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Localization and ontogeny of aquaporin-1 and -4 expression in iris and ciliary epithelial cells in rats

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Abstract

The precise localization of aquaporin (AQP)1 and AQP4 was studied in iris and ciliary epithelial cells, in both mature and developing rats, to elucidate the molecular mechanisms underlying aqueous humor balance. Anterior segments of eyes dissected from embryonic day (E)13, E15, E18, and E20, postnatal day (P)0, P7, and P14, and postnatal week 8 rats were subjected to immunofluorescence analysis with AQP isoform-specific antibodies. In adult rat eye, AQP1 was localized to the apical and basolateral plasma membranes of iris epithelial cell layers and of anterior ciliary non-pigmented epithelial (NPE) cells. Conversely, AQP4 was localized to the basolateral plasma membrane of NPE cells in ciliary epithelium and the posterior iris. Developmentally, AQP1 was detected as early as E15 in immature iris and ciliary epithelial cells, and expression persisted throughout development up to adulthood. In contrast, AQP4 was first observed at P7 in the developing pars plicata, and the AQP4-positive area gradually spread to cover the entire pars plicata as development proceeded. These findings indicate that both AQP1 and AQP4 contribute to aqueous humor secretion in the rat eye, thereby maintaining proper intraocular pressure. Moreover, AQP appears to play a major role in aqueous humor secretion in early eye development. This study thus provides a basis for understanding the molecular mechanisms of aqueous humor secretion in pathological and physiological conditions.

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References

  • Arguillere P, Patey A, Hirsch M (1986) Quantitative analysis of tight junctions during ciliary epithelium development. Exp Eye Res 42:239–248

    Article  PubMed  CAS  Google Scholar 

  • Beebe DC (1986) Development of the ciliary body: a brief review. Trans Ophthalmol Soc UK 105:123–130

    PubMed  Google Scholar 

  • Bondy C, Chin E, Smith BL, Preston GM, Agre P (1993) Developmental gene expression and tissue distribution of the CHIP28 water-channel protein. Proc Natl Acad Sci USA 90:4500–4504

    Article  PubMed  CAS  Google Scholar 

  • Calamita G, Bishai WR, Preston GM, Guggino WB, Agre P (1995) Molecular cloning and characterization of aqpZ, a water channel from Escherichia coli. J Biol Chem 270:29063–29066

    Article  PubMed  CAS  Google Scholar 

  • Caprioli J (1992) The ciliary epithelia and aqueous humor. In: Hart WM (ed) Adler’s physiology of the eye. Mosby, St. Louis, pp 228–247

    Google Scholar 

  • Chrispeels MJ, Agre P (1994) Aquaporins water channel proteins of plant and animal cells. Trends Biochem Sci 19:421–425

    Article  PubMed  CAS  Google Scholar 

  • Dalloz C, Sarig R, Fort P, Yaffe D, Bordais A, Pannicke T, Grosche J, Mornet D, Reichenbach A, Sahel J, Nudel U, Rendon A (2003) Targeted inactivation of dystrophin gene product Dp71: phenotypic impact in mouse retina. Hum Mol Genet 12:1543–1554

    Article  PubMed  CAS  Google Scholar 

  • Dunn JJ, Lytle C, Crook RB (2001) Immunolocalization of the Na–K–Cl cotransporter in bovine ciliary epithelium. Invest Ophthalmol Vis Sci 42:343–353

    PubMed  CAS  Google Scholar 

  • Frigeri A, Nicchia GP, Balena R, Nico B, Svelto M (2004) Aquaporins in skeletal muscle: reassessment of the functional role of aquaporin-4. FASEB J 18:905–907

    PubMed  CAS  Google Scholar 

  • Ghosh S, Hernando N, Martin–Alonso JM, Martin–Vasallo P, Coca–Prados M (1991) Expression of multiple Na+,K(+)–ATPase genes reveals a gradient of isoforms along the nonpigmented ciliary epithelium: functional implications in aqueous humor secretion. J Cell Physiol 149:184–194

    Article  PubMed  CAS  Google Scholar 

  • Green K, Pederson JE (1973) Aqueous humor formation. Exp Eye Res 16:273–286

    Article  PubMed  CAS  Google Scholar 

  • Hamann S, Zeuthen T, La Cour M, Nagelhus EA, Ottersen OP, Agre P, Nielsen S (1998) Aquaporins in complex tissues: distribution of aquaporins 1–5 in human and rat eye. Am J Physiol 274:C1332–C1345

    PubMed  CAS  Google Scholar 

  • Han Z, Wax MB, Patil RV (1998) Regulation of aquaporin-4 water channels by phorbol ester-dependent protein phosphorylation. J Biol Chem 273:6001–6004

    Article  PubMed  CAS  Google Scholar 

  • Han Z, Patil RV (2000) Protein kinase A-dependent phosphorylation of aquaporin-1. Biochem Biophys Res Commun 273:328–332

    Article  PubMed  CAS  Google Scholar 

  • Hasegawa H, Lian SC, Finkbeiner WE, Verkman AS (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 

  • King LS, Choi M, Fernandez PC, Cartron JP, Agre P (2001) Defective urinary-concentrating ability due to a complete deficiency of aquaporin-1. N Engl J Med 345:175–179

    Article  PubMed  CAS  Google Scholar 

  • Latker CH, Beebe DC (1984) Developmental changes in the blood-ocular barriers in chicken embryos. Exp Eye Res 39:401–414

    Article  PubMed  CAS  Google Scholar 

  • Linser PJ, Plunkett JA (1989) A role for carbonic anhydrase in early eye morphogenesis. Invest Ophthalmol Vis Sci 30:783–785

    PubMed  CAS  Google Scholar 

  • Matsuzaki T, Tajika Y, Tserentsoodol N, Suzuki T, Aoki T, Hagiwara H, Takata K (2002) Aquaporins : a water channel family. Anat Sci Int 77:85–93

    Article  PubMed  Google Scholar 

  • Nielsen S, Smith BL, Christensen EI, Agre P (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 

  • Patil RV, Saito I, Yang X, Wax MB (1997a) Expression of aquaporins in the rat ocular tissue. Exp Eye Res 64:203–209

    Article  PubMed  CAS  Google Scholar 

  • Patil RV, Han Z, Wax MB (1997b) Regulation of water channel activity of aquaporin 1 by arginine vasopressin and atrial natriuretic peptide. Biochem Biophys Res Commun 238:392–396

    Article  PubMed  CAS  Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Reichman EF, Beebe DC (1992) Changes in cellular dynamics during the development of the ciliary epithelium. Dev Dyn 193:125–135

    PubMed  CAS  Google Scholar 

  • Scott WJ Jr, Lane PD, Randall JL, Schreiner CM (1984) Malformations in nonlimb structures induced by acetazolamide and other inhibitors of carbonic anhydrase. Ann N Y Acad Sci 429:447–456

    Article  PubMed  CAS  Google Scholar 

  • Stamer WD, Snyder RW, Smith BL, Agre P, Regan JW (1994) Localization of aquaporin CHIP in the human eye: implications in the pathogenesis of glaucoma and other disorders of ocular fluid balance. Invest Ophthalmol Vis Sci 35:3867–3872

    PubMed  CAS  Google Scholar 

  • Verkman AS (2003) Role of aqaporin water channels in eye function. Exp Eye Res 76:137–143

    Article  PubMed  CAS  Google Scholar 

  • Ward DT, Yau SK, Mee AP, Mawer EB, Miller CA, Garland HO, Riccardi D (2001) Functional, molecular, and biochemical characterization of streptozotocin-induced diabetes. J Am Soc Nephrol 12:779–790

    PubMed  CAS  Google Scholar 

  • Yamamoto N, Yoneda K, Asai K, Sobue K, Tada T, Fujita Y, Katsuya H, Fujita M, Aihara N, Mase M, Yamada K, Miura Y, Kato T (2001) Alterations in the expression of the AQP family in cultured rat astrocytes during hypoxia and reoxygenation. Mol Brain Res 90:26–38

    Article  PubMed  CAS  Google Scholar 

  • Zhang D, Vetrivel L, Verkman AS (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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Authors and Affiliations

  1. Department of Ophthalmology, Kyorin University School of Medicine, 6-20-2 Shinkawa, Mitaka, Tokyo, 181-8611, Japan

    Yasuko Yamaguchi, Akito Hirakata & Tetsuo Hida

  2. Laboratory Medicine, Kyorin University School of Medicine, 6-20-2 Shinkawa, Mitaka, Tokyo, 181-8611, Japan

    Takashi Watanabe

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  1. Yasuko Yamaguchi
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  2. Takashi Watanabe
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  3. Akito Hirakata
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  4. Tetsuo Hida
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Correspondence to Yasuko Yamaguchi.

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Yamaguchi, Y., Watanabe, T., Hirakata, A. et al. Localization and ontogeny of aquaporin-1 and -4 expression in iris and ciliary epithelial cells in rats. Cell Tissue Res 325, 101–109 (2006). https://doi.org/10.1007/s00441-005-0122-z

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  • DOI: https://doi.org/10.1007/s00441-005-0122-z

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