Reproductive Biology and Endocrinology | |
Progesterone, estradiol, arachidonic acid, oxytocin, forskolin and cAMP influence on aquaporin 1 and 5 expression in porcine uterine explants during the mid-luteal phase of the estrous cycle and luteolysis: an in vitro study | |
Mariusz T Skowronski3  Soren Nielsen2  Stanisław Okrasa1  Bartosz Wojciechowicz1  Patrycja Młotkowska1  Agnieszka Skowronska4  | |
[1] Department of Animal Physiology, Faculty of Biology and Biotechnology, University of Warmia and Mazury in Olsztyn, Olsztyn, Poland;Department of Health Science and Technology, Faculty of Medicine, Aalborg University, Aalborg, Denmark;Institute of Veterinary, Poznań University of Life Sciences, Poznań, Poland;Department of Human Physiology, Faculty of Medical Sciences, University of Warmia and Mazury in Olsztyn, Olsztyn, Poland | |
关键词: in vitro study; Pig; Estrous cycle; Uterus; Aquaporins; | |
Others : 1131983 DOI : 10.1186/s12958-015-0004-5 |
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received in 2014-08-19, accepted in 2015-02-07, 发布年份 2015 | |
【 摘 要 】
Background
The cell membrane water channel protein, aquaporins (AQPs), regulate cellular water transport and cell volume and play a key role in water homeostasis. Recently, AQPs are considered as important players in the field of reproduction. In previous studies, we have established the presence of AQP1 and 5 in porcine uterus. Their expression at protein level altered in distinct tissues of the female reproductive system depending on the phase of the estrous cycle. However, the regulation of aquaporin genes and proteins expression has not been examined in porcine uterine tissue. Therefore, we have designed an in vitro experiment to explain whether steroid hormones, progesterone (P4) and estradiol (E2), and other factors: oxytocine (OT), arachidonic acid (AA; substrate for prostaglandins synthesis) as well as forskolin (FSK; adenylate cyclase activator) and cAMP (second messenger, cyclic adenosine monophosphate) may impact AQPs expression.
Methods
Uterine tissues were collected on Days 10–12 and 14–16 of the estrous cycle representing the mid-luteal phase and luteolysis. Real-time PCR and Western blot analysis were performed to examine the expression of porcine AQP1 and AQP5. Their expression in the uterine explants was also evaluated by immunohistochemistry.
Results
The results indicated that uterine expression of AQP1 and AQP5 potentially remains under control of steroid hormones and AA-derived compounds (e.g. prostaglandins). P4, E2, AA, FSK and cAMP cause translocation of AQP5 from apical to the basolateral plasma membrane of the epithelial cells, which might affect the transcellular water movement (through epithelial cells) between uterine lumen and blood vessels. The AC/cAMP pathway is involved in the intracellular signals transduction connected with the regulation of AQPs expression in the pig uterus.
Conclusions
This study documented specific patterns of AQP1 and AQP5 expression in response to P4, E2, AA, FSK and cAMP, thereby providing new indirect evidence of their role in maintaining the local fluid balance within the uterus during the mid-luteal phase of the estrous cycle and luteolysis in pigs.
【 授权许可】
2015 Skowronska et al.; licensee BioMed Central.
【 预 览 】
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Figure 1. | 23KB | Image | download |
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【 参考文献 】
- [1]Zhang D, Tan YJ, Qu F, Sheng JZ, Huang HF: Functions of water channels in male and female reproductive systems. Mol Asp Medic 2012, 33:676-90.
- [2]Hua Y, Jiang W, Zhang W, Shen Q, Chen M, Zhu X: Expression and significance of aquaporins during pregnancy. Front Biosc 2013, 18:1373-83.
- [3]Meng QX, Gao HJ, Xu CM, Dong MY, Sheng X, Sheng J-Z, et al.: Reduced expression and function of aquaporin-3 in mouse metaphase-II oocytes induced by controlled ovarian hyperstimulation were associated with subsequent low fertilization rate. Cell Physiol Biochem 2008, 21:123-8.
- [4]McConnell NA, Yunus RS, Gross SA, Bost KL, Clemens MG, Hughes FM Jr: Water permeability of an ovarian antral follicle is predominantly transcellular and mediated by aquaporins. Endocrinology 2002, 143:2905-12.
- [5]Richard C, Gao JU, 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, 144:1533-41.
- [6]Lindsay LA, Murphy CR: Redistribution of aquaporins in uterine epithelial cells at the time of implantation in the rat. Acta Histochem 2004, 106:299-307.
- [7]Skowronski MT: 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. BioMed Central Full Text
- [8]Damiano AE, Zotta E, Goldstein J, Reisin I, Ibarra C: Water channel proteins AQP3 and AQP9 are present in syncytiotrophoblast of human term placenta. Placenta 2001, 22:776-81.
- [9]Wang S, Amidi F, Beall M, Gui L, Ross MG: Aquaporin 3 expression in human fetal membranes and its up-regulation by cyclic adenosine monophosphate in amnion epithelial cell culture. J Soc Gynecol Investig 2006, 13:181-5.
- [10]Zhu XQ, Jiang SS, Zhu XJ, Zou SW, Wang Y, Hu YC: Expression of aquaporin 1 and aquaporin 3 in fetal membranes and placenta in human term pregnancies with oligohydramnios. Placenta 2009, 30:670-6.
- [11]Zou LB, Zhang RJ, Tan YJ, Ding GI, Shi S, Zhang D, 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:E1399-408.
- [12]Agre P, King L, Yasui M, Guggino WB, Ottersen OP, Fujiyoshi Y, et al.: Aquaporin water channels – from atomic structure to clinical medicine. J Physiol 2002, 542:3-16.
- [13]Nielsen S, King LS, Christensen BM, Agre P: Aquaporins in complex tissue. II. Subcellular distribution in respiratory and glandular tissues of rat. Am J Physiol 1997, 273:C1549-61.
- [14]Verkman AS: More than just water channels: unexpected cellular roles of aquaporins. J Cell Sci 2005, 118:3225-32.
- [15]Li X, Yu H, Koide SS: The water channel gene in human uterus. Biochem Mol Biol Int 1994, 32:371-7.
- [16]Li XJ, Yu HM, Koide SS: Regulation of water channel gene (AQP-CHIP) expression by estradiol and anordiol in rat uterus. Yao Xue Xue Bao 1997, 32:586-92.
- [17]Jablonski EM, McConnell NA, Hughes FM Jr, Huet-Hudson YM: Estrogen regulation of aquaporins in the mouse uterus: potential roles in uterine water movement. Biol Reprod 2003, 69:1481-7.
- [18]Lindsay LA, Murphy CR: Redistribution of aquaporins 1 and 5 in the rat uterus is dependent on progesterone: a study with light and electron microscopy. Reproduction 2006, 131:369-78.
- [19]Aralla M, Borromeo V, Groppetti D, Secchi C, Cremonesi F, Arrighi S: A collaboration of aquaporins handles water transport in relation to the estrous cycle in the bitch uterus. Theriogenology 2009, 72:310-21.
- [20]Klein C, Troedsson MHT, Rutllant J: Expression of aquaporin water channels in equine endometrium is differentially regulated during the oestrous cycle and early pregnancy. Reprod Dom Anim 2013, 48:529-37.
- [21]Wang S, Chen J, Au KT, Ross MG: Expression of aquaporin 8 and its up-regulation by cyclic adenosine monophosphate in human WISH cells. Am J Obstet Gynecol 2003, 188:997-1001.
- [22]Wang S, Amidi F, Yin S, Beall M, Ross MG: Cyclic adenosine monophosphate regulation of aquaporin gene expression in human amnion epithelia. Reprod Sci 2007, 14:234-40.
- [23]Yang F, Kawedia JD, Menon AG: Cyclic AMP regulates aquaporin 5 expression at both transcriptional and post-transcriptional levels through a protein kinase A pathway. J Biol Chem 2003, 278:32173-80.
- [24]Belkacemi L, Beall MH, Magee TR, Pourtemour M, Ross MG: AQP1 gene expression is up-regulated by arginine vasopressin and cyclic AMP agonist in trophoblast cells. Life Sci 2008, 82:1272-80.
- [25]Hildenbrand A, Lalitkumar L, Nielsen S, Gemzell-Danielsson K, Stavreus-Evers A: Expression of aquaporin 2 in human endometrium. Reprod Endocrinol 2006, 86:1452-8.
- [26]Feng C, Sun CC, Wang TT, He RH, Sheng JZ, Huang HF: Decreased expression of endometrial vessel AQP1 and endometrial epithelium AQP2 related to an ovulatory uterine bleeding in premenopausal women. Menopause 2011, 15:648-54.
- [27]Skowronski MT, Kwon TH, Nielsen S: Immunolocalization of aquaporin 1, 5, and 9 in the female pig reproductive system. J Histochem Cytochem 2009, 57:61-7.
- [28]Akins EL, Morrisete MC: Gross ovarian changes during the estrous cycle of swine. Am J Vet Res 1968, 29:1953-7.
- [29]Skowronski MT, Lebeck J, Rojek A, Praetorius J, Fuchtbauer EM, Frokiaer J, et al.: AQP7 is localized in capillaries of adipose tissue, cardiac and striated muscle: implications in glycerol metabolism. Am J Physiol Renal Physiol 2007, 292:F956-65.
- [30]Terris J, Ecelbarger CA, Nielsen S, Knepper MA: Long-term regulation of four renal aquaporins in rats. Am J Physiol 1996, 271:F414-22.
- [31]Kobayashi M, Takahashi E, Miyagawa S, Watanabe H, Iguchi T: Chromatin immunoprecipitation-mediated target identification proved aquaporin 5 is regulated directly by estrogen in the uterus. Genes Cells 2006, 11:1133-43.
- [32]Ing NH: Steroid hormones regulate gene expression posttranscriptionally by altering the stabilities of messenger RNAs. Biol Reprod 2005, 72:1290-6.
- [33]Krzymowski T, Stefanczyk-Krzymowska S: The role of endometrium in endocrine regulation of the animal oestrous cycle. Reprod Dom Anim 2008, 43:80-91.
- [34]Finlay TH, Katz J, Kirsh L, Levitz M, Nathoo SA, Seiler S: Estrogen-stimulated uptake of plasminogen by the mouse uterus. Endocrinology 1983, 112:856-61.
- [35]Norman SJ, Poyser N: Effects of inhibitors of arachidonic acid turnover on the production of prostaglandins by the guinea-pig uterus. J Reprod Fertil 2000, 118:181-6.
- [36]Hertelendy F, Zakar T: Prostaglandins and the myometrium and cervix. Prostaglandin Leukotriens Essential Fatty Acids 2004, 70:207-22.
- [37]Franczak A, Kotwica G, Kurowicka B, Oponowicz A, Wacławek-Potocka J, Petroff BK: Expression of enzymes of cyclooxygenase pathway and secretion of prostaglandin E2 and F2α by porcine myometrium during luteolysis and early pregnancy. Theriogenology 2006, 66:1049-56.
- [38]Irvine RF: How is the level of free arachidonic acid controlled in cells? Biochem J 1982, 204:3-16.
- [39]Blitek A, Waclawik A, Kaczmarek MM, Stadejek T, Pejsak Z, Ziecik AJ: Expression of cyclooxygenase-1 and −2 in the porcine endometrium during the oestrous cycle and early pregnancy. Reprod Dom Anim 2006, 41:251-7.
- [40]Blitek A, Ziecik A: Prostaglandins F2α and E2 secretion by porcine epithelial and stromal endometrial cells on different days of the oestrus cycle. Reprod Dom Anim 2004, 39:340-6.
- [41]Gleeson AR, Thorburn GD, Cox RI: Prostaglandin F concentrations in the utero-ovarian venous plasma of the sow during the late luteal phase of the oestrous cycle. Prostaglandins 1974, 5:521-9.
- [42]Zelenina M, Christensen BM, Palmer J, Nairn AC, Nielsen S, Aperia A: Prostaglandin E2 interaction with AVP: effects on AQP2 phosphorylation and distribution. Am J Physiol Renal Physiol 2000, 278:F388-94.
- [43]Uzumcu M, Braileanu GT, Carnahan KG, Ludwig TE, Mirando MA: Oxytocin –stimulated phosphoinositide hydrolysis and prostaglandin F secretion by luminal epithelial, glandular epithelial and stromal cells from pig endometrium. I. Response of cyclic pig on day 16 postestrus. Biol Reprod 1998, 59:1259-65.
- [44]Trout WE, Smith GW, Gentry PC, Galvin JM, Keisler DH: Oxytocin secretion by the endometrium of the pig during maternal recognition of pregnancy. Biol Reprod 1995, 52(Suppl 1):189. abstract
- [45]Whiteaker SS, Mirando MA, Becker WC, Hostetler CE: Detection of functional oxytocin receptors on endometrium of pigs. Biol Reprod 1994, 51:92-8.
- [46]Okano A, Okuda K, Takahashi M, Schams D: Oxytocin receptors in porcine endometrium during the estrous cycle and early pregnancy. Animal Reprod Sci 1996, 41:61-70.
- [47]Gilbert CL, Jenkins , Wathes DC: Pulsatile release of oxytocin into the circulation of the ewe during oestrous, mating and the early luteal phase. J Reprod Fertil 1991, 91:337-46.
- [48]Ducza E, Seres AB, Hajagos-Toth J, Falkay G, Gaspar R: Oxytocin regulates the expression of aquaporin 5 in the late-pregnant rat uterus. Mol Reprod Dev 2014, 81:524-30.
- [49]Wang S, Kallichanda N, Song W, Ramierez B, Ross MG: Expression of aquaporin 8 in human placenta and chorioamniotic membranes: evidence of molecular mechanism for intramembranous amniotic fluid resorbtion. Am J Obstet Gynecol 2001, 185:1226-31.
- [50]Garcia F, Kierbel A, Larocca MC, Gradilone SA, Splinter P, LaRusso NF, et al.: The water channel aquaporin-8 is mainly intracellular in rat hepatocytes and its plasma membrane insertion is stimulated by cyclic AMP. J Biol Chem 2001, 276:12147-52.