In rodent species, the ovary and the end of oviduct are encapsulated by a thin membrane called ovarian bursa. The biological functions of ovarian bursa remain unexplored despite its structural arrangement in facilitating oocytes transport into oviduct. In the present study, we observed a rapid fluid accumulation and reabsorption within the ovarian bursa after ovarian stimulation (PMSG-primed hCG injection), suggesting that the ovarian bursa might play an active role in regulating local fluid homeostasis around the timing of ovulation. We hypothesized that the aquaporin proteins, which are specialized channels for water transport, might be involved in this process. By screening the expression of aquaporin family members (Aqp1-9) in the ovarian tissue and isolated ovarian bursa (0, 1, 2 and 5 h after hCG injection), we found that AQP2 and AQP5 mRNA showed dynamic changes after hCG treatment, showing upregulation at 1–2 h followed by gradually decrease at 5 h, which is closely related with the intra-bursa fluid dynamics. Further immunofluorescence examinations of AQP2 and AQP5 in the ovarian bursa revealed that AQP2 is specifically localized in the outer layer (peritoneal side) while AQP5 localized in the inner layer (ovarian side) of the bursa, such cell type specific and spatial-temporal expressions of AQP2 and 5 support our hypothesis that they might be involved in efficient water transport through ovarian bursa under ovulation related hormonal regulation. The physiological significance of aquaporin-mediated water transport in the context of ovarian bursa still awaits further clarification.
References
[1]
Vanderhyden BC, Rouleau A, Armstrong DT (1986) Effect of removal of the ovarian bursa of the rat on infundibular retrieval and subsequent development of ovulated oocytes. J Reprod Fertil 77: 393–399.
[2]
Wang ZB, Li M, Li JC (2010) Recent advances in the research of lymphatic stomata. Anat Rec (Hoboken) 293: 754–761.
[3]
Shinohara H, Nakatani T, Matsuda T (1987) Postnatal development of the ovarian bursa of the golden hamster (Mesocricetus auratus): its complete closure and morphogenesis of lymphatic stomata. Am J Anat 179: 385–402.
[4]
Hayashi K, Ogushi S, Kurimoto K, Shimamoto S, Ohta H, et al. (2012) Offspring from oocytes derived from in vitro primordial germ cell-like cells in mice. Science 338: 971–975.
[5]
Shkolnik K, Tadmor A, Ben-Dor S, Nevo N, Galiani D, et al. (2011) Reactive oxygen species are indispensable in ovulation. Proc Natl Acad Sci U S A 108: 1462–1467.
[6]
Van der Hoek KH, Maddocks S, Woodhouse CM, van Rooijen N, Robertson SA, et al. (2000) Intrabursal injection of clodronate liposomes causes macrophage depletion and inhibits ovulation in the mouse ovary. Biol Reprod 62: 1059–1066.
[7]
Guerre EJ, Clark MR, Muse KN, Curry TJ (1991) Intrabursal administration of protein kinase or proteinase inhibitors: effects on ovulation in the rat. Fertil Steril 56: 126–133.
[8]
Parr EL (1974) Beta-galactosidase in rat ovarian bursa fluid at ovulation. Biol Reprod 11: 504–508.
[9]
Nakatani T, Shinohara H, Matsuda T (1986) On the ovarian bursa of the golden hamster. II. Intercellular connections in the bursal epithelium and passage of ferritin from the cavity into lymphatics. J Anat 148: 1–12.
[10]
Shinohara H, Nakatani T, Morisawa S, Matsuda T (1986) On the ovarian bursa of the golden hamster. I. Scanning electron microscopy of the inner surface and stomatal orifices. J Anat 147: 45–54.
[11]
Shinohara H, Nakatani T, Matsuda T (1985) The presence of lymphatic stomata in the ovarian bursa of the golden hamster. Anat Rec 213: 44–52.
[12]
Sui MH, Li JC (2001) [The presence of the lymphatic stomata in ovarian bursa of guinea pig and the ultrastructure of ovarian bursa]. Shi Yan Sheng Wu Xue Bao 34: 291–297.
[13]
King LS, Kozono D, Agre P (2004) From structure to disease: the evolving tale of aquaporin biology. Nat Rev Mol Cell Biol 5: 687–698.
[14]
Verkman AS (2005) More than just water channels: unexpected cellular roles of aquaporins. J Cell Sci 118: 3225–3232.
[15]
Huang HF, He RH, Sun CC, Zhang Y, Meng QX, et al. (2006) Function of aquaporins in female and male reproductive systems. Hum Reprod Update 12: 785–795.
[16]
Zhang D, Tan YJ, Qu F, Sheng JZ, Huang HF (2012) Functions of water channels in male and female reproductive systems. Mol Aspects Med 33: 676–690.
[17]
Chen Q, Zhang Y, Peng H, Lei L, Kuang H, et al. (2011) Transient {beta}2-adrenoceptor activation confers pregnancy loss by disrupting embryo spacing at implantation. J Biol Chem 286: 4349–4356.
[18]
Li M, Zhou TH, Gao Y, Zhang N, Li JC (2007) Ultrastructure and estrogen regulation of the lymphatic stomata of ovarian bursa in mice. Anat Rec (Hoboken) 290: 1195–1202.
[19]
Parr EL (1974) Histological examination of the rat ovarian follicle wall prior to ovulation. Biol Reprod 11: 483–503.
[20]
Sasaki S (2012) Aquaporin 2: from its discovery to molecular structure and medical implications. Mol Aspects Med 33: 535–546.
[21]
Ma T, Song Y, Gillespie A, Carlson EJ, Epstein CJ, et al. (1999) Defective secretion of saliva in transgenic mice lacking aquaporin-5 water channels. J Biol Chem 274: 20071–20074.
[22]
Song Y, Verkman AS (2001) Aquaporin-5 dependent fluid secretion in airway submucosal glands. J Biol Chem 276: 41288–41292.
[23]
Kobayashi M, Takahashi E, Miyagawa S, Watanabe H, Iguchi T (2006) Chromatin immunoprecipitation-mediated target identification proved aquaporin 5 is regulated directly by estrogen in the uterus. Genes Cells 11: 1133–1143.
[24]
Zou LB, Zhang RJ, Tan YJ, Ding GL, Shi S, et al. (2011) 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 96: E1399–E1408.
[25]
Hausman GJ, Barb CR, Lents CA (2012) Leptin and reproductive function. Biochimie 94: 2075–2081.
[26]
Rodriguez A, Catalan V, Gomez-Ambrosi J, Garcia-Navarro S, Rotellar F, et al. (2011) Insulin- and leptin-mediated control of aquaglyceroporins in human adipocytes and hepatocytes is mediated via the PI3K/Akt/mTOR signaling cascade. J Clin Endocrinol Metab 96: E586–E597.
[27]
Chen Q, Peng H, Lei L, Zhang Y, Kuang H, et al. (2011) Aquaporin3 is a sperm water channel essential for postcopulatory sperm osmoadaptation and migration. Cell Res 21: 922–933.
[28]
Sun XL, Zhang J, Fan Y, Ding JH, Sha JH, et al. (2009) Aquaporin-4 deficiency induces subfertility in female mice. Fertil Steril 92: 1736–1743.
[29]
Su W, Qiao Y, Yi F, Guan X, Zhang D, et al. (2010) Increased female fertility in aquaporin 8-deficient mice. IUBMB Life 62: 852–857.
[30]
Sha XY, Xiong ZF, Liu HS, Zheng Z, Ma TH (2011) Pregnant phenotype in aquaporin 8-deficient mice. Acta Pharmacol Sin 32: 840–844.
[31]
Rodgers RJ, Irving-Rodgers HF (2010) Formation of the ovarian follicular antrum and follicular fluid. Biol Reprod 82: 1021–1029.
[32]
Thoroddsen A, Dahm-Kahler P, Lind AK, Weijdegard B, Lindenthal B, et al. (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.
[33]
McConnell NA, Yunus RS, Gross SA, Bost KL, Clemens MG, et al. (2002) Water permeability of an ovarian antral follicle is predominantly transcellular and mediated by aquaporins. Endocrinology 143: 2905–2912.
[34]
Rojek A, Fuchtbauer EM, Kwon TH, Frokiaer J, Nielsen S (2006) Severe urinary concentrating defect in renal collecting duct-selective AQP2 conditional-knockout mice. Proc Natl Acad Sci U S A 103: 6037–6042.
