Titin-dependent biomechanical feedback tailors sarcomeres to specialized muscle functions in insects
Sarcomeres are the universal contractile units of muscles that enable animals to move. Insect muscles display a remarkable functional diversity: they operate at extremely different contraction frequencies (ranging from ~1 to 1000 hertz) and amplitudes during flying, walking, and crawling. This is puzzling because sarcomeres are built from essentially the same actin-myosin components. Here, we address how functionally different sarcomeres are made. We show that the giant protein titin and the regulation of developmental contractility are key for the sarcomere specializations. I-band titin spans and determines the length of the sarcomeric I-band in a muscle type-specific manner. Unexpectedly, I-band titin also rules the length of the force-generating myosin filament using a feedback mechanism that is modulated by myosin contractility. We propose a model of how sarcomere specializations in insects are tuned, provide evidence for this model, and discuss its validity beyond insects.
Authors
- Nicolas Brouilly (ORCID: https://orcid.org/0000-0002-4584-0164)
- Wouter Koolhaas
- Jean-François Rupprecht (ORCID: https://orcid.org/0000-0001-8904-5878)
- Sabina Avosani (ORCID: https://orcid.org/0000-0001-8605-5237)
- Vincent Loreau (ORCID: https://orcid.org/0000-0002-0556-2825)
- Christophe Pitaval
- Frank Schnorrer (ORCID: https://orcid.org/0000-0002-9518-7263)
- Bianca Habermann (ORCID: https://orcid.org/0000-0002-2457-7504)
- Anne C. von Philipsborn (ORCID: https://orcid.org/0000-0002-7921-8744)
- Dirk Görlich (ORCID: https://orcid.org/0000-0002-4343-5210)
- Nuno Miguel Luis (ORCID: https://orcid.org/0000-0001-5438-9638)
- Paul de Boissier (ORCID: https://orcid.org/0000-0003-2246-1580)
- Pierre Mangeol (ORCID: https://orcid.org/0000-0002-8305-7322)
- Eunice HoYee Chan (ORCID: https://orcid.org/0000-0003-3162-3609)
- S J Reiter
- Aditya Sane
Institutions
- Centre National de la Recherche Scientifique (FR)
- University of Fribourg (CH)
- Aix-Marseille Université (FR)
- Max Planck Institute of Biochemistry (DE)
- Living Systems (United States) (US)
- Max Planck Institute for Multidisciplinary Sciences (DE)
Publication Details
- Journal
- Science Advances
- Published
- 2025-05-09
- DOI
- https://doi.org/10.1126/sciadv.ads8716
- Citations
- 7
- Primary Topic
- Cardiomyopathy and Myosin Studies
- Type
- article
- Field-Weighted Citation Impact
- 9.72