Mouse models for pendrin-associated loss of cochlear and vestibular function

Cellular Physiology and Biochemistry

Volumn 32, Issue , 2013, Pages 157-165

  Wangemann, Philine ^a  

^a KANSAS STATE UNIVERSITY   (United States)

Author keywords

Cochlea; Endolymphatic sac; Enlarged vestibular aqueduct; Genetic disease model; Hearing; Slc26a4

Indexed keywords

PENDRIN;

ACIDIFICATION; COCHLEA; COCHLEA POTENTIAL; ENDOLYMPHATIC SAC; HEARING; INNER EAR; INNER EAR DISEASE; NITRATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; POINT MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; VESTIBULAR DISORDER; VESTIBULAR FUNCTION; VESTIBULAR LABYRINTH;

ANIMALS; ANION TRANSPORT PROTEINS; COCHLEA; COCHLEAR DISEASES; DISEASE MODELS, ANIMAL; HUMANS; MICE; VESTIBULAR DISEASES; VESTIBULAR FUNCTION TESTS;

EID: 84892947302     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000356635     Document Type: Review

References (53)

1. Soleimani M, Greeley T, Petrovic S, Wang Z, Amlal H, Kopp P, Burnham CE: Pendrin: an apical Cl-/OH-/HCO3-Exchanger in the Kidney Cortex. Am J Physiol Renal Physiol 2001;280:F356-F364.
2. Scott DA, Karniski LP: Human pendrin expressed in Xenopus laevis oocytes mediates chloride/formate exchange. Am J Physiol Cell Physiol 2000;278:C207-C211.
3. Scott DA, Wang R, Kreman TM, Sheffield VC, Karniski LP: The Pendred syndrome gene encodes a chlorideiodide transport protein. Nat Genet 1999;21:440-443.
4. 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 U S A 2001;98:4221-4226.
5. Royaux IE, Suzuki K, Mori A, Katoh R, Everett LA, Kohn LD, Green ED: Pendrin, the protein encoded by the Pendred syndrome gene (PDS), is an apical porter of iodide in the thyroid and is regulated by thyroglobulin in FRTL-5 cells. Endocrinology 2000;141:839-845.
6. 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
7. Nakao I, Kanaji S, Ohta S, Matsushita H, Arima K, Yuyama N, Yamaya M, Nakayama K, Kubo H, Watanabe M, Sagara H, Sugiyama K, Tanaka H, Toda S, Hayashi H, Inoue H, Hoshino T, Shiraki A, Inoue M, Suzuki K, Aizawa H, Okinami S, Nagai H, Hasegawa M, Fukuda T, Green ED, Izuhara K: Identification of pendrin as a common mediator for mucus production in bronchial asthma and chronic obstructive pulmonary disease. J Immunol 2008;180:6262-6269.
8. Bidart JM, Lacroix L, Evain-Brion D, Caillou B, Lazar V, Frydman R, Bellet D, Filetti S, Schlumberger M: Expression of Na+/I-symporter and Pendred syndrome genes in trophoblast cells. J Clin Endocrinol Metab 2000;85:4367-4372.
9. Rillema JA, Hill MA: Prolactin regulation of the pendrin-iodide transporter in the mammary gland. Am J Physiol Endocrinol Metab 2003;284:E25-E28
10. Alesutan I, Daryadel A, Mohebbi N, Pelzl L, Leibrock C, Voelkl J, Bourgeois S, Dossena S, Nofziger C, Paulmichl M, Wagner CA, Lang F: Impact of bicarbonate, ammonium chloride, and acetazolamide on hepatic and renal SLC26A4 expression. Cell Physiol Biochem 2011;28:553-558.
11. 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.
12. Pryor SP, Madeo AC, Reynolds JC, Sarlis NJ, Arnos KS, Nance WE, Yang Y, Zalewski CK, Brewer CC, Butman JA, Griffith AJ: SLC26A4/PDS genotype-phenotype 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.
13. Zhou G, Gopen Q: Characteristics of vestibular evoked myogenic potentials in children with enlarged vestibular aqueduct. Laryngoscope 2011;121:220-225.
14. Sugiura M, Sato E, Nakashima T, Sugiura J, Furuhashi A, Yoshino T, Nakayama A, Mori N, Murakami H, Naganawa S: Long-term follow-up in patients with Pendred syndrome: vestibular, auditory and other phenotypes. Eur Arch Otorhinolaryngol 2005;262:737-743.
15. 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.
16. Abe S, Usami S, Hoover DM, Cohn E, Shinkawa H, Kimberling WJ: Fluctuating sensorineural hearing loss associated with enlarged vestibular aqueduct maps to 7q31, the region containing the Pendred gene. Am J Med Genet 1999;82:322-328.
17. Fraser GR: Association of congenital deafness with goitre (Pendred's syndrome) a study of 207 families. Ann Hum Genet 1965;28. 201-249.
18. 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.
19. Park HJ, Shaukat S, Liu XZ, Hahn SH, Naz S, Ghosh M, Kim HN, Moon SK, Abe S, Tukamoto K, Riazuddin S, Kabra M, Erdenetungalag R, Radnaabazar J, Khan S, Pandya A, Usami SI, Nance WE, Wilcox ER, Riazuddin S, Griffith AJ: Origins and frequencies of SLC26A4 (PDS) mutations in east and south Asians: global implications for the epidemiology of deafness. J Med Genet 2003;40:242-248.
20. 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;281:11-17.
21. 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;28:545-552.
22. Ito T, Muskett J, Chattaraj P, Choi BY, Lee KY, Zalewski C, King KA, Li X, Wangemann P, Shawker T, Brewer CC, Alper SL, Griffith AJ: SLC26A4 mutation testing for hearing loss associated with enlargement of the vestibular aqueduct. World J Otorhinolaryngology 2013;3:26-34.
23. 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 2005, pp. 43-84.
24. Cheung CY, Brace RA: Amniotic fluid volume and composition in mouse pregnancy. J Soc Gynecol Investig 2005;12;558-562.
25. 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-.
26. Li X, Zhou F, Marcus DC, Wangemann P: Endolymphatic Na+ and K+ concentrations during cochlear growth and enlargement in mice lacking Slc26a4/pendrin. PLoS One 2013;8:e65977
27. Cantos R, Cole LK, Acampora D, Simeone A, Wu DK: Patterning of the mammalian cochlea. Proc Natl Acad Sci U S A 2000;97:11707-11713.
28. Geleoc GS, Holt JR: Developmental acquisition of sensory transduction in hair cells of the mouse inner ear. Nat Neurosci 2003;6:1019-1020.
29. 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.
30. Nordemar H: Postnatal development of the vestibular sensory epithelium in the mouse. Acta Otolaryngol 1983;96:447-456.
31. Desmadryl G, Sans A: Afferent innervation patterns in crista ampullaris of the mouse during ontogenesis. Brain Res Dev Brain Res 1990;52:183-189.
32. 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.
33. 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.
34. 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.
35. Wangemann P: Supporting sensory transduction: cochlear fluid homeostasis and the endocochlear potential. J Physiol 2006;576:11-21.
36. 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.
37. 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.
38. 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.
39. 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.
40. 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.
41. 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
42. 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.
43. 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
44. 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-.
45. 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.
46. 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.
47. 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.
48. 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
49. 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.
50. 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.
51. 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.
52. Li X, Sanneman JD, Harbidge DG, Zhou F, Ito T, Nelson R, Picard N, Chambrey R, Eladari D, Miesner T, Griffith AJ, Marcus DC, Wangemann P: SLC26A4 targeted to the endolymphatic sac rescues hearing and balance in Slc26a4 mutant mice. PLoS Genet 2013;9:e1003641.
53. Choi BY, Kim HM, Ito T, Lee KY, Li X, Monahan K, Wen Y, Wilson E, Kurima K, Saunders 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;121:4516-4525.