Seasonal variation of NGF in seminal plasma and expression of NGF and its cognate receptors NTRK1 and p75NTR in the sex organs of rams

•NGF system presence and gene expression were studied in the ram genital organs.•NGF was measured in seminal plasma to correlate it with ram reproductive seasonality.•NGF, NTRK1 and p75NTR mRNA and protein were detected in all male organs examined.•All gene transcripts were higher in the seminal ves...

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Veröffentlicht in:Domestic animal endocrinology 2024-10, Vol.89, p.106877, Article 106877
Hauptverfasser: Mercati, Francesca, Guelfi, Gabriella, Martí, José Ignacio, Dall'Aglio, Cecilia, Calleja, Lucía, Caivano, Domenico, Marenzoni, Maria Luisa, Capaccia, Camilla, Anipchenko, Polina, Palermo, Francesco Alessandro, Cocci, Paolo, Rende, Mario, Zerani, Massimo, Maranesi, Margherita
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container_title Domestic animal endocrinology
container_volume 89
creator Mercati, Francesca
Guelfi, Gabriella
Martí, José Ignacio
Dall'Aglio, Cecilia
Calleja, Lucía
Caivano, Domenico
Marenzoni, Maria Luisa
Capaccia, Camilla
Anipchenko, Polina
Palermo, Francesco Alessandro
Cocci, Paolo
Rende, Mario
Zerani, Massimo
Maranesi, Margherita
description •NGF system presence and gene expression were studied in the ram genital organs.•NGF was measured in seminal plasma to correlate it with ram reproductive seasonality.•NGF, NTRK1 and p75NTR mRNA and protein were detected in all male organs examined.•All gene transcripts were higher in the seminal vesicles than in other organs.•The concentration of the NGF seminal plasma was greater from January to May. Nerve growth factor (NGF) has long been known as the main ovulation-inducing factor in induced ovulation species, however, recent studies suggested the NGF role also in those with spontaneous ovulation. The first aim of this study was to evaluate the presence and gene expression of NGF and its cognate receptors, high-affinity neurotrophic tyrosine kinase 1 receptor (NTRK1) and low-affinity p75 nerve growth factor receptor (p75NTR), in the ram genital tract. Moreover, the annual trend of NGF seminal plasma values was investigated to evaluate the possible relationship between the NGF production variations and the ram reproductive seasonality. The presence and expression of the NGF/receptors system was evaluated in the testis, epididymis, vas deferens ampullae, seminal vesicles, prostate, and bulbourethral glands through immunohistochemistry and real-time PCR (qPCR), respectively. Genital tract samples were collected from 5 adult rams, regularly slaughtered at a local abattoir. Semen was collected during the whole year weekly, from 5 different adult rams, reared in a breeding facility, with an artificial vagina. NGF seminal plasma values were assessed through the ELISA method. NGF, NTRK1 and p75NTR immunoreactivity was detected in all male organs examined. NGF-positive immunostaining was observed in the spermatozoa of the germinal epithelium, in the epididymis and the cells of the secretory epithelium of annexed glands, NTRK1 receptor showed a localization pattern like that of NGF, whereas p75NTR immunopositivity was localized in the nerve fibers and ganglia. NGF gene transcript was highest (p < 0.01) in the seminal vesicles and lowest (p < 0.01) in the testis than in the other tissues. NTRK1 gene transcript was highest (p < 0.01) in the seminal vesicles and lowest (p < 0.05) in all the other tissues examined. Gene expression of p75NTR was highest (p < 0.01) in the seminal vesicles and lowest (p < 0.01) in the testis and bulbourethral glands. NGF seminal plasma concentration was greater from January to May (p < 0.01) than in the other months. This study highligh
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Nerve growth factor (NGF) has long been known as the main ovulation-inducing factor in induced ovulation species, however, recent studies suggested the NGF role also in those with spontaneous ovulation. The first aim of this study was to evaluate the presence and gene expression of NGF and its cognate receptors, high-affinity neurotrophic tyrosine kinase 1 receptor (NTRK1) and low-affinity p75 nerve growth factor receptor (p75NTR), in the ram genital tract. Moreover, the annual trend of NGF seminal plasma values was investigated to evaluate the possible relationship between the NGF production variations and the ram reproductive seasonality. The presence and expression of the NGF/receptors system was evaluated in the testis, epididymis, vas deferens ampullae, seminal vesicles, prostate, and bulbourethral glands through immunohistochemistry and real-time PCR (qPCR), respectively. Genital tract samples were collected from 5 adult rams, regularly slaughtered at a local abattoir. Semen was collected during the whole year weekly, from 5 different adult rams, reared in a breeding facility, with an artificial vagina. NGF seminal plasma values were assessed through the ELISA method. NGF, NTRK1 and p75NTR immunoreactivity was detected in all male organs examined. NGF-positive immunostaining was observed in the spermatozoa of the germinal epithelium, in the epididymis and the cells of the secretory epithelium of annexed glands, NTRK1 receptor showed a localization pattern like that of NGF, whereas p75NTR immunopositivity was localized in the nerve fibers and ganglia. NGF gene transcript was highest (p < 0.01) in the seminal vesicles and lowest (p < 0.01) in the testis than in the other tissues. NTRK1 gene transcript was highest (p < 0.01) in the seminal vesicles and lowest (p < 0.05) in all the other tissues examined. Gene expression of p75NTR was highest (p < 0.01) in the seminal vesicles and lowest (p < 0.01) in the testis and bulbourethral glands. NGF seminal plasma concentration was greater from January to May (p < 0.01) than in the other months. This study highlighted that the NGF system was expressed in the tissues of all the different genital tracts examined, confirming the role of NGF in ram reproduction. Sheep are short-day breeders, with an anestrus that corresponds to the highest seminal plasma NGF levels, thus suggesting the intriguing idea that this factor could participate in an inhibitory mechanism of male reproductive activity, activated during the female anestrus.]]></description><identifier>ISSN: 0739-7240</identifier><identifier>ISSN: 1879-0054</identifier><identifier>EISSN: 1879-0054</identifier><identifier>DOI: 10.1016/j.domaniend.2024.106877</identifier><identifier>PMID: 39068905</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Accessory sex glands ; Animals ; Ewe ; Gene Expression Regulation - physiology ; Genitalia, Male - chemistry ; Genitalia, Male - metabolism ; Male ; Nerve Growth Factor - genetics ; Nerve Growth Factor - metabolism ; Ovulation ; Ovulation inducing factor ; Receptor, Nerve Growth Factor - genetics ; Receptor, Nerve Growth Factor - metabolism ; Receptor, trkA - genetics ; Receptor, trkA - metabolism ; Seasons ; Semen - chemistry ; Semen - metabolism ; Seminal plasma ; Sheep ; Sheep - metabolism</subject><ispartof>Domestic animal endocrinology, 2024-10, Vol.89, p.106877, Article 106877</ispartof><rights>2024 The Authors</rights><rights>Copyright © 2024 The Authors. Published by Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c296t-be7e3c2ca63633096d3a95045a288f0b64b9d522ee2ddf22ccea65f6ee8fbf823</cites><orcidid>0000-0001-6451-3751</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.domaniend.2024.106877$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>315,781,785,3551,27926,27927,45997</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39068905$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Mercati, Francesca</creatorcontrib><creatorcontrib>Guelfi, Gabriella</creatorcontrib><creatorcontrib>Martí, José Ignacio</creatorcontrib><creatorcontrib>Dall'Aglio, Cecilia</creatorcontrib><creatorcontrib>Calleja, Lucía</creatorcontrib><creatorcontrib>Caivano, Domenico</creatorcontrib><creatorcontrib>Marenzoni, Maria Luisa</creatorcontrib><creatorcontrib>Capaccia, Camilla</creatorcontrib><creatorcontrib>Anipchenko, Polina</creatorcontrib><creatorcontrib>Palermo, Francesco Alessandro</creatorcontrib><creatorcontrib>Cocci, Paolo</creatorcontrib><creatorcontrib>Rende, Mario</creatorcontrib><creatorcontrib>Zerani, Massimo</creatorcontrib><creatorcontrib>Maranesi, Margherita</creatorcontrib><title>Seasonal variation of NGF in seminal plasma and expression of NGF and its cognate receptors NTRK1 and p75NTR in the sex organs of rams</title><title>Domestic animal endocrinology</title><addtitle>Domest Anim Endocrinol</addtitle><description><![CDATA[•NGF system presence and gene expression were studied in the ram genital organs.•NGF was measured in seminal plasma to correlate it with ram reproductive seasonality.•NGF, NTRK1 and p75NTR mRNA and protein were detected in all male organs examined.•All gene transcripts were higher in the seminal vesicles than in other organs.•The concentration of the NGF seminal plasma was greater from January to May. Nerve growth factor (NGF) has long been known as the main ovulation-inducing factor in induced ovulation species, however, recent studies suggested the NGF role also in those with spontaneous ovulation. The first aim of this study was to evaluate the presence and gene expression of NGF and its cognate receptors, high-affinity neurotrophic tyrosine kinase 1 receptor (NTRK1) and low-affinity p75 nerve growth factor receptor (p75NTR), in the ram genital tract. Moreover, the annual trend of NGF seminal plasma values was investigated to evaluate the possible relationship between the NGF production variations and the ram reproductive seasonality. The presence and expression of the NGF/receptors system was evaluated in the testis, epididymis, vas deferens ampullae, seminal vesicles, prostate, and bulbourethral glands through immunohistochemistry and real-time PCR (qPCR), respectively. Genital tract samples were collected from 5 adult rams, regularly slaughtered at a local abattoir. Semen was collected during the whole year weekly, from 5 different adult rams, reared in a breeding facility, with an artificial vagina. NGF seminal plasma values were assessed through the ELISA method. NGF, NTRK1 and p75NTR immunoreactivity was detected in all male organs examined. NGF-positive immunostaining was observed in the spermatozoa of the germinal epithelium, in the epididymis and the cells of the secretory epithelium of annexed glands, NTRK1 receptor showed a localization pattern like that of NGF, whereas p75NTR immunopositivity was localized in the nerve fibers and ganglia. NGF gene transcript was highest (p < 0.01) in the seminal vesicles and lowest (p < 0.01) in the testis than in the other tissues. NTRK1 gene transcript was highest (p < 0.01) in the seminal vesicles and lowest (p < 0.05) in all the other tissues examined. Gene expression of p75NTR was highest (p < 0.01) in the seminal vesicles and lowest (p < 0.01) in the testis and bulbourethral glands. NGF seminal plasma concentration was greater from January to May (p < 0.01) than in the other months. This study highlighted that the NGF system was expressed in the tissues of all the different genital tracts examined, confirming the role of NGF in ram reproduction. Sheep are short-day breeders, with an anestrus that corresponds to the highest seminal plasma NGF levels, thus suggesting the intriguing idea that this factor could participate in an inhibitory mechanism of male reproductive activity, activated during the female anestrus.]]></description><subject>Accessory sex glands</subject><subject>Animals</subject><subject>Ewe</subject><subject>Gene Expression Regulation - physiology</subject><subject>Genitalia, Male - chemistry</subject><subject>Genitalia, Male - metabolism</subject><subject>Male</subject><subject>Nerve Growth Factor - genetics</subject><subject>Nerve Growth Factor - metabolism</subject><subject>Ovulation</subject><subject>Ovulation inducing factor</subject><subject>Receptor, Nerve Growth Factor - genetics</subject><subject>Receptor, Nerve Growth Factor - metabolism</subject><subject>Receptor, trkA - genetics</subject><subject>Receptor, trkA - metabolism</subject><subject>Seasons</subject><subject>Semen - chemistry</subject><subject>Semen - metabolism</subject><subject>Seminal plasma</subject><subject>Sheep</subject><subject>Sheep - metabolism</subject><issn>0739-7240</issn><issn>1879-0054</issn><issn>1879-0054</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkcFu1DAQhi0EokvhFcBHLlkcO7GdY1XRgqiKRMvZcuxJ8SqxgydblRfguet0S9UbJ8sz__-NZn5CPtRsW7NaftptfZpsDBD9ljPelKrUSr0gm1qrrmKsbV6SDVOiqxRv2BF5g7hjjKnifk2ORFfkHWs35O8VWEzRjvTW5mCXkCJNA708P6MhUoQprL15tDhZaqOncDdnQHymW6thQerSTbQL0AwO5iVlpJfXP77VD_1ZteWzIpdfULB3NOUbG3FlZDvhW_JqsCPCu8f3mPw8-3x9-qW6-H7-9fTkonK8k0vVgwLhuLNSSCFYJ72wXcua1nKtB9bLpu98yzkA937g3Dmwsh0kgB76QXNxTD4euHNOv_eAi5kCOhhHGyHt0QimW6llXesiVQepywkxw2DmHCab_5iamTUEszNPIZg1BHMIoTjfPw7Z9xP4J9-_qxfByUEAZdXbANmgKxQHPpTjLQUb_jvkHtQjnN8</recordid><startdate>202410</startdate><enddate>202410</enddate><creator>Mercati, Francesca</creator><creator>Guelfi, Gabriella</creator><creator>Martí, José Ignacio</creator><creator>Dall'Aglio, Cecilia</creator><creator>Calleja, Lucía</creator><creator>Caivano, Domenico</creator><creator>Marenzoni, Maria Luisa</creator><creator>Capaccia, Camilla</creator><creator>Anipchenko, Polina</creator><creator>Palermo, Francesco Alessandro</creator><creator>Cocci, Paolo</creator><creator>Rende, Mario</creator><creator>Zerani, Massimo</creator><creator>Maranesi, Margherita</creator><general>Elsevier Inc</general><scope>6I.</scope><scope>AAFTH</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><orcidid>https://orcid.org/0000-0001-6451-3751</orcidid></search><sort><creationdate>202410</creationdate><title>Seasonal variation of NGF in seminal plasma and expression of NGF and its cognate receptors NTRK1 and p75NTR in the sex organs of rams</title><author>Mercati, Francesca ; Guelfi, Gabriella ; Martí, José Ignacio ; Dall'Aglio, Cecilia ; Calleja, Lucía ; Caivano, Domenico ; Marenzoni, Maria Luisa ; Capaccia, Camilla ; Anipchenko, Polina ; Palermo, Francesco Alessandro ; Cocci, Paolo ; Rende, Mario ; Zerani, Massimo ; Maranesi, Margherita</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c296t-be7e3c2ca63633096d3a95045a288f0b64b9d522ee2ddf22ccea65f6ee8fbf823</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Accessory sex glands</topic><topic>Animals</topic><topic>Ewe</topic><topic>Gene Expression Regulation - physiology</topic><topic>Genitalia, Male - chemistry</topic><topic>Genitalia, Male - metabolism</topic><topic>Male</topic><topic>Nerve Growth Factor - genetics</topic><topic>Nerve Growth Factor - metabolism</topic><topic>Ovulation</topic><topic>Ovulation inducing factor</topic><topic>Receptor, Nerve Growth Factor - genetics</topic><topic>Receptor, Nerve Growth Factor - metabolism</topic><topic>Receptor, trkA - genetics</topic><topic>Receptor, trkA - metabolism</topic><topic>Seasons</topic><topic>Semen - chemistry</topic><topic>Semen - metabolism</topic><topic>Seminal plasma</topic><topic>Sheep</topic><topic>Sheep - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Mercati, Francesca</creatorcontrib><creatorcontrib>Guelfi, Gabriella</creatorcontrib><creatorcontrib>Martí, José Ignacio</creatorcontrib><creatorcontrib>Dall'Aglio, Cecilia</creatorcontrib><creatorcontrib>Calleja, Lucía</creatorcontrib><creatorcontrib>Caivano, Domenico</creatorcontrib><creatorcontrib>Marenzoni, Maria Luisa</creatorcontrib><creatorcontrib>Capaccia, Camilla</creatorcontrib><creatorcontrib>Anipchenko, Polina</creatorcontrib><creatorcontrib>Palermo, Francesco Alessandro</creatorcontrib><creatorcontrib>Cocci, Paolo</creatorcontrib><creatorcontrib>Rende, Mario</creatorcontrib><creatorcontrib>Zerani, Massimo</creatorcontrib><creatorcontrib>Maranesi, Margherita</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</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>Domestic animal endocrinology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Mercati, Francesca</au><au>Guelfi, Gabriella</au><au>Martí, José Ignacio</au><au>Dall'Aglio, Cecilia</au><au>Calleja, Lucía</au><au>Caivano, Domenico</au><au>Marenzoni, Maria Luisa</au><au>Capaccia, Camilla</au><au>Anipchenko, Polina</au><au>Palermo, Francesco Alessandro</au><au>Cocci, Paolo</au><au>Rende, Mario</au><au>Zerani, Massimo</au><au>Maranesi, Margherita</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Seasonal variation of NGF in seminal plasma and expression of NGF and its cognate receptors NTRK1 and p75NTR in the sex organs of rams</atitle><jtitle>Domestic animal endocrinology</jtitle><addtitle>Domest Anim Endocrinol</addtitle><date>2024-10</date><risdate>2024</risdate><volume>89</volume><spage>106877</spage><pages>106877-</pages><artnum>106877</artnum><issn>0739-7240</issn><issn>1879-0054</issn><eissn>1879-0054</eissn><abstract><![CDATA[•NGF system presence and gene expression were studied in the ram genital organs.•NGF was measured in seminal plasma to correlate it with ram reproductive seasonality.•NGF, NTRK1 and p75NTR mRNA and protein were detected in all male organs examined.•All gene transcripts were higher in the seminal vesicles than in other organs.•The concentration of the NGF seminal plasma was greater from January to May. Nerve growth factor (NGF) has long been known as the main ovulation-inducing factor in induced ovulation species, however, recent studies suggested the NGF role also in those with spontaneous ovulation. The first aim of this study was to evaluate the presence and gene expression of NGF and its cognate receptors, high-affinity neurotrophic tyrosine kinase 1 receptor (NTRK1) and low-affinity p75 nerve growth factor receptor (p75NTR), in the ram genital tract. Moreover, the annual trend of NGF seminal plasma values was investigated to evaluate the possible relationship between the NGF production variations and the ram reproductive seasonality. The presence and expression of the NGF/receptors system was evaluated in the testis, epididymis, vas deferens ampullae, seminal vesicles, prostate, and bulbourethral glands through immunohistochemistry and real-time PCR (qPCR), respectively. Genital tract samples were collected from 5 adult rams, regularly slaughtered at a local abattoir. Semen was collected during the whole year weekly, from 5 different adult rams, reared in a breeding facility, with an artificial vagina. NGF seminal plasma values were assessed through the ELISA method. NGF, NTRK1 and p75NTR immunoreactivity was detected in all male organs examined. NGF-positive immunostaining was observed in the spermatozoa of the germinal epithelium, in the epididymis and the cells of the secretory epithelium of annexed glands, NTRK1 receptor showed a localization pattern like that of NGF, whereas p75NTR immunopositivity was localized in the nerve fibers and ganglia. NGF gene transcript was highest (p < 0.01) in the seminal vesicles and lowest (p < 0.01) in the testis than in the other tissues. NTRK1 gene transcript was highest (p < 0.01) in the seminal vesicles and lowest (p < 0.05) in all the other tissues examined. Gene expression of p75NTR was highest (p < 0.01) in the seminal vesicles and lowest (p < 0.01) in the testis and bulbourethral glands. NGF seminal plasma concentration was greater from January to May (p < 0.01) than in the other months. This study highlighted that the NGF system was expressed in the tissues of all the different genital tracts examined, confirming the role of NGF in ram reproduction. Sheep are short-day breeders, with an anestrus that corresponds to the highest seminal plasma NGF levels, thus suggesting the intriguing idea that this factor could participate in an inhibitory mechanism of male reproductive activity, activated during the female anestrus.]]></abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>39068905</pmid><doi>10.1016/j.domaniend.2024.106877</doi><orcidid>https://orcid.org/0000-0001-6451-3751</orcidid><oa>free_for_read</oa></addata></record>
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subjects Accessory sex glands
Animals
Ewe
Gene Expression Regulation - physiology
Genitalia, Male - chemistry
Genitalia, Male - metabolism
Male
Nerve Growth Factor - genetics
Nerve Growth Factor - metabolism
Ovulation
Ovulation inducing factor
Receptor, Nerve Growth Factor - genetics
Receptor, Nerve Growth Factor - metabolism
Receptor, trkA - genetics
Receptor, trkA - metabolism
Seasons
Semen - chemistry
Semen - metabolism
Seminal plasma
Sheep
Sheep - metabolism
title Seasonal variation of NGF in seminal plasma and expression of NGF and its cognate receptors NTRK1 and p75NTR in the sex organs of rams
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