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Amino Acids

, Volume 51, Issue 4, pp 641–646 | Cite as

Taurine protects against NMDA-induced retinal damage by reducing retinal oxidative stress

  • Azliana Jusnida Ahmad Jafri
  • Renu AgarwalEmail author
  • Igor Iezhitsa
  • Puneet Agarwal
  • Nafeeza Mohd Ismail
Original Article

Abstract

This study aimed to evaluate effect of TAU on NMDA-induced changes in retinal redox status, retinal cell apoptosis and retinal morphology in Sprague–Dawley rats. Taurine was injected intravitreally as pre-, co- or post-treatment with NMDA and 7 days post-treatment retinae were processed for estimation of oxidative stress, retinal morphology using H&E staining and retinal cell apoptosis using TUNEL staining. Treatment with TAU, particularly pre-treatment, significantly increased retinal glutathione, superoxide dismutase and catalase levels compared to NMDA-treated rats; whereas, the levels of malondialdehyde reduced significantly. Reduction in retinal oxidative stress in TAU pre-treated group was associated with significantly greater fractional thickness of ganglion cell layer within inner retina and retinal cell density in inner retina. TUNEL staining showed significantly reduced apoptotic cell count in TAU pre-treated group compared to NMDA group. It could be concluded that TAU protects against NMDA-induced retinal injury in rats by reducing retinal oxidative stress.

Keywords

NMDA Taurine Retina Oxidative stress 

Abbreviations

CAT

Catalase

ET-1

Endothelin-1

ER

Endoplasmic reticulum

TAU

Taurine

GCL

Ganglion cell layer

IR

Inner retina

MDA

Malondialdehyde

NMDA

N-Methyl-d-aspartate

NO

Nitric oxide

NOS

Nitric oxide synthase

GSH

Reduced glutathione

SOD

Superoxide dismutase

SD

Standard deviation

Notes

Acknowledgements

We acknowledge the administrative and facility support by Research Management Institute, Institute of Medical Molecular Biotechnology (IMMB) and Laboratory Animal Care Unit, Universiti Teknologi MARA, Malaysia. The authors also acknowledge the financial support by Universiti Teknologi MARA, Malaysia, under Grant no. 600-IRMI/DANA 5/3/Bestari (P) (003/2018).

Compliance with ethical standards

Conflict of interest

Authors declare that no conflicts of interest exist.

Ethical approval

The study was approved by The Committee of Animal Research and Ethics (UiTM CARE). Study was done in Compliance with the local institutional ethical guidelines and according to ARVO statement for ophthalmic and vision research.

References

  1. Agarwal R, Agarwal P (2017) Rodent models of glaucoma and their applicability for drug discovery. Expert Opin Drug Discov 12:261–270CrossRefPubMedGoogle Scholar
  2. Araszkiewicz A, Zozulinska-Ziolkiewicz D (2016) Retinal neurodegeneration in the course of diabetes-pathogenesis and clinical perspective. Curr Neuropharmacol 14:805–809CrossRefPubMedPubMedCentralGoogle Scholar
  3. Arfuzir NN, Lambuk L, Jafri AJ, Agarwal R, Iezhitsa I, Sidek S, Agarwal P, Bakar NS, Kutty MK, Yusof AP, Krasilnikova A, Spasov A, Ozerov A, Mohd Ismail N (2016) Protective effect of magnesium acetyltaurate against endothelin-induced retinal and optic nerve injury. Neuroscience 325:153–164CrossRefPubMedGoogle Scholar
  4. Arfuzir NNN, Agarwal R, Iezhitsa I, Agarwal P, Sidek S, Spasov A, Ozerov A, Mohd Ismail N (2018) Effect of magnesium acetyltaurate and taurine on endothelin1-induced retinal nitrosative stress in rats. Curr Eye Res 43:1032–1040CrossRefGoogle Scholar
  5. Awai M, Koga T, Inomata Y, Oyadomari S, Gotoh T, Mori M, Tanihara H (2006) NMDA-induced retinal injury is mediated by an endoplasmic reticulum stress-related protein, CHOP/GADD153. J Neurochem 96:43–52CrossRefPubMedGoogle Scholar
  6. Belluzzi O, Puopolo M, Benedusi M, Kratskin I (2004) Selective neuroinhibitory effects of taurine in slices of rat main olfactory bulb. Neuroscience 124:929–944CrossRefPubMedGoogle Scholar
  7. Boşgelmez II, Güvendik G (2004) Effects of taurine on oxidative stress parameters and chromium levels altered by acute hexavalent chromium exposure in mice kidney tissue. Biol Trace Elem Res 102:209–225CrossRefPubMedGoogle Scholar
  8. Chan CY, Sun HS, Shah SM, Agovic MS, Ho I, Friedman E, Banerjee SP (2013) Direct interaction of taurine with the NMDA glutamate receptor subtype via multiple mechanisms. Adv Exp Med Biol 775:45–52CrossRefPubMedGoogle Scholar
  9. Chan CY, Singh I, Magnuson H, Zohaib M, Bakshi KP, Le François B, Anazco-Ayala A, Lee EJ, Tom A, YeeMon K, Ragnauth A, Friedman E, Banerjee SP (2015) Taurine targets the GluN2b-containing NMDA receptor subtype. Adv Exp Med Biol 803:531–544CrossRefPubMedGoogle Scholar
  10. Choi DW (1988) Glutamate neurotoxicity and diseases of the nervous system. Neuron 1:623–634CrossRefPubMedGoogle Scholar
  11. Dell RB, Holleran S, Ramakrishnan R (2002) Sample size determination. ILAR J 43:207–213CrossRefPubMedPubMedCentralGoogle Scholar
  12. El Idrissi A, Trenkner E (1999) Growth factors and taurine protect against excitotoxicity by stabilizing calcium homeostasis and energy metabolism. J Neurosci 19:9459–9468CrossRefPubMedGoogle Scholar
  13. Forder JP, Tymianski M (2009) Postsynaptic mechanisms of excitotoxicity: involvement of postsynaptic density proteins, radicals, and oxidant molecules. Neuroscience 158:293–300CrossRefPubMedGoogle Scholar
  14. Hansen SH, Grunnet N (2013) Taurine, glutathione and bioenergetics. Adv Exp Med Biol 776:3–12CrossRefPubMedGoogle Scholar
  15. Ishikawa M (2013) Abnormalities in glutamate metabolism and excitotoxicity in the retinal diseases. Scientifica (Cairo) 2013:528940Google Scholar
  16. Jafri AJA, Arfuzir NNN, Lambuk L, Iezhitsa I, Agarwal R, Agarwal P, Razali N, Krasilnikova A, Kharitonova M, Demidov V, Serebryansky E, Skalny A, Spasov A, Yusof APM, Ismail NM (2017) Protective effect of magnesium acetyltaurate against NMDA-induced retinal damage involves restoration of minerals and trace elements homeostasis. J Trace Elem Med Biol 39:147–154CrossRefPubMedGoogle Scholar
  17. Jafri AJA, Agarwal R, Iezhitsa I, Agarwal P, Spasov A, Ozerov A, Ismail NM (2018) Protective effect of magnesium acetyltaurate and taurine against NMDA-induced retinal damage involves reduced nitrosative stress. Mol Vis 24:495–508PubMedPubMedCentralGoogle Scholar
  18. Lambuk L, Jafri AJ, Arfuzir NN, Iezhitsa I, Agarwal R, Rozali KN, Agarwal P, Bakar NS, Kutty MK, Yusof AP, Krasilnikova A, Spasov A, Ozerov A, Ismail NM (2017) Neuroprotective effect of magnesium acetyltaurate against NMDA-induced excitotoxicity in rat retina. Neurotox Res 31:31–45CrossRefPubMedGoogle Scholar
  19. Lambuk L, Iezhitsa I, Agarwal R, Bakar NS, Agarwal P, Ismail NM (2018) Antiapoptotic effect of taurine against NMDA-induced retinal excitotoxicity in rats. NeuroToxicology 70:62–71CrossRefPubMedGoogle Scholar
  20. Leon R, Wu H, Jin Y, Wei J, Buddhala C, Prentice H, Wu JY (2009) Protective function of taurine in glutamate-induced apoptosis in cultured neurons. J Neurosci Res 87:1185–1194CrossRefPubMedGoogle Scholar
  21. Menéndez N, Solís JM, Herreras O, Galarreta M, Conejero C, Martín del Río R (1993) Taurine release evoked by NMDA receptor activation is largely dependent on calcium mobilization from intracellular stores. Eur J Neurosci 5:1273–1279CrossRefPubMedGoogle Scholar
  22. Mohd Lazaldin MA, Iezhitsa I, Agarwal R, Bakar NS, Agarwal P, Mohd Ismail N (2018) Time- and dose-related effects of amyloid beta1–40 on retina and optic nerve morphology in rats. Int J Neurosci 20:1–14Google Scholar
  23. Nguyen TT, Bhattarai JP, Park SJ, Han SK (2013) Activation of glycine and extrasynaptic GABA(A) receptors by taurine on the substantia gelatinosa neurons of the trigeminal subnucleus caudalis. Neural Plast 2013:740581CrossRefPubMedPubMedCentralGoogle Scholar
  24. Nonaka H, Tsujino T, Watari Y, Emoto N, Yokoyama M (2001) Taurine prevents the decrease in expression and secretion of extracellular superoxide dismutase induced by homocysteine: amelioration of homocysteine-induced endoplasmic reticulum stress by taurine. Circulation 104:1165–1170CrossRefPubMedGoogle Scholar
  25. Oliveira MW, Minotto JB, de Oliveira MR, Zanotto-Filho A, Behr GA, Rocha RF, Moreira JC, Klamt F (2010) Scavenging and antioxidant potential of physiological taurine concentrations against different reactive oxygen/nitrogen species. Pharmacol Rep 62:185–193CrossRefPubMedGoogle Scholar
  26. Pushpakiran G, Mahalakshmi K, Anuradha CV (2004) Taurine restores ethanol-induced depletion of antioxidants and attenuates oxidative stress in rat tissues. Amino Acids 27:91–96CrossRefPubMedGoogle Scholar
  27. Razali N, Agarwal R, Agarwal P, Tripathy M, Kapitonova MY, Kutty MK, Smirnov A, Khalid Z, Ismail NM (2016) Topical trans-resveratrol ameliorates steroid-induced anterior and posterior segment changes in rats. Exp Eye Res 143:9–16CrossRefPubMedGoogle Scholar
  28. Reyes RC, Brennan AM, Shen Y, Baldwin Y, Swanson RA (2012) Activation of neuronal NMDA receptors induces superoxide-mediated oxidative stress in neighboring neurons and astrocytes. J Neurosci 32:12973–12978CrossRefPubMedPubMedCentralGoogle Scholar
  29. Ripps H, Shen W (2012) Review: taurine: a “very essential” amino acid. Mol Vis 18:2673–2686PubMedPubMedCentralGoogle Scholar
  30. Yarbrough GG, Singh DK, Taylor DA (1981) Neuropharmacological characterization of a taurine antagonist. J Pharmacol Exp Ther 219:604–613PubMedGoogle Scholar
  31. Yu J, Kim AK (2009) Effect of taurine on antioxidant enzyme system in B16F10 melanoma cells. Adv Exp Med Biol 643:491–499CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Center for Neuroscience Research, Faculty of MedicineUniversiti Teknologi MARA Sungai Buloh CampusSungai BulohMalaysia
  2. 2.I-PPerForM, Faculty of MedicineUniversiti Teknologi MARA Sungai Buloh CampusSungai BulohMalaysia
  3. 3.Research Institute of PharmacologyVolgograd State Medical UniversityVolgogradRussia
  4. 4.Faculty of MedicineInternational Medical University, IMU Clinical SchoolSerembanMalaysia

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