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PreprintCited by 199Circadian rhythm and melatoninCellular transport and secretionCircular RNAs in diseases

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Circadian control of the secretory pathway is a central mechanism in tissue homeostasis

Open access
Chang, Joan, Garva, Richa, Pickard, Adam, Chloé Yeung, Ching-Yan, Mallikarjun, Venkatesh, Swift, Joe, Holmes, David F., Calverley, Ben, Lu, Yinhui, Adamson, Antony, Raymond-Hayling, Helena, Jensen, Oliver, Shearer, Tom, Meng, Qing Jun, Kadler, Karl E.·2018·Nature Cell Biology
DOI 10.1101/304014PMC PMC7613259

Preprint — published as 10.1038/s41556-019-0441-z

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Abstract

Collagen is the most abundant secreted protein in vertebrates that persists throughout life without renewal. The unchanging nature of collagen contrasts with observed continued collagen synthesis throughout adulthood and with conventional transcriptional and translational homeostatic mechanisms that replace damaged proteins with new copies. Here we show circadian clock regulation of procollagen transport from ER-to-Golgi and Golgi-to-plasma membrane by sequential rhythmic expression of SEC61, TANGO1, PDE4D and VPS33B. The result is nocturnal procollagen synthesis and daytime collagen fibril assembly in mice. Rhythmic collagen degradation by CTSK maintains collagen homeostasis. This circadian cycle of collagen synthesis, assembly and degradation affects only a pool of newly-synthesized collagen whilst maintaining the persistent collagen network. Disabling the circadian clock causes collagen accumulation and abnormal fibrils in vivo . In conclusion, our study has identified a circadian clock mechanism of protein homeostasis in which a sacrificial pool of collagen is synthesized and removed to maintain tissue function.

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  1. 10.1126/science.aal3321 · DOI · Paper page
  2. 10.1002/bip.1977.360160506 · DOI
  3. 10.1146/annurev.biochem.77.032207.120833 · DOI · Paper page
  4. 10.1242/jcs.03098 · DOI
  5. 10.1016/j.tcb.2011.02.003 · DOI
  6. 10.1172/JCI31487 · DOI
  7. 10.1016/j.cellsig.2016.07.009 · DOI
  8. 10.7554/eLife.05958 · DOI
  9. 10.1074/jbc.M006700200 · DOI
  10. 10.1074/jbc.M109.077503 · DOI
  11. 10.1126/scitranslmed.aad8335 · DOI
  12. 10.1096/fj.12-225599 · DOI
  13. 10.1074/jbc.M709885200 · DOI
  14. 10.1186/2193-1801-2-109 · DOI
  15. 1999, Mechanical loading regulates tenascin-C expression in the osteotendinous junction, J Cell Sci, 112, 3157
  16. 10.1034/j.1600-0838.2002.120205.x · DOI
  17. Birch, H. L. , McLaughlin, L. , Smith, R. K. & Goodship, A. E. Treadmill exercise-induced tendon hypertrophy: assessment of tendons with different mechanical functions. Equine Vet J Suppl, 222–226 (1999). · DOI
  18. 10.3109/03008208009152109 · DOI
  19. 10.1111/j.1469-7793.2001.00297.x · DOI
  20. 1999, Type I collagen synthesis and degradation in peritendinous tissue after exercise determined by microdialysis in humans, J Physiol, 521 Pt 1, 299
  21. 10.1210/jc.79.3.730 · DOI
  22. 10.1007/BF01626611 · DOI
  23. 10.1002/jbmr.5650101207 · DOI
  24. 10.1038/nrm1766 · DOI
  25. 10.1038/35036078 · DOI
  26. 10.1172/JCI82755 · DOI
  27. 10.1136/annrheumdis-2016-209428 · DOI
  28. 10.1002/gene.20102 · DOI
  29. 10.1038/srep05183 · DOI
  30. 10.1083/jcb.200312071 · DOI
  31. 10.1007/978-1-59745-413-1_9 · DOI
  32. 10.1101/gr.195404.115 · DOI
  33. 10.1042/bse0360001 · DOI
  34. 10.1016/j.cell.2008.12.025 · DOI
  35. 10.1016/j.devcel.2014.06.018 · DOI
  36. 10.1038/ncomms12111 · DOI
  37. 10.1074/jbc.271.4.2126 · DOI
  38. 10.1042/bj3310727 · DOI
  39. 10.1016/S0092-8674(00)81199-X · DOI · Paper page
  40. 10.1007/s00223-002-2092-4 · DOI
  41. 10.1080/15476286.2014.996467 · DOI
  42. 10.1146/annurev.bi.65.070196.001415 · DOI
  43. 10.1146/annurev-biophys-050511-102312 · DOI
  44. 10.1146/annurev-cellbio-092910-154125 · DOI
  45. 10.1038/nature02218 · DOI
  46. 10.7554/eLife.32723 · DOI
  47. 10.1016/B978-0-12-386471-0.00009-2 · DOI · Paper page
  48. 10.1042/BJ20111379 · DOI
  49. 10.1074/jbc.M708198200 · DOI
  50. 10.1371/journal.pone.0059779 · DOI
  51. 10.1126/scitranslmed.aal2774 · DOI
  52. 1989, Type I procollagen N-proteinase from chick embryo tendons. Purification of a new 500-kDa form of the enzyme and identification of the catalytically active polypeptides, J Biol Chem, 264, 11336, 10.1016/S0021-9258(18)60469-7 · DOI
  53. 1985, Type I procollagen carboxyl-terminal proteinase from chick embryo tendons. Purification and characterization, J Biol Chem, 260, 15996, 10.1016/S0021-9258(17)36357-3 · DOI
  54. 10.1126/science.8171325 · DOI · Paper page
  55. 10.1038/nrm3496 · DOI
  56. 10.1002/jor.23517 · DOI
  57. 10.1074/jbc.M304325200 · DOI
  58. 10.1146/annurev.biochem.67.1.609 · DOI
  59. 10.1074/jbc.M409622200 · DOI · Paper page
  60. 10.1083/jcb.136.3.729 · DOI
  61. 10.1083/jcb.60.1.92 · DOI
  62. 1987, Assembly of collagen fibrils de novo by cleavage of the type I pC-collagen with procollagen C-proteinase. Assay of critical concentration demonstrates that collagen self-assembly is a classical example of an entropy-driven process, J Biol Chem, 262, 15696, 10.1016/S0021-9258(18)47783-6 · DOI
  63. 10.1016/j.devcel.2009.10.010 · DOI
  64. 10.1016/j.cell.2007.06.045 · DOI · Paper page
  65. 10.1073/pnas.0308709101 · DOI · Paper page
  66. 10.1038/srep13555 · DOI
  67. 10.1002/jcp.22915 · DOI
  68. 10.1006/meth.2001.1262 · DOI · Paper page
  69. 10.1038/nprot.2013.086 · DOI
  70. 10.1016/j.matbio.2010.08.009 · DOI
  71. 10.1016/j.cels.2017.05.009 · DOI
  72. 10.1074/mcp.M115.055897 · DOI · Paper page
  73. 10.1038/nmeth.3901 · DOI · Paper page
  74. 10.1016/j.euprot.2015.02.002 · DOI
  75. 10.2202/1544-6115.1027 · DOI · Paper page
  76. 10.2307/2346101 · DOI
  77. 10.1093/bioinformatics/btw405 · DOI
  78. 1996, R: A Language for Data Analysis and Graphics, Journal of Computational and Graphical Statistics, 5, 299, 10.1080/10618600.1996.10474713 · DOI
  79. 10.1093/nar/gkp889 · DOI · Paper page

Metadata

Authors
Chang, J., Garva, R., Pickard, A., Chloé Yeung, C.-Y., Mallikarjun, V., Swift, J., Holmes, D. F., Calverley, B., Lu, Y., Adamson, A., Raymond-Hayling, H., Jensen, O., Shearer, T., Meng, Q. J., & Kadler, K. E.
Affiliations
  • Manchester Academic Health Science Centre (GB)
  • University of Manchester (GB)
Corresponding author
  • Meng, Qing Jun
  • Kadler, Karl E.
ORCID
Venue
Nature Cell Biology
Publisher
openRxiv
Published
2018-05-01
Volume
22
Issue
1
Pages
74-86
ISSN
1465-7392 (ISSN-L)
DOI
10.1101/304014
PMC
PMC7613259
OpenAlex
W2997202359
Cited by
199
References
1
Citations by year
2026: 21 · 2025: 31 · 2024: 29 · 2023: 23 · 2022: 27 · 2021: 47 · 2020: 17 · 2019: 3 · 2018: 1
FWCI
14.62
Type
journal article
Language
en
Open access
Locations
  • Nature Cell Biology (publishedVersion)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
  • Research Explorer (The University of Manchester) (submittedVersion)
Funders
  • Wellcome Trust (203128, 203128/Z/16/Z, 110126/Z/15/Z, 210062/Z/17/Z, 110126)
  • Shriners Hospitals for Children
  • Arthritis Research UK (20875)
  • Research Councils UK (BB/L024551/1)
  • University of Manchester (203128/Z/16/Z)
  • Versus Arthritis (20875)
  • Sir Richard Stapley Educational Trust
  • Directorate for Biological Sciences
  • Medical Research Council (BB/L024551/1, MR/P010709/1, 203128/Z/16/Z)
  • Biotechnology and Biological Sciences Research Council (BB/R014361/1, BB/L024551/1, 203128/Z/16/Z)
Topics
  • Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Circular RNAs in diseases
Keywords
circadian clock, collagen homeostasis, secretory pathway, endoplasmic reticulum, Sec61, TANGO1, PDE4D, VPS33B, collagen fibril assembly, collagen degradation, cathepsin K, proteostasis, NR1D1, SR9009
MeSH terms
SEC Translocation Channels, Animals, Carbazoles, Collagen, Extracellular Matrix, Homeostasis, Mice, Transgenic, Pyrrolidines, Sulfonamides, Thiophenes, Vesicular Transport Proteins, Aryl Hydrocarbon Receptor Nuclear Translocator, Cyclic Nucleotide Phosphodiesterases, Type 4, Secretory Pathway, Circadian Clocks

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