Development and Reproduction (한국발생생물학회지:발생과생식)

The Korean Society of Developmental Biology (한국발생생물학회)
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Differential Expressions of Aquaporin Subtypes in Female Reproductive Tract of Mice

  • Im, Ji Woo (Dept. of Physiology, College of Medicine, Dong-A University) ;
  • Lee, Chae Young (Dept. of Physiology, College of Medicine, Dong-A University) ;
  • Kim, Dong-Hwan (Human Life Research Center, Dong-A University) ;
  • Bae, Hae-Rahn (Dept. of Physiology, College of Medicine, Dong-A University)
  • Received : 2020.08.01
  • Accepted : 2020.09.18
  • Published : 2020.09.30
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Abstract

Although many aquaporin (AQP) transcripts have been demonstrated to express in the female reproductive tract, the defined localizations and functions of AQP subtype proteins remain unclear. In this study, we investigated the expression of AQP1, AQP3, AQP5, AQP6, and AQP9 proteins in female reproductive tract of mouse and characterized their precise localizations at the cellular and subcellular levels. Immunofluorescence analyses for AQP1, AQP3, AQP6, and AQP9 showed that these proteins were abundantly expressed in female reproductive tract and that intense immunoreactivities were observed in mucosa epithelial cells with a subtype-specific pattern. The most abundant aquaporin in both vagina and uterine cervix was AQP3. Each of AQP1, AQP3, AQP6, and AQP9 exhibited its distinct distribution in stratified squamous or columnar epithelial cells. AQP9 expression was predominant in oviduct and ovary. AQP1, AQP3, AQP6, and AQP9 proteins were mostly seen in apical membrane of ciliated epithelial cells of the oviduct as well as in both granulosa and theca cells of ovarian follicles. Most of AQP subtypes were also expressed in surface epithelial cells and glandular cells of endometrium in the uterus, but their expression levels were relatively lower than those observed in the vagina, uterine cervix, oviduct and ovary. This is the first study to investigate the expression and localization of 5 AQP subtype proteins simultaneously in female reproductive tract of mouse. Our results suggest that AQP subtypes work together to transport water and glycerol efficiently across the mucosa epithelia for lubrication, proliferation, energy metabolism and pH regulation in female reproductive tract.

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References

  1. Calamita G, Perret J, Delporte C (2018) Aquaglyceroporins: Drug targets for metabolic diseases? Front Physiol 9:851. https://doi.org/10.3389/fphys.2018.00851
  2. Dajani S, Saripalli A, Sharma-Walia N (2018) Water transport proteins-aquaporins (AQPs) in cancer biology. Oncotarget 9:36392-36405. https://doi.org/10.18632/oncotarget.26351
  3. Galan-Cobo A, Ramirez-Lorca R, Serna A, Echevarria M (2015) Overexpression of AQP3 modifies the cell cycle and the proliferation rate of mammalian cells in culture. PLoS One 10:e0137692. https://doi.org/10.1371/journal.pone.0137692
  4. Galan-Cobo A, Ramirez-Lorca R, Toledo-Aral JJ, Echevarria M (2016) Aquaporin-1 plays important role in proliferation by affecting cell cycle progression. J Cell Physiol 231:243-256. https://doi.org/10.1002/jcp.25078
  5. Geng X, McDermott J, Lundgren J, Liu L, Tsai KJ, Shen J, Liu Z (2017) Role of AQP9 in transport of monomethyselenic acid and selenite. Biometals 30:747-755. https://doi.org/10.1007/s10534-017-0042-x
  6. Hall JE, Mathias RT (2014) The aquaporin zero puzzle. Biophys J 107:10-15. https://doi.org/10.1016/j.bpj.2014.05.023
  7. Hara M, Ma T, Verkman AS (2002) Selectively reduced glycerol in skin of aquaporin-3-deficienct mice may account for impaired skin hydration, elasticity, and barrier recovery. J Biol Chem 227:46616-46621. https://doi.org/10.1074/jbc.M209003200
  8. 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. https://doi.org/10.1093/humupd/dml035
  9. Ikeda M, Beitz E, Kozono D, Guggino WB, Agre P, Yasui M (2002) Characterization of aquaporin-6 as a nitrate channel in mammalian cells. Requirement of pore-lining residue threonine 63. J Biol Chem 277:39873-39879. https://doi.org/10.1074/jbc.M207008200
  10. Ishibashi K, Hara S, Kondo S (2009) Aquaporin water channels in mammals. Clin Exp Nephol 13:107-117. https://doi.org/10.1007/s10157-008-0118-6
  11. Kim SO, Oh KJ, Lee HS, Ahn K, Kim SW, Park K (2011) Expression of aquaporin water channels in the vagina in premenopausal women. J Sex Med 8:1925-1930. https://doi.org/10.1111/j.1743-6109.2011.02284.x
  12. Lee HJ, Jee BC, Kim SK, Kim H, Lee JR, Suh CS, Kim SH (2016) Expressions of aquaporin family in human luteinized granulosa cells and their correlations with IVF outcomes. Hum Reprod 31:822-831. https://doi.org/10.1093/humrep/dew006
  13. Ma J, Zhou C, Yang J, Ding X, Zhu Y, Chen X (2016) Expression of AQP6 and AQP8 in epithelial ovarian tumor. J Mol Histol 47:129-134 https://doi.org/10.1007/s10735-016-9657-4
  14. Ma T, Song Y, Yang B, Gillespie A, Carlson EJ, Epstein CJ, Verkman AS (2000) Nephrogenic diabetes insipidus in mice lacking aquaporin-3 water channels. Proc Natl Acad Sci USA 97:4386-4391. https://doi.org/10.1073/pnas.080499597
  15. Morinaga T, Nakakoshi M, Hirao A, Imai M, Ishibashi K (2002) Mouse aquaporin 10 gene (AQP10) is a pseudogene. Biochem Biophys Res Commun 294:630-634. https://doi.org/10.1016/S0006-291X(02)00536-3
  16. Nah WH, Oh YS, Hwang JH, Gye MC (2015) Changes in aquaporin 5 in the non-ciliated cells of mouse oviduct according to sexual maturation and oestrous cycle. Reprod Fertil Dev 29:336-344. https://doi.org/10.1071/rd15186
  17. 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 57:323-330. https://doi.org/10.1002/1098-2795(200012)57:4<323::AID-MRD3>3.0.CO;2-5
  18. Ohshiro K, Yaoita E, Yoshida Y, Fujinaka H, Matsuki A, Kamiie J, Kovalenko P, Yamamoto T (2001) Expression and immunolocalization of AQP6 in intercalated cells of the rat kidney collecting duct. Arch Histol Cytol 64:329-338. https://doi.org/10.1679/aohc.64.329
  19. Rojek AM, Skowronski MT, Fuchtbauer EM, Fuchtbauer AC, Fenton RA, Agre P, Frokiaer J, Nielsen S (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
  20. Seo MJ, Lim JH, Kim DH, Bae HR (2018) Loss of aquaporin-3 in placenta and fetal membranes induces growth restriction in mice. Dev Reprod 22:263-273. https://doi.org/10.12717/DR.2018.22.3.263
  21. Skowronski MT, Kwon TH, Nielsen S (2009) Immunolocalization of aquaporin 1, 5, and 9 in the female pig reproductive system. J Histochem Cytochem 57:61-67. https://doi.org/10.1369/jhc.2008.952499
  22. Verkman AS (2005) Novel roles of aquaporins revealed by phenotype analysis of knock-out mice. Rev Physiol Biochem Pharmacol 155:31-55. https://doi.org/10.1007/3-540-28217-3_2
  23. Verkman AS (2011) Aquaporins at a glance. J Cell Sci 124:2107-2112. https://doi.org/10.1242/jcs.079467
  24. Verkman AS (2012) Aquaporins in clinical medicine. Annu Rev Med 63:303-316. https://doi.org/10.1146/annurev-med-043010-193843
  25. Yang C, Lim W, Bae H, Song G (2016) Aquaporin 3 is regulated by estrogen in the chicken oviduct and is involved in progression of epithelial cell-derived ovarian carcinomas. Domest Anim Endocrinol 55:97-106. https://doi.org/10.1016/j.domaniend.2015.12.003
  26. Yasui M (2009) pH regulated anion permeability of aquaporin-6. Handb Exp Pharmacol 190:299-308. https://doi.org/10.1007/978-3-540-79885-9_15
  27. Zhu C, Jiang Z, Bazer FW, Johnson GA, Burghardt RC, Wu G (2015a) Aquaporins in the female reproductive system of mammals. Front Biosci (Landmark Ed) 20:838-871. https://doi.org/10.2741/4341
  28. Zhu J, Xia J, Jiang J, Jiang R, He Y, Lin H (2015b) Effects of estrogen deprivation on expression of aquaporins in rat vagina. Menopause 22:893-898. https://doi.org/10.1097/GME.0000000000000403