Release from Myosin V via Regulated Recruitment of an E3 Ubiquitin Ligase Controls Organelle Localization

Yau, Richard G.; Peng, Yutian; Valiathan, Rajeshwari R.; Birkeland, Shanda R.; Wilson, Thomas E.; Weisman, Lois S.

doi:10.1016/j.devcel.2014.02.001

Cited by 28 publications

(53 citation statements)

References 40 publications

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“…They carry a C-terminal RING finger domain that can catalyze both K48-and K63-linked ubiquitin chains (Loring et al 2008) and a central FHA domain that is thought to bind Thr-phosphorylated proteins (Durocher et al 2000). So far, Dma1 and Dma2 have been redundantly involved in spindle positioning, septin organization, and vacuole inheritance (Fraschini et al 2004;Merlini et al 2012;Chahwan et al 2013;Yau et al 2014). In this paper, we show that Dma1 and Dma2 also contribute to formin regulation.…”

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confidence: 81%

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Control of Formin Distribution and Actin Cable Assembly by the E3 Ubiquitin Ligases Dma1 and Dma2

Juanes¹,

Piatti²

2016

Genetics

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Formins are widespread actin-polymerizing proteins that play pivotal roles in a number of processes, such as cell polarity, morphogenesis, cytokinesis, and cell migration. In agreement with their crucial function, formins are prone to a variety of regulatory mechanisms that include autoinhibition, post-translational modifications, and interaction with formin modulators. Furthermore, activation and function of formins is intimately linked to their ability to interact with membranes. In the budding yeast Saccharomyces cerevisiae, the two formins Bni1 and Bnr1 play both separate and overlapping functions in the organization of the actin cytoskeleton. In addition, they are controlled by both common and different regulatory mechanisms. Here we show that proper localization of both formins requires the redundant E3 ubiquitin ligases Dma1 and Dma2, which were previously involved in spindle positioning and septin organization. In dma1 dma2 double mutants, formin distribution at polarity sites is impaired, thus causing defects in the organization of the actin cable network and hypersensitivity to the actin depolymerizer latrunculin B. Expression of a hyperactive variant of Bni1 (Bni1-V360D) rescues these defects and partially restores proper spindle positioning in the mutant, suggesting that the failure of dma1 dma2 mutant cells to position the spindle is partly due to faulty formin activity. Strikingly, Dma1/2 interact physically with both formins, while their ubiquitin-ligase activity is required for formin function and polarized localization. Thus, ubiquitylation of formin or a formin interactor(s) could promote formin binding to membrane and its ability to nucleate actin. Altogether, our data highlight a novel level of formin regulation that further expands our knowledge of the complex and multilayered controls of these key cytoskeleton organizers. KEYWORDS actin; formin; ubiquitylation; budding yeast T HE ability to polarize is a fundamental property of all types of cells, being crucial for numerous cellular processes such as proliferation, differentiation, and morphogenesis. Indeed, dysregulation of cell polarity can underlie developmental disorders and cancers (Wodarz and Nathke 2007). Cell polarization is strictly linked to the reorganization of the cytoskeleton and in particular of the actin network, whose dynamics must be tightly controlled for polarized processes to occur properly.The unicellular budding yeast Saccharomyces cerevisiae divides asymmetrically and undergoes highly polarized cell growth throughout its life cycle. Most aspects of polarized growth in budding yeast arise from a precise arrangement of the cortical actin cytoskeleton during the cell cycle. Three main actin structures can be found in yeast cells: (i) actin patches, which are sites of active endocytosis, (ii) actin cables, which serve as tracks for polarized secretion and segregation of organelles, and (iii) the contractile acto-myosin ring, which is involved in cytokinesis (Adams and Pringle 1984;Kilmartin and Adams 1984;Bi et ...

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confidence: 81%

“…The redundant Dma1 and Dma2 proteins are E3 ubiquitin ligases of the RING finger family (Joazeiro and Weissman 2000) that had been previously implicated in a number of polarized processes, such as septin organization, spindle positioning, and vacuole inheritance (Fraschini et al 2004;Merlini et al 2012;Chahwan et al 2013;Yau et al 2014). …”

Section: Discussionmentioning

confidence: 99%

Control of Formin Distribution and Actin Cable Assembly by the E3 Ubiquitin Ligases Dma1 and Dma2

Juanes¹,

Piatti²

2016

Genetics

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“…Recently, yeast E3 ligase Dma1 has been shown to control the release of the myosin V cargo (25). It seems likely that the Arabidopsis homolog of this ubiquitin ligase similarly functions as a regulator of myosin XI cargo attachment.…”

Section: Resultsmentioning

confidence: 99%

Myosin-driven transport network in plants

Kurth

Peremyslov

Turner

et al. 2017

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

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We investigate the myosin XI-driven transport network in Arabidopsis using protein-protein interaction, subcellular localization, gene knockout, and bioinformatics analyses. The two major groups of nodes in this network are myosins XI and their membrane-anchored receptors (MyoB) that, together, drive endomembrane trafficking and cytoplasmic streaming in the plant cells. The network shows high node connectivity and is dominated by generalists, with a smaller fraction of more specialized myosins and receptors. We show that interaction with myosins and association with motile vesicles are common properties of the MyoB family receptors. We identify previously uncharacterized myosin-binding proteins, putative myosin adaptors that belong to two unrelated families, with four members each (MadA and MadB). Surprisingly, MadA1 localizes to the nucleus and is rapidly transported to the cytoplasm, suggesting the existence of myosin XI-driven nucleocytoplasmic trafficking. In contrast, MadA2 and MadA3, as well as MadB1, partition between the cytosolic pools of motile endomembrane vesicles that colocalize with myosin XI-K and diffuse material that does not. Gene knockout analysis shows that MadB1-4 contribute to polarized root hair growth, phenocopying myosins, whereas MadA1-4 are redundant for this process. Phylogenetic analysis reveals congruent evolutionary histories of the myosin XI, MyoB, MadA, and MadB families. All these gene families emerged in green algae and show concurrent expansions via serial duplication in flowering plants. Thus, the myosin XI transport network increased in complexity and robustness concomitantly with the land colonization by flowering plants and, by inference, could have been a major contributor to this process.myosins | receptors | adaptors | cytoplasmic streaming | nuclear transport F or half of a century, it had been assumed that rapid organelle trafficking and cytoplasmic streaming in plant cells rely on myosin motors (1) and, in particular, class XI myosins that are homologous to fungal and animal class V myosins (2). Over the past decade, a massive amount of information on specific functions of myosins and mechanisms of myosin XI-dependent processes in plants has been obtained (3-5). The first genetic evidence of myosin function in cell expansion involved the demonstration of a dramatic reduction of the polarized root hair growth upon inactivation of the myosin XI-K and XI-2 genes (6, 7). Subsequently, it has been shown that myosindependent trafficking is required for the growth of multiple cell types, as well as normal plant growth and development (4,(8)(9)(10). Among the 13 paralogous myosins XI encoded in the Arabidopsis thaliana genome, the highly expressed myosins XI-K, XI-1, and XI-2 have been shown to provide the most pronounced, functionally redundant contributions to each of these processes. In contrast, another highly expressed paralog, myosin XI-I, plays only limited roles in cell and plant growth but has a specialized function in nuclear repositioning through binding nuclear e...

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“…Myo2 also transports vacuoles through binding the vacuole specific adaptor Vac17, which is degraded following ubiquitination mediated by a novel E3-ubiquitin ligase Dma1 and its paralogue Dma2, to release the cargo. Dma1 and Dma2 are also required for peroxisome movements in yeast [37]. GTP hydrolysis by associated Rabs is also proposed as a mechanism for release of exocytic vesicles from myosin V in yeast [38], so it remains to be seen if either or both mechanisms function in plants to release peroxisomes from their molecular motors.…”

Section: Peroxisome Movementmentioning

confidence: 99%

The life of the peroxisome: from birth to death

Baker

Paudyal

2014

Current Opinion in Plant Biology

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Peroxisomes are dynamic and metabolically plastic organelles. Their multiplicity of functions impacts on many aspects of plant development and survival. New functions for plant peroxisomes such as in the synthesis of biotin, ubiquinone and phylloquinone are being uncovered and their role in generating reactive oxygen species (ROS) and reactive nitrogen species (RNS) as signalling hubs in defence and development is becoming appreciated. Understanding of the biogenesis of peroxisomes, mechanisms of import and turnover of their protein complement, and the wholesale destruction of the organelle by specific autophagic processes is giving new insight into the ways that plants can adjust peroxisome function in response to changing needs.

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Release from Myosin V via Regulated Recruitment of an E3 Ubiquitin Ligase Controls Organelle Localization

Cited by 28 publications

References 40 publications

Control of Formin Distribution and Actin Cable Assembly by the E3 Ubiquitin Ligases Dma1 and Dma2

Control of Formin Distribution and Actin Cable Assembly by the E3 Ubiquitin Ligases Dma1 and Dma2

Myosin-driven transport network in plants

The life of the peroxisome: from birth to death

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