Dynamic constriction and fission of endoplasmic reticulum membranes by reticulon

Javier Espadas, Diana Pendin, Rebeca Bocanegra, Artur Escalada, Giulia Misticoni, Tatiana Trevisan, Ariana Velasco Del Olmo, Aldo Montagna, Sergio Bova, Borja Ibarra, Peter I. Kuzmin, Pavel V. Bashkirov, Anna V. Shnyrova, Vadim A. Frolov, Andrea Daga

Research output: Contribution to journalArticle

Abstract

The endoplasmic reticulum (ER) is a continuous cell-wide membrane network. Network formation has been associated with proteins producing membrane curvature and fusion, such as reticulons and atlastin. Regulated network fragmentation, occurring in different physiological contexts, is less understood. Here we find that the ER has an embedded fragmentation mechanism based upon the ability of reticulon to produce fission of elongating network branches. In Drosophila, Rtnl1-facilitated fission is counterbalanced by atlastin-driven fusion, with the prevalence of Rtnl1 leading to ER fragmentation. Ectopic expression of Drosophila reticulon in COS-7 cells reveals individual fission events in dynamic ER tubules. Consistently, in vitro analyses show that reticulon produces velocity-dependent constriction of lipid nanotubes leading to stochastic fission via a hemifission mechanism. Fission occurs at elongation rates and pulling force ranges intrinsic to the ER, thus suggesting a principle whereby the dynamic balance between fusion and fission controlling organelle morphology depends on membrane motility.

Original languageEnglish
Number of pages1
JournalNature Communications
Volume10
Issue number1
DOIs
Publication statusPublished - Nov 22 2019

Fingerprint

endoplasmic reticulum
Constriction
Endoplasmic Reticulum
fission
constrictions
Fusion reactions
membranes
Membranes
Drosophila
fragmentation
fusion
Nanotubes
Elongation
Membrane Fusion
COS Cells
Lipids
organelles
locomotion
Organelles
pulling

ASJC Scopus subject areas

  • Chemistry(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Physics and Astronomy(all)

Cite this

Dynamic constriction and fission of endoplasmic reticulum membranes by reticulon. / Espadas, Javier; Pendin, Diana; Bocanegra, Rebeca; Escalada, Artur; Misticoni, Giulia; Trevisan, Tatiana; Velasco Del Olmo, Ariana; Montagna, Aldo; Bova, Sergio; Ibarra, Borja; Kuzmin, Peter I.; Bashkirov, Pavel V.; Shnyrova, Anna V.; Frolov, Vadim A.; Daga, Andrea.

In: Nature Communications, Vol. 10, No. 1, 22.11.2019.

Research output: Contribution to journalArticle

Espadas, J, Pendin, D, Bocanegra, R, Escalada, A, Misticoni, G, Trevisan, T, Velasco Del Olmo, A, Montagna, A, Bova, S, Ibarra, B, Kuzmin, PI, Bashkirov, PV, Shnyrova, AV, Frolov, VA & Daga, A 2019, 'Dynamic constriction and fission of endoplasmic reticulum membranes by reticulon', Nature Communications, vol. 10, no. 1. https://doi.org/10.1038/s41467-019-13327-7
Espadas J, Pendin D, Bocanegra R, Escalada A, Misticoni G, Trevisan T et al. Dynamic constriction and fission of endoplasmic reticulum membranes by reticulon. Nature Communications. 2019 Nov 22;10(1). https://doi.org/10.1038/s41467-019-13327-7
Espadas, Javier ; Pendin, Diana ; Bocanegra, Rebeca ; Escalada, Artur ; Misticoni, Giulia ; Trevisan, Tatiana ; Velasco Del Olmo, Ariana ; Montagna, Aldo ; Bova, Sergio ; Ibarra, Borja ; Kuzmin, Peter I. ; Bashkirov, Pavel V. ; Shnyrova, Anna V. ; Frolov, Vadim A. ; Daga, Andrea. / Dynamic constriction and fission of endoplasmic reticulum membranes by reticulon. In: Nature Communications. 2019 ; Vol. 10, No. 1.
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