A monoastral mitotic spindle determines lineage fate and position in the mouse embryo.


Journal

Nature cell biology
ISSN: 1476-4679
Titre abrégé: Nat Cell Biol
Pays: England
ID NLM: 100890575

Informations de publication

Date de publication:
02 2022
Historique:
received: 05 02 2021
accepted: 30 11 2021
pubmed: 2 2 2022
medline: 1 3 2022
entrez: 1 2 2022
Statut: ppublish

Résumé

During mammalian development, the first asymmetric cell divisions segregate cells into inner and outer positions of the embryo to establish the pluripotent and trophectoderm lineages. Typically, polarity components differentially regulate the mitotic spindle via astral microtubule arrays to trigger asymmetric division patterns. However, early mouse embryos lack centrosomes, the microtubule-organizing centres (MTOCs) that usually generate microtubule asters. Thus, it remains unknown whether spindle organization regulates lineage segregation. Here we find that heterogeneities in cell polarity in the early 8-cell-stage mouse embryo trigger the assembly of a highly asymmetric spindle organization. This spindle arises in an unusual modular manner, forming a single microtubule aster from an apically localized, non-centrosomal MTOC, before joining it to the rest of the spindle apparatus. When fully assembled, this 'monoastral' spindle triggers spatially asymmetric division patterns to segregate cells into inner and outer positions. Moreover, the asymmetric inheritance of spindle components causes differential cell polarization to determine pluripotent versus trophectoderm lineage fate.

Identifiants

pubmed: 35102267
doi: 10.1038/s41556-021-00826-3
pii: 10.1038/s41556-021-00826-3
doi:

Substances chimiques

Cell Cycle Proteins 0
Microtubule-Associated Proteins 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Video-Audio Media

Langues

eng

Sous-ensembles de citation

IM

Pagination

155-167

Subventions

Organisme : NICHD NIH HHS
ID : R01 HD102013
Pays : United States

Informations de copyright

© 2022. The Author(s), under exclusive licence to Springer Nature Limited.

Références

Knoblich, J. A. Asymmetric cell division: recent developments and their implications for tumour biology. Nat. Rev. Mol. Cell Biol. 11, 849–860 (2010).
pubmed: 21102610 pmcid: 3941022 doi: 10.1038/nrm3010
Johnson, M. H. & Ziomek, C. A. The foundation of two distinct cell lineages within the mouse morula. Cell 24, 71–80 (1981).
pubmed: 7237545 doi: 10.1016/0092-8674(81)90502-X
Samarage, C. R. et al. Cortical tension allocates the first inner cells of the mammalian embryo. Dev. Cell 34, 435–447 (2015).
pubmed: 26279486 doi: 10.1016/j.devcel.2015.07.004
Johnson, M. H. & Ziomek, C. A. Induction of polarity in mouse 8-cell blastomeres: specificity, geometry, and stability. J. Cell Biol. 91, 303–308 (1981).
pubmed: 7298724 doi: 10.1083/jcb.91.1.303
Nishioka, N. et al. The Hippo signaling pathway components Lats and Yap pattern Tead4 activity to distinguish mouse trophectoderm from inner cell mass. Dev. Cell 16, 398–410 (2009).
pubmed: 19289085 doi: 10.1016/j.devcel.2009.02.003
Hirate, Y. et al. Polarity-dependent distribution of angiomotin localizes Hippo signaling in preimplantation embryos. Curr. Biol. 23, 1181–1194 (2013).
pubmed: 23791731 pmcid: 3742369 doi: 10.1016/j.cub.2013.05.014
Leung, C. Y. & Zernicka-Goetz, M. Angiomotin prevents pluripotent lineage differentiation in mouse embryos via Hippo pathway-dependent and -independent mechanisms. Nat. Commun. 4, 2251 (2013).
pubmed: 23903990 doi: 10.1038/ncomms3251
Cockburn, K., Biechele, S., Garner, J. & Rossant, J. The Hippo pathway member Nf2 is required for inner cell mass specification. Curr. Biol. 23, 1195–1201 (2013).
pubmed: 23791728 doi: 10.1016/j.cub.2013.05.044
Lim, H. Y. G. & Plachta, N. Cytoskeletal control of early mammalian development. Nat. Rev. Mol. Cell Biol. 22, 548–562 (2021).
pubmed: 33927361 doi: 10.1038/s41580-021-00363-9
Watanabe, T., Biggins, J., Tannan, N. & Srinivas, S. Limited predictive value of blastomere angle of division in trophectoderm and inner cell mass specification. Development 141, 2279–2288 (2014).
pubmed: 24866117 pmcid: 4034423 doi: 10.1242/dev.103267
Maitre, J. L. et al. Asymmetric division of contractile domains couples cell positioning and fate specification. Nature 536, 344–348 (2016).
pubmed: 27487217 pmcid: 4998956 doi: 10.1038/nature18958
Niwayama, R. et al. A tug-of-war between cell shape and polarity controls division orientation to ensure robust patterning in the mouse blastocyst. Dev. Cell 51, 564–574.e6 (2019).
pubmed: 31735668 pmcid: 6892278 doi: 10.1016/j.devcel.2019.10.012
White, M. D. et al. Long-lived binding of Sox2 to DNA predicts cell fate in the four-cell mouse embryo. Cell 165, 75–87 (2016).
pubmed: 27015308 doi: 10.1016/j.cell.2016.02.032
Torres-Padilla, M. E., Parfitt, D. E., Kouzarides, T. & Zernicka-Goetz, M. Histone arginine methylation regulates pluripotency in the early mouse embryo. Nature 445, 214–218 (2007).
pubmed: 17215844 pmcid: 3353120 doi: 10.1038/nature05458
Tabansky, I. et al. Developmental bias in cleavage-stage mouse blastomeres. Curr. Biol. 23, 21–31 (2013).
pubmed: 23177476 doi: 10.1016/j.cub.2012.10.054
Goolam, M. et al. Heterogeneity in Oct4 and Sox2 targets biases cell fate in 4-cell mouse embryos. Cell 165, 61–74 (2016).
pubmed: 27015307 pmcid: 4819611 doi: 10.1016/j.cell.2016.01.047
Wang, J. et al. Asymmetric expression of LincGET biases in two-cell mouse embryos. Cell 175, 1887–1901.e18 (2018).
pubmed: 30550787 doi: 10.1016/j.cell.2018.11.039
Casser, E. et al. Totipotency segregates between the sister blastomeres of two-cell stage mouse embryos. Sci. Rep. 7, 8299 (2017).
pubmed: 28811525 pmcid: 5557898 doi: 10.1038/s41598-017-08266-6
Grill, S. W. & Hyman, A. A. Spindle positioning by cortical pulling forces. Dev. Cell 8, 461–465 (2005).
pubmed: 15809029 doi: 10.1016/j.devcel.2005.03.014
Gueth-Hallonet, C. et al. γ-Tubulin is present in acentriolar MTOCs during early mouse development. J. Cell Sci. 105, 157–166 (1993).
pubmed: 8360270 doi: 10.1242/jcs.105.1.157
Clift, D. & Schuh, M. A three-step MTOC fragmentation mechanism facilitates bipolar spindle assembly in mouse oocytes. Nat. Commun. 6, 7217 (2015).
pubmed: 26147444 doi: 10.1038/ncomms8217
Schatten, G., Simerly, C. & Schatten, H. Microtubule configurations during fertilization, mitosis, and early development in the mouse and the requirement for egg microtubule-mediated motility during mammalian fertilization. Proc. Natl Acad. Sci. USA 82, 4152–4156 (1985).
pubmed: 3889922 pmcid: 397953 doi: 10.1073/pnas.82.12.4152
Howe, K. & FitzHarris, G. A non-canonical mode of microtubule organization operates throughout pre-implantation development in mouse. Cell Cycle 12, 1616–1624 (2013).
pubmed: 23624836 pmcid: 3680541 doi: 10.4161/cc.24755
Korotkevich, E. et al. The apical domain is required and sufficient for the first lineage segregation in the mouse embryo. Dev. Cell 40, 235–247.e7 (2017).
pubmed: 28171747 pmcid: 5300053 doi: 10.1016/j.devcel.2017.01.006
Lim, H. Y. G. et al. Keratins are asymmetrically inherited fate determinants in the mammalian embryo. Nature 585, 404–409 (2020).
pubmed: 32848249 doi: 10.1038/s41586-020-2647-4
Zenker, J. et al. Expanding actin rings zipper the mouse embryo for blastocyst formation.Cell 173, 776–791.e17 (2018).
pubmed: 29576449 doi: 10.1016/j.cell.2018.02.035
Tolic, I. M. Mitotic spindle: kinetochore fibers hold on tight to interpolar bundles. Eur. Biophys. J. 47, 191–203 (2018).
pubmed: 28725997 doi: 10.1007/s00249-017-1244-4
Colicino, E. G. & Hehnly, H. Regulating a key mitotic regulator, polo-like kinase 1 (PLK1). Cytoskeleton 75, 481–494 (2018).
pubmed: 30414309 doi: 10.1002/cm.21504
Zenker, J. et al. A microtubule-organizing center directing intracellular transport in the early mouse embryo. Science 357, 925–928 (2017).
pubmed: 28860385 doi: 10.1126/science.aam9335
Choi, Y. K., Liu, P., Sze, S. K., Dai, C. & Qi, R. Z. CDK5RAP2 stimulates microtubule nucleation by the gamma-tubulin ring complex. J. Cell Biol. 191, 1089–1095 (2010).
pubmed: 21135143 pmcid: 3002024 doi: 10.1083/jcb.201007030
Schulze, E., Asai, D. J., Bulinski, J. C. & Kirschner, M. Posttranslational modification and microtubule stability. J. Cell Biol. 105, 2167–2177 (1987).
pubmed: 3316248 doi: 10.1083/jcb.105.5.2167
Dudka, D., Castrogiovanni, C., Liaudet, N., Vassal, H. & Meraldi, P. Spindle-length-dependent HURP localization allows centrosomes to control kinetochore–fiber plus-end dynamics. Curr. Biol. 29, 3563–3578.e6 (2019).
pubmed: 31668617 doi: 10.1016/j.cub.2019.08.061
Morris, S. A. et al. Origin and formation of the first two distinct cell types of the inner cell mass in the mouse embryo. Proc. Natl Acad. Sci. USA 107, 6364–6369 (2010).
pubmed: 20308546 pmcid: 2852013 doi: 10.1073/pnas.0915063107
Rappaport, R. Cytokinesis in animal cells. Int. Rev. Cytol. 31, 169–213 (1971).
pubmed: 4400359 doi: 10.1016/S0074-7696(08)60059-5
Saias, L. et al. Decrease in cell volume generates contractile forces driving dorsal closure. Dev. Cell 33, 611–621 (2015).
pubmed: 25982674 doi: 10.1016/j.devcel.2015.03.016
Lu, L. Y. et al. Polo-like kinase 1 is essential for early embryonic development and tumor suppression. Mol. Cell. Biol. 28, 6870–6876 (2008).
pubmed: 18794363 pmcid: 2573299 doi: 10.1128/MCB.00392-08
Jang, Y. J., Ma, S., Terada, Y. & Erikson, R. L. Phosphorylation of threonine 210 and the role of serine 137 in the regulation of mammalian polo-like kinase. J. Biol. Chem. 277, 44115–44120 (2002).
pubmed: 12207013 doi: 10.1074/jbc.M202172200
McNally, F. J. & Vale, R. D. Identification of katanin, an ATPase that severs and disassembles stable microtubules. Cell 75, 419–429 (1993).
pubmed: 8221885 doi: 10.1016/0092-8674(93)90377-3
Anani, S., Bhat, S., Honma-Yamanaka, N., Krawchuk, D. & Yamanaka, Y. Initiation of Hippo signaling is linked to polarity rather than to cell position in the pre-implantation mouse embryo. Development 141, 2813–2824 (2014).
pubmed: 24948601 doi: 10.1242/dev.107276
Feldman, J. L. & Priess, J. R. A role for the centrosome and PAR-3 in the hand-off of MTOC function during epithelial polarization. Curr. Biol. 22, 575–582 (2012).
pubmed: 22425160 pmcid: 3409831 doi: 10.1016/j.cub.2012.02.044
Alarcon, V. B. Cell polarity regulator PARD6B is essential for trophectoderm formation in the preimplantation mouse embryo. Biol. Reprod. 83, 347–358 (2010).
pubmed: 20505164 pmcid: 2924801 doi: 10.1095/biolreprod.110.084400
Gard, D. L. Microtubule organization during maturation of Xenopus oocytes: assembly and rotation of the meiotic spindles. Dev. Biol. 151, 516–530 (1992).
pubmed: 1601183 doi: 10.1016/0012-1606(92)90190-R
Schuh, M. & Ellenberg, J. Self-organization of MTOCs replaces centrosome function during acentrosomal spindle assembly in live mouse oocytes. Cell 130, 484–498 (2007).
pubmed: 17693257 doi: 10.1016/j.cell.2007.06.025
Mayer, T. U. et al. Small molecule inhibitor of mitotic spindle bipolarity identified in a phenotype-based screen. Science 286, 971–974 (1999).
pubmed: 10542155 doi: 10.1126/science.286.5441.971
Ishii, R. & Shimizu, T. Equalization of unequal first cleavage in the Tubifex egg by introduction of an additional centrosome: implications for the absence of cortical mechanisms for mitotic spindle asymmetry. Dev. Biol. 189, 49–56 (1997).
pubmed: 9281336 doi: 10.1006/dbio.1997.8653
Ren, X. & Weisblat, D. A. Asymmetrization of first cleavage by transient disassembly of one spindle pole aster in the leech Helobdella robusta. Dev. Biol. 292, 103–115 (2006).
pubmed: 16458880 doi: 10.1016/j.ydbio.2005.12.049
Bergstralh, D. T., Dawney, N. S. & St Johnston, D. Spindle orientation: a question of complex positioning. Development 144, 1137–1145 (2017).
pubmed: 28351864 doi: 10.1242/dev.140764
Bornens, M. Centrosome composition and microtubule anchoring mechanisms. Curr. Opin. Cell Biol. 14, 25–34 (2002).
pubmed: 11792541 doi: 10.1016/S0955-0674(01)00290-3
Panamarova, M. et al. The BAF chromatin remodelling complex is an epigenetic regulator of lineage specification in the early mouse embryo. Development 143, 1271–1283 (2016).
pubmed: 26952987 pmcid: 4852518
Coelho, P. A. et al. Spindle formation in the mouse embryo requires Plk4 in the absence of centrioles. Dev. Cell 27, 586–597 (2013).
pubmed: 24268700 pmcid: 3898710 doi: 10.1016/j.devcel.2013.09.029
Courtois, A., Schuh, M., Ellenberg, J. & Hiiragi, T. The transition from meiotic to mitotic spindle assembly is gradual during early mammalian development. J. Cell Biol. 198, 357–370 (2012).
pubmed: 22851319 pmcid: 3413348 doi: 10.1083/jcb.201202135
Schultz, R. M. Regulation of zygotic gene activation in the mouse. Bioessays 15, 531–538 (1993).
pubmed: 8135766 doi: 10.1002/bies.950150806
Akera, T. et al. Spindle asymmetry drives non-Mendelian chromosome segregation. Science 358, 668–672 (2017).
pubmed: 29097549 pmcid: 5906099 doi: 10.1126/science.aan0092
So, C. et al. A liquid-like spindle domain promotes acentrosomal spindle assembly in mammalian oocytes. Science 364, eaat9557 (2019).
pubmed: 31249032 pmcid: 6629549 doi: 10.1126/science.aat9557
Hertwig, O. Das Problem der Befruchtung und der Isotropie des Eies, eine Theorie der Vererbung. Enaische Z. Naturwissenschaft 18, 276–318 (1884).
Strauss, B., Adams, R. J. & Papalopulu, N. A default mechanism of spindle orientation based on cell shape is sufficient to generate cell fate diversity in polarised Xenopus blastomeres. Development 133, 3883–3893 (2006).
pubmed: 16943269 doi: 10.1242/dev.02578
Wyatt, T. P. et al. Emergence of homeostatic epithelial packing and stress dissipation through divisions oriented along the long cell axis. Proc. Natl Acad. Sci. USA 112, 5726–5731 (2015).
pubmed: 25908119 pmcid: 4426437 doi: 10.1073/pnas.1420585112
Gray, D. et al. First cleavage of the mouse embryo responds to change in egg shape at fertilization. Curr. Biol. 14, 397–405 (2004).
pubmed: 15028215 doi: 10.1016/j.cub.2004.02.031
Skamagki, M., Wicher, K. B., Jedrusik, A., Ganguly, S. & Zernicka-Goetz, M. Asymmetric localization of Cdx2 mRNA during the first cell-fate decision in early mouse development. Cell Rep. 3, 442–457 (2013).
pubmed: 23375373 pmcid: 3607255 doi: 10.1016/j.celrep.2013.01.006
Chi, F., Sharpley, M. S., Nagaraj, R., Roy, S. S. & Banerjee, U. Glycolysis-independent glucose metabolism distinguishes TE from ICM fate during mammalian embryogenesis. Dev. Cell 53, 9–26.e4 (2020).
pubmed: 32197068 pmcid: 7289320 doi: 10.1016/j.devcel.2020.02.015
Ranjan, R., Snedeker, J. & Chen, X. Asymmetric centromeres differentially coordinate with mitotic machinery to ensure biased sister chromatid segregation in germline stem cells. Cell Stem Cell 25, 666–681.e5 (2019).
pubmed: 31564548 pmcid: 6842444 doi: 10.1016/j.stem.2019.08.014
Kaur, G. et al. Probing transcription factor diffusion dynamics in the living mammalian embryo with photoactivatable fluorescence correlation spectroscopy. Nat. Commun. 4, 1637 (2013).
pubmed: 23535658 doi: 10.1038/ncomms2657
Fierro-Gonzalez, J. C., White, M. R., Silva, J. & Plachta, N. Cadherin-dependent filopodia control preimplantation embryo compaction. Nat. Cell Biol. 15, 1424–1433 (2013).
pubmed: 24270889 doi: 10.1038/ncb2875
Loughlin, R., Wilbur, J. D., McNally, F. J., Nedelec, F. J. & Heald, R. Katanin contributes to interspecies spindle length scaling in Xenopus. Cell 147, 1397–1407 (2011).
pubmed: 22153081 pmcid: 3240848 doi: 10.1016/j.cell.2011.11.014

Auteurs

Oz Pomp (O)

Department of Cell and Developmental Biology, Institute for Regenerative Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.

Hui Yi Grace Lim (HYG)

Institute of Molecular and Cell Biology, ASTAR, Singapore, Singapore.

Robin M Skory (RM)

Department of Cell and Developmental Biology, Institute for Regenerative Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.

Adam A Moverley (AA)

Department of Cell and Developmental Biology, Institute for Regenerative Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.

Piotr Tetlak (P)

Department of Cell and Developmental Biology, Institute for Regenerative Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.

Stephanie Bissiere (S)

Department of Cell and Developmental Biology, Institute for Regenerative Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA.

Nicolas Plachta (N)

Department of Cell and Developmental Biology, Institute for Regenerative Medicine, Perelman School of Medicine, University of Pennsylvania, Philadelphia, PA, USA. nicolas.plachta@pennmedicine.upenn.edu.

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