Taurine chloramine produced from taurine under inflammation provides anti-inflammatory and cytoprotective effects

Amino Acids

Volumn 46, Issue 1, 2014, Pages 89-100

  Kim, Chaekyun ^a   Cha, Young Nam ^a  

^a Inha University School of Medicine   (South Korea)

Author keywords

Antioxidant; Inflammation; Neutrophils; Taurine; Taurine chloramine

Indexed keywords

ANIMALS; ANTIOXIDANTS; APOPTOSIS; CHRONIC DISEASE; CYTOPROTECTION; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; MACROPHAGE ACTIVATION; MACROPHAGES; NEUTROPHIL ACTIVATION; NEUTROPHILS; OXIDOREDUCTASES; TAURINE;

EID: 84895904897     PISSN: 09394451     EISSN: 14382199     Source Type: Journal    
DOI: 10.1007/s00726-013-1545-6     Document Type: Review

References (101)

1. Aruoma OI, Halliwell B, Hoey BM, Butler J (1988) The antioxidant action of taurine, hypotaurine and their metabolic precursors. Biochem J 256:251-255
2. Babior BM (1999) NADPH oxidase: an update. Blood 93:1464-1476
3. Balla G, Vercellotti GM, Muller-Eberhard U, Eaton J, Jacob HS (1991) Exposure of endothelial cells to free heme potentiates damage mediated by granulocytes and toxic oxygen species. Lab Investig 64:648-655
4. Barua M, Liu Y, Quinn MR (2001) 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 167:2275-2281
5. Bhattacharya SK, Sarkar MK (1986) Effect of some centrally administered putative amino acid neurotransmitters on carrageenan-induced paw oedema in rats. J Pharm Pharmacol 38:144-146
6. Choi HS, Cha YN, Kim C (2006) Taurine chloramine inhibits PMA-stimulated superoxide production in human neutrophils perhaps by inhibiting phosphorylation and translocation of p47(phox). Int Immunopharmacol 6:1431-1440
7. Chorazy M, Kontny E, Marcinkiewicz J, Maslinski W (2002) Taurine chloramine modulates cytokine production by human peripheral blood mononuclear cells. Amino Acids 23:407-413
8. Chorazy-Massalska M, Kontny E, Kornatka A, Rell-Bakalarska M, Marcinkiewicz J, Maslinski W (2004) 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 22:692-698
9. Davies JM, Horwitz DA, Davies KJ (1994) Inhibition of collagenase activity by N-chlorotaurine, a product of activated neutrophils. Arthritis Rheum 37:424-427
10. Dinauer MC (2003) Regulation of neutrophil function by Rac GTPases. Curr Opin Hematol 10:8-15
11. Dinkova-Kostova AT, Holtzclaw WD, Cole RN, Itoh K, Wakabayashi N, Katoh Y, Yamamoto M, Talalay P (2002) Direct evidence that sulfhydryl groups of Keap1 are the sensors regulating induction of phase 2 enzymes that protect against carcinogens and oxidants. Proc Natl Acad Sci USA 99:11908-11913
12. Eitzinger C, Ehrlenbach S, Lindner H, Kremser L, Gottardi W, Debabov D, Anderson M, Nagl M, Orth D (2012) N-chlorotaurine, a long-lived oxidant produced by human leukocytes, inactivates Shiga toxin of enterohemorrhagic Escherichia coli. PLoS ONE 7:e47105
13. Emerson DK, McCormick ML, Schmidt JA, Knudson CM (2005) Taurine monochloramine activates a cell death pathway involving Bax and Caspase-9. J Biol Chem 280:3233-3241
14. Englert RP, Shacter E (2002) Distinct modes of cell death induced by different reactive oxygen species: amino acyl chloramines mediate hypochlorous acid-induced apoptosis. J Biol Chem 277:20518-20526
15. Fukuda K, Hirai Y, Yoshida H, Nakajima T, Usui T (1982) Free amino acid content of lymphocytes and granulocytes compared. Clin Chem 28:1758-1761
16. Gabriel SE (2001) The epidemiology of rheumatoid arthritis. Rheum Dis Clin North Am 27:269-281
17. Gottardi W, Nagl M (2002) Chemical properties of N-chlorotaurine sodium, a key compound in the human defence system. Arch Pharm (Weinheim) 335:411-421
18. Gottardi W, Nagl M (2005) Chlorine covers on living bacteria: the initial step in antimicrobial action of active chlorine compounds. J Antimicrob Chemother 55:475-482
19. Gottardi W, Nagl M (2010) N-chlorotaurine, a natural antiseptic with outstanding tolerability. J Antimicrob Chemother 65:399-409
20. Gottardi W, Hagleitner M, Nagl M (2005) N,N-dichlorotaurine: chemical and bactericidal properties. Arch Pharm (Weinheim) 338:473-483
21. Grisham MB, Jefferson MM, Melton DF, Thomas EL (1984) Chlorination of endogenous amines by isolated neutrophils. Ammonia-dependent bactericidal, cytotoxic, and cytolytic activities of the chloramines. J Biol Chem 259:10404-10413
22. Groemping Y, Rittinger K (2005) Activation and assembly of the NADPH oxidase: a structural perspective. Biochem J 386:401-416
23. Heller-Stilb B, van Roeyen C, Rascher K, Hartwig HG, Huth A, Seeliger MW, Warskulat U, Haussinger D (2002) Disruption of the taurine transporter gene (taut) leads to retinal degeneration in mice. Faseb J 16:231-233
24. Holland R, Hawkins AE, Eggler AL, Mesecar AD, Fabris D, Fishbein JC (2008) Prospective type 1 and type 2 disulfides of Keap1 protein. Chem Res Toxicol 21:2051-2060
25. Huie RE, Padmaja S (1993) The reaction of no with superoxide. Free Radic Res Commun 18:195-199
26. Huxtable RJ (1992) Physiological actions of taurine. Physiol Rev 72:101-163
27. Ignarro LJ (1996) Physiology and pathophysiology of nitric oxide. Kidney Int Suppl 55:S2-S5
28. Kanayama A, Inoue J, Sugita-Konishi Y, Shimizu M, Miyamoto Y (2002) Oxidation of Ikappa Balpha at methionine 45 is one cause of taurine chloramine-induced inhibition of NF-kappa B activation. J Biol Chem 277:24049-24056
29. Kang IS, Kim C (2013) Taurine chloramine administered in vivo increases NRF2-regulated antioxidant enzyme expression in murine peritoneal macrophages. Adv Exp Med Biol 775:259-267
30. Kim JW, Kim C (2005) Inhibition of LPS-induced NO production by taurine chloramine in macrophages is mediated through Ras-ERK-NF-kappaB. Biochem Pharmacol 70:1352-1360
31. Kim C, Park E, Quinn MR, Schuller-Levis G (1996) The production of superoxide anion and nitric oxide by cultured murine leukocytes and the accumulation of TNF-alpha in the conditioned media is inhibited by taurine chloramine. Immunopharmacology 34:89-95
32. Kim C, Chung JK, Jeong JM, Chang YS, Lee YJ, Kim YJ, Lee MC, Koh CS, Kim BK (1998) Uptake of taurine and taurine chloramine in murine macrophages and their distribution in mice with experimental inflammation. Adv Exp Med Biol 442:169-176
33. Kim KS, Park EK, Ju SM, Jung HS, Bang JS, Kim C, Lee YA, Hong SJ, Lee SH, Yang HI, Yoo MC (2007) Taurine chloramine differentially inhibits matrix metalloproteinase 1 and 13 synthesis in interleukin-1beta stimulated fibroblast-like synoviocytes. Arthritis Res Ther 9:R80
34. Kim C, Jang JS, Cho MR, Agarawal SR, Cha YN (2010a) Taurine chloramine induces heme oxygenase-1 expression via Nrf2 activation in murine macrophages. Int Immunopharmacol 10:440-446
35. Kim KS, Choi HM, Oh DH, Kim C, Jeong JS, Yoo MC, Yang HI (2010b) Effect of taurine chloramine on the production of matrix metalloproteinases (MMPs) in adiponectin- or IL-1beta-stimulated fibroblast-like synoviocytes. J Biomed Sci 17(Suppl 1):S27
36. Kim BS, Cho IS, Park SY, Schuller-Levis G, Levis W, Park E (2011) Taurine chloramine inhibits NO and TNF-alpha production in zymosan plus interferon-gamma activated RAW 264.7 cells. J Drugs Dermatol 10:659-665
37. Kim BS, Spinner DS, Kascsak RJ, Park SY, Cho IS, Schuller-Levis G, Park E (2013) Inflammatory mediators are inhibited by a taurine metabolite in CpG oligodeoxynucleotide and IFN-r activated macrophage cell line. J Drugs Dermatol 12:551-557
38. Klamt F, Shacter E (2005) Taurine chloramine, an oxidant derived from neutrophils, induces apoptosis in human B lymphoma cells through mitochondrial damage. J Biol Chem 280:21346-21352
39. Kontny E, Grabowska A, Kowalczewski J, Kurowska M, Janicka I, Marcinkiewicz J, Maslinski W (1999) Taurine chloramine inhibition of cell proliferation and cytokine production by rheumatoid arthritis fibroblast-like synoviocytes. Arthritis Rheum 42:2552-2560
40. Kontny E, Szczepanska K, Kowalczewski J, Kurowska M, Janicka I, Marcinkiewicz J, Maslinski W (2000) The mechanism of taurine chloramine inhibition of cytokine (interleukin-6, interleukin-8) production by rheumatoid arthritis fibroblast-like synoviocytes. Arthritis Rheum 43:2169-2177
41. Kontny E, Wojtecka LE, Rell-Bakalarska K, Dziewczopolski W, Maslinski W, Maslinski S (2002) Impaired generation of taurine chloramine by synovial fluid neutrophils of rheumatoid arthritis patients. Amino Acids 23:415-418
42. Kontny E, Maslinski W, Marcinkiewicz J (2003a) Anti-inflammatory activities of taurine chloramine: implication for immunoregulation and pathogenesis of rheumatoid arthritis. Adv Exp Med Biol 526:329-340
43. Kontny E, Rudnicka W, Kowalczewski J, Marcinkiewicz J, Maslinski W (2003b) Selective inhibition of cyclooxygenase 2-generated prostaglandin E2 synthesis in rheumatoid arthritis synoviocytes by taurine chloramine. Arthritis Rheum 48:1551-1555
44. Kumar S, Bandyopadhyay U (2005) Free heme toxicity and its detoxification systems in human. Toxicol Lett 157:175-188
45. Kwasny-Krochin B, Bobek M, Kontny E, Gluszko P, Biedron R, Chain BM, Maslinski W, Marcinkiewicz J (2002) Effect of taurine chloramine, the product of activated neutrophils, on the development of collagen-induced arthritis in DBA 1/J mice. Amino Acids 23:419-426
46. Levis W, Schuller-Levis GB, Park E (2003) Deficient tumor necrosis factor-alpha production in lipoarabinomannan activated macrophages from toll-like receptor-4 deficient mice: implication for mycobacterial susceptibility. Int J Lepr Other Mycobact Dis 71:1-9
47. Liu Y, Quinn MR (2002) Chemokine production by rat alveolar macrophages is inhibited by taurine chloramine. Immunol Lett 80:27-32
48. Liu Y, Tonna-DeMasi M, Park E, Schuller-Levis G, Quinn MR (1998) Taurine chloramine inhibits production of nitric oxide and prostaglandin E2 in activated C6 glioma cells by suppressing inducible nitric oxide synthase and cyclooxygenase-2 expression. Brain Res Mol Brain Res 59:189-195
49. Liu Y, Schuller-Levis G, Quinn MR (1999) Monocyte chemoattractant protein-1 and macrophage inflammatory protein-2 production is inhibited by taurine chloramine in rat C6 glioma cells. Immunol Lett 70:9-14
50. Marcinkiewicz J, Kontny E (2012) Taurine and inflammatory diseases. Amino Acids (Epub ahead of print)
51. Marcinkiewicz J, Grabowska A, Bereta J, Stelmaszynska T (1995) Taurine chloramine, a product of activated neutrophils, inhibits in vitro the generation of nitric oxide and other macrophage inflammatory mediators. J Leukoc Biol 58:667-674
52. Marcinkiewicz J, Grabowska A, Bereta J, Bryniarski K, Nowak B (1998a) Taurine chloramine down-regulates the generation of murine neutrophil inflammatory mediators. Immunopharmacology 40:27-38
53. Marcinkiewicz J, Grabowska A, Chain BM (1998b) Modulation of antigen-specific T-cell activation in vitro by taurine chloramine. Immunology 94:325-330
54. Marcinkiewicz J, Nowak B, Grabowska A, Bobek M, Petrovska L, Chain B (1999) Regulation of murine dendritic cell functions in vitro by taurine chloramine, a major product of the neutrophil myeloperoxidase-halide system. Immunology 98:371-378
55. Marcinkiewicz J, Chain B, Nowak B, Grabowska A, Bryniarski K, Baran J (2000) Antimicrobial and cytotoxic activity of hypochlorous acid: interactions with taurine and nitrite. Inflamm Res 49:280-289
56. Marcinkiewicz J, Mak M, Bobek M, Biedron R, Bialecka A, Koprowski M, Kontny E, Maslinski W (2005) Is there a role of taurine bromamine in inflammation? interactive effects with nitrite and hydrogen peroxide. Inflamm Res 54:42-49
57. Martinez-Losa M, Cortijo J, Piqueras L, Sanz MJ, Morcillo EJ (2009) Taurine chloramine inhibits functional responses of human eosinophils in vitro. Clin Exp Allergy 39:537-546
58. Martini C, Hammerer-Lercher A, Zuck M, Jekle A, Debabov D, Anderson M, Nagl M (2012) 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 56:1979-1984
59. Motterlini R, Green CJ, Foresti R (2002) Regulation of heme oxygenase-1 by redox signals involving nitric oxide. Antioxid Redox Signal 4:615-624
60. Nagl M, Hess MW, Pfaller K, Hengster P, Gottardi W (2000) Bactericidal activity of micromolar N-chlorotaurine: evidence for its antimicrobial function in the human defense system. Antimicrob Agents Chemother 44:2507-2513
61. Nauseef WM (2004) Assembly of the phagocyte NADPH oxidase. Histochem Cell Biol 122:277-291
62. Neher A, Nagl M, Appenroth E, Gstottner M, Wischatta M, Reisigl F, Schindler M, Ulmer H, Stephan K (2004) Acute otitis externa: efficacy and tolerability of N-chlorotaurine, a novel endogenous antiseptic agent. Laryngoscope 114:850-854
63. Neher A, Gstottner M, Nagl M, Scholtz A, Gunkel AR (2007) N-chlorotaurine-a new safe substance for postoperative ear care. Auris Nasus Larynx 34:19-22
64. Ogino T, Kobuchi H, Sen CK, Roy S, Packer L, Maguire JJ (1997) Monochloramine inhibits phorbol ester-inducible neutrophil respiratory burst activation and T cell interleukin-2 receptor expression by inhibiting inducible protein kinase C activity. J Biol Chem 272:26247-26252
65. Olszanecki R, Marcinkiewicz J (2004) Taurine chloramine and taurine bromamine induce heme oxygenase-1 in resting and LPS-stimulated J774.2 macrophages. Amino Acids 27:29-35
66. Olszanecki R, Kurnyta M, Biedron R, Chorobik P, Bereta M, Marcinkiewicz J (2008) The role of heme oxygenase-1 in down regulation of PGE2 production by taurine chloramine and taurine bromamine in J774.2 macrophages. Amino Acids 35:359-364
67. 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
68. Park E, Schuller-Levis G, Quinn MR (1995) 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 154:4778-4784
69. Park E, Schuller-Levis G, Jia JH, Quinn MR (1997) Preactivation exposure of RAW 264.7 cells to taurine chloramine attenuates subsequent production of nitric oxide and expression of iNOS mRNA. J Leukoc Biol 61:161-166
70. Park E, Alberti J, Quinn MR, Schuller-Levis G (1998) Taurine chloramine inhibits the production of superoxide anion, IL-6 and IL-8 in activated human polymorphonuclear leukocytes. Adv Exp Med Biol 442:177-182
71. Park E, Levis WR, Quinn MR, Park SY, Schuller-Levis GB (2000a) Regulation of nitric oxide induced by mycobacterial lipoarabinomannan in murine macrophages: effects of interferon-beta and taurine-chloramine. Int J Lepr Other Mycobact Dis 68:444-451
72. Park E, Quinn MR, Schuller-Levis G (2000b) Taurine chloramine attenuates the hydrolytic activity of matrix metalloproteinase-9 in LPS-activated murine peritoneal macrophages. Adv Exp Med Biol 483:389-398
73. Park E, Jia J, Quinn MR, Schuller-Levis G (2002) Taurine chloramine inhibits lymphocyte proliferation and decreases cytokine production in activated human leukocytes. Clin Immunol 102:179-184
74. Pero RW, Sheng Y, Olsson A, Bryngelsson C, Lund-Pero M (1996) Hypochlorous acid/N-chloramines are naturally produced DNA repair inhibitors. Carcinogenesis 17:13-18
75. Piao S, Cha YN, Kim C (2011) Taurine chloramine protects RAW 264.7 macrophages against hydrogen peroxide-induced apoptosis by increasing antioxidants. J Clin Biochem Nutr 49:50-56
76. Pilz M, Holinka J, Vavken P, Marian B, Krepler P (2012) Taurine chloramine induces apoptosis in human osteosarcoma cell lines. J Orthop Res 30:2046-2051
77. Quinn MR, Park E, Schuller-Levis G (1996) Taurine chloramine inhibits prostaglandin E2 production in activated RAW 264.7 cells by post-transcriptional effects on inducible cyclooxygenase expression. Immunol Lett 50:185-188
78. Quinn MR, Barua M, Liu Y, Serban V (2003) 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 526:341-348
79. Schuller-Levis GB, Park E (2003) Taurine: new implications for an old amino acid. FEMS Microbiol Lett 226:195-202
80. Schuller-Levis GB, Levis WR, Ammazzalorso M, Nosrati A, Park E (1994) Mycobacterial lipoarabinomannan induces nitric oxide and tumor necrosis factor alpha production in a macrophage cell line: down regulation by taurine chloramine. Infect Immun 62:4671-4674
81. Schwienbacher M, Treml B, Pinna A, Geiger R, Reinstadler H, Pircher I, Schmidl E, Willomitzer C, Neumeister J, Pilch M, Hauer M, Hager T, Sergi C, Scholl-Burgi S, Giese T, Lockinger A, Nagl M (2011) Tolerability of inhaled N-chlorotaurine in an acute pig streptococcal lower airway inflammation model. BMC Infect Dis 11:231
82. Son M, Kim HK, Kim WB, Yang J, Kim BK (1996) Protective effect of taurine on indomethacin-induced gastric mucosal injury. Adv Exp Med Biol 403:147-155
83. Son M, Ko JI, Kim WB, Kang HK, Kim BK (1998) Taurine can ameliorate inflammatory bowel disease in rats. Adv Exp Med Biol 442:291-298
84. Srisook K, Cha YN (2004) Biphasic induction of heme oxygenase-1 expression in macrophages stimulated with lipopolysaccharide. Biochem Pharmacol 68:1709-1720
85. Sun Jang J, Piao S, Cha YN, Kim C (2009) Taurine chloramine activates Nrf2, increases HO-1 expression and protects cells from death caused by hydrogen peroxide. J Clin Biochem Nutr 45:37-43
86. Tallan HH, Jacobson E, Wright CE, Schneidman K, Gaull GE (1983) Taurine uptake by cultured human lymphoblastoid cells. Life Sci 33:1853-1860
87. Tenhunen R, Marver HS, Schmid R (1968) The enzymatic conversion of heme to bilirubin by microsomal heme oxygenase. Proc Natl Acad Sci USA 61:748-755
88. Teuchner B, Eitzinger C, Lutz M, Hager T, Schmid E, Bechrakis NE, Zuck M, Jekle A, Debabov D, Anderson M, Nagl M (2012) N-chlorotaurine and its analogues N,N-dichloro-2,2-dimethyltaurine and N-monochloro-2,2-dimethyltaurine are safe and effective bactericidal agents in ex vivo corneal infection models. Acta Ophthalmol 90:e632-e637
89. Tiedemann F, Gmelin L (1827) Einige neue Bestandtheile der Galle des Ochsen. Ann Phys 85:326-337
90. Verdrengh M, Tarkowski A (2005) Inhibition of septic arthritis by local administration of taurine chloramine, a product of activated neutrophils. J Rheumatol 32:1513-1517
91. Wang Q, Hyde DM, Giri SN (1992) 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
92. Wang L, Belisle B, Bassiri M, Xu P, Debabov D, Celeri C, Alvarez N, Robson MC, Payne WG, Najafi R, Khosrovi B (2011a) Chemical characterization and biological properties of NVC-422, a novel, stable N-chlorotaurine analog. Antimicrob Agents Chemother 55:2688-2692
93. Wang Y, Cha YN, Kim KS, Kim C (2011b) Taurine chloramine inhibits osteoclastogenesis and splenic lymphocyte proliferation in mice with collagen-induced arthritis. Eur J Pharmacol 668:325-330
94. Weiss SJ, Klein R, Slivka A, Wei M (1982) Chlorination of taurine by human neutrophils. Evidence for hypochlorous acid generation. J Clin Investig 70:598-607
95. Wirleitner B, Neurauter G, Nagl M, Fuchs D (2004) Down-regulatory effect of N-chlorotaurine on tryptophan degradation and neopterin production in human PBMC. Immunol Lett 93:143-149
96. Witko V, Nguyen AT, Descamps-Latscha B (1992) Microtiter plate assay for phagocyte-derived taurine-chloramines. J Clin Lab Anal 6:47-53
97. Wojtecka-Lukasik E, Gujski M, Roguska K, Maslinska D, Maslinski S (2005) Taurine chloramine modifies adjuvant arthritis in rats. Inflamm Res 54(Suppl 1):S21-S22
98. Ximenes VF, Padovan CZ, Carvalho DA, Fernandes JR (2010) Oxidation of melatonin by taurine chloramine. J Pineal Res 49:115-122
99. Ximenes VF, da Fonseca LM, de Almeida AC (2011) Taurine bromamine: a potent oxidant of tryptophan residues in albumin. Arch Biochem Biophys 507:315-322
100. Yazdanbakhsh M, Eckmann CM, Roos D (1987) Killing of schistosomula by taurine chloramine and taurine bromamine. Am J Trop Med Hyg 37:106-110
101. Zhen L, King AA, Xiao Y, Chanock SJ, Orkin SH, Dinauer MC (1993) Gene targeting of X chromosome-linked chronic granulomatous disease locus in a human myeloid leukemia cell line and rescue by expression of recombinant gp91phox. Proc Natl Acad Sci USA 90:9832-9836