The role of potassium recirculation in cochlear amplification

Current Opinion in Otolaryngology and Head and Neck Surgery

Volumn 17, Issue 5, 2009, Pages 394-399

  Mistrik, Pavel ^a   Ashmore, Jonathan ^a,b  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Cochlea; Cochlear amplifier; Computational modeling; Endolymph; Gap junctions; Hair cells; Potassium; Stria vascularis; Transporters

Indexed keywords

POTASSIUM;

CELL EXPANSION; CELLULAR DISTRIBUTION; COCHLEA; CORTI ORGAN; HAIR CELL; HEARING LOSS; HUMAN; NONHUMAN; POTASSIUM TRANSPORT; PRIORITY JOURNAL; REVIEW;

ANIMALS; COCHLEA; COMPUTATIONAL BIOLOGY; GAP JUNCTIONS; HAIR CELLS, AUDITORY, OUTER; HEARING; HUMANS; OTOACOUSTIC EMISSIONS, SPONTANEOUS; POTASSIUM; STRIA VASCULARIS;

EID: 70349673748     PISSN: 10689508     EISSN: None     Source Type: Journal    
DOI: 10.1097/MOO.0b013e328330366f     Document Type: Review

References (54)

1. Steinbrecht RA. Ions and mucoid substances in sensory organs: microanalytical data from insect sensilla. Symp Soc Exp Biol 1989; 43:131-138.
2. Kharkovets T, Dedek K, Maier H, et al. Mice with altered KCNQ4 K+ channels implicate sensory outer hair cells in human progressive deafness. EMBO J 2006; 25:642-652. (Pubitemid 43237670)
3. Marcotti W, Johnson SL, Holley MC, Kros CJ. Developmental changes in the expression of potassium currents of embryonic, neonatal and mature mouse inner hair cells. J Physiol 2003; 548:383-400. (Pubitemid 36527462)
4. Dallos P. Cochlear amplification, outer hair cells and prestin. Curr Opin Neurobiol 2008; 18:370-376.
5. Ashmore J. Cochlear outer hair cell motility. Physiol Rev 2008; 88:173-210.
6. Hudspeth AJ. Making an effort to listen: mechanical amplification in the ear. Neuron 2008; 59:530-545.
7. 2+ current-driven nonlinear amplification by the mammalian cochlea in vitro. Nat Neurosci 2005; 8:149-155.
8. Martin P, Hudspeth AJ. Active hair-bundle movements can amplify a hair cell's response to oscillatory mechanical stimuli. Proc Natl Acad Sci U S A 1999; 96:14306-14311. (Pubitemid 30000646)
9. Brown SD, Hardisty-Hughes RE, Mburu P. Quiet as a mouse: dissecting the molecular and genetic basis of hearing. Nat Rev Genet 2008; 9:277-290. A comprehensive and up-to-date review of the gene mutations affecting cochlear function in mouse models of hearing and deafness.
10. Lang F, Vallon V, Knipper M, Wangemann P. Functional significance of channels and transporters expressed in the inner ear and kidney. Am J Physiol Cell Physiol 2007; 293:C1187-C1208. (Pubitemid 47558943)
11. Hibino H, Kurachi Y. Molecular and physiological bases of the K+ circulation in the mammalian inner ear. Physiology (Bethesda) 2006; 21:336-345. (Pubitemid 44511761)
12. Wangemann P. Supporting sensory transduction: cochlear fluid homeostasis and the endocochlear potential. J Physiol 2006; 576:11-21. (Pubitemid 44426214)
13. + currents in mature mouse inner hair cells. J Physiol 2004; 557:613-633.
14. Winter H, Bragg C, Zimmerman U, et al. Thyroid hormone receptor alpha1 is a critical regulator for the expression of ion channels during final differentiation of outer hair cells. Histochem Cell Biol 2007; 128:65-75. (Pubitemid 46986251)
15. Johnstone BM, Patuzzi R, Syka J, Sykova E. Stimulus-related potassium changes in the organ of Corti of guinea-pig. J Physiol 1989; 408:77-92. (Pubitemid 19040010)
16. Zidanic M, Brownell WE. Fine structure of the intracochlear potential field. I: The silent current. Biophys J 1990; 57:1253-1268.
17. Mountain DC, Cody AR. Multiple modes of inner hair cell stimulation. Hear Res 1999; 132:1-14. (Pubitemid 29261943)
18. Boettger T, Rust MB, Maier H, et al. Loss of K-Cl co-transporter KCC3 causes deafness, neurodegeneration and reduced seizure threshold. EMBO J 2003; 22:5422-5434. (Pubitemid 37279952)
19. Boettger T, Hubner CA, Maier H, et al. Deafness and renal tubular acidosis in mice lacking the K-Cl co-transporter Kcc4. Nature 2002; 416:874-878. (Pubitemid 34453746)
20. Jagger DJ, Forge A. Compartmentalized and signal-selective gap junctional coupling in the hearing cochlea. J Neurosci 2006; 26:1260-1268. (Pubitemid 43237058)
21. Cohen-Salmon M, Ott T, Michel V, et al. Targeted ablation of connexin26 in the inner ear epithelial gap junction network causes hearing impairment and cell death. Curr Biol 2002; 12:1106-1111. (Pubitemid 34766932)
22. Zhao HB, Yu N, Fleming CR. Gap junctional hemichannel-mediated ATP release and hearing controls in the inner ear. Proc Natl Acad Sci U S A 2005; 102:18724-18729. (Pubitemid 43011293)
23. 2+ propagation. Using imaging methods combined with focal delivery of ATP or photostimulation with caged IP(3), calcium signals are studied in organotypic cochlear cultures.
24. Teubner B, Michel V, Pesch J, et al. Connexin30 (Gjb6)-deficiency causes severe hearing impairment and lack of endocochlear potential. Hum Mol Genet 2003; 12:13-21. (Pubitemid 36097711)
25. Gow A, Davies C, Southwood CM, et al. Deafness in Claudin 11-null mice reveals the critical contribution of basal cell tight junctions to stria vascularis function. J Neurosci 2004; 24:7051-7062. (Pubitemid 39096371)
26. + diffusion potentials.
27. + transport proteins in the developing cochlear lateral wall of guinea pigs with hereditary deafness. Eur J Neurosci 2008; 27:145-154.
28. Cohen-Salmon M, Regnault B, Cayet N, et al. Connexin30 deficiency causes intrastrial fluid-blood barrier disruption within the cochlear stria vascularis. Proc Natl Acad Sci U S A 2007; 104:6229-6234. (Pubitemid 47186077)
29. Marcus DC, Wu T, Wangemann P, Kofuji P. KCNJ10 (Kir4.1) potassium channel knockout abolishes endocochlear potential. Am J Physiol Cell Physiol 2002; 282:C403-C407. (Pubitemid 34663200)
30. Wangemann P, Itza EM, Albrecht B, et al. Loss of KCNJ10 protein expression abolishes endocochlear potential and causes deafness in Pendred syndrome mouse model. BMC Med 2004; 2:30. (Pubitemid 40251702)
31. Rickheit G, Maier H, Strenzke N, et al. Endocochlear potential depends on Cl-channels: mechanism underlying deafness in Bartter syndrome IV. EMBO J 2008; 27:2907-2917. Identifies the role of barttin, a subunit of expressed ClC-Ka and ClC-Kb channels in the marginal cells of stria vascularis, as being essential for the generation of the endocochlear potential. Without this chloride return path, the reduction of endocochlear potential leads to deafness.
32. Knipper M, Claussen C, Ruttiger L, et al. Deafness in LIMP2-deficient mice due to early loss of the potassium channel KCNQ1/KCNE1 in marginal cells of the stria vascularis. J Physiol 2006; 576:73-86. (Pubitemid 44426222)
33. Yamasaki M, Komune S, Shimozono M, et al. Development of monovalent ions in the endolymph in mouse cochlea. ORL J Otorhinolaryngol Relat Spec 2000; 62:241-246. (Pubitemid 30759363)
34. Quraishi IH, Raphael RM. Generation of the endocochlear potential: a biophysical model. Biophys J 2008; 94:L64-L66. Develops a simple mathematical model of the generation of the endocochlear potential in stria vascularis. The model captures critical biophysical interactions between distinct stria vascularis compartments.
35. Russell IJ, Cody AR, Richardson GP. The responses of inner and outer hair cells in the basal turn of the guinea-pig cochlea and in the mouse cochlea grown in vitro. Hear Res 1986; 22:199-216.
36. Kemp DT. Otoacoustic emissions, their origin in cochlear function, and use. Br Med Bull 2002; 63:223-241.
37. Kharkovets T, Hardelin JP, Safieddine S, et al. KCNQ4, a K+ channel mutated in a form of dominant deafness, is expressed in the inner ear and the central auditory pathway. Proc Natl Acad Sci U S A 2000; 97:4333-4338. (Pubitemid 30226133)
38. Mustapha M, Fang Q, Gong TW, et al. Deafness and permanently reduced potassium channel gene expression and function in hypothyroid Pit1dw mutants. J Neurosci 2009; 29:1212-1223. An animal model of secondary hypothyroidism revealing novel defects of thyroid hormone deficiency related to deafness. The defects include impaired expression of KCNJ10 and KCNQ4 channels and sensory and strial cells deterioration all involved in K recirculation.
39. Hernandez VH, Bortolozzi M, Pertegato V, et al. Unitary permeability of gap junction channels to second messengers measured by FRET microscopy. Nat Methods 2007; 4:353-358. (Pubitemid 46772768)
40. Ortolano S, Di PG, Crispino G, et al. Coordinated control of connexin 26 and connexin 30 at the regulatory and functional level in the inner ear. Proc Natl Acad Sci U S A 2008; 105:18776-18781.
41. Nickel R, Forge A. Gap junctions and connexins in the inner ear: their roles in homeostasis and deafness. Curr Opin Otolaryngol Head Neck Surg 2008; 16:452-457.
42. Zhao HB, Kikuchi T, Ngezahayo A, White TW. Gap junctions and cochlear homeostasis. J Membr Biol 2006; 209:177-186.
43. Engel-Yeger B, Zaaroura S, Zlotogora J, et al. The effects of a connexin 26 mutation - 35delG - on oto-acoustic emissions and brainstem evoked potentials: homozygotes and carriers. Hear Res 2002; 163:93-100. (Pubitemid 34098845)
44. Morell RJ, Kim HJ, Hood LJ, et al. Mutations in the connexin 26 gene (GJB2) among Ashkenazi Jews with nonsyndromic recessive deafness. N Engl J Med 1998; 339:1500-1505. (Pubitemid 28543498)
45. + exhibits incomplete supporting cell maturation and a malformation of the spaces of Nuel.
46. Minekawa A, Narui Y, Inoshita A, et al. Cochlear outer hair cells in a dominant-negative Connexin26 mutant mouse preserved non-linear capacitance with impaired distortion product otoacoustic emission. Assoc Res Otolaryngol Abs 2009; 32:107.
47. Strelioff D. A computer simulation of the generation and distribution of cochlear potentials. J Acoust Soc Am 1973; 54:620-629.
48. Dallos P. Some electrical circuit properties of the organ of Corti. I: Analysis without reactive elements. Hear Res 1983; 12:89-119.
49. Mountain DC, Hubbard AE. A piezoelectric model of outer hair cell function. J Acoust Soc Am 1994; 95:350-354. (Pubitemid 24027832)
50. O'Beirne GA, Patuzzi RB. Mathematical model of outer hair cell regulation including ion transport and cell motility. Hear Res 2007; 234:29-51.
51. Mistrik P, Mullaley C, Mammano F, Ashmore J. Three-dimensional current flow in a large-scale model of the cochlea and the mechanism of amplification of sound. J R Soc Interface 2009; 6:279-291. An in-silico model of the cochlear partition, exploring the flow of current between different compartments when the cochlea is stimulated by sound. By including realistic physiological intercellular flow, the model also addresses the question of high-frequency attenuation of OHC receptor potentials.
52. Ramamoorthy S, Deo NV, Grosh K. A mechano-electro-acoustical model for the cochlea: response to acoustic stimuli. J Acoust Soc Am 2007; 121:2758-2773. (Pubitemid 46701274)
53. Mammano F, Ashmore JF. Differential expression of outer hair cell potassium currents in the isolated cochlea of the guinea-pig. J Physiol 1996; 496 (Pt 3):639-646. (Pubitemid 26387849)
54. Raybould NP, Jagger DJ, Housley GD. Positional analysis of guinea pig inner hair cell membrane conductances: implications for regulation of the membrane filter. J Assoc Res Otolaryngol 2001; 2:362-376.