Characterization of new otic enhancers of the pou3f4 gene reveal distinct signaling pathway regulation and spatio-temporal patterns

PLoS ONE

Volumn 5, Issue 12, 2010, Pages

  Robert Moreno, Àlex ^a   Naranjo, Silvia ^b   de la Calle Mustienes, Elisa ^b   Gómez Skarmeta, José Luis ^b   Alsina, Berta ^a  

^a Barcelona Biomedical Research Park   (Spain)

^b UNIVERSIDAD PABLO DE OLAVIDE   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

FIBROBLAST GROWTH FACTOR; RETINOIC ACID; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR PAX2; TRANSCRIPTION FACTOR POU; TRANSCRIPTION FACTOR POU3F4; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; GREEN FLUORESCENT PROTEIN; POU3F4 PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ANIMAL TISSUE; ARTICLE; BINDING SITE; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; ENHANCER REGION; EPITHELIUM CELL; GENE ACTIVATION; GENE EXPRESSION; GENE IDENTIFICATION; GENE LOCUS; GENE SWITCHING; GENETIC REGULATION; INNER EAR; MESENCHYME CELL; NONHUMAN; ORGANOGENESIS; REGULATORY SEQUENCE; SIGNAL TRANSDUCTION; ZEBRA FISH; ANIMAL; BIOLOGICAL MODEL; EAR; GENE DELETION; GENETICS; HUMAN; METABOLISM; MOUSE; MUTATION; PRENATAL DEVELOPMENT; TIME; XENOPUS;

DANIO RERIO;

ANIMALS; BINDING SITES; EAR; ENHANCER ELEMENTS, GENETIC; GENE DELETION; GREEN FLUORESCENT PROTEINS; HUMANS; MICE; MODELS, GENETIC; MUTATION; POU DOMAIN FACTORS; TIME FACTORS; TRANSCRIPTION FACTORS; XENOPUS; ZEBRAFISH;

EID: 79251510881     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0015907     Document Type: Article

References (58)

1. Kelley MW (2006) Regulation of cell fate in the sensory epithelia of the inner ear. Nat Rev Neurosci 7(11): 837-849.
2. Torres M, Giraldez F (1998) The development of the vertebrate inner ear. Mech Dev 71(1-2): 5-21.
3. Bejerano G, Pheasant M, Makunin I, Stephen S, Kent WJ, et al. (2004) Ultraconserved elements in the human genome. Science 304(5675): 1321-1325.
4. Sandelin A, Bailey P, Bruce S, Engstrom PG, Klos JM, et al. (2004) Arrays of ultraconserved non-coding regions span the loci of key developmental genes in vertebrate genomes. BMC Genomics 5(1): 99.
5. Gomez-Skarmeta JL, Lenhard B, Becker TS (2006) New technologies, new findings, and new concepts in the study of vertebrate cis-regulatory sequences. Dev Dyn 235(4): 870-885.
6. Visel A, Bristow J, Pennacchio LA (2007) Enhancer identification through comparative genomics. Semin Cell Dev Biol 18(1): 140-152.
7. Navratilova P, Becker TS (2009) Genomic regulatory blocks in vertebrates and implications in human disease. Brief Funct Genomic Proteomic 8(4): 333-342.
8. Brown KK, Reiss JA, Crow K, Ferguson HL, Kelly C, et al. (2010) Deletion of an enhancer near DLX5 and DLX6 in a family with hearing loss, craniofacial defects, and an inv(7)(q21.3q35). Hum Genet 127(1): 19-31.
9. Vahava O, Morell R, Lynch ED, Weiss S, Kagan ME, et al. (1998) Mutation in transcription factor POU4F3 associated with inherited progressive hearing loss in humans. Science 279(5358): 1950-1954.
10. de Kok YJ, van der Maarel SM, Bitner-Glindzicz M, Huber I, Monaco AP, et al. (1995) Association between X-linked mixed deafness and mutations in the POU domain gene POU3F4. Science 267(5198): 685-688.
11. Le Moine C, Young WS, 3rd (1992) RHS2, a POU domain-containing gene, and its expression in developing and adult rat. Proc Natl Acad Sci U S A 89(8): 3285-3289.
12. Phippard D, Boyd Y, Reed V, Fisher G, Masson WK, et al. (2000) The sexlinked fidget mutation abolishes Brn4/Pou3f4 gene expression in the embryonic inner ear. Hum Mol Genet 9(1): 79-85.
13. Phippard D, Lu L, Lee D, Saunders JC, Crenshaw EB, 3rd (1999) Targeted mutagenesis of the POU-domain gene Brn4/Pou3f4 causes developmental defects in the inner ear. J Neurosci 19(14): 5980-5989.
14. Bitner-Glindzicz M, Turnpenny P, Hoglund P, Kaariainen H, Sankila EM, et al. (1995) Further mutations in brain 4 (POU3F4) clarify the phenotype in the Xlinked deafness, DFN3. Hum Mol Genet 4(8): 1467-1469.
15. de Kok YJ, Merkx GF, van der Maarel SM, Huber I, Malcolm S, et al. (1995) A duplication/paracentric inversion associated with familial X-linked deafness (DFN3) suggests the presence of a regulatory element more than 400 kb upstream of the POU3F4 gene. Hum Mol Genet 4(11): 2145-2150.
16. de Kok YJ, Vossenaar ER, Cremers CW, Dahl N, Laporte J, et al. (1996) Identification of a hot spot for microdeletions in patients with X-linked deafness type 3 (DFN3) 900 kb proximal to the DFN3 gene POU3F4. Hum Mol Genet 5(9): 1229-1235.
17. Ahn KJ, Passero F, Jr., Crenshaw EB, 3rd (2009) Otic mesenchyme expression of cre recombinase directed by the inner ear enhancer of the Brn4/Pou3f4 gene. Genesis 47(3): 137-141.
18. Naranjo S, Voesenek K, de la Calle-Mustienes E, Robert-Moreno A, Kokotas H, et al. (2010) Multiple enhancers located in a 1-mb region upstream of POU3F4 promote expression during inner ear development and may be required for hearing. Hum Genet 128(4): 411-9.
19. Cremers FP, Cremers CW, Ropers HH (2000) The ins and outs of X-linked deafness type 3. Adv Otorhinolaryngol 56: 184-195.
20. Thisse B, Heyer V, Lux A, Alunni V, Degrave A, et al. (2004) Spatial and temporal expression of the zebrafish genome by large-scale in situ hybridization screening. Methods Cell Biol 77: 505-519.
21. Bessa J, Tena JJ, de la Calle-Mustienes E, Fernandez-Minan A, Naranjo S, et al. (2009) Zebrafish enhancer detection (ZED) vector: A new tool to facilitate transgenesis and the functional analysis of cis-regulatory regions in zebrafish. Dev Dyn 238(9): 2409-2417.
22. Aguilera C, Hoya-Arias R, Haegeman G, Espinosa L, Bigas A (2004) Recruitment of IkappaBalpha to the hes1 promoter is associated with transcriptional repression. Proc Natl Acad Sci U S A 101(47): 16537-16542.
23. Hans S, Westerfield M (2007) Changes in retinoic acid signaling alter otic patterning. Development 134(13): 2449-2458.
24. Liu W, Oh SH, Kang Yk Y, Li G, Doan TM, et al. (2003) Bone morphogenetic protein 4 (BMP4): A regulator of capsule chondrogenesis in the developing mouse inner ear. Dev Dyn 226(3): 427-438.
25. Chang W, ten Dijke P, Wu DK (2002) BMP pathways are involved in otic capsule formation and epithelial-mesenchymal signaling in the developing chicken inner ear. Dev Biol 251(2): 380-394.
26. Phillips BT, Bolding K, Riley BB (2001) Zebrafish fgf3 and fgf8 encode redundant functions required for otic placode induction. Dev Biol 235(2): 351-365.
27. Phillips BT, Storch EM, Lekven AC, Riley BB (2004) A direct role for fgf but not wnt in otic placode induction. Development 131(4): 923-931.
28. Leger S, Brand M (2002) Fgf8 and Fgf3 are required for zebrafish ear placode induction, maintenance and inner ear patterning. Mech Dev 119(1): 91-108.
29. Maroon H, Walshe J, Mahmood R, Kiefer P, Dickson C, Mason I (2002) Fgf3 and Fgf8 are required together for formation of the otic placode and vesicle. Development 129: 2099-2108.
30. Braunstein EM, Crenshaw EB, 3rd, Morrow BE, Adams JC (2008) Cooperative function of Tbx1 and Brn4 in the periotic mesenchyme is necessary for cochlea formation. J Assoc Res Otolaryngol 9(1): 33-43.
31. Yamagishi H, Maeda J, Hu T, McAnally J, Conway SJ, et al. (2003) Tbx1 is regulated by tissue-specific forkhead proteins through a common sonic hedgehog-responsive enhancer. Genes Dev 17(2): 269-281.
32. Petit C (1996) Genes responsible for human hereditary deafness: Symphony of a thousand. Nat Genet 14(4): 385-391.
33. Dror AA, Avraham KB (2009) Hearing loss: Mechanisms revealed by genetics and cell biology. Annu Rev Genet 43: 411-437.
34. Spitz F, Gonzalez F, Peichel C, Vogt TF, Duboule D, et al. (2001) Large scale transgenic and cluster deletion analysis of the HoxD complex separate an ancestral regulatory module from evolutionary innovations. Genes Dev 15(17): 2209-2214.
35. de la Calle-Mustienes E, Feijoo CG, Manzanares M, Tena JJ, Rodriguez- Seguel E, et al. (2005) A functional survey of the enhancer activity of conserved non-coding sequences from vertebrate iroquois cluster gene deserts. Genome Res 15(8): 1061-1072.
36. Vendrell V, Carnicero E, Giraldez F, Alonso MT, Schimmang T (2000) Induction of inner ear fate by FGF3. Development 127(10): 2011-2019.
37. Ladher RK, Anakwe KU, Gurney AL, Schoenwolf GC, Francis-West PH (2000) Identification of synergistic signals initiating inner ear development. Science 290(5498): 1965-1967.
38. Wright TJ, Mansour SL (2003) Fgf3 and Fgf10 are required for mouse otic placode induction. Development 130(15): 3379-3390.
39. Alvarez Y, Alonso MT, Vendrell V, Zelarayan LC, Chamero P, et al. (2003) Requirements for FGF3 and FGF10 during inner ear formation. Development 130(25): 6329-6338.
40. 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(2): 203-215.
41. Alsina B, Abello G, Ulloa E, Henrique D, Pujades C, et al. (2004) FGF signaling is required for determination of otic neuroblasts in the chick embryo. Dev Biol 267(1): 119-134.
42. Abello G, Khatri S, Radosevic M, Scotting PJ, Giraldez F, et al. (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(1): 166-178.
43. 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(16): 6125-6134.
44. Begemann G, Schilling TF, Rauch GJ, Geisler R, Ingham PW (2001) The zebrafish neckless mutation reveals a requirement for raldh2 in mesodermal signals that pattern the hindbrain. Development 16: 3081-3094.
45. Dupe V, Ghyselinck NB, Wendling O, Chambon P, Mark M (1999) Key roles of retinoic acid receptors alpha and beta in the patterning of the caudal hindbrain, pharyngeal arches and otocyst in the mouse. Development 22: 5051-5059.
46. Gale E, Zile M, Maden M (1999) Hindbrain respecification in the retinoiddeficient quail. Mech. Dev;1-2): 43-54.
47. Lefebvre PP, Malgrange B, Staecker H, Moonen G, Van de Water TR (1993) Retinoic acid stimulates regeneration of mammalian auditory hair cells. Science 260(5108): 692-695.
48. Raz Y, Kelley MW (1997) Effects of retinoid and thyroid receptors during development of the inner ear. Semin Cell Dev Biol 8(3): 257-264.
49. Daudet N, Lewis J (2005) Two contrasting roles for notch activity in chick inner ear development: Specification of prosensory patches and lateral inhibition of hair-cell differentiation. Development 132(3): 541-551.
50. Daudet N, Ariza-McNaughton L, Lewis J (2007) Notch signalling is needed to maintain, but not to initiate, the formation of prosensory patches in the chick inner ear. Development 134(12): 2369-2378.
51. Cole LK, Le Roux I, Nunes F, Laufer E, Lewis J, et al. (2000) Sensory organ generation in the chicken inner ear: Contributions of bone morphogenetic protein 4, serrate1, and lunatic fringe. J Comp Neurol 424(3): 509-520.
52. Pujades C, Kamaid A, Alsina B, Giraldez F (2006) BMP-signaling regulates the generation of hair-cells. Dev Biol 292(1): 55-67.
53. Riccomagno MM, Martinu L, Mulheisen M, Wu DK, Epstein DJ (2002) Specification of the mammalian cochlea is dependent on sonic hedgehog. Genes Dev 16(18): 2365-2378.
54. Arnold JS, Braunstein EM, Ohyama T, Groves AK, Adams JC, et al. (2006) Tissue-specific roles of Tbx1 in the development of the outer, middle and inner ear, defective in 22q11DS patients. Hum Mol Genet 15(10): 1629-1639.
55. Inoue M, Kamachi Y, Matsunami H, Imada K, Uchikawa M, et al. (2007) PAX6 and SOX2-dependent regulation of the Sox2 enhancer N-3 involved in embryonic visual system development. Genes Cells 12(9): 1049-1061.
56. Conte I, Bovolenta P (2007) Comprehensive characterization of the cisregulatory code responsible for the spatio-temporal expression of olSix3.2 in the developing medaka forebrain. Genome Biol 8(7): R137.
57. Guerrero L, Marco-Ferreres R, Serrano AL, Arredondo JJ, Cervera M (2010) Secondary enhancers synergise with primary enhancers to guarantee fine-tuned muscle gene expression. Dev Biol 337(1): 16-28.
58. Papatsenko D, Goltsev Y, Levine M (2009) Organization of developmental enhancers in the drosophila embryo. Nucleic Acids Res 37(17): 5665-5677.