Switching from weak to strong cortical attachment of microtubules accounts for the transition from nuclear centration to spindle elongation in metazoans
Shohei Tada,
Yoshitaka Yamazaki,
Kazunori Yamamoto,
Ken Fujii,
Takahiro G. Yamada,
Noriko F. Hiroi,
Akatsuki Kimura,
Akira Funahashi
Affiliations
Shohei Tada
Center for Biosciences and Informatics, Graduate School of Fundamental Science and Technology, Keio University, Yokohama, Kanagawa, 223-8522, Japan
Yoshitaka Yamazaki
Center for Biosciences and Informatics, Graduate School of Fundamental Science and Technology, Keio University, Yokohama, Kanagawa, 223-8522, Japan
Kazunori Yamamoto
Cell Architecture Laboratory, Department of Chromosome Science, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan; Genetics Program, The Graduate University for Advanced Studies, SOKENDAI, Mishima, Shizuoka 411-8540, Japan; Faculty of Applied Bioscience, Kanagawa Institute of Technology, Atsugi, Kanagawa, 243-0292, Japan; Division of Developmental Physiology, Institute for Genetic Medicine, Hokkaido University, Sapporo, Hokkaido, 060-0815, Japan
Ken Fujii
Cell Architecture Laboratory, Department of Chromosome Science, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan; Genetics Program, The Graduate University for Advanced Studies, SOKENDAI, Mishima, Shizuoka 411-8540, Japan
Takahiro G. Yamada
Center for Biosciences and Informatics, Graduate School of Fundamental Science and Technology, Keio University, Yokohama, Kanagawa, 223-8522, Japan; Department of Biosciences and Informatics, Keio University, Yokohama, Kanagawa, 223-8522, Japan
Noriko F. Hiroi
School of Medicine, Keio University, Shinjuku-ward, Tokyo, 160-8582, Japan; Faculty of Creative Engineering, Kanagawa Institute of Technology, Atsugi, Kanagawa, 243-0292, Japan
Akatsuki Kimura
Cell Architecture Laboratory, Department of Chromosome Science, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan; Genetics Program, The Graduate University for Advanced Studies, SOKENDAI, Mishima, Shizuoka 411-8540, Japan; Center for Data Assimilation Research and Applications, Joint Support-Center for Data Science Research, Research Organization of Information and Systems (ROIS), Tachikawa, 190-8562, Japan; Corresponding authors.
Akira Funahashi
Center for Biosciences and Informatics, Graduate School of Fundamental Science and Technology, Keio University, Yokohama, Kanagawa, 223-8522, Japan; Department of Biosciences and Informatics, Keio University, Yokohama, Kanagawa, 223-8522, Japan; Corresponding authors.
The centrosome is a major microtubule organizing center in animal cells. The position of the centrosomes inside the cell is important for cell functions such as cell cycle, and thus should be tightly regulated. Theoretical models based on the forces generated along the microtubules have been proposed to account for the dynamic movements of the centrosomes during the cell cycle. These models, however, often adopted inconsistent assumptions to explain distinct but successive movements, thus preventing a unified model for centrosome positioning. For the centration of the centrosomes, weak attachment of the astral microtubules to the cell cortex was assumed. In contrast, for the separation of the centrosomes during spindle elongation, strong attachment was assumed. Here, we mathematically analyzed these processes at steady state and found that the different assumptions are proper for each process. We experimentally validated our conclusion using nematode and sea urchin embryos by manipulating their shapes. Our results suggest the existence of a molecular mechanism that converts the cortical attachment from weak to strong during the transition from centrosome centration to spindle elongation.
