Journal of Molecular Histology

, Volume 38, Issue 1, pp 87–95 | Cite as

Aquaporins are upregulated in glandular epithelium at the time of implantation in the rat

  • Laura A. Lindsay
  • Christopher R. Murphy
Original Paper


Regulation of luminal fluid is essential for blastocyst implantation. While it has been known for quite some time that there is a reduction in the amount of luminal fluid at the time of implantation, the mechanisms regulating this process are only just emerging. Previous studies have shown an upregulation of aquaporin (AQP) 5 channels in luminal epithelial cells at the time of implantation providing a mechanism for fluid reabsorption across the surface epithelium. However to date the contribution of fluid reabsorption by glandular epithelial cells has not been established. This study using reverse transcriptase polymerase chain reaction demonstrates the presence of several AQP isoforms in the rat uterus at the time of implantation while immunofluorescence data demonstrates an apical distribution of AQPs5 and 9 in the glandular epithelium at the time of implantation. The presence of AQPs5 and 9 in the apical plasma membrane of the glandular epithelium seen in this study provides a mechanism for transcellular fluid transport across these glandular epithelial cells similar to that seen in luminal epithelial cells. The reabsorption of glandular fluid via AQP channels may also regulate luminal fluid volume and be involved in the reduction in luminal fluid seen at the time of implantation.


Pregnancy Glandular epithelium Aquaporins 


  1. Akman MA, Erden HF, Bahceci M (2005) Endometrial fluid visualized through ultrasonography during ovarian stimulation in IVF cycles impairs the outcome in tubal factor, but not PCOS, patients. Hum Reprod 20:906–909PubMedCrossRefGoogle Scholar
  2. Anderson JN, Clark JH, Peck EJ Jr (1972) The relationship between nuclear receptor-estrogen binding and uterotrophic responses. Biochem Biophys Res Commun 48:1460–1468PubMedCrossRefGoogle Scholar
  3. Borgnia M, Nielsen S, Engel A, Agre P (1999) Cellular and molecular biology of the aquaporin water channels. Annu Rev Biochem 68:425–458PubMedCrossRefGoogle Scholar
  4. Damiano AE, Zotta E, Ibarra C (2006) Functional and molecular expression of AQP9 channel and UT-A transporter in normal and preeclamptic human placentas. Placenta 27:1073–1081PubMedCrossRefGoogle Scholar
  5. Enders A, Schlafke S (1967) A morphological analysis of the early implantation stages in the rat. Am J Anat 120:185–225CrossRefGoogle Scholar
  6. Fujita A, Horio Y, Nielsen S, Nagelhus EA, Hata F, Ottersen OP, Kurachi Y (1999) High-resolution immunogold cytochemistry indicates that AQP4 is concentrated along the basal membrane of parietal cell in rat stomach. FEBS Lett 459:305–309PubMedCrossRefGoogle Scholar
  7. Given RL, Enders AC (1981) Mouse uterine glands during the peri-implantation period. II. Autoradiographic studies. Anat Rec 199:109–127PubMedCrossRefGoogle Scholar
  8. He RH, Sheng JZ, Luo Q, Jin F, Wang B, Qian YL, Zhou CY, Sheng X, Huang HF (2006) Aquaporin-2 expression in human endometrium correlates with serum ovarian steroid hormones. Life Sci 79:423–429PubMedCrossRefGoogle Scholar
  9. Hildenbrand A, Lalitkumar L, Nielsen S, Gemzell-Danielsson K, Stavreus-Evers A (2006) Expression of aquaporin 2 in human endometrium. Fertil Steril 86:1452–1458PubMedCrossRefGoogle Scholar
  10. Jablonski EM, McConnell NA, Hughes FM Jr, Huet-Hudson YM (2003) Estrogen regulation of aquaporins in the mouse uterus: potential roles in uterine water movement. Biol Reprod 69:1481–1487PubMedCrossRefGoogle Scholar
  11. Kobayashi M, Takahashi E, Miyagawa S, Watanabe H, Iguchi T (2006) Chromatin immunoprecipitation-mediated target identification proved aquaporin 5 is regulated directly by estrogen in the uterus. Genes Cells 11:1133–1143PubMedCrossRefGoogle Scholar
  12. Li X, Yu H, Koide SS (1994) The water channel gene in human uterus. Biochem Mol Biol Int 32:371–377PubMedGoogle Scholar
  13. Lindsay LA, Murphy CR (2004a) Aquaporin-1 increases in the rat myometrium during early pregnancy. J Mol Histol 35:75–79CrossRefGoogle Scholar
  14. Lindsay LA, Murphy CR (2004b) Redistribution of aquaporins in uterine epithelial cells at the time of implantation in the rat. Acta Histochem 106:299–307CrossRefGoogle Scholar
  15. Lindsay LA, Murphy CR (2006) Redistribution of aquaporins 1 and 5 in the rat uterus is dependent on progesterone: a study with light and electron microscopy. Reproduction 131:369–378PubMedCrossRefGoogle Scholar
  16. Ljungkvist I (1971a) Attachment reaction of rat uterine luminal epithelium. II. The effect of progesterone on the morphology of the uterine glands and the luminal epithelium of the spayed, virgin rat. Acta Soc Med Ups 76:110–126Google Scholar
  17. Ljungkvist I (1971b) Attachment reaction of rat uterine luminal epithelium. III. The effect of estradiol, estrone and estriol on the morphology of the luminal epithelium of the spayed, virgin rat. Acta Soc Med Ups 76:139–157Google Scholar
  18. Ljungkvist I (1972) Attachment reaction of rat uterine luminal epithelium. IV. The cellular changes in the attachment reaction and its hormonal regulation. Fertil Steril 23:847–865PubMedGoogle Scholar
  19. Ma T, Yang B, Verkman AS (1997) Cloning of a novel water and urea-permeable aquaporin from mouse expressed strongly in colon, placenta, liver, and heart. Biochem Biophys Res Commun 240:324–328PubMedCrossRefGoogle Scholar
  20. Matthews CJ, Thomas EJ, Redfern CP, Hirst BH (1993) Ion transport by human endometrial epithelia in vitro. Hum Reprod 8:1570–1575PubMedGoogle Scholar
  21. Mobasheri A, Wray S, Marples D (2005) Distribution of AQP2 and AQP3 water channels in human tissue microarrays. J Mol Histol 36:1–14PubMedCrossRefGoogle Scholar
  22. Naftalin RJ, Thiagarajah JR, Pedley KC, Pocock VJ, Milligan SR (2002) Progesterone stimulation of fluid absorption by the rat uterine gland. Reproduction 123:633–638PubMedCrossRefGoogle Scholar
  23. Offenberg H, Barcroft LC, Caveney A, Viuff D, Thomsen PD, Watson AJ (2000) mRNAs encoding aquaporins are present during murine preimplantation development. Mol Reprod Dev 57:323–330PubMedCrossRefGoogle Scholar
  24. Parvin MN, Tsumura K, Akamatsu T, Kanamori N, Hosoi K (2002) Expression and localisation of AQP5 in the stomach and duodenum of the rat. Biochim Biophys Acta 1542:116–124PubMedCrossRefGoogle Scholar
  25. Richard C, Gao J, Brown N, Reese J (2003) Aquaporin water channel genes are differentially expressed and regulated by ovarian steroids during the periimplantation period in the mouse. Endocrinology 144:1533–1541PubMedCrossRefGoogle Scholar
  26. Verkman AS, Mitra AK (2000) Structure and function of aquaporin water channels. Am J Physiol Renal Physiol 278:F13–F28PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, Inc. 2007

Authors and Affiliations

  1. 1.School of Medical Sciences (Anatomy and Histology)The University of SydneySydneyAustralia

Personalised recommendations