The role of Pendrin in the development of the murine inner ear

Cellular Physiology and Biochemistry

Volumn 28, Issue 3, 2011, Pages 527-534

  Wangemann, Philine ^a  

^a KANSAS STATE UNIVERSITY   (United States)

Author keywords

Cochlea; Development; Endolymphatic sac; Enlarged vestibular aqueduct; Genetic disease model; Hearing; Slc26a

Indexed keywords

PENDRIN; POTASSIUM CHANNEL; POTASSIUM ION;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; CELL COMMUNICATION; COCHLEA; ENDOLYMPHATIC SAC; HAIR CELL; HEARING; HEARING LOSS; INNER EAR; MOUSE; NONHUMAN; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; VESTIBULE AQUEDUCT;

EID: 82255196404     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000335113     Document Type: Review

References (53)

1. Valvassori GE, Clemis JD: The large vestibular aqueduct syndrome. Laryngoscope 1978;88:723-728.
2. Arcand P, Desrosiers M, Dube J, Abela A: The large vestibular aqueduct syndrome and sensorineural hearing loss in the pediatric population. J Otolaryngol 1991;20:247-250.
3. Yuan Y, You Y, Huang D, Cui J, Wang Y, Wang Q, Yu F, Kang D, Yuan H, Han D, Dai P: Comprehensive molecular etiology analysis of nonsyndromic hearing impairment from typical areas in China. J Transl Med 2009;7:79.
4. Wu CC, Lu YC, Chen PJ, Yeh PL, Su YN, Hwu WL, Hsu CJ: Phenotypic analyses and mutation screening of the SLC26A4 and FOXI1 genes in 101 Taiwanese families with bilateral nonsyndromic enlarged vestibular aqueduct (DFNB4) or Pendred syndrome. Audiol Neurootol 2010;15:57-66.
5. Choi BY, Stewart AK, Madeo AC, Pryor SP, Lenhard S, Kittles R, Eisenman D, Jeffrey KH, Niparko J, Thomsen J, Arnos KS, Nance WE, King KA, Zalewski CK, Brewer CC, Shawker T, Reynolds JC, Butman JA, Karniski LP, Alper SL, Griffith AJ: Hypo-Functional SLC26A4 variants associated with nonsyndromic hearing loss and enlargement of the vestibular aqueduct: Genotype-phenotype correlation or coincidental polymorphisms? Hum Mutat 2009;30:599-608.
6. Pryor SP, Madeo AC, Reynolds JC, Sarlis NJ, Arnos KS, Nance WE, Yang Y, Zalewski CK, Brewer CC, Butman JA, Griffith AJ: SLC26A4/PDS genotypephenotype correlation in hearing loss with enlargement of the vestibular aqueduct (EVA): evidence that Pendred syndrome and non-syndromic EVA are distinct clinical and genetic entities. J Med Genet 2005;42:159-165. (Pubitemid 40204371)
7. Zhou G, Gopen Q: Characteristics of vestibular evoked myogenic potentials in children with enlarged vestibular aqueduct. Laryngoscope 2011;121:220-225.
8. Sugiura M, Sato E, Nakashima T, Sugiura J, Furuhashi A, Yoshino T, Nakayama A, Mori N, Murakami H, Naganawa S: Longterm follow-up in patients with Pendred syndrome: vestibular, auditory and other phenotypes. Eur Arch Otorhinolaryngol 2005;262:737-743. (Pubitemid 41428265)
9. Griffith AJ, Wangemann P: Hearing loss associated with enlargement of the vestibular aqueduct: Mechanistic insights from clinical phenotypes, genotypes, and mouse models. Hear Res 2011;in press.
10. Ito T, Choi BY, King KA, Zalewski CK, Muskett J, Chattaraj P, Shawker T, Reynolds JC, Butman JA, Brewer CC, Wangemann P, Alper SL, Griffith AJ: SLC26A4 genotypes and phenotypes associated with enlargement of the vestibular aqueduct. Cell Physiol Biochem 2011; in press.
11. Mansour SL, Schoenwolf GC: Morphogenesis of the inner ear, in Kelley MW, Wu D, Popper AN, Fay RR (eds): Springer Handbook of Auditory Research: Development of the inner ear. Springer New York, 2005, pp. 43-84.
12. Cheung CY, Brace RA: Amniotic fluid volume and composition in mouse pregnancy. J Soc Gynecol Investig 2005;12:558-562. (Pubitemid 41737719)
13. Kim HM, Wangemann P: Failure of fluid absorption in the endolymphatic sac initiates cochlear enlargement that leads to deafness in mice lacking pendrin expression. PLoS One 2010;5:e14041.
14. Wangemann P: Supporting sensory transduction: cochlear fluid homeostasis and the endocochlear potential. J Physiol 2006;576:11-21. (Pubitemid 44426214)
15. Anniko M, Wroblewski R: Elemental composition of the developing inner ear. Ann Otol Rhinol Laryngol 1981;90:25-32. (Pubitemid 11191782)
16. Cantos R, Cole LK, Acampora D, Simeone A, Wu DK: Patterning of the mammalian cochlea. Proc Natl Acad Sci USA 2000;97:11707-11713.
17. Geleoc GS, Holt JR: Developmental acquisition of sensory transduction in hair cells of the mouse inner ear. Nat Neurosci 2003;6:1019-1020. (Pubitemid 37186191)
18. Lelli A, Asai Y, Forge A, Holt JR, Geleoc GS: Tonotopic gradient in the developmental acquisition of sensory transduction in outer hair cells of the mouse cochlea. J Neurophysiol 2009;101:2961-2973.
19. Nordemar H: Postnatal development of the vestibular sensory epithelium in the mouse. Acta Otolaryngol 1983;96:447-456. (Pubitemid 13013916)
20. Desmadryl G, Sans A: Afferent innervation patterns in crista ampullaris of the mouse during ontogenesis. Brain Res Dev Brain Res 1990;52:183-189. (Pubitemid 20081076)
21. Steel KP, Barkway C: Another role for melanocytes: their importance for normal stria vascularis development in the mammalian inner ear. Development 1989;107:453-463. (Pubitemid 20006085)
22. Yamasaki M, Komune S, Shimozono M, Matsuda K, Haruta A: Development of monovalent ions in the endolymph in mouse cochlea. ORL J Otorhinolaryngol Relat Spec 2000;62:241-246.
23. Wangemann P, Nakaya K, Wu T, Maganti R, Itza EM, Sanneman J, Harbidge D, Billings S, Marcus DC: 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 2007;292:1345-1353.
24. Royaux IE, Wall SM, Karniski LP, Everett LA, Suzuki K, Knepper MA, Green ED: Pendrin, encoded by the Pendred syndrome gene, resides in the apical region of renal intercalated cells and mediates bicarbonate secretion. Proc Natl Acad Sci USA 2001;98:4221-4226. (Pubitemid 32249925)
25. Wangemann P, Itza EM, Albrecht B, Wu T, Jabba SV, Maganti RJ, Lee JH, Everett LA, Wall SM, Royaux IE, Green ED, Marcus DC: Loss of KCNJ10 protein expression abolishes endocochlear potential and causes deafness in Pendred syndrome mouse model. BMC Medicine 2004;2:30.
26. Dou H, Xu J, Wang Z, Smith AN, Soleimani M, Karet FE, Greinwald JH, Jr., Choo D: Co-expression of pendrin, vacuolar H+-ATPase alpha4-subunit and carbonic anhydrase II in epithelial cells of the murine endolymphatic sac. J Histochem Cytochem 2004;52:1377-1384. (Pubitemid 39362461)
27. Royaux IE, Belyantseva IA, Wu T, Kachar B, Everett LA, Marcus DC, Green ED: Localization and functional studies of pendrin in the mouse inner ear provide insight about the etiology of deafness in pendred syndrome. J Assoc Res Otolaryngol 2003;4:394-404. (Pubitemid 37187818)
28. Lee JH, Chiba T, Marcus DC: P2X2 receptor mediates stimulation of parasensory cation absorption by cochlear outer sulcus cells and vestibular transitional cells. J Neurosci 2001;21:9168-9174. (Pubitemid 33096860)
29. Kim SH, Marcus DC: Regulation of sodium transport in the inner ear. Hear Res 2011;280:21-29.
30. Kim HM, Wangemann P: Epithelial cell stretching and luminal acidification lead to a retarded development of stria vascularis and deafness in mice lacking pendrin. PLoS One 2011;6:e17949.
31. Nakaya K, Harbidge DG, Wangemann P, Schultz BD, Green E, Wall SM, Marcus DC: Lack of pendrin HCO3-transport elevates vestibular endolymphatic [Ca2+] by inhibition of acid-sensitive TRPV5 and TRPV6. Am J Physiol Renal Physiol 2007;292:1314-1321.
32. Everett LA, Belyantseva IA, Noben-Trauth K, Cantos R, Chen A, Thakkar SI, Hoogstraten-Miller SL, Kachar B, Wu DK, Green ED: Targeted disruption of mouse Pds provides insight about the inner-ear defects encountered in Pendred syndrome. Hum Mol Genet 2001;10:153-161. (Pubitemid 32098125)
33. Jabba SV, Oelke A, Singh R, Maganti RJ, Feming S, Wall SM, Everett LA, Green ED, Wangemann P: Macrophage invasion contributes to degeneration of stria vascularis in Pendred syndrome mouse model. BMC Med 2006;4:37.
34. Singh R, Wangemann P: Free radical stress mediated loss of Kcnj10 protein expression in stria vascularis contributes to deafness in Pendred syndrome mouse model. Am J Physiol Renal Physiol 2008;294:F139-F148
35. Wangemann P, Jabba SV, Singh R, Wu T, Oelke A, Gollapudi ASB, Marcus DC: Deafness in Pendred Syndrome is related to free radical stress in stria vascularis. Proc Meniere's Meeting 2005;5:36-41.
36. Wangemann P, Kim HM, Billings S, Nakaya K, Li X, Singh R, Sharlin DS, Forrest D, Marcus DC, Fong P: Developmental delays consistent with cochlear hypothyroidism contribute to failure to develop hearing in mice lacking Slc26a4/pendrin expression. Am J Physiol Renal Physiol 2009;297:F1435-F1447.
37. Dror AA, Politi Y, Shahin H, Lenz DR, Dossena S, Nofziger C, Fuchs H, Hrabe dA, Paulmichl M, Weiner S, Avraham KB: Calcium oxalate stone formation in the inner ear as a result of an Slc26a4 mutation. J Biol Chem 2010;285:21724-21735.
38. Lu YC, Wu CC, Shen WS, Yang TH, Yeh TH, Chen PJ, Yu IS, Lin SW, Wong JM, Chang Q, Lin X, Hsu CJ: Establishment of a Knock-In Mouse Model with the SLC26A4 c.919-2A〉G Mutation and Characterization of Its Pathology. PLoS One 2011;6:e22150.
39. Campos-Barros A, Amma LL, Faris JS, Shailam R, Kelley MW, Forrest D: Type 2 iodothyronine deiodinase expression in the cochlea before the onset of hearing. Proc Natl Acad Sci USA 2000;97:1287-1292. (Pubitemid 30080851)
40. 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)
41. Wangemann P: K+ cycling and the endocochlear potential. Hear Res 2002;165:1-9.
42. Wangemann P, Shen Z, Liu J: K+-induced stimulation of K+ secretion involves activation of the IsK channel in vestibular dark cells. Hear Res 1996;100:201-210. (Pubitemid 26359779)
43. Wangemann P, Liu J, Marcus DC: Ion transport mechanisms responsible for K+ secretion and the transepithelial voltage across marginal cells of stria vascularis in vitro. Hear Res 1995;84:19-29.
44. Unsold B, Kerst G, Brousos H, Hubner M, Schreiber R, Nitschke R, Greger R, Bleich M: KCNE1 reverses the response of the human K+ channel KCNQ1 to cytosolic pH changes and alters its pharmacology and sensitivity to temperature. Pflugers Arch 2000;441:368-378. (Pubitemid 32128179)
45. Suzuki H, Oshima A, Tsukamoto K, Abe S, Kumakawa K, Nagai K, Satoh H, Kanda Y, Iwasaki S, Usami S: Clinical characteristics and genotype-phenotype correlation of hearing loss patients with SLC26A4 mutations. Acta Otolaryngol 2007;127:1292-1297. (Pubitemid 350175286)
46. Cama E, Alemanno MS, Bellacchio E, Santarelli R, Carella M, Zelante L, Palladino T, Inches I, di Paola F, Arslan E, Melchionda S: Identification of a novel mutation in the SLC26A4 gene in an Italian with fluctuating sensorineural hearing loss. Int J Pediatr Otorhinolaryngol 2009;73:1458-1463.
47. Kitamura K, Takahashi K, Noguchi Y, Kuroishikawa Y, Tamagawa Y, Ishikawa K, Ichimura K, Hagiwara H: Mutations of the Pendred syndrome gene (PDS) in patients with large vestibular aqueduct. Acta Otolaryngol 2000;120:137-141.
48. Yamauchi D, Nakaya K, Raveendran NN, Harbidge DG, Singh R, Wangemann P, Marcus DC: Expression of epithelial calcium transport system in rat cochlea and vestibular labyrinth. BMC Physiol 2010;10:1.
49. Barone S, Amlal H, Xu J, Soleimani M: Deletion of the Cl-/HCO3-exchanger pendrin downregulates calcium-absorbing proteins in the kidney and causes calcium wasting. Nephrol Dial Transplant 2011; in press.
50. Hulander M, Kiernan AE, Blomqvist SR, Carlsson P, Samuelsson EJ, Johansson BR, Steel KP, Enerback S: Lack of pendrin expression leads to deafness and expansion of the endolymphatic compartment in inner ears of Foxi1 null mutant mice. Development 2003;130:2013-2025. (Pubitemid 36575925)
51. Hulander M, Wurst W, Carlsson P, Enerback S: The winged helix transcription factor Fkh10 is required for normal development of the inner ear. Nat Genet 1998;20:374-376. (Pubitemid 28541637)
52. Sajan SA, Warchol ME, Lovett M: Toward a systems biology of mouse inner ear organogenesis: gene expression pathways, patterns and network analysis. Genetics 2007;177:631-653. (Pubitemid 47555877)
53. Choi BY, Kim HM, Ito T, Lee KY, Li Z, Monahan K, Wen Y, Wilson E, Kurima K, Saunder TL, Petralia RS, Wangemann P, Friedman TB, Griffith AJ: Mouse model of enlarged vestibular aqueducts defines temporal requirement of Slc26a4 expression for hearing acquisition. J Clin Invest 2011; in press.