Chibby promotes ciliary vesicle formation and basal body docking during airway cell differentiation

Burke, Michael C.; Li, Feng Qian; Cyge, Benjamin; Arashiro, Takeshi; Brechbuhl, Heather M.; Chen, Xingwang; Siller, Saul S.; Weiss, Matthew A.; O’Connell, Christopher B.; Love, Damon; Westlake, Christopher J.; Reynolds, Susan D.; Kuriyama, Ryoko; Takemaru, Ken Ichi

doi:10.1083/jcb.201406140

Cited by 84 publications

(131 citation statements)

References 52 publications

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“…Failure in vesicle docking to distal ends of centrioles has been previously reported for components of distal appendages, such as Cep164 and Cep123, that serve as adaptors for the binding of vesicles to the distal ends (Schmidt et al, 2012;Sillibourne et al, 2013;Tanos et al, 2013;Burke et al, 2014;Joo et al, 2013;Ye et al, 2014). Our data show that WDR8 or Cep135 knockdown does not decrease the centriolar levels of Cep164 or Cep123.…”

Section: Discussionsupporting

confidence: 53%

“…Distal appendage proteins, including Cep164 and Cep123 (also known as Cep89), have been reported to be indispensable for this initial step of ciliary membrane biogenesis (Schmidt et al, 2012;Tanos et al, 2013;Joo et al, 2013;Sillibourne et al, 2013;Burke et al, 2014;Ye et al, 2014). Moreover, a cascade of small GTPases regulates vesicle docking and fusion at the mother centriole.…”

Section: Introductionmentioning

confidence: 99%

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WDR8 is a centriolar satellite and centriole-associated protein that promotes ciliary vesicle docking during ciliogenesis

Kurtulmus

Wang

Ruppert

et al. 2016

Journal of Cell Science

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Ciliogenesis initiates at the mother centriole through a series of events that include membrane docking, displacement of cilia-inhibitory proteins and axoneme elongation. Centriolar proteins, in particular at distal and subdistal appendages, carry out these functions. Recently, cytoplasmic complexes named centriolar satellites have also been shown to promote ciliogenesis. Little is known about the functional and molecular relationship between appendage proteins, satellites and cilia biogenesis. Here, we identified the WD-repeat protein 8 (WDR8, also known as WRAP73) as a satellite and centriolar component. We show that WDR8 interacts with the satellite proteins SSX2IP and PCM1 as well as the centriolar proximal end component Cep135. Cep135 is required for the recruitment of WDR8 to centrioles. Depletion experiments revealed that WDR8 and Cep135 have strongly overlapping functions in ciliogenesis. Both are indispensable for ciliary vesicle docking to the mother centriole and for unlocking the distal end of the mother centriole from the ciliary inhibitory complex CP110-Cep97. Our data thus point to an important function of centriolar proximal end proteins in ciliary membrane biogenesis, and establish WDR8 and Cep135 as two factors that are essential for the initial steps of ciliation.

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Section: Discussionsupporting

confidence: 53%

Section: Introductionmentioning

confidence: 99%

WDR8 is a centriolar satellite and centriole-associated protein that promotes ciliary vesicle docking during ciliogenesis

Kurtulmus

Wang

Ruppert

et al. 2016

Journal of Cell Science

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“…The mother centrioles are distinguished from immature daughter centrioles by the presence of accessory structures, including the subdistal and distal appendages at their distal end. While the subdistal appendages anchor cytoplasmic microtubules, the distal appendages (also called "transition fibers" at the ciliary base) are thought to be critical for the recruitment of small vesicles and subsequent docking of basal bodies to the plasma membrane (5)(6)(7)(8). Since no protein synthesis occurs in cilia, ciliary proteins are transported from the cell body via polarized vesicle trafficking (9,10).…”

mentioning

confidence: 99%

BAR Domain-Containing FAM92 Proteins Interact with Chibby1 To Facilitate Ciliogenesis

Chen

Fisher

et al. 2016

Molecular and Cellular Biology

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dChibby1 (Cby1) is a small, conserved coiled-coil protein that localizes to centrioles/basal bodies and plays a crucial role in the formation and function of cilia. During early stages of ciliogenesis, Cby1 is required for the efficient recruitment of small vesicles at the distal end of centrioles to facilitate basal body docking to the plasma membrane. Here, we identified family with sequence similarity 92, member A (FAM92A) and FAM92B, which harbor predicted lipid-binding BAR domains, as novel Cby1-interacting partners using tandem affinity purification and mass spectrometry. We found that in cultured cell lines, FAM92A colocalizes with Cby1 at the centrioles/basal bodies of primary cilia, while FAM92B is undetectable. In airway multiciliated cells, both FAM92A and -92B colocalize with Cby1 at the base of cilia. Notably, the centriolar localization of FAM92A and -92B depends largely on Cby1. Knockdown of FAM92A in RPE1 cells impairs ciliogenesis. Consistent with the membrane-remodeling properties of BAR domains, FAM92A and -92B in cooperation with Cby1 induce deformed membrane-like structures containing the small GTPase Rab8 in cultured cells. Our results therefore suggest that FAM92 proteins interact with Cby1 to promote ciliogenesis via regulation of membrane-remodeling processes.

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“…[18][19][20][21][22] More recently, we demonstrated that, during differentiation of airway ciliated cells, Cby1 localizes to nascent centrioles and interacts with Rabin8, a guanine nucleotide exchange factor (GEF) for the small GTPase Rab8 to promote Rab8 recruitment for efficient assembly of membranous structures, called ciliary vesicles, at the distal end of centrioles. 18 Intriguingly, Rab8 has been shown to regulate cell shape, and expression of dominant-negative Rab8 mutants or depletion of Rab8 by small interfering (si) RNAs promotes an epithelial cell-like morphology including tight cell-cell contacts and actin stress fiber formation. 37 Therefore, it is possible that Cby1 K D suppresses Rab8 activity, leading to MET-like changes, independent of or in parallel to its association with b-catenin.…”

Section: Discussionmentioning

confidence: 99%

“…Cby1 also plays a crucial role during ciliogenesis, likely independent of b-catenin signaling. [18][19][20][21][22] Using human colon adenocarcinoma SW480 cells in which APC is mutated, we reported that stable expression of wildtype Cby1, but not a 14-3-3-binding-defective mutant (Cby1S20A), results in cytoplasmic translocation of b-catenin, concomitant with a reduction in b-catenin signaling and cell growth. 23 These results suggest a role for Cby1 as a tumor suppressor in colon cancer.…”

Section: Introductionmentioning

confidence: 99%

Chibby1 knockdown promotes mesenchymal-to-epithelial transition-like changes

Fischer

Wong

et al. 2017

Cell Cycle

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Chibby1 (Cby1) was originally isolated as a binding partner for b-catenin, a dual function protein in cell-cell adhesion and in canonical Wnt signaling. The canonical Wnt/b-catenin pathway is dysregulated in various diseases including cancer, most notably of the gastrointestinal origin. To investigate the role of Cby1 in colorectal tumorigenesis, we generated stable Cby1-knockdown (K D ) SW480 colon cancer cells. Unexpectedly, we found that Cby1 K D induces mesenchymal-to-epithelial transition (MET)-like changes in SW480 as well as in HEK293 cells. Cby1-K D cells displayed a cuboidal epithelial morphology with tight cellcell contacts. In Cby1-K D cells, the plasma membrane localization of E-cadherin and b-catenin was dramatically increased with formation of cortical actin rings, while the levels of the mesenchymal marker vimentin were decreased. Consistent with these changes, in wound healing assays, Cby1-K D cells exhibited epithelial cell-like properties as they migrated collectively as epithelial sheets. Furthermore, the anchorage-independent growth of Cby1-K D cells was reduced as determined by soft agar assays. These findings suggest that chronic Cby1 K D in colon cancer cells may counteract tumor progression by promoting the MET process.

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Chibby promotes ciliary vesicle formation and basal body docking during airway cell differentiation

Abstract: In the early stages of cilia formation in the mouse airway epithelium, Chibby is recruited to the distal appendages of centrioles and is necessary for efficient ciliary vesicle formation and basal body docking at the apical cell membrane.

Cited by 84 publications

References 52 publications

WDR8 is a centriolar satellite and centriole-associated protein that promotes ciliary vesicle docking during ciliogenesis

WDR8 is a centriolar satellite and centriole-associated protein that promotes ciliary vesicle docking during ciliogenesis

BAR Domain-Containing FAM92 Proteins Interact with Chibby1 To Facilitate Ciliogenesis

Chibby1 knockdown promotes mesenchymal-to-epithelial transition-like changes

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