Taurine deficiency damages retinal neurones: cone photoreceptors and retinal ganglion cells

详细信息    查看全文

• 作者：David Gaucher (1234)
  Emilie Arnault (123)
  Zoé Husson (123)
  Nicolas Froger (123)
  Elisabeth Dubus (123)
  Pauline Gondouin (123)
  Diane Dherbécourt (123)
  Julie Degardin (123)
  Manuel Simonutti (123)
  Stéphane Fouquet (123)
  M. A. Benahmed (56)
  K. Elbayed (6)
  Izzie-Jacques Namer (57)
  Pascale Massin (8)
  José-Alain Sahel (12391011)
  Serge Picaud (12311) serge.picaud@inserm.fr
• 关键词：Retina – Taurine deficiency – Ganglion cells – Autofluorescence – Degeneration – Retinal pigment epithelium
• 刊名：Amino Acids
• 出版年：2012
• 出版时间：November 2012
• 年：2012
• 卷：43
• 期：5
• 页码：1979-1993
• 全文大小：1.9 MB
• 参考文献：1. Anderson PA, Baker DH et al (1979) Biochemical lesions associated with taurine deficiency in the cat. J Anim Sci 49(5):1227–1234
  2. Anderson JR, Jones BW et al (2011) Exploring the retinal connectome. Mol Vis 17:355–379
  3. Barber AJ (2003) A new view of diabetic retinopathy: a neurodegenerative disease of the eye. Prog Neuropsychopharmacol Biol Psychiatry 27(2):283–290
  4. Barnett KC, Burger IH (1980) Taurine deficiency retinopathy in the cat. J Small Anim Pract 21(10):521–534
  5. Bellhorn RW (1976) Feline central retinal degeneration. Trans Sect Ophthalmol Am Acad Ophthalmol Otolaryngol 81(4 Pt 1):OP683–OP686
  6. Bulley S, Shen W (2011) Reciprocal regulation between taurine and glutamate response via Ca2+-dependent pathways in retinal third-order neurons. J Biomed Sci 17(Suppl 1):S5
  7. Chang B, Heckenlively JR et al (2006) The nob2 mouse, a null mutation in Cacna1f: anatomical and functional abnormalities in the outer retina and their consequences on ganglion cell visual responses. Vis Neurosci 23(1):11–24
  8. Cho NC, Poulsen GL et al (2000) Selective loss of S-cones in diabetic retinopathy. Arch Ophthalmol 118(10):1393–1400
  9. Cocker SE, Lake N (1987) Electroretinographic alterations and their reversal in rats treated with guanidinoethyl sulfonate, a taurine depletor. Exp Eye Res 45(6):977–987
  10. Coupland SG, Zackon DH et al (2001) Vigabatrin effect on inner retinal function. Ophthalmology 108(8):1493–1496 (discussion 1497–1498)
  11. Duboc A, Hanoteau N et al (2004) Vigabatrin, the GABA-transaminase inhibitor, damages cone photoreceptors in rats. Ann Neurol 55(5):695–705
  12. Franconi F, Bennardini F et al (1995) Plasma and platelet taurine are reduced in subjects with insulin-dependent diabetes mellitus: effects of taurine supplementation. Am J Clin Nutr 61(5):1115–1119
  13. Fuchs C, Forster V et al (2005) Retinal-cell-conditioned medium prevents TNF-alpha-induced apoptosis of purified ganglion cells. Invest Ophthalmol Vis Sci 46(8):2983–2991
  14. Haeseleer F, Imanishi Y et al (2004) Essential role of Ca2+-binding protein 4, a Cav1.4 channel regulator, in photoreceptor synaptic function. Nat Neurosci 7(10):1079–1087
  15. Hayes KC, Carey RE, Schmidt SY (1975) Retinal degeneration associated with taurine deficiency in the cat. Science 188(4191):949–951
  16. Hillenkamp J, Hussain AA et al (2004) Taurine uptake by human retinal pigment epithelium: implications for the transport of small solutes between the choroid and the outer retina. Invest Ophthalmol Vis Sci 45(12):4529–4534
  17. Hiramatsu M (2003) A role for guanidino compounds in the brain. Mol Cell Biochem 244(1–2):57–62
  18. Humayun MS, Prince M et al (1999) Morphometric analysis of the extramacular retina from postmortem eyes with retinitis pigmentosa. Invest Ophthalmol Vis Sci 40(1):143–148
  19. Huxtable RJ (1989) Taurine in the central nervous system and the mammalian actions of taurine. Prog Neurobiol 32(6):471–533
  20. Imaki H, Jacobson SG et al (1993) Retinal morphology and visual pigment levels in 6- and 12-month-old rhesus monkeys fed a taurine-free human infant formula. J Neurosci Res 36(3):290–304
  21. Imaki H, Messing J, Sturman JA (1998) Extensive taurine depletion and retinal degeneration in cats treated with beta-alanine for 40 weeks. Adv Exp Med Biol 442:449–460
  22. Jacobson SG, Kemp CM et al (1987) Rhodopsin topography and rod-mediated function in cats with the retinal degeneration of taurine deficiency. Exp Eye Res 45(4):481–490
  23. Jammoul F, Wang Q et al (2009) Taurine deficiency is a cause of vigabatrin-induced retinal phototoxicity. Ann Neurol 65(1):98–107
  24. Jammoul F, Degardin J et al (2010) Taurine deficiency damages photoreceptors and retinal ganglion cells in vigabatrin-treated neonatal rats. Mol Cell Neurosci 43(4):414–421
  25. Kolomiets B, Dubus E et al (2010) Late histological and functional changes in the P23H rat retina after photoreceptor loss. Neurobiol Dis 38(1):47–58
  26. Lake N, Malik N (1987) Retinal morphology in rats treated with a taurine transport antagonist. Exp Eye Res 44(3):331–346
  27. Lake N, Marshall J, Voaden MJ (1977) The entry of taurine into the neural retina and pigment epithelium of the frog. Brain Res 128(3):497–503
  28. Leon A, Levick WR, Sarossy MG (1995) Lesion topography and new histological features in feline taurine deficiency retinopathy. Exp Eye Res 61(6):731–741
  29. Louzada PR, Paula Lima AC et al (2004) Taurine prevents the neurotoxicity of beta-amyloid and glutamate receptor agonists: activation of GABA receptors and possible implications for Alzheimer’s disease and other neurological disorders. Faseb J 18(3):511–518
  30. Macaione S, Ruggeri P et al (1974) Free amino acids in developing rat retina. J Neurochem 22(6):887–891
  31. Militante JD, Lombardini JB (1998) Pharmacological characterization of the effects of taurine on calcium uptake in the rat retina. Amino Acids 15(1–2):99–108
  32. Militante JD, Lombardini JB (2002) Taurine: evidence of physiological function in the retina. Nutr Neurosci 5(2):75–90
  33. Moloney MA, Casey RG et al (2010) Two weeks taurine supplementation reverses endothelial dysfunction in young male type 1 diabetics. Diab Vasc Dis Res 2010:28
  34. Nadal-Nicolas FM, Jimenez-Lopez M et al (2009) Brn3a as a marker of retinal ganglion cells: qualitative and quantitative time course studies in naive and optic nerve-injured retinas. Invest Ophthalmol Vis Sci 50(8):3860–3868
  35. Nakamura T, Ushiyama C et al (1999) Effects of taurine and vitamin E on microalbuminuria, plasma metalloproteinase-9, and serum type IV collagen concentrations in patients with diabetic nephropathy. Nephron 83(4):361–362
  36. Pasantes-Morales H, Quesada O et al (1983) Effects of the taurine transport antagonist, guanidinoethane sulfonate, and beta-alanine on the morphology of rat retina. J Neurosci Res 9(2):135–143
  37. Peterson WM, Miller SS (1995) Identification and functional characterization of a dual GABA/taurine transporter in the bullfrog retinal pigment epithelium. J Gen Physiol 106(6):1089–1122
  38. Piotto M, Moussalieh FM et al (2008) Metabolic characterization of primary human colorectal cancers using high resolution magic angle spinning 1H magnetic resonance spectroscopy. Metabolomics 5:292–301
  39. Pow DV, Sullivan R et al (2002) Localization of taurine transporters, taurine, and (3)H taurine accumulation in the rat retina, pituitary, and brain. Glia 37(2):153–168
  40. Quesada O, Picones A, Pasantes-Morales H (1988) Effect of light deprivation on the ERG responses of taurine-deficient rats. Exp Eye Res 46(1):13–20
  41. Ravindran J, Blumbergs P et al (2001) Visual field loss associated with vigabatrin: pathological correlations. J Neurol Neurosurg Psychiatry 70(6):787–789
  42. Satsu H, Watanabe H et al (1997) Characterization and regulation of taurine transport in Caco-2, human intestinal cells. J Biochem 121(6):1082–1087
  43. Schmidt SY, Berson EL, Hayes KC (1976) Retinal degeneration in the taurine-deficient cat. Trans Sect Ophthalmol Am Acad Ophthalmol Otolaryngol 81(4 Pt 1): OP687–OP693
  44. Schmitz-Valckenberg S, Holz FG et al (2008) Fundus autofluorescence imaging: review and perspectives. Retina 28(3):385–409
  45. Shimada C, Tanaka S et al (1992) Beneficial effect of intravenous taurine infusion on electroretinographic disorder in taurine deficient rats. Jpn J Pharmacol 59(1):43–50
  46. Sparrow JR, Yoon KD et al (2010) Interpretations of fundus autofluorescence from studies of the bisretinoids of the retina. Invest Ophthalmol Vis Sci 51(9):4351–4357
  47. Specht D, Tom Dieck S et al (2007) Structural and functional remodeling in the retina of a mouse with a photoreceptor synaptopathy: plasticity in the rod and degeneration in the cone system. Eur J Neurosci 26(9):2506–2515
  48. Tachikawa M, Kasai Y et al (2009) The blood-brain barrier transport and cerebral distribution of guanidinoacetate in rats: involvement of creatine and taurine transporters. J Neurochem 111(2):499–509
  49. Tomi M, Tajima A et al (2008) Function of taurine transporter (Slc6a6/TauT) as a GABA transporting protein and its relevance to GABA transport in rat retinal capillary endothelial cells. Biochim Biophys Acta 1778(10):2138–2142
  50. Tornquist P, Alm A et al (1986) Carrier-mediated transport of amino acids through the blood-retinal and the blood-brain barriers. Graefes Arch Clin Exp Ophthalmol 224:21–25
  51. Udawatte C, Qian H et al (2008) Taurine suppresses the spread of cell death in electrically coupled RPE cells. Mol Vis 14:1940–1950
  52. Vinnakota S, Qian X et al (1997) Molecular characterization and in situ localization of a mouse retinal taurine transporter. J Neurochem 69(6):2238–2250
  53. Voaden MJ, Lake N et al (1977) Studies on the distribution of taurine and other neuroactive amino acids in the retina. Exp Eye Res 25(3):249–257
  54. Wang QP, Jammoul F et al (2008) Treatment of epilepsy: the GABA-transaminase inhibitor, vigabatrin, induces neuronal plasticity in the mouse retina. Eur J Neurosci 27(8):2177–2187
  55. Wild JM, Robson CR et al (2006) Detecting vigabatrin toxicity by imaging of the retinal nerve fiber layer. Invest Ophthalmol Vis Sci 47(3):917–924
  56. Yu X, Xu Z et al (2008) Dietary taurine supplementation ameliorates diabetic retinopathy via anti-excitotoxicity of glutamate in streptozotocin-induced Sprague-Dawley rats. Neurochem Res 33(3):500–507
  57. Zeng K, Xu H et al (2009) Dietary taurine supplementation prevents glial alterations in retina of diabetic rats. Neurochem Res 34(2):244–254
• 作者单位：1. INSERM, U-968, Insitut de la Vision Retinal Information Processing: Pharmacology and Pathologies, 17, rue Moreau, 75012 Paris, France2. UPMC Univ Paris 06, UMR_S968, Institut de la Vision, 75012 Paris, France3. CNRS, UMR 7210, Institut de la Vision, 75012 Paris, France4. Service d’ophtalmologie du Nouvel H?pital Civil, Strasbourg, France5. Université de Strasbourg, UMR7237, Strasbourg, France6. Université de Strasbourg, UMR7177, Strasbourg, France7. Department of Biophysics and Nuclear Medicine, H?pitaux Universitaires de Strasbourg, Strasbourg, France8. H?pital Lariboisière, Paris, France9. Centre Hospitalier National d’Ophtalmologie des Quinze-Vingts, Paris, France10. Institute of Ophthalmology, University College, London, UK11. Fondation Ophtalmologique Adolphe de Rothschild, Paris, France
• ISSN：1438-2199

文摘

In 1970s, taurine deficiency was reported to induce photoreceptor degeneration in cats and rats. Recently, we found that taurine deficiency contributes to the retinal toxicity of vigabatrin, an antiepileptic drug. However, in this toxicity, retinal ganglion cells were degenerating in parallel to cone photoreceptors. The aim of this study was to re-assess a classic mouse model of taurine deficiency following a treatment with guanidoethane sulfonate (GES), a taurine transporter inhibitor to determine whether retinal ganglion cells are also affected. GES treatment induced a significant reduction in the taurine plasma levels and a lower weight increase. At the functional level, photopic electroretinograms were reduced indicating a dysfunction in the cone pathway. A change in the autofluorescence appearance of the eye fundus was explained on histological sections by an increased autofluorescence of the retinal pigment epithelium. Although the general morphology of the retina was not affected, cell damages were indicated by the general increase in glial fibrillary acidic protein expression. When cell quantification was achieved on retinal sections, the number of outer/inner segments of cone photoreceptors was reduced (20 %) as the number of retinal ganglion cells (19 %). An abnormal synaptic plasticity of rod bipolar cell dendrites was also observed in GES-treated mice. These results indicate that taurine deficiency can not only lead to photoreceptor degeneration but also to retinal ganglion cell loss. Cone photoreceptors and retinal ganglion cells appear as the most sensitive cells to taurine deficiency. These results may explain the recent therapeutic interest of taurine in retinal degenerative pathologies.