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TANGO1/cTAGE5 receptor as a polyvalent template for assembly of large COPII coats

Journal Article · · Proceedings of the National Academy of Sciences of the United States of America
 [1];  [1]
  1. Memorial Sloan Kettering Cancer Center, New York, NY (United States)

The supramolecular cargo procollagen is loaded into coat protein complex II (COPII)-coated carriers at endoplasmic reticulum (ER) exit sites by the receptor molecule TANGO1/cTAGE5. Electron microscopy studies have identified a tubular carrier of suitable dimensions that is molded by a distinctive helical array of the COPII inner coat protein Sec23/24•Sar1; the helical arrangement is absent from canonical COPII-coated small vesicles. In this study, we combined X-ray crystallographic and biochemical analysis to characterize the association of TANGO1/cTAGE5 with COPII proteins. The affinity for Sec23 is concentrated in the proline-rich domains (PRDs) of TANGO1 and cTAGE5, but Sec23 recognizes merely a PPP motif. The PRDs contain repeated PPP motifs separated by proline-rich linkers, so a single TANGO1/cTAGE5 receptor can bind multiple copies of coat protein in a close-packed array. We propose that TANGO1/cTAGE5 promotes the accretion of inner coat proteins to the helical lattice. As a result, we show that PPP motifs in the outer coat protein Sec31 also bind to Sec23, suggesting that stepwise COPII coat assembly will ultimately displace TANGO1/cTAGE5 and compartmentalize its operation to the base of the growing COPII tubule.

Research Organization:
Argonne National Laboratory (ANL), Argonne, IL (United States)
Sponsoring Organization:
Memorial Sloan Kettering Cancer Center
OSTI ID:
1322365
Journal Information:
Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 36 Vol. 113; ISSN 0027-8424
Publisher:
National Academy of SciencesCopyright Statement
Country of Publication:
United States
Language:
ENGLISH

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Cited By (22)

Subtomogram averaging of COPII assemblies reveals how coat organization dictates membrane shape journal October 2018
TANGO1 and SEC12 are copackaged with procollagen I to facilitate the generation of large COPII carriers journal December 2018
TANGO1 assembles into rings around COPII coats at ER exit sites journal March 2017
Protein sorting at the ER–Golgi interface journal November 2016
New insights into protein secretion: TANGO1 runs rings around the COPII coat journal March 2017
COPII-coated membranes function as transport carriers of intracellular procollagen I journal April 2017
TANGO1 recruits Sec16 to coordinately organize ER exit sites for efficient secretion journal April 2017
Protein transport by vesicles and tunnels journal February 2019
Fatty-acid binding protein 5 modulates the SAR1 GTPase cycle and enhances budding of large COPII cargoes journal February 2019
Integrated Stress Response and Decreased ECM in Cultured Stromal Cells From Keratoconus Corneas journal June 2018
Regulation of the Sar1 GTPase Cycle Is Necessary for Large Cargo Secretion from the Endoplasmic Reticulum journal August 2017
Role of Host Cell Secretory Machinery in Zika Virus Life Cycle journal October 2018
The Functional Role of SEC23 in Vesicle Transportation, Autophagy and Cancer journal January 2019
TANGO1 builds a machine for collagen export by recruiting and spatially organizing COPII, tethers and membranes journal March 2018
Membrane Transport at an Organelle Interface in the Early Secretory Pathway: Take Your Coat Off and Stay a While: Evolution of the metazoan early secretory pathway journal May 2018
Tango1 coordinates the formation of endoplasmic reticulum/Golgi docking sites to mediate secretory granule formation journal November 2019
ER-to-Golgi trafficking of procollagen in the absence of large carriers journal December 2018
Not just a cargo receptor for large cargoes; an emerging role of TANGO1 as an organizer of ER exit sites journal May 2019
Proximity-dependent proteomics of the Chlamydia trachomatis inclusion membrane reveals functional interactions with endoplasmic reticulum exit sites posted_content March 2018
COPII gets in shape: Lessons derived from morphological aspects of early secretion journal August 2018
COPII‐mediated trafficking at the ER/ERGIC interface journal May 2019
Proximity-dependent proteomics of the Chlamydia trachomatis inclusion membrane reveals functional interactions with endoplasmic reticulum exit sites journal April 2019

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