Function and regulation of <i>Saccharomyces cerevisiae</i> myosins-I in endocytic budding

Giblin, Jonathan P.; Fernández-Golbano, Isabel María; Idrissi, Fátima-Zahra; Geli, Maribel

doi:10.1042/bst0391185

Cited by 12 publications

(8 citation statements)

References 55 publications

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“…Myo1s are ancient, widely expressed myosins that link membranes to the actin cytoskeleton (McIntosh and Ostap 2016;Kollmar and Mühlhausen 2017). The budding and fission yeast Myo1s recruit activators of the Arp2/3 complex to actin patches to drive internalization of endocytic vesicles (Giblin et al 2011). Each chytrid species has one or two Myo1s, which we predict serve the same function and localize to the cortical actin patches observed in Bd and Sp zoospores and sporangia (Fig 1; (Medina et al 2020).…”

Section: Chytrids Have Typical Fungal Myosins As Well As Myth-ferm Mymentioning

confidence: 67%

The actin networks of chytrid fungi reveal evolutionary loss of cytoskeletal complexity in the fungal kingdom

Prostak

Robinson

Titus

et al. 2020

Preprint

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Cells from across the eukaryotic tree use actin polymers and a number of conserved regulators for a wide variety of functions including endocytosis, cytokinesis, and cell migration. Despite this conservation, the actin cytoskeleton has undergone significant evolution and diversification, highlighted by the differences in the actin cytoskeletal networks of mammalian cells and yeast. Chytrid fungi diverged before the emergence of the Dikarya (multicellular fungi and yeast), and therefore provide a unique opportunity to study the evolution of the actin cytoskeleton. Chytrids have two life stages: zoospore cells that can swim with a flagellum, and sessile sporangial cells that, like multicellular fungi, are encased in a chitinous cell wall. Here we show that zoospores of the amphibian-killing chytrid Batrachochytrium dendrobatidis (Bd) build dynamic actin structures that resemble those of animal cells, including pseudopods, an actin cortex, and filopodia-like actin spikes. In contrast, Bd sporangia assemble actin patches similar to those of yeast, as well as perinuclear actin shells. Our identification of actin cytoskeletal elements in the genomes of five species of chytrid fungi indicate that these actin structures are controlled by both fungalspecific components as well as actin regulators and myosin motors found in animals but not other fungal lineages. The use of specific small molecule inhibitors indicate that nearly all of Bd's actin structures are dynamic and use distinct nucleators: while pseudopods and actin patches are Arp2/3-dependent, the actin cortex appears formin-dependent, and actin spikes require both nucleators. The presence of animal-and yeast-like actin cytoskeletal components in the genome combined with the intermediate actin phenotypes in Bd suggests that the simplicity of the yeast cytoskeleton may be due to evolutionary loss. evolutionary Rosetta Stone with which we can map the simplified actin features of yeast to those of animals.Bd, like other chytrids, has two developmental stages: motile "zoospore" cells that lack a cellwall and swim with a flagellum, and non-motile sporangia that grow and produce new zoospores ( Fig. 1b; (Berger et al. 2005;Longcore et al. 1999). We recently showed that zoospores can also crawl across surfaces using actin-filled, Arp2/3-dependent pseudopods (Fritz-Laylin, Lord, et al. 2017). Other than these pseudopods, actin's role in any developmental stage of Bd has not been studied. To fill this knowledge gap, we identified homologs of key actin regulatory proteins and myosin motors in multiple species of chytrids and related fungi. We also identified new actin structures in zoospores and sporangia, and tested the requirements of Arp2/3 and formin family proteins for their assembly. We find that both the regulatory networks and actin structures of Bd are intermediate in complexity between animals and Dikarya, suggesting that the streamlined actin networks of common model fungi are a result of secondary evolutionary loss of actin network components. RESULTS Bd has dev...

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Section: Chytrids Have Typical Fungal Myosins As Well As Myth-ferm Mymentioning

confidence: 67%

The actin networks of chytrid fungi reveal evolutionary loss of cytoskeletal complexity in the fungal kingdom

Prostak

Robinson

Titus

et al. 2020

Preprint

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“…pombe and S . cerevisiae type I myosins induce Arp2/3-complex dependent actin polymerization in vitro [32,39–42], which requires their interaction with the conserved homologs of Wiskott-Aldrich syndrome protein (WASP) and WASP-interacting protein (WIP) [32,39]. …”

Section: Resultsmentioning

confidence: 99%

Evolution of the SH3 Domain Specificity Landscape in Yeasts

et al. 2015

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To explore the conservation of Src homology 3 (SH3) domain-mediated networks in evolution, we compared the specificity landscape of these domains among four yeast species, Saccharomyces cerevisiae, Ashbya gossypii, Candida albicans, and Schizosaccharomyces pombe, encompassing 400 million years of evolution. We first aligned and catalogued the families of SH3-containing proteins in these four species to determine the relationships between homologous domains. Then, we tagged and purified all soluble SH3 domains (82 in total) to perform a quantitative peptide assay (SPOT) for each SH3 domain. All SPOT readouts were hierarchically clustered and we observed that the organization of the SH3 specificity landscape in three distinct profile classes remains conserved across these four yeast species. We also produced a specificity profile for each SH3 domain from manually aligned top SPOT hits and compared the within-family binding motif consensus. This analysis revealed a striking example of binding motif divergence in a C. albicans Rvs167 paralog, which cannot be explained by overall SH3 sequence or interface residue divergence, and we validated this specificity change with a yeast two-hybrid (Y2H) assay. In addition, we show that position-weighted matrices (PWM) compiled from SPOT assays can be used for binding motif screening in potential binding partners and present cases where motifs are either conserved or lost among homologous SH3 interacting proteins. Finally, by comparing pairwise SH3 sequence identity to binding profile correlation we show that for ~75% of all analyzed families the SH3 specificity profile was remarkably conserved over a large evolutionary distance. Thus, a high sequence identity within an SH3 domain family predicts conserved binding specificity, whereas divergence in sequence identity often coincided with a change in binding specificity within this family. As such, our results are important for future studies aimed at unraveling complex specificity networks of peptide recognition domains in higher eukaryotes, including mammals.

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“…Myosin Is have been implicated in endocytosis in several different organisms including yeast [Giblin et al, 2011] and Entamoeba [Voigt et al, 1999]. The yeast myosin Is have long tails and they target to the plasma membrane where they work in concert with each other to drive membrane invagination and vesicle scission in an actindependent manner [Giblin et al, 2011]. Vertebrate longtailed Myo1e [Krendel et al, 2007;Cheng et al, 2012;Maxeiner et al, 2015] and short-tailed Myo1g [Dart et al, 2012] each play a crucial role in endocytosis, including Fcg receptor-driven phagocytosis [Dart et al, 2012;Maxeiner et al, 2015].…”

Section: Discussionmentioning

confidence: 99%

Selective localization of myosin‐I proteins in macropinosomes and actin waves

et al. 2016

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Class I myosins are widely expressed with roles in endocytosis and cell migration in a variety of cell types. Dictyostelium express multiple myosin Is, including three short-tailed (Myo1A, Myo1E, Myo1F) and three long-tailed (Myo1B, Myo1C, Myo1D). Here we report the molecular basis of the specific localizations of short-tailed Myo1A, Myo1E and Myo1F compared to our previously determined localization of long-tailed Myo1B. Myo1A and Myo1B have common and unique localizations consistent with the various features of their tail region; specifically the BH sites in their tails are required for their association with the plasma membrane and heads are sufficient for relocalization to the front of polarized cells. Myo1A does not localize to actin waves and macropinocytic protrusions, in agreement with the absence of a tail region which is required for these localizations of Myo1B. However, in spite of the overall similarity of their domain structures, the cellular distributions of Myo1E and Myo1F are quite different from Myo1A. Myo1E and Myo1F, but not Myo1A, are associated with macropinocytic cups and actin waves. The localizations of Myo1E and Myo1F in macropinocytic structures and actin waves differ from the localization of Myo1B. Myo1B colocalizes with F-actin in the actin waves and at the tips of mature macropinocytic cups whereas Myo1E and Myo1F are in the interior of actin waves and along the entire surface of macropinocytic cups. Our results point to different mechanisms of targeting of short- and long-tailed myosin Is, and are consistent with these myosins having both shared and divergent cellular functions.

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Function and regulation of Saccharomyces cerevisiae myosins-I in endocytic budding

Cited by 12 publications

References 55 publications

The actin networks of chytrid fungi reveal evolutionary loss of cytoskeletal complexity in the fungal kingdom

The actin networks of chytrid fungi reveal evolutionary loss of cytoskeletal complexity in the fungal kingdom

Evolution of the SH3 Domain Specificity Landscape in Yeasts

Selective localization of myosin‐I proteins in macropinosomes and actin waves

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