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Collagen has a unique SEC24 preference for efficient export from the endoplasmic reticulum

Chung-Ling Lu, Steven Ortmeier, Jon Brudvig, Tamara Moretti, Jacob Cain, Simeon A. Boyadjiev, View ORCID ProfileJill M. Weimer, View ORCID ProfileJinoh Kim
doi: https://doi.org/10.1101/2021.02.23.431880
Chung-Ling Lu
1Department of Biomedical Sciences, College of Veterinary Medicine, Iowa State University, Ames, IA, 50011, USA
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Steven Ortmeier
2Pediatrics and Rare Diseases Group, Sanford Research, Sioux Falls, SD, 57104, USA
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Jon Brudvig
2Pediatrics and Rare Diseases Group, Sanford Research, Sioux Falls, SD, 57104, USA
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Tamara Moretti
1Department of Biomedical Sciences, College of Veterinary Medicine, Iowa State University, Ames, IA, 50011, USA
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Jacob Cain
2Pediatrics and Rare Diseases Group, Sanford Research, Sioux Falls, SD, 57104, USA
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Simeon A. Boyadjiev
3Department of Pediatrics, University of California Davis School of Medicine, Sacramento, CA, 95817, USA
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Jill M. Weimer
2Pediatrics and Rare Diseases Group, Sanford Research, Sioux Falls, SD, 57104, USA
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  • ORCID record for Jill M. Weimer
Jinoh Kim
1Department of Biomedical Sciences, College of Veterinary Medicine, Iowa State University, Ames, IA, 50011, USA
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  • For correspondence: jinohk@iastate.edu
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ABSTRACT

SEC24 is mainly involved in cargo sorting during COPII vesicle assembly. There are four SEC24 paralogs (A to D) in mammals, which are classified into two subgroups (SEC24A/B and SEC24C/D). Pathological mutations in SEC24D cause osteogenesis imperfecta with craniofacial dysplasia in humans. sec24d mutant fish also recapitulate the phenotypes. Consistent with the skeletal phenotypes, the secretion of collagen was severely defective in mutant fish, emphasizing the importance of SEC24D in collagen secretion. However, SEC24D patient-derived fibroblasts show only a mild secretion phenotype, suggesting tissue-specificity in the secretion process. Using Sec24d KO mice and cultured cells, we show that SEC24A and SEC24B also contribute to ER export of procollagen. In contrast, fibronectin 1 requires either SEC24C or SEC24D for ER export. On the basis of our results, we propose that procollagen interacts with multiple SEC24 paralogs for efficient export from the ER, and that this is the basis for tissue-specific phenotypes resulting from SEC24 paralog deficiency.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Synopsis: SEC24D gene mutations cause predominantly bone defects. A prevailing explanation is that SEC24D sorts procollagen. Using Sec24d KO mice and cultured cells, we show that SEC24A and SEC24B also contribute to ER export of procollagen. In contrast, fibronectin 1 requires either SEC24C or SEC24D for ER export. This finding is significant as it forms the basis for tissue-specific and cargo-specific utilization of SEC24 paralogs for ER export.

  • Figures were modified in the main text and new figures were added in the supplemental information and the main text was changed accordingly.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. All rights reserved. No reuse allowed without permission.
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Posted October 28, 2021.
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Collagen has a unique SEC24 preference for efficient export from the endoplasmic reticulum
Chung-Ling Lu, Steven Ortmeier, Jon Brudvig, Tamara Moretti, Jacob Cain, Simeon A. Boyadjiev, Jill M. Weimer, Jinoh Kim
bioRxiv 2021.02.23.431880; doi: https://doi.org/10.1101/2021.02.23.431880
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Collagen has a unique SEC24 preference for efficient export from the endoplasmic reticulum
Chung-Ling Lu, Steven Ortmeier, Jon Brudvig, Tamara Moretti, Jacob Cain, Simeon A. Boyadjiev, Jill M. Weimer, Jinoh Kim
bioRxiv 2021.02.23.431880; doi: https://doi.org/10.1101/2021.02.23.431880

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