CLIP170-like tip1p Spatially Organizes Microtubular Dynamics in Fission Yeast

Brunner, Damian; Nurse, Paul

doi:10.1016/s0092-8674(00)00091-x

Cited by 264 publications

(303 citation statements)

References 54 publications

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“…These components could interact either directly with proteins of the mitochondrial outer membrane or through linker proteins. Previous studies have identified several proteins in S. pombe that interact with microtubules and concentrate at the cell tips [tip1p (21), tea1p (22), and tea2p (23)], but these species do not appear to play a direct role in facilitating microtubule interaction with mitochondria, because cells mutant for these components still distribute mitochondria toward the cell tips (B. Weir and M.P.Y., unpublished observations). Future genetic and biochemical approaches should lead to the identification of proteins that enable cells to couple microtubule and spindle dynamics with the productive and coordinated distribution of mitochondria.…”

Section: Discussionmentioning

confidence: 99%

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

Yaffe

Stuurman

Vale

2003

Proc. Natl. Acad. Sci. U.S.A.

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Microtubules mediate mitochondrial distribution in the yeastSchizosaccharomyces 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.

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Section: Discussionmentioning

confidence: 99%

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

Yaffe

Stuurman

Vale

2003

Proc. Natl. Acad. Sci. U.S.A.

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“…Regulation of the local (25) or global (24) catastrophe rate (by appropriate microtubule-associated proteins) may tune the average length of the MTs to the appropriate value, and the mechanism will work independently of the size of the system. In small systems, where buckling forces are large, the mechanism, in addition, may be able to self-regulate.…”

Section: Conclusion and Discussionmentioning

confidence: 99%

Dynamics of microtubule asters in microfabricated chambers: The role of catastrophes

Faivre-Moskalenko

Dogterom

2002

Proc. Natl. Acad. Sci. U.S.A.

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Recent in vivo as well as in vitro experiments have indicated that microtubule pushing alone is sufficient to position a microtubuleorganizing center within a cell. Here, we investigate the effect of catastrophes on the dynamics of microtubule asters within microfabricated chambers that mimic the confining geometry of living cells. The use of a glass bead as the microtubule-organizing center allows us to manipulate the aster by using optical tweezers. In the case in which microtubules preexist, we show that because of microtubule buckling, repositioning almost never occurs after relocation with the optical tweezers, although initial microtubule growth always leads the aster to the geometrical center of the chamber. When a catastrophe promoter is added, we find instead that the aster is able to efficiently explore the chamber geometry even after being relocated with the optical tweezers. As predicted by theoretical calculations, the results of our in vitro experiments clearly demonstrate the need for catastrophes for proper positioning in a confining geometry. These findings correlate with recent observations of nuclear positioning in fission yeast cells.T he correct positioning of microtubule (MT)-organizing centers (MTOCs) within the geometry of a living cell plays a role in a wide variety of morphological processes. These processes include positioning of the nucleus to define the future division plane of the cell and the positioning of microtubule asters during formation and orientation of the mitotic spindle (1-4). In each case, interactions of the microtubules with the confining cell membrane somehow make sure that the organizing center positions itself correctly with respect to the geometry of the cell. Although it has been shown that the molecular motor dynein is involved in many cases (5-9), there are other cases in which microtubule pushing alone seems to be sufficient to ensure proper positioning. In interphase fission yeast cells, for example, motions of the nucleus have been directly correlated with the dynamics of MTs interacting with the cell ends (10). In these experiments, the observed nuclear dynamics can be explained fully without assuming any motor activity. We have shown in previous in vitro experiments that simple pushing by freshly nucleated MTs indeed will allow MT asters, grown from isolated centrosomes or even MT-nucleating beads, to find the geometrical center of microfabricated chambers (11). Theoretical considerations, however, indicate that once an MT array is fully developed (or preexists), MT pushing alone does not allow the organizing center to maintain a central position or actively explore the geometry. Dynamic instability of microtubules, in the form of occasional switches (catastrophes) to a shrinking state, is expected to play an important role. Catastrophes may be needed to avoid buckling of continuously growing MTs under their own polymerization force, leading to long MTs circling around the edges of the chamber and destabilization of the central position (11). In addition, ...

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“…TOG and its orthologues all contain multiple HEAT repeats that may serve as a scaffold for other components to assemble into complexes (Neuwald and Hirano, 2000). In normal brain, TOG may function in cell morphogenesis and establishment of cellular polarity (Charrasse et al, 1995(Charrasse et al, , 1998Brunner and Nurse, 2000). It also has been suggested that proteins of the TOG family interact with the cell cortex to mediate motility (Schroer, 2001).…”

Section: Introductionmentioning

confidence: 99%

The Microtubule-associated Protein Tumor Overexpressed Gene Binds to the RNA Trafficking Protein Heterogeneous Nuclear Ribonucleoprotein A2

Kosturko

Maggipinto

D'Sa

et al. 2005

MBoC

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In neural cells, such as oligodendrocytes and neurons, transport of certain RNAs along microtubules is mediated by the cis-acting heterogeneous nuclear ribonucleoprotein A2 response element (A2RE) trafficking element and the cognate trans-acting heterogeneous nuclear ribonucleoprotein (hnRNP) A2 trafficking factor. Using a yeast two-hybrid screen, we have identified a microtubule-associated protein, tumor overexpressed gene (TOG)2, as an hnRNP A2 binding partner. The C-terminal third of TOG2 is sufficient for hnRNP A2 binding. TOG2, the large protein isoform of TOG, is the only isoform detected in oligodendrocytes in culture. TOG coimmunoprecipitates with hnRNP A2 present in the cytoskeleton (CSK) fraction of neural cells, and both coprecipitate with microtubule stabilized pellets. Staining with anti-TOG reveals puncta that are localized in proximity to microtubules, often at the plus ends. TOG is colocalized with hnRNP A2 and A2RE-mRNA in trafficking granules that remain associated with CSK-insoluble tissue. These data suggest that TOG mediates the association of hnRNP A2-positive granules with microtubules during transport and/or localization. INTRODUCTIONThe heterogeneous nuclear ribonucleoprotein (hnRNP) A2 is implicated in RNA processing, RNA transport, and translation regulation (Dreyfuss et al., 1993;Siomi and Dreyfuss, 1995;Hamilton et al., 1999;Kwon et al., 1999). HnRNP A2 binds to a specific cis-acting element, hnRNP A2 response element (A2RE), found in several dendritically localized mRNAs Munro et al., 1999). This interaction is necessary for transport of A2RE-mRNAs to the periphery of neural cells (Munro et al., 1999;Shan et al., 2003).A2RE-mRNAs, hnRNP A2, and other components form complexes that look by light microscopy like granules that are transported to the cell periphery by a microtubule-and kinesin-based mechanism. In cultured oligodendrocytes and neurons, granules containing A2RE-mRNAs and hnRNP A2 are associated with the cytoskeleton (CSK) . HnRNP A2 and some A2RE-mRNAs copurify with the CSK from rat brain (Hoek et al., 1998;Boccaccio et al., 1999).To identify molecular partners of hnRNP A2, we performed yeast two-hybrid analysis. One of the components identified is the tumor overexpressed gene (TOG) protein, a microtubule-associated protein (MAP) ubiquitously expressed in human tissues. TOG is a single copy gene that generates two mRNA splice variants (Nagase et al., 1995;Charrasse et al., 1998) encoding proteins that differ by a 60-aa insert near the C terminus. In dividing cells, TOG localizes with centrosome and spindle microtubules and may be necessary for microtubule rearrangements and spindle assembly (Charrasse et al., 1998;Lee et al., 2001). Orthologues of colonic and hepatic tumor overexpressed gene (ch-TOG) (Homo sapiens), Dis1p, Stu2p, XMAP215, ZYG-9, and mini spindles, in fission yeast, budding yeast, Xenopus laevis, Caenorhabditis elegans, and Drosophila melanogaster, respectively, have similar functions. TOG and its orthologues all contain multiple HEAT repeats that may serv...

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CLIP170-like tip1p Spatially Organizes Microtubular Dynamics in Fission Yeast

Cited by 264 publications

References 54 publications

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

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

Dynamics of microtubule asters in microfabricated chambers: The role of catastrophes

The Microtubule-associated Protein Tumor Overexpressed Gene Binds to the RNA Trafficking Protein Heterogeneous Nuclear Ribonucleoprotein A2

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