Resilin matrix distribution, variability and function in Drosophila

Steven Lerch,Klaus-Dieter Klass,Bernard Moussian,Nicole Gehring,Fritz-Olaf Lehmann,Barbara Eckel,Renata Zuber,Yiwen Wang

doi:10.1186/s12915-020-00902-4

Abstract

BackgroundElasticity prevents fatigue of tissues that are extensively and repeatedly deformed. Resilin is a resilient and elastic extracellular protein matrix in joints and hinges of insects. For its mechanical properties, Resilin is extensively analysed and applied in biomaterial and biomedical sciences. However, there is only indirect evidence for Resilin distribution and function in an insect. Commonly, the presence of dityrosines that covalently link Resilin protein monomers (Pro-Resilin), which are responsible for its mechanical properties and fluoresce upon UV excitation, has been considered to reflect Resilin incidence.ResultsUsing a GFP-tagged Resilin version, we directly identify Resilin in pliable regions of the Drosophila body, some of which were not described before. Interestingly, the amounts of dityrosines are not proportional to the amounts of Resilin in different areas of the fly body, arguing that the mechanical properties of Resilin matrices vary according to their need. For a functional analysis of Resilin matrices, applying the RNA interference and Crispr/Cas9 techniques, we generated flies with reduced or eliminated Resilin function, respectively. We find that these flies are flightless but capable of locomotion and viable suggesting that other proteins may partially compensate for Resilin function. Indeed, localizations of the potentially elastic protein Cpr56F and Resilin occasionally coincide.ConclusionsThus, Resilin-matrices are composite in the way that varying amounts of different elastic proteins and dityrosinylation define material properties. Understanding the biology of Resilin will have an impact on Resilin-based biomaterial and biomedical sciences.

Highlights

Elasticity prevents fatigue of tissues that are extensively and repeatedly deformed
We are reluctant to exclude such a situation as we observed that occasionally the tips of the proboscis, for instance, that were devoid of any Pro-Resilin-GFP signal, displayed weak auto-fluorescence when excited with a light of 355 nm (Fig. 2). These findings suggest that commonly all dityrosine bonds (DT) regions in the fly body cuticle include Pro-Resilin-GFP
In line with a recent hypothesis [9], our results indicate that more than a Resilin protein is needed for construction of a Resilin-based elastic module in the insect cuticle

Summary

Introduction

Elasticity prevents fatigue of tissues that are extensively and repeatedly deformed. Resilin is a resilient and elastic extracellular protein matrix in joints and hinges of insects. The presence of dityrosines that covalently link Resilin protein monomers (Pro-Resilin), which are responsible for its mechanical properties and fluoresce upon UV excitation, has been considered to reflect Resilin incidence. Elasticity and resilience are essential for the integrity of tissues that function through repeated and extensive deformation. Outside the R&R-2 motif, Pro-Resilin sequences in different insects vary considerably. In principle, these sequences are characterised by stretches of non-conserved repetitive blocks that account for the elasticity of Pro-Resilins [10, 16,17,18]

Methods

Results

Discussion

Conclusion