Immunolocalization of aquaporin 5 during rat ovarian follicle development and expansion of the preovulatory cumulus oophorus

Acta Histochemica

Volumn 116, Issue 3, 2014, Pages 457-465

  Starowicz, Agnieszka ^a   Grzesiak, Malgorzata ^a   Mobasheri, Ali ^b,c   Szoltys, Maria ^a  

^a JAGIELLONIAN UNIVERSITY   (Poland)

^b UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^c KING ABDULAZIZ UNIVERSITY   (Saudi Arabia)

Author keywords

Aquaporin 5; Cumulus oocyte complex; Follicle; Ovary; Rat

Indexed keywords

ANDROGEN; ANDROGEN RECEPTOR; AQUAPORIN 5; LUTEINIZING HORMONE; AQP5 PROTEIN, RAT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APICAL MEMBRANE; ARTICLE; CELL SWELLING; CONTROLLED STUDY; CUMULUS OOPHORUS; EPITHELIUM CELL; EXTRACELLULAR MATRIX; FEMALE; GRANULOSA CELL; HORMONE RESPONSIVE ELEMENT; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; IMMUNOLOCALIZATION; NONHUMAN; OOCYTE; OVARY FOLLICLE DEVELOPMENT; OVARY FOLLICLE MATURATION; OVIDUCT; OVULATION; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; ZONA PELLUCIDA; ANIMAL; ANTIBODY SPECIFICITY; CUMULUS CELL; CYTOLOGY; METABOLISM; OVARY FOLLICLE; PHYSIOLOGY; PROTEIN TRANSPORT; WISTAR RAT;

ANIMALS; AQUAPORIN 5; CUMULUS CELLS; FEMALE; OOCYTES; ORGAN SPECIFICITY; OVARIAN FOLLICLE; OVULATION; PROTEIN TRANSPORT; RATS, WISTAR;

EID: 84899900403     PISSN: 00651281     EISSN: 16180372     Source Type: Journal    
DOI: 10.1016/j.acthis.2013.10.001     Document Type: Article

References (43)

1. Aralla A., 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, 72:310-321.
2. Agre P., King L.S., Yasui M., Guggino W.B., Ottersen O.P., Fujiyoshi Y., et al. Aquaporin water channels - from atomic structure to clinical medicine. J Physiol 2002, 542:3-16.
3. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254.
4. Branes M.C., Morales B., Rios M., Villalon M.J. Regulation of the immunoexpression of aquaporin 9 by ovarian hormones in the rat oviductal epithelium. Am J Physiol Cell Physiol 2005, 288:C1048-C1057.
5. Brown H.M., Dunning K.R., Robker R.L., Boerboom D., Pritchard M., Lane M., et al. ADAMTS1 cleavage of versican mediates essential structural remodeling of the ovarian follicle and cumulus-oocyte matrix during ovulation in mice. Biol Reprod 2010, 83:549-557.
6. Camaioni A., Hascall V.C., Yangishita M., D'Alessandris K., Salustri A. Dynamics of the extracellular matrix in the cumulus oophorus. Microscopy of reproduction and development: a dynamic approach 1997, 137-141. Delfino A, Roma. P.M. Motta (Ed.).
7. D'Alessandris K., Canipari R., Di Giacomo M., Epifano O., Camaioni A., Siracusa G., et al. Control of mouse cumulus cell-oocyte complex integrity before and after ovulation: plasminogen activator synthesis and matrix degradation. Endocrinology 2001, 142:3033-3040.
8. Da Silva N., Silberstein C., Beaulieu V., Christine Pietrement Ch, Van Hoek A.N., Brown D., et al. Postnatal expression of aquaporins in epithelial cells of the rat epididymis. Biol Reprod 2006, 74:427-438.
9. Dekel N., Kraicer P.F., Phillips D.M., Sanchez R.S., Segal S.J. Cellular associations in the rat oocyte-cumulus cell complex: morphology and ovulatory changes. Gamete Res 1978, 1:47-57.
10. Edashige K., Sakamoto M., Kasai M. Expression of mRNAs of the aquaporin family in mouse oocytes and embryos. Cryobiology 2000, 40:171-175.
11. Familiari G., Verlengia C., Nottola S.A., Tripodi A., Hyttel P., Macchiarelli G., et al. Ultrastructural features of bovine cumulus-corona cells surrounding oocytes, zygotes and early embryos. Reprod Fertil Dev 1998, 10:315-326.
12. Ford P., Merot J., Jawerbaum A., Gimeno M.A.F., Capurro C., Parisi M. Water permeability in rat oocytes at different maturity stages: aquaporin-9 expression. J Membrane Biol 2000, 176:151-158.
13. Gilchrist R.B., Ritter L.J., Armstrong D.T. Oocyte-somatic cell interactions during follicle development in mammals. Anim Reprod Sci 2004, 82-83:431-446.
14. Grzesiak M., Williams L., Luck M.R. Testosterone influences water transport in porcine granulosa cells. Reprod Dom Anim 2013, 48:e52-e54.
15. Hermo L., Schellenberg M., Liu L.Y., Dayanandan B., Zhang T., Mandato C.A., Smith C.E. Membrane domain specificity in the spatial distribution of aquaporins 5, 7, 9, and 11 in efferent ducts and epididymis of rats. J Histochem Cytochem 2008, 56:1121-1135.
16. Huang H.F., He R.H., Sun C.C., Zhang Y., Meng O.X., Ma Y.Y. Function of aquaporins in female and male reproductive systems. Hum Reprod Update 2006, 12:785-795.
17. Hunger J., Bernecker A., Bakker H.J., Bonn M., Richter R.P. Hydration dynamics of hyaluronan and dextran. Biophys J 2012, 103:L10-L12.
18. Ishibashi K., Hara S., Kondo S. Aquaporin water channels in mammals. Clin Exp Nephrol 2009, 13:107-117.
19. Klein C., Troedsson M.H.T., Rutllant J. Expression of aquaporin water channels in equine endometrium is differentially regulated during the oestrous cycle and early pregnancy. Reprod Dom Anim 2013, 48:529-537.
20. 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, 11:1133-1143.
21. Kawashima I., Liu Z., Mullany L.K., Mihara T., Richards J.S., Shimada M. EGF-like factors induce expansion of the cumulus cell-oocyte complexes by activating calpain-mediated cell movement. Endocrinology 2012, 153:3949-3959.
22. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227:680-685.
23. 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. Reproduction 2006, 131:369-378.
24. McConnell N.A., Yunus R.S., Gross S.A., Bost K.L., Clemens M.G., Hughes F.M. Water permeability of an ovarian antral follicle is predominantly transcellular and mediated by aquaporins. Endocrinology 2002, 143:2905-2912.
25. Meng Q., Gao H., Xu C.H., Dong M., Sheng X., Sheng J., Huang H. 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, 21:123-128.
26. Mobasheri A., Kendall B.H., Maxwell J.E., Sawran A.V., German A.J., Marples D., et al. Cellular localization of aquaporins along the secretory pathway of the lactating bovine mammary gland: an immunohistochemical study. Acta Histochem 2011, 113:137-149.
27. Moehren U., Denayer S., Podvinec M., Verrijdt G., Claessens F. Identification of androgen-selective androgen-response elements in the human aquaporin-5 and Rad9 genes. Biochem J 2008, 411:679-686.
28. Motta P.M., Nottola S.A., Familiari G., Macchiarelli G., Correr S., Makabe S. Structure and function of the human oocyte-cumulus-corona cell complex before and after ovulation. Protoplasma 1999, 206:270-277.
29. Okada A., Ohta Y., Inoue S., Hiroi H., Muramatsu M., Iguchi T. Expression of estrogen, progesterone and androgen receptors in the oviduct of developing, cycling and pre-implantation rats. J Mol Endocrinol 2003, 30:301-315.
30. Pelletier G., Labrie C., Labie F. Localization of oestrogen receptor α, oestrogen receptor β and androgen receptors in the rat reproductive organs. J Endocrinol 2000, 165:359-370.
31. Rodgers R.J., Irving-Rodgers H.F. Formation of the ovarian follicular antrum and follicular fluid. Biol Reprod 2010, 82:1021-1029.
32. Salustri A. Paracrine actions of oocytes in the mouse pre-ovulatory follicle. Int J Dev Biol 2000, 44:591-597.
33. Skowronski M.T., Kwon T., Nielsen S. Immunolocalization of aquaporin 1, 5, and 9 in the female pig reproductive system. J Histochem Cytochem 2009, 57:61-67.
34. 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, 8:109-120.
35. Sotello J.R., Porter K. An electron microscope study of the rat ovum. J Biophys Biochem Cytol 1959, 5:327-340.
36. Szoltys M., Sakiewicz A., Galas J., Jaworska-Caudelier M., Kula E. Changes in follicular fluid concentrations of steroids, the pattern of steroid secretion and aromatization capability of incubated preovulatory follicular wall of rats. Reprod Biol 2001, 1:42-50.
37. Szoltys M., Slomczynska M., Knapczyk-Stwora K., Durlej M., Lechowska A., Starowicz A. Immunolocalization of androgen receptor and steroidogenic enzymes in cumuli oophori of pre- and post-ovulatory rats. Acta Histochem 2010, 112:576-582.
38. Szoltys M., Slomczynska M. Changes in distribution of androgen receptor during maturation of rat ovarian follicles. J Exp Clin Endocrinol Diabetes 2000, 108:228-234.
39. Takata K., Matuszak T., Tajika Y., Aquaporins: water channel proteins of the cell membrane. Prog Histochem Cytochem 2004, 39:1-83.
40. 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.
41. West-Farrell E.R., Xu M., Gomberg M.A., Chow Y.H., Woodruff T.K., Shea L.D. The mouse follicle microenvironment regulates antrum formation and steroid production: alterations in gene expression profiles. Biol Reprod 2009, 80:432-439.
42. Zhang D., Tan Y.J., Qu F., Sheng J.Z., Huang H.F. Functions of water channels in male and female reproductive systems. Mol Aspects Med 2012, 33:676-690.
43. Zhang H., Zhang Y., Zhao H., Zhang Y., Chen Q., et al. Hormonal regulation of ovarian bursa fluid in mice and involvement of aquaporins. PLoS ONE 2013, 8:e638623.