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Aquaporins and CFTR in Ocular Epithelial Fluid Transport

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Abstract

Aquaporins (AQPs) and the cystic fibrosis transmembrane conductance regulator (CFTR) provide the molecular routes for transport of water and chloride, respectively, through many epithelial tissues. In ocular epithelia, fluid transport generally involves secondary active chloride transport, which creates the osmotic gradient to drive transepithelial water transport. This review is focused on the role of AQPs and CFTR in water and ion transport across corneal/conjunctival epithelia, corneal endothelium, ciliary epithelium, and retinal pigment epithelium. The potential relevance of water and chloride transport to common disorders of ocular fluid balance is also considered. Recent data suggest AQPs and CFTR as attractive targets for drug development for therapy of keratoconjunctivitis sicca, recurrent corneal erosions, corneal edema, glaucoma, retinal detachment, and retinal ischemia.

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References

  • Agre P., Kozono D. 2003. Aquaporin water channels: molecular mechanisms for human diseases. FEBS Lett. 27:72–78

    Article  CAS  Google Scholar 

  • Al-Nakkash L., Reinach P.S. 2001. Activation of a CFTR-mediated chloride current in a rabbit corneal epithelial cell line. Invest. Ophthalmol. Vis. Sci. 42:2364–2370

    PubMed  CAS  Google Scholar 

  • Ansari E.A., Sahni K., Etherington C., Morton A., Conway S.P, Moya E., Littlewood J.M. 1999. Ocular signs and symptoms and vitamin A status in patients with cystic fibrosis treated with daily vitamin A supplements. Br. J. Ophthalmol. 83:688–691

    Article  PubMed  CAS  Google Scholar 

  • Blaug S., Quinn R., Quong J., Jalickee S., Miller S.S. 2003. Retinal pigment epithelial function: a role for CFTR? Doc. Ophthalmol. 106:43–50

    Google Scholar 

  • Bonanno J.A. 2003. Identity and regulation of ion transport mechanisms in the corneal endothelium. Prog. Retin. Eye Res. 22:69–94

    Article  PubMed  CAS  Google Scholar 

  • Botelho S.Y., Goldstein A.M, Rosenlund M.L. 1973. Tear sodium, potassium, chloride, and calcium at various flow rates: children with cystic fibrosis and unaffected siblings with and without corneal staining. 1973. J. Pediatr. 83:601–606

    Google Scholar 

  • Bringmann A., Uckermann O., Pannicke T., Iandiev I., Reichenbach A., Wiedemann P. 2005. Neuronal versus glial cell swelling in the ischaemic retina. Acta. Ophth. Scand. 83:528–538

    Article  Google Scholar 

  • Candia O.A. 2004. Electrolyte and fluid transport across corneal, conjunctival, and lens epithelia. Exp. Eye Res. 78: 527–535

    Article  PubMed  CAS  Google Scholar 

  • Chakravarti S., Wu F., Vij N., Roberts L., Joyce S. 2004. Microarray studies reveal macrophage-like function of stromal keratocytes in the cornea. Invest. Ophthalmol. Vis. Sci. 45:3475–3484

    Article  PubMed  Google Scholar 

  • Connors N.C., Kofuji P. 2006. Potassium channel Kir4.1 macromolecular complex in retinal glial cells. Glia. 53:124–131

    Article  PubMed  Google Scholar 

  • Da T., Verkman A.S. 2004. Aquaporin-4 gene disruption in mice protects against impaired retinal function and cell death after ischemia. Invest. Ophthalmol. Vis. Sci. 45:4477–4483

    Article  PubMed  Google Scholar 

  • Dartt D.A. 2002. Regulation of mucin and fluid secretion by conjunctival epithelial cells. Prog. Retin. Eye Res. 21:555–576

    Article  PubMed  CAS  Google Scholar 

  • Do C.W., Kong C.W., To C.H. 2004. cAMP inhibits transepithelial chloride secretion across bovine ciliary body epithelium. Invest. Ophthalmol. Vis. Sci. 45:3638–3643

    Article  PubMed  Google Scholar 

  • Do C.W., Civan M.M. 2004. Basis of chloride transport in ciliary epithelium. J. Membrane. Biol. 200:1–13

    Article  CAS  Google Scholar 

  • Fischbarg J. 2003. On the mechanism of fluid transport across corneal endothelium and epithelia in general. J. Exp. Zoolog. A. Comp. Exp. Biol. 300:30–40

    Article  PubMed  CAS  Google Scholar 

  • Fischbarg J., Diecke F.P. 2005. A mathematical model of electrolyte and fluid transport across corneal endothelium. J. Membrane. Biol. 203:41–56

    Article  CAS  Google Scholar 

  • Fischbarg J., Motoreano R. 1982. Osmotic permeabilities across corneal endothelium and antidiuretic hormone-stimulated toad urinary bladder structure. Biochim. Biophys. Acta. 690:207–214

    Article  PubMed  CAS  Google Scholar 

  • Freegard T.J. 1997. The physical basis of transparency of the normal cornea. Eye. 11:465–471

    PubMed  Google Scholar 

  • Frigeri A., Gropper M., Turck C.W., Verkman A.S. 1995. Immunolocalization of the mercurial-insensitive water channel and glycerol intrinsic protein in epithelial cell plasma membranes. Proc. Natl. Acad. Sci. USA 92:4328–4331

    Article  PubMed  CAS  Google Scholar 

  • Gallemore R.P., Hughes B.A., Miller S.S. 1997. Retinal pigment epithelial transport mechanisms and their contribution to the electroretinogram. Prog. Retinal Eye Res. 16:609–566

    Google Scholar 

  • Gilbard J.P. 1994. Treatment of keratoconjunctivitis sicca in rabbits with 3-isobutyl-1-methylxanthine. Arch. Ophthalmol. 112:1614–1616

    PubMed  CAS  Google Scholar 

  • Gilbard J.P., Rossi S.R., Heyda K.G., Dartt D.A. 1991. Stimulation of tear secretion and treatment of dry-eye disease with 3-isobutyl-1-methylxanthine. Arch. Ophthalmol. 109:672–676

    PubMed  CAS  Google Scholar 

  • Hamann S. 2002. Molecular mechanisms of water transport in the eye. Int. Rev. Cytol. 215:395–431

    Article  PubMed  CAS  Google Scholar 

  • Hamann S., Zeuthen T., La Cour M., Nagelhus E.A., Ottersen O.P., Agre P., Nielsen S. 1998. Aquaporins in complex tissues: distribution of aquaporins 1–5 in human and rat eye. Am. J. Physiol. 274:C1332–1345

    PubMed  CAS  Google Scholar 

  • Hara-Chikuma M., Verkman A. S. 2006. Aquaporin-1 facilitates epithelial cell migration in kidney proximal tubule. J. Am. Soc. Nephrol. 17:39–45

    Article  PubMed  CAS  Google Scholar 

  • Hartzell C., Qu Z., Putzier I., Artinian L., Chien L., Cui Y. 2005. Looking chloride channels straight in the eye: bestrophins, lipofuscinosis, and retinal degeneration. Physiology 20:292–302

    Article  PubMed  CAS  Google Scholar 

  • Hasegawa H., Lian S.C., Finkbeiner W.B., Verkman A.S. 1994. Extrarenal tissue distribution of CHIP28 water channels by in situ hybridization and antibody staining. Am. J. Physiol. 266:C893–C903

    PubMed  CAS  Google Scholar 

  • Iandiev I., Pannicke T., Reichel M.B., Wiedemann P., Reichenbach A., Bringmann A. 2005. Expression of aquaporin-1 immunoreactivity by photoreceptor cells in the mouse retina. Neurosci. Lett. 388:96–99

    Article  PubMed  CAS  Google Scholar 

  • Jentsch T.J., Stein. V., Weinreich. F., Zdebik A.A. 2002. Molecular structure and physiologic function of chloride channels. Physiol. Rev. 82:503–568

    PubMed  CAS  Google Scholar 

  • Joyce N.C. 2003. Proliferative capacity of the corneal endothelium. Prog. Retin. Eye Res. 22:359–389

    Article  PubMed  CAS  Google Scholar 

  • Kang F., Kuang K., Li J., Fischbarg J. 1999. Cultured bovine corneal epithelial cells express a functional aquaporin water channel. Invest. Ophthalmol. Vis. Sci. 40:253–257

    PubMed  CAS  Google Scholar 

  • Kenney M.C., Atilano S.R., Zorapapel N., Holguin B., Gaster R.N., Ljubimov A.V. 2004. Altered expression of aquaporins in bullous keratopathy and Fuchs’ dystrophy corneas. J. Histochem. Cytochem. 52:1341–1340

    Article  PubMed  CAS  Google Scholar 

  • Kompella U.B., Kim K.J., Lee V.H. 1993. Active chloride transport in the pigmented rabbit conjunctiva. 12:1041–1048

    Google Scholar 

  • Klyce S.D., Neufeld A.H., Zadunaisky J.A. 1973. The activation of chloride transport by epinephrine and DB cyclic-AMP in the cornea of the rabbit. Invest. Ophthalmol. 12:127–139

    PubMed  CAS  Google Scholar 

  • Klyce S.D., Wong R.K.S. 1977. Site and mode of adrenaline action on chloride transport across the rabbit corneal epithelium. J. Physiol. 266:777–799

    PubMed  CAS  Google Scholar 

  • Kim I.B., Lee E.J., Oh S.J., Park C.B., Pow D.V., Chun M.H. 2002. Light and electron microscopic analysis of aquaporin 1-like-immunoreactive amacrine cells in the rat retina. J. Comp. Neurol. 452:178–191

    Article  PubMed  Google Scholar 

  • Kim I.B., Oh S.J., Nielsen S., Chun M.H. 1998. Immunocytochemical localization of aquaporin 1 in the rat retina. Neurosci. Lett. 244:52–54

    Article  PubMed  CAS  Google Scholar 

  • Kuang K., Yiming M., Wen Q., Li Y., Ma L., Iserovich P., Verkman A.S., Fischbarg J. 2004. Fluid transport across cultured layers of corneal endothelium from aquaporin-1 null mice. Exp. Eye Res. 78:791–798

    Article  PubMed  CAS  Google Scholar 

  • Lass J.H., Spurney R.V., Dutt R.M., Andersson H., Kochar H., Rodman H.M., Stern R.C., Doershuk C.F. 1985. A morphologic and fluorophometric analysis of the corneal endothelium in type I diabetes mellitus and cystic fibrosis. Am. J. Ophthalmol. 100:783–788

    PubMed  CAS  Google Scholar 

  • Lemp M.A. 1995. Report of the National Eye Institute/Industry Workshop on clinical trials for dry eyes. CLAO J. 21:221–232

    PubMed  CAS  Google Scholar 

  • Levin M.H., Verkman A.S. 2004. Aquaporin-dependent water permeation at the mouse ocular surface: in vivo microfluorimetric measurements in cornea and conjunctiva. Invest. Ophthalmol. Vis. Sci. 46:1428–1434

    Article  Google Scholar 

  • Levin, M.H., Verkman, A.S. 2005a. Delayed corneal epithelial wound healing in aquaporin-3-null mice. Invest. Ophthalmol. Vis. Sci. 45:E-Abstract 3618

  • Levin M.H., Verkman A.S. 2005. CFTR-regulated chloride transport at the ocular surface in living mice measured by potential differences. Invest. Ophthalmol. Vis. Sci. 45:4423–4432

    Article  Google Scholar 

  • Li Y., Kuang K., Yerxa B., Wen Q., Rosskothen H., Fischbarg J. 2001. Rabbit conjunctival epithelium transports fluid and P2Y2(2) receptor agonists stimulate Cl− and fluid secretion. Am. J. Physiol. 281:C595–C602

    CAS  Google Scholar 

  • Li J., Patil R.V., Verkman A.S. 2002. Mildly abnormal retinal function in transgenic mice without Müller cell aquaporin-4 water channels. Invest. Ophthalmol. Vis. Sci. 43:573–579

    PubMed  Google Scholar 

  • Li J., Verkman A.S. 2001. Impaired hearing in mice lacking aquaporin-4 water channels. J. Biol. Chem. 276:31233–31237

    Article  PubMed  CAS  Google Scholar 

  • Loewen M.E., Smith N.K., Hamilton D.L., Grahn B.H., Forsyth G.W. 2003. CLCA protein and chloride transport in canine retinal pigment epithelium. Am. J. Physiol. 285:C1314–1321

    CAS  Google Scholar 

  • Ma T., Thiagarajah J.R., Yang H., Sonawane N.D., Folli C., Gallietta L.J., Verkman A.S. 2002a. Thiazolidinone CFTR inhibitor identified by high-throughput screening blocks cholera toxin-induced intestinal fluid secretion. J. Clin. Invest. 110:1651–1658

    Article  CAS  Google Scholar 

  • Ma T., Vetrivel L., Yang H., Pedemonte N., Zegarra-Moran O., Galietta L.J., Verkman A.S. 2002b. High-affinity activators of cystic fibrosis transmembrane conductance regulator (CFTR) chloride conductance identified by high-throughput screening. J. Biol. Chem. 277:37235–37241

    Article  CAS  Google Scholar 

  • Macnamara E., Sams G.W., Smith K., Ambati J., Singh N., Ambati B.K. 2004. Aquaporin-1 expression is decreased in human and mouse corneal endothelial dysfunction. Mol. Vis. 10:51–56

    PubMed  CAS  Google Scholar 

  • Maminishkis A., Jalickee S., Blaug S.A., Rymer J., Yerxa B.R., Peterson W.M., Miller S.S. 2002. The P2Y(2) receptor agonist INS37217 stimulates RPE fluid transport in vitro and retinal reattachment in rat. Invest. Ophthalmol. Vis. Sci. 43:3555–3566

    PubMed  Google Scholar 

  • Mandell R.B., Fatt I. 1965. Thinning of the human cornea on awakening. Nature 208:292–293

    Article  PubMed  CAS  Google Scholar 

  • Manley G.T., Fujimura M., Ma T., Noshita N., Filiz F., Bollen A., Chan P., Verkman A.S. 2000. Aquaporin-4 deletion in mice reduces brain edema following acute water intoxication and ischemic stroke. Nature Medicine 6:159–163

    Article  PubMed  CAS  Google Scholar 

  • Marmor M.F. 1990. Control of subretinal fluid: experimental and clinical studies. Eye 4:340–344

    PubMed  Google Scholar 

  • Marmor M.F. 1999. Mechanisms of fluid accumulation in retinal edema. Doc. Ophthalmol. 97:239–249

    Article  PubMed  CAS  Google Scholar 

  • Marmorstein A.D., Marmorstein L.Y., Royborn M., Wang X., Holyfield J.G., Petrukhin K. 2000. Bestrophin, the product of the Best vitelliform macular dystrophy gene (VMD2), localizes to the basolateral membrane of the retinal pigment epithelium. Proc. Natl. Acad. Sci. USA 97:12758–12763

    Article  PubMed  CAS  Google Scholar 

  • Mathers W.D., Lane J.A., Sutphin J.E., Zimmerman M.B. 1996. Model for ocular tear film function. Cornea 15:110–119

    PubMed  CAS  Google Scholar 

  • Maurice D.M. 1957. The structure and transparency of the cornea. J. Physiol. 136:263–286

    PubMed  CAS  Google Scholar 

  • McCannel C.A., Scanlon P.D., Thibodeau S., Brubaker R.F. 1992. A study of aqueous humor formation in patients with cystic fibrosis. Invest. Ophthalmol. Vis. Sci. 33:160–164

    PubMed  CAS  Google Scholar 

  • Meyer C.H., Hotta K., Peterson W.M., Toth C.A., Jaffe G.J. 2002. Effect of INS38717, a P2Y(2) agonist, on experimental retinal detachment and electroretinogram in adult rabbits. Invest. Ophthalmol. Vis. Sci. 43:3567–3574

    PubMed  Google Scholar 

  • Miller S.S., Hughes B.A., Machen T.E. 1982. Fluid transport across retinal pigment epithelium is inhibited by cyclic AMP. Proc. Natl. Acad. Sci. USA 79:2111–2115

    Article  PubMed  CAS  Google Scholar 

  • Mishima S., Hedbys B.O. 1967. The permeability of the corneal epithelium and endothelium to water. Exp. Eye Res. 6:10–32

    PubMed  CAS  Google Scholar 

  • Morkeberg J.C., Edmund C., Prause J.U., Lanng S., Koch C., Michaelsen K.F. 1995. Ocular findings in cystic fibrosis patients receiving vitamin A supplementation. Graëfes Arch. Clin. Exp. Ophthalmol. 233:709–713

    Article  PubMed  CAS  Google Scholar 

  • Mrugacz M., Minarowska A. 2002. Eye symptoms of cystic fibrosis. Klin. Oczna. 104:418–420

    PubMed  Google Scholar 

  • Muanprasat C., Sonawane N.D., Salinas D.B., Taddei A., Galietta L.J., Verkman A.S. 2004. Discovery of glycine hydrazide pore-occluding CFTR inhibitors: mechanism, structure-activity analysis and in vivo efficacy. J. Gen. Physiol. 124:125–137

    Article  PubMed  CAS  Google Scholar 

  • Murakami T., Fujihara T., Nakamura M., Nakata K. 2000 P2Y(2) receptor stimulation increases tear fluid secretion in rabbits. Curr. Eye Res. 21:782–787

    Article  PubMed  CAS  Google Scholar 

  • Nagelhus E.A., Horio A., Inanobe Al., Fujita F.M., Haug S. Nielson S., Kurachi Y., Ottersen O.P. 1999. Immungold evidence suggests that coupling of K+ siphoning and water transport in rat retinal Müller cells is mediated by a coenrichment of Kir4.1 and AQP4 in specific membrane domains. Glia 26:47–54

    Article  PubMed  CAS  Google Scholar 

  • Nagelhus E.A., Veruki M.L., Torp R., Haug F., Laake J.H., Nielsen S. Agre P., Ottersen O.P. 1998. Aquaporin-4 water channel protein in the rat retina and optic nerve: polarized expression in Müller cells and fibrous astrocytes. J. Neuroscience 18:2506–2519

    CAS  Google Scholar 

  • Nielsen S., Smith B.I., Christensen E.I., Agre P.A. 1993. Distribution of the aquaporin CHIP in secretory and resorptive epithelia and capillary endothelia. Proc. Natl. Acad. Sci. USA 90:7275–7279

    Article  PubMed  CAS  Google Scholar 

  • Paradiso A.M., Coakley R.D., Boucher R.C. 2003. Polarized distribution of HCO −3 transport in normal and cystic fibrosis nasal epithelia. J. Physiol. 548:203–218

    Article  PubMed  CAS  Google Scholar 

  • Patil R.V., Saito I., Yang X., Wax M.B. 1997. Expression of aquaporins in the rat ocular tissue. Exp. Eye Res. 64:203–209

    Article  PubMed  CAS  Google Scholar 

  • Patil R.V., Han Z., Yiming M., Yang J., Iserovich P., Wax M.B., Fischbarg J. 2001. Fluid transport by human nonpigmented ciliary epithelial layers in culture: a homeostatic role for aquaporin-1. Am. J. Physiol. 281:C1139–C1145

    CAS  Google Scholar 

  • Pilewsky J.M., Frizzell R.A. 1999. Role of CFTR in airway disease. Physiol. Rev. 79:S215–S255

    Google Scholar 

  • Rabinowitz Y.S., Dong L., Wistow G. 2005. Gene expression studies of human keratoconus cornea for NEIBank: a novel cornea-expressed gene and the absence of transcripts for aquaporin 5. Invest. Ophthalmol. Vis. Sci. 46:1239–1246

    Article  PubMed  Google Scholar 

  • Reigada D., Mitchell C.H. 2004. Release of ATP from retinal pigment epithelial cells involves both CFTR and vesicular transport. Am. J. Physiol. 288:C132–C140

    Google Scholar 

  • Ruiz A., Rok D. 1996. Characterization of the 3′ UTR sequence encoded by the AQP-1 gene in human retinal pigment epithelium. Biochim. Biophys. Acta. 1282:174–178

    Article  PubMed  Google Scholar 

  • Ruiz-Ederra J., Verkman A.S. 2006. Mouse model of sustained elevation in intraocular pressure produced by episcleral vein occlusion. Exp. Eye Res. 82:879–884

    Article  PubMed  CAS  Google Scholar 

  • Sheppard D.M., Welsh M.J. 1999. Structure and function of the CFTR chloride channel. Physiol. Rev. 79:S23–S45

    PubMed  CAS  Google Scholar 

  • Sheppard J.D., Orenstein D.M., Chao C., Butala S., Kowalski R.P. 1989. The ocular surface in cystic fibrosis. Ophthalmology. 96:1624–1630

    PubMed  CAS  Google Scholar 

  • Shiue M.H., Gukasyan H.J., Kim K., Loo D.D., Lee V.H.L. 2002. Characterization of cyclic AMP-regulated chloride conductance in the pigmented rabbit conjunctival epithelial cells. Can. J. Physiol. Pharmacol. 80:533–540

    Article  PubMed  CAS  Google Scholar 

  • Song J., Lee Y.G., Houston J., Petroll W.M., Chakravarti S., Cavanagh H.D., Jester J.V. 2003. Neonatal corneal stromal development in the normal and lumican-deficient mouse. Invest. Ophthalmol. Vis. Sci. 44:548–557

    Article  PubMed  Google Scholar 

  • Stamer W.D., Bok D., Hu J., Jaffe G.J., McKay B.S. 2003. Aquaporin-1 channels in the human retinal pigment epithelium: role in transepithelial water movement. Invest. Ophthalmol. Vis. Sci. 44:2803–2808

    Article  PubMed  Google Scholar 

  • Stamer W.D., Peppel K., O’Donnell M.E., Roberts B.C., Wu F., Epstein D.S. 2001. Expression of aquaporin-1 in human trabecular meshwork cells: role in resting cell volume. Invest. Ophthalmol. Vis. Sci. 42:1803–1811

    PubMed  CAS  Google Scholar 

  • Sun X.C., Bonanno J.A. 2002. Expression, localization, and functional evaluation of CFTR in bovine corneal endothelial cells. Am. J. Physiol. 282:C673–C683

    CAS  Google Scholar 

  • Sun X.C., Zhai C.B., Cui M., Chen Y., Levin L.R., Buck J., Bonanno J.A. 2003. HCO −3 -dependent soluble adenylyl cyclase activates cystic fibrosis transmembrane conductance regulator in corneal endothelium. Am. J. Physiol. 284:C1114–C1122

    CAS  Google Scholar 

  • Sun X.C., Cui M., Bonanno J.A. 2004. [HCO3−]-regulated expression and activity of soluble adenylyl cyclase in corneal endothelial and Calu-3 cells. BMC Physiol. 4:8

    Article  PubMed  Google Scholar 

  • Thiagarajah J.R., Verkman A.S. 2002. Aquaporin deletion in mice reduces corneal water permeability and delays restoration of transparency after swelling. J. Biol. Chem. 277:19139–19144

    Article  PubMed  CAS  Google Scholar 

  • Turner H.C., Alvarez L.J., Candia O.A. 2000. Cyclic AMP-dependent stimulation of basolateral K+ conductance in the rabbit conjunctival epithelium. Exp. Eye Res. 70:295–305

    Article  PubMed  CAS  Google Scholar 

  • Turner H.C., Bernstein A., Candia O.A. 2002. Presence of CFTR in the conjunctival epithelium. Curr. Eye Res. 24:182–187

    Article  PubMed  Google Scholar 

  • Verkman A.S. 2005. More than just water channels: unexpected cellular roles of aquaporins. J. Cell Sci. 118:3225–3232

    Article  PubMed  CAS  Google Scholar 

  • Watsky M.A., Jablonski M.M., Edelhauser H.F. 1988. Comparison of conjunctival and corneal surface area in rabbit and human. Curr. Eye Res. 7:483–486

    PubMed  CAS  Google Scholar 

  • Weinreb R.N., Khaw P.T. 2004. Primary open-angle glaucoma. Lancet 363:1711–1720

    Article  PubMed  Google Scholar 

  • Welsh M.J., Smith J.J. 2001. cAMP stimulation of HCO −3 secretion across airway epithelia. Jop. 2:291–293

    PubMed  CAS  Google Scholar 

  • Wen Q., Diecke F.P., Iserovich P., Kurang K., Sparrow J., Fischbarg J. 2001. Immunocytochemical localization of aquaporin-1 in bovine corneal endothelial cells and keratocytes. Exp. Biol. Med. (Maywood). 226:463–467

    CAS  Google Scholar 

  • Wolosin J.M., Candia O.A. 1987. Cl− secretagogues increase basolateral K+ conductance of frog corneal epithelium. Am. J. Physiol. 253:C555–C560

    PubMed  CAS  Google Scholar 

  • Wu J., Marmorstein A.D., Kofuji P., Peachey N.S. 2004. Contribution of Kir4.1 to the mouse electroretinogram. Mol. Vis. 10:650–654

    PubMed  CAS  Google Scholar 

  • Wu J., Peachey N.S., Marmorstein A.D. 2004. Light-evoked response of the mouse retinal pigment epithelium. J. Neurophysiol. 91:1134–1142

    Article  PubMed  Google Scholar 

  • Yang H., Reinach P.S., Koniarek J.P., Wang Z., Iserovich P., Fischbarg J. 2000. Fluid transport by cultured corneal epithelial cell layers. Br. J. Ophthalmol. 84:199–204

    Article  PubMed  CAS  Google Scholar 

  • Yi D.H., Dana M.R. 2002. Corneal edema after cataract surgery: incidence and etiology. Semin. Ophthalmol. 17:110–114

    Article  PubMed  Google Scholar 

  • Zhang D., Vetrivel L., Verkman A.S. 2002. Aquaporin deletion in mice reduces intraocular pressure and aqueous fluid production. J. Gen. Physiol. 119:561–569

    PubMed  CAS  Google Scholar 

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  1. Departments of Medicine and Physiology, Cardiovascular Research Institute, Graduate Group in Biophysics, University of California, San Francisco, CA, 94143-0521, USA

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Levin, M., Verkman, A. Aquaporins and CFTR in Ocular Epithelial Fluid Transport. J Membrane Biol 210, 105–115 (2006). https://doi.org/10.1007/s00232-005-0849-1

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