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Mechanisms and Genes in Drosophila Hearing

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Mechanisms and Genes in Drosophila Hearing Review article e-Neuroforum 2014 · 5:72–76 M. Kittelmann · M.C. Göpfert DOI 10.1007/s13295-014-0063-7 Abteilung Zelluläre Neurobiologie, Universität Göttingen, Göttingen © Springer-Verlag 2014 Mechanisms and genes in Drosophila hearing Introduction Another important aspect was the ability ceivers, functionally corresponding to our to analyze molecular hearing mechanisms tympanic membrane. As the arista is stiff- The genome sequence of the fruit fly noninvasively, due to the direct coupling ly coupled to the funiculus, both compart- Drosophila melanogaster was published between molecular processes and the sys- ments swing around the longitudinal axis in 2000. One year later, a study screening tematic performance of the fly ear. of the latter upon exposure to sound. The the fly genome for disease-related genes funiculus rotation is directly detected by followed: 548 genes implicated in 714 hu- The Drosophila ear the mechanosensory cells of the Johnston’s man diseases were found. The first au- organ—the fly equivalent of the organ of thor of the study, Laurence Reiter, com- Drosophila males use courtship songs to Corti in the human ear. The Johnston’s or- mented “this came as a bit of a surprise as attract females. When females are in the gan is located in the pedicellus of the an- most people don’t think to study hearing proximity, males extend one of their wings tenna and consists of about 200 chordo- or cancer in Drosophila”. In terms of hear- and vibrate it in a regular pattern, result- tonal stretch receptors. Each of these re- ing, this is entirely true: we have known ing in a courtship song dominated by fre- ceptors contains two or three sensory that Drosophila can hear since the 1960s; quencies of around 200 Hz. These songs cells and several supporting cells, which however, for a long time, only few sci- enhance the receptivity of the females to form via mitotic division of a precursor entists investigated hearing in flies. The copulation and animate other males to cell. This precursor cell is specified via findings of these studies were astonishing sing along. the transcription factor atonal, which al- and hearing in fruit flies has thus become Males as well as females detect the so regulates the development of hair cells a very competitive field of research over courtship songs with their antennae. in the vertebrate ear. Despite this simi- the past years. Not only was the availabili- These are located at the front of the fly larity, fly auditory sensory cells and ver- ty of new genetic methods to analyze and head (. Fig. 1). Every antenna is com- tebrate hair cells are anatomically differ- manipulate the function of sensory cells posed of three main compartments—the ent: in flies these cells are bipolar mecha- in Drosophila essential, but the identifica- proximal scapus, the pedicellus and the nosensory neurons with a proximal axon tion of many functional parallels between distal funiculus. The club-shaped funicu- and a distal ciliated dendrite that is direct- fly and vertebrate hearing was also crucial. lus and its feathery arista are the sound re- ly attached to the funiculus via an extra- Fig. 1 8 Fly hearing organ a lateral view of the fly head. The antenna comprises the scapus (s), the pedicellus (p) and a funic- ulus (f) with a laterally attached arista (a). b Schemata of the antennal ear. The arista (a) and the funiculus (f) together form the sound receiver and rotate around the longitudinal axis of the latter when stimulated acoustically (dotted line and black arrows). Vibration of the funiculus is directly detected by the mechanosensory neurons of the Johnston’s organ in the pedi- cellus (p), which thus act as gravity and wind receptors or auditory sound receptors. c Schemata of a single mechanosenso- ry neuron of the Johnston’s organ with its proximal dendritic cilium, soma and axon. The Nan-Iav TRP ion channels localize to the proximal part of the cilium, the NOMPC TRP channels to the distal ciliary tip 72 | e-Neuroforum 3 · 2014 the loss of the other neuron classes does not affect this process. In addition to active amplification characteristics, mechanical signatures of transduction can be identified by analyz- ing the performance of the fly antennal re- ceiver and these are similar to the mech- anisms detectable in the mechanosenso- ry hair bundles of hair cells (. Fig. 2). Quantitatively, these transduction signa- tures in the fly ear can be well explained by the “gating spring model” of hair cell transduction. This model assumes a se- rial arrangement of mechanically ac- tivated ion channels, “gating springs” and motors. The gating springs are elas- tic elements that transfer force to the ion channel, whereby the deformation of the spring determines the opening probability of the channel. Upon opening of the chan- nel, the gating springs are relieved, which reduces the stiffness of the antennal re- ceiver. After prolonged deflection, chan- nels are closed by motors and the original stiffness is restored. Physical simulations have revealed that Fig. 2 8 a Active amplification and transduction. Sound-induced vibrations of the antennal receiv- the interplay between opening of the ion er (1) are transferred to the neurons of the Johnston’s organ (2), which then convert the vibration in- channels and the resulting motor move- to an electric signal (3). The transmission is realized by mechanically activated ion channels. The cou- ments is sufficient to explain active am- pling of the mechanical stimulus to the ion channels occurs via “gating springs”. Together with motors plification in the fly ear. This implies that (4), opening of the ion channels causes an active movement of the neurons, which amplify the sound- induced vibrations of the sound receiver. b Structure of the NOMPC protein. Besides a channel pore re- active amplification and transduction are gion, NOMPC contains 29 ankyrin residues that possibly act as a “gating spring”. Adapted from Göpfert coupled. The same transduction-driven [4] (a) and Zanini und Göpfert [10] (b) amplification mechanism explains the ac- tive motility of the sensory hair bundles cellular cap. The vibrations of the funic- Auditory mechanisms: active of vertebrate hair cells, which, alongside ulus are converted into electrical signals, amplification and transduction Prestin-driven somatic motility, contrib- which are then encoded as action poten- utes to active amplification in the verte- tials by the neurons and transmitted via The Drosophila ear does not contain a brate ear. their axons into the antennal mechano- middle ear and sensory cells are directly sensory motor center in the fly brain. coupled to the sound receiver. Therefore, Channels, gating Regarding their axonal projection tar- the neurons directly influence the mech- springs and motors get, the approximately 500 mechano- anistic behavior of the sound receiver, sensory neurons can be subdivided in- which can be measured noninvasively via Several ion channels of the transient re- to five classes, of which only the first two laser Doppler vibrometry. Analyses of the ceptor potential (TRP) family are in- are apparently true “hearing cells”: Cal- vibration characteristics of the antennal volved in transduction and amplification cium imaging showed that the 250 neu- receiver have shown that it exhibits all fea- in the fly ear, including the TRPN1 chan- rons of classes A and B are very sensitive tures of the cochlear receiver in vertebrate nel “No mechanoreceptor potential C” to vibrations of the funiculus, whereas the ears, i.e. it is an active amplifier based on (NOMPC), and the TRPV channels Nan- 200 neurons of classes C and E preferen- the active movement of the hair cells. Ge- chung (Nan) and Inactive (Iav). tially respond to sustained mechanical de- netic manipulations showed that corre- NOMPC is a mechanically activated flection of the funiculus and detect gravity sponding active deflection of the mech- mechanotransduction channel that lo- and wind. The remaining 50 class D neu- anosensory neurons in the Johnston’s or- calizes to the distal ciliary region of the rons are activated by prolonged deflection gan cause active amplification in the fly mechanosensory neurons. Loss of the and vibration of the funiculus, although ear and that only class A and B auditory channel leads to a complete loss of ac- large deflection and vibration amplitudes neurons are necessary: without these neu- tive amplification and sensitive hearing are required. rons, amplification is disrupted, whereas response. Without NOMPC, only loud e-Neuroforum 3 · 2014 | 73 Abstract · Zusammenfassung sounds can evoke an electric response yet been identified on a molecular level. e-Neuroforum 2014 · 5:72–76 in the fly ear. The latter responses likely NOMPC itself seems to be a good candi- DOI 10.1007/s13295-014-0063-7 © Springer-Verlag 2014 originate from the gravity and wind-sensi- date, as its N-terminus contains a molec- tive class C and E neurons, since they per- ular spring composed of 29 ankyrin res- M. Kittelmann · M.C. Göpfert sist when class A and B neurons are ab- idues. Recent findings suggest that this Mechanisms and genes lated and correlate with the calcium sig- spring couples the NOMPC channel to in Drosophila hearing nals in class C and E neurons. Signatures microtubules. Manipulation of the num- of the channel opening mechanics in the ber of ankyrin residues will be needed to Abstract The fruit fly Drosophila melanogaster com- antennal receiver provide evidence that show if these act as a gating spring. It is municates acoustically and hears with its an- NOMPC could be the transduction chan- also possible that the cell membrane em- tennae. Fundamental aspects of hearing can nel of the class A and B auditory neurons: bedding these channels acts as the gating be studied in these antennal ears, the audi- analyzing the mechanical responses of the spring—a possibility that is currently dis- tory sensory cells of which are evolutionarily sound receiver over a broad range of stim- cussed for hair cells.
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