Skip to main content

Advertisement

SpringerLink
Log in

Taurine mitigates nitrite-induced methemoglobin formation and oxidative damage in human erythrocytes

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Nitrite is present as a noxious contaminant in drinking water and causes oxidative damage in various tissues of humans and animals. It is a well-known methemoglobin-forming agent that has been shown to damage blood cells. The protective effect of taurine, a semi-essential sulfur-containing amino acid, was studied on sodium nitrite (NaNO2)-induced oxidative damage in human erythrocytes. Erythrocytes were incubated with NaNO2, in the presence and absence of taurine, and changes in oxidative stress parameters determined. Pretreatment with taurine significantly ameliorated NaNO2-induced oxidative damage to lipids, proteins, and plasma membrane. It also reduced the NaNO2-induced increase in methemoglobin levels and ROS production. Taurine improved the antioxidant capacity of cells, restored the alterations in the activities of various metabolic enzymes, and prevented morphological changes in erythrocytes. Thus, taurine can be potentially used as a protective agent against the damaging effects of nitrite.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

ABTS:

2,2′-Azino-bis(3-ethylbenzothiazoline-6-sulfonic acid)

AMP:

Adenosine 5′-monophosphate

AO:

Antioxidant

ATP:

Adenosine 5′-triphosphate

ATPase:

Adenosine triphosphatase

CUPRAC:

Cupric reducing antioxidant capacity

DCF:

2,7-Dichlorofluorescein

DCFH-DA:

2,7-Dichlorodihydrofluorescein diacetate

DHE:

Dihydroethidium

GSH:

Reduced glutathione

GSSG:

Oxidized glutathione

Hb:

Hemoglobin

H2O2 :

Hydrogen peroxide

MetHb:

Methemoglobin

NAD(P)+ and NAD(P)H:

Oxidized and reduced nicotinamide adenine dinucleotide (phosphate)

Na,K-ATPase:

Sodium potassium ATPase

NaNO2 :

Sodium nitrite

NO:

Nitric oxide

PBS:

Phosphate-buffered saline

ROS:

Reactive oxygen species

SOD:

Cu,Zn superoxide dismutase

TBARS:

Thiobarbituric acid reactive substances

References

  • Adedara IA, Ojuade TJD, Olabiyi BF et al (2016) Taurine ameliorates renal oxidative damage and thyroid dysfunction in rats chronically exposed to fluoride. Biol Trace Elem Res. doi:10.1007/s12011-016-0784-2

  • Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126

    Article  CAS  Google Scholar 

  • Anderson ME (1998) Glutathione: an overview of biosynthesis and modulation. Chem Biol Interact 111–112:1–14

    Article  Google Scholar 

  • Ansari FA, Mahmood R (2016) Sodium nitrite enhances generation of reactive oxygen species that decrease antioxidant power and inhibit plasma membrane redox system of human erythrocytes. Cell Biol Int 40:887–894. doi:10.1002/cbin.10628

    Article  CAS  Google Scholar 

  • Ansari FA, Ali SN, Mahmood R (2015) Sodium nitrite-induced oxidative stress causes membrane damage, protein oxidation, lipid peroxidation and alters major metabolic pathways in human erythrocytes. Toxicol in Vitro 29:1878–1886. doi:10.1016/j.tiv.2015.07.022

    Article  CAS  Google Scholar 

  • Antonelou MH, Kriebardis AG, Velentzas AD et al (2011) Oxidative stress-associated shape transformation and membrane proteome remodeling in erythrocytes of end stage renal disease patients on hemodialysis. J Proteome 74:2441–2452. doi:10.1016/j.jprot.2011.04.009

    Article  CAS  Google Scholar 

  • Apak R, Güçlü K, Demirata B et al (2007) Comparative evaluation of various total antioxidant capacity assays applied to phenolic compounds with the CUPRAC assay. Molecules 12:1496–1547

    Article  CAS  Google Scholar 

  • Aruoma OI, Halliwell B, Hoey BM, Butler J (1988) The antioxidant action of taurine, hypotaurine and their metabolic precursors. Biochem J 256:251–255

    Article  CAS  Google Scholar 

  • Balasubramaniam P, Malathi A (1992) Comparative study of hemoglobin estimated by Drabkin’s and Sahli’s methods. J Postgrad Med 38:8–9

    CAS  Google Scholar 

  • Benesch RE, Benesch R, Yung S (1973) Equations for the spectrophotometric analysis of hemoglobin mixtures. Anal Biochem 55:245–248. doi:10.1016/0003-2697(73)90309-6

    Article  CAS  Google Scholar 

  • Bonting SL, Simon KA, Hawkins NM (1961) Studies on sodium-potassium-activated adenosine triphosphatase: I. Quantitative distribution in several tissues of the cat. Arch Biochem Biophys 95:416–423. doi:10.1016/0003-9861(61)90170-9

    Article  CAS  Google Scholar 

  • Bryan NS, Loscalzo J (eds) (2011) Nitrite and nitrate in human health and disease. Humana Press, Totowa, NJ

    Google Scholar 

  • Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Methods Enzymol 52:302–310

    Article  CAS  Google Scholar 

  • Butler AR, Feelisch M (2008) Therapeutic uses of inorganic nitrite and nitrate from the past to the future. Circulation 117:2151–2159

    Article  CAS  Google Scholar 

  • Çekiç SD, Kara N, Tütem E et al (2012) Protein-incorporated serum total antioxidant capacity measurement by a modified CUPRAC (cupric reducing antioxidant capacity) method. Anal Lett 45:754–763. doi:10.1080/00032719.2011.653901

    Article  Google Scholar 

  • Choi EJ, Tang Y, Lee CB et al (2015) Investigation of antioxidant and anticancer potential of taurine by means of multiple chemical and biological assays. Adv Exp Med Biol 803:179–189. doi:10.1007/978-3-319-15126-7_16

    Article  Google Scholar 

  • Chow CK, Hong CB (2002) Dietary vitamin E and selenium and toxicity of nitrite and nitrate. Toxicology 180:195–207

    Article  CAS  Google Scholar 

  • Chui JSW, Poon WT, Chan KC et al (2005) Nitrite-induced methaemoglobinaemia—aetiology, diagnosis and treatment. Anaesthesia 60:496–500. doi:10.1111/j.1365-2044.2004.04076.x

    Article  CAS  Google Scholar 

  • Cozzi R, Ricordy R, Bartolini F et al (1995) Taurine and ellagic acid: two differently-acting natural antioxidants. Environ Mol Mutagen 26:248–254

    Article  CAS  Google Scholar 

  • Crane RK, Sols A (1953) The association of hexokinase with particulate fractions of brain and other tissue homogenates. J Biol Chem 203:273–292

    CAS  Google Scholar 

  • Dalle-Donne I, Aldini G, Carini M et al (2006) Protein carbonylation, cellular dysfunction, and disease progression. J Cell Mol Med 10:389–406

    Article  CAS  Google Scholar 

  • Das J, Sil PC (2012) Taurine ameliorates alloxan-induced diabetic renal injury, oxidative stress-related signaling pathways and apoptosis in rats. Amino Acids 43:1509–1523. doi:10.1007/s00726-012-1225-y

    Article  CAS  Google Scholar 

  • Ellman GL, Courtney KD, Andres V Jr, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95. doi:10.1016/0006-2952(61)90145-9

    Article  CAS  Google Scholar 

  • Erman F, Balkan J, Cevikbaş U et al (2004) Betaine or taurine administration prevents fibrosis and lipid peroxidation induced by rat liver by ethanol plus carbon tetrachloride intoxication. Amino Acids 27:199–205. doi:10.1007/s00726-004-0105-5

    Article  CAS  Google Scholar 

  • Escobar JA, Rubio MA, Lissi EA (1996) SOD and catalase inactivation by singlet oxygen and peroxyl radicals. Free Radic Biol Med 20:285–290

    Article  CAS  Google Scholar 

  • Feng T, Liu P, Zhang Z et al (2016) Combination of DFP and taurine counteracts the aluminum-induced alterations in oxidative stress and ATPase in cortex and blood of rats. Biol Trace Elem Res. doi:10.1007/s12011-016-0692-5

  • Flohé L, Günzler WA (1984) Assays of glutathione peroxidase. Methods Enzymol 105:114–120

    Article  Google Scholar 

  • Furfaro AL, Nitti M, Marengo B et al (2012) Impaired synthesis contributes to diabetes-induced decrease in liver glutathione. Int J Mol Med 29:899–905. doi:10.3892/ijmm.2012.915

    CAS  Google Scholar 

  • Galloway JN, Aber JD, Erisman JW et al (2003) The nitrogen cascade. Bioscience 53:341–356

    Article  Google Scholar 

  • Gaucher D, Arnault E, Husson Z et al (2012) Taurine deficiency damages retinal neurones: cone photoreceptors and retinal ganglion cells. Amino Acids 43:1979–1993. doi:10.1007/s00726-012-1273-3

    Article  CAS  Google Scholar 

  • Gay C, Gebicki JM (2000) A critical evaluation of the effect of sorbitol on the ferric-xylenol orange hydroperoxide assay. Anal Biochem 284:217–220. doi:10.1006/abio.2000.4696

    Article  CAS  Google Scholar 

  • Gürer H, Özgünes H, Saygin E, Ercal N (2001) Antioxidant effect of taurine against lead-induced oxidative stress. Arch Environ Contam Toxicol 41:397–402. doi:10.1007/s002440010265

    Article  Google Scholar 

  • Hamaguchi T, Azuma J, Schaffer S (1991) Interaction of taurine with methionine: inhibition of myocardial phospholipid methyltransferase. J Cardiovasc Pharmacol 18:224–230

    Article  CAS  Google Scholar 

  • Hissin PJ, Hilf R (1976) A fluorometric method for determination of oxidized and reduced glutathione in tissues. Anal Biochem 74:214–226. doi:10.1016/0003-2697(76)90326-2

    Article  CAS  Google Scholar 

  • Jansson EA, Huang L, Malkey R et al (2008) A mammalian functional nitrate reductase that regulates nitrite and nitric oxide homeostasis. Nat Chem Biol 4:411–417. doi:10.1038/nchembio.92

    Article  CAS  Google Scholar 

  • Jarolim P, Lahav M, Liu SC, Palek J (1990) Effect of hemoglobin oxidation products on the stability of red cell membrane skeletons and the associations of skeletal proteins: correlation with a release of hemin. Blood 76:2125–2131

    CAS  Google Scholar 

  • Jia R, Han C, Lei JL et al (2015) Effects of nitrite exposure on haematological parameters, oxidative stress and apoptosis in juvenile turbot (Scophthalmus maximus). Aquat Toxicol 169:1–9. doi:10.1016/j.aquatox.2015.09.016

    Article  CAS  Google Scholar 

  • Keller A, Mohamed A, Dröse S et al (2004) Analysis of dichlorodihydrofluorescein and dihydrocalcein as probes for the detection of intracellular reactive oxygen species. Free Radic Res 38:1257–1267. doi:10.1080/10715760400022145

    Article  CAS  Google Scholar 

  • Khundmiri SJ, Asghar M, Khan F et al (2004) Effect of ischemia and reperfusion on enzymes of carbohydrate metabolism in rat kidney. J Nephrol 17:377–383

    CAS  Google Scholar 

  • Kim-Shapiro DB, Schechter AN, Gladwin MT (2006) Unraveling the reactions of nitric oxide, nitrite, and hemoglobin in physiology and therapeutics. Arterioscler Thromb Vasc Biol 26:697–705. doi:10.1161/01.ATV.0000204350.44226.9a

    Article  CAS  Google Scholar 

  • Kuma F, Ishizawa S, Hirayama K, Nakajima H (1972) Studies on methemoglobin reductase. I. Comparative studies of diaphorses from normal and methemoglobinemic erythocytes. J Biol Chem 247:550–555

    CAS  Google Scholar 

  • Levine RL, Garland D, Oliver CN et al (1990) Determination of carbonyl content in oxidatively modified proteins. Methods Enzymol 186:464–478

    Article  CAS  Google Scholar 

  • Lissi E (1998) Autocatalytic oxidation of hemoglobin by nitrite: a possible mechanism. Free Radic Biol Med 24:1535–1536

    Article  CAS  Google Scholar 

  • Lundberg JO, Weitzberg E, Gladwin MT (2008) The nitrate-nitrite-nitric oxide pathway in physiology and therapeutics. Nat Rev Drug Discov 7:156–167. doi:10.1038/nrd2466

    Article  CAS  Google Scholar 

  • Manna P, Sinha M, Sil PC (2009) Taurine plays a beneficial role against cadmium-induced oxidative renal dysfunction. Amino Acids 36:417–428. doi:10.1007/s00726-008-0094-x

    Article  CAS  Google Scholar 

  • Mannervik B, Carlberg I (1985) Glutathione reductase. Methods Enzymol 113:484–490

    Article  Google Scholar 

  • Marklund S, Marklund G (1974) Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem FEBS 47:469–474

    Article  CAS  Google Scholar 

  • Marouf BH, Aziz TA, Zalzala MH, Hussain SA (2010) Free radical scavenging activity of benfotiamine in nitrite-induced hemoglobin oxidation and membrane fragility models. J Pharm Biomed Sci 1:13–18

    Google Scholar 

  • McNally B, Griffin JL, Roberts LD (2016) Dietary inorganic nitrate: from villain to hero in metabolic disease? Mol Nutr Food Res 60:67–78. doi:10.1002/mnfr.201500153

    Article  CAS  Google Scholar 

  • Mensinga TT, Speijers GJ, Meulenbelt J (2003) Health implications of exposure to environmental nitrogenous compounds. Toxicol Rev 22:41–51

    Article  CAS  Google Scholar 

  • Mohrenweiser HW, Novotny JE (1982) ACP1GUA-1—a low-activity variant of human erythrocyte acid phosphatase: association with increased glutathione reductase activity. Am J Hum Genet 34:425–433

    CAS  Google Scholar 

  • Nandhini TA, Anuradha CV (2003) Inhibition of lipid peroxidation, protein glycation and elevation of membrane ion pump activity by taurine in RBC exposed to high glucose. Clin Chim Acta 336:129–135

    Article  CAS  Google Scholar 

  • Pan C, Giraldo GS, Prentice H, Wu J-Y (2010) Taurine protection of PC12 cells against endoplasmic reticulum stress induced by oxidative stress. J Biomed Sci 17:1–7. doi:10.1186/1423-0127-17-S1-S17

    Article  Google Scholar 

  • Peacock A, Martin FH, Carr A (2013) Energy drink ingredients. Contribution of caffeine and taurine to performance outcomes. Appetite 64:1–4. doi:10.1016/j.appet.2012.12.021

    Article  Google Scholar 

  • Pedersen RC, Berry AJ (1977) Sensitive, optimized assay for serum AMP deaminase. Clin Chem 23:1726–1733

    CAS  Google Scholar 

  • Percy MJ, McFerran NV, Lappin TRJ (2005) Disorders of oxidised haemoglobin. Blood Rev 19:61–68. doi:10.1016/j.blre.2004.02.001

    Article  CAS  Google Scholar 

  • Pushpakiran G, Mahalakshmi K, Anuradha CV (2004) Taurine restores ethanol-induced depletion of antioxidants and attenuates oxidative stress in rat tissues. Amino Acids 27:91–96. doi:10.1007/s00726-004-0066-8

    Article  CAS  Google Scholar 

  • Qiao M, Liu P, Ren X et al (2015) Potential protection of taurine on antioxidant system and ATPase in brain and blood of rats exposed to aluminum. Biotechnol Lett 37:1579–1584. doi:10.1007/s10529-015-1846-9

    Article  CAS  Google Scholar 

  • Re R, Pellegrini N, Proteggente A et al (1999) Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radic Biol Med 26:1231–1237

    Article  CAS  Google Scholar 

  • Redmond HP, Wang JH, Bouchier-Hayes D (1996) Taurine attenuates nitric oxide- and reactive oxygen intermediate-dependent hepatocyte injury. Arch Surg 131:1280–1288

    Article  CAS  Google Scholar 

  • Refsgaard HHF, Tsai L, Stadtman ER (2000) Modifications of proteins by polyunsaturated fatty acid peroxidation products. Proc Natl Acad Sci U S A 97:611–616

    Article  CAS  Google Scholar 

  • Ripps H, Shen W (2012) Review: taurine: a “very essential” amino acid. Mol Vis 18:2673–2686

    CAS  Google Scholar 

  • Schaffer SW, Azuma J, Madura JD (1995) Mechanisms underlying taurine-mediated alterations in membrane function. Amino Acids 8:231–246. doi:10.1007/BF00806821

    Article  CAS  Google Scholar 

  • Schaffer SW, Ju Jong C, Ramila KC, Azuma J (2010) Physiological roles of taurine in heart and muscle. J Biomed Sci 17:S2. doi:10.1186/1423-0127-17-S1-S2

    Article  Google Scholar 

  • Schütt F, Aretz S, Auffarth GU, Kopitz J (2012) Moderately reduced ATP levels promote oxidative stress and debilitate autophagic and phagocytic capacities in human RPE cells. Investig Opthalmology Vis Sci 53:5354. doi:10.1167/iovs.12-9845

    Article  Google Scholar 

  • Sedlak J, Lindsay RH (1968) Estimation of total, protein-bound, and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal Biochem 25:192–205

    Article  CAS  Google Scholar 

  • Shonk CE, Boxer GE (1964) Enzyme patterns in human tissues. I. Methods for the determination of glycolytic enzymes. Cancer Res 24:709–721

    CAS  Google Scholar 

  • Snyder SL, Sobocinski PZ (1975) An improved 2,4,6-trinitrobenzenesulfonic acid method for the determination of amines. Anal Biochem 64:284–288. doi:10.1016/0003-2697(75)90431-5

    Article  CAS  Google Scholar 

  • Soldatow VY, LeCluyse EL, Griffith LG, Rusyn I (2013) In vitro models for liver toxicity testing. Toxicol Res 2:23–39. doi:10.1039/C2TX20051A

    Article  CAS  Google Scholar 

  • Spengler MI, Svetaz MJ, Leroux MB et al (2014) Lipid peroxidation affects red blood cells membrane properties in patients with systemic lupus erythematosus. Clin Hemorheol Microcirc 58:489–495. doi:10.3233/CH-131716

    CAS  Google Scholar 

  • Tamura T, Stadtman TC (1996) A new selenoprotein from human lung adenocarcinoma cells: purification, properties, and thioredoxin reductase activity. Proc Natl Acad Sci 93:1006–1011

    Article  CAS  Google Scholar 

  • Tavazzi B, Amorini AM, Fazzina G et al (2001) Oxidative stress induces impairment of human erythrocyte energy metabolism through the oxygen radical-mediated direct activation of AMP-deaminase. J Biol Chem 276:48083–48092. doi:10.1074/jbc.M101715200

    Article  CAS  Google Scholar 

  • Vatassery GT, SantaCruz KS, DeMaster EG et al (2004) Oxidative stress and inhibition of oxidative phosphorylation induced by peroxynitrite and nitrite in rat brain subcellular fractions. Neurochem Int 45:963–970. doi:10.1016/j.neuint.2004.06.009

    Article  CAS  Google Scholar 

  • Wojtala A, Bonora M, Malinska D et al (2014) Methods to monitor ROS production by fluorescence microscopy and fluorometry. Methods Enzymol 542:243–262. doi:10.1016/B978-0-12-416618-9.00013-3

    Article  CAS  Google Scholar 

  • Yalçinkaya S, Unlüçerçi Y, Giriş M et al (2009) Oxidative and nitrosative stress and apoptosis in the liver of rats fed on high methionine diet: protective effect of taurine. Nutrition 25:436–444. doi:10.1016/j.nut.2008.09.017

    Article  Google Scholar 

  • Yu J, Kim AK (2009) Effect of taurine on antioxidant enzyme system in B16F10 melanoma cells. Adv Exp Med Biol 643:491–499. doi:10.1007/978-0-387-75681-3_51

    Article  CAS  Google Scholar 

  • Zhou L, Zahid M, Anwar MM et al (2016) Suggestive evidence for the induction of colonic aberrant crypts in mice fed sodium nitrite. Nutr Cancer 68:105–112. doi:10.1080/01635581.2016.1102298

    Article  CAS  Google Scholar 

  • Zulli A (2011) Taurine in cardiovascular disease. Curr Opin Clin Nutr Metab Care 14:57–60. doi:10.1097/MCO.0b013e328340d863

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We acknowledge the financial support to the department from the University Grants Commission (SAP-DRS-III) and DST-FIST. FAA is the recipient of UGC-CSIR senior research fellowship (NET-SRF).

Author information

Authors and Affiliations

  1. Department of Biochemistry, Faculty of Life Sciences, Aligarh Muslim University, Aligarh, U.P., 202002, India

    Fariheen Aisha Ansari, Shaikh Nisar Ali & Riaz Mahmood

Authors
  1. Fariheen Aisha Ansari
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Shaikh Nisar Ali
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Riaz Mahmood
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Riaz Mahmood.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Responsible editor: Philippe Garrigues

Highlights

• Sodium nitrite induces oxidative stress in human erythrocytes.

• Taurine significantly lowered nitrite-induced methemoglobin formation and ROS production.

• Taurine also protected the lowering of antioxidant defense systems.

• Antioxidant capacity of cells was restored.

• Taurine prevented nitrite-induced alterations in erythrocyte morphology.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ansari, F.A., Ali, S.N. & Mahmood, R. Taurine mitigates nitrite-induced methemoglobin formation and oxidative damage in human erythrocytes. Environ Sci Pollut Res 24, 19086–19097 (2017). https://doi.org/10.1007/s11356-017-9512-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-017-9512-5

Keywords

Search

Navigation