Reactive Oxygen Species (ROS) are Critical for Morphine Exacerbation of HIV-1 gp120-Induced Pain
Many HIV patients develop chronic pain and use opioid-derived medicine as primary analgesics. Emerging clinical evidence suggests that chronic use of opioid analgesics paradoxically heightens pain states in patients. This side effect of opioid analgesics has a significant negative impact on clinical...
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| Veröffentlicht in: | Journal of neuroimmune pharmacology 2021-09, Vol.16 (3), p.581-591 |
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| creator | Shi, Yuqiang Yuan, Subo Tang, Shao-Jun |
| description | Many HIV patients develop chronic pain and use opioid-derived medicine as primary analgesics. Emerging clinical evidence suggests that chronic use of opioid analgesics paradoxically heightens pain states in patients. This side effect of opioid analgesics has a significant negative impact on clinical practice, but the underlying pathogenic mechanism remains elusive. Using a mouse model of HIV-associated pain, we simulated the development of morphine exacerbation on pain and investigated potential underlying cellular and molecular pathways. We found that repeated morphine treatment promoted astrocyte activation in the spinal dorsal horn (SDH) and up-regulation of pro-inflammatory cytokines IL-1β and TNF-α. Furthermore, we observed that morphine administration potentiated mitochondrial reactive oxygen species (ROS) in the SDH of the HIV pain model, especially on astrocytes. Systemic application of the ROS scavenger phenyl-N-t-butyl nitrone (PBN) not only blocked the enhancement of gp120-induced hyperalgesia by morphine but also astrocytic activation and cytokine up-regulation. These findings suggest a critical role of ROS in mediating the exacerbation of gp120-induced pain by morphine.
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| doi_str_mv | 10.1007/s11481-020-09951-6 |
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Graphical abstract</description><identifier>ISSN: 1557-1890</identifier><identifier>EISSN: 1557-1904</identifier><identifier>DOI: 10.1007/s11481-020-09951-6</identifier><identifier>PMID: 32827051</identifier><language>eng</language><publisher>New York: Springer US</publisher><subject>Analgesics ; Analgesics, Opioid - toxicity ; Biomedical and Life Sciences ; Biomedicine ; Cell Biology ; HIV Infections ; HIV-1 ; Humans ; Hyperalgesia ; Immunology ; Morphine ; Morphine - toxicity ; Narcotics ; Neurosciences ; Pain ; Pharmacology/Toxicology ; Reactive Oxygen Species ; Spinal Cord ; Virology</subject><ispartof>Journal of neuroimmune pharmacology, 2021-09, Vol.16 (3), p.581-591</ispartof><rights>Springer Science+Business Media, LLC, part of Springer Nature 2020</rights><rights>2020. Springer Science+Business Media, LLC, part of Springer Nature.</rights><rights>Springer Science+Business Media, LLC, part of Springer Nature 2020.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c523t-f43ce7c3621b0c584141fe62d4679fbf33d882679554299ea3083332724f88073</citedby><cites>FETCH-LOGICAL-c523t-f43ce7c3621b0c584141fe62d4679fbf33d882679554299ea3083332724f88073</cites><orcidid>0000-0002-6076-5481</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s11481-020-09951-6$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s11481-020-09951-6$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>230,314,780,784,885,27924,27925,41488,42557,51319</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/32827051$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Shi, Yuqiang</creatorcontrib><creatorcontrib>Yuan, Subo</creatorcontrib><creatorcontrib>Tang, Shao-Jun</creatorcontrib><title>Reactive Oxygen Species (ROS) are Critical for Morphine Exacerbation of HIV-1 gp120-Induced Pain</title><title>Journal of neuroimmune pharmacology</title><addtitle>J Neuroimmune Pharmacol</addtitle><addtitle>J Neuroimmune Pharmacol</addtitle><description>Many HIV patients develop chronic pain and use opioid-derived medicine as primary analgesics. Emerging clinical evidence suggests that chronic use of opioid analgesics paradoxically heightens pain states in patients. This side effect of opioid analgesics has a significant negative impact on clinical practice, but the underlying pathogenic mechanism remains elusive. Using a mouse model of HIV-associated pain, we simulated the development of morphine exacerbation on pain and investigated potential underlying cellular and molecular pathways. We found that repeated morphine treatment promoted astrocyte activation in the spinal dorsal horn (SDH) and up-regulation of pro-inflammatory cytokines IL-1β and TNF-α. Furthermore, we observed that morphine administration potentiated mitochondrial reactive oxygen species (ROS) in the SDH of the HIV pain model, especially on astrocytes. Systemic application of the ROS scavenger phenyl-N-t-butyl nitrone (PBN) not only blocked the enhancement of gp120-induced hyperalgesia by morphine but also astrocytic activation and cytokine up-regulation. These findings suggest a critical role of ROS in mediating the exacerbation of gp120-induced pain by morphine.
Graphical abstract</description><subject>Analgesics</subject><subject>Analgesics, Opioid - toxicity</subject><subject>Biomedical and Life Sciences</subject><subject>Biomedicine</subject><subject>Cell Biology</subject><subject>HIV Infections</subject><subject>HIV-1</subject><subject>Humans</subject><subject>Hyperalgesia</subject><subject>Immunology</subject><subject>Morphine</subject><subject>Morphine - toxicity</subject><subject>Narcotics</subject><subject>Neurosciences</subject><subject>Pain</subject><subject>Pharmacology/Toxicology</subject><subject>Reactive Oxygen Species</subject><subject>Spinal Cord</subject><subject>Virology</subject><issn>1557-1890</issn><issn>1557-1904</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><recordid>eNp9kU1v1DAQhi0EomXLH-CALHEph1B_xvYFCa0KXaloUVu4Gq8z2brK2qmdVO2_J8u2hXLg5JHmmdczehB6Q8kHSog6KpQKTSvCSEWMkbSqn6F9KqWqqCHi-UOtDdlDr0q5IkQIQchLtMeZZopIuo9-noHzQ7gBvLy9W0PE5z34AAUfni3P32OXAc9zGIJ3HW5Txl9T7i9DBHx86zzklRtCiji1-GTxo6J43dNpm0VsRg8N_uZCPEAvWtcVeH3_ztD3z8cX85PqdPllMf90WnnJ-FC1gntQnteMroiXWlBBW6hZI2pl2lXLeaM1m2opBTMGHCeac84UE63WRPEZ-rjL7cfVBhoPccius30OG5fvbHLBPu3EcGnX6cYqbZSSYgo4vA_I6XqEMthNKB66zkVIY7FM8JobI_QWffcPepXGHKfzLJPSUCnUxM4Q21E-p1IytI_LUGK3Au1OoJ0E2t8C7Xbo7d9nPI48GJsAvgPK1IpryH_-_k_sL9YFozM</recordid><startdate>20210901</startdate><enddate>20210901</enddate><creator>Shi, Yuqiang</creator><creator>Yuan, Subo</creator><creator>Tang, Shao-Jun</creator><general>Springer US</general><general>Springer Nature B.V</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>3V.</scope><scope>7X7</scope><scope>7XB</scope><scope>88E</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>BENPR</scope><scope>CCPQU</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>K9.</scope><scope>M0S</scope><scope>M1P</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-6076-5481</orcidid></search><sort><creationdate>20210901</creationdate><title>Reactive Oxygen Species (ROS) are Critical for Morphine Exacerbation of HIV-1 gp120-Induced Pain</title><author>Shi, Yuqiang ; Yuan, Subo ; Tang, Shao-Jun</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c523t-f43ce7c3621b0c584141fe62d4679fbf33d882679554299ea3083332724f88073</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Analgesics</topic><topic>Analgesics, Opioid - toxicity</topic><topic>Biomedical and Life Sciences</topic><topic>Biomedicine</topic><topic>Cell Biology</topic><topic>HIV Infections</topic><topic>HIV-1</topic><topic>Humans</topic><topic>Hyperalgesia</topic><topic>Immunology</topic><topic>Morphine</topic><topic>Morphine - toxicity</topic><topic>Narcotics</topic><topic>Neurosciences</topic><topic>Pain</topic><topic>Pharmacology/Toxicology</topic><topic>Reactive Oxygen Species</topic><topic>Spinal Cord</topic><topic>Virology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Shi, Yuqiang</creatorcontrib><creatorcontrib>Yuan, Subo</creatorcontrib><creatorcontrib>Tang, Shao-Jun</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central</collection><collection>ProQuest One Community College</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Journal of neuroimmune pharmacology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Shi, Yuqiang</au><au>Yuan, Subo</au><au>Tang, Shao-Jun</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Reactive Oxygen Species (ROS) are Critical for Morphine Exacerbation of HIV-1 gp120-Induced Pain</atitle><jtitle>Journal of neuroimmune pharmacology</jtitle><stitle>J Neuroimmune Pharmacol</stitle><addtitle>J Neuroimmune Pharmacol</addtitle><date>2021-09-01</date><risdate>2021</risdate><volume>16</volume><issue>3</issue><spage>581</spage><epage>591</epage><pages>581-591</pages><issn>1557-1890</issn><eissn>1557-1904</eissn><abstract>Many HIV patients develop chronic pain and use opioid-derived medicine as primary analgesics. Emerging clinical evidence suggests that chronic use of opioid analgesics paradoxically heightens pain states in patients. This side effect of opioid analgesics has a significant negative impact on clinical practice, but the underlying pathogenic mechanism remains elusive. Using a mouse model of HIV-associated pain, we simulated the development of morphine exacerbation on pain and investigated potential underlying cellular and molecular pathways. We found that repeated morphine treatment promoted astrocyte activation in the spinal dorsal horn (SDH) and up-regulation of pro-inflammatory cytokines IL-1β and TNF-α. Furthermore, we observed that morphine administration potentiated mitochondrial reactive oxygen species (ROS) in the SDH of the HIV pain model, especially on astrocytes. Systemic application of the ROS scavenger phenyl-N-t-butyl nitrone (PBN) not only blocked the enhancement of gp120-induced hyperalgesia by morphine but also astrocytic activation and cytokine up-regulation. These findings suggest a critical role of ROS in mediating the exacerbation of gp120-induced pain by morphine.
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| subjects | Analgesics Analgesics, Opioid - toxicity Biomedical and Life Sciences Biomedicine Cell Biology HIV Infections HIV-1 Humans Hyperalgesia Immunology Morphine Morphine - toxicity Narcotics Neurosciences Pain Pharmacology/Toxicology Reactive Oxygen Species Spinal Cord Virology |
| title | Reactive Oxygen Species (ROS) are Critical for Morphine Exacerbation of HIV-1 gp120-Induced Pain |
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