Abstract

SummaryAcross their lives, biological sensors maintain near-constant functional outputs despite countless exogenous and endogenous perturbations. This sensory homeostasis is the product of multiple dynamic equilibria, the breakdown of which contributes to age-related decline. The mechanisms of homeostatic maintenance, however, are still poorly understood. The ears of vertebrates and insects are characterized by exquisite sensitivities but also by marked functional vulnerabilities. Being under the permanent load of thermal and acoustic noise, auditory transducer channels exemplify the homeostatic challenge. We show that (1) NompC-dependent mechanotransducers in the ear of the fruit fly Drosophila melanogaster undergo continual replacement with estimated turnover times of 9.1 hr; (2) a de novo synthesis of NompC can restore transducer function in the adult ears of congenitally hearing-impaired flies; (3) key components of the auditory transduction chain, including NompC, are under activity-dependent transcriptional control, likely forming a transducer-operated mechanosensory gain control system that extends beyond hearing organs.

Highlights

  • Ever since the seminal work of Rudolf Schoenheimer (Schoenheimer, 1946), the predominant theory of life is based on the concept of dynamic equilibria, where seemingly invariable states–or performances–are in truth the product of a homeostatic balance between assembling and disassembling processes

  • SUMMARY Across their lives, biological sensors maintain near-constant functional outputs despite countless exogenous and endogenous perturbations. This sensory homeostasis is the product of multiple dynamic equilibria, the breakdown of which contributes to age-related decline

  • We show that (1) NompC-dependent mechanotransducers in the ear of the fruit fly Drosophila melanogaster undergo continual replacement with estimated turnover times of 9.1 hr; (2) a de novo synthesis of NompC can restore transducer function in the adult ears of congenitally hearing-impaired flies; (3) key components of the auditory transduction chain, including NompC, are under activity-dependent transcriptional control, likely forming a transducer-operated mechanosensory gain control system that extends beyond hearing organs

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Summary

Introduction

Ever since the seminal work of Rudolf Schoenheimer (Schoenheimer, 1946), the predominant theory of life is based on the concept of dynamic equilibria, where seemingly invariable states–or performances–are in truth the product of a homeostatic balance between assembling and disassembling processes. Questions around the molecular and mechanistic logic of homeostasis have remained at the forefront of the life sciences; their answers will be of relevance for understanding the process of aging. During their development and life courses, biological tissues are being constantly modeled and re-modeled. The transduction of mechanical forces into biochemical signals is a key requirement for the development and homeostatic maintenance of all complex organs. Those organs that are themselves specialized for the transduction of minute mechanical forces, such as hearing organs, are arguably among the most complex sensory organs that have evolved (Albert and Kozlov, 2016).

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