Evaluating Autophagy in Preimplantation Embryos

References

• Ravanan P, Srikumar IF, Talwar P. Autophagy: The spotlight for cellular stress responses. Life Sci. 20170901st ed. 2017;188:53–67.
   PubMed Web of Science ®Google Scholar
• Song W-H, Yi Y-J, Sutovsky M, et al. Autophagy and ubiquitin-proteasome system contribute to sperm mitophagy after mammalian fertilization. Proc Natl Acad Sci U S A. 2016;113:E5261–5270.
   PubMed Web of Science ®Google Scholar
• Kuma A, Hatano M, Matsui M, et al. The role of autophagy during the early neonatal starvation period. Nature. 2004;432:1032–1036.
   PubMed Web of Science ®Google Scholar
• Zhao X, Jiang Y, Jiang T, et al. Physiological and pathological regulation of autophagy in pregnancy. Arch Gynecol Obstet. 2020;302:293–303.
   PubMed Web of Science ®Google Scholar
• Mizushima N. The pleiotropic role of autophagy: from protein metabolism to bactericide. Cell Death Differ. 2005;12 Suppl 2:1535–1541.
   PubMed Web of Science ®Google Scholar
• Ogata M, Hino S, Saito A, et al. Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol Cell Biol. 20061009th ed. 2006;26:9220–9231.
   PubMed Web of Science ®Google Scholar
• Tsukamoto S, Kuma A, Murakami M, et al. Autophagy is essential for preimplantation development of mouse embryos. Science. 2008;321:117–120.
   PubMed Web of Science ®Google Scholar
• Lee WS, Yoo WH, Chae HJ. ER Stress and Autophagy. Curr Mol Med. 2015;15:735–745.
   PubMed Web of Science ®Google Scholar
• Kamimoto T, Shoji S, Hidvegi T, et al. Intracellular inclusions containing mutant alpha1-antitrypsin Z are propagated in the absence of autophagic activity. J Biol Chem. 20051219th ed. 2006;281:4467–4476.
   PubMed Web of Science ®Google Scholar
• Ravikumar B, Vacher C, Berger Z, et al. Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat Genet. 20040516th ed. 2004;36:585–595.
   PubMed Web of Science ®Google Scholar
• Choi SE, Lee SM, Lee YJ, et al. Protective role of autophagy in palmitate-induced INS-1 beta-cell death. Endocrinology. 20080904th ed. 2009;150:126–134.
   Google Scholar
• Giordano S, Darley-Usmar V, Zhang J. Autophagy as an essential cellular antioxidant pathway in neurodegenerative disease. Redox Biol. 20131225th ed. 2013;2:82–90.
   Google Scholar
• Nakashima A, Aoki A, Kusabiraki T, et al. Role of autophagy in oocytogenesis, embryogenesis, implantation, and pathophysiology of pre-eclampsia. J Obstet Gynaecol Res. 2017;43:633–643.
   PubMed Web of Science ®Google Scholar
• Song S, Tan J, Miao Y, et al. Crosstalk of autophagy and apoptosis: Involvement of the dual role of autophagy under ER stress. J Cell Physiol. 2017;232:2977–2984.
   PubMed Web of Science ®Google Scholar
• Mizushima N. Autophagy: process and function. Genes Dev. 2007;21:2861–2873.
   PubMed Web of Science ®Google Scholar
• Saxton RA, Sabatini DM. mTOR Signaling in Growth, Metabolism, and Disease. Cell. 2017;169:361–371.
   PubMed Web of Science ®Google Scholar
• Tan SH, Shui G, Zhou J, et al. Induction of autophagy by palmitic acid via protein kinase C-mediated signaling pathway independent of mTOR (mammalian target of rapamycin). J Biol Chem. 2012;287:14364–14376.
   PubMed Web of Science ®Google Scholar
• Hiebel C, Kromm T, Stark M, et al. Cannabinoid receptor 1 modulates the autophagic flux independent of mTOR- and BECLIN1-complex. J Neurochem. 2014;131:484–497.
   PubMed Web of Science ®Google Scholar
• Yamamoto A, Mizushima N, Tsukamoto S. Fertilization-induced autophagy in mouse embryos is independent of mTORC1. Biol Reprod. 2014;91:7.
   PubMed Web of Science ®Google Scholar
• Kim J, Kundu M, Viollet B, et al. AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nat Cell Biol. 20110123rd ed. 2011;13:132–141.
   PubMed Web of Science ®Google Scholar
• Melia TJ, Lystad AH, Simonsen A. Autophagosome biogenesis: From membrane growth to closure. J Cell Biol [Internet]. 2020;219. Available from: https://www.ncbi.nlm.nih.gov/pubmed/32357219.
   PubMed Web of Science ®Google Scholar
• Cianfanelli V, De Zio D, Di Bartolomeo S, et al. Ambra1 at a glance. J Cell Sci. 2015;128:2003–2008.
   PubMed Web of Science ®Google Scholar
• Nazio F, Strappazzon F, Antonioli M, et al. mTOR inhibits autophagy by controlling ULK1 ubiquitylation, self-association and function through AMBRA1 and TRAF6. Nat Cell Biol. 20130324th ed. 2013;15:406–416.
   PubMed Web of Science ®Google Scholar
• Zhu Y, Zhao L, Liu L, et al. Beclin 1 cleavage by caspase-3 inactivates autophagy and promotes apoptosis. Protein Cell. 20100604th ed. 2010;1:468–477.
   Google Scholar
• Hill SM, Wrobel L, Rubinsztein DC. Post-translational modifications of Beclin 1 provide multiple strategies for autophagy regulation. Cell Death Differ. 20181213th ed. 2019;26:617–629.
   Google Scholar
• Noda T, Matsunaga K, Taguchi-Atarashi N, et al. Regulation of membrane biogenesis in autophagy via PI3P dynamics. Semin Cell Dev Biol. 20100418th ed. 2010;21:671–676.
   Google Scholar
• Mizushima N, Yamamoto A, Hatano M, et al. Dissection of autophagosome formation using Apg5-deficient mouse embryonic stem cells. J Cell Biol. 2001;152:657–668.
   PubMed Web of Science ®Google Scholar
• Fujita N, Itoh T, Omori H, et al. The Atg16L complex specifies the site of LC3 lipidation for membrane biogenesis in autophagy. Mol Biol Cell. 2008;19:2092–2100.
   PubMed Web of Science ®Google Scholar
• Agrotis A, Pengo N, Burden JJ, et al. Redundancy of human ATG4 protease isoforms in autophagy and LC3/GABARAP processing revealed in cells. Autophagy. 20190201st ed. 2019;15:976–997.
   Google Scholar
• Kabeya Y, Mizushima N, Ueno T, et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 2000;19:5720–5728.
   PubMed Web of Science ®Google Scholar
• Singh B, Bhaskar S. Methods for Detection of Autophagy in Mammalian Cells. Methods Mol Biol. 2019;2045:245–258.
   PubMedGoogle Scholar
• Zhou F, Wu Z, Zhao M, et al. Rab5-dependent autophagosome closure by ESCRT. J Cell Biol. 2019;218:1908–1927.
   PubMed Web of Science ®Google Scholar
• Pfitzner A-K, Mercier V, Jiang X, et al. An ESCRT-III Polymerization Sequence Drives Membrane Deformation and Fission. Cell. 2020;182:1140–1155.e18.
   PubMed Web of Science ®Google Scholar
• Lamark T, Svenning S, Johansen T. Regulation of selective autophagy: the p62/SQSTM1 paradigm. Essays Biochem. 20171212th ed. 2017;61:609–624.
   PubMed Web of Science ®Google Scholar
• Kirkin V, Lamark T, Sou YS, et al. A role for NBR1 in autophagosomal degradation of ubiquitinated substrates. Mol Cell. 2009;33:505–516.
   PubMed Web of Science ®Google Scholar
• Zhao YG, Zhang H. Autophagosome maturation: An epic journey from the ER to lysosomes. J Cell Biol. 20181221st ed. 2019;218:757–770.
   PubMed Web of Science ®Google Scholar
• Maday S, Wallace KE, Holzbaur EL. Autophagosomes initiate distally and mature during transport toward the cell soma in primary neurons. J Cell Biol. 20120213th ed. 2012;196:407–417.
   PubMed Web of Science ®Google Scholar
• Kimura S, Noda T, Yoshimori T. Dynein-dependent movement of autophagosomes mediates efficient encounters with lysosomes. Cell Struct Funct. 20080404th ed. 2008;33:109–122.
   Google Scholar
• Pankiv S, Alemu EA, Brech A, et al. FYCO1 is a Rab7 effector that binds to LC3 and PI3P to mediate microtubule plus end-directed vesicle transport. J Cell Biol. 2010;188:253–269.
   PubMed Web of Science ®Google Scholar
• Köchl R, Hu XW, Chan EY, et al. Microtubules facilitate autophagosome formation and fusion of autophagosomes with endosomes. Traffic. 2006;7:129–145.
   PubMed Web of Science ®Google Scholar
• Jordens I, Fernandez-Borja M, Marsman M, et al. The Rab7 effector protein RILP controls lysosomal transport by inducing the recruitment of dynein-dynactin motors. Curr Biol. 2001;11:1680–1685.
   PubMed Web of Science ®Google Scholar
• Razi M, Chan EY, Tooze SA. Early endosomes and endosomal coatomer are required for autophagy. J Cell Biol. 20090413th ed. 2009;185:305–321.
   PubMed Web of Science ®Google Scholar
• Ganley IG. Autophagosome maturation and lysosomal fusion. Essays Biochem. 2013;55:65–78.
   PubMed Web of Science ®Google Scholar
• Sagné C, Agulhon C, Ravassard P, et al. Identification and characterization of a lysosomal transporter for small neutral amino acids. Proc Natl Acad Sci U S A. 20010605th ed. 2001;98:7206–7211.
   PubMed Web of Science ®Google Scholar
• Shi L, Wu J. Epigenetic regulation in mammalian preimplantation embryo development. Reprod Biol Endocrinol. 20090605th ed. 2009;7:59.
   Google Scholar
• Leung ZCL, Abu Rafea B, Watson AJ, et al. Free fatty acid treatment of mouse preimplantation embryos demonstrates contrasting effects of palmitic acid and oleic acid on autophagy. Am J Physiol Cell Physiol. 2022;
   Web of Science ®Google Scholar
• Ekizceli G, Inan S, Oktem G, et al. Assessment of mTOR pathway molecules during implantation in rats. Biotech Histochem. 20170831st ed. 2017;92:450–458.
   PubMed Web of Science ®Google Scholar
• Lee SE, Hwang KC, Sun SC, et al. Modulation of autophagy influences development and apoptosis in mouse embryos developing in vitro. Mol Reprod Dev. 20110616th ed. 2011;78:498–509.
   Google Scholar
• Sharma K, Asp NT, Harrison SP, et al. Autophagy modulates cell fate decisions during lineage commitment. Autophagy. 2021;1–17.
   PubMed Web of Science ®Google Scholar
• Puscheck EE, Awonuga AO, Yang Y, et al. Molecular biology of the stress response in the early embryo and its stem cells. Adv Exp Med Biol. 2015;843:77–128.
   PubMed Web of Science ®Google Scholar
• Dumollard R, Ward Z, Carroll J, et al. Regulation of redox metabolism in the mouse oocyte and embryo. Development. 20061221st ed. 2007;134:455–465.
   Google Scholar
• Bradley J, Swann K. Mitochondria and lipid metabolism in mammalian oocytes and early embryos. Int J Dev Biol. 2019;63:93–103.
   PubMed Web of Science ®Google Scholar
• Leese HJ, Barton AM. Pyruvate and glucose uptake by mouse ova and preimplantation embryos. J Reprod Fertil. 1984;72:9–13.
   PubMedGoogle Scholar
• Leese HJ, Guerif F, Allgar V, et al. Biological optimization, the Goldilocks principle, and how much is lagom in the preimplantation embryo. Mol Reprod Dev. 2016;83:748–754.
   PubMed Web of Science ®Google Scholar
• Leese HJ. Quiet please, do not disturb: a hypothesis of embryo metabolism and viability. Bioessays. 2002;24:845–849.
   PubMed Web of Science ®Google Scholar
• Robker RL, Akison LK, Bennett BD, et al. Obese women exhibit differences in ovarian metabolites, hormones, and gene expression compared with moderate-weight women. J Clin Endocrinol Metab. 20090217th ed. 2009;94:1533–1540.
   PubMed Web of Science ®Google Scholar
• Igosheva N, Abramov AY, Poston L, et al. Maternal diet-induced obesity alters mitochondrial activity and redox status in mouse oocytes and zygotes. PLoS One. 20100409th ed. 2010;5:e10074.
   Google Scholar
• Wu LL, Dunning KR, Yang X, et al. High-fat diet causes lipotoxicity responses in cumulus-oocyte complexes and decreased fertilization rates. Endocrinology. 20100922nd ed. 2010;151:5438–5445.
   Google Scholar
• Yousif MD, Calder MD, Du JT, et al. Oleic Acid Counters Impaired Blastocyst Development Induced by Palmitic Acid During Mouse Preimplantation Development: Understanding Obesity-Related Declines in Fertility. Reprod Sci. 20200615th ed. 2020;27:2038–2051.
   PubMed Web of Science ®Google Scholar
• Pasquier B. Autophagy inhibitors. Cell Mol Life Sci. 2016;73:985–1001.
   PubMed Web of Science ®Google Scholar
• Wu Y-T, Tan H-L, Shui G, et al. Dual role of 3-methyladenine in modulation of autophagy via different temporal patterns of inhibition on class I and III phosphoinositide 3-kinase. J Biol Chem. 2010;285:10850–10861.
   PubMed Web of Science ®Google Scholar
• Caro LH, Plomp PJ, Wolvetang EJ, et al. 3-Methyladenine, an inhibitor of autophagy, has multiple effects on metabolism. Eur J Biochem. 1988;175:325–329.
   PubMedGoogle Scholar
• Petherick KJ, Conway OJL, Mpamhanga C, et al. Pharmacological inhibition of ULK1 kinase blocks mammalian target of rapamycin (mTOR)-dependent autophagy. J Biol Chem. 2015;290:11376–11383.
   PubMed Web of Science ®Google Scholar
• Bago R, Malik N, Munson MJ, et al. Characterization of VPS34-IN1, a selective inhibitor of Vps34, reveals that the phosphatidylinositol 3-phosphate-binding SGK3 protein kinase is a downstream target of class III phosphoinositide 3-kinase. Biochem J. 2014;463:413–427.
   PubMed Web of Science ®Google Scholar
• Klionsky DJ, Elazar Z, Seglen PO, et al. Does bafilomycin A1 block the fusion of autophagosomes with lysosomes? Autophagy. 2008;4:849–850.
   PubMed Web of Science ®Google Scholar
• Mauthe M, Orhon I, Rocchi C, et al. Chloroquine inhibits autophagic flux by decreasing autophagosome-lysosome fusion. Autophagy. 20180720th ed. 2018;14:1435–1455.
   Google Scholar
• Florey O, Gammoh N, Kim SE, et al. V-ATPase and osmotic imbalances activate endolysosomal LC3 lipidation. Autophagy. 2015;11:88–99.
   PubMed Web of Science ®Google Scholar
• Galluzzi L, Green DR. Autophagy-Independent Functions of the Autophagy Machinery. Cell. 2019;177:1682–1699.
   PubMed Web of Science ®Google Scholar
• Kuijk EW, du Puy L, van Tol HTA, et al. Validation of reference genes for quantitative RT-PCR studies in porcine oocytes and preimplantation embryos. BMC Dev Biol. 2007;7:58.
   PubMed Web of Science ®Google Scholar
• Nascimento PS, Moura MT, Silva RLO, et al. Housekeeping genes for RT-qPCR in ovine preimplantation embryos. Zygote. 2020;1–8.
   PubMed Web of Science ®Google Scholar
• Mamo S, Gal AB, Bodo S, et al. Quantitative evaluation and selection of reference genes in mouse oocytes and embryos cultured in vivo and in vitro. BMC Dev Biol. 2007;7:14.
   PubMed Web of Science ®Google Scholar
• Song S, Guo Q, Zhu Y, et al. Exploring the role of autophagy during early human embryonic development through single-cell transcriptome and methylome analyses. Sci China Life Sci. 2021;
   Google Scholar
• Adil A, Kumar V, Jan AT, et al. Single-Cell Transcriptomics: Current Methods and Challenges in Data Acquisition and Analysis. Front Neurosci. 2021;15:591122.
   PubMed Web of Science ®Google Scholar
• Iyer S, Mukherjee S, Kumar M. Watching the embryo: Evolution of the microscope for the study of embryogenesis. Bioessays. 2021;43:e2000238.
   PubMed Web of Science ®Google Scholar
• Klionsky DJ, Eskelinen E-L. The vacuole versus the lysosome: when size matters. Autophagy. 2014;10:185–187.
   PubMed Web of Science ®Google Scholar
• Swaim WD. Overview of confocal microscopy. Methods Mol Biol. 2010;588:187–201.
   PubMedGoogle Scholar
• Mullins JM. Fluorochromes: properties and characteristics. Methods Mol Biol. 2010;588:123–134.
   PubMedGoogle Scholar
• Klionsky DJ, Abdelmohsen K, Abe A, et al. Guidelines for the use and interpretation of assays for monitoring autophagy ( 3rd edition). Autophagy. 2016;12:1–222.
   PubMed Web of Science ®Google Scholar
• Lou X, Kang M, Xenopoulos P, et al. A rapid and efficient 2D/3D nuclear segmentation method for analysis of early mouse embryo and stem cell image data. Stem Cell Reports. 2014;2:382–397.
   PubMed Web of Science ®Google Scholar
• Bass JJ, Wilkinson DJ, Rankin D, et al. An overview of technical considerations for Western blotting applications to physiological research. Scand J Med Sci Sports. 2017;27:4–25.
   PubMed Web of Science ®Google Scholar
• Fear JM, Hansen PJ. Developmental changes in expression of genes involved in regulation of apoptosis in the bovine preimplantation embryo. Biol Reprod. 2011;84:43–51.
   PubMed Web of Science ®Google Scholar
• Zamfirescu RC, Day ML, Morris MB. mTORC1/2 signaling is downregulated by amino acid-free culture of mouse preimplantation embryos and is only partially restored by amino acid readdition. Am J Physiol Cell Physiol. 2021;320:C30–C44.
   PubMed Web of Science ®Google Scholar
• Tsukamoto S, Hara T, Yamamoto A, et al. Fluorescence-based visualization of autophagic activity predicts mouse embryo viability. Sci Rep. 2014;4:4533.
   PubMed Web of Science ®Google Scholar
• Kaizuka T, Morishita H, Hama Y, et al. An Autophagic Flux Probe that Releases an Internal Control. Mol Cell. 2016;64:835–849.
   PubMed Web of Science ®Google Scholar
• Mizushima N, Yamamoto A, Matsui M, et al. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol Biol Cell. 2004;15:1101–1111.
   PubMed Web of Science ®Google Scholar
• Vazin T, Freed WJ. Human embryonic stem cells: derivation, culture, and differentiation: a review. Restor Neurol Neurosci. 2010;28:589–603.
   PubMed Web of Science ®Google Scholar
• Oda M, Shiota K, Tanaka S. Trophoblast stem cells. Methods Enzymol. 2006;419:387–400.
   PubMed Web of Science ®Google Scholar
• Yan L, Yang M, Guo H, et al. Single-cell RNA-Seq profiling of human preimplantation embryos and embryonic stem cells. Nat Struct Mol Biol. 2013;20:1131–1139.
   PubMed Web of Science ®Google Scholar
• Kaminskyy V, Abdi A, Zhivotovsky B. A quantitative assay for the monitoring of autophagosome accumulation in different phases of the cell cycle. Autophagy. 2011;7:83–90.
   PubMed Web of Science ®Google Scholar
• Pugsley HR. Quantifying autophagy: Measuring LC3 puncta and autolysosome formation in cells using multispectral imaging flow cytometry. Methods. 2017;112:147–156.
   PubMed Web of Science ®Google Scholar
• Mauro-Lizcano M, Esteban-Martínez L, Seco E, et al. New method to assess mitophagy flux by flow cytometry. Autophagy. 2015;11:833–843.
   PubMed Web of Science ®Google Scholar
• Tra T, Gong L, Kao L-P, et al. Autophagy in human embryonic stem cells. PLoS One. 2011;6:e27485.
   PubMed Web of Science ®Google Scholar
• Song BS, Yoon SB, Kim JS, et al. Induction of autophagy promotes preattachment development of bovine embryos by reducing endoplasmic reticulum stress. Biol Reprod. 20120701st ed. 2012;87(8):1–11.
   Google Scholar