skip to main content
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

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

Abstract

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.

Authors:
 [1];  [1];  [2];  [3]; ORCiD logo [2]; ORCiD logo [1]
  1. Department of Molecular and Cell Biology and Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, CA 94720, Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, CA 94720
  2. Department of Chemistry, University of California, Berkeley, Berkeley, CA 94720
  3. Department of Molecular and Cell Biology and Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, CA 94720
Publication Date:
Sponsoring Org.:
USDOE
OSTI Identifier:
1352291
Resource Type:
Published Article
Journal Name:
Journal of Cell Biology
Additional Journal Information:
Journal Name: Journal of Cell Biology Journal Volume: 216 Journal Issue: 6; Journal ID: ISSN 0021-9525
Publisher:
Rockefeller University Press
Country of Publication:
United States
Language:
English

Citation Formats

Gorur, Amita, Yuan, Lin, Kenny, Samuel J., Baba, Satoshi, Xu, Ke, and Schekman, Randy. COPII-coated membranes function as transport carriers of intracellular procollagen I. United States: N. p., 2017. Web. doi:10.1083/jcb.201702135.
Gorur, Amita, Yuan, Lin, Kenny, Samuel J., Baba, Satoshi, Xu, Ke, & Schekman, Randy. COPII-coated membranes function as transport carriers of intracellular procollagen I. United States. doi:10.1083/jcb.201702135.
Gorur, Amita, Yuan, Lin, Kenny, Samuel J., Baba, Satoshi, Xu, Ke, and Schekman, Randy. Thu . "COPII-coated membranes function as transport carriers of intracellular procollagen I". United States. doi:10.1083/jcb.201702135.
@article{osti_1352291,
title = {COPII-coated membranes function as transport carriers of intracellular procollagen I},
author = {Gorur, Amita and Yuan, Lin and Kenny, Samuel J. and Baba, Satoshi and Xu, Ke and Schekman, Randy},
abstractNote = {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.},
doi = {10.1083/jcb.201702135},
journal = {Journal of Cell Biology},
number = 6,
volume = 216,
place = {United States},
year = {2017},
month = {4}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
DOI: 10.1083/jcb.201702135

Citation Metrics:
Cited by: 2 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Loss of SEC-23 in Caenorhabditis elegans Causes Defects in Oogenesis, Morphogenesis, and Extracellular Matrix Secretion
journal, November 2003

  • Roberts, Brett; Clucas, Caroline; Johnstone, Iain L.
  • Molecular Biology of the Cell, Vol. 14, Issue 11
  • DOI: 10.1091/mbc.E03-03-0162

Multicolor Fluorescence Nanoscopy in Fixed and Living Cells by Exciting Conventional Fluorophores with a Single Wavelength
journal, October 2010


Neural tube opening and abnormal extraembryonic membrane development in SEC23A deficient mice
journal, October 2015

  • Zhu, Min; Tao, Jiayi; Vasievich, Matthew P.
  • Scientific Reports, Vol. 5, Issue 1
  • DOI: 10.1038/srep15471

Multibudded tubules formed by COPII on artificial liposomes
journal, June 2011

  • Bacia, Kirsten; Futai, Eugene; Prinz, Simone
  • Scientific Reports, Vol. 1, Issue 1
  • DOI: 10.1038/srep00017

Global defects in collagen secretion in a Mia3/TANGO1 knockout mouse
journal, May 2011

  • Wilson, Deanna G.; Phamluong, Khanhky; Li, Li
  • The Journal of Cell Biology, Vol. 193, Issue 5
  • DOI: 10.1083/jcb.201007162

Molecular basis for the action of the collagen-specific chaperone Hsp47/SERPINH1 and its structure-specific client recognition
journal, July 2012

  • Widmer, C.; Gebauer, J. M.; Brunstein, E.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 33
  • DOI: 10.1073/pnas.1208072109

Accumulation of Laminin Monomers in Drosophila Glia Leads to Glial Endoplasmic Reticulum Stress and Disrupted Larval Locomotion
journal, January 2016


ER-to-Golgi Carriers Arise through Direct En Bloc Protrusion and Multistage Maturation of Specialized ER Exit Domains
journal, October 2003


Antisera and cDNA probes to human and certain animal model bone matrix noncollagenous proteins
journal, January 1995

  • Fisher, Larry W.; Stubbs, John T.; Young, Marian F.
  • Acta Orthopaedica Scandinavica, Vol. 66, Issue sup266
  • DOI: 10.3109/17453679509157649

Sequence-specific Recognition of Collagen Triple Helices by the Collagen-specific Molecular Chaperone HSP47
journal, July 2002

  • Tasab, Mohammed; Jenkinson, Lynsey; Bulleid, Neil J.
  • Journal of Biological Chemistry, Vol. 277, Issue 38
  • DOI: 10.1074/jbc.M202782200

SLY1 and Syntaxin 18 specify a distinct pathway for procollagen VII export from the endoplasmic reticulum
journal, May 2014

  • Nogueira, Cristina; Erlmann, Patrik; Villeneuve, Julien
  • eLife, Vol. 3
  • DOI: 10.7554/eLife.02784

Concentration of Sec12 at ER exit sites via interaction with cTAGE5 is required for collagen export
journal, September 2014

  • Saito, Kota; Yamashiro, Koh; Shimazu, Noriko
  • The Journal of Cell Biology, Vol. 206, Issue 6
  • DOI: 10.1083/jcb.201312062

Intracellular mechanisms of molecular recognition and sorting for transport of large extracellular matrix molecules
journal, September 2016

  • Ishikawa, Yoshihiro; Ito, Shinya; Nagata, Kazuhiro
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 41
  • DOI: 10.1073/pnas.1609571113

Intracellular interaction of collagen-specific stress protein HSP47 with newly synthesized procollagen
journal, April 1996


COPII-Coated Vesicle Formation Reconstituted with Purified Coat Proteins and Chemically Defined Liposomes
journal, April 1998


Embryonic Lethality of Molecular Chaperone Hsp47 Knockout Mice Is Associated with Defects in Collagen Biosynthesis
journal, September 2000

  • Nagai, Naoko; Hosokawa, Masanori; Itohara, Shigeyoshi
  • The Journal of Cell Biology, Vol. 150, Issue 6
  • DOI: 10.1083/jcb.150.6.1499

A novel multiprotein complex is required to generate the prechylomicron transport vesicle from intestinal ER
journal, March 2010

  • Siddiqi, Shahzad; Saleem, Umair; Abumrad, Nada A.
  • Journal of Lipid Research, Vol. 51, Issue 7
  • DOI: 10.1194/jlr.M005611

TANGO1/cTAGE5 receptor as a polyvalent template for assembly of large COPII coats
journal, August 2016

  • Ma, Wenfu; Goldberg, Jonathan
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 36
  • DOI: 10.1073/pnas.1605916113

Segregation of COPI-rich and anterograde-cargo-rich domains in endoplasmic-reticulum-to-Golgi transport complexes
journal, August 1999


Sizing and phenotyping of cellular vesicles using Nanoparticle Tracking Analysis
journal, December 2011

  • Dragovic, Rebecca A.; Gardiner, Christopher; Brooks, Alexandra S.
  • Nanomedicine: Nanotechnology, Biology and Medicine, Vol. 7, Issue 6
  • DOI: 10.1016/j.nano.2011.04.003

TANGO1 Facilitates Cargo Loading at Endoplasmic Reticulum Exit Sites
journal, March 2009


COPII-coated vesicles: flexible enough for large cargo?
journal, August 2005


Regulation of the CUL3 Ubiquitin Ligase by a Calcium-Dependent Co-adaptor
journal, October 2016


Hsp47: a molecular chaperone that interacts with and stabilizes correctly-folded procollagen
journal, May 2000

  • Tasab, Mohammed; Batten, Margaret R.; Bulleid, Neil J.
  • The EMBO Journal, Vol. 19, Issue 10
  • DOI: 10.1093/emboj/19.10.2204

Sedlin Controls the ER Export of Procollagen by Regulating the Sar1 Cycle
journal, September 2012


Synthetic Peptide Antisera: Their Production and Use in the Cloning of Matrix Proteins
journal, January 1989

  • Fisher, Larry W.; Lindner, Wolfgang; Young, Marian F.
  • Connective Tissue Research, Vol. 21, Issue 1-4
  • DOI: 10.3109/03008208909049994

Ubiquitin-dependent regulation of COPII coat size and function
journal, February 2012

  • Jin, Lingyan; Pahuja, Kanika Bajaj; Wickliffe, Katherine E.
  • Nature, Vol. 482, Issue 7386
  • DOI: 10.1038/nature10822

Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM)
journal, August 2006

  • Rust, Michael J.; Bates, Mark; Zhuang, Xiaowei
  • Nature Methods, Vol. 3, Issue 10
  • DOI: 10.1038/nmeth929

Efficient coupling of Sec23-Sec24 to Sec13-Sec31 drives COPII-dependent collagen secretion and is essential for normal craniofacial development
journal, August 2008

  • Townley, A. K.; Feng, Y.; Schmidt, K.
  • Journal of Cell Science, Vol. 121, Issue 18
  • DOI: 10.1242/jcs.031070

Sec24b selectively sorts Vangl2 to regulate planar cell polarity during neural tube closure
journal, December 2009

  • Merte, Janna; Jensen, Devon; Wright, Kevin
  • Nature Cell Biology, Vol. 12, Issue 1
  • DOI: 10.1038/ncb2002

Mutations in SEC24D, Encoding a Component of the COPII Machinery, Cause a Syndromic Form of Osteogenesis Imperfecta
journal, March 2015

  • Garbes, Lutz; Kim, Kyungho; Rieß, Angelika
  • The American Journal of Human Genetics, Vol. 96, Issue 3
  • DOI: 10.1016/j.ajhg.2015.01.002

Multicolor Far-Field Fluorescence Nanoscopy through Isolated Detection of Distinct Molecular Species
journal, August 2008

  • Bossi, Mariano; Fölling, Jonas; Belov, Vladimir N.
  • Nano Letters, Vol. 8, Issue 8
  • DOI: 10.1021/nl801471d

Direct in Vitro and in Vivo Evidence for Interaction between Hsp47 Protein and Collagen Triple Helix
journal, January 2012

  • Ono, Takashi; Miyazaki, Takahiro; Ishida, Yoshihito
  • Journal of Biological Chemistry, Vol. 287, Issue 9
  • DOI: 10.1074/jbc.M111.280248

Secretory COPII coat component Sec23a is essential for craniofacial chondrocyte maturation
journal, September 2006

  • Lang, Michael R.; Lapierre, Lynne A.; Frotscher, Michael
  • Nature Genetics, Vol. 38, Issue 10
  • DOI: 10.1038/ng1880

TANGO1 and Mia2/cTAGE5 (TALI) cooperate to export bulky pre-chylomicrons/VLDLs from the endoplasmic reticulum
journal, May 2016

  • Santos, António J. M.; Nogueira, Cristina; Ortega-Bellido, Maria
  • The Journal of Cell Biology, Vol. 213, Issue 3
  • DOI: 10.1083/jcb.201603072

Uncoupled Packaging of Amyloid Precursor Protein and Presenilin 1 into Coat Protein Complex II Vesicles
journal, December 2004

  • Kim, Jinoh; Hamamoto, Susan; Ravazzola, Mariella
  • Journal of Biological Chemistry, Vol. 280, Issue 9
  • DOI: 10.1074/jbc.M411091200

TFG Promotes Organization of Transitional ER and Efficient Collagen Secretion
journal, May 2016


A pseudoatomic model of the COPII cage obtained from cryo-electron microscopy and mass spectrometry
journal, December 2012

  • Noble, Alex J.; Zhang, Qian; O'Donnell, Jason
  • Nature Structural & Molecular Biology, Vol. 20, Issue 2
  • DOI: 10.1038/nsmb.2467

Pelvic problems for mammals
journal, October 1997

  • Presley, Robert
  • Nature, Vol. 389, Issue 6650
  • DOI: 10.1038/38891

Three-Dimensional Super-Resolution Imaging by Stochastic Optical Reconstruction Microscopy
journal, February 2008


Cranio-lenticulo-sutural dysplasia is caused by a SEC23A mutation leading to abnormal endoplasmic-reticulum-to-Golgi trafficking
journal, September 2006

  • Boyadjiev, Simeon A.; Fromme, J. Christopher; Ben, Jin
  • Nature Genetics, Vol. 38, Issue 10
  • DOI: 10.1038/ng1876

cTAGE5 mediates collagen secretion through interaction with TANGO1 at endoplasmic reticulum exit sites
journal, July 2011

  • Saito, Kota; Yamashiro, Koh; Ichikawa, Yuki
  • Molecular Biology of the Cell, Vol. 22, Issue 13
  • DOI: 10.1091/mbc.E11-02-0143

The pH-dependent Client Release from the Collagen-specific Chaperone HSP47 Is Triggered by a Tandem Histidine Pair
journal, April 2016

  • Oecal, Sinan; Socher, Eileen; Uthoff, Matthias
  • Journal of Biological Chemistry, Vol. 291, Issue 24
  • DOI: 10.1074/jbc.M115.706069

Type I Collagen in Hsp47-null Cells Is Aggregated in Endoplasmic Reticulum and Deficient in N-Propeptide Processing and Fibrillogenesis
journal, May 2006

  • Ishida, Yoshihito; Kubota, Hiroshi; Yamamoto, Akitsugu
  • Molecular Biology of the Cell, Vol. 17, Issue 5
  • DOI: 10.1091/mbc.E05-11-1065

Shaping Cells and Organs in Drosophila by Opposing Roles of Fat Body-Secreted Collagen IV and Perlecan
journal, August 2011


Sec24D-Dependent Transport of Extracellular Matrix Proteins Is Required for Zebrafish Skeletal Morphogenesis
journal, April 2010


Long-term sun exposure alters the collagen of thepapillary dermis
journal, February 1996

  • Bernstein, Eric F.; Chen, Yue Qiu; Kopp, Jeffrey B.
  • Journal of the American Academy of Dermatology, Vol. 34, Issue 2
  • DOI: 10.1016/S0190-9622(96)80114-9

Visualization of ER-to-Golgi Transport in Living Cells Reveals a Sequential Mode of Action for COPII and COPI
journal, September 1997


Icy: an open bioimage informatics platform for extended reproducible research
journal, June 2012

  • de Chaumont, Fabrice; Dallongeville, Stéphane; Chenouard, Nicolas
  • Nature Methods, Vol. 9, Issue 7
  • DOI: 10.1038/nmeth.2075

SEC23-SEC31 the Interface Plays Critical Role for Export of Procollagen from the Endoplasmic Reticulum
journal, February 2012

  • Kim, Sun-Don; Pahuja, Kanika Bajaj; Ravazzola, Mariella
  • Journal of Biological Chemistry, Vol. 287, Issue 13
  • DOI: 10.1074/jbc.M111.283382

COPII and the regulation of protein sorting in mammals
journal, December 2011

  • Zanetti, Giulia; Pahuja, Kanika Bajaj; Studer, Sean
  • Nature Cell Biology, Vol. 14, Issue 1
  • DOI: 10.1038/ncb2390

A Monoclonal Antibody Specific for the Amino Terminal Cleavage Site of Procollagen Type I
journal, July 1983