BMP signaling requires retromer-dependent recycling of the type I receptor

Gleason, Ryan J; Akintobi, Adenrele M.; Grant, Barth D.; Padgett, Richard W.

doi:10.1073/pnas.1319947111

Cited by 72 publications

(115 citation statements)

References 41 publications

(42 reference statements)

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“…Several co-factors have been identified as regulators of BMP receptor trafficking [31–38]. Some of them down-regulate BMP signaling [31–35,38], while others help maintain it [36,37]. We propose that the Scrib-Rab5 system is a flexible module for receptor trafficking and can be utilized for optimizing a signal.…”

Section: Discussionmentioning

confidence: 99%

Scribbled Optimizes BMP Signaling through Its Receptor Internalization to the Rab5 Endosome and Promote Robust Epithelial Morphogenesis

2016

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Epithelial cells are characterized by apical-basal polarity. Intrinsic factors underlying apical-basal polarity are crucial for tissue homeostasis and have often been identified to be tumor suppressors. Patterning and differentiation of epithelia are key processes of epithelial morphogenesis and are frequently regulated by highly conserved extrinsic factors. However, due to the complexity of morphogenesis, the mechanisms of precise interpretation of signal transduction as well as spatiotemporal control of extrinsic cues during dynamic morphogenesis remain poorly understood. Wing posterior crossvein (PCV) formation in Drosophila serves as a unique model to address how epithelial morphogenesis is regulated by secreted growth factors. Decapentaplegic (Dpp), a conserved bone morphogenetic protein (BMP)-type ligand, is directionally trafficked from longitudinal veins (LVs) into the PCV region for patterning and differentiation. Our data reveal that the basolateral determinant Scribbled (Scrib) is required for PCV formation through optimizing BMP signaling. Scrib regulates BMP-type I receptor Thickveins (Tkv) localization at the basolateral region of PCV cells and subsequently facilitates Tkv internalization to Rab5 endosomes, where Tkv is active. BMP signaling also up-regulates scrib transcription in the pupal wing to form a positive feedback loop. Our data reveal a unique mechanism in which intrinsic polarity genes and extrinsic cues are coupled to promote robust morphogenesis.

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Section: Discussionmentioning

confidence: 99%

Scribbled Optimizes BMP Signaling through Its Receptor Internalization to the Rab5 Endosome and Promote Robust Epithelial Morphogenesis

2016

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“…Retromer protein VPS-35/Vps35 and retromerassociated protein SNX-3/Snx3 are key components for retrograde recycling in many different organisms. In C. elegans, SNX-3 and VPS-35 have been found to regulate the proper sorting of retrograde cargo MIG-14, Type I TGF-β receptor SMA-6, and TGN-38 (7,44,66). As our aforementioned results indicate that retromer associated proteins RME-8 and SNX-1 limit HGRS-1 degradative domain size, we also investigated the role of VPS-35 and SNX-3 in maintaining the degradative domain.…”

Section: Not All Retromer Associated Proteins Are Important For Domainmentioning

confidence: 93%

SNX-1 and RME-8 oppose the assembly of HGRS-1/ESCRT-0 degradative microdomains on endosomes

Norris

Tammineni

Wang

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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After endocytosis, transmembrane cargo reaches endosomes, where it encounters complexes dedicated to opposing functions: recycling and degradation. Microdomains containing endosomal sorting complexes required for transport (ESCRT)-0 component Hrs [hepatocyte growth factor-regulated tyrosine kinase substrate (HGRS-1) in Caenorhabditis elegans] mediate cargo degradation, concentrating ubiquitinated cargo and organizing the activities of ESCRT. At the same time, retromer associated sorting nexin one (SNX-1) and its binding partner, J-domain protein RME-8, sort cargo away from degradation, promoting cargo recycling to the Golgi. Thus, we hypothesized that there could be important regulatory interactions between retromer and ESCRT that balance degradative and recycling functions. Taking advantage of the naturally large endosomes of the C. elegans coelomocyte, we visualized complementary ESCRT-0 and RME-8/SNX-1 microdomains in vivo and assayed the ability of retromer and ESCRT microdomains to regulate one another. We found in snx-1(0) and rme-8(ts) mutants increased endosomal coverage and intensity of HGRS-1-labeled microdomains, as well as increased total levels of HGRS-1 bound to membranes. These effects are specific to SNX-1 and RME-8, as loss of other retromer components SNX-3 and vacuolar protein sorting-associated protein 35 (VPS-35) did not affect HGRS-1 microdomains. Additionally, knockdown of hgrs-1 had little to no effect on SNX-1 and RME-8 microdomains, suggesting directionality to the interaction. Separation of the functionally distinct ESCRT-0 and SNX-1/RME-8 microdomains was also compromised in the absence of RME-8 and SNX-1, a phenomenon we observed to be conserved, as depletion of Snx1 and Snx2 in HeLa cells also led to greater overlap of Rme-8 and Hrs on endosomes.endosome | SNX-1 | RME-8 | Hrs | clathrin

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“…To verify the generality of our finding, we further examined two other endogenous CIE cargo proteins: GLUT1 and DAF-4 (dauer formation-defective-4), the C. elegans homolog of type II BMP (bone morphogenetic protein) receptor. Both proteins are CIE cargoes that are transported via the Arf6-associated itinerary (2,35,41). As shown in Fig.…”

Section: Dual Involvement Of Sec-10 In Apical and Basolateral Endosomalmentioning

confidence: 99%

SEC-10 and RAB-10 coordinate basolateral recycling of clathrin-independent cargo through endosomal tubules in Caenorhabditis elegans

Chen

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

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Despite the increasing number of regulatory proteins identified in clathrin-independent endocytic (CIE) pathways, our understanding of the exact functions of these proteins and the sequential manner in which they function remains limited. In this study, using the Caenorhabditis elegans intestine as a model, we observed a unique structure of interconnected endosomal tubules, which is required for the basolateral recycling of several CIE cargoes including hTAC, GLUT1, and DAF-4. SEC-10 is a subunit of the octameric protein complex exocyst. Depleting SEC-10 and several other exocyst components disrupted the endosomal tubules into various ring-like structures. An epistasis analysis further suggested that SEC-10 operates at the intermediate step between early endosomes and recycling endosomes. The endosomal tubules were also sensitive to inactivation of the Rab GTPase RAB-10 and disruption of microtubules. Taken together, our data suggest that SEC-10 coordinates with RAB-10 and microtubules to form the endosomal tubular network for efficient recycling of particular CIE cargoes.endosomal tubules | recycling | microtubule | clathrin-independent endocytosis | live worm imaging

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BMP signaling requires retromer-dependent recycling of the type I receptor

Cited by 72 publications

References 41 publications

Scribbled Optimizes BMP Signaling through Its Receptor Internalization to the Rab5 Endosome and Promote Robust Epithelial Morphogenesis

Scribbled Optimizes BMP Signaling through Its Receptor Internalization to the Rab5 Endosome and Promote Robust Epithelial Morphogenesis

SNX-1 and RME-8 oppose the assembly of HGRS-1/ESCRT-0 degradative microdomains on endosomes

SEC-10 and RAB-10 coordinate basolateral recycling of clathrin-independent cargo through endosomal tubules in Caenorhabditis elegans

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