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Erschienen in: Journal of Assisted Reproduction and Genetics 10/2019

08.08.2019 | Embryo Biology

FoxO transcription factors 1 regulate mouse preimplantation embryo development

verfasst von: Nilay Kuscu, Nazli Ece Gungor-Ordueri, Berna Sozen, Dileyra Adiguzel, Ciler Celik-Ozenci

Erschienen in: Journal of Assisted Reproduction and Genetics | Ausgabe 10/2019

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Abstract

Purpose

The aim of the present study is to investigate role of FoxO transcription factors in preimplantation embryo development by knocking down FoxO1, FoxO3, and FoxO4 genes and also to assess cell cycle arrest related proteins, p53 and p21, and apoptosis-related proteins, fas ligand (FASL), and cleaved caspase 3.

Methods

Knockdown of FoxOs using siRNA was confirmed utilizing RT-PCR and qRT-PCR in gene level and using immunofluorescence in protein level. Following knockdown of FoxO1, FoxO3, and FoxO4 in two-cell mouse embryos with or without resveratrol treatment; developmental competence of embryos and expression patterns of SIRT1, p53, p21, FASL, and CLEAVED CASPASE 3 proteins in embryos by immunofluorescence were assessed after 48 h. ROS levels were measured in knockdown embryos. Terminal deoxynucleotidyl transferase dUTP nick end labeling assay was used to determine resveratrol dose.

Results

Successful knockdown of FoxO genes in mouse embryos utilizing a non-invasive siRNA method was achieved. Significantly, knockdown of FoxO genes impaired preimplantation embryo development which cannot be prevented by resveratrol treatment. Immunofluorescence results showed that resveratrol could protect embryos from cell cycle arrest and apoptosis. FOXO proteins regulate apoptosis and cell cycle related proteins in mouse preimplantation embryos. Moreover, there might be an autofeedback mechanism where FOXO1, FOXO3, and FOXO4 regulate SIRT1 protein expression.

Conclusions

These results suggest that FOXO transcription factors could contribute to mouse preimplantation embryo development, and it remains to investigate whether they have crucial roles in human preimplantation embryo and infertility.
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Literatur
1.
Zurück zum Zitat Banks AS, Kon N, Knight C, Matsumoto M, Gutierrez-Juarez R, Rossetti L, et al. SirT1 gain of function increases energy efficiency and prevents diabetes in mice. Cell Metab. 2008;8:333–41.PubMedPubMedCentral Banks AS, Kon N, Knight C, Matsumoto M, Gutierrez-Juarez R, Rossetti L, et al. SirT1 gain of function increases energy efficiency and prevents diabetes in mice. Cell Metab. 2008;8:333–41.PubMedPubMedCentral
2.
3.
Zurück zum Zitat Brunet A, Sweeney LB, Sturgill JF, Chua KF, Greer PL, Lin Y, et al. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science. 2004;303:2011–5.PubMed Brunet A, Sweeney LB, Sturgill JF, Chua KF, Greer PL, Lin Y, et al. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science. 2004;303:2011–5.PubMed
4.
Zurück zum Zitat Chan WH. Resveratrol protects against 2-bromopropane-induced apoptosis and disruption of embryonic development in blastocysts. Int J Mol Sci. 2011;12:4991–5010.PubMedPubMedCentral Chan WH. Resveratrol protects against 2-bromopropane-induced apoptosis and disruption of embryonic development in blastocysts. Int J Mol Sci. 2011;12:4991–5010.PubMedPubMedCentral
5.
Zurück zum Zitat Chen LJ, Xu WM, Yang M, Wang K, Chen Y, Huang XJ, et al. HUWE1 plays important role in mouse preimplantation embryo development and the dysregulation is associated with poor embryo development in humans. Sci Rep. 2016;6:37928.PubMedPubMedCentral Chen LJ, Xu WM, Yang M, Wang K, Chen Y, Huang XJ, et al. HUWE1 plays important role in mouse preimplantation embryo development and the dysregulation is associated with poor embryo development in humans. Sci Rep. 2016;6:37928.PubMedPubMedCentral
6.
Zurück zum Zitat Coffre M, Benhamou D, Riess D, Blumenberg L, Snetkova V, Hines MJ, et al. miRNAs are essential for the regulation of the PI3K/AKT/FOXO pathway and receptor editing during B cell maturation. Cell Rep. 2016;17:2271–85.PubMedPubMedCentral Coffre M, Benhamou D, Riess D, Blumenberg L, Snetkova V, Hines MJ, et al. miRNAs are essential for the regulation of the PI3K/AKT/FOXO pathway and receptor editing during B cell maturation. Cell Rep. 2016;17:2271–85.PubMedPubMedCentral
7.
Zurück zum Zitat Daitoku H, Hatta M, Matsuzaki H, Aratani S, Ohshima T, Miyagishi M, et al. Silent information regulator 2 potentiates Foxo1-mediated transcription through its deacetylase activity. Proc Natl Acad Sci U S A. 2004;101:10042–7.PubMedPubMedCentral Daitoku H, Hatta M, Matsuzaki H, Aratani S, Ohshima T, Miyagishi M, et al. Silent information regulator 2 potentiates Foxo1-mediated transcription through its deacetylase activity. Proc Natl Acad Sci U S A. 2004;101:10042–7.PubMedPubMedCentral
8.
Zurück zum Zitat Delhanty JD, Harper JC, Ao A, Handyside AH, Winston RM. Multicolour FISH detects frequent chromosomal mosaicism and chaotic division in normal preimplantation embryos from fertile patients. Hum Genet. 1997;99:755–60.PubMed Delhanty JD, Harper JC, Ao A, Handyside AH, Winston RM. Multicolour FISH detects frequent chromosomal mosaicism and chaotic division in normal preimplantation embryos from fertile patients. Hum Genet. 1997;99:755–60.PubMed
9.
Zurück zum Zitat Gertz M, Nguyen GT, Fischer F, Suenkel B, Schlicker C, Franzel B, et al. A molecular mechanism for direct sirtuin activation by resveratrol. PLoS One. 2012;7:e49761.PubMedPubMedCentral Gertz M, Nguyen GT, Fischer F, Suenkel B, Schlicker C, Franzel B, et al. A molecular mechanism for direct sirtuin activation by resveratrol. PLoS One. 2012;7:e49761.PubMedPubMedCentral
10.
Zurück zum Zitat Greer EL, Brunet A. FOXO transcription factors at the interface between longevity and tumor suppression. Oncogene. 2005;24:7410–25.PubMed Greer EL, Brunet A. FOXO transcription factors at the interface between longevity and tumor suppression. Oncogene. 2005;24:7410–25.PubMed
11.
Zurück zum Zitat Griendling KK, Berk BC, Socorro L, Tsuda T, Delafontaine P, Alexander RW. Secondary signalling mechanisms in angiotensin II-stimulated vascular smooth muscle cells. Clin Exp Pharmacol Physiol. 1988;15:105–12.PubMed Griendling KK, Berk BC, Socorro L, Tsuda T, Delafontaine P, Alexander RW. Secondary signalling mechanisms in angiotensin II-stimulated vascular smooth muscle cells. Clin Exp Pharmacol Physiol. 1988;15:105–12.PubMed
12.
Zurück zum Zitat Gungor-Ordueri NE, Tang EI, Celik-Ozenci C, Cheng CY. Ezrin is an actin binding protein that regulates Sertoli cell and spermatid adhesion during spermatogenesis. Endocrinology. 2014;155:3981–95.PubMedPubMedCentral Gungor-Ordueri NE, Tang EI, Celik-Ozenci C, Cheng CY. Ezrin is an actin binding protein that regulates Sertoli cell and spermatid adhesion during spermatogenesis. Endocrinology. 2014;155:3981–95.PubMedPubMedCentral
14.
Zurück zum Zitat Hori YS, Kuno A, Hosoda R, Horio Y. Regulation of FOXOs and p53 by SIRT1 modulators under oxidative stress. PLoS One. 2013;8:e73875.PubMedPubMedCentral Hori YS, Kuno A, Hosoda R, Horio Y. Regulation of FOXOs and p53 by SIRT1 modulators under oxidative stress. PLoS One. 2013;8:e73875.PubMedPubMedCentral
15.
Zurück zum Zitat Huang LH, Shiao NH, Hsuuw YD, Chan WH. Protective effects of resveratrol on ethanol-induced apoptosis in embryonic stem cells and disruption of embryonic development in mouse blastocysts. Toxicology. 2007;242:109–22.PubMed Huang LH, Shiao NH, Hsuuw YD, Chan WH. Protective effects of resveratrol on ethanol-induced apoptosis in embryonic stem cells and disruption of embryonic development in mouse blastocysts. Toxicology. 2007;242:109–22.PubMed
16.
Zurück zum Zitat Jeong JK, Kang MH, Gurunathan S, Cho SG, Park C, Park JK, et al. Pifithrin-alpha ameliorates resveratrol-induced two-cell block in mouse preimplantation embryos in vitro. Theriogenology. 2015;83:862–73.PubMed Jeong JK, Kang MH, Gurunathan S, Cho SG, Park C, Park JK, et al. Pifithrin-alpha ameliorates resveratrol-induced two-cell block in mouse preimplantation embryos in vitro. Theriogenology. 2015;83:862–73.PubMed
17.
Zurück zum Zitat Kawamura Y, Uchijima Y, Horike N, Tonami K, Nishiyama K, Amano T, et al. Sirt3 protects in vitro-fertilized mouse preimplantation embryos against oxidative stress-induced p53-mediated developmental arrest. J Clin Invest. 2010;120:2817–28.PubMedPubMedCentral Kawamura Y, Uchijima Y, Horike N, Tonami K, Nishiyama K, Amano T, et al. Sirt3 protects in vitro-fertilized mouse preimplantation embryos against oxidative stress-induced p53-mediated developmental arrest. J Clin Invest. 2010;120:2817–28.PubMedPubMedCentral
18.
Zurück zum Zitat Kitamura YI, Kitamura T, Kruse JP, Raum JC, Stein R, Gu W, et al. FoxO1 protects against pancreatic beta cell failure through NeuroD and MafA induction. Cell Metab. 2005;2:153–63.PubMed Kitamura YI, Kitamura T, Kruse JP, Raum JC, Stein R, Gu W, et al. FoxO1 protects against pancreatic beta cell failure through NeuroD and MafA induction. Cell Metab. 2005;2:153–63.PubMed
19.
Zurück zum Zitat Kuscu N, Celik-Ozenci C. FOXO1, FOXO3, AND FOXO4 are differently expressed during mouse oocyte maturation and preimplantation embryo development. Gene Expr Patterns. 2015;18:16–20.PubMed Kuscu N, Celik-Ozenci C. FOXO1, FOXO3, AND FOXO4 are differently expressed during mouse oocyte maturation and preimplantation embryo development. Gene Expr Patterns. 2015;18:16–20.PubMed
20.
Zurück zum Zitat Kyoung Kim H, Kyoung Kim Y, Song IH, Baek SH, Lee SR, Hye Kim J, et al. Down-regulation of a forkhead transcription factor, FOXO3a, accelerates cellular senescence in human dermal fibroblasts. J Gerontol A Biol Sci Med Sci. 2005;60:4–9.PubMed Kyoung Kim H, Kyoung Kim Y, Song IH, Baek SH, Lee SR, Hye Kim J, et al. Down-regulation of a forkhead transcription factor, FOXO3a, accelerates cellular senescence in human dermal fibroblasts. J Gerontol A Biol Sci Med Sci. 2005;60:4–9.PubMed
21.
Zurück zum Zitat Lam EW, Francis RE, Petkovic M. FOXO transcription factors: key regulators of cell fate. Biochem Soc Trans. 2006;34:722–6.PubMed Lam EW, Francis RE, Petkovic M. FOXO transcription factors: key regulators of cell fate. Biochem Soc Trans. 2006;34:722–6.PubMed
22.
Zurück zum Zitat Langley E, Pearson M, Faretta M, Bauer UM, Frye RA, Minucci S, et al. Human SIR2 deacetylates p53 and antagonizes PML/p53-induced cellular senescence. EMBO J. 2002;21:2383–96.PubMedPubMedCentral Langley E, Pearson M, Faretta M, Bauer UM, Frye RA, Minucci S, et al. Human SIR2 deacetylates p53 and antagonizes PML/p53-induced cellular senescence. EMBO J. 2002;21:2383–96.PubMedPubMedCentral
23.
Zurück zum Zitat Lee MT, Bonneau AR, Giraldez AJ. Zygotic genome activation during the maternal-to-zygotic transition. Annu Rev Cell Dev Biol. 2014;30:581–613.PubMedPubMedCentral Lee MT, Bonneau AR, Giraldez AJ. Zygotic genome activation during the maternal-to-zygotic transition. Annu Rev Cell Dev Biol. 2014;30:581–613.PubMedPubMedCentral
24.
Zurück zum Zitat Leese HJ. Quiet please, do not disturb: a hypothesis of embryo metabolism and viability. Bioessays. 2002;24:845–9.PubMed Leese HJ. Quiet please, do not disturb: a hypothesis of embryo metabolism and viability. Bioessays. 2002;24:845–9.PubMed
25.
Zurück zum Zitat Leese HJ, Donnay I, Thompson JG. Human assisted conception: a cautionary tale. Lessons from domestic animals. Hum Reprod. 1998;13(Suppl 4):184–202.PubMed Leese HJ, Donnay I, Thompson JG. Human assisted conception: a cautionary tale. Lessons from domestic animals. Hum Reprod. 1998;13(Suppl 4):184–202.PubMed
26.
Zurück zum Zitat Link W, Fernandez-Marcos PJ. FOXO transcription factors at the interface of metabolism and cancer. Int J Cancer. 2017;141:2379–91.PubMed Link W, Fernandez-Marcos PJ. FOXO transcription factors at the interface of metabolism and cancer. Int J Cancer. 2017;141:2379–91.PubMed
27.
Zurück zum Zitat Liu M, Yin Y, Ye X, Zeng M, Zhao Q, Keefe DL, et al. Resveratrol protects against age-associated infertility in mice. Hum Reprod. 2013;28:707–17.PubMed Liu M, Yin Y, Ye X, Zeng M, Zhao Q, Keefe DL, et al. Resveratrol protects against age-associated infertility in mice. Hum Reprod. 2013;28:707–17.PubMed
28.
Zurück zum Zitat Liu X, Feng J, Tang L, Liao L, Xu Q, Zhu S. The regulation and function of miR-21-FOXO3a-miR-34b/c signaling in breast cancer. Int J Mol Sci. 2015;16:3148–62.PubMedPubMedCentral Liu X, Feng J, Tang L, Liao L, Xu Q, Zhu S. The regulation and function of miR-21-FOXO3a-miR-34b/c signaling in breast cancer. Int J Mol Sci. 2015;16:3148–62.PubMedPubMedCentral
29.
Zurück zum Zitat Maiese K, Chong ZZ, Shang YC. OutFOXOing disease and disability: the therapeutic potential of targeting FoxO proteins. Trends Mol Med. 2008;14:219–27.PubMedPubMedCentral Maiese K, Chong ZZ, Shang YC. OutFOXOing disease and disability: the therapeutic potential of targeting FoxO proteins. Trends Mol Med. 2008;14:219–27.PubMedPubMedCentral
30.
Zurück zum Zitat Mansouri L, Xie Y, Rappolee DA. Adaptive and pathogenic responses to stress by stem cells during development. Cells. 2012;1:1197–224.PubMedPubMedCentral Mansouri L, Xie Y, Rappolee DA. Adaptive and pathogenic responses to stress by stem cells during development. Cells. 2012;1:1197–224.PubMedPubMedCentral
31.
Zurück zum Zitat Matsuzaki H, Daitoku H, Hatta M, Tanaka K, Fukamizu A. Insulin-induced phosphorylation of FKHR (Foxo1) targets to proteasomal degradation. Proc Natl Acad Sci U S A. 2003;100:11285–90.PubMedPubMedCentral Matsuzaki H, Daitoku H, Hatta M, Tanaka K, Fukamizu A. Insulin-induced phosphorylation of FKHR (Foxo1) targets to proteasomal degradation. Proc Natl Acad Sci U S A. 2003;100:11285–90.PubMedPubMedCentral
32.
Zurück zum Zitat Nasr-Esfahani MM, Johnson MH. The origin of reactive oxygen species in mouse embryos cultured in vitro. Development. 1991;113:551–60.PubMed Nasr-Esfahani MM, Johnson MH. The origin of reactive oxygen species in mouse embryos cultured in vitro. Development. 1991;113:551–60.PubMed
33.
Zurück zum Zitat O’Meara CM, Murray JD, Mamo S, Gallagher E, Roche J, Lonergan P. Gene silencing in bovine zygotes: siRNA transfection versus microinjection. Reprod Fertil Dev. 2011;23:534–43.PubMed O’Meara CM, Murray JD, Mamo S, Gallagher E, Roche J, Lonergan P. Gene silencing in bovine zygotes: siRNA transfection versus microinjection. Reprod Fertil Dev. 2011;23:534–43.PubMed
34.
Zurück zum Zitat O’Neill C. Evidence for the requirement of autocrine growth factors for development of mouse preimplantation embryos in vitro. Biol Reprod. 1997;56:229–37.PubMed O’Neill C. Evidence for the requirement of autocrine growth factors for development of mouse preimplantation embryos in vitro. Biol Reprod. 1997;56:229–37.PubMed
35.
Zurück zum Zitat O’Neill C. Autocrine mediators are required to act on the embryo by the 2-cell stage to promote normal development and survival of mouse preimplantation embryos in vitro. Biol Reprod. 1998;58:1303–9.PubMed O’Neill C. Autocrine mediators are required to act on the embryo by the 2-cell stage to promote normal development and survival of mouse preimplantation embryos in vitro. Biol Reprod. 1998;58:1303–9.PubMed
36.
Zurück zum Zitat Obsil T, Obsilova V. Structure/function relationships underlying regulation of FOXO transcription factors. Oncogene. 2008;27:2263–75.PubMed Obsil T, Obsilova V. Structure/function relationships underlying regulation of FOXO transcription factors. Oncogene. 2008;27:2263–75.PubMed
37.
Zurück zum Zitat Qiao L, Shao J. SIRT1 regulates adiponectin gene expression through Foxo1-C/enhancer-binding protein alpha transcriptional complex. J Biol Chem. 2006;281:39915–24.PubMed Qiao L, Shao J. SIRT1 regulates adiponectin gene expression through Foxo1-C/enhancer-binding protein alpha transcriptional complex. J Biol Chem. 2006;281:39915–24.PubMed
38.
Zurück zum Zitat Riley JK, Carayannopoulos MO, Wyman AH, Chi M, Ratajczak CK, Moley KH. The PI3K/Akt pathway is present and functional in the preimplantation mouse embryo. Dev Biol. 2005;284:377–86.PubMed Riley JK, Carayannopoulos MO, Wyman AH, Chi M, Ratajczak CK, Moley KH. The PI3K/Akt pathway is present and functional in the preimplantation mouse embryo. Dev Biol. 2005;284:377–86.PubMed
39.
Zurück zum Zitat Rodriguez R, Meuth M. Chk1 and p21 cooperate to prevent apoptosis during DNA replication fork stress. Mol Biol Cell. 2006;17:402–12.PubMedPubMedCentral Rodriguez R, Meuth M. Chk1 and p21 cooperate to prevent apoptosis during DNA replication fork stress. Mol Biol Cell. 2006;17:402–12.PubMedPubMedCentral
40.
Zurück zum Zitat Sin TK, Yung BY, Siu PM. Modulation of SIRT1-Foxo1 signaling axis by resveratrol: implications in skeletal muscle aging and insulin resistance. Cell Physiol Biochem. 2015;35:541–52.PubMed Sin TK, Yung BY, Siu PM. Modulation of SIRT1-Foxo1 signaling axis by resveratrol: implications in skeletal muscle aging and insulin resistance. Cell Physiol Biochem. 2015;35:541–52.PubMed
41.
Zurück zum Zitat Singhal R, Bard JE, Nowak NJ, Buck MJ, Kandel ES. FOXO1 regulates expression of a microRNA cluster on X chromosome. Aging (Albany NY). 2013;5:347–56. Singhal R, Bard JE, Nowak NJ, Buck MJ, Kandel ES. FOXO1 regulates expression of a microRNA cluster on X chromosome. Aging (Albany NY). 2013;5:347–56.
42.
Zurück zum Zitat Su WH, Wong EWP, Mruk DD, Cheng CY. The scribble/Lgl/Dlg polarity protein complex is a regulator of blood-testis barrier dynamics and spermatid polarity during spermatogenesis. Endocrinology. 2012;153:6041–53.PubMedPubMedCentral Su WH, Wong EWP, Mruk DD, Cheng CY. The scribble/Lgl/Dlg polarity protein complex is a regulator of blood-testis barrier dynamics and spermatid polarity during spermatogenesis. Endocrinology. 2012;153:6041–53.PubMedPubMedCentral
43.
Zurück zum Zitat Tothova Z, Kollipara R, Huntly BJ, Lee BH, Castrillon DH, Cullen DE, et al. FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell. 2007;128:325–39.PubMed Tothova Z, Kollipara R, Huntly BJ, Lee BH, Castrillon DH, Cullen DE, et al. FoxOs are critical mediators of hematopoietic stem cell resistance to physiologic oxidative stress. Cell. 2007;128:325–39.PubMed
44.
Zurück zum Zitat Tuteja G, Kaestner KH. Forkhead transcription factors II. Cell. 2007a;131:192–192.e1.PubMed Tuteja G, Kaestner KH. Forkhead transcription factors II. Cell. 2007a;131:192–192.e1.PubMed
45.
Zurück zum Zitat Tuteja G, Kaestner KH. SnapShot: forkhead transcription factors I. Cell. 2007b;130:1160.PubMed Tuteja G, Kaestner KH. SnapShot: forkhead transcription factors I. Cell. 2007b;130:1160.PubMed
46.
Zurück zum Zitat Tzivion G, Dobson M, Ramakrishnan G. FoxO transcription factors; regulation by AKT and 14-3-3 proteins. Biochim Biophys Acta. 2011;1813:1938–45.PubMed Tzivion G, Dobson M, Ramakrishnan G. FoxO transcription factors; regulation by AKT and 14-3-3 proteins. Biochim Biophys Acta. 2011;1813:1938–45.PubMed
47.
Zurück zum Zitat Urbanek P, Klotz LO. Posttranscriptional regulation of FOXO expression: microRNAs and beyond. Br J Pharmacol. 2017;174:1514–32.PubMed Urbanek P, Klotz LO. Posttranscriptional regulation of FOXO expression: microRNAs and beyond. Br J Pharmacol. 2017;174:1514–32.PubMed
48.
Zurück zum Zitat van der Horst A, Tertoolen LG, De Vries-Smits LM, Frye RA, Medema RH, Burgering BM. FOXO4 is acetylated upon peroxide stress and deacetylated by the longevity protein hSir2(SIRT1). J Biol Chem. 2004;279:28873–9.PubMed van der Horst A, Tertoolen LG, De Vries-Smits LM, Frye RA, Medema RH, Burgering BM. FOXO4 is acetylated upon peroxide stress and deacetylated by the longevity protein hSir2(SIRT1). J Biol Chem. 2004;279:28873–9.PubMed
49.
Zurück zum Zitat Wang F, Tian X, Zhang L, He C, Ji P, Li Y, et al. Beneficial effect of resveratrol on bovine oocyte maturation and subsequent embryonic development after in vitro fertilization. Fertil Steril. 2014;101:577–86.PubMed Wang F, Tian X, Zhang L, He C, Ji P, Li Y, et al. Beneficial effect of resveratrol on bovine oocyte maturation and subsequent embryonic development after in vitro fertilization. Fertil Steril. 2014;101:577–86.PubMed
50.
Zurück zum Zitat Watroba M, Maslinska D, Maslinski S. Current overview of functions of FoxO proteins, with special regards to cellular homeostasis, cell response to stress, as well as inflammation and aging. Adv Med Sci. 2012;57:183–95.PubMed Watroba M, Maslinska D, Maslinski S. Current overview of functions of FoxO proteins, with special regards to cellular homeostasis, cell response to stress, as well as inflammation and aging. Adv Med Sci. 2012;57:183–95.PubMed
51.
Zurück zum Zitat Xiong S, Salazar G, Patrushev N, Alexander RW. FoxO1 mediates an autofeedback loop regulating SIRT1 expression. J Biol Chem. 2011;286:5289–99.PubMed Xiong S, Salazar G, Patrushev N, Alexander RW. FoxO1 mediates an autofeedback loop regulating SIRT1 expression. J Biol Chem. 2011;286:5289–99.PubMed
52.
Zurück zum Zitat Xue Z, Huang K, Cai C, Cai L, Jiang CY, Feng Y, et al. Genetic programs in human and mouse early embryos revealed by single-cell RNA sequencing. Nature. 2013;500:593–7.PubMedPubMedCentral Xue Z, Huang K, Cai C, Cai L, Jiang CY, Feng Y, et al. Genetic programs in human and mouse early embryos revealed by single-cell RNA sequencing. Nature. 2013;500:593–7.PubMedPubMedCentral
53.
Zurück zum Zitat Yun JM, Chien A, Jialal I, Devaraj S. Resveratrol up-regulates SIRT1 and inhibits cellular oxidative stress in the diabetic milieu: mechanistic insights. J Nutr Biochem. 2012;23:699–705.PubMed Yun JM, Chien A, Jialal I, Devaraj S. Resveratrol up-regulates SIRT1 and inhibits cellular oxidative stress in the diabetic milieu: mechanistic insights. J Nutr Biochem. 2012;23:699–705.PubMed
54.
Zurück zum Zitat Zhao DC, Li YM, Ma JL, Yi N, Yao ZY, Li YP, et al. Single-cell RNA sequencing reveals distinct gene expression patterns in glucose metabolism of human preimplantation embryos. Reprod Fertil Dev. 2019;31:237–47.PubMed Zhao DC, Li YM, Ma JL, Yi N, Yao ZY, Li YP, et al. Single-cell RNA sequencing reveals distinct gene expression patterns in glucose metabolism of human preimplantation embryos. Reprod Fertil Dev. 2019;31:237–47.PubMed
Metadaten
Titel
FoxO transcription factors 1 regulate mouse preimplantation embryo development
verfasst von
Nilay Kuscu
Nazli Ece Gungor-Ordueri
Berna Sozen
Dileyra Adiguzel
Ciler Celik-Ozenci
Publikationsdatum
08.08.2019
Verlag
Springer US
Erschienen in
Journal of Assisted Reproduction and Genetics / Ausgabe 10/2019
Print ISSN: 1058-0468
Elektronische ISSN: 1573-7330
DOI
https://doi.org/10.1007/s10815-019-01555-1

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