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Mitochondrial positioning in fission yeast is driven by association with dynamic microtubules and mitotic spindle poles.

ABSTRACT: Microtubules mediate mitochondrial distribution in the yeast Schizosaccharomyces pombe and many higher eukaryotic cells. In higher eukaryotes, kinesin motor proteins have been shown to transport mitochondria along microtubules, but the nature of the mitochondria-microtubule interactions in S. pombe has not been explored. By time lapse, total internal reflection fluorescence microscopy, or spinning-disk confocal microscopy, mitochondria appeared to be both tethered to ends and bound laterally along the sides of microtubules. Mitochondrial tubules extended and retracted when attached to the tips of elongating or shortening microtubules, respectively, but translocation along established microtubules was never observed. Mitochondria that were not associated with microtubules were largely immobile until they were "captured" by a growing microtubule. In mitotic cells, a portion of the mitochondria was tethered to the spindle-pole bodies and moved to the cellular ends during spindle elongation. This association may be important for organelle inheritance during cell division. Thus, in contrast to kinesin-mediated transport used by higher eukaryotes, mitochondrial motility and distribution in fission yeast are driven largely by microtubule polymerization and the elongation of the mitotic spindle.

SUBMITTER: Yaffe MP

PROVIDER: S-EPMC208773 | biostudies-literature | 2003 Sep

REPOSITORIES: biostudies-literature

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Mitochondrial positioning in fission yeast is driven by association with dynamic microtubules and mitotic spindle poles.

Yaffe Michael P MP Stuurman Nico N Vale Ronald D RD

Proceedings of the National Academy of Sciences of the United States of America 20030912 20

Microtubules mediate mitochondrial distribution in the yeast Schizosaccharomyces pombe and many higher eukaryotic cells. In higher eukaryotes, kinesin motor proteins have been shown to transport mitochondria along microtubules, but the nature of the mitochondria-microtubule interactions in S. pombe has not been explored. By time lapse, total internal reflection fluorescence microscopy, or spinning-disk confocal microscopy, mitochondria appeared to be both tethered to ends and bound laterally alo ...[more]

PMID: 12972644

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Project description:The asymmetrically dividing yeast S. cerevisiae assembles a bipolar spindle well after establishing the future site of cell division (i.e., the bud neck) and the division axis (i.e., the mother-bud axis). A surveillance mechanism called spindle position checkpoint (SPOC) delays mitotic exit and cytokinesis until the spindle is properly positioned relative to the mother-bud axis, thereby ensuring the correct ploidy of the progeny. SPOC relies on the heterodimeric GTPase-activating protein Bub2/Bfa1 that inhibits the small GTPase Tem1, in turn essential for activating the mitotic exit network (MEN) kinase cascade and cytokinesis. The Bub2/Bfa1 GAP and the Tem1 GTPase form a complex at spindle poles that undergoes a remarkable asymmetry during mitosis when the spindle is properly positioned, with the complex accumulating on the bud-directed old spindle pole. In contrast, the complex remains symmetrically localized on both poles of misaligned spindles. The mechanism driving asymmetry of Bub2/Bfa1/Tem1 in mitosis is unclear. Furthermore, whether asymmetry is involved in timely mitotic exit is controversial. We investigated the mechanism by which the GAP Bub2/Bfa1 controls GTP hydrolysis on Tem1 and generated a series of mutants leading to constitutive Tem1 activation. These mutants are SPOC-defective and invariably lead to symmetrical localization of Bub2/Bfa1/Tem1 at spindle poles, indicating that GTP hydrolysis is essential for asymmetry. Constitutive tethering of Bub2 or Bfa1 to both spindle poles impairs SPOC response but does not impair mitotic exit. Rather, it facilitates mitotic exit of MEN mutants, likely by increasing the residence time of Tem1 at spindle poles where it gets active. Surprisingly, all mutant or chimeric proteins leading to symmetrical localization of Bub2/Bfa1/Tem1 lead to increased symmetry at spindle poles of the Kar9 protein that mediates spindle positioning and cause spindle misalignment. Thus, asymmetry of the Bub2/Bfa1/Tem1 complex is crucial to control Kar9 distribution and spindle positioning during mitosis.

Dataset Information

Mitochondrial positioning in fission yeast is driven by association with dynamic microtubules and mitotic spindle poles.

Publications

Mitochondrial positioning in fission yeast is driven by association with dynamic microtubules and mitotic spindle poles.

Similar Datasets

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