RFX transcription factors are essential for hearing in mice

Nature Communications

Volumn 6, Issue , 2015, Pages

  Elkon, Ran ^a   Milon, Beatrice ^b   Morrison, Laura ^b   Shah, Manan ^b   Vijayakumar, Sarath ^c   Racherla, Manoj ^b   Leitch, Carmen C ^b   Silipino, Lorna ^b   Hadi, Shadan ^d   Weiss Gayet, Michèle ^e   Barras, Emmanuèle ^f   Schmid, Christoph D ^g   Ait Lounis, Aouatef ^f,i   Barnes, Ashley ^b   Song, Yang ^b   Eisenman, David J ^b   Eliyahu, Efrat ^h   Frolenkov, Gregory I ^d   Strome, Scott E ^b   Durand, Bénédicte ^e   Zaghloul, Norann A ^b   Jones, Sherri M ^c   Reith, Walter ^f   Hertzano, Ronna ^b   more..

^a TEL AVIV UNIVERSITY   (Israel)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^d UNIVERSITY OF KENTUCKY   (United States)

^e UNIVERSITÉ LYON 1   (France)

^f UNIVERSITY OF GENEVA MEDICAL SCHOOL   (Switzerland)

^g UNIVERSITY OF BASEL   (Switzerland)

^h MOUNT SINAI SCHOOL OF MEDICINE   (United States)

ⁱ UNIVERSITY OF SCIENCES AND TECHNOLOGY HOUARI BOUMEDIENE   (Algeria)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS AND CELL COMPONENTS; DISABILITY; EMBRYONIC DEVELOPMENT; GENOMICS; HEARING; MAMMAL; MOLECULAR ANALYSIS; REGENERATION; RODENT;

MAMMALIA; MUS;

DNA BINDING PROTEIN; REGULATORY FACTOR X TRANSCRIPTION FACTOR; REGULATORY FACTOR X1; RFX1 PROTEIN, HUMAN; RFX1 PROTEIN, MOUSE; TRANSCRIPTION FACTOR; TRANSCRIPTOME;

ANIMAL; C57BL MOUSE; CHROMATIN IMMUNOPRECIPITATION; COCHLEAR HAIR CELL; COMPARATIVE STUDY; DNA SEQUENCE; EVOLUTION; FEMALE; GENE EXPRESSION REGULATION; HEARING; INSTITUTE FOR CANCER RESEARCH MOUSE; KNOCKOUT MOUSE; MALE; METABOLISM; MULTIGENE FAMILY; NEWBORN; PHYSIOLOGY; ULTRASTRUCTURE; ZEBRA FISH;

ANIMALS; ANIMALS, NEWBORN; BIOLOGICAL EVOLUTION; CHROMATIN IMMUNOPRECIPITATION; DNA-BINDING PROTEINS; FEMALE; GENE EXPRESSION REGULATION; HAIR CELLS, AUDITORY; HEARING; MALE; MICE, INBRED C57BL; MICE, INBRED ICR; MICE, KNOCKOUT; MULTIGENE FAMILY; REGULATORY FACTOR X TRANSCRIPTION FACTORS; REGULATORY FACTOR X1; SEQUENCE ANALYSIS, DNA; TRANSCRIPTION FACTORS; TRANSCRIPTOME; ZEBRAFISH;

EID: 84944340041     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms9549     Document Type: Article

References (70)

1. Morton, N. E. Genetic epidemiology of hearing impairment. Ann. NY Acad. Sci. 630, 16-31 (1991).
2. Yamasoba, T. et al. Current concepts in age-related hearing loss: epidemiology and mechanistic pathways. Hear. Res. 303, 30-38 (2013).
3. Schwander, M., Kachar, B. & Muller, U. Review series: the cell biology of hearing. J. Cell Biol. 190, 9-20 (2010).
4. Ruben, R. J. Development of the inner ear of the mouse: a radioautographic study of terminal mitoses. Acta Otolaryngol. 220(Suppl): 1-44 (1967).
5. Bermingham, N. A. et al. Math1: an essential gene for the generation of inner ear hair cells. Science 284, 1837-1841 (1999).
6. Hertzano, R. et al. Transcription profiling of inner ears from Pou4f3(ddl/ddl) identifies Gfi1 as a target of the Pou4f3 deafness gene. Hum. Mol. Genet. 13, 2143-2153 (2004).
7. Wallis, D. et al. The zinc finger transcription factor Gfi1, implicated in lymphomagenesis, is required for inner ear hair cell differentiation and survival. Development 130, 221-232 (2003).
8. Erkman, L. et al. Role of transcription factors Brn-3.1 and Brn-3.2 in auditory and visual system development. Nature 381, 603-606 (1996).
9. Costa, A. et al. Generation of sensory hair cells by genetic programming with a combination of transcription factors. Development 142, 1948-1959 (2015).
10. Hertzano, R. et al. Cell type-specific transcriptome analysis reveals a major role for Zeb1 and miR-200b in mouse inner ear morphogenesis. PLoS Genet. 7, e1002309 (2011).
11. Thiede, B. R. et al. Retinoic acid signalling regulates the development of tonotopically patterned hair cells in the chicken cochlea. Nat. Commun. 5, 3840 (2014).
12. Ku, Y. C. et al. The transcriptome of utricle hair cell regeneration in the avian inner ear. J. Neurosci. 34, 3523-3535 (2014).
13. Kwan, K. Y., Shen, J. & Corey, D. P. C-MYC transcriptionally amplifies SOX2 target genes to regulate self-renewal in multipotent otic progenitor cells. Stem Cell Rep. 4, 47-60 (2015).
14. Hertzano, R. & Elkon, R. High throughput gene expression analysis of the inner ear. Hear. Res. 288, 77-88 (2012).
15. Liu, H. et al. Characterization of transcriptomes of cochlear inner and outer hair cells. J. Neurosci. 34, 11085-11095 (2014).
16. Durruthy-Durruthy, R. et al. Reconstruction of the mouse otocyst and early neuroblast lineage at single-cell resolution. Cell 157, 964-978 (2014).
17. El Zein, L. et al. RFX3 governs growth and beating efficiency of motile cilia in mouse and controls the expression of genes involved in human ciliopathies. J. Cell Sci. 122, 3180-3189 (2009).
18. Chen, P., Johnson, J. E., Zoghbi, H. Y. & Segil, N. The role of Math1 in inner ear development: Uncoupling the establishment of the sensory primordium from hair cell fate determination. Development 129, 2495-2505 (2002).
19. Belyantseva, I. A., Adler, H. J., Curi, R., Frolenkov, G. I. & Kachar, B. Expression and localization of prestin and the sugar transporter GLUT-5 during development of electromotility in cochlear outer hair cells. J. Neurosci. 20, RC116 (2000).
20. Simmons, D. D., Tong, B., Schrader, A. D. & Hornak, A. J. Oncomodulin identifies different hair cell types in the mammalian inner ear. J. Comp. Neurol. 518, 3785-3802 (2010).
21. Elkon, R., Linhart, C., Sharan, R., Shamir, R. & Shiloh, Y. Genome-wide in silico identification of transcriptional regulators controlling the cell cycle in human cells. Genome Res. 13, 773-780 (2003).
22. Elkon, R. et al. Dissection of a DNA-damage-induced transcriptional network using a combination of microarrays, RNA interference and computational promoter analysis. Genome Biol. 6, R43 (2005).
23. Ahmed, Z. M. et al. Mutations of LRTOMT, a fusion gene with alternative reading frames, cause nonsyndromic deafness in humans. Nat. Genet. 40, 1335-1340 (2008).
24. Jones, C. et al. Ciliary proteins link basal body polarization to planar cell polarity regulation. Nat. Genet. 40, 69-77 (2008).
25. Cui, C. et al. Wdpcp, a PCP protein required for ciliogenesis, regulates directional cell migration and cell polarity by direct modulation of the actin cytoskeleton. PLoS Biol. 11, e1001720 (2013).
26. Naz, S. et al. Mutations in a novel gene, TMIE, are associated with hearing loss linked to the DFNB6 locus. Am. J. Hum. Genet. 71, 632-636 (2002).
27. Mitchem, K. L. et al. Mutation of the novel gene Tmie results in sensory cell defects in the inner ear of spinner, a mouse model of human hearing loss DFNB6. Hum. Mol. Genet. 11, 1887-1898 (2002).
28. Ahmed, Z. M., Riazuddin, S., Riazuddin, S. & Wilcox, E. R. The molecular genetics of Usher syndrome. Clin. Genet. 63, 431-444 (2003).
29. Thomas, J. et al. Transcriptional control of genes involved in ciliogenesis: a first step in making cilia. Biol. Cell 102, 499-513 (2010).
30. Cai, T. et al. Characterization of the transcriptome of nascent hair cells and identification of direct targets of the Atoh1 transcription factor. J. Neurosci. 35, 5870-5883 (2015).
31. Scheffer, D. I., Shen, J., Corey, D. P. & Chen, Z. Y. Gene expression by mouse inner ear hair cells during development. J. Neurosci. 35, 6366-6380 (2015).
32. Ait-Lounis, A. et al. The transcription factor Rfx3 regulates beta-cell differentiation, function, and glucokinase expression. Diabetes 59, 1674-1685 (2010).
33. McDermott, Jr. B. M. et al. Transgenic labeling of hair cells in the zebrafish acousticolateralis system. Gene Expr. Patterns 10, 113-118 (2010).
34. Steiner, A. B., Kim, T., Cabot, V. & Hudspeth, A. J. Dynamic gene expression by putative hair-cell progenitors during regeneration in the zebrafish lateral line. Proc. Natl Acad. Sci. USA 111, E1393-E1401 (2014).
35. Choksi, S. P., Lauter, G., Swoboda, P. & Roy, S. Switching on cilia: transcriptional networks regulating ciliogenesis. Development 141, 1427-1441 (2014).
36. Emery, P., Durand, B., Mach, B. & Reith, W. RFX proteins, a novel family of DNA binding proteins conserved in the eukaryotic kingdom. Nucleic Acids Res. 24, 803-807 (1996).
37. Reith, W. et al. RFX1, a transactivator of hepatitis B virus enhancer I, belongs to a novel family of homodimeric and heterodimeric DNA-binding proteins. Mol. Cell. Biol. 14, 1230-1244 (1994).
38. Axelrod, J. D. Basal bodies, kinocilia and planar cell polarity. Nat. Genet. 40, 10-11 (2008).
39. Gale, J. E., Marcotti, W., Kennedy, H. J., Kros, C. J. & Richardson, G. P. FM1-43 dye behaves as a permeant blocker of the hair-cell mechanotransducer channel. J. Neurosci. 21, 7013-7025 (2001).
40. Burns, J. C., Kelly, M. C., Hoa, M., Morell, R. J. & Kelley, M. W. Single-cell RNA-Seq resolves cellular complexity in sensory organs from the neonatal inner ear. Nat. Commun. 6, 8557 doi: 10.1038/ncomms9557 (2015).
41. Li, S. et al. Hearing loss caused by progressive degeneration of cochlear hair cells in mice deficient for the Barhl1 homeobox gene. Development 129, 3523-3532 (2002).
42. Hertzano, R. et al. Transcription profiling of inner ears from Pou4f3(ddl/ddl) identifies Gfi1 as a target of the Pou4f3 deafness gene. Hum. Mol. Genet. 13, 2143-2153 (2004).
43. Sadanaga, M. & Morimitsu, T. Development of endocochlear potential and its negative component in mouse cochlea. Hear. Res. 89, 155-161 (1995).
44. Beurg, M., Nam, J. H., Chen, Q. & Fettiplace, R. Calcium balance and mechanotransduction in rat cochlear hair cells. J. Neurophysiol. 104, 18-34 (2010).
45. Van Campen, L. E., Murphy, W. J., Franks, J. R., Mathias, P. I. & Toraason, M. A. Oxidative DNA damage is associated with intense noise exposure in the rat. Hear. Res. 164, 29-38 (2002).
46. Min, K. et al. Transcription factor RFX1 is crucial for maintenance of genome integrity in Fusarium graminearum. Eukaryot. Cell 13, 427-436 (2014).
47. Zhang, Y., Yuan, F., Wang, D., Gu, L. & Li, G. M. Identification of regulatory factor X as a novel mismatch repair stimulatory factor. J. Biol. Chem. 283, 12730-12735 (2008).
48. Xiang, M. et al. Essential role of POU-domain factor Brn-3c in auditory and vestibular hair cell development. Proc. Natl Acad. Sci. USA 94, 9445-9450 (1997).
49. Newton, F. G. et al. Forkhead transcription factor Fd3F cooperates with Rfx to regulate a gene expression program for mechanosensory cilia specialization. Dev. Cell 22, 1221-1233 (2012).
50. Cachero, S. et al. The gene regulatory cascade linking proneural specification with differentiation in Drosophila sensory neurons. PLoS Biol. 9, e1000568 (2011).
51. Lumpkin, E. A. et al. Math1-driven GFP expression in the developing nervous system of transgenic mice. Gene Expr. Patterns 3, 389-395 (2003).
52. Westerfield, M. The Zebrafish Book: A Guide for the Laboratory Use of Zebrafish (Danio rerio) (Univ. of Oregon Press, 2000).
53. Bonnafe, E. et al. The transcription factor RFX3 directs nodal cilium development and left-right asymmetry specification. Mol. Cell. Biol. 24, 4417-4427 (2004).
54. Yang, H. et al. Gfi1-Cre knock-in mouse line: A tool for inner ear hair cellspecific gene deletion. Genesis 48, 400-406 (2010).
55. Matei, V. et al. Smaller inner ear sensory epithelia in Neurog 1 null mice are related to earlier hair cell cycle exit. Dev. Dyn. 234, 633-650 (2005).
56. Gallardo, V. E. & Behra, M. Fluorescent activated cell sorting (FACS) combined with gene expression microarrays for transcription enrichment profiling of zebrafish lateral line cells. Methods 62, 226-231 (2013).
57. Ulitsky, I. et al. Expander: from expression microarrays to networks and functions. Nat. Protoc. 5, 303-322 (2010).
58. Trapnell, C., Pachter, L. & Salzberg, S. L. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 25, 1105-1111 (2009).
59. Anders, S., Pyl, P. T. & Huber, W. HTSeq - a Python framework to work with high-throughput sequencing data. Bioinformatics 31, 166-169 (2014).
60. Flicek, P. et al. Ensembl 2014. Nucleic Acids Res. 42, D749-D755 (2014).
61. Huang da, W., Sherman, B. T. & Lempicki, R. A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57 (2009).
62. Linhart, C., Halperin, Y. & Shamir, R. Transcription factor and microRNA motif discovery: the Amadeus platform and a compendium of metazoan target sets. Genome Res. 18, 1180-1189 (2008).
63. Smith, R. J. & Van Camp, G. Hereditary Hearing Loss Homepage. http://hereditaryhearingloss.org.
64. Sayers, E. W. et al. Database resources of the National Center for Biotechnology Information. Nucleic Acids Res. 38, D5-16 (2010).
65. Masternak, K., Peyraud, N., Krawczyk, M., Barras, E. & Reith, W. Chromatin remodeling and extragenic transcription at the MHC class II locus control region. Nat. Immunol. 4, 132-137 (2003).
66. Jimenez, A. M., Stagner, B. B., Martin, G. K. & Lonsbury-Martin, B. L. Agerelated loss of distortion product otoacoustic emissions in four mouse strains. Hear. Res. 138, 91-105 (1999).
67. Guimaraes, P., Zhu, X., Cannon, T., Kim, S. & Frisina, R. D. Sex differences in distortion product otoacoustic emissions as a function of age in CBA mice. Hear. Res. 192, 83-89 (2004).
68. Mock, B., Jones, T. A. & Jones, S. M. Gravity receptor aging in the CBA/CaJ strain: a comparison to auditory aging. J. Assoc. Res. Otolaryngol. 12, 173-183 (2011).
69. Martin, G. K. et al. Comparison of distortion product otoacoustic emissions in 28 inbred strains of mice. Hear. Res. 234, 59-72 (2007).
70. Matys, V. et al. TRANSFAC and its module TRANSCompel: transcriptional gene regulation in eukaryotes. Nucleic Acids Res. 34, D108-D110 (2006).