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Published in: Reproductive Biology and Endocrinology 1/2020

01-12-2020 | Endometrial Cancer | Review

Organoid technology in female reproductive biomedicine

Authors: Heidar Heidari-Khoei, Fereshteh Esfandiari, Mohammad Amin Hajari, Zeynab Ghorbaninejad, Abbas Piryaei, Hossein Baharvand

Published in: Reproductive Biology and Endocrinology | Issue 1/2020

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Abstract

Recent developments in organoid technology are revolutionizing our knowledge about the biology, physiology, and function of various organs. Female reproductive biology and medicine also benefit from this technology. Organoids recapitulate features of different reproductive organs including the uterus, fallopian tubes, and ovaries, as well as trophoblasts. The genetic stability of organoids and long-lasting commitment to their tissue of origin during long-term culture makes them attractive substitutes for animal and in vitro models. Despite current limitations, organoids offer a promising platform to address fundamental questions regarding the reproductive system’s physiology and pathology. They provide a human source to harness stem cells for regenerative medicine, heal damaged epithelia in specific diseases, and study biological processes in healthy and pathological conditions. The combination of male and female reproductive organoids with other technologies, such as microfluidics technology, would enable scientists to create a multi-organoid-on-a-chip platform for the next step to human-on-a-chip platforms for clinical applications, drug discovery, and toxicology studies. The present review discusses recent advances in producing organoid models of reproductive organs and highlights their applications, as well as technical challenges and future directions.
Literature
1.
go back to reference Young AN, Moyle-Heyrman G, Kim JJ, Burdette JE. Microphysiologic systems in female reproductive biology. Exp Biol Med. 2017;242(17):1690–700.CrossRef Young AN, Moyle-Heyrman G, Kim JJ, Burdette JE. Microphysiologic systems in female reproductive biology. Exp Biol Med. 2017;242(17):1690–700.CrossRef
2.
go back to reference Laronda MM, Burdette JE, Kim JJ, Woodruff TK. Recreating the female reproductive tract in vitro using iPSC technology in a linked microfluidics environment. Stem Cell Res Ther. 2013;4(1):S13.PubMedPubMedCentralCrossRef Laronda MM, Burdette JE, Kim JJ, Woodruff TK. Recreating the female reproductive tract in vitro using iPSC technology in a linked microfluidics environment. Stem Cell Res Ther. 2013;4(1):S13.PubMedPubMedCentralCrossRef
3.
go back to reference Turco MY, Gardner L, Hughes J, Cindrova-Davies T, Gomez MJ, Farrell L, et al. Long-term, hormone-responsive organoid cultures of human endometrium in a chemically defined medium. Nat Cell Biol. 2017;19(5):568–77.PubMedPubMedCentralCrossRef Turco MY, Gardner L, Hughes J, Cindrova-Davies T, Gomez MJ, Farrell L, et al. Long-term, hormone-responsive organoid cultures of human endometrium in a chemically defined medium. Nat Cell Biol. 2017;19(5):568–77.PubMedPubMedCentralCrossRef
4.
go back to reference Boretto M, Cox B, Noben M, Hendriks N, Fassbender A, Roose H, et al. Development of organoids from mouse and human endometrium showing endometrial epithelium physiology and long-term expandability. Development. 2017;144(10):1775–86. Boretto M, Cox B, Noben M, Hendriks N, Fassbender A, Roose H, et al. Development of organoids from mouse and human endometrium showing endometrial epithelium physiology and long-term expandability. Development. 2017;144(10):1775–86.
5.
go back to reference Haider S, Meinhardt G, Saleh L, Kunihs V, Gamperl M, Kaindl U, et al. Self-renewing trophoblast organoids recapitulate the developmental program of the early human placenta. Stem cell Rep. 2018;11(2):537–51.CrossRef Haider S, Meinhardt G, Saleh L, Kunihs V, Gamperl M, Kaindl U, et al. Self-renewing trophoblast organoids recapitulate the developmental program of the early human placenta. Stem cell Rep. 2018;11(2):537–51.CrossRef
6.
go back to reference Weimar CH, Uiterweer EDP, Teklenburg G, Heijnen CJ, Macklon NS. In-vitro model systems for the study of human embryo–endometrium interactions. Reprod Biomed Online. 2013;27(5):461–76.PubMedCrossRef Weimar CH, Uiterweer EDP, Teklenburg G, Heijnen CJ, Macklon NS. In-vitro model systems for the study of human embryo–endometrium interactions. Reprod Biomed Online. 2013;27(5):461–76.PubMedCrossRef
8.
go back to reference Ferraz MA, Henning HH, Stout TA, Vos PL, Gadella BM. Designing 3-dimensional in vitro oviduct culture systems to study mammalian fertilization and embryo production. Ann Biomed Eng. 2017;45(7):1731–44.PubMedCrossRef Ferraz MA, Henning HH, Stout TA, Vos PL, Gadella BM. Designing 3-dimensional in vitro oviduct culture systems to study mammalian fertilization and embryo production. Ann Biomed Eng. 2017;45(7):1731–44.PubMedCrossRef
9.
go back to reference Łaniewski P, Gomez A, Hire G, So M, Herbst-Kralovetz MM. Human three-dimensional endometrial epithelial cell model to study host interactions with vaginal bacteria and Neisseria gonorrhoeae. Infect Immun. 2017;85(3):e01049–16. Łaniewski P, Gomez A, Hire G, So M, Herbst-Kralovetz MM. Human three-dimensional endometrial epithelial cell model to study host interactions with vaginal bacteria and Neisseria gonorrhoeae. Infect Immun. 2017;85(3):e01049–16.
11.
go back to reference Bersinger NA, Genewein E, Müller O, Altermatt H, McKinnon B, Mueller M. Morphology of human endometrial explants and secretion of stromal marker proteins in short-and long-term cultures. Gynecol Surg. 2010;7(1):75–80.CrossRef Bersinger NA, Genewein E, Müller O, Altermatt H, McKinnon B, Mueller M. Morphology of human endometrial explants and secretion of stromal marker proteins in short-and long-term cultures. Gynecol Surg. 2010;7(1):75–80.CrossRef
12.
go back to reference Schäfer WR, Fischer L, Roth K, Jüllig AK, Stuckenschneider JE, Schwartz P, et al. Critical evaluation of human endometrial explants as an ex vivo model system: a molecular approach. Mol Hum Reprod. 2010;17(4):255–65.PubMedCrossRef Schäfer WR, Fischer L, Roth K, Jüllig AK, Stuckenschneider JE, Schwartz P, et al. Critical evaluation of human endometrial explants as an ex vivo model system: a molecular approach. Mol Hum Reprod. 2010;17(4):255–65.PubMedCrossRef
13.
go back to reference Lancaster MA, Knoblich JA. Organogenesis in a dish: modeling development and disease using organoid technologies. Science. 2014;345(6194):1247125.PubMedCrossRef Lancaster MA, Knoblich JA. Organogenesis in a dish: modeling development and disease using organoid technologies. Science. 2014;345(6194):1247125.PubMedCrossRef
14.
go back to reference Hill SJ, Decker B, Roberts EA, Horowitz NS, Muto MG, Worley MJ, et al. Prediction of DNA repair inhibitor response in short-term patient-derived ovarian cancer organoids. Cancer Discov. 2018;8(11):1404–21.PubMedPubMedCentralCrossRef Hill SJ, Decker B, Roberts EA, Horowitz NS, Muto MG, Worley MJ, et al. Prediction of DNA repair inhibitor response in short-term patient-derived ovarian cancer organoids. Cancer Discov. 2018;8(11):1404–21.PubMedPubMedCentralCrossRef
15.
go back to reference Kopper O, de Witte CJ, Lõhmussaar K, Valle-Inclan JE, Hami N, Kester L, et al. An organoid platform for ovarian cancer captures intra-and interpatient heterogeneity. Nat Med. 2019;25(5):838.PubMedCrossRef Kopper O, de Witte CJ, Lõhmussaar K, Valle-Inclan JE, Hami N, Kester L, et al. An organoid platform for ovarian cancer captures intra-and interpatient heterogeneity. Nat Med. 2019;25(5):838.PubMedCrossRef
16.
go back to reference Maenhoudt N, Defraye C, Boretto M, Jan Z, Heremans R, Boeckx B, et al. Developing organoids from ovarian cancer as experimental and preclinical models. Stem Cell Rep. 2020;14(4):717–29.CrossRef Maenhoudt N, Defraye C, Boretto M, Jan Z, Heremans R, Boeckx B, et al. Developing organoids from ovarian cancer as experimental and preclinical models. Stem Cell Rep. 2020;14(4):717–29.CrossRef
17.
go back to reference Maru Y, Tanaka N, Itami M, Hippo Y. Efficient use of patient-derived organoids as a preclinical model for gynecologic tumors. Gynecol Oncol. 2019;154(1):189–98.PubMedCrossRef Maru Y, Tanaka N, Itami M, Hippo Y. Efficient use of patient-derived organoids as a preclinical model for gynecologic tumors. Gynecol Oncol. 2019;154(1):189–98.PubMedCrossRef
18.
go back to reference Brüssow KP, Ratky J, Rodriguez-Martinez H. Fertilization and early embryonic development in the porcine fallopian tube. Reprod Domest Anim. 2008;43:245–51.PubMedCrossRef Brüssow KP, Ratky J, Rodriguez-Martinez H. Fertilization and early embryonic development in the porcine fallopian tube. Reprod Domest Anim. 2008;43:245–51.PubMedCrossRef
19.
go back to reference Salvador S, Gilks B, Köbel M, Huntsman D, Rosen B, Miller D. The fallopian tube: primary site of most pelvic high-grade serous carcinomas. Int J Gynecol Cancer. 2009;19(1):58–64.PubMedCrossRef Salvador S, Gilks B, Köbel M, Huntsman D, Rosen B, Miller D. The fallopian tube: primary site of most pelvic high-grade serous carcinomas. Int J Gynecol Cancer. 2009;19(1):58–64.PubMedCrossRef
20.
go back to reference Price M, Ades A, Welton N, Simms I, Horner P. Pelvic inflammatory disease and salpingitis: incidence of primary and repeat episodes in England. Epidemiol Infect. 2017;145(1):208–15.PubMedCrossRef Price M, Ades A, Welton N, Simms I, Horner P. Pelvic inflammatory disease and salpingitis: incidence of primary and repeat episodes in England. Epidemiol Infect. 2017;145(1):208–15.PubMedCrossRef
21.
go back to reference Xiao S, Coppeta JR, Rogers HB, Isenberg BC, Zhu J, Olalekan SA, et al. A microfluidic culture model of the human reproductive tract and 28-day menstrual cycle. Nat Commun. 2017;8:14584.PubMedPubMedCentralCrossRef Xiao S, Coppeta JR, Rogers HB, Isenberg BC, Zhu J, Olalekan SA, et al. A microfluidic culture model of the human reproductive tract and 28-day menstrual cycle. Nat Commun. 2017;8:14584.PubMedPubMedCentralCrossRef
22.
go back to reference Yucer N, Holzapfel M, Vogel TJ, Lenaeus L, Ornelas L, Laury A, et al. Directed differentiation of human induced pluripotent stem cells into fallopian tube epithelium. Sci Rep. 2017;7(1):10741.PubMedPubMedCentralCrossRef Yucer N, Holzapfel M, Vogel TJ, Lenaeus L, Ornelas L, Laury A, et al. Directed differentiation of human induced pluripotent stem cells into fallopian tube epithelium. Sci Rep. 2017;7(1):10741.PubMedPubMedCentralCrossRef
23.
go back to reference Xie Y, Park E-S, Xiang D, Li Z. Long-term organoid culture reveals enrichment of organoid-forming epithelial cells in the fimbrial portion of mouse fallopian tube. Stem Cell Res. 2018;32:51–60.PubMedCrossRef Xie Y, Park E-S, Xiang D, Li Z. Long-term organoid culture reveals enrichment of organoid-forming epithelial cells in the fimbrial portion of mouse fallopian tube. Stem Cell Res. 2018;32:51–60.PubMedCrossRef
24.
go back to reference Boretto M, Maenhoudt N, Luo X, Hennes A, Boeckx B, Bui B, et al. Patient-derived organoids from endometrial disease capture clinical heterogeneity and are amenable to drug screening. Nat Cell Biol. 2019;21(8):1041–51.PubMedCrossRef Boretto M, Maenhoudt N, Luo X, Hennes A, Boeckx B, Bui B, et al. Patient-derived organoids from endometrial disease capture clinical heterogeneity and are amenable to drug screening. Nat Cell Biol. 2019;21(8):1041–51.PubMedCrossRef
25.
go back to reference Kessler M, Hoffmann K, Brinkmann V, Thieck O, Jackisch S, Toelle B, et al. The notch and Wnt pathways regulate stemness and differentiation in human fallopian tube organoids. Nat Commun. 2015;6:8989.PubMedCrossRef Kessler M, Hoffmann K, Brinkmann V, Thieck O, Jackisch S, Toelle B, et al. The notch and Wnt pathways regulate stemness and differentiation in human fallopian tube organoids. Nat Commun. 2015;6:8989.PubMedCrossRef
26.
go back to reference Girda E, Huang EC, Leiserowitz GS, Smith LH. The use of endometrial cancer patient-derived organoid culture for drug sensitivity testing is feasible. Int J Gynecol Cancer. 2017;27(8):1701–7.PubMedPubMedCentralCrossRef Girda E, Huang EC, Leiserowitz GS, Smith LH. The use of endometrial cancer patient-derived organoid culture for drug sensitivity testing is feasible. Int J Gynecol Cancer. 2017;27(8):1701–7.PubMedPubMedCentralCrossRef
27.
go back to reference Turco MY, Gardner L, Kay RG, Hamilton RS, Prater M, Hollinshead MS, et al. Trophoblast organoids as a model for maternal–fetal interactions during human placentation. Nature. 2018;564(7735):263.PubMedPubMedCentralCrossRef Turco MY, Gardner L, Kay RG, Hamilton RS, Prater M, Hollinshead MS, et al. Trophoblast organoids as a model for maternal–fetal interactions during human placentation. Nature. 2018;564(7735):263.PubMedPubMedCentralCrossRef
28.
go back to reference Maru Y, Tanaka N, Ebisawa K, Odaka A, Sugiyama T, Itami M, et al. Establishment and characterization of patient-derived organoids from a young patient with cervical clear cell carcinoma. Cancer Sci. 2019;110(9):2992.PubMedPubMedCentralCrossRef Maru Y, Tanaka N, Ebisawa K, Odaka A, Sugiyama T, Itami M, et al. Establishment and characterization of patient-derived organoids from a young patient with cervical clear cell carcinoma. Cancer Sci. 2019;110(9):2992.PubMedPubMedCentralCrossRef
29.
go back to reference de Faria A, Zancanela D, Ramos A, Torqueti M, Ciancaglini P. Estrogen and phenol red free medium for osteoblast culture: study of the mineralization ability. Cytotechnology. 2016;68(4):1623–32.PubMedCrossRef de Faria A, Zancanela D, Ramos A, Torqueti M, Ciancaglini P. Estrogen and phenol red free medium for osteoblast culture: study of the mineralization ability. Cytotechnology. 2016;68(4):1623–32.PubMedCrossRef
30.
go back to reference Liu X, Chen B, Chen L, Ren W-T, Liu J, Wang G, et al. U-shape suppressive effect of phenol red on the epileptiform burst activity via activation of estrogen receptors in primary hippocampal culture. PLoS One. 2013;8(4):e60189.PubMedPubMedCentralCrossRef Liu X, Chen B, Chen L, Ren W-T, Liu J, Wang G, et al. U-shape suppressive effect of phenol red on the epileptiform burst activity via activation of estrogen receptors in primary hippocampal culture. PLoS One. 2013;8(4):e60189.PubMedPubMedCentralCrossRef
31.
go back to reference Kim S-M, Kim J-S. A review of mechanisms of implantation. Develop Reprod. 2017;21(4):351.CrossRef Kim S-M, Kim J-S. A review of mechanisms of implantation. Develop Reprod. 2017;21(4):351.CrossRef
32.
go back to reference Morice P, Leary A, Creutzberg C, Abu-Rustum N, Darai E. Endometrial cancer. Lancet. 2016;387(10023):1094–108.PubMedCrossRef Morice P, Leary A, Creutzberg C, Abu-Rustum N, Darai E. Endometrial cancer. Lancet. 2016;387(10023):1094–108.PubMedCrossRef
33.
go back to reference Bläuer M, Heinonen P, Martikainen P, Tomas E, Ylikomi T. A novel organotypic culture model for normal human endometrium: regulation of epithelial cell proliferation by estradiol and medroxyprogesterone acetate. Hum Reprod. 2005;20(4):864–71.PubMedCrossRef Bläuer M, Heinonen P, Martikainen P, Tomas E, Ylikomi T. A novel organotypic culture model for normal human endometrium: regulation of epithelial cell proliferation by estradiol and medroxyprogesterone acetate. Hum Reprod. 2005;20(4):864–71.PubMedCrossRef
34.
go back to reference Senol S, Sayar I, Ceyran AB, Ibiloglu I, Akalin I, Firat U, et al. Stromal clues in endometrial carcinoma: loss of expression of β-catenin, epithelial-mesenchymal transition regulators, and estrogen-progesterone receptor. Int J Gynecol Pathol. 2016;35(3):238.PubMedPubMedCentralCrossRef Senol S, Sayar I, Ceyran AB, Ibiloglu I, Akalin I, Firat U, et al. Stromal clues in endometrial carcinoma: loss of expression of β-catenin, epithelial-mesenchymal transition regulators, and estrogen-progesterone receptor. Int J Gynecol Pathol. 2016;35(3):238.PubMedPubMedCentralCrossRef
35.
go back to reference Pineda MJ, Lu Z, Cao D, Kim JJ. Influence of cancer-associated endometrial stromal cells on hormone-driven endometrial tumor growth. Horm Cancer. 2015;6(4):131–41.PubMedPubMedCentralCrossRef Pineda MJ, Lu Z, Cao D, Kim JJ. Influence of cancer-associated endometrial stromal cells on hormone-driven endometrial tumor growth. Horm Cancer. 2015;6(4):131–41.PubMedPubMedCentralCrossRef
36.
go back to reference Arnold JT, Kaufman DG, Seppala M, Lessey BA. Endometrial stromal cells regulate epithelial cell growth in vitro: a new co-culture model. Hum Reprod. 2001;16(5):836–45.PubMedCrossRef Arnold JT, Kaufman DG, Seppala M, Lessey BA. Endometrial stromal cells regulate epithelial cell growth in vitro: a new co-culture model. Hum Reprod. 2001;16(5):836–45.PubMedCrossRef
37.
go back to reference Stzepourginski I, Nigro G, Jacob J-M, Dulauroy S, Sansonetti PJ, Eberl G, et al. CD34+ mesenchymal cells are a major component of the intestinal stem cells niche at homeostasis and after injury. Proc Natl Acad Sci. 2017;114(4):E506–E13.PubMedCrossRefPubMedCentral Stzepourginski I, Nigro G, Jacob J-M, Dulauroy S, Sansonetti PJ, Eberl G, et al. CD34+ mesenchymal cells are a major component of the intestinal stem cells niche at homeostasis and after injury. Proc Natl Acad Sci. 2017;114(4):E506–E13.PubMedCrossRefPubMedCentral
38.
go back to reference Wang Y, Di Salvo M, Gunasekara DB, Dutton J, Proctor A, Lebhar MS, et al. Self-renewing monolayer of primary colonic or rectal epithelial cells. Cell Mol Gastroenterol Hepatol. 2017;4(1):165–82.e7.PubMedPubMedCentralCrossRef Wang Y, Di Salvo M, Gunasekara DB, Dutton J, Proctor A, Lebhar MS, et al. Self-renewing monolayer of primary colonic or rectal epithelial cells. Cell Mol Gastroenterol Hepatol. 2017;4(1):165–82.e7.PubMedPubMedCentralCrossRef
39.
go back to reference He N, van Iperen L, de Jong D, Szuhai K, Helmerhorst FM, van der Westerlaken LA, et al. Human extravillous trophoblasts penetrate decidual veins and lymphatics before remodeling spiral arteries during early pregnancy. PLoS One. 2017;12(1):e0169849.PubMedPubMedCentralCrossRef He N, van Iperen L, de Jong D, Szuhai K, Helmerhorst FM, van der Westerlaken LA, et al. Human extravillous trophoblasts penetrate decidual veins and lymphatics before remodeling spiral arteries during early pregnancy. PLoS One. 2017;12(1):e0169849.PubMedPubMedCentralCrossRef
40.
go back to reference Knöfler M, Haider S, Saleh L, Pollheimer J, Gamage TK, James J. Human placenta and trophoblast development: key molecular mechanisms and model systems. Cell Mol Life Sci. 2019;76(18):3479–96.PubMedPubMedCentralCrossRef Knöfler M, Haider S, Saleh L, Pollheimer J, Gamage TK, James J. Human placenta and trophoblast development: key molecular mechanisms and model systems. Cell Mol Life Sci. 2019;76(18):3479–96.PubMedPubMedCentralCrossRef
41.
go back to reference Chang C-W, Wakeland AK, Parast MM. Trophoblast lineage specification, differentiation and their regulation by oxygen tension. J Endocrinol. 2018;236(1):R43–56.PubMedPubMedCentralCrossRef Chang C-W, Wakeland AK, Parast MM. Trophoblast lineage specification, differentiation and their regulation by oxygen tension. J Endocrinol. 2018;236(1):R43–56.PubMedPubMedCentralCrossRef
43.
go back to reference Gagnon R. Placental insufficiency and its consequences. Eur J Obstet Gynecol Reprod Biol. 2003;110:S99–S107.PubMedCrossRef Gagnon R. Placental insufficiency and its consequences. Eur J Obstet Gynecol Reprod Biol. 2003;110:S99–S107.PubMedCrossRef
44.
45.
go back to reference Grigsby PL. Animal models to study placental development and function throughout normal and dysfunctional human pregnancy. Semin Reprod Med. 2016;34(1):11–6. Grigsby PL. Animal models to study placental development and function throughout normal and dysfunctional human pregnancy. Semin Reprod Med. 2016;34(1):11–6.
46.
go back to reference Malassine A, Frendo JL, Evain-Brion D. A comparison of placental development and endocrine functions between the human and mouse model. Hum Reprod Update. 2003;9(6):531–9.PubMedCrossRef Malassine A, Frendo JL, Evain-Brion D. A comparison of placental development and endocrine functions between the human and mouse model. Hum Reprod Update. 2003;9(6):531–9.PubMedCrossRef
47.
go back to reference Orendi K, Kivity V, Sammar M, Grimpel Y, Gonen R, Meiri H, et al. Placental and trophoblastic in vitro models to study preventive and therapeutic agents for preeclampsia. Placenta. 2011;32:S49–54.PubMedCrossRef Orendi K, Kivity V, Sammar M, Grimpel Y, Gonen R, Meiri H, et al. Placental and trophoblastic in vitro models to study preventive and therapeutic agents for preeclampsia. Placenta. 2011;32:S49–54.PubMedCrossRef
48.
go back to reference Weber M, Knoefler I, Schleussner E, Markert UR, Fitzgerald JS. HTR8/SVneo cells display trophoblast progenitor cell-like characteristics indicative of self-renewal, repopulation activity, and expression of “Stemness-” associated transcription factors. Biomed Res Int. 2013;2013:243649.PubMedPubMedCentralCrossRef Weber M, Knoefler I, Schleussner E, Markert UR, Fitzgerald JS. HTR8/SVneo cells display trophoblast progenitor cell-like characteristics indicative of self-renewal, repopulation activity, and expression of “Stemness-” associated transcription factors. Biomed Res Int. 2013;2013:243649.PubMedPubMedCentralCrossRef
49.
go back to reference Lee CQ, Gardner L, Turco M, Zhao N, Murray MJ, Coleman N, et al. What is trophoblast? A combination of criteria define human first-trimester trophoblast. Stem Cell Rep. 2016;6(2):257–72.CrossRef Lee CQ, Gardner L, Turco M, Zhao N, Murray MJ, Coleman N, et al. What is trophoblast? A combination of criteria define human first-trimester trophoblast. Stem Cell Rep. 2016;6(2):257–72.CrossRef
50.
go back to reference Telugu B, Adachi K, Schlitt J, Ezashi T, Schust D, Roberts R, et al. Comparison of extravillous trophoblast cells derived from human embryonic stem cells and from first trimester human placentas. Placenta. 2013;34(7):536–43.PubMedPubMedCentralCrossRef Telugu B, Adachi K, Schlitt J, Ezashi T, Schust D, Roberts R, et al. Comparison of extravillous trophoblast cells derived from human embryonic stem cells and from first trimester human placentas. Placenta. 2013;34(7):536–43.PubMedPubMedCentralCrossRef
51.
go back to reference McMaster MT, Librach CL, Zhou Y, Lim K-H, Janatpour MJ, DeMars R, et al. Human placental HLA-G expression is restricted to differentiated cytotrophoblasts. J Immunol. 1995;154(8):3771–8.PubMed McMaster MT, Librach CL, Zhou Y, Lim K-H, Janatpour MJ, DeMars R, et al. Human placental HLA-G expression is restricted to differentiated cytotrophoblasts. J Immunol. 1995;154(8):3771–8.PubMed
52.
go back to reference Okae H, Toh H, Sato T, Hiura H, Takahashi S, Shirane K, et al. Derivation of human trophoblast stem cells. Cell Stem Cell. 2018;22(1):50–63.e6.PubMedCrossRef Okae H, Toh H, Sato T, Hiura H, Takahashi S, Shirane K, et al. Derivation of human trophoblast stem cells. Cell Stem Cell. 2018;22(1):50–63.e6.PubMedCrossRef
53.
go back to reference Biyani M, Nishigaki K, Biyani M. Chapter 20 - biomolecular display technology: a new tool for drug discovery. In: Verma AS, Singh A, editors. Animal biotechnology. San Diego: Academic; 2014. p. 369–84.CrossRef Biyani M, Nishigaki K, Biyani M. Chapter 20 - biomolecular display technology: a new tool for drug discovery. In: Verma AS, Singh A, editors. Animal biotechnology. San Diego: Academic; 2014. p. 369–84.CrossRef
54.
go back to reference Taylor D. The pharmaceutical industry and the future of drug development. In: Pharmaceuticals in the Environment: the Royal Society of Chemistry; 2016. p. 1–33. Taylor D. The pharmaceutical industry and the future of drug development. In: Pharmaceuticals in the Environment: the Royal Society of Chemistry; 2016. p. 1–33.
55.
go back to reference Mak IW, Evaniew N, Ghert M. Lost in translation: animal models and clinical trials in cancer treatment. Am J Transl Res. 2014;6(2):114.PubMedPubMedCentral Mak IW, Evaniew N, Ghert M. Lost in translation: animal models and clinical trials in cancer treatment. Am J Transl Res. 2014;6(2):114.PubMedPubMedCentral
56.
go back to reference Henderson VC, Kimmelman J, Fergusson D, Grimshaw JM, Hackam DG. Threats to validity in the design and conduct of preclinical efficacy studies: a systematic review of guidelines for in vivo animal experiments. PLoS Med. 2013;10(7):e1001489.PubMedPubMedCentralCrossRef Henderson VC, Kimmelman J, Fergusson D, Grimshaw JM, Hackam DG. Threats to validity in the design and conduct of preclinical efficacy studies: a systematic review of guidelines for in vivo animal experiments. PLoS Med. 2013;10(7):e1001489.PubMedPubMedCentralCrossRef
57.
go back to reference Horvath P, Aulner N, Bickle M, Davies AM, Del Nery E, Ebner D, et al. Screening out irrelevant cell-based models of disease. Nat Rev Drug Discov. 2016;15(11):751–69.PubMedCrossRef Horvath P, Aulner N, Bickle M, Davies AM, Del Nery E, Ebner D, et al. Screening out irrelevant cell-based models of disease. Nat Rev Drug Discov. 2016;15(11):751–69.PubMedCrossRef
58.
go back to reference Dolsten M, Søgaard M. Precision medicine: an approach to R&D for delivering superior medicines to patients. Clin Transl Sci. 2012;1(1):7. Dolsten M, Søgaard M. Precision medicine: an approach to R&D for delivering superior medicines to patients. Clin Transl Sci. 2012;1(1):7.
59.
go back to reference Zuberi A, Lutz C. Mouse models for drug discovery. Can new tools and technology improve translational power? ILAR J. 2017;57(2):178–85.CrossRef Zuberi A, Lutz C. Mouse models for drug discovery. Can new tools and technology improve translational power? ILAR J. 2017;57(2):178–85.CrossRef
61.
go back to reference Brannen KC, Chapin RE, Jacobs AC, Green ML. Alternative models of developmental and reproductive toxicity in pharmaceutical risk assessment and the 3Rs. ILAR J. 2017;57(2):144–56.CrossRef Brannen KC, Chapin RE, Jacobs AC, Green ML. Alternative models of developmental and reproductive toxicity in pharmaceutical risk assessment and the 3Rs. ILAR J. 2017;57(2):144–56.CrossRef
62.
go back to reference Chapman KL, Holzgrefe H, Black LE, Brown M, Chellman G, Copeman C, et al. Pharmaceutical toxicology: designing studies to reduce animal use, while maximizing human translation. Regul Toxicol Pharmacol. 2013;66(1):88–103.PubMedCrossRef Chapman KL, Holzgrefe H, Black LE, Brown M, Chellman G, Copeman C, et al. Pharmaceutical toxicology: designing studies to reduce animal use, while maximizing human translation. Regul Toxicol Pharmacol. 2013;66(1):88–103.PubMedCrossRef
63.
go back to reference Edmondson R, Broglie JJ, Adcock AF, Yang L. Three-dimensional cell culture systems and their applications in drug discovery and cell-based biosensors. Assay Drug Dev Technol. 2014;12(4):207–18.PubMedPubMedCentralCrossRef Edmondson R, Broglie JJ, Adcock AF, Yang L. Three-dimensional cell culture systems and their applications in drug discovery and cell-based biosensors. Assay Drug Dev Technol. 2014;12(4):207–18.PubMedPubMedCentralCrossRef
64.
65.
go back to reference Augustyniak J, Bertero A, Coccini T, Baderna D, Buzanska L, Caloni F. Organoids are promising tools for species-specific in vitro toxicological studies. J Appl Toxicol. 2019;39(12):1610–22.PubMedCrossRef Augustyniak J, Bertero A, Coccini T, Baderna D, Buzanska L, Caloni F. Organoids are promising tools for species-specific in vitro toxicological studies. J Appl Toxicol. 2019;39(12):1610–22.PubMedCrossRef
66.
go back to reference Liu F, Huang J, Ning B, Liu Z, Chen S, Zhao W. Drug discovery via human-derived stem cell organoids. Front Pharmacol. 2016;7:334.PubMedPubMedCentral Liu F, Huang J, Ning B, Liu Z, Chen S, Zhao W. Drug discovery via human-derived stem cell organoids. Front Pharmacol. 2016;7:334.PubMedPubMedCentral
67.
68.
go back to reference Dekkers JF, Berkers G, Kruisselbrink E, Vonk A, De Jonge HR, Janssens HM, et al. Characterizing responses to CFTR-modulating drugs using rectal organoids derived from subjects with cystic fibrosis. Sci Transl Med. 2016;8(344):344ra84.PubMedCrossRef Dekkers JF, Berkers G, Kruisselbrink E, Vonk A, De Jonge HR, Janssens HM, et al. Characterizing responses to CFTR-modulating drugs using rectal organoids derived from subjects with cystic fibrosis. Sci Transl Med. 2016;8(344):344ra84.PubMedCrossRef
69.
go back to reference Dekkers JF, van der Ent CK, Beekman JM. Novel opportunities for CFTR-targeting drug development using organoids. Rare Dis. 2013;1(1):939–45. Dekkers JF, van der Ent CK, Beekman JM. Novel opportunities for CFTR-targeting drug development using organoids. Rare Dis. 2013;1(1):939–45.
71.
go back to reference Noordhoek J, Gulmans V, Van Der Ent K, Beekman JM. Intestinal organoids and personalized medicine in cystic fibrosis: a successful patient-oriented research collaboration. Curr Opin Pulm Med. 2016;22(6):610–6.PubMedCrossRef Noordhoek J, Gulmans V, Van Der Ent K, Beekman JM. Intestinal organoids and personalized medicine in cystic fibrosis: a successful patient-oriented research collaboration. Curr Opin Pulm Med. 2016;22(6):610–6.PubMedCrossRef
72.
go back to reference Rabiu KA, Adewunmi AA, Akinlusi FM, Akinola OI. Female reproductive tract infections: understandings and care seeking behaviour among women of reproductive age in Lagos, Nigeria. BMC Womens Health. 2010;10(1):8.PubMedPubMedCentralCrossRef Rabiu KA, Adewunmi AA, Akinlusi FM, Akinola OI. Female reproductive tract infections: understandings and care seeking behaviour among women of reproductive age in Lagos, Nigeria. BMC Womens Health. 2010;10(1):8.PubMedPubMedCentralCrossRef
73.
go back to reference Wasserheit JN, Holmes KK. Reproductive tract infections: challenges for international health policy, programs, and research. In: Germain A, Holmes KK, Piot P, Wasserheit JN, editors. Reproductive tract infections: global impact and priorities for Women’s reproductive health. Boston: Springer US; 1992. p. 7–33.CrossRef Wasserheit JN, Holmes KK. Reproductive tract infections: challenges for international health policy, programs, and research. In: Germain A, Holmes KK, Piot P, Wasserheit JN, editors. Reproductive tract infections: global impact and priorities for Women’s reproductive health. Boston: Springer US; 1992. p. 7–33.CrossRef
74.
go back to reference Hillier SL, Nugent RP, Eschenbach DA, Krohn MA, Gibbs RS, Martin DH, et al. Association between bacterial vaginosis and preterm delivery of a low-birth-weight infant. N Engl J Med. 1995;333(26):1737–42.PubMedCrossRef Hillier SL, Nugent RP, Eschenbach DA, Krohn MA, Gibbs RS, Martin DH, et al. Association between bacterial vaginosis and preterm delivery of a low-birth-weight infant. N Engl J Med. 1995;333(26):1737–42.PubMedCrossRef
75.
go back to reference Taylor BD, Darville T, Haggerty CL. Does bacterial vaginosis cause pelvic inflammatory disease? Sex Transm Infect. 2013;40(2):117–22.CrossRef Taylor BD, Darville T, Haggerty CL. Does bacterial vaginosis cause pelvic inflammatory disease? Sex Transm Infect. 2013;40(2):117–22.CrossRef
76.
go back to reference Prusty RK, Unisa S. Reproductive tract infections and treatment seeking behavior among married adolescent women 15-19 years in India. Int J MCH AIDS. 2013;2(1):103.PubMedPubMedCentralCrossRef Prusty RK, Unisa S. Reproductive tract infections and treatment seeking behavior among married adolescent women 15-19 years in India. Int J MCH AIDS. 2013;2(1):103.PubMedPubMedCentralCrossRef
77.
go back to reference Spurgeon ME, Uberoi A, McGregor SM, Wei T, Ward-Shaw E, Lambert PF. A novel in vivo infection model to study papillomavirus-mediated disease of the female reproductive tract. mBio. 2019;10(2):e00180–19.PubMedPubMedCentralCrossRef Spurgeon ME, Uberoi A, McGregor SM, Wei T, Ward-Shaw E, Lambert PF. A novel in vivo infection model to study papillomavirus-mediated disease of the female reproductive tract. mBio. 2019;10(2):e00180–19.PubMedPubMedCentralCrossRef
78.
go back to reference Merbah M, Introini A, Fitzgerald W, Grivel JC, Lisco A, Vanpouille C, et al. Cervico-vaginal tissue ex vivo as a model to study early events in HIV-1 infection. Am J Reprod Immunol. 2011;65(3):268–78.PubMedPubMedCentralCrossRef Merbah M, Introini A, Fitzgerald W, Grivel JC, Lisco A, Vanpouille C, et al. Cervico-vaginal tissue ex vivo as a model to study early events in HIV-1 infection. Am J Reprod Immunol. 2011;65(3):268–78.PubMedPubMedCentralCrossRef
79.
go back to reference Hvid M, Baczynska A, Deleuran B, Fedder J, Knudsen HJ, Christiansen G, et al. Interleukin-1 is the initiator of fallopian tube destruction during chlamydia trachomatis infection. Cell Microbiol. 2007;9(12):2795–803.PubMedCrossRef Hvid M, Baczynska A, Deleuran B, Fedder J, Knudsen HJ, Christiansen G, et al. Interleukin-1 is the initiator of fallopian tube destruction during chlamydia trachomatis infection. Cell Microbiol. 2007;9(12):2795–803.PubMedCrossRef
80.
go back to reference Xue Y, Zheng H, Mai Z, Qin X, Chen W, Huang T, et al. An in vitro model of azithromycin-induced persistent chlamydia trachomatis infection. FEMS Microbiol Lett. 2017;364(14):fnx145.CrossRef Xue Y, Zheng H, Mai Z, Qin X, Chen W, Huang T, et al. An in vitro model of azithromycin-induced persistent chlamydia trachomatis infection. FEMS Microbiol Lett. 2017;364(14):fnx145.CrossRef
81.
go back to reference Paul T, Knight S, Raulston J, Wyrick P. Delivery of azithromycin to chlamydia trachomatis-infected polarized human endometrial epithelial cells by polymorphonuclear leucocytes. J Antimicrob Chemother. 1997;39(5):623–30.PubMedCrossRef Paul T, Knight S, Raulston J, Wyrick P. Delivery of azithromycin to chlamydia trachomatis-infected polarized human endometrial epithelial cells by polymorphonuclear leucocytes. J Antimicrob Chemother. 1997;39(5):623–30.PubMedCrossRef
82.
go back to reference Davis C, Raulston J, Wyrick P. Protein disulfide isomerase, a component of the estrogen receptor complex, is associated with chlamydia trachomatis serovar E attached to human endometrial epithelial cells. Infect Immun. 2002;70(7):3413–8.PubMedPubMedCentralCrossRef Davis C, Raulston J, Wyrick P. Protein disulfide isomerase, a component of the estrogen receptor complex, is associated with chlamydia trachomatis serovar E attached to human endometrial epithelial cells. Infect Immun. 2002;70(7):3413–8.PubMedPubMedCentralCrossRef
83.
go back to reference Guseva NV, Dessus-Babus SC, Whittimore JD, Moore CG, Wyrick PB. Characterization of estrogen-responsive epithelial cell lines and their infectivity by genital chlamydia trachomatis. Microbes Infect. 2005;7(15):1469–81.PubMedCrossRef Guseva NV, Dessus-Babus SC, Whittimore JD, Moore CG, Wyrick PB. Characterization of estrogen-responsive epithelial cell lines and their infectivity by genital chlamydia trachomatis. Microbes Infect. 2005;7(15):1469–81.PubMedCrossRef
84.
go back to reference Mukura LR, Hickey DK, Rodriguez-Garcia M, Fahey JV, Wira CR. Chlamydia trachomatis regulates innate immune barrier integrity and mediates cytokine and antimicrobial responses in human uterine ECC-1 epithelial cells. Am J Reprod Immunol. 2017;78(6):e12764.CrossRef Mukura LR, Hickey DK, Rodriguez-Garcia M, Fahey JV, Wira CR. Chlamydia trachomatis regulates innate immune barrier integrity and mediates cytokine and antimicrobial responses in human uterine ECC-1 epithelial cells. Am J Reprod Immunol. 2017;78(6):e12764.CrossRef
85.
go back to reference King AE, Wheelhouse N, Cameron S, McDonald SE, Lee KF, Entrican G, et al. Expression of secretory leukocyte protease inhibitor and elafin in human fallopian tube and in an in-vitro model of chlamydia trachomatis infection. Hum Reprod. 2009;24(3):679–86.PubMedCrossRef King AE, Wheelhouse N, Cameron S, McDonald SE, Lee KF, Entrican G, et al. Expression of secretory leukocyte protease inhibitor and elafin in human fallopian tube and in an in-vitro model of chlamydia trachomatis infection. Hum Reprod. 2009;24(3):679–86.PubMedCrossRef
86.
go back to reference Shaw JLV, Wills GS, Lee K-F, Horner PJ, McClure MO, Abrahams VM, et al. Chlamydia trachomatis infection increases fallopian tube PROKR2 via TLR2 and NFκB activation resulting in a microenvironment predisposed to ectopic pregnancy. Am J Pathol. 2011;178(1):253–60.PubMedPubMedCentralCrossRef Shaw JLV, Wills GS, Lee K-F, Horner PJ, McClure MO, Abrahams VM, et al. Chlamydia trachomatis infection increases fallopian tube PROKR2 via TLR2 and NFκB activation resulting in a microenvironment predisposed to ectopic pregnancy. Am J Pathol. 2011;178(1):253–60.PubMedPubMedCentralCrossRef
87.
go back to reference Guseva NV, Dessus-Babus S, Moore CG, Whittimore JD, Wyrick PB. Differences in chlamydia trachomatis serovar E growth rate in polarized endometrial and endocervical epithelial cells grown in three-dimensional culture. Infect Immun. 2007;75(2):553–64.PubMedCrossRef Guseva NV, Dessus-Babus S, Moore CG, Whittimore JD, Wyrick PB. Differences in chlamydia trachomatis serovar E growth rate in polarized endometrial and endocervical epithelial cells grown in three-dimensional culture. Infect Immun. 2007;75(2):553–64.PubMedCrossRef
88.
go back to reference Kokab A, Jennings R, Eley A, Pacey AA, Cross NA. Analysis of modulated gene expression in a model of interferon-γ-induced persistence of chlamydia trachomatis in HEp-2 cells. Microb Pathog. 2010;49(5):217–25.PubMedCrossRef Kokab A, Jennings R, Eley A, Pacey AA, Cross NA. Analysis of modulated gene expression in a model of interferon-γ-induced persistence of chlamydia trachomatis in HEp-2 cells. Microb Pathog. 2010;49(5):217–25.PubMedCrossRef
89.
go back to reference Huston WM, Gloeckl S, de Boer L, Beagley KW, Timms P. Apoptosis is induced in chlamydia trachomatis-infected HEp-2 cells by the addition of a combination innate immune activation compounds and the inhibitor Wedelolactone. Am J Reprod Immunol. 2011;65(5):460–5.PubMedCrossRef Huston WM, Gloeckl S, de Boer L, Beagley KW, Timms P. Apoptosis is induced in chlamydia trachomatis-infected HEp-2 cells by the addition of a combination innate immune activation compounds and the inhibitor Wedelolactone. Am J Reprod Immunol. 2011;65(5):460–5.PubMedCrossRef
90.
go back to reference Nickerson CA, Richter EG, Ott CM. Studying host–pathogen interactions in 3-D: Organotypic models for infectious disease and drug development. J Neuroimmune Pharmacol. 2007;2(1):26–31.PubMedCrossRef Nickerson CA, Richter EG, Ott CM. Studying host–pathogen interactions in 3-D: Organotypic models for infectious disease and drug development. J Neuroimmune Pharmacol. 2007;2(1):26–31.PubMedCrossRef
91.
go back to reference Hjelm BE, Berta AN, Nickerson CA, Arntzen CJ, Herbst-Kralovetz MM. Development and characterization of a three-dimensional Organotypic human vaginal epithelial cell Model1. Biol Reprod. 2010;82(3):617–27.PubMedPubMedCentralCrossRef Hjelm BE, Berta AN, Nickerson CA, Arntzen CJ, Herbst-Kralovetz MM. Development and characterization of a three-dimensional Organotypic human vaginal epithelial cell Model1. Biol Reprod. 2010;82(3):617–27.PubMedPubMedCentralCrossRef
92.
go back to reference LaMarca HL, Ott CM. Höner zu Bentrup K, LeBlanc CL, Pierson DL, Nelson AB, et al. three-dimensional growth of extravillous cytotrophoblasts promotes differentiation and invasion. Placenta. 2005;26(10):709–20.PubMedCrossRef LaMarca HL, Ott CM. Höner zu Bentrup K, LeBlanc CL, Pierson DL, Nelson AB, et al. three-dimensional growth of extravillous cytotrophoblasts promotes differentiation and invasion. Placenta. 2005;26(10):709–20.PubMedCrossRef
93.
go back to reference Long JP, Pierson S, Hughes JH. Rhinovirus replication in HeLa cells cultured under conditions of simulated microgravity. Aviat Space Environ Med. 1998;69(9):851–6.PubMed Long JP, Pierson S, Hughes JH. Rhinovirus replication in HeLa cells cultured under conditions of simulated microgravity. Aviat Space Environ Med. 1998;69(9):851–6.PubMed
94.
go back to reference Nickerson CA, Goodwin TJ, Terlonge J, Ott CM, Buchanan KL, Uicker WC, et al. Three-dimensional tissue assemblies: novel models for the study of salmonella enterica serovar typhimurium pathogenesis. Infect Immun. 2001;69(11):7106–20.PubMedPubMedCentralCrossRef Nickerson CA, Goodwin TJ, Terlonge J, Ott CM, Buchanan KL, Uicker WC, et al. Three-dimensional tissue assemblies: novel models for the study of salmonella enterica serovar typhimurium pathogenesis. Infect Immun. 2001;69(11):7106–20.PubMedPubMedCentralCrossRef
95.
go back to reference McCracken KW, Catá EM, Crawford CM, Sinagoga KL, Schumacher M, Rockich BE, et al. Modelling human development and disease in pluripotent stem-cell-derived gastric organoids. Nature. 2014;516(7531):400.PubMedPubMedCentralCrossRef McCracken KW, Catá EM, Crawford CM, Sinagoga KL, Schumacher M, Rockich BE, et al. Modelling human development and disease in pluripotent stem-cell-derived gastric organoids. Nature. 2014;516(7531):400.PubMedPubMedCentralCrossRef
96.
go back to reference Bartfeld S, Clevers H. Organoids as model for infectious diseases: culture of human and murine stomach organoids and microinjection of helicobacter pylori. J Vis Exp. 2015;105:e53359. Bartfeld S, Clevers H. Organoids as model for infectious diseases: culture of human and murine stomach organoids and microinjection of helicobacter pylori. J Vis Exp. 2015;105:e53359.
97.
go back to reference Forbester JL, Goulding D, Vallier L, Hannan N, Hale C, Pickard D, et al. The interaction of Salmonella enterica Serovar typhimurium with intestinal organoids derived from human induced pluripotent stem cells. Infect Immun. 2015;83(7):2926–34. Forbester JL, Goulding D, Vallier L, Hannan N, Hale C, Pickard D, et al. The interaction of Salmonella enterica Serovar typhimurium with intestinal organoids derived from human induced pluripotent stem cells. Infect Immun. 2015;83(7):2926–34.
98.
go back to reference Leslie JL, Huang S, Opp JS, Nagy MS, Kobayashi M, Young VB, et al. Persistence and toxin production by Clostridium difficile within human intestinal organoids result in disruption of epithelial paracellular barrier function. Infect Immun. 2015;83(1):138–45.PubMedCrossRef Leslie JL, Huang S, Opp JS, Nagy MS, Kobayashi M, Young VB, et al. Persistence and toxin production by Clostridium difficile within human intestinal organoids result in disruption of epithelial paracellular barrier function. Infect Immun. 2015;83(1):138–45.PubMedCrossRef
99.
go back to reference Garcez PP, Loiola EC, da Costa RM, Higa LM, Trindade P, Delvecchio R, et al. Zika virus impairs growth in human neurospheres and brain organoids. Science. 2016;352(6287):816–8.PubMedCrossRef Garcez PP, Loiola EC, da Costa RM, Higa LM, Trindade P, Delvecchio R, et al. Zika virus impairs growth in human neurospheres and brain organoids. Science. 2016;352(6287):816–8.PubMedCrossRef
100.
go back to reference Kessler M, Hoffmann K, Fritsche K, Brinkmann V, Mollenkopf H-J, Thieck O, et al. Chronic chlamydia infection in human organoids increases stemness and promotes age-dependent CpG methylation. Nat Commun. 2019;10(1):1194.PubMedPubMedCentralCrossRef Kessler M, Hoffmann K, Fritsche K, Brinkmann V, Mollenkopf H-J, Thieck O, et al. Chronic chlamydia infection in human organoids increases stemness and promotes age-dependent CpG methylation. Nat Commun. 2019;10(1):1194.PubMedPubMedCentralCrossRef
101.
go back to reference Botesteanu D-A, Lee J-M, Levy D. Modeling the dynamics of high-grade serous ovarian cancer progression for transvaginal ultrasound-based screening and early detection. PLoS One. 2016;11(6):e0156661.PubMedPubMedCentralCrossRef Botesteanu D-A, Lee J-M, Levy D. Modeling the dynamics of high-grade serous ovarian cancer progression for transvaginal ultrasound-based screening and early detection. PLoS One. 2016;11(6):e0156661.PubMedPubMedCentralCrossRef
102.
go back to reference Zhang W, Wei L, Li L, Yang B, Kong B, Yao G, et al. Ovarian serous carcinogenesis from tubal secretory cells. Histol Histopathol. 2015;30(11):1295–302.PubMed Zhang W, Wei L, Li L, Yang B, Kong B, Yao G, et al. Ovarian serous carcinogenesis from tubal secretory cells. Histol Histopathol. 2015;30(11):1295–302.PubMed
103.
105.
go back to reference Chen EY, Mehra K, Mehrad M, Ning G, Miron A, Mutter GL, et al. Secretory cell outgrowth, PAX2 and serous carcinogenesis in the fallopian tube. J Pathol. 2010;222(1):110–6.PubMedPubMedCentral Chen EY, Mehra K, Mehrad M, Ning G, Miron A, Mutter GL, et al. Secretory cell outgrowth, PAX2 and serous carcinogenesis in the fallopian tube. J Pathol. 2010;222(1):110–6.PubMedPubMedCentral
106.
107.
go back to reference Arnold M, Pandeya N, Byrnes G, Renehan AG, Stevens GA, Ezzati M, et al. Global burden of cancer attributable to high body-mass index in 2012: a population-based study. Lancet Oncol. 2015;16(1):36–46.PubMedCrossRef Arnold M, Pandeya N, Byrnes G, Renehan AG, Stevens GA, Ezzati M, et al. Global burden of cancer attributable to high body-mass index in 2012: a population-based study. Lancet Oncol. 2015;16(1):36–46.PubMedCrossRef
108.
go back to reference Marshall AD, Bailey CG, Champ K, Vellozzi M, O'Young P, Metierre C, et al. CTCF genetic alterations in endometrial carcinoma are pro-tumorigenic. Oncogene. 2017;36:4100.PubMedPubMedCentralCrossRef Marshall AD, Bailey CG, Champ K, Vellozzi M, O'Young P, Metierre C, et al. CTCF genetic alterations in endometrial carcinoma are pro-tumorigenic. Oncogene. 2017;36:4100.PubMedPubMedCentralCrossRef
109.
go back to reference Kokka F, Brockbank E, Oram D, Gallagher C, Bryant A. Hormonal therapy in advanced or recurrent endometrial cancer. Cochrane Database Syst Rev. 2010;(12):Cd007926. Kokka F, Brockbank E, Oram D, Gallagher C, Bryant A. Hormonal therapy in advanced or recurrent endometrial cancer. Cochrane Database Syst Rev. 2010;(12):Cd007926.
110.
go back to reference Martin-Hirsch PP, Bryant A, Keep SL, Kitchener HC, Lilford R. Adjuvant progestagens for endometrial cancer. Cochrane Database Syst Rev. 2011;6:CD001040. Martin-Hirsch PP, Bryant A, Keep SL, Kitchener HC, Lilford R. Adjuvant progestagens for endometrial cancer. Cochrane Database Syst Rev. 2011;6:CD001040.
111.
go back to reference Zhang J, Späth SS, Marjani SL, Zhang W, Pan X. Characterization of cancer genomic heterogeneity by next-generation sequencing advances precision medicine in cancer treatment. Precis Clin Med. 2018;1(1):29–48.PubMedPubMedCentralCrossRef Zhang J, Späth SS, Marjani SL, Zhang W, Pan X. Characterization of cancer genomic heterogeneity by next-generation sequencing advances precision medicine in cancer treatment. Precis Clin Med. 2018;1(1):29–48.PubMedPubMedCentralCrossRef
112.
go back to reference Sato T, Stange DE, Ferrante M, Vries RG, Van Es JH, Van Den Brink S, et al. Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett's epithelium. Gastroenterology. 2011;141(5):1762–72.PubMedCrossRef Sato T, Stange DE, Ferrante M, Vries RG, Van Es JH, Van Den Brink S, et al. Long-term expansion of epithelial organoids from human colon, adenoma, adenocarcinoma, and Barrett's epithelium. Gastroenterology. 2011;141(5):1762–72.PubMedCrossRef
113.
go back to reference Boj SF, Hwang C-I, Baker LA, Chio IIC, Engle DD, Corbo V, et al. Organoid models of human and mouse ductal pancreatic cancer. Cell. 2015;160(1):324–38.PubMedCrossRef Boj SF, Hwang C-I, Baker LA, Chio IIC, Engle DD, Corbo V, et al. Organoid models of human and mouse ductal pancreatic cancer. Cell. 2015;160(1):324–38.PubMedCrossRef
114.
go back to reference Gao B, Peyton M, Huang C, Park H, Girard L, Sorrelle N, et al. 3D spheroid/organoid models of lung cancer to study lung cancer pathogenesis and testing of new therapeutics. J Thorac Oncol. 2017;12(8):S1544.CrossRef Gao B, Peyton M, Huang C, Park H, Girard L, Sorrelle N, et al. 3D spheroid/organoid models of lung cancer to study lung cancer pathogenesis and testing of new therapeutics. J Thorac Oncol. 2017;12(8):S1544.CrossRef
115.
go back to reference Gao D, Vela I, Sboner A, Iaquinta PJ, Karthaus WR, Gopalan A, et al. Organoid cultures derived from patients with advanced prostate cancer. Cell. 2014;159(1):176–87.PubMedPubMedCentralCrossRef Gao D, Vela I, Sboner A, Iaquinta PJ, Karthaus WR, Gopalan A, et al. Organoid cultures derived from patients with advanced prostate cancer. Cell. 2014;159(1):176–87.PubMedPubMedCentralCrossRef
116.
go back to reference Pauli C, Hopkins BD, Prandi D, Shaw R, Fedrizzi T, Sboner A, et al. Personalized in vitro and in vivo cancer models to guide precision medicine. Cancer Discov. 2017;7(5):462–77.PubMedPubMedCentralCrossRef Pauli C, Hopkins BD, Prandi D, Shaw R, Fedrizzi T, Sboner A, et al. Personalized in vitro and in vivo cancer models to guide precision medicine. Cancer Discov. 2017;7(5):462–77.PubMedPubMedCentralCrossRef
117.
go back to reference Dasari VR, Mazack V, Feng W, Nash J, Carey DJ, Gogoi R. Verteporfin exhibits YAP-independent anti-proliferative and cytotoxic effects in endometrial cancer cells. Oncotarget. 2017;8(17):28628.PubMedPubMedCentralCrossRef Dasari VR, Mazack V, Feng W, Nash J, Carey DJ, Gogoi R. Verteporfin exhibits YAP-independent anti-proliferative and cytotoxic effects in endometrial cancer cells. Oncotarget. 2017;8(17):28628.PubMedPubMedCentralCrossRef
118.
go back to reference Kunitomi H, Banno K, Yanokura M, Takeda T, Iijima M, Nakamura K, et al. New use of microsatellite instability analysis in endometrial cancer. Oncol Lett. 2017;14(3):3297–301.PubMedPubMedCentralCrossRef Kunitomi H, Banno K, Yanokura M, Takeda T, Iijima M, Nakamura K, et al. New use of microsatellite instability analysis in endometrial cancer. Oncol Lett. 2017;14(3):3297–301.PubMedPubMedCentralCrossRef
119.
go back to reference Anglesio MS, Papadopoulos N, Ayhan A, Nazeran TM, Noë M, Horlings HM, et al. Cancer-associated mutations in endometriosis without cancer. N Engl J Med. 2017;376(19):1835–48.PubMedPubMedCentralCrossRef Anglesio MS, Papadopoulos N, Ayhan A, Nazeran TM, Noë M, Horlings HM, et al. Cancer-associated mutations in endometriosis without cancer. N Engl J Med. 2017;376(19):1835–48.PubMedPubMedCentralCrossRef
120.
121.
go back to reference Cervelló I, Gil-Sanchis C, Santamaría X, Cabanillas S, Díaz A, Faus A, et al. Human CD133+ bone marrow-derived stem cells promote endometrial proliferation in a murine model of Asherman syndrome. Fertil Steril. 2015;104(6):1552–60 e3.PubMedCrossRef Cervelló I, Gil-Sanchis C, Santamaría X, Cabanillas S, Díaz A, Faus A, et al. Human CD133+ bone marrow-derived stem cells promote endometrial proliferation in a murine model of Asherman syndrome. Fertil Steril. 2015;104(6):1552–60 e3.PubMedCrossRef
122.
123.
go back to reference Kuramoto G, Takagi S, Ishitani K, Shimizu T, Okano T, Matsui H. Preventive effect of oral mucosal epithelial cell sheets on intrauterine adhesions. Hum Reprod. 2014;30(2):406–16.PubMedCrossRef Kuramoto G, Takagi S, Ishitani K, Shimizu T, Okano T, Matsui H. Preventive effect of oral mucosal epithelial cell sheets on intrauterine adhesions. Hum Reprod. 2014;30(2):406–16.PubMedCrossRef
124.
go back to reference Singh N, Mohanty S, Seth T, Shankar M, Bhaskaran S, Dharmendra S. Autologous stem cell transplantation in refractory Asherman's syndrome: a novel cell based therapy. J Hum Reprod Sci. 2014;7(2):93.PubMedPubMedCentralCrossRef Singh N, Mohanty S, Seth T, Shankar M, Bhaskaran S, Dharmendra S. Autologous stem cell transplantation in refractory Asherman's syndrome: a novel cell based therapy. J Hum Reprod Sci. 2014;7(2):93.PubMedPubMedCentralCrossRef
125.
go back to reference Alawadhi F, Du H, Cakmak H, Taylor HS. Bone marrow-derived stem cell (BMDSC) transplantation improves fertility in a murine model of Asherman's syndrome. PLoS One. 2014;9(5):e96662.PubMedPubMedCentralCrossRef Alawadhi F, Du H, Cakmak H, Taylor HS. Bone marrow-derived stem cell (BMDSC) transplantation improves fertility in a murine model of Asherman's syndrome. PLoS One. 2014;9(5):e96662.PubMedPubMedCentralCrossRef
127.
go back to reference Azizi R, Aghebati-Maleki L, Nouri M, Marofi F, Negargar S, Yousefi M. Stem cell therapy in Asherman syndrome and thin endometrium: stem cell-based therapy. Biomed Pharmacother. 2018;102:333–43.PubMedCrossRef Azizi R, Aghebati-Maleki L, Nouri M, Marofi F, Negargar S, Yousefi M. Stem cell therapy in Asherman syndrome and thin endometrium: stem cell-based therapy. Biomed Pharmacother. 2018;102:333–43.PubMedCrossRef
128.
go back to reference Domnina A, Novikova P, Obidina J, Fridlyanskaya I, Alekseenko L, Kozhukharova I, et al. Human mesenchymal stem cells in spheroids improve fertility in model animals with damaged endometrium. Stem Cell Res Ther. 2018;9(1):50.PubMedPubMedCentralCrossRef Domnina A, Novikova P, Obidina J, Fridlyanskaya I, Alekseenko L, Kozhukharova I, et al. Human mesenchymal stem cells in spheroids improve fertility in model animals with damaged endometrium. Stem Cell Res Ther. 2018;9(1):50.PubMedPubMedCentralCrossRef
129.
go back to reference Sudoma I, Pylyp L, Kremenska Y, Goncharova Y. Application of autologous adipose-derived stem cells for thin endometrium treatment in patients with failed ART programs. J Stem Cell Ther Transplant. 2019;3:001–8.CrossRef Sudoma I, Pylyp L, Kremenska Y, Goncharova Y. Application of autologous adipose-derived stem cells for thin endometrium treatment in patients with failed ART programs. J Stem Cell Ther Transplant. 2019;3:001–8.CrossRef
130.
131.
132.
go back to reference Yui S, Nakamura T, Sato T, Nemoto Y, Mizutani T, Zheng X, et al. Functional engraftment of colon epithelium expanded in vitro from a single adult Lgr5+ stem cell. Nat Med. 2012;18(4):618–23.PubMedCrossRef Yui S, Nakamura T, Sato T, Nemoto Y, Mizutani T, Zheng X, et al. Functional engraftment of colon epithelium expanded in vitro from a single adult Lgr5+ stem cell. Nat Med. 2012;18(4):618–23.PubMedCrossRef
133.
go back to reference Wei N, Quan Z, Tang H, Zhu J. Three-dimensional organoid system transplantation Technologies in Future Treatment of central nervous system diseases. Stem Cells Int. 2017;2017:5682354.PubMedPubMedCentralCrossRef Wei N, Quan Z, Tang H, Zhu J. Three-dimensional organoid system transplantation Technologies in Future Treatment of central nervous system diseases. Stem Cells Int. 2017;2017:5682354.PubMedPubMedCentralCrossRef
134.
go back to reference Soldin OP, Chung SH, Mattison DR. Sex differences in drug disposition. Biomed Res Int. 2011;2011:187103. Soldin OP, Chung SH, Mattison DR. Sex differences in drug disposition. Biomed Res Int. 2011;2011:187103.
135.
go back to reference Gandhi M, Aweeka F, Greenblatt RM, Blaschke TF. Sex differences in pharmacokinetics and pharmacodynamics. Annu Rev Pharmacol Toxicol. 2004;44:499–523.PubMedCrossRef Gandhi M, Aweeka F, Greenblatt RM, Blaschke TF. Sex differences in pharmacokinetics and pharmacodynamics. Annu Rev Pharmacol Toxicol. 2004;44:499–523.PubMedCrossRef
136.
go back to reference Eddie SL, Kim JJ, Woodruff TK, Burdette JE. Microphysiological modeling of the reproductive tract: a fertile endeavor. Exp Biol Med. 2014;239(9):1192–202.CrossRef Eddie SL, Kim JJ, Woodruff TK, Burdette JE. Microphysiological modeling of the reproductive tract: a fertile endeavor. Exp Biol Med. 2014;239(9):1192–202.CrossRef
138.
go back to reference Zanger UM, Schwab M. Cytochrome P450 enzymes in drug metabolism: regulation of gene expression, enzyme activities, and impact of genetic variation. Pharmacol Ther. 2013;138(1):103–41.PubMedCrossRef Zanger UM, Schwab M. Cytochrome P450 enzymes in drug metabolism: regulation of gene expression, enzyme activities, and impact of genetic variation. Pharmacol Ther. 2013;138(1):103–41.PubMedCrossRef
139.
go back to reference MacGregor D, Leng G. Modelling the hypothalamic control of growth hormone secretion. J Neuroendocrinol. 2005;17(12):788–803.PubMedCrossRef MacGregor D, Leng G. Modelling the hypothalamic control of growth hormone secretion. J Neuroendocrinol. 2005;17(12):788–803.PubMedCrossRef
140.
go back to reference Chowen JA, Frago LM, Argente J. The regulation of GH secretion by sex steroids. Eur J Endocrinol. 2004;151(Suppl 3):U95–100.PubMedCrossRef Chowen JA, Frago LM, Argente J. The regulation of GH secretion by sex steroids. Eur J Endocrinol. 2004;151(Suppl 3):U95–100.PubMedCrossRef
141.
go back to reference Valle A, Silvestri E, Moreno M, Chambery A, Oliver J, Roca P, et al. Combined effect of gender and caloric restriction on liver proteomic expression profile. J Proteome Res. 2008;7(7):2872–81.PubMedCrossRef Valle A, Silvestri E, Moreno M, Chambery A, Oliver J, Roca P, et al. Combined effect of gender and caloric restriction on liver proteomic expression profile. J Proteome Res. 2008;7(7):2872–81.PubMedCrossRef
142.
go back to reference Kimura H, Sakai Y, Fujii T. Organ/body-on-a-chip based on microfluidic technology for drug discovery. Drug Metab Pharmacokinet. 2018;33(1):43–8.PubMedCrossRef Kimura H, Sakai Y, Fujii T. Organ/body-on-a-chip based on microfluidic technology for drug discovery. Drug Metab Pharmacokinet. 2018;33(1):43–8.PubMedCrossRef
143.
go back to reference Nawroth J, Rogal J, Weiss M, Brucker SY, Loskill P. Organ-on-a-Chip Systems for Women's health applications. Adv Healthc Mater. 2018;7(2):1700550.CrossRef Nawroth J, Rogal J, Weiss M, Brucker SY, Loskill P. Organ-on-a-Chip Systems for Women's health applications. Adv Healthc Mater. 2018;7(2):1700550.CrossRef
144.
go back to reference Mouw JK, Ou G, Weaver VM. Extracellular matrix assembly: a multiscale deconstruction. Nat Rev Mol. 2014;15(12):771.CrossRef Mouw JK, Ou G, Weaver VM. Extracellular matrix assembly: a multiscale deconstruction. Nat Rev Mol. 2014;15(12):771.CrossRef
145.
go back to reference Gjorevski N, Sachs N, Manfrin A, Giger S, Bragina ME, Ordóñez-Morán P, et al. Designer matrices for intestinal stem cell and organoid culture. Nature. 2016;539(7630):560.PubMedCrossRef Gjorevski N, Sachs N, Manfrin A, Giger S, Bragina ME, Ordóñez-Morán P, et al. Designer matrices for intestinal stem cell and organoid culture. Nature. 2016;539(7630):560.PubMedCrossRef
146.
go back to reference Workman MJ, Mahe MM, Trisno S, Poling HM, Watson CL, Sundaram N, et al. Engineered human pluripotent-stem-cell-derived intestinal tissues with a functional enteric nervous system. Nat Med. 2017;23(1):49.PubMedCrossRef Workman MJ, Mahe MM, Trisno S, Poling HM, Watson CL, Sundaram N, et al. Engineered human pluripotent-stem-cell-derived intestinal tissues with a functional enteric nervous system. Nat Med. 2017;23(1):49.PubMedCrossRef
147.
go back to reference Tsai S, McOlash L, Palen K, Johnson B, Duris C, Yang Q, et al. Development of primary human pancreatic cancer organoids, matched stromal and immune cells and 3D tumor microenvironment models. BMC Cancer. 2018;18(1):335.PubMedPubMedCentralCrossRef Tsai S, McOlash L, Palen K, Johnson B, Duris C, Yang Q, et al. Development of primary human pancreatic cancer organoids, matched stromal and immune cells and 3D tumor microenvironment models. BMC Cancer. 2018;18(1):335.PubMedPubMedCentralCrossRef
148.
go back to reference Richards Z, McCray T, Marsili J, Zenner ML, Manlucu JT, Garcia J, et al. Prostate stroma increases the viability and maintains the branching phenotype of human prostate organoids. iScience. 2019;12:304–17.PubMedPubMedCentralCrossRef Richards Z, McCray T, Marsili J, Zenner ML, Manlucu JT, Garcia J, et al. Prostate stroma increases the viability and maintains the branching phenotype of human prostate organoids. iScience. 2019;12:304–17.PubMedPubMedCentralCrossRef
149.
go back to reference Singh V, Gohil N, Ramirez Garcia R, Braddick D, Fofié CK. Recent advances in CRISPR-Cas9 genome editing technology for biological and biomedical investigations. J Cell Biochem. 2018;119(1):81–94.PubMedCrossRef Singh V, Gohil N, Ramirez Garcia R, Braddick D, Fofié CK. Recent advances in CRISPR-Cas9 genome editing technology for biological and biomedical investigations. J Cell Biochem. 2018;119(1):81–94.PubMedCrossRef
151.
go back to reference Chatterjee K, Pratiwi FW, Wu FCM, Chen P, Chen B-C. Recent progress in light sheet microscopy for biological applications. Appl Spectrosc. 2018;72(8):1137–69.PubMedCrossRef Chatterjee K, Pratiwi FW, Wu FCM, Chen P, Chen B-C. Recent progress in light sheet microscopy for biological applications. Appl Spectrosc. 2018;72(8):1137–69.PubMedCrossRef
Metadata
Title
Organoid technology in female reproductive biomedicine
Authors
Heidar Heidari-Khoei
Fereshteh Esfandiari
Mohammad Amin Hajari
Zeynab Ghorbaninejad
Abbas Piryaei
Hossein Baharvand
Publication date
01-12-2020
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2020
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/s12958-020-00621-z

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