Skip to main content

Advertisement

Log in

Cellular and subcellular localization of aquaporins 1, 3, 8, and 9 in amniotic membranes during pregnancy in mice

  • Regular Article
  • Published:
Cell and Tissue Research Aims and scope Submit manuscript

Abstract

The amniotic membrane encloses the amniotic fluid and plays roles in the regulation of amniotic fluid flux through the intramembranous pathway during pregnancy. Aquaporins (AQPs) 1, 3, 8, and 9 are expressed in amniotic membranes. AQPs are water channel proteins that facilitate the rapid flux of water or small molecules across the plasma membrane. Recently, additional roles of AQPs in facilitating cell migration, proliferation, and apoptosis have been suggested, with AQPs being distributed in the appropriate subcellular regions for their functions. The cellular and subcellular distributions of AQPs in the amniotic membrane however remain unclear. We have examined the cellular and subcellular localization of AQPs in amniotic membranes during pregnancy in mice. After embryonic day 12 (E12), AQP1 was distributed in the plasma membrane of finely branched cell processes in the amniotic fibroblasts. AQP3 was present in both epithelial cells and fibroblasts between E10 and E12. The distribution of AQP3 in the epithelial cells dynamically changed as follows: at E14 in the lateral membrane and apical junction; at E16 in the lateral membrane alone; at E17 in the lateral membrane and cytoplasm. AQP8 was expressed in the epithelial cells and complementarily localized in the apical junction and the lateral membrane. AQP9 was detected only in the apoptotic cells of the epithelium. These cellular and subcellular localizations of amniotic AQPs indicate that each AQP plays distinct functional roles, such as in water and urea transport, cell migration, cell proliferation, and apoptosis, for amniotic fluid homeostasis or tissue remodeling of amniotic membranes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Altuntas A, Yilmaz MD, Aktepe F, Kahveci OK, Derekoy S, Dilek H, Serteser M (2006) Expression and distribution of aquaporin-1 in nasal polyps: does it have any significance in edema formation? Am J Rhinol 20:128–131

    PubMed  Google Scholar 

  • Ananth CV, Oyelese Y, Srinivas N, Yeo L, Vintzileos AM (2004) Preterm premature rupture of membranes, intrauterine infection, and oligohydramnios: risk factors for placental abruption. Obstet Gynecol 104:71–77

    PubMed  Google Scholar 

  • Beall MH, Wijngaard JP van den, Gemert MJ van, Ross MG (2007a) Regulation of amniotic fluid volume. Placenta 28:824–832

    Article  CAS  PubMed  Google Scholar 

  • Beall MH, Wang S, Yang B, Chaudhri N, Amidi F, Ross MG (2007b) Placental and membrane aquaporin water channels: correlation with amniotic fluid volume and composition. Placenta 28:421–428

    Article  CAS  PubMed  Google Scholar 

  • Brace RA (1997) Physiology of amniotic fluid volume regulation. Clin Obstet Gynecol 40:280–289

    Article  CAS  PubMed  Google Scholar 

  • Brace RA, Vermin ML, Huijssoon E (2004) Regulation of amniotic fluid volume: intramembranous solute and volume fluxes in late gestation fetal sheep. Am J Obstet Gynecol 191:837–846

    Article  PubMed  Google Scholar 

  • Calamita G, Ferri D, Bazzini C, Mazzone A, Botta G, Liquori GE, Paulmichl M, Portincasa P, Meyer G, Svelto M (2005) Expression and subcellular localization of the AQP8 and AQP1 water channels in the mouse gall-bladder epithelium. Biol Cell 97:415–423

    Article  CAS  PubMed  Google Scholar 

  • Cao C, Sun Y, Healey S, Bi Z, Hu G, Wan S, Kouttab N, Chu W, Wan Y (2006) EGFR-mediated expression of aquaporin-3 is involved in human skin fibroblast migration. Biochem J 400:225–234

    Article  CAS  PubMed  Google Scholar 

  • Cohly HH, Isokpehi R, Rajnarayanan RV (2008) Compartmentalization of aquaporins in the human intestine. Int J Environ Res Public Health 5:115–119

    CAS  PubMed  Google Scholar 

  • Faber JJ, Anderson DF (2002) Absorption of amniotic fluid by amniochorion in sheep. Am J Physiol Heart Circ Physiol 282:H850–H854

    CAS  PubMed  Google Scholar 

  • Hara-Chikuma M, Verkman AS (2008a) Aquaporin-3 facilitates epidermal cell migration and proliferation during wound healing. J Mol Med 86:221–231

    Article  CAS  PubMed  Google Scholar 

  • Hara-Chikuma M, Verkman AS (2008b) Prevention of skin tumorigenesis and impairment of epidermal cell proliferation by targeted aquaporin-3 gene disruption. Mol Cell Biol 28:326–332

    Article  CAS  PubMed  Google Scholar 

  • Harman CR (2008) Amniotic fluid abnormalities. Semin Perinatol 32:288–294

    Article  PubMed  Google Scholar 

  • Hayashi M, Zhu K, Sagesaka T, Fukasawa I, Inaba N (2008) Amniotic fluid levels of tumor necrosis factor-alpha and soluble tumor necrosis factor receptor 1 before and after the onset of labor in normal pregnancies. Horm Metab Res 40:251–256

    Article  CAS  PubMed  Google Scholar 

  • Hoque MO, Soria JC, Woo J, Lee T, Lee J, Jang SJ, Upadhyay S, Trink B, Monitto C, Desmaze C, Mao L, Sidransky D, Moon C (2006) Aquaporin 1 is overexpressed in lung cancer and stimulates NIH-3T3 cell proliferation and anchorage-independent growth. Am J Pathol 168:1345–1353

    Article  CAS  PubMed  Google Scholar 

  • Huang HF, He RH, Sun CC, Zhang Y, Meng QX, Ma YY (2006) Function of aquaporins in female and male reproductive systems. Hum Reprod Update 12:785–795

    Article  CAS  PubMed  Google Scholar 

  • Hung TH, Hsieh CC, Hsu JJ, Lo LM, Chiu TH, Hsieh TT (2007) Risk factors for placental abruption in an Asian population. Reprod Sci 14:59–65

    Article  PubMed  Google Scholar 

  • Huysseune S, Kienlen-Campard P, Hebert S, Tasiaux B, Leroy K, Devuyst O, Brion JP, De Strooper B, Octave JN (2009) Epigenetic control of aquaporin 1 expression by the amyloid precursor protein. FASEB J 23:4158–4167

    Article  CAS  PubMed  Google Scholar 

  • Ishibashi K, Hara S, Kondo S (2009) Aquaporin water channels in mammals. Clin Exp Nephrol 13:107–117

    Article  CAS  PubMed  Google Scholar 

  • Jablonski EM, Webb AN, McConnell NA, Riley MC, Hughes FM Jr (2004) Plasma membrane aquaporin activity can affect the rate of apoptosis but is inhibited after apoptotic volume decrease. Am J Physiol Cell Physiol 286:C975–C985

    Article  CAS  PubMed  Google Scholar 

  • Jessica Chen M, Sepramaniam S, Armugam A, Shyan Choy M, Manikandan J, Melendez AJ, Jeyaseelan K, Sang Cheung N (2008) Water and ion channels: crucial in the initiation and progression of apoptosis in central nervous system? Curr Neuropharmacol 6:102–116

    Article  PubMed  Google Scholar 

  • Johnston H, Koukoulas I, Jeyaseelan K, Armugam A, Earnest L, Baird R, Dawson N, Ferraro T, Wintour EM (2000) Ontogeny of aquaporins 1 and 3 in ovine placenta and fetal membranes. Placenta 21:88–99

    Article  CAS  PubMed  Google Scholar 

  • Kataoka S, Furuta I, Yamada H, Kato EH, Ebina Y, Kishida T, Kobayashi N, Fujimoto S (2002) Increased apoptosis of human fetal membranes in rupture of the membranes and chorioamnionitis. Placenta 23:224–231

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi K, Inai T, Shibata Y, Yasui M (2009) Dynamic changes in amniotic tight junctions during pregnancy. Placenta 30:840–847

    Article  CAS  PubMed  Google Scholar 

  • Lei H, Furth EE, Kalluri R, Chiou T, Tilly KI, Tilly JL, Elkon KB, Jeffrey JJ, Strauss JF 3rd (1996) A program of cell death and extracellular matrix degradation is activated in the amnion before the onset of labor. J Clin Invest 98:1971–1978

    Article  CAS  PubMed  Google Scholar 

  • Lingwood BE, Wintour EM (1983) Permeability of ovine amnion and amniochorion to urea and water. Obstet Gynecol 61:227–232

    CAS  PubMed  Google Scholar 

  • Liu H, Zheng Z, Wintour EM (2008) Aquaporins and fetal fluid balance. Placenta 29:840–847

    Article  CAS  PubMed  Google Scholar 

  • Loitto VM, Huang C, Sigal YJ, Jacobson K (2007) Filopodia are induced by aquaporin-9 expression. Exp Cell Res 313:1295–1306

    Article  CAS  PubMed  Google Scholar 

  • 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 240:324–328

    Article  CAS  PubMed  Google Scholar 

  • Matsumoto LC, Cheung CY, Brace RA (2000) Effect of esophageal ligation on amniotic fluid volume and urinary flow rate in fetal sheep. Am J Obstet Gynecol 182:699–705

    Article  CAS  PubMed  Google Scholar 

  • Maymon E, Ghezzi F, Edwin SS, Mazor M, Yoon BH, Gomez R, Romero R (1999) The tumor necrosis factor alpha and its soluble receptor profile in term and preterm parturition. Am J Obstet Gynecol 181:1142–1148

    Article  CAS  PubMed  Google Scholar 

  • Menon R, Lombardi SJ, Fortunato SJ (2002) TNF-alpha promotes caspase activation and apoptosis in human fetal membranes. J Assist Reprod Genet 19:201–204

    Article  PubMed  Google Scholar 

  • Minami S, Kobayashi H, Yamashita A, Yanagita T, Uezono Y, Yokoo H, Shiraishi S, Saitoh T, Asada Y, Komune S, Wada A (2001) Selective expression of aquaporin 1, 4 and 5 in the rat middle ear. Hear Res 158:51–56

    Article  CAS  PubMed  Google Scholar 

  • Mittal P, Romero R, Mazaki-Tovi S, Tromp G, Tarca AL, Kim YM, Chaiworapongsa T, Kusanovic JP, Erez O, Than NG, Hassan SS (2009) Fetal membranes as an interface between inflammation and metabolism: increased aquaporin 9 expression in the presence of spontaneous labor at term and chorioamnionitis. J Matern Fetal Neonatal Med 22:1167–1175

    Article  CAS  PubMed  Google Scholar 

  • Monzani E, Bazzotti R, Perego C, La Porta CA (2009) AQP1 is not only a water channel: it contributes to cell migration through Lin7/beta-catenin. PLoS ONE 4:e6167

    Article  PubMed  Google Scholar 

  • Nagahara M, Waguri-Nagaya Y, Yamagami T, Aoyama M, Tada T, Inoue K, Asai K, Otsuka T (2010) TNF-alpha-induced aquaporin 9 in synoviocytes from patients with OA and RA. Rheumatology (Oxford) 49:898–906

    Article  CAS  Google Scholar 

  • Nielsen S, King LS, Christensen BM, Agre P (1997) Aquaporins in complex tissues. II. Subcellular distribution in respiratory and glandular tissues of rat. Am J Physiol 273:C1549–C1561

    CAS  PubMed  Google Scholar 

  • Nielsen S, Frokiaer J, Marples D, Kwon TH, Agre P, Knepper MA (2002) Aquaporins in the kidney: from molecules to medicine. Physiol Rev 82:205–244

    CAS  PubMed  Google Scholar 

  • Papadopoulos MC, Saadoun S, Verkman AS (2008) Aquaporins and cell migration. Pflugers Arch 456:693–700

    Article  CAS  PubMed  Google Scholar 

  • Qi H, Li L, Zong W, Hyer BJ, Huang J (2009) Expression of aquaporin 8 is diversely regulated by osmotic stress in amnion epithelial cells. J Obstet Gynaecol Res 35:1019–1025

    Article  CAS  PubMed  Google Scholar 

  • Risher WC, Andrew RD, Kirov SA (2009) Real-time passive volume responses of astrocytes to acute osmotic and ischemic stress in cortical slices and in vivo revealed by two-photon microscopy. Glia 57:207–221

    Article  PubMed  Google Scholar 

  • Saadoun S, Papadopoulos MC, Hara-Chikuma M, Verkman AS (2005) Impairment of angiogenesis and cell migration by targeted aquaporin-1 gene disruption. Nature 434:786–792

    Article  CAS  PubMed  Google Scholar 

  • Tsukita S, Furuse M (2000) The structure and function of claudins, cell adhesion molecules at tight junctions. Ann NY Acad Sci 915:129–135

    Article  CAS  PubMed  Google Scholar 

  • Underwood MA, Gilbert WM, Sherman MP (2005) Amniotic fluid: not just fetal urine anymore. J Perinatol 25:341–348

    Article  PubMed  Google Scholar 

  • Verkman AS, Hara-Chikuma M, Papadopoulos MC (2008) Aquaporins—new players in cancer biology. J Mol Med 86:523–529

    Article  CAS  PubMed  Google Scholar 

  • Watson KJ, Kim I, Baquero AF, Burks CA, Liu L, Gilbertson TA (2007) Expression of aquaporin water channels in rat taste buds. Chem Senses 32:411–421

    Article  CAS  PubMed  Google Scholar 

  • Wintour EM, Shandley L (1993) Effects of fetal fluid balance on amniotic fluid volume. Semin Perinatol 17:158–172

    CAS  PubMed  Google Scholar 

  • Zhang Z, Chen Z, Song Y, Zhang P, Hu J, Bai C (2010) Expression of aquaporin 5 increases proliferation and metastasis potential of lung cancer. J Pathol 221:210–220

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Masato Yasui.

Additional information

This work was supported by a Grant-in-Aid for Young Scientists (20790177) from the Japan Society of Promotion of Science, a Grant-in-Aid for Specially Promoted Research from the Ministry of Education, Culture, Sports, Science, and Technology (MEXT) of Japan, and a Grant-in-Aid for Global Center-of-Excellence Program for Human Metabolomic Systems Biology from MEXT.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kobayashi, K., Yasui, M. Cellular and subcellular localization of aquaporins 1, 3, 8, and 9 in amniotic membranes during pregnancy in mice. Cell Tissue Res 342, 307–316 (2010). https://doi.org/10.1007/s00441-010-1065-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00441-010-1065-6

Keyword

Navigation