Hearing in Drosophila: Development of Johnston's organ and emerging parallels to vertebrate ear development

Developmental Dynamics

Volumn 232, Issue 3, 2005, Pages 550-558

  Boekhoff Falk, Grace ^a  

^a UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

atonal; cut; distal less; myosin VIIA; nompA; nompC; prestin; SLC26, TRPV; spalt

Indexed keywords

ACOUSTIC NERVE FIBER; ANTENNA; ATH GENE; ATONAL GENE; AUDITORY SYSTEM; COCHLEA; CRINKLED GENE; DEVELOPMENTAL GENETICS; DISTAL LESS GENE; DLX GENE; DROSOPHILA; EAR; EAR DEVELOPMENT; GENE; HAIR CELL; HEARING; HEARING IMPAIRMENT; HUMAN; INACTIVE GENE; JOHNSTON ORGAN; MECHANOTRANSDUCTION; MYOSIN VIIA GENE; NANCHUNG GENE; NONHUMAN; ORGANOGENESIS; PRESTIN GENE; PRIORITY JOURNAL; REVIEW; SALL GENE; SPALT GENE; SPALT RELATED GENE; TRPV GENE; VERTEBRATE;

ANIMALS; DROSOPHILA; EAR; EMBRYO, NONMAMMALIAN; GENES, INSECT; HEARING; HUMANS; MODELS, ANATOMIC; SENSE ORGANS; VERTEBRATES;

EID: 14644443566     PISSN: 10588388     EISSN: None     Source Type: Journal    
DOI: 10.1002/dvdy.20207     Document Type: Review

References (99)

1. Acampora D, Merlo GR, Paleari L, Zerega B, Postiglione MP, Mantero S, Bober E, Barbieri O, Simeone A, Levi G. 1999. Craniofacial, vestibular and bone defects in mice lacking the Distal-less-related gene Dlx5. Development 126:3795-3809.
2. Adams M, Celniker S, Holt R, Evans CA, Gocayne J, Amanatides P, Scherer S, Li P, Hoskins R, Galle R, George R, Lewis S, Richards S, Ashburner M, Henderson S, Sutton G, Wortman J, Yandell M, Zhang Q, Chen L, Brandon R, Rogers Y, Blazej R, Champe M, Pfeiffer B, Wan K, Doyle C, Baxter E, Kelt G, Nelson C, Gabor Miklos G, Abril J, Agbayani A, An H, Andrews-Pfannkoch C, Baldwin D, Ballew R, Basu A, Baxendale J, Bayraktaroglu L, Beasley E, Beeson K, Benos P, Berman B, Bhandari D, Bolshakov S, Borkova D, Botchan M, Bouck J, Brokstein P, Brottier P, Burtis K, Busam D, Butler H, Cadieu E, Center A, Chandra I, Cherry J, Cawley S, Dahlke C, Davenport L, Davies P, de Pablos B, Delcher A, Deng Z, Mays A, Dew I, Dietz S, Dodson K, Doup L, Downes M, Dugan-Rocha S, Dunkov B, Dunn P, Durbin K, Evangelista C, Ferraz C, Ferriera S, Fleischmann W, Fosler C, Gabrielian A, Garg N, Gelbart W, Glasser K, Glodek A, Gong F, Gorrell J, Gu Z, Guan P, Harris M, Harris N, Harvey D, Heiman T, Hernandez J, Houck J, Hostin D, Houston K, Rowland T, Wei M, Ibegwam C, et al. 2000. The genome sequence of Drosophila melanogaster. Science 287:2185-2195.
3. Alper S, Chernova M, Stewart A. 2001. Regulation of Na+-independent Cl-/HCO3- exchangers by pH. J Pancreas 2:171-175.
4. Arendt D, Wittbrodt J. 2001. Reconstructing the eyes of Urbilateria. Philos Trans R Soc Lond Series B Biol Sci 356:1545-1563.
5. Bermingham NS, Hassan BA, Price SD, Vollrath MA, Ben-Arie N, Eatock RA, Bellen HJ, Lysakowski A, Zoghbi HY. 1999. Math1: an essential gene for the generation of inner ear hair cells. Science 284:1837-1841.
6. Blochlinger K, Jan L, Jan Y. 1991. Transformation of sensory organ identity by ectopic expression of Cut in Drosophila. Genes Dev 5:1124-1135.
7. Bodmer R, Jan YN. 1987. Morphological differentiation of the embryonic peripheral neurons in Drosophila. Roux's Arch Dev Biol 196:69-77.
8. Bodmer R, Barbel S, Shepherd S, Jack JW, Jan LY, Jan YN. 1987. Transformation of sensory organs by mutations of the cut locus of D. melanogaster. Cell 51:293-307.
9. Boyan G. 1993. Another look at insect audition: the tympanic receptors as an evolutionary specialization of the chordotonal system. J Insect Physiol 39:187-200.
10. Brinkmann M, Oliver D, Thurm U. 1996. Mechanoelectric transduction in nematocytes of a hydropolyp (Corynidae). J Comp Physiol 178:125-138.
11. Caldwell J, Eberl D. 2002. Towards a molecular understanding of Drosophila hearing. J Neurobiol 53:172-189.
12. Chung Y, Zhu J, Han Y, Kernan M. 2001. nompA encodes a PNS-specific, ZP domain protein required to connect mechanosensory dendrites to sensory structures. Neuron 29:415-428.
13. Clapham D. 2003. TRP channels as cellular sensors. Nature 426:517-524.
14. Cohen S. 1993. In: Bate M, Martinez-Arias A, editors. The development of Drosophila melanogaster. Vol. 2. New York: Cold Spring Harbor Laboratory Press, p 747-841.
15. Cohen SM. 1990. Specification of limb development in the Drosophila embryo by positional cues from segmentation genes. Nature 343:173-177.
16. Colbert H, Smith T, Bargmann C. 1997. OSM-9, a novel protein with structural similarity to channels, is required for olfaction, mechanosensation, and olfactory adaptation in Caenorhabditis elegans. J Neurosci 17:8259-8269.
17. Corey D. 2003. New TRP channels in hearing and mechanosensation. Neuron 39:575-588.
18. Corey D, Garcia-Anoveros J. 1996. Mechanosensation and the DEG/ENaC ion channels. Science 273:323-324.
19. Crackower MA, Scherer SW, Rommens JM, Hui CC, Poorkaj P, Soder S, Cobben JM, Hudgins L, Evans JP, Tsui LC. 1996. Characterization of the split hand/split foot malformation locus SHFM1 at 7q213-q221 and analysis of a candidate gene for its expression during limb development. Hum Mol Genet 5:571-579.
20. Dallos P. 1992. The active cochlea. J Neurosci 12:4575-4585.
21. Dallos P, Fakler B. 2002. Prestin, a new type of motor protein. Nat Rev Mol Cell Biol 3:104-111.
22. Dambly-Chaudiere C, Ghysen A. 1986. The sense organs in the Drosophila larva and their relation to the embryonic pattern of sensory neurons. Roux's Arch Dev Biol 195:222-228.
23. Depew MJ, Liu JK, Long JE, Presley R, Meneses JJ, Pedersen RA, Rubenstein JL. 1999. Dlx5 regulates regional development of the branchial arches and sensory capsules. Development 126:3831-3846.
24. Dong PDS, Chu J, Panganiban G. 2000. Coexpression of the homeobox genes Distal-less and homothorax determines Drosophila antennal identity. Development 127:209-216.
25. Dong PDS, Dicks JS, Panganiban G. 2002. Distal-less and homothorax regulate multiple targets to pattern the Drosophila antenna. Development 129:1967-1974.
26. Dong PDS, Todi SV, Eberl DF, Boekhoff-Falk G. 2003. Drosophila spalt/spalt-related mutants exhibit Townes-Brocks' Syndrome phenotypes. Proc Natl Acad Sci U S A 100:10293-10298.
27. Eberl DF. 1999. Feeling the vibes: chordotonal mechanisms in insect hearing. Curr Opin Neurobiol 9:389-393.
28. Eberl DF, Duyk GM, Perrimon N. 1997. A genetic screen for mutations that disrupt an auditory response in Drosophila melanogaster. Proc Natl Acad Sci USA 94:14837-14842.
29. Eberl D, Hardy R, Kernan M. 2000. Genetically similar transduction mechanisms for touch and hearing in Drosophila. J Neurosci 20:5981-5988.
30. Eddison M, Le Roux I, Lewis J. 2000. Notch signaling in the development of the inner ear: lessons from Drosophila. Proc Natl Acad Sci U S A 97:11692-11699.
31. Elstob PR, Brodu V, Gould AP. 2001. spalt-dependent switching between two cell fates that are induced by the Drosophila EGF receptor. Development 128:723-732.
32. Ernstrom G, Chalfie M. 2002. Genetics of sensory mechanotransduction. Annu Rev Genet 36:411-453.
33. Erwin DH, Davidson EH. 2002. The last common bilaterian ancestor. Development 129:3021-3032.
34. Fritzsch B, Beisel K. 2001. Evolution and development of the vertebrate ear. Brain Res Bull 55:711-721.
35. Fullard J, Yack J. 1993. The evolutionary biology of insect hearing. Trends Ecol Evol 8:248-252.
36. Gehring W. 2002. The genetic control of eye development and its implications for the evolution of the various eye-types. Int J Dev Biol 46:65-73.
37. Gillot C, editor. 1995. Book entomology. New York: Plenum Press.
38. Gong Z, Son W, Chung Y, Kim J, Shin D, McClung C, Lee Y, Lee H, Chang D-J, Kaang B-K, Cho H, Oh U, Hirsh J, Kernan M, Kim C. 2004. The interdependent TRPV channel subunits Inactive and Nanchung mediate hearing in Drosophila. J Neurosci 24:9059-9066.
39. Göpfert M, Robert D. 2001. Turning the key on Drosophila audition. Nature 411:908.
40. Göpfert M, Robert D. 2002. The mechanical basis of Drosophila audition. J Exp Biol 205:1199-1208.
41. Göpfert M, Robert D. 2003. Motion generation by Drosophila mechanosensory neurons. Proc Natl Acad Sci U S A 100:5514-5519.
42. Grens A, Mason E, Marsh J, Bode H. 1995. Evolutionary conservation of a cell fate specification gene: the Hydra achaetescute homolog has proneural activity in Drosophila. Development 121:4027-4035.
43. Hasson T, Heintzelman MB, Satnos-Sacchi J, Corey DP, Mooseker MS. 1995. Expression in the cochlea and retina of myosin Vila, the gene product defective in Usher syndrome type 1B. Proc Natl Acad Sci U S A 92:9815-9819.
44. Hausmann K, Holstein T. 1985. Sensory receptor with bilateral symmetrical polarity. Naturwissenschaften 72:145-146.
45. Hoy RR. 1998. Acute as a bug's ear: an informal discussion of hearing in insects. In: Hoy RR, Popper AN, Fay RR, editors. Comparative hearing: insects. New York: Springer, p 1-17.
46. Hoy R, Robert D. 1996. Tympanal hearing in insects. Annu Rev Entomol 41:433-450.
47. Hudspeth A. 1997. Mechanical amplification of stimuli by hair cells. Curr Opin Neurobiol 7:480-486.
48. Ignatius J, Knutila S, Scherer SW, Trask B, Kere J. 1996. Split hand/split foot malformation, deafness, and mental retardation with a complex cytogenetic rearrangement involving 7q213. J Med Genet 33:507-510.
49. Jarman AP. 2002. Studies of mechanosensation using the fly. Hum Mol Genet 11:1215-1218.
50. Jarman A, Ahmed I. 1998. The specificity of proneural genes in determining Drosophila sense organ identity. Mech Dev 76:117-125.
51. Jarman AP, Grau Y, Jan LY, Jan YN. 1993. atonal is a proneural gene that directs chordotonal organ formation in the Drosophila peripheral nervous system. Cell 73:1307-1321.
52. Jarman AP, Sun Y, Jan LY, Jan YN. 1995. Role of the proneural gene, atonal, in formation of Drosophila chordotonal organs and photoreceptors. Development 21:2019-2030.
53. Jovine L, Qi H, Williams Z, Litscher E, Wassarman P. 2002. The ZP domain is a conserved module for polymerization of extracellular proteins. Nat Cell Biol 4:457-461.
54. Kandel E, Schwartz J, Jessell T, editors. 2000. Book principles of neural science. New York: McGraw-Hill.
55. Keats B, Corey D. 1999. The Usher syndromes. Am J Med Genet 89:158-166.
56. Kemp DT. 2002. Otoacoustic emission, their origin in cochlear function, and use. British Medical Bulletin 63:223-241.
57. Kernan M, Cowan D, Zuker C. 1994. Genetic dissection of mechanosensory transduction: mechanoreception-defective mutations of Drosophila. Neuron 12:1195-1206.
58. Killick R, Legan P, Malenczak C, Richardson G. 1995. Molecular cloning of chick beta-tectorin, an extracellular matrix molecule of the inner ear. J Cell Biol 129:535-547.
59. Kim J, Chung Y, Park D, Choi S, Shin D, Soh H, Lee H, Son W, Yim J, Park C, Kernan M, Kim C. 2003. A TRPV family ion channel required for hearing in Drosophila. Nature 424:81-84.
60. Kohlhase J, Wischermann A, Reichenbach H, Froster U, Engel W. 1998. Mutations in the SALL1 putative transcription factor gene cause Townes-Brocks syndrome. Nat Genet 18:81-83.
61. Kohlhase J, Heinrich M, Schubert L, Liebers M, Kispert A, Laccone F, Turnpenny P, Winter R, Reardon W. 2002. Okihiro syndrome is caused by SALL4 mutations. Hum Mol Genet 11:2979-2987.
62. Kumar J, Moses K. 2001. Eye specification in Drosophila: perspectives and implications. Semin Cell Dev Biol 12:469-474.
63. Küppers J. 1974. Measurements on the ionic milieu of the receptor terminal in mechanoreceptive sensillae of insects. In: Schwartzkopf J, editor. Symposium on mechanoreception. Koln: Westdeutscher Verlag, p 387-394.
64. Kurant E, Pai CY, Sharf R, Halachmi N, Sun YH, Salzberg A. 1998. Dorsotonals/homothorax, the Drosophila homologue of meis1 interacts with extradenticle in patterning of the embryonic PNS. Development 125:1037-1048.
65. Legan P, Rau A, Keen J, Richardson G. 1997. The mouse tectorins. Modular matrix proteins of the inner ear homologous to components of the sperm-egg adhesion system. J Biol Chem 272:8791-8801.
66. Liedtke W, Choe Y, Marti-Renom M, Bell A, Denis C, SaIi A, Hudspeth A, Friedman J, Heller S. 2000. Vanilloid receptor-related osmotically activated channel (VR-OAC), a candidate vertebrate osmoreceptor. Cell 103:525-535.
67. Littleton J, Ganetzky B. 2000. Ion channels and synaptic organization: analysis of the Drosophila genome. Neuron 26:35-43.
68. Mano I, Driscoll M. 1999. DEG/ENaC channels: a touchy superfamily that watches its salt. Bioessays 21:568-578.
69. Meech R, Holley M. 2001. Ion-age molecular motors. Nat Neurosci 4:771-773.
70. Merlo GR, Paleari L, Mantero S, Genova F, Beverdam A, Palmisano GL, Barbieri O, Levi G. 2002. Mouse model of split hand/foot malformation type I. Genesis 33:97-101.
71. Merritt D. 1997. Transformation of external sensilla to chordotonal sensilla in the cut mutant of Drosophila assessed by single-cell marking in the embryo and larva. Microsc Res Tech 39:492-505.
72. Mishra P, Muranjan M, Bharucha BA. 2000. Autosomal dominant ectrodactyly with sensorineural deafness. Clin Dysmorphol 9:119-121.
73. Mutai H, Heller S. 2003. Vertebrate and invertebrate TRPV-like mechanoreceptors. Cell Calcium 33:471-478.
74. Niwa N, Hiromi Y, Okabe M. 2004. A conserved developmental program for sensory organ formation in Drosophila melanogaster. Nat Genet 36:293-297.
75. Nobili R, Mammano F, Ashmore J. 1998. How well do we understand the cochlea? Trends Neurosci 21:159-167.
76. Petersen M. 2002. Non-syndromic autosomal-dominant deafness. Clin Genet 62:1-13.
77. Pichaud F, Desplan C. 2002. Pax genes and eye organogenesis. Curr Opin Genet Dev 12:430-434.
78. Robledo RF, Rajan L, Li X, Lufkin T. 2002. The Dlx5 and Dlx6 homeobox genes are essential for craniofacial, axial and appendicular skeletal development. Genes Dev 16:1089-1101.
79. Robles L, Ruggero M. 2001. Mechanics of the mammalian cochlea. Physiol Rev 81:1305-1352.
80. Ruggero M. 1992. Responses to sound of the basilar membrane of the mammalian cochlea. Curr Opin Neurobiol 2:449-456.
81. Rusten TE, Gantera R, Urban J, Technau G, Kafatos FC, Barrio R. 2001. Spalt modifies EGFR-mediated induction of chordotonal precursors in the embryonic PNS of Drosophila promoting the development of oenocytes. Development 128:711-722.
82. Scherer SW, Poorkaj P, Massa H, Soder S, Allen T, Nunes M, Geshuri D, Wong E, Belloni E, Little S, et al. 1994. Physical mapping of the split hand/split foot locus on chromosome 7 and implication in syndromic ectrodactyly. Hum Mol Genet 3:1345-1354.
83. Sidi S, Friedrich R, Nicolson T. 2003. NompC TRP channel required for vertebrate sensory hair cell mechanotransduction. Science 301:96-99.
84. Skeath J. 1999. At the nexus between pattern formation and cell-type specification: the generation of individual neuroblast fates in the Drosophila embryonic central nervous system. Bioessays 21:922-931.
85. Solomon K, Fritz A. 2002. Concerted action of two dlx paralogs in sensory placode formation. Development 129:3127-3136.
86. Stumpner A, von Heiversen D. 2001. Evolution and function of auditory systems in insects. Naturwissenschaften 88:159-170.
87. Tabin CJ, Carroll SB, Panganiban G. 1999. Out on a limb: parallels in vertebrae and invertebrate limb patterning and the origin of appendages. Am Zool 39:650-663.
88. Tackels-Horne D, Toburen A, Sangiorgi E, Gurrieri F, de Mollerat X, Fischetto R, Causio F, Clarkson K, Stevenson RE, Schwartz CE. 2001. Split hand/split foot malformation with hearing loss: first report of families linked to the SHFM1 locus in 7q21. Clin Genet 59:28-36.
89. Thurm U, Küppers J. 1980. In: Locke M, Smith D, editors. Insect biology in the future. New York: Academic Press, p 735-763.
90. Tobin D, Madsen D, Kahn-Kirby A, Peckol E, Moulder G, Barstead R, Maricq A, Bargmann C. 2002. Combinatorial expression of TRPV channel proteins defines their sensory functions and subcellular localization in C. elegans neurons. Neuron 35:307-318.
91. Todi S, Sharma Y, Eberl D. 2004. Anatomical and molecular design of the Drosophila antenna as a flagellar auditory organ. Microsc Res Tech 63:388-399.
92. Wagner-Bernholz JT, Wilson C, Gibson G, Schuh R, Gehring WJ. 1991. Identification of target genes of the homeotic gene Antennapedia by enhancer detection. Genes Dev 5:2467-2480.
93. Walker RG. 2003. More whistles and bells for fly hearing. Proc Natl Acad Sci USA 100:5581-5582.
94. Walker RG, Willingham AT, Zuker CS. 2000. A Drosophila mechanosensory transduction channel. Science 287:2229-2234.
95. Weber T, Goepfert M, Winter H, Zimmermann U, Kohler H, Meier A, Hendrich O, Rohbock K, Robert D, Knipper M. 2003. Expression of prestin-homologous solute carrier (SLC26) in auditory organs of nonmamalian vertebrates and insects. Proc Natl Acad Sci U S A 100:7690-7695.
96. Weil D, Blanchard S, Kaplan J, Guilford P, Gibson F, Walsh J, Mburu P, Varela A, Levilliers J, Weston M, Kelley P, Kimberling W, Mariette Wagenaar M, Levi-Acobas F, Larget-Piet D, Munnich A, Steel K, Brown S, Petit C. 1995. Defective myosin VILA gene responsible for Usher syndrome type IB. Nature 374:60-61.
97. Wolfrum U, Liu X, Schmitt A, Udovichenko I, Williams D. 1998. Myosin VIIa as a common component of cilia and microvilli. Cell Motil Cytoskeleton 40:261-271.
98. Yager D. 1999. Structure, development and evolution of insect auditory systems. Microsc Res Tech 47:380-400.
99. Zheng J, Shen W, He D, Long K, Madison L, Dallos P. 2000. Prestin is the motor protein of cochlear outer hair cells. Nature 405:149-155.