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Sequential and compartmentalized action of Rabs, SNAREs, and MAL in the apical delivery of fusiform vesicles in urothelial umbrella cells

Uroplakins (UPs) are major differentiation products of urothelial umbrella cells and play important roles in forming the permeability barrier and in the expansion/stabilization of the apical membrane. Further, UPIa serves as a uropathogenic Escherichia coli receptor. Although it is understood that U...

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Autores principales: Wankel, Bret, Ouyang, Jiangyong, Guo, Xuemei, Hadjiolova, Krassimira, Miller, Jeremy, Liao, Yi, Tham, Daniel Kai Long, Romih, Rok, Andrade, Leonardo R., Gumper, Iwona, Simon, Jean-Pierre, Sachdeva, Rakhee, Tolmachova, Tanya, Seabra, Miguel C., Fukuda, Mitsunori, Schaeren-Wiemers, Nicole, Hong, Wan Jin, Sabatini, David D., Wu, Xue-Ru, Kong, Xiangpeng, Kreibich, Gert, Rindler, Michael J., Sun, Tung-Tien
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The American Society for Cell Biology 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4865319/
https://www.ncbi.nlm.nih.gov/pubmed/27009205
http://dx.doi.org/10.1091/mbc.E15-04-0230
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author Wankel, Bret
Ouyang, Jiangyong
Guo, Xuemei
Hadjiolova, Krassimira
Miller, Jeremy
Liao, Yi
Tham, Daniel Kai Long
Romih, Rok
Andrade, Leonardo R.
Gumper, Iwona
Simon, Jean-Pierre
Sachdeva, Rakhee
Tolmachova, Tanya
Seabra, Miguel C.
Fukuda, Mitsunori
Schaeren-Wiemers, Nicole
Hong, Wan Jin
Sabatini, David D.
Wu, Xue-Ru
Kong, Xiangpeng
Kreibich, Gert
Rindler, Michael J.
Sun, Tung-Tien
author_facet Wankel, Bret
Ouyang, Jiangyong
Guo, Xuemei
Hadjiolova, Krassimira
Miller, Jeremy
Liao, Yi
Tham, Daniel Kai Long
Romih, Rok
Andrade, Leonardo R.
Gumper, Iwona
Simon, Jean-Pierre
Sachdeva, Rakhee
Tolmachova, Tanya
Seabra, Miguel C.
Fukuda, Mitsunori
Schaeren-Wiemers, Nicole
Hong, Wan Jin
Sabatini, David D.
Wu, Xue-Ru
Kong, Xiangpeng
Kreibich, Gert
Rindler, Michael J.
Sun, Tung-Tien
author_sort Wankel, Bret
collection PubMed
description Uroplakins (UPs) are major differentiation products of urothelial umbrella cells and play important roles in forming the permeability barrier and in the expansion/stabilization of the apical membrane. Further, UPIa serves as a uropathogenic Escherichia coli receptor. Although it is understood that UPs are delivered to the apical membrane via fusiform vesicles (FVs), the mechanisms that regulate this exocytic pathway remain poorly understood. Immunomicroscopy of normal and mutant mouse urothelia show that the UP-delivering FVs contained Rab8/11 and Rab27b/Slac2-a, which mediate apical transport along actin filaments. Subsequently a Rab27b/Slp2-a complex mediated FV–membrane anchorage before SNARE-mediated and MAL-facilitated apical fusion. We also show that keratin 20 (K20), which forms a chicken-wire network ∼200 nm below the apical membrane and has hole sizes allowing FV passage, defines a subapical compartment containing FVs primed and strategically located for fusion. Finally, we show that Rab8/11 and Rab27b function in the same pathway, Rab27b knockout leads to uroplakin and Slp2-a destabilization, and Rab27b works upstream from MAL. These data support a unifying model in which UP cargoes are targeted for apical insertion via sequential interactions with Rabs and their effectors, SNAREs and MAL, and in which K20 plays a key role in regulating vesicular trafficking.
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spelling pubmed-48653192016-07-30 Sequential and compartmentalized action of Rabs, SNAREs, and MAL in the apical delivery of fusiform vesicles in urothelial umbrella cells Wankel, Bret Ouyang, Jiangyong Guo, Xuemei Hadjiolova, Krassimira Miller, Jeremy Liao, Yi Tham, Daniel Kai Long Romih, Rok Andrade, Leonardo R. Gumper, Iwona Simon, Jean-Pierre Sachdeva, Rakhee Tolmachova, Tanya Seabra, Miguel C. Fukuda, Mitsunori Schaeren-Wiemers, Nicole Hong, Wan Jin Sabatini, David D. Wu, Xue-Ru Kong, Xiangpeng Kreibich, Gert Rindler, Michael J. Sun, Tung-Tien Mol Biol Cell Articles Uroplakins (UPs) are major differentiation products of urothelial umbrella cells and play important roles in forming the permeability barrier and in the expansion/stabilization of the apical membrane. Further, UPIa serves as a uropathogenic Escherichia coli receptor. Although it is understood that UPs are delivered to the apical membrane via fusiform vesicles (FVs), the mechanisms that regulate this exocytic pathway remain poorly understood. Immunomicroscopy of normal and mutant mouse urothelia show that the UP-delivering FVs contained Rab8/11 and Rab27b/Slac2-a, which mediate apical transport along actin filaments. Subsequently a Rab27b/Slp2-a complex mediated FV–membrane anchorage before SNARE-mediated and MAL-facilitated apical fusion. We also show that keratin 20 (K20), which forms a chicken-wire network ∼200 nm below the apical membrane and has hole sizes allowing FV passage, defines a subapical compartment containing FVs primed and strategically located for fusion. Finally, we show that Rab8/11 and Rab27b function in the same pathway, Rab27b knockout leads to uroplakin and Slp2-a destabilization, and Rab27b works upstream from MAL. These data support a unifying model in which UP cargoes are targeted for apical insertion via sequential interactions with Rabs and their effectors, SNAREs and MAL, and in which K20 plays a key role in regulating vesicular trafficking. The American Society for Cell Biology 2016-05-15 /pmc/articles/PMC4865319/ /pubmed/27009205 http://dx.doi.org/10.1091/mbc.E15-04-0230 Text en © 2016 Wankel et al. This article is distributed by The American Society for Cell Biology under license from the author(s). Two months after publication it is available to the public under an Attribution–Noncommercial–Share Alike 3.0 Unported Creative Commons License (http://creativecommons.org/licenses/by-nc-sa/3.0). “ASCB®,” “The American Society for Cell Biology®,” and “Molecular Biology of the Cell®” are registered trademarks of The American Society for Cell Biology.
spellingShingle Articles
Wankel, Bret
Ouyang, Jiangyong
Guo, Xuemei
Hadjiolova, Krassimira
Miller, Jeremy
Liao, Yi
Tham, Daniel Kai Long
Romih, Rok
Andrade, Leonardo R.
Gumper, Iwona
Simon, Jean-Pierre
Sachdeva, Rakhee
Tolmachova, Tanya
Seabra, Miguel C.
Fukuda, Mitsunori
Schaeren-Wiemers, Nicole
Hong, Wan Jin
Sabatini, David D.
Wu, Xue-Ru
Kong, Xiangpeng
Kreibich, Gert
Rindler, Michael J.
Sun, Tung-Tien
Sequential and compartmentalized action of Rabs, SNAREs, and MAL in the apical delivery of fusiform vesicles in urothelial umbrella cells
title Sequential and compartmentalized action of Rabs, SNAREs, and MAL in the apical delivery of fusiform vesicles in urothelial umbrella cells
title_full Sequential and compartmentalized action of Rabs, SNAREs, and MAL in the apical delivery of fusiform vesicles in urothelial umbrella cells
title_fullStr Sequential and compartmentalized action of Rabs, SNAREs, and MAL in the apical delivery of fusiform vesicles in urothelial umbrella cells
title_full_unstemmed Sequential and compartmentalized action of Rabs, SNAREs, and MAL in the apical delivery of fusiform vesicles in urothelial umbrella cells
title_short Sequential and compartmentalized action of Rabs, SNAREs, and MAL in the apical delivery of fusiform vesicles in urothelial umbrella cells
title_sort sequential and compartmentalized action of rabs, snares, and mal in the apical delivery of fusiform vesicles in urothelial umbrella cells
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4865319/
https://www.ncbi.nlm.nih.gov/pubmed/27009205
http://dx.doi.org/10.1091/mbc.E15-04-0230
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