In Vivo Calcium Imaging Visualizes Incision-Induced Primary Afferent Sensitization and Its Amelioration by Capsaicin Pretreatment
Previous studies have shown that infiltration of capsaicin into the surgical site can prevent incision-induced spontaneous pain like behaviors and heat hyperalgesia. In the present study, we aimed to monitor primary sensory neuron Ca activity in the intact dorsal root ganglia (DRG) using Pirt-GCaMP3...
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creator | Ishida, Hirotake Zhang, Yan Gomez, Ruben Shannonhouse, John Son, Hyeonwi Banik, Ratan Kim, Yu Shin |
description | Previous studies have shown that infiltration of capsaicin into the surgical site can prevent incision-induced spontaneous pain like behaviors and heat hyperalgesia. In the present study, we aimed to monitor primary sensory neuron Ca
activity in the intact dorsal root ganglia (DRG) using Pirt-GCaMP3 male and female mice pretreated with capsaicin or vehicle before the plantar incision. Intraplantar injection of capsaicin (0.05%) significantly attenuated spontaneous pain, mechanical, and heat hypersensitivity after plantar incision. The Ca
response in
DRG and in
spinal cord was significantly enhanced in the ipsilateral side compared with contralateral side or naive control. Primary sensory nerve fiber length was significantly decreased in the incision skin area in capsaicin-pretreated animals detected by immunohistochemistry and placental alkaline phosphatase (PLAP) staining. Thus, capsaicin pretreatment attenuates incisional pain by suppressing Ca
response because of degeneration of primary sensory nerve fibers in the skin.
Postoperative surgery pain is a major health and economic problem worldwide with ∼235 million major surgical procedures annually. Approximately 50% of these patients report uncontrolled or poorly controlled postoperative pain. However, mechanistic studies of postoperative surgery pain in primary sensory neurons have been limited to
models or small numbers of neurons. Using an innovative, distinctive, and interdisciplinary
populational dorsal root ganglia (DRG) imaging (>1800 neurons/DRG) approach, we revealed increased DRG neuronal Ca
activity from postoperative pain mouse model. This indicates widespread DRG primary sensory neuron plasticity. Increased neuronal Ca
activity occurs among various sizes of neurons but mostly in small-diameter and medium-diameter nociceptors. Capsaicin pretreatment as a therapeutic option significantly attenuates Ca
activity and postoperative pain. |
doi_str_mv | 10.1523/JNEUROSCI.0457-21.2021 |
format | Article |
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activity in the intact dorsal root ganglia (DRG) using Pirt-GCaMP3 male and female mice pretreated with capsaicin or vehicle before the plantar incision. Intraplantar injection of capsaicin (0.05%) significantly attenuated spontaneous pain, mechanical, and heat hypersensitivity after plantar incision. The Ca
response in
DRG and in
spinal cord was significantly enhanced in the ipsilateral side compared with contralateral side or naive control. Primary sensory nerve fiber length was significantly decreased in the incision skin area in capsaicin-pretreated animals detected by immunohistochemistry and placental alkaline phosphatase (PLAP) staining. Thus, capsaicin pretreatment attenuates incisional pain by suppressing Ca
response because of degeneration of primary sensory nerve fibers in the skin.
Postoperative surgery pain is a major health and economic problem worldwide with ∼235 million major surgical procedures annually. Approximately 50% of these patients report uncontrolled or poorly controlled postoperative pain. However, mechanistic studies of postoperative surgery pain in primary sensory neurons have been limited to
models or small numbers of neurons. Using an innovative, distinctive, and interdisciplinary
populational dorsal root ganglia (DRG) imaging (>1800 neurons/DRG) approach, we revealed increased DRG neuronal Ca
activity from postoperative pain mouse model. This indicates widespread DRG primary sensory neuron plasticity. Increased neuronal Ca
activity occurs among various sizes of neurons but mostly in small-diameter and medium-diameter nociceptors. Capsaicin pretreatment as a therapeutic option significantly attenuates Ca
activity and postoperative pain.</description><identifier>ISSN: 0270-6474</identifier><identifier>EISSN: 1529-2401</identifier><identifier>DOI: 10.1523/JNEUROSCI.0457-21.2021</identifier><identifier>PMID: 34452938</identifier><language>eng</language><publisher>United States: Society for Neuroscience</publisher><subject>Afferent Pathways - chemistry ; Afferent Pathways - drug effects ; Afferent Pathways - metabolism ; Alkaline phosphatase ; Animal models ; Animals ; Attenuation ; Calcium - metabolism ; Calcium imaging ; Calcium ions ; Capsaicin ; Capsaicin - administration & dosage ; Degeneration ; Dorsal root ganglia ; Female ; Fibers ; Ganglia ; Ganglia, Spinal - chemistry ; Ganglia, Spinal - metabolism ; Hindlimb - innervation ; Hindlimb - metabolism ; Hyperalgesia - metabolism ; Hyperalgesia - prevention & control ; Hypersensitivity ; Immunohistochemistry ; Male ; Mice ; Mice, Inbred C57BL ; Neurons ; Nociceptors ; Pain ; Pain perception ; Pain, Postoperative - metabolism ; Pain, Postoperative - prevention & control ; Placental alkaline phosphatase ; Plantar Plate - chemistry ; Plantar Plate - innervation ; Plantar Plate - metabolism ; Pretreatment ; Sensory neurons ; Sensory System Agents - administration & dosage ; Skin ; Spinal cord ; Surgery ; Surgical Wound - metabolism</subject><ispartof>The Journal of neuroscience, 2021-10, Vol.41 (41), p.8494-8507</ispartof><rights>Copyright © 2021 the authors.</rights><rights>Copyright Society for Neuroscience Oct 13, 2021</rights><rights>Copyright © 2021 the authors 2021</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c394t-1d74b1d658391cb4d79e57f578b8e7c348e7f94ee9ff14397abb60263b3d5db53</citedby><cites>FETCH-LOGICAL-c394t-1d74b1d658391cb4d79e57f578b8e7c348e7f94ee9ff14397abb60263b3d5db53</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8513701/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8513701/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,723,776,780,881,27901,27902,53766,53768</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34452938$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Ishida, Hirotake</creatorcontrib><creatorcontrib>Zhang, Yan</creatorcontrib><creatorcontrib>Gomez, Ruben</creatorcontrib><creatorcontrib>Shannonhouse, John</creatorcontrib><creatorcontrib>Son, Hyeonwi</creatorcontrib><creatorcontrib>Banik, Ratan</creatorcontrib><creatorcontrib>Kim, Yu Shin</creatorcontrib><title>In Vivo Calcium Imaging Visualizes Incision-Induced Primary Afferent Sensitization and Its Amelioration by Capsaicin Pretreatment</title><title>The Journal of neuroscience</title><addtitle>J Neurosci</addtitle><description>Previous studies have shown that infiltration of capsaicin into the surgical site can prevent incision-induced spontaneous pain like behaviors and heat hyperalgesia. In the present study, we aimed to monitor primary sensory neuron Ca
activity in the intact dorsal root ganglia (DRG) using Pirt-GCaMP3 male and female mice pretreated with capsaicin or vehicle before the plantar incision. Intraplantar injection of capsaicin (0.05%) significantly attenuated spontaneous pain, mechanical, and heat hypersensitivity after plantar incision. The Ca
response in
DRG and in
spinal cord was significantly enhanced in the ipsilateral side compared with contralateral side or naive control. Primary sensory nerve fiber length was significantly decreased in the incision skin area in capsaicin-pretreated animals detected by immunohistochemistry and placental alkaline phosphatase (PLAP) staining. Thus, capsaicin pretreatment attenuates incisional pain by suppressing Ca
response because of degeneration of primary sensory nerve fibers in the skin.
Postoperative surgery pain is a major health and economic problem worldwide with ∼235 million major surgical procedures annually. Approximately 50% of these patients report uncontrolled or poorly controlled postoperative pain. However, mechanistic studies of postoperative surgery pain in primary sensory neurons have been limited to
models or small numbers of neurons. Using an innovative, distinctive, and interdisciplinary
populational dorsal root ganglia (DRG) imaging (>1800 neurons/DRG) approach, we revealed increased DRG neuronal Ca
activity from postoperative pain mouse model. This indicates widespread DRG primary sensory neuron plasticity. Increased neuronal Ca
activity occurs among various sizes of neurons but mostly in small-diameter and medium-diameter nociceptors. Capsaicin pretreatment as a therapeutic option significantly attenuates Ca
activity and postoperative pain.</description><subject>Afferent Pathways - chemistry</subject><subject>Afferent Pathways - drug effects</subject><subject>Afferent Pathways - metabolism</subject><subject>Alkaline phosphatase</subject><subject>Animal models</subject><subject>Animals</subject><subject>Attenuation</subject><subject>Calcium - metabolism</subject><subject>Calcium imaging</subject><subject>Calcium ions</subject><subject>Capsaicin</subject><subject>Capsaicin - administration & dosage</subject><subject>Degeneration</subject><subject>Dorsal root ganglia</subject><subject>Female</subject><subject>Fibers</subject><subject>Ganglia</subject><subject>Ganglia, Spinal - chemistry</subject><subject>Ganglia, Spinal - metabolism</subject><subject>Hindlimb - innervation</subject><subject>Hindlimb - metabolism</subject><subject>Hyperalgesia - metabolism</subject><subject>Hyperalgesia - prevention & control</subject><subject>Hypersensitivity</subject><subject>Immunohistochemistry</subject><subject>Male</subject><subject>Mice</subject><subject>Mice, Inbred C57BL</subject><subject>Neurons</subject><subject>Nociceptors</subject><subject>Pain</subject><subject>Pain perception</subject><subject>Pain, Postoperative - metabolism</subject><subject>Pain, Postoperative - prevention & control</subject><subject>Placental alkaline phosphatase</subject><subject>Plantar Plate - chemistry</subject><subject>Plantar Plate - innervation</subject><subject>Plantar Plate - metabolism</subject><subject>Pretreatment</subject><subject>Sensory neurons</subject><subject>Sensory System Agents - administration & dosage</subject><subject>Skin</subject><subject>Spinal cord</subject><subject>Surgery</subject><subject>Surgical Wound - metabolism</subject><issn>0270-6474</issn><issn>1529-2401</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkctu1DAUhi0EotPCK1SW2LDJ4GucbJBGo0KDKoooZWv5lsFVYg92Uqnd9c3r0bSjwsaWzvnOfy4_AKcYLTEn9NO372fXPy-v1t0SMS4qgpcEEfwKLEq2rQhD-DVYICJQVTPBjsBxzjcIIYGweAuOKGMFo80CPHQB_va3Ea7VYPw8wm5UGx82JZhnNfh7l2EXjM8-hqoLdjbOwh_JjyrdwVXfu-TCBK9cyH7y92oqGFTBwm7KcDW6wce0D-q70mKblTc-FAE3JaemsRS_A296NWT3_uk_Addfzn6tz6uLy6_denVRGdqyqcJWMI1tzRvaYqOZFa3jouei0Y0ThrLy9i1zru17zGgrlNY1IjXV1HKrOT0Bn_e621mPzprSOqlBbve7yKi8_DcT_B-5ibey4ZiWuxWBj08CKf6dXZ7k6LNxw6CCi3OWhNc1KoenO_TDf-hNnFMo6xWqobxFQrBC1XvKpJhzcv1hGIzkzmV5cFnuXJYEy53LpfD05SqHsmdb6SOix6bg</recordid><startdate>20211013</startdate><enddate>20211013</enddate><creator>Ishida, Hirotake</creator><creator>Zhang, Yan</creator><creator>Gomez, Ruben</creator><creator>Shannonhouse, John</creator><creator>Son, Hyeonwi</creator><creator>Banik, Ratan</creator><creator>Kim, Yu Shin</creator><general>Society for Neuroscience</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>7QG</scope><scope>7QR</scope><scope>7TK</scope><scope>7U7</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>P64</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20211013</creationdate><title>In Vivo Calcium Imaging Visualizes Incision-Induced Primary Afferent Sensitization and Its Amelioration by Capsaicin Pretreatment</title><author>Ishida, Hirotake ; Zhang, Yan ; Gomez, Ruben ; Shannonhouse, John ; Son, Hyeonwi ; Banik, Ratan ; Kim, Yu Shin</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c394t-1d74b1d658391cb4d79e57f578b8e7c348e7f94ee9ff14397abb60263b3d5db53</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Afferent Pathways - chemistry</topic><topic>Afferent Pathways - drug effects</topic><topic>Afferent Pathways - metabolism</topic><topic>Alkaline phosphatase</topic><topic>Animal models</topic><topic>Animals</topic><topic>Attenuation</topic><topic>Calcium - metabolism</topic><topic>Calcium imaging</topic><topic>Calcium ions</topic><topic>Capsaicin</topic><topic>Capsaicin - administration & dosage</topic><topic>Degeneration</topic><topic>Dorsal root ganglia</topic><topic>Female</topic><topic>Fibers</topic><topic>Ganglia</topic><topic>Ganglia, Spinal - chemistry</topic><topic>Ganglia, Spinal - metabolism</topic><topic>Hindlimb - innervation</topic><topic>Hindlimb - metabolism</topic><topic>Hyperalgesia - metabolism</topic><topic>Hyperalgesia - prevention & control</topic><topic>Hypersensitivity</topic><topic>Immunohistochemistry</topic><topic>Male</topic><topic>Mice</topic><topic>Mice, Inbred C57BL</topic><topic>Neurons</topic><topic>Nociceptors</topic><topic>Pain</topic><topic>Pain perception</topic><topic>Pain, Postoperative - metabolism</topic><topic>Pain, Postoperative - prevention & control</topic><topic>Placental alkaline phosphatase</topic><topic>Plantar Plate - chemistry</topic><topic>Plantar Plate - innervation</topic><topic>Plantar Plate - metabolism</topic><topic>Pretreatment</topic><topic>Sensory neurons</topic><topic>Sensory System Agents - administration & dosage</topic><topic>Skin</topic><topic>Spinal cord</topic><topic>Surgery</topic><topic>Surgical Wound - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ishida, Hirotake</creatorcontrib><creatorcontrib>Zhang, Yan</creatorcontrib><creatorcontrib>Gomez, Ruben</creatorcontrib><creatorcontrib>Shannonhouse, John</creatorcontrib><creatorcontrib>Son, Hyeonwi</creatorcontrib><creatorcontrib>Banik, Ratan</creatorcontrib><creatorcontrib>Kim, Yu Shin</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ishida, Hirotake</au><au>Zhang, Yan</au><au>Gomez, Ruben</au><au>Shannonhouse, John</au><au>Son, Hyeonwi</au><au>Banik, Ratan</au><au>Kim, Yu Shin</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>In Vivo Calcium Imaging Visualizes Incision-Induced Primary Afferent Sensitization and Its Amelioration by Capsaicin Pretreatment</atitle><jtitle>The Journal of neuroscience</jtitle><addtitle>J Neurosci</addtitle><date>2021-10-13</date><risdate>2021</risdate><volume>41</volume><issue>41</issue><spage>8494</spage><epage>8507</epage><pages>8494-8507</pages><issn>0270-6474</issn><eissn>1529-2401</eissn><abstract>Previous studies have shown that infiltration of capsaicin into the surgical site can prevent incision-induced spontaneous pain like behaviors and heat hyperalgesia. In the present study, we aimed to monitor primary sensory neuron Ca
activity in the intact dorsal root ganglia (DRG) using Pirt-GCaMP3 male and female mice pretreated with capsaicin or vehicle before the plantar incision. Intraplantar injection of capsaicin (0.05%) significantly attenuated spontaneous pain, mechanical, and heat hypersensitivity after plantar incision. The Ca
response in
DRG and in
spinal cord was significantly enhanced in the ipsilateral side compared with contralateral side or naive control. Primary sensory nerve fiber length was significantly decreased in the incision skin area in capsaicin-pretreated animals detected by immunohistochemistry and placental alkaline phosphatase (PLAP) staining. Thus, capsaicin pretreatment attenuates incisional pain by suppressing Ca
response because of degeneration of primary sensory nerve fibers in the skin.
Postoperative surgery pain is a major health and economic problem worldwide with ∼235 million major surgical procedures annually. Approximately 50% of these patients report uncontrolled or poorly controlled postoperative pain. However, mechanistic studies of postoperative surgery pain in primary sensory neurons have been limited to
models or small numbers of neurons. Using an innovative, distinctive, and interdisciplinary
populational dorsal root ganglia (DRG) imaging (>1800 neurons/DRG) approach, we revealed increased DRG neuronal Ca
activity from postoperative pain mouse model. This indicates widespread DRG primary sensory neuron plasticity. Increased neuronal Ca
activity occurs among various sizes of neurons but mostly in small-diameter and medium-diameter nociceptors. Capsaicin pretreatment as a therapeutic option significantly attenuates Ca
activity and postoperative pain.</abstract><cop>United States</cop><pub>Society for Neuroscience</pub><pmid>34452938</pmid><doi>10.1523/JNEUROSCI.0457-21.2021</doi><tpages>14</tpages></addata></record> |
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subjects | Afferent Pathways - chemistry Afferent Pathways - drug effects Afferent Pathways - metabolism Alkaline phosphatase Animal models Animals Attenuation Calcium - metabolism Calcium imaging Calcium ions Capsaicin Capsaicin - administration & dosage Degeneration Dorsal root ganglia Female Fibers Ganglia Ganglia, Spinal - chemistry Ganglia, Spinal - metabolism Hindlimb - innervation Hindlimb - metabolism Hyperalgesia - metabolism Hyperalgesia - prevention & control Hypersensitivity Immunohistochemistry Male Mice Mice, Inbred C57BL Neurons Nociceptors Pain Pain perception Pain, Postoperative - metabolism Pain, Postoperative - prevention & control Placental alkaline phosphatase Plantar Plate - chemistry Plantar Plate - innervation Plantar Plate - metabolism Pretreatment Sensory neurons Sensory System Agents - administration & dosage Skin Spinal cord Surgery Surgical Wound - metabolism |
title | In Vivo Calcium Imaging Visualizes Incision-Induced Primary Afferent Sensitization and Its Amelioration by Capsaicin Pretreatment |
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