Neuroscience Bulletin

, Volume 34, Issue 6, pp 939–950 | Cite as

Taurine Transporter dEAAT2 is Required for Auditory Transduction in Drosophila

  • Ying Sun
  • Yanyan Jia
  • Yifeng Guo
  • Fangyi ChenEmail author
  • Zhiqiang YanEmail author
Original Article


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.


Drosophila dEAAT2 Taurine Chordotonal neurons Sound transduction 



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.

Compliance with ethical standards

Conflict of interest

All authors claim that there are no conflicts of interest.

Supplementary material

12264_2018_255_MOESM1_ESM.pdf (1.6 mb)
Supplementary material 1 (PDF 1592 kb)

Supplementary material 2 (MP4 1228 kb)


  1. 1.
    Huxtable R. Physiological actions of taurine. Physiol Rev 1992, 72: 101–163.CrossRefGoogle Scholar
  2. 2.
    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.CrossRefGoogle Scholar
  3. 3.
    Ripps H, Shen W. Taurine: a “very essential” amino acid. Mol Vis 2012, 18: 2673.PubMedPubMedCentralGoogle Scholar
  4. 4.
    Sturman J, Gaull G. Taurine in the brain and liver of the developing human and monkey. J Neurochem 1975, 25: 831–835.CrossRefGoogle Scholar
  5. 5.
    Sturman JA, Hayes KC. The biology of taurine in nutrition and development. Adv Nutr Res 1980: 231–299.Google Scholar
  6. 6.
    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.Google Scholar
  7. 7.
    Periman M. Taurine and auditory system maturation. Pediatrics 1989, 83: 796–798.Google Scholar
  8. 8.
    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.CrossRefGoogle Scholar
  9. 9.
    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.CrossRefGoogle Scholar
  10. 10.
    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.PubMedGoogle Scholar
  11. 11.
    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. Scholar
  12. 12.
    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.CrossRefGoogle Scholar
  13. 13.
    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.CrossRefGoogle Scholar
  14. 14.
    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.CrossRefGoogle Scholar
  15. 15.
    Harding N, Davies W. Cellular localisation of taurine in the organ of Corti. Hear Res 1993, 65: 211–215.CrossRefGoogle Scholar
  16. 16.
    Horner KC, Aurousseau C. Immunoreactivity for taurine in the cochlea: its abundance in supporting cells. Hear Res 1997, 109: 135–142.CrossRefGoogle Scholar
  17. 17.
    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.CrossRefGoogle Scholar
  18. 18.
    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.CrossRefGoogle Scholar
  19. 19.
    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.CrossRefGoogle Scholar
  20. 20.
    Danbolt NC. Glutamate uptake. Prog Neurobiol 2001, 65: 1–105.CrossRefGoogle Scholar
  21. 21.
    Torres GE, Amara SG. Glutamate and monoamine transporters: new visions of form and function. Curr Opin Neurobiol 2007, 17: 304–312.CrossRefGoogle Scholar
  22. 22.
    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.CrossRefGoogle Scholar
  23. 23.
    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.CrossRefGoogle Scholar
  24. 24.
    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.CrossRefGoogle Scholar
  25. 25.
    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.CrossRefGoogle Scholar
  26. 26.
    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.CrossRefGoogle Scholar
  27. 27.
    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.CrossRefGoogle Scholar
  28. 28.
    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.CrossRefGoogle Scholar
  29. 29.
    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.CrossRefGoogle Scholar
  30. 30.
    Tian Y, Zhang ZC, Han J. Drosophila studies on aurism spectrum disorders. Neurosci Bull 2017, 33: 737–746.CrossRefGoogle Scholar
  31. 31.
    Pan Y. Sandman is a Sleep Switch in Drosophila. Neurosci Bull 2016, 32: 503–504.CrossRefGoogle Scholar
  32. 32.
    Ou J, Gao Z, Song L, Ho MS. Analysis of glial distribution in Drosophila adult brains. Neurosci Bull 2016, 32: 162–170.CrossRefGoogle Scholar
  33. 33.
    Field LH, Matheson T. Chordotonal organs of insects. Adv Insect Physiol 1998, 27: 1–228.CrossRefGoogle Scholar
  34. 34.
    Boekhoff-Falk G. Hearing in Drosophila: development of Johnston’s organ and emerging parallels to vertebrate ear development. Dev Dyn 2005, 232: 550–558.CrossRefGoogle Scholar
  35. 35.
    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.CrossRefGoogle Scholar
  36. 36.
    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.CrossRefGoogle Scholar
  37. 37.
    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.CrossRefGoogle Scholar
  38. 38.
    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.CrossRefGoogle Scholar
  39. 39.
    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.CrossRefGoogle Scholar
  40. 40.
    Anderson M, Zheng Q, Dong X. Investigation of pain mechanisms by calcium imaging approaches. Neurosci Bull 2018, 34: 194–199.CrossRefGoogle Scholar
  41. 41.
    Li K, Gong Z. Feeling hot and cold: thermal sensation in Drosophila. Neurosci Bull 2017, 33: 317–322.CrossRefGoogle Scholar
  42. 42.
    Eberl DF. Feeling the vibes: chordotonal mechanisms in insect hearing. Curr Opin Neurobiol 1999, 9: 389–393.CrossRefGoogle Scholar
  43. 43.
    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.CrossRefGoogle Scholar
  44. 44.
    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.CrossRefGoogle Scholar
  45. 45.
    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.CrossRefGoogle Scholar
  46. 46.
    Kernan M, Cowan D, Zuker C. Genetic dissection of mechanotransduction: Drosophila mutations defective in mechanoreception. Neuron 1994, 12: 1195–1206.CrossRefGoogle Scholar
  47. 47.
    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.CrossRefGoogle Scholar
  48. 48.
    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.CrossRefGoogle Scholar
  49. 49.
    Ebacher DJ, Todi SV, Eberl DF, Boekhoff-Falk GE. cut mutant Drosophila auditory organs differentiate abnormally and degenerate. Fly 2007, 1: 86–94.CrossRefGoogle Scholar
  50. 50.
    Gong Z. Two interdependent TRPV channel subunits, inactive and nanchung, mediate hearing in Drosophila. J Neurosci 2004, 24: 9059–9066.CrossRefGoogle Scholar
  51. 51.
    Effertz T, Wiek R, Göpfert MC. NompC TRP channel is essential for Drosophila sound receptor function. Curr Biol 2011, 21: 592–597.CrossRefGoogle Scholar
  52. 52.
    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.PubMedGoogle Scholar
  53. 53.
    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.CrossRefGoogle Scholar
  54. 54.
    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.PubMedGoogle Scholar
  55. 55.
    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.CrossRefGoogle Scholar
  56. 56.
    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.Google Scholar
  57. 57.
    Militante J, Lombardini J. Pharmacological characterization of the effects of taurine on calcium uptake in the rat retina. Amino Acids 1998, 15: 99–108.CrossRefGoogle Scholar
  58. 58.
    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.Google Scholar
  59. 59.
    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.CrossRefGoogle Scholar
  60. 60.
    Pramod AB, Foster J, Carvelli L, Henry LK. SLC6 transporters: structure, function, regulation, disease association and therapeutics. Mol Aspects Med 2013, 34: 197–219.CrossRefGoogle Scholar
  61. 61.
    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.CrossRefGoogle Scholar
  62. 62.
    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.CrossRefGoogle Scholar

Copyright information

© Shanghai Institutes for Biological Sciences, CAS and Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  1. 1.State Key Laboratory of Medical Neurobiology, Human Phenome Institute, Ministry of Education Key Laboratory of Contemporary Anthropology, Collaborative Innovation Center of Genetics and Development, Department of Physiology and Biophysics, School of Life SciencesFudan UniversityShanghaiChina
  2. 2.Department of Human Anatomy, School of Basic Medicine SciencesSouthwest Medical UniversityLuzhouChina
  3. 3.Department of Biomedical EngineeringSouthern University of Science and TechnologyShenzhenChina

Personalised recommendations