The subcellular distribution of aquaporin 5 in the cochlea reveals a water shunt at the perilymph-endolymph barrier

Neuroscience

Volumn 168, Issue 4, 2010, Pages 957-970

  Hirt, B ^a,b   Penkova, Z H ^c   Eckhard, A ^a,b   Liu, W ^d   Rask Andersen, H ^d   Muller M ^a   Lowenheim H ^a  

^a UNIVERSITY HOSPITAL TÜBINGEN   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c TRAKIA UNIVERSITY   (Bulgaria)

^d UPPSALA UNIVERSITY HOSPITAL   (Sweden)

Author keywords

Aquaporin 5; Cochlea; Endolymph homeostasis; Endolymphatic hydrops; Human; Sj gren's syndrome

Indexed keywords

AQUAPORIN 4; AQUAPORIN 5; AQP5 PROTEIN, HUMAN; AQP5 PROTEIN, MOUSE; AQP5 PROTEIN, RAT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; APICAL MEMBRANE; ARTICLE; CELL MEMBRANE; CELL POLARITY; CELL TYPE; CELLULAR DISTRIBUTION; COCHLEA; COCHLEA DUCT; CONTROLLED STUDY; ENDOLYMPH AND PERILYMPH; EPITHELIUM CELL; HUMAN; HUMAN TISSUE; MENIERE DISEASE; MOUSE; NONHUMAN; PERCEPTION DEAFNESS; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN DEFECT; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; REGULATORY MECHANISM; SJOEGREN SYNDROME; WATER TRANSPORT; ANIMAL; CELL FRACTIONATION; ENDOLYMPH; EPITHELIUM; FEMALE; GERBIL; GROWTH, DEVELOPMENT AND AGING; GUINEA PIG; MALE; METABOLISM; MIDDLE AGED; NEWBORN; PERILYMPH; SPECIES DIFFERENCE;

ANIMALS; ANIMALS, NEWBORN; AQUAPORIN 5; CELL MEMBRANE; COCHLEA; ENDOLYMPH; EPITHELIUM; FEMALE; GERBILLINAE; GUINEA PIGS; HUMANS; MALE; MICE; MIDDLE AGED; PERILYMPH; RATS; SPECIES SPECIFICITY; SUBCELLULAR FRACTIONS;

EID: 77953684283     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2009.09.002     Document Type: Article

References (71)

1. Bacman S., Sterin-Borda L., Camusso J.J., Arana R., Hubscher O., Borda E. Circulating antibodies against rat parotid gland M3 muscarinic receptors in primary Sjogren's syndrome. Clin Exp Immunol 1996, 104:454-459.
2. Boki K.A., Ioannidis J.P., Segas J.V., Maragkoudakis P.V., Petrou D., Adamopoulos G.K., Moutsopoulos H.M. How significant is sensorineural hearing loss in primary Sjogren's syndrome?. An individually matched case-control study. J Rheumatol 2001, 28:798-801.
3. Bondy C., Chin E., Smith B.L., Preston G.M., Agre P. Developmental gene expression and tissue distribution of the CHIP28 water-channel protein. Proc Natl Acad Sci U S A 1993, 90:4500-4504.
4. Bosher S.K., Warren R.L. A study of the electrochemistry and osmotic relationships of the cochlear fluids in the neonatal rat at the time of the development of the endocochlear potential. J Physiol 1971, 212:739-761.
5. Burghardt B., Nielsen S., Steward M.C. The role of aquaporin water channels in fluid secretion by the exocrine pancreas. J Membr Biol 2006, 210:143-153.
6. Chiba T., Marcus D.C. Basolateral K+ conductance establishes driving force for cation absorption by outer sulcus epithelial cells. J Membr Biol 2001, 184:101-112.
7. Doi K., Mori N., Matsunaga T. Effects of adenylate cyclase activation on electrical resistance of scala media. Acta Otolaryngol Suppl 1993, 501:76-79.
8. Freeman S.R., Sheehan P.Z., Thorpe M.A., Rutka J.A. Ear, nose, and throat manifestations of Sjogren's syndrome: retrospective review of a multidisciplinary clinic. J Otolaryngol 2005, 34:20-24.
9. Gautam D., Heard T.S., Cui Y., Miller G., Bloodworth L., Wess J. Cholinergic stimulation of salivary secretion studied with M1 and M3 muscarinic receptor single- and double-knockout mice. Mol Pharmacol 2004, 66:260-267.
10. Gresz V., Kwon T.H., Gong H., Agre P., Steward M.C., King L.S., Nielsen S. Immunolocalization of AQP-5 in rat parotid and submandibular salivary glands after stimulation or inhibition of secretion in vivo. Am J Physiol Gastrointest Liver Physiol 2004, 287:G151-G161.
11. Gresz V., Kwon T.H., Hurley P.T., Varga G., Zelles T., Nielsen S., Case R.M., Steward M.C. Identification and localization of aquaporin water channels in human salivary glands. Am J Physiol Gastrointest Liver Physiol 2001, 281:G247-G254.
12. Hallpike C., Cairns H. Observations on the pathology of Meniere's syndrome. J Laryngol Otol 1938, 53:625-655.
13. Hamann S., Zeuthen T., La Cour M., Nagelhus E.A., Ottersen O.P., Agre P., Nielsen S. Aquaporins in complex tissues: distribution of aquaporins 1-5 in human and rat eye. Am J Physiol 1998, 274:C1332-C1345.
14. Huang D., Chen P., Chen S., Nagura M., Lim D.J., Lin X. Expression patterns of aquaporins in the inner ear: evidence for concerted actions of multiple types of aquaporins to facilitate water transport in the cochlea. Hear Res 2002, 165:85-95.
15. Ishida N., Hirai S.I., Mita S. Immunolocalization of aquaporin homologs in mouse lacrimal glands. Biochem Biophys Res Commun 1997, 238:891-895.
16. Ishikawa Y., Skowronski M.T., Ishida H. Persistent increase in the amount of aquaporin-5 in the apical plasma membrane of rat parotid acinar cells induced by a muscarinic agonist SNI-2011. FEBS Lett 2000, 477:253-257.
17. Ishikawa Y., Yuan Z., Inoue N., Skowronski M.T., Nakae Y., Shono M., Cho G., Yasui M., Agre P., Nielsen S. Identification of AQP5 in lipid rafts and its translocation to apical membranes by activation of M3 mAChRs in interlobular ducts of rat parotid gland. Am J Physiol Cell Physiol 2005, 289:C1303-C1311.
18. Ito S., Fisch U., Dillier N., Pollak A. Endolymphatic pressure in experimental hydrops. Arch Otolaryngol Head Neck Surg 1987, 113:833-835.
19. Jahnke K. The fine structure of freeze-fractured intercellular junctions in the guinea pig inner ear. Acta Otolaryngol Suppl 1975, 336:1-40.
20. Kassan S.S., Moutsopoulos H.M. Clinical manifestations and early diagnosis of Sjogren syndrome. Arch Intern Med 2004, 164:1275-1284.
21. Khan K.M., Drescher M.J., Hatfield J.S., Khan A.M., Drescher D.G. Muscarinic receptor subtypes are differentially distributed in the rat cochlea. Neuroscience 2002, 111:291-302.
22. Kim S.H., Kim K.X., Raveendran N.N., Wu T., Pondugula S.R., Marcus D.C. Regulation of ENaC-mediated sodium transport by glucocorticoids in Reissner's membrane epithelium. Am J Physiol Cell Physiol 2009, 296:C544-C557.
23. Kimura R.S., Schuknecht H.F. Membranous hydrops in the inner ear of the guinea pig after obliteration of the endolymphatic sac. Pract Otorhinolaryngol 1965, 27:343-354.
24. King L.S., Kozono D., Agre P. From structure to disease: the evolving tale of aquaporin biology. Nat Rev Mol Cell Biol 2004, 5:687-698.
25. King L.S., Nielsen S., Agre P. Aquaporins in complex tissues. I. Developmental patterns in respiratory and glandular tissues of rat. Am J Physiol 1997, 273:C1541-C1548.
26. Konishi T., Hamrick P.E. Ion transport in the cochlea of guinea pig. II. Chloride transport. Acta Otolaryngol 1978, 86:176-184.
27. Konishi T., Hamrick P.E., Mori H. Water permeability of the endolymph-perilymph barrier in the guinea pig cochlea. Hear Res 1984, 15:51-58.
28. Konishi T., Hamrick P.E., Walsh P.J. Ion transport in guinea pig cochlea. I. Potassium and sodium transport. Acta Otolaryngol 1978, 86:22-34.
29. Konishi T., Salt A.N., Hamrick P.E. Effects of exposure to noise on ion movement in guinea pig cochlea. Hear Res 1979, 1:325-342.
30. Krane C.M., Melvin J.E., Nguyen H.V., Richardson L., Towne J.E., Doetschman T., Menon A.G. Salivary acinar cells from aquaporin 5-deficient mice have decreased membrane water permeability and altered cell volume regulation. J Biol Chem 2001, 276:23413-23420.
31. 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.
32. Lee J.H., Marcus D.C. Endolymphatic sodium homeostasis by Reissner's membrane. Neuroscience 2003, 119:3-8.
33. Li J., Ha Y.M., Ku N.Y., Choi S.Y., Lee S.J., Oh S.B., Kim J.S., Lee J.H., Lee E.B., Song Y.W., Park K. Inhibitory effects of autoantibodies on the muscarinic receptors in Sjogren's syndrome. Lab Invest 2004, 84:1430-1438.
34. Li J., Verkman A.S. Impaired hearing in mice lacking aquaporin-4 water channels. J Biol Chem 2001, 276:31233-31237.
35. Lopez I.A., Ishiyama G., Lee M., Baloh R.W., Ishiyama A. Immunohistochemical localization of aquaporins in the human inner ear. Cell Tissue Res 2007, 328:453-460.
36. Lundquist P.G. Aspects on endolymphatic sac morphology and function. Arch Otorhinolaryngol 1976, 212:231-240.
37. Ma T., Song Y., Gillespie A., Carlson E.J., Epstein C.J., Verkman A.S. Defective secretion of saliva in transgenic mice lacking aquaporin-5 water channels. J Biol Chem 1999, 274:20071-20074.
38. Matsuzaki T., Suzuki T., Koyama H., Tanaka S., Takata K. Aquaporin-5 (AQP5), a water channel protein, in the rat salivary and lacrimal glands: immunolocalization and effect of secretory stimulation. Cell Tissue Res 1999, 295:513-521.
39. Menière P. Mémoire sur des lésions de l'oreille interne donnant lieu à des symptomes de congestion cérébrale apoplectiforme. Gaz Med de Paris 1861, 16:597-601.
40. Merves M., Krane C.M., Dou H., Greinwald J.H., Menon A.G., Choo D. Expression of aquaporin 1 and 5 in the developing mouse inner ear and audiovestibular assessment of an Aqp5 null mutant. J Assoc Res Otolaryngol 2003, 4:264-275.
41. Mhatre A.N., Jero J., Chiappini I., Bolasco G., Barbara M., Lalwani A.K. Aquaporin-2 expression in the mammalian cochlea and investigation of its role in Meniere's disease. Hear Res 2002, 170:59-69.
42. Mhatre A.N., Steinbach S., Hribar K., Hoque A.T., Lalwani A.K. Identification of aquaporin 5 (AQP5) within the cochlea: cDNA cloning and in situ localization. Biochem Biophys Res Commun 1999, 264:157-162.
43. Miyabe Y., Kikuchi T., Kobayashi T. Comparative immunohistochemical localizations of aquaporin-1 and aquaporin-4 in the cochleae of three different species of rodents. Tohoku J Exp Med 2002, 196:247-257.
44. Moore M., Ma T., Yang B., Verkman A.S. Tear secretion by lacrimal glands in transgenic mice lacking water channels AQP1, AQP3, AQP4 and AQP5. Exp Eye Res 2000, 70:557-562.
45. Müller M. Developmental changes of frequency representation in the rat cochlea. Hear Res 1991, 56:1-7.
46. Müller M. The cochlear place-frequency map of the adult and developing Mongolian gerbil. Hear Res 1996, 94:148-156.
47. Müller M., von Hunerbein K., Hoidis S., Smolders J.W. A physiological place-frequency map of the cochlea in the CBA/J mouse. Hear Res 2005, 202:63-73.
48. Nakamura M., Tada Y., Akaishi T., Nakata K. M3 muscarinic receptor mediates regulation of protein secretion in rabbit lacrimal gland. Curr Eye Res 1997, 16:614-619.
49. Nakamura T., Matsui M., Uchida K., Futatsugi A., Kusakawa S., Matsumoto N., Nakamura K., Manabe T., Taketo M.M., Mikoshiba K. M(3) muscarinic acetylcholine receptor plays a critical role in parasympathetic control of salivation in mice. J Physiol 2004, 558:561-575.
50. Nielsen S., King L.S., Christensen B.M., Agre P. Aquaporins in complex tissues. II. Subcellular distribution in respiratory and glandular tissues of rat. Am J Physiol 1997, 273:C1549-C1561.
51. Rask-Andersen H., DeMott J.E., Bagger-Sjoback D., Salt A.N. Morphological changes of the endolymphatic sac induced by microinjection of artificial endolymph into the cochlea. Hear Res 1999, 138:81-90.
52. Rybak L.P., Whitworth C., Scott V. Development of endocochlear potential and compound action potential in the rat. Hear Res 1992, 59:189-194.
53. Salt A.N., DeMott J.E. Endolymph volume changes during osmotic dehydration measured by two marker techniques. Hear Res 1995, 90:12-23.
54. Salt A.N., DeMott J. Longitudinal endolymph flow associated with acute volume increase in the guinea pig cochlea. Hear Res 1997, 107:29-40.
55. Sawada S., Takeda T., Kitano H., Takeuchi S., Okada T., Ando M., Suzuki M., Kakigi A. Aquaporin-1 (AQP1) is expressed in the stria vascularis of rat cochlea. Hear Res 2003, 181:15-19.
56. Shin K., Fogg V.C., Margolis B. Tight junctions and cell polarity. Annu Rev Cell Dev Biol 2006, 22:207-235.
57. Spicer S.S., Schulte B.A. The fine structure of spiral ligament cells relates to ion return to the stria and varies with place-frequency. Hear Res 1996, 100:80-100.
58. Stankovic K.M., Adams J.C., Brown D. Immunolocalization of aquaporin CHIP in the guinea pig inner ear. Am J Physiol 1995, 269:C1450-C1456.
59. Steinfeld S., Cogan E., King L.S., Agre P., Kiss R., Delporte C. Abnormal distribution of aquaporin-5 water channel protein in salivary glands from Sjogren's syndrome patients. Lab Invest 2001, 81:143-148.
60. Sterkers O., Ferrary E., Amiel C. Inter- and intracompartmental osmotic gradients within the rat cochlea. Am J Physiol 1984, 247:F602-F606.
61. Sterkers O., Saumon G., Tran Ba Huy P., Amiel C. K, Cl, and H2O entry in endolymph, perilymph, and cerebrospinal fluid of the rat. Am J Physiol 1982, 243:F173-F180.
62. Takumi Y., Nagelhus E.A., Eidet J., Matsubara A., Usami S., Shinkawa H., Nielsen S., Ottersen O.P. Select types of supporting cell in the inner ear express aquaporin-4 water channel protein. Eur J Neurosci 1998, 10:3584-3595.
63. Tsubota K., Hirai S., King L.S., Agre P., Ishida N. Defective cellular trafficking of lacrimal gland aquaporin-5 in Sjogren's syndrome. Lancet 2001, 357:688-689.
64. Tsuji J., Liberman M.C. Intracellular labeling of auditory nerve fibers in guinea pig: central and peripheral projections. J Comp Neurol 1997, 381:188-202.
65. Tumiati B., Casoli P., Parmeggiani A. Hearing loss in the Sjogren syndrome. Ann Intern Med 1997, 126:450-453.
66. Vetter D.E., Mann J.R., Wangemann P., Liu J., McLaughlin K.J., Lesage F., Marcus D.C., Lazdunski M., Heinemann S.F., Barhanin J. Inner ear defects induced by null mutation of the isk gene. Neuron 1996, 17:1251-1264.
67. Wangemann P. Supporting sensory transduction: cochlear fluid homeostasis and the endocochlear potential. J Physiol 2006, 576:11-21.
68. Yamakawa K. Über die pathologische Veränderung bei einem Meniere-Kranken. J Otorhinolaryngol Soc Jpn 1938, 5:159-165.
69. Yoshida M., Lowry L.D. Hydrostatic pressure measurement of endolymph and perilymph in the guinea pig cochlea. Am J Otolaryngol 1984, 5:159-165.
70. Ziavra N., Politi E.N., Kastanioudakis I., Skevas A., Drosos A.A. Hearing loss in Sjogren's syndrome patients: a comparative study. Clin Exp Rheumatol 2000, 18:725-728.
71. Zidanic M., Brownell W.E. Fine structure of the intracochlear potential field. I. The silent current. Biophys J 1990, 57:1253-1268.