pharmacology. Drug treatments Rats Rats, Wistar Receptors, Opioid, mu - antagonists & inhibitors Receptors, Opioid, mu - metabolism Spinal Cord - drug effects Spinal Cord - metabolism Vertebrates: nervous system and sense organs |
| title | Ultra-low dose naloxone restores the antinociceptive effect of morphine in pertussis toxin-treated rats by reversing the coupling of μ-opioid receptors from Gs-protein to coupling to Gi-protein |
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