Hedgehog signaling regulates sensory cell formation and auditory function in mice and humans

Journal of Neuroscience

Volumn 28, Issue 29, 2008, Pages 7350-7358

  Driver, Elizabeth Carroll ^a   Pryor, Shannon P ^a   Hill, Patrick ^c   Turner, Joyce ^b   Rüther, Ulrich ^c   Biesecker, Leslie G ^b   Griffith, Andrew J ^a   Kelley, Matthew W ^a  

^a NATIONAL INSTITUTE ON DEAFNESS AND OTHER COMMUNICATION DISORDERS   (United States)

^b NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^c HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

Cell fate; Cochlea; Development; Hair cell; Hedgehog; Pallister hall syndrome

Indexed keywords

NOTCH RECEPTOR; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GLI3; GLI3 PROTEIN, HUMAN; KRUPPEL LIKE FACTOR; NERVE PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FEMALE; HEARING LOSS; HUMAN; MOUSE; NEUROEPITHELIUM; NONHUMAN; PALLISTER HALL SYNDROME; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; SENSORY NERVE CELL; SIGNAL TRANSDUCTION; ANIMAL; BIOSYNTHESIS; C3H MOUSE; C57BL MOUSE; CELL DIFFERENTIATION; COCHLEA; COMPARATIVE STUDY; GENE EXPRESSION REGULATION; GENETICS; HAIR CELL; HEARING; INSTITUTE FOR CANCER RESEARCH MOUSE; MOUSE MUTANT; ORGAN CULTURE TECHNIQUE; PATHOLOGY; PHYSIOLOGY; PREGNANCY; PRENATAL DEVELOPMENT; TRANSGENIC MOUSE;

ANIMALS; AUDITORY PERCEPTION; CELL DIFFERENTIATION; COCHLEA; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HAIR CELLS, AUDITORY; HEDGEHOG PROTEINS; HUMANS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, INBRED ICR; MICE, MUTANT STRAINS; MICE, TRANSGENIC; NERVE TISSUE PROTEINS; NEURONS, AFFERENT; ORGAN CULTURE TECHNIQUES; PREGNANCY; SIGNAL TRANSDUCTION;

EID: 49049120372     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0312-08.2008     Document Type: Article

References (48)

1. Bai CB, Joyner AL (2001) Gli1 can rescue the in vivo function of Gli2. Development 128:5161-5172.
2. Bermingham NA, 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.
3. Bok J, Bronner-Fraser M, Wu DK (2005) Role of the hindbrain in dorsoventral but not anteroposterior axial specification of the inner ear. Development 132:2115-2124.
4. Bok J, Dolson DK, Hill P, Rüther U, Epstein DJ, Wu DK (2007) Opposing gradients of Gli repressor and activators mediate SHH signaling along the dorsoventral axis of the inner ear. Development 134:1713-1722.
5. Böse J, Grotewold L, Rüther U (2002) Pallister-Hall syndrome phenotype in mice mutant for Gli3. Hum Mol Genet 11:1129-1135.
6. Brooker R, Hozumi K, Lewis J (2006) Notch ligands with contrasting functions: Jagged1 and Delta1 in the mouse inner ear. Development 133:1277-1286.
7. Chen P, Segil N (1999) p27(Kip1) links cell proliferation to morphogenesis in the developing organ of Corti. Development 126:1581-1590.
8. Colvin JS, Bohne BA, Harding GW, McEwen DG, Ornitz DM (1996) Skeletal overgrowth and deafness in mice lacking fibroblast growth factor receptor 3. Nat Genet 12:390-397.
9. Dai P, Akimaru H, Tanaka Y, Maekawa T, Nakafuku M, Ishii S (1999) Sonic hedgehog-induced activation of the Gli1 promoter is mediated by GLI3. J Biol Chem 274:8143-8152.
10. Davis RL (2003) Gradients of neurotrophins, ion channels, and tuning in the cochlea. Neuroscientist 9:311-316.
11. De Strooper B, Annaert W, Cupers P, Saftig P, Craessaerts K, Mumm JS, Schroeter EH, Schrijvers V, Wolfe MS, Ray WJ, Goate A, Kopan R (1999) A presenilin-1-dependent gamma-secretase-like protease mediates release of Notch intracellular domain. Nature 398:518-522.
12. Hadland BK, Manley NR, Su D, Longmore GD, Moore CL, Wolfe MS, Schroeter EH, Kopan R (2001) Gamma-secretase inhibitors repress thymocyte development. Proc Natl Acad Sci U S A 98:7487-7491.
13. Hill P, Wang B, Rüther U (2007) The molecular basis of Pallister Hall associated polydactyly. Hum Mol Genet 16:2089-2096.
14. Hogan B (1994) Manipulating the mouse embryo: a laboratory manual, Ed 2. Plainview, NY: Cold Spring Harbor Laboratory.
15. Hooper JE, Scott MP (2005) Communicating with Hedgehogs. Nat Rev Mol Cell Biol 6:306-317.
16. Huangfu D, Anderson KV (2006) Signaling from Smo to Ci/Gli: conservation and divergence of Hedgehog pathways from Drosophila to vertebrates. Development 133:3-14.
17. International Organization for Standardization (1984) Acoustics - threshold of hearing by air conduction as a function of age and sex for otologically normal persons. Geneva: ISO 7029-1984.
18. Jacob J, Briscoe J (2003) Gli proteins and the control of spinal-cord patterning. EMBO Rep 4:761-765.
19. Johnston JJ, Olivos-Glander I, Killoran C, Elson E, Turner JT, Peters KF, Abbott MH, Aughton DJ, Aylsworth AS, Bamshad MJ, Booth C, Curry CJ, David A, Dinulos MB, Flannery DB, Fox MA, Graham JM, Grange DK, Guttmacher AE, Hannibal MC, et al. (2005) Molecular and clinical analyses of Greig cephalopolysyndactyly and Pallister-Hall syndromes: robust phenotype prediction from the type and position of GLI3 mutations. Am J Hum Genet 76:609-622.
20. Kang S, Graham JM Jr, Olney AH, Biesecker LG (1997) GLI3 frameshift mutations cause autosomal dominant Pallister-Hall syndrome. Nat Genet 15:266-268.
21. Kaufman MH (1992) The atlas of mouse development. London: Academic.
22. Kawamoto K, Ishimoto S, Minoda R, Brough DE, Raphael Y (2003) Math1 gene transfer generates new cochlear hair cells in mature guinea pigs in vivo. J Neurosci 23:4395-4400.
23. Kelley MW (2003) Cell adhesion molecules during inner ear and hair cell development, including notch and its ligands. Curr Top Dev Biol 57:321-356.
24. Kiernan AE, Cordes R, Kopan R, Gossler A, Gridley T (2005a) The Notch ligands DLL1 and JAG2 act synergistically to regulate hair cell development in the mammalian inner ear. Development 132:4353-4362.
25. Kiernan AE, Pelling AL, Leung KK, Tang AS, Bell DM, Tease C, Lovell-Badge R, Steel KP, Cheah KS (2005b) Sox2 is required for sensory organ development in the mammalian inner ear. Nature 434:1031-1035.
26. Kiernan AE, Xu J, Gridley T (2006) The Notch ligand JAG1 is required for sensory progenitor development in the mammalian inner ear. PLoS Genet 2:e4.
27. 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. Nat Genet 21:289-292.
28. Montcouquiol M, Kelley MW (2003) Planar and vertical signals control cellular differentiation and patterning in the mammalian cochlea. J Neurosci 23:9469-9478.
29. Mueller KL, Jacques BE, Kelley MW (2002) Fibroblast growth factor signaling regulates pillar cell development in the organ of corti. J Neurosci 22:9368-9377.
30. Murtaugh LC, Chyung JH, Lassar AB (1999) Sonic hedgehog promotes somitic chondrogenesis by altering the cellular response to BMP signaling. Genes Dev 13:225-237.
31. Nicolas M, Wolfer A, Raj K, Kummer JA, Mill P, van Noort M, Hui CC, Clevers H, Dotto GP, Radtke F (2003) Notch1 functions as a tumor suppressor in mouse skin. Nat Genet 33:416-421.
32. Pirvola U, Ylikoski J, Trokovic R, Hébert JM, McConnell SK, Partanen J (2002) FGFR1 is required for the development of the auditory sensory epithelium. Neuron 35:671-680.
33. Riccomagno MM, Martinu L, Mulheisen M, Wu DK, Epstein DJ (2002) Specification of the mammalian cochlea is dependent on Sonic hedgehog. Genes Dev 16:2365-2378.
34. Riccomagno MM, Takada S, Epstein DJ (2005) Wnt-dependent regulation of inner ear morphogenesis is balanced by the opposing and supporting roles of SHH. Genes Dev 19:1612-1623.
35. Rubel EW (1978) Ontogeny of structure and function in the vertebrate auditory system. In: Handbook of sensory physiology, Vol IX (Jacobson M, ed), pp 135-237. Berlin: Springer.
36. Sasaki H, Nishizaki Y, Hui C, Nakafuku M, Kondoh H (1999) Regulation of Gli2 and Gli3 activities by an amino-terminal repression domain: implication of Gli2 and Gli3 as primary mediators of SHH signaling. Development 126:3915-3924.
37. Sher AE (1971) The embryonic and postnatal development of the inner ear of the mouse. Acta Otolaryngol [Suppl] 285:1-77.
38. Szymko-Bennett YM, Mastroianni MA, Shotland LI, Davis J, Ondrey FG, Balog JZ, Rudy SF, McCullagh L, Levy HP, Liberfarb RM, Francomano CA, Griffith AJ (2001) Auditory dysfunction in Stickler syndrome. Arch Otolaryngol Head Neck Surg 127:1061-1068.
39. Takebayashi S, Yamamoto N, Yabe D, Fukuda H, Kojima K, Ito J, Honjo T (2007) Multiple roles of Notch signaling in cochlear development. Dev Biol 307:165-178.
40. Vortkamp A, Gessler M, Grzeschik KH (1991) GLI3 zinc-finger gene interrupted by translocations in Greig syndrome families. Nature 352:539-540.
41. Wang B, Fallon JF, Beachy PA (2000) Hedgehog-regulated processing of Gli3 produces an anterior/posterior repressor gradient in the developing vertebrate limb. Cell 100:423-434.
42. Wang Y, McMahon AP, Allen BL (2007) Shifting paradigms in Hedgehog signaling. Curr Opin Cell Biol 19:159-165.
43. Wersall J (1956) Studies on the structure and innervation of the sensory epithelium of the cristae ampulares in the guinea pig; a light and electron microscopic investigation. Acta Otolaryngol Suppl 126:1-85.
44. Woods C, Montcouquiol M, Kelley MW (2004) Math1 regulates development of the sensory epithelium in the mammalian cochlea. Nat Neurosci 7:1310-1318.
45. Xiang M, Gao WQ, Hasson T, Shin JJ (1998) Requirement for Brn-3c in maturation and survival, but not in fate determination of inner ear hair cells. Development 125:3935-3946.
46. Yabe D, Komuro R, Liang G, Goldstein JL, Brown MS (2003) Liver-specific mRNA for Insig-2 down-regulated by insulin: implications for fatty acid synthesis. Proc Natl Acad Sci U S A 100:3155-3160.
47. Zheng JL, Gao WQ (1997) Analysis of rat vestibular hair cell development and regeneration using calretinin as an early marker. J Neurosci 17:8270-8282.
48. 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.