Taurine and inflammatory diseases

Janusz Marcinkiewicz, Ewa Kontny, Janusz Marcinkiewicz, Ewa Kontny

Abstract

Taurine (2-aminoethanesulfonic acid) is the most abundant free amino acid in humans and plays an important role in several essential biological processes such as bile acid conjugation, maintenance of calcium homeostasis, osmoregulation and membrane stabilization. Moreover, attenuation of apoptosis and its antioxidant activity seem to be crucial for the cytoprotective effects of taurine. Although these properties are not tissue specific, taurine reaches particularly high concentrations in tissues exposed to elevated levels of oxidants (e.g., inflammatory cells). It suggests that taurine may play an important role in inflammation associated with oxidative stress. Indeed, at the site of inflammation, taurine is known to react with and detoxify hypochlorous acid generated by the neutrophil myeloperoxidase (MPO)-halide system. This reaction results in the formation of less toxic taurine chloramine (TauCl). Both haloamines, TauCl and taurine bromamine (TauBr), the product of taurine reaction with hypobromous acid (HOBr), exert antimicrobial and anti-inflammatory properties. In contrast to a well-documented regulatory role of taurine and taurine haloamines (TauCl, TauBr) in acute inflammation, their role in the pathogenesis of inflammatory diseases is not clear. This review summarizes our current knowledge concerning the role of taurine, TauCl and TauBr in the pathogenesis of inflammatory diseases initiated or propagated by MPO-derived oxidants. The aim of this paper is to show links between inflammation, neutrophils, MPO, oxidative stress and taurine. We will discuss the possible contribution of taurine and taurine haloamines to the pathogenesis of inflammatory diseases, especially in the best studied example of rheumatoid arthritis.

Figures

Fig. 1
Fig. 1
Hypohalous acids, the major products of PO–halide system exert both a beneficial (microbicidal) and detrimental (tissue injury) role in neutrophil-associated inflammation
Fig. 2
Fig. 2
Fate of endogenous and diet taurine in activated neutrophils
Fig. 3
Fig. 3
Biological functions of intracellular taurine and the immune cells
Fig. 4
Fig. 4
Targets of HOCl at a site of inflammation and its interaction with taurine. Inside phagolysosomes, HOCl kills ingested microbes. Outside phagolysosomes, taurine neutralizes detrimental effects of HOCl on neighboring cells and protects “self” molecules from oxidative modification. TauCl, the product of this reaction, is less toxic than HOCl. TauCl is not membrane permeable, oxidizes distinct targets and causes less damage to biologically active molecules (Marcinkiewicz and Kontny 2012)
Fig. 5
Fig. 5
Association of taurine with the antioxidant network: a redundancy of the immune system. Taurine haloamines, the products of MPO–halide system, function as a physiological link between cysteine pathway and the heme-oxygenase-1 system (HO-1)
Fig. 6
Fig. 6
Effect of TauCl on pro- and anti-inflammatory cytokine release from articular adipose tissue (AAT), subcutaneous (ScAT) adipose tissue and synovial membrane (SM) explants. Tissue explants were cultured for 18 h in 37 °C in culture medium alone (control; white bars) or treated with LPS (1 μg/ml) in the absence (black bars) or presence of TauCl (500 μM) (gray bars), then cytokine concentrations in culture supernatants were measured by ELISA. Values are the mean and SEM of 35–53 (AAT), 20–25 (ScAT) or 14–24 (SM) experiments. *Indicates statistically significant differences between untreated and treated cultures; #Indicates statistically significant differences between LPS− versus LPS+ TauCl-treated cultures; *,#p < 0.05; **,##p < 0.01; ***,###p < 0.001
Fig. 7
Fig. 7
Effect of TauCl on IL-1β and IL-1Ra release from articular adipose tissue (AAT), subcutaneous (ScAT) adipose tissue and synovial membrane (SM) explants. Explanations as in Fig. 1. Values are the mean and SEM of 37–41 (AAT), 19–23 (ScAT) or 17–18 (SM) experiments
Fig. 8
Fig. 8
Effect of TauCl on the release of classical adipokines from articular adipose tissue (AAT), subcutaneous (ScAT) adipose tissue and synovial membrane (SM) explants. Explanations as in Fig. 1. Values are the mean and SEM of 54 (AAT), 20–23 (ScAT) or 25–28 (SM) experiments

References

    1. Bartok B, Firestein GS. Fibroblast-like synoviocytes: key effector cells in rheumatoid arthritis. Immunol Rev. 2010;233:233–255. doi: 10.1111/j.0105-2896.2009.00859.x.
    1. Barua M, Liu Y, Quinn MR. Taurine chloramine inhibits inducible nitric oxide synthase and TNF-alpha gene expression in activated alveolar macrophages: decreased NF-kappaB activation and IkappaB kinase activity. J Immunol. 2001;167(4):2275–2281.
    1. Bouckenooghe T, Remacle C, Reusens B. Is taurine a functional nutrient? Curr Opin Clin Nutr Metab Care. 2006;9:728–733. doi: 10.1097/01.mco.0000247469.26414.55.
    1. Chorąży-Massalska M, Kontny E, Kornatka A, Rell-Bakalarska M, Marcinkiewicz J, Maśliński W. The effect of taurine chloramine on pro-inflammatory cytokine production by peripheral blood mononuclear cells isolated from rheumatoid arthritis and osteoarthritis patients. Clin Exp Rheumatol. 2004;22(6):692–698.
    1. Costeron JW, Stewart PS, Greenberg EP. Bacterial biofilms: a common cause of persistent infections. Science. 1991;284:1318–1322. doi: 10.1126/science.284.5418.1318.
    1. Detert J, Pischon N, Burmester GR, Buttgereit F. The association between rheumatoid arthritis and periodontal disease. Arthritis Res Ther. 2010;12:218. doi: 10.1186/ar3106.
    1. Firestein GS. Etiology and pathogenesis of rheumatoid arthritis. In: Firestein GS, Budd RC, Harris T, McInnes IB, Ruddy S, Sergent JS, editors. Kelly’s textbook of rheumatology. 8. Philadelphia: Saunders Elsevier; 2009. pp. 1035–1086.
    1. Frommer KW, Zimmermann B, Meier FM, Schröder D, Heil M, Schäffler A, Büchler C, Steinmeyer J, Brentano F, Gay S, Müller-Ladner U, Neumann E. Adiponectin-mediated changes in effector cells involved in the pathophysiology of rheumatoid arthritis. Arthritis Rheum. 2010;62:2886–2899. doi: 10.1002/art.27616.
    1. Gabay C, Lamacchia C, Palmer G. IL-1 pathways in inflammation and human diseases. Nat Rev Rheumatol. 2010;6:232–241. doi: 10.1038/nrrheum.2010.4.
    1. Gaut JP, Yeh GC, Tran HD, Byun J, Henderson JP, Richter GM, Brennan ML, Lusis AJ, Belaaouaj A, Hotchkiss RS, Heinecke JW. Neutrophils employ the myeloperoxidase system to generate antimicrobial brominating and chlorinating oxidants during sepsis. Proc Natl Acad Sci. 2001;98:11961–11966. doi: 10.1073/pnas.211190298.
    1. Gierut A, Perlman H, Pope RM. Innate immunity and rheumatoid arthritis. Rheum Dis Clin North Am. 2010;36:271–296. doi: 10.1016/j.rdc.2010.03.004.
    1. Gottardi W, Nagl M. N-chlorotaurine, a natural antiseptic with outstanding tolerability. J Antimicrob Chemother. 2010;65:399–409. doi: 10.1093/jac/dkp466.
    1. Gottardi W, Hagleitner M, Nagl M. N, N-dichlorotaurine: chemical and bactericidal properties. Arch Pharm (Weinheim) 2005;338(10):473–483. doi: 10.1002/ardp.200500146.
    1. Green TR, Fellman JH, Eicher AL, Pratt KL. Antioxidant role and subcellular localisation of hypotaurine and taurine in human neutrophils. Biochim Biophys Acta. 1991;1073:91–97. doi: 10.1016/0304-4165(91)90187-L.
    1. Gregersen PK, Silver J, Winchester RJ. The shared epitope hypothesis. An approach to understanding the molecular genetics of susceptibility to rheumatoid arthritis. Arthritis Rheum. 1987;30:178–182. doi: 10.1002/art.1780301102.
    1. Gustafson B. Adipose tissue, inflammation and atherosclerosis. J Atheroscler Thromb. 2010;17:332–341. doi: 10.5551/jat.3939.
    1. Henderson JP, Byun J, Williams MV, et al. Production of brominating intermediates by myeloperoxidase. J Biol Chem. 2001;11:7867–7875. doi: 10.1074/jbc.M005379200.
    1. Huxtable RJ. Physiological actions of taurine. Physiol Rev. 1992;72:101–163.
    1. Jang JS, Piao S, Cha YN, Kim Ch. Taurine chloramine activates Nrf2, increases HO-1 expression and protects cells from death caused by hydrogen peroxide. J Clin Biochem Nutr. 2009;45:37–43. doi: 10.3164/jcbn.08-262.
    1. Jeon SH, Lee MY, Rahman MM, Kim SJ, et al. The antioxidant, taurine reduced lipopolysaccharide (LPS)-induced generation of ROS, and activation of MAPKs and Bax in cultured pneumocytes. Pulm Pharmacol Ther. 2009;22:562–566. doi: 10.1016/j.pupt.2009.07.004.
    1. Jong CJ, Azuma J, Schaffer SW. Role of mitochondrial permeability transition in taurine deficiency-induced apoptosis. Exp Clin Cardiol. 2011;16(4):125–128.
    1. Joo K, Lee Y, Choi D, Han J, Hong S, Kim YM, Jung Y. An anti-inflammatory mechanism of taurine conjugated 5-aminosalicylic acid against experimental colitis: taurine chloramine potentiates inhibitory effect of 5-aminosalicylic acid on IL-1beta-mediated NFkappaβ activation. Eur J Pharmacol. 2009;618(1–3):91–97. doi: 10.1016/j.ejphar.2009.07.009.
    1. Kim C, Cha YN. Production of reactive oxygen and nitrogen species in phagocytes is regulated by taurine chloramine. Adv Exp Med Biol. 2009;643:463–472. doi: 10.1007/978-0-387-75681-3_48.
    1. Kim C, Park E, Quinn MR, Schuller-Levis G. The production of superoxide anion and nitric oxide by cultured murine leukocytes and the accumulation of TNF-α in the conditioned media is inhibited by taurine chloramine. Immunopharmacology. 1996;34(2–3):89–95. doi: 10.1016/0162-3109(96)00113-0.
    1. Kim C, Choi HS, Kim JW. Taurine chloramine inhibits the production of nitric oxide and superoxide anion by modulating specific mitogen-activated protein kinases. Adv Exp Med Biol. 2006;583:493–498. doi: 10.1007/978-0-387-33504-9_55.
    1. Kim KS, Park EK, Ju SM, Jung HS, Bang JS, Kim C, Lee YA, Hong SJ, Lee SH, Yang HI, Yoo MC. Taurine chloramine differentially inhibits matrix metalloproteinase 1 and 13 synthesis in interleukin-1beta stimulated fibroblast-like synoviocytes. Arthritis Res Ther. 2007;9:R80. doi: 10.1186/ar2279.
    1. Kim C, Jang JS, Cho MR, Agarawal SR, Cha YN. Taurine chloramine induces heme oxygenase-1 expression via Nrf2 activation in murine macrophages. Int Immunopharmacol. 2010;10(4):440–446. doi: 10.1016/j.intimp.2009.12.018.
    1. Kim KS, Choi HM, da Oh H, Kim C, Jeong JS, Yoo MC, Yang HI. Effect of taurine chloramine on the production of matrix metalloproteinases (MMPs) in adiponectin- or IL-1beta-stimulated fibroblast-like synoviocytes. J Biomed Sci. 2010;17(Suppl 1):S27. doi: 10.1186/1423-0127-17-S1-S27.
    1. Klamt F, Shacter E. Taurine chloramine, an oxidant derived from neutrophils, induces apoptosis in human B lymphoma cells through mitochondrial damage. J Biol Chem. 2005;280(22):21346–21352. doi: 10.1074/jbc.M501170200.
    1. Klebanoff SJ. Myeloperoxidase-halide-hydrogen peroxide antibacterial system. J Bacteriol. 1968;95:2131–2138.
    1. Klebanoff SJ. Myeloperoxidase: friend and foe. J Leukoc Biol. 2005;77:598–625. doi: 10.1189/jlb.1204697.
    1. Klein-Wieringa IR, Kloppenburg M, Bastiaansen-Jenniskens YM, Yusuf E, Kwekkeoopm JC, El-Bannoudi H, Nelissen RG, Zuurmond A, Stojanovic-Susulic V, Van Osch GJ, Toes RE, Ioan-Facsinay A. The infrapetellar fat pad of patients with osteoarthritis has an inflammatory phenotype. Ann Rheum Dis. 2011;70:851–857. doi: 10.1136/ard.2010.140046.
    1. Kontny E, Grabowska A, Kowalczewski J, Kurowska M, Janicka I, Marcinkiewicz J, Maśliński W. Taurine chloramine inhibition of cell proliferation and cytokine production by rheumatoid arthritis fibroblast-like synoviocytes. Arthritis Rheum. 1999;42:2552–2560. doi: 10.1002/1529-0131(199912)42:12<2552::AID-ANR7>;2-V.
    1. Kontny E, Szczepańska K, Kowalczewski J, Kurowska M, Janicka I, Marcinkiewicz J, Maśliński W. The mechanism of taurine chloramine inhibition of cytokine (IL-6, IL-8) production by rheumatoid arthritis fibroblast-like synoviocytes. Arthritis Rheum. 2000;43:2169–2177. doi: 10.1002/1529-0131(200010)43:10<2169::AID-ANR4>;2-#.
    1. Kontny E, Wojtecka-Łukasik E, Rell-Bakalarska K, Dziewczopolski W, Maśliński W, Maślinski S. Impaired generation of taurine chloramine by synovial fluid neutrophils of rheumatoid arthritis patients. Amino Acids. 2002;23:415–418. doi: 10.1007/s00726-002-0205-z.
    1. Kontny E, Maśliński W, Marcinkiewicz J. Anti-inflammatory activities of taurine chloramine: implication for immunoregulation and pathogenesis of rheumatoid arthritis. Adv Exp Med Biol. 2003;526:329–340. doi: 10.1007/978-1-4615-0077-3_41.
    1. Kontny E, Rudnicka W, Kowalczewski J, Marcinkiewicz J, Maślinski W. Selective inhibition of cyclooxygenase-2-generated prostaglandin E2 synthesis in rheumatoid arthritis synoviocytes by taurine chloramine. Arthritis Rheum. 2003;48:1551–1555. doi: 10.1002/art.10975.
    1. Kontny E, Chorąży-Massalska M, Rudnicka W, Janicka I, Marcinkiewicz J, Maśliński W. The effect of taurine and its metabolites on the pathogenic functions of rheumatoid arthritis fibroblast-like synoviocytes. Centr Eur J Immunol. 2003;28:167–172.
    1. Kontny E, Rudnicka W, Chorazy-Massalska M, Marcinkiewicz J, Maśliński W. Taurine chloramine inhibits proliferation of rheumatoid arthritis synoviocytes by triggering a p53-dependent pathway. Inflamm Res. 2006;55:446–455. doi: 10.1007/s00011-006-5067-5.
    1. Kontny E, Chorąży-Massalska M, Rudnicka W, Marcinkiewicz J, Maśliński W. Cytotoxicity of taurine metabolites depends on the cell type. Adv Exp Med Biol. 2006;583:157–171. doi: 10.1007/978-0-387-33504-9_16.
    1. Kontny E, Chorazy-Massalska M, Rudnicka W, Marcinkiewicz J, Maśliński W. Comparison of taurine chloramine and taurine bromamine effects on rheumatoid arthritis synoviocytes. Amino Acids. 2007;32(3):447–452. doi: 10.1007/s00726-006-0368-0.
    1. Kontny E, Plebanczyk M, Lisowska B, Olszewska M, Maldyk P, Maslinski W. Comparison of rheumatoid articular adipose and synovial tissue reactivity to proinflammatory stimuli: contribution to adipocytokine network. Ann Rheum Dis. 2012;71:262–267. doi: 10.1136/annrheumdis-2011-200123.
    1. Kwaśny-Krochin B, Bobek M, Kontny E, Gluszko P, Biedroń R, Chain BM, Maśliński W, Marcinkiewicz J. Effect of taurine chloramine, the product of activated neutrophils, on the development of collagen-induced arthritis in DBA 1/J mice. Amino Acids. 2002;23:419–426. doi: 10.1007/s00726-002-0207-x.
    1. Learn DB, Fried VA, Thomas EL. Taurine and hypotaurine content of human leukocytes. J Leukoc Biol. 1990;48:174–182.
    1. Low E, Nair S, Shiau T, Belisle B, Debabov D, Celeri C, Zuck M, Najafi R, Georgopapadakou N, Jain R. N,N-dichloroaminosulfonic acids as novel topical antimicrobial agents. Bioorg Med Chem Lett. 2009;19(1):196–198. doi: 10.1016/j.bmcl.2008.10.114.
    1. Maher SG, Condron CEM, Bouchier-Hayes DJ, Toomey DM. Taurine attenuates CD3/interleukin-2-induced T cell apoptosis in an in vitro model of activation-induced cell death (AICD) Clin Exp Immunol. 2005;139:279–286. doi: 10.1111/j.1365-2249.2005.02694.x.
    1. Mainnemare A, Mégarbane B, Soueidan A, Daniel A, Chapple IL. Hypochlorous acid and taurine-N-monochloramine in periodontal diseases. J Dent Res. 2004;83(11):823–831. doi: 10.1177/154405910408301101.
    1. Marcinkiewicz J. Taurine bromamine: a new therapeutic option in inflammatory skin diseases. Polish Arch Internal Med. 2009;119:673–675.
    1. Marcinkiewicz J, Kontny E (2012) Taurine, taurine derivatives and immune system. In: A El Idrissi, W L’Amoreaux (eds) Taurine in health and disease, Transworld Research Network Chapter 6, 2011: 000–000 ISBN:978-81-7895-520-9
    1. Marcinkiewicz J, Grabowska A, Bereta J, Stelmaszyńska T. Taurine chloramine a product of activated neutrophils, inhibits in vitro the generation of nitric oxide and other macrophage inflammatory mediators. J Leukoc Biol. 1995;58:667–674.
    1. Marcinkiewicz J, Grabowska A, Bereta J, Stelmaszyńska T. Taurine chloramine a product of activated neutrophils, inhibits in vitro the release of tumor necrosis factor in activated RAW 264.7 cells. J Leukoc Biol. 1995;54:119.
    1. Marcinkiewicz J, Grabowska A, Bereta J, Bryniarski K, Nowak B. Taurine chloramine down-regulates the generation of murine neutrophil inflammatory mediators. Immunopharmacology. 1998;40(1):27–38. doi: 10.1016/S0162-3109(98)00023-X.
    1. Marcinkiewicz J, Chain B, Nowak B, et al. Antimicrobial and cytotoxic activity of hypochlorous acid: interactions with taurine and nitrite. Inflamm Res. 2000;49:280–289. doi: 10.1007/PL00000208.
    1. Marcinkiewicz J, Mak M, Bobek M, Biedroń R, Białecka A, Koprowski M, Kontny E, Maśliński W. Is there a role of taurine bromamine in inflammation? Interactive effects with nitrite and hydrogen peroxide. Inflamm Res. 2005;54(1):42–49. doi: 10.1007/s00011-004-1322-9.
    1. Marcinkiewicz J, Biedroń R, Białecka A, et al. Susceptibility of Propionibacterium acnes and Staphylococcus epidermidis to killing by MPO–halide system products. Implication for taurine bromamine as a new candidate for topical therapy in treating acne vulgaris. Arch Immunol Ther Exp. 2006;54(1):61–68. doi: 10.1007/s00005-006-0007-1.
    1. Marcinkiewicz J, Kurnyta M, Biedroń R, Bobek M, Kontny E, Maśliński W. Anri-inflammatory effects of taurine derivatives (taurine chloramine, taurine bromamine, and taurolidine) are mediated by different mechanisms. Adv Exp Med Biol. 2006;583:481–492. doi: 10.1007/978-0-387-33504-9_54.
    1. Marcinkiewicz J, Głuszko P, Kontny E, Kwaśny-Krochin B, Bobek M, Wierzchowski W, Ciszek M, Maśliński W. Is taurolidine a candidate for treatment of rheumatoid arthritis? Clin Exp Rheumatol. 2007;25:211–218.
    1. Marcinkiewicz J, Wojas-Pelc A, Walczewska M, Lipko-Godlewska S, Jachowicz R, Maciejewska A, Białecka A, Kasprowicz A. Topical taurine bromamine, a new candidate in the treatment of moderate inflammatory acne vulgaris. Eur J Dermatol. 2008;18:433–439.
    1. Marcinkiewicz J, Walczewska M, Olszanecki R, Bobek M, Biedroń R, Dulak J, Józkowicz A, Kontny E, Maślinski W. Taurine haloamines and heme oxygenase-1 cooperate in the regulation of inflammation and attenuation of oxidative stress. Adv Exp Med Biol. 2009;643:439–450. doi: 10.1007/978-0-387-75681-3_46.
    1. Martini C, Hammerer-Lercher A, Zuck M, Jekle A, Debabov D, Anderson M, Nagl M. Antimicrobial and anticoagulant activities of N-chlorotaurine, N,N-dichloro-2,2-dimethyltaurine, and N-monochloro-2,2-dimethyltaurine in human blood. Antimicrob Agents Chemother. 2012;56(4):1979–1984. doi: 10.1128/AAC.05685-11.
    1. McCourt M, Wang JH, Sookhai S, Redmond HP. Taurolidine inhibits tumor cell growth in vitro and in vivo. Ann Surg Oncol. 2000;7:685–691. doi: 10.1007/s10434-000-0685-6.
    1. Muż B, Kontny E, Marcinkiewicz J, Maśliński W. Heme oxygenase-1 participates in the anti-inflammatory activity of taurine chloramine. Amino Acids. 2008;35:397–402. doi: 10.1007/s00726-007-0605-1.
    1. Nagl M, Teuchner B, Pöttinger E, Ulmer H, Gottardi W. Tolerance of N-chlorotaurine, a new antimicrobial agent, in infectious conjunctivitis: a phase II pilot study. Ophthalmologica. 2000;214(2):111–114. doi: 10.1159/000027477.
    1. Nagl M, Hess MW, Pfaller K, Hengster P, Gottardi W. Bactericidal activity of micromolar N-chlorotaurine: evidence for its antimicrobial function in the human defense system. Antimicrob Agents Chemother. 2000;44:2507–2513. doi: 10.1128/AAC.44.9.2507-2513.2000.
    1. Nagl M, Lass-Flörl C, Neher A, Gunkel A, Gottardi W. Enhanced fungicidal activity of N-chlorotaurine in nasal secretion. J Antimicrob Chemother. 2001;47(6):871–874. doi: 10.1093/jac/47.6.871.
    1. Nagl M, Nguyen VA, Gottardi W, et al. Tolerability and efficacy of N-chlorotaurine in comparison with chloramine T for treatment of chronic leg ulcers with a purulent coating: a randomized phase II study. Br J Dermatol. 2003;149:590–597. doi: 10.1046/j.1365-2133.2003.05432.x.
    1. Neary PM, Hallihan P, Wang JH, Pfirrmann RW, Bouchier-Hayes DJ, Redmond HP. The evolving role of taurolidine in cancer therapy. Ann Surg Oncol. 2010;17:1135–1143. doi: 10.1245/s10434-009-0867-9.
    1. Neher A, Gstöttner M, Nagl M, Scholtz A, Gunkel AR. N-chlorotaurine—a new safe substance for postoperative ear care. Auris Nasus Larynx. 2007;34(1):19–22. doi: 10.1016/j.anl.2006.09.001.
    1. Neumann E, Fromer KW, Vasile M, Müller-Ladner U. Adipocytokines as diving forces in rheumatoid arthritis and related inflammatory diseases? Arthritis Rheum. 2011;63:1159–1169. doi: 10.1002/art.30291.
    1. O’Toole GA, Kaplan HB, Kolter R. Biofilm formation as microbial development. Annu Rev Microbiol. 2000;54:49–79. doi: 10.1146/annurev.micro.54.1.49.
    1. Oliveira MWS, Minotto JB, de Oliveira MR, et al. Scavenging and antioxidant potential of physiological taurine concetrations against different reactive oxygen/nitrogen species. Pharm Raports. 2010;62:185–193.
    1. Olszanecki R, Marcinkiewicz J. Taurine chloramine and taurine bromamine induce heme-oxygenase-1 in resting and LPS-stimulated J774.2 macrophages. Amino Acids. 2004;27:29–35. doi: 10.1007/s00726-004-0097-1.
    1. Olszanecki R, Kurnyta M, Biedroń R, Chorobik P, Bereta M, Marcinkiewicz J. The role of heme oxygenase-1 in downregulation of PGE2 production by taurine chloramine and taurine bromamine in J774.2 macrophages. Amino Acids. 2008;35(2):359–364. doi: 10.1007/s00726-007-0609-x.
    1. Park E, Quinn MR, Wright CE, Schuller-Levis G. Taurine chloramine inhibits the synthesis of nitric oxide and the release of tumor necrosis factor in activated RAW 264.7 cells. J Leukoc Biol. 1993;54(2):119–124.
    1. Park E, Schuller-Levis G, Quinn MR. Taurine chloramine inhibits production of nitric oxide and TNF-alpha in activated RAW 264.7 cells by mechanisms that involve transcriptional and translational events. J Immunol. 1995;154:4778–4784.
    1. Park E, Schuller-Levis G, Jia JH, Quinn MR. Preactivation exposure of RAW 264.7 cells to taurine chloramine attenuates subsequent production of nitric oxide and expression of iNOS mRNA. J Leukoc Biol. 1997;61(2):161–166.
    1. Park E, Quinn MR, Schuller-Levis G. Taurine chloramine attenuates the hydrolytic activity of matrix metalloproteinase-9 in LPS-activated murine peritoneal macrophages. Adv Exp Med Biol. 2000;483:389–398. doi: 10.1007/0-306-46838-7_44.
    1. Quinn MR, Barua M, Liu Y, Serban V. Taurine chloramine inhibits production of inflammatory mediators and iNOS gene expression in alveolar macrophages, a tale of two pathways: part I, NF-kappaB signaling. Adv Exp Med Biol. 2003;526:341–348. doi: 10.1007/978-1-4615-0077-3_42.
    1. Redmond P, et al. Immunonutrition: the role of taurine. Nutrition. 1998;14:599–614. doi: 10.1016/S0899-9007(98)00097-5.
    1. Rosen H, Klebanoff SJ, Yi Wang, et al. Methionine oxidation contributes to bacterial killing by myeloperoxidase system of neutrophils. PNAS. 2009;106(44):18686–18691. doi: 10.1073/pnas.0909464106.
    1. Ryter SW, Otterbein LE, Morse D, Choi AM. Heme oxygenase carbon monoxide signaling pathways: regulation and functional significance. Mol Cell Biochem. 2002;234–235(1–2):249–263. doi: 10.1023/A:1015957026924.
    1. Schaffer SW, Azuma J, Mozaffari M. Role of antioxidant activity of taurine in diabetes. Can J Physiol Pharmacol. 2009;87:91–99. doi: 10.1139/Y08-110.
    1. Scherer HU, Burmester GR. Adaptive immunity in rheumatic diseases: bystander or pathogenic player? Best Pract Res Clin Rheumatol. 2011;25:785–800. doi: 10.1016/j.berh.2011.11.005.
    1. Schett G, Coates LC, Ash ZR, Finzel S, Conaghan PG. Structural damage in rheumatoid arthritis, psoriatic arthritis, and ankylosing spondylitis: traditional views, novel insights gained from TNF blockade, and concepts for the future. Arthritis Res Ther. 2011;13(suppl 1):S4.
    1. Schneider A, Cack U, Rothe K, Bennek J. Peritoneal taurolidine lavage in children with localized peritonitis due to appendicitis. Pediatr Surg Int. 2005;21:445–448. doi: 10.1007/s00383-005-1428-3.
    1. Schuller-Levis GB, Park E. Taurine and its chloramine: modulators of immunity. Neurochem Res. 2004;29(1):117–126. doi: 10.1023/B:NERE.0000010440.37629.17.
    1. Schuller-Levis G, Metha PD, Rudelli R, Struman J. Immunologic consequences of taurine deficiency in cats. J Leukoc Biol. 1990;47:321–331.
    1. Scott DL. Biologics-based therapy for the treatment of rheumatoid arthritis. Nature. 2012;91:30–43.
    1. Shiau TP, Houchin A, Nair S, Xu P, Low E, Najafi RR, Jain R. Stieglitz rearrangement of N,N-dichloro-beta, beta-disubstituted taurines under mild aqueous conditions. Bioorg Med Chem Lett. 2008;19(4):1110–1114. doi: 10.1016/j.bmcl.2008.12.109.
    1. Shimizu M, Zhao Z, Ishimoto Y, Satsu H. Dietary taurine attenuates dextran sulfate sodium (DSS)-induced experimental colitis in mice. Adv Exp Med Biol. 2009;643:265–271. doi: 10.1007/978-0-387-75681-3_27.
    1. Smith J. Neutrophils, host defence, and inflammation: a double-edged sword. J Leukoc Biol. 1994;56:672–686.
    1. Stofkova A. Leptin and adiponectin: from energy and metabolic dysbalance to inflammation and autoimmunity. Endocr Regul. 2009;43:157–168.
    1. Sturmann JA. Taurine in development. Physiol Rev. 1993;73:119–147.
    1. Thomas EL. Myeloperoxidase, hydrogen peroxide, chloride antimicrobial system: effect of exogenous system on antibacterial action against Escherichia coli. Infect Immun. 1979;25:110–114.
    1. Thomas EL, Bozeman PM, Jefferson MM, et al. Oxidation of bromide by the human leukocyte enzymes myeloperoxidase and eosinophil peroxidase. J Biol Chem. 1995;270:2906–2913. doi: 10.1074/jbc.270.7.2906.
    1. Verdrengh M, Tarkowski A. Inhibition of septic arthritis by local administration of taurine chloramine, a product of activated neutrophils. J Rheumatol. 2005;32:1513–1517.
    1. Wagener FA, Volk HD, Willis D, Abraham NG, et al. Different faces of the heme–heme oxygenase system in inflammation. Pharmacol Rev. 2003;55:551–571. doi: 10.1124/pr.55.3.5.
    1. Wang L, Na Zhao, Fang Zhang, Wang Yue, Liang M. Effect of taurine on leukocyte function. Eur J Pharmacol. 2009;616:275–280. doi: 10.1016/j.ejphar.2009.05.027.
    1. Wang Y, Cha YN, Kim KS, Kim C. Taurine chloramines inhibits osteoclastogenesis and splenic lymphocyte proliferation in mice with collagen-induced arthritis. Eur J Pharmacol. 2011;668:325–330. doi: 10.1016/j.ejphar.2011.07.017.
    1. Weiss SJ. Tissue destruction by neutrophils. N Engl J Med. 1988;320:365–376.
    1. Weiss SJ, Klein R, Slivka A, et al. Chlorination of taurine by human neutrophils: evidence for hypochlorous acid generation. J Clin Invest. 1982;70:598–603. doi: 10.1172/JCI110652.
    1. Willatts S, Radford S, Leitermann M. Effect of antiendotoxic agent, taurolidine, in the treatment of sepsis syndrome: a placebo-controlled, double-blind trial. Crit Care Med. 1995;23:1033–1039. doi: 10.1097/00003246-199506000-00007.
    1. Wojtecka-Łukasik E, Gujski M, Roguska K, Maslinska D, Maslinski S. Taurine chloramine modifies adjuvant arthritis in rats. Inflamm Res. 2005;54(suppl 1):S21–S22. doi: 10.1007/s00011-004-0409-3.
    1. Yazdanbakhsh M, Eckmann CM, Roos D. Killing of schistosomula by taurine chloramine and taurine bromamine. Am J Trop Med Hyg. 1987;37:106–110.

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