Drosophila auditory organ genes and genetic hearing defects

Cell

Volumn 150, Issue 5, 2012, Pages 1042-1054

  Senthilan, Pingkalai R ^a   Piepenbrock, David ^a   Ovezmyradov, Guvanch ^a   Nadrowski, Björn ^a   Bechstedt, Susanne ^b   Pauls, Stephanie ^a   Winkler, Margret ^a   Möbius, Wiebke ^c   Howard, Jonathon ^b   Göpfert, Martin C ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b MAX PLANCK INSTITUTE OF MOLECULAR CELL BIOLOGY AND GENETICS   (Germany)

^c MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AXONEMAL DYNEIN; ION CHANNEL; IONOTROPIC RECEPTOR; SENSORY RHODOPSIN;

ANIMAL EXPERIMENT; ARTICLE; AUDITORY STIMULATION; CHEMORECEPTOR; CONTROLLED STUDY; DROSOPHILA; EAR; GENE; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC ASSOCIATION; GENETIC DISORDER; GENETIC SUSCEPTIBILITY; HEARING; HEARING IMPAIRMENT; HEARING LOSS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SENSORIMOTOR FUNCTION; SIGNAL TRANSDUCTION; SOUND;

VERTEBRATA;

EID: 84865690410     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2012.06.043     Document Type: Article

References (101)

1. J.T. Albert, B. Nadrowski, and M.C. Göpfert Mechanical signatures of transducer gating in the Drosophila ear Curr. Biol. 17 2007 1000 1006
2. M. Ashburner, C.A. Ball, J.A. Blake, D. Botstein, H. Butler, J.M. Cherry, A.P. Davis, K. Dolinski, S.S. Dwight, J.T. Eppig The Gene Ontology Consortium Gene ontology: tool for the unification of biology Nat. Genet. 25 2000 25 29
3. D.A. Baker, K.M. Beckingham, and J.D. Armstrong Functional dissection of the neural substrates for gravitaxic maze behavior in Drosophila melanogaster J. Comp. Neurol. 501 2007 756 764
4. S. Bechstedt, and J. Howard Hearing mechanics: a fly in your ear Curr. Biol. 18 2008 R869 R870
5. S. Bechstedt, J.T. Albert, D.P. Kreil, T. Müller-Reichert, M.C. Göpfert, and J. Howard A doublecortin containing microtubule-associated protein is implicated in mechanotransduction in Drosophila sensory cilia Nat. Commun. 1 2010 11
6. H.J. Bellen, R.W. Levis, Y. He, J.W. Carlson, M. Evans-Holm, E. Bae, J. Kim, A. Metaxakis, C. Savakis, and K.L. Schulze The Drosophila gene disruption project: progress using transposons with distinctive site specificities Genetics 188 2011 731 743
7. R. Benton, K.S. Vannice, C. Gomez-Diaz, and L.B. Vosshall Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila Cell 136 2009 149 162
8. N.A. Bermingham, B.A. Hassan, S.D. Price, M.A. Vollrath, N. Ben-Arie, R.A. Eatock, H.J. Bellen, A. Lysakowski, and H.Y. Zoghbi Math1: an essential gene for the generation of inner ear hair cells Science 284 1999 1837 1841
9. B.T. Bloomquist, R.D. Shortridge, S. Schneuwly, M. Perdew, C. Montell, H. Steller, G.M. Rubin, and W.L. Pak Isolation of a putative phospholipase C gene of Drosophila, norpA, and its role in phototransduction Cell 54 1988 723 733
10. S. Cachero, T.I. Simpson, P.I. Zur Lage, L. Ma, F.G. Newton, E.E. Holohan, J.D. Armstrong, and A.P. Jarman The gene regulatory cascade linking proneural specification with differentiation in Drosophila sensory neurons PLoS Biol. 9 2011 e1000568
11. S. Carbon, A. Ireland, C.J. Mungall, S. Shu, B. Marshall, S. Lewis, G.O. Ami AmiGO Hub Web Presence Working Group AmiGO: online access to ontology and annotation data Bioinformatics 25 2009 288 289
12. J. Chevesich, A.J. Kreuz, and C. Montell Requirement for the PDZ domain protein, INAD, for localization of the TRP store-operated channel to a signaling complex Neuron 18 1997 95 105
13. S. Chien, L.T. Reiter, E. Bier, and M. Gribskov Homophila: human disease gene cognates in Drosophila Nucleic Acids Res. 30 2002 149 151
14. W.H. Chou, A. Huber, J. Bentrop, S. Schulz, K. Schwab, L.V. Chadwell, R. Paulsen, and S.G. Britt Patterning of the R7 and R8 photoreceptor cells of Drosophila: evidence for induced and default cell-fate specification Development 126 1999 607 616
15. B. Cook, R.W. Hardy, W.B. McConnaughey, and C.S. Zuker Preserving cell shape under environmental stress Nature 452 2008 361 364
16. J.L. Cooper, B.J. Till, and S. Henikoff Fly-TILL: reverse genetics using a living point mutation resource Fly (Austin) 2 2008 300 302
17. A.A. Dror, and K.B. Avraham Hearing loss: mechanisms revealed by genetics and cell biology Annu. Rev. Genet. 43 2009 411 437
18. D.F. Eberl, and G. Boekhoff-Falk Development of Johnston's organ in Drosophila Int. J. Dev. Biol. 51 2007 679 687
19. D.F. Eberl, G.M. Duyk, and N. Perrimon A genetic screen for mutations that disrupt an auditory response in Drosophila melanogaster Proc. Natl. Acad. Sci. USA 94 1997 14837 14842
20. D.F. Eberl, R.W. Hardy, and M.J. Kernan Genetically similar transduction mechanisms for touch and hearing in Drosophila J. Neurosci. 20 2000 5981 5988
21. T. Effertz, R. Wiek, and M.C. Göpfert NompC TRP channel is essential for Drosophila sound receptor function Curr. Biol. 21 2011 592 597
22. B. Fritzsch, K.W. Beisel, S. Pauley, and G. Soukup Molecular evolution of the vertebrate mechanosensory cell and ear Int. J. Dev. Biol. 51 2007 663 678
23. P.G. Gillespie, and U. Müller Mechanotransduction by hair cells: models, molecules, and mechanisms Cell 139 2009 33 44
24. Z. Gong, W. Son, Y.D. Chung, J. Kim, D.W. Shin, C.A. McClung, Y. Lee, H.W. Lee, D.J. Chang, and B.K. Kaang Two interdependent TRPV channel subunits, inactive and Nanchung, mediate hearing in Drosophila J. Neurosci. 24 2004 9059 9066
25. M.C. Göpfert, and D. Robert Biomechanics. Turning the key on Drosophila audition Nature 411 2001 908
26. M.C. Göpfert, J.T. Albert, B. Nadrowski, and A. Kamikouchi Specification of auditory sensitivity by Drosophila TRP channels Nat. Neurosci. 9 2006 999 1000
27. B.P. Gupta, and V. Rodrigues Atonal is a proneural gene for a subset of olfactory sense organs in Drosophila Genes Cells 2 1997 225 233
28. H. Haeberle, M. Fujiwara, J. Chuang, M.M. Medina, M.V. Panditrao, S. Bechstedt, J. Howard, and E.A. Lumpkin Molecular profiling reveals synaptic release machinery in Merkel cells Proc. Natl. Acad. Sci. USA 101 2004 14503 14508
29. 2+ channel in Drosophila photoreceptors Neuron 8 1992 643 651
30. W.A. Harris, and W.S. Stark Hereditary retinal degeneration in Drosophila melanogaster. A mutant defect associated with the phototransduction process J. Gen. Physiol. 69 1977 261 291
31. J. Herrero, F. Al-Shahrour, R. Díaz-Uriarte, A. Mateos, J.M. Vaquerizas, J. Santoyo, and J. Dopazo GEPAS: A web-based resource for microarray gene expression data analysis Nucleic Acids Res. 31 2003 3461 3467
32. M.S. Hildebrand, S.S. Newton, S.P. Gubbels, A.M. Sheffield, A. Kochhar, M.G. de Silva, H.H. Dahl, S.D. Rose, M.A. Behlke, and R.J. Smith Advances in molecular and cellular therapies for hearing loss Mol. Ther. 16 2008 224 236
33. A.J. Hudspeth Making an effort to listen: mechanical amplification in the ear Neuron 59 2008 530 545
34. A.P. Jarman, Y. Grau, L.Y. Jan, and Y.N. Jan atonal is a proneural gene that directs chordotonal organ formation in the Drosophila peripheral nervous system Cell 73 1993 1307 1321
35. A.P. Jarman, E.H. Grell, L. Ackerman, L.Y. Jan, and Y.N. Jan Atonal is the proneural gene for Drosophila photoreceptors Nature 369 1994 398 400
36. A.P. Jarman, Y. Sun, L.Y. Jan, and Y.N. Jan Role of the proneural gene, atonal, in formation of Drosophila chordotonal organs and photoreceptors Development 121 1995 2019 2030
37. A. Kamikouchi, H.K. Inagaki, T. Effertz, O. Hendrich, A. Fiala, M.C. Göpfert, and K. Ito The neural basis of Drosophila gravity-sensing and hearing Nature 458 2009 165 171
38. L. Kang, J. Gao, W.R. Schafer, Z. Xie, and X.Z. Xu C. elegans TRP family protein TRP-4 is a pore-forming subunit of a native mechanotransduction channel Neuron 67 2010 381 391
39. M. Kapushesky, P. Kemmeren, A.C. Culhane, S. Durinck, J. Ihmels, C. Körner, M. Kull, A. Torrente, U. Sarkans, J. Vilo, and A. Brazma Expression Profiler: next generation-an online platform for analysis of microarray data Nucleic Acids Res. 32 2004 W465-470
40. R.G. Kavlie, M.J. Kernan, and D.F. Eberl Hearing in Drosophila requires TilB, a conserved protein associated with ciliary motility Genetics 185 2010 177 188
41. M. Kernan, D. Cowan, and C. Zuker Genetic dissection of mechanosensory transduction: mechanoreception-defective mutations of Drosophila Neuron 12 1994 1195 1206
42. J. Kim, Y.D. Chung, D.Y. Park, S. Choi, D.W. Shin, H. Soh, H.W. Lee, W. Son, J. Yim, and C.S. Park A TRPV family ion channel required for hearing in Drosophila Nature 424 2003 81 84
43. A. Laurençon, R. Dubruille, E. Efimenko, G. Grenier, R. Bissett, E. Cortier, V. Rolland, P. Swoboda, and B. Durand Identification of novel regulatory factor X (RFX) target genes by comparative genomics in Drosophila species Genome Biol. 8 2007 R195
44. W. Liedtke, Y. Choe, M.A. Martí-Renom, A.M. Bell, C.S. Denis, A. Sali, A.J. Hudspeth, J.M. Friedman, and S. Heller Vanilloid receptor-related osmotically activated channel (VR-OAC), a candidate vertebrate osmoreceptor Cell 103 2000 525 535
45. L. Liu, Y. Li, R. Wang, C. Yin, Q. Dong, H. Hing, C. Kim, and M.J. Welsh Drosophila hygrosensation requires the TRP channels water witch and nanchung Nature 450 2007 294 298
46. (-Δ Δ C(T)) Method Methods 25 2001 402 408
47. Q. Lu, P.R. Senthilan, T. Effertz, B. Nadrowski, and M.C. Göpfert Using Drosophila for studying fundamental processes in hearing Integr. Comp. Biol. 49 2009 674 680
48. L. Ma, and A.P. Jarman Dilatory is a Drosophila protein related to AZI1 (CEP131) that is located at the ciliary base and required for cilium formation J. Cell Sci. 124 2011 2622 2630
49. M.P. McKenna, D.S. Hekmat-Scafe, P. Gaines, and J.R. Carlson Putative Drosophila pheromone-binding proteins expressed in a subregion of the olfactory system J. Biol. Chem. 269 1994 16340 16347
50. B.M. McDermott Jr., J.M. Baucom, and A.J. Hudspeth Analysis and functional evaluation of the hair-cell transcriptome Proc. Natl. Acad. Sci. USA 104 2007 11820 11825
51. M. Miron, O.Z. Woody, A. Marcil, C. Murie, R. Sladek, and R.A. Nadon A methodology for global validation of microarray experiments BMC Bioinformatics 7 2006 333
52. C. Montell, K. Jones, E. Hafen, and G. Rubin Rescue of the Drosophila phototransduction mutation trp by germline transformation Science 230 1985 1040 1043
53. B. Nadrowski, J.T. Albert, and M.C. Göpfert Transducer-based force generation explains active process in Drosophila hearing Curr. Biol. 18 2008 1365 1372
54. H.B. Nelson, R.G. Heiman, C. Bolduc, G.E. Kovalick, P. Whitley, M. Stern, and K. Beckingham Calmodulin point mutations affect Drosophila development and behavior Genetics 147 1997 1783 1798
55. B.A. Niemeyer, E. Suzuki, K. Scott, K. Jalink, and C.S. Zuker The Drosophila light-activated conductance is composed of the two channels TRP and TRPL Cell 85 1996 651 659
56. N. Niwa, Y. Hiromi, and M. Okabe A conserved developmental program for sensory organ formation in Drosophila melanogaster Nat. Genet. 36 2004 293 297
57. Y. Okazaki, M. Furuno, T. Kasukawa, J. Adachi, H. Bono, S. Kondo, I. Nikaido, N. Osato, R. Saito, H. Suzuki FANTOM Consortium RIKEN Genome Exploration Research Group Phase I & II Team Analysis of the mouse transcriptome based on functional annotation of 60,770 full-length cDNAs Nature 420 2002 563 573
58. C. Petit From deafness genes to hearing mechanisms: harmony and counterpoint Trends Mol. Med. 12 2006 57 64
59. 2+ in cochlear outer hair cells in the guinea pig and rat J. Physiol. 579 2007 101 113
60. J.P. Roche, P.A. Wackym, J.A. Cioffi, A.E. Kwitek, C.B. Erbe, and P. Popper In silico analysis of 2085 clones from a normalized rat vestibular periphery 3′ cDNA library Audiol. Neurootol. 10 2005 310 322
61. M. Rosenzweig, K. Kang, and P.A. Garrity Distinct TRP channels are required for warm and cool avoidance in Drosophila melanogaster Proc. Natl. Acad. Sci. USA 105 2008 14668 14673
62. R. Sarpal, S.V. Todi, E. Sivan-Loukianova, S. Shirolikar, N. Subramanian, E.C. Raff, J.W. Erickson, K. Ray, and D.F. Eberl Drosophila KAP interacts with the kinesin II motor subunit KLP64D to assemble chordotonal sensory cilia, but not sperm tails Curr. Biol. 13 2003 1687 1696
63. E. Savary, J.P. Hugnot, Y. Chassigneux, C. Travo, C. Duperray, T. Van De Water, and A. Zine Distinct population of hair cell progenitors can be isolated from the postnatal mouse cochlea using side population analysis Stem Cells 25 2007 332 339
64. E. Schaeffer, D. Smith, G. Mardon, W. Quinn, and C.S. Zuker Isolation and characterization of two new drosophila protein kinase C genes, including one specifically expressed in photoreceptor cells Cell 57 1989 403 412
65. S. Schulz, A. Huber, K. Schwab, and R. Paulsen A novel Ggamma isolated from Drosophila constitutes a visual G protein gamma subunit of the fly compound eye J. Biol. Chem. 274 1999 37605 37610
66. K. Scott, and C.S. Zuker Assembly of the Drosophila phototransduction cascade into a signalling complex shapes elementary responses Nature 395 1998 805 808
67. Y. Sharma, U. Cheung, E.W. Larsen, and D.F. Eberl PPTGAL, a convenient Gal4 P-element vector for testing expression of enhancer fragments in drosophila Genesis 34 2002 115 118
68. W.L. Shen, Y. Kwon, A.A. Adegbola, J. Luo, A. Chess, and C. Montell Function of rhodopsin in temperature discrimination in Drosophila Science 331 2011 1333 1336
69. B.H. Shieh, and B. Niemeyer A novel protein encoded by the InaD gene regulates recovery of visual transduction in Drosophila Neuron 14 1995 201 210
70. S. Sidi, R.W. Friedrich, and T. Nicolson NompC TRP channel required for vertebrate sensory hair cell mechanotransduction Science 301 2003 96 99
71. Thisse, B., and Thisse, C. (2004). Fast release clones: a high throughput expression analysis. ZFIN direct data submission (http://zfin.org).
72. J.-Y. Tinevez, F. Jülicher, and P. Martin Unifying the various incarnations of active hair-bundle motility by the vertebrate hair cell Biophys. J. 93 2007 4053 4067
73. S.V. Todi, J.D. Franke, D.P. Kiehart, and D.F. Eberl Myosin VIIA defects, which underlie the Usher 1B syndrome in humans, lead to deafness in Drosophila Curr. Biol. 15 2005 862 868
74. D. Vasiliauskas, E.O. Mazzoni, S.G. Sprecher, K. Brodetskiy, R.J. Johnston Jr., P. Lidder, N. Vogt, A. Celik, and C. Desplan Feedback from rhodopsin controls rhodopsin exclusion in Drosophila photoreceptors Nature 479 2011 108 112
75. R.G. Walker, and A.J. Hudspeth Calmodulin controls adaptation of mechanoelectrical transduction by hair cells of the bullfrog's sacculus Proc. Natl. Acad. Sci. USA 93 1996 2203 2207
76. R.G. Walker, A.T. Willingham, and C.S. Zuker A Drosophila mechanosensory transduction channel Science 287 2000 2229 2234
77. T. Wang, Y. Jiao, and C. Montell Dissection of the pathway required for generation of vitamin A and for Drosophila phototransduction J. Cell Biol. 177 2007 305 316
78. T. Weber, M.C. Göpfert, H. Winter, U. Zimmermann, H. Kohler, A. Meier, O. Hendrich, K. Rohbock, D. Robert, and M. Knipper Expression of prestin-homologous solute carrier (SLC26) in auditory organs of nonmammalian vertebrates and insects Proc. Natl. Acad. Sci. USA 100 2003 7690 7695
79. D. Weil, S. Blanchard, J. Kaplan, P. Guilford, F. Gibson, J. Walsh, P. Mburu, A. Varela, J. Levilliers, and M.D. Weston Defective myosin VIIA gene responsible for Usher syndrome type 1B Nature 374 1995 60 61
80. T. Yamada, Y. Takeuchi, N. Komori, H. Kobayashi, Y. Sakai, Y. Hotta, and H. Matsumoto A 49-kilodalton phosphoprotein in the Drosophila photoreceptor is an arrestin homolog Science 248 1990 483 486
81. S. Yarfitz, G.A. Niemi, J.L. McConnell, C.L. Fitch, and J.B. Hurley A G beta protein in the Drosophila compound eye is different from that in the brain Neuron 7 1991 429 438
82. S. Yorozu, A. Wong, B.J. Fischer, H. Dankert, M.J. Kernan, A. Kamikouchi, K. Ito, and D.J. Anderson Distinct sensory representations of wind and near-field sound in the Drosophila brain Nature 458 2009 201 205
83. J. Zheng, W. Shen, D.Z.Z. He, K.B. Long, L.D. Madison, and P. Dallos Prestin is the motor protein of cochlear outer hair cells Nature 405 2000 149 155
84. Baker, J.D., Adhikarakunnathu, S., and Kernan, M.J. (2004). Mechanosensory-defective, male-sterile unc mutants identify a novel basal body protein required for ciliogenesis in Drosophila. Development 131, 3411-3422.
85. Chou, W.H., Huber, A., Bentrop, J., Schulz, S., Schwab, K., Chadwell, L.V., Paulsen, R., and Britt, S.G. (1999). Patterning of the R7 and R8 photoreceptor cells of Drosophila: evidence for induced and default cell-fate specification. Development 126, 607-616.
86. Cosetti, M., Culang, D., Kotla, S., O'Brien, P., Eberl, D.F., and Hannan, F. (2008). Unique transgenic animal model for hereditary hearing loss. Ann. Otol. Rhinol. Laryngol. 117, 827-833.
87. Dubruille, R., Laurençon, A., Vandaele, C., Shishido, E., Coulon-Bublex, M., Swoboda, P., Couble, P., Kernan, M., and Durand, B. (2002). Drosophila regulatory factor X is necessary for ciliated sensory neuron differentiation. Development 129, 5487-5498.
88. Dong, P.D., Dicks, J.S., and Panganiban, G. (2002). Distal-less and homothorax regulate multiple targets to pattern the Drosophila antenna. Development 129, 1967-1974.
89. Dong, P.D., Todi, S.V., Eberl, D.F., and Boekhoff-Falk, G. (2003). Drosophila spalt/spalt-related mutants exhibit Townes-Brocks' syndrome phenotypes. Proc. Natl. Acad. Sci. USA 100, 10293-10298.
90. Ebacher, D.J., Todi, S.V., Eberl, D.F., and Boekhoff-Falk, G.E. (2007). Cut mutant Drosophila auditory organs differentiate abnormally and degenerate. Fly (Austin) 1, 86-94.
91. Elliott, S.L., Cullen, C.F., Wrobel, N., Kernan, M.J., and Ohkura, H. (2005). EB1 is essential during Drosophila development and plays a crucial role in the integrity of chordotonal mechanosensory organs. Mol. Biol. Cell 16, 891-901.
92. Göpfert, M.C., and Robert, D. (2003). Motion generation by Drosophila mechanosensory neurons. Proc. Natl. Acad. Sci. USA 100, 5514-5519.
93. Göpfert, M.C., Stocker, H., and Robert, D. (2002). atonal is required for exoskeletal joint formation in the Drosophila auditory system. Dev. Dyn. 225, 106-109.
94. Göpfert, M.C., Albert, J.T., Nadrowski, B., and Kamikouchi, A. (2006). Specification of auditory sensitivity by Drosophila TRP channels. Nat. Neurosci. 9, 999-1000.
95. Han, Y.G., Kwok, B.H., and Kernan, M.J. (2003). Intraflagellar transport is required in Drosophila to differentiate sensory cilia but not sperm. Curr. Biol. 13, 1679-1686.
96. (-Δ Δ C(T)) Method. Methods 25, 402-408.
97. Martinez-Campos, M., Basto, R., Baker, J., Kernan, M., and Raff, J.W. (2004). The Drosophila pericentrin-like protein is essential for cilia/flagella function, but appears to be dispensable for mitosis. J. Cell Biol. 165, 673-683.
98. Pfaffl, M.W. (2002). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45.
99. Schoen, C.J., Emery, S.B., Thorne, M.C., Ammana, H.R., Sliwerska, E., Arnett, J., Hortsch, M., Hannan, F., Burmeister, M., and Lesperance, M.M. (2010). Increased activity of Diaphanous homolog 3 (DIAPH3)/diaphanous causes hearing defects in humans with auditory neuropathy and in Drosophila. Proc. Natl. Acad. Sci. USA 107, 13396-13401.
100. Sun, Y., Liu, L., Ben-Shahar, Y., Jacobs, J.S., Eberl, D.F., and Welsh, M.J. (2009). TRPA channels distinguish gravity sensing from hearing in Johnston's organ. Proc. Natl. Acad. Sci. USA 106, 13606-13611.
101. Toivonen, J.M., O'Dell, K.M., Petit, N., Irvine, S.C., Knight, G.K., Lehtonen, M., Longmuir, M., Luoto, K., Touraille, S., Wang, Z., et al. (2001). Technical knockout, a Drosophila model of mitochondrial deafness. Genetics 159, 241-254.