Drosophila dEAAT2, a member of the excitatory amino-acid transporter (EAAT) family, has been described as mediating the high-affinity transport of taurine, which is a free amino-acid abundant in both insects and mammals. However, the role of taurine and its transporter in hearing is not clear. Here, we report that dEAAT2 is required for the larval startle response to sound stimuli. dEAAT2 was found to be enriched in the distal region of chordotonal neurons where sound transduction occurs. The Ca2+ imaging and electrophysiological results showed that disrupted dEAAT2 expression significantly reduced the response of chordotonal neurons to sound. More importantly, expressing dEAAT2 in the chordotonal neurons rescued these mutant phenotypes. Taken together, these findings indicate a critical role for Drosophila dEAAT2 in sound transduction by chordotonal neurons.
This is a preview of subscription content, log in to check access.
Buy single article
Instant unlimited access to the full article PDF.
Price includes VAT for USA
Huxtable R. Physiological actions of taurine. Physiol Rev 1992, 72: 101–163.
Green TR, Fellman JH, Eicher AL, Pratt KL. Antioxidant role and subcellular location of hypotaurine and taurine in human neutrophils. Biochim Biophys Acta 1991, 1073: 91–97.
Ripps H, Shen W. Taurine: a “very essential” amino acid. Mol Vis 2012, 18: 2673.
Sturman J, Gaull G. Taurine in the brain and liver of the developing human and monkey. J Neurochem 1975, 25: 831–835.
Sturman JA, Hayes KC. The biology of taurine in nutrition and development. Adv Nutr Res 1980: 231–299.
Davies W, Harding N, Kay I, Hopkins P. The role of taurine in mammalian hearing. In: Huxtable RJ, Michalk D (eds). Taurine in Health and Disease. Advances in Experimental Medicine and Biology. Boston, MA. Springer 1994, 359: 393–398.
Periman M. Taurine and auditory system maturation. Pediatrics 1989, 83: 796–798.
Davies WE, Hopkins PC, Rose SJ, Dhillon SK. The influence of different taurine diets on hearing development in normal babies. Adv Exp Med Biol 1996, 403: 631–637.
Dhillon SK, Davies WE, Hopkins PC, Rose SJ. Effects of dietary taurine on auditory function in full term infants. Adv Exp Med Biol 1998, 442: 507–514.
Tyson JE, Lasky R, Flood D, Mize C, Picone T, Paule CL. Randomized trial of taurine supplementation for infants ≤ 1,300-gram birth weight: effect on auditory brainstem-evoked responses. Pediatrics 1989, 83: 406–415.
Verner AM, McGuire W, Craig JS. Effect of taurine supplementation on growth and development in preterm or low birth weight infants. Cochrane Database Syst Rev 2007. https://doi.org/10.1002/14651858.cd006072.pub2.
Xu H, Wang W, Tang ZQ, Xu TL, Chen L. Taurine acts as a glycine receptor agonist in slices of rat inferior colliculus. Hear Res 2006, 220: 95–105.
Xu H, Zhou KQ, Huang YN, Chen L, Xu TL. Taurine activates strychnine-sensitive glycine receptors in neurons of the rat inferior colliculus. Brain Res 2004, 1021: 232–240.
Song NY, Shi HB, Li CY, Yin SK. Interaction between taurine and GABA(A)/glycine receptors in neurons of the rat anteroventral cochlear nucleus. Brain Res 2012, 1472: 1–10.
Harding N, Davies W. Cellular localisation of taurine in the organ of Corti. Hear Res 1993, 65: 211–215.
Horner KC, Aurousseau C. Immunoreactivity for taurine in the cochlea: its abundance in supporting cells. Hear Res 1997, 109: 135–142.
Usami S, Ottersen OP. The localization of taurine-like immunoreactivity in the organ of Corti: a semiquantitative, post-embedding immuno-electron microscopic analysis in the rat with some observations in the guinea pig. Brain Res 1995, 676: 277–284.
Warskulat U, Flögel U, Jacoby C, Hartwig HG, Thewissen M, Merx MW, et al. Taurine transporter knockout depletes muscle taurine levels and results in severe skeletal muscle impairment but leaves cardiac function uncompromised. FASEB J 2004, 18: 577–579.
Warskulat U, Borsch E, Reinehr R, Heller-Stilb B, Roth C, Witt M, et al. Taurine deficiency and apoptosis: findings from the taurine transporter knockout mouse. Arch Biochem Biophys 2007, 462: 202–209.
Danbolt NC. Glutamate uptake. Prog Neurobiol 2001, 65: 1–105.
Torres GE, Amara SG. Glutamate and monoamine transporters: new visions of form and function. Curr Opin Neurobiol 2007, 17: 304–312.
Rothstein JD, Martin L, Levey AI, Dykes-Hoberg M, Jin L, Wu D, et al. Localization of neuronal and glial glutamate transporters. Neuron 1994, 13: 713–725.
Rebillard G, Ruel J, Nouvian R, Saleh H, Pujol R, Dehnes Y, et al. Glutamate transporters in the guinea-pig cochlea: partial mRNA sequences, cellular expression and functional implications. Eur J Neurosci 2003, 17: 83–92.
Glowatzki E, Cheng N, Hiel H, Yi E, Tanaka K, Ellis-Davies GC, et al. The glutamate-aspartate transporter GLAST mediates glutamate uptake at inner hair cell afferent synapses in the mammalian cochlea. J Neurosci 2006, 26: 7659–7664.
Besson MT, Soustelle L, Birman S. Identification and structural characterization of two genes encoding glutamate transporter homologues differently expressed in the nervous system of Drosophila melanogaster. FEBS Lett 1999, 443: 97–104.
Besson MT, Soustelle L, Birman S. Selective high-affinity transport of aspartate by a Drosophila homologue of the excitatory amino-acid transporters. Curr Biol 2000, 10: 207–210.
Stacey SM, Muraro NI, Peco E, Labbé A, Thomas GB, Baines RA, et al. Drosophila glial glutamate transporter Eaat1 is regulated by fringe-mediated notch signaling and is essential for larval locomotion. J Neurosci 2010, 30: 14446–14457.
Besson MT, Ré DB, Moulin M, Birman S. High affinity transport of taurine by the Drosophila aspartate transporter dEAAT2. J Biol Chem 2005, 280: 6621–6626.
Besson M, Sinakevitch I, Melon C, Iché-Torres M, Birman S. Involvement of the Drosophila taurine/aspartate transporter dEAAT2 in selective olfactory and gustatory perceptions. J Comp Neurol 2011, 519: 2734–2757.
Tian Y, Zhang ZC, Han J. Drosophila studies on aurism spectrum disorders. Neurosci Bull 2017, 33: 737–746.
Pan Y. Sandman is a Sleep Switch in Drosophila. Neurosci Bull 2016, 32: 503–504.
Ou J, Gao Z, Song L, Ho MS. Analysis of glial distribution in Drosophila adult brains. Neurosci Bull 2016, 32: 162–170.
Field LH, Matheson T. Chordotonal organs of insects. Adv Insect Physiol 1998, 27: 1–228.
Boekhoff-Falk G. Hearing in Drosophila: development of Johnston’s organ and emerging parallels to vertebrate ear development. Dev Dyn 2005, 232: 550–558.
Senthilan PR, Piepenbrock D, Ovezmyradov G, Nadrowski B, Bechstedt S, Pauls S, et al. Drosophila auditory organ genes and genetic hearing defects. Cell 2012, 150: 1042–1054.
Kamikouchi A, Inagaki HK, Effertz T, Hendrich O, Fiala A, Göpfert MC, et al. The neural basis of Drosophila gravity-sensing and hearing. Nature 2009, 458: 165–171.
Yorozu S, Wong A, Fischer BJ, Dankert H, Kernan MJ, Kamikouchi A, et al. Distinct sensory representations of wind and near-field sound in the Drosophila brain. Nature 2009, 458: 201–205.
Zhang W, Yan Z, Jan LY, Jan YN. Sound response mediated by the TRP channels NOMPC, NANCHUNG, and INACTIVE in chordotonal organs of Drosophila larvae. Proc Natl Acad Sci U S A 2013, 110: 13612–13617.
Han C, Jan LY, Jan YN. Enhancer-driven membrane markers for analysis of nonautonomous mechanisms reveal neuron–glia interactions in Drosophila. Proc Natl Acad Sci U S A 2011, 108: 9673–9678.
Anderson M, Zheng Q, Dong X. Investigation of pain mechanisms by calcium imaging approaches. Neurosci Bull 2018, 34: 194–199.
Li K, Gong Z. Feeling hot and cold: thermal sensation in Drosophila. Neurosci Bull 2017, 33: 317–322.
Eberl DF. Feeling the vibes: chordotonal mechanisms in insect hearing. Curr Opin Neurobiol 1999, 9: 389–393.
Roy M, Sivan-Loukianova E, Eberl DF. Cell-type-specific roles of Na+/K+ ATPase subunits in Drosophila auditory mechanosensation. Proc Natl Acad Sci U S A 2013, 110: 181–186.
Todi SV, Sharma Y, Eberl DF. Anatomical and molecular design of the Drosophila antenna as a flagellar auditory organ. Microsc Res Tech 2004, 63: 388–399.
Yan Z, Zhang W, He Y, Gorczyca D, Xiang Y, Cheng LE, et al. Drosophila NOMPC is a mechanotransduction channel subunit for gentle-touch sensation. Nature 2013, 493: 221.
Kernan M, Cowan D, Zuker C. Genetic dissection of mechanotransduction: Drosophila mutations defective in mechanoreception. Neuron 1994, 12: 1195–1206.
Eberl DF, Duyk GM, Perrimon N. A genetic screen for mutations that disrupt an auditory response in Drosophila melanogaster. Proc Natl Acad Sci U S A 1997, 94: 14837–14842.
Jarman AP, Grau Y, Jan LY, Jan YN. atonal is a proneural gene that directs chordotonal organ formation in the Drosophila peripheral nervous system. Cell 1993, 73: 1307–1321.
Ebacher DJ, Todi SV, Eberl DF, Boekhoff-Falk GE. cut mutant Drosophila auditory organs differentiate abnormally and degenerate. Fly 2007, 1: 86–94.
Gong Z. Two interdependent TRPV channel subunits, inactive and nanchung, mediate hearing in Drosophila. J Neurosci 2004, 24: 9059–9066.
Effertz T, Wiek R, Göpfert MC. NompC TRP channel is essential for Drosophila sound receptor function. Curr Biol 2011, 21: 592–597.
Reddy D. Distribution of free ammo acids and related compounds in ocular fluids, lens, and plasma of various mammalian species. Invest Ophthalmol 1967, 6: 478–483.
Heinämäki A, Muhonen A, Piha R. Taurine and other free amino acids in the retina, vitreous, lens, irisciliary body, and cornea of the rat eye. Neurochem Res 1986, 11: 535–542.
Altshuler D, Turco JL, Rush J, Cepko C. Taurine promotes the differentiation of a vertebrate retinal cell type in vitro. Development 1993, 119: 1317–1328.
Rego AC, Santos MS, Oliveira CR. Oxidative stress, hypoxia, and ischemia-like conditions increase the release of endogenous amino acids by distinct mechanisms in cultured retinal cells. J Neurochem 1996, 66: 2506–2516.
Petrosian AM, Haroutounian JE. The role of taurine in osmotic, mechanical, and chemical protection of the retinal rod outer segments. Adv Exp Med Biol 1998: 407–413.
Militante J, Lombardini J. Pharmacological characterization of the effects of taurine on calcium uptake in the rat retina. Amino Acids 1998, 15: 99–108.
Jiang Z, Bulley S, Guzzone J, Ripps H, Shen W. The modulatory role of taurine in retinal ganglion cells. Adv Exp Med Biol 2013: 53–68.
Belluzzi O, Puopolo M, Benedusi M, Kratskin I. Selective neuroinhibitory effects of taurine in slices of rat main olfactory bulb. Neuroscience 2004, 124: 929–944.
Pramod AB, Foster J, Carvelli L, Henry LK. SLC6 transporters: structure, function, regulation, disease association and therapeutics. Mol Aspects Med 2013, 34: 197–219.
Heller-Stilb B, van Roeyen C, Rascher K, Hartwig HG, Huth A, Seeliger MW, et al. Disruption of the taurine transporter gene (taut) leads to retinal degeneration in mice. FASEB J 2002, 16: 231–233.
Strausfeld NJ, Sinakevitch I, Vilinsky I. The mushroom bodies of Drosophila melanogaster: an immunocytological and golgi study of Kenyon cell organization in the calyces and lobes. Microsc Res Tech 2003, 62: 151–169.
We thank Blooming Drosophila Stock Center and Yuh-Nung Jan for fly lines and the Shanghai Institute of Biochemistry and Cell Biology, Chinese Academy of Sciences, for the microinjection of plasmids into Drosophila embryos. The research was supported by funds from The Ministry of Science and Technology of China (2017YFA0103900 and 2016YFA0502800), The National Natural Science Foundation of China (31571083), The Program for Professor of Special Appointment (Eastern Scholar of Shanghai; TP2014008), The Shanghai Rising-Star Program (14QA1400800) and a grant from the Young 1000 Talent Program of China to ZY. The research was also supported by The National Natural Science Foundation of China (81470701), The National Natural Science Foundation of China (81771882) and The Fundamental Research (Discipline Layout) Foundation from Shenzhen Committee of Science, Technology and Innovation (JCYJ20170817111912585) to FC.
Conflict of interest
All authors claim that there are no conflicts of interest.
About this article
Cite this article
Sun, Y., Jia, Y., Guo, Y. et al. Taurine Transporter dEAAT2 is Required for Auditory Transduction in Drosophila. Neurosci. Bull. 34, 939–950 (2018) doi:10.1007/s12264-018-0255-1
- Drosophila dEAAT2
- Chordotonal neurons
- Sound transduction