Broadly conserved roles of TMEM131 family proteins in intracellular collagen assembly and secretory cargo trafficking

Zhang, Zhe; Bai, Meirong; Barbosa, Guilherme Oliveira; Chen, Andrew; Wei, Yuehua; Luo, Shuo; Wang, Xin; Wang, Bingying; Tsukui, Tohru; Li, Hao; Sheppard, Dean; Kornberg, Thomas B.; Dengke, K.

doi:10.1126/sciadv.aay7667

Cited by 46 publications

(53 citation statements)

References 68 publications

(88 reference statements)

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“…SURO-2/TMEM39, a suro-2 gene product, is a highly conserved protein found in animals. The secretion level of collagen proteins was drastically reduced in the suro-2 mutant, indicating SURO-2, rather than TANGO1/cTAGE5, may play a fundamental role in bulky collagen secretion like recently reported TMEM131 27 . Since TANGO1/cTAGE5 have only been found in higher animals, the TANGO1-cTAGE system may have evolved to enable transport of diverse collagens.…”

Section: Discussionmentioning

confidence: 53%

“…Recently reported TMEM131 recruits premature collagen monomers through the bacterial PapD chaperone-like domain and functions in collagen assembly and secretion. The C-terminal region of TMEM131 interacts with TRAPPC8, a component of the TRAPP tethering complex, and functions in collagen secretion 27 . In this regard, SURO-2/TMEM39 and TMEM-131/TMEM131 seem to cooperate in collagen secretion.…”

Section: Discussionmentioning

confidence: 99%

“…Recruitment and interaction of these proteins with COPII-related vesicles may be su cient for the export of bulky collagen from ER 11 . A recent study reported that TMEM131, ranging from nematodes to humans, commonly plays an important role in regulating collagen secretion 27 . However, the understanding of the underlying mechanism of collagen secretion through evolutionarily large vesicles is still limited.…”

Section: Introductionmentioning

confidence: 99%

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SURO-2/TMEM39 Facilitates Collagen Secretion through the Formation of Large COPII Vesicles

Lee

Sung²,

Lee³

et al. 2020

Preprint

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Fibrosis of various tissues is a typical disease caused by excessive production and secretion of extracellular matrix. We used Caenorhabditis elegans to investigate the formation of large transport vesicles to understand collagen secretion, a critical factor in fibrosis formation. The suro-2 mutant displays obvious defects in collagen secretion and cuticle structure including a rupture phenotype in early adults. Transmission electron microscopy exhibited that the cuticle thickness of the suro-2 mutant was severely reduced. SURO-2/TMEM39 has 8 transmembrane domains and localizes in the endoplasmic reticulum (ER) membrane. SURO-2 interacts directly with NPP-20/Sec13, a component of the coat protein II (COPII) complex responsible for ER-to-Golgi transport. SURO-2 and NPP-20 localized at the same large puncta, a large COPII vesicle enough to accommodate collagens. We report here that SURO-2/TMEM39 is highly conserved among animal species and is a specialized regulator of bulky collagen secretion rather than general transport in C. elegans.

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Section: Discussionmentioning

confidence: 53%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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SURO-2/TMEM39 Facilitates Collagen Secretion through the Formation of Large COPII Vesicles

Lee

Sung²,

Lee³

et al. 2020

Preprint

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“…Interestingly, a recent study described another single-pass transmembrane protein TMEM131 with two adjacent predicted membrane helices, which functions at the interface of two compartments. Again one of these helices must span the membrane, while the other is likely inserted into one leaflet of a compartment membrane (Zhang et al, 2020).…”

Section: Resultsmentioning

confidence: 99%

TANGO1 membrane helices create a lipid diffusion barrier at curved membranes

Raote

Ernst

Campelo

et al. 2020

Preprint

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20We have previously shown TANGO1 organises membranes at the interface of the 21 endoplasmic reticulum (ER) and ERGIC/Golgi (Raote et al., 2018). TANGO1 corrals 22 retrograde membranes at ER exit sites to create an export conduit. Here the retrograde 23 membrane is, in itself, an anterograde carrier. This mode of forward transport necessitates a 24 mechanism to prevent membrane mixing between ER and the retrograde membrane. 25TANGO1 has an unusual membrane helix organisation, composed of one membrane-26 spanning helix (TM) and another that penetrates the inner leaflet (IM). We have reconstituted 27 these membrane helices in model membranes and shown that TM and IM together reduce the 28 flow of lipids at a region of defined shape. We have also shown that the helices align 29 TANGO1 around an ER exit site. We suggest this is a mechanism to prevent membrane 30 mixing during TANGO1-mediated transfer of bulky secretory cargos from the ER to the 31 ERGIC/Golgi via a tunnel. 32 59 ER fold and trimerize into rigid, rod-like elements that are considered too large for 60 conventional COPII coated vesicle-mediated transport (Burgeson et al., 1985; Gorur et al.,

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“…Through its membrane helices, TANGO1 organizes ER exit sites by creating a lipid diffusion barrier and an export conduit for collagen (20). While requirement of TANGO1 for secretion may depend on specific collagen types, it remains unclear whether TANGO1's functions are broadly conserved in all animals (21,22).…”

Section: Introductionmentioning

confidence: 99%

The conserved ER-transmembrane protein TMEM39 coordinates with COPII to promote collagen secretion and prevent ER stress

Zhang

Luo

Barbosa

et al. 2020

Preprint

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Dysregulation of collagen production and secretion contributes to aging and tissue fibrosis of major organs. How premature collagen proteins in the endoplasmic reticulum (ER) route in specialized vesicles for secretion remains to be fully elucidated. Here, we report that TMEM39, an ER-localized transmembrane protein, regulates production and secretory cargo trafficking of procollagen. We identify the C. elegans orthologue TMEM-39 from an unbiased RNAi screen and show that deficiency of tmem-39 leads to striking defects in cuticle collagen production and constitutively high ER stress response. RNAi knockdown of the tmem-39 orthologue in Drosophila causes similar defects in collagen secretion in fat body cells. The cytosolic domain of the human orthologue TMEM39A binds to Sec23A, a vesicle coat protein that drives collagen secretion and vesicular trafficking. We propose that roles of TMEM39 in collagen secretion and preventing ER stress are likely evolutionarily conserved.

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Broadly conserved roles of TMEM131 family proteins in intracellular collagen assembly and secretory cargo trafficking

Cited by 46 publications

References 68 publications

SURO-2/TMEM39 Facilitates Collagen Secretion through the Formation of Large COPII Vesicles

SURO-2/TMEM39 Facilitates Collagen Secretion through the Formation of Large COPII Vesicles

TANGO1 membrane helices create a lipid diffusion barrier at curved membranes

The conserved ER-transmembrane protein TMEM39 coordinates with COPII to promote collagen secretion and prevent ER stress

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