COPII-coated membranes function as transport carriers of intracellular procollagen I

Gorur, Amita; Yuan, Lin; Kenny, Samuel J.; Baba, Satoshi; Xu, Ke; Schekman, Randy

doi:10.1083/jcb.201702135

COPII-coated membranes function as transport carriers of intracellular procollagen I

Journal Article · Thu Apr 20 00:00:00 EDT 2017 · Journal of Cell Biology

DOI:https://doi.org/10.1083/jcb.201702135· OSTI ID:1352291

Gorur, Amita; Yuan, Lin; Kenny, Samuel J.; Baba, Satoshi; ;

The coat protein complex II (COPII) is essential for the transport of large cargo, such as 300-nm procollagen I (PC1) molecules, from the endoplasmic reticulum (ER) to the Golgi. Previous work has shown that the CUL3-KLHL12 complex increases the size of COPII vesicles at ER exit sites to more than 300 nm in diameter and accelerates the secretion of PC1. However, the role of large COPII vesicles as PC1 transport carriers was not unambiguously demonstrated. In this study, using stochastic optical reconstruction microscopy, correlated light electron microscopy, and live-cell imaging, we demonstrate the existence of mobile COPII-coated vesicles that completely encapsulate the cargo PC1 and are physically separated from ER. We also developed a cell-free COPII vesicle budding reaction that reconstitutes the capture of PC1 into large COPII vesicles. This process requires COPII proteins and the GTPase activity of the COPII subunit SAR1. We conclude that large COPII vesicles are bona fide carriers of PC1.

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Sponsoring Organization:: USDOE

OSTI ID:: 1352291

Journal Information:: Journal of Cell Biology, Journal Name: Journal of Cell Biology Journal Issue: 6 Vol. 216; ISSN 0021-9525

Publisher:: Rockefeller University PressCopyright Statement

Country of Publication:: United States

Language:: English

References (59)

COPII: A membrane coat formed by Sec proteins that drive vesicle budding from the endoplasmic reticulum Barlowe, C. Cell, Vol. 77, Issue 6 https://doi.org/10.1016/0092-8674(94)90138-4	journal	June 1994
Hsp47 as a Collagen-Specific Molecular Chaperone Ishida, Yoshihito; Nagata, Kazuhiro Biology of Serpins https://doi.org/10.1016/B978-0-12-386471-0.00009-2	book	January 2011
Structural implications from an electronmicroscopic comparison of procollagen V with procollagen I, pC-collagen I, procollagen IV, and a Drosophila procollagen. Bächinger, H. P.; Doege, K. J.; Petschek, J. P. Journal of Biological Chemistry, Vol. 257, Issue 24 https://doi.org/10.1016/S0021-9258(18)33314-3	journal	December 1982
Visualizing Intracellular Events In Vivo by Combined Video Fluorescence and 3‐D Electron Microscopy Mironov, Alexander A.; Beznoussenko, Galina V.; Luini, Alberto Methods in Enzymology https://doi.org/10.1016/S0076-6879(05)04005-X	book	January 2005
Visualization of ER-to-Golgi Transport in Living Cells Reveals a Sequential Mode of Action for COPII and COPI Scales, Suzie J.; Pepperkok, Rainer; Kreis, Thomas E. Cell, Vol. 90, Issue 6 https://doi.org/10.1016/S0092-8674(00)80379-7	journal	September 1997
COPII-Coated Vesicle Formation Reconstituted with Purified Coat Proteins and Chemically Defined Liposomes Matsuoka, Ken; Orci, Lelio; Amherdt, Mylène Cell, Vol. 93, Issue 2 https://doi.org/10.1016/S0092-8674(00)81577-9	journal	April 1998
Long-term sun exposure alters the collagen of thepapillary dermis Bernstein, Eric F.; Chen, Yue Qiu; Kopp, Jeffrey B. Journal of the American Academy of Dermatology, Vol. 34, Issue 2 https://doi.org/10.1016/S0190-9622(96)80114-9	journal	February 1996
Segregation of COPI-rich and anterograde-cargo-rich domains in endoplasmic-reticulum-to-Golgi transport complexes Shima, David T.; Scales, Suzie J.; Kreis, Thomas E. Current Biology, Vol. 9, Issue 15 https://doi.org/10.1016/S0960-9822(99)80365-0	journal	August 1999
ER-to-Golgi Carriers Arise through Direct En Bloc Protrusion and Multistage Maturation of Specialized ER Exit Domains Mironov, Alexander A.; Mironov, Alexander A.; Beznoussenko, Galina V. Developmental Cell, Vol. 5, Issue 4 https://doi.org/10.1016/S1534-5807(03)00294-6	journal	October 2003
Mutations in SEC24D, Encoding a Component of the COPII Machinery, Cause a Syndromic Form of Osteogenesis Imperfecta Garbes, Lutz; Kim, Kyungho; Rieß, Angelika The American Journal of Human Genetics, Vol. 96, Issue 3 https://doi.org/10.1016/j.ajhg.2015.01.002	journal	March 2015
Multicolor Fluorescence Nanoscopy in Fixed and Living Cells by Exciting Conventional Fluorophores with a Single Wavelength Testa, Ilaria; Wurm, Christian A.; Medda, Rebecca Biophysical Journal, Vol. 99, Issue 8 https://doi.org/10.1016/j.bpj.2010.08.012	journal	October 2010
COPII-coated vesicles: flexible enough for large cargo? Fromme, J. Christopher; Schekman, Randy Current Opinion in Cell Biology, Vol. 17, Issue 4 https://doi.org/10.1016/j.ceb.2005.06.004	journal	August 2005
TANGO1 Facilitates Cargo Loading at Endoplasmic Reticulum Exit Sites Saito, Kota; Chen, Mei; Bard, Fred Cell, Vol. 136, Issue 5 https://doi.org/10.1016/j.cell.2008.12.025	journal	March 2009
Regulation of the CUL3 Ubiquitin Ligase by a Calcium-Dependent Co-adaptor McGourty, Colleen A.; Akopian, David; Walsh, Carolyn Cell, Vol. 167, Issue 2 https://doi.org/10.1016/j.cell.2016.09.026	journal	October 2016
TFG Promotes Organization of Transitional ER and Efficient Collagen Secretion McCaughey, Janine; Miller, Victoria J.; Stevenson, Nicola L. Cell Reports, Vol. 15, Issue 8 https://doi.org/10.1016/j.celrep.2016.04.062	journal	May 2016
Shaping Cells and Organs in Drosophila by Opposing Roles of Fat Body-Secreted Collagen IV and Perlecan Pastor-Pareja, José Carlos; Xu, Tian Developmental Cell, Vol. 21, Issue 2 https://doi.org/10.1016/j.devcel.2011.06.026	journal	August 2011
Sizing and phenotyping of cellular vesicles using Nanoparticle Tracking Analysis Dragovic, Rebecca A.; Gardiner, Christopher; Brooks, Alexandra S. Nanomedicine: Nanotechnology, Biology and Medicine, Vol. 7, Issue 6 https://doi.org/10.1016/j.nano.2011.04.003	journal	December 2011
Multicolor Far-Field Fluorescence Nanoscopy through Isolated Detection of Distinct Molecular Species Bossi, Mariano; Fölling, Jonas; Belov, Vladimir N. Nano Letters, Vol. 8, Issue 8 https://doi.org/10.1021/nl801471d	journal	August 2008
Pelvic problems for mammals Presley, Robert Nature, Vol. 389, Issue 6650 https://doi.org/10.1038/38891	journal	October 1997
Ubiquitin-dependent regulation of COPII coat size and function Jin, Lingyan; Pahuja, Kanika Bajaj; Wickliffe, Katherine E. Nature, Vol. 482, Issue 7386 https://doi.org/10.1038/nature10822	journal	February 2012
Sec24b selectively sorts Vangl2 to regulate planar cell polarity during neural tube closure Merte, Janna; Jensen, Devon; Wright, Kevin Nature Cell Biology, Vol. 12, Issue 1 https://doi.org/10.1038/ncb2002	journal	December 2009
COPII and the regulation of protein sorting in mammals Zanetti, Giulia; Pahuja, Kanika Bajaj; Studer, Sean Nature Cell Biology, Vol. 14, Issue 1 https://doi.org/10.1038/ncb2390	journal	December 2011
Cranio-lenticulo-sutural dysplasia is caused by a SEC23A mutation leading to abnormal endoplasmic-reticulum-to-Golgi trafficking Boyadjiev, Simeon A.; Fromme, J. Christopher; Ben, Jin Nature Genetics, Vol. 38, Issue 10 https://doi.org/10.1038/ng1876	journal	September 2006
Secretory COPII coat component Sec23a is essential for craniofacial chondrocyte maturation Lang, Michael R.; Lapierre, Lynne A.; Frotscher, Michael Nature Genetics, Vol. 38, Issue 10 https://doi.org/10.1038/ng1880	journal	September 2006
Icy: an open bioimage informatics platform for extended reproducible research de Chaumont, Fabrice; Dallongeville, Stéphane; Chenouard, Nicolas Nature Methods, Vol. 9, Issue 7 https://doi.org/10.1038/nmeth.2075	journal	June 2012
Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM) Rust, Michael J.; Bates, Mark; Zhuang, Xiaowei Nature Methods, Vol. 3, Issue 10 https://doi.org/10.1038/nmeth929	journal	August 2006
A pseudoatomic model of the COPII cage obtained from cryo-electron microscopy and mass spectrometry Noble, Alex J.; Zhang, Qian; O'Donnell, Jason Nature Structural & Molecular Biology, Vol. 20, Issue 2 https://doi.org/10.1038/nsmb.2467	journal	December 2012
Multibudded tubules formed by COPII on artificial liposomes Bacia, Kirsten; Futai, Eugene; Prinz, Simone Scientific Reports, Vol. 1, Issue 1 https://doi.org/10.1038/srep00017	journal	June 2011
Neural tube opening and abnormal extraembryonic membrane development in SEC23A deficient mice Zhu, Min; Tao, Jiayi; Vasievich, Matthew P. Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep15471	journal	October 2015
Molecular basis for the action of the collagen-specific chaperone Hsp47/SERPINH1 and its structure-specific client recognition Widmer, C.; Gebauer, J. M.; Brunstein, E. Proceedings of the National Academy of Sciences, Vol. 109, Issue 33 https://doi.org/10.1073/pnas.1208072109	journal	July 2012
TANGO1/cTAGE5 receptor as a polyvalent template for assembly of large COPII coats Ma, Wenfu; Goldberg, Jonathan Proceedings of the National Academy of Sciences, Vol. 113, Issue 36 https://doi.org/10.1073/pnas.1605916113	journal	August 2016
Intracellular mechanisms of molecular recognition and sorting for transport of large extracellular matrix molecules Ishikawa, Yoshihiro; Ito, Shinya; Nagata, Kazuhiro Proceedings of the National Academy of Sciences, Vol. 113, Issue 41 https://doi.org/10.1073/pnas.1609571113	journal	September 2016
Direct in Vitro and in Vivo Evidence for Interaction between Hsp47 Protein and Collagen Triple Helix Ono, Takashi; Miyazaki, Takahiro; Ishida, Yoshihito Journal of Biological Chemistry, Vol. 287, Issue 9 https://doi.org/10.1074/jbc.M111.280248	journal	January 2012
SEC23-SEC31 the Interface Plays Critical Role for Export of Procollagen from the Endoplasmic Reticulum Kim, Sun-Don; Pahuja, Kanika Bajaj; Ravazzola, Mariella Journal of Biological Chemistry, Vol. 287, Issue 13 https://doi.org/10.1074/jbc.M111.283382	journal	February 2012
The pH-dependent Client Release from the Collagen-specific Chaperone HSP47 Is Triggered by a Tandem Histidine Pair Oecal, Sinan; Socher, Eileen; Uthoff, Matthias Journal of Biological Chemistry, Vol. 291, Issue 24 https://doi.org/10.1074/jbc.M115.706069	journal	April 2016
Sequence-specific Recognition of Collagen Triple Helices by the Collagen-specific Molecular Chaperone HSP47 Tasab, Mohammed; Jenkinson, Lynsey; Bulleid, Neil J. Journal of Biological Chemistry, Vol. 277, Issue 38 https://doi.org/10.1074/jbc.M202782200	journal	July 2002
Uncoupled Packaging of Amyloid Precursor Protein and Presenilin 1 into Coat Protein Complex II Vesicles Kim, Jinoh; Hamamoto, Susan; Ravazzola, Mariella Journal of Biological Chemistry, Vol. 280, Issue 9 https://doi.org/10.1074/jbc.M411091200	journal	December 2004
Intracellular interaction of collagen-specific stress protein HSP47 with newly synthesized procollagen Satoh, M. The Journal of Cell Biology, Vol. 133, Issue 2 https://doi.org/10.1083/jcb.133.2.469	journal	April 1996
Embryonic Lethality of Molecular Chaperone Hsp47 Knockout Mice Is Associated with Defects in Collagen Biosynthesis Nagai, Naoko; Hosokawa, Masanori; Itohara, Shigeyoshi The Journal of Cell Biology, Vol. 150, Issue 6 https://doi.org/10.1083/jcb.150.6.1499	journal	September 2000
Global defects in collagen secretion in a Mia3/TANGO1 knockout mouse Wilson, Deanna G.; Phamluong, Khanhky; Li, Li The Journal of Cell Biology, Vol. 193, Issue 5 https://doi.org/10.1083/jcb.201007162	journal	May 2011
Concentration of Sec12 at ER exit sites via interaction with cTAGE5 is required for collagen export Saito, Kota; Yamashiro, Koh; Shimazu, Noriko The Journal of Cell Biology, Vol. 206, Issue 6 https://doi.org/10.1083/jcb.201312062	journal	September 2014
TANGO1 and Mia2/cTAGE5 (TALI) cooperate to export bulky pre-chylomicrons/VLDLs from the endoplasmic reticulum Santos, António J. M.; Nogueira, Cristina; Ortega-Bellido, Maria The Journal of Cell Biology, Vol. 213, Issue 3 https://doi.org/10.1083/jcb.201603072	journal	May 2016
Loss of SEC-23 in Caenorhabditis elegans Causes Defects in Oogenesis, Morphogenesis, and Extracellular Matrix Secretion Roberts, Brett; Clucas, Caroline; Johnstone, Iain L. Molecular Biology of the Cell, Vol. 14, Issue 11 https://doi.org/10.1091/mbc.E03-03-0162	journal	November 2003
Type I Collagen in Hsp47-null Cells Is Aggregated in Endoplasmic Reticulum and Deficient in N-Propeptide Processing and Fibrillogenesis Ishida, Yoshihito; Kubota, Hiroshi; Yamamoto, Akitsugu Molecular Biology of the Cell, Vol. 17, Issue 5 https://doi.org/10.1091/mbc.E05-11-1065	journal	May 2006
cTAGE5 mediates collagen secretion through interaction with TANGO1 at endoplasmic reticulum exit sites Saito, Kota; Yamashiro, Koh; Ichikawa, Yuki Molecular Biology of the Cell, Vol. 22, Issue 13 https://doi.org/10.1091/mbc.E11-02-0143	journal	July 2011
Hsp47: a molecular chaperone that interacts with and stabilizes correctly-folded procollagen Tasab, Mohammed; Batten, Margaret R.; Bulleid, Neil J. The EMBO Journal, Vol. 19, Issue 10 https://doi.org/10.1093/emboj/19.10.2204	journal	May 2000
A Monoclonal Antibody Specific for the Amino Terminal Cleavage Site of Procollagen Type I Foellmer, Harald G.; Kawahara, Kazuko; Madri, Joseph A. European Journal of Biochemistry, Vol. 134, Issue 1 https://doi.org/10.1111/j.1432-1033.1983.tb07549.x	journal	July 1983
Three-Dimensional Super-Resolution Imaging by Stochastic Optical Reconstruction Microscopy Huang, B.; Wang, W.; Bates, M. Science, Vol. 319, Issue 5864 https://doi.org/10.1126/science.1153529	journal	February 2008
Sedlin Controls the ER Export of Procollagen by Regulating the Sar1 Cycle Venditti, R.; Scanu, T.; Santoro, M. Science, Vol. 337, Issue 6102 https://doi.org/10.1126/science.1224947	journal	September 2012
A novel multiprotein complex is required to generate the prechylomicron transport vesicle from intestinal ER Siddiqi, Shahzad; Saleem, Umair; Abumrad, Nada A. Journal of Lipid Research, Vol. 51, Issue 7 https://doi.org/10.1194/jlr.M005611	journal	March 2010
COPII proteins are required for Golgi fusion but not for endoplasmic reticulum budding of the pre-chylomicron transport vesicle Siddiqi, S. A. Journal of Cell Science, Vol. 116, Issue 2 https://doi.org/10.1242/jcs.00215	journal	December 2002
Efficient coupling of Sec23-Sec24 to Sec13-Sec31 drives COPII-dependent collagen secretion and is essential for normal craniofacial development Townley, A. K.; Feng, Y.; Schmidt, K. Journal of Cell Science, Vol. 121, Issue 18 https://doi.org/10.1242/jcs.031070	journal	August 2008
COPI-coated ER-to-Golgi transport complexes segregate from COPII in close proximity to ER exit sites Stephens, D. J.; Lin-Marq, N.; Pagano, A. Journal of Cell Science, Vol. 113, Issue 12 https://doi.org/10.1242/jcs.113.12.2177	journal	June 2000
Imaging of procollagen transport reveals COPI-dependent cargo sorting during ER-to-Golgi transport in mammalian cells Stephens, David J.; Pepperkok, Rainer Journal of Cell Science, Vol. 115, Issue 6 https://doi.org/10.1242/jcs.115.6.1149	journal	March 2002
Sec24D-Dependent Transport of Extracellular Matrix Proteins Is Required for Zebrafish Skeletal Morphogenesis Sarmah, Swapnalee; Barrallo-Gimeno, Alejandro; Melville, David B. PLoS ONE, Vol. 5, Issue 4 https://doi.org/10.1371/journal.pone.0010367	journal	April 2010
Accumulation of Laminin Monomers in Drosophila Glia Leads to Glial Endoplasmic Reticulum Stress and Disrupted Larval Locomotion Petley-Ragan, L. M.; Ardiel, E. L.; Rankin, C. H. Journal of Neuroscience, Vol. 36, Issue 4 https://doi.org/10.1523/JNEUROSCI.1797-15.2016	journal	January 2016
Synthetic Peptide Antisera: Their Production and Use in the Cloning of Matrix Proteins Fisher, Larry W.; Lindner, Wolfgang; Young, Marian F. Connective Tissue Research, Vol. 21, Issue 1-4 https://doi.org/10.3109/03008208909049994	journal	January 1989
Antisera and cDNA probes to human and certain animal model bone matrix noncollagenous proteins Fisher, Larry W.; Stubbs, John T.; Young, Marian F. Acta Orthopaedica Scandinavica, Vol. 66, Issue sup266 https://doi.org/10.3109/17453679509157649	journal	January 1995
SLY1 and Syntaxin 18 specify a distinct pathway for procollagen VII export from the endoplasmic reticulum Nogueira, Cristina; Erlmann, Patrik; Villeneuve, Julien eLife, Vol. 3 https://doi.org/10.7554/eLife.02784	journal	May 2014

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