Skip to main content
Erschienen in: Journal of Assisted Reproduction and Genetics 10/2017

24.06.2017 | Commentary

Using stem cell oxygen physiology to optimize blastocyst culture while minimizing hypoxic stress

verfasst von: Alan Bolnick, Awoniyi O Awonuga, Yu Yang, Mohammed Abdulhasan, Yufen Xie, Sichang Zhou, Elizabeth E. Puscheck, Daniel A. Rappolee

Erschienen in: Journal of Assisted Reproduction and Genetics | Ausgabe 10/2017

Einloggen, um Zugang zu erhalten

Abstract

This review is a response to the Fellows Forum on testing 2% oxygen for best culture of human blastocysts (J Ass Reprod Gen 34:303–8, 1; J Ass Reprod Gen 34:309–14, 2) prior to embryo transfer. It is a general analysis in support of the position that an understanding of stem cell physiology and responses to oxygen are necessary for optimization of blastocyst culture in IVF and to enhance reproductive success in fertile women.
Literatur
1.
Zurück zum Zitat Kaser DJ. On developing a thesis for reproductive endocrinology and infertility fellowship: a case study of ultra-low (2%) oxygen tension for extended culture of human embryos. J Assist Reprod Genet. 2017;34:303–8.CrossRefPubMed Kaser DJ. On developing a thesis for reproductive endocrinology and infertility fellowship: a case study of ultra-low (2%) oxygen tension for extended culture of human embryos. J Assist Reprod Genet. 2017;34:303–8.CrossRefPubMed
2.
Zurück zum Zitat Morin SJ. Oxygen tension in embryo culture: does a shift to 2% O2 in extended culture represent the most physiologic system? J Assist Reprod Genet. 2017;34:309–14.CrossRefPubMed Morin SJ. Oxygen tension in embryo culture: does a shift to 2% O2 in extended culture represent the most physiologic system? J Assist Reprod Genet. 2017;34:309–14.CrossRefPubMed
3.
Zurück zum Zitat Bontekoe S, Mantikou E, van Wely M, Seshadri S, Repping S, Mastenbroek S. Low oxygen concentrations for embryo culture in assisted reproductive technologies. Cochrane Database Syst Rev. 2012;7:CD008950. Bontekoe S, Mantikou E, van Wely M, Seshadri S, Repping S, Mastenbroek S. Low oxygen concentrations for embryo culture in assisted reproductive technologies. Cochrane Database Syst Rev. 2012;7:CD008950.
4.
Zurück zum Zitat Gomes Sobrinho DB, Oliveira JBA, Petersen CG, Mauri AL, Silva LFI, Massaro FC, et al. IVF/ICSI outcomes after culture of human embryos at low oxygen tension: a meta-analysis. Reprod Biol Endocrinol. 2011;9:143.CrossRefPubMedPubMedCentral Gomes Sobrinho DB, Oliveira JBA, Petersen CG, Mauri AL, Silva LFI, Massaro FC, et al. IVF/ICSI outcomes after culture of human embryos at low oxygen tension: a meta-analysis. Reprod Biol Endocrinol. 2011;9:143.CrossRefPubMedPubMedCentral
5.
Zurück zum Zitat Mohyeldin A, Garzon-Muvdi T, Quinones-Hinojosa A. Oxygen in stem cell biology: a critical component of the stem cell niche. Cell Stem Cell. 2010;7:150–61.CrossRefPubMed Mohyeldin A, Garzon-Muvdi T, Quinones-Hinojosa A. Oxygen in stem cell biology: a critical component of the stem cell niche. Cell Stem Cell. 2010;7:150–61.CrossRefPubMed
7.
Zurück zum Zitat Rodesch F, Simon P, Donner C, Jauniaux E. Oxygen measurements in endometrial and trophoblastic tissues during early pregnancy. Obstet Gynecol. 1992;80:283–5.PubMed Rodesch F, Simon P, Donner C, Jauniaux E. Oxygen measurements in endometrial and trophoblastic tissues during early pregnancy. Obstet Gynecol. 1992;80:283–5.PubMed
8.
Zurück zum Zitat Bavister BD. Culture of preimplantation embryos: facts and artifacts. Hum Reprod Update. 1995;1:91–148.CrossRefPubMed Bavister BD. Culture of preimplantation embryos: facts and artifacts. Hum Reprod Update. 1995;1:91–148.CrossRefPubMed
9.
Zurück zum Zitat Fischer B, Bavister BD. Oxygen tension in the oviduct and uterus of rhesus monkeys, hamsters and rabbits. J Reprod Fertil. 1993;99 Fischer B, Bavister BD. Oxygen tension in the oviduct and uterus of rhesus monkeys, hamsters and rabbits. J Reprod Fertil. 1993;99
10.
Zurück zum Zitat Yedwab GA, Paz G, Homonnai TZ, David MP, Kraicer PF. The temperature, pH, and partial pressure of oxygen in the cervix and uterus of women and uterus of rats during the cycle. Fertil Steril. 1976;27:304–9.CrossRefPubMed Yedwab GA, Paz G, Homonnai TZ, David MP, Kraicer PF. The temperature, pH, and partial pressure of oxygen in the cervix and uterus of women and uterus of rats during the cycle. Fertil Steril. 1976;27:304–9.CrossRefPubMed
11.
Zurück zum Zitat Puscheck EE, Awonuga AO, Yang Y, Jiang Z, Rappolee DA. Molecular biology of the stress response in the early embryo and its stem cells. Adv Exp Med Biol. 2015;843:77–128.CrossRefPubMed Puscheck EE, Awonuga AO, Yang Y, Jiang Z, Rappolee DA. Molecular biology of the stress response in the early embryo and its stem cells. Adv Exp Med Biol. 2015;843:77–128.CrossRefPubMed
12.
Zurück zum Zitat McLaren A, Snow ML. Embryogenesis in mammals. Amsterdam. New York: Elsevier; 1976. McLaren A, Snow ML. Embryogenesis in mammals. Amsterdam. New York: Elsevier; 1976.
13.
Zurück zum Zitat Guo G, von Meyenn F, Santos F, Chen Y, Reik W, Bertone P, et al. Naive pluripotent stem cells derived directly from isolated cells of the human inner cell mass. Stem Cell Reports. 2016;6:437–46.CrossRefPubMedPubMedCentral Guo G, von Meyenn F, Santos F, Chen Y, Reik W, Bertone P, et al. Naive pluripotent stem cells derived directly from isolated cells of the human inner cell mass. Stem Cell Reports. 2016;6:437–46.CrossRefPubMedPubMedCentral
14.
Zurück zum Zitat Tang F, Barbacioru C, Bao S, Lee C, Nordman E, Wang X, et al. Tracing the derivation of embryonic stem cells from the inner cell mass by single-cell RNA-Seq analysis. Cell Stem Cell. 2010;6:468–78.CrossRefPubMedPubMedCentral Tang F, Barbacioru C, Bao S, Lee C, Nordman E, Wang X, et al. Tracing the derivation of embryonic stem cells from the inner cell mass by single-cell RNA-Seq analysis. Cell Stem Cell. 2010;6:468–78.CrossRefPubMedPubMedCentral
15.
Zurück zum Zitat Tanaka S, Kunath T, Hadjantonakis AK, Nagy A, Rossant J. Promotion of trophoblast stem cell proliferation by FGF4. Science. 1998;282:2072–5.CrossRefPubMed Tanaka S, Kunath T, Hadjantonakis AK, Nagy A, Rossant J. Promotion of trophoblast stem cell proliferation by FGF4. Science. 1998;282:2072–5.CrossRefPubMed
16.
Zurück zum Zitat Chai N, Patel Y, Jacobson K, McMahon J, McMahon A, Rappolee DA. FGF is an essential regulator of the fifth cell division in preimplantation mouse embryos. Dev Biol. 1998;198:105–15.CrossRefPubMed Chai N, Patel Y, Jacobson K, McMahon J, McMahon A, Rappolee DA. FGF is an essential regulator of the fifth cell division in preimplantation mouse embryos. Dev Biol. 1998;198:105–15.CrossRefPubMed
17.
18.
Zurück zum Zitat Rich PR. The molecular machinery of Keilin’s respiratory chain. Biochem Soc Trans. 2003;31:1095–105.CrossRefPubMed Rich PR. The molecular machinery of Keilin’s respiratory chain. Biochem Soc Trans. 2003;31:1095–105.CrossRefPubMed
19.
Zurück zum Zitat Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science. 2009;324:1029–33.CrossRefPubMedPubMedCentral Vander Heiden MG, Cantley LC, Thompson CB. Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science. 2009;324:1029–33.CrossRefPubMedPubMedCentral
20.
Zurück zum Zitat Houghton FD, Thompson JG, Kennedy CJ, Leese HJ. Oxygen consumption and energy metabolism of the early mouse embryo. Mol Reprod Dev. 1996;44:476–85.CrossRefPubMed Houghton FD, Thompson JG, Kennedy CJ, Leese HJ. Oxygen consumption and energy metabolism of the early mouse embryo. Mol Reprod Dev. 1996;44:476–85.CrossRefPubMed
21.
Zurück zum Zitat Gardner DK. Lactate production by the mammalian blastocyst: manipulating the microenvironment for uterine implantation and invasion? BioEssays. 2015;37:364–71.CrossRefPubMedPubMedCentral Gardner DK. Lactate production by the mammalian blastocyst: manipulating the microenvironment for uterine implantation and invasion? BioEssays. 2015;37:364–71.CrossRefPubMedPubMedCentral
22.
Zurück zum Zitat Houghton FD. Energy metabolism of the inner cell mass and trophectoderm of the mouse blastocyst. Differentiation. 2006;74:11–8.CrossRefPubMed Houghton FD. Energy metabolism of the inner cell mass and trophectoderm of the mouse blastocyst. Differentiation. 2006;74:11–8.CrossRefPubMed
23.
Zurück zum Zitat Van Blerkom J, Cox H, Davis P. Regulatory roles for mitochondria in the peri-implantation mouse blastocyst: possible origins and developmental significance of differential DeltaPsim. Reproduction. 2006;131:961–76.CrossRefPubMed Van Blerkom J, Cox H, Davis P. Regulatory roles for mitochondria in the peri-implantation mouse blastocyst: possible origins and developmental significance of differential DeltaPsim. Reproduction. 2006;131:961–76.CrossRefPubMed
24.
Zurück zum Zitat Xie Y, Zhou S, Jiang Z, Dai J, Puscheck EE, Lee I, et al. Hypoxic stress induces, but cannot sustain trophoblast stem cell differentiation to labyrinthine placenta due to mitochondrial insufficiency. Stem Cell Res. 2014;13:478–91.CrossRefPubMedPubMedCentral Xie Y, Zhou S, Jiang Z, Dai J, Puscheck EE, Lee I, et al. Hypoxic stress induces, but cannot sustain trophoblast stem cell differentiation to labyrinthine placenta due to mitochondrial insufficiency. Stem Cell Res. 2014;13:478–91.CrossRefPubMedPubMedCentral
25.
Zurück zum Zitat Leese HJ, Baumann CG, Brison DR, McEvoy TG, Sturmey RG. Metabolism of the viable mammalian embryo: quietness revisited. Mol Hum Reprod. 2008;14:667–72.CrossRefPubMedPubMedCentral Leese HJ, Baumann CG, Brison DR, McEvoy TG, Sturmey RG. Metabolism of the viable mammalian embryo: quietness revisited. Mol Hum Reprod. 2008;14:667–72.CrossRefPubMedPubMedCentral
26.
Zurück zum Zitat Westfall SD, Sachdev S, Das P, Hearne LB, Hannink M, Roberts RM, et al. Identification of oxygen-sensitive transcriptional programs in human embryonic stem cells. Stem Cells Dev. 2008;17:869–81.CrossRefPubMedPubMedCentral Westfall SD, Sachdev S, Das P, Hearne LB, Hannink M, Roberts RM, et al. Identification of oxygen-sensitive transcriptional programs in human embryonic stem cells. Stem Cells Dev. 2008;17:869–81.CrossRefPubMedPubMedCentral
27.
Zurück zum Zitat Krisher RL, Prather RS. A role for the Warburg effect in preimplantation embryo development: metabolic modification to support rapid cell proliferation. Mol Reprod Dev. 2012;79:311–20.CrossRefPubMedPubMedCentral Krisher RL, Prather RS. A role for the Warburg effect in preimplantation embryo development: metabolic modification to support rapid cell proliferation. Mol Reprod Dev. 2012;79:311–20.CrossRefPubMedPubMedCentral
28.
Zurück zum Zitat Gott AL, Hardy K, Winston RM, Leese HJ. Non-invasive measurement of pyruvate and glucose uptake and lactate production by single human preimplantation embryos. Hum Reprod. 1990;5:104–8.CrossRefPubMed Gott AL, Hardy K, Winston RM, Leese HJ. Non-invasive measurement of pyruvate and glucose uptake and lactate production by single human preimplantation embryos. Hum Reprod. 1990;5:104–8.CrossRefPubMed
29.
Zurück zum Zitat Yang Y, Bolnick A, Shamir A, Abdulhasan M, Li Q, Parker GC, et al. Blastocyst-derived stem cell populations under stress: impact of nutrition and metabolism on stem cell potency loss and miscarriage. Stem Cell Rev Rep. 2017:1–11. Yang Y, Bolnick A, Shamir A, Abdulhasan M, Li Q, Parker GC, et al. Blastocyst-derived stem cell populations under stress: impact of nutrition and metabolism on stem cell potency loss and miscarriage. Stem Cell Rev Rep. 2017:1–11.
30.
Zurück zum Zitat Wilcox AJ, Weinberg CR, O'Connor JF, Baird DD, Schlatterer JP, Canfield RE, et al. Incidence of early loss of pregnancy. N Engl J Med. 1988;319:189–94.CrossRefPubMed Wilcox AJ, Weinberg CR, O'Connor JF, Baird DD, Schlatterer JP, Canfield RE, et al. Incidence of early loss of pregnancy. N Engl J Med. 1988;319:189–94.CrossRefPubMed
31.
Zurück zum Zitat Seeber BE. What serial hCG can tell you, and cannot tell you, about an early pregnancy. Fertil Steril. 2012;98:1074–7.CrossRefPubMed Seeber BE. What serial hCG can tell you, and cannot tell you, about an early pregnancy. Fertil Steril. 2012;98:1074–7.CrossRefPubMed
32.
Zurück zum Zitat Thouas GA, Korfiatis NA, French AJ, Jones GM, Trounson AO. Simplified technique for differential staining of inner cell mass and trophectoderm cells of mouse and bovine blastocysts. Reprod BioMed Online. 2001;3:25–9.CrossRefPubMed Thouas GA, Korfiatis NA, French AJ, Jones GM, Trounson AO. Simplified technique for differential staining of inner cell mass and trophectoderm cells of mouse and bovine blastocysts. Reprod BioMed Online. 2001;3:25–9.CrossRefPubMed
33.
Zurück zum Zitat Niakan KK, Eggan K. Analysis of human embryos from zygote to blastocyst reveals distinct gene expression patterns relative to the mouse. Dev Biol. 2013;375:54–64.CrossRefPubMed Niakan KK, Eggan K. Analysis of human embryos from zygote to blastocyst reveals distinct gene expression patterns relative to the mouse. Dev Biol. 2013;375:54–64.CrossRefPubMed
34.
Zurück zum Zitat Zhou S, Xie Y, Puscheck EE, Rappolee DA. Oxygen levels that optimize TSC culture are identified by maximizing growth rates and minimizing stress. Placenta. 2011;32:475–81.CrossRefPubMedPubMedCentral Zhou S, Xie Y, Puscheck EE, Rappolee DA. Oxygen levels that optimize TSC culture are identified by maximizing growth rates and minimizing stress. Placenta. 2011;32:475–81.CrossRefPubMedPubMedCentral
35.
36.
Zurück zum Zitat Rappolee DA. Impact of transient stress and stress enzymes on development. Dev Biol. 2007;304:1–8.CrossRefPubMed Rappolee DA. Impact of transient stress and stress enzymes on development. Dev Biol. 2007;304:1–8.CrossRefPubMed
37.
Zurück zum Zitat Slater JA, Zhou S, Puscheck EE, Rappolee DA. Stress-induced enzyme activation primes murine embryonic stem cells to differentiate toward the first extraembryonic lineage. Stem Cells Dev. 2014;23:3049–64.CrossRefPubMedPubMedCentral Slater JA, Zhou S, Puscheck EE, Rappolee DA. Stress-induced enzyme activation primes murine embryonic stem cells to differentiate toward the first extraembryonic lineage. Stem Cells Dev. 2014;23:3049–64.CrossRefPubMedPubMedCentral
38.
Zurück zum Zitat Awonuga AO, Zhong W, Abdallah ME, Slater JA, Zhou SC, Xie YF, et al. Eomesodermin, HAND1, and CSH1 proteins are induced by cellular stress in a stress-activated protein kinase-dependent manner. Mol Reprod Dev. 2011;78:519–28.CrossRefPubMedPubMedCentral Awonuga AO, Zhong W, Abdallah ME, Slater JA, Zhou SC, Xie YF, et al. Eomesodermin, HAND1, and CSH1 proteins are induced by cellular stress in a stress-activated protein kinase-dependent manner. Mol Reprod Dev. 2011;78:519–28.CrossRefPubMedPubMedCentral
39.
Zurück zum Zitat Yang Y, Arenas-Hernandez M, Gomez-Lopez N, Dai J, Parker GC, Puscheck EE, et al. Hypoxic stress forces irreversible differentiation of a majority of mouse trophoblast stem cells despite FGF4. Biol Reprod. 2016;95:110.CrossRefPubMed Yang Y, Arenas-Hernandez M, Gomez-Lopez N, Dai J, Parker GC, Puscheck EE, et al. Hypoxic stress forces irreversible differentiation of a majority of mouse trophoblast stem cells despite FGF4. Biol Reprod. 2016;95:110.CrossRefPubMed
40.
Zurück zum Zitat Wang Y, Puscheck EE, Lewis JJ, Trostinskaia AB, Wang F, Rappolee DA. Increases in phosphorylation of SAPK/JNK and p38MAPK correlate negatively with mouse embryo development after culture in different media. Fertil Steril. 2005;83(Suppl 1):1144–54.CrossRefPubMed Wang Y, Puscheck EE, Lewis JJ, Trostinskaia AB, Wang F, Rappolee DA. Increases in phosphorylation of SAPK/JNK and p38MAPK correlate negatively with mouse embryo development after culture in different media. Fertil Steril. 2005;83(Suppl 1):1144–54.CrossRefPubMed
41.
Zurück zum Zitat Chakraborty D, Cui W, Rosario GX, Scott RL, Dhakal P, Renaud SJ et al. HIF-KDM3A-MMP12 regulatory circuit ensures trophoblast plasticity and placental adaptations to hypoxia. Proc Natl Acad Sci USA 2016. Chakraborty D, Cui W, Rosario GX, Scott RL, Dhakal P, Renaud SJ et al. HIF-KDM3A-MMP12 regulatory circuit ensures trophoblast plasticity and placental adaptations to hypoxia. Proc Natl Acad Sci USA 2016.
42.
Zurück zum Zitat Wale PL, Gardner DK. Time-lapse analysis of mouse embryo development in oxygen gradients. Reprod BioMed Online. 2010;21:402–10.CrossRefPubMed Wale PL, Gardner DK. Time-lapse analysis of mouse embryo development in oxygen gradients. Reprod BioMed Online. 2010;21:402–10.CrossRefPubMed
43.
Zurück zum Zitat Yang E, van Nimwegen E, Zavolan M, Rajewsky N, Schroeder M, Magnasco M, et al. Decay rates of human mRNAs: correlation with functional characteristics and sequence attributes. Genome Res. 2003;13:1863–72.CrossRefPubMedPubMedCentral Yang E, van Nimwegen E, Zavolan M, Rajewsky N, Schroeder M, Magnasco M, et al. Decay rates of human mRNAs: correlation with functional characteristics and sequence attributes. Genome Res. 2003;13:1863–72.CrossRefPubMedPubMedCentral
44.
Zurück zum Zitat Sharova LV, Sharov AA, Nedorezov T, Piao Y, Shaik N, Ko MS. Database for mRNA half-life of 19 977 genes obtained by DNA microarray analysis of pluripotent and differentiating mouse embryonic stem cells. DNA Res. 2009;16:45–58.CrossRefPubMed Sharova LV, Sharov AA, Nedorezov T, Piao Y, Shaik N, Ko MS. Database for mRNA half-life of 19 977 genes obtained by DNA microarray analysis of pluripotent and differentiating mouse embryonic stem cells. DNA Res. 2009;16:45–58.CrossRefPubMed
45.
Zurück zum Zitat Herbert M, Wolstenholme J, Murdoch AP, Butler TJ. Mitotic activity during preimplantation development of human embryos. J Reprod Fertil. 1995;103:209–14.CrossRefPubMed Herbert M, Wolstenholme J, Murdoch AP, Butler TJ. Mitotic activity during preimplantation development of human embryos. J Reprod Fertil. 1995;103:209–14.CrossRefPubMed
46.
Zurück zum Zitat Yang Y, Jiang Z, Bolnick A, Dai J, Puscheck EE, Rappolee DA. Departure from optimal O2 level for mouse trophoblast stem cell proliferation and potency leads to most rapid AMPK activation. J Reprod Dev. 2016; Yang Y, Jiang Z, Bolnick A, Dai J, Puscheck EE, Rappolee DA. Departure from optimal O2 level for mouse trophoblast stem cell proliferation and potency leads to most rapid AMPK activation. J Reprod Dev. 2016;
47.
Zurück zum Zitat Li Q, Yang Y, Louden E, Puscheck E, Rappolee D. High throughput screens for embryonic stem cells; stress-forced potency-stemness loss enables toxicological assays. In: Faqi A, editor. Methods. In Toxicology and Pharmacology: Springer; 2016. Li Q, Yang Y, Louden E, Puscheck E, Rappolee D. High throughput screens for embryonic stem cells; stress-forced potency-stemness loss enables toxicological assays. In: Faqi A, editor. Methods. In Toxicology and Pharmacology: Springer; 2016.
48.
Zurück zum Zitat Bolnick A, Abdulhasan M, Kilburn B, Xie Y, Howard M, Andresen P, et al. Commonly used fertility drugs, a diet supplement, and stress force AMPK-dependent block of stemness and development in cultured mammalian embryos. J Assist Reprod Genet. 2016;33:1027–39.CrossRefPubMedPubMedCentral Bolnick A, Abdulhasan M, Kilburn B, Xie Y, Howard M, Andresen P, et al. Commonly used fertility drugs, a diet supplement, and stress force AMPK-dependent block of stemness and development in cultured mammalian embryos. J Assist Reprod Genet. 2016;33:1027–39.CrossRefPubMedPubMedCentral
49.
Zurück zum Zitat Xie Y, Awonuga A, Liu J, Rings E, Puscheck EE, Rappolee DA. Stress induces AMPK-dependent loss of potency factors Id2 and Cdx2 in early embryos and stem cells [corrected]. Stem Cells Dev. 2013;22:1564–75.CrossRefPubMedPubMedCentral Xie Y, Awonuga A, Liu J, Rings E, Puscheck EE, Rappolee DA. Stress induces AMPK-dependent loss of potency factors Id2 and Cdx2 in early embryos and stem cells [corrected]. Stem Cells Dev. 2013;22:1564–75.CrossRefPubMedPubMedCentral
50.
Zurück zum Zitat Zhong W, Xie Y, Abdallah M, Awonuga AO, Slater JA, Sipahi L, et al. Cellular stress causes reversible, PRKAA1/2-, and proteasome-dependent ID2 protein loss in trophoblast stem cells. Reproduction. 2010;140:921–30.CrossRefPubMedPubMedCentral Zhong W, Xie Y, Abdallah M, Awonuga AO, Slater JA, Sipahi L, et al. Cellular stress causes reversible, PRKAA1/2-, and proteasome-dependent ID2 protein loss in trophoblast stem cells. Reproduction. 2010;140:921–30.CrossRefPubMedPubMedCentral
51.
Zurück zum Zitat Xie Y, Abdallah ME, Awonuga AO, Slater JA, Puscheck EE, Rappolee DA. Benzo(a)pyrene causes PRKAA1/2-dependent ID2 loss in trophoblast stem cells. Mol Reprod Dev. 2010;77:533–9.CrossRefPubMed Xie Y, Abdallah ME, Awonuga AO, Slater JA, Puscheck EE, Rappolee DA. Benzo(a)pyrene causes PRKAA1/2-dependent ID2 loss in trophoblast stem cells. Mol Reprod Dev. 2010;77:533–9.CrossRefPubMed
52.
Zurück zum Zitat Bolnick A, Kilburn B, Abdulhasan M, Shamir A, Dai J, Puscheck E et al. 2-cell embryos are more sensitive than blastocysts to AMPK-dependent suppression of anabolism and potency/stemness by commonly used drugs, a diet supplement and stress. J Assist Reprod Genet 2017; to be submittted. Bolnick A, Kilburn B, Abdulhasan M, Shamir A, Dai J, Puscheck E et al. 2-cell embryos are more sensitive than blastocysts to AMPK-dependent suppression of anabolism and potency/stemness by commonly used drugs, a diet supplement and stress. J Assist Reprod Genet 2017; to be submittted.
53.
Zurück zum Zitat Heo YS, Cabrera LM, Bormann CL, Shah CT, Takayama S, Smith GD. Dynamic microfunnel culture enhances mouse embryo development and pregnancy rates. Hum Reprod. 2010;25:613–22.CrossRefPubMedPubMedCentral Heo YS, Cabrera LM, Bormann CL, Shah CT, Takayama S, Smith GD. Dynamic microfunnel culture enhances mouse embryo development and pregnancy rates. Hum Reprod. 2010;25:613–22.CrossRefPubMedPubMedCentral
54.
Zurück zum Zitat Yang Y, Jiang Z, Bolnick A, Dai J, Puscheck EE, Rappolee DA. Departure from optimal O2 level for mouse trophoblast stem cell proliferation and potency leads to most rapid AMPK activation. J Reprod Dev. 2017;63:87–94.CrossRefPubMed Yang Y, Jiang Z, Bolnick A, Dai J, Puscheck EE, Rappolee DA. Departure from optimal O2 level for mouse trophoblast stem cell proliferation and potency leads to most rapid AMPK activation. J Reprod Dev. 2017;63:87–94.CrossRefPubMed
55.
Zurück zum Zitat Yang Y, Xu Y, Ding C, Khoudja RY, Lin M, Awonuga AO, et al. Comparison of 2, 5, and 20% O2 on the development of post-thaw human embryos. J Assist Reprod Genet. 2016;33:919–27.CrossRefPubMedPubMedCentral Yang Y, Xu Y, Ding C, Khoudja RY, Lin M, Awonuga AO, et al. Comparison of 2, 5, and 20% O2 on the development of post-thaw human embryos. J Assist Reprod Genet. 2016;33:919–27.CrossRefPubMedPubMedCentral
56.
Zurück zum Zitat Feil D, Lane M, Roberts CT, Kelley RL, Edwards LJ, Thompson JG, et al. Effect of culturing mouse embryos under different oxygen concentrations on subsequent fetal and placental development. J Physiol. 2006;572:87–96.CrossRefPubMedPubMedCentral Feil D, Lane M, Roberts CT, Kelley RL, Edwards LJ, Thompson JG, et al. Effect of culturing mouse embryos under different oxygen concentrations on subsequent fetal and placental development. J Physiol. 2006;572:87–96.CrossRefPubMedPubMedCentral
57.
Zurück zum Zitat Chen B, Longtine MS, Nelson DM. Pericellular oxygen concentration of cultured primary human trophoblasts. Placenta. 2013;34:106–9.CrossRefPubMed Chen B, Longtine MS, Nelson DM. Pericellular oxygen concentration of cultured primary human trophoblasts. Placenta. 2013;34:106–9.CrossRefPubMed
58.
Zurück zum Zitat Lee MS, Lee YS, Lee HH, Song HY. Human endometrial cell coculture reduces the endocrine disruptor toxicity on mouse embryo development. J Occup Med Toxicol. 2012;7:7.CrossRefPubMedPubMedCentral Lee MS, Lee YS, Lee HH, Song HY. Human endometrial cell coculture reduces the endocrine disruptor toxicity on mouse embryo development. J Occup Med Toxicol. 2012;7:7.CrossRefPubMedPubMedCentral
59.
Zurück zum Zitat Borman ED, Foster WG, Greenacre MKE, Muir CC, deCatanzaro D. Stress lowers the threshold dose at which bisphenol A disrupts blastocyst implantation, in conjunction with decreased uterine closure and E-cadherin. Chem Biol Interact. 2015;237:87–95.CrossRefPubMed Borman ED, Foster WG, Greenacre MKE, Muir CC, deCatanzaro D. Stress lowers the threshold dose at which bisphenol A disrupts blastocyst implantation, in conjunction with decreased uterine closure and E-cadherin. Chem Biol Interact. 2015;237:87–95.CrossRefPubMed
60.
Zurück zum Zitat Jauniaux E, Watson A, Burton G. Evaluation of respiratory gases and acid-base gradients in human fetal fluids and uteroplacental tissue between 7 and 16 weeks’ gestation. Am J Obstet Gynecol. 2001;184:998–1003.CrossRefPubMed Jauniaux E, Watson A, Burton G. Evaluation of respiratory gases and acid-base gradients in human fetal fluids and uteroplacental tissue between 7 and 16 weeks’ gestation. Am J Obstet Gynecol. 2001;184:998–1003.CrossRefPubMed
61.
Zurück zum Zitat Genbacev O, Joslin R, Damsky CH, Polliotti BM, Fisher SJ. Hypoxia alters early gestation human cytotrophoblast differentiation/invasion in vitro and models the placental defects that occur in preeclampsia. J Clin Invest. 1996;97:540–50.CrossRefPubMedPubMedCentral Genbacev O, Joslin R, Damsky CH, Polliotti BM, Fisher SJ. Hypoxia alters early gestation human cytotrophoblast differentiation/invasion in vitro and models the placental defects that occur in preeclampsia. J Clin Invest. 1996;97:540–50.CrossRefPubMedPubMedCentral
62.
Zurück zum Zitat Kilburn BA, Wang J, Duniec-Dmuchowski ZM, Leach RE, Romero R, Armant DR. Extracellular matrix composition and hypoxia regulate the expression of HLA-G and integrins in a human trophoblast cell line. Biol Reprod. 2000;62:739–47.CrossRefPubMed Kilburn BA, Wang J, Duniec-Dmuchowski ZM, Leach RE, Romero R, Armant DR. Extracellular matrix composition and hypoxia regulate the expression of HLA-G and integrins in a human trophoblast cell line. Biol Reprod. 2000;62:739–47.CrossRefPubMed
63.
Zurück zum Zitat Caniggia I, Mostachfi H, Winter J, Gassmann M, Lye SJ, Kuliszewski M, et al. Hypoxia-inducible factor-1 mediates the biological effects of oxygen on human trophoblast differentiation through TGFbeta(3). J Clin Invest. 2000;105:577–87.CrossRefPubMedPubMedCentral Caniggia I, Mostachfi H, Winter J, Gassmann M, Lye SJ, Kuliszewski M, et al. Hypoxia-inducible factor-1 mediates the biological effects of oxygen on human trophoblast differentiation through TGFbeta(3). J Clin Invest. 2000;105:577–87.CrossRefPubMedPubMedCentral
64.
Zurück zum Zitat Red-Horse K, Zhou Y, Genbacev O, Prakobphol A, Foulk R, McMaster M, et al. Trophoblast differentiation during embryo implantation and formation of the maternal-fetal interface. J Clin Invest. 2004;114:744–54.CrossRefPubMedPubMedCentral Red-Horse K, Zhou Y, Genbacev O, Prakobphol A, Foulk R, McMaster M, et al. Trophoblast differentiation during embryo implantation and formation of the maternal-fetal interface. J Clin Invest. 2004;114:744–54.CrossRefPubMedPubMedCentral
65.
Zurück zum Zitat Zhou Y, Damsky CH, Fisher SJ. Preeclampsia is associated with failure of human cytotrophoblasts to mimic a vascular adhesion phenotype. One cause of defective endovascular invasion in this syndrome? J Clin Invest. 1997;99:2152–64.CrossRefPubMedPubMedCentral Zhou Y, Damsky CH, Fisher SJ. Preeclampsia is associated with failure of human cytotrophoblasts to mimic a vascular adhesion phenotype. One cause of defective endovascular invasion in this syndrome? J Clin Invest. 1997;99:2152–64.CrossRefPubMedPubMedCentral
66.
Zurück zum Zitat Burton GJ, Jauniaux E. Placental oxidative stress: from miscarriage to preeclampsia. J Soc Gynecol Investig. 2004;11:342–52.CrossRefPubMed Burton GJ, Jauniaux E. Placental oxidative stress: from miscarriage to preeclampsia. J Soc Gynecol Investig. 2004;11:342–52.CrossRefPubMed
67.
Zurück zum Zitat Quinn P, Harlow GM. The effect of oxygen on the development of preimplantation mouse embryos in vitro. J Exp Zool. 1978;206:73–80.CrossRefPubMed Quinn P, Harlow GM. The effect of oxygen on the development of preimplantation mouse embryos in vitro. J Exp Zool. 1978;206:73–80.CrossRefPubMed
68.
Zurück zum Zitat Pabon JE Jr, Findley WE, Gibbons WE. The toxic effect of short exposures to the atmospheric oxygen concentration on early mouse embryonic development. Fertil Steril. 1989;51:896–900.CrossRefPubMed Pabon JE Jr, Findley WE, Gibbons WE. The toxic effect of short exposures to the atmospheric oxygen concentration on early mouse embryonic development. Fertil Steril. 1989;51:896–900.CrossRefPubMed
69.
Zurück zum Zitat Umaoka Y, Noda Y, Narimoto K, Mori T. Effects of oxygen toxicity on early development of mouse embryos. Mol Reprod Dev. 1992;31:28–33.CrossRefPubMed Umaoka Y, Noda Y, Narimoto K, Mori T. Effects of oxygen toxicity on early development of mouse embryos. Mol Reprod Dev. 1992;31:28–33.CrossRefPubMed
70.
Zurück zum Zitat Li J, Foote RH. Culture of rabbit zygotes into blastocysts in protein-free medium with one to twenty per cent oxygen. J Reprod Fertil. 1993;98:163–7.CrossRefPubMed Li J, Foote RH. Culture of rabbit zygotes into blastocysts in protein-free medium with one to twenty per cent oxygen. J Reprod Fertil. 1993;98:163–7.CrossRefPubMed
71.
Zurück zum Zitat Orsi NM, Leese HJ. Protection against reactive oxygen species during mouse preimplantation embryo development: role of EDTA, oxygen tension, catalase, superoxide dismutase and pyruvate. Mol Reprod Dev. 2001;59:44–53.CrossRefPubMed Orsi NM, Leese HJ. Protection against reactive oxygen species during mouse preimplantation embryo development: role of EDTA, oxygen tension, catalase, superoxide dismutase and pyruvate. Mol Reprod Dev. 2001;59:44–53.CrossRefPubMed
72.
Zurück zum Zitat Banwell KM, Lane M, Russell DL, Kind KL, Thompson JG. Oxygen concentration during mouse oocyte in vitro maturation affects embryo and fetal development. Hum Reprod. 2007;22:2768–75.CrossRefPubMed Banwell KM, Lane M, Russell DL, Kind KL, Thompson JG. Oxygen concentration during mouse oocyte in vitro maturation affects embryo and fetal development. Hum Reprod. 2007;22:2768–75.CrossRefPubMed
73.
Zurück zum Zitat Thompson JG, McNaughton C, Gasparrini B, McGowan LT, Tervit HR. Effect of inhibitors and uncouplers of oxidative phosphorylation during compaction and blastulation of bovine embryos cultured in vitro. J Reprod Fertil. 2000;118:47–55.CrossRefPubMed Thompson JG, McNaughton C, Gasparrini B, McGowan LT, Tervit HR. Effect of inhibitors and uncouplers of oxidative phosphorylation during compaction and blastulation of bovine embryos cultured in vitro. J Reprod Fertil. 2000;118:47–55.CrossRefPubMed
74.
Zurück zum Zitat Thompson JG, Simpson AC, Pugh PA, Donnelly PE, Tervit HR. Effect of oxygen concentration on in-vitro development of preimplantation sheep and cattle embryos. J Reprod Fertil. 1990;89:573–8.CrossRefPubMed Thompson JG, Simpson AC, Pugh PA, Donnelly PE, Tervit HR. Effect of oxygen concentration on in-vitro development of preimplantation sheep and cattle embryos. J Reprod Fertil. 1990;89:573–8.CrossRefPubMed
75.
Zurück zum Zitat Dumoulin JC, Meijers CJ, Bras M, Coonen E, Geraedts JP, Evers JL. Effect of oxygen concentration on human in-vitro fertilization and embryo culture. Hum Reprod. 1999;14:465–9.CrossRefPubMed Dumoulin JC, Meijers CJ, Bras M, Coonen E, Geraedts JP, Evers JL. Effect of oxygen concentration on human in-vitro fertilization and embryo culture. Hum Reprod. 1999;14:465–9.CrossRefPubMed
76.
Zurück zum Zitat Dumoulin JC, Vanvuchelen RC, Land JA, Pieters MH, Geraedts JP, Evers JL. Effect of oxygen concentration on in vitro fertilization and embryo culture in the human and the mouse. Fertil Steril. 1995;63:115–9.CrossRefPubMed Dumoulin JC, Vanvuchelen RC, Land JA, Pieters MH, Geraedts JP, Evers JL. Effect of oxygen concentration on in vitro fertilization and embryo culture in the human and the mouse. Fertil Steril. 1995;63:115–9.CrossRefPubMed
77.
Zurück zum Zitat Harlow GM, Quinn P. Foetal and placental growth in the mouse after pre-implantation development in vitro under oxygen concentrations of 5 and 20%. Aust J Biol Sci. 1979;32:363–9.CrossRefPubMed Harlow GM, Quinn P. Foetal and placental growth in the mouse after pre-implantation development in vitro under oxygen concentrations of 5 and 20%. Aust J Biol Sci. 1979;32:363–9.CrossRefPubMed
78.
Zurück zum Zitat Kind KL, Collett RA, Harvey AJ, Thompson JG. Oxygen-regulated expression of GLUT-1, GLUT-3, and VEGF in the mouse blastocyst. Mol Reprod Dev. 2005;70:37–44.CrossRefPubMed Kind KL, Collett RA, Harvey AJ, Thompson JG. Oxygen-regulated expression of GLUT-1, GLUT-3, and VEGF in the mouse blastocyst. Mol Reprod Dev. 2005;70:37–44.CrossRefPubMed
79.
Zurück zum Zitat Harvey AJ, Kind KL, Thompson JG. Regulation of gene expression in bovine blastocysts in response to oxygen and the iron chelator desferrioxamine. Biol Reprod. 2007;77:93–101.CrossRefPubMed Harvey AJ, Kind KL, Thompson JG. Regulation of gene expression in bovine blastocysts in response to oxygen and the iron chelator desferrioxamine. Biol Reprod. 2007;77:93–101.CrossRefPubMed
80.
Zurück zum Zitat Kurosawa H, Utsunomiya H, Shiga N, Takahashi A, Ihara M, Ishibashi M, et al. Development of a new clinically applicable device for embryo evaluation which measures embryo oxygen consumption. Hum Reprod. 2016;31:2321–30.CrossRefPubMed Kurosawa H, Utsunomiya H, Shiga N, Takahashi A, Ihara M, Ishibashi M, et al. Development of a new clinically applicable device for embryo evaluation which measures embryo oxygen consumption. Hum Reprod. 2016;31:2321–30.CrossRefPubMed
81.
Zurück zum Zitat Zhang YS, Ribas J, Nadhman A, Aleman J, Selimovic S, Lesher-Perez SC, et al. A cost-effective fluorescence mini-microscope for biomedical applications. Lab Chip. 2015;15:3661–9.CrossRefPubMedPubMedCentral Zhang YS, Ribas J, Nadhman A, Aleman J, Selimovic S, Lesher-Perez SC, et al. A cost-effective fluorescence mini-microscope for biomedical applications. Lab Chip. 2015;15:3661–9.CrossRefPubMedPubMedCentral
82.
Zurück zum Zitat Swain JE, Carrell D, Cobo A, Meseguer M, Rubio C, Smith GD. Optimizing the culture environment and embryo manipulation to help maintain embryo developmental potential. Fertil Steril. 2016;105:571–87.CrossRefPubMed Swain JE, Carrell D, Cobo A, Meseguer M, Rubio C, Smith GD. Optimizing the culture environment and embryo manipulation to help maintain embryo developmental potential. Fertil Steril. 2016;105:571–87.CrossRefPubMed
Metadaten
Titel
Using stem cell oxygen physiology to optimize blastocyst culture while minimizing hypoxic stress
verfasst von
Alan Bolnick
Awoniyi O Awonuga
Yu Yang
Mohammed Abdulhasan
Yufen Xie
Sichang Zhou
Elizabeth E. Puscheck
Daniel A. Rappolee
Publikationsdatum
24.06.2017
Verlag
Springer US
Erschienen in
Journal of Assisted Reproduction and Genetics / Ausgabe 10/2017
Print ISSN: 1058-0468
Elektronische ISSN: 1573-7330
DOI
https://doi.org/10.1007/s10815-017-0971-x

Weitere Artikel der Ausgabe 10/2017

Journal of Assisted Reproduction and Genetics 10/2017 Zur Ausgabe

Alter verschlechtert Prognose bei Endometriumkarzinom

11.05.2024 Endometriumkarzinom Nachrichten

Ein höheres Alter bei der Diagnose eines Endometriumkarzinoms ist mit aggressiveren Tumorcharakteristika assoziiert, scheint aber auch unabhängig von bekannten Risikofaktoren die Prognose der Erkrankung zu verschlimmern.

Darf man die Behandlung eines Neonazis ablehnen?

08.05.2024 Gesellschaft Nachrichten

In einer Leseranfrage in der Zeitschrift Journal of the American Academy of Dermatology möchte ein anonymer Dermatologe bzw. eine anonyme Dermatologin wissen, ob er oder sie einen Patienten behandeln muss, der eine rassistische Tätowierung trägt.

Erhöhte Mortalität bei postpartalem Brustkrebs

07.05.2024 Mammakarzinom Nachrichten

Auch für Trägerinnen von BRCA-Varianten gilt: Erkranken sie fünf bis zehn Jahre nach der letzten Schwangerschaft an Brustkrebs, ist das Sterberisiko besonders hoch.

Menopausale Hormontherapie für Frauen über 65?

07.05.2024 Klimakterium und Menopause Nachrichten

In den USA erhalten nicht wenige Frauen auch noch im Alter über 65 eine menopausale Hormontherapie. Welche positiven und negativen gesundheitlichen Konsequenzen daraus möglicherweise resultieren, wurde anhand von Versicherungsdaten analysiert.

Update Gynäkologie

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert – ganz bequem per eMail.