The neurovascular mechanism of clitoral erection: nitric oxide and cGMP‐stimulated activation of BKCa channels
Female sexual function is under‐studied, and mechanisms of clitoral engorgement‐relaxation are incompletely understood. Penile erection results from nitric oxide (NO) ‐induced cyclic guanosine monophosphate (cGMP) accumulation. cGMP‐dependent protein kinase (PKG) activates large‐conductance, calcium...
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| creator | Gragasin, Ferrante S. Michelakis, Evangelos D. Hogan, Angie Moudgil, Rohit Hashimoto, Kyoko Wu, Xichen Bonnet, Sandra Haromy, Al Archer, Stephen L. |
| description | Female sexual function is under‐studied, and mechanisms of clitoral engorgement‐relaxation are incompletely understood. Penile erection results from nitric oxide (NO) ‐induced cyclic guanosine monophosphate (cGMP) accumulation. cGMP‐dependent protein kinase (PKG) activates large‐conductance, calcium‐activated potassium channels (BKCa), thereby hyperpolarizing and relaxing vascular and trabecular smooth muscle cells, allowing engorgement. We hypothesize rat clitorises relax by a similar mechanism. Rat clitorises express components of the proposed pathway: neuronal and endothelial NO synthases, soluble guanylyl cyclase (sGC), type 5 phosphodiesterase (PDE‐5), and BKCa channels. The NO donor diethylamine NONOate (DEANO), the PKG activator 8‐pCPT‐cGMP, and the PDE‐5 inhibitor sildenafil, cause dose‐dependent clitoral relaxation that is inhibited by antagonists of PKG (Rp‐8‐Br‐cGMPS) or BKCa channels (iberiotoxin). Electrical field stimulation induces tetrodotoxin‐sensitive NO release and relaxation that is inhibited by the Na+ channel blocker tetrodotoxin or sGC inhibitor 1H‐(1,2,4)oxadiozolo(4,3‐a)quinoxalin‐1‐one. Human BKCa channels, transferred to Chinese hamster ovary cells via an adenoviral vector, and endogenous rat clitoral smooth muscle K+ current are activated by this PKG‐dependent mechanism. Laser confocal microscopy reveals protein expression of BKCa channels on clitoral smooth muscle cells; these cells exhibit BKCa channel activity that is activated by both DEANO and sildenafil. We conclude that neurovascular derived NO causes clitoral relaxation via a PKG‐dependent activation of BKCa channels. The BKCa channel is an appealing target for drug therapy of female erectile dysfunction.— Gragasin, F. S., Michelakis, E. D., Hogan, A., Moudgil, R., Hashimoto, K., Wu, X., Bonnet, S., Haromy, A., Archer, S. L. The neurovascular mechanism of clitoral erection: nitric oxide and cGMP‐stimulated activation of BKCa channels. FASEB J. 18, 1382‐1391 (2004) |
| doi_str_mv | 10.1096/fj.04-1978com |
| format | Article |
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Penile erection results from nitric oxide (NO) ‐induced cyclic guanosine monophosphate (cGMP) accumulation. cGMP‐dependent protein kinase (PKG) activates large‐conductance, calcium‐activated potassium channels (BKCa), thereby hyperpolarizing and relaxing vascular and trabecular smooth muscle cells, allowing engorgement. We hypothesize rat clitorises relax by a similar mechanism. Rat clitorises express components of the proposed pathway: neuronal and endothelial NO synthases, soluble guanylyl cyclase (sGC), type 5 phosphodiesterase (PDE‐5), and BKCa channels. The NO donor diethylamine NONOate (DEANO), the PKG activator 8‐pCPT‐cGMP, and the PDE‐5 inhibitor sildenafil, cause dose‐dependent clitoral relaxation that is inhibited by antagonists of PKG (Rp‐8‐Br‐cGMPS) or BKCa channels (iberiotoxin). Electrical field stimulation induces tetrodotoxin‐sensitive NO release and relaxation that is inhibited by the Na+ channel blocker tetrodotoxin or sGC inhibitor 1H‐(1,2,4)oxadiozolo(4,3‐a)quinoxalin‐1‐one. Human BKCa channels, transferred to Chinese hamster ovary cells via an adenoviral vector, and endogenous rat clitoral smooth muscle K+ current are activated by this PKG‐dependent mechanism. Laser confocal microscopy reveals protein expression of BKCa channels on clitoral smooth muscle cells; these cells exhibit BKCa channel activity that is activated by both DEANO and sildenafil. We conclude that neurovascular derived NO causes clitoral relaxation via a PKG‐dependent activation of BKCa channels. The BKCa channel is an appealing target for drug therapy of female erectile dysfunction.— Gragasin, F. S., Michelakis, E. D., Hogan, A., Moudgil, R., Hashimoto, K., Wu, X., Bonnet, S., Haromy, A., Archer, S. L. The neurovascular mechanism of clitoral erection: nitric oxide and cGMP‐stimulated activation of BKCa channels. FASEB J. 18, 1382‐1391 (2004)</description><identifier>ISSN: 0892-6638</identifier><identifier>EISSN: 1530-6860</identifier><identifier>DOI: 10.1096/fj.04-1978com</identifier><identifier>PMID: 15333581</identifier><language>eng</language><publisher>United States: Federation of American Societies for Experimental Biology</publisher><subject>Animals ; Calcium - metabolism ; CHO Cells ; Clitoris - anatomy & histology ; Clitoris - blood supply ; Clitoris - innervation ; Clitoris - physiology ; Cricetinae ; Cyclic GMP - metabolism ; Cyclic GMP-Dependent Protein Kinases - metabolism ; Electric Stimulation ; electrical field stimulation ; Electrophysiology ; Female ; Humans ; Immunohistochemistry ; In Vitro Techniques ; Large-Conductance Calcium-Activated Potassium Channels ; laser capture microdissection ; Lasers ; Microdissection ; Muscle Relaxation - drug effects ; Muscle, Smooth - blood supply ; Muscle, Smooth - drug effects ; Muscle, Smooth - innervation ; Muscle, Smooth - physiology ; Nitric Oxide - biosynthesis ; Nitric Oxide - metabolism ; nitric oxide electrode ; phosphodiesterase 5 ; Piperazines - pharmacology ; Potassium Channels, Calcium-Activated - genetics ; Potassium Channels, Calcium-Activated - metabolism ; protein kinase G ; Purines ; Rats ; Rats, Sprague-Dawley ; Signal Transduction - drug effects ; sildenafil ; Sildenafil Citrate ; Sulfones</subject><ispartof>The FASEB journal, 2004-09, Vol.18 (12), p.1382-1391</ispartof><rights>FASEB</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1096%2Ffj.04-1978com$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1096%2Ffj.04-1978com$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,27903,27904,45553,45554</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/15333581$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Gragasin, Ferrante S.</creatorcontrib><creatorcontrib>Michelakis, Evangelos D.</creatorcontrib><creatorcontrib>Hogan, Angie</creatorcontrib><creatorcontrib>Moudgil, Rohit</creatorcontrib><creatorcontrib>Hashimoto, Kyoko</creatorcontrib><creatorcontrib>Wu, Xichen</creatorcontrib><creatorcontrib>Bonnet, Sandra</creatorcontrib><creatorcontrib>Haromy, Al</creatorcontrib><creatorcontrib>Archer, Stephen L.</creatorcontrib><title>The neurovascular mechanism of clitoral erection: nitric oxide and cGMP‐stimulated activation of BKCa channels</title><title>The FASEB journal</title><addtitle>FASEB J</addtitle><description>Female sexual function is under‐studied, and mechanisms of clitoral engorgement‐relaxation are incompletely understood. Penile erection results from nitric oxide (NO) ‐induced cyclic guanosine monophosphate (cGMP) accumulation. cGMP‐dependent protein kinase (PKG) activates large‐conductance, calcium‐activated potassium channels (BKCa), thereby hyperpolarizing and relaxing vascular and trabecular smooth muscle cells, allowing engorgement. We hypothesize rat clitorises relax by a similar mechanism. Rat clitorises express components of the proposed pathway: neuronal and endothelial NO synthases, soluble guanylyl cyclase (sGC), type 5 phosphodiesterase (PDE‐5), and BKCa channels. The NO donor diethylamine NONOate (DEANO), the PKG activator 8‐pCPT‐cGMP, and the PDE‐5 inhibitor sildenafil, cause dose‐dependent clitoral relaxation that is inhibited by antagonists of PKG (Rp‐8‐Br‐cGMPS) or BKCa channels (iberiotoxin). Electrical field stimulation induces tetrodotoxin‐sensitive NO release and relaxation that is inhibited by the Na+ channel blocker tetrodotoxin or sGC inhibitor 1H‐(1,2,4)oxadiozolo(4,3‐a)quinoxalin‐1‐one. Human BKCa channels, transferred to Chinese hamster ovary cells via an adenoviral vector, and endogenous rat clitoral smooth muscle K+ current are activated by this PKG‐dependent mechanism. Laser confocal microscopy reveals protein expression of BKCa channels on clitoral smooth muscle cells; these cells exhibit BKCa channel activity that is activated by both DEANO and sildenafil. We conclude that neurovascular derived NO causes clitoral relaxation via a PKG‐dependent activation of BKCa channels. The BKCa channel is an appealing target for drug therapy of female erectile dysfunction.— Gragasin, F. S., Michelakis, E. D., Hogan, A., Moudgil, R., Hashimoto, K., Wu, X., Bonnet, S., Haromy, A., Archer, S. L. The neurovascular mechanism of clitoral erection: nitric oxide and cGMP‐stimulated activation of BKCa channels. FASEB J. 18, 1382‐1391 (2004)</description><subject>Animals</subject><subject>Calcium - metabolism</subject><subject>CHO Cells</subject><subject>Clitoris - anatomy & histology</subject><subject>Clitoris - blood supply</subject><subject>Clitoris - innervation</subject><subject>Clitoris - physiology</subject><subject>Cricetinae</subject><subject>Cyclic GMP - metabolism</subject><subject>Cyclic GMP-Dependent Protein Kinases - metabolism</subject><subject>Electric Stimulation</subject><subject>electrical field stimulation</subject><subject>Electrophysiology</subject><subject>Female</subject><subject>Humans</subject><subject>Immunohistochemistry</subject><subject>In Vitro Techniques</subject><subject>Large-Conductance Calcium-Activated Potassium Channels</subject><subject>laser capture microdissection</subject><subject>Lasers</subject><subject>Microdissection</subject><subject>Muscle Relaxation - drug effects</subject><subject>Muscle, Smooth - blood supply</subject><subject>Muscle, Smooth - drug effects</subject><subject>Muscle, Smooth - innervation</subject><subject>Muscle, Smooth - physiology</subject><subject>Nitric Oxide - biosynthesis</subject><subject>Nitric Oxide - metabolism</subject><subject>nitric oxide electrode</subject><subject>phosphodiesterase 5</subject><subject>Piperazines - pharmacology</subject><subject>Potassium Channels, Calcium-Activated - genetics</subject><subject>Potassium Channels, Calcium-Activated - metabolism</subject><subject>protein kinase G</subject><subject>Purines</subject><subject>Rats</subject><subject>Rats, Sprague-Dawley</subject><subject>Signal Transduction - drug effects</subject><subject>sildenafil</subject><subject>Sildenafil Citrate</subject><subject>Sulfones</subject><issn>0892-6638</issn><issn>1530-6860</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2004</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpFkb1OwzAUhS0EglIYWZEntsCN4zgJG1SUv1ZFAmbLtW9UV0lc4qTQjUfgGXkSElHEdHV0Pn3DPYSchHAeQiYu8uU58CDMklS7cocMwjiCQKQCdskA0owFQkTpATn0fgkAIYRinxx0UBTFaTggq5cF0grb2q2V122halqiXqjK-pK6nOrCNq5WBcUadWNddUkr29RWU_dhDVJVGapvp0_fn1--sWUnaNBQ1aFr1eO94_pxpGjvrLDwR2QvV4XH4-0dktfxzcvoLpjMbu9HV5NgwTKYBsqYiGfIskwDsCQWc5PERicaNWdiHs77FoViueIJS3iUMGQ8UxwTg8AwGpKzX--qdm8t-kaW1mssClWha70UImVxzNMOPN2C7bxEI1e1LVW9kX8_6oDLX-DdFrj570H2A8h8KYHL7QBy_HzNxg_A-zyaTaMfxZx9ag</recordid><startdate>200409</startdate><enddate>200409</enddate><creator>Gragasin, Ferrante S.</creator><creator>Michelakis, Evangelos D.</creator><creator>Hogan, Angie</creator><creator>Moudgil, Rohit</creator><creator>Hashimoto, Kyoko</creator><creator>Wu, Xichen</creator><creator>Bonnet, Sandra</creator><creator>Haromy, Al</creator><creator>Archer, Stephen L.</creator><general>Federation of American Societies for Experimental Biology</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>7X8</scope></search><sort><creationdate>200409</creationdate><title>The neurovascular mechanism of clitoral erection: nitric oxide and cGMP‐stimulated activation of BKCa channels</title><author>Gragasin, Ferrante S. ; Michelakis, Evangelos D. ; Hogan, Angie ; Moudgil, Rohit ; Hashimoto, Kyoko ; Wu, Xichen ; Bonnet, Sandra ; Haromy, Al ; Archer, Stephen L.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-h290M-add349e299c002756bd75dc7cec426b1b349ee6a2fa47274372e249a4e7de02e3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2004</creationdate><topic>Animals</topic><topic>Calcium - metabolism</topic><topic>CHO Cells</topic><topic>Clitoris - anatomy & histology</topic><topic>Clitoris - blood supply</topic><topic>Clitoris - innervation</topic><topic>Clitoris - physiology</topic><topic>Cricetinae</topic><topic>Cyclic GMP - metabolism</topic><topic>Cyclic GMP-Dependent Protein Kinases - metabolism</topic><topic>Electric Stimulation</topic><topic>electrical field stimulation</topic><topic>Electrophysiology</topic><topic>Female</topic><topic>Humans</topic><topic>Immunohistochemistry</topic><topic>In Vitro Techniques</topic><topic>Large-Conductance Calcium-Activated Potassium Channels</topic><topic>laser capture microdissection</topic><topic>Lasers</topic><topic>Microdissection</topic><topic>Muscle Relaxation - drug effects</topic><topic>Muscle, Smooth - blood supply</topic><topic>Muscle, Smooth - drug effects</topic><topic>Muscle, Smooth - innervation</topic><topic>Muscle, Smooth - physiology</topic><topic>Nitric Oxide - biosynthesis</topic><topic>Nitric Oxide - metabolism</topic><topic>nitric oxide electrode</topic><topic>phosphodiesterase 5</topic><topic>Piperazines - pharmacology</topic><topic>Potassium Channels, Calcium-Activated - genetics</topic><topic>Potassium Channels, Calcium-Activated - metabolism</topic><topic>protein kinase G</topic><topic>Purines</topic><topic>Rats</topic><topic>Rats, Sprague-Dawley</topic><topic>Signal Transduction - drug effects</topic><topic>sildenafil</topic><topic>Sildenafil Citrate</topic><topic>Sulfones</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Gragasin, Ferrante S.</creatorcontrib><creatorcontrib>Michelakis, Evangelos D.</creatorcontrib><creatorcontrib>Hogan, Angie</creatorcontrib><creatorcontrib>Moudgil, Rohit</creatorcontrib><creatorcontrib>Hashimoto, Kyoko</creatorcontrib><creatorcontrib>Wu, Xichen</creatorcontrib><creatorcontrib>Bonnet, Sandra</creatorcontrib><creatorcontrib>Haromy, Al</creatorcontrib><creatorcontrib>Archer, Stephen L.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>MEDLINE - Academic</collection><jtitle>The FASEB journal</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Gragasin, Ferrante S.</au><au>Michelakis, Evangelos D.</au><au>Hogan, Angie</au><au>Moudgil, Rohit</au><au>Hashimoto, Kyoko</au><au>Wu, Xichen</au><au>Bonnet, Sandra</au><au>Haromy, Al</au><au>Archer, Stephen L.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>The neurovascular mechanism of clitoral erection: nitric oxide and cGMP‐stimulated activation of BKCa channels</atitle><jtitle>The FASEB journal</jtitle><addtitle>FASEB J</addtitle><date>2004-09</date><risdate>2004</risdate><volume>18</volume><issue>12</issue><spage>1382</spage><epage>1391</epage><pages>1382-1391</pages><issn>0892-6638</issn><eissn>1530-6860</eissn><abstract>Female sexual function is under‐studied, and mechanisms of clitoral engorgement‐relaxation are incompletely understood. Penile erection results from nitric oxide (NO) ‐induced cyclic guanosine monophosphate (cGMP) accumulation. cGMP‐dependent protein kinase (PKG) activates large‐conductance, calcium‐activated potassium channels (BKCa), thereby hyperpolarizing and relaxing vascular and trabecular smooth muscle cells, allowing engorgement. We hypothesize rat clitorises relax by a similar mechanism. Rat clitorises express components of the proposed pathway: neuronal and endothelial NO synthases, soluble guanylyl cyclase (sGC), type 5 phosphodiesterase (PDE‐5), and BKCa channels. The NO donor diethylamine NONOate (DEANO), the PKG activator 8‐pCPT‐cGMP, and the PDE‐5 inhibitor sildenafil, cause dose‐dependent clitoral relaxation that is inhibited by antagonists of PKG (Rp‐8‐Br‐cGMPS) or BKCa channels (iberiotoxin). Electrical field stimulation induces tetrodotoxin‐sensitive NO release and relaxation that is inhibited by the Na+ channel blocker tetrodotoxin or sGC inhibitor 1H‐(1,2,4)oxadiozolo(4,3‐a)quinoxalin‐1‐one. Human BKCa channels, transferred to Chinese hamster ovary cells via an adenoviral vector, and endogenous rat clitoral smooth muscle K+ current are activated by this PKG‐dependent mechanism. Laser confocal microscopy reveals protein expression of BKCa channels on clitoral smooth muscle cells; these cells exhibit BKCa channel activity that is activated by both DEANO and sildenafil. We conclude that neurovascular derived NO causes clitoral relaxation via a PKG‐dependent activation of BKCa channels. The BKCa channel is an appealing target for drug therapy of female erectile dysfunction.— Gragasin, F. S., Michelakis, E. D., Hogan, A., Moudgil, R., Hashimoto, K., Wu, X., Bonnet, S., Haromy, A., Archer, S. L. The neurovascular mechanism of clitoral erection: nitric oxide and cGMP‐stimulated activation of BKCa channels. FASEB J. 18, 1382‐1391 (2004)</abstract><cop>United States</cop><pub>Federation of American Societies for Experimental Biology</pub><pmid>15333581</pmid><doi>10.1096/fj.04-1978com</doi><tpages>10</tpages></addata></record> |
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| subjects | Animals Calcium - metabolism CHO Cells Clitoris - anatomy & histology Clitoris - blood supply Clitoris - innervation Clitoris - physiology Cricetinae Cyclic GMP - metabolism Cyclic GMP-Dependent Protein Kinases - metabolism Electric Stimulation electrical field stimulation Electrophysiology Female Humans Immunohistochemistry In Vitro Techniques Large-Conductance Calcium-Activated Potassium Channels laser capture microdissection Lasers Microdissection Muscle Relaxation - drug effects Muscle, Smooth - blood supply Muscle, Smooth - drug effects Muscle, Smooth - innervation Muscle, Smooth - physiology Nitric Oxide - biosynthesis Nitric Oxide - metabolism nitric oxide electrode phosphodiesterase 5 Piperazines - pharmacology Potassium Channels, Calcium-Activated - genetics Potassium Channels, Calcium-Activated - metabolism protein kinase G Purines Rats Rats, Sprague-Dawley Signal Transduction - drug effects sildenafil Sildenafil Citrate Sulfones |
| title | The neurovascular mechanism of clitoral erection: nitric oxide and cGMP‐stimulated activation of BKCa channels |
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