Abstract
Taurine and zinc exert neurotrophic effects. Zinc modulates Na+/Cl−-dependent transporters. This study examined the effect of zinc (ZnSO4) ex vivo and zinc chelator N,N,N′,N′-tetrakis-(2-pyridylmethyl) ethylenediamine (TPEN) in vivo on [3H]taurine transport in goldfish retina. The effect of TPEN in vivo on taurine and zinc levels was determined. Isolated cells were incubated in Ringer with zinc (0.1–100 μM). Taurine transport was done with taurine (0.001–1 mM) and 50 nM [3H]taurine. Zinc (100 μM) noncompetitively inhibited taurine transport. TPEN was administered intraocularly and retinas extracted 3, 5 and 10 days later. Taurine was determined by HPLC (nmol/mg protein) and zinc by spectrophotometry ICP (mg/mg protein). Taurine and zinc levels decreased at 3 days and increased at 10 days after TPEN administration. At 10 days after intraocular TPEN, taurine transport affinity increased (K s = 0.018 ± 0.006 vs. 0.028 ± 0.008 mM). Apparently, zinc deficiency affects the taurine–zinc complex and taurine availability. The increased taurine uptake affinity by TPEN was possibly associated with a response to maximize retinal taurine content at low zinc concentration.
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Abbreviations
- DMSO:
-
Dimethyl sulfoxide
- i.o.:
-
Intraocular injection
- EC50 :
-
Mean effective concentration
- TPEN:
-
N,N,N′,N′-tetrakis-(2-pyridylmethyl) ethylenediamine
References
Ahn Y, Kim Y, Hong S, Koh Y (1998) Depletion of intracellular zinc induces protein synthesis-dependent neuronal apoptosis in mouse cortical culture. Exp Neurol 154:47–56
Chai F, Truong-Tran A, Ho L, Zalewski D (1999) Regulation of caspase activation and apoptosis by cellular zinc fluxes and zinc deprivation: a review. Immunol Cell Biol 77:272–278
Erikson K, Aschner M (2002) Manganese causes differential regulation of glutamate transporter (GLAST), taurine transporter and metallothionein in cultured rat astrocytes. Neurotoxicology 23:595–602
Fazzino F, Urbina M, Mata S, Lima L (2006) Taurine transport and transporter localization in blood peripheral lymphocytes of controls and major depression patients. Adv Exp Med Biol 583:423–426
García-Colunga J, Reyes-Haro D, Godoy-García U, Miledi R (2005) Zinc modulation of serotonin uptake in the adult rat corpus callosum. J Neurosci Res 80:145–149
Giros B, Caron M (1993) Molecular characterization of the dopamine transporter. Trends Pharmacol Sci 14:43–49
Glover C, Hogstrand C (2002) Amino acid modulation of in vivo intestinal zinc absorption in freshwater rainbow trout. J Exp Biol 205:151–158
Gong H, Amemiya T (2001) Optic nerve changes in zinc-deficient rats. Exp Eye Res 72:363–369
González-Quevedo A, Obregón F, Urbina M, Roussó T, Lima L (2003) Effects of taurine deficiency and chronic methanol administration on rat retina, optic nerve and brain amino acids and monoamines. Nutr Neurosci 6:253–261
Grafe F, Wohlrad W, Neubert R, Brandsch M (2004) Functional characterization of sodium-and chloride-dependent taurine transport in human keratinocytes. Eur J Pharm Biopharm 57:337–341
Grahn B, Paterson P, Gottschall-Pass K, Zhang Z (2001) Zinc and the eye. J Am Coll Nutr 20:106–118
Guerra A, Urbina M, Lima L (2000) Modulation of taurine uptake in the goldfish retina and axonal transport to the tectum. Effect of optic crush and axotomy. Amino Acids 19:1–17
Harraki B, Guiraud P, Rochat M, Faure H, Richard M, Fusselier M, Favier A (1994) Effect of taurine, l-glutamine and l-histidine addition in an amino acid glucose solution on the cellular bioavailability of zinc. Bio Metals 7:237–243
Harrison N, Gibbons S (1994) Zn+2: an endogenous modulator of ligand and voltage-gated ion channels. Neuropharmacology 33:935–952
Huszti Z, Horvath-Sziklai A, Noszal B, Madarasz E, Deli A (2001) Enhancing effect of zinc on astroglial and cerebral endothelial histamine uptake. Biochem Pharmacol 62:1491–1500
Ilouz R, Kaidanovich O, Gurwitz D, Eldar-Finkelman H (2002) Biochem Biophys Res Commun 295:102–106
Jacobson SG, Meadows NJ, Keeling PW, Mitchell WD, Thompson RP (1986) Rod-mediated retinal dysfunction in cats with zinc depletion: comparison with taurine depletion. Clin Sci (Lond) 71:559–564
Kaneda M, Andrásfalvy B, Kaneko A (2000) Modulation by Zn2+ of GABA responses in bipolar cells of the mouse retina. Vis Neurosci 17:273–281
Kaneda M, Ishii K, Akagi T, Tatsukawa T, Hashikawa T (2005) Endogenous zinc can be a modulator of glycinergic signaling pathway in the rat retina. J Mol Histol 36:179–185
Kreitzer MA, Birnbaum AD, Qian H, Malchow RP (2009) Pharmacological characterization, localization, and regulation of ionotropic glutamate receptors in skate horizontal cells. Vis Neurosci 14:1–13
Law R (1998) The role of taurine in the regulation of brain cell volume in chronically hyponatraemic rats. Neurochem Int 33:467–472
Lees G, Lehmann A, Sandberg M, Hamberger A (1990) The neurotoxicity of zinc in the rat hippocampus. Neurosci Lett 120:155–158
Lima L (1999) Taurine and its trophic effects in the retina. Neurochem Res 24:1333–1338
Lima L, Cubillos S (1998) Taurine might be acting as a trophic factor in the retina by modulating phosphorylation of cellular proteins. J Neurosci Res 53:377–384
Lima L, Matus P, Drujan B (1991) Differential taurine uptake in central and peripheral regions of goldfish retina. J Neurosci Res 28:422–427
Lima L, Matus P, Drujan B (1993) Taurine-induced regeneration of goldfish retina in culture may involve a calcium-mediated mechanism. J Neurochem 60:2153–2157
Lima L, Cubillos S, Guerra A (2000) Regulation of high-affinity taurine transport in goldfish and rat retinal cells. Adv Exp Med Biol 483:431–440
Lima L, Obregón F, Matus P (1998) Taurine, glutamate and GABA modulate the outgrowth from goldfish retinal explants and its concentrations are affected by the crush of the optic nerve. Amino Acids 15:195–209
Lima L, Obregón F, Roussó T, Quintal M, Benzo Z, Auladel C (2004) Content and concentration of taurine, hypotaurine, and zinc in the retina, the hippocampus, and the dentate gyrus of the rat at various postnatal days. Neurochem Res 29:247–255
Loland C, Norregaard L, Gether U (1999) Defining proximity relationships in the tertiary structure of the dopamine transporter. Identification of a conserved glutamic acid as a third coordinate in the endogenous zn21-binding site. J Biol Chem 274:36928–36934
Lowry O, Rosebrough N, Farr A, Randall R (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275
Mazdai M, Strain J, Cotter T, Hannigan B (1991) Programmed cell death (apoptosis) in lymphoid and myeloid cell lines during zinc deficiency. Clin Exp Immunol 83:338–343
Militante J, Lombardini J (1999) Taurine uptake activity in the rat retina: protein kinase C-independent inhibition by chelerythrine. Brain Res 818:368–374
Militante J, Lombardini J (2002) Taurine: evidence of physiological function in the retina. Nutr Neurosci 5:75–90
Noh K, Kim Y, Koh J (1999) Mediation by membrane protein kinase C of zinc-induced oxidative neuronal injury in mouse cortical cultures. J Neurochem 72:1609–1616
Norgaard-Nielsen K, Norregaard L, Hastrup H, Javitch J, Gether U (2002) Zn2+ site engineering at the oligomeric interface of the dopamine transporter. FEBS Lett 524:87–91
Norregaard L, Frederiksen D, Nielsen E, Gether U (1998) Delineation of an endogenous zinc-binding site in the human dopamine transporter. EMBO J 17:4266–4273
Nusetti S, Obregon F, Quintal M, Benzo Z, Lima L (2005) Taurine and zinc modulate outgrowth from goldfish retinal explants. Neurochem Res 30:1483–1492
Nusetti S, Obregón F, Lima L (2006) Neuritic outgrowth from goldfish retinal explants, interaction of taurine and zinc. Adv Exp Med Biol 583:435–440
Nusetti S, Salazar V, Lima L (2009) Localization of taurine transporter, taurine and zinc in goldfish retina. Adv Exp Med Biol 643:233–242
Oteiza P, Hurley L, Lonnerdal B, Keen C (1990) Effects of zinc deficiency on microtubule polymerization in the developing rat brain. Biol Trace Elem Res 24:13–23
Pasantes-Morales H, Cruz C (1984) Protective effect of taurine and zinc on peroxidation-induced damage in photoreceptor outer segments. J Neurosci Res 11:303–311
Redenti S, Ripps H, Chappell RL (2007) Zinc release at the synaptic terminals of rod photoreceptors. Exp Eye Res 85:580–584
Rogers J, Hurley L (1987) Effects of zinc deficiency on morphogenesis of the fetal rat eye. Development 99:231–238
Saghizadeh M, Akhmedov NB, Yamashita CK, Gribanova Y, Theendakara V, Mendoza E, Nelson SF, Ljubimov AV, Farber DB (2009) ZBED4, a BED-type zinc-finger protein in the cones of human retina. Invest Ophthalmol Vis Sci 50:3580–3588
Salceda R, Saldaña M (1993) Glutamate and taurine uptake by retinal pigment epithelium during rat development. Comp Biochem Physiol 104:311–316
Sandstead H, Christopher F, Penland J (2000) History of zinc as related to brain function. J Nutr 130:496–502
Schetz J, Chu A, Sibley D (1999) Zinc modulates antagonist interactions with D2-like dopamine receptors through distinct molecular mechanisms. J Pharmacol Exp Ther 289:956–964
Scholze P, Norregaard L, Singer E, Freissmuth M, Gether U, Sitte H (2002) The role of zinc ions in reverse transport mediated by monoamine transporters. J Biol Chem 277:21505–21513
Spiridon M, Kamm D, Billups B, Mobbs P, Attwell D (1998) Modulation by zinc of the glutamate transporters in glial cells and cones isolated from the tiger salamander retina. J Physiol 506:363–376
Sturman J, Moretz R, French J, Wisniewski H (1985) Postnatal taurine deficiency in the kitten results in a persistence of the cerebellar external granule cell layer: correction by taurine feeding. J Neurosci Res 13:428–521
Sun Z, Zhang DQ, McMahon DG (2009) Zinc modulation of hemi-gap-junction channel currents in retinal horizontal cells. J Neurophysiol 101:1774–1780
Takeda A (2001) Zinc homeostasis and functions in the brain. Biometals 14:343–351
Tang X, Shay N (2001) Zinc has an insulin-like effect on glucose transport mediated by phosphoinositol-3-kinase and Akt in 3T3-L1 fibroblasts and adipocytes. J Nutr 131:1414–1420
Tapia F (1994) GraphPad Instat Softward. V2.05a
Ugarte M, Osborne N (2001) Zinc in the retina. Prog Neurobiol 64:219–249
Vallee B, Falcchuk K (1993) The biochemical basis of zinc physiology. Physiol Rev 73:79–105
van Gelder N (1983) A central mechanism of action for taurine: osmoregulation, bivalent cations, and excitation threshold. Neurochem Res 8:687–699
Vanderberg R, Mitrovic D, Johnston R (1998) Molecular basis for differential inhibition of glutamate transporter subtypes by zinc ions. Mol Pharmacol 54:189–196
Wallwork J, Sandstead H (1983) Effect of zinc deficiency on appetite and free amino acid concentrations in rat brain. J Nutr 113:47–54
Weiss J, Sensi S, Koh J (2000) Zn2+ a novel mediator of neural injury in brain disease. Trends Pharmacol Sci 21:395–401
Wu Q, Wada M, Shimada A, Yamamoto A, Fujita T (2006) Funcional characterization of Zn2(+)-sensitive GABA transporter expressed in primary cultures of astrocytes from rat cerebral cortex. Brain Res 1075:100–109
Yoo M, Lee J, Lee S, Koh J, Yoon Y (2004) Protection by pyruvate of rat retinal cells against zinc toxicity in vitro, and pressure-induced ischemia in vivo. Invest Ophthalmol Vis Sci 45:1523–1530
Acknowledgments
This work was supported by Grant S1-2001-903 from Fondo Nacional de Investigación, Tecnología e Innovación (FONACIT), Venezuela. S. Nusetti was a Ph.D. student of Centro de Estudios Avanzados, Instituto Venezolano de Investigaciones Científicas, with financial support from Universidad de Oriente and FONACIT.
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Nusetti, S., Urbina, M., Obregón, F. et al. Effects of zinc ex vivo and intracellular zinc chelator in vivo on taurine uptake in goldfish retina. Amino Acids 38, 1429–1437 (2010). https://doi.org/10.1007/s00726-009-0357-1
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DOI: https://doi.org/10.1007/s00726-009-0357-1