Cdc42 and its BORG2 and BORG3 effectors control the subcellular localization of septins between actin stress fibers and microtubules

Salameh, Joëlle; Cantaloube, Isabelle; Benoit, Béatrice; Poüs, Christian; Baillet, Anita

doi:10.1016/j.cub.2021.07.004

Cited by 26 publications

(53 citation statements)

References 79 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The findings of this study lead to several remaining open questions. In the absence of the identification of actin-binding domains on septins, it is still unclear if SF decoration by septins in cells reflects direct septin-actin interactions, or if such binding occurs through myosin-II or/and Borg proteins (Calvo et al, 2015; Farrugia et al, 2020; Joberty et al, 2001; Joo et al, 2007; Liu et al, 2014; Mostowy et al, 2010; Salameh et al, 2021). The fact that septins are found only on contractile SFs lets one suppose that myosin-II related signaling might be involved in their recruitment to SFs but this remains to be shown.…”

Section: Discussionmentioning

confidence: 99%

“…There is no doubt that septins can associate both with actin and microtubules in cells (Bowen et al, 2011; Nagata et al, 2004; Nagata et al, 2003; Spiliotis et al, 2008; Spiliotis et al, 2005; Surka et al, 2002; Verdier-Pinard et al, 2017). The microtubule-binding domain on septins was identified recently (Kuzmic et al, 2022), but actin-binding domains have not yet been identified making it unclear if actin-septin binding involves direct interactions, or if such binding occurs through myosin-II (Joo et al, 2007; Mostowy et al, 2010) or/and Borg proteins (Calvo et al, 2015; Farrugia et al, 2020; Joberty et al, 2001; Liu et al, 2014; Salameh et al, 2021). Similarly, although recombinant and cell-purified mammalian septins bind lipid membranes in the absence of other physiological partners (Bridges et al, 2016; Dolat and Spiliotis, 2016; Szuba et al, 2021; Tanaka-Takiguchi et al, 2009; Yamada et al, 2016), whether there is direct septin-membrane binding in cells has not been formally shown; the identification of the membrane-binding site of septins is a matter of debate (Cavini et al, 2021).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Human septins in cells organize as octamer-based filaments mediating actin-membrane anchoring

Martins

Taveneau

Castro-Linares

et al. 2022

Preprint

View full text Add to dashboard Cite

Septins are cytoskeletal proteins conserved from algae and protists to mammals. Septin knock-out animals have established that septins are essential for animal physiology, but their molecular function remains elusive. A unique feature of septins is their presence as heteromeric complexes that polymerize into filaments in solution and on lipid membranes. Although animal septins associate extensively with actin-based structures in cells, whether actin-decorating septins organize as filaments and if septin organization impacts septin function is not known. Customizing a tripartite split-GFP complementation assay for probing the presence and composition of septin filaments in situ in cells, we show that all septins decorating actin stress fibers are present as filaments whose integrity depends on octameric septin protomers. Atomic force microscopy nanoindentation measurements on cells confirmed that cell stiffness depends on the presence of octamer-containing septin filaments. Super-resolution structured illumination microscopy revealed septin fibers with widths compatible with their organization as paired septin filaments. Nanometer-resolved distance measurements and single-protein tracking further showed that actin-associated septin filaments are membrane-bound and largely immobilized. Finally, reconstitution assays on supported lipid bilayers showed that septin filaments mediate actin-membrane anchoring. We propose that septin organization as octamer-based filaments is essential for septin function in anchoring and stabilizing actin fibers at the plasma membrane.

show abstract

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Human septins in cells organize as octamer-based filaments mediating actin-membrane anchoring

Martins

Taveneau

Castro-Linares

et al. 2022

Preprint

View full text Add to dashboard Cite

show abstract

“…Overexpression of Cdc42 cause a loss of septin filaments ( Joberty et al, 2001 ). A recent study shows that Cdc42 controls the subcellular localization of septins between actin stress fibers and microtubules ( Salameh et al, 2021 ).…”

Section: Septins In Endothelial Cellsmentioning

confidence: 99%

Role of Septins in Endothelial Cells and Platelets

Neubauer

Zieger

2021

Front. Cell Dev. Biol.

View full text Add to dashboard Cite

Septins are conserved cytoskeletal GTP-binding proteins identified in almost all eukaryotes except higher plants. Mammalian septins comprise 13 family members with either ubiquitous or organ- and tissue-specific expression patterns. They form filamentous oligomers and complexes with other proteins to serve as diffusions barrier and/or multi-molecular scaffolds to function in a physiologically regulated manner. Diverse septins are highly expressed in endothelial cells and platelets, which play an important role in hemostasis, a process to prevent blood loss after vascular injury. Endothelial septins are involved in cellular processes such as exocytosis and in processes concerning organismal level, like angiogenesis. Septins are additionally found in endothelial cell-cell junctions where their presence is required to maintain the integrity of the barrier function of vascular endothelial monolayers. In platelets, septins are important for activation, degranulation, adhesion, and aggregation. They have been identified as mediators of distinct platelet functions and being essential in primary and secondary hemostatic processes. Septin-knockout mouse studies show the relevance of septins in several aspects of hemostasis. This is in line with reports that dysregulation of septins is clinically relevant in human bleeding disorders. The precise function of septins in the biology of endothelial cells and platelets remains poorly understood. The following mini-review highlights the current knowledge about the role of septin cytoskeleton in regulating critical functions in these two cell types.

show abstract

“…Anita Baillet (Université Paris-Saclay, INSERM, France) found that the interplay between septins, actin and microtubules can be regulated by the nucleotide state of Cdc42 and its downstream effectors of the BORG family. Indeed, Taxol ®induced Cdc42 inactivation triggers the release of BORG2 from stress fibers and its subsequent proteasome-mediated degradation, resulting in the striking relocalization of septins from actin to microtubules (Salameh et al, 2021). Folma Buss (University of Cambridge, UK) spoke about their work that identified LRCH3 not only as a novel adaptor protein linking the actin-based motor MYO6 and the RhoGEF DOCK7 and forming the septin DISP complex, but also as a novel regulator of septin organization (O'Loughlin et al, 2018).…”

Section: Septin Compartmentalization and Related Functionsmentioning

confidence: 99%

Meeting report – the ever-fascinating world of septins

Baillet

McMurray

Oakes

2021

Journal of Cell Science

Self Cite

View full text Add to dashboard Cite

Septins are GTP-binding proteins that assemble into hetero-oligomers. They can interact with each other end-to-end to form filaments, making them the fourth element of the cytoskeleton. To update the current knowledge on the ever-increasing implications of these fascinating proteins in cellular functions, a hundred expert scientists from across the globe gathered from 12 to 15 October 2021 in Berlin for the first hybrid-format (on site and virtual) EMBO workshop Molecular and Cell Biology of Septins.

show abstract

Cdc42 and its BORG2 and BORG3 effectors control the subcellular localization of septins between actin stress fibers and microtubules

Cited by 26 publications

References 79 publications

Human septins in cells organize as octamer-based filaments mediating actin-membrane anchoring

Human septins in cells organize as octamer-based filaments mediating actin-membrane anchoring

Role of Septins in Endothelial Cells and Platelets

Meeting report – the ever-fascinating world of septins

Contact Info

Product

Resources

About