Epiblast fragmentation by shedding-a novel mechanism to eliminate cells in post-implantation mouse embryos.
Journal
Cell death and differentiation
ISSN: 1476-5403
Titre abrégé: Cell Death Differ
Pays: England
ID NLM: 9437445
Informations de publication
Date de publication:
06 2022
06 2022
Historique:
received:
16
08
2021
accepted:
26
11
2021
revised:
24
11
2021
pubmed:
8
1
2022
medline:
11
6
2022
entrez:
7
1
2022
Statut:
ppublish
Résumé
The role of programmed cell death during embryonic development has been described previously, but its specific contribution to peri- and post-implantation stages is still debatable. Here, we used transmission electron microscopy and immunostaining of E5.5-7.5 mouse embryos to investigate death processes during these stages of development. We report that in addition to canonical apoptosis observed in E5.5-E7.5 embryos, a novel type of cell elimination occurs in E7.5 embryos among the epiblasts at the apical side, in which cells shed membrane-enclosed fragments of cytosol and organelles into the lumen, leaving behind small, enucleated cell remnants at the apical surface. This process is caspase-independent as it occurred in Apaf1 knockout embryos. We suggest that this novel mechanism controls epiblast cell numbers. Altogether, this work documents the activation of two distinct programs driving irreversible terminal states of epiblast cells in the post-implantation mouse embryo.
Identifiants
pubmed: 34992231
doi: 10.1038/s41418-021-00918-5
pii: 10.1038/s41418-021-00918-5
pmc: PMC9177684
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1255-1266Informations de copyright
© 2021. The Author(s), under exclusive licence to ADMC Associazione Differenziamento e Morte Cellulare.
Références
Zakeri Z, Penaloza CG, Smith K, Ye Y, Lockshin RA. What cell death does in development. Int J Devel Biol. 2015;59:11–22.
doi: 10.1387/ijdb.150220zz
Hernández‐Martínez R, Covarrubias L. Interdigital cell death function and regulation: new insights on an old programmed cell death model. Dev Growth Differ. 2011;53:245–58.
pubmed: 21338350
doi: 10.1111/j.1440-169X.2010.01246.x
Suzanne M, Steller H. Shaping organisms with apoptosis. Cell Death Diff. 2013;20:669–75.
doi: 10.1038/cdd.2013.11
Manjón C, Sánchez-Herrero E, Suzanne M. Sharp boundaries of dpp signalling trigger local cell death required for drosophila leg morphogenesis. Nat Cell Biol. 2007;9:57–63.
pubmed: 17143268
doi: 10.1038/ncb1518
Kuan C-Y, Roth KA, Flavell RA, Rakic P. Mechanisms of programmed cell death in the developing brain. Trends Neurosci. 2000;23:291–7.
pubmed: 10856938
doi: 10.1016/S0166-2236(00)01581-2
Brison DR, Schultz RM. Apoptosis during mouse blastocyst formation: evidence for a role for survival factors including transforming growth factor α. Biol Reprod. 1997;56:1088–96.
pubmed: 9160705
doi: 10.1095/biolreprod56.5.1088
El-Shershaby A, Hinchliffe J. Cell redundancy in the zona-intact preimplantation mouse blastocyst: a light and electron microscope study of dead cells and their fate. Development. 1974;31:643–54.
doi: 10.1242/dev.31.3.643
Morris SA, Teo RT, Li H, Robson P, Glover DM, Zernicka-Goetz M. Origin and formation of the first two distinct cell types of the inner cell mass in the mouse embryo. Proc Natl Acad Sci USA. 2010;107:6364–9.
pubmed: 20308546
pmcid: 2852013
doi: 10.1073/pnas.0915063107
Byrne A, Southgate J, Brison D, Leese H. Analysis of apoptosis in the preimplantation bovine embryo using tunel. Reproduction. 1999;117:97–105.
doi: 10.1530/jrf.0.1170097
Coucouvanis E, Martin GR. Signals for death and survival: a two-step mechanism for cavitation in the vertebrate embryo. Cell. 1995;83:279–87.
pubmed: 7585945
doi: 10.1016/0092-8674(95)90169-8
Coucouvanis E, Martin GR. Bmp signaling plays a role in visceral endoderm differentiation and cavitation in the early mouse embryo. Development. 1999;126:535–46.
pubmed: 9876182
doi: 10.1242/dev.126.3.535
Abud HE. Shaping developing tissues by apoptosis. Cell Death Differ. 2004;11:797.
pubmed: 15167902
doi: 10.1038/sj.cdd.4401455
Bedzhov I, Zernicka-Goetz M. Self-organizing properties of mouse pluripotent cells initiate morphogenesis upon implantation. Cell. 2014;156:1032–44.
pubmed: 24529478
pmcid: 3991392
doi: 10.1016/j.cell.2014.01.023
Kim YS, Fan R, Kremer L, Kuempel-Rink N, Mildner K, Zeuschner D, et al. Deciphering epiblast lumenogenesis reveals proamniotic cavity control of embryo growth and patterning. Sci Adv. 2021;7:eabe1640.
pubmed: 33692105
pmcid: 7946377
doi: 10.1126/sciadv.abe1640
Singla S, Iwamoto-Stohl LK, Zhu M, Zernicka-Goetz M. Autophagy-mediated apoptosis eliminates aneuploid cells in a mouse model of chromosome mosaicism. Nat Commun. 2020;11:1–15.
doi: 10.1038/s41467-020-16796-3
Molè MA, Weberling A, Fässler R, Campbell A, Fishel S, Zernicka-Goetz M. Integrin β1 coordinates survival and morphogenesis of the embryonic lineage upon implantation and pluripotency transition. Cell Rep. 2021;34:108834.
pubmed: 33691117
pmcid: 7966855
doi: 10.1016/j.celrep.2021.108834
Snow MH. Cell death in embryonic development. Perspectives on mammalian cell death. Oxford University Press, Oxford; 1987. p. 202–28.
Gardner R, Cockroft D. Complete dissipation of coherent clonal growth occurs before gastrulation in mouse epiblast. Development. 1998;125:2397–402.
pubmed: 9609822
doi: 10.1242/dev.125.13.2397
O’Farrell PH, Stumpff J, Su TT. Embryonic cleavage cycles: how is a mouse like a fly? Curr Biol. 2004;14:R35–R45.
pubmed: 14711435
pmcid: 2712630
doi: 10.1016/j.cub.2003.12.022
Streffer C, Beuningen DV, Molls M, Zamboglou N, Schulz S. Kinetics of cell proliferation in the pre‐implanted mouse embryo in vivo and in vitro. Cell Prolif. 1980;13:135–43.
doi: 10.1111/j.1365-2184.1980.tb00456.x
Poelmann R. Differential mitosis and degeneration patterns in relation to the alterations in the shape of the embryonic ectoderm of early post-implantation mouse embryos. Development. 1980;55:33–51.
doi: 10.1242/dev.55.1.33
Pereira PN, Dobreva MP, Graham L, Huylebroeck D, Lawson KA, Zwijsen A. Amnion formation in the mouse embryo: the single amniochorionic fold model. BMC Dev Biol. 2011;11:48.
pubmed: 21806820
pmcid: 3163621
doi: 10.1186/1471-213X-11-48
Tam P, Beddington R. Establishment and organization of germ layers in the gastrulating mouse embryo. In: Derek J Chadwick JM, editor. Postimplantation development in the mouse: Ciba foundation symposium 165. Wiley: Chichester; 1992. p. 27–49.
Manova K, Tomihara‐Newberger C, Wang S, Godelman A, Kalantry S, Witty‐Blease K, et al. Apoptosis in mouse embryos: elevated levels in pregastrulae and in the distal anterior region of gastrulae of normal and mutant mice. Dev Dyn. 1998;213:293–308.
pubmed: 9825865
doi: 10.1002/(SICI)1097-0177(199811)213:3<293::AID-AJA6>3.0.CO;2-D
Sanders E, Torkkeli P, French A. Patterns of cell death during gastrulation in chick and mouse embryos. Anat Embryol. 1997;195:147–54.
doi: 10.1007/s004290050033
Los M, Wesselborg S, Schulze-Osthoff K. The role of caspases in development, immunity, and apoptotic signal transduction: lessons from knockout mice. Immunity. 1999;10:629–39.
pubmed: 10403638
doi: 10.1016/S1074-7613(00)80062-X
Lee SC, Chan J, Clement MV, Pervaiz S. Functional proteomics of resveratrol‐induced colon cancer cell apoptosis: caspase‐6‐mediated cleavage of lamin a is a major signaling loop. Proteomics. 2006;6:2386–94.
pubmed: 16518869
doi: 10.1002/pmic.200500366
Menon V, Ghaffari S. Erythroid enucleation: a gateway into a “bloody” world. Exp Hematol. 2021;95:13–22.
pubmed: 33440185
pmcid: 8147720
doi: 10.1016/j.exphem.2021.01.001
Yoshida H, Kong Y-Y, Yoshida R, Elia AJ, Hakem A, Hakem R, et al. Apaf1 is required for mitochondrial pathways of apoptosis and brain development. Cell. 1998;94:739–50.
pubmed: 9753321
doi: 10.1016/S0092-8674(00)81733-X
Nagasaka A, Kawane K, Yoshida H, Nagata S. Apaf-1-independent programmed cell death in mouse development. Cell Death Diff. 2010;17:931–41.
doi: 10.1038/cdd.2009.186
Yuan J, Kroemer G. Alternative cell death mechanisms in development and beyond. Genes Dev. 2010;24:2592–602.
pubmed: 21123646
pmcid: 2994033
doi: 10.1101/gad.1984410
Cocucci E, Meldolesi J. Ectosomes and exosomes: shedding the confusion between extracellular vesicles. Trends Cell Biol. 2015;25:364–72.
pubmed: 25683921
doi: 10.1016/j.tcb.2015.01.004
Williams J, Duckworth C, Burkitt M, Watson A, Campbell B, Pritchard D. Epithelial cell shedding and barrier function: a matter of life and death at the small intestinal villus tip. Vet Pathol. 2015;52:445–55.
pubmed: 25428410
pmcid: 4441880
doi: 10.1177/0300985814559404
Bullen TF, Forrest S, Campbell F, Dodson AR, Hershman MJ, Pritchard DM, et al. Characterization of epithelial cell shedding from human small intestine. Lab Invest. 2006;86:1052.
pubmed: 16909128
doi: 10.1038/labinvest.3700464
Gudipaty SA, Rosenblatt J. Epithelial cell extrusion: pathways and pathologies. Semin Cell Dev Biol. 2017;67:132–40.
pubmed: 27212253
doi: 10.1016/j.semcdb.2016.05.010
Farkaš R. The complex secretions of the salivary glands of drosophila melanogaster, a model system. In: Cohen E. MB, (ed). Extracellular composite matrices in arthropods. Cham: Springer; 2016. p. 557–600.
doi: 10.1007/978-3-319-40740-1_15
Farkaš R, Ďatková Z, Mentelova L, Löw P, Beňová-Liszeková D, Beňo M, et al. Apocrine secretion in drosophila salivary glands: Subcellular origin, dynamics, and identification of secretory proteins. PloS ONE. 2014;9:e94383.
pubmed: 24732043
pmcid: 3986406
doi: 10.1371/journal.pone.0094383
Basilicata MF, Frank M, Solter D, Brabletz T, Stemmler MP. Inappropriate cadherin switching in the mouse epiblast compromises proper signaling between the epiblast and the extraembryonic ectoderm during gastrulation. Sci Rep. 2016;6:1–15.
doi: 10.1038/srep26562
Mathiah N, Despin‐Guitard E, Stower M, Nahaboo W, Eski ES, Singh SP, et al. Asymmetry in the frequency and position of mitosis in the mouse embryo epiblast at gastrulation. EMBO Rep. 2020;21:e50944.
Ichikawa T, Nakazato K, Keller PJ, Kajiura-Kobayashi H, Stelzer EH, Mochizuki A, et al. Live imaging of whole mouse embryos during gastrulation: migration analyses of epiblast and mesodermal cells. PLoS ONE. 2013;8:e64506.
pubmed: 23861733
pmcid: 3704669
doi: 10.1371/journal.pone.0064506