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Tetraspanin 4 stabilizes membrane swellings and facilitates their maturation into migrasomes
Raviv Dharan1,2, Yuwei Huang3, Sudheer Kumar Cheppali1,2
1School of Chemistry, Raymond & Beverly Sackler Faculty of Exact Sciences, Tel Aviv University, Tel Aviv, Israel.
Abstract:
Migrasomes are newly discovered cell organelles forming by local swelling of retraction fibers. The migrasome formation critically depends on tetraspanin proteins present in the retraction fiber membranes and is modulated by the membrane tension and bending rigidity. It remained unknown how and in which time sequence these factors are involved in migrasome nucleation, growth, and stabilization, and what are the possible intermediate stages of migrasome biogenesis. Here using live cell imaging and a biomimetic system for migrasomes and retraction fibers, we reveal that migrasome formation is a two-stage process. At the first stage, which in biomimetic system is mediated by membrane tension, local swellings largely devoid of tetraspanin 4 form on the retraction fibers. At the second stage, tetraspanin 4 molecules migrate toward and onto these swellings, which grow up to several microns in size and transform into migrasomes. This tetraspanin 4 recruitment to the swellings is essential for migrasome growth and stabilization. Based on these findings we propose that the major role of tetraspanin proteins is in stabilizing the migrasome structure, while the migrasome nucleation and initial growth stages can be driven by membrane mechanical stresses.
Insights
Migrasome formation involves two stages: initial swelling driven by membrane tension, followed by tetraspanin 4 recruitment for growth and stabilization. This reveals key mechanisms in cell organelle biogenesis.
Area of Science:
- Cell Biology
- Biophysics
Background:
- Migrasomes are novel cell organelles formed from retraction fibers.
- Tetraspanin proteins, membrane tension, and bending rigidity are crucial for migrasome formation.
- The precise sequence and interplay of these factors in migrasome biogenesis remain unclear.
Purpose of the Study:
- To elucidate the temporal sequence of factors involved in migrasome nucleation, growth, and stabilization.
- To identify intermediate stages in migrasome biogenesis.
- To understand the roles of membrane tension and tetraspanin proteins in migrasome formation.
Main Methods:
- Live cell imaging.
- Development of a biomimetic system for studying retraction fibers and migrasomes.
Main Results:
- Migrasome formation occurs in two distinct stages.
- Stage 1: Localized swellings form on retraction fibers, driven by membrane tension and initially lacking tetraspanin 4.
- Stage 2: Tetraspanin 4 is recruited to these swellings, promoting their growth into stable migrasomes.
Conclusions:
- Migrasome biogenesis is a two-stage process initiated by membrane mechanical stresses.
- Tetraspanin 4 recruitment is essential for the growth and stabilization of migrasomes.
- Tetraspanin proteins primarily stabilize migrasome structure, while initial formation relies on membrane mechanics.
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