Summary.
Interleukin-6 (IL-6) and interleukin-8 (IL-8) are implicated in the pathogenesis of rheumatic diseases. In affected joints fibroblast-like synoviocytes (FLS) are the major source of these pro-inflammatory cytokines. We have previously found that production of both cytokines is inhibited in vitro by taurine chloramine (Tau-Cl). Heme oxygenase (HO-1) activity was also reported to restrict synthesis of various inflammatory mediators, including IL-6 and IL-8. The aim of present study was to investigate whether this enzyme activity is implicated in the mechanism of Tau-Cl suppressive effect. We have shown that in rheumatoid FLS both hemin (known HO-1 inducer) and Tau-Cl significantly up-regulate HO-1 expression at the mRNA and protein levels and simultaneously inhibit IL-1β-triggered production of pro-inflammatory cytokines. However, the inhibitory potency of these compounds differs, because hemin is more potent inhibitor of IL-8 than IL-6 production, while Tau-Cl exerts opposite effect. Importantly, pretreatment of the cells with HO-1 inhibitor completely reverses the inhibitory effect of hemin on both cytokines production. However, in Tau-Cl treated cells this inhibitor fully restores only IL-8 secretion but has weaker effect on IL-6 response. Thus, the present results: (i) support HO-1 activity to be relevant to negatively control production of pro-inflammatory cytokines, and (ii) underline implication of HO-1 in mediating Tau-Cl inhibitory action.
Similar content being viewed by others
References
J Alam JL Cook (2007) ArticleTitleHow many transcription factors does it take to turn on the heme oxygenase-1 gene? Am J Respir Cell Mol Biol 36 166–174 Occurrence Handle16990612 Occurrence Handle10.1165/rcmb.2006-0340TR Occurrence Handle1:CAS:528:DC%2BD2sXhvFWjur0%3D
MJ Alcaraz A Habib M Lebret C Creminon S Levy-Toledano J Maclouf (2000) ArticleTitleEnhanced expression of haem oxygenase-1 by nitric oxide and antiinflammatory drugs in NIH 3T3 fibroblasts Br J Pharmacol 130 57–64 Occurrence Handle10780998 Occurrence Handle10.1038/sj.bjp.0703281 Occurrence Handle1:CAS:528:DC%2BD3cXjsFykur0%3D
CS Bonnet DA Walsh (2005) ArticleTitleOsteoarthritis, angiogenesis and inflammation Rheumatology (Oxford) 44 7–16 Occurrence Handle10.1093/rheumatology/keh344 Occurrence Handle1:STN:280:DC%2BD2cnjsFyktA%3D%3D
DL Cecil DM Rose R Terkeltaub R Liu-Bryan (2005) ArticleTitleRole of interleukin-8 in PiT-1 expression and CXCR1-mediated inorganic phosphate uptake in chondrocytes Arthritis Rheum 52 144–154 Occurrence Handle15641067 Occurrence Handle10.1002/art.20748 Occurrence Handle1:CAS:528:DC%2BD2MXht1Kisbc%3D
B Dawn R Bolli (2005) ArticleTitleHO-1 induction by HIF-1: a new mechanism for delayed cardioprotection? Am J Physiol Heart Circ Physiol 289 H522–H524 Occurrence Handle16014614 Occurrence Handle10.1152/ajpheart.00274.2005 Occurrence Handle1:CAS:528:DC%2BD2MXotFaqtb4%3D
W Gottardi M Nagl (2002) ArticleTitleChemical properties of N-chlorotaurine sodium, a key compound in the human defence system Arch Pharm (Weinheim) 335 411–421 Occurrence Handle10.1002/1521-4184(200212)335:9<411::AID-ARDP411>3.0.CO;2-D Occurrence Handle1:CAS:528:DC%2BD38Xps12jsbc%3D
FM Ho HC Kang ST Lee Y Chao YC Chen LJ Huang WW Lin (2007) ArticleTitleThe anti-inflammatory actions of LCY-2-CHO, a carbazole analogue, in vascular smooth muscle cells Biochem Pharmacol 74 298–308 Occurrence Handle17499220 Occurrence Handle10.1016/j.bcp.2007.04.008 Occurrence Handle1:CAS:528:DC%2BD2sXmsFKgtLk%3D
LC Huber O Distler I Tarner RE Gay S Gay T Pap (2006) ArticleTitleSynovial fibroblasts: key players in rheumatoid arthritis Rheumatology (Oxford) 45 669–675 Occurrence Handle10.1093/rheumatology/kel065 Occurrence Handle1:CAS:528:DC%2BD28Xmt1Wrsr4%3D
CD Jun Y Kim EY Choi M Kim B Park B Youn K Yu KS Choi KH Yoon SC Choi MS Lee KI Park M Choi Y Chung J Oh (2006) ArticleTitleGliotoxin reduces the severity of trinitrobenzene sulfonic acid-induced colitis in mice: evidence of the connection between heme oxygenase-1 and the nuclear factor-kappaB pathway in vitro and in vivo Inflamm Bowel Dis 12 619–629 Occurrence Handle16804400 Occurrence Handle10.1097/01.ibd.0000225340.99108.8a
K Kataoka H Handa M Nishizawa (2001) ArticleTitleInduction of cellular antioxidative stress genes through heterodimeric transcription factor Nrf2/small Maf by antirheumatic gold(I) compounds J Biol Chem 276 34074–34081 Occurrence Handle11429414 Occurrence Handle10.1074/jbc.M105383200 Occurrence Handle1:CAS:528:DC%2BD3MXmslylur0%3D
C Kim HS Choi JW Kim (2006) ArticleTitleTaurine chloramine inhibits the production of nitric oxide and superoxide anion by modulating specific mitogen-activated protein kinases Adv Exp Med Biol 583 493–498 Occurrence Handle17153636 Occurrence Handle10.1007/978-0-387-33504-9_55 Occurrence Handle1:CAS:528:DC%2BD1MXhtFWis7c%3D
KS Kim EK Park SM Ju HS Jung JS Bang C Kim YA Lee SJ Hong SH Lee HI Yang MC Yoo (2007) ArticleTitleTaurine chloramine differentially inhibits matrix metalloproteinase 1 and 13 synthesis in interleukin-1beta-stimulated fibroblast-like synoviocytes Arthritis Res Ther 9 R80 Occurrence Handle17697361 Occurrence Handle10.1186/ar2279 Occurrence Handle1:CAS:528:DC%2BD2sXhtVOntLvP
Y Kirino M Takeno S Murakami M Kobayashi H Kobayashi K Miura H Ideguchi S Ohno A Ueda Y Ishigatsubo (2007) ArticleTitleTumor necrosis factor alpha acceleration of inflammatory responses by down-regulating heme oxygenase 1 in human peripheral monocytes Arthritis Rheum 56 464–475 Occurrence Handle17265482 Occurrence Handle10.1002/art.22370 Occurrence Handle1:CAS:528:DC%2BD2sXislShtbs%3D
KA Kirkby CA Adin (2006) ArticleTitleProducts of heme oxygenase and their potential therapeutic applications Am J Physiol Renal Physiol 290 F563–F571 Occurrence Handle16461755 Occurrence Handle10.1152/ajprenal.00220.2005 Occurrence Handle1:CAS:528:DC%2BD28XjtFCnsb4%3D
H Kobayashi M Takeno T Saito Y Takeda Y Kirino K Noyori T Hayashi A Ueda Y Ishigatsubo (2006) ArticleTitleRegulatory role of heme oxygenase 1 in inflammation of rheumatoid arthritis Arthritis Rheum 54 1132–1142 Occurrence Handle16572448 Occurrence Handle10.1002/art.21754 Occurrence Handle1:CAS:528:DC%2BD28XksVyhtL4%3D
E Kontny A Grabowska J Kowalczewski M Kurowska I Janicka J Marcinkiewicz W Maslinski (1999) ArticleTitleTaurine chloramine inhibition of cell proliferation and cytokine production by rheumatoid arthritis fibroblast-like synoviocytes Arthritis Rheum 42 2552–2560 Occurrence Handle10616000 Occurrence Handle10.1002/1529-0131(199912)42:12<2552::AID-ANR7>3.0.CO;2-V Occurrence Handle1:CAS:528:DC%2BD3cXjslagug%3D%3D
E Kontny K Szczepanska J Kowalczewski M Kurowska I Janicka J Marcinkiewicz W Maslinski (2000) ArticleTitleThe mechanism of taurine chloramine inhibition of cytokine (interleukin-6, interleukin-8) production by rheumatoid arthritis fibroblast-like synoviocytes Arthritis Rheum 43 2169–2177 Occurrence Handle11037876 Occurrence Handle10.1002/1529-0131(200010)43:10<2169::AID-ANR4>3.0.CO;2-# Occurrence Handle1:CAS:528:DC%2BD3cXnslWjsrY%3D
E Kontny W Rudnicka J Kowalczewski J Marcinkiewicz W Maslinski (2003) ArticleTitleSelective inhibition of cyclooxygenase 2-generated prostaglandin E2 synthesis in rheumatoid arthritis synoviocytes by taurine chloramine Arthritis Rheum 48 1551–1555 Occurrence Handle12794822 Occurrence Handle10.1002/art.10975 Occurrence Handle1:CAS:528:DC%2BD3sXltlSgur0%3D
E Kontny M Chorazy-Massalska W Rudnicka J Marcinkiewicz W Maslinski (2006a) ArticleTitleCytotoxicity of taurine metabolites depends on the cell type Adv Exp Med Biol 583 157–171 Occurrence Handle10.1007/978-0-387-33504-9_16 Occurrence Handle1:CAS:528:DC%2BD1MXhtFWjuro%3D
E Kontny W Rudnicka M Chorazy-Massalska J Marcinkiewicz W Maslinski (2006b) ArticleTitleTaurine chloramine inhibits proliferation of rheumatoid arthritis synoviocytes by triggering a p53-dependent pathway Inflamm Res 55 446–455 Occurrence Handle10.1007/s00011-006-5067-5 Occurrence Handle1:CAS:528:DC%2BD2sXjsFWlsg%3D%3D
E Kontny M Chorazy-Massalska W Rudnicka J Marcinkiewicz W Maslinski (2007) ArticleTitleComparison of taurine chloramine and taurine bromamine effects on rheumatoid arthritis synoviocytes Amino Acids 32 447–452 Occurrence Handle16868648 Occurrence Handle10.1007/s00726-006-0368-0 Occurrence Handle1:CAS:528:DC%2BD2sXjvFanu7Y%3D
A Mainnemare B Megarbane A Soueidan A Daniel IL Chapple (2004) ArticleTitleHypochlorous acid and taurine-N-monochloramine in periodontal diseases J Dent Res 83 823–831 Occurrence Handle15505230 Occurrence Handle1:CAS:528:DC%2BD2cXhtVenurzE
CJ Malemud (2004) ArticleTitleCytokines as therapeutic targets for osteoarthritis Bio Drugs 18 23–35 Occurrence Handle1:CAS:528:DC%2BD2cXitV2jur0%3D
J Marcinkiewicz M Kurnyta R Biedron M Bobek E Kontny W Maslinski (2006) ArticleTitleAnti-inflammatory effects of taurine derivatives (taurine chloramine, taurine bromamine, and taurolidine) are mediated by different mechanisms Adv Exp Med Biol 583 481–492 Occurrence Handle17153635 Occurrence Handle10.1007/978-0-387-33504-9_54 Occurrence Handle1:CAS:528:DC%2BD1MXhtFWis7Y%3D
IB McInnes G Schett (2007) ArticleTitleCytokines in the pathogenesis of rheumatoid arthritis Nat Rev Immunol 7 429–442 Occurrence Handle17525752 Occurrence Handle10.1038/nri2094 Occurrence Handle1:CAS:528:DC%2BD2sXls1Kgt74%3D
Y Miyamoto A Kanayama J Inoue YS Konishi M Shimizu (2003) ArticleTitleTaurine is involved in oxidation of IkappaB alpha at Met45: N-halogenated taurine and anti-inflammatory action Adv Exp Med Biol 526 373–380 Occurrence Handle12908622 Occurrence Handle1:CAS:528:DC%2BD3sXnsVyhtbo%3D
K Mizuno T Toma H Tsukiji H Okamoto H Yamazaki K Ohta Y Kasahara S Koizumi A Yachie (2005) ArticleTitleSelective expansion of CD16highCCR2-subpopulation of circulating monocytes with preferential production of haem oxygenase (HO)-1 in response to acute inflammation Clin Exp Immunol 142 461–470 Occurrence Handle16297158 Occurrence Handle1:CAS:528:DC%2BD2MXhtlWqtrrN
R Ockaili R Natarajan F Salloum BJ Fisher D Jones AA Fowler Suffix3rd RC Kukreja (2005) ArticleTitleHIF-1 activation attenuates postischemic myocardial injury: role for heme oxygenase-1 in modulating microvascular chemokine generation Am J Physiol Heart Circ Physiol 289 H542–H548 Occurrence Handle15805230 Occurrence Handle10.1152/ajpheart.00089.2005 Occurrence Handle1:CAS:528:DC%2BD2MXotFaqtb0%3D
R Olszanecki J Marcinkiewicz (2004) ArticleTitleTaurine chloramine and taurine bromamine induce heme oxygenase-1 in resting and LPS-stimulated J774.2 macrophages Amino Acids 27 29–35 Occurrence Handle15309569 Occurrence Handle10.1007/s00726-004-0097-1 Occurrence Handle1:CAS:528:DC%2BD2cXmsVKktL8%3D
LD Orozco MH Kapturczak B Barajas X Wang MM Weinstein J Wong J Deshane S Bolisetty Z Shaposhnik DM Shih A Agarwal AJ Lusis JA Araujo (2007) ArticleTitleHeme oxygenase-1 expression in macrophages plays a beneficial role in atherosclerosis Circ Res 100 1703–1711 Occurrence Handle17495224 Occurrence Handle10.1161/CIRCRESAHA.107.151720 Occurrence Handle1:CAS:528:DC%2BD2sXmslygtLw%3D
GA Ricchetti LM Williams BM Foxwell (2004) ArticleTitleHeme oxygenase 1 expression induced by IL-10 requires STAT-3 and phosphoinositol-3 kinase and is inhibited by lipopolysaccharide J Leukoc Biol 76 719–726 Occurrence Handle15240748 Occurrence Handle10.1189/jlb.0104046 Occurrence Handle1:CAS:528:DC%2BD2cXnsVaksbw%3D
SW Ryter J Alam AM Choi (2006) ArticleTitleHeme oxygenase-1/carbon monoxide: from basic science to therapeutic applications Physiol Rev 86 583–650 Occurrence Handle16601269 Occurrence Handle10.1152/physrev.00011.2005 Occurrence Handle1:CAS:528:DC%2BD28Xktlylu7k%3D
T Shinohara T Kaneko Y Nagashima A Ueda A Tagawa Y Ishigatsubo (2005) ArticleTitleAdenovirus-mediated transfer and overexpression of heme oxygenase 1 cDNA in lungs attenuates elastase-induced pulmonary emphysema in mice Hum Gene Ther 16 318–327 Occurrence Handle15812227 Occurrence Handle10.1089/hum.2005.16.318 Occurrence Handle1:CAS:528:DC%2BD2MXivFWltrw%3D
JA Stebulis RG Rossetti FJ Atez RB Zurier (2005) ArticleTitleFibroblast-like synovial cells derived from synovial fluid J Rheumatol 32 301–306 Occurrence Handle15693092 Occurrence Handle1:CAS:528:DC%2BD2MXitVemt78%3D
K Tron R Novosyadlyy J Dudas A Samoylenko T Kietzmann G Ramadori (2005) ArticleTitleUpregulation of heme oxygenase-1 gene by turpentine oil-induced localized inflammation: involvement of interleukin-6 Lab Invest 85 376–387 Occurrence Handle15640832 Occurrence Handle10.1038/labinvest.3700228 Occurrence Handle1:CAS:528:DC%2BD2MXhtlert7g%3D
K Tron A Samoylenko G Musikowski F Kobe S Immenschuh F Schaper G Ramadori T Kietzmann (2006) ArticleTitleRegulation of rat heme oxygenase-1 expression by interleukin-6 via the Jak/STAT pathway in hepatocytes J Hepatol 45 72–80 Occurrence Handle16510205 Occurrence Handle10.1016/j.jhep.2005.12.019 Occurrence Handle1:CAS:528:DC%2BD28XlsFKktLw%3D
CT Wang YT Lin BL Chiang YH Lin SM Hou (2006) ArticleTitleHigh molecular weight hyaluronic acid down-regulates the gene expression of osteoarthritis-associated cytokines and enzymes in fibroblast-like synoviocytes from patients with early osteoarthritis Osteoarthritis Cartilage 14 1237–1247 Occurrence Handle16806998 Occurrence Handle10.1016/j.joca.2006.05.009
J Zwerina S Tzima S Hayer K Redlich O Hoffmann B Hanslik-Schnabel JS Smolen G Kollias G Schett (2005) ArticleTitleHeme oxygenase 1 (HO-1) regulates osteoclastogenesis and bone resorption Faseb J 19 2011–2013 Occurrence Handle16234431 Occurrence Handle1:CAS:528:DC%2BD2MXhtlSmtLbO
Author information
Authors and Affiliations
Additional information
Authors’ address: Ewa Kontny, Ph.D., Department of Pathophysiology and Immunology, Institute of Rheumatology, Spartańska 1, 02-637 Warsaw, Poland
Rights and permissions
About this article
Cite this article
Muż, B., Kontny, E., Marcinkiewicz, J. et al. Heme oxygenase-1 participates in the anti-inflammatory activity of taurine chloramine. Amino Acids 35, 397–402 (2008). https://doi.org/10.1007/s00726-007-0605-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00726-007-0605-1