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WIREs Dev Biol
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Organelle size scaling over embryonic development

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Abstract Cell division without growth results in progressive cell size reductions during early embryonic development. How do the sizes of intracellular structures and organelles scale with cell size and what are the functional implications of such scaling relationships? Model organisms, in particular Caenorhabditis elegans worms, Drosophila melanogaster flies, Xenopus laevis frogs, and Mus musculus mice, have provided insights into developmental size scaling of the nucleus, mitotic spindle, and chromosomes. Nuclear size is regulated by nucleocytoplasmic transport, nuclear envelope proteins, and the cytoskeleton. Regulators of microtubule dynamics and chromatin compaction modulate spindle and mitotic chromosome size scaling, respectively. Developmental scaling relationships for membrane‐bound organelles, like the endoplasmic reticulum, Golgi, mitochondria, and lysosomes, have been less studied, although new imaging approaches promise to rectify this deficiency. While models that invoke limiting components and dynamic regulation of assembly and disassembly can account for some size scaling relationships in early embryos, it will be exciting to investigate the contribution of newer concepts in cell biology such as phase separation and interorganellar contacts. With a growing understanding of the underlying mechanisms of organelle size scaling, future studies promise to uncover the significance of proper scaling for cell function and embryonic development, as well as how aberrant scaling contributes to disease. This article is categorized under: Establishment of Spatial and Temporal Patterns > Regulation of Size, Proportion, and Timing Early Embryonic Development > Fertilization to Gastrulation Comparative Development and Evolution > Model Systems
Developmental size regulation of intracellular structures in Xenopus. (a) Blastomeres were isolated from different stage Xenopus laevis embryos and stained for the nuclear pore complex (NPC). Scale bar, 50 μm. (Reprinted with permission from Jevtic and Levy (). Copyright 2015 Cell Press) (b) Nuclei were assembled in X. laevis egg extract in microfluidic channels of varying dimensions. Channel dimensions are indicated as height × width. Membranes, DNA, and incorporated dUTP are labeled green, blue, and red, respectively. Scale bar, 20 μm. (Reprinted with permission from Hara and Merten (). Copyright 2015 Cell Press) (c) Nuclei and cytoplasm from stage 10 X. laevis embryos were encapsulated in droplets of varying volume and allowed to reach steady‐state sizes. Droplet volumes are indicated above each panel. Nuclei are visualized by import of GFP‐NLS. Scale bar, 50 μm. (Reprinted with permission from P. Chen et al. (). Copyright 2019 Rockefeller University Press) (d) Different stage X. laevis embryos were fixed and stained for tubulin (yellow) and DNA (red). Scale bar, 20 μm. (Reprinted with permission from Wuhr et al. (). Copyright 2008 Cell Press) (e) Spindles were assembled in different volumes of X. laevis egg extract. Tubulin, DNA, and NuMA are labeled red, blue, and green, respectively. Droplet diameters are indicated above each panel. Scale bar, 25 μm. (Reprinted with permission from Hazel et al. (). Copyright 2013 AAAS) (f) Condensed mitotic chromosomes from different stage X. laevis embryos are shown. For comparison, unreplicated (Unrep) and replicated (Rep) sperm chromosomes were incubated in X. laevis egg extract. DNA and kinetochores are labeled blue and red, respectively. Scale bar, 5 μm. (Reprinted with permission from Kieserman and Heald (). Copyright 2011 Taylor & Francis) (g) As cells become smaller during early Xenopus development, palmitoylated importin α is increasingly partitioned to the plasma membrane. In the case of the nucleus, this reduces nuclear import and size. In the case of the spindle, reduced kif2a inhibition promotes MT depolymerization and spindle shortening. (Reprinted with permission from Brownlee and Heald (). Copyright 2019 Cell Press)
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Nuclear‐to‐cytoplasmic (N/C) volume ratios generally increase during early development in different species. Caenorhabditis elegans worm data are from Hara and Kimura (). Fission yeast data are from Neumann and Nurse (). Mus musculus data are from Tsichlaki and FitzHarris (). Hemicentrotus pulcherrimus sea urchin data are from Masui and Kominami (). Asterina pectinifera starfish data are from Masui, Yoneda, and Kominami (). Danio rerio zebrafish data are from Joseph et al. (). Xenopus laevis frog data are from Jevtic and Levy ()
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Developmental size regulation of intracellular structures in other model organisms. (a) Different stage Drosophila melanogaster embryos showing labeled nuclei. Numbers denote the nuclear cycle. Note that nuclei are present in a syncytium until cellularization at nuclear cycle 14. (Reprinted with permission from Kotadia et al. (). Copyright 2010 Wiley‐Blackwell) (b) Different stage Mus musculus embryos with DNA labeled green and cell cortex labeled red with phalloidin. (Reprinted with permission from Tsichlaki and FitzHarris (). Copyright 2016 Springer Nature) and made available under a Creative Commons Attribution 4.0 International License (c) Different stage Paracentrotus lividus sea urchin embryos microinjected with ATTO 565‐labeled tubulin. Scale bar, 20 μm. (Reprinted with permission from Lacroix et al. (). Copyright 2018 Cell Press)
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Developmental size regulation of intracellular structures in Caenorhabditis elegans. (a) Different stage C. elegans embryos with nuclei labeled green for H2B and plasma membrane labeled red. Scale bar, 10 μm. (Reprinted with permission from Fickentscher and Weiss (). Copyright 2017 Springer Nature) and made available under a Creative Commons Attribution 4.0 International License. (b) Different stage C. elegans embryos expressing GFP‐tagged β‐tubulin. Scale bar, 20 μm. (Reprinted with permission from Lacroix et al. (). Copyright 2018 Cell Press) (c) Different stage C. elegans embryos expressing GFP‐tagged γ‐tubulin and H2B. Scale bar, 10 μm. (Reprinted with permission from Greenan et al. (). Copyright 2010 Cell Press) The cartoon model in the “C. elegans spindle size regulators” box was reprinted with permission from Lacroix et al. (). Copyright 2018 Cell Press)
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Models for developmental organelle size scaling. (a) Small red circles represent components that limit assembly and/or growth of the larger red organelle. Over development, limiting components are partitioned into greater numbers of smaller cells, such that the absolute amounts of limiting components per cell decrease leading to smaller organelle size. (b) Green rectangles assemble to form a linear structure whose length is dictated by the blue ruler. Developmental changes in the size of the ruler or building blocks might lead to reductions in the overall size of the structure. (c) A balance of assembly and disassembly sets steady‐state organelle size. Developmental changes in assembly and disassembly rates would lead to organelle size scaling. (d) The orange and blue organelles are connected through membranes. Developmental reductions in the size of one organelle might lead to concomitant size scaling of the interconnected organelle. Another possible scenario is that total membrane amount remains constant but membrane distribution changes such that one organelle increases in size and the other becomes smaller
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Comparative Development and Evolution > Model Systems
Early Embryonic Development > Fertilization to Gastrulation
Establishment of Spatial and Temporal Patterns > Regulation of Size, Proportion, and Timing