Using Xenopus to discover new genes involved in branchiootorenal spectrum disorders

Comparative Biochemistry and Physiology Part - C: Toxicology and Pharmacology

Volumn 178, Issue , 2015, Pages 16-24

  Moody, Sally A ^a   Neilson, Karen M ^a   Kenyon, Kristy L ^b   Alfandari, Dominique ^c   Pignoni, Francesca ^d  

^a GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^b HOBART AND WILLIAM SMITH COLLEGES   (United States)

^c UNIVERSITY OF MASSACHUSETTS   (United States)

^d SUNY UPSTATE MEDICAL UNIVERSITY   (United States)

Author keywords

2G4 Eb1; Branchiootorenal; Eya1; Mcsr1; Six1; Sobp; Xenopus; Zmym2

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR EYA1; TRANSCRIPTION FACTOR SIX1; UNCLASSIFIED DRUG;

BRANCHIOOTORENAL SYNDROME; GENE EXPRESSION; GENETIC SCREENING; HUMAN; KIDNEY DEVELOPMENT; MULTIGENE FAMILY; NONHUMAN; PRIORITY JOURNAL; PROTEIN TARGETING; REVIEW; XENOPUS LAEVIS; ANIMAL; EMBRYOLOGY; GENETIC TRANSCRIPTION; GENETICS; KIDNEY; PHYSIOLOGY; XENOPUS;

ANIMALS; BRANCHIO-OTO-RENAL SYNDROME; HUMANS; KIDNEY; TRANSCRIPTION, GENETIC; XENOPUS;

EID: 84948099018     PISSN: 15320456     EISSN: 18781659     Source Type: Journal    
DOI: 10.1016/j.cbpc.2015.06.007     Document Type: Review

References (136)

1. D.S. Andersen, S.J. Raja, J. Colombani, R.L. Shaw, P.F. Langton, A. Akhtar, and N. Tapon Drosophila MCRS2 associates with RNA polymerase II complexes to regulate transcription Mol. Cell. Biol. 47 2010 4744 4755
2. A. Anderson, B.P. Weasner, B.M. Weasner, and J.P. Kumar The Drosophila Wilm's tumor1-associating protein (WTAP) homolog is required for eye development Dev. Biol. 390 2014 170 180
3. A.P. Bailey, S. Bhattacharyya, M. Bronner-Fraser, and A. Streit Lens specification is the ground state of all sensory placodes, from which FGF promotes olfactory identity Dev. Cell 11 2006 505 517
4. B. Bajoghli, N. Aghaallaei, and T. Czerby Groucho corepressor proteins regulate otic vesicle outgrowth Dev. Dyn. 233 2005 760 771
5. B.C. Bane, J.M. Van Rybroek, S.J. Kolker, D.L. Weeks, and J.M. Manaligod EYA1 expression in the developing inner ear Ann. Otol. Rhinol. Laryngol. 114 2005 853 858
6. S. Bhattacharyya, and M. Bronner-Fraser Hierarchy of regulatory events in sensory placode development Curr. Opin. Genet. Dev. 14 2004 520 526
7. Y. Bidet, T. Jagla, J.P. Da Ponte, B. Dastugue, and K. Jagla Modifiers of muscle and heart cell fate specification identified by gain-of-function screen in Drosophila Mech. Dev. 120 2003 991 1007
8. E. Birk, A. Har-Zahav, C.M. Manzini, M. Pasmanik-Chor, L. Kornreich, C.A. Walsh, K. Noben-Trauth, A. Albin, A.J. Simon, L. Colleaux, Y. Morad, L. Rainshtein, D.J. Tischfield, P. Wang, N. Magai, N. Shoshani, G. Rechavi, D. Gothelf, G. Maydan, M. Shohat, and L. Basel-Vanagaite SOBP is mutated in syndromic and non-syndromic intellectual disability and is highly expressed in the brain limbic system Am. J. Hum. Genet. 87 2010 694 700
9. J. Blanco, T. Pauli, M. Seimiya, G. Udolph, and W.J. Gehring Genetic interactions of eyes absent, twin of eyeless and orthodenticle regulate sine oculis expression during ocellar development in Drosophila Dev. Biol. 344 2010 1088 1099
10. E. Blanco, M. Ruiz-Romero, S. Beltran, M. Bosch, A. Punset, F. Serras, and M. Corominas Gene expression following induction of regeneration in Drosophila wing imaginal discs. Expression profile of regenerating wing discs BMC Dev. Biol. 10 2010 94
11. I.L. Blitz, J. Biesinger, X. Xie, and K.W.Y. Cho Biallelic genome modification in F0 Xenopus tropicalis embryos using the CRISPR/Cas system Genesis 51 2013 827 834
12. E.A. Bosman, E. Quint, E. Fuchs, M. Hrabe de Angelis, and K.P. Steel Catweasel mice: a novel role for Six1 in sensory patch development and a model for branchio-otic-renal syndrome Dev. Biol. 328 2009 285 296
13. O. Bricaud, and A. Collazo The transcription factor six1 inhibits neuronal and promotes hair cell fates in the developing zebrafish (Danio rerio) inner ear J. Neurosci. 26 2006 10438 10451
14. O. Bricaud, and A. Collazo Balancing cell numbers during organogenesis: Six1a differentially affects neurons and sensory hair cells in the inner ear Dev. Biol. 357 2011 191 201
15. S. Brodbeck, and C. Englert Genetic determination of nephrogenesis: the Pax/Eya/Six gene network Pediatr. Nephrol. 19 2004 249 255
16. S.A. Brugmann, and S.A. Moody Induction and specification of the vertebrate ectodermal placodes: precursors of the cranial sensory organs Biol. Cell. 97 2005 303 319
17. S.A. Brugmann, P.D. Pandur, K.L. Kenyon, F. Pignoni, and S.A. Moody Six1 promotes a placodal fate within the lateral neurogenic ectoderm by functioning as both a transcriptional activator and repressor Development 131 2004 5871 5881
18. E.H. Chang, M. Menezes, N.C. Meyer, R.A. Cucci, V.S. Vervoort, C.E. Schwartz, and R.J. Smith Branchio-oto-renal syndrome: the mutation spectrum in EYA1 and its phenotypic consequences Hum. Mutat. 23 2004 582 589
19. Z. Chen, M. Montcouquioi, R. Calderon, N.A. Jenkins, N.G. Copeland, M.W. Kelley, and K. Noben-Trauth Jac1/Sobp, encoding a nuclear zinc finger protein, is critical for cochlear growth, cell fate and patterning of the organ of Corti J. Neurosci. 28 2008 6633 6641
20. B. Chen, E.H. Kim, and P.X. Xu Initiation of olfactory placode development and neurogenesis is blocked in mice lacking both Six1 and Six4 Dev. Biol. 326 2009 75 85
21. B.N. Cheyette, P.J. Green, K. Martin, H. Garren, V. Hartenstein, and S.L. Zipursky The Drosophila sine oculis locus encodes a homeodomain-containing protein required for the development of the entire visual system Neuron 12 1994 977 996
22. N.A. Christophorou, A.P. Bailey, S. Hanson, and A. Streit Activation of Six1 target genes is required for sensory placode formation Dev. Biol. 336 2009 327 336
23. L. Davidovic, E. Bechara, M. Gravel, X.H. Jaglin, S. Tremblay, A. Sik, B. Bardoni, and R.W. Khandjian The nuclear Microspherule protein 58 is a novel RNA-binding protein that interacts with fragile X mental retardation protein in polyribosomal mRNPs from neurons Hum. Mol. Genet. 15 2006 1525 1538
24. C.D. Duggan, S. DeMaria, A. Baudhuin, D. Stafford, and J. Ngai Foxg1 is required for development of the vertebrate olfactory system J. Neurosci. 28 2008 5229 5239
25. A. Elepfandt, I. Eistetter, A. Flelig, E. Gunther, M. Hainich, S. Hepperle, and B. Traub Hearing threshold and frequency discrimination in the purely aquatic frog Xenopus laevis (Pipidae): measurement by means of conditioning J. Exp. Biol. 203 2000 3621 3629
26. N. Figeac, O. Serralbo, C. Marcelle, and P.S. Zammit ErbB3 binding protein-1 (ebp-1) controls proliferation and myogenic differentiation of muscle stem cells Dev. Biol. 386 2014 135 151
27. F.C. Fraser, J.R. Sproule, and F. Halal Frequency of the branchio-oto-renal (BOR) syndrome in children with profound hearing loss Am. J. Med. Genet. 7 1980 341 349
28. H.P. Gerber, K. Seipel, O. Georgiev, M. Hofferer, M. Hug, S. Rusconi, and W. Shcaffner Transcriptional activation modulated by homopolymorphic proline stretches Science 263 1994 808 811
29. M.J. Gilchrist From expression cloning to gene modeling: the development of Xenopus gene sequence resources Genesis 50 2012 143 154
30. L. Giot, J.S. Bader, C. Brouwer, A. Chaudhuri, B. Kuang, Y. Li, Y.L. Hao, C.E. Ooi, B. Godwin, E. Vitols, G. Vijayadamodar, P. Pochart, H. Machineni, M. Welsh, Y. Kong, B. Zerhusen, R. Malcolm, Z. Varrone, A. Collis, M. Minto, S. Burgess, L. McDaniel, E. Stimpson, F. Spriggs, J. Williams, K. Neurath, N. Ioime, M. Agee, E. Voss, K. Furtak, R. Renzulli, N. Aanensen, S. Carrolla, E. Bickelhaupt, Y. Lazovatsky, A. DaSilva, J. Zhong, C.A. Stanyon, R.L. Finley, K.P. White, M. Braverman, T. Jarvie, S. Gold, M. Leach, J. Knight, R.S. Shimkets, M.P. McKenna, J. Chant, and J.M. Rothberg A protein interaction map of Drosophila melanogaster Science 302 2003 1727 1736
31. C.B. Gocke, and H. Yu Znf198 stabilizes the lsd1-corest-hdac1 complex on chromatin through its mym-type zinc fingers PLoS One 3 2008 1 12
32. P.A. Gray, H. Fu, P. Luo, Q. Zhao, J. Yu, A. Ferrari, T. Tenzen, D.I. Yuk, E.F. Tsung, Z. Cai, J.A. Alberta, L.P. Cheng, Y. Liu, J.M. Stenman, M.T. Valerius, N. Billings, H.A. Kim, M.E. Greenberg, A.P. McMahon, D.H. Rowitch, C.D. Stiles, and Q. Ma Mouse brain organization revealed through direct genome-scale TF expression analysis Science 306 2004 2255 2257
33. R. Grifone, J. Demignon, C. Houbron, E. Souil, C. Niro, M.J. Seller, G. Hamard, and P. Maire Six1 and Six4 homeoproteins are required for Pax3 and Mrf expression during myogenesis in the mouse embryo Development 293 2005 2235 2249
34. T. Grocott, M. Tambalo, and A. Streit The peripheral sensory nervous system in the vertebrate head: A gene regulatory perspective Dev. Biol. 370 2012 3 23
35. K. Han, and J.L. Manley Transcriptional repression by the Drosophila even-skipped protein: definition of minimal repression domain Genes Dev. 7 1993 491 503
36. R.M. Harland, and R.M. Grainger Xenopus research: metamorphosed by genetics and genomics Trends Genet. 27 2011 507 515
37. V. Hatini, Y. Xin, G. Balas, and E. Lai Dynamics of placodal lineage development revealed by targeted transgene expression Dev. Dyn. 215 1999 332 343
38. T. Hayashi, C. Xu, and R.W. Carthew Cell-type-specific transcription of prospero is controlled by combinatorial signaling in the Drosophila eye Development 135 2008 2787 2796
39. U. Hellsten, R.M. Harland, M.J. Gilchrist, D. Hendrix, J. Jurka, V. Kapitonov, I. Ovcharenko, N.H. Putnam, S. Shu, L. Taher, I.L. Blitz, B. Blumberg, D.S. Dichman, I. Dubchak, E. Amaya, D.C. Detter, R. Fletcher, D.S. Gerhard, D. Goodstein, T. Grave, I.V. Grigoriev, J. Grimwood, T. Kawashima, E. Lindquist, S.M. Lucas, P.E. Mead, T. Mitros, H. Ogino, Y. Ohta, A.V. Poliakov, N. Pollet, J. Robert, A. Salamov, A.K. Sater, J. Schmutz, A. Terry, P.D. Vize, W.C. Warren, D. Wells, A. Willis, R.K. Wilson, L.B. Zimmerman, A.M. Zorn, R. Grainger, T. Grammer, M.K. Khokha, P.M. Richardson, and D.S. Rokhsar The genome of the Western clawed frog Xenopus tropicalis Science 328 2010 633 636
40. N. Hilgert, R.J.H. Smith, and G. Van Camp Function and expression pattern of nonsyndromic deafness genes Curr. Mol. Med. 9 2009 546 564
41. B.E. Hoskins, C.H. Cramer, D. Silvius, D. Zou, R.M. Raymond, D.J. Orten, W.J. Kimberling, R.J. Smith, D. Weil, C. Petit, E.A. Otto, P.X. Xu, and F. Hildebrandt Transcription factor Six5 is mutated in patients with Branchio-Oto-Renal Syndrome Am. J. Hum. Genet. 80 2007 800 804
42. C.C. Hsu, C.H. Che, T.I. Hsu, J.J. Hung, J.L. Ko, B. Zhang, Y.C. Lee, H.K. Chen, W.C. Chang, and D.Y. Lin The 58 Kda Microspherule Protein (Msp58) represses human telomerase reverse transcriptase (Htert) gene expression and cell proliferation by interacting with telomerase transcriptional element-interacting factor (Teif) Biochim. Biophys. Acta 1843 2014 565 579
43. C.H. Hwang, A. Simeone, E. Lai, and D.K. Wu Foxg1 is required for proper separation and formation of sensory cristae during inner ear development Dev. Dyn. 238 2009 2725 2734
44. K. Ikeda, Y. Watanabe, H. Ohto, and K. Kawakami Molecular interaction and synergistic activation of a promoter by Six, Eya, and Dach proteins mediated through CREB binding protein Mol. Cell. Biol. 22 2002 6759 6766
45. K. Ikeda, S. Ookawara, S. Sato, Z. Ando, R. Kageyama, and K. Kawakami Six1 is essential for early neurogenesis in the development of olfactory epithelium Dev. Biol. 311 2007 53 68
46. K. Ikeda, R. Kageyama, Y. Suzuki, and K. Kawakami Six1 is indispensable for production of functional progenitor cells during olfactory epithelial development Int. J. Dev. Biol. 54 2010 1453 1464
47. T. Ito, Y. Noguchi, T. Yashima, and K. Kitamura SIX1 mutation associated with enlargement of the vestibular aqueduct in a patient with branchio-oto syndrome Laryngoscope 116 2006 797 799
48. B. Jusiak, F. Wang, U.C. Karandikar, S.J. Kwak, H. Wang, R. Chen, and G. Mardon Genome-wide DNA binding pattern of the homeodomain transcriptional factor Sine oculis (So) in the developing eye of Drosophila melanogaster Genomics Data 2 2014 153 155
49. B. Jusiak, U.C. Karandikar, S.J. Kwak, F. Wang, H. Wang, R. Chen, and G. Mardon Regulation of Drosophila eye development by the transcription factor Sine oculis PLoS One 9 2014 e89695
50. K. Kawakami, S. Sato, H. Ozaki, and K. Ikeda Six family genes-structure and function as transcription factors and their roles in development Bioessays 22 2000 616 626
51. S. Kawauchi, J. Kim, R. Santos, H.H. Wu, A.D. Lander, and A.L. Calof Foxg1 promotes olfactory neurogenesis by antagonizing Gdf11 Development 136 2009 1453 1464
52. B.K. Kay, M.P. Williamson, and M. Sudol The importance of being proline: the interaction of proline-rich motifs in signaling proteins with their cognate domains FASEB J. 14 2000 231 241
53. K.L. Kenyon, S.A. Moody, and M. Jamrich A novel forkhead gene mediates early steps during Xenopus lens formation Development 126 1999 5107 5116
54. K.L. Kenyon, D.J. Li, C. Clouser, S. Tran, and F. Pignoni Fly SIX-type homeodomain proteins Sine oculis and Optix partner with different cofactors during eye development Dev. Dyn. 234 2005 497 504
55. K.L. Kenyon, D. Yang-Zhou, C.Q. Cai, S. Tran, C. Clouser, G. Decene, S. Ranade, and F. Pignoni Partner specificity is essential for proper function of the SIX-type homeodomain proteins Sine oculis and Optix during fly eye development Dev. Biol. 286 2005 158 168
56. S.B. Khatri, and A.K. Groves Expression of the Foxi2 and Foxi3 transcription factors during development of chicken sensory placodes and pharyngeal arches Gene Expr. Patterns 13 2013 38 42
57. M.K. Khokha Xenopus white papers and resources: folding functional genomics and genetics into the frog Genesis 50 2012 133 142
58. C.K. Kim, T.L. Nguyen, K.M. Joo, D.H. Nam, J. Park, K.H. Lee, S.W. Cho, and J.Y. Ahn Negative regulation of p53 by the long isoform of ErbB3 binding protein Ebp1 in brain tumors Cancer Res. 70 2010 9730 9741
59. M. Kobayashi, K. Nishikawa, T. Suzuki, and M. Yamamoto The homeobox protein Six3 interacts with the Groucho corepressor and acts as a transcriptional repressor in eye and forebrain formation Dev. Biol. 232 2001 315 326
60. A. Kochhar, D.J. Orten, J.L. Sorensen, S.M. Fischer, C.W. Cremers, W.J. Kimberling, and R.J. Smith SIX1 mutation screening in 247 branchio-otic-renal syndrome families: a recurrent missense mutation associated with BOR Hum. Mutat. 29 2008 565
61. Y. Konishi, K. Ikeda, Y. Iwakura, and K. Kawakami Six1 and Six4 promote survival of sensory neurons during early trigeminal gangliogenesis Brain Res. 1116 2006 93 102
62. E. Kowalinski, G. Bange, B. Bradatsch, E. Hurt, K. Wild, and I. Sinning The crystal structure of EBP1 reveals a methionine aminopeptidase fold as binding platform for multiple interactions FEBS Lett. 581 2007 4450 4454
63. P. Krug, V. Moriniere, S. Marlin, V. Koubi, H.D. Gabriel, E. Colin, D. Bonneau, R. Salomon, C. Antignac, and L. Heidet Mutation screening of the EYA1, SIX1, and SIX5 genes in a large cohort of patients harboring branchio-oto-renal syndrome calls into question the pathogenic role of SIX5 mutations Hum. Mutat. 32 2011 183 190
64. C. Laclef, E. Souil, J. Demignon, and P. Maire Thymus, kidney and craniofacial abnormalities in Six 1 deficient mice Mech. Dev. 120 2003 669 679
65. J. Li, G.I. Lee, S.R. Van Doern, and J.C. Walker The FHA domain mediates phosphoprotein interactions J. Cell Sci. 23 2000 4143 4149
66. X. Li, K.A. Oghi, J. Zhang, A. Krones, K.T. Bush, C.K. Glass, S.K. Nigam, A.K. Aggarwal, R. Maas, D.W. Rose, and M.G. Rosenfeld Eya protein phosphatase activity regulates Six1-Dach-Eya transcriptional effects in mammalian organogenesis Nature 426 2003 247 254
67. Y. Li, J.M. Manaligod, and D.L. Weeks EYA1 mutations associated with the branchio-otic renal syndrome result in defective otic development in Xenopus laevis Biol. Cell. 102 2010 277 292
68. Z. Liu, J.Y. Ahn, X. Liu, and K. Ye Ebp1 isoforms distinctively regulate cell survival and differentiation Proc. Natl. Acad. Sci. U. S. A. 103 2006 10917 10922
69. Y. Lu, H. Zhou, W. Chen, Y. Zhang, and A.W. Hamburger The ErbB3 binding protein EBP1 regulates ErbB2 protein levels and tamoxifen sensitivity in breast cancer cells Breast Cancer Res. Treat. 126 2011 27 36
70. M. Mason, M. Wang, and P. Narins Structure and function of the middle ear apparatus of the aquatic frog, Xenopus laevis Proc. Inst. Acoust. 31 2009 13 21
71. T.P. Monie, A.J. Perrin, J.R. Birtley, T.R. Sweeney, I. Karakasiliotis, Y. Chaudry, L.O. Roberts, S. Matthews, I.G. Goodfellow, and S. Curry Structural insights into the transcriptional and translational roles of Ebp1 EMBO J. 26 2007 3936 3944
72. S.A. Moody, and A.S. LaMantia Transcriptional regulation of cranial sensory placode development Curr. Top. Dev. Biol. 111 2015 301 350
73. S.A. Moody, and J.P. Saint-Jeannet Development of the Pre-placodal ectoderm and cranial sensory placodes S.A. Moody, Principles of developmental genetics 2nd edition 2014 Elsevier Inc. 331 356
74. A.M. Morgan, and E. Rubenstein Proline: The distribution, frequency, positioning, and common functional roles of proline and polyproline sequences in the human proteome PLoS One 8 2013 e53785
75. C.C. Morton, and W.E. Nance Newborn hearing screening - a silent revolution N. Engl. J. Med. 354 2006 2151 2164
76. M.A. Mosrati, B. Hammami, I.B. Rebeh, L. Ayadi, L. Dhouib, K. Ben Mahfoudh, B. Hakim, I. Charfeddine, J. Mnif, A. Ghorbel, and S. Masmoudi A novel dominant mutation in SIX1, affecting a highly conserved residue, results in only auditory defects in humans Eur. J. Med. Genet. 54 2011 e484 e488
77. T. Nakayama, M.B. Fish, M. Fisher, J. Oomen-Hajagos, G.H. Thomsen, and R.M. Grainger Simple and efficient CRISPR/Cas9-mediated targeted mutagenesis in Xenopus tropicalis Genesis 51 2013 835 843
78. T. Nakayama, I.L. Blitz, M.B. Fish, A.O. Odeleye, S. Manohar, K.W. Cho, and R.M. Grainger Cas9-based genome editing in Xenopus tropicalis Methods Enzymol. 546 2014 355 375
79. K.M. Neilson, F. Pignoni, B. Yan, and S.A. Moody Developmental expression patterns of candidate co-factors for vertebrate Six family transcription factors Dev. Dyn. 239 2010 3446 3466
80. R.M. Nissen, J. Yan, A. Amsterdam, N. Hopkins, and S.M. Burgess Zebrafish foxi modulates cellular responses to Fgf signaling required for the integrity of ear and jaw patterning Development 130 2003 2543 2554
81. Y. Noguchi, T. Ito, A. Nishio, K. Honda, and K. Kitamura Audiovestibular findings in a branchio-oto syndrome patient with a SIX1 mutation Acta Otolaryngol. 131 2011 413 418
82. H. Ohto, T. Takizawa, T. Saito, M. Kobayashi, K. Ikeda, and K. Kawakami Tissue and developmental distribution of Six family gene products Int. J. Dev. Biol. 42 1998 141 148
83. H. Ohto, S. Kamada, K. Tago, S. Tominaga, H. Ozaki, S. Sato, and K. Kawakami Cooperation of Six and Eya in activation of their target genes through nuclear translocation of Eya Mol. Cell. Biol. 19 1999 6815 6824
84. T. Ohyama, and A.K. Groves Expression of mouse Foxi class genes in early craniofacial development Dev. Dyn. 231 2004 640 646
85. H. Ozaki, Y. Watanabe, K. Takahashi, K. Kitamura, A. Tanaka, K. Urase, T. Momoi, K. Sudo, J. Sakagami, M. Asano, Y. Iwakura, and K. Kawakami Six4, a putative myogenin gene regulator, is not essential for mouse embryonic development Mol. Cell. Biol. 21 2001 3343 3350
86. H. Ozaki, Y. Watanabe, K. Ikeda, and K. Kawakami Impaired interactions between mouse Eya1 harboring mutations found in patients with branchio-oto-renal syndrome and Six, Dach, and G proteins J. Hum. Genet. 47 2002 107 116
87. H. Ozaki, K. Nakamura, J. Funahashi, K. Ikeda, G. Yamada, H. Tokano, H.O. Okamura, K. Kitamur, S. Muto, H. Kotaki, K. Sudo, R. Horai, Y. Iwakura, and K. Kawakami Six1 controls patterning of the mouse otic vesicle Development 131 2004 551 562
88. P.D. Pandur, and S.A. Moody Xenopus Six1 gene is expressed in neurogenic cranial placodes and maintained in the differentiating lateral lines Mech. Dev. 96 2000 253 257
89. A.N. Patrick, B.J. Schiemann, K. Yang, R. Zhao, and H.L. Ford Biochemical and functional characterization for six SIX1 Branchio-otic-renal syndrome mutations J. Biol. Chem. 284 2009 20781 20790
90. A.N. Patrick, J.H. Cabrera, A.L. Smith, X.S. Chen, H.L. Ford, and R. Zhao Structure function analyses of the human SIX1-EYA2 complex reveal insights into metastasis and BOR Syndrome Nat. Struct. Mol. Biol. 20 2013 447 453
91. S. Pauley, E. Lai, and B. Fritzsch Foxg1 is required for morphogenesis and histogenesis of the mammalian inner ear Dev. Dyn. 235 2006 2470 2480
92. T. Pauli, M. Seimiya, J. Blanco, and W.J. Gehring Identification of functional sine oculis motifs in the autoregulatory element of its own gene, in the eyeless enhancer and in the signalling gene hedgehog Development 132 2005 2771 2782
93. F. Pignoni, B. Hu, K.H. Zavitz, J. Xiao, P.A. Garrity, and S.L. Zipursky The eye-specification proteins So and Eya form a complex and regulate multiple steps in Drosophila eye development Cell 91 1997 881 891
94. C. Piñeiro, C.S. Lopes, and F. Casares A conserved transcriptional network regulates lamina development in the Drosophila visual system Development 141 2014 2838 2847
95. T.R. Powers, S.M. Virk, C. Trujillo-Provencio, and E.E. Serrano Probing the Xenopus laevis inner ear transcriptome for biological function BMC Genomics 13 2012 225
96. S.J. Raja, I. Charapitsa, T. Conrad, J.M. Vaquerizas, P. Gebhardt, H. Holz, J. Kadlec, S. Fraterman, N.M. Luscombe, and A. Akhtar The nonspecific lethal complex is a transcriptional regulator in Drosophila Mol. Cell 38 2010 827 841
97. R.G. Ruf, P.X. Xu, D. Silvius, E.A. Otto, F. Beekmann, U.T. Muerb, S. Kumar, T.J. Neuhaus, M.J. Kemper, R.M.J. Raymond, P.D. Brophy, J. Berkman, M. Gattas, V. Hyland, E.M. Ruf, C. Schwartz, E.H. Chang, R.J. Smith, C.A. Stratakis, D. Weil, C. Petit, and F. Hildebrandt SIX1 mutations cause branchio-oto-renal syndrome by disruption of EYA1-SIX1-DNA complexes Proc. Natl. Acad. Sci. U. S. A. 101 2004 8090 8095
98. J.P. Saint-Jeannet, and S.A. Moody Establishing the pre-placodal region and breaking it into placodes with distinct identities Dev. Biol. 389 2014 13 27
99. L. Sandell Neural crest cells in ear development P.A. Trainor, Neural crest cells. Evolution, development and disease 2014 Elsevier 167 188
100. K. Sanggaard, N.D. Rendtorff, K.W. Kjaer, H. Eiberg, T. Johnsen, S. Gimsing, J. Dyrmose, K.O. Nielsen, K. Lage, and L. Tranebjaerg Branchio-otic-renal syndrome: detection of EYA1 and SIX1 mutations in five out of six Danish families by combining linkage, MLPA and sequencing analyses Eur. J. Hum. Genet. 15 2007 1121 1131
101. G. Schlosser, and K. Ahrens Molecular anatomy of placode development in Xenopus laevis Dev. Biol. 271 2004 439 466
102. G. Schlosser, T. Awtry, S.A. Brugmann, E.D. Jensen, K. Neilson, G. Ruan, A. Stammler, D. Voelker, B. Yan, C. Zhang, M.W. Klymkowsky, and S.A. Moody Eya1 and Six1 promote neurogenesis in the cranial placodes in a SoxB1-dependent fashion Dev. Biol. 320 2008 199 214
103. R.L. Schoffelen, J.M. Segenhout, and P. Van Dijk Mechanics of the exceptional anuran ear J. Comp. Physiol. A. 194 2008 417 428
104. M. Self, O.V. Lsagutin, B. Bowling, J. Hendrix, Y. Cal, G.R. Dressler, and G. Oliver Six2 is required for suppression of nephrogenesis and progenitor renewal in the developing kidney EMBO J. 25 2006 5214 5228
105. H.C. Seo, J. Curtiss, M. Mlodzik, and A. Fjose Six class homeobox genes in drosophila belong to three distinct families and are involved in head development Mech. Dev. 83 1999 127-123
106. M.A. Serikaku, and J.E. O'Tousa sine oculis is a homeobox gene required for Drosophila visual system development Genetics 138 1994 1137 1150
107. H. Shi, S. Chen, H. Jin, C. Xu, G. Dong, W. Wang, H. Zhang, W. Lin, J. Zhang, L. Davidovic, L. Yao, and D. Fan Downregulation of MSP58 inhibits growth of human colorectal cancer cells via regulation of the cyclin D1-cyclin-dependent kinase 4-p21 pathway Cancer Sci. 100 2009 1585 1590
108. S.J. Silver, E.L. Davies, L. Doyon, and I. Rebay Functional dissection of eyes absent reveals new modes of regulation within the retinal determination gene network Mol. Cell. Biol. 23 2003 5989 5999
109. R.J.H. Smith Branchiootorenal spectrum disorders Gene Reviews 2014 (http://www.ncbi.nlm.nih.gov/books/NBK1380/)
110. R.J.H. Smith, A.E. Shearer, M.S. Hildebrand, and G. Van Camp Deafness and hereditary hearing loss overview Gene Reviews 2014 (http://www.ncbi.nlm.nih.gov/books/NBK1434/)
111. K.S. Solomon, J.M. Logsdo, and A. Fritz Expression and phylogenetic analyses of three zebrafish Foxi class genes Dev. Dyn. 228 2003 301 307
112. M. Squatrito, M. Mancino, M. Donzelli, L.B. Areces, and G.F. Draetta EBP1 is a nucleolar growth-regulating protein that is part of pre-ribosomal ribonucleoprotein complexes Oncogene 23 2004 4454 4465
113. A. Streit Early development of the cranial sensory nervous system: from a common field to individual placodes Dev. Biol. 276 2004 1 15
114. H. Sun, and T. Hunter Poly-small ubiquitin-like modifier (poly-SUMO)-binding proteins identified through a string search J. Biol. Chem. 287 2012 42071 42083
115. H.V. Toriello, W. Reardon, and R.J. Gorlin Hereditary hearing loss and its syndromes 2004 Oxford University Press
116. P. Van Dijk, M.J. Mason, R.L. Schoffelen, P.M. Narins, and S.W. Meenderink Mechanics of the frog ear Hear. Res. 273 2011 46 58
117. G.N. Wheeler, and A.W. Brändli Simple vertebrate models for chemical genetics and drug discovery screens: Lessons from zebrafish and Xenopus Dev. Dyn. 238 2009 1287 1308
118. M.P. Williamson The structure and function of proline-rich regions in proteins Biochem. J. 297 1994 249 260
119. L. Wu, Z.G. Zhang, H.Z. Qin, J. Zhang, G.D. Gao, W. Lin, J. Wang, and J. Zhang Downregulation of MSP58 suppresses cell proliferation in neuroblastoma cell lines NeuroReport 23 2012 932 936
120. X. Xia, A. Cheng, T. Lessor, Y. Zhang, and A.W. Hamburger Ebp1, an ErbB-3 binding protein, interacts with Rb and affects Rb transcriptional regulation J. Cell. Physiol. 187 2001 209 217
121. P.X. Xu, J. Adams, H. Peters, M.C. Brown, S. Heaney, and R. Maas Eya1-deficient mice lack ears and kidneys and show abnormal apoptosis of organ primordia Nat. Genet. 23 1999 113 117
122. P.X. Xu, W. Zheng, L. Huang, P. Maire, C. Laclef, and D. Silvius Six1 is required for the early organogenesis of mammalian kidney Development 130 2003 3085 3094
123. H. Yan, J. Canon, and U. Banerjee A transcriptional chain linking eye specification to terminal determination of cone cells in the Drosophila eye Dev. Biol. 263 2003 323 329
124. B. Yan, K.M. Neilson, R. Ranganathan, T. Maynard, A. Streit, and S. Moody Microarray identification of novel genes downstream of Six1, a critical factor in cranial placode, somite and kidney development Dev. Dyn. 244 2015 181 210
125. J.Y. Yoo, X.W. Wang, A.K. Rishi, T. Lessor, X.M. Xia, T.A. Gusstafson, and A.W. Hamburger Interaction of the PA2G4 (EBP1) protein with ErbB-3 and regulation of this binding by heregulin Br. J. Cancer 82 2000 683 690
126. T. Zhang, S. Ranade, C.Q. Cai, C. Clouser, and F. Pignoni Direct control of neurogenesis by selector factors in the fly eye: regulation of atonal by Ey and So Development 133 2006 4881 4889
127. Y. Zhang, Y. Lu, H. Zhou, M. Lee, Z. Liu, B.A. Hassel, and A.W. Hamburger Alterations in cell growth and signaling in ErbB3 binding protein-1 (Ebp1) deficient mice BMC Cell Biol. 9 2008 69
128. W. Zheng, L. Huang, Z.B. Wei, D. Silvius, B. Tang, and P.X. Xu The role of Six1 in mammalian auditory system development Development 130 2003 3989 4000
129. M. Zhong, X. Zhang, B. Li, C.S. Chen, G.L. Ji, S.X. Li, D.Q. Bi, Q.C. Zhao, and H. Shi Expression of MSP58 in hepatocellular carcinoma Med. Oncol. 30 2013 539 549
130. H. Zhou, K. Mazan-Mamczarz, J.L. Martindale, A. Barker, Z. Liu, M. Gorospe, P.J. Leedman, R.B. Gartenhaus, A.W. Hamburger, and Y. Zhang Post-transcriptional regulation of androgen receptor mRNA by an ErbB3 binding protein 1 in prostate cancer Nucleic Acids Res. 38 2010 3619 3631
131. H. Zhou, Y. Zhang, and A.W. Hamburger EBP1 inhibits translation of androgen receptor mRNA in castration resistant prostate cancer cells Anticancer Res. 31 2011 3129 3135
132. Q. Zhou, T. Zhang, J.C. Jemc, Y. Chen, R. Chen, I. Rebay, and F. Pignoni Onset of atonal expression in Drosophila retinal progenitors involves redundant and synergistic contribution of Ey/Pax6 and So binding sites within two distant enhancers Dev. Biol. 386 2014 152 164
133. C.C. Zhu, M.A. Dyer, M. Uchikawa, H. Kondoh, O.V. Lagutin, and G. Oliver Six3-mediated auto repression and eye development requires its interaction with members of the Groucho-related family of co-repressors Development 129 2002 2835 2849
134. D. Zou, D. Silvius, B. Fritzsch, and P.X. Xu Eya1 and Six1 are essential for early steps of sensory neurogenesis in mammalian cranial placodes Development 131 2004 5561 5572
135. D. Zou, D. Silvius, J. Davenport, R. Grifone, P. Maire, and P.X. Xu Patterning of the third pharyngeal pouch into thymus/parathyroid by Six and Eya1 Dev. Biol. 293 2006 499 512
136. D. Zou, D. Silvius, S. Rodrigo-Blomqvist, S. Enerback, and P.X. Xu Eya1 regulates the growth of otic epithelium and interacts with Pax2 during the development of all sensory areas of the inner ear Dev. Biol. 298 2006 430 441