Cross-talk between Human Spinal Cord μ-opioid Receptor 1Y Isoform and Gastrin-releasing Peptide Receptor Mediates Opioid-induced Scratching Behavior
WHAT WE ALREADY KNOW ABOUT THIS TOPICThe spinal administration of opioids can cause intense pruritisInteractions between specific μ-opioid receptor isoforms and the gastrin releasing peptide receptor in spinal tissues likely mediate morphine-induced pruritus WHAT THIS ARTICLE TELLS US THAT IS NEWHum...
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| Veröffentlicht in: | Anesthesiology (Philadelphia) 2019-08, Vol.131 (2), p.381-391 |
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| creator | Liu, Xian-Yu Ginosar, Yehuda Yazdi, Joseph Hincker, Alexander Chen, Zhou-Feng |
| description | WHAT WE ALREADY KNOW ABOUT THIS TOPICThe spinal administration of opioids can cause intense pruritisInteractions between specific μ-opioid receptor isoforms and the gastrin releasing peptide receptor in spinal tissues likely mediate morphine-induced pruritus
WHAT THIS ARTICLE TELLS US THAT IS NEWHuman spinal cord tissue expresses the 1Y isoform of the μ-opioid receptor, and that isoform functionally interacts with the gastrin releasing peptide receptor to cause cellular calcium influxBlocking interactions between the 1Y isoform and the gastrin releasing peptide receptor does not reduce opioid analgesiaEliminating interactions between the 1Y isoform and the gastrin releasing peptide receptor or reducing 1Y isoform activation may reduce opioid-induced pruritis
BACKGROUND:Although spinal opioids are safe and effective, pruritus is common and distressing. The authors previously demonstrated in mouse spinal cord that interactions between μ-opioid receptor isoform 1D and gastrin releasing peptide receptor mediate morphine-induced scratch. The C-terminal of 1D inhibits morphine-induced scratch without affecting analgesia. The authors hypothesize that human spinal cord also contains itch-specific μ-opioid receptor isoforms which interact with gastrin releasing peptide receptor.
METHODS:Reverse transcription polymerase chain reaction was performed on human spinal cord complimentary DNA from two human cadavers. Calcium responses to morphine (1 μM) were examined using calcium imaging microscopy on human cells (HEK293) coexpressing gastrin releasing peptide receptor and different human μ-opioid receptor isoforms. The authors assessed morphine-induced scratching behavior and thermal analgesia in mice following intrathecal injection of morphine (0.3 nmol) and a transactivator of transcription peptide designed from C-terminal sequences of 1Y isoform (0, 0.1, and 0.4 nmol).
RESULTS:The authors demonstrated 1Y expression in the spinal cord dorsal horn. Morphine administration evoked a calcium response (mean ± SD) (57 ± 13 nM) in cells coexpressing both gastrin releasing peptide receptor and the 1Y isomer. This was blocked by 10 μM naltrexone (0.7 ± 0.4 nM; P < 0.0001), 1 μM gastrin-releasing peptide receptor antagonist (3 ± 2 nM; P < 0.0001), or 200 μM 1Y-peptide (2 + 2 nM; P < 0.0001). In mice, 0.4 nmol 1Y-peptide significantly attenuated morphine-induced scratching behaviors (scratching bouts, vehicle vs. 1Y-peptide) (92 ± 31 vs. 38 ± 29; P = 0.011; n = 6 to 7 mice per g |
| doi_str_mv | 10.1097/ALN.0000000000002776 |
| format | Article |
| fullrecord | <record><control><sourceid>pubmed_cross</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_7098053</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>31314749</sourcerecordid><originalsourceid>FETCH-LOGICAL-c5086-46fc8987e6a240b37ef08dd23430fc84f863b5f95671919b038dad39799bc4f23</originalsourceid><addsrcrecordid>eNp9kdFuFCEUhomxsWv1DYzhBagwzAxwY1I32jZZrbF64RVh4EwHOwsTYLvxQXwbn8Fncta1tXohNwTO_30k_Ag9Y_SYUSVenKzeHdN7qxKifYAWrKkkYUw0D9FivuWE06o6RI9z_jIfRcPlI3TIGWe1qNUCfVummDMpZrzGHZQtQMBnm7UJ-HLywYx4GZPDP76TOPnoHf4AFqYSE2af8XmOfUxrbILDpyaX5ANJMILJPlzh93POO_hDvAXnTYGML36piA9uY8HhS5tMscOOeQWDufExPUEHvRkzPP29H6FPb15_XJ6R1cXp-fJkRWxDZUvqtrdSSQGtqWracQE9lc5VvOZ0ntS9bHnX9KppBVNMdZRLZxxXQqnO1n3Fj9DLvXfadGtwFkJJZtRT8muTvupovP57Evygr-KNFlRJ2vBZUO8FdveNCfo7llG9q0nPNel_a5qx5_ffvYNue5kDch_YxrFAytfjZgtJD2DGMvzf_RPyw6Ky</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype></control><display><type>article</type><title>Cross-talk between Human Spinal Cord μ-opioid Receptor 1Y Isoform and Gastrin-releasing Peptide Receptor Mediates Opioid-induced Scratching Behavior</title><source>MEDLINE</source><source>Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals</source><source>Journals@Ovid Complete</source><creator>Liu, Xian-Yu ; Ginosar, Yehuda ; Yazdi, Joseph ; Hincker, Alexander ; Chen, Zhou-Feng</creator><creatorcontrib>Liu, Xian-Yu ; Ginosar, Yehuda ; Yazdi, Joseph ; Hincker, Alexander ; Chen, Zhou-Feng</creatorcontrib><description>WHAT WE ALREADY KNOW ABOUT THIS TOPICThe spinal administration of opioids can cause intense pruritisInteractions between specific μ-opioid receptor isoforms and the gastrin releasing peptide receptor in spinal tissues likely mediate morphine-induced pruritus
WHAT THIS ARTICLE TELLS US THAT IS NEWHuman spinal cord tissue expresses the 1Y isoform of the μ-opioid receptor, and that isoform functionally interacts with the gastrin releasing peptide receptor to cause cellular calcium influxBlocking interactions between the 1Y isoform and the gastrin releasing peptide receptor does not reduce opioid analgesiaEliminating interactions between the 1Y isoform and the gastrin releasing peptide receptor or reducing 1Y isoform activation may reduce opioid-induced pruritis
BACKGROUND:Although spinal opioids are safe and effective, pruritus is common and distressing. The authors previously demonstrated in mouse spinal cord that interactions between μ-opioid receptor isoform 1D and gastrin releasing peptide receptor mediate morphine-induced scratch. The C-terminal of 1D inhibits morphine-induced scratch without affecting analgesia. The authors hypothesize that human spinal cord also contains itch-specific μ-opioid receptor isoforms which interact with gastrin releasing peptide receptor.
METHODS:Reverse transcription polymerase chain reaction was performed on human spinal cord complimentary DNA from two human cadavers. Calcium responses to morphine (1 μM) were examined using calcium imaging microscopy on human cells (HEK293) coexpressing gastrin releasing peptide receptor and different human μ-opioid receptor isoforms. The authors assessed morphine-induced scratching behavior and thermal analgesia in mice following intrathecal injection of morphine (0.3 nmol) and a transactivator of transcription peptide designed from C-terminal sequences of 1Y isoform (0, 0.1, and 0.4 nmol).
RESULTS:The authors demonstrated 1Y expression in the spinal cord dorsal horn. Morphine administration evoked a calcium response (mean ± SD) (57 ± 13 nM) in cells coexpressing both gastrin releasing peptide receptor and the 1Y isomer. This was blocked by 10 μM naltrexone (0.7 ± 0.4 nM; P < 0.0001), 1 μM gastrin-releasing peptide receptor antagonist (3 ± 2 nM; P < 0.0001), or 200 μM 1Y-peptide (2 + 2 nM; P < 0.0001). In mice, 0.4 nmol 1Y-peptide significantly attenuated morphine-induced scratching behaviors (scratching bouts, vehicle vs. 1Y-peptide) (92 ± 31 vs. 38 ± 29; P = 0.011; n = 6 to 7 mice per group), without affecting morphine antinociception in warm water tail immersion test (% of maximum possible effect) (70 ± 21 vs. 67 ± 22; P = 0.80; n = 6 mice per group).
CONCLUSIONS:Human μ-opioid receptor 1Y isomer is a C-terminal splicing variant of Oprm1 gene identified in human spinal cord. Cross-talk between 1Y and gastrin releasing peptide receptor is required for mediating opioid-induced pruritus. Disrupting the cross talk may have implications for therapeutic uncoupling of desired analgesic effects from side effects of opioids.</description><identifier>ISSN: 0003-3022</identifier><identifier>EISSN: 1528-1175</identifier><identifier>DOI: 10.1097/ALN.0000000000002776</identifier><identifier>PMID: 31314749</identifier><language>eng</language><publisher>United States: Copyright by , the American Society of Anesthesiologists, Inc. Wolters Kluwer Health, Inc</publisher><subject>Aged ; Analgesics, Opioid - adverse effects ; Animals ; Behavior, Animal ; Cadaver ; Disease Models, Animal ; Humans ; Male ; Mice ; Mice, Inbred C57BL ; Morphine - adverse effects ; Naltrexone - administration & dosage ; Narcotic Antagonists - administration & dosage ; Pruritus - chemically induced ; Pruritus - prevention & control ; Receptors, Bombesin - drug effects ; Receptors, Opioid, mu - drug effects ; Spinal Cord</subject><ispartof>Anesthesiology (Philadelphia), 2019-08, Vol.131 (2), p.381-391</ispartof><rights>Copyright © by 2019, the American Society of Anesthesiologists, Inc. Wolters Kluwer Health, Inc. All Rights Reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5086-46fc8987e6a240b37ef08dd23430fc84f863b5f95671919b038dad39799bc4f23</citedby><cites>FETCH-LOGICAL-c5086-46fc8987e6a240b37ef08dd23430fc84f863b5f95671919b038dad39799bc4f23</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27923,27924</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31314749$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Liu, Xian-Yu</creatorcontrib><creatorcontrib>Ginosar, Yehuda</creatorcontrib><creatorcontrib>Yazdi, Joseph</creatorcontrib><creatorcontrib>Hincker, Alexander</creatorcontrib><creatorcontrib>Chen, Zhou-Feng</creatorcontrib><title>Cross-talk between Human Spinal Cord μ-opioid Receptor 1Y Isoform and Gastrin-releasing Peptide Receptor Mediates Opioid-induced Scratching Behavior</title><title>Anesthesiology (Philadelphia)</title><addtitle>Anesthesiology</addtitle><description>WHAT WE ALREADY KNOW ABOUT THIS TOPICThe spinal administration of opioids can cause intense pruritisInteractions between specific μ-opioid receptor isoforms and the gastrin releasing peptide receptor in spinal tissues likely mediate morphine-induced pruritus
WHAT THIS ARTICLE TELLS US THAT IS NEWHuman spinal cord tissue expresses the 1Y isoform of the μ-opioid receptor, and that isoform functionally interacts with the gastrin releasing peptide receptor to cause cellular calcium influxBlocking interactions between the 1Y isoform and the gastrin releasing peptide receptor does not reduce opioid analgesiaEliminating interactions between the 1Y isoform and the gastrin releasing peptide receptor or reducing 1Y isoform activation may reduce opioid-induced pruritis
BACKGROUND:Although spinal opioids are safe and effective, pruritus is common and distressing. The authors previously demonstrated in mouse spinal cord that interactions between μ-opioid receptor isoform 1D and gastrin releasing peptide receptor mediate morphine-induced scratch. The C-terminal of 1D inhibits morphine-induced scratch without affecting analgesia. The authors hypothesize that human spinal cord also contains itch-specific μ-opioid receptor isoforms which interact with gastrin releasing peptide receptor.
METHODS:Reverse transcription polymerase chain reaction was performed on human spinal cord complimentary DNA from two human cadavers. Calcium responses to morphine (1 μM) were examined using calcium imaging microscopy on human cells (HEK293) coexpressing gastrin releasing peptide receptor and different human μ-opioid receptor isoforms. The authors assessed morphine-induced scratching behavior and thermal analgesia in mice following intrathecal injection of morphine (0.3 nmol) and a transactivator of transcription peptide designed from C-terminal sequences of 1Y isoform (0, 0.1, and 0.4 nmol).
RESULTS:The authors demonstrated 1Y expression in the spinal cord dorsal horn. Morphine administration evoked a calcium response (mean ± SD) (57 ± 13 nM) in cells coexpressing both gastrin releasing peptide receptor and the 1Y isomer. This was blocked by 10 μM naltrexone (0.7 ± 0.4 nM; P < 0.0001), 1 μM gastrin-releasing peptide receptor antagonist (3 ± 2 nM; P < 0.0001), or 200 μM 1Y-peptide (2 + 2 nM; P < 0.0001). In mice, 0.4 nmol 1Y-peptide significantly attenuated morphine-induced scratching behaviors (scratching bouts, vehicle vs. 1Y-peptide) (92 ± 31 vs. 38 ± 29; P = 0.011; n = 6 to 7 mice per group), without affecting morphine antinociception in warm water tail immersion test (% of maximum possible effect) (70 ± 21 vs. 67 ± 22; P = 0.80; n = 6 mice per group).
CONCLUSIONS:Human μ-opioid receptor 1Y isomer is a C-terminal splicing variant of Oprm1 gene identified in human spinal cord. Cross-talk between 1Y and gastrin releasing peptide receptor is required for mediating opioid-induced pruritus. Disrupting the cross talk may have implications for therapeutic uncoupling of desired analgesic effects from side effects of opioids.</description><subject>Aged</subject><subject>Analgesics, Opioid - adverse effects</subject><subject>Animals</subject><subject>Behavior, Animal</subject><subject>Cadaver</subject><subject>Disease Models, Animal</subject><subject>Humans</subject><subject>Male</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Morphine - adverse effects</subject><subject>Naltrexone - administration & dosage</subject><subject>Narcotic Antagonists - administration & dosage</subject><subject>Pruritus - chemically induced</subject><subject>Pruritus - prevention & control</subject><subject>Receptors, Bombesin - drug effects</subject><subject>Receptors, Opioid, mu - drug effects</subject><subject>Spinal Cord</subject><issn>0003-3022</issn><issn>1528-1175</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2019</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kdFuFCEUhomxsWv1DYzhBagwzAxwY1I32jZZrbF64RVh4EwHOwsTYLvxQXwbn8Fncta1tXohNwTO_30k_Ag9Y_SYUSVenKzeHdN7qxKifYAWrKkkYUw0D9FivuWE06o6RI9z_jIfRcPlI3TIGWe1qNUCfVummDMpZrzGHZQtQMBnm7UJ-HLywYx4GZPDP76TOPnoHf4AFqYSE2af8XmOfUxrbILDpyaX5ANJMILJPlzh93POO_hDvAXnTYGML36piA9uY8HhS5tMscOOeQWDufExPUEHvRkzPP29H6FPb15_XJ6R1cXp-fJkRWxDZUvqtrdSSQGtqWracQE9lc5VvOZ0ntS9bHnX9KppBVNMdZRLZxxXQqnO1n3Fj9DLvXfadGtwFkJJZtRT8muTvupovP57Evygr-KNFlRJ2vBZUO8FdveNCfo7llG9q0nPNel_a5qx5_ffvYNue5kDch_YxrFAytfjZgtJD2DGMvzf_RPyw6Ky</recordid><startdate>201908</startdate><enddate>201908</enddate><creator>Liu, Xian-Yu</creator><creator>Ginosar, Yehuda</creator><creator>Yazdi, Joseph</creator><creator>Hincker, Alexander</creator><creator>Chen, Zhou-Feng</creator><general>Copyright by , the American Society of Anesthesiologists, Inc. Wolters Kluwer Health, Inc</general><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>5PM</scope></search><sort><creationdate>201908</creationdate><title>Cross-talk between Human Spinal Cord μ-opioid Receptor 1Y Isoform and Gastrin-releasing Peptide Receptor Mediates Opioid-induced Scratching Behavior</title><author>Liu, Xian-Yu ; Ginosar, Yehuda ; Yazdi, Joseph ; Hincker, Alexander ; Chen, Zhou-Feng</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5086-46fc8987e6a240b37ef08dd23430fc84f863b5f95671919b038dad39799bc4f23</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2019</creationdate><topic>Aged</topic><topic>Analgesics, Opioid - adverse effects</topic><topic>Animals</topic><topic>Behavior, Animal</topic><topic>Cadaver</topic><topic>Disease Models, Animal</topic><topic>Humans</topic><topic>Male</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Morphine - adverse effects</topic><topic>Naltrexone - administration & dosage</topic><topic>Narcotic Antagonists - administration & dosage</topic><topic>Pruritus - chemically induced</topic><topic>Pruritus - prevention & control</topic><topic>Receptors, Bombesin - drug effects</topic><topic>Receptors, Opioid, mu - drug effects</topic><topic>Spinal Cord</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Liu, Xian-Yu</creatorcontrib><creatorcontrib>Ginosar, Yehuda</creatorcontrib><creatorcontrib>Yazdi, Joseph</creatorcontrib><creatorcontrib>Hincker, Alexander</creatorcontrib><creatorcontrib>Chen, Zhou-Feng</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Anesthesiology (Philadelphia)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Liu, Xian-Yu</au><au>Ginosar, Yehuda</au><au>Yazdi, Joseph</au><au>Hincker, Alexander</au><au>Chen, Zhou-Feng</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Cross-talk between Human Spinal Cord μ-opioid Receptor 1Y Isoform and Gastrin-releasing Peptide Receptor Mediates Opioid-induced Scratching Behavior</atitle><jtitle>Anesthesiology (Philadelphia)</jtitle><addtitle>Anesthesiology</addtitle><date>2019-08</date><risdate>2019</risdate><volume>131</volume><issue>2</issue><spage>381</spage><epage>391</epage><pages>381-391</pages><issn>0003-3022</issn><eissn>1528-1175</eissn><abstract>WHAT WE ALREADY KNOW ABOUT THIS TOPICThe spinal administration of opioids can cause intense pruritisInteractions between specific μ-opioid receptor isoforms and the gastrin releasing peptide receptor in spinal tissues likely mediate morphine-induced pruritus
WHAT THIS ARTICLE TELLS US THAT IS NEWHuman spinal cord tissue expresses the 1Y isoform of the μ-opioid receptor, and that isoform functionally interacts with the gastrin releasing peptide receptor to cause cellular calcium influxBlocking interactions between the 1Y isoform and the gastrin releasing peptide receptor does not reduce opioid analgesiaEliminating interactions between the 1Y isoform and the gastrin releasing peptide receptor or reducing 1Y isoform activation may reduce opioid-induced pruritis
BACKGROUND:Although spinal opioids are safe and effective, pruritus is common and distressing. The authors previously demonstrated in mouse spinal cord that interactions between μ-opioid receptor isoform 1D and gastrin releasing peptide receptor mediate morphine-induced scratch. The C-terminal of 1D inhibits morphine-induced scratch without affecting analgesia. The authors hypothesize that human spinal cord also contains itch-specific μ-opioid receptor isoforms which interact with gastrin releasing peptide receptor.
METHODS:Reverse transcription polymerase chain reaction was performed on human spinal cord complimentary DNA from two human cadavers. Calcium responses to morphine (1 μM) were examined using calcium imaging microscopy on human cells (HEK293) coexpressing gastrin releasing peptide receptor and different human μ-opioid receptor isoforms. The authors assessed morphine-induced scratching behavior and thermal analgesia in mice following intrathecal injection of morphine (0.3 nmol) and a transactivator of transcription peptide designed from C-terminal sequences of 1Y isoform (0, 0.1, and 0.4 nmol).
RESULTS:The authors demonstrated 1Y expression in the spinal cord dorsal horn. Morphine administration evoked a calcium response (mean ± SD) (57 ± 13 nM) in cells coexpressing both gastrin releasing peptide receptor and the 1Y isomer. This was blocked by 10 μM naltrexone (0.7 ± 0.4 nM; P < 0.0001), 1 μM gastrin-releasing peptide receptor antagonist (3 ± 2 nM; P < 0.0001), or 200 μM 1Y-peptide (2 + 2 nM; P < 0.0001). In mice, 0.4 nmol 1Y-peptide significantly attenuated morphine-induced scratching behaviors (scratching bouts, vehicle vs. 1Y-peptide) (92 ± 31 vs. 38 ± 29; P = 0.011; n = 6 to 7 mice per group), without affecting morphine antinociception in warm water tail immersion test (% of maximum possible effect) (70 ± 21 vs. 67 ± 22; P = 0.80; n = 6 mice per group).
CONCLUSIONS:Human μ-opioid receptor 1Y isomer is a C-terminal splicing variant of Oprm1 gene identified in human spinal cord. Cross-talk between 1Y and gastrin releasing peptide receptor is required for mediating opioid-induced pruritus. Disrupting the cross talk may have implications for therapeutic uncoupling of desired analgesic effects from side effects of opioids.</abstract><cop>United States</cop><pub>Copyright by , the American Society of Anesthesiologists, Inc. Wolters Kluwer Health, Inc</pub><pmid>31314749</pmid><doi>10.1097/ALN.0000000000002776</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Aged Analgesics, Opioid - adverse effects Animals Behavior, Animal Cadaver Disease Models, Animal Humans Male Mice Mice, Inbred C57BL Morphine - adverse effects Naltrexone - administration & dosage Narcotic Antagonists - administration & dosage Pruritus - chemically induced Pruritus - prevention & control Receptors, Bombesin - drug effects Receptors, Opioid, mu - drug effects Spinal Cord |
| title | Cross-talk between Human Spinal Cord μ-opioid Receptor 1Y Isoform and Gastrin-releasing Peptide Receptor Mediates Opioid-induced Scratching Behavior |
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