open access

Vol 79, No 4 (2020)
Original article
Published online: 2020-05-18
Submitted: 2020-01-14
Accepted: 2020-04-24
Get Citation

G protein-coupled oestrogen receptor 1, oestrogen receptors and androgen receptor in the sand rat (Psammomys obesus) efferent ducts

R. Menad, M. Fernini, L. Lakabi, N. Soudani, S. Smaï, X. Bonnet, T. Gernigon-Spychalowicz, E. Moudilou, J.-M. Exbrayat
DOI: 10.5603/FM.a2020.0053
·
Pubmed: 32459366
·
Folia Morphol 2020;79(4):756-766.

open access

Vol 79, No 4 (2020)
ORIGINAL ARTICLES
Published online: 2020-05-18
Submitted: 2020-01-14
Accepted: 2020-04-24

Abstract

Background: The efferent ducts are mainly involved in the reabsorption of the seminiferous tubular fluid. Testosterone and oestrogens regulate efferent ducts functions via their receptors.

Materials and methods:
This paper presents an experimental investigation on the location of the P450 aromatase, the 17-b oestradiol (E2), the androgen receptor (AR), the oestrogen receptor 1 (ESR1), the oestrogen receptor 2 (ESR2) and the G protein-coupled oestrogen receptor 1 (GPER1) in the efferent ducts using Psammomys obesus as an animal model to highlight the effect of the season on the histology and the distribution of these receptors.

Results:
We observed a proliferation of the connective tissue, decreasing in the height of the epithelium during the resting season compared to the breeding season. Ciliated cells expressed P450 aromatase, AR, E2, ESR1, ESR2 and GPER1 during both seasons. Basal cells showed a positive staining for the ESR1 and the GPER1 during both season, the AR and E2 during the breeding season and ESR2 during the resting season.

Conclusions:
Our result shows that the expression of androgen receptor and oestrogen receptors in the efferent ducts vary by season witch suggest that they are largely involved in the regulation of the efferent ducts functions.

Abstract

Background: The efferent ducts are mainly involved in the reabsorption of the seminiferous tubular fluid. Testosterone and oestrogens regulate efferent ducts functions via their receptors.

Materials and methods:
This paper presents an experimental investigation on the location of the P450 aromatase, the 17-b oestradiol (E2), the androgen receptor (AR), the oestrogen receptor 1 (ESR1), the oestrogen receptor 2 (ESR2) and the G protein-coupled oestrogen receptor 1 (GPER1) in the efferent ducts using Psammomys obesus as an animal model to highlight the effect of the season on the histology and the distribution of these receptors.

Results:
We observed a proliferation of the connective tissue, decreasing in the height of the epithelium during the resting season compared to the breeding season. Ciliated cells expressed P450 aromatase, AR, E2, ESR1, ESR2 and GPER1 during both seasons. Basal cells showed a positive staining for the ESR1 and the GPER1 during both season, the AR and E2 during the breeding season and ESR2 during the resting season.

Conclusions:
Our result shows that the expression of androgen receptor and oestrogen receptors in the efferent ducts vary by season witch suggest that they are largely involved in the regulation of the efferent ducts functions.

Get Citation

Keywords

G protein-coupled oestrogen receptor 1, oestrogen receptor, androgen receptor, aromatase, efferent ducts, sand rat

About this article
Title

G protein-coupled oestrogen receptor 1, oestrogen receptors and androgen receptor in the sand rat (Psammomys obesus) efferent ducts

Journal

Folia Morphologica

Issue

Vol 79, No 4 (2020)

Article type

Original article

Pages

756-766

Published online

2020-05-18

DOI

10.5603/FM.a2020.0053

Pubmed

32459366

Bibliographic record

Folia Morphol 2020;79(4):756-766.

Keywords

G protein-coupled oestrogen receptor 1
oestrogen receptor
androgen receptor
aromatase
efferent ducts
sand rat

Authors

R. Menad
M. Fernini
L. Lakabi
N. Soudani
S. Smaï
X. Bonnet
T. Gernigon-Spychalowicz
E. Moudilou
J.-M. Exbrayat

References (79)
  1. Albanito L, Lappano R, Madeo A, et al. Effects of atrazine on estrogen receptor α- and G protein-coupled receptor 30-mediated signaling and proliferation in cancer cells and cancer-associated fibroblasts. Environ Health Perspect. 2015; 123(5): 493–499.
  2. Arrighi S, Romanello MG, Domeneghini C. Ultrastructure of the Epithelium That Lines the Ductuli efferentes in Domestic Equidae, with Particular Reference to Spermatophagy. Cells Tissues Organs. 1994; 149(3): 174–184.
  3. Belhocine M, Gernigon-Spychalowicz T, Jacob MP, et al. Immunoexpression of gelatinase (MMP-2 and MMP-9) in the seminal vesicles and ventral prostate of Libyan jird (Meriones libycus) during the seasonal cycle of reproduction. Histol Histopathol. 2010; 25(5): 619–636.
  4. Belhocine M, Gernigon-Spychalowicz T, Robert AM, et al. Ecophysiological responses of the seminal vesicle of Libyan jird (Meriones libycus) to the Saharan conditions: histological, morphometric and immunohistochemical analysis. Histol Histopathol. 2007; 22(6): 603–615.
  5. Belhocine M. Etude histo-cytologique des variations saisonnièresde l’appareil reproducteur male d’un rongeur déserticole nocturne, le mérion du désert (Meriones Crassus) et de son espèce sympatrique, le mérion de Libye (Meriones libycus). USTHB Algiers. 1998.
  6. Bilińska B, Schmalz-Fraczek B, Sadowska J, et al. Localization of cytochrome P450 aromatase and estrogen receptors alpha and beta in testicular cells--an immunohistochemical study of the bank vole. Acta Histochem. 2000; 102(2): 167–181.
  7. Byers SW, Musto NA, Dym M. Culture of ciliated and nonciliated cells from rat ductuli efferentes. J Androl. 1985; 6(5): 271–278.
  8. Carreau S, Lambard S, Delalande C, et al. Aromatase expression and role of estrogens in male gonad : a review. Reprod Biol Endocrinol. 2003; 1: 35.
  9. Clulow J, Jones RC, Hansen LA, et al. Fluid and electrolyte reabsorption in the ductuli efferentes testis. J Reprod Fertil. 1998: 1–14.
  10. Creasy DM, Chapin RE. Chapter 59 – Male Reproductive System [Internet]. Third Edit. Haschek and Rousseaux’s Handbook of Toxicologic Pathology. Elsevier 2013: 2493–2598.
  11. Danzo BJ. Environmental xenobiotics may disrupt normal endocrine function by interfering with the binding of physiological ligands to steroid receptors and binding proteins. Environ Health Perspect. 1997; 105(3): 294–301.
  12. Eddy EM, Washburn TF, Bunch DO, et al. Targeted disruption of the estrogen receptor gene in male mice causes alteration of spermatogenesis and infertility. Endocrinology. 1996; 137(11): 4796–4805.
  13. Ergün S, Ungefroren H, Holstein AF, et al. Estrogen and progesterone receptors and estrogen receptor-related antigen (ER-D5) in human epididymis. Mol Reprod Dev. 1997; 47(4): 448–455, doi: 10.1002/(SICI)1098-2795(199708)47:4<448::AID-MRD12>3.0.CO;2-S.
  14. Filardo EJ, Graeber CT, Quinn JA, et al. Distribution of GPR30, a seven membrane-spanning estrogen receptor, in primary breast cancer and its association with clinicopathologic determinants of tumor progression. Clin Cancer Res. 2006; 12(21): 6359–6366.
  15. Filardo EJ, Thomas P. GPR30: a seven-transmembrane-spanning estrogen receptor that triggers EGF release. Trends Endocrinol Metab. 2005; 16(8): 362–367.
  16. Fisher JS, Millar MR, Majdic G, et al. Immunolocalisation of oestrogen receptor-alpha within the testis and excurrent ducts of the rat and marmoset monkey from perinatal life to adulthood. J Endocrinol. 1997; 153(3): 485–495.
  17. Gabe M. Histological techniques. Masson. 1976.
  18. Gao F, Ma X, Ostmann AB, et al. GPR30 activation opposes estrogen-dependent uterine growth via inhibition of stromal ERK1/2 and estrogen receptor alpha (ERα) phosphorylation signals. Endocrinology. 2011; 152(4): 1434–1447.
  19. Gernigon T, Malaprade D, Mesbah A, et al. Aspects cytologiques du testicule et de l’épididyme du rat des sables (Psammomys obesus) dans son biotope. Le Rongeur L’esp. 1991: 129–142.
  20. Gernigon-Spychalowicz T. Etudes cytologiques et biochimiques des variationssaisonnières de l’appareil génital mâle d’un rongeur saharien diurne, le rat des sables (Psammomys obesus). USTHB Algiers. 1992.
  21. Goyal HO, Bartol FF, Wiley AA, et al. Immunolocalization of androgen receptor and estrogen receptor in the developing testis and excurrent ducts of goats. Anat Rec. 1997; 249(1): 54–62, doi: 10.1002/(SICI)1097-0185(199709)249:1<54::AID-AR7>3.0.CO;2-F.
  22. Hansen LA, Clulow J, Jones RC. The role of Na+-H+ exchange in fluid and solute transport in the rat efferent ducts. Exp Physiol. 1999; 84(3): 521–527.
  23. Heldring N, Pike A, Andersson S, et al. Estrogen receptors: how do they signal and what are their targets. Physiol Rev. 2007; 87(3): 905–931.
  24. Hermo L, Oka R, Morales C. Secretion and endocytosis in the male reproductive tract: a role in sperm maturation. Int Rev Cytol. 1994: 105–189.
  25. Hess RA, Fernandes SAF, Gomes GRO, et al. Estrogen and its receptors in efferent ductules and epididymis. J Androl. 2011; 32(6): 600–613.
  26. Hess RA, Zhou Q, Nie R, et al. Estrogens and epididymal function. Reprod Fertil Dev. 2001; 13(4): 273–283.
  27. Hess RA. Estrogen in the adult male reproductive tract : A review. 2003; 14: 1–14.
  28. Hess R. The efferent ductules: structure and functions. The Epididymis: From Molecules to Clinical Practice. Springer. 2002: 49–80.
  29. Hess RA, Gist DH, Bunick D, et al. Estrogen receptor (alpha and beta) expression in the excurrent ducts of the adult male rat reproductive tract. J Androl. 1997; 18(6): 602–611.
  30. Huang GS, Gunter MJ, Arend RC, et al. Co-expression of GPR30 and ERbeta and their association with disease progression in uterine carcinosarcoma. Am J Obstet Gynecol. 2010; 203(3): 242.e1–242.e5.
  31. Ilio KY, Hess RA. Structure and function of the ductuli efferentes: a review. Microsc Res Tech. 1994; 29(6): 432–467.
  32. Joseph A, Hess R, Schaeffer D, et al. Absence of estrogen receptor alpha leads to physiological alterations in the mouse epididymis and consequent defects in sperm function1. Biology of Reproduction. 2010; 82(5): 948–957.
  33. Joseph A, Shur BD, Hess RA. Estrogen, efferent ductules, and the epididymis. Biol Reprod. 2011; 84(2): 207–217.
  34. Khammar F. Variations saisonnières de l’activité endocrine de deuxespèces de rongeurs désertiques, le rat des sables (Psammomysobesus) et la gerbille (Gerbillus gerbillus). USTHB Algiers. 1987.
  35. Kwon S, Hess RA, Bunick D, et al. Estrogen receptors are present in the epididymis of the rooster. J Androl. 1997; 18(4): 378–384.
  36. Lee KH, Bunick D, Lamprecht G, et al. Differential Expression of Genes Important to Efferent Ductules Ion Homeostasis across Postnatal Development in Estrogen Receptor-慣 Knockout and Wildtype Mice. Asian-Australasian J Anim Sci. 2008; 21(4): 510–522.
  37. Lee KH, Finnigan-Bunick C, Bahr J, et al. Estrogen regulation of ion transporter messenger RNA levels in mouse efferent ductules are mediated differentially through estrogen receptor (ER) alpha and ER beta. Biol Reprod. 2001; 65(5): 1534–1541.
  38. Leung GPH, Cheung KH, Leung CT, et al. Regulation of epididymal principal cell functions by basal cells: role of transient receptor potential (Trp) proteins and cyclooxygenase-1 (COX-1). Mol Cell Endocrinol. 2004; 216(1-2): 5–13.
  39. Liverman CS, Brown JW, Sandhir R, et al. Role of the oestrogen receptors GPR30 and ERalpha in peripheral sensitization: relevance to trigeminal pain disorders in women. Cephalalgia. 2009; 29(7): 729–741.
  40. Lucas TFG, Royer C, Siu ER, et al. Expression and signaling of G protein-coupled estrogen receptor 1 (GPER) in rat sertoli cells. Biol Reprod. 2010; 83(2): 307–317.
  41. Martoja R, Martoja-Pierson M. Initiation aux techniques de l’histologie animale. 1967.
  42. Menad R, Fernini M, Smaï S, et al. GPER1 in sand rat epididymis: Effects of seasonal variations, castration and efferent ducts ligation. Anim Reprod Sci. 2017; 183: 9–20.
  43. Menad R, Smaï S, Moudilou E, et al. Immunolocalization of estrogen and androgen receptors in the caput epididymidis of the fat sand rat (Psammomys obesus): Effects of seasonal variations, castration and efferent duct ligation. Acta Histochem. 2014; 116(4): 559–569.
  44. Menad R, Smaï S, Bonnet X, et al. Seasonal variations of aromatase and estrogen receptors expression in the testis of free-ranging sand rats. Acta Histochem. 2017; 119(4): 382–391.
  45. Menad R. Régionalisation structurale et fonctionnelle de l’épididyme d’un rongeur déserticole diurne, psammomys obesus CRETZSCHMAR, 1828. USTHB Algiers. 2008.
  46. Mobilio C, Campus A. Osservazioni sull’epididimo dei nostri animali domestici. Arch Ital Anat Embriol. 1912; 11: 419–479.
  47. Nanjappa MK, Hess RA, Medrano TI, et al. Membrane-Localized Estrogen Receptor 1 Is Required for Normal Male Reproductive Development and Function in Mice. Endocrinology. 2016; 157(7): 2909–2919.
  48. Nie R, Zhou Q, Jassim E, et al. Differential expression of estrogen receptors alpha and beta in the reproductive tracts of adult male dogs and cats. Biol Reprod. 2002; 66(4): 1161–1168.
  49. Oliveira CA, Carnes K, França LR, et al. Infertility and testicular atrophy in the antiestrogen-treated adult male rat. Biol Reprod. 2001; 65(3): 913–920.
  50. Oliveira CA, Mahecha GAB, Carnes K, et al. Differential hormonal regulation of estrogen receptors ERalpha and ERbeta and androgen receptor expression in rat efferent ductules. Reproduction. 2004; 128(1): 73–86.
  51. Oliveira CA, Zhou Q, Carnes K, et al. ER function in the adult male rat: short- and long-term effects of the antiestrogen ICI 182,780 on the testis and efferent ductules, without changes in testosterone. Endocrinology. 2002; 143(6): 2399–2409.
  52. Oliveira RL, Nogueira JC, Mahecha GAB, et al. Seasonal variation in estrogen receptor ERα, but not ERβ, androgen receptor and aromatase, in the efferent ductules and epididymis of the big fruit-eating bat Artibeus lituratus. Gen Comp Endocrinol. 2012; 179(1): 1–13.
  53. Oliveira RL, Oliveira CA. Reproductive biology of male bats: anatomy, physiology and endocrinology. Bats Biol Bahavior Conserv Nov Sci Publ New York. 2011: 135–75.
  54. Pereira MFN, Fernandes SAF, Nascimento AR, et al. Effects of the oestrogen receptor antagonist Fulvestrant on expression of genes that affect organization of the epididymal epithelium. Andrology. 2014; 2(4): 559–571.
  55. Pereyra-Martinez AC, Roselli CE, Stadelman HL, et al. Cytochrome P450 aromatase in testis and epididymis of male rhesus monkeys. Endocrine. 2001; 16(1): 15–9.
  56. Prossnitz ER, Arterburn JB, Sklar LA. NIH Public Access. 2008; 505: 138–142.
  57. Prossnitz ER, Barton M. Estrogen biology: new insights into GPER function and clinical opportunities. Mol Cell Endocrinol. 2014; 389(1-2): 71–83.
  58. Prossnitz ER, Barton M. The G-protein-coupled estrogen receptor GPER in health and disease. Nat Rev Endocrinol. 2011; 7(12): 715–726.
  59. Rago V, Maggiolini M, Vivacqua A, et al. Differential expression of estrogen receptors (ERalpha/ERbeta) in testis of mature and immature pigs. Anat Rec A Discov Mol Cell Evol Biol. 2004; 281(2): 1234–1239.
  60. Rago V, Romeo F, Giordano F, et al. Identification of the estrogen receptor GPER in neoplastic and non-neoplastic human testes. Reprod Biol Endocrinol. 2011; 9: 135.
  61. Revankar CM, Cimino DF, Sklar LA, et al. A transmembrane intracellular estrogen receptor mediates rapid cell signaling. Science. 2005; 307(5715): 1625–1630.
  62. Roselli CE, West NB, Brenner RM. Androgen receptor and 5 alpha-reductase activity in the ductuli efferentes and epididymis of adult rhesus macaques. Biol Reprod. 1991; 44(4): 739–745.
  63. Rosenfeld CS, Ganjam VK, Taylor JA, et al. Transcription and translation of estrogen receptor-beta in the male reproductive tract of estrogen receptor-alpha knock-out and wild-type mice. Endocrinology. 1998; 139(6): 2982–2987.
  64. Saunders PT, Sharpe RM, Williams K, et al. Differential expression of oestrogen receptor alpha and beta proteins in the testes and male reproductive system of human and non-human primates. Mol Hum Reprod. 2001; 7(3): 227–236.
  65. Sheng ZG, Zhu BZ. Low concentrations of bisphenol A induce mouse spermatogonial cell proliferation by G protein-coupled receptor 30 and estrogen receptor-α. Environ Health Perspect. 2011; 119(12): 1775–1780.
  66. Sirianni R, Chimento A, Ruggiero C, et al. The novel estrogen receptor, G protein-coupled receptor 30, mediates the proliferative effects induced by 17beta-estradiol on mouse spermatogonial GC-1 cell line. Endocrinology. 2008; 149(10): 5043–5051.
  67. Stanišić V, Lonard D, O’Malley B. Modulation of Steroid Hormone Receptor Activity. Progress in Brain Research. Elsevier. 2010: 153–176.
  68. Stoffel MH, Friess AE. Morphological characteristics of boar efferent ductules and epididymal duct. Microsc Res Tech. 1994; 29(6): 411–431.
  69. Terasawa E, Noel SD, Keen KL. Rapid action of oestrogen in luteinising hormone-releasing hormone neurones: the role of GPR30. J Neuroendocrinol. 2009; 21(4): 316–321.
  70. Toda K, Okada T, Hayashi Y, et al. Preserved tissue structure of efferent ductules in aromatase-deficient mice. J Endocrinol. 2008; 199(1): 137–146.
  71. Tsubota T, Howell-Skalla L, Nitta H, et al. Seasonal changes in spermatogenesis and testicular steroidogenesis in the male black bear Ursus americanus. J Reprod Fertil. 1997; 109(1): 21–27.
  72. Ungefroren H, Ivell R, Ergün S. Region-specific expression of the androgen receptor in the human epididymis. Mol Hum Reprod. 1997; 3(11): 933–940.
  73. Van Pe, De Ro, Van De, et al. Gustafsson J-A, Kuiper GGJM. Ontogeny of estrogen receptor-β expression in rat testis. Endocrinology. 1999; 140(1): 478–83.
  74. Vaucher L, Funaro MG, Mehta A, et al. Activation of GPER-1 estradiol receptor downregulates production of testosterone in isolated rat Leydig cells and adult human testis. PLoS One. 2014; 9(4): e92425.
  75. West NB, Brenner RM. Estrogen receptor in the ductuli efferentes, epididymis, and testis of rhesus and cynomolgus macaques. Biol Reprod. 1990; 42(3): 533–538.
  76. Zhang H, Sheng X, Hu X, et al. Seasonal changes in spermatogenesis and immunolocalization of cytochrome P450 17alpha-hydroxylase/c17-20 lyase and cytochrome P450 aromatase in the wild male ground squirrel (Citellus dauricus Brandt). J Reprod Dev. 2010; 56(3): 297–302.
  77. Zhang KS, Chen HQ, Chen YS, et al. Bisphenol A stimulates human lung cancer cell migration via upregulation of matrix metalloproteinases by GPER/EGFR/ERK1/2 signal pathway. Biomed Pharmacother. 2014; 68(8): 1037–1043.
  78. Zhou Q, Clarke L, Nie R, et al. Estrogen action and male fertility: roles of the sodium/hydrogen exchanger-3 and fluid reabsorption in reproductive tract function. Proc Natl Acad Sci. 2001; 98(24): 14132–14137.
  79. Zhou Q, Nie R, Prins GS, et al. Localization of androgen and estrogen receptors in adult male mouse reproductive tract. J Androl. 2002; 23(6): 870–881.

Important: This website uses cookies. More >>

The cookies allow us to identify your computer and find out details about your last visit. They remembering whether you've visited the site before, so that you remain logged in - or to help us work out how many new website visitors we get each month. Most internet browsers accept cookies automatically, but you can change the settings of your browser to erase cookies or prevent automatic acceptance if you prefer.

By  "Via Medica sp. z o.o." sp.k., Świętokrzyska 73, 80–180 Gdańsk, Poland

tel.:+48 58 320 94 94, faks:+48 58 320 94 60, e-mail:  viamedica@viamedica.pl