Journal of Animal Reproduction and Biotechnology (한국동물생명공학회지)

The Korean Society of Animal Reproduction and Biotechnology (한국동물생명공학회)
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Aquaporin 4 expression is downregulated in large bovine ovarian follicles

  • Kim, Chang-Woon (Department of Physiology and Institute of Health Sciences, College of Medicine, Gyeongsang National University) ;
  • Choi, Eun-Ju (Department of Physiology and Institute of Health Sciences, College of Medicine, Gyeongsang National University) ;
  • Kim, Eun-Jin (Department of Physiology and Institute of Health Sciences, College of Medicine, Gyeongsang National University) ;
  • Siregar, Adrian S. (Department of Physiology and Institute of Health Sciences, College of Medicine, Gyeongsang National University) ;
  • Han, Jaehee (Department of Physiology and Institute of Health Sciences, College of Medicine, Gyeongsang National University) ;
  • Kang, Dawon (Department of Physiology and Institute of Health Sciences, College of Medicine, Gyeongsang National University)
  • Received : 2020.10.23
  • Accepted : 2020.12.07
  • Published : 2020.12.31
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Abstract

Aquaporin channels (AQPs) are known to play an important role in the development of ovarian follicles through their function in water transport pathways. Compared to other AQPs, research on the role of AQP4 in female reproductive physiology, particularly in cattle, remains limited. In our previous study, gene chip microarray data showed a downregulation of AQP4 in bovine cystic follicles. This study was performed to validate the AQP4 expression level at the protein level in bovine follicles using immunohistochemistry, Western blotting, and immunoprecipitation assays. Immunostaining data showed that AQP4 was expressed in granulosa and theca cells of bovine ovarian follicles. The ovarian follicles were classified according to size as small (< 10 mm) or large (> 25 mm) in diameter. Consistent with earlier microarray data, semi-quantitative PCR data showed a decrease in AQP4 mRNA expression in large follicles. Western blot analysis showed a downregulation of the AQP4 protein in large follicles. In addition, AQP4 was immunoprecipitated and blotted with anti-AQP4 antibody in small and large follicles. Accordingly, AQP4 exhibited a low expression in large follicles. These results show that AQP4 is downregulated in bovine ovarian large follicles, suggesting that the downregulation of AQP4 expression may interfere with follicular water transport, leading to bovine follicular cysts.

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References

  1. Achebe FU. 2019. Relationship of maximum follicular size, age of woman, and reproductive implications in women attending fertility clinic in St. Margaret's Hospital, Lokoja, using Creighton Model FertilityCareTM System and NaProTECHNOLOGY. Niger. J. Gen. Pract. 17:51-63. https://doi.org/10.4103/NJGP.NJGP_9_18
  2. Choe C, Cho YW, Kim CW, Son DS, Han J, Kang D. 2010. Identification of differentially expressed genes in bovine follicular cystic ovaries. Korean J. Physiol. Pharmacol. 14:265-272. https://doi.org/10.4196/kjpp.2010.14.5.265
  3. Choe C, Son DS, Cho SR, Kim HJ, Choi SH, Kang D. 2008. Alteration in concentrations of blood urea nitrogen and sex steroid hormone in Korean cattle with reproductive disorders. J. Emb. Trans. 23:59-64.
  4. Christensen AP, Patel SH, Grasa P, Christian HC, Williams SA. 2015. Oocyte glycoproteins regulate the form and function of the follicle basal lamina and theca cells. Dev. Biol. 401:287-298. https://doi.org/10.1016/j.ydbio.2014.12.024
  5. Fan Y, Zhang J, Sun XL, Gao L, Zeng XN, Ding JH, Cao C, Niu L, Hu G. 2005. Sex- and region-specific alterations of basal amino acid and monoamine metabolism in the brain of aquaporin-4 knockout mice. J. Neurosci. Res. 82:458-464. https://doi.org/10.1002/jnr.20664
  6. Gu F, Hata R, Toku K, Yang L, Ma YJ, Maeda N, Sakanaka M, Tanaka J. 2003. Testosterone up-regulates aquaporin-4 expression in cultured astrocytes. J. Neurosci. Res. 72:709-715. https://doi.org/10.1002/jnr.10603
  7. Hackeloer BJ, Fleming R, Robinson HP, Adam AH, Coutts JR. 1979. Correlation of ultrasonic and endocrinologic assessment of human follicular development. Am. J. Obstet. Gynecol. 135:122-128. https://doi.org/10.1016/S0002-9378(79)80029-0
  8. Kengaku K, Tanaka T, Kamomae H. 2007. Changes in the peripheral concentrations of inhibin, follicle-stimulating hormone, luteinizing hormone, progesterone and estradiol17beta during turnover of cystic follicles in dairy cows with spontaneous follicular cysts. J. Reprod. Dev. 53:987-993. https://doi.org/10.1262/jrd.18107
  9. Mader S and Brimberg L. 2019. Aquaporin-4 water channel in the brain and its implication for health and disease. Cells 8:90. https://doi.org/10.3390/cells8020090
  10. Mateo-Otero Y, Sanchez JM, Recuero S, Bages-Arnal S, McDonald M, Kenny DA, Yeste M, Lonergan P, Fernandez-Fuertes B. 2020. Effect of exposure to seminal plasma through natural mating in cattle on conceptus length and gene expression. Front. Cell Dev. Biol. 8:341. https://doi.org/10.3389/fcell.2020.00341
  11. McConnell NA, Yunus RS, Gross SA, Bost KL, Clemens MG, Hughes FM Jr. 2002. Water permeability of an ovarian antral follicle is predominantly transcellular and mediated by aquaporins. Endocrinology 143:2905-2912. https://doi.org/10.1210/en.143.8.2905
  12. Menezo YJ and Herubel F. 2002. Mouse and bovine models for human IVF. Reprod. Biomed. Online 4:170-175. https://doi.org/10.1016/S1472-6483(10)61936-0
  13. Nowak M, Grzesiak M, Saito N, Kwaeniewska M, Sechman A, Hrabia A. 2017. Expression of aquaporin 4 in the chicken ovary in relation to follicle development. Reprod. Domest. Anim. 52:857-864. https://doi.org/10.1111/rda.12990
  14. Papadopoulos MC, Manley GT, Krishna S, Verkman AS. 2004. Aquaporin-4 facilitates reabsorption of excess fluid in vasogenic brain edema. FASEB J. 18:1291-1293. https://doi.org/10.1096/fj.04-1723fje
  15. Qu F, Wang FF, Lu XE, Dong MY, Sheng JZ, Lv PP, Ding GL, Shi BW, Zhang D, Huang HF. 2010. Altered aquaporin expression in women with polycystic ovary syndrome: hyperandrogenism in follicular fluid inhibits aquaporin-9 in granulosa cells through the phosphatidylinositol 3-kinase pathway. Hum. Reprod. 25:1441-1450. https://doi.org/10.1093/humrep/deq078
  16. 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 144:1533-1541. https://doi.org/10.1210/en.2002-0033
  17. Siregar AS, Nyiramana MM, Kim EJ, Shin EJ, Kim CW, Lee DK, Hong SG, Han J, Kang D. 2019. TRPV1 is associated with testicular apoptosis in mice. J. Anim. Reprod. Biotechnol. 34:311-317. https://doi.org/10.12750/JARB.34.4.311
  18. Skowronska A, Mlotkowska P, Eliszewski M, Nielsen S, Skowronski MT. 2015. Expression of aquaporin 1, 5 and 9 in the ovarian follicles of cycling and early pregnant pigs. Physiol. Res. 64:237-245.
  19. Su W, Guan X, Zhang D, Sun M, Yang L, Yi F, Hao F, Feng X, Ma T. 2013. Occurrence of multi-oocyte follicles in aquaporin 8-deficient mice. Reprod. Biol. Endocrinol. 11:88. https://doi.org/10.1186/1477-7827-11-88
  20. Sun XL, Ding JH, Fan Y, Zhang J, Gao L, Hu G. 2007. Aquaporin 4 regulates the effects of ovarian hormones on monoamine neurotransmission. Biochem. Biophys. Res. Commun. 353:457-462. https://doi.org/10.1016/j.bbrc.2006.12.040
  21. Sun XL, Zhang J, Fan Y, Ding JH, Sha JH, Hu G. 2009. Aquaporin-4 deficiency induces subfertility in female mice. Fertil. Steril. 92:1736-1743. https://doi.org/10.1016/j.fertnstert.2008.07.1785
  22. Tak HM, Han J, Kang D. 2010. Fibrinogen mRNA expression upregulated in follicular cyst of Korean cattle. J. Emb. Trans. 25:29-34.
  23. Thoroddsen A, Dahm-Kahler P, Lind AK, Weijdegard B, Lindenthal B, Muller J, Brannstrom M. 2011. 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. 96:1021-1028. https://doi.org/10.1210/jc.2010-2545
  24. Verkman AS. 2009. Knock-out models reveal new aquaporin functions. Handb. Exp. Pharmacol. (190):359-381.
  25. Zeng XN, Sun XL, Gao L, Fan Y, Ding JH, Hu G. 2007. Aquaporin-4 deficiency down-regulates glutamate uptake and GLT-1 expression in astrocytes. Mol. Cell. Neurosci. 34:34-39. https://doi.org/10.1016/j.mcn.2006.09.008
  26. Zhu C, Jiang Z, Bazer FW, Johnson GA, Burghardt RC, Wu G. 2015. Aquaporins in the female reproductive system of mammals. Front. Biosci. (Landmark Ed.) 20:838-871. https://doi.org/10.2741/4341