Skip to main content
SpringerLink
Log in

Mechanisms underlying taurine-mediated alterations in membrane function

  • Published:
Amino Acids Aims and scope Submit manuscript

Summary

Taurine mediates a plethora of membrane-linked effects in excitable tissues. To account for these multiple actions, four hypotheses have been proposed. One theory is based on the observation that taurine diminishes the inflammatory response of several cytotoxic oxidants. It is proposed that a reduction in the extent of membrane oxidative injury contributes to these cytoprotective actions. The second theory maintains that alterations in protein phosphorylation may underlie certain effects of taurine, particularly its effect on calcium transport. The third hypothesis assumes that the interaction of taurine with the neutral phospholipids leads to altered membrane calcium binding and function. The final theory ties the actions of taurine to inhibition of phospholipid N-methylation and the resulting changes in membrane composition and structure. While each of these hypotheses has merit, none of them can fully explain the membrane actions of taurine. Further studies are required to ascertain the importance of each theory.

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

Similar content being viewed by others

References

  • Alvarez JG, Storey BT (1983) Taurine, hypotaurine, epinephrine and albumin inhibit lipid peroxidation in rabbit spermatozoa and protect against loss of motility. Biol Reprod 29: 548–555

    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

    Google Scholar 

  • Banks MA, Porter DW, Martin WG, Castranova V (1991) Ozone-induced lipid peroxidation and membrane leakage in isolated rat alveolar macrophages: protective effects of taurine. J Nutr Biochem 2: 308–313

    Google Scholar 

  • Brown MF, Seelig J (1977) Ion-induced changes in head group conformation of lecithin bilayers. Nature 269: 721–723

    Google Scholar 

  • Calvez J-Y, Zachowski A, Herrmann A, Morrot G, Devaux PF (1988) Asymmetric distribution of phospholipids in spectrin-poor erythrocyte vesicles. Biochemistry 27: 5666–5670

    Google Scholar 

  • Cantin AM (1994) Taurine modulation of hypochlorous acid-induced lung epithelial cell injury in vitro. J Clin Invest 93: 606–614

    Google Scholar 

  • Chapman RA, Suleiman M-S, Earm YE (1993) Taurine and the heart. Cardiovasc Res 27: 358–363

    Google Scholar 

  • Chovan JP, Kulakowski EC, Benson BW, Schaffer SW (1979) Taurine enhancement of calcium binding to rat heart sarcolemma. Biochim Biophys Acta 551: 129–136

    Google Scholar 

  • Chovan JP, Kulakowski EC, Sheakowski S, Schaffer SW (1980) Calcium regulation by the low-affinity taurine binding sites of cardiac sarcolemma. Mol Pharmacol 17: 295–300

    Google Scholar 

  • Crews FT (1985) Phospholipid methylation and membrane function. In: Kuo JF (ed) Phospholipids and cellular regulation. CRC Press, Boca Raton, pp 131–158

    Google Scholar 

  • Cullis PR, Hope MJ, Tilcock CPS (1986) Lipid polymorphism and the roles of lipids in membranes. Chem Physics Lipids 40: 127–144

    Google Scholar 

  • DeBoeck H, Zidovetzki R (1989) Effects of diacylglycerols on the structure of phosphatidylcholine bilayers: A2H and31P nmr study. Biochemistry 28: 7439–7446

    Google Scholar 

  • Ekerdt R, Papahadjopoulos D (1982) Intermembrane contact affects calcium binding to phospholipid vesicles. Proc Natl Acad Sci USA 79: 2273–2277

    Google Scholar 

  • Epand RM (1990) Relationship of phospholipid hexagonal phases to biological phenomena. Biochem Cell Biol 68: 17–23

    Google Scholar 

  • Ganguly PK, Panagia V, Okumura K, Dhalla NS (1985) Activation of Ca2+-stimulated ATPase by phospholipid N-methylation in cardiac sarcoplasmic reticulum. Biochem Biophys Res Commun 130: 472–478

    Google Scholar 

  • Goldberg EM, Lester DS, Borchardt DB, Zidovetzki R (1994) Effects of diacylglycerols and Ca2+ on structure of phosphatidylcholine/phosphatidylserine bilayers. Biophys J 66: 382–393

    Google Scholar 

  • Gopalakrishna R, Chen ZH, Gundimeda U (1993) Nitric oxide and nitric oxide-generating agents induce a reversible inactivation of protein kinase C activity and phorbol ester binding. J Biol Chem 268: 27180–27185

    Google Scholar 

  • Gordon RE, Shaked AA, Solano DF (1986) Taurine protects hamster bronchioles from acute NO2-induced alterations. Am J Pathol 125: 585–600

    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

    Google Scholar 

  • Harada H, Cusack, BJ, Olson RD, Stroo W, Azuma J, Hamaguchi T, Schaffer SW (1990) Taurine deficiency and doxorubicin: interaction with the cardiac sarcolemmal calcium pump. Biochem Pharmacol 39: 745–751

    Google Scholar 

  • Hayes KC (1988) Taurine nutrition. Nutr Res Rev 1: 99–113

    Google Scholar 

  • Hayes KC, Carey RE, Schmidt SY (1975) Retinal degeneration associated with taurine deficiency in the cat. Science 188: 949–951

    Google Scholar 

  • Hui SW, Boni LT, Stewart TP, Isac T (1983) Identification of phosphatidylserine and phosphatidylcholine in calcium-induced phase separated domains. Biochemistry 22: 3511–3516

    Google Scholar 

  • Huxtable RJ (1987) From heart to hypothesis: a mechanism for the calcium modulatory actions of taurine. In: Huxtable RJ, Franconi F, Giotti A (eds) The biology of taurine: methods and mechanisms. Plenum Press, New York, pp 371–388

    Google Scholar 

  • Huxtable RJ (1992) The physiological actions of taurine. Physiol Rev 72: 101–163

    Google Scholar 

  • Huxtable R, Bressler R (1973) Effect of taurine on a muscle intracellular membrane. Biochim Biophys Acta 323: 573–583

    Google Scholar 

  • Ihara Y, Takahashi K, Harada H, Sawamura A, Schaffer S, Azuma J (1992) Taurine attenuates contracture induced by perfusion with low sodium, high calcium medium in chick hearts. In: Lombardini JB, Schaffer SW, Azuma J (eds) Nutritional value and mechanisms of action. New York, pp 145–152 (Adv Exp Med Biol, vol 315) Plenum Press

    Google Scholar 

  • Imaki H, Moretz RC, Wisniewski HM, Sturman JA (1986) Feline materal taurine deficiency: effects on retina and tapetum of the offspring. Dev Neurosci 8: 160–181

    Google Scholar 

  • Irving CS, Hammer BE, Danyluk SS, Klein PD (1980)13C nuclear magnetic resonance study of the complexation of calcium by taurine. J Inorganic Biochem 13: 137–150

    Google Scholar 

  • Kirk GL, Gruner SM, Stein DL (1984) A thermodynamic model of the lamellar to inverse hexagonal phase transition of lipid membrane-water systems. Biochemistry 23: 1093–1102

    Google Scholar 

  • Kulakowski EC, Maturo J, Schaffer SW (1978) The identification of taurine receptors from rat heart sarcolemma. Biochem Biophys Res Commun 80: 936–941

    Google Scholar 

  • Kulakowski EC, Maturo J, Schaffer SW (1981) Solubilization and characterization of cardiac sarcolemmal taurine-binding proteins. Arch Biochem Biophys 210: 204–209

    Google Scholar 

  • Lampson WG, Kramer JH, Schaffer SW (1983) Potentiation of the actions of insulin by taurine. Can J Physiol Pharmacol 61: 457–463

    Google Scholar 

  • Langer GA (1978) The structure and function of the myocardial cell surface. Am J Physiol 235: H461-H468

    Google Scholar 

  • Langer GA, Rich TL (1993) Further characterization of the Na-Ca exchange-dependent Ca compartment in rat ventricular cells. Am J Physiol 265: C556-C561

    Google Scholar 

  • Li Y-P, Lombardini JB (1991a) Inhibition by taurine of the phosphorylation of specific synaptosomal proteins in the rat cortex: effects of taurine on the stimulation of calcium uptake in mitochondria and inhibition of phosphoinositide turnover. Brain Res 553: 89–96

    Google Scholar 

  • Li Y-P, Lombardini JB (1991b) Taurine inhibits protein kinase C-catalyzed phosphorylation of specific proteins in a rat cortical P2 fraction. J Neurochem 56: 1747–1753

    Google Scholar 

  • Liebowitz SM, Lombardini JB, Allen CI (1989) Sulfone analogues of taurine as modifiers of calcium uptake and protein phosphorylation in rat retina. Biochem Pharmacol 38: 399–406

    Google Scholar 

  • Lin YY, Wright CE, Zagorski M, Nakanishi K (1988)13C-NMR study of taurine and chlorotaurine in human cells. Biochim Biophys Acta 969: 242–248

    Google Scholar 

  • Lombardini JB (1985) Taurine effects on the transition temperature in Arrhenius plots of ATP-dependent calcium ion uptake in rat retinal membrane preparations. Biochem Pharmacol 34: 3741–3745

    Google Scholar 

  • Lombardini JB (1991) Taurine: retinal function. Brain Res Rev 16: 151–169

    Google Scholar 

  • Lombardini JB (1992a) Effects of taurine on protein phosphorylation in mammalian tissues. In: Lombardini JB, Schaffer SW, Azuma J (eds) Nutritional value and mechanisms of action. Plenum Press, New York, pp 309–318 (Adv Exp Med Biol, vol 315)

    Google Scholar 

  • Lombardini JB (1992b) Effects of taurine on the phosphorylation of specific proteins in subcellular fractions of the rat retina. Neurochem Res 17: 821–824

    Google Scholar 

  • Lombardini JB (1993) Partial characterization of an 20 K Mr retinal protein whose phosphorylation is inhibited by taurine. Biochem Pharmacol 46: 1445–1451

    Google Scholar 

  • McLaughlin A, Grathwohl C, McLaughlin S (1978) The adsorption of divalent cations to phosphatidylcholine bilayer membranes. Biochim Biophys Acta 513: 338–357

    Google Scholar 

  • McLaughlin S, Mulrine N, Gresalfi T, Vaio G, McLaughlin A (1981) Adsorption of divalent cations to bilayer membranes containing phosphatidylserine. J Gen Physiol 77: 445–473

    Google Scholar 

  • Musters RJP, Otten E, Biegelmann E, Bijvelt J, Keijzer JJH, Post JA, Op den Kamp JAF, Verkleij AJ (1993) Loss of asymmetric distribution of sarcolemmal phosphatidylethanolamine during simulated ischemia in the isolated neonatal rat cardiomyocyte. Circ Res 73: 514–523

    Google Scholar 

  • Nakada T, Hida K, Kwee IL (1992) Brain pH and lactic acidosis: quantitative analysis of taurine effect. Neuroscience Res 15: 115–123

    Google Scholar 

  • Nakamori K, Koyama I, Nakamura T, Nemoto M, Yoshida T, Umeda M, Inoue K (1993) Quantitative evaluation of the effectiveness of taurine in protecting the ocular surface against oxidant. Chem Pharm Bull 41: 335–338

    Google Scholar 

  • Novotony MJ, Hogan PM, Paley DM, Adams HR (1991) Systolic and diastolic dysfunction of the left ventricle induced by dietary taurine deficiency in cats. Am J Physiol 261: H121-H127

    Google Scholar 

  • Oja SS, Kontro P (1983) Taurine. In: Lajtha A (ed) Handbook of neurochemistry, vol 3. Plenum Publishing Corp., New York, pp 501–533

    Google Scholar 

  • Palackal T, Moretz R, Wisniewski H, Sturman J (1986) Abnormal visual cortex development in the kitten associated with maternal dietary taurine deprivation. J Neurosci Res 15: 223–239

    Google Scholar 

  • Palackal T, Neuringer M, Sturman J (1993) Laminar analysis of the number of neurons, astrocytes, oligodendrocytes and microglia in the visual cortex (area 17) of 6- and 12-month-old rhesus monkeys fed a human infant soy-protein formula with or without taurine supplementation from birth. Dev Neurosci 15: 54–67

    Google Scholar 

  • Panagia V, Okumura K, Makino N, Dhalla NS (1986) Stimulation of Ca2+-pump in rat heart sarcolemma by phosphatidylethanolamine N-methylation. Biochim Biophys Acta 856: 383–387

    Google Scholar 

  • Panagia V, Makino N, Ganguly PK, Dhalla NS (1987) Inhibition of Na+-Ca2+ exchange in heart sarcolemmal vesicles by phosphatidylethanolamine N-methylation. Eur J Biochem 166: 597–603

    Google Scholar 

  • Park E, Quinn MR, Wright CE, Schuller-Levis G (1993) Taurine chloramine inhibits the synthesis of nitric oxide and the release of tumor necrosis factor in activated RAW 264.7 cells. J Leukoc Biol 54: 119–124

    Google Scholar 

  • Pasantes-Morales H, Cruz C (1984) Protective effect of taurine and zinc on peroxidationinduced damage in photoreceptor outer segments. J Neurosci Res 11: 303–311

    Google Scholar 

  • Pasantes-Morales H, Cruz C (1985) Taurine and hypotaurine inhibit light-induced lipid peroxidation and protect rod outer segment structure. Brain Res 330: 154–157

    Google Scholar 

  • Pasantes-Morales H, Martin del Rio R (1990) Taurine and mechanisms of cell volume regulation. In: Pasantes-Morales H, Shain W, Martin del Rio R (eds) Taurine: functional neurochemistry, physiology and cardiology. Wiley Liss Inc, New York, pp 317–328

    Google Scholar 

  • Pasantes-Morales H, Wright CE, Gaull GE (1985) Taurine protection of lymphoblastoid cells from iron-ascorbate induced damage. Biochem Pharmacol 34: 2205–2207

    Google Scholar 

  • Pion, PD, Kittleson MD, Rodgers QR, Morris JG (1987) Myocardial failure in cats associated with low plasma taurine: a reversible cardiomyopathy. Science 237: 764–768

    Google Scholar 

  • Post JA, Langer GA, Op den Kamp JAF, Verkleij AJ (1988) Phospholipid asymmetry in cardiac sarcolemma: analysis of intact cells and gas-dissected membranes. Biochim Biophys Acta 943: 256–266

    Google Scholar 

  • Post JA, Kuwata JH, Langer GA (1993) A discrete Na+/Ca2+ exchange dependent, Ca2+ compartment in cultured neonatal rat heart cells. Characteristics, localization and possible physiological function. Cell Calcium 14: 61–71

    Google Scholar 

  • Punna S, Ballard C, Hamaguchi T, Azuma J, Schaffer S (1994) Effect of taurine and methionine on sarcoplasmic reticular Ca2+ transport and phospholipid methyltransferase activity. J Cardiovasc Pharmacol 24: 286–292

    Google Scholar 

  • Schaffer SW, Azuma J (1992) Physiological effects of taurine in the heart. In: Lombardini JB, Schaffer SW, Azuma J (eds) Nutritional value and mechanisms of action. Plenum Press, New York, pp 105–120 (Adv Exp Med Biol, vol 315)

    Google Scholar 

  • Schaffer SW, Allo S, Harada H, Azuma J (1990) Regulation of calcium homeostasis by taurine: role of calmodulin. In: Pasantes-Morales H, Shain W, Martin del Rio R (eds) Taurine: functional neurochemistry, physiology and cardiology. Wiley-Liss, New York, pp 217–225

    Google Scholar 

  • Schaffer SW, Punna S, Duan J, Harada H, Hamaguchi T, Azuma J (1992) Mechanism underlying physiological modulation of myocardial contraction by taurine. In: Lombardini JB, Schaffer SW, Azuma J (eds) Nutritional value and mechanisms of action. Plenum Press, New York, pp 193–198 (Adv Exp Med Biol, vol 315)

    Google Scholar 

  • Schroit AJ, Zwaal RFA (1991) Transbilayer movement of phospholipids in red cell and platelet membranes. Biochim Biophys Acta 1071: 313–329

    Google Scholar 

  • Schuller-Levis G, Mehta PD, Rudelli R, Sturman J (1990) Immunologic consequences of taurine deficiency in cats. J Leukocyte Biol 47: 321–331

    Google Scholar 

  • Sebring LA, Huxtable RJ (1985) Taurine modulation of calcium binding to cardiac sarcolemma. J Pharmacol Exp Therap 232: 445–451

    Google Scholar 

  • Sebring LA, Huxtable RJ (1986) Low affinity binding of taurine to phospholiposomes and cardiac sarcolemma. Biochem Biophys Acta 884: 559–566

    Google Scholar 

  • Siegel DP (1986a) Inverted micellar intermediates and the transition between lamellar, cubic and inverted hexagonal lipid phases. I. Mechanism of the L a to HII phase transitions. Biophys J 49: 1155–1170

    Google Scholar 

  • Siegel DP (1986b) Inverted micellar intermediates and the transitions between lamellar, cubic and inverted hexagonal lipid phases. II. Implications for membrane-membrane interactions and membrane fusion. Biophys J 49: 1171–1183

    Google Scholar 

  • Silvius JR, Gagne J (1984) Calcium-induced fusion and lateral phase separations in phosphatidylcholine-phosphatidylserine vesicles. Correlation by calorimetric and fusion measurements. Biochemistry 23: 3241–3247

    Google Scholar 

  • Sturman J (1991) Dietary taurine and feline reproduction and development. J Nutr 121: S166-S170

    Google Scholar 

  • Sturman JA (1993) Taurine in development. Physiol Rev 73: 119–147

    Google Scholar 

  • Sturman JA, Messing JM (1991) Dietary taurine content and feline reproduction and outcome. J Nutr 121: 1195–1203

    Google Scholar 

  • Sturman J, Messing JM (1992) High dietary taurine effects on feline tissue taurine concentrations and reproductive performance. J Nutr 122: 82–88

    Google Scholar 

  • Sturman JA, Moretz RC, French JH, Wisniewski HM (1985) Taurine deficiency in the developing cat: persistence of the cerebellar external granule cell layer. J Neurosci Res 13: 405–416

    Google Scholar 

  • Takihara K, Azuma J, Awata N, Ohta H, Sawamura A, Kishimoto S, Sperelakis N (1985) Taurine's possible protective role in age dependent response to calcium paradox. Life Sci 37: 1705–1710

    Google Scholar 

  • Tilcock CPS, Bally MB, Farren SB, Cullis PR, Gruner SM (1984) Cation-dependent segregation phenomena and phase behavior in model membrane systems containing phosphatidylserine: influence of cholesterol and acyl chain composition. Biochemistry 23: 2696–2703

    Google Scholar 

  • Trachtman H, del Pizzo R, Futterweit S, Levine D, Rao PS, Valderrama E, Sturman JA (1992) Taurine attenuates renal disease in chronic puromycin aminonucleoside nephropathy. Am J Physiol 262: F117-F123

    Google Scholar 

  • Trachtman H, Futterweit S, Bienkowski RS (1993) Taurine prevents glucose-induced lipid peroxidation and increased collagen production in cultured rat mesangial cells. Biochem Biophys Res Commun 191: 759–765

    Google Scholar 

  • Vallecalle-Sandoval M-H, Heaney G, Sersen E, Sturman JA (1991) Comparison of the developmental changes of the brainstem auditory evoked response (baer) in taurinesupplemented and taurine-deficient kittens. Int J Dev Neurosci 9: 571–579

    Google Scholar 

  • Wang Q, Giri SN, Hyde DM, Nakashima JM (1989) Effects of taurine on bleomycininduced lung fibrosis in hamsters. Proc Soc Exp Biol Med 190: 330–338

    Google Scholar 

  • Wang Q, Giri SN, Hyde DM, Li C (1991) Amelioration of bleomycin-induced pulmonary fibrosis in hamsters by combined treatment with taurine and niacin. Biochem Pharmacol 42: 1115–1122

    Google Scholar 

  • Wang Q, Hollinger MA, Giri SN (1992a) Attenuation of amiodarone-induced lung fibrosis and phospholipidosis in hamsters by taurine and/or niacin treatment. J Pharmacol Exp Therap 262: 127–132

    Google Scholar 

  • Wang Q, Hyde DM, Giri SN (1992b) Abatement of bleomycin-induced increases in vascular permeability, inflammatory cell infiltration, and fibrotic lesions in hamster lungs by combined treatment with taurine and niacin. Lab Invest 67: 234–242

    Google Scholar 

  • Waterfield CJ, Turton JA, Scales MDC, Timbrell JA (1993) Reduction of liver taurine in rats byβ-alanine treatment increases carbon tetrachloride toxicity. Toxicology 77: 7–20

    Google Scholar 

  • Weiss SJ (1989) Tissue destruction by neurophils. N Engl J Med 320: 365–376

    Google Scholar 

  • Wright CE, Tallan HH, Lin YY, Gaull CE (1986) Taurine: biological update. Ann Rev Biochem 55: 427–453

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Pharmacology, School of Medicine, University of South Alabama, 36688, Mobile, Alabama, USA

    S. W. Schaffer

  2. Department of Medicine III, School of Medicine, Osaka University Suita-City, Osaka, Japan

    J. Azuma

  3. Department of Chemistry, College of Arts and Sciences, University of South Alabama Mobile, Alabama, USA

    J. D. Madura

Authors
  1. S. W. Schaffer
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. J. Azuma
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. J. D. Madura
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Schaffer, S.W., Azuma, J. & Madura, J.D. Mechanisms underlying taurine-mediated alterations in membrane function. Amino Acids 8, 231–246 (1995). https://doi.org/10.1007/BF00806821

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00806821

Keywords

Search

Navigation