Cell type-specific transcriptome analysis reveals a major role for Zeb1 and miR-200b in mouse inner ear morphogenesis

PLoS Genetics

Volumn 7, Issue 9, 2011, Pages

  Hertzano, Ronna ^a   Elkon, Ran ^b   Kurima, Kiyoto ^c   Morrisson, Annie ^a   Chan, Siaw Lin ^a   Sallin, Michelle ^a   Biedlingmaier, Andrew ^a   Darling, Douglas S ^d   Griffith, Andrew J ^c   Eisenman, David J ^a   Strome, Scott E ^a  

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

^b NETHERLANDS CANCER INSTITUTE   (Netherlands)

^c NATIONAL INSTITUTE ON DEAFNESS AND OTHER COMMUNICATION DISORDERS   (United States)

^d UNIVERSITY OF LOUISVILLE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHROMOSOME PROTEIN; MICRORNA; MIR 200B; PROTEIN TWIRLER; PROTEIN ZEB1; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN; HOMEODOMAIN PROTEIN; KRUPPEL LIKE FACTOR; MIRN200 MICRORNA, MOUSE; MIRN96 MICRORNA, MOUSE; ZEB1 PROTEIN, MOUSE;

ANIMAL TISSUE; ARTICLE; CELL SPECIFICITY; CONTROLLED STUDY; EPITHELIUM CELL; GENE; GENE CLUSTER; GENE EXPRESSION; GENETIC TRANSCRIPTION; INNER EAR; INNER EAR MALFORMATION; MESENCHYME CELL; MORPHOGENESIS; MOUSE; MUTANT; NEWBORN; NONHUMAN; REGULATORY MECHANISM; ZEB1 GENE; ANIMAL; CYTOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; HEARING IMPAIRMENT; HISTOLOGY; INSTITUTE FOR CANCER RESEARCH MOUSE; MESODERM; METABOLISM; METHODOLOGY; PHYSIOLOGY; PRENATAL DEVELOPMENT; VESTIBULE;

MAMMALIA; MUS;

ANIMALS; DEAFNESS; EAR, INNER; EPITHELIAL CELLS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; KRUPPEL-LIKE TRANSCRIPTION FACTORS; MESODERM; MICE; MICE, INBRED ICR; MICRORNAS; MORPHOGENESIS; VESTIBULE, LABYRINTH;

EID: 80053437834     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1002309     Document Type: Article

References (40)

1. Friedman TB, Schultz JM, Ben-Yosef T, Pryor SP, Lagziel A, et al. (2003) Recent advances in the understanding of syndromic forms of hearing loss. Ear Hear 24: 289-302.
2. Raviv D, Dror AA, Avraham KB, (2010) Hearing loss: a common disorder caused by many rare alleles. Ann NY Acad Sci 1214: 168-79.
3. Friedman LM, Dror AA, Avraham KB, (2007) Mouse models to study inner ear development and hereditary hearing loss. Int J Dev Biol 51: 609-631.
4. Hertzano R, Puligilla C, Chan SL, Timothy C, Depireux DA, et al. (2010) CD44 is a marker for the outer pillar cells in the early postnatal mouse inner ear. J Assoc Res Otolaryngol 11: 407-418.
5. Nielsen JS, McNagny KM, (2008) Novel functions of the CD34 family. J Cell Sci 121: 3683-3692.
6. Pavlidis P, (2003) Using ANOVA for gene selection from microarray studies of the nervous system. Methods 31: 282-289.
7. Do JH, Choi DK, (2008) Clustering approaches to identifying gene expression patterns from DNA microarray data. Mol Cells 25: 279-288.
8. Ochs MF, Peterson AJ, Kossenkov A, Bidaut G, (2007) Incorporation of gene ontology annotations to enhance microarray data analysis. Methods Mol Biol 377: 243-254.
9. Schoen CJ, Emery SB, Thorne MC, Ammana HR, Sliwerska E, et al. (2010) Increased activity of Diaphanous homolog 3 (DIAPH3)/diaphanous causes hearing defects in humans with auditory neuropathy and in Drosophila. Proc Natl Acad Sci U S A 107: 13396-13401.
10. Ulitsky I, Shamir R, (2007) Identification of functional modules using network topology and high-throughput data. BMC Syst Biol 1: 8.
11. Mencia A, Modamio-Hoybjor S, Redshaw N, Morin M, Mayo-Merino F, et al. (2009) Mutations in the seed region of human miR-96 are responsible for nonsyndromic progressive hearing loss. Nat Genet 41: 609-613.
12. Lewis MA, Quint E, Glazier AM, Fuchs H, De Angelis MH, et al. (2009) An ENU-induced mutation of miR-96 associated with progressive hearing loss in mice. Nat Genet 41: 614-618.
13. Weston MD, Pierce ML, Rocha-Sanchez S, Beisel KW, Soukup GA, (2006) MicroRNA gene expression in the mouse inner ear. Brain Res 1111: 95-104.
14. Elkon R, Agami R, (2008) Removal of AU bias from microarray mRNA expression data enhances computational identification of active microRNAs. PLoS Comput Biol 4: e1000189.
15. Van Dongen S, Abreu-Goodger C, Enright AJ, (2008) Detecting microRNA binding and siRNA off-target effects from expression data. Nat Methods 5: 1023-1025.
16. Smirnova L, Grafe A, Seiler A, Schumacher S, Nitsch R, et al. (2005) Regulation of miRNA expression during neural cell specification. Eur J Neurosci 21: 1469-1477.
17. Sacheli R, Nguyen L, Borgs L, Vandenbosch R, Bodson M, et al. (2009) Expression patterns of miR-96, miR-182 and miR-183 in the development inner ear. Gene Expr Patterns 9: 364-370.
18. Linhart C, Halperin Y, Shamir R, (2008) Transcription factor and microRNA motif discovery: the Amadeus platform and a compendium of metazoan target sets. Genome Res 18: 1180-1189.
19. Ikeda K, Kawakami K, (1995) DNA binding through distinct domains of zinc-finger-homeodomain protein AREB6 has different effects on gene transcription. Eur J Biochem 233: 73-82.
20. Postigo AA, Ward E, Skeath JB, Dean DC, (1999) zfh-1, the Drosophila homologue of ZEB, is a transcriptional repressor that regulates somatic myogenesis. Mol Cell Biol 19: 7255-7263.
21. Spoelstra NS, Manning NG, Higashi Y, Darling D, Singh M, et al. (2006) The transcription factor ZEB1 is aberrantly expressed in aggressive uterine cancers. Cancer Res 66: 3893-3902.
22. Burk U, Schubert J, Wellner U, Schmalhofer O, Vincan E, et al. (2008) A reciprocal repression between ZEB1 and members of the miR-200 family promotes EMT and invasion in cancer cells. EMBO Rep 9 (6): 582-9.
23. Lyon MF, (1958) Twirler: a mutant affecting the inner ear of the house mouse. J Embryol Exp Morphol 6: 105-116.
24. Kurima K, Hertzano R, Gavrilova O, Monahan K, Shpargel KB, et al. (2011) A Noncoding Point Mutation of Zeb1 Causes Multiple Developmental Malformations and Obesity in Twirler mice. PLoS Genetics, accepted.
25. Goodyear RJ, Richardson GP, (2002) Extracellular matrices associated with the apical surfaces of sensory epithelia in the inner ear: molecular and structural diversity. J Neurobiol 53: 212-227.
26. Zhao X, Yang H, Yamoah EN, Lundberg YW, (2007) Gene targeting reveals the role of Oc90 as the essential organizer of the otoconial organic matrix. Dev Biol 304: 508-524.
27. Wang W, Cherry JM, Nochomovitz Y, Jolly E, Botstein D, et al. (2005) Inference of combinatorial regulation in yeast transcriptional networks: a case study of sporulation. Proc Natl Acad Sci U S A 102: 1998-2003.
28. Pilpel Y, Sudarsanam P, Church GM, (2001) Identifying regulatory networks by combinatorial analysis of promoter elements. Nat Genet 29: 153-159.
29. Hornstein E, Shomron N, (2006) Canalization of development by microRNAs. Nat Genet 38 (Suppl): S20-24.
30. Liu Y, Peng X, Tan J, Darling DS, Kaplan HJ, et al. (2008) Zeb1 mutant mice as a model of posterior corneal dystrophy. Invest Ophthalmol Vis Sci 49: 1843-1849.
31. Park PJ, (2009) ChIP-seq: advantages and challenges of a maturing technology. Nat Rev Genet 10: 669-680.
32. Verpy E, Leibovici M, Petit C, (1999) Characterization of otoconin-95, the major protein of murine otoconia, provides insights into the formation of these inner ear biominerals. Proc Natl Acad Sci USA 96: 529-534.
33. Cohen-Salmon M, El-Amraoui A, Leibovici M, Petit C, (1997) Otogelin: a glycoprotein specific to the acellular membranes of the inner ear. Proc Natl Acad Sci USA 94: 14450-14455.
34. Legan PK, Lukashkina VA, Goodyear RJ, Kossi M, Russell IJ, et al. (2000) A targeted deletion in alpha-tectorin reveals that the tectorial membrane is required for the gain and timing of cochlear feedback. Neuron 28: 273-285.
35. Driver EC, Kelley MW, (2010) Transfection of mouse cochlear explants by electroporation. Curr Protoc Neurosci Chapter 4 (Unit 4 34): 31-10.
36. Ulitsky I, Maron-Katz A, Shavit S, Sagir D, Linhart C, et al. (2010) Expander: from expression microarrays to networks and functions. Nat Protoc 5: 303-322.
37. Lewis BP, Burge CB, Bartel DP, (2005) Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120: 15-20.
38. Sayers EW, Barrett T, Benson DA, Bolton E, Bryant SH, et al. (2011) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res 38: D5-16.
39. Friedman LM, Dror AA, Mor E, Tenne T, Toren G, et al. (2009) MicroRNAs are essential for development and function of inner ear hair cells in vertebrates. Proc Natl Acad Sci U S A 106: 7915-7920.
40. Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, et al. (2005) Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci U S A 102: 15545-15550.