A physical mechanism of TANGO1-mediated bulky cargo export

Raote, Ishier; Chabanon, Morgan; Walani, Nikhil; Arroyo, Marino; García‐Parajó, María F.; Malhotra, Vivek; Campelo, Felix

doi:10.7554/elife.59426

Cited by 36 publications

(38 citation statements)

References 98 publications

(190 reference statements)

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“…(ii) The localization and function of COPII as a gatekeeper at the ER–ERES boundary is consistent with its emerging role in quality control ( Ma et al, 2017 ; Mezzacasa and Helenius, 2002 ). (iii) Our model is compatible with the export mechanism proposed for large cargo molecules such as procollagen ( Raote et al, 2020 ; Raote and Malhotra, 2019 ; Raote et al, 2018 ; Saito et al, 2009 ). Essentially, the localization of COPII to the ER–ERES boundary is preempting the need for a variety of coat configurations to fit different cargo shapes and sizes.…”

Section: Discussionsupporting

confidence: 81%

COPII collar defines the boundary between ER and ER exit site and does not coat cargo containers

Shomron

Nevo-Yassaf

Aviad

et al. 2021

Journal of Cell Biology

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COPII and COPI mediate the formation of membrane vesicles translocating in opposite directions within the secretory pathway. Live-cell and electron microscopy revealed a novel mode of function for COPII during cargo export from the ER. COPII is recruited to membranes defining the boundary between the ER and ER exit sites, facilitating selective cargo concentration. Using direct observation of living cells, we monitored cargo selection processes, accumulation, and fission of COPII-free ERES membranes. CRISPR/Cas12a tagging, the RUSH system, and pharmaceutical and genetic perturbations of ER-Golgi transport demonstrated that the COPII coat remains bound to the ER–ERES boundary during protein export. Manipulation of the cargo-binding domain in COPII Sec24B prohibits cargo accumulation in ERES. These findings suggest a role for COPII in selecting and concentrating exported cargo rather than coating Golgi-bound carriers. These findings transform our understanding of coat proteins’ role in ER-to-Golgi transport.

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Section: Discussionsupporting

confidence: 81%

COPII collar defines the boundary between ER and ER exit site and does not coat cargo containers

Shomron

Nevo-Yassaf

Aviad

et al. 2021

Journal of Cell Biology

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“…These accumulated elastic stresses can provide the energy required for membrane fission (Long et al, 2010). Such fission would likely be supported by force applied to the bud as depicted in the Raote-Chabanon model (Figure 2C; Raote et al, 2020a). In another scenario, COPII mediates fission.…”

Section: Tango1 and The Regulation Of Copii-mediated Membrane Fissionmentioning

confidence: 99%

“…How can the molecular and physical properties of TANGO1 regulate carrier size and/or donor-acceptor membrane connectivity? Raote, Chabanon, and colleagues took to biophysicsbased modeling to address this question (Raote et al, 2020a). They examined how a physical TANGO1 fence affects COPII coat polymerization, curvature, membrane tension, and the force required to buckle the membrane while transiently stabilizing a non-constricted neck that allows for cargo packaging and formation of a large carrier.…”

Section: Tango1 and A Balancing Act Between Fission And Fusionmentioning

confidence: 99%

“…A key issue raised by the model is the timing of fission, which is controlled by TANGO1 activities. The interactions of TANGO1 with rigid long procollagens during loading into carriers may physically inhibit the fission reaction (Figure 2C; Raote et al, 2020a). TANGO1 activities can also regulate Sar1.…”

Section: Tango1 and The Regulation Of Copii-mediated Membrane Fissionmentioning

confidence: 99%

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A tango for coats and membranes: New insights into ER-to-Golgi traffic

Aridor

2022

Cell Reports

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The realization that the meticulous organization of cellular organelles is not required for the reconstitution of select intracellular traffic steps has revolutionized cell biology. It transformed the discipline from a morphological one into a molecular one. It helped in defining the activities of COPII and COPI vesicle coats in secretion. The work established the principles of the vesicular traffic model as envisioned by George Palade 50 years ago. However, in recent years, numerous advances in cellular and imaging technologies afforded an unprecedented molecular resolution that sheds new light on COPII activities and biosynthetic traffic between the ER and the Golgi. In the following review, I summarize this new information and attempt to provide a unified physical-molecular-morphological description of this traffic step. This information expands on the simplistic principles of vesicular traffic and provides novel frameworks to examine and explain physiological secretion. COAT-MEDIATED INTRACELLULAR TRAFFIC: CHALLENGING THE DOGMAIntracellular traffic is carried by vesicles-this dogma, pioneered by the work of George Palade, has guided the field for the past 50 years (Palade, 1975). Vesicular traffic has been documented across species throughout evolution and in the different cellular sorting sites during endo-and exocytosis (Mellman and Emr, 2013;Traub and Bonifacino, 2013). Vesicles bud from donor membranes, travel in space, tether, and fuse with acceptor membranes to deliver cargoes (Figure 1). Vesicles are formed by the activity of coats, cytosolic protein complexes that are recruited to donor membranes to bud vesicles. Recruitment is mediated by small guanosine triphosphatases (GTPases) (secretion) or through activation by facilitators that drive conformational change (internalization; Kirchhausen et al., 2014;Miller and Schekman, 2013). Once recruited, coats interact with membranes and cargoes. Through such interactions, the coats sort and collect cargoes, tethers, and fusion machinery into membrane domains that are molded into buds and vesicles with help from coat polymerization. Once vesicles bud and uncoat, tether and fusion activities will deliver cargo to the acceptor membrane. This dogma was established from robust combinations of data using genetic, cellular, and biochemical approaches in cells and cell-free reconstitution systems (Kirchhausen et al., 2014;Miller and Schekman, 2013). Yet recent work focusing on one of the key sorting sites in cells at ER exit sites that were monitored in an unprecedented resolution suggest otherwise (Shomron et al., 2021;Weigel et al., 2021). Instead of vesicles, connectivity between donor and acceptor membranes may drive traffic (Figure 1C), and ER exit site components, including TANGO1, direct such connectivity (Raote et al., 2021; Figure 2). Instead of coat-mediated vesicle formation, coat-assisted filters are proposed, sorting cargoes at an ER exit site gate. We may even have two coats, not one, contributing to the formation of one single tubular transport carri...

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“…Antonio's TRAPPIII structure reveals insights into the mechanisms of Rab1 activation to regulate secretory trafficking ( 4 ). Ishier Raote (CRG, Spain) shared the latest about the function of TANGO1 in creating a tunnel at the ER for export of bulky cargo ( 5 , 6 , 7 ), including some exciting unpublished results about the role of liquid–liquid phase separation (LLPS) in the assembly of TANGO1 at ER exit sites. Sessions 2 and 3, focused on trafficking through the Golgi compartments and secretory pathway, included talks by Ivan Castello Serrano (University of Virginia, USA) about the importance of lipid rafts for export of transmembrane proteins from the Golgi network, and Anup Parchure (Yale University, USA) whose work suggests that secretory granule biogenesis at the TGN is facilitated by LLPS.…”

Section: The Sciencementioning

confidence: 99%

An online gathering about the latest on molecular membrane biology

Bottanelli

Spang

Stefan

et al. 2021

Journal of Biological Chemistry

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This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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A physical mechanism of TANGO1-mediated bulky cargo export

Cited by 36 publications

References 98 publications

COPII collar defines the boundary between ER and ER exit site and does not coat cargo containers

COPII collar defines the boundary between ER and ER exit site and does not coat cargo containers

A tango for coats and membranes: New insights into ER-to-Golgi traffic

An online gathering about the latest on molecular membrane biology

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