This study aimed to examine the effect of follicle-stimulating hormone (FSH), luteinizing hormone (LH), prolactin (PRL), and growth hormone (GH) on Aquaporin 5 (AQP5) expression in granulosa (Gc) and theca cells (Tc) from medium (MF) and large (LF) ovarian follicles of pigs. The results showed that GH significantly decreased the expression of AQP5 in Gc from MF in relation to the control. In the Gc of large follicles, PRL stimulated the expression of AQP5. However, the increased expression of AQP5 in the Tc of LF was indicated by GH and PRL in relation to the control. A significantly higher expression of the AQP5 protein in the Gc from MF and LF was indicated by FSH and PRL. In co-cultures, an increased expression of AQP5 was observed in the Gc from LF incubated with LH, PRL, and GH. A significantly increased expression of AQP5 was also observed in co-cultures of Tc from all type of follicles incubated with LH, whereas PRL stimulated the expression of AQP5 in Tc from MF. Moreover, AQP5 protein expression increased in the co-culture isolated from MF and LF after treatment with FSH, LH, PRL, and GH. AQP5 immunoreactivity was observed in the cytoplasm, mainly in the perinuclear region and endosomes, as well as in the cell membranes of Gc and Tc from the LF and MF.

Department of Anatomy Poznan University of Medical Sciences 61 701 Poznan Poland

Department of Animal Anatomy and Physiology University of Warmia and Mazury in Olsztyn 10 719 Olsztyn Poland

Department of Animal Physiology The Kielanowski Institute of Animal Physiology and Nutrition Polish Academy of Sciences 05 110 Jabłonna Poland

Department of Histology and Embryology; Poznan University of Medical Sciences 61 701 Poznan Poland

Department of Human Physiology School of Medicine University of Warmia and Mazury in Olsztyn 10 752 Olsztyn Poland

Department of Obstetrics and Gynecology University Hospital and Masaryk University 602 00 Brno Czech Republic

Interdisciplinary Center of Modern Technology Nicolaus Copernicus University in Torun 87 100 Torun Poland

Veterinary Center Nicolaus Copernicus University in Torun 87 100 Torun Poland

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Preston G.M., Carroll T.P., Guggino W.B., Agre P. Appearance of water channels in Xenopus oocytes expressing red cell CHIP28 protein. Science. 1992;256:385–387. doi: 10.1126/science.256.5055.385. PubMed DOI

Verkman A.S. Aquaporins. Curr. Biol. 2013;23:R52–R55. doi: 10.1016/j.cub.2012.11.025. PubMed DOI PMC

Verkman A.S., Mitra A.K. Structure and function of aquaporin water channels. Am. J. Physiol. Renal. Physiol. 2000;278:13–28. doi: 10.1152/ajprenal.2000.278.1.F13. PubMed DOI

Carbrey J.M., Agre P. Discovery of the aquaporins and development of the field. Handb. Exp. Pharm. 2009:3–28. doi: 10.1007/978-3-540-79885-9. PubMed DOI

Skowronski M.T., Lebeck J., Rojek A., Praetorius J., Füchtbauer E.M., Frøkiaer J., Nielsen S. AQP7 is localized in capillaries of adipose tissue, cardiac and striated muscle: implications in glycerol metabolism. Am. J. Physiol. Renal. Physiol. 2007;292:956–965. doi: 10.1152/ajprenal.00314.2006. PubMed DOI

Rojek A.M., Skowronski M.T., Füchtbauer E.M., Füchtbauer A.C., Fenton R.A., Agre P., Frøkiaer J., Nielsen S. Defective glycerol metabolism in aquaporin 9 (AQP9) knockout mice. Proc. Natl. Acad. Sci. USA. 2007;104:3609–3614. doi: 10.1073/pnas.0610894104. PubMed DOI PMC

Bragiel A.M., Wang D., Pieczonka T.D., Shono M., Ishikawa Y. Mechanisms Underlying Activation of α1-Adrenergic Receptor-Induced Trafficking of AQP5 in Rat Parotid Acinar Cells under Isotonic or Hypotonic Conditions. Int. J. Mol. Sci. 2017;17:1022. doi: 10.3390/ijms17071022. PubMed DOI PMC

Li X., Yu H., Koide S.S. The water channel gene in human uterus. Biochem. Mol. Biol. Int. 1994;32:371–377. PubMed

Escobar J., Gormaz M., Arduini A., Gosens K., Martinez A., Perales A., Escrig R., Tormos E., Roselló M., Orellana C., et al. Expression of aquaporins early in human pregnancy. Early Human Develop. 2012;88:589–594. doi: 10.1016/j.earlhumdev.2012.01.009. PubMed DOI

Klein C., Troedsson M.H., Rutllant J. Expression of aquaporin water channels in equine endometrium is differentially regulated during the oestrous cycle and early pregnancy. Reprod. Domest. Anim. 2012;48:529–537. doi: 10.1111/rda.12116. PubMed DOI

Kobayashi M., Takahashi E., Miyagawa S., Watanabe H., Iguichi T. Chromatin immunoprecipitation mediated target identification proved aquaporin 5 is regulated directly by estrogen in the uterus. Genes Cells. 2006;11:1133–1143. doi: 10.1111/j.1365-2443.2006.01009.x. PubMed DOI

Lindsay L.A., Murphy C.R. Redistribution of aquaporins 1 and 5 in the rat uterus is dependent on progesterone: a study with light and electron microscopy. Reprod. 2006;131:369–378. doi: 10.1530/rep.1.00914. PubMed DOI

Richard C., Gao J., Brown N., Reese J. Aquaporin water channel genes are differentially expressed and regulated by ovarian steroids during the periimplantation period in the mouse. Endocrinology. 2003;144:1533–1541. doi: 10.1210/en.2002-0033. PubMed DOI

Jablonski E.M., McConnell N.A., Hughes F.M., Jr., Huet-Hudson Y.M. Estrogen regulation of aquaporins in the mouse uterus: potential roles in uterine water movement. Biol. Reprod. 2003;69:1481–1487. doi: 10.1095/biolreprod.103.019927. PubMed DOI

Hildenbrand A., Lalitkumar L., Nielsen S., Genzell-Danilsson K., Stavreus- Evers A. Expression of aquaporin 2 in human endometrium. Fertil. Steril. 2006;86:1452–1458. doi: 10.1016/j.fertnstert.2006.03.058. PubMed DOI

Zou L.B., Zhang R.J., Tan Y.J., Ding G.L., Shi S., Zhang D., He R.H., Liu A.X., Wang T.T., Leung P.C.K., et al. Identification of Estrogen Response Element in the Aquaporin-2 Gene That Mediates Estrogen-Induced Cell Migration and Invasion in Human Endometrial Carcinoma. J. Clin. Endocrinol. Metab. 2011;96:1399–1408. doi: 10.1210/jc.2011-0426. PubMed DOI

Ducza E., Seres A.B., Hajagos-Tóth J., Falkay G., Gáspár R. Oxytocin regulates the expression of aquaporin 5 in the late-pregnant rat uterus. Mol. Reprod. Dev. 2014;81:524–530. doi: 10.1002/mrd.22320. PubMed DOI

Csányi A., Bóta J., Falkay G., Gáspár R., Ducza E. The Effects of Female Sexual Hormones on the Expression of Aquaporin 5 in the Late-Pregnant Rat Uterus. Int. J. Mol. Sci. 2016;17:1300. doi: 10.3390/ijms17081300. PubMed DOI PMC

Ducza E., Csányi A., Gáspár R. Aquaporins during Pregnancy: Their Function and Significance. Int. J. Mol. Sci. 2017;18:2593. doi: 10.3390/ijms18122593. PubMed DOI PMC

Skowronski M.T., Kwon T.H., Nielsen S. Immunolocalization of aquaporin 1, 5 and 9 in the female pig reproductive system. J. Histochem. Cytochem. 2009;57:61–67. doi: 10.1369/jhc.2008.952499. PubMed DOI PMC

Lindsay L.A., Murphy C.R. Aquaporins are upregulated in glandular epithelium at the time of implantation in the rat. J. Mol. Hist. 2007;38:87–95. doi: 10.1007/s10735-007-9083-8. PubMed DOI

Thoroddsen A., Dahm-Kähler P., Lind A.K., Weijdegård B., Lindenthal B., Müller J., Brännström M. The water permeability channels aquaporins 1–4 are differentially expressed in granulosa and theca cells of the preovulatory follicle during precise stages of human ovulation. J. Clin. Endocrinol. Metab. 2011;96:1021–1028. doi: 10.1210/jc.2010-2545. PubMed DOI

McConnell N.A., Yunus R.S., Gross S.A., Bost K.L., Clemens M.G., Hughes F.M., Jr. Water permeability of an ovarian antral follicle is predominantly transcellular and mediated by aquaporins. Endocrinology. 2002;143:2905–2912. doi: 10.1210/endo.143.8.8953. PubMed DOI

Starowicz A., Grzesiak M., Mobasheri A., Szoltys M. Immunolocalization of aquaporin 5 during rat ovarian follicle development and expansion of the preovulatory cumulus oophorus. Acta. Histochem. 2014;116:457–465. doi: 10.1016/j.acthis.2013.10.001. PubMed DOI

Rodgers R.J., Irving-Rodgers H.F. Formation of the ovarian follicular antrum and follicular fluid. Biol. Reprod. 2010;82:1021–1029. doi: 10.1095/biolreprod.109.082941. PubMed DOI

Skowronski M.T. Distribution and quantitative changes in amounts of aquaporin 1, 5 and 9 in the pig uterus during the estrous cycle and early pregnancy. Reprod. Biol. Endocrinol. 2010;8:109. doi: 10.1186/1477-7827-8-109. PubMed DOI PMC

Skowronski M.T., Skowronska A., Nielsen S. Fluctuation of aquaporin 1, 5, and 9 expression in the pig oviduct during the estrous cycle and early pregnancy. J. Histochem. Cytochem. 2011;59:419–427. doi: 10.1369/0022155411400874. PubMed DOI PMC

Skowronski M.T., Mlotkowska P., Tanski D., Lepiarczyk E., Oklinski M.K., Nielsen S., Skowronska A. Pituitary Gonadotropins, Prolactin and Growth Hormone Differentially Regulate AQP1 Expression in the Porcine Ovarian Follicular Cells. Int. J. Mol. Sci. 2018;19:5. doi: 10.3390/ijms19010005. PubMed DOI PMC

Britt K.L., Findlay J.K. Estrogen actions in the ovary revisited. J. Endocrinol. 2002;175:269–276. doi: 10.1677/joe.0.1750269. PubMed DOI

Filicori M., Cognigni G.E., Gamberini E., Parmegiani L., Troilo E., Roset B. Efficacy of low-dose human chorionic gonadotropin alone to complete controlled ovarian stimulation. Fertil. Steril. 2005;84:394–401. doi: 10.1016/j.fertnstert.2005.02.036. PubMed DOI

Skowronska A., Mlotkowska P., Okrasa S., Nielsen S., Skowronski M.T. Modulatory effects of steroid hormones, oxytocin, arachidonic acid, forskolin and cyclic AMP on the expression of aquaporin 1 and aquaporin 5 in the porcine uterus during placentation. J. Physiol. Pharmacol. 2016;67:311–319. PubMed

Skowronska A., Mlotkowska P., Majewski M., Nielsen S., Skowronski M.T. Expression of aquaporin 1 and 5 and their regulation by ovarian hormones, arachidonic acid, forskolin and cAMP during implantation in pigs. Physiol. Res. 2016;65:637–650. PubMed

Chen Q., Peng H., Lei L., Zhang Y., Kuang H., Cao Y., Shi Q.X., Ma T., Duan E. Aquaporin3 is a sperm water channel essential for postcopulatory sperm osmoadaptation and migration. Cell Res. 2011;21:922–933. doi: 10.1038/cr.2010.169. PubMed DOI PMC

Sun X.L., Zhang J., Fan Y., Ding J.H., Sha J.H., Hu G. Aquaporin-4 deficiency induces subfertility in female mice. Fertil. Steril. 2008;92:1736–1743. doi: 10.1016/j.fertnstert.2008.07.1785. PubMed DOI

Su W., Qiao Y., Yi F., Guan X., Zhang D., Zhang S., Hao F., Xiao Y., Zhang H., Guo L., et al. Increased female fertility in aquaporin 8-deficient mice. IUBMB Life. 2010;62:852–857. doi: 10.1002/iub.398. PubMed DOI

Sha X.Y., Xiong Z.F., Liu H.S., Zheng Z., Ma T.H. Pregnant phenotype in aquaporin 8-deficient mice. Acta Pharmacol. Sin. 2011;32:840–844. doi: 10.1038/aps.2011.45. PubMed DOI PMC

Skowronska A., Mlotkowska P., Eliszewski M., Nielsen S., Skowronski M.T. Expression of aquaporin 1, 5 and 9 in the ovarian follicles of cycling and early pregnant pigs. Physiol. Res. 2015;64:237–245. PubMed

Zhu C., Jiang Z., Bazer F.W., Johnson G.A., Burghardt R.C., Wu G. Aquaporins in the female reproductive system of mammals. Front Biosci. (Landmark Ed) 2015;20:838–871. PubMed

Madej A., Lang A., Brandt Y., Kindhal H., Madens M.T., Einarsson S. Factors regulating ovarian function in pigs. Domest. Anim. Endocrinol. 2005;29:347–361. doi: 10.1016/j.domaniend.2005.02.030. PubMed DOI

Gregoraszczuk E.L., Gertler A., Bylica A. Response of porcine theca and granulosa cells to GH during short-term in vitro culture. Anim. Reprod. 2000;58:113–125. doi: 10.1016/S0378-4320(99)00083-4. PubMed DOI

Kolodziejczyk J., Gertler A., Leibovich H., Rzasa J., Gregoraszczuk E.L. Synergistic action of growth hormone and insulin-like growth factor I (IGF-I) on proliferation and estradiol secretion in porcine granulosa and theca cells cultured alone or in coculture. Theriogenology. 2003;60:559–570. doi: 10.1016/S0093-691X(03)00032-3. PubMed DOI

Devesa J., Caicedo D. The Role of Growth Hormone on Ovarian Functioning and Ovarian Angiogenesis. Front Endocrinol. (Lausanne) 2019;10:450. doi: 10.3389/fendo.2019.00450. PubMed DOI PMC

Wang W., Li Q., Yang T., Li D., Ding F., Sun H., Bai G. RNA interference-mediated silencing of aquaporin (AQP)-5 hinders angiogenesis of colorectal tumor by suppressing the production of vascular endothelial growth factor. Neoplasma. 2018;65:55–65. doi: 10.4149/neo_2018_161019N487. PubMed DOI

Breves J., Inokuchi M., Yamaguchi Y., Seale A., Watanabe S., Lerner D., Kaneko T., Grau E. Hormonal regulation of aquaporin 3: Opposing actions of prolactin and cortisol in tilapia gill. J. Endocrinol. 2016;230:325–337. doi: 10.1530/JOE-16-0162. PubMed DOI

Vogel C., Marcotte E.M. Insights into the regulation of protein abundance from proteomic and transcriptomic analyses. Nat. Rev. Genet. 2012;13:227–232. doi: 10.1038/nrg3185. PubMed DOI PMC

Pelagalli A., Squillacioti C., Ali S., Liguori G., Mirabella N. Cellular distribution of aquaporins in testes of normal and cryptorchid dogs: A preliminary study on dynamic roles. Anim. Reprod. Sci. 2019;204:22–30. doi: 10.1016/j.anireprosci.2019.03.001. PubMed DOI

Wu H., Chen L., Zhang X., Zhou Q., Li J.M., Berger S., Borok Z., Zhou B., Xiao Z., Yin H., et al. Aqp5 is a new transcriptional target of Dot1a and a regulator of Aqp2. PLoS ONE. 2013;8:e53342. doi: 10.1371/journal.pone.0053342. PubMed DOI PMC

Papadopoulos M.C., Saadoun S. Key roles of aquaporins in tumor biology. Biochim. Biophys Acta. 2015;1848:2576–2583. doi: 10.1016/j.bbamem.2014.09.001. PubMed DOI

Madeira A., Mósca A.F., Moura T.F., Soveral G. Aquaporin-5 is expressed in adipocytes with implications in adipose differentiation. IUBMB Life. 2015;67:54–60. doi: 10.1002/iub.1345. PubMed DOI

Akins E.L., Morrissette M.C. Gross ovarian changes during estrous cycle of swine. Am. J. Vet. Res. 1968;10:1953–1957. PubMed

Stokłosowa S., Bahr J., Gregoraszczuk E.L. Some morphological and characteristics of cells of the porcine theca interna in tissue culture. Biol. Reprod. 1978;19:712–719. doi: 10.1095/biolreprod19.4.712. PubMed DOI

Nynca A., Jablonska O., Slomczynska M., Petroff B.K., Ciereszko R.E. Effects of phytoestrogen daidzein and estradiol on steroidogenesis and expression of estrogen receptors in porcine luteinized granulosa cells from large follicles. J. Physiol. Pharmacol. 2009;60:95–105. PubMed

Changes in Aquaporin 1, 5 and 9 Gene Expression in the Porcine Oviduct According to Estrous Cycle and Early Pregnancy