Contractions transport exfoliated epithelial cells through the neonatal epididymis

in Reproduction

Correspondence should be addressed to R Middendorff; Email: ralf.middendorff@anatomie.med.uni-giessen.de
Restricted access

Contractions of the adult epididymal duct are well known in the context of sperm transport. Some reports also describe contractions of the epididymal duct during development, but data about their character, regulation and function are sparse. In the foetal human epididymis we found luminal cells and could identify them as exfoliated epithelial cells originating from the epididymis and not from testis by using antibodies against neutral endopeptidase as an epithelial epididymal duct marker. Exfoliated cells were also found in the epididymal duct after birth. Time-lapse imaging revealed directional transport of luminal cells in the neonatal rat epididymis interrupted by pendular movement. Spontaneous contractions were discovered in the neonatal epididymis and an association between these contractions and the transport of the luminal cells could be observed. Both, transport and spontaneous contractions, were affected significantly by substances known to contract (noradrenaline) or relax (the phosphodiesterase 5 inhibitor sildenafil) smooth muscle cells. Immunohistochemistry showed staining for the proliferation marker proliferating-cell-nuclear-antigen (PCNA) in cells of the ductal lumen of the neonatal rat epididymis indicating the extrusion of cells also during proliferation. Our data showed spontaneous contractions of the immature epididymal duct associated with the transport of exfoliated luminal cells before the first occurrence of sperm cells. Results suggest an important role including both (i) a mechanical place holder function of exfoliated luminal cells (ii) together with a novel idea of organized waste disposal of these cells during development.

 

     An official journal of

    Society for Reproduction and Fertility

 

Sept 2018 onwards Past Year Past 30 Days
Abstract Views 104 104 104
Full Text Views 8 8 8
PDF Downloads 5 5 5
  • AbeKTakanoHItoT 1984 Interruption of the luminal flow in the epididymal duct of the corpus epididymidis in the mouse, with special reference to differentiation of the epididymal epithelium. Archivum Histologicum Japonicum 47 137147. (https://doi.org/10.1679/aohc.47.137)

    • Search Google Scholar
    • Export Citation
  • BattagliaG 1958 Sulla motilita dell’epididimo del ratto in colture organotipiche rotanti. Archivio Italiano di Anatomia e di Embriologia 63 4755.

    • Search Google Scholar
    • Export Citation
  • BegueliniMRGóesRMRahalPMorielle-VersuteETabogaSR 2015 Impact of the processes of total testicular regression and recrudescence on the epididymal physiology of the bat Myotis nigricans (Chiroptera: Vespertilionidae). PLoS ONE 10 e0128484. (https://doi.org/10.1371/journal.pone.0128484)

    • Search Google Scholar
    • Export Citation
  • BouchardMSouabniAMandlerMNeubüserABusslingerM 2002 Nephric lineage specification by Pax2 and Pax8. Genes and Development 16 29582970. (https://doi.org/10.1101/gad.240102)

    • Search Google Scholar
    • Export Citation
  • Campolina-SilvaGHHessRAOliveiraCA 2019 Seasonal variation of cell proliferation and apoptosis in the efferent ductules and epididymis of the Neotropical bat Artibeus lituratus (Chiroptera, Phyllostomidae). General and Comparative Endocrinology 273 310. (https://doi.org/10.1016/j.ygcen.2018.02.003)

    • Search Google Scholar
    • Export Citation
  • ChenHRuanYCXuWMChenJChanHC 2012 Regulation of male fertility by CFTR and implications in male infertility. Human Reproduction Update 18 703713. (https://doi.org/10.1093/humupd/dms027)

    • Search Google Scholar
    • Export Citation
  • ClermontYFlanneryJ 1970 Mitotic activity in the epithelium of the epididymis in young and old adult rats. Biology of Reproduction 3 283292. (https://doi.org/10.1093/biolreprod/3.3.283)

    • Search Google Scholar
    • Export Citation
  • CosentinoMJCockettAT 1986 Structure and function of the epididymis. Urological Research 14 229240.

  • DavidoffMSMiddendorffRMayerBdeVenteJKoeslingDHolsteinAF 1997 Nitric oxide/cGMP pathway components in the Leydig cells of the human testis. Cell and Tissue Research 287 161170. (https://doi.org/10.1007/s004410050742)

    • Search Google Scholar
    • Export Citation
  • DycheWJ 1979 A comparative study of the differentiation and involution of the Mullerian duct and Wolffian duct in the male and female fetal mouse. Journal of Morphology 162 175209. (https://doi.org/10.1002/jmor.1051620203)

    • Search Google Scholar
    • Export Citation
  • ElfgenVMietensAMeweMHauTMiddendorffR 2018 Contractility of the epididymal duct – function, regulation and potential drug effects. Reproduction 156 R125R141. (https://doi.org/10.1530/REP-17-0754)

    • Search Google Scholar
    • Export Citation
  • HermoLBarinKRobaireB 1992 Structural differentiation of the epithelial cells of the testicular excurrent duct system of rats during postnatal development. Anatomical Record 233 205228. (https://doi.org/10.1002/ar.1092330205)

    • Search Google Scholar
    • Export Citation
  • HibJCaldeyro-BarciaR 1974 Neurohormonal control of epididymal contractions. Basic Life Sciences 4 111126. (https://doi.org/10.1007/978-1-4684-2892-6_8)

    • Search Google Scholar
    • Export Citation
  • HintonBTGaldamezMMSutherlandABomgardnerDXuBAbdel-FattahRYangL 2011 How do you get six meters of epididymis inside a human scrotum? Journal of Andrology 32 558564. (https://doi.org/10.2164/jandrol.111.013029)

    • Search Google Scholar
    • Export Citation
  • HirashimaT 2014 Pattern formation of an epithelial tubule by mechanical instability during epididymal development. Cell Reports 9 866873. (https://doi.org/10.1016/j.celrep.2014.09.041)

    • Search Google Scholar
    • Export Citation
  • JaakkolaUMTaloA 1982 Relation of electrical activity to luminal transport in the cauda epididymidis of the rat in vitro. Journal of Reproduction and Fertility 64 121126. (https://doi.org/10.1530/jrf.0.0640121)

    • Search Google Scholar
    • Export Citation
  • JaakkolaUMTaloA 1983 Movements of the luminal contents in two different regions of the caput epididymidis of the rat in vitro. Journal of Physiology 336 453463. (https://doi.org/10.1113/jphysiol.1983.sp014590)

    • Search Google Scholar
    • Export Citation
  • KnightTW 1972 In vivo effects of oxytocin on the contractile activity of the cannulated epididymis and vas deferens in rams. Journal of Reproduction and Fertility 28 141. (https://doi.org/10.1530/jrf.0.0280141)

    • Search Google Scholar
    • Export Citation
  • KnightTW 1974 A qualitative study of factors affecting the contractions of the epididymis and ductus deferens of the ram. Journal of Reproduction and Fertility 40 1929. (https://doi.org/10.1530/jrf.0.0400019)

    • Search Google Scholar
    • Export Citation
  • LuschnigSUvA 2014 Luminal matrices: an inside view on organ morphogenesis. Experimental Cell Research 321 6470. (https://doi.org/10.1016/j.yexcr.2013.09.010)

    • Search Google Scholar
    • Export Citation
  • MietensATaschSFeuerstackeCEichnerGVolkmannJSchermulyRTGrimmingerFMüllerDMiddendorffR 2012 Phosphodiesterase 5 (PDE5) inhibition, ANP and NO rapidly reduce epididymal duct contractions, but long-term PDE5 inhibition in vivo does not. Molecular and Cellular Endocrinology 349 145153. (https://doi.org/10.1016/j.mce.2011.09.039)

    • Search Google Scholar
    • Export Citation
  • MietensATaschSStammlerAKonradLFeuerstackeCMiddendorffR 2014 Time-lapse imaging as a tool to investigate contractility of the epididymal duct – effects of cGMP signaling. PLoS ONE 9 e92603. (https://doi.org/10.1371/journal.pone.0092603)

    • Search Google Scholar
    • Export Citation
  • ParkerGAPicutCA 2016 Atlas of Histology of the Juvenile Rat. Boston: Academic Press.

  • PicutCARemickAKde RijkEPCTSimonsMLStumpDGParkerGA 2015 Postnatal development of the testis in the rat: morphologic study and correlation of morphology to neuroendocrine parameters. Toxicologic Pathology 43 326342. (https://doi.org/10.1177/0192623314547279)

    • Search Google Scholar
    • Export Citation
  • RobaireBHintonBT 2014 The epididymis. In Knobil and Neill’s Physiology of Reproduction. Eds PlantTM & ZeleznikAJ. Elsevier Science.

  • RobaireBHintonBTOrgebin-CristM-C 2006 The epididymis. In Knobil and Neill’s Physiology of Reproduction3rd ed. Ed NeillJD. Elsevier Science.

    • Search Google Scholar
    • Export Citation
  • SimonPBäumnerSBuschORöhrichRKaeseMRichterichPWehrendAMüllerKGerardy-SchahnRMühlenhoffM et al. 2013 Polysialic acid is present in mammalian semen as a post-translational modification of the neural cell adhesion molecule NCAM and the polysialyltransferase ST8SiaII. Journal of Biological Chemistry 288 1882518833. (https://doi.org/10.1074/jbc.M113.451112)

    • Search Google Scholar
    • Export Citation
  • SimonPFeuerstackeCKaeseMSaboorFMiddendorffRGaluskaSP 2015 Polysialylation of NCAM characterizes the proliferation period of contractile elements during postnatal development of the epididymis. PLoS ONE 10 e0123960. (https://doi.org/10.1371/journal.pone.0123960)

    • Search Google Scholar
    • Export Citation
  • SujaritSJonesRC 1991 3Hthymidine uptake by the epididymis, seminal vesicles and prostate gland during postnatal development of the rat. Reproduction Fertility and Development 3 313319. (https://doi.org/10.1071/RD9910313)

    • Search Google Scholar
    • Export Citation
  • SunELFlickingerCJ 1979 Development of cell types and of regional differences in the postnatal rat epididymis. American Journal of Anatomy 154 2755. (https://doi.org/10.1002/aja.1001540104)

    • Search Google Scholar
    • Export Citation
  • TaloAJaakkolaUMMarkkula-ViitanenM 1979 Spontaneous electrical activity of the rat epididymis in vitro. Journal of Reproduction and Fertility 57 423429. (https://doi.org/10.1530/jrf.0.0570423)

    • Search Google Scholar
    • Export Citation
  • ThongAMüllerDFeuerstackeCMietensAStammlerAMiddendorffR 2014 Neutral endopeptidase (CD10) is abundantly expressed in the epididymis and localized to a distinct population of epithelial cells – its relevance for CNP degradation. Molecular and Cellular Endocrinology 382 234243. (https://doi.org/10.1016/j.mce.2013.09.027)

    • Search Google Scholar
    • Export Citation
  • van de VeldeRLRisleyPL 1963 The origin and development of smooth muscle and contractility in the ductus epididymidis of the rat. Journal of Embryology and Experimental Morphology 11 369382.

    • Search Google Scholar
    • Export Citation