The Cdc15 and Imp2 SH3 domains cooperatively scaffold a network of proteins that redundantly ensure efficient cell division in fission yeast

Ren, Liping; Willet, Alaina H.; Roberts-Galbraith, Rachel H.; McDonald, Nathan A.; Feoktistova, Anna; Chen, Jun‐Song; Huang, Haiming; Guillen, Rodrigo X.; Boone, Charles; Sidhu, Sachdev S.; Beckley, Janel R.; Gould, Kathleen L.

doi:10.1091/mbc.e14-10-1451

Cited by 53 publications

(109 citation statements)

References 66 publications

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“…Note that our specificity profile logos for the Sp Hof1 and Sp Hof1-2 SH3 domains are similar to the + XLPXXP motif observed by Ren and colleagues for these SH3 domains [21]. …”

Section: Supporting Informationsupporting

confidence: 81%

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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“…Note that our specificity profile logos for the Sp Hof1 and Sp Hof1-2 SH3 domains are similar to the + XLPXXP motif observed by Ren and colleagues for these SH3 domains [21]. …”

Section: Supporting Informationsupporting

confidence: 81%

Evolution of the SH3 Domain Specificity Landscape in Yeasts

et al. 2015

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“…8 While this is still surprising, the lack of oligomerization may be compensated for by other protein-protein interactions which enforce a local concentration of Imp2 at the division site. 42 Clearly though, these examples highlight the value of clarifying the importance of F-BAR domain oligomerization in other F-BAR proteins. As it is now established that F-BAR domains utilize different interaction surfaces to bind one another and oligomerize, this will not be a simple matter of creating homologous mutations, but will require elucidation of each protein's mechanism of oligomerization.…”

Section: Oligomerization and Membrane Bendingmentioning

confidence: 99%

“…This high avidity membrane binding is critical to accumulate and stabilize Cdc15 at the cell division site 9 where it recruits and scaffolds multiple cytokinesis proteins. 41,42 Mutations that disrupt F-BAR oligomerization sharply decrease the abundance and increase the turnover of Cdc15 at the division site, which consequently leads to cytokinetic failures. 9 Mutations in Fer that block oligomerization compromised its ability to induce lamellipodia formation and enhance cell migration, possibly due to a loss of strong localization to the leading edge membrane.…”

Section: Oligomerization and Membrane Bendingmentioning

confidence: 99%

“…69,70 Using redundant SH3 domains, these proteins recruit crucial contractile ring proteins including Fic1, Spa2, Rgf3, and Pxl1. 41,42 Oligomerization by Cdc15 is critical to localize its partners; oligomerization mutants recruit »50% less SH3 binding partners, compromising cytokinesis. 9 In S. cerevisiae, the homologous Hof1 F-BAR protein is also important for cytokinesis, recruiting Inn1 through its SH3 domain which activates the chitin synthase necessary for division.…”

Section: Scaffolding Functionsmentioning

confidence: 99%

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Linking up at the BAR: Oligomerization and F-BAR protein function

McDonald

Gould

2016

Cell Cycle

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As cells grow, move, and divide, they must reorganize and rearrange their membranes and cytoskeleton. The F-BAR protein family links cellular membranes with actin cytoskeletal rearrangements in processes including endocytosis, cytokinesis, and cell motility. Here we review emerging information on mechanisms of F-BAR domain oligomerization and membrane binding, and how these activities are coordinated with additional domains to accomplish scaffolding and signaling functions.

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“…In a quest to understand this Mid1-independent cytokinesis, the authors show that S. japonicus Cdc15 anchors the cytokinetic ring in the cell middle according to inhibitory spatial signals from the polarity kinase Pom1 at cell tips. Cdc15 is a conserved FCH family protein that stabilizes and scaffolds the cytokinetic ring in S. pombe cells as well [13–15]. The authors propose that S. japonicus Cdc15, unlike its S. pombe counterpart, can mark the cell middle during mitosis in the absence of Mid1.…”

mentioning

confidence: 99%