Opposing functions of F-BAR proteins in neuronal membrane protrusion, tubule formation, and neurite outgrowth

Taylor, Kendra L.; Taylor, Richard T.; Richters, Karl E; Huynh, Brandon; Carrington, Justin; McDermott, Maeve E; Wilson, Rebecca L.; Dent, Erik W.

doi:10.26508/lsa.201800288

Cited by 20 publications

(23 citation statements)

References 58 publications

(102 reference statements)

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“…Interestingly, a recent work showed FBP17 isoform-specific function in neuronal morphology as well as an IDR-dependent membrane tubulation activity in cells. The IDR domain of FBP17 was found to be more potent in inducing neurite formation (Taylor et al, 2019). Consistent with our findings, such property of IDR of FBP17 is not shared by the IDR in CIP4.…”

Section: Limitations Of the Studysupporting

confidence: 90%

Comparative study of curvature sensing mediated by F-BAR domain and an intrinsically disordered region of FBP17

Zhuang

Miao

et al. 2020

Preprint

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Membrane curvature has emerged as an intriguing physical organization principle underlying biological signaling and membrane trafficking. FBP17 of the CIP4/FBP17/Toca-1 F-BAR family is unique in the BAR family because its structurally folded F-BAR domain does not contain any hydrophobic motifs that insert into lipid bilayer. While it has been widely assumed so, whether the banana-shaped F-BAR domain alone can sense curvature has never been experimentally demonstrated. Using a nanopillar-supported lipid bilayer system, we found that the F-BAR domain of FBP17 displayed minimal curvature sensing in vitro. We further identified an alternatively spliced intrinsically disordered region (IDR) of FBP17 next to its F-BAR domain that is conserved in sequence across species. The IDR senses membrane curvature and its sensing ability greatly exceeds that of F-BAR domain alone. In living cells, presence of the IDR domain changed the dynamics of FBP17 recruitment in a curvature-coupled cortical wave system. Collectively, we propose that FBP17 does sense curvature but contrary to the common belief, its curvature sensing capability largely originates from its disordered region, not F-BAR domain itself.

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Section: Limitations Of the Studysupporting

confidence: 90%

Comparative study of curvature sensing mediated by F-BAR domain and an intrinsically disordered region of FBP17

Zhuang

Miao

et al. 2020

Preprint

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“…The FBAR domain of FBP17 is necessary and sufficient for curvature sensing. ,, Upon transient transfection, we found that the truncated tdTom-SspBmicro-FBAR construct appeared to be almost exclusively cytosolic and did not result in the formation of membrane tubulation, whereas similar expression levels of full-length FBP17 constructs showed considerable amounts of tubulation before light. The observation that the FBP17 FBAR has a lower affinity for the membrane than full-length FBP17 has also been suggested in a recent study that shows multiple regions of FBP17 outside of its FBAR domain, contributing to its membrane binding . Upon coexpression of tdTomato-SspBmicro-FBP17BAR and iLID-EGFP-CAAX, blue light elicited a robust membrane tubulation response (Figure D, with full field images in Figure S4).…”

Section: Resultssupporting

confidence: 72%

“…The observation that the FBP17 FBAR has a lower affinity for the membrane than full-length FBP17 has also been suggested in a recent study that shows multiple regions of FBP17 outside of its FBAR domain contributing to its membrane binding. 35 Upon co-expression of tdTomato-micro-FBP17BAR and iLID-EGFP-CAAX, blue light elicited a robust membrane tubulation response ( Figure 2D, with full field images in Supplementary Figure S4 ). Red channel images show tdTom-micro-FBP17BAR is highly cytosolic before addition of blue light.…”

Section: Construction and Optimization Of The Opto-fbar Systemsmentioning

confidence: 99%

Light-Inducible Generation of Membrane Curvature in Live Cells with Engineered BAR Domain Proteins

2020

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Nanoscale membrane curvature is now understood to play an active role in essential cellular processes such as endocytosis, exocytosis and actin dynamics. Previous studies have shown that membrane curvatures directly affect protein functions and intracellular signaling. However, few methods are able to precisely manipulate membrane curvature in live cells. Here, we report the development of a new method of generating nanoscale membrane curvature in live cells that is controllable, reversible, and capable of precise spatial and temporal manipulation. For this purpose, we make use of BAR domain proteins, a family of well-studied membrane-remodeling and membrane-sculpting proteins. Specifically, we engineered two optogenetic systems, opto-FBAR and opto-IBAR, that allow light-inducible formation of positive and negative membrane curvature respectively. Using opto-FBAR, blue light activation results in the formation of tubular membrane invaginations (positive curvature), controllable down to the subcellular level. Using opto-IBAR, blue light illumination results in the formation of membrane protrusions or filopodia (negative curvature). These systems present a novel approach for light-inducible manipulation of nanoscale membrane curvature in live cells. Highlights• Opto-FBAR enables light-inducible positive membrane curvature formation.• Opto-IBAR enables light-inducible negative membrane curvature formation.• Light-inducible activation enables precise spatial and temporal control.• Opto-BAR systems present a new approach for studying membranes in live cells.

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“…Interestingly, a recent work showed FBP17 isoform-specific function in neuronal morphology as well as an IDR-dependent membrane tubulation activity in cells. The IDR domain of FBP17 was found to be more potent in inducing neurite formation ( Taylor et al., 2019 ). Consistent with our findings, such property of IDR of FBP17L is not shared by the IDR in CIP4.…”

Section: Discussionmentioning

confidence: 99%

Comparative Study of Curvature Sensing Mediated by F-BAR and an Intrinsically Disordered Region of FBP17

Zhuang

Miao

et al. 2020

iScience

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Membrane curvature has emerged as an intriguing physical principle underlying biological signaling and membrane trafficking. The CIP4/FBP17/Toca-1 F-BAR subfamily is unique in the BAR family because its structurally folded F-BAR domain does not contain any hydrophobic motifs that insert into membrane. Although widely assumed so, whether the banana-shaped F-BAR domain alone can sense curvature has never been experimentally demonstrated. Using a nanobar-supported lipid bilayer system, we found that the F-BAR domain of FBP17 displayed minimal curvature sensing in vitro. In comparison, an alternatively spliced intrinsically disordered region (IDR) adjacent to the F-BAR domain has the membrane curvature-sensing ability greatly exceeding that of F-BAR domain alone. In living cells, the presence of the IDR delayed the recruitment of FBP17 in curvature-coupled cortical waves. Collectively, we propose that contrary to the common belief, FBP17's curvature-sensing capability largely originates from IDR, and not the F-BAR domain alone.

show abstract

Opposing functions of F-BAR proteins in neuronal membrane protrusion, tubule formation, and neurite outgrowth

Cited by 20 publications

References 58 publications

Comparative study of curvature sensing mediated by F-BAR domain and an intrinsically disordered region of FBP17

Comparative study of curvature sensing mediated by F-BAR domain and an intrinsically disordered region of FBP17

Light-Inducible Generation of Membrane Curvature in Live Cells with Engineered BAR Domain Proteins

Comparative Study of Curvature Sensing Mediated by F-BAR and an Intrinsically Disordered Region of FBP17

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