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Published in: Reproductive Biology and Endocrinology 1/2018

Open Access 01-12-2018 | Research

Trophoblast differentiation, invasion and hormone secretion in a three-dimensional in vitro implantation model with rhesus monkey embryos

Authors: T. Arthur Chang, Gennadiy I. Bondarenko, Behzad Gerami-Naini, Jessica G. Drenzek, Maureen Durning, Mark A. Garthwaite, Jenna Kropp Schmidt, Thaddeus G. Golos

Published in: Reproductive Biology and Endocrinology | Issue 1/2018

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Abstract

Background

The initiation of primate embryo invasion into the endometrium and the formation of the placenta from trophoblasts, fetal mesenchyme, and vascular components are essential for the establishment of a successful pregnancy. The mechanisms which direct morphogenesis of the chorionic villi, and the interactions between trophectoderm-derived trophoblasts and the fetal mesenchyme to direct these processes during placentation are not well understood due to a dearth of systems to examine and manipulate real-time primate implantation. Here we describe an in vitro three-dimensional (3-D) model to study implantation which utilized IVF-generated rhesus monkey embryos cultured in a Matrigel explant system.

Methods

Blastocyst stage embryos were embedded in a 3-D microenvironment of a Matrigel carrier and co-cultured with a feeder layer of cells generating conditioned medium. Throughout the course of embryo co-culture embryo growth and secretions were monitored. Embedded embryos were then sectioned and stained for markers of trophoblast function and differentiation.

Results

Signs of implantation were observed including enlargement of the embryo mass, and invasion and proliferation of trophoblast outgrowths. Expression of chorionic gonadotropin defined by immunohistochemical staining, and secretion of chorionic gonadotropin and progesterone coincident with the appearance of trophoblast outgrowths, supported the conclusion that a trophoblast cell lineage formed from implanted embryos. Positive staining for selected markers including Ki67, MHC class I, NeuN, CD31, vonWillebrand Factor and Vimentin, suggest growth and differentiation of the embryo following embedding.

Conclusions

This 3-D in vitro system will facilitate further study of primate embryo biology, with potential to provide a platform for study of genes related to implantation defects and trophoblast differentiation.
Appendix
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Literature
2.
go back to reference Hohn HP, Denker HW. Experimental modulation of cell-cell adhesion, invasiveness and differentiation in trophoblast cells. Cells Tissues Organs. 2002;172:218–36.CrossRefPubMed Hohn HP, Denker HW. Experimental modulation of cell-cell adhesion, invasiveness and differentiation in trophoblast cells. Cells Tissues Organs. 2002;172:218–36.CrossRefPubMed
3.
go back to reference Weimar CH, Post Uiterweer ED, Teklenburg G, Heijnen CJ, Macklon NS. In-vitro model systems for the study of human embryo-endometrium interactions. Reprod BioMed Online. 2013;27:461–76.CrossRefPubMed Weimar CH, Post Uiterweer ED, Teklenburg G, Heijnen CJ, Macklon NS. In-vitro model systems for the study of human embryo-endometrium interactions. Reprod BioMed Online. 2013;27:461–76.CrossRefPubMed
4.
go back to reference Carver J, Martin K, Spyropoulou I, Barlow D, Sargent I, Mardon H. An in-vitro model for stromal invasion during implantation of the human blastocyst. Hum Reprod. 2003;18:283–90.CrossRefPubMed Carver J, Martin K, Spyropoulou I, Barlow D, Sargent I, Mardon H. An in-vitro model for stromal invasion during implantation of the human blastocyst. Hum Reprod. 2003;18:283–90.CrossRefPubMed
5.
go back to reference Bentin-Ley U, Pedersen B, Lindenberg S, Larsen JF, Hamberger L, Horn T. Isolation and culture of human endometrial cells in a three-dimensional culture system. J Reprod Fertil. 1994;101:327–32.CrossRefPubMed Bentin-Ley U, Pedersen B, Lindenberg S, Larsen JF, Hamberger L, Horn T. Isolation and culture of human endometrial cells in a three-dimensional culture system. J Reprod Fertil. 1994;101:327–32.CrossRefPubMed
6.
go back to reference Wang H, Pilla F, Anderson S, Martinez-Escribano S, Herrer I, Moreno-Moya JM, Musti S, Bocca S, Oehninger S, Horcajadas JA. A novel model of human implantation: 3D endometrium-like culture system to study attachment of human trophoblast (jar) cell spheroids. Mol Hum Reprod. 2012;18:33–43.CrossRefPubMed Wang H, Pilla F, Anderson S, Martinez-Escribano S, Herrer I, Moreno-Moya JM, Musti S, Bocca S, Oehninger S, Horcajadas JA. A novel model of human implantation: 3D endometrium-like culture system to study attachment of human trophoblast (jar) cell spheroids. Mol Hum Reprod. 2012;18:33–43.CrossRefPubMed
7.
go back to reference Ho H, Singh H, Aljofan M, Nie G. A high-throughput in vitro model of human embryo attachment. Fertil Steril. 2012;97:974–8.CrossRefPubMed Ho H, Singh H, Aljofan M, Nie G. A high-throughput in vitro model of human embryo attachment. Fertil Steril. 2012;97:974–8.CrossRefPubMed
8.
go back to reference Bentin-Ley U, Horn T, Sjogren A, Sorensen S, Falck Larsen J, Hamberger L. Ultrastructure of human blastocyst-endometrial interactions in vitro. J Reprod Fertil. 2000;120:337–50.CrossRefPubMed Bentin-Ley U, Horn T, Sjogren A, Sorensen S, Falck Larsen J, Hamberger L. Ultrastructure of human blastocyst-endometrial interactions in vitro. J Reprod Fertil. 2000;120:337–50.CrossRefPubMed
9.
go back to reference Lacey H, Haigh T, Westwood M, Aplin JD. Mesenchymally-derived insulin-like growth factor 1 provides a paracrine stimulus for trophoblast migration. BMC Dev Biol. 2002;2:5.CrossRefPubMedPubMedCentral Lacey H, Haigh T, Westwood M, Aplin JD. Mesenchymally-derived insulin-like growth factor 1 provides a paracrine stimulus for trophoblast migration. BMC Dev Biol. 2002;2:5.CrossRefPubMedPubMedCentral
10.
go back to reference Meseguer M, Aplin JD, Caballero-Campo P, O'Connor JE, Martin JC, Remohi J, Pellicer A, Simon C. Human endometrial mucin MUC1 is up-regulated by progesterone and down-regulated in vitro by the human blastocyst. Biol Reprod. 2001;64:590–601.CrossRefPubMed Meseguer M, Aplin JD, Caballero-Campo P, O'Connor JE, Martin JC, Remohi J, Pellicer A, Simon C. Human endometrial mucin MUC1 is up-regulated by progesterone and down-regulated in vitro by the human blastocyst. Biol Reprod. 2001;64:590–601.CrossRefPubMed
11.
go back to reference Holmberg JC, Haddad S, Wunsche V, Yang Y, Aldo PB, Gnainsky Y, Granot I, Dekel N, Mor G. An in vitro model for the study of human implantation. Am J Reprod Immunol. 2012;67:169–78.CrossRefPubMed Holmberg JC, Haddad S, Wunsche V, Yang Y, Aldo PB, Gnainsky Y, Granot I, Dekel N, Mor G. An in vitro model for the study of human implantation. Am J Reprod Immunol. 2012;67:169–78.CrossRefPubMed
12.
go back to reference Hohn HP, Linke M, Denker HW. Adhesion of trophoblast to uterine epithelium as related to the state of trophoblast differentiation: in vitro studies using cell lines. Mol Reprod Dev. 2000;57:135–45.CrossRefPubMed Hohn HP, Linke M, Denker HW. Adhesion of trophoblast to uterine epithelium as related to the state of trophoblast differentiation: in vitro studies using cell lines. Mol Reprod Dev. 2000;57:135–45.CrossRefPubMed
13.
14.
go back to reference Carter AM, Enders AC, Pijnenborg R. The role of invasive trophoblast in implantation and placentation of primates. Philos Trans R Soc Lond Ser B Biol Sci. 2015;370:20140070.CrossRef Carter AM, Enders AC, Pijnenborg R. The role of invasive trophoblast in implantation and placentation of primates. Philos Trans R Soc Lond Ser B Biol Sci. 2015;370:20140070.CrossRef
15.
go back to reference Gilchrist RB, Nayudu PL, Hodges JK. Maturation, fertilization, and development of marmoset monkey oocytes in vitro. Biol Reprod. 1997;56:238–46.CrossRefPubMed Gilchrist RB, Nayudu PL, Hodges JK. Maturation, fertilization, and development of marmoset monkey oocytes in vitro. Biol Reprod. 1997;56:238–46.CrossRefPubMed
16.
go back to reference Marshall VS, Browne MA, Knowles L, Golos TG, Thomson JA. Ovarian stimulation of marmoset monkeys (Callithrix jacchus) using recombinant human follicle stimulating hormone. J Med Primatol. 2003;32:57–66.CrossRefPubMed Marshall VS, Browne MA, Knowles L, Golos TG, Thomson JA. Ovarian stimulation of marmoset monkeys (Callithrix jacchus) using recombinant human follicle stimulating hormone. J Med Primatol. 2003;32:57–66.CrossRefPubMed
17.
go back to reference Sasaki E, Suemizu H, Shimada A, Hanazawa K, Oiwa R, Kamioka M, Tomioka I, Sotomaru Y, Hirakawa R, Eto T, et al. Generation of transgenic non-human primates with germline transmission. Nature. 2009;459:523–U550.CrossRefPubMed Sasaki E, Suemizu H, Shimada A, Hanazawa K, Oiwa R, Kamioka M, Tomioka I, Sotomaru Y, Hirakawa R, Eto T, et al. Generation of transgenic non-human primates with germline transmission. Nature. 2009;459:523–U550.CrossRefPubMed
18.
go back to reference Pope CE, Pope VZ, Beck LR. Development of baboon preimplantation embryos to post-implantation stages in vitro. Biol Reprod. 1982;27:915–23.CrossRefPubMed Pope CE, Pope VZ, Beck LR. Development of baboon preimplantation embryos to post-implantation stages in vitro. Biol Reprod. 1982;27:915–23.CrossRefPubMed
19.
go back to reference Wolf DP, Vandevoort CA, Meyer-Haas GR, Zelinski-Wooten MB, Hess DL, Baughman WL, Stouffer RL. In vitro fertilization and embryo transfer in the rhesus monkey. Biol Reprod. 1989;41:335–46.CrossRefPubMed Wolf DP, Vandevoort CA, Meyer-Haas GR, Zelinski-Wooten MB, Hess DL, Baughman WL, Stouffer RL. In vitro fertilization and embryo transfer in the rhesus monkey. Biol Reprod. 1989;41:335–46.CrossRefPubMed
20.
go back to reference Zhang L, Weston AM, Denniston RS, Goodeaux LL, Godke RA, Wolf DP. Developmental potential of rhesus monkey embryos produced by in vitro fertilization. Biol Reprod. 1994;51:433–40.CrossRefPubMed Zhang L, Weston AM, Denniston RS, Goodeaux LL, Godke RA, Wolf DP. Developmental potential of rhesus monkey embryos produced by in vitro fertilization. Biol Reprod. 1994;51:433–40.CrossRefPubMed
21.
go back to reference Bavister BD, Boatman DE, Leibfried L, Loose M, Vernon MW. Fertilization and cleavage of rhesus-monkey oocytes Invitro. Biol Reprod. 1983;28:983–99.CrossRefPubMed Bavister BD, Boatman DE, Leibfried L, Loose M, Vernon MW. Fertilization and cleavage of rhesus-monkey oocytes Invitro. Biol Reprod. 1983;28:983–99.CrossRefPubMed
23.
go back to reference Fishel SB, Edwards RG, Evans CJ. Human chorionic gonadotropin secreted by preimplantation embryos cultured in vitro. Science. 1984;223:816–8.CrossRefPubMed Fishel SB, Edwards RG, Evans CJ. Human chorionic gonadotropin secreted by preimplantation embryos cultured in vitro. Science. 1984;223:816–8.CrossRefPubMed
24.
go back to reference Lopata A, Kohlman DJ, Bowes LG, Watkins WB. Culture of marmoset blastocysts on matrigel: a model of differentiation during the implantation period. Anat Rec. 1995;241:469–86.CrossRefPubMed Lopata A, Kohlman DJ, Bowes LG, Watkins WB. Culture of marmoset blastocysts on matrigel: a model of differentiation during the implantation period. Anat Rec. 1995;241:469–86.CrossRefPubMed
25.
go back to reference Lopata A, Oliva K, Stanton PG, Robertson DM. Analysis of chorionic gonadotrophin secreted by cultured human blastocysts. Mol Hum Reprod. 1997;3:517–21.CrossRefPubMed Lopata A, Oliva K, Stanton PG, Robertson DM. Analysis of chorionic gonadotrophin secreted by cultured human blastocysts. Mol Hum Reprod. 1997;3:517–21.CrossRefPubMed
26.
go back to reference Enders AC, Boatman D, Morgan P, Bavister BD. Differentiation of blastocysts derived from in vitro-fertilized rhesus monkey ova. Biol Reprod. 1989;41:715–27.CrossRefPubMed Enders AC, Boatman D, Morgan P, Bavister BD. Differentiation of blastocysts derived from in vitro-fertilized rhesus monkey ova. Biol Reprod. 1989;41:715–27.CrossRefPubMed
27.
go back to reference Schindler M, Nur EKA, Ahmed I, Kamal J, Liu HY, Amor N, Ponery AS, Crockett DP, Grafe TH, Chung HY, et al. Living in three dimensions: 3D nanostructured environments for cell culture and regenerative medicine. Cell Biochem Biophys. 2006;45:215–27.CrossRefPubMed Schindler M, Nur EKA, Ahmed I, Kamal J, Liu HY, Amor N, Ponery AS, Crockett DP, Grafe TH, Chung HY, et al. Living in three dimensions: 3D nanostructured environments for cell culture and regenerative medicine. Cell Biochem Biophys. 2006;45:215–27.CrossRefPubMed
29.
go back to reference Miller RK, Genbacev O, Turner MA, Aplin JD, Caniggia I, Huppertz B. Human placental explants in culture: approaches and assessments. Placenta. 2005;26:439–48.CrossRefPubMed Miller RK, Genbacev O, Turner MA, Aplin JD, Caniggia I, Huppertz B. Human placental explants in culture: approaches and assessments. Placenta. 2005;26:439–48.CrossRefPubMed
30.
go back to reference LaMarca HL, Ott CM, Honer Zu Bentrup K, Leblanc CL, Pierson DL, Nelson AB, Scandurro AB, Whitley GS, Nickerson CA, Morris CA. Three-dimensional growth of extravillous cytotrophoblasts promotes differentiation and invasion. Placenta. 2005;26:709–20.CrossRefPubMed LaMarca HL, Ott CM, Honer Zu Bentrup K, Leblanc CL, Pierson DL, Nelson AB, Scandurro AB, Whitley GS, Nickerson CA, Morris CA. Three-dimensional growth of extravillous cytotrophoblasts promotes differentiation and invasion. Placenta. 2005;26:709–20.CrossRefPubMed
31.
go back to reference Liu H, Collins SF, Suggs LJ. Three-dimensional culture for expansion and differentiation of mouse embryonic stem cells. Biomaterials. 2006;27:6004–14.CrossRefPubMed Liu H, Collins SF, Suggs LJ. Three-dimensional culture for expansion and differentiation of mouse embryonic stem cells. Biomaterials. 2006;27:6004–14.CrossRefPubMed
32.
go back to reference Liu H, Lin J, Roy K. Effect of 3D scaffold and dynamic culture condition on the global gene expression profile of mouse embryonic stem cells. Biomaterials. 2006;27:5978–89.CrossRefPubMed Liu H, Lin J, Roy K. Effect of 3D scaffold and dynamic culture condition on the global gene expression profile of mouse embryonic stem cells. Biomaterials. 2006;27:5978–89.CrossRefPubMed
33.
go back to reference Gerami-Naini B, Dovzhenko OV, Durning M, Wegner FH, Thomson JA, Golos TG. Trophoblast differentiation in embryoid bodies derived from human embryonic stem cells. Endocrinology. 2004;145:1517–24.CrossRefPubMed Gerami-Naini B, Dovzhenko OV, Durning M, Wegner FH, Thomson JA, Golos TG. Trophoblast differentiation in embryoid bodies derived from human embryonic stem cells. Endocrinology. 2004;145:1517–24.CrossRefPubMed
34.
go back to reference Wolfgang MJ, Marshall VS, Eisele SG, Schotzko ML, Thomson JA, Golos TG. Efficient method for expressing transgenes in nonhuman primate embryos using a stable episomal vector. Mol Reprod Dev. 2002;62:69–73.CrossRefPubMed Wolfgang MJ, Marshall VS, Eisele SG, Schotzko ML, Thomson JA, Golos TG. Efficient method for expressing transgenes in nonhuman primate embryos using a stable episomal vector. Mol Reprod Dev. 2002;62:69–73.CrossRefPubMed
35.
go back to reference Wolfgang MJ, Eisele SG, Knowles L, Browne MA, Schotzko ML, Golos TG. Pregnancy and live birth from nonsurgical transfer of in vivo- and in vitro-produced blastocysts in the rhesus monkey. J Med Primatol. 2001;30:148–55.CrossRefPubMed Wolfgang MJ, Eisele SG, Knowles L, Browne MA, Schotzko ML, Golos TG. Pregnancy and live birth from nonsurgical transfer of in vivo- and in vitro-produced blastocysts in the rhesus monkey. J Med Primatol. 2001;30:148–55.CrossRefPubMed
36.
go back to reference Wolfgang MJ, Eisele SG, Browne MA, Schotzko ML, Garthwaite MA, Durning M, Ramezani A, Hawley RG, Thomson JA, Golos TG. Rhesus monkey placental transgene expression after lentiviral gene transfer into preimplantation embryos. Proc Natl Acad Sci U S A. 2001;98:10728–32.CrossRefPubMedPubMedCentral Wolfgang MJ, Eisele SG, Browne MA, Schotzko ML, Garthwaite MA, Durning M, Ramezani A, Hawley RG, Thomson JA, Golos TG. Rhesus monkey placental transgene expression after lentiviral gene transfer into preimplantation embryos. Proc Natl Acad Sci U S A. 2001;98:10728–32.CrossRefPubMedPubMedCentral
37.
go back to reference McKiernan SH, Bavister BD, Tasca RJ. Energy substrate requirements for in-vitro development of hamster 1- and 2-cell embryos to the blastocyst stage. Hum Reprod. 1991;6:64–75.CrossRefPubMed McKiernan SH, Bavister BD, Tasca RJ. Energy substrate requirements for in-vitro development of hamster 1- and 2-cell embryos to the blastocyst stage. Hum Reprod. 1991;6:64–75.CrossRefPubMed
38.
go back to reference McKiernan SH, Clayton MK, Bavister BD. Analysis of stimulatory and inhibitory amino acids for development of hamster one-cell embryos in vitro. Mol Reprod Dev. 1995;42:188–99.CrossRefPubMed McKiernan SH, Clayton MK, Bavister BD. Analysis of stimulatory and inhibitory amino acids for development of hamster one-cell embryos in vitro. Mol Reprod Dev. 1995;42:188–99.CrossRefPubMed
39.
go back to reference McKiernan SH, Bavister BD. Gonadotrophin stimulation of donor females decreases post-implantation viability of cultured one-cell hamster embryos. Hum Reprod. 1998;13:724–9.CrossRefPubMed McKiernan SH, Bavister BD. Gonadotrophin stimulation of donor females decreases post-implantation viability of cultured one-cell hamster embryos. Hum Reprod. 1998;13:724–9.CrossRefPubMed
40.
go back to reference Rozner AE, Durning M, Kropp J, Wiepz GJ, Golos TG. Macrophages modulate the growth and differentiation of rhesus monkey embryonic trophoblasts. Am J Reprod Immunol. 2016;76:364–75.CrossRefPubMedPubMedCentral Rozner AE, Durning M, Kropp J, Wiepz GJ, Golos TG. Macrophages modulate the growth and differentiation of rhesus monkey embryonic trophoblasts. Am J Reprod Immunol. 2016;76:364–75.CrossRefPubMedPubMedCentral
41.
go back to reference Schramm RD, Paprocki AM, VandeVoort CA. Causes of developmental failure of in-vitro matured rhesus monkey oocytes: impairments in embryonic genome activation. Hum Reprod. 2003;18:826–33.CrossRefPubMed Schramm RD, Paprocki AM, VandeVoort CA. Causes of developmental failure of in-vitro matured rhesus monkey oocytes: impairments in embryonic genome activation. Hum Reprod. 2003;18:826–33.CrossRefPubMed
42.
go back to reference McKiernan SH, Bavister BD. Culture of one-cell hamster embryos with water soluble vitamins: pantothenate stimulates blastocyst production. Hum Reprod. 2000;15:157–64.CrossRefPubMed McKiernan SH, Bavister BD. Culture of one-cell hamster embryos with water soluble vitamins: pantothenate stimulates blastocyst production. Hum Reprod. 2000;15:157–64.CrossRefPubMed
43.
go back to reference Seshagiri PB, Hearn JP. In-vitro development of in-vivo produced rhesus monkey morulae and blastocysts to hatched, attached, and post-attached blastocyst stages: morphology and early secretion of chorionic gonadotropin. Hum Reprod. 1993;8:279–87.CrossRefPubMed Seshagiri PB, Hearn JP. In-vitro development of in-vivo produced rhesus monkey morulae and blastocysts to hatched, attached, and post-attached blastocyst stages: morphology and early secretion of chorionic gonadotropin. Hum Reprod. 1993;8:279–87.CrossRefPubMed
44.
go back to reference Ziegler TE, Matteri RL, Wegner FH. Detection of urinary gonadotropins in Callitrichid monkeys with a sensitive immunoassay based upon a unique monoclonal-antibody. Am J Primatol. 1993;31:181–8.CrossRef Ziegler TE, Matteri RL, Wegner FH. Detection of urinary gonadotropins in Callitrichid monkeys with a sensitive immunoassay based upon a unique monoclonal-antibody. Am J Primatol. 1993;31:181–8.CrossRef
45.
go back to reference Munro CJ, Laughlin LS, Illera JC, Dieter J, Hendrickx AG, Lasley BL. ELISA for the measurement of serum and urinary chorionic gonadotropin concentrations in the laboratory macaque. Am J Primatol. 1997;41:307–22.CrossRefPubMed Munro CJ, Laughlin LS, Illera JC, Dieter J, Hendrickx AG, Lasley BL. ELISA for the measurement of serum and urinary chorionic gonadotropin concentrations in the laboratory macaque. Am J Primatol. 1997;41:307–22.CrossRefPubMed
46.
go back to reference Bielert C, Czaja JA, Eisele S, Scheffler G, Robinson JA, Goy RW. Mating in the rhesus monkey (Macaca mulatta) after conception and its relationship to oestradiol and progesterone levels throughout pregnancy. J Reprod Fertil. 1976;46:179–87.CrossRefPubMed Bielert C, Czaja JA, Eisele S, Scheffler G, Robinson JA, Goy RW. Mating in the rhesus monkey (Macaca mulatta) after conception and its relationship to oestradiol and progesterone levels throughout pregnancy. J Reprod Fertil. 1976;46:179–87.CrossRefPubMed
47.
go back to reference Slukvin II, Lunn DP, Watkins DI, Golos TG. Placental expression of the nonclassical MHC class I molecule Mamu-AG at implantation in the rhesus monkey. Proc Natl Acad Sci U S A. 2000;97:9104–9.CrossRefPubMedPubMedCentral Slukvin II, Lunn DP, Watkins DI, Golos TG. Placental expression of the nonclassical MHC class I molecule Mamu-AG at implantation in the rhesus monkey. Proc Natl Acad Sci U S A. 2000;97:9104–9.CrossRefPubMedPubMedCentral
48.
go back to reference Bondarenko GI, Burleigh DW, Durning M, Breburda EE, Grendell RL, Golos TG. Passive immunization against the MHC class I molecule Mamu-AG disrupts rhesus placental development and endometrial responses. J Immunol. 2007;179:8042–50.CrossRefPubMed Bondarenko GI, Burleigh DW, Durning M, Breburda EE, Grendell RL, Golos TG. Passive immunization against the MHC class I molecule Mamu-AG disrupts rhesus placental development and endometrial responses. J Immunol. 2007;179:8042–50.CrossRefPubMed
49.
go back to reference McConkey CA, Delorme-Axford E, Nickerson CA, Kim KS, Sadovsky Y, Boyle JP, Coyne CB. A three-dimensional culture system recapitulates placental syncytiotrophoblast development and microbial resistance. Sci Adv. 2016;2:e1501462.CrossRefPubMedPubMedCentral McConkey CA, Delorme-Axford E, Nickerson CA, Kim KS, Sadovsky Y, Boyle JP, Coyne CB. A three-dimensional culture system recapitulates placental syncytiotrophoblast development and microbial resistance. Sci Adv. 2016;2:e1501462.CrossRefPubMedPubMedCentral
50.
go back to reference Enders AC, Meyers S, Vandevoort CA, Douglas GC. Interactions of macaque blastocysts with epithelial cells in vitro. Hum Reprod. 2005;20:3026–32.CrossRefPubMed Enders AC, Meyers S, Vandevoort CA, Douglas GC. Interactions of macaque blastocysts with epithelial cells in vitro. Hum Reprod. 2005;20:3026–32.CrossRefPubMed
51.
go back to reference Pankov R, Cukierman E, Katz BZ, Matsumoto K, Lin DC, Lin S, Hahn C, Yamada KM. Integrin dynamics and matrix assembly: tensin-dependent translocation of alpha(5)beta(1) integrins promotes early fibronectin fibrillogenesis. J Cell Biol. 2000;148:1075–90.CrossRefPubMedPubMedCentral Pankov R, Cukierman E, Katz BZ, Matsumoto K, Lin DC, Lin S, Hahn C, Yamada KM. Integrin dynamics and matrix assembly: tensin-dependent translocation of alpha(5)beta(1) integrins promotes early fibronectin fibrillogenesis. J Cell Biol. 2000;148:1075–90.CrossRefPubMedPubMedCentral
52.
go back to reference Burrows TD, King A, Smith SK, Loke YW. Human trophoblast adhesion to matrix proteins: inhibition and signal transduction. Hum Reprod. 1995;10:2489–500.CrossRefPubMed Burrows TD, King A, Smith SK, Loke YW. Human trophoblast adhesion to matrix proteins: inhibition and signal transduction. Hum Reprod. 1995;10:2489–500.CrossRefPubMed
53.
go back to reference Davidson LM, Coward K. Molecular mechanisms of membrane interaction at implantation. Birth Defects Res C Embryo Today. 2016;108:19–32.CrossRefPubMed Davidson LM, Coward K. Molecular mechanisms of membrane interaction at implantation. Birth Defects Res C Embryo Today. 2016;108:19–32.CrossRefPubMed
54.
go back to reference Fisher SJ, Cui TY, Zhang L, Hartman L, Grahl K, Zhang GY, Tarpey J, Damsky CH. Adhesive and degradative properties of human placental cytotrophoblast cells in vitro. J Cell Biol. 1989;109:891–902.CrossRefPubMed Fisher SJ, Cui TY, Zhang L, Hartman L, Grahl K, Zhang GY, Tarpey J, Damsky CH. Adhesive and degradative properties of human placental cytotrophoblast cells in vitro. J Cell Biol. 1989;109:891–902.CrossRefPubMed
55.
go back to reference Aplin JD, Haigh T, Jones CJ, Church HJ, Vicovac L. Development of cytotrophoblast columns from explanted first-trimester human placental villi: role of fibronectin and integrin alpha5beta1. Biol Reprod. 1999;60:828–38.CrossRefPubMed Aplin JD, Haigh T, Jones CJ, Church HJ, Vicovac L. Development of cytotrophoblast columns from explanted first-trimester human placental villi: role of fibronectin and integrin alpha5beta1. Biol Reprod. 1999;60:828–38.CrossRefPubMed
56.
go back to reference Blankenship TN, Enders AC. Trophoblast cell-mediated modifications to uterine spiral arteries during early gestation in the macaque. Acta Anat (Basel). 1997;158:227–36.CrossRef Blankenship TN, Enders AC. Trophoblast cell-mediated modifications to uterine spiral arteries during early gestation in the macaque. Acta Anat (Basel). 1997;158:227–36.CrossRef
57.
go back to reference Kliman HJ, Nestler JE, Sermasi E, Sanger JM, Strauss JF 3rd. Purification, characterization, and in vitro differentiation of cytotrophoblasts from human term placentae. Endocrinology. 1986;118:1567–82.CrossRefPubMed Kliman HJ, Nestler JE, Sermasi E, Sanger JM, Strauss JF 3rd. Purification, characterization, and in vitro differentiation of cytotrophoblasts from human term placentae. Endocrinology. 1986;118:1567–82.CrossRefPubMed
58.
go back to reference Seshagiri PB, Terasawa E, Hearn JP. The secretion of gonadotrophin-releasing hormone by peri-implantation embryos of the rhesus monkey: comparison with the secretion of chorionic gonadotrophin. Hum Reprod. 1994;9:1300–7.CrossRefPubMed Seshagiri PB, Terasawa E, Hearn JP. The secretion of gonadotrophin-releasing hormone by peri-implantation embryos of the rhesus monkey: comparison with the secretion of chorionic gonadotrophin. Hum Reprod. 1994;9:1300–7.CrossRefPubMed
59.
go back to reference Blaschitz A, Weiss U, Dohr G, Desoye G. Antibody reaction patterns in first trimester placenta: implications for trophoblast isolation and purity screening. Placenta. 2000;21:733–41.CrossRefPubMed Blaschitz A, Weiss U, Dohr G, Desoye G. Antibody reaction patterns in first trimester placenta: implications for trophoblast isolation and purity screening. Placenta. 2000;21:733–41.CrossRefPubMed
60.
go back to reference Haigh T, Chen C, Jones CJ, Aplin JD. Studies of mesenchymal cells from 1st trimester human placenta: expression of cytokeratin outside the trophoblast lineage. Placenta. 1999;20:615–25.CrossRefPubMed Haigh T, Chen C, Jones CJ, Aplin JD. Studies of mesenchymal cells from 1st trimester human placenta: expression of cytokeratin outside the trophoblast lineage. Placenta. 1999;20:615–25.CrossRefPubMed
61.
go back to reference Muhlhauser J, Crescimanno C, Kasper M, Zaccheo D, Castellucci M. Differentiation of human trophoblast populations involves alterations in cytokeratin patterns. J Histochem Cytochem. 1995;43:579–89.CrossRefPubMed Muhlhauser J, Crescimanno C, Kasper M, Zaccheo D, Castellucci M. Differentiation of human trophoblast populations involves alterations in cytokeratin patterns. J Histochem Cytochem. 1995;43:579–89.CrossRefPubMed
62.
go back to reference DaSilva-Arnold S, James JL, Al-Khan A, Zamudio S, Illsley NP. Differentiation of first trimester cytotrophoblast to extravillous trophoblast involves an epithelial-mesenchymal transition. Placenta. 2015;36:1412–8.CrossRefPubMed DaSilva-Arnold S, James JL, Al-Khan A, Zamudio S, Illsley NP. Differentiation of first trimester cytotrophoblast to extravillous trophoblast involves an epithelial-mesenchymal transition. Placenta. 2015;36:1412–8.CrossRefPubMed
63.
go back to reference Boyson JE, Iwanaga KK, Golos TG, Watkins DI. Identification of a novel MHC class I gene, Mamu-AG, expressed in the placenta of a primate with an inactivated G locus. J Immunol. 1997;159:3311–21.PubMed Boyson JE, Iwanaga KK, Golos TG, Watkins DI. Identification of a novel MHC class I gene, Mamu-AG, expressed in the placenta of a primate with an inactivated G locus. J Immunol. 1997;159:3311–21.PubMed
64.
go back to reference Slukvin II, Boyson JE, Watkins DI, Golos TG. The rhesus monkey analogue of human lymphocyte antigen-G is expressed primarily in villous syncytiotrophoblasts. Biol Reprod. 1998;58:728–38.CrossRefPubMed Slukvin II, Boyson JE, Watkins DI, Golos TG. The rhesus monkey analogue of human lymphocyte antigen-G is expressed primarily in villous syncytiotrophoblasts. Biol Reprod. 1998;58:728–38.CrossRefPubMed
65.
go back to reference Ryan AF, Grendell RL, Geraghty DE, Golos TG. A soluble isoform of the rhesus monkey nonclassical MHC class I molecule Mamu-AG is expressed in the placenta and the testis. J Immunol. 2002;169:673–83.CrossRefPubMed Ryan AF, Grendell RL, Geraghty DE, Golos TG. A soluble isoform of the rhesus monkey nonclassical MHC class I molecule Mamu-AG is expressed in the placenta and the testis. J Immunol. 2002;169:673–83.CrossRefPubMed
Metadata
Title
Trophoblast differentiation, invasion and hormone secretion in a three-dimensional in vitro implantation model with rhesus monkey embryos
Authors
T. Arthur Chang
Gennadiy I. Bondarenko
Behzad Gerami-Naini
Jessica G. Drenzek
Maureen Durning
Mark A. Garthwaite
Jenna Kropp Schmidt
Thaddeus G. Golos
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2018
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/s12958-018-0340-3

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