Comparing contractile apparatus‐driven cytokinesis mechanisms across kingdoms

Balasubramanian, Mohan K.; Srinivasan, R.; Huang, Yinyi; Ng, Kian-Hong

doi:10.1002/cm.21082

Cited by 38 publications

(36 citation statements)

References 183 publications

(238 reference statements)

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“…For example, is the role of actin in endocytosis, well documented in the opisthokonts (Goode et al 2015), universal (and thus presumably ancestral) in eukaryotes more generally? Does the formation of cleavage furrows (which is nearly universal in eukaryotes other than higher plants) always involve actin (Balasubramanian et al 2012), even though type-II myosin (a component of the opisthokont actomyosin ring) is not present in groups other than the opisthokonts and their "close" relatives the amoebozoa (Richards and Cavalier-Smith 2005)?…”

Section: Discussionmentioning

confidence: 99%

Evidence That an Unconventional Actin Can Provide Essential F-Actin Function and That a Surveillance System Monitors F-Actin Integrity inChlamydomonas

2015

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Actin is one of the most conserved eukaryotic proteins. It is thought to have multiple essential cellular roles and to function primarily or exclusively as filaments ("F-actin"). Chlamydomonas has been an enigma, because a null mutation (ida5-1) in its single gene for conventional actin does not affect growth. A highly divergent actin gene, NAP1, is upregulated in ida5-1 cells, but it has been unclear whether NAP1 can form filaments or provide actin function. Here, we used the actin-depolymerizing drug latrunculin B (LatB), the F-actin-specific probe Lifeact-Venus, and genetic and molecular methods to resolve these issues. LatB-treated wild-type cells continue to proliferate; they initially lose Lifeact-stained structures but recover them concomitant with upregulation of NAP1. Thirty-nine LatB-sensitive mutants fell into four genes (NAP1 and LAT1-LAT3) in which we identified the causative mutations using a novel combinatorial pool-sequencing strategy. LAT1-LAT3 are required for NAP1 upregulation upon LatB treatment, and ectopic expression of NAP1 largely rescues the LatB sensitivity of the lat1-lat3 mutants, suggesting that the LAT gene products comprise a regulatory hierarchy with NAP1 expression as the major functional output. Selection of LatB-resistant revertants of a nap1 mutant yielded dominant IDA5 mutations that presumably render F-IDA5 resistant to LatB, and nap1 and lat mutations are synthetically lethal with ida5-1 in the absence of LatB. We conclude that both IDA5 and the divergent NAP1 can form filaments and redundantly provide essential F-actin functions and that a novel surveillance system, probably responding to a loss of F-actin, triggers NAP1 expression and perhaps other compensatory responses.

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Section: Discussionmentioning

confidence: 99%

Evidence That an Unconventional Actin Can Provide Essential F-Actin Function and That a Surveillance System Monitors F-Actin Integrity inChlamydomonas

2015

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“…Septum growth is spatially coordinated during septation in S. pombe Stochastic growth also occurs in cells; it occurs in septation during cytokinesis in fungi and bacteria when cell wall synthases grow the division septum (Balasubramanian et al, 2012;Pollard and Wu, 2010), in the assembly of microtubules or actin filaments in the cytoskeleton (Desai and Mitchison, 1997;Vavylonis et al, 2005) or in polymerase-mediated DNA synthesis from nucleotides (Geertsema et al, 2014). In such cases, molecular randomness leads to shape or length fluctuations in the assembled structures.…”

Section: Discussion Stochastic Growth Leads To Rough Interfacesmentioning

confidence: 99%

The fission yeast cytokinetic contractile ring regulates septum shape and closure

Thiyagarajan

Munteanu

Arasada

et al. 2015

Journal of Cell Science

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During cytokinesis, fission yeast and other fungi and bacteria grow a septum that divides the cell in two. In fission yeast closure of the circular septum hole by the β-glucan synthases (Bgs) and other glucan synthases in the plasma membrane is tightly coupled to constriction of an actomyosin contractile ring attached to the membrane. It is unknown how septum growth is coordinated over scales of several microns to maintain septum circularity. Here, we documented the shapes of ingrowing septum edges by measuring the roughness of the edges, a measure of the deviation from circularity. The roughness was small, with spatial correlations indicative of spatially coordinated growth. We hypothesized that Bgs-mediated septum growth is mechanosensitive and coupled to contractile ring tension. A mathematical model showed that ring tension then generates almost circular septum edges by adjusting growth rates in a curvature-dependent fashion. The model reproduced experimental roughness statistics and showed that septum synthesis sets the mean closure rate. Our results suggest that the fission yeast cytokinetic ring tension does not set the constriction rate but regulates septum closure by suppressing roughness produced by inherently stochastic molecular growth processes.

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“…[1][2][3][4] Because of the highly stereotyped sequence of events that characterize this process and of the strong phylogenetic conservation of the underlying molecular machinery, 2,5 cytokinesis is currently considered a 'default' biological process, occurring similarly in the different cell types. However, it is well known that specialized proliferating cells are characterized by significant variations of the standard scheme, such as incomplete cytokinesis in trophoblast cells, hepatocytes, Purkinije neurons, cardiomyocytes 6 and spermatogonia 7 and asymmetric cytokinesis in meiotic oocytes and in cortical neuroepithelial precursors.…”

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confidence: 99%

Tissue-specific control of midbody microtubule stability by Citron kinase through modulation of TUBB3 phosphorylation

et al. 2015

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Cytokinesis, the physical separation of daughter cells at the end of cell cycle, is commonly considered a highly stereotyped phenomenon. However, in some specialized cells this process may involve specific molecular events that are still largely unknown. In mammals, loss of Citron-kinase (CIT-K) leads to massive cytokinesis failure and apoptosis only in neuronal progenitors and in male germ cells, resulting in severe microcephaly and testicular hypoplasia, but the reasons for this specificity are unknown. In this report we show that CIT-K modulates the stability of midbody microtubules and that the expression of tubulin β-III (TUBB3) is crucial for this phenotype. We observed that TUBB3 is expressed in proliferating CNS progenitors, with a pattern correlating with the susceptibility to CIT-K loss. More importantly, depletion of TUBB3 in CIT-K-dependent cells makes them resistant to CIT-K loss, whereas TUBB3 overexpression increases their sensitivity to CIT-K knockdown. The loss of CIT-K leads to a strong decrease in the phosphorylation of S444 on TUBB3, a post-translational modification associated with microtubule stabilization. CIT-K may promote this event by interacting with TUBB3 and by recruiting at the midbody casein kinase-2α (CK2α) that has previously been reported to phosphorylate the S444 residue. Indeed, CK2α is lost from the midbody in CIT-K-depleted cells. Moreover, expression of the nonphosphorylatable TUBB3 mutant S444A induces cytokinesis failure, whereas expression of the phospho-mimetic mutant S444D rescues the cytokinesis failure induced by both CIT-K and CK2α loss. Altogether, our findings reveal that expression of relatively low levels of TUBB3 in mitotic cells can be detrimental for their cytokinesis and underscore the importance of CIT-K in counteracting this event.

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Comparing contractile apparatus‐driven cytokinesis mechanisms across kingdoms

Cited by 38 publications

References 183 publications

Evidence That an Unconventional Actin Can Provide Essential F-Actin Function and That a Surveillance System Monitors F-Actin Integrity inChlamydomonas

Evidence That an Unconventional Actin Can Provide Essential F-Actin Function and That a Surveillance System Monitors F-Actin Integrity inChlamydomonas

The fission yeast cytokinetic contractile ring regulates septum shape and closure

Tissue-specific control of midbody microtubule stability by Citron kinase through modulation of TUBB3 phosphorylation

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