{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,20]],"date-time":"2026-07-20T14:20:54Z","timestamp":1784557254244,"version":"3.55.0"},"reference-count":114,"publisher":"Bioscientifica","issue":"1","content-domain":{"domain":["joe.bioscientifica.com"],"crossmark-restriction":true},"short-container-title":[],"published-print":{"date-parts":[[2018,7]]},"abstract":"\n Polycystic ovarian syndrome (PCOS) is a low-grade inflammatory disease characterized by hyperandrogenism and ovarian hyperinnervation. The aim of this work is to investigate whether\n in vivo<\/jats:italic>\n bilateral superior ovarian nerve (SON) section in adult rats with estradiol valerate-induced PCOS (PCO rats) affects macrophage spleen cells (M\u0424) and modifies the steroidogenic ability of their secretions. Culture media of M\u0424 from PCO rats and PCO rats with SON section (PCO-SON rats) were used to stimulate\n in vitro<\/jats:italic>\n intact ovaries. Compared with macrophages PCO, macrophages from PCO-SON rats released less tumor necrosis factor-\u03b1 and nitric oxide, expressed lower\n Bax<\/jats:italic>\n and\n Nfkb<\/jats:italic>\n mRNA and showed reduced TUNEL staining. Also, in PCO rats, the SON section decreased kisspeptin and nerve growth factor mRNA expressions, without changes in\n Trka<\/jats:italic>\n receptor mRNA levels. Macrophage secretions from PCO-SON rats decreased androstenedione and stimulated progesterone release in PCO ovaries, compared to macrophage secretions from PCO rats. No changes were observed in ovarian estradiol response. These findings emphasize the importance of the SON in spleen M\u03a6, since its manipulation leads to secondary modifications of immunological and neural mediators, which might influence ovarian steroidogenesis. In PCO ovaries, the reduction of androstenedione and the improvement of progesterone release induced by PCO-SON M\u03a6 secretion, might be beneficial considering the hormonal anomalies characteristic of PCOS. We present functional evidence that modulation of the immune-endocrine function by peripheral sympathetic nervous system might have implications for understanding the pathophysiology of PCOS.\n <\/jats:p>","DOI":"10.1530\/joe-17-0736","type":"journal-article","created":{"date-parts":[[2018,5,2]],"date-time":"2018-05-02T07:50:13Z","timestamp":1525247413000},"page":"33-45","update-policy":"https:\/\/doi.org\/10.1530\/crossmarkpolicy-5","source":"Crossref","is-referenced-by-count":10,"title":["Sympathetic innervation regulates macrophage activity in rats with polycystic ovary"],"prefix":"10.1530","volume":"238","author":[{"given":"Florencia","family":"Figueroa","sequence":"first","affiliation":[{"name":"1Laboratorio de Biolog\u00eda de la Reproducci\u00f3n, Facultad de Qu\u00edmica, Bioqu\u00edmica y Farmacia, Universidad Nacional de San Luis, San Luis, Argentina"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gisela","family":"Mendoza","sequence":"additional","affiliation":[{"name":"1Laboratorio de Biolog\u00eda de la Reproducci\u00f3n, Facultad de Qu\u00edmica, Bioqu\u00edmica y Farmacia, Universidad Nacional de San Luis, San Luis, Argentina"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dar\u00edo","family":"Cardozo","sequence":"additional","affiliation":[{"name":"1Laboratorio de Biolog\u00eda de la Reproducci\u00f3n, Facultad de Qu\u00edmica, Bioqu\u00edmica y Farmacia, Universidad Nacional de San Luis, San Luis, Argentina"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fabi\u00e1n","family":"Mohamed","sequence":"additional","affiliation":[{"name":"2Area Morfolog\u00eda, Facultad de Qu\u00edmica, Bioqu\u00edmica y Farmacia, Universidad Nacional de San Luis, San Luis, Argentina"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Liliana","family":"Oliveros","sequence":"additional","affiliation":[{"name":"1Laboratorio de Biolog\u00eda de la Reproducci\u00f3n, Facultad de Qu\u00edmica, Bioqu\u00edmica y Farmacia, Universidad Nacional de San Luis, San Luis, Argentina"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Myriam","family":"Forneris","sequence":"additional","affiliation":[{"name":"1Laboratorio de Biolog\u00eda de la Reproducci\u00f3n, Facultad de Qu\u00edmica, Bioqu\u00edmica y Farmacia, Universidad Nacional de San Luis, San Luis, Argentina"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"416","reference":[{"key":"ref331","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1186\/1477-7827-8-99","article-title":"Unilateral sectioning of the superior ovarian nerve of rats with polycystic ovarian syndrome restores ovulation in the innervated ovary","volume":"8","year":"2010","journal-title":"Reproductive Biology and Endocrinology"},{"key":"ref671","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1530\/JOE-15-0538","article-title":"Kisspeptin across the human lifespan: evidence from animal studies and beyond","volume":"229","year":"2016","journal-title":"Journal of Endocrinology"},{"key":"ref131","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1530\/JOE-16-0181","article-title":"Kisspeptin level in the aging ovary is regulated by the sympathetic nervous system","volume":"232","year":"2017","journal-title":"Journal of Endocrinology"},{"key":"ref1071","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1002\/jnr.490170206","article-title":"Receptors for nerve growth factor on rat spleen mononuclear cells","volume":"17","year":"1987","journal-title":"Journal of Neuroscience Research"},{"key":"ref211","first-page":"520","article-title":"KiSS-1 in the mammalian ovary: distribution of kisspeptin in human and marmoset and alterations in KiSS-1 mRNA levels in a rat model of ovulatory dysfunction","volume":"296","year":"2009","journal-title":"American Journal of Physiology: Endocrinology and Metabolism"},{"key":"ref601","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1016\/0889-1591(89)90029-9","article-title":"Origin of noradrenergic innervations of the spleen in rats","volume":"3","year":"1989","journal-title":"Brain, Behavior, and Immunity"},{"key":"ref1051","doi-asserted-by":"crossref","first-page":"840","DOI":"10.1016\/j.fertnstert.2013.11.027","article-title":"Hyperandrogenemia is implicated in both the metabolic and reproductive morbidities of polycystic ovary syndrome","volume":"101","year":"2014","journal-title":"Fertility and Sterility"},{"key":"ref491","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1016\/j.cellsig.2006.06.007","article-title":"Beta2 adrenergic receptor activation stimulates pro-inflammatory cytokine production in macrophages via PKA- and NF-kappa B-independent mechanisms","volume":"19","year":"2007","journal-title":"Cellular Signalling"},{"key":"ref251","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1089\/ars.2005.7.395","article-title":"Redox regulation of NF-kappaB activation: distinct redox regulation between the cytoplasm and the nucleus","volume":"7","year":"2005","journal-title":"Antioxidants and Redox Signaling"},{"key":"ref661","doi-asserted-by":"crossref","first-page":"72","DOI":"10.1016\/j.ejogrb.2009.11.018","article-title":"Increased plasma metastin levels in adolescent women with polycystic ovary syndrome","volume":"149","year":"2010","journal-title":"European Journal of Obstetrics and Gynecology and Reproductive Biology"},{"key":"ref1091","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1038\/nrurol.2015.277","article-title":"Kisspeptin signalling in the physiology and pathophysiology of the urogenital system","volume":"13","year":"2016","journal-title":"Nature Reviews Urology"},{"key":"ref1011","doi-asserted-by":"crossref","first-page":"595","DOI":"10.1016\/S0008-6363(99)00395-8","article-title":"Tumor necrosis factor-alpha induces apoptosis via inducible nitric oxide synthase in neonatal mouse cardiomyocytes","volume":"45","year":"2000","journal-title":"Cardiovascular Research"},{"key":"ref811","doi-asserted-by":"crossref","first-page":"656","DOI":"10.1007\/BF03345620","article-title":"Decreased expression of kisspeptin mediates acute immune\/inflammatory stress-induced suppression of gonadotropin secretion in female rat","volume":"31","year":"2008","journal-title":"Journal of Endocrinological Investigation"},{"key":"ref21","doi-asserted-by":"crossref","first-page":"2696","DOI":"10.1210\/endo.133.6.8243293","article-title":"Ovarian steroidal response to gonadotropins and beta-adrenergic stimulation is enhanced in polycystic ovary syndrome: role of sympathetic innervations","volume":"133","year":"1993","journal-title":"Endocrinology"},{"key":"ref741","first-page":"1293","article-title":"Effect of secretion of splenocytes after superior ovarian nerve section on the ovarian steroidogenesis","volume":"6","year":"1999","journal-title":"Neuroimmunomodulation"},{"key":"ref201","doi-asserted-by":"crossref","first-page":"453","DOI":"10.1016\/j.ejphar.2004.07.044","article-title":"Nerve growth factor and its receptor in asthma and inflammation","volume":"500","year":"2004","journal-title":"European Journal of Pharmacology"},{"key":"ref61","doi-asserted-by":"crossref","first-page":"645","DOI":"10.1016\/j.freeradbiomed.2007.04.026","article-title":"Methods to detect nitric oxide and its metabolites in biological samples","volume":"43","year":"2007","journal-title":"Free Radical Biology and Medicine"},{"key":"ref41","doi-asserted-by":"crossref","first-page":"647","DOI":"10.1095\/biolreprod35.3.647","article-title":"Development of the polycystic ovarian condition (PCO) in the estradiol valerate-treated rat","volume":"35","year":"1986","journal-title":"Biology of Reproduction"},{"key":"ref691","first-page":"675","article-title":"\u03b2-Adrenergic agonists exert their \u2018anti-inflammatory\u2019 effects in monocytic cells through the I\u03baB\/NF-\u03baB pathway","volume":"279","year":"2000","journal-title":"American Journal of Physiology: Lung Cellular and Molecular Physiology"},{"key":"ref931","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1038\/nrm2083","article-title":"Integrating cell-signalling pathways with NF-kappa B and IKK function","volume":"8","year":"2007","journal-title":"Nature Reviews Molecular Cell Biology"},{"key":"ref441","doi-asserted-by":"crossref","first-page":"595","DOI":"10.1016\/S0008-6363(99)00395-8","article-title":"Tumor necrosis factor-alpha induces apoptosis via inducible nitric oxide synthase in neonatal mouse cardiomyocytes","volume":"45","year":"2000","journal-title":"Cardiovascular Research"},{"key":"ref901","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1186\/1477-7827-8-99","article-title":"Unilateral sectioning of the superior ovarian nerve of rats with polycystic ovarian syndrome restores ovulation in the innervated ovary","volume":"8","year":"2010","journal-title":"Reproductive Biology and Endocrinology"},{"key":"ref921","first-page":"35","article-title":"Secretion from neuropeptide treated splenocytes modifies ovarian steroidogenesis","volume":"61","year":"2001","journal-title":"Medicina"},{"key":"ref841","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1016\/S1642-431X(12)60015-1","article-title":"The influence of tumor necrosis factor alpha (TNF) on the secretory function of bovine corpus luteum: TNF and its receptors expression during the estrous cycle","volume":"8","year":"2008","journal-title":"Biology of Reproduction"},{"key":"ref31","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1016\/0889-1591(89)90029-9","article-title":"Origin of noradrenergic innervations of the spleen in rats","volume":"3","year":"1989","journal-title":"Brain, Behavior, and Immunity"},{"key":"ref721","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1530\/REP-15-0216","article-title":"Role of macrophage secretions on rat polycystic ovary: its effect on apoptosis","volume":"150","year":"2015","journal-title":"Reproduction"},{"key":"ref881","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1046\/j.1474-8673.2003.00280.x","article-title":"Autonomic innervation of immune organs and neuroimmune modulation","volume":"23","year":"2003","journal-title":"Autonomic and Autacoid Pharmacology"},{"key":"ref571","doi-asserted-by":"crossref","first-page":"462","DOI":"10.1002\/jemt.10232","article-title":"Role of the central and peripheral nervous system in the ovarian function.","volume":"59","year":"2002","journal-title":"Microscopy Research and Technique"},{"key":"ref381","doi-asserted-by":"crossref","first-page":"356","DOI":"10.1049\/iet-syb.2008.0172","article-title":"Crosstalk between p53 and nuclear factor-kB systems: pro- and anti-apoptotic functions of NF-kB","volume":"3","year":"2009","journal-title":"IET Systems Biology"},{"key":"ref511","first-page":"40","article-title":"Bidirectional communication between the neuroendocrine system and the immune system: relevance to health and diseases","volume":"19","year":"2012","journal-title":"Annals of Neurosciences"},{"key":"ref541","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1093\/humupd\/dmh011","article-title":"Macrophage contributions to ovarian functions","volume":"10","year":"2004","journal-title":"Human Reproduction Update"},{"key":"ref101","doi-asserted-by":"crossref","first-page":"83","DOI":"10.1530\/JOE-15-0538","article-title":"Kisspeptin across the human lifespan: evidence from animal studies and beyond","volume":"229","year":"2016","journal-title":"Journal of Endocrinology"},{"key":"ref121","first-page":"675","article-title":"\u03b2-Adrenergic agonists exert their \u2018anti-inflammatory\u2019 effects in monocytic cells through the I\u03baB\/NF-\u03baB pathway","volume":"279","year":"2000","journal-title":"American Journal of Physiology: Lung Cellular and Molecular Physiology"},{"key":"ref351","first-page":"35","article-title":"Secretion from neuropeptide treated splenocytes modifies ovarian steroidogenesis","volume":"61","year":"2001","journal-title":"Medicina"},{"key":"ref11","doi-asserted-by":"crossref","first-page":"1019","DOI":"10.1189\/jlb.69.6.1019","article-title":"Nerve growth factor regulates TNF-alpha production in mouse macrophages via MAP kinase activation","volume":"69","year":"2001","journal-title":"Journal of Leukocyte Biology"},{"key":"ref1111","doi-asserted-by":"crossref","first-page":"119","DOI":"10.1093\/humupd\/dmh011","article-title":"Macrophage contributions to ovarian functions","volume":"10","year":"2004","journal-title":"Human Reproduction Update"},{"key":"ref961","doi-asserted-by":"crossref","first-page":"4966","DOI":"10.1210\/en.2012-1279","article-title":"Evidence for a celiac ganglion-ovarian kisspeptin neural network in the rat: intraovarian anti-kisspeptin delays vaginal opening and alters estrous cyclicity","volume":"153","year":"2012","journal-title":"Endocrinology"},{"key":"ref651","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1016\/j.mce.2017.01.017","article-title":"Microparticles: inflammatory and haemostatic biomarkers in polycystic ovary syndrome","volume":"443","year":"2017","journal-title":"Molecular and Cellular Endocrinology"},{"key":"ref391","doi-asserted-by":"crossref","first-page":"4966","DOI":"10.1210\/en.2012-1279","article-title":"Evidence for a celiac ganglion-ovarian kisspeptin neural network in the rat: intraovarian anti-kisspeptin delays vaginal opening and alters estrous cyclicity","volume":"153","year":"2012","journal-title":"Endocrinology"},{"key":"ref641","first-page":"261","article-title":"The adrenergic innervation of mammalian ovaries","volume-title":"Catecholamines as Hormone Regulators","year":"1985"},{"key":"ref801","doi-asserted-by":"crossref","first-page":"26205","DOI":"10.1038\/srep26205","article-title":"Fractalkine restores the decreased expression of StAR and progesterone in granulosa cells from patients with polycystic ovary syndrome","volume":"6","year":"2016","journal-title":"Scientific Reports"},{"key":"ref911","doi-asserted-by":"crossref","first-page":"345","DOI":"10.1016\/j.tem.2011.04.005","article-title":"Pituitary-ovary-spleen axis in ovulation.","volume":"22","year":"2011","journal-title":"Trends in Endocrinology and Metabolism"},{"key":"ref561","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1016\/j.ejogrb.2013.09.026","article-title":"Effect of HSP10 on apoptosis induced by testosterone in cultured mouse ovarian granulose cells","volume":"171","year":"2013","journal-title":"European Journal of Obstetrics and Gynecology and Reproductive Biology"},{"key":"ref711","doi-asserted-by":"crossref","first-page":"733","DOI":"10.1016\/j.lfs.2012.03.019","article-title":"Macrophage secretions modulate the steroidogenesis of polycystic ovary in rats: Effect of testosterone on macrophage pro-inflammatory cytokines","volume":"90","year":"2012","journal-title":"Life Sciences"},{"key":"ref1131","doi-asserted-by":"crossref","first-page":"301","DOI":"10.1016\/j.ejogrb.2013.09.026","article-title":"Effect of HSP10 on apoptosis induced by testosterone in cultured mouse ovarian granulose cells","volume":"171","year":"2013","journal-title":"European Journal of Obstetrics and Gynecology and Reproductive Biology"},{"key":"ref261","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1016\/0304-3940(88)90354-0","article-title":"Anatomical localization of afferent and postganglionic sympathetic neurons innervating the rat ovary","volume":"85","year":"1988","journal-title":"Neuroscience Letters"},{"key":"ref291","doi-asserted-by":"crossref","first-page":"1907","DOI":"10.4049\/jimmunol.172.3.1907","article-title":"TNF-alpha-induced apoptosis of macrophages following inhibition of NF-kappa B: a central role for disruption of mitochondria","volume":"172","year":"2004","journal-title":"Journal of Immunology"},{"key":"ref631","doi-asserted-by":"crossref","first-page":"645","DOI":"10.1016\/j.freeradbiomed.2007.04.026","article-title":"Methods to detect nitric oxide and its metabolites in biological samples","volume":"43","year":"2007","journal-title":"Free Radical Biology and Medicine"},{"key":"ref01","doi-asserted-by":"crossref","first-page":"462","DOI":"10.1002\/jemt.10232","article-title":"Role of the central and peripheral nervous system in the ovarian function.","volume":"59","year":"2002","journal-title":"Microscopy Research and Technique"},{"key":"ref941","first-page":"143","article-title":"Neuro-endocrine networks controlling immune system in health and disease","volume":"5","year":"2014","journal-title":"Frontiers in Immunology"},{"key":"ref191","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1055\/s-2007-1022545","article-title":"Testosterone environment of splenocytes modifies the steroidogenesis of polycystic ovary in rats","volume":"40","year":"2008","journal-title":"Hormone and Metabolic Research"},{"key":"ref621","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1016\/S0165-5728(02)00435-6","article-title":"Catecholamines in a macrophage cell line","volume":"135","year":"2003","journal-title":"Journal of Neuroimmunology"},{"key":"ref851","doi-asserted-by":"crossref","first-page":"1059","DOI":"10.1210\/endo.141.3.7395","article-title":"An increased intraovarian synthesis of nerve growth factor and its low affinity receptor is a principal component of steroid-induced polycystic ovary in the rat","volume":"141","year":"2000","journal-title":"Endocrinology"},{"key":"ref241","doi-asserted-by":"crossref","first-page":"656","DOI":"10.1007\/BF03345620","article-title":"Decreased expression of kisspeptin mediates acute immune\/inflammatory stress-induced suppression of gonadotropin secretion in female rat","volume":"31","year":"2008","journal-title":"Journal of Endocrinological Investigation"},{"key":"ref461","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1016\/S0165-5728(01)00417-9","article-title":"Prolonged alpha-adrenergic stimulation causes changes in leukocyte distribution and lymphocyte apoptosis in the rat","volume":"120","year":"2001","journal-title":"Journal of Neuroimmunology"},{"key":"ref761","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1055\/s-2007-1022545","article-title":"Testosterone environment of splenocytes modifies the steroidogenesis of polycystic ovary in rats","volume":"40","year":"2008","journal-title":"Hormone and Metabolic Research"},{"key":"ref791","doi-asserted-by":"crossref","first-page":"180","DOI":"10.1134\/S1990747816020069","article-title":"Molecular mechanisms of the regulation by kisspeptin of the formation and functional activity of Treg and Th17","volume":"10","year":"2016","journal-title":"Biochemistry (Moscow) Supplement Series A: Membrane and Cell Biology"},{"key":"ref1021","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1186\/1477-7827-3-44","article-title":"Rats with steroid-induced polycystic ovary develops hypertension and increased sympathetic nervous system activity","volume":"3","year":"2005","journal-title":"Reproductive Biology and Endocrinology"},{"key":"ref431","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1055\/s-0035-1556568","article-title":"The emerging role of chronic low-grade inflammation in the pathophysiology of polycystic ovary syndrome","volume":"33","year":"2015","journal-title":"Seminars in Reproductive Medicine"},{"key":"ref591","doi-asserted-by":"crossref","first-page":"2696","DOI":"10.1210\/endo.133.6.8243293","article-title":"Ovarian steroidal response to gonadotropins and beta-adrenergic stimulation is enhanced in polycystic ovary syndrome: role of sympathetic innervations","volume":"133","year":"1993","journal-title":"Endocrinology"},{"key":"ref221","doi-asserted-by":"crossref","first-page":"180","DOI":"10.1134\/S1990747816020069","article-title":"Molecular mechanisms of the regulation by kisspeptin of the formation and functional activity of Treg and Th17","volume":"10","year":"2016","journal-title":"Biochemistry (Moscow) Supplement Series A: Membrane and Cell Biology"},{"key":"ref731","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1016\/S0960-0760(02)00149-8","article-title":"Neonatal superior ovarian nerve transection disturbs the cycle activity of the female rats","volume":"82","year":"2002","journal-title":"Journal of Steroid Biochemistry and Molecular Biology"},{"key":"ref1001","doi-asserted-by":"crossref","first-page":"257","DOI":"10.1055\/s-0035-1556568","article-title":"The emerging role of chronic low-grade inflammation in the pathophysiology of polycystic ovary syndrome","volume":"33","year":"2015","journal-title":"Seminars in Reproductive Medicine"},{"key":"ref71","first-page":"261","article-title":"The adrenergic innervation of mammalian ovaries","volume-title":"Catecholamines as Hormone Regulators","year":"1985"},{"key":"ref971","doi-asserted-by":"crossref","first-page":"3964","DOI":"10.1167\/iovs.04-0439","article-title":"Inflammatory cytokines induce apoptosis of corneal endothelium through nitric oxide","volume":"45","year":"2004","journal-title":"Investigative Ophthalmology and Visual Science"},{"key":"ref181","first-page":"965","article-title":"A neuroimmune regulation at peripheral level on the steroidogenesis of polycystic ovary in rats","volume":"49","year":"2003","journal-title":"Cellular and Molecular Biology"},{"key":"ref1061","doi-asserted-by":"crossref","first-page":"251","DOI":"10.1016\/j.cellsig.2006.06.007","article-title":"Beta2 adrenergic receptor activation stimulates pro-inflammatory cytokine production in macrophages via PKA- and NF-kappa B-independent mechanisms","volume":"19","year":"2007","journal-title":"Cellular Signalling"},{"key":"ref1101","first-page":"147","article-title":"Innervation pattern of polycystic ovaries in the women","volume":"61","year":"2014","journal-title":"Journal of Chemical Neuroanatomy"},{"key":"ref451","doi-asserted-by":"crossref","first-page":"44","DOI":"10.1186\/1477-7827-3-44","article-title":"Rats with steroid-induced polycystic ovary develops hypertension and increased sympathetic nervous system activity","volume":"3","year":"2005","journal-title":"Reproductive Biology and Endocrinology"},{"key":"ref581","doi-asserted-by":"crossref","first-page":"1019","DOI":"10.1189\/jlb.69.6.1019","article-title":"Nerve growth factor regulates TNF-alpha production in mouse macrophages via MAP kinase activation","volume":"69","year":"2001","journal-title":"Journal of Leukocyte Biology"},{"key":"ref891","doi-asserted-by":"crossref","first-page":"e1028","DOI":"10.3390\/ijms18051028","article-title":"NGF and its receptors in the regulation of inflammatory response","volume":"18","year":"2017","journal-title":"International Journal of Molecular Sciences"},{"key":"ref341","doi-asserted-by":"crossref","first-page":"345","DOI":"10.1016\/j.tem.2011.04.005","article-title":"Pituitary-ovary-spleen axis in ovulation.","volume":"22","year":"2011","journal-title":"Trends in Endocrinology and Metabolism"},{"key":"ref371","first-page":"143","article-title":"Neuro-endocrine networks controlling immune system in health and disease","volume":"5","year":"2014","journal-title":"Frontiers in Immunology"},{"key":"ref501","doi-asserted-by":"crossref","first-page":"128","DOI":"10.1002\/jnr.490170206","article-title":"Receptors for nerve growth factor on rat spleen mononuclear cells","volume":"17","year":"1987","journal-title":"Journal of Neuroscience Research"},{"key":"ref171","first-page":"1293","article-title":"Effect of secretion of splenocytes after superior ovarian nerve section on the ovarian steroidogenesis","volume":"6","year":"1999","journal-title":"Neuroimmunomodulation"},{"key":"ref861","doi-asserted-by":"crossref","first-page":"1907","DOI":"10.4049\/jimmunol.172.3.1907","article-title":"TNF-alpha-induced apoptosis of macrophages following inhibition of NF-kappa B: a central role for disruption of mitochondria","volume":"172","year":"2004","journal-title":"Journal of Immunology"},{"key":"ref991","doi-asserted-by":"crossref","first-page":"e005790","DOI":"10.1161\/JAHA.117.005790","article-title":"Potent vasoconstrictor kisspeptin-10 induces atherosclerotic plaque progression and instability: reversal by its receptor GPR54 antagonist","volume":"6","year":"2017","journal-title":"Journal of the American Heart Association"},{"key":"ref771","doi-asserted-by":"crossref","first-page":"453","DOI":"10.1016\/j.ejphar.2004.07.044","article-title":"Nerve growth factor and its receptor in asthma and inflammation","volume":"500","year":"2004","journal-title":"European Journal of Pharmacology"},{"key":"ref781","first-page":"520","article-title":"KiSS-1 in the mammalian ovary: distribution of kisspeptin in human and marmoset and alterations in KiSS-1 mRNA levels in a rat model of ovulatory dysfunction","volume":"296","year":"2009","journal-title":"American Journal of Physiology: Endocrinology and Metabolism"},{"key":"ref981","doi-asserted-by":"crossref","first-page":"555","DOI":"10.1093\/humrep\/det422","article-title":"Dopamine in human follicular fluid is associated with cellular uptake and metabolism-dependent generation of reactive oxygen species in granulosa cells: implications for physiology and pathology","volume":"29","year":"2014","journal-title":"Human Reproduction"},{"key":"ref281","doi-asserted-by":"crossref","first-page":"1059","DOI":"10.1210\/endo.141.3.7395","article-title":"An increased intraovarian synthesis of nerve growth factor and its low affinity receptor is a principal component of steroid-induced polycystic ovary in the rat","volume":"141","year":"2000","journal-title":"Endocrinology"},{"key":"ref321","doi-asserted-by":"crossref","first-page":"e1028","DOI":"10.3390\/ijms18051028","article-title":"NGF and its receptors in the regulation of inflammatory response","volume":"18","year":"2017","journal-title":"International Journal of Molecular Sciences"},{"key":"ref51","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1016\/S0165-5728(02)00435-6","article-title":"Catecholamines in a macrophage cell line","volume":"135","year":"2003","journal-title":"Journal of Neuroimmunology"},{"key":"ref401","doi-asserted-by":"crossref","first-page":"3964","DOI":"10.1167\/iovs.04-0439","article-title":"Inflammatory cytokines induce apoptosis of corneal endothelium through nitric oxide","volume":"45","year":"2004","journal-title":"Investigative Ophthalmology and Visual Science"},{"key":"ref91","doi-asserted-by":"crossref","first-page":"72","DOI":"10.1016\/j.ejogrb.2009.11.018","article-title":"Increased plasma metastin levels in adolescent women with polycystic ovary syndrome","volume":"149","year":"2010","journal-title":"European Journal of Obstetrics and Gynecology and Reproductive Biology"},{"key":"ref111","first-page":"583","article-title":"Ovarian innervation","volume-title":"Encyclopedia of Reproduction","year":"1999"},{"key":"ref271","doi-asserted-by":"crossref","first-page":"245","DOI":"10.1016\/S1642-431X(12)60015-1","article-title":"The influence of tumor necrosis factor alpha (TNF) on the secretory function of bovine corpus luteum: TNF and its receptors expression during the estrous cycle","volume":"8","year":"2008","journal-title":"Biology of Reproduction"},{"key":"ref871","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1016\/j.fertnstert.2016.05.003","article-title":"Criteria, prevalence, and phenotypes of polycystic ovary syndrome","volume":"106","year":"2016","journal-title":"Fertility and Sterility"},{"key":"ref1121","doi-asserted-by":"crossref","first-page":"148","DOI":"10.1016\/j.ejogrb.2011.07.012","article-title":"Low-grade chronic inflammation in the peripheral blood and ovaries of women with polycystic ovarian syndrome","volume":"159","year":"2011","journal-title":"European Journal of Obstetrics and Gynecology and Reproductive Biology"},{"key":"ref301","doi-asserted-by":"crossref","first-page":"6","DOI":"10.1016\/j.fertnstert.2016.05.003","article-title":"Criteria, prevalence, and phenotypes of polycystic ovary syndrome","volume":"106","year":"2016","journal-title":"Fertility and Sterility"},{"key":"ref701","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1530\/JOE-16-0181","article-title":"Kisspeptin level in the aging ovary is regulated by the sympathetic nervous system","volume":"232","year":"2017","journal-title":"Journal of Endocrinology"},{"key":"ref531","first-page":"147","article-title":"Innervation pattern of polycystic ovaries in the women","volume":"61","year":"2014","journal-title":"Journal of Chemical Neuroanatomy"},{"key":"ref1081","first-page":"40","article-title":"Bidirectional communication between the neuroendocrine system and the immune system: relevance to health and diseases","volume":"19","year":"2012","journal-title":"Annals of Neurosciences"},{"key":"ref231","doi-asserted-by":"crossref","first-page":"26205","DOI":"10.1038\/srep26205","article-title":"Fractalkine restores the decreased expression of StAR and progesterone in granulosa cells from patients with polycystic ovary syndrome","volume":"6","year":"2016","journal-title":"Scientific Reports"},{"key":"ref361","doi-asserted-by":"crossref","first-page":"49","DOI":"10.1038\/nrm2083","article-title":"Integrating cell-signalling pathways with NF-kappa B and IKK function","volume":"8","year":"2007","journal-title":"Nature Reviews Molecular Cell Biology"},{"key":"ref551","doi-asserted-by":"crossref","first-page":"148","DOI":"10.1016\/j.ejogrb.2011.07.012","article-title":"Low-grade chronic inflammation in the peripheral blood and ovaries of women with polycystic ovarian syndrome","volume":"159","year":"2011","journal-title":"European Journal of Obstetrics and Gynecology and Reproductive Biology"},{"key":"ref521","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1038\/nrurol.2015.277","article-title":"Kisspeptin signalling in the physiology and pathophysiology of the urogenital system","volume":"13","year":"2016","journal-title":"Nature Reviews Urology"},{"key":"ref611","doi-asserted-by":"crossref","first-page":"647","DOI":"10.1095\/biolreprod35.3.647","article-title":"Development of the polycystic ovarian condition (PCO) in the estradiol valerate-treated rat","volume":"35","year":"1986","journal-title":"Biology of Reproduction"},{"key":"ref421","doi-asserted-by":"crossref","first-page":"e005790","DOI":"10.1161\/JAHA.117.005790","article-title":"Potent vasoconstrictor kisspeptin-10 induces atherosclerotic plaque progression and instability: reversal by its receptor GPR54 antagonist","volume":"6","year":"2017","journal-title":"Journal of the American Heart Association"},{"key":"ref151","doi-asserted-by":"crossref","first-page":"437","DOI":"10.1530\/REP-15-0216","article-title":"Role of macrophage secretions on rat polycystic ovary: its effect on apoptosis","volume":"150","year":"2015","journal-title":"Reproduction"},{"key":"ref81","doi-asserted-by":"crossref","first-page":"155","DOI":"10.1016\/j.mce.2017.01.017","article-title":"Microparticles: inflammatory and haemostatic biomarkers in polycystic ovary syndrome","volume":"443","year":"2017","journal-title":"Molecular and Cellular Endocrinology"},{"key":"ref311","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1046\/j.1474-8673.2003.00280.x","article-title":"Autonomic innervation of immune organs and neuroimmune modulation","volume":"23","year":"2003","journal-title":"Autonomic and Autacoid Pharmacology"},{"key":"ref1041","doi-asserted-by":"crossref","first-page":"640","DOI":"10.1016\/j.tips.2004.10.007","article-title":"Complexity of the bi-directional neuroimmune junction in the spleen.","volume":"25","year":"2004","journal-title":"Trends in Pharmacological Sciences"},{"key":"ref411","doi-asserted-by":"crossref","first-page":"555","DOI":"10.1093\/humrep\/det422","article-title":"Dopamine in human follicular fluid is associated with cellular uptake and metabolism-dependent generation of reactive oxygen species in granulosa cells: implications for physiology and pathology","volume":"29","year":"2014","journal-title":"Human Reproduction"},{"key":"ref161","doi-asserted-by":"crossref","first-page":"75","DOI":"10.1016\/S0960-0760(02)00149-8","article-title":"Neonatal superior ovarian nerve transection disturbs the cycle activity of the female rats","volume":"82","year":"2002","journal-title":"Journal of Steroid Biochemistry and Molecular Biology"},{"key":"ref1031","doi-asserted-by":"crossref","first-page":"50","DOI":"10.1016\/S0165-5728(01)00417-9","article-title":"Prolonged alpha-adrenergic stimulation causes changes in leukocyte distribution and lymphocyte apoptosis in the rat","volume":"120","year":"2001","journal-title":"Journal of Neuroimmunology"},{"key":"ref141","doi-asserted-by":"crossref","first-page":"733","DOI":"10.1016\/j.lfs.2012.03.019","article-title":"Macrophage secretions modulate the steroidogenesis of polycystic ovary in rats: Effect of testosterone on macrophage pro-inflammatory cytokines","volume":"90","year":"2012","journal-title":"Life Sciences"},{"key":"ref821","doi-asserted-by":"crossref","first-page":"395","DOI":"10.1089\/ars.2005.7.395","article-title":"Redox regulation of NF-kappaB activation: distinct redox regulation between the cytoplasm and the nucleus","volume":"7","year":"2005","journal-title":"Antioxidants and Redox Signaling"},{"key":"ref831","doi-asserted-by":"crossref","first-page":"217","DOI":"10.1016\/0304-3940(88)90354-0","article-title":"Anatomical localization of afferent and postganglionic sympathetic neurons innervating the rat ovary","volume":"85","year":"1988","journal-title":"Neuroscience Letters"},{"key":"ref471","doi-asserted-by":"crossref","first-page":"640","DOI":"10.1016\/j.tips.2004.10.007","article-title":"Complexity of the bi-directional neuroimmune junction in the spleen.","volume":"25","year":"2004","journal-title":"Trends in Pharmacological Sciences"},{"key":"ref751","first-page":"965","article-title":"A neuroimmune regulation at peripheral level on the steroidogenesis of polycystic ovary in rats","volume":"49","year":"2003","journal-title":"Cellular and Molecular Biology"},{"key":"ref951","doi-asserted-by":"crossref","first-page":"356","DOI":"10.1049\/iet-syb.2008.0172","article-title":"Crosstalk between p53 and nuclear factor-kB systems: pro- and anti-apoptotic functions of NF-kB","volume":"3","year":"2009","journal-title":"IET Systems Biology"},{"key":"ref481","doi-asserted-by":"crossref","first-page":"840","DOI":"10.1016\/j.fertnstert.2013.11.027","article-title":"Hyperandrogenemia is implicated in both the metabolic and reproductive morbidities of polycystic ovary syndrome","volume":"101","year":"2014","journal-title":"Fertility and Sterility"},{"key":"ref681","first-page":"583","article-title":"Ovarian innervation","volume-title":"Encyclopedia of Reproduction","year":"1999"}],"container-title":["Journal of Endocrinology"],"original-title":[],"link":[{"URL":"https:\/\/joe.bioscientifica.com\/view\/journals\/joe\/238\/1\/JOE-17-0736.xml","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/joe.bioscientifica.com\/downloadpdf\/journals\/joe\/238\/1\/JOE-17-0736.xml","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,7,20]],"date-time":"2026-07-20T13:56:12Z","timestamp":1784555772000},"score":1,"resource":{"primary":{"URL":"http:\/\/journals.bioscientifica.com\/joe\/article\/238\/1\/33-45\/5028"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2018,7]]},"references-count":114,"journal-issue":{"issue":"1"},"URL":"https:\/\/doi.org\/10.1530\/joe-17-0736","relation":{},"ISSN":["0022-0795","1479-6805"],"issn-type":[{"value":"0022-0795","type":"print"},{"value":"1479-6805","type":"electronic"}],"subject":[],"published":{"date-parts":[[2018,7]]}}}