Abstract
During cell proliferation, many types of organelles must be correctly distributed into daughter cells before cytokinesis. Pioneering microscopic and molecular physiological experiments revealed that organelle proliferation and segregation into daughter cells of Cyanidioschyzon merolae are tightly regulated. The first breakthroughs were achieved using synchronized cell cultures treated with cell-cycle inhibitors, which enabled elucidation of the sequential patterns of organelle divisions within the cell division cycle. In addition, the dynamics of organelle movements during cell division suggested that they were mediated by the cytoskeletal network and motor proteins. Recent state-of-the-art investigations into the molecular functions of a kinesin-like protein (TOP) and a mitotic kinase (AUR) have revealed that an integrated regulatory mechanism controls the division of many types of organelles. Transcriptomic and proteomic analyses suggest that C. merolae cells lack a classical actomyosin-based cytokinesis system. However, eukaryotic elongation factor 1 alpha (eEF-1α) is specifically and spatiotemporally enriched at the cell division site during cytokinesis, suggesting that C. merolae cells utilize an evolutionarily ancient cell division system.
References
Bunai F, Ando K, Ueno H, Numata O (2006) Tetrahymena eukaryotic translation elongation factor 1A (eEF1A) bundles filamentous actin through dimer formation. J Biochem 140:393–399. doi.org/10.1093/jb/mvj169
Durso NA, Cyr RJ (1994) A calmodulin-sensitive interaction between microtubules and a higher plant homolog of elongation factor-1 alpha. Plant Cell 6:893–905. https://doi.org/10.1105/tpc.6.6.893
Fujimoto H, Mabuchi I (2010) Elongation factors are involved in cytokinesis of sea urchin eggs. Genes Cells 15:123–135. https://doi.org/10.1111/j.1365-2443.2009.01370.x
Fujiwara T, Misumi O, Tashiro K et al (2009) Periodic gene expression patterns during the highly synchronized cell nucleus and organelle division cycles in the unicellular red alga Cyanidioschyzon merolae. DNA Res 16:59–72. https://doi.org/10.1093/dnares/dsn032
Hirokawa N (1998) Kinesin and dynein superfamily proteins and the mechanism of organelle transport. Science 279:519–526. https://doi.org/10.1126/science.279.5350.519
Hirokawa N, Noda Y, Tanaka Y, Niwa S (2009) Kinesin superfamily motor proteins and intracellular transport. Nat Rev Mol Cell Biol 10:682–696. https://doi.org/10.1038/nrm2774
Imoto Y, Fujiwara T, Yoshida Y et al (2010) Division of cell nuclei, mitochondria, plastids, and microbodies mediated by mitotic spindle poles in the primitive red alga Cyanidioschyzon merolae. Protoplasma 241:63–74. https://doi.org/10.1007/s00709-010-0107-y
Imoto Y, Nishida K, Yagisawa F et al (2011) Involvement of elongation factor-1α in cytokinesis without actomyosin contractile ring in the primitive red alga Cyanidioschyzon merolae. Cytologia 76:431–437. https://doi.org/10.1508/cytologia.76.431
Kato S, Imoto Y, Ohnuma M et al (2011) Aurora kinase of the red alga Cyanidioschyzon merolae is related to both mitochondrial division and mitotic spindle formation. Cytologia 76:465–472
Kobayashi Y, Kanesaki Y, Tanaka A et al (2009) Tetrapyrrole signal as a cell-cycle coordinator from organelle to nuclear DNA replication in plant cells. Proc Natl Acad Sci U S A 106:803–807. https://doi.org/10.1073/pnas.0804270105
Kobayashi Y, Imamura S, Hanaoka M, Tanaka K (2011) A tetrapyrrole-regulated ubiquitin ligase controls algal nuclear DNA replication. Nat Cell Biol 13:483–487. https://doi.org/10.1038/ncb2203
Maruyama S, Kuroiwa H, Miyagishima S et al (2007) Centromere dynamics in the primitive red alga Cyanidioschyzon merolae. Plant J 49:1122–1129. https://doi.org/10.1111/j.1365-313X.2006.03024.x
Matsuzaki M, Misumi O, Shin-I T et al (2004) Genome sequence of the ultrasmall unicellular red alga Cyanidioschyzon merolae 10D. Nature 428:653–657. https://doi.org/10.1038/nature02398
Moriyama T, Tajima N, Sekine K, Sato N (2014) Localization and phylogenetic analysis of enzymes related to organellar genome replication in the unicellular rhodophyte Cyanidioschyzon merolae. Genome Biol Evol 6:228–237. https://doi.org/10.1093/gbe/evu009
Nishida K, Yagisawa F, Kuroiwa H et al (2005) Cell cycle-regulated, microtubule-independent organelle division in Cyanidioschyzon merolae. Mol Biol Cell 16:2493–2502. https://doi.org/10.1091/mbc.E05
Numata O, Kurasawa Y, Gonda K, Watanabe Y (2000) Tetrahymena elongation factor-1α is localized with calmodulin in the division furrow. J Biochem 127:51–56. https://doi.org/10.1093/oxfordjournals.jbchem.a022583
Shiina N, Gotoh Y, Kubomura N et al (1994) Microtubule severing by elongation factor 1. Science 266:282–285. https://doi.org/10.1126/science.7939665
Sumiya N, Fujiwara T, Era A, Miyagishima S (2016) Chloroplast division checkpoint in eukaryotic algae. Proc Natl Acad Sci 113:E7629–E7638. https://doi.org/10.1073/pnas.1612872113
Suzuki K, Kawazu T, Mita T, Takahashi H, Itoh R, Toda K, Kuroiwa T (1995) Cytokinesis by a contractile ring in the primitive red alga Cyanidium caldarium RK-1. Eur J Cell Biol 67:170–178
Takahashi H, Takano H, Kuroiwa H et al (1998) A possible role for actin dots in the formation of the contractile ring in the ultra-micro alga Cyanidium caldarium RK-1. Protoplasma 202:91–104. https://doi.org/10.1007/BF01280878
Yagisawa F, Fujiwara T, Kuroiwa H et al (2012) Mitotic inheritance of endoplasmic reticulum in the primitive red alga Cyanidioschyzon merolae. Protoplasma 249:1129–1135. https://doi.org/10.1007/s00709-011-0359-1
Yagisawa F, Fujiwara T, Ohnuma M et al (2013) Golgi inheritance in the primitive red alga, Cyanidioschyzon merolae. Protoplasma 250:943–948. https://doi.org/10.1007/s00709-012-0467-6
Yoshida Y, Kuroiwa H, Hirooka S et al (2009) The bacterial ZapA-like protein ZED is required for mitochondrial division. Curr Biol 19:1491–1497. https://doi.org/10.1016/j.cub.2009.07.035
Yoshida Y, Fujiwara T, Imoto Y et al (2013) The kinesin-like protein TOP promotes aurora localisation and induces mitochondrial, chloroplast and nuclear division. J Cell Sci 126:2392–2400. https://doi.org/10.1242/jcs.116798
Acknowledgments
This work was supported by a Human Frontier Science Program Long Term Fellowship (LT000356/2011-L to Y.Y.) and a grant from the Japan Society for the Promotion of Science Fellowship (no. 14J04556 to Y.I.).
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Yoshida, Y., Imoto, Y. (2017). Regulation of Organelle and Cell Division by Cytoskeletal and Motor Proteins in Cyanidioschyzon merolae . In: Kuroiwa, T., et al. Cyanidioschyzon merolae. Springer, Singapore. https://doi.org/10.1007/978-981-10-6101-1_16
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