An Alteration in ELMOD3, an Arl2 GTPase-Activating Protein, Is Associated with Hearing Impairment in Humans

PLoS Genetics

Volumn 9, Issue 9, 2013, Pages

  Jaworek, Thomas J ^a   Richard, Elodie M ^a,b   Ivanova, Anna A ^c   Giese, Arnaud P J ^a,b   Choo, Daniel I ^b   Khan, Shaheen N ^d   Riazuddin, Sheikh ^d,e   Kahn, Richard A ^c   Riazuddin, Saima ^a,b  

^a CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^b UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d UNIVERSITY OF THE PUNJAB   (Pakistan)

^e UNIVERSITY OF HEALTH SCIENCES   (Pakistan)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; PROTEIN ELMOD3; UNCLASSIFIED DRUG;

5' UNTRANSLATED REGION; ACTIN FILAMENT; ACTIN POLYMERIZATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY DETECTION; ARTICLE; CONTROLLED STUDY; CORTI ORGAN; DFNB88 GENE; ELMOD3 GENE; GENE; GENE EXPRESSION PROFILING; GENE LOCUS; GENE MAPPING; GENE MUTATION; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC LINKAGE; GENETIC TRANSCRIPTION; HEARING IMPAIRMENT; HUMAN; HUMAN CELL; IMMUNOLOCALIZATION; IMMUNOREACTIVITY; MICROVILLUS; MORPHOGENESIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN POLYMERIZATION; PROTEIN PROTEIN INTERACTION; RAT; SHORT TANDEM REPEAT; TRANSLATION INITIATION;

ACTIN CYTOSKELETON; ANIMALS; CELL MEMBRANE; CELL MOVEMENT; EAR, INNER; GTP-BINDING PROTEINS; GTPASE-ACTIVATING PROTEINS; HAIR CELLS, AUDITORY; HEARING LOSS; HEK293 CELLS; HUMANS; MICE; MUTATION;

EID: 84884696370     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003774     Document Type: Article

References (40)

1. Brown SD, Hardisty-Hughes RE, Mburu P, (2008) Quiet as a mouse: dissecting the molecular and genetic basis of hearing. Nature reviews Genetics 9: 277-290.
2. Frolenkov GI, Belyantseva IA, Friedman TB, Griffith AJ, (2004) Genetic insights into the morphogenesis of inner ear hair cells. Nature reviews Genetics 5: 489-498.
3. Petit C, Richardson GP, (2009) Linking genes underlying deafness to hair-bundle development and function. Nature neuroscience 12: 703-710.
4. Richardson GP, de Monvel JB, Petit C, (2011) How the genetics of deafness illuminates auditory physiology. Annual review of physiology 73: 311-334.
5. Kitajiri S, Sakamoto T, Belyantseva IA, Goodyear RJ, Stepanyan R, et al. (2010) Actin-bundling protein TRIOBP forms resilient rootlets of hair cell stereocilia essential for hearing. Cell 141: 786-798.
6. Drummond MC, Belyantseva IA, Friderici KH, Friedman TB, (2011) Actin in hair cells and hearing loss. Hear Res 288: 89-99.
7. Johnson KR, Longo-Guess CM, Gagnon LH, (2012) Mutations of the mouse ELMO domain containing 1 gene (Elmod1) link small GTPase signaling to actin cytoskeleton dynamics in hair cell stereocilia. PLoS One 7: e36074.
8. Rzadzinska AK, Schneider ME, Davies C, Riordan GP, Kachar B, (2004) An actin molecular treadmill and myosins maintain stereocilia functional architecture and self-renewal. J Cell Biol 164: 887-897.
9. Manor U, Kachar B, (2008) Dynamic length regulation of sensory stereocilia. Semin Cell Dev Biol 19: 502-510.
10. Zhang DS, Piazza V, Perrin BJ, Rzadzinska AK, Poczatek JC, et al. (2012) Multi-isotope imaging mass spectrometry reveals slow protein turnover in hair-cell stereocilia. Nature 481: 520-524.
11. Grimsley-Myers CM, Sipe CW, Geleoc GS, Lu X, (2009) The small GTPase Rac1 regulates auditory hair cell morphogenesis. J Neurosci 29: 15859-15869.
12. Grimsley-Myers CM, Sipe CW, Wu DK, Lu X, (2012) Redundant functions of Rac GTPases in inner ear morphogenesis. Dev Biol 362: 172-186.
13. Kalinec F, Zhang M, Urrutia R, Kalinec G, (2000) Rho GTPases mediate the regulation of cochlear outer hair cell motility by acetylcholine. J Biol Chem 275: 28000-28005.
14. Matsumoto N, Kitani R, Maricle A, Mueller M, Kalinec F, (2010) Pivotal role of actin depolymerization in the regulation of cochlear outer hair cell motility. Biophys J 99: 2067-2076.
15. Li CC, Chiang TC, Wu TS, Pacheco-Rodriguez G, Moss J, et al. (2007) ARL4D recruits cytohesin-2/ARNO to modulate actin remodeling. Mol Biol Cell 18: 4420-4437.
16. East M, Bowzard JB, Dacks J, Kahn RA, (2012) ELMO domains: evolutionary and functional characterization of a novel GTPase activating protein (GAP) domain for Arf family GTPases. J Biol Chem 287: 39538-53.
17. Lindner TH, Hoffmann K, (2005) easyLINKAGE: a PERL script for easy and automated two-/multi-point linkage analyses. Bioinformatics 21: 405-407.
18. Flex E, Mangino M, Mazzoli M, Martini A, Migliosi V, et al. (2003) Mapping of a new autosomal dominant non-syndromic hearing loss locus (DFNA43) to chromosome 2p12. J Med Genet 40: 278-281.
19. Cooper DN, Krawczak M, Antonorakis SE (1995) The nature and mechanisms of human gene mutation. In: Scriver C, Beaudet al., Sly WS, Valle D, editors. The Metabolic and Molecular Bases of Inherited Disease. 7th ed. New York: McGraw-Hill. pp. 259-291.
20. Adzhubei IA, Schmidt S, Peshkin L, Ramensky VE, Gerasimova A, et al. (2010) A method and server for predicting damaging missense mutations. Nat Methods 7: 248-249.
21. Yue P, Melamud E, Moult J, (2006) SNPs3D: candidate gene and SNP selection for association studies. BMC Bioinformatics 7: 166.
22. Schwarz JM, Rodelsperger C, Schuelke M, Seelow D, (2010) MutationTaster evaluates disease-causing potential of sequence alterations. Nat Methods 7: 575-576.
23. Ferrer-Costa C, Orozco M, de la Cruz X, (2004) Sequence-based prediction of pathological mutations. Proteins 57: 811-819.
24. Kumar P, Henikoff S, Ng PC, (2009) Predicting the effects of coding non-synonymous variants on protein function using the SIFT algorithm. Nat Protoc 4: 1073-1081.
25. Zheng L, Zheng J, Whitlon DS, Garcia-Anoveros J, Bartles JR, (2010) Targeting of the hair cell proteins cadherin 23, harmonin, myosin XVa, espin, and prestin in an epithelial cell model. J Neurosci 30: 7187-7201.
26. Loomis PA, Zheng L, Sekerkova G, Changyaleket B, Mugnaini E, et al. (2003) Espin cross-links cause the elongation of microvillus-type parallel actin bundles in vivo. J Cell Biol 163: 1045-1055.
27. Casella JF, Flanagan MD, Lin S, (1981) Cytochalasin D inhibits actin polymerization and induces depolymerization of actin filaments formed during platelet shape change. Nature 293: 302-305.
28. Goddette DW, Frieden C, (1985) The binding of cytochalasin D to monomeric actin. Biochem Biophys Res Commun 128: 1087-1092.
29. Bowzard JB, Cheng D, Peng J, Kahn RA, (2007) ELMOD2 is an Arl2 GTPase-activating protein that also acts on Arfs. J Biol Chem 282: 17568-17580.
30. Peng AW, Belyantseva IA, Hsu PD, Friedman TB, Heller S, (2009) Twinfilin 2 regulates actin filament lengths in cochlear stereocilia. J Neurosci 29: 15083-15088.
31. Hertzano R, Elkon R, Kurima K, Morrisson A, Chan SL, et al. (2011) Cell type-specific transcriptome analysis reveals a major role for Zeb1 and miR-200b in mouse inner ear morphogenesis. PLoS Genet 7: e1002309.
32. Margaron Y, Fradet N, Cote JF, (2013) ELMO recruits actin cross-linking family 7 (ACF7) at the cell membrane for microtubule capture and stabilization of cellular protrusions. J Biol Chem 288: 1184-1199.
33. Zhou C, Cunningham L, Marcus AI, Li Y, Kahn RA, (2006) Arl2 and Arl3 regulate different microtubule-dependent processes. Mol Biol Cell 17: 2476-2487.
34. Goldberg J, (1999) Structural and functional analysis of the ARF1-ARFGAP complex reveals a role for coatomer in GTP hydrolysis. Cell 96: 893-902.
35. DePristo MA, Banks E, Poplin R, Garimella KV, Maguire JR, et al. (2011) A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat Genet 43: 491-498.
36. Li H, Durbin R, (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
37. Aricescu AR, Assenberg R, Bill RM, Busso D, Chang VT, et al. (2006) Eukaryotic expression: developments for structural proteomics. Acta crystallographica Section D, Biological crystallography 62: 1114-1124.
38. Belyantseva IA, (2009) Helios Gene Gun-mediated transfection of the inner ear sensory epithelium. Methods Mol Biol 493: 103-123.
39. Riazuddin S, Belyantseva IA, Giese AP, Lee K, Indzhykulian AA, et al. (2012) Alterations of the CIB2 calcium- and integrin-binding protein cause Usher syndrome type 1J and nonsyndromic deafness DFNB48. Nat Genet 44: 1265-1271.
40. Marth GT, Yu F, Indap AR, Garimella K, Gravel S, et al. (2011) The functional spectrum of low-frequency coding variation. Genome Biol 12: R84.