Expression of Islet1 marks the sensory and neuronal lineages in the mammalian inner ear

Journal of Comparative Neurology

Volumn 477, Issue 4, 2004, Pages 412-421

  Radde Gallwitz, Kristen ^a   Pan, Ling ^b   Gan, Lin ^b   Lin, Xi ^a   Segil, Neil ^c   Chen, Ping ^a,c  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ROCHESTER   (United States)

^c HOUSE EAR INSTITUTE   (United States)

Author keywords

bHLH; LIM HD; Math1; Organ of Corti; Sensory hair cells; Spiral ganglion neurons

Indexed keywords

LIM PROTEIN; PROTEIN ISL1; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUDITORY SYSTEM; BHLH GENE; COCHLEA DUCT; CORTI ORGAN; EMBRYO; FEMALE; GENE; HAIR CELL; INNER EAR; MAMMAL; MOUSE; NERVE CELL DIFFERENTIATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; SENSORY NERVE CELL; SPIRAL GANGLION;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL LINEAGE; DNA-BINDING PROTEINS; EAR, INNER; FLUORESCENT ANTIBODY TECHNIQUE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; HOMEODOMAIN PROTEINS; IN SITU HYBRIDIZATION; LUMINESCENT PROTEINS; MICE; NEURONS, AFFERENT; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANSCRIPTION FACTORS;

EID: 4444272245     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.20257     Document Type: Article

References (56)

1. Adam J, Myat A, Le Rous I, Eddison M, Henrique D, Horowicz D, Lewis J. 1998. Cell fate choices and the expression of Notch, Delta and Serrate homologues in the chick inner ear: parallels with Drosophila sense-organ development. Development 125:4645-4654.
2. Allan DW, Thor S. 2003. Together at last: bHLH and LIM-HD regulators cooperate to specify motor neurons. Neuron 38:675-677.
3. Bachy I, Vernier P, Retaux S. 2001. The LIM-homeodomain gene family in the developing Xenopus brain: conservation and divergences with the mouse related to the evolution of the forebrain. J Neurosci 21:7620-7629.
4. Ben-Arie N, Bellen HJ, Armstrong DL, McCall AE, Gordadze PR, Guo Q, Matzuk MM, Zoghbi HY. 1997. Mathl is essential for genesis of cerebellar granule neurons. Nature 390:169-172.
5. Bermingham NA, Hassan BA, Price SD, Vollrath MA, Ben-Arie N, Eatock RA, Bellen HJ, Lysakowski A, Zoghbi HY. 1999. Mathl: an essential gene for the generation of inner ear hair cells. Science 284:1837-1841.
6. Bermingham NA, Hassan BA, Wang VY, Fernandez M, Banfi S, Bellen HJ, Fritzsch B, Zoghbi HY. 2001. Proprioceptor pathway development is dependent on Math1. Neuron 30:411-422.
7. Bilkei-Gorzo A, Racz I, Michel K, Zimmer A. 2002. Diminished anxiety- and depression-related behaviors in mice with selective deletion of the Tac1 gene. J Neurosci 22:10046-10052.
8. Bryant J, Goodyear RJ, Richardson GP. 2002. Sensory organ development in the inner ear: molecular and cellular mechanisms. Br Med Bull 63:39-57.
9. Chen P, Segil N. 1999. p27(Kip1) links cell proliferation to morphogenesis in the developing organ of Corti. Development 126:1581-1590.
10. Chen P, Johnson JE, Zoghbi HY, Segil N. 2002. The role of Math1 in inner ear development: uncoupling the establishment of the sensory primordium from hair cell fate determination. Development 129:2495-2505.
11. Chen P, Zindy F, Abdala C, Liu F, Li X, Roussel MF, Segil N. 2003. Progressive hearing loss in mice lacking the cyclin-dependent kinase inhibitor Ink4d. Nat Cell Biol 5:422-426.
12. Fekete D, Wu DK. 2002. Revisiting cell fate specification in the inner ear. Curr Opin Neurobiol 12:35-42.
13. Fritzsch B, Barald KF, Lomax MI. 1997. Early embryology of the vertebrate ear. In: Rubel EW, Popper AN, Fay RR, editors. Development of the auditory system. New York: Springer, p 80-145.
14. Fritzsch B, Beisel KW, Jones K, Farinas I, Maklad A, Lee J, Reichardt LF. 2002. Development and evolution of inner ear sensory epithelia and their innervation. J Neurobiol 53:143-156.
15. Gao WQ. 2003. Hair cell development in higher vertebrates. Curr Top Dev Biol 57:293-319.
16. Gowan K, Helms AW, Hunsaker TL, Collisson T, Ebert PJ, Odom R, Johnson JE. 2001. Crossinhibitory activities of ngn1 and math1 allow specification of distinct dorsal interneurons. Neuron 31:219-232.
17. Hasson T, Heintzelman MB, Santos-Sacchi J, Corey DP, Mooseker MS. 1995. Expression in cochlea and retina of myosin Vila, the gene product defective in Usher syndrome type 1B. Proc Natl Acad Sci USA 92:9815-9819.
18. Helms AW, Abney AL, Ben-Arie N, Zoghbi HY, Johnson JE. 2000. Auto-regulation and multiple enhancers control Math 1 expression in the developing nervous system. Development 127:1185-1196.
19. Hoang B, Moos M Jr, Vukicevic S, Luyten FP. 1996. Primary structure and tissue distribution of FRZB, a novel protein related to Drosophila frizzled, suggest a role in skeletal morphogenesis. J Biol Chem 271: 26131-26137.
20. Jonk LJ, de Jonge ME, Pals CE, Wissink S, Vervaart JM, Schoorlemmer J, Kruijer W. 1994. Cloning and expression during development of three murine members of the COUP family of nuclear orphan receptors. Mech Dev 47:81-97.
21. Kawamoto K, Ishimoto S, Minoda R, Brough DE, Raphael Y. 2003. Math 1 gene transfer generates new cochlear hair cells in mature guinea pigs in vivo. J Neurosci 23:4395-4400.
22. Kelley MW, Bianchi LM. 2001. Development and neuronal innervation of the organ of Corti. In: Willott JF, editor. Handbook of mouse auditory research. New York: CRC. p 137-156.
23. Kim WY, Fritzsch B, Serls A, Bakel LA, Huang EJ, Reichardt LF, Barth DS, Lee JE. 2001. NeuroD-null mice are deaf due to a severe loss of the inner ear sensory neurons during development. Development 128:417-426.
24. Lanford PJ, Lan Y, Jiang R, Lindsell C, Weinmaster G, Gridley T, Kelley MW. 1999. Notch signalling pathway mediates hair cell development in mammalian cochlea [see comments]. Nat Genet 21:289-292.
25. Lanford PJ, Shailam CR, Gridley NT, Kelley MW. 2000. Expression of Math1 and HES5 in the cochlea of wildtype and Jag2 mutant mice. J Assoc Res Otolaryngol 1:161-171.
26. Lawoko-Kerali G, Rivolta MN, Holley M. 2002. Expression of the transcription factors GATA3 and Pax2 during development of the mammalian inner ear. J Comp Neurol 442:378-391.
27. Lee JE. 1997a. Basic helix-loop-helix genes in neural development. Curr Opin Neurobiol 7:13-20.
28. Lee JE. 1997b. NeuroD and neurogenesis. Dev Neurosci 19:27-32.
29. Lee SK, Pfaff SL. 2003. Synchronization of neurogenesis and motor neuron specification by direct coupling of bHLH and homeodomain transcription factors. Neuron 38:731-745.
30. Lee MK, Tuttle JB, Rebhun LI, Cleveland DW, Frankfurter A. 1990. The expression and posttranslational modification of a neuron-specific β-tubulin isotype during chick embryogenesis. Cell Motil Cytoskel 17: 118-132.
31. Lewis J. 1996. Neurogenic genes and vertebrate neurogenesis. Curr Opin Neurobiol 6:3-10.
32. Leyns L, Bouwmeester T, Kim SH, Piccolo S, De Robertis EM. 1997. Frzb-1 is a secreted antagonist of Wnt signaling expressed in the Spemann organizer. Cell 88:747-756.
33. Liu M, Pereira FA, Price SD, Chu M, Shope C, Himes D, Eatock RA, Brownell WE, Lysakowski A, Tsai M. 2000. Essential role of Beta2/NeuroD1 in development of the vestibular and auditory systems. Genes Dev 14:2839-2854.
34. Lowenheim H, Furness DN, Kil J, Zinn C, Gultig K, Fero ML, Frost D, Gummer AW, Roberts JM, Rubel EW, Hackney CM, Zenner HP. 1999. Gene disruption of p27(Kip1) allows cell proliferation in the postnatal and adult organ of Corti. Proc Natl Acad Sci U S A 96:4084-4088.
35. Lumpkin EA, Collisson T, Parab P, Omer-Abdalla A, Haeberle H, Chen P, Doetzlhofer A, White P, Groves A, Segil N, Johnson JE. 2003. Math 1-driven GFP expression in the developing nervous system of transgenic mice. Gene Expr Patterns 3:389-395.
36. Ma Q, Kintner C, Anderson DJ. 1996. Identification of neurogenin, a vertebrate neuronal determination gene. Cell 87:43-52.
37. Ma Q, Chen Z, del Barco Barrantes I, dela Pompa JL, Anderson DJ. 1998. Neurogenini is essential for the determination of neuronal precursors for proximal cranial sensory ganglia. Neuron 20:469-482.
38. Ma Q, Fode C, Guillemot F, Anderson DJ. 1999. Neurogeninl and neurogenin2 control two distinct waves of neurogenesis in developing dorsal root ganglia. Genes Dev 13:1717-1728.
39. Ma Q, Anderson DJ, Fritzsch B. 2000. Neurogenin 1 null mutant ears develop fewer, morphologically normal hair cells in smaller sensory epithelia devoid of innervation. J Assoc Res Otolaryngol 1:129-144.
40. Morrison A, Hodgette C, Gossler A, Hrabe de Angelis M, Lewis J. 1999. Expression of Delta1 and Serrat1 (Jagged1) in the mouse inner ear. Mech Dev 84:169-172.
41. Morrow EM, Furukawa T, Lee JE, Cepko CL. 1999. NeuroD regulates multiple functions in the developing neural retina in rodent. Development 126:23-36.
42. Morsli H, Choo D, Ryan A, Johnson R, Wu DK. 1998. Development of the mouse inner ear and origin of its sensory organs. J Neurosci 18:3327-3335.
43. Pfaff SL, Mendelsohn M, Stewart CL, Edlund T, Jessell TM. 1996. Requirement for LIM homeobox gene Isl1 in motor neuron generation reveals a motor neuron-dependent step in interneuron differentiation. Cell 84:309-320.
44. Riley BB. 2003. Genes controlling the development of the zebrafish inner ear and hair cells. Curr Top Dev Biol 57:357-388.
45. Romand R, Varela-Nieto I. 2003. Development of auditory and vestibular system-3: molecular development of the inner ear. Curr Top Dev Biol 57:1-481.
46. Ruben RJ. 1967. Development of the inner ear of the mouse: a radioauto-graphic study of terminal mitoses. Acta Otolaryngol 220(Suppl)1-44.
47. Sahly I, El-Amraoui A, Abitbol M, Petit C, Dufier JL. 1997. Expression of myosin Vila during mouse embryogenesis. Anat Embryol (Berl) 196: 159-170.
48. Sher AE. 1971. The embryonic and postnatal development of the inner ear of the mouse. Acta Otolaryngol Suppl 285:1-77.
49. Shou J, Zheng JL, Gao WQ. 2003. Robust generation of new hair cells in the mature mammalian inner ear by adenoviral expression of Hath1. Mol Cell Neurosci 23:169-179.
50. Stone JS, Shang JL, Tomarev S. 2003. Expression of Prox1 defines regions of the avian otocyst that give rise to sensory or neural cells. J Comp Neurol 460:487-502.
51. Thaler JP, Koo SJ, Kania A, Lettier K, Andrews S, Cox C, Jessell TM, Praff SL. 2004. A postmitotic role for Isl-class LIM homeodomain proteins in the assignment of visceral spinal motor neuron identity. Neuron 41: 337-350.
52. Theiler K. 1989. The house mouse: atlas of embryonic development. New York: Springer-Verlag.
53. Wang S, Krinks M, Lin K, Luyten FP, Moos M Jr. 1997. Frzb, a secreted protein expressed in the Spemann organizer, binds and inhibits Wnt-8. Cell 88:757-766.
54. Yang Z, Dirg K, Pan L, Deng M, Gan L. 2003. Math5 determines the competence state of retinal ganglion cell progenitors. Dev Biol 264: 240-254.
55. Zheng JL, Gao WQ. 2000. Overexpression of Math1 induces robust production of extra hair cells in postnatal rat inner ears. Nat Neurosci 3:580-586.
56. Zheng JL, Shou J, Guillemot F, Kageyama R, Gao WQ. 2000. Hes1 is a negative regulator of inner ear hair cell differentiation. Development 127:4551-60.