Stu2, the Budding Yeast XMAP215/Dis1 Homolog, Promotes Assembly of Yeast Microtubules by Increasing Growth Rate and Decreasing Catastrophe Frequency

Podolski, Marija; Mahamdeh, Mohammed; Howard, Jonathon

doi:10.1074/jbc.m114.584300

Cited by 52 publications

(64 citation statements)

References 36 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Dis1–eGFP associated weakly with the MT lattice and accumulated on and tracked growing MT plus-ends in a spot-like manner (Fig. 1C), similar to other TOG orthologues (Brouhard et al, 2008; Li et al, 2012; Podolski et al, 2014); by contrast, Dis1–eGFP was not observed on shrinking MT ends, similar to Alp14, the other TOG orthologue in fission yeast (Al-Bassam et al, 2012; Garcia et al, 2001; Hussmann et al, 2016; Nakaseko et al, 2001). …”

Section: Resultssupporting

confidence: 55%

“…2C). Whereas 20 nM Dis1–eGFP localised to growing MT ends in a spot-like manner, as with XMAP215 (Brouhard et al, 2008; Li et al, 2012; Podolski et al, 2014) (Fig. 2C and ), upon the addition of 200 nM Mal3, the amount of Dis1–eGFP at MT ends was strongly increased; Dis1–eGFP localised now to a much more elongated region at growing MT ends, rather reminiscent of the appearance of end-tracking Mal3–GFP (…”

Section: Resultsmentioning

confidence: 81%

“…Members of this protein family contain N-terminal TOG domains that bind soluble tubulin and a separate MT-binding site (Al-Bassam et al, 2006; Widlund et al, 2011) that, in combination, allow them to act as MT polymerases accelerating MT growth (Al-Bassam et al, 2012; Ayaz et al, 2012, 2014; Brouhard et al, 2008; Li et al, 2012; Podolski et al, 2014; Reber et al, 2013; Roostalu et al, 2015; Takeshita et al, 2013). Consequently, these TOG proteins localise to the very MT end, in contrast to EB1 family proteins that bind to an extended region (Maurer et al, 2014).…”

Section: Introductionmentioning

confidence: 99%

See 2 more Smart Citations

An unconventional interaction between Dis1/TOG and Mal3/EB1 in fission yeast promotes the fidelity of chromosome segregation

Matsuo

Maurer

Yukawa

et al. 2016

Journal of Cell Science

View full text Add to dashboard Cite

Dynamic microtubule plus-ends interact with various intracellular target regions such as the cell cortex and the kinetochore. Two conserved families of microtubule plus-end-tracking proteins, the XMAP215, ch-TOG or CKAP5 family and the end-binding 1 (EB1, also known as MAPRE1) family, play pivotal roles in regulating microtubule dynamics. Here, we study the functional interplay between fission yeast Dis1, a member of the XMAP215/TOG family, and Mal3, an EB1 protein. Using an in vitro microscopy assay, we find that purified Dis1 autonomously tracks growing microtubule ends and is a bona fide microtubule polymerase. Mal3 recruits additional Dis1 to microtubule ends, explaining the synergistic enhancement of microtubule dynamicity by these proteins. A non-canonical binding motif in Dis1 mediates the interaction with Mal3. X-ray crystallography shows that this new motif interacts in an unconventional configuration with the conserved hydrophobic cavity formed within the Mal3 C-terminal region that typically interacts with the canonical SXIP motif. Selectively perturbing the Mal3–Dis1 interaction in living cells demonstrates that it is important for accurate chromosome segregation. Whereas, in some metazoans, the interaction between EB1 and the XMAP215/TOG family members requires an additional binding partner, fission yeast relies on a direct interaction, indicating evolutionary plasticity of this critical interaction module.

show abstract

Section: Resultssupporting

confidence: 55%

Section: Resultsmentioning

confidence: 81%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

An unconventional interaction between Dis1/TOG and Mal3/EB1 in fission yeast promotes the fidelity of chromosome segregation

Matsuo

Maurer

Yukawa

et al. 2016

Journal of Cell Science

View full text Add to dashboard Cite

show abstract

“…Next, to structurally understand how CLASPs can associate with tubulin or MTs as rescue factors and Stu2 as an MT polymerase [28], we modeled the complex of TOGs and αβ-tubulin in the various states. Currently, several structures of αβ-tubulin in the different conformations are available: the straight form, corresponding to the tubulin structure in the MT lattice, obtained from the zinc-induced tubulin sheets by high-resolution electron microscopy (EM); the curved form in the protofilament, from stathmin-bound tubulin by X-ray crystallography; and the curved-sheared form of MTs induced to depolymerize by kinesin-13, obtained by cryo-EM at 11 Å resolution (PDB codes 1JFF, 1SA0 and 3J2U, respectively; Supplementary Fig.…”

Section: Resultsmentioning

confidence: 99%

CLASP2 Has Two Distinct TOG Domains That Contribute Differently to Microtubule Dynamics

Maki

Grimaldi

Fuchigami

et al. 2015

Journal of Molecular Biology

View full text Add to dashboard Cite

CLIP-associated proteins CLASPs are mammalian microtubule (MT) plus-end tracking proteins (+TIPs) that promote MT rescue in vivo. Their plus-end localization is dependent on other +TIPs, EB1 and CLIP-170, but in the leading edge of the cell, CLASPs display lattice-binding activity. MT association of CLASPs is suggested to be regulated by multiple TOG (tumor overexpressed gene) domains and by the serine-arginine (SR)-rich region, which contains binding sites for EB1. Here, we report the crystal structures of the two TOG domains of CLASP2. Both domains consist of six HEAT repeats, which are similar to the canonical paddle-like tubulin-binding TOG domains, but have arched conformations. The degrees and directions of curvature are different between the two TOG domains, implying that they have distinct roles in MT binding. Using biochemical, molecular modeling and cell biological analyses, we have investigated the interactions between the TOG domains and αβ-tubulin and found that each domain associates differently with αβ-tubulin. Our findings suggest that, by varying the degrees of domain curvature, the TOG domains may distinguish the structural conformation of the tubulin dimer, discriminate between different states of MT dynamic instability and thereby function differentially as stabilizers of MTs.

show abstract

“…The neuronal microtubule stabilizer Tau also increases v g and decreases f cat [42–44]. The same holds true for Stu2, the budding yeast homolog of XMAP215 [45], and the budding yeast kinesin Kip2 (Hibbel, unpublished) and dynactin [46,47]. Conversely, the tubulin-sequestering protein Op18/Stathmin decreases v g and increases f cat [48,49].…”

Section: Regulation Of Dynamics By Mapsmentioning

confidence: 98%

Regulation of Microtubule Growth and Catastrophe: Unifying Theory and Experiment

Bowne-Anderson

Hibbel

Howard

2015

Trends in Cell Biology

Self Cite

View full text Add to dashboard Cite

Recent studies have found that microtubule-associated proteins (MAPs) can regulate the dynamical properties of microtubules in unexpected ways. For most MAPs, there is an inverse relationship between their effects on the speed of growth and the frequency of catastrophe, the conversion of a growing microtubule to a shrinking one. Such a negative correlation is predicted by the standard GTP-cap model, which posits that catastrophe is due to loss of a stabilizing cap of GTP-tubulin at the end of a growing microtubule. However, many other MAPs, notably Kinesin-4 and combinations of EB1 with XMAP215, contradict this general rule. In this review, we show that a more nuanced, but still simple, GTP-cap model, can account for the diverse regulatory activities of MAPs.

show abstract

Stu2, the Budding Yeast XMAP215/Dis1 Homolog, Promotes Assembly of Yeast Microtubules by Increasing Growth Rate and Decreasing Catastrophe Frequency

Cited by 52 publications

References 36 publications

An unconventional interaction between Dis1/TOG and Mal3/EB1 in fission yeast promotes the fidelity of chromosome segregation

An unconventional interaction between Dis1/TOG and Mal3/EB1 in fission yeast promotes the fidelity of chromosome segregation

CLASP2 Has Two Distinct TOG Domains That Contribute Differently to Microtubule Dynamics

Regulation of Microtubule Growth and Catastrophe: Unifying Theory and Experiment

Contact Info

Product

Resources

About