Otic ablation of smoothened reveals direct and indirect requirements for hedgehog signaling in inner ear development

Development

Volumn 138, Issue 18, 2011, Pages 3967-3976

  Brown, Alexander S ^a   Epstein, Douglas J ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Cochlear vestibular ganglia; Inner ear; Mouse; Neurogenesis; Otic vesicle; Sonic hedgehog

Indexed keywords

SMOOTHENED PROTEIN; SONIC HEDGEHOG PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; COCHLEA; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; GENE EXPRESSION; GENE INACTIVATION; GENE REPRESSION; GENETIC TRANSCRIPTION; INNER EAR; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; VESTIBULAR SYSTEM;

ANIMALS; CELLS, CULTURED; COCHLEA; EAR, INNER; EMBRYO, MAMMALIAN; GENE DELETION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEDGEHOG PROTEINS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEUROGENESIS; ORGAN SPECIFICITY; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION;

ANIMALIA; ERINACEIDAE;

EID: 80051952308     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.066126     Document Type: Article

References (65)

1. Abello, G., Khatri, S., Radosevic, M., Scotting, P. J., Giraldez, F. and Alsina, B. (2010). Independent regulation of Sox3 and Lmx1b by FGF and BMP signaling influences the neurogenic and non-neurogenic domains in the chick otic placode. Dev. Biol. 339, 166-178
2. Acampora, D., Mazan, S., Avantaggiato, V., Barone, P., Tuorto, F., Lallemand, Y., Brulet, P. and Simeone, A. (1996). Epilepsy and brain abnormalities in mice lacking the Otx1 gene. Nat. Genet. 14, 218-222
3. Acampora, D., Merlo, G. R., Paleari, L., Zerega, B., Postiglione, M. P., Mantero, S., Bober, E., Barbieri, O., Simeone, A. and Levi, G. (1999). Craniofacial, vestibular and bone defects in mice lacking the Distal-less-related gene Dlx5. Development 126, 3795-3809
4. Alsina, B., Abello, G., Ulloa, E., Henrique, D., Pujades, C. and Giraldez, F. (2004). FGF signaling is required for determination of otic neuroblasts in the chick embryo. Dev. Biol. 267, 119-134
5. Ard, M. D. and Morest, D. K. (1984). Cell-death during development of the cochlear and vestibular ganglia of the chick. Int. J. Dev. Neurosci. 2, 535-547
6. Bok, J., Bronner-Fraser, M. and Wu, D. K. (2005). Role of the hindbrain in dorsoventral but not anteroposterior axial specification of the inner ear. Development 132, 2115-2124
7. Bok, J., Chang, W. and Wu, D. K. (2007a). Patterning and morphogenesis of the vertebrate inner ear. Int. J. Dev. Biol. 51, 521-533
8. Bok, J., Dolson, D. K., Hill, P., Ruther, U., Epstein, D. J. and Wu, D. K. (2007b). Opposing gradients of Gli repressor and activators mediate Shh signaling along the dorsoventral axis of the inner ear. Development 134, 1713-1722
9. Bok, J., Raft, S., Kong, K. A., Koo, S. K., Drager, U. C. and Wu, D. K. (2011). Transient retinoic acid signaling confers anterior-posterior polarity to the inner ear. Proc. Natl. Acad. Sci. USA 108, 161-166
10. Braunstein, E. M., Monks, D. C., Aggarwal, V. S., Arnold, J. S. and Morrow, B. E. (2009). Tbx1 and Brn4 regulate retinoic acid metabolic genes during cochlear morphogenesis. BMC Dev. Biol. 9, 31.
11. Burton, Q., Cole, L. K., Mulheisen, M., Chang, W. and Wu, D. K. (2004). The role of Pax2 in mouse inner ear development. Dev. Biol. 272, 161-175
12. Cayuso, J., Ulloa, F., Cox, B., Briscoe, J. and Marti, E. (2006). The Sonic hedgehog pathway independently controls the patterning, proliferation and survival of neuroepithelial cells by regulating Gli activity. Development 133, 517-528
13. Chiang, C., Litingtung, Y., Lee, E., Young, K. E., Corden, J. L., Westphal, H. and Beachy, P. A. (1996). Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383, 407-413
14. Dahmane, N. and Ruiz Altaba, A. (1999). Sonic hedgehog regulates the growth and patterning of the cerebellum. Development 126, 3089-3100
15. DasGupta, R. and Fuchs, E. (1999). Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. Development 126, 4557-4568
16. Depew, M. J., Liu, J. K., Long, J. E., Presley, R., Meneses, J. J., Pedersen, R. A. and Rubenstein, J. L. (1999). Dlx5 regulates regional development of the branchial arches and sensory capsules. Development 126, 3831-3846
17. Dessaud, E., McMahon, A. P. and Briscoe, J. (2008). Pattern formation in the vertebrate neural tube: a sonic hedgehog morphogen-regulated transcriptional network. Development 135, 2489-2503
18. Ernfors, P., Van De Water, T., Loring, J. and Jaenisch, R. (1995). Complementary roles of BDNF and NT-3 in vestibular and auditory development. Neuron 14, 1153-1164
19. Favor, J., Sandulache, R., Neuhauser-Klaus, A., Pretsch, W., Chatterjee, B., Senft, E., Wurst, W., Blanquet, V., Grimes, P., Sporle, R. et al. (1996). The mouse Pax2(1Neu) mutation is identical to a human PAX2 mutation in a family with renal-coloboma syndrome and results in developmental defects of the brain, ear, eye, and kidney. Proc. Natl. Acad. Sci. USA 93, 13870-13875
20. Fekete, D. M. and Wu, D. K. (2002). Revisiting cell fate specification in the inner ear. Curr. Opin. Neurobiol. 12, 35-42
21. Freyer, L. and Morrow, B. E. (2010). Canonical Wnt signaling modulates Tbx1, Eya1, and Six1 expression, restricting neurogenesis in the otic vesicle. Dev. Dyn. 239, 1708-1722
22. Fritzsch, B., Signore, M. and Simeone, A. (2001). Otx1 null mutant mice show partial segregation of sensory epithelia comparable to lamprey ears. Dev. Genes Evol. 211, 388-396
23. Garg, V., Yamagishi, C., Hu, T., Kathiriya, I. S., Yamagishi, H. and Srivastava, D. (2001). Tbx1, a DiGeorge syndrome candidate gene, is regulated by sonic hedgehog during pharyngeal arch development. Dev. Biol. 235, 62-73
24. Giraldez, F. (1998). Regionalized organizing activity of the neural tube revealed by the regulation of lmx1 in the otic vesicle. Dev. Biol. 203, 189-200
25. Hamby, J. M., Connolly, C. J., Schroeder, M. C., Winters, R. T., Showalter, H. D., Panek, R. L., Major, T. C., Olsewski, B., Ryan, M. J., Dahring, T. et al. (1997). Structure-activity relationships for a novel series of pyrido[2,3-d]pyrimidine tyrosine kinase inhibitors. J. Med. Chem. 40, 2296-2303
26. Hammond, K. L. and Whitfield, T. T. (2006). The developing lamprey ear closely resembles the zebrafish otic vesicle: otx1 expression can account for all major patterning differences. Development 133, 1347-1357
27. Hebert, J. M. and McConnell, S. K. (2000). Targeting of cre to the Foxg1 (BF-1) locus mediates loxP recombination in the telencephalon and other developing head structures. Dev. Biol. 222, 296-306
28. Hellard, D., Brosenitsch, T., Fritzsch, B. and Katz, D. M. (2004). Cranial sensory neuron development in the absence of brain-derived neurotrophic factor in BDNF/Bax double null mice. Dev. Biol. 275, 34-43
29. Kenney, A. M. and Rowitch, D. H. (2000). Sonic hedgehog promotes G(1) cyclin expression and sustained cell cycle progression in mammalian neuronal precursors. Mol. Cell. Biol. 20, 9055-9067
30. Kil, S. H., Streit, A., Brown, S. T., Agrawal, N., Collazo, A., Zile, M. H. and Groves, A. K. (2005). Distinct roles for hindbrain and paraxial mesoderm in the induction and patterning of the inner ear revealed by a study of vitamin-Adeficient quail. Dev. Biol. 285, 252-271
31. Klein, P. S. and Melton, D. A. (1996). A molecular mechanism for the effect of lithium on development. Proc. Natl. Acad. Sci. USA 93, 8455-8459
32. Koundakjian, E. J., Appler, J. L. and Goodrich, L. V. (2007). Auditory neurons make stereotyped wiring decisions before maturation of their targets. J. Neurosci. 27, 14078-14088
33. Lawoko-Kerali, G., Rivolta, M. N. and Holley, M. (2002). Expression of the transcription factors GATA3 and Pax2 during development of the mammalian inner ear. J. Comp. Neurol. 442, 378-391
34. Lawoko-Kerali, G., Rivolta, M. N., Lawlor, P., Cacciabue-Rivolta, D. I., Langton-Hewer, C., van Doorninck, J. H. and Holley, M. C. (2004). GATA3 and NeuroD distinguish auditory and vestibular neurons during development of the mammalian inner ear. Mech. Dev. 121, 287-299
35. Liang, J. K., Bok, J. and Wu, D. K. (2010). Distinct contributions from the hindbrain and mesenchyme to inner ear morphogenesis. Dev. Biol. 337, 324-334
36. Liao, J., Kochilas, L., Nowotschin, S., Arnold, J. S., Aggarwal, V. S., Epstein, J. A., Brown, M. C., Adams, J. and Morrow, B. E. (2004). Full spectrum of malformations in velo-cardio-facial syndrome/DiGeorge syndrome mouse models by altering Tbx1 dosage. Hum. Mol. Genet. 13, 1577-1585
37. Lillevali, K., Haugas, M., Matilainen, T., Pussinen, C., Karis, A. and Salminen, M. (2006). Gata3 is required for early morphogenesis and Fgf10 expression during otic development. Mech. Dev. 123, 415-429
38. Lin, Z., Cantos, R., Patente, M. and Wu, D. K. (2005). Gbx2 is required for the morphogenesis of the mouse inner ear: a downstream candidate of hindbrain signaling. Development 132, 2309-2318
39. Litingtung, Y. and Chiang, C. (2000). Specification of ventral neuron types is mediated by an antagonistic interaction between Shh and Gli3. Nat. Neurosci. 3, 979-985
40. Long, F., Zhang, X. M., Karp, S., Yang, Y. and McMahon, A. P. (2001). Genetic manipulation of hedgehog signaling in the endochondral skeleton reveals a direct role in the regulation of chondrocyte proliferation. Development 128, 5099-5108
41. Ma, Q., Chen, Z., del Barco Barrantes, I., de la Pompa, J. L. and Anderson, D. J. (1998). Neurogenin1 is essential for the determination of neuronal precursors for proximal cranial sensory ganglia. Neuron 20, 469-482
42. Madisen, L., Zwingman, T. A., Sunkin, S. M., Oh, S. W., Zariwala, H. A., Gu, H., Ng, L. L., Palmiter, R. D., Hawrylycz, M. J., Jones, A. R. et al. (2010). A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 13, 133-140
43. Martin, P. and Swanson, G. J. (1993). Descriptive and experimental analysis of the epithelial remodellings that control semicircular canal formation in the developing mouse inner ear. Dev. Biol. 159, 549-558
44. Martin, P. and Cockroft, D. L. (2008). Culture of postimplantation mouse embryos. Methods Mol. Biol. 461, 7-22
45. Matise, M. P., Epstein, D. J., Park, H. L., Platt, K. A. and Joyner, A. L. (1998). Gli2 is required for induction of floor plate and adjacent cells, but not most ventral neurons in the mouse central nervous system. Development 125, 2759-2770
46. Merlo, G. R., Paleari, L., Mantero, S., Zerega, B., Adamska, M., Rinkwitz, S., Bober, E. and Levi, G. (2002). The Dlx5 homeobox gene is essential for vestibular morphogenesis in the mouse embryo through a BMP4-mediated pathway. Dev. Biol. 248, 157-169
47. Morsli, H., Tuorto, F., Choo, D., Postiglione, M. P., Simeone, A. and Wu, D. K. (1999). Otx1 and Otx2 activities are required for the normal development of the mouse inner ear. Development 126, 2335-2343
48. Nissim, S., Allard, P., Bandyopadhyay, A., Harfe, B. D. and Tabin, C. J. (2007). Characterization of a novel ectodermal signaling center regulating Tbx2 and Shh in the vertebrate limb. Dev. Biol. 304, 9-21
49. Pachnis, V., Mankoo, B. and Costantini, F. (1993). Expression of the c-ret protooncogene during mouse embryogenesis. Development 119, 1005-1017
50. Phippard, D., Lu, L., Lee, D., Saunders, J. C. and Crenshaw, E. B., 3rd (1999). Targeted mutagenesis of the POU-domain gene Brn4/Pou3f4 causes developmental defects in the inner ear. J. Neurosci. 19, 5980-5989
51. Radde-Gallwitz, K., Pan, L., Gan, L., Lin, X., Segil, N. and Chen, P. (2004). Expression of Islet1 marks the sensory and neuronal lineages in the mammalian inner ear. J. Comp. Neurol. 477, 412-421
52. Raft, S., Nowotschin, S., Liao, J. and Morrow, B. E. (2004). Suppression of neural fate and control of inner ear morphogenesis by Tbx1. Development 131, 1801-1812
53. Riccomagno, M. M., Martinu, L., Mulheisen, M., Wu, D. K. and Epstein, D. J. (2002). Specification of the mammalian cochlea is dependent on Sonic hedgehog. Genes Dev. 16, 2365-2378
54. Riccomagno, M. M., Takada, S. and Epstein, D. J. (2005). Wnt-dependent regulation of inner ear morphogenesis is balanced by the opposing and supporting roles of Shh. Genes Dev. 19, 1612-1623
55. Robledo, R. F. and Lufkin, T. (2006). Dlx5 and Dlx6 homeobox genes are required for specification of the mammalian vestibular apparatus. Genesis 44, 425-437
56. Rowitch, D. H., St-Jacques, B., Lee, S. M. K., Flax, J. D., Snyder, E. Y. and McMahon, A. P. (1999). Sonic hedgehog regulates proliferation and inhibits differentiation of CNS precursor cells. J. Neurosci. 19, 8954-8965
57. Rubel, E. W. and Fritzsch, B. (2002). Auditory system development: primary auditory neurons and their targets. Annu. Rev. Neurosci. 25, 51-101
58. Schneider-Maunoury, S. and Pujades, C. (2007). Hindbrain signals in otic regionalization: walk on the wild side. Int. J. Dev. Biol. 51, 495-506
59. Schwander, M., Kachar, B. and Muller, U. (2010). Review series: The cell biology of hearing. J. Cell Biol. 190, 9-20
60. Straka, H., Vibert, N., Vidal, P. P., Moore, L. E. and Dutia, M. B. (2005). Intrinsic membrane properties of vertebrate vestibular neurons: function, development and plasticity. Prog. Neurobiol. 76, 349-392
61. Torres, M., Gomez-Pardo, E. and Gruss, P. (1996). Pax2 contributes to inner ear patterning and optic nerve trajectory. Development 122, 3381-3391
62. Vazquez-Echeverria, C., Dominguez-Frutos, E., Charnay, P., Schimmang, T. and Pujades, C. (2008). Analysis of mouse kreisler mutants reveals new roles of hindbrain-derived signals in the establishment of the otic neurogenic domain. Dev. Biol. 322, 167-178
63. Wechsler-Reya, R. J. and Scott, M. P. (1999). Control of neuronal precursor proliferation in the cerebellum by Sonic Hedgehog. Neuron 22, 103-114
64. Xu, H., Viola, A., Zhang, Z., Gerken, C. P., Lindsay-Illingworth, E. A. and Baldini, A. (2007). Tbx1 regulates population, proliferation and cell fate determination of otic epithelial cells. Dev. Biol. 302, 670-682
65. Yamagishi, H., Maeda, J., Hu, T., McAnally, J., Conway, S. J., Kume, T., Meyers, E. N., Yamagishi, C. and Srivastava, D. (2003). Tbx1 is regulated by tissue-specific forkhead proteins through a common Sonic hedgehog-responsive enhancer. Genes Dev. 17, 269-281.