Advertisement

Journal of Molecular Histology

, Volume 50, Issue 1, pp 21–34 | Cite as

Hormonal control of vas deferens fluid volume and aquaporin expression in rats

  • Nur Siti Khadijah Ramli
  • Nelli Giribabu
  • Kamarulzaman Karim
  • Naguib SallehEmail author
Original Paper

Abstract

Precise regulation of vas deferens fluid volume which is important for sperm survival might be influenced by testosterone. In order to investigate changes in vas deferens fluid volume and aquoporins (AQP) isoforms expression under testosterone influence, orchidectomized Sprague–Dawley rats were given 125 and 250 µg/kg/day testosterone with or without flutamide, an androgen receptor blocker or finasteride, a 5alpha-reductase inhibitor for seven consecutive days. Following treatment completion, vas deferens was perfused and changes in the fluid secretion rate and osmolality were determined in the presence of acetazolamide. Rats were then sacrificed and vas deferens was harvested for histology, tissue expression and distribution analyses of AQP-1, AQP-2, AQP-5, AQP-7 and AQP-9 proteins by Western blotting and immunohistochemistry, respectively. Our findings indicate that testosterone causes vas deferens fluid secretion rate to increase, which was antagonized by acetazolamide. Fluid osmolality increased following testosterone treatment and further increased when acetazolamide was given. Co-administration of flutamide or finasteride with testosterone causing both fluid secretion rate and osmolality to decrease. Histology revealed increased size of vas deferens lumen with increased thickness of vas deferens stroma. Expression of AQP-1, AQP-2 and AQP-9 were detected in vas deferens but not AQP-5 and AQP-7, and the levels of these proteins were increased by testosterone treatment mainly at the apical membrane of vas deferens epithelium. In conclusion, increased in vas deferens fluid secretion rate under testosterone influence mediated via the up-regulation of AQP-1, 2 and 9 might be important for vas deferens fluid homeostasis in order to ensure normal male fertility.

Keywords

AQP isoforms Vas deferens Testosterone Acetazolamide 

Notes

Acknowledgements

This study was funded by Fundamental research Grant Scheme (FP025-2014A)and PPP Grant (PG230-2015B), University of Malaya, Kuala Lumpur, Malaysia.

Author contribution

NSKR, NG and KK performed the research; NSKR, NG analyzed the data; NSKR wrote the preliminary manuscript while NS critically evaluates the manuscript and prepared the final proof.

Compliance with ethical standards

Conflict of interest

The authors declare that there is no conflict of interest that could be perceived as prejudicing the impartiality of the research reported.

References

  1. Agarwal SK, Gupta A (2008) Aquaporins: the renal water channels. Indian J Nephrol 18:95–100.  https://doi.org/10.4103/0971-4065.43687 CrossRefGoogle Scholar
  2. Arrighi S, Aralla M (2014) Immunolocalization of aquaporin water channels in the domestic cat male genital tract. Reprod Domes Anim 49:17–26  https://doi.org/10.1111/rda.12213 CrossRefGoogle Scholar
  3. Chinigarzadeh A, Muniandy S, Salleh N (2016) Estradiol, progesterone and genistein differentially regulate levels of aquaporin (AQP)-1, 2, 5 and 7 expression in the uteri of ovariectomized, sex-steroid. Defic Rats Steroids 115:47–55.  https://doi.org/10.1016/j.steroids.2016.08.007 CrossRefGoogle Scholar
  4. Chinigarzadeh A, Muniandy S, Salleh N (2017) Combinatorial effect of genistein and female sex-steroids on uterine fluid volume and secretion rate and aquaporin (AQP)-1, 2, 5, and 7 expression in the uterus in rats. Environ Toxicol 32:832–844.  https://doi.org/10.1002/tox.22283 CrossRefGoogle Scholar
  5. Danyu L, Ying L, Zhenwu B, Heming Y, Xuejun L (2008) Aquaporin 1 expression in the testis, epididymis and vas deferens of postnatal ICR mice. Cell Biol Int 32:532–541.  https://doi.org/10.1016/j.cellbi.2008.01.002 CrossRefGoogle Scholar
  6. Domeniconi RF, Orsi AM, Justulin LA Jr, Beu CC, Felisbino SL (2007) Aquaporin 9 (AQP9) localization in the adult dog testis excurrent ducts by immunohistochemistry. Anat Rec (Hoboken, NJ: 2007) 290:1519–1525  https://doi.org/10.1002/ar.20611 Google Scholar
  7. Domeniconi RF, Orsi AM, Justulin LA Jr, Leme Beu CC, Felisbino SL (2008) Immunolocalization of aquaporins 1, 2 and 7 in rete testis, efferent ducts, epididymis and vas deferens of adult dog. Cell Tissue Res 332:329–335.  https://doi.org/10.1007/s00441-008-0592-x CrossRefGoogle Scholar
  8. Duan L, Di Q (2017) Acetazolamide suppresses multi-drug resistance-related protein 1 and P-glycoprotein expression by inhibiting aquaporins expression in a mesial temporal epilepsy rat model medical science monitor: international. Med J Exp Clin Res 23:5818–5825Google Scholar
  9. Estrada M, Varshney A, Ehrlich BE (2006) Elevated testosterone induces apoptosis in neuronal cells. J Biol Chem 281(35):25492–25501CrossRefGoogle Scholar
  10. Gholami K, Muniandy S, Salleh N (2013) In-vivo functional study on the involvement of CFTR, SLC26A6, NHE-1 and CA isoenzymes II and XII in uterine fluid pH, volume and electrolyte regulation in rats under different sex-steroid influence. Int J Med Sci 10:1121–1134.  https://doi.org/10.7150/ijms.5918 CrossRefGoogle Scholar
  11. Gholami K, Muniandy S, Salleh N (2014) Modulation of sodium-bicarbonate co-transporter (SLC4A4/NBCe1) protein and mRNA expression in rat’s uteri by sex-steroids and at different phases of the oestrous cycle. Res Vet Sci 96:164–170.  https://doi.org/10.1016/j.rvsc.2013.11.005 CrossRefGoogle Scholar
  12. Giribabu N, Karim K, Kilari EK, Kassim NM, Salleh N (2018) Anti-inflammatory, antiapoptotic and proproliferative effects of vitis vinifera seed ethanolic extract in the liver of streptozotocin-nicotinamide-induced type 2 diabetes in male rats. Can J Diabetes 42:138–149.  https://doi.org/10.1016/j.jcjd.2017.04.005 CrossRefGoogle Scholar
  13. Gu F et al (2003) Testosterone up-regulates aquaporin-4 expression in cultured astrocytes vol 72.  https://doi.org/10.1002/jnr.10603
  14. Herbst KL, Bhasin S (2004) Testosterone action on skeletal muscle. Curr Opin Clin Nutr Metab Care 7:271–277CrossRefGoogle Scholar
  15. Hermo L, Schellenberg M, Liu LY, Dayanandan B, Zhang T, Mandato CA, Smith CE (2008) Membrane domain specificity in the spatial distribution of aquaporins 5, 7, 9, and 11 in efferent ducts and epididymis of rats. J Histochem Cytochem 56:1121–1135.  https://doi.org/10.1369/jhc.2008.951947 CrossRefGoogle Scholar
  16. Hu Q, Jin J, Zhou H, Yu D, Qian W, Zhong Y, Zhang J, Tang C, Liu P, Zhou Y, Wang X, Sheng L (2018) Crocetin attenuates DHT-induced polycystic ovary syndrome in mice via revising kisspeptin neurons. Biomed Pharmacother 107:1363–1369. https://doi.org/10.1016/j.biopha.2018.08.135 CrossRefGoogle Scholar
  17. Huang H-F, He R-H, Sun C-C, Zhang Y, Meng Q-X, Ma Y-Y (2006a) Function of aquaporins in female and male reproductive systems. Hum Reprod Update 12:785–795.  https://doi.org/10.1093/humupd/dml035 CrossRefGoogle Scholar
  18. Huang HF, He RH, Sun CC, Zhang Y, Meng QX, Ma YY (2006b) Function of aquaporins in female and male reproductive systems. Hum Reprod Update 12:785–795.  https://doi.org/10.1093/humupd/dml035 CrossRefGoogle Scholar
  19. Ismail N, Giribabu N, Muniandy S, Salleh N (2015) Enhanced expression of sodium hydrogen exchanger (NHE)-1, 2 and 4 in the cervix of ovariectomised rats by. Phytoestrogen Genistein Int J Med Sci 12:468–477.  https://doi.org/10.7150/ijms.11210 CrossRefGoogle Scholar
  20. Khadijah Ramli NS, Giribabu N, Muniandy S, Salleh N (2018) Testosterone up-regulates vacuolar ATPase expression and functional activities in vas deferens of. Orchid Rats Theriogenol 108:354–361.  https://doi.org/10.1016/j.theriogenology.2017.12.035 CrossRefGoogle Scholar
  21. Kwon T-H, Frøkiær J, Nielsen S (2013) Regulation of aquaporin-2 in the kidney: a molecular mechanism of body-water homeostasis. Kidney Res Clin Pract 32:96–102.  https://doi.org/10.1016/j.krcp.2013.07.005 CrossRefGoogle Scholar
  22. Lee SH, Zwiazek JJ (2015) Regulation of aquaporin-mediated water transport in arabidopsis roots exposed to NaCl. Plant Cell Physiol 56:750–758.  https://doi.org/10.1093/pcp/pcv003 CrossRefGoogle Scholar
  23. Li L, Mu X, Ye L, Ze Y, Hong F (2018) Suppression of testosterone production by nanoparticulate TiO2 is associated with ERK1/2-PKA-PKC signaling pathways in rat primary cultured Leydig cells. Int J Nanomedicine 13:5909–5924.  https://doi.org/10.2147/IJN.S175608 CrossRefGoogle Scholar
  24. Loh SY, Giribabu N, Salleh N (2017) Effects of gonadectomy and testosterone treatment on aquaporin expression in the kidney of normotensive and hypertensive rats. Exp Biol Med (Maywood NJ) 242:1376–1386.  https://doi.org/10.1177/1535370217703360 CrossRefGoogle Scholar
  25. Lu Y, Li D, W Bi Y, Yu ZM, li H X (2008a) Expression and immunohistochemical localization of aquaporin-1 in male reproductive organs of the mouse 37.  https://doi.org/10.1111/j.1439-0264.2007.00827.x
  26. Lu DY, Li Y, Bi ZW, Yu HM, Li XJ (2008b) Expression and immunohistochemical localization of aquaporin-1 in male reproductive organs of the mouse. Anat Histol Embryol 37:1–8.  https://doi.org/10.1111/j.1439-0264.2007.00827.x CrossRefGoogle Scholar
  27. Masyuk AI, Marinelli RA, LaRusso NF (2002) Water transport by epithelia of the. Dig Tract Gastroenterol 122:545–562.  https://doi.org/10.1053/gast.2002.31035 Google Scholar
  28. Mohd Mokhtar H, Giribabu N, Kassim N, Muniandy S, Salleh N (2014) Testosterone decreases fluid and chloride secretions in the uterus of adult female rats via down-regulating cystic fibrosis transmembrane regulator (CFTR) expression and functional activity J Steroid Biochem Mol Biol 144:361–372  https://doi.org/10.1016/j.jsbmb.2014.08.007 CrossRefGoogle Scholar
  29. Pastor-Soler N et al (2001) Aquaporin 9 expression along the male reproductive tract. Biol Reprod 65:384–393CrossRefGoogle Scholar
  30. Pastor-Soler NM, Fisher JS, Sharpe R, Hill E, Van Hoek A, Brown D, Breton S (2010) Aquaporin 9 expression in the developing rat epididymis is modulated by steroid hormones. Reproduction 139:613–621.  https://doi.org/10.1530/REP-09-0284 CrossRefGoogle Scholar
  31. Pei L, Yang G, Jiang J, Jiang R, Deng Q, Chen B, Gan X (2013) Expression of aquaporins in prostate and seminal vesicles of diabetic rats J Sex Med 10:2975–2985  https://doi.org/10.1111/jsm.12276 CrossRefGoogle Scholar
  32. Ramli NS, Giribabu N, Muniandy S, Salleh N (2016) Testosterone regulates levels of cystic fibrosis transmembrane regulator, adenylate cyclase, and cAMP in the seminal vesicles of orchidectomized rats. Theriogenology 85:238–246.  https://doi.org/10.1016/j.theriogenology.2015.09.036 CrossRefGoogle Scholar
  33. Rojek AM et al (2007) Defective glycerol metabolism in aquaporin 9 (AQP9) knockout mice. Proc Natl Acad Sci USA 104:3609–3614.  https://doi.org/10.1073/pnas.0610894104 CrossRefGoogle Scholar
  34. Ruan YC, Shum WW, Belleannée C, Da Silva N, Breton S (2012a) ATP secretion in the male reproductive tract: essential role of. CFTR J Physiol 590:4209–4222CrossRefGoogle Scholar
  35. Ruan YC, Shum WWC, Belleannée C, Da Silva N, Breton S (2012b) ATP secretion in the male reproductive tract: essential role of CFTR. J Physiol 590:4209–4222.  https://doi.org/10.1113/jphysiol.2012.230581 CrossRefGoogle Scholar
  36. Salleh N, Mokhtar HM, Kassim NM, Giribabu N (2015) Testosterone induces increase in aquaporin (AQP)-1, 5, and 7 expressions in the uteri of ovariectomized. Rats J Membr Biol 248:1097–1105.  https://doi.org/10.1007/s00232-015-9823-8 CrossRefGoogle Scholar
  37. Shahzad H, Giribabu N, Karim K, Muniandy S, Kassim NM, Salleh N (2017) Quercetin alters uterine fluid volume and aquaporin (AQP) subunits (AQP-1, 2, 5 & 7) expression in the uterus in the presence of sex-steroids in rats. Reprod Toxicol (Elmsford. NY) 69:276–285.  https://doi.org/10.1016/j.reprotox.2017.03.012 CrossRefGoogle Scholar
  38. Skowronski MT (2010) Distribution and quantitative changes in amounts of aquaporin 1, 5 and 9 in the pig uterus during the estrous cycle and early pregnancy Reproductive. Biol Endocrinol 8:109.  https://doi.org/10.1186/1477-7827-8-109 CrossRefGoogle Scholar
  39. Skowronski MT, Leska A, Robak A, Nielsen S (2009) Immunolocalization of aquaporin-1, -5, and – 7 in the avian testis and vas deferens. J Histochem Cytochem 57:915–922.  https://doi.org/10.1369/jhc.2009.954057 CrossRefGoogle Scholar
  40. Spritzer MD, Daviau ED, Coneeny MK, Engelman SM, Prince WT, Rodriguez-Wisdom KN (2011) Effects of testosterone on spatial learning and memory in adult male rats. Hormones Behav 59:484–496.  https://doi.org/10.1016/j.yhbeh.2011.01.009 CrossRefGoogle Scholar
  41. Spritzer MD, Fox EC, Larsen GD, Batson CG, Wagner BA, Maher J (2013) Testosterone influences spatial strategy preferences among adult male rats. Hormones Behav 63:800–812.  https://doi.org/10.1016/j.yhbeh.2013.03.018 CrossRefGoogle Scholar
  42. Stevens AL, Breton S, Gustafson CE, Bouley R, Nelson RD, Kohan DE, Brown D (2000) Aquaporin 2 is a vasopressin-independent, constitutive apical membrane protein in rat vas deferens. Am J Physiol Cell Physiol 278:C791–C802.  https://doi.org/10.1152/ajpcell.2000.278.4.C791 CrossRefGoogle Scholar
  43. Tambo A, Roshan MH, Pace NP (2016) Testosterone and cardiovascular disease. Open Cardiovasc Med J 10:1–10.  https://doi.org/10.2174/1874192401610010001 CrossRefGoogle Scholar
  44. Tanimura Y, Hiroaki Y, Fujiyoshi Y (2009) Acetazolamide reversibly inhibits water conduction by aquaporin-4. J Struct Biol 166:16–21.  https://doi.org/10.1016/j.jsb.2008.11.010 CrossRefGoogle Scholar
  45. Toot J et al (2008) Testosterone influences renal electrolyte excretion in SHR/y and WKY males. BMC Physiol 8:5.  https://doi.org/10.1186/1472-6793-8-5 CrossRefGoogle Scholar
  46. Verkman AS, Anderson MO, Papadopoulos MC (2014) Aquaporins: important but elusive drug targets. Nat Rev Drug Discov 13:259–277.  https://doi.org/10.1038/nrd4226 CrossRefGoogle Scholar
  47. Yeung C-H (2010) Aquaporins in spermatozoa and testicular germ cells: identification and potential role Asian. J Androl 12:490–499.  https://doi.org/10.1038/aja.2010.40 Google Scholar
  48. Zhu C, Chen Z, Jiang Z (2016) Expression, distribution and role of aquaporin water channels in human and animal stomach and intestines. Int J Mol Sci 17:1399.  https://doi.org/10.3390/ijms17091399 CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Nur Siti Khadijah Ramli
    • 1
  • Nelli Giribabu
    • 1
  • Kamarulzaman Karim
    • 1
  • Naguib Salleh
    • 1
    Email author
  1. 1.Department of Physiology, Faculty of MedicineUniversity of Malaya, 50603 Lembah PantaiKuala LumpurMalaysia

Personalised recommendations