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A tensile trilayered cytoskeletal endotube drives capillary-like lumenogenesis
Khan,Liakot A.1; Jafari,Gholamali1; Zhang,Nan1,2; Membreno,Edward1; Yan,Siyang1; Zhang,Hongjie1,3; Gobel,Verena1
2019
Source PublicationJournal of Cell Biology
ISSN0021-9525
Volume218Issue:7Pages:2403-2424
Abstract

Unicellular tubes are components of internal organs and capillaries. It is unclear how they meet the architectural challenge to extend a centered intracellular lumen of uniform diameter. In an RNAi-based Caenorhabditis elegans screen, we identified three intermediate filaments (IFs)—IFA-4, IFB-1, and IFC-2—as interactors of the lumenal membrane-actin linker ERM-1 in excretory-canal tubulogenesis. We find that IFs, generally thought to affect morphogenesis indirectly by maintaining tissue integrity, directly promote lumenogenesis in this capillary-like single-cell tube. We show that ERM-1, ACT-5/actin, and TBB-2/ tubulin recruit membrane-forming endosomal and flux-promoting canalicular vesicles to the lumen, whereas IFs, themselves recruited to the lumen by ERM-1 and TBB-2, restrain lateral vesicle access. IFs thereby prevent cystogenesis, equilibrate the lumen diameter, and promote lumen forward extension. Genetic and imaging analyses suggest that IFB-1/IFA-4 and IFB-1/IFC-2 polymers form a perilumenal triple IF lattice, sandwiched between actin and helical tubulin. Our findings characterize a novel mechanism of capillary-like lumenogenesis, where a tensile trilayered cytoskeletal endotube transforms concentric into directional growth.

DOI10.1083/jcb.201811175
URLView the original
Indexed BySCIE
Language英語English
WOS Research AreaCell Biology
WOS SubjectCell Biology
WOS IDWOS:000473328200027
Scopus ID2-s2.0-85069266128
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Citation statistics
Document TypeJournal article
CollectionFaculty of Health Sciences
Corresponding AuthorGobel,Verena
Affiliation1.Mucosal Immunology and Biology Research Center,Developmental Biology and Genetics Core,Massachusetts General Hospital for Children,Harvard Medical School,Boston,United States
2.Key Laboratory of Zoonosis Research,Institute of Zoonosis,College of Veterinary Medicine,Jilin University,Changchun,China
3.Faculty of Health Sciences,University of Macau,Taipa,Macao
Recommended Citation
GB/T 7714
Khan,Liakot A.,Jafari,Gholamali,Zhang,Nan,et al. A tensile trilayered cytoskeletal endotube drives capillary-like lumenogenesis[J]. Journal of Cell Biology, 2019, 218(7), 2403-2424.
APA Khan,Liakot A.., Jafari,Gholamali., Zhang,Nan., Membreno,Edward., Yan,Siyang., Zhang,Hongjie., & Gobel,Verena (2019). A tensile trilayered cytoskeletal endotube drives capillary-like lumenogenesis. Journal of Cell Biology, 218(7), 2403-2424.
MLA Khan,Liakot A.,et al."A tensile trilayered cytoskeletal endotube drives capillary-like lumenogenesis".Journal of Cell Biology 218.7(2019):2403-2424.
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