Canal cristae growth and fiber extension to the outer hair cells of the mouse ear require Prox1 activity

PLoS ONE

Volumn 5, Issue 2, 2010, Pages

  Fritzsch, Bernd ^a   Dillard, Miriam ^b   Lavado, Alfonso ^b   Harvey, Natasha L ^b,c   Jahan, Israt ^a  

^a UNIVERSITY OF IOWA   (United States)

^b ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^c HANSON INSTITUTE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL FUNCTION; CELL GROWTH; COCHLEA; CONTROLLED STUDY; CORTI ORGAN; EMBRYO; GENE; HAIR CELL; HOMEOBOX; INNER EAR; INNERVATION; MOUSE; MOUSE STRAIN; NERVE FIBER; NESTIN CRE GENE; NONHUMAN; PROX1 GENE; VESTIBULE; ANIMAL; ANIMAL EMBRYO; CONFOCAL MICROSCOPY; EPITHELIUM; FEMALE; GENE EXPRESSION REGULATION; GENETICS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; METABOLISM; MOUSE MUTANT; MUTATION; NEWBORN; PREGNANCY; PRENATAL DEVELOPMENT; TIME; TRANSGENIC MOUSE; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

NES;

HOMEODOMAIN PROTEIN; PROSPERO RELATED HOMEOBOX 1 PROTEIN; PROSPERO-RELATED HOMEOBOX 1 PROTEIN; TUMOR SUPPRESSOR PROTEIN;

ANIMALS; ANIMALS, NEWBORN; CELL DIFFERENTIATION; COCHLEA; EAR, INNER; EMBRYO, MAMMALIAN; EPITHELIUM; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HAIR CELLS, AUDITORY, OUTER; HOMEODOMAIN PROTEINS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; MICROSCOPY, ELECTRON, TRANSMISSION; MUTATION; PREGNANCY; TIME FACTORS; TUMOR SUPPRESSOR PROTEINS; VESTIBULE, LABYRINTH;

EID: 77949609638     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0009377     Document Type: Article

References (77)

1. Fritzsch B, Beisel KW, Hansen LA (2006) The molecular basis of neurosensory cell formation in ear development: a blueprint for hair cell and sensory neuron regeneration? Bioessays 28: 1181-1193.
2. Kelley MW (2006) Regulation of cell fate in the sensory epithelia of the inner ear. Nat Rev Neurosci 7: 837-849.
3. Puligilla C, Feng F, Ishikawa K, Bertuzzi S, Dabdoub A, et al. (2007) Disruption of fibroblast growth factor receptor 3 signaling results in defects in cellular differentiation, neuronal patterning, and hearing impairment. Dev Dyn 236: 1905-1917.
4. Dabdoub A, Puligilla C, Jones JM, Fritzsch B, Cheah KS, et al. (2008) Sox2 signaling in prosensory domain specification and subsequent hair cell differentiation in the developing cochlea. Proc Natl Acad Sci U S A 105: 18396-18401.
5. Kelley MW (2006) Hair cell development: Commitment through differentiation. Brain Res.
6. Fritzsch B, Beisel KW, Bermingham NA (2000) Developmental evolutionary biology of the vertebrate ear: conserving mechanoelectric transduction and developmental pathways in diverging morphologies. Neuroreport 11: R35-44.
7. Adam J, Myat A, Le Roux I, Eddison M, Henrique D, et al. (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.
8. Caldwell JC, Eberl DF (2002) Towards a molecular understanding of Drosophila hearing. J Neurobiol 53: 172-189.
9. Jackson Behan K, Fair J, Singh S, Bogwitz M, Perry T, et al. (2005) Alternative splicing removes an Ets interaction domain from Lozenge during Drosophila eye development. Dev Genes Evol 215: 423-435.
10. Domingos PM, Brown S, Barrio R, Ratnakumar K, Frankfort BJ, et al. (2004) Regulation of R7 and R8 differentiation by the spalt genes. Dev Biol 273: 121-133.
11. Reddy GV, Rodrigues V (1999) A glial cell arises from an additional division within the mechanosensory lineage during development of the microchaete on the Drosophila notum. Development 126: 4617-4622.
12. Sen A, Reddy GV, Rodrigues V (2003) Combinatorial expression of Prospero, Seven-up, and Elav identifies progenitor cell types during sense-organ differentiation in the Drosophila antenna. Dev Biol 254: 79-92.
13. Cook T, Pichaud F, Sonneville R, Papatsenko D, Desplan C (2003) Distinction between color photoreceptor cell fates is controlled by Prospero in Drosophila. Dev Cell 4: 853-864.
14. Hayashi T, Saigo K (2001) Diversification of cell types in the Drosophila eye by differential expression of prepattern genes. Mech Dev 108: 13-27.
15. Oliver G, Sosa-Pineda B, Geisendorf S, Spana EP, Doe CQ, et al. (1993) Prox 1, a prospero-related homeobox gene expressed during mouse development. Mech Dev 44: 3-16.
16. Risebro CA, Searles RG, Melville AA, Ehler E, Jina N, et al. (2009) Prox1 maintains muscle structure and growth in the developing heart. Development 136: 495-505.
17. Wang J, Kilic G, Aydin M, Burke Z, Oliver G, et al. (2005) Prox1 activity controls pancreas morphogenesis and participates in the production of "secondary transition" pancreatic endocrine cells. Dev Biol 286: 182-194.
18. Wigle JT, Chowdhury K, Gruss P, Oliver G (1999) Prox1 function is crucial for mouse lens-fibre elongation. Nat Genet 21: 318-322.
19. Wigle JT, Harvey N, Detmar M, Lagutina I, Grosveld G, et al. (2002) An essential role for Prox1 in the induction of the lymphatic endothelial cell phenotype. Embo J 21: 1505-1513.
20. Dyer MA, Livesey FJ, Cepko CL, Oliver G (2003) Prox1 function controls progenitor cell proliferation and horizontal cell genesis in the mammalian retina. Nat Genet 34: 53-58.
21. Lavado A, Oliver G (2007) Prox1 expression patterns in the developing and adult murine brain. Dev Dyn 236: 518-524.
22. Burke Z, Oliver G (2002) Prox1 is an early specific marker for the developing liver and pancreas in the mammalian foregut endoderm. Mech Dev 118: 147-155.
23. Johnson NC, Dillard ME, Baluk P, McDonald DM, Harvey NL, et al. (2008) Lymphatic endothelial cell identity is reversible and its maintenance requires Prox1 activity. Genes Dev 22: 3282-3291.
24. Petrova TV, Nykanen A, Norrmen C, Ivanov KI, Andersson LC, et al. (2008) Transcription factor PROX1 induces colon cancer progression by promoting the transition from benign to highly dysplastic phenotype. Cancer Cell 13: 407-419.
25. Misra K, Gui H, Matise MP (2008) Prox1 regulates a transitory state for interneuron neurogenesis in the spinal cord. Dev Dyn 237: 393-402.
26. Glasgow E, Tomarev SI (1998) Restricted expression of the homeobox gene prox 1 in developing zebrafish. Mech Dev 76: 175-178.
27. 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.
28. Bermingham-McDonogh O, Oesterle EC, Stone JS, Hume CR, Huynh HM, et al. (2006) Expression of Prox1 during mouse cochlear development. J Comp Neurol 496: 172-186.
29. Kirjavainen A, Sulg M, Heyd F, Alitalo K, Yla-Herttuala S, et al. (2008) Prox1 interacts with Atoh1 and Gfi1, and regulates cellular differentiation in the inner ear sensory epithelia. Dev Biol 322: 33-45.
30. Harvey NL, Srinivasan RS, Dillard ME, Johnson NC, Witte MH, et al. (2005) Lymphatic vascular defects promoted by Prox1 haploinsufficiency cause adult-onset obesity. Nat Genet 37: 1072-1081.
31. Wigle JT, Oliver G (1999) Prox1 function is required for the development of the murine lymphatic system. Cell 98: 769-778.
32. Hayashi S, McMahon AP (2002) Efficient recombination in diverse tissues by a tamoxifen-inducible form of Cre: a tool for temporally regulated gene activation/inactivation in the mouse. Dev Biol 244: 305-318.
33. Ohyama T, Groves AK (2004) Generation of Pax2-Cre mice by modification of a Pax2 bacterial artificial chromosome. Genesis 38: 195-199.
34. Ben-Arie N, Bellen HJ, Armstrong DL, McCall AE, Gordadze PR, et al. (1997) Math1 is essential for genesis of cerebellar granule neurons. Nature 390: 169-172.
35. Srinivasan RS, Dillard ME, Lagutin OV, Lin F-J, Tsai S, et al. (2007) Lineage tracing demonstrates the venous origin of the mammalian lymphatic vasculature. Genes & Dev in press.
36. Betz UA, Vosshenrich CA, Rajewsky K, Muller W (1996) Bypass of lethality with mosaic mice generated by Cre-loxP-mediated recombination. Curr Biol 6: 1307-1316.
37. Fritzsch B, Matei VA, Nichols DH, Bermingham N, Jones K, et al. (2005) Atoh1 null mice show directed afferent fiber growth to undifferentiated ear sensory epithelia followed by incomplete fiber retention. Dev Dyn 233: 570-583.
38. Matei VA, Feng F, Pauley S, Beisel KW, Nichols MG, et al. (2006) Near-infrared laser illumination transforms the fluorescence absorbing X-Gal reaction product BCI into a transparent, yet brightly fluorescent substance. Brain Res Bull 70: 33-43.
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: 129-143.
40. Matei V, Pauley S, Kaing S, Rowitch D, Beisel KW, et al. (2005) Smaller inner ear sensory epithelia in Neurog1 null mice are related to earlier hair cell cycle exit. Dev Dyn 234: 633-650.
41. Fritzsch B, Muirhead KA, Feng F, Gray BD, Ohlsson-Wilhelm BM (2005) Diffusion and imaging properties of three new lipophilic tracers, NeuroVuetrade mark Maroon, NeuroVuetrade mark Red and NeuroVuetrade mark Green and their use for double and triple labeling of neuronal profile. Brain Res Bull 66: 249-258.
42. von Bartheld CS (2001) Comparison of 2-D and 3-D counting: the need for calibration and common sense. Trends Neurosci 24: 504-506.
43. Ward TS, Rosen GD, von Bartheld CS (2007) Optical disector counting in cryosections and vibratome sections underestimates particle numbers: Effects of tissue quality. Microsc Res Tech.
44. Ruben RJ (1967) Development of the inner ear of the mouse: a radioautographic study of terminal mitoses. Acta Otolaryngol Suppl 220: 221-244.
45. Lee YS, Liu F, Segil N (2006) A morphogenetic wave of p27Kip1 transcription directs cell cycle exit during organ of Corti development. Development 133: 2817-2826.
46. 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.
47. 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.
48. Ohyama T, Mohamed OA, Taketo MM, Dufort D, Groves AK (2006) Wnt signals mediate a fate decision between otic placode and epidermis. Development 133: 865-875.
49. Jones C, Chen P (2007) Planar cell polarity signaling in vertebrates. Bioessays 29: 120-132.
50. Bermingham NA, Hassan BA, Price SD, Vollrath MA, Ben-Arie N, et al. (1999) Math1: an essential gene for the generation of inner ear hair cells. Science 284: 1837-1841.
51. Pauley S, Kopecky B, Beisel K, Soukup G, Fritzsch B (2008) Stem cells and molecular strategies to restore hearing. Panminerva Med 50: 41-53.
52. Rubel EW, Fritzsch B (2002) Auditory system development: primary auditory neurons and their targets. Annu Rev Neurosci 25: 51-101.
53. Morris JK, Maklad A, Hansen LA, Feng F, Sorensen C, et al. (2006) A disorganized innervation of the inner ear persists in the absence of ErbB2. Brain Res 1091: 186-199.
54. Fritzsch B (2003) Development of inner ear afferent connections: forming primary neurons and connecting them to the developing sensory epithelia. Brain Res Bull 60: 423-433.
55. Koundakjian EJ, Appler JL, Goodrich LV (2007) Auditory neurons make stereotyped wiring decisions before maturation of their targets. J Neurosci 27: 14078-14088.
56. Huang LC, Thorne PR, Housley GD, Montgomery JM (2007) Spatiotemporal definition of neurite outgrowth, refinement and retraction in the developing mouse cochlea. Development 134: 2925-2933.
57. Li H, Liu H, Heller S (2003) Pluripotent stem cells from the adult mouse inner ear. Nat Med 9: 1293-1299.
58. Simmons DD (2002) Development of the inner ear efferent system across vertebrate species. J Neurobiol 53: 228-250.
59. Bruce LL, Kingsley J, Nichols DH, Fritzsch B (1997) The development of vestibulocochlear efferents and cochlear afferents in mice. Int J Dev Neurosci 15: 671-692.
60. Jensen-Smith H, Gray B, Muirhead K, Ohlsson-Wilhelm B, Fritzsch B (2007) Long-distance three-color neuronal tracing in fixed tissue using NeuroVue dyes. Immunol Invest 36: 763-789.
61. Karis A, Pata I, van Doorninck JH, Grosveld F, de Zeeuw CI, et al. (2001) Transcription factor GATA-3 alters pathway selection of olivocochlear neurons and affects morphogenesis of the ear. J Comp Neurol 429: 615-630.
62. Pauley S, Wright TJ, Pirvola U, Ornitz D, Beisel K, et al. (2003) Expression and function of FGF10 in mammalian inner ear development. Dev Dyn 227: 203-215.
63. Pauley S, Lai E, Fritzsch B (2006) Foxg1 is required for morphogenesis and histogenesis of the mammalian inner ear. Dev Dyn 235: 2470-2482.
64. Kiernan AE, Pelling AL, Leung KK, Tang AS, Bell DM, et al. (2005) Sox2 is required for sensory organ development in the mammalian inner ear. Nature 434: 1031-1035.
65. Nichols DH, Pauley S, Jahan I, Beisel KW, Millen KJ, et al. (2008) Lmx1a is required for segregation of sensory epithelia and normal ear histogenesis and morphogenesis. Cell Tissue Res 334: 339-358.
66. 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.
67. Chang W, Brigande JV, Fekete DM, Wu DK (2004) The development of semicircular canals in the inner ear: role of FGFs in sensory cristae. Development 131: 4201-4211.
68. Fritzsch B, Pauley S, Beisel KW (2006) Cells, molecules and morphogenesis: the making of the vertebrate ear. Brain Res 1091: 151-171.
69. Chen P, Segil N (1999) p27(Kip1) links cell proliferation to morphogenesis in the developing organ of Corti. Development 126: 1581-1590.
70. Farinas I, Jones KR, Tessarollo L, Vigers AJ, Huang E, et al. (2001) Spatial shaping of cochlear innervation by temporally regulated neurotrophin expression. J Neurosci 21: 6170-6180.
71. Fritzsch B, Tessarollo L, Coppola E, Reichardt LF (2004) Neurotrophins in the ear: their roles in sensory neuron survival and fiber guidance. Prog Brain Res 146: 265-278.
72. Hidalgo A, Griffiths R (2004) Coupling glial numbers and axonal patterns. Cell Cycle 3: 1118-1120.
73. 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.
74. Pirvola U, Ylikoski J, Trokovic R, Hebert J, McConnell S, et al. (2002) FGFR1 Is Required for the Development of the Auditory Sensory Epithelium. Neuron 35: 671.
75. Pirvola U, Spencer-Dene B, Xing-Qun L, Kettunen P, Thesleff I, et al. (2000) FGF/FGFR-2(IIIb) signaling is essential for inner ear morphogenesis. J Neurosci 20: 6125-6134.
76. Shim K, Minowada G, Coling DE, Martin GR (2005) Sprouty2, a mouse deafness gene, regulates cell fate decisions in the auditory sensory epithelium by antagonizing FGF signaling. Dev Cell 8: 553-564.
77. Hayashi T, Cunningham D, Bermingham-McDonogh O (2007) Loss of Fgfr3 leads to excess hair cell development in the mouse organ of Corti. Dev Dyn 236: 525-533.