In vitro mimicking of estrous cycle stages in porcine oviduct epithelium cells: Estradiol and progesterone regulate differentiation, gene expression, and cellular function

Biology of Reproduction

Volumn 89, Issue 3, 2013, Pages

  Chen, Shuai ^a   Einspanier, Ralf ^a   Schoen, Jennifer ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Estrous cycle stages; Fluid movement pattern; Hormonal stimulation; Oviduct epithelium; Sperm binding

Indexed keywords

COMPLEMENT COMPONENT C3; ESTRADIOL; ESTROGEN RECEPTOR ALPHA; G PROTEIN COUPLED RECEPTOR 30; HEAT SHOCK PROTEIN 90; MESSENGER RNA; MUCIN 1; PROGESTERONE; PROGESTERONE RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL COUNT; CELL DENSITY; CELL DIFFERENTIATION; CELL FUNCTION; CELL POPULATION; CILIARY MOTILITY; CONTROLLED STUDY; DIESTRUS; ELECTRIC CONDUCTIVITY; ELECTRIC RESISTANCE; ELECTRON MICROSCOPY; EPITHELIUM CELL; ESTRUS; ESTRUS CYCLE; EUKARYOTIC FLAGELLUM; FEMALE; GENE EXPRESSION REGULATION; GILT (SWINE); HISTOLOGY; HORMONAL REGULATION; HORMONE RESPONSE; IN VITRO STUDY; MARKER GENE; NONHUMAN; OVIDUCT EPITHELIUM CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; SECRETORY CELL; SECRETORY GRANULE; SPERM; UTERINE TUBE MUCOSA;

ESTROUS CYCLE STAGES; FLUID MOVEMENT PATTERN; HORMONAL STIMULATION; OVIDUCT EPITHELIUM; SPERM BINDING;

ANIMALS; CELL COMMUNICATION; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELLS, CULTURED; EPITHELIAL CELLS; ESTRADIOL; ESTROUS CYCLE; FALLOPIAN TUBES; FEMALE; GENE EXPRESSION REGULATION; MALE; MODELS, BIOLOGICAL; PROGESTERONE; SPERMATOZOA; SWINE;

EID: 84889586113     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.113.108829     Document Type: Article

References (45)

1. Killian GJ. Evidence for the role of oviduct secretions in sperm function, fertilization and embryo development. Anim Reprod Sci 2004; 82-83: 141-153.
2. Lyons RA, Saridogan E, Djahanbakhch O. The reproductive significance of human fallopian tube cilia. Hum Reprod Update 2006; 12:363-372.
3. Abe H, Hoshi H. Regional and cyclic variations in the ultrastructural features of secretory cells in the oviductal epithelium of the Chinese Meishan pig. Reprod Domest Anim 2007; 42:292-298.
4. Steinhauer N, Boos A, Gunzel-Apel AR. Morphological changes and proliferative activity in the oviductal epithelium during hormonally defined stages of the oestrous cycle in the bitch. Reprod Domest Anim 2004; 39:110-119.
5. Aguilar JJ, Cuervo-Arango J, Mouguelar H, Losinno L. Histological characteristics of the equine oviductal mucosa at different reproductive stages. J Equine Vet Sci 2012; 32:99-105.
6. Abe H, Oikawa T. Observations by scanning electron microscopy of oviductal epithelial cells from cows at follicular and luteal phases. Anat Rec 1993; 235:399-410.
7. Donnez J, Casanas-Roux F, Caprasse J, Ferin J, Thomas K. Cyclic changes in ciliation, cell height, and mitotic activity in human tubal epithelium during reproductive life. Fertil Steril 1985; 43:554-559.
8. Kawakami E, Kashiwagi C, Hori T, Tsutsui T. Effects of canine oviduct epithelial cells on movement and capacitation of homologous spermatozoa in vitro. Anim Reprod Sci 2001; 68:121-131.
9. Tienthai P, Johannisson A, Rodriguez-Martinez H. Sperm capacitation in the porcine oviduct. Anim Reprod Sci 2004; 80:131-146.
10. Fazeli A, Elliott RM, Duncan AE, Moore A, Watson PF, Holt WV. In vitro maintenance of boar sperm viability by a soluble fraction obtained from oviductal apical plasma membrane preparations. Reproduction 2003; 125:509-517.
11. Topfer-Petersen E, Wagner A, Friedrich J, Petrunkina A, Ekhlasi-Hundrieser M, Waberski D, Drommer W. Function of the mammalian oviductal sperm reservoir. J Exp Zool 2002; 292:210-215.
12. Suarez S, Redfern K, Raynor P, Martin F, Phillips DM. Attachment of boar sperm to mucosal explants of oviduct in vitro: possible role in formation of a sperm reservoir. Biol Reprod 1991; 44:998-1004.
13. Lefebvre R, Chenoweth PJ, Drost M, LeClear CT, MacCubbin M, Dutton JT, Suarez SS. Characterization of the oviductal sperm reservoir in cattle. Biol Reprod 1995; 53:1066-1074.
14. Petrunkina AM, Gehlhaar R, Drommer W, Waberski D, Topfer-Petersen E. Selective sperm binding to pig oviductal epithelium in vitro. Reproduction 2001; 121:889-896.
15. Thomas PG, Ball BA, Brinsko SP. Interaction of equine spermatozoa with oviduct epithelial cell explants is affected by estrous cycle and anatomic origin of explant. Biol Reprod 1994; 51:222-228.
16. Orihuela PA, Ortiz ME, Croxatto HB. Sperm migration into and through the oviduct following artificial insemination at different stages of the estrous cycle in the rat. Biol Reprod 1999; 60:908-913.
17. Nakahari T, Nishimura A, Shimamoto C, Sakai A, Kuwabara H, Nakano T, Tanaka S, Kohda Y, Matsumura H, Mori H. The regulation of ciliary beat frequency by ovarian steroids in the guinea pig fallopian tube: interactions between oestradiol and progesterone. Biomed Res 2011; 32: 321-328.
18. Nishimura A, Sakuma K, Shimamoto C, Ito S, Nakano T, Daikoku E, Ohmichi M, Ushiroyama T, Ueki M, Kuwabara H, Mori H, Nakahari T. Ciliary beat frequency controlled by oestradiol and progesterone during ovarian cycle in guinea-pig fallopian tube. Exp Physiol 2010; 95:819-828.
19. Miessen K, Sharbati S, Einspanier R, Schoen J. Modelling the porcine oviduct epithelium: a polarized in vitro system suitable for long-term cultivation. Theriogenology 2011; 76:900-910.
20. Schoen J, Bondzio A, Topp K, Einspanier R. Establishment and characterization of an adherent pure epithelial cell line derived from the bovine oviduct. Theriogenology 2008; 69:536-545.
21. Rottmayer R, Ulbrich SE, Kolle S, Prelle K, Neumueller C, Sinowatz F, Meyer HH, Wolf E, Hiendleder S. A bovine oviduct epithelial cell suspension culture system suitable for studying embryo-maternal interactions: morphological and functional characterization. Reproduction 2006; 132:637-648.
22. Levanon K, Ng V, Piao HY, Zhang Y, Chang MC, Roh MH, Kindelberger DW, Hirsch MS, Crum CP, Marto JA, Drapkin R. Primary ex vivo cultures of human fallopian tube epithelium as a model for serous ovarian carcinogenesis. Oncogene 2010; 29:1103-1113.
23. Rajagopal M, Tollner TL, Finkbeiner WE, Cherr GN, Widdicombe JH. Differentiated structure and function of primary cultures of monkey oviductal epithelium. In Vitro Cell Dev Biol Anim 2006; 42:248-254.
24. Wesierska-Gadek J, Schreiner T, Maurer M, Waringer A, Ranftler C. Phenol red in the culture medium strongly affects the susceptibility of human MCF-7 cells to roscovitine. Cell Mol Biol Lett 2007; 12:280-293.
25. Henricks DM, Guthrie HD, Handlin DL. Plasma estrogen, progesterone and luteinizing hormone levels during the estrous cycle in pigs. Biol Reprod 1972; 6:210-218.
26. Peralta LE, Olarte MR, Arganaraz M, Ciocca D, Miceli DC. Progesterone receptors: their localization, binding activity and expression in the pig oviduct during follicular and luteal phases. Domest Anim Endocrinol 2005; 28:74-84.
27. Satir P. Mechanisms of ciliary movement: contributions from electron microscopy. Scanning Microsc 1992; 6:573-579.
28. Sandoz D, Biosvieux-Ulrich E, Laugier C, Brard E. Ciliogenesis in the mucous cells of the quail oviduct. II. Hormonal control [in French].J Cell Biol 1976; 71:460-471.
29. Rezac P, Kukla R, Poschl M. Effect of sow parity on vaginal electrical impedance. Anim Reprod Sci 2002; 72:223-234.
30. Rezac P, Olic I. Relationship between opposite changes of vaginal and vestibular impedance during estrous cycle in sows. Theriogenology 2006; 66:868-876.
31. Ulbrich SE, Kettler A, Einspanier R. Expression and localization of estrogen receptor alpha, estrogen receptor beta and progesterone receptor in the bovine oviduct in vivo and in vitro. J Steroid Biochem Mol Biol 2003; 84:279-289.
32. Bauersachs S, Rehfeld S, Ulbrich SE, Mallok S, Prelle K, Wenigerkind H, Einspanier R, Blum H, Wolf E. Monitoring gene expression changes in bovine oviduct epithelial cells during the oestrous cycle. J Mol Endocrinol 2004; 32:449-466.
33. Kadam KM, D'Souza SJ, Natraj U. Identification of cellular isoform of oviduct-specific glycoprotein: role in oviduct tissue remodeling? Cell Tissue Res 2007; 330:545-556.
34. Thomas P, Pang Y, Filardo EJ, Dong J. Identity of an estrogen membrane receptor coupled to a G protein in human breast cancer cells. Endocrinology 2005; 146:624-632.
35. Otto C, Fuchs I, Kauselmann G, Kern H, Zevnik B, Andreasen P, Schwarz G, Altmann H, Klewer M, Schoor M, Vonk R, Fritzemeier KH. GPR30 does not mediate estrogenic responses in reproductive organs in mice. Biol Reprod 2009; 80:34-41.
36. Vigil P, Salgado AM, Cortes ME. Ultrastructural interaction between spermatozoon and human oviductal cells in vitro. J Electron Microsc (Tokyo) 2012; 61:123-126.
37. Bureau M, Bailey JL, Sirard M-A. Binding regulation of porcine spermatozoa to oviductal vesicles in vitro. J Androl 2002; 23:188-193.
38. Carrasco LC, Romar R, Aviles M, Gadea J, Coy P. Determination of glycosidase activity in porcine oviductal fluid at the different phases of the estrous cycle. Reproduction 2008; 136:833-842.
39. Talbot P, Shur BD, Myles DG. Cell adhesion and fertilization: steps in oocyte transport, sperm-zona pellucida interactions, and sperm-egg fusion. Biol Reprod 2003; 68:1-9.
40. Taylor U, Rath D, Zerbe H, Schuberth HJ. Interaction of intact porcine spermatozoa with epithelial cells and neutrophilic granulocytes during uterine passage. Reprod Domest Anim 2008; 43:166-175.
41. Kolle S, Dubielzig S, Reese S, Wehrend A, Konig P, Kummer W. Ciliary transport, gamete interaction, and effects of the early embryo in the oviduct: ex vivo analyses using a new digital videomicroscopic system in the cow. Biol Reprod 2009; 81:267-274.
42. Lyons RA, Djahanbakhch O, Mahmood T, Saridogan E, Sattar S, Sheaff MT, Naftalin AA, Chenoy R. Fallopian tube ciliary beat frequency in relation to the stage of menstrual cycle and anatomical site. Hum Reprod 2002; 17:584-588.
43. Noreikat K, Wolff M, Kummer W, Kolle S. Ciliary activity in the oviduct of cycling, pregnant, and muscarinic receptor knockout mice. Biol Reprod 2012; 86:120.
44. Salathe M. Regulation of mammalian ciliary beating. Annu Rev Physiol 2007; 69:401-422.
45. Pedersen H. Absence of dynein arms in endometrial cilia: cause of infertility? Acta Obstet Gynecol Scand 1983; 62:625-627.