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

Journal of Clinical Endocrinology and Metabolism - Tập 96 Số 4 - Trang 1021-1028 - 2011
Ásgeir Thoroddsen1, Pernilla Dahm‐Kähler1, Anna‐Karin Lind1, Birgitta Weijdegård1, B. Lindenthal2, Jörg Müller2, Mats Brännström1
1Department of Obstetrics and Gynaecology (A.T., P.D.-K., A.K.L., B.W., M.B.), Sahlgrenska Academy, University of Gothenburg, SE-413 45 Göteborg, Sweden;
2Global Therapeutic Research (B.L., J.M.), Bayer Schering Pharma AG, 13353 Berlin, Germany

Tóm tắt

AbstractContext:Changes in vascular permeability and expansion of the fluid-filled antrum are major events in the LH-induced ovulatory process.Objectives:Our objective was to investigate the presence and expression levels of aquaporins (AQPs) in the granulosa and theca cell compartments of the follicle during defined phases of human ovulation.Design and Setting:We conducted a prospective experimental study at the Department of Obstetrics and Gynaecology at a university hospital.Participants:Twenty-eight women underwent laparoscopic sterilization and at the same time follicle retrieval at four periovulatory phases.Main Outcome Measures:mRNA levels of AQP1-4 were measured in separated granulosa and theca cells from preovulatory phase, early ovulatory (EO) phase, late ovulatory phase, and postovulatory phase. Immunohistochemistry was done for AQP1-4 in intact human follicles.Results:All four AQPs were expressed in both the theca and granulosa cells during ovulation. In granulosa cells, AQP1 levels increased in the late ovulatory and postovulatory phases. Expression of AQP2-3 followed a similar pattern with a marked increase in the EO phase, whereas AQP4 levels decreased from preovulatory to the EO phase. The presence of AQP1-4 in the human follicle was verified by immunohistochemistry.Conclusions:The results show for the first time the presence of AQP1-4 in human follicles during ovulation. The marked early rise in expression of AQP2 and AQP3 suggests a role during the process leading to follicular rupture, and the late rise of AQP1 suggests a role in corpus luteum formation.

Từ khóa


Tài liệu tham khảo

Andersen, 1995, Time interval from human chorionic gonadotrophin (HCG) injection to follicular rupture., Hum Reprod, 10, 3202, 10.1093/oxfordjournals.humrep.a135888

Hanna, 1994, Characteristics of follicular evacuation during human ovulation., Ultrasound Obstet Gynecol, 4, 488, 10.1046/j.1469-0705.1994.04060488.x

Rodgers, 1999, Development of the ovarian follicular epithelium., Mol Cell Endocrinol, 151, 171, 10.1016/S0303-7207(99)00087-8

Lenz, 1985, Ultrasonic study of follicular maturation, ovulation and development of corpus luteum during normal menstrual cycles., Acta Obstet Gynecol Scand, 64, 15, 10.3109/00016348509154681

Hirshfield, 1991, Development of follicles in the mammalian ovary., Int Rev Cytol, 124, 43, 10.1016/S0074-7696(08)61524-7

Gosden, 1988, Physiological factors underlying the formation of ovarian follicular fluid., J Reprod Fertil, 82, 813, 10.1530/jrf.0.0820813

Rodgers, 2010, Formation of the ovarian follicular antrum and follicular fluid., Biol Reprod, 82, 1021, 10.1095/biolreprod.109.082941

Kranzfelder, 1992, Preovulatory changes in the perifollicular capillary network in the rat: role of eicosanoids., Biol Reprod, 46, 379, 10.1095/biolreprod46.3.379

Zackrisson, 2000, Evidence for the involvement of blood flow-related mechanisms in the ovulatory process of the rat., Hum Reprod, 15, 264, 10.1093/humrep/15.2.264

Brännström, 1998, Preovulatory changes of blood flow in different regions of the human follicle., Fertil Steril, 69, 435, 10.1016/S0015-0282(97)00544-X

Waseda, 2003, Hemodynamic response of ovarian artery after hCG injection., Mol Cell Endocrinol, 202, 71, 10.1016/S0303-7207(03)00065-0

Abisogun, 1988, Modulatory role of eicosanoids in vascular changes during the preovulatory period in the rat., Biol Reprod, 38, 756, 10.1095/biolreprod38.4.756

Espey, 1963, Measurements of intrafollicular pressures in the rabbit ovary., Am J Physiol, 205, 1067, 10.1152/ajplegacy.1963.205.6.1067

Matousek, 2001, Novel method for intrafollicular pressure measurements in the rat ovary: increased intrafollicular pressure after hCG stimulation., Reproduction, 121, 307, 10.1530/rep.0.1210307

Agre, 2002, Aquaporin water channels: from atomic structure to clinical medicine., J Physiol, 542, 3, 10.1113/jphysiol.2002.020818

Huang, 2006, Function of aquaporins in female and male reproductive systems., Hum Reprod Update, 12, 785, 10.1093/humupd/dml035

Lindsay, 2007, Aquaporins are upregulated in glandular epithelium at the time of implantation in the rat., J Mol Histol, 38, 87, 10.1007/s10735-007-9083-8

Li, 1997, Regulation of water channel gene (AQP-CHIP) expression by estradiol and anordiol in rat uterus., Yao Xue Xue Bao, 32, 586

Jablonski, 2003, Estrogen regulation of aquaporins in the mouse uterus: potential roles in uterine water movement., Biol Reprod, 69, 1481, 10.1095/biolreprod.103.019927

Richard, 2003, Aquaporin water channel genes are differentially expressed and regulated by ovarian steroids during the periimplantation period in the mouse., Endocrinology, 144, 1533, 10.1210/en.2002-0033

Skowronski, 2009, Immunolocalization of aquaporin 1, 5, and 9 in the female pig reproductive system., J Histochem Cytochem, 57, 61, 10.1369/jhc.2008.952499

Mobasheri, 2005, Distribution of AQP2 and AQP3 water channels in human tissue microarrays., J Mol Histol, 36, 1, 10.1007/s10735-004-2633-4

Hildenbrand, 2006, Expression of aquaporin 2 in human endometrium., Fertil Steril, 86, 1452, 10.1016/j.fertnstert.2006.03.058

Mints, 2007, Expression of aquaporin-1 in endometrial blood vessels in menorrhagia., Int J Mol Med, 19, 407

McConnell, 2002, Water permeability of an ovarian antral follicle is predominantly transcellular and mediated by aquaporins., Endocrinology, 143, 2905, 10.1210/endo.143.8.8953

Livak, 2001, Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method., Methods, 25, 402, 10.1006/meth.2001.1262

Löfman, 2002, A method for longitudinal microscopic in vivo examinations of morphology, vascularity, and motility in the ovary and the oviduct of the rat., J Soc Gynecol Investig, 9, 379

Runesson, 2000, Gonadotropin- and cytokine-regulated expression of the chemokine interleukin 8 in the human preovulatory follicle of the menstrual cycle., The Journal of clinical endocrinology and metabolism, 85, 4387

Hillier, 1991, Effect of recombinant activin on androgen synthesis in cultured human thecal cells., J Clin Endocrinol Metab, 72, 1206, 10.1210/jcem-72-6-1206

Rung, 2006, Depletion of substrates for protein prenylation increases apoptosis in human periovulatory granulosa cells., Mol Reprod Dev, 73, 1277, 10.1002/mrd.20551

Russell, 2007, Molecular mechanisms of ovulation: co-ordination through the cumulus complex., Hum Reprod Update, 13, 289, 10.1093/humupd/dml062

Espey, 2000, Characterization of ovarian carbonyl reductase gene expression during ovulation in the gonadotropin-primed immature Rat., Biol Reprod, 62, 390, 10.1095/biolreprod62.2.390

Young, 2003, Controlled ovulation of the dominant follicle: a critical role for LH in the late follicular phase of the menstrual cycle., Hum Reprod, 18, 2257, 10.1093/humrep/deg467

Qu, 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, 10.1093/humrep/deq078

Sun, 2009, Aquaporin-4 deficiency induces subfertility in female mice., Fertil Steril, 92, 1736, 10.1016/j.fertnstert.2008.07.1785

Agre, 1987, Purification and partial characterization of the Mr 30,000 integral membrane protein associated with the erythrocyte Rh(D) antigen., J Biol Chem, 262, 17497, 10.1016/S0021-9258(18)45408-7

Lindsay, 2006, Redistribution of aquaporins 1 and 5 in the rat uterus is dependent on progesterone: a study with light and electron microscopy., Reproduction, 131, 369, 10.1530/rep.1.00914

Feng, 2008, Decreased expression of endometrial vessel AQP1 and endometrial epithelium AQP2 related to anovulatory uterine bleeding in premenopausal women., Menopause, 15, 648, 10.1097/gme.0b013e31816086ef

He, 2006, Aquaporin-2 expression in human endometrium correlates with serum ovarian steroid hormones., Life Sci, 79, 423, 10.1016/j.lfs.2006.01.020

Chaffin, 2002, Local role of progesterone in the ovary during the periovulatory interval., Rev Endocr Metab Disord, 3, 65, 10.1023/A:1012704903128