Mice deficient in H+-ATPase a4 subunit have severe hearing impairment associated with enlarged endolymphatic compartments within the inner ear

DMM Disease Models and Mechanisms

Volumn 6, Issue 2, 2013, Pages 434-442

  Lorente Cánovas, Beatriz ^a   Ingham, Neil ^a   Norgett, Elizabeth E ^b   Golder, Zoe J ^b   Frankl, Fiona E Karet ^b,c   Steel, Karen P ^a,d  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c KING'S COLLEGE LONDON   (United Kingdom)

^d MEDICAL RESEARCH COUNCIL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATASE V0A4; CARRIER PROTEINS AND BINDING PROTEINS; PENDRIN; POTASSIUM CHANNEL; PROTEIN FOXI1; PROTON PUMP; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUDITORY SYSTEM FUNCTION; COCHLEAR NUCLEUS; CONTROLLED STUDY; EVOKED BRAIN STEM AUDITORY RESPONSE; GENE EXPRESSION; GENE MUTATION; HEARING ACUITY; HEARING IMPAIRMENT; HETEROZYGOTE; HOMOZYGOTE; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; STRIA VASCULARIS; VESTIBULE AQUEDUCT;

ANIMALS; ANIMALS, NEWBORN; ANION TRANSPORT PROTEINS; EAR, INNER; ENDOLYMPH; ENDOLYMPHATIC SAC; EPITHELIUM; EVOKED POTENTIALS, AUDITORY; FORKHEAD TRANSCRIPTION FACTORS; HAIR CELLS, AUDITORY, OUTER; HEARING LOSS; HUMANS; KCNQ1 POTASSIUM CHANNEL; MICE; MICE, KNOCKOUT; MUTATION; PHENOTYPE; POTASSIUM CHANNELS, INWARDLY RECTIFYING; PROTEIN SUBUNITS; PROTON-TRANSLOCATING ATPASES; STRIA VASCULARIS;

EID: 84875127469     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.010645     Document Type: Article

References (36)

1. Andreucci, E., Bianchi, B., Carboni, I., Lavoratti, G., Mortilla, M., Fonda, C., Bigozzi, M., Genuardi, M., Giglio, S. and Pela, I. (2009). Inner ear abnormalities in four patients with dRTA and SNHL: clinical and genetic heterogeneity. Pediatr. Nephrol. 24, 2147-2153.
2. Cable, J. and Steel, K. P. (1991). Identification of two types of melanocyte within the stria vascularis of the mouse inner ear. Pigment Cell Res. 4, 87-101.
3. Cable, J., Huszar, D., Jaenisch, R. and Steel, K. P. (1994). Effects of mutations at the W locus (c-kit) on inner ear pigmentation and function in the mouse. Pigment Cell Res. 7, 17-32.
4. Casimiro, M. C., Knollmann, B. C., Ebert, S. N., Vary, J. C., Jr, Greene, A. E., Franz, M. R., Grinberg, A., Huang, S. P. and Pfeifer, K. (2001). Targeted disruption of the Kcnq1 gene produces a mouse model of Jervell and Lange-Nielsen Syndrome. Proc. Natl. Acad. Sci. USA 98, 2526-2531. (Pubitemid 32209515)
5. Dou, H., Finberg, K., Cardell, E. L., Lifton, R. and Choo, D. (2003). Mice lacking the B1 subunit of H+-ATPase have normal hearing. Hear. Res. 180, 76-84. (Pubitemid 36627605)
6. Dou, H., Xu, J., Wang, Z., Smith, A. N., Soleimani, M., Karet, F. E., Greinwald, J. H., Jr and Choo, D. (2004). Co-expression of pendrin, vacuolar H+-ATPase alpha4-subunit and carbonic anhydrase II in epithelial cells of the murine endolymphatic sac. J. Histochem. Cytochem. 52, 1377-1384. (Pubitemid 39362461)
7. Everett, L. A., Glaser, B., Beck, J. C., Idol, J. R., Buchs, A., Heyman, M., Adawi, F., Hazani, E., Nassir, E., Baxevanis, A. D. et al. (1997). Pendred syndrome is caused by mutations in a putative sulphate transporter gene (PDS). Nat. Genet. 17, 411-422. (Pubitemid 27518389)
8. Everett, L. A., Morsli, H., Wu, D. K. and Green, E. D. (1999). Expression pattern of the mouse ortholog of the Pendred's syndrome gene (Pds) suggests a key role for pendrin in the inner ear. Proc. Natl. Acad. Sci. USA 96, 9727-9732. (Pubitemid 29398800)
9. Everett, L. A., Belyantseva, I. A., Noben-Trauth, K., Cantos, R., Chen, A., Thakkar, S. I., Hoogstraten-Miller, S. L., Kachar, B., Wu, D. K. and Green, E. D. (2001). Targeted disruption of mouse Pds provides insight about the inner-ear defects encountered in Pendred syndrome. Hum. Mol. Genet. 10, 153-161. (Pubitemid 32098125)
10. Gow, A., Davies, C., Southwood, C. M., Frolenkov, G., Chrustowski, M., Ng, L., Yamauchi, D., Marcus, D. C. and Kachar, B. (2004). Deafness in Claudin 11-null mice reveals the critical contribution of basal cell tight junctions to stria vascularis function. J. Neurosci. 24, 7051-7062. (Pubitemid 39096371)
11. Hibino, H., Horio, Y., Inanobe, A., Doi, K., Ito, M., Yamada, M., Gotow, T., Uchiyama, Y., Kawamura, M., Kubo, T. et al. (1997). An ATP-dependent inwardly rectifying potassium channel, KAB-2 (Kir4. 1), in cochlear stria vascularis of inner ear: its specific subcellular localization and correlation with the formation of endocochlear potential. J. Neurosci. 17, 4711-4721. (Pubitemid 27246928)
12. Hibino, H., Nin, F., Tsuzuki, C. and Kurachi, Y. (2010). How is the highly positive endocochlear potential formed? The specific architecture of the stria vascularis and the roles of the ion-transport apparatus. Pflugers Arch. 459, 521-533.
13. Hulander, M., Kiernan, A. E., Blomqvist, S. R., Carlsson, P., Samuelsson, E. J., Johansson, B. R., Steel, K. P. and Enerbäck, S. (2003). Lack of pendrin expression leads to deafness and expansion of the endolymphatic compartment in inner ears of Foxi1 null mutant mice. Development 130, 2013-2025. (Pubitemid 36575925)
14. Ingham, N. J., Pearson, S. and Steel, K. P. (2011). Using the auditory brainstem response (abr) to determine sensitivity of hearing in mutant mice. Curr. Protoc. Mouse Biol., 9, 279-287.
15. Karet, F. E., Finberg, K. E., Nelson, R. D., Nayir, A., Mocan, H., Sanjad, S. A., Rodriguez-Soriano, J., Santos, F., Cremers, C. W., Di Pietro, A. et al. (1999). Mutations in the gene encoding B1 subunit of H+-ATPase cause renal tubular acidosis with sensorineural deafness. Nat. Genet. 21, 84-90. (Pubitemid 29036289)
16. Kiernan, A. E. (2006). The paintfill method as a tool for analyzing the three-dimensional structure of the inner ear. Brain Res. 1091, 270-276. (Pubitemid 43993897)
17. Kim, H. M. and Wangemann, P. (2011). Epithelial cell stretching and luminal acidification lead to a retarded development of stria vascularis and deafness in mice lacking pendrin. PLoS ONE 6, e17949.
18. Marcus, D. C., Wu, T., Wangemann, P. and Kofuji, P. (2002). KCNJ10 (Kir4.1) potassium channel knockout abolishes endocochlear potential. Am. J. Physiol. Cell. Physiol. 282, C403-C407. (Pubitemid 34663200)
19. Miranda, K. C., Karet, F. E. and Brown, D. (2010). An extended nomenclature for mammalian V-ATPase subunit genes and splice variants. PLoS ONE 5, e9531.
20. Neyroud, N., Tesson, F., Denjoy, I., Leibovici, M., Donger, C., Barhanin, J., Fauré, S., Gary, F., Coumel, P., Petit, C. et al. (1997). A novel mutation in the potassium channel gene KVLQT1 causes the Jervell and Lange-Nielsen cardioauditory syndrome. Nat. Genet. 15, 186-189. (Pubitemid 27061640)
21. Norgett, E. E., Golder, Z. J., Lorente-Cánovas, B., Ingham, N., Steel, K. P. and Karet Frankl, F. E. (2012). Atp6v0a4 knockout mouse is a model of distal renal tubular acidosis with hearing loss, with additional extrarenal phenotype. Proc. Natl. Acad. Sci. USA 109, 13775-13780.
22. Patuzzi, R. (2011). Ion flow in cochlear hair cells and the regulation of hearing sensitivity. Hear. Res. 280, 3-20.
23. Patuzzi, R. B., Yates, G. K. and Johnstone, B. M. (1989). Changes in cochlear microphonic and neural sensitivity produced by acoustic trauma. Hear. Res. 39, 189-202. (Pubitemid 19121520)
24. Rivas, A. and Francis, H. W. (2005). Inner ear abnormalities in a Kcnq1 (Kvlqt1) knockout mouse: a model of Jervell and Lange-Nielsen syndrome. Otol. Neurotol. 26, 415-424. (Pubitemid 40663867)
25. Salt, A. N. (2001). Regulation of endolymphatic fluid volume. Ann. N. Y. Acad. Sci. 942, 306-312. (Pubitemid 33022245)
26. Smith, A. N., Skaug, J., Choate, K. A., Nayir, A., Bakkaloglu, A., Ozen, S., Hulton, S. A., Sanjad, S. A., Al-Sabban, E. A., Lifton, R. P. et al. (2000). Mutations in ATP6N1B, encoding a new kidney vacuolar proton pump 116-kD subunit, cause recessive distal renal tubular acidosis with preserved hearing. Nat. Genet. 26, 388-389.
27. Steel, K. P. and Barkway, C. (1989). Another role for melanocytes: their importance for normal stria vascularis development in the mammalian inner ear. Development 107, 453-463. (Pubitemid 20006085)
28. Stover, E. H., Borthwick, K. J., Bavalia, C., Eady, N., Fritz, D. M., Rungroj, N., Giersch, A. B., Morton, C. C., Axon, P. R., Akil, I. et al. (2002). Novel ATP6V1B1 and ATP6V0A4 mutations in autosomal recessive distal renal tubular acidosis with new evidence for hearing loss. J. Med. Genet. 39, 796-803. (Pubitemid 35346947)
29. Takeuchi, S. and Ando, M. (1999). Voltage-dependent outward K (+) current in intermediate cell of stria vascularis of gerbil cochlea. Am. J. Physiol. 277, C91-C99. (Pubitemid 29352629)
30. Tasaki, I. and Spyropoulos, C. S. (1959). Stria vascularis as source of endocochlear potential. J. Neurophysiol. 22, 149-155.
31. Trowe, M. O., Maier, H., Petry, M., Schweizer, M., Schuster-Gossler, K. and Kispert, A. (2011). Impaired stria vascularis integrity upon loss of E-cadherin in basal cells. Dev. Biol. 359, 95-107.
32. Vargas-Poussou, R., Houillier, P., Le Pottier, N., Strompf, L., Loirat, C., Baudouin, V., Macher, M. A., Déchaux, M., Ulinski, T., Nobili, F. et al. (2006). Genetic investigation of autosomal recessive distal renal tubular acidosis: evidence for early sensorineural hearing loss associated with mutations in the ATP6V0A4 gene. J. Am. Soc. Nephrol. 17, 1437-1443. (Pubitemid 43673425)
33. Vidarsson, H., Westergren, R., Heglind, M., Blomqvist, S. R., Breton, S. and Enerbäck, S. (2009). The forkhead transcription factor Foxi1 is a master regulator of vacuolar H-ATPase proton pump subunits in the inner ear, kidney and epididymis. PLoS ONE 4, e4471.
34. Wangemann, P. (2002). K+ cycling and the endocochlear potential. Hear. Res. 165, 1-9.
35. Wangemann, P., Itza, E. M., Albrecht, B., Wu, T., Jabba, S. V., Maganti, R. J., Lee, J. H., Everett, L. A., Wall, S. M., Royaux, I. E. et al. (2004). Loss of KCNJ10 protein expression abolishes endocochlear potential and causes deafness in Pendred syndrome mouse model. BMC Med. 2, 30.
36. Wangemann, P., Nakaya, K., Wu, T., Maganti, R. J., Itza, E. M., Sanneman, J. D., Harbidge, D. G., Billings, S. and Marcus, D. C. (2007). Loss of cochlear HCO3-secretion causes deafness via endolymphatic acidification and inhibition of Ca2+ reabsorption in a Pendred syndrome mouse model. Am. J. Physiol. Renal Physiol. 292, F1345-F1353. (Pubitemid 46701861)