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PreprintCited by 1Cellular transport and secretionMicrotubule and mitosis dynamicsAutophagy in Disease and Therapy

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Evolution of the ribbon-like organization of the Golgi apparatus in animal cells

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Benvenuto, Giovanna, Leone, Serena, Astoricchio, Emanuele, Bormke, Sophia, Jasek, Sanja, D’Aniello, Enrico, Kittelmann, Maike, McDonald, Kent, Hartenstein, Volker, Baena, Valentina, Escrivà, Héctor, Bertrand, Stephanie, Schierwater, Bernd, Burkhardt, Pawel, Ruiz-Trillo, Iñaki, Jékely, Gáspár, Ullrich-Lüter, Jack, Lüter, Carsten, D’Aniello, Salvatore, Arnone, Maria Ina, Ferraro, Francesco·2023·bioRxiv (Cold Spring Harbor Laboratory)
DOI 10.1101/2023.02.16.528797

Preprint — published as 10.1016/j.celrep.2024.113791

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Abstract

Summary: The Golgi ribbon is a structural organization formed by linked Golgi stacks that is believed to be exclusive to vertebrate cells. Its functional contribution to cellular processes is unclear, yet its disruption is associated with several human pathologies. In this study we address the evolutionary origin of the Golgi ribbon, describe a potential molecular mechanism for its emergence and identify a cellular process in which it may be involved. We observed the ribbon-like architecture in the cells of several metazoan taxa, suggesting its early appearance during animal evolution before the emergence of vertebrates. Supported by AlphaFold2 modelling, we propose that the evolution of the complex between two Golgi resident proteins, Golgin-45 and GRASP, led to the tethering of Golgi stacks into the ribbon-like configuration. Finally, we find that the ribbon is assembled during the early embryogenesis of deuterostome animals, a strong indication of its role in development. Overall, our study indicates that the Golgi ribbon is functionally relevant beyond vertebrates and calls for further investigations to decipher its elusive functions. Graphical abstract:

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Metadata

Authors
Benvenuto, G., Leone, S., Astoricchio, E., Bormke, S., Jasek, S., D’Aniello, E., Kittelmann, M., McDonald, K., Hartenstein, V., Baena, V., Escrivà, H., Bertrand, S., Schierwater, B., Burkhardt, P., Ruiz-Trillo, I., Jékely, G., Ullrich-Lüter, J., Lüter, C., D’Aniello, S., Arnone, M. I., & Ferraro, F.
Affiliations
  • Stazione Zoologica Anton Dohrn (IT)
  • Museum für Naturkunde (DE)
  • University of Exeter (GB)
  • Oxford Brookes University (GB)
  • University of California, Berkeley (US)
  • University of California, Los Angeles (US)
  • UConn Health (US)
  • University of Veterinary Medicine Hannover, Foundation (DE)
  • University of Bergen (NO)
Corresponding author
Ferraro, Francesco
ORCID
Venue
bioRxiv (Cold Spring Harbor Laboratory)
Publisher
openRxiv
Published
2023-02-16
DOI
10.1101/2023.02.16.528797
OpenAlex
W4321018440
Cited by
1
References
11
Citations by year
2025: 1
Type
posted content
Language
en
Open access
Licence
cc-by-nc-nd
Locations
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • Radar (Oxford Brookes University) (submittedVersion, cc-by-nc-nd)
Funders
  • University of Connecticut Health Center
  • Centre National de la Recherche Scientifique
  • Université Pierre et Marie Curie
  • Universitat de Barcelona
  • Stazione Zoologica Anton Dohrn
  • Directorate for Biological Sciences
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Autophagy in Disease and Therapy
Keywords
Golgi ribbon, Golgi stacks, GRASP, animal evolution, Golgi resident proteins, protein complex evolution

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