Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.21451/1984-3143-AR2018-0012
Animal Reproduction (AR)
Conference Paper

Modeling early embryo-maternal interactions in vitro

Jennifer Schoen, Shuai Chen

Downloads: 0
Views: 1413

Abstract

Environmental conditions experienced during early embryonic development influence growth, metabolism, and gene expression of the embryo as well as the epigenetic profile of the offspring. The environment of the early embryo consists of the luminal fluid within the oviduct and uterus and the epithelial cells composing this fluid. Whether the embryo is able to shape its own microenvironment by interacting with the epithelial lining of the oviduct/uterus and which factors potentially interfere with or regulate these interactions remains to be elucidated. As early embryonic signals and the respective maternal responses are subtle and local events, it is challenging to study them in vivo. Therefore, adequate in vitro-models optimally mimicking the contact zone between the maternal reproductive tract and the early embryo are needed to a) elucidate basic mechanisms involved in early embryonic development and b) reduce the number of experimental animals used for such studies. Functional epithelial cells are generally defined by a polarized distribution of organelles and proteins. Proper polarization is tightly connected with physiological cell behavior and in vivo-like reactivity of the epithelium. Therefore, this review summarizes current strategies for in vitro preservation of epithelial cell polarity. It presents recent advances in 3D culture of female reproductive tract epithelia and embryo-epithelial co-cultures. A special emphasis is set on compartmentalized culture systems, powerful tools for studying early embryo-maternal interactions in vitro. In such systems, cultured epithelial cells are manipulable from their basolateral as well as their apical cell pole, allowing concomitant application of embryonic as well as maternal effectors from the appropriate cellular compartment.

Keywords

embryo-maternal interactions, endometrium, oviduct, three dimensional cell culture models.

References

Absalon-Medina VA, Butler WR, Gilbert RO. 2014. Preimplantation embryo metabolism and culture systems: experience from domestic animals and clinical implications. J Assist Reprod Genet, 31:393-409.

Alminana C, Heath PR, Wilkinson S, Sanchez-Osorio J, Cuello C, Parrilla I, Gil MA, Vazquez JL, Vazquez JM, Roca J, Martinez EA, Fazeli A. 2012. Early developing pig embryos mediate their own environment in the maternal tract. PLoS One, 7:e33625.

Arnold JT, Kaufman DG, Seppala M, Lessey BA. 2001. Endometrial stromal cells regulate epithelial cell growth in vitro: a new co-culture model. Hum Reprod, 16:836-845.

Aumailley M, Timpl R. 1986. Attachment of cells to basement membrane collagen type IV. J Cell Biol, 103:1569-1575.

Briton-Jones C, Lok IH, Yuen PM, Chiu TT, Cheung LP, Haines C. 2002. Human oviductin mRNA expression is not maintained in oviduct mucosal cell culture. Fertil Steril, 77:576-580.

Briton-Jones C, Lok IH, Cheung CK, Chiu TT, Cheung LP, Haines C. 2004. Estradiol regulation of oviductin/oviduct-specific glycoprotein messenger ribonucleic acid expression in human oviduct mucosal cells in vitro. Fertil Steril, 81(suppl. 1):749-756.

Buck VU, Gellersen B, Leube RE, Classen-Linke I. 2015. Interaction of human trophoblast cells with gland-like endometrial spheroids: a model system for trophoblast invasion. Hum Reprod, 30:906-916.

Carvalho AV, Canon E, Jouneau L, Archilla C, Laffont L, Moroldo M, Ruffini S, Corbin E, Mermillod P, Duranthon V. 2017. Different co-culture systems have the same impact on bovine embryo transcriptome. Reproduction, 154:695-710.

Chen S, Einspanier R, Schoen J. 2013. In vitro mimicking of estrous cycle stages in porcine oviduct epithelium cells: estradiol and progesterone regulate differentiation, gene expression, and cellular function. Biol Reprod, 89:54. doi: 10.1095/biolreprod. 113.108829.

Chen S, Palma-Vera SE, Langhammer M, Galuska SP, Braun BC, Krause E, Lucas-Hahn A, Schoen J. 2017. An air-liquid interphase approach for modeling the early embryo-maternal contact zone. Sci Rep, 7:42298.

Classen-Linke I, Kusche M, Knauthe R, Beier HM. 1997. Establishment of a human endometrial cell culture system and characterization of its polarized hormone responsive epithelial cells. Cell Tissue Res, 287:171-185.

Cordova A, Perreau C, Tsikis G, Reynaud K, Locatelli Y, Ponsart C, Mermillod P. 2012. Effect of bovine oviductal epithelial cell co-culture on early cleavage kinetics of bovine IVP embryos. Reprod Domest Anim, 47:447-448.

Cordova A, Perreau C, Uzbekova S, Ponsart C, Locatelli Y, Mermillod P. 2014. Development rate and gene expression of IVP bovine embryos cocultured with bovine oviduct epithelial cells at early or late stage of preimplantation development. Theriogenology, 81:1163-1173.

Coy P, Canovas S, Mondejar I, Saavedra MD, Romar R, Grullon L, Matas C, Aviles M. 2008. Oviduct-specific glycoprotein and heparin modulate sperm-zona pellucida interaction during fertilization and contribute to the control of polyspermy. Proc Natl Acad Sci USA, 105:15809-15814.

Cunha GR, Bigsby RM, Cooke PS, and Sugimura Y. 1985. Stromal-epithelial interactions in adult organs. Cell Differ, 17(3):137-148.

Danesh MS, Sharbati J, Einspanier R, Gabler C. 2016. mRNA expression pattern of selected candidate genes differs in bovine oviductal epithelial cells in vitro compared with the in vivo state and during cell culture passages. Reprod Biol Endocrinol, 14:44. doi: 10.1186/s12958-016-0176-7.

De Pauw IM, Van Soom A, Laevens H, Verberckmoes S, de Kruif A. 2002. Sperm binding to epithelial oviduct explants in bulls with different nonreturn rates investigated with a new in vitro model. Biol Reprod, 67:1073-1079.

Ellenbroek SI, Iden S, Collard JG. 2012. Cell polarity proteins and cancer. Semin Cancer Biol, 22:208-215.

Fazeli A. 2011. Maternal communication with gametes and embryo: a personal opinion. Reprod Domest Anim, 46(suppl. 2):75-78.

Fazeli A, Holt WV. 2016. Cross talk during the periconception period. Theriogenology, 86:438-442.

Ferraz M, Henning HHW, Costa PF, Malda J, Melchels FP, Wubbolts R, Stout TAE, Vos P, Gadella BM. 2017. Improved bovine embryo production in an oviduct-on-a-chip system: prevention of poly-spermic fertilization and parthenogenic activation. Lab Chip, 17:905-916.

Freeman DA, Woods GL, Vanderwall DK, Weber JA. 1992. Embryo-initiated oviductal transport in mares. J Reprod Fertil, 95:535-538.

Garcia EV, Hamdi M, Barrera AD, Sanchez-Calabuig MJ, Gutierrez-Adan A, Rizos D. 2017. Bovine embryo-oviduct interaction in vitro reveals an early cross talk mediated by BMP signaling. Reproduction, 153:631-643.

Goff AK, Smith LC. 1998. Effect of steroid treatment of endometrial cells on blastocyst development during co-culture. Theriogenology, 49:1021-1030.

Gualtieri R, Mollo V, Braun S, Barbato V, Fiorentino I, Talevi R. 2012. Long-term viability and differentiation of bovine oviductal monolayers: bidimensional versus three-dimensional culture. Theriogenology 78:1456-1464.

Henry F, Eder S, Reynaud K, Schon J, Wibbelt G, Fontbonne A, Muller K. 2015. Seminal fluid promotes in vitro sperm-oviduct binding in the domestic cat (Felis catus). Theriogenology, 83:1373-1380.

Kessler M, Hoffmann K, Brinkmann V, Thieck O, Jackisch S, Toelle B, Berger H, Mollenkopf HJ, Mangler M, Sehouli J, Fotopoulou C, Meyer TF. 2015. The Notch and Wnt pathways regulate stemness and differentiation in human fallopian tube organoids. Nat Commun, 6:8989. doi: 10.1038/ncomms9989.

Kurita T, Cooke PS, and Cunha GR. 2001. Epithelial-stromal tissue interaction in paramesonephric (Mullerian) epithelial differentiation. Dev Biol, 240(1):194-211.

Kurita T. 2011. Normal and abnormal epithelial differentiation in the female reproductive tract. Differentiation, 82:117-126.

Lee KF, Yao YQ, Kwok KL, Xu JS, Yeung WS. 2002. Early developing embryos affect the gene expression patterns in the mouse oviduct. Biochem Biophys Res Commun, 292:564-570.

Leese HJ, Hugentobler SA, Gray SM, Morris DG, Sturmey RG, Whitear SL, Sreenan JM. 2008. Female reproductive tract fluids: composition, mechanism of formation and potential role in the developmental origins of health and disease. Reprod Fertil Dev, 20:1-8.

Levanon K, Ng V, Piao HY, Zhang Y, Chang MC, Roh MH, Kindelberger DW, Hirsch MS, Crum CP, Marto JA, Drapkin R. 2010. Primary ex vivo cultures of human fallopian tube epithelium as a model for serous ovarian carcinogenesis. Oncogene, 29:1103-1113.

Li SJ, Wang TS, Qin FN, Huang Z, Liang XH, Gao F, Song Z, Yang ZM. 2015. Differential regulation of receptivity in two uterine horns of a recipient mouse following asynchronous embryo transfer. Sci Rep, 5:15897. doi: 10.1038/srep15897.

Locatelli Y, Cognie Y, Vallet JC, Baril G, Verdier M, Poulin N, Legendre X, Mermillod P. 2005. Successful use of oviduct epithelial cell coculture for in vitro production of viable red deer (Cervus elaphus) embryos. Theriogenology, 64:1729-1739.

Maillo V, Gaora PO, Forde N, Besenfelder U, Havlicek V, Burns GW, Spencer TE, Gutierrez-Adan A, Lonergan P, Rizos D. 2015. Oviduct-embryo interactions in cattle: two-way traffic or a one-way street? Biol Reprod, 92:144. doi: 10.1095/biolreprod. 115.127969.

Maillo V, Acuna OS, Aviles M, Lonergan P, Rizos D.

2016. 74 The bovine embryo influences the proteome of the oviductal fluid. Reprod Fertil Dev, 29:144. (abstract).

MacKintosh SB, Serino LP, Iddon PD, Brown R, Conlan RS, Wright CJ, Maffeis TG, Raxworthy MJ, and Sheldon IM. 2015. A three-dimensional model of primary bovine endometrium using an electrospun scaffold. Biofabrication,  7(2):025010.

Miessen K, Sharbati S, Einspanier R, Schoen J. 2011. Modelling the porcine oviduct epithelium: a polarized in vitro system suitable for long-term cultivation. Theriogenology, 76:900-910.

Munson L, Wilkinson JE, Schlafer DH. 1990. Effects of substrata on the polarization of bovine endometrial epithelial cells in vitro. Cell Tissue Res, 261:155-161.

Olalekan SA, Burdette JE, Getsios S, Woodruff TK, Kim JJ. 2017. Development of a novel human recellularized endometrium that responds to a 28 day hormone treatment. Biol Reprod, 96:971-981.

Ostrowski LE, Nettesheim P. 1995. Inhibition of ciliated cell differentiation by fluid submersion. Exp Lung Res, 21:957-970.

Pierro E, Minici F, Alesiani O, Miceli F, Proto C, Screpanti I, Mancuso S, Lanzone A. 2001. Stromal-epithelial interactions modulate estrogen responsiveness in normal human endometrium. Biol Reprod, 64:831-838.

Qi X, Qu Y, Nan Z, Jin Y, Zhao X, Wang A. 2012. Caprine endometrial stromal cells modulate the effects of steroid hormones on cytokine secretion by endometrial epithelial cells in vitro. Reprod Biol, 12:309-315.

Reischl J, Prelle K, Schol H, Neumuller C, Einspanier R, Sinowatz F, Wolf E. 1999. Factors affecting proliferation and dedifferentiation of primary bovine oviduct epithelial cells in vitro. Cell Tissue Res, 296:371-383.

Rizos D, Maillo V, Sanchez-Calabuig MJ, and Lonergan P. 2017. The consequences of maternal-embryonic cross talk during the periconception period on subsequent embryonic development. Adv Exp Med Biol, 1014:69-86.

Rottmayer R, Ulbrich SE, Kolle S, Prelle K, Neumueller C, Sinowatz F, Meyer HH, Wolf E, Hiendleder S. 2006. A bovine oviduct epithelial cell suspension culture system suitable for studying embryo-maternal interactions: morphological and functional characterization. Reproduction, 132:637-648.

Schmaltz-Panneau B, Cordova A, Dhorne-Pollet S, Hennequet-Antier C, Uzbekova S, Martinot E, Doret S, Martin P, Mermillod P, Locatelli Y. 2014. Early bovine embryos regulate oviduct epithelial cell gene expression during in vitro co-culture. Anim Reprod Sci, 149:103-116.

Schmaltz-Panneau B, Locatelli Y, Uzbekova S, Perreau C, Mermillod P. 2015. Bovine oviduct epithelial cells dedifferentiate partly in culture, while maintaining their ability to improve early embryo development rate and quality. Reprod Domest Anim, 50:719-729.

Schoen J, Bondzio A, Topp K, Einspanier R. 2008. Establishment and characterization of an adherent pure epithelial cell line derived from the bovine oviduct. Theriogenology, 69:536-545.

Simintiras CA, Frohlich T, Sathyapalan T, Arnold GJ, Ulbrich SE, Leese HJ, Sturmey RG. 2016. Modelling oviduct fluid formation in vitro. Reproduction. doi:10.1530/REP-15-0508.

Simintiras CA, Sturmey RG. 2017. Genistein crosses the bioartificial oviduct and alters secretion composition. Reprod Toxicol, 71:63-70.

Smits K, De Coninck DI, Van NF, Govaere J, Van PM, Peelman L, Deforce D, and Van SA. 2016. The equine embryo influences immune-related gene expression in the oviduct. Biol Reprod, 94:36. doi: 10.1095/biolreprod.115.136432.

Turco MY, Gardner L, Hughes J, Cindrova-Davies T, Gomez MJ, Farrell L, Hollinshead M, Marsh SGE, Brosens JJ, Critchley HO, Simons BD, Hemberger M, Koo BK, Moffett A, Burton GJ. 2017. Long-term, hormone-responsive organoid cultures of human endometrium in a chemically defined medium. Nat Cell Biol, 19:568-577.

Umezu T, Tomooka Y. 2004. An evidence of stromal cell populations functionally linked with epithelial cell populations in the mouse oviduct. Zoolog Sci, 21:319-326.

van der Weijden VA, Chen S, Bauersachs S, Ulbrich SE, Schoen J. 2017. Gene expression of bovine embryos developing at the air-liquid interface on oviductal epithelial cells (ALI-BOEC). Reprod Biol Endocrinol, 15:91. doi: 10.1186/s12958-017-0310-1.

Waberski D, Magnus F, Mendonca Ferreira F, Petrunkina AM, Weitze KF, Topfer-Petersen E. 2005. Importance of sperm-binding assays for fertility prognosis of porcine spermatozoa. Theriogenology, 63:470-484.

Wang H, Pilla F, Anderson S, Martinez-Escribano S, Herrer I, Moreno-Moya JM, Musti S, Bocca S, Oehninger S, Horcajadas JA. 2012. A novel model of human implantation: 3D endometrium-like culture system to study attachment of human trophoblast (Jar) cell spheroids. Mol Hum Reprod, 18:33-43.

Weber JA, Freeman DA, Vanderwall DK, Woods GL. 1991. Prostaglandin E2 secretion by oviductal transport-stage equine embryos. Biol Reprod, 45:540-543.

Weimar CH, Post Uiterweer ED, Teklenburg G, Heijnen CJ, Macklon NS. 2013. In-vitro model systems for the study of human embryo-endometrium interactions. Reprod Biomed Online, 27:461-476.

Xiao S, Coppeta JR, Rogers HB, Isenberg BC, Zhu J, Olalekan SA, McKinnon KE, Dokic D, Rashedi AS, Haisenleder DJ, Malpani SS, Arnold-Murray CA, Chen K, Jiang M, Bai L, Nguyen CT, Zhang J, Laronda MM, Hope TJ, Maniar KP, Pavone ME, Avram MJ, Sefton EC, Getsios S, Burdette JE, Kim JJ, Borenstein JT, Woodruff TK. 2017. A microfluidic culture model of the human reproductive tract and 28-day menstrual cycle. Nat Commun, 8:14584. doi: 10.1038/ncomms14584.

Zihni C, Mills C, Matter K, Balda MS. 2016. Tight junctions: from simple barriers to multifunctional molecular gates. Nat Rev Mol Cell Biol, 17:564-580.

5b8e928a0e8825113fdd6776 animreprod Articles
Links & Downloads

Anim Reprod

Share this page
Page Sections