Missing Information from the Estrogen Receptor Puzzle: Where Are They Localized in Bull Reproductive Tissues and Spermatozoa?
Language English Country Switzerland Media electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
PubMed
31936899
PubMed Central
PMC7016540
DOI
10.3390/cells9010183
PII: cells9010183
Knihovny.cz E-resources
- Keywords
- bovine, epididymis, plasma membrane, reproduction, steroid hormones, testes,
- MeSH
- Epididymis metabolism MeSH
- Receptors, Estrogen metabolism MeSH
- Receptors, G-Protein-Coupled metabolism MeSH
- Reproduction * MeSH
- Cattle metabolism MeSH
- Spermatozoa metabolism MeSH
- Testis metabolism MeSH
- Animals MeSH
- Check Tag
- Male MeSH
- Cattle metabolism MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Receptors, Estrogen MeSH
- Receptors, G-Protein-Coupled MeSH
Estrogens are steroid hormones that affect a wide range of physiological functions. The effect of estrogens on male reproductive tissues and sperm cells through specific receptors is essential for sperm development, maturation, and function. Although estrogen receptors (ERs) have been studied in several mammalian species, including humans, they have not yet been described in bull spermatozoa and reproductive tissues. In this study, we analyzed the presence of all types of ERs (ESR1, ESR2, and GPER1) in bull testicular and epididymal tissues and epididymal and ejaculated spermatozoa, and we characterize them here for the first time. We observed different localizations of each type of ER in the sperm head by immunofluorescent microscopy. Additionally, using a selected polyclonal antibody, we found that each type of ER in bull sperm extracts had two isoforms with different molecular masses. The detailed detection of ERs is a prerequisite not only for understanding the effect of estrogen on all reproductive events but also for further studying the negative effect of environmental estrogens (endocrine disruptors) on processes that lead to fertilization.
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Rosselli M., Reinhart K., Imthurn B., Keller P.J., Dubey R.K. Cellular and biochemical mechanisms by which environmental oestrogens influence reproductive function. Hum. Reprod. Update. 2000;6:332–350. doi: 10.1093/humupd/6.4.332. PubMed DOI
Hess R.A. Estrogen in the adult male reproductive tract: A review. Reprod. Biol. Endocrinol. 2003;1:52. doi: 10.1186/1477-7827-1-52. PubMed DOI PMC
Dostalova P., Zatecka E., Dvorakova-Hortova K. Of oestrogens and sperm: A review of the roles of oestrogens and oestrogen receptors in male reproduction. Int. J. Mol. Sci. 2017;18:904. doi: 10.3390/ijms18050904. PubMed DOI PMC
Hess R.A., Cooke P.S. Estrogen in the male: A historical perspective. Biol. Reprod. 2018;99:27–44. doi: 10.1093/biolre/ioy043. PubMed DOI PMC
O’donnell L., Robertson K.M., Jones M.E., Simpson E.R. Estrogen and spermatogenesis. Endocr. Rev. 2001;22:289–318. doi: 10.1210/edrv.22.3.0431. PubMed DOI
Robertson K.M., O’Donnell L., Jones M.E., Meachem S.J., Boon W.C., Fisher C.R., Graves K.H., McLachlan R.I., Simpson E.R. Impairment of spermatogenesis in mice lacking a functional aromatase (cyp 19) gene. Proc. Natl. Acad. Sci. USA. 1999;96:7986–7991. doi: 10.1073/pnas.96.14.7986. PubMed DOI PMC
Eddy E., Washburn T., Bunch D., Goulding E., Gladen B., Lubahn D., Korach K. Targeted disruption of the estrogen receptor gene in male mice causes alteration of spermatogenesis and infertility. Endocrinology. 1996;137:4796–4805. doi: 10.1210/endo.137.11.8895349. PubMed DOI
Hess R.A., Bunick D., Lee K.-H., Bahr J., Taylor J.A., Korach K.S., Lubahn D.B. A role for oestrogens in the male reproductive system. Nature. 1997;390:509. doi: 10.1038/37352. PubMed DOI PMC
Luconi M., Muratori M., Forti G., Baldi E. Identification and characterization of a novel functional estrogen receptor on human sperm membrane that interferes with progesterone effects. J. Clin. Endocrinol. Metab. 1999;84:1670–1678. doi: 10.1210/jcem.84.5.5670. PubMed DOI
Sebkova N., Cerna M., Ded L., Peknicova J., Dvorakova-Hortova K. The slower the better: How sperm capacitation and acrosome reaction is modified in the presence of estrogens. Reproduction. 2012;143:297–307. doi: 10.1530/REP-11-0326. PubMed DOI
Ded L., Sebkova N., Cerna M., Elzeinova F., Dostalova P., Peknicova J., Dvorakova-Hortova K. In vivo exposure to 17β-estradiol triggers premature sperm capacitation in cauda epididymis. Reproduction. 2013;145:255–263. doi: 10.1530/REP-12-0472. PubMed DOI
Bathla H., Guraya S., Sanghal G. Role of estradiol in the capacitation and acrosome reaction of hamster epididymal spermatozoa in the isolated uterus of mice incubated in vitro. Indian J. Physiol. Pharm. 1999;43:211–217. PubMed
He Y., Yue L., He Y., Zhang J., Zheng J., Gao X. Effects of estrogen on acrosome reaction and intracellular calcium in human spermatozoa and the possible mechanism concerned. J. Sichuan Univ. Med Sci. Ed. 2005;36:500–502. PubMed
Adeoya-Osiguwa S., Markoulaki S., Pocock V., Milligan S., Fraser L. 17β-Estradiol and environmental estrogens significantly affect mammalian sperm function. Hum. Reprod. 2003;18:100–107. doi: 10.1093/humrep/deg037. PubMed DOI
Acconcia F., Kumar R. Signaling regulation of genomic and nongenomic functions of estrogen receptors. Cancer Lett. 2006;238:1–14. doi: 10.1016/j.canlet.2005.06.018. PubMed DOI
Pedram A., Razandi M., Sainson R.C., Kim J.K., Hughes C.C., Levin E.R. A conserved mechanism for steroid receptor translocation to the plasma membrane. J. Biol. Chem. 2007;282:22278–22288. doi: 10.1074/jbc.M611877200. PubMed DOI
Levin E.R. Plasma membrane estrogen receptors. Trends Endocrinol. Metab. 2009;20:477–482. doi: 10.1016/j.tem.2009.06.009. PubMed DOI PMC
Revankar C.M., Cimino D.F., Sklar L.A., Arterburn J.B., Prossnitz E.R. A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science. 2005;307:1625–1630. doi: 10.1126/science.1106943. PubMed DOI
Sakamoto H., Matsuda K.-i., Hosokawa K., Nishi M., Morris J.F., Prossnitz E.R., Kawata M. Expression of G protein-coupled receptor-30, a G protein-coupled membrane estrogen receptor, in oxytocin neurons of the rat paraventricular and supraoptic nuclei. Endocrinology. 2007;148:5842–5850. doi: 10.1210/en.2007-0436. PubMed DOI
Kuiper G., Enmark E., Pelto-Huikko M., Nilsson S., Gustafsson J.-A. Cloning of a novel receptor expressed in rat prostate and ovary. Proc. Natl. Acad. Sci. USA. 1996;93:5925–5930. doi: 10.1073/pnas.93.12.5925. PubMed DOI PMC
Mosselman S., Polman J., Dijkema R. ERβ: Identification and characterization of a novel human estrogen receptor. FEBS Lett. 1996;392:49–53. doi: 10.1016/0014-5793(96)00782-X. PubMed DOI
Filardo E., Quinn J., Pang Y., Graeber C., Shaw S., Dong J., Thomas P. Activation of the novel estrogen receptor G protein-coupled receptor 30 (GPR30) at the plasma membrane. Endocrinology. 2007;148:3236–3245. doi: 10.1210/en.2006-1605. PubMed DOI
Kumar R., Zakharov M.N., Khan S.H., Miki R., Jang H., Toraldo G., Singh R., Bhasin S., Jasuja R. The dynamic structure of the estrogen receptor. J. Amino Acids. 2011;2011 doi: 10.4061/2011/812540. PubMed DOI PMC
Kang L., Zhang X., Xie Y., Tu Y., Wang D., Liu Z., Wang Z.-Y. Involvement of estrogen receptor variant ER-α36, not GPR30, in nongenomic estrogen signaling. Mol. Endocrinol. 2010;24:709–721. doi: 10.1210/me.2009-0317. PubMed DOI PMC
Whiting K.P., Restall C.J., Brain P.F. Steroid hormone-induced effects on membrane fluidity and their potential roles in non-genomic mechanisms. Life Sci. 2000;67:743–757. doi: 10.1016/S0024-3205(00)00669-X. PubMed DOI
Curtis Hewitt S., Collins J., Grissom S., Deroo B., Korach K.S. Global uterine genomics in vivo: Microarray evaluation of the estrogen receptor α-growth factor cross-talk mechanism. Mol. Endocrinol. 2005;19:657–668. doi: 10.1210/me.2004-0142. PubMed DOI
Sirianni R., Chimento A., Ruggiero C., De Luca A., Lappano R., Andò S., Maggiolini M., Pezzi V. The novel estrogen receptor, G protein-coupled receptor 30, mediates the proliferative effects induced by 17β-estradiol on mouse spermatogonial GC-1 cell line. Endocrinology. 2008;149:5043–5051. doi: 10.1210/en.2007-1593. PubMed DOI
Zhou Q., Nie R., Prins G.S., Saunders P.T., Katzenellenbogen B.S., Hess R.A. Localization of androgen and estrogen receptors in adult male mouse reproductive tract. J. Androl. 2002;23:870–881. doi: 10.1002/j.1939-4640.2002.tb02345.x. PubMed DOI
Lucas T.F.G., Siu E.R., Esteves C.A., Monteiro H.P., Oliveira C.A., Porto C.S., Lazari M.F.M. 17Beta-Estradiol Induces the Translocation of the Estrogen Receptors ESR1 and ESR2 to the Cell Membrane, MAPK3/1 Phosphorylation and Proliferation of Cultured Immature Rat Sertoli Cells1. Biol. Reprod. 2008;78:101–114. doi: 10.1095/biolreprod.107.063909. PubMed DOI
Zaya R., Hennick C., Pearl C.A. In vitro expression of androgen and estrogen receptors in prepubertal and adult rat epididymis. Gen. Comp. Endocrinol. 2012;178:573–586. doi: 10.1016/j.ygcen.2012.07.004. PubMed DOI
Bilińska B., Schmalz-Frączek B., Kotula M., Carreau S. Photoperiod-dependent capability of androgen aromatization and the role of estrogens in the bank vole testis visualized by means of immunohistochemistry. Mol. Cell. Endocrinol. 2001;178:189–198. doi: 10.1016/S0303-7207(01)00427-0. PubMed DOI
Kotula-Balak M., Hejmej A., Lydka M., Cierpich A., Bilinska B. Detection of aromatase, androgen, and estrogen receptors in bank vole spermatozoa. Theriogenology. 2012;78:385–392. doi: 10.1016/j.theriogenology.2012.02.018. PubMed DOI
Zarzycka M., Gorowska-Wojtowicz E., Tworzydlo W., Klak A., Kozub K., Hejmej A., Bilinska B., Kotula-Balak M. Are aryl hydrocarbon receptor and G-protein–coupled receptor 30 involved in the regulation of seasonal testis activity in photosensitive rodent—the bank vole (Myodes glareolus)? Theriogenology. 2016;86:674–686. doi: 10.1016/j.theriogenology.2016.02.019. PubMed DOI
Parlevliet J.M., Pearl C.A., Hess M.F., Famula T.R., Roser J.F. Immunolocalization of estrogen and androgen receptors and steroid concentrations in the stallion epididymis. Theriogenology. 2006;66:755–765. doi: 10.1016/j.theriogenology.2005.12.013. PubMed DOI
Pearl C.A., Mason H., Roser J.F. Immunolocalization of estrogen receptor alpha, estrogen receptor beta and androgen receptor in the pre-, peri-and post-pubertal stallion testis. Anim. Reprod. Sci. 2011;125:103–111. doi: 10.1016/j.anireprosci.2011.03.007. PubMed DOI
Mäkinen S., Mäkelä S., Weihua Z., Warner M., Rosenlund B., Salmi S., Hovatta O., Gustafsson J.-Å. Localization of oestrogen receptors alpha and beta in human testis. Mol. Hum. Reprod. 2001;7:497–503. doi: 10.1093/molehr/7.6.497. PubMed DOI
Saunders P.T., Sharpe R.M., Williams K., Macpherson S., Urquart H., Irvine D.S., Millar M.R. Differential expression of oestrogen receptor α and β proteins in the testes and male reproductive system of human and non-human primates. Mol. Hum. Reprod. 2001;7:227–236. doi: 10.1093/molehr/7.3.227. PubMed DOI
Fietz D., Ratzenböck C., Hartmann K., Raabe O., Kliesch S., Weidner W., Klug J., Bergmann M. Expression pattern of estrogen receptors α and β and G-protein-coupled estrogen receptor 1 in the human testis. Histochem. Cell Biol. 2014;142:421–432. doi: 10.1007/s00418-014-1216-z. PubMed DOI
Rago V., Siciliano L., Aquila S., Carpino A. Detection of estrogen receptors ER-alpha and ER-beta in human ejaculated immature spermatozoa with excess residual cytoplasm. Reprod. Biol. Endocrinol. 2006;4:36. doi: 10.1186/1477-7827-4-36. PubMed DOI PMC
Gunawan A., Kaewmala K., Uddin M.J., Cinar M.U., Tesfaye D., Phatsara C., Tholen E., Looft C., Schellander K. Association study and expression analysis of porcine ESR1 as a candidate gene for boar fertility and sperm quality. Anim. Reprod. Sci. 2011;128:11–21. doi: 10.1016/j.anireprosci.2011.08.008. PubMed DOI
Rago V., Aquila S., Panza R., Carpino A. Cytochrome P450arom, androgen and estrogen receptors in pig sperm. Reprod. Biol. Endocrinol. 2007;5:23. doi: 10.1186/1477-7827-5-23. PubMed DOI PMC
Rago V., Maggiolini M., Vivacqua A., Palma A., Carpino A. Differential expression of estrogen receptors (ERα/ERβ) in testis of mature and immature pigs. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 2004;281:1234–1239. doi: 10.1002/ar.a.20131. PubMed DOI
Pearl C.A., At-Taras E., Berger T., Roser J.F. Reduced endogenous estrogen delays epididymal development but has no effect on efferent duct morphology in boars. Reproduction. 2007;134:593–604. doi: 10.1530/REP-06-0239. PubMed DOI
Pearl C.A., Berger T., Roser J.F. Estrogen and androgen receptor expression in relation to steroid concentrations in the adult boar epididymis. Domest. Anim. Endocrinol. 2007;33:451–459. doi: 10.1016/j.domaniend.2006.09.003. PubMed DOI
Krejčířová R., Maňasová M., Sommerová V., Langhamerová E., Rajmon R., Maňásková-Postlerová P. G protein-coupled estrogen receptor (GPER) in adult boar testes, epididymis and spermatozoa during epididymal maturation. Int. J. Biol. Macromol. 2018;116:113–119. doi: 10.1016/j.ijbiomac.2018.05.015. PubMed DOI
Carreau S., Bouraima-Lelong H., Delalande C. Estrogens–new players in spermatogenesis. Reprod. Biol. 2011;11:174–193. doi: 10.1016/S1642-431X(12)60065-5. PubMed DOI
Aquila S., De Amicis F. Steroid receptors and their ligands: Effects on male gamete functions. Exp. Cell Res. 2014;328:303–313. doi: 10.1016/j.yexcr.2014.07.015. PubMed DOI
Dumasia K., Kumar A., Deshpande S., Sonawane S., Balasinor N. Differential roles of estrogen receptors, ESR1 and ESR2, in adult rat spermatogenesis. Mol. Cell. Endocrinol. 2016;428:89–100. doi: 10.1016/j.mce.2016.03.024. PubMed DOI
Dumasia K., Kumar A., Deshpande S., Balasinor N.H. Estrogen, through estrogen receptor 1, regulates histone modifications and chromatin remodeling during spermatogenesis in adult rats. Epigenetics. 2017;12:953–963. doi: 10.1080/15592294.2017.1382786. PubMed DOI PMC
Krejčířová R., Postlerová P., Rajmon R. Localization of Estrogen Receptors in Male Reproductive Tissues and Sperm Cells–A Review. SAB. 2018;49:274–284. doi: 10.2478/sab-2018-0034. DOI
Nielsen M., Bøgh I.B., Schmidt M., Greve T. Immunohistochemical localization of estrogen receptor-α in sex ducts and gonads of newborn piglets. Histochem. Cell Biol. 2001;115:521–526. doi: 10.1007/s004180100269. PubMed DOI
Hess R., Carnes K. The role of estrogen in testis and the male reproductive tract: A review and species comparison. Anim. Reprod. 2004;1:5–30.
Hess R.A. The Epididymis: From Molecules to Clinical Practice. Springer; Boston, MA, USA: 2002. The efferent ductules: Structure and functions; pp. 49–80.
Hemeida N., Sack W., McEntee K. Ductuli efferentes in the epididymis of boar, goat, ram, bull, and stallion. Am. J. Vet. Res. 1978;39:1892–1900. PubMed
Joseph A., Shur B.D., Ko C., Chambon P., Hess R.A. Epididymal hypo-osmolality induces abnormal sperm morphology and function in the estrogen receptor alpha knockout mouse. Biol. Reprod. 2010;82:958–967. doi: 10.1095/biolreprod.109.080366. PubMed DOI PMC
Gur Y., Breitbart H. Mammalian sperm translate nuclear-encoded proteins by mitochondrial-type ribosomes. Genes Dev. 2006;20:411–416. doi: 10.1101/gad.367606. PubMed DOI PMC
Saberwal G.S., Sharma M., Balasinor N., Choudhary J., Juneja H. Estrogen receptor, calcium mobilization and rat sperm motility. Mol. Cell. Biochem. 2002;237:11–20. doi: 10.1023/A:1016549922439. PubMed DOI
Luconi M., Francavilla F., Porazzi I., Macerola B., Forti G., Baldi E. Human spermatozoa as a model for studying membrane receptors mediating rapid nongenomic effects of progesterone and estrogens. Steroids. 2004;69:553–559. doi: 10.1016/j.steroids.2004.05.013. PubMed DOI
Ded L., Dostalova P., Dorosh A., Dvorakova-Hortova K., Peknicova J. Effect of estrogens on boar sperm capacitation in vitro. Reprod. Biol. Endocrinol. 2010;8:87. doi: 10.1186/1477-7827-8-87. PubMed DOI PMC
Pais V., Leav I., Lau K.-M., Jiang Z., Ho S.-M. Estrogen receptor-β expression in human testicular germ cell tumors. Clin. Cancer. Res. 2003;9:4475–4482. PubMed
Kitiyanant Y., Chaisalee B., Pavasuthipaisit K. Evaluation of the acrosome reaction and viability in buffalo spermatozoa using two staining methods: The effects of heparin and calcium ionophore A23187. Int. J. Androl. 2002;25:215–222. doi: 10.1046/j.1365-2605.2002.00350.x. PubMed DOI
Leahy T., Gadella B.M. Sperm surface changes and physiological consequences induced by sperm handling and storage. Reproduction. 2011;142:759–778. doi: 10.1530/REP-11-0310. PubMed DOI
Cormier N., Bailey J.L. A differential mechanism is involved during heparin-and cryopreservation-induced capacitation of bovine spermatozoa. Biol. Reprod. 2003;69:177–185. doi: 10.1095/biolreprod.102.011056. PubMed DOI
Bailey J., Buhr M. Cryopreservation alters the Ca2+ flux of bovine spermatozoa. Can. J. Anim. Sci. 1994;74:45–51. doi: 10.4141/cjas94-007. DOI
Zhao Y., Buhr M.M. Cryopreservation extenders affect calcium flux in bovine spermatozoa during a temperature challenge. J. Androl. 1995;16:278–285. doi: 10.1002/j.1939-4640.1995.tb00526.x. PubMed DOI
Costello S., Michelangeli F., Nash K., Lefievre L., Morris J., Machado-Oliveira G., Barratt C., Kirkman-Brown J., Publicover S. Ca2+-stores in sperm: Their identities and functions. Reproduction. 2009;138:425–437. doi: 10.1530/REP-09-0134. PubMed DOI PMC
Fukami K., Yoshida M., Inoue T., Kurokawa M., Fissore R.A., Yoshida N., Mikoshiba K., Takenawa T. Phospholipase Cδ4 is required for Ca2+ mobilization essential for acrosome reaction in sperm. J. Cell Biol. 2003;161:79–88. doi: 10.1083/jcb.200210057. PubMed DOI PMC
Nenci I. Receptor and centriole pathways of steroid action in normal and neoplastic cells. Cancer Res. 1978;38:4204–4211. PubMed
Reiffsteck A., Dehennin L., Scholler R. Estrogens in seminal plasma of human and animal species: Identification and quantitative estimation by gas chromatography—Mass spectrometry associated with stable isotope dilution. J. Steroid Biochem. 1982;17:567–572. doi: 10.1016/0022-4731(82)90017-6. PubMed DOI
Lamy J., Corbin E., Blache M.-C., Garanina A.S., Uzbekov R., Mermillod P., Saint-Dizier M. Steroid hormones regulate sperm–oviduct interactions in the bovine. Reproduction. 2017;154:497–508. doi: 10.1530/REP-17-0328. PubMed DOI
Katleba K.D., Legacki E.L., Conley A.J., Berger T. Steroid regulation of early postnatal development in the corpus epididymidis of pigs. J. Endocrinol. 2015;225:125–134. doi: 10.1530/JOE-15-0001. PubMed DOI
Martínez-Traverso G.B., Pearl C.A. Immunolocalization of G protein-coupled estrogen receptor in the rat epididymis. Reprod. Biol. Endocrinol. 2015;13:48. doi: 10.1186/s12958-015-0042-z. PubMed DOI PMC
Publicover S., Harper C.V., Barratt C. [Ca 2+] i signalling in sperm—making the most of what you’ve got. Nat. Cell Biol. 2007;9:235. doi: 10.1038/ncb0307-235. PubMed DOI
Gautier C., Barrier-Battut I., Guénon I., Goux D., Delalande C., Bouraïma-Lelong H. Implication of the estrogen receptors GPER, ESR1, ESR2 in post-testicular maturations of equine spermatozoa. Gen. Comp. Endocrinol. 2016;233:100–108. doi: 10.1016/j.ygcen.2016.05.022. PubMed DOI
Arkoun B., Gautier C., Delalande C., Barrier-Battut I., Guenon I., Goux D., Bouraïma-Lelong H. Stallion spermatozoa: Putative target of estrogens; presence of the estrogen receptors ESR1, ESR2 and identification of the estrogen-membrane receptor GPER. Gen. Comp. Endocrinol. 2014;200:35–43. doi: 10.1016/j.ygcen.2014.02.016. PubMed DOI
Cornwall G.A. Posttranslational Protein Modifications in the Reproductive System. Springer; New York, NY, USA: 2014. Role of posttranslational protein modifications in epididymal sperm maturation and extracellular quality control; pp. 159–180. PubMed DOI
Belleannee C., Belghazi M., Labas V., Teixeira-Gomes A.P., Gatti J.L., Dacheux J.L., Dacheux F. Purification and identification of sperm surface proteins and changes during epididymal maturation. Proteomics. 2011;11:1952–1964. doi: 10.1002/pmic.201000662. PubMed DOI
Prossnitz E.R., Oprea T.I., Sklar L.A., Arterburn J.B. The ins and outs of GPR30: A transmembrane estrogen receptor. J. Steroid Biochem. Mol. Biol. 2008;109:350–353. doi: 10.1016/j.jsbmb.2008.03.006. PubMed DOI PMC
Schwartz N., Verma A., Bivens C.B., Schwartz Z., Boyan B.D. Rapid steroid hormone actions via membrane receptors. Biochim. Biophys. Acta. 2016;1863:2289–2298. doi: 10.1016/j.bbamcr.2016.06.004. PubMed DOI
Wang Z., Zhang X., Shen P., Loggie B.W., Chang Y., Deuel T.F. Identification, cloning, and expression of human estrogen receptor-α36, a novel variant of human estrogen receptor-α66. Biochem. Biophys. Res. Commun. 2005;336:1023–1027. doi: 10.1016/j.bbrc.2005.08.226. PubMed DOI
Walther N., Lioutas C., Tillmann G., Ivell R. Cloning of bovine estrogen receptor beta (ERβ): Expression of novel deleted isoforms in reproductive tissues. Mol. Cell. Endocrinol. 1999;152:37–45. doi: 10.1016/S0303-7207(99)00064-7. PubMed DOI
Shoda T., Hirata S., Kato J., Hoshi K. Cloning of the novel isoform of the estrogen receptor beta cDNA (ERβ isoform M cDNA) from the human testicular cDNA library. J. Steroid Biochem. Mol. Biol. 2002;82:201–208. doi: 10.1016/S0960-0760(02)00186-3. PubMed DOI
Lewandowski S., Kalita K., Kaczmarek L. Estrogen receptor β: Potential functional significance of a variety of mRNA isoforms. Febs Lett. 2002;524:1–5. doi: 10.1016/S0014-5793(02)03015-6. PubMed DOI
Oliveira P.F., Alves M.G., Martins A.D., Correia S., Bernardino R.L., Silva J., Barros A., Sousa M., Cavaco J.E., Socorro S. Expression pattern of G protein-coupled receptor 30 in human seminiferous tubular cells. Gen. Comp. Endocrinol. 2014;201:16–20. doi: 10.1016/j.ygcen.2014.02.022. PubMed DOI
Zimin A.V., Delcher A.L., Florea L., Kelley D.R., Schatz M.C., Puiu D., Hanrahan F., Pertea G., Van Tassell C.P., Sonstegard T.S. A whole-genome assembly of the domestic cow, Bos taurus. Genome Biol. 2009;10:R42. doi: 10.1186/gb-2009-10-4-r42. PubMed DOI PMC
Hillier L.W., Fulton R.S., Fulton L.A., Graves T.A., Pepin K.H., Wagner-McPherson C., Layman D., Maas J., Jaeger S., Walker R. The DNA sequence of human chromosome 7. Nature. 2003;424:157. doi: 10.1038/nature01782. PubMed DOI
Razandi M., Pedram A., Greene G.L., Levin E.R. Cell membrane and nuclear estrogen receptors (ERs) originate from a single transcript: Studies of ERα and ERβ expressed in Chinese hamster ovary cells. Mol. Endocrinol. 1999;13:307–319. doi: 10.1210/mend.13.2.0239. PubMed DOI