Skip to main content

Advertisement

Log in

Heme oxygenase-1 participates in the anti-inflammatory activity of taurine chloramine

  • Published:
Amino Acids Aims and scope Submit manuscript

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.

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

Access this article

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

Instant access to the full article PDF.

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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • CJ Malemud (2004) ArticleTitleCytokines as therapeutic targets for osteoarthritis Bio Drugs 18 23–35 Occurrence Handle1:CAS:528:DC%2BD2cXitV2jur0%3D

    CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

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

Reprints 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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00726-007-0605-1

Navigation