Molecular plasticity and functional enhancements of leg muscles in response to hypergravity in the fruit fly Drosophila melanogaster

Abstract

Studies of organismal and tissue biomechanics have clearly demonstrated that musculoskeletal design is strongly dependent on experienced loads, which can vary in the short term, as a result of growth during life history and during the evolution of animal body size. However, how animals actually perceive and make adjustments to their load-bearing musculoskeletal elements that accommodate variation in their body weight is poorly understood. We developed an experimental model system that can be used to start addressing these open questions, and uses hypergravity centrifugation to experimentally manipulate the loads experienced by We examined effects of this manipulation on leg muscle alternative splicing of the sarcomere gene troponin T (; Fbgn0004169, herein referred to by its synonym ), a process that was previously demonstrated to precisely correlate with quantitative variation in body weight in Lepidoptera and rat. In a similar fashion, hypergravity centrifugation caused fast (i.e. within 24 h) changes to fly leg muscle alternative splicing that correlated with body weight variation across eight lines. Hypergravity treatment also appeared to enhance leg muscle function, as centrifuged flies showed an increased negative geotaxis response and jump ability. Although the identity and location of the sensors and effectors involved remains unknown, our results provide further support for the existence of an evolutionarily conserved mechanism that translates signals that encode body weight into appropriate skeletal muscle molecular and functional responses.

The effects of genetic background on exercise performance in Drosophila

“…One method to increase load-bearing in flies is by simulating a hypergravity environment through centrifugation [ 42 ]. It is estimated that spinning flies at 12 g causes the leg muscles to support an additional 17–25 times the flies’ body weight [ 43 ]. Exposing flies to 12g for a 24-hour period resulted in increased jumping, negative geotaxis ability, and altered troponin T isoform splicing [ 43 ].…”

“…It is estimated that spinning flies at 12 g causes the leg muscles to support an additional 17–25 times the flies’ body weight [ 43 ]. Exposing flies to 12g for a 24-hour period resulted in increased jumping, negative geotaxis ability, and altered troponin T isoform splicing [ 43 ]. Additionally, when exposed to either 3g or 5g for a 2-week time period, male flies gained improved longevity [ 44 ] and, as they aged, performed similar to or better than flies exposed to only 1g on various behaviour assessments (spontaneous movement and climbing ability), indicating that their rate of ageing may have been slowed by hypergravity treatment [ 45 ].…”

Parasitic gut infection causes functional and molecular resemblance of Libellula pulchella dragonfly flight muscle to skeletal muscle of obese vertebrates

“…Zucker rats; Schilder et al, 2011). In healthy rats (Marden et al, 2008;Schilder and Raynor, 2017), Tnt alternative splicing is adjusted in a quantitative fashion in response to body weight changes due to natural growth or experimental body weight manipulations. Our current study suggests that similar, body weight-dependent adjustments in Tnt alternative splicing occur in L. pulchella flight muscle, as in noninfected individuals there was a statistically significant, positive correlation between body mass and the relative abundance of Tnt_Lp261 (Fig.…”

“…Tnt splice variant expression was analyzed in similar fashion to previous insect studies on this gene (Marden et al, 1999;Schilder and Raynor, 2017). Briefly, total RNA was extracted from frozen basalar muscle using Trizol reagent (Invitrogen, Carlsbad, CA, USA), precipitated in isopropanol and washed in ethanol, according to the manufacturer's instructions.…”

“…Thus, rat skeletal muscle Tnt expression of >300 g obese rats resembles that of much younger (<150 g), non-obese specimens. In contrast, experiments in non-obese, healthy rats, flies (Drosophila melanogaster) and moths (Spodoptera frugiperda), demonstrated that the relative abundance of Tnt mRNAs splice variants in load-bearing muscle is adjusted in proportion to body weight increase resulting from natural growth or experimental body weight manipulations (Marden et al, 2008;Schilder and Raynor, 2017;Schilder et al, 2011). Obesity therefore appears to cause an impairment of a sensing mechanism that relates body weight to skeletal muscle molecular composition.…”