miR-7 mediates the signaling pathway of NE affecting FSH and LH synthesis in pig pituitary

in Journal of Endocrinology

Correspondence should be addressed to J Zhang or S Cui: 2253055127@qq.com or cuisheng@cau.edu.cn

*(X Li and H Li contributed equally to this work)

Restricted access

MicroRNA-7 (miR-7) is an important modulator of a plenty of gene expressions and the interrelated biological processes, highly expressed in porcine pituitary. Norepinephrine (NE), acting as an important neurotransmitter or/and a hormone secreted excessively under stress, affects the synthesis and secretion of various hormones, including pituitary follicle-stimulating hormone (FSH) and luteinizing hormone (LH), which are the key hormones which regulate sexual maturation and reproductive functions. However, the relationship among NE, miR-7 and gonadotropin needs to be elucidated. The aim of this study was to identify whether miR-7 involved in the NE-adrenoceptor signaling pathway affects the synthesis and secretion of FSH and LH in porcine pituitary. Our results showed that the NE intracerebroventricular injection increased pituitary miR-7 level and the synthesis and secretion of FSH and LH in porcine, whereas the inhibition of either endogenous miR-7 or β-adrenergic receptors hindered the rise of FSH and LH synthesis induced by NE in cultured primary porcine anterior pituitary cells. Further, we identified the molecular type of β-adrenergic receptors and the signaling pathway in porcine pituitary, and we found that NE played its roles relying on adrenoceptor beta 2 (β2AR) and the RAF/MEK/ERK1/2 signaling pathway. The phosphorylation of ERK1/2 upregulated miR-7 level which subsequently enhanced FSH and LH synthesis by targeting to Golgi glycoprotein 1 (GLG1). These suggest that miR-7 mediates NE’s effect on promoting FSH and LH synthesis in porcine pituitary.

 

      Society for Endocrinology

Sept 2018 onwards Past Year Past 30 Days
Abstract Views 516 516 232
Full Text Views 43 43 23
PDF Downloads 15 15 7
  • AgarwalRKChandnaVKEngelkingLRLightbownKKumarMS 1993 Distribution of catecholamines in the central nervous system of the pig. Brain Research Bulletin 285291. (https://doi.org/10.1016/0361-9230(93)90189-i)

    • Search Google Scholar
    • Export Citation
  • AguileraG 1994 Regulation of pituitary ACTH secretion during chronic stress. Frontiers in Neuroendocrinology 321350. (https://doi.org/10.1006/frne.1994.1013)

    • Search Google Scholar
    • Export Citation
  • AhlesAEngelhardtS 2014 Polymorphic variants of adrenoceptors: pharmacology, physiology, and role in disease. Pharmacological Reviews 598637. (https://doi.org/10.1124/pr.113.008219)

    • Search Google Scholar
    • Export Citation
  • AhmedKLapierreMPGasserEDenzlerRYangYRulickeTKeroJLatreilleMStoffelM 2017 Loss of microRNA-7a2 induces hypogonadotropic hypogonadism and infertility. Journal of Clinical Investigation 10611074. (https://doi.org/10.1172/JCI90031)

    • Search Google Scholar
    • Export Citation
  • Bedran-de-CastroJCPetrovicSLMccannSM 1990 Involvement of beta-adrenergic receptors in the differential release of gonadotropins in acutely orchidectomized rats. Brazilian Journal of Medical and Biological Research 10251027.

    • Search Google Scholar
    • Export Citation
  • BorrowAPHeckALMillerAMShengJAStoverSADanielsRMBalesNJFleuryTKHandaRJ 2019 Chronic variable stress alters hypothalamic-pituitary-adrenal axis function in the female mouse. Physiology and Behavior 112613. (https://doi.org/10.1016/j.physbeh.2019.112613)

    • Search Google Scholar
    • Export Citation
  • BrinkmeierMLDavisSWCarninciPMacdonaldJWKawaiJGhoshDHayashizakiYLyonsRHCamperSA 2009 Discovery of transcriptional regulators and signaling pathways in the developing pituitary gland by bioinformatic and genomic approaches. Genomics 449460. (https://doi.org/10.1016/j.ygeno.2008.11.010)

    • Search Google Scholar
    • Export Citation
  • BrownJLRobersonM 2017 Novel insights into gonadotropin-releasing hormone action in the pituitary gonadotrope. Seminars in Reproductive Medicine 130138. (https://doi.org/10.1055/s-0037-1599084)

    • Search Google Scholar
    • Export Citation
  • ChobanianNSKushlinskiiNEBassalykLSKuzminaZVGershteinESSavelevaEVBaryshnikovAIuKadagidzeZG 1994 Hypophyseal hormones in young patients with breast cancer. Klinicheskaia Meditsina 3740.

    • Search Google Scholar
    • Export Citation
  • ChristensenABentleyGECabreraROrtegaHHPerfitoNWuTJMicevychP 2012 Hormonal regulation of female reproduction. Hormone and Metabolic Research 587591. (https://doi.org/10.1055/s-0032-1306301)

    • Search Google Scholar
    • Export Citation
  • CoxBRooseHVennekensAVankelecomH 2017 Pituitary stem cell regulation: who is pulling the strings? Journal of Endocrinology R135R158. (https://doi.org/10.1530/JOE-17-0083)

    • Search Google Scholar
    • Export Citation
  • DavisSWEllsworthBSPerez MillanMIGergicsPSchadeVFoyouziNBrinkmeierMLMortensenAHCamperSA 2013 Pituitary gland development and disease: from stem cell to hormone production. Current Topics in Developmental Biology 147. (https://doi.org/10.1016/B978-0-12-416021-7.00001-8)

    • Search Google Scholar
    • Export Citation
  • De SouzaEB 1985 Beta-2-adrenergic receptors in pituitary. Identification, characterization, and autoradiographic localization. Neuroendocrinology 289296. (https://doi.org/10.1159/000124192)

    • Search Google Scholar
    • Export Citation
  • De SouzaEB 1987 Modulation of beta-adrenergic receptors in the pituitary gland following adrenalectomy in rats. Neuroscience Letters 281286. (https://doi.org/10.1016/0304-3940(87)90259-x)

    • Search Google Scholar
    • Export Citation
  • DegreefMVan NuijsALNMaudensKE 2018 Validation of a simple, fast liquid chromatography-tandem mass spectrometry method for the simultaneous quantification of 40 antidepressant drugs or their metabolites in plasma. Clinica Chimica Acta: International Journal of Clinical Chemistry 243257. (https://doi.org/10.1016/j.cca.2018.06.047)

    • Search Google Scholar
    • Export Citation
  • DenefCBaesM 1982 Beta-adrenergic stimulation of prolactin release from superfused pituitary cell aggregates. Endocrinology 356358. (https://doi.org/10.1210/endo-111-1-356)

    • Search Google Scholar
    • Export Citation
  • DrouvaSVGalloRV 1976 Catecholamine involvement in episodic luteinizing hormone release in adult ovariectomized rats. Endocrinology 651658. (https://doi.org/10.1210/endo-99-3-651)

    • Search Google Scholar
    • Export Citation
  • DuboisPMElamraouiA 1995 Embryology of the pituitary gland. Trends in Endocrinology and Metabolism 17. (https://doi.org/10.1016/1043-2760(94)00090-q)

    • Search Google Scholar
    • Export Citation
  • GiussaniDAMoorePJBennetLSpencerJAHansonMA 1995 Alpha 1- and alpha 2-adrenoreceptor actions of phentolamine and prazosin on breathing movements in fetal sheep in utero. Journal of Physiology 249255. (https://doi.org/10.1113/jphysiol.1995.sp020807)

    • Search Google Scholar
    • Export Citation
  • GloverARZhaoJTGillAJWeissJMugridgeNKimEFeeneyALIpJCReidGClarkeS 2015 MicroRNA-7 as a tumor suppressor and novel therapeutic for adrenocortical carcinoma. Oncotarget 3667536688. (https://doi.org/10.18632/oncotarget.5383)

    • Search Google Scholar
    • Export Citation
  • GuSJingLLiYHuangJHWangF 2018 Stress induced hormone and neuromodulator changes in menopausal depressive rats. Frontiers in Psychiatry 253. (https://doi.org/10.3389/fpsyt.2018.00253)

    • Search Google Scholar
    • Export Citation
  • HeJRMolnarJBarracloughCA 1993 Morphine amplifies norepinephrine (NE)-induced LH release but blocks NE-stimulated increases in LHRH mRNA levels: comparison of responses obtained in ovariectomized, estrogen-treated normal and androgen-sterilized rats. Brain Research: Molecular Brain Research 7178. (https://doi.org/10.1016/0169-328x(93)90111-2)

    • Search Google Scholar
    • Export Citation
  • HeJWeiCLiYLiuYWangYPanJLiuJWuYCuiS 2018a Zearalenone and alpha-zearalenol inhibit the synthesis and secretion of pig follicle stimulating hormone via the non-classical estrogen membrane receptor GPR30. Molecular and Cellular Endocrinology 4354. (https://doi.org/10.1016/j.mce.2017.08.010)

    • Search Google Scholar
    • Export Citation
  • HeJZhangJWangYLiuWGouKLiuZCuiS 2018b MiR-7 mediates the zearalenone signaling pathway regulating FSH synthesis and secretion by targeting FOS in female pigs. Endocrinology 29933006. (https://doi.org/10.1210/en.2018-00097)

    • Search Google Scholar
    • Export Citation
  • HeckALHandaRJ 2019 Sex differences in the hypothalamic-pituitary-adrenal axis’ response to stress: an important role for gonadal hormones. Neuropsychopharmacology 4558. (https://doi.org/10.1038/s41386-018-0167-9)

    • Search Google Scholar
    • Export Citation
  • JavelleMTimmermansMC 2012 In situ localization of small RNAs in plants by using LNA probes. Nature Protocols 533541. (https://doi.org/10.1038/nprot.2012.006)

    • Search Google Scholar
    • Export Citation
  • JiangHFanDZhouGLiXDengH 2010 Phosphatidylinositol 3-kinase inhibitor(LY294002) induces apoptosis of human nasopharyngeal carcinoma in vitro and in vivo. Journal of Experimental and Clinical Cancer Research 34. (https://doi.org/10.1186/1756-9966-29-34)

    • Search Google Scholar
    • Export Citation
  • JohnsonEOKamilarisTCChrousosGPGoldPW 1992 Mechanisms of stress: a dynamic overview of hormonal and behavioral homeostasis. Neuroscience and Biobehavioral Reviews 115130. (https://doi.org/10.1016/s0149-7634(05)80175-7)

    • Search Google Scholar
    • Export Citation
  • KageyamaK 2013 Regulation of gonadotropins by corticotropin-releasing factor and urocortin. Frontiers in Endocrinology 12. (https://doi.org/10.3389/fendo.2013.00012)

    • Search Google Scholar
    • Export Citation
  • KelbermanDRizzotiKLovell-BadgeRRobinsonICDattaniMT 2009 Genetic regulation of pituitary gland development in human and mouse. Endocrine Reviews 790829. (https://doi.org/10.1210/er.2009-0008)

    • Search Google Scholar
    • Export Citation
  • Kredo-RussoSNessAMandelbaumADWalkerMDHornsteinE 2012 Regulation of pancreatic microRNA-7 expression. Experimental Diabetes Research 695214. (https://doi.org/10.1155/2012/695214)

    • Search Google Scholar
    • Export Citation
  • LeiYCaoYXXuCBZhangY 2008 The Raf-1 inhibitor GW5074 and dexamethasone suppress sidestream smoke-induced airway hyperresponsiveness in mice. Respiratory Research 71. (https://doi.org/10.1186/1465-9921-9-71)

    • Search Google Scholar
    • Export Citation
  • LennartssonAKKushnirMMBergquistJBilligHJonsdottirIH 2012 Sex steroid levels temporarily increase in response to acute psychosocial stress in healthy men and women. International Journal of Psychophysiology 246253. (https://doi.org/10.1016/j.ijpsycho.2012.03.001)

    • Search Google Scholar
    • Export Citation
  • LiSLvXZhaiKXuRZhangYZhaoSQinXYinLLouJ 2016 MicroRNA-7 inhibits neuronal apoptosis in a cellular Parkinson’s disease model by targeting Bax and Sirt2. American Journal of Translational Research 9931004.

    • Search Google Scholar
    • Export Citation
  • LoboRAGrangerLRPaulWLGoebelsmannUMishellDRJr 1983 Psychological stress and increases in urinary norepinephrine metabolites, platelet serotonin, and adrenal androgens in women with polycystic ovary syndrome. American Journal of Obstetrics and Gynecology 496503. (https://doi.org/10.1016/0002-9378(83)90324-1)

    • Search Google Scholar
    • Export Citation
  • MiyakeATsakaKSakumotoTKawamuraYAonoTKurachiK 1983 Norepinephrine induces releases of both LH-RH from the hypothalamus and LH from the rat pituitary in vitro. Endocrinologia Japonica 509512. (https://doi.org/10.1507/endocrj1954.30.509)

    • Search Google Scholar
    • Export Citation
  • MobergGP 1991 How behavioral stress disrupts the endocrine control of reproduction in domestic animals. Journal of Dairy Science 304311. (https://doi.org/10.3168/jds.S0022-0302(91)78174-5)

    • Search Google Scholar
    • Export Citation
  • MohammadiHRezaeiMFaghihiFKhazaieH 2019 Hypothalamic-pituitary-gonadal activity in paradoxical and psychophysiological insomnia. Journal of Medical Signals and Sensors 5967. (https://doi.org/10.4103/jmss.JMSS_31_18)

    • Search Google Scholar
    • Export Citation
  • MohrAMMottJL 2015 Overview of microRNA biology. Seminars in Liver Disease 311. (https://doi.org/10.1055/s-0034-1397344)

  • MonaghanKAKhongTBurnsCJSpencerA 2011 The novel JAK inhibitor CYT387 suppresses multiple signalling pathways, prevents proliferation and induces apoptosis in phenotypically diverse myeloma cells. Leukemia 18911899. (https://doi.org/10.1038/leu.2011.175)

    • Search Google Scholar
    • Export Citation
  • MunabiNCEnglandRWEdwardsAKKitajewskiAATanQKWeinsteinAKungJEWilcoxMKitajewskiJKShawberCJ 2016 Propranolol targets hemangioma stem cells via cAMP and mitogen-activated protein kinase regulation. Stem Cells Translational Medicine 4555. (https://doi.org/10.5966/sctm.2015-0076)

    • Search Google Scholar
    • Export Citation
  • MusumeciGCastorinaSCastrogiovanniPLoretoCLeonardiRAielloFCMagroGImbesiR 2015 A journey through the pituitary gland: development, structure and function, with emphasis on embryo-foetal and later development. Acta Histochemica 355366. (https://doi.org/10.1016/j.acthis.2015.02.008)

    • Search Google Scholar
    • Export Citation
  • O’HayreMEichelKAvinoSZhaoXSteffenDJFengXKawakamiKAokiJMesserKSunaharaR 2017 Genetic evidence that beta-arrestins are dispensable for the initiation of beta2-adrenergic receptor signaling to ERK. Science Signaling eaal3395. (https://doi.org/10.1126/scisignal.aal3395)

    • Search Google Scholar
    • Export Citation
  • OyolaMGHandaRJ 2017 Hypothalamic-pituitary-adrenal and hypothalamic-pituitary-gonadal axes: sex differences in regulation of stress responsivity. Stress 476494. (https://doi.org/10.1080/10253890.2017.1369523)

    • Search Google Scholar
    • Export Citation
  • PocetaJSHamlinMNHaackDWBohrDF 1981 Stereotaxic placement of cannulae in cerebral ventricles of the pig. Anatomical Record 349356. (https://doi.org/10.1002/ar.1092000315)

    • Search Google Scholar
    • Export Citation
  • QiuJZhangJZhouYLiXLiHLiuJGouKZhaoJCuiS 2019 MicroRNA-7 inhibits melatonin synthesis by acting as a linking molecule between leptin and norepinephrine signaling pathways in pig pineal gland. Journal of Pineal Research e12552. (https://doi.org/10.1111/jpi.12552)

    • Search Google Scholar
    • Export Citation
  • RamaswamySWeinbauerGF 2014 Endocrine control of spermatogenesis: role of FSH and LH/testosterone. Spermatogenesis e996025. (https://doi.org/10.1080/21565562.2014.996025)

    • Search Google Scholar
    • Export Citation
  • RojewskaEPopiolek-BarczykKKolosowskaNPiotrowskaAZychowskaMMakuchWPrzewlockaBMikaJ 2015 PD98059 influences immune factors and enhances opioid analgesia in model of neuropathy. PLoS ONE e0138583. (https://doi.org/10.1371/journal.pone.0138583)

    • Search Google Scholar
    • Export Citation
  • SchwarzLALuoL 2015 Organization of the locus coeruleus-norepinephrine system. Current Biology R1051R1056. (https://doi.org/10.1016/j.cub.2015.09.039)

    • Search Google Scholar
    • Export Citation
  • TanakaMYasuokaAYoshinumaHSaitoYAsakuraTTanabeS 2018 Seasoning ingredients in a medium-fat diet regulate lipid metabolism in peripheral tissues via the hypothalamic-pituitary axis in growing rats. Bioscience Biotechnology and Biochemistry 497506. (https://doi.org/10.1080/09168451.2018.1427551)

    • Search Google Scholar
    • Export Citation
  • ThackrayVGHunnicuttJLMemonAKGhochaniYMellonPL 2009 Progesterone Inhibits basal and gonadotropin-releasing hormone induction of luteinizing hormone beta-subunit gene expression. Endocrinology 23952403. (https://doi.org/10.1210/en.2008-1027)

    • Search Google Scholar
    • Export Citation
  • ToufexisDRivarolaMALaraHViauV 2014 Stress and the reproductive axis. Journal of Neuroendocrinology 573586. (https://doi.org/10.1111/jne.12179)

    • Search Google Scholar
    • Export Citation
  • van EerdenburgFJDierxJA 2002 A new technique for long term, stress free, cannulation of the lateral ventricle in postpubertal, freely moving, pigs. Journal of Neuroscience Methods 1320. (https://doi.org/10.1016/s0165-0270(02)00226-1)

    • Search Google Scholar
    • Export Citation
  • Von EulerUS 1946 Sympathin in adrenergic nerve fibres. Journal of Physiology 26.

  • WierinckxARocheMLegras-LachuerCTrouillasJRaverotGLachuerJ 2017 MicroRNAs in pituitary tumors. Molecular and Cellular Endocrinology 5161. (https://doi.org/10.1016/j.mce.2017.01.021)

    • Search Google Scholar
    • Export Citation
  • YuanBSunGJZhangGLWuJXuCDaiLSChenJYuXFZhaoZHZhangJB 2015 Identification of target genes for adenohypophysis-prefer miR-7 and miR-375 in cattle. Genetics and Molecular Research 97539763. (https://doi.org/10.4238/2015.August.19.8)

    • Search Google Scholar
    • Export Citation
  • ZhangJQiuJZhouYWangYLiHZhangTJiangYGouKCuiS 2018 LIM homeobox transcription factor Isl1 is required for melatonin synthesis in the pig pineal gland. Journal of Pineal Research e12481. (https://doi.org/10.1111/jpi.12481)

    • Search Google Scholar
    • Export Citation
  • ZhengWFengNWangYNollLXuSLiuXLuNZouHGuJYuanY 2019 Effects of zearalenone and its derivatives on the synthesis and secretion of mammalian sex steroid hormones: a review. Food and Chemical Toxicology 262276. (https://doi.org/10.1016/j.fct.2019.02.031)

    • Search Google Scholar
    • Export Citation
  • ZhuYLZhangSJDengYMDongXWJiangJXXieQM 2010 Leukotriene B4, administered via intracerebroventricular injection, attenuates the antigen-induced asthmatic response in sensitized guinea pigs. Journal of Neuroinflammation 12. (https://doi.org/10.1186/1742-2094-7-12)

    • Search Google Scholar
    • Export Citation