Psoriasis is associated with low serum levels of hydrogen sulfide, a potential anti-inflammatory molecule

Tohoku Journal of Experimental Medicine

Volumn 228, Issue 4, 2012, Pages 325-332

  Alshorafa, Ammar K H ^a   Guo, Qing ^a   Zeng, Fanqin ^a   Chen, Mingchun ^a   Yin, Ruofei ^a   Tan, Guozhen ^a   Tang, Zengqi ^a  

^a SUN YAT SEN UNIVERSITY   (China)

Author keywords

Hydrogen sulfide; Inflammatory cytokines; Mitogen activated protein kinases; Nuclear factor kappa B; Psoriasis

Indexed keywords

HYDROGEN SULFIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; INTERLEUKIN 8; MITOGEN ACTIVATED PROTEIN KINASE P38; NITRIC OXIDE; TUMOR NECROSIS FACTOR ALPHA;

ADULT; AGED; ARTICLE; BLOOD LEVEL; CELL VIABILITY; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; DISEASE ASSOCIATION; DISEASE SEVERITY; ENZYME ACTIVATION; FEMALE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; KERATINOCYTE; MALE; PATHOGENESIS; PSORIASIS; PSORIASIS SEVERITY INDEX; SCHOOL CHILD; UPREGULATION;

ANTI-INFLAMMATORY AGENTS; BLOTTING, WESTERN; CELL LINE; DNA PRIMERS; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME-LINKED IMMUNOSORBENT ASSAY; HUMANS; HYDROGEN SULFIDE; INTERLEUKIN-6; INTERLEUKIN-8; KERATINOCYTES; NITRIC OXIDE; NITRITES; PSORIASIS; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TETRAZOLIUM SALTS; THIAZOLES; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84869021999     PISSN: 00408727     EISSN: 13493329     Source Type: Journal    
DOI: 10.1620/tiem.228.325     Document Type: Article

References (44)

1. Amigo, M., Paya, M., Braza-Boils, A., De Rosa, S. & Terencio, M.C. (2008) Avarol inhibits TNF-alpha generation and NF-kappaB activation in human cells and in animal models. Life Sci., 82, 256-264.
2. Arican, O., Aral, M., Sasmaz, S. & Ciragil, P. (2005) Serum levels of TNF-alpha, IFN-gamma, IL-6, IL-8, IL-12, IL-17, and IL-18 in patients with active psoriasis and correlation with disease severity. Mediators Inflamm., 2005, 273-279.
3. Cai, Y., Fleming, C. & Yan, J. (2012) New insights of T cells in the pathogenesis of psoriasis. Cell Mol. Immunol., 9, 302-309.
4. Cho, J.W., Lee, K.S. & Kim, C.W. (2007) Curcumin attenuates the expression of IL-lbeta, IL-6, and TNF-alpha as well as cyclin E in TNF-alpha-treated HaCaT cells; NF-kappaB and MAPKs as potential upstream targets Int. J. Mol. Med., 19, 469-474.
5. De Vry, C.G., Valdez, M., Lazarov, M., Muhr, E., Buelow, R., Fong, T. & Iyer, S. (2005) Topical application of a novel immunomodulatory peptide, RDP58, reduces skin inflamma-tion in the phorbol ester-induced dermatitis model. J. Invest. Dermatol., 125, 473-481.
6. Du, J., Cheng, B., Zhu, X. & Ling, C. (2011) Ginsenoside rgl, a novel glucocorticoid receptor agonist of plant origin, main-tains glucocorticoid efficacy with reduced side effects. J. Immunol., 187, 942-950.
7. Gobbi, G., Ricci, F., Malinverno, C., Carubbi, C., Pambianco, M., Panfilis, G., Vitale, M. & Mirandola, P. (2009) Hydrogen sulfide impairs keratinocyte cell growth and adhesion inhib-iting mitogen-activated protein kinase signaling. Lab. Invest., 89, 994-1006.
8. Grossman, R.M., Krueger, J., Yourish, D., Granelli-Piperno, A., Murphy, D.P., May, L.T., Kupper, T.S., Sehgal, P.B. & Gottlieb, A.B. (1989) Interleukin 6 is expressed in high levels in psoriatic skin and stimulates proliferation of cultured human keratinocytes. Proc. Natl. Acad. Sci. USA, 86, 6367-6371.
9. Hattori, T., Obinata, H., Ogawa, A., Kishi, M., Tatei, K., Ishikawa, O. & Izumi, T. (2008) G2A plays proinflammatory roles in human keratinocytes under oxidative stress as a receptor for 9-hydroxyoctadecadienoic acid. J. Invest. Dermatol., 128, 1123-1133.
10. Higuchi, M., Higashi, N., Taki, H. & Osawa, T. (1990) Cytolytic mechanisms of activated macrophages. Tumor necrosis factor and L-arginine-dependent mechanisms act synergistically as the major cytolytic mechanisms of activated macrophages. J. Immunol., 144, 1425-1431.
11. Hong, I., Rho, H.S., Kim, D.H. & Lee, M.O. (2010) Activation of LXRalpha induces lipogenesis in HaCaT cells. Arch. Pharm. Res., 33, 1443-1449.
12. Ikuta, S., Edamatsu, H., Li, M., Hu, L. & Kataoka, T. (2008) Crucial role of phospholipase C epsilon in skin inflammation induced by tumor-promoting phorbol ester. Cancer Res., 68, 64-72.
13. Jeong, S.H., Park, J.H., Kim, J.N., Park, Y.H., Shin, S.Y., Lee, Y.H., Kye, Y.C. & Son, S.W. (2010) Up-regulation of TNF-alpha secretion by cigarette smoke is mediated by Egr-1 in HaCaT human keratinocytes. Exp. Dermatol., 19, e206-212.
14. Kemeny, L., Michel, G., Dobozy, A. & Ruzicka, T. (1994) Cyto-kine system as potential target for antipsoriatic therapy. Exp. Dermatol., 3, 1-8.
15. Krueger, J.G. & Bowcock, A. (2005) Psoriasis pathophysiology: current concepts of pathogenesis. Ann. Rheum. Dis., 64 Suppl 2, ii30-ii36.
16. Kurylowicz, A. & Nauman, J. (2008) The role of nuclear factor-kappaB in the development of autoimmune diseases: a link between genes and environment. Acta Biochim. Pol., 55, 629-647.
17. Kwon, D.J., Bae, Y.S., Ju, S.M., Goh, A.R., Choi, S.Y. & Park, J. (2011) Casuarinin suppresses TNF-alpha-induced ICAM-1 expression via blockade of NF-kappaB activation in HaCaT cells. Biochem. Biophys. Res. Commun., 409, 780-785.
18. Lee, C.S., Lee, S.A., Kim, Y.J., Seo, S.J. & Lee, M.W., (2011) 3,4,5-Tricaffeoylquinic acid inhibits tumor necrosis factor-alpha-stimulated production of inflammatory mediators in keratinocytes via suppression of Akt- and NF-kappaB-path-ways. Int. Immunopharmacol., 11, 1715-1723.
19. Li, L., Hsu, A. & Moore, P.K. (2009) Actions and interactions of nitric oxide, carbon monoxide and hydrogen sulphide in the cardiovascular system and in inflammation-a tale of three gases! Pharmacol. Ther, 123, 386-400.
20. Mancardi, D., Penna, C., Merlino, A., Del Soldato, P., Wink, D.A. & Pagliaro, P. (2009) Physiological and pharmacological features of the novel gasotransmitter: hydrogen sulfide. Biochim. Biophys. Acta, 1787, 864-872.
21. Mizumura, K., Gon, Y., Kumasawa, F., Onose, A., Maruoka, S., Matsumoto, K., Hayashi, S., Kobayashi, T. & Hashimoto, S. (2010) Apoptosis signal-regulating kinase 1-mediated signaling pathway regulates lipopolysaccharide-induced tissue factor expression in pulmonary microvasculature. Int. Immu-nopharmacol., 10, 1062-1067.
22. Moore, P.K., Bhatia, M. & Moochhala, S. (2003) Hydrogen sulfide: from the smell of the past to the mediator of the future? Trends Pharmacol. Sci., 24, 609-611.
23. Nestle, F.O., Di Meglio, P., Qin, J.Z. & Nickoloff, B.J. (2009) Skin immune sentinels in health and disease. Nat. Rev. Immunol., 9, 679-691.
24. Oh, G.S., Pae, H.O., Lee, B.S., Kim, B.N., Kim, J.M., Kim, H.R., Jeon, S.B., Jeon, W.K., Chae, H.J. & Chung, H.T. (2006) Hydrogen sulfide inhibits nitric oxide production and nuclear factor-kappaB via heme oxygenase-1 expression in RAW264.7 macrophages stimulated with lipopolysaccharide. Free Radic. Biol. Med., 41, 106-119.
25. Olson, K.R. (2011) The therapeutic potential of hydrogen sulfide: separating hype from hope. Am. J. Physiol. Regul. Integr. Comp. Physiol., 301, R297-312.
26. Ormerod, A.D., Weller, R., Copeland, P., Benjamin, N., Ralston, S.H., Grabowksi, P. & Herriot, R. (1998) Detection of nitric oxide and nitric oxide synthases in psoriasis. Arch. Dermatol. Res., 290, 3-8.
27. Pei, Y., Barber, L.A., Murphy, R.C., Johnson, C.A., Kelley, S.W., Dy, L.C., Fertel, R.H., Nguyen, T.M., Williams, D.A. & Travers, J.B. (1998) Activation of the epidermal platelet-acti-vating factor receptor results in cytokine and cyclooxy-genase-2 biosynthesis. J Immunol., 161, 1954-1961.
28. Portugal-Cohen, M. & Kohen, R. (2009) Exposure of human kera-tinocytes to ischemia, hyperglycemia and their combination induces oxidative stress via the enzymes inducible nitric oxide synthase and xanthine oxidase. I Dermatol. Sci., 55, 82-90.
29. Sabat, R., Philipp, S., Hoflich, C., Kreutzer, S., Wallace, E., Asadullah, K., Volk, H.D., Sterry, W. & Wolk, K. (2007) Immunopathogenesis of psoriasis. Exp. Dermatol., 16, 779-798.
30. Schottelius, A.J., Moldawer, L.L., Dinarello, C.A., Asadullah, K., Sterry, W. & Edwards, C.K 3rd. (2004) Biology of tumor necrosis factor-alpha-implications for psoriasis. Exp. Dermatol., 13, 193-222.
31. Sigurdardottir, S.L., Thorleifsdottir, R.H., Valdimarsson, H., & Johnston, A., (2012) The Role of the Palatine Tonsils in the Pathogenesis and Treatment of Psoriasis. Br. I Dermatol., [Epub ahead of print].
32. Sun, J., Han, J., Zhao, Y., Zhu, Q. & Hu, J. (2012) Curcumin induces apoptosis in tumor necrosis factor-alpha-treated HaCaT cells. Int. Immunopharmacol., 13, 170-174.
33. Traub, M. & Marshall, K. (2007) Psoriasis-pathophysiology, conventional, and alternative approaches to treatment. Altern. Med. Rev., 12, 319-330.
34. Tsuruta, D. (2009) NF-kappaB links keratinocytes and lympho-cytes in the pathogenesis of psoriasis. Recent Pat. Inflamm. Allergy Drug Discov, 3, 40-48.
35. Wallace, J.L., Ferraz, J.G. & Muscara, M.N. (2012) Hydrogen sulfide: an endogenous mediator of resolution of inflammation and injury. Antioxid. Redox. Signal., 17, 58-67.
36. Wang, B.J., Sheu, H.M., Guo, Y.L., Lee, Y.H., Lai, C.S., Pan, M.H. & Wang, Y.J. (2010) Hexavalent chromium induced ROS formation, Akt, NF-kappaB, and MAPK activation, and TNF-alpha and IL-lalpha production in keratinocytes. Toxicol. Lett., 198, 216-224.
37. Li, L., Rose, P. & Moore, P.K. (2011) Hydrogen sulfide and cell signalling. Annu. Rev. Pharmacol. Toxicol., 51, 169-187
38. Wang, R. (2002) Two's company, three's a crowd: can H2S be the third endogenous gaseous transmitter? FASEB J., 16, 1792-1798.
39. Whiteman, M. & Winyard, P.G. (2011) Hydrogen sulfide and inflammation: the good, the bad, the ugly and the promising Expert Rev. Clin. Pharmacol., 4, 13-32.
40. Wolfram, J.A., Diaconu, D., Hatala, D.A., Rastegar, J., Knutsen, D.A., Lowther, A., Askew, D., Gilliam, A.C., McCormick, T.S. & Ward, N.L. (2009) Keratinocyte but not endothelial cell-specific overexpression of Tie2 leads to the development of psoriasis. Am. J. Pathol., 174, 1443-1458.
41. Yamaoka, J., Kume, T., Akaike, A. & Miyachi, Y. (2000) Suppres-sive effect of zinc ion on iNOS expression induced by inter-feron-gamma or tumor necrosis factor-alpha in murine kerati-nocytes. J. Dermatol. Sci., 23, 27-35.
42. You, X.J., Xu, C., Lu, J.Q., Zhu, X.Y., Gao, L., Cui, X.R., Li, Y., Gu, H. & Ni, X. (2011) Expression of cystathionine beta-synthase and cystathionine gamma-lyase in human pregnant myometrium and their roles in the control of uterine contrac-tility. PLoS One, 6, e23788.
43. Yu, B., Koga, T., Urabe, K., Moroi, Y., Maeda, S., Yanagihara, Y. & Furue, M. (2002) Differential regulation of thymus- and activation-regulated chemokine induced by IL-4, IL-13, TNF-alpha and IFN-gamma in human keratinocyte and fibroblast. J. Dermatol. Sci., 30, 29-36.
44. Zalewska, A., Glowacka, E., Wyczolkowska, J., Tchorzewski, H., Narbutt, J. & Sysa-Jedrzejowska, A. (2006) Interleukin 6 and 8 levels in plasma and fibroblast cultures in psoriasis. Media-tors Infamm., 2006, 81767.