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Hydrogen sulfide diminishes the levels of thymic stromal lymphopoietin in activated mast cells

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Abstract

Bamboo salt (BS) is a Korean traditional type of salt and has been reported to have therapeutic effects on allergic inflammation. Thymic stromal lymphopoietin (TSLP) aggravates inflammation in the pathogenesis of allergic reactions, such as allergic rhinitis (AR). To confirm an active compound of BS, we investigated the effect of sulfur, a compound of BS, on the levels of TSLP in a human mast cell line, HMC-1 cells and a mouse model of AR using hydrogen sulfide (H2S) donor, sodium hydrosulfide (NaSH). We treated NaSH or BS in HMC-1 cells and activated the HMC-1 cells with phorbol myristate acetate and calcium ionophore A23187 (PMACI). ELISA for the production measurement of TSLP, PCR for the mRNA expression measurement of TSLP, and western blot analysis for the expression measurement of upstream mediators were performed. Mice were treated with NaSH and sensitized with ovalbumin (OVA). The levels of TSLP were measured in serum and nasal mucosa tissue in an OVA-induced AR mouse model. NaSH or BS diminished the production and mRNA expression of TSLP as well as interleukin (IL)-6 and tumor necrosis factor (TNF)-α in the PMACI-activated HMC-1 cells. NaSH or BS diminished the level of intracellular calcium in the PMACI-activated HMC-1 cells. NaSH or BS reduced the expression and activity of caspase-1 in the PMACI-activated HMC-1 cells. And NaSH or BS inhibited the expression of receptor interacting protein-2 and the phosphorylation of extracellular signal-regulated kinase in the PMACI-activated HMC-1 cells. The translocation of NF-κB into the nucleus as well as the phosphorylation and degradation of IκBα in the cytoplasm were diminished by NaSH or BS in the PMACI-activated HMC-1 cells. Furthermore, NaSH inhibited the production of TSLP, IL-6, and IL-8 in TNF-α-activated HMC-1 cells. Finally, the administration of NaSH showed a decrease in number of rubs on mice with OVA-induced AR. And the levels of immunoglobulin E and TSLP in the serum and the level of TSLP in the nasal mucosa tissue of the OVA-induced AR mice were reduced by NaSH. In conclusion, these findings show that H2S, as an active compound of BS is a potential agent to cure allergic inflammation.

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References

  1. Amin K (2012) The role of mast cells in allergic inflammation. Respir Med 106:9–14

    Article  PubMed  Google Scholar 

  2. Ataide MA, Andrade WA, Zamboni DS, Wang D, Souza Mdo C, Franklin BS, Elian S, Martins FS, Pereira D, Reed G, Fitzgerald KA, Golenbock DT, Gazzinelli RT (2014) Malaria-induced NLRP12/NLRP3-dependent caspase-1 activation mediates inflammation and hypersensitivity to bacterial superinfection. PLoS Pathog 10:e1003885

    Article  PubMed Central  PubMed  Google Scholar 

  3. Ather JL, Hodgkins SR, Janssen-Heininger YM, Poynter ME (2011) Airway epithelial NF-κB activation promotes allergic sensitization to an innocuous inhaled antigen. Am J Respir Cell Mol Biol 44:631–638

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  4. Bauchart-Thevret C, Stoll B, Chacko S, Burrin DG (2009) Sulfur amino acid deficiency upregulates intestinal methionine cycle activity and suppresses epithelial growth in neonatal pigs. Am J Physiol Endocrinol Metab 296:E1239–E1250

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  5. Bunyavanich S, Melen E, Wilk JB, Granada M, Soto-Quiros ME, Avila L, Lasky-Su J, Hunninghake GM, Wickman M, Pershagen G, O’Connor GT, Weiss ST, Celedón JC (2011) Thymic stromal lymphopoietin (TSLP) is associated with allergic rhinitis in children with asthma. Clin Mol Allergy 9:1

    Article  PubMed Central  PubMed  Google Scholar 

  6. Chen BC, Hsieh SL, Lin WW (2001) Involvement of protein kinases in the potentiation of lipopolysaccharide-induced inflammatory mediator formation by thapsigargin in peritoneal macrophages. J Leukoc Biol 69:280–288

    CAS  PubMed  Google Scholar 

  7. Chen BC, Lin WW (2001) PKC- and ERK-dependent activation of I kappa B kinase by lipopolysaccharide in macrophages: enhancement by P2Y receptor-mediated CaMK activation. Br J Pharmacol 134:1055–1065

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  8. Cianferoni A, Spergel J (2014) The importance of TSLP in allergic disease and its role as a potential therapeutic target. Expert Rev Clin Immunol 10:1463–1474

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  9. Collaco CR, Hochman DJ, Goldblum RM, Brooks EG (2006) Effect of sodium sulfite on mast cell degranulation and oxidant stress. Ann Allergy Asthma Immunol 96:550–556

    Article  CAS  PubMed  Google Scholar 

  10. Ekinci EI, Clarke S, Thomas MC, Moran JL, Cheong K, MacIsaac RJ, Jerums G (2011) Dietary salt intake and mortality in patients with type 2 diabetes. Diabetes Care 34:703–709

    Article  PubMed Central  PubMed  Google Scholar 

  11. Fan TJ, Han LH, Cong RS, Liang J (2005) Caspase family proteases and apoptosis. Acta Biochim Biophys Sin (Shanghai) 37:719–727

    Article  CAS  Google Scholar 

  12. Fink SL, Bergsbaken T, Cookson BT (2008) Anthrax lethal toxin and Salmonella elicit the common cell death pathway of caspase-1-dependent pyroptosis via distinct mechanisms. Proc Natl Acad Sci USA 105:4312–4317

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  13. Fouche G, van Rooyen S, Faleschini T (2013) Siphonochilus aethiopicus, a traditional remedy for the treatment of allergic asthma. TANG 3:e6

    Google Scholar 

  14. Gade AR, Kang M, Akbarali HI (2013) Hydrogen sulfide as an allosteric modulator of ATP-sensitive potassium channels in colonic inflammation. Mol Pharmacol 83:294–306

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  15. Galli SJ, Tsai M, Piliponsky AM (2008) The development of allergic inflammation. Nature 454:445–454

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  16. García-García E, Sánchez-Mejorada G, Rosales C (2001) Phosphatidylinositol 3-kinase and ERK are required for NF-kappaB activation but not for phagocytosis. J Leukoc Biol 70:649–658

    PubMed  Google Scholar 

  17. Goh FY, Cook KL, Upton N, Tao L, Lah LC, Leung BP, Wong WS (2013) Receptor-interacting protein 2 gene silencing attenuates allergic airway inflammation. J Immunol 191:2691–2699

    Article  CAS  PubMed  Google Scholar 

  18. Grimble RF (2006) The effects of sulfur amino acid intake on immune function in humans. J Nutr 136:1660S–16605S

    CAS  PubMed  Google Scholar 

  19. Guo Z, Zhang M, An H, Chen W, Liu S, Guo J, Yu Y, Cao X (2003) Fas ligation induces IL-1beta-dependent maturation and IL-1beta-independent survival of dendritic cells: different roles of ERK and NF-kappaB signaling pathways. Blood 102:4441–4447

    Article  CAS  PubMed  Google Scholar 

  20. Han NR, Kim HM, Jeong HJ (2012) Thymic stromal lymphopoietin is regulated by the intracellular calcium. Cytokine 59:215–217

    Article  CAS  PubMed  Google Scholar 

  21. Han NR, Oh HA, Nam SY, Moon PD, Kim DW, Kim HM, Jeong HJ (2014) TSLP induces mast cell development and aggravates allergic reactions through the activation of MDM2 and STAT6. J Invest Dermatol 134:2521–2530

    Article  CAS  PubMed  Google Scholar 

  22. He R, Geha RS (2010) Thymic stromal lymphopoietin. Ann N Y Acad Sci 1183:13–24

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  23. Heib V, Becker M, Warger T, Rechtsteiner G, Tertilt C, Klein M, Bopp T, Taube C, Schild H, Schmitt E, Stassen M (2007) Mast cells are crucial for early inflammation, migration of Langerhans cells, and CTL responses following topical application of TLR7 ligand in mice. Blood 110:946–953

    Article  CAS  PubMed  Google Scholar 

  24. Hsieh CJ, Hall K, Ha T, Li C, Krishnaswamy G, Chi DS (2007) Baicalein inhibits IL-1beta- and TNF-alpha-induced inflammatory cytokine production from human mast cells via regulation of the NF-kappaB pathway. Clin Mol Allergy 5:5

    Article  PubMed Central  PubMed  Google Scholar 

  25. Hu LF, Li Y, Neo KL, Yong QC, Lee SW, Tan BK, Bian JS (2011) Hydrogen sulfide regulates Na+/H+ exchanger activity via stimulation of phosphoinositide 3-kinase/Akt and protein kinase G pathways. J Pharmacol Exp Ther 339:726–735

    Article  CAS  PubMed  Google Scholar 

  26. Hua W, Chen Q, Gong F, Xie C, Zhou S, Gao L (2013) Cardioprotection of H2S by downregulating iNOS and upregulating HO-1 expression in mice with CVB3-induced myocarditis. Life Sci 93:949–954

    Article  CAS  PubMed  Google Scholar 

  27. Hwang KM, Jung KO, Song CH, Park KY (2008) Increased antimutagenic and anticlastogenic effects of doenjang (Korean fermented soybean paste) prepared with bamboo salt. J Med Food 11:717–722

    Article  CAS  PubMed  Google Scholar 

  28. Iwasaki M, Saito K, Takemura M, Sekikawa K, Fujii H, Yamada Y, Wada H, Mizuta K, Seishima M, Ito Y (2003) TNF-alpha contributes to the development of allergic rhinitis in mice. J Allergy Clin Immunol 112:134–140

    Article  CAS  PubMed  Google Scholar 

  29. Janeway CA Jr, Travers P, Walport M et al (2001) Immunobiology: the immune system in health and disease, 5th edn. Garland Science, New York

    Google Scholar 

  30. Jeffery PK, Haahtela T (2006) Allergic rhinitis and asthma: inflammation in a one-airway condition. BMC Pulm Med 6:S5

    Article  PubMed Central  PubMed  Google Scholar 

  31. Jeong HJ, Shin SY, Oh HA, KimMH Cho JS, Kim HM (2011) IL-32 up-regulation is associated with inflammatory cytokine production in allergic rhinitis. J Pathol 224:553–563

    Article  CAS  PubMed  Google Scholar 

  32. Jessup HK, Allakhverdi Z, Comeau MR, Park-Yoon BR, Ziegler SF, Delespesse G (2007) Thymic stromal lymphopoietin (TSLP) is a potent activator of human mast cells. J Immunol 178(38):4

    Google Scholar 

  33. Kamimura D, Ishihara K, Hirano T (2003) IL-6 signal transduction and its physiological roles: the signal orchestration model. Rev Physiol Biochem Pharmacol 149:1–38

    CAS  PubMed  Google Scholar 

  34. Kassel O, Sancono A, Krätzschmar J, Kreft B, Stassen M, Cato AC (2001) Glucocorticoids inhibit MAP kinase via increased expression and decreased degradation of MKP-1. EMBO J 20:7108–7116

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  35. Kim KY, Nam SY, Shin TY, Park KY, Jeong HJ, Kim HM (2012) Bamboo salt reduces allergic responses by modulating the caspase-1 activation in an OVA-induced allergic rhinitis mouse model. Food Chem Toxicol 50:3480–3488

    Article  CAS  PubMed  Google Scholar 

  36. Kim MS, Lim WK, Park RK, Shin T, Yoo YH, Hong SH, An NH, Kim HM (2005) Involvement of mitogen-activated protein kinase and NF-kappaB activation in Ca2+-induced IL-8 production in human mast cells. Cytokine 32:226–233

    Article  CAS  PubMed  Google Scholar 

  37. Kim YH, Ryu HI (2003) Elements in a bamboo salt and comparison of its elemental contents with those in other salts. Yakhak Hoeji 47:135–141

    Google Scholar 

  38. Kimura S, Pawankar R, Mori S, Nonaka M, Masuno S, Yagi T, Okubo K (2011) Increased expression and role of thymic stromal lymphopoietin in nasal polyposis. Allergy Asthma Immunol Res 3:186–193

    Article  PubMed Central  PubMed  Google Scholar 

  39. Knisz J, Banks A, McKeag L, Metcalfe DD, Rothman PB, Brown JM (2009) Loss of SOCS7 in mice results in severe cutaneous disease and increased mast cell activation. Clin Immunol 132:277–284

    Article  CAS  PubMed  Google Scholar 

  40. Korideck H, Peterson JD (2009) Noninvasive quantitative tomography of the therapeutic response to dexamethasone in ovalbumin-induced murine asthma. J Pharmacol Exp Ther 329:882–889

    Article  CAS  PubMed  Google Scholar 

  41. Kouzaki H, O’Grady SM, Lawrence CB, Kita H (2009) Proteases induce production of thymic stromal lymphopoietin by airway epithelial cells through protease-activated receptor-2. J Immunol 183:1427–1434

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  42. Kumar RK, Herbert C, Foster PS (2008) The “classical” ovalbumin challenge model of asthma in mice. Curr Drug Targets 9:485–494

    Article  CAS  PubMed  Google Scholar 

  43. Li L, Bin LH, Li F, Liu Y, Chen D, Zhai Z, Shu HB (2005) TRIP6 is a RIP2-associated common signaling component of multiple NF-kappaB activation pathways. J Cell Sci 118:555–563

    Article  CAS  PubMed  Google Scholar 

  44. Liu YH, Lu M, Xie ZZ, Hua F, Xie L, Gao JH, Koh YH, Bian JS (2014) Hydrogen sulfide prevents heart failure development via inhibition of renin release from mast cells in isoproterenol-treated rats. Antioxid Redox Signal 20:759–769

    Article  CAS  PubMed  Google Scholar 

  45. Martinon F, Tschopp J (2004) Inflammatory caspases: linking an intracellular innate immune system to autoinflammatory diseases. Cell 117:561–574

    Article  CAS  PubMed  Google Scholar 

  46. Miyata M, Hatsushika K, Ando T, Shimokawa N, Ohnuma Y, Katoh R, Suto H, Ogawa H, Masuyama K, Nakao A (2008) Mast cell regulation of epithelial TSLP expression plays an important role in the development of allergic rhinitis. Eur J Immunol 38:1487–1492

    Article  CAS  PubMed  Google Scholar 

  47. Mizutani N, Sae-Wong C, Kangsanant S, Nabe T, Yoshino S (2015) Thymic stromal lymphopoietin-induced interleukin-17A is involved in the development of IgE-mediated atopic dermatitis-like skin lesions in mice. Immunology. doi:10.1111/imm.12528

    PubMed Central  Google Scholar 

  48. Mogensen TH (2009) Pathogen recognition and inflammatory signaling in innate immune defenses. Clin Microbiol Rev 22:240–273

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  49. Moon PD, Kim HM (2011) Thymic stromal lymphopoietin is expressed and produced by caspase-1/NF-κB pathway in mast cells. Cytokine 54:239–243

    Article  CAS  PubMed  Google Scholar 

  50. Mou Z, Xia J, Tan Y, Wang X, Zhang Y, Zhou B, Li H, Han D (2009) Overexpression of thymic stromal lymphopoietin in allergic rhinitis. Acta Otolaryngol 129:297–301

    Article  CAS  PubMed  Google Scholar 

  51. Muto T, Fukuoka A, Kabashima K, Ziegler SF, Nakanishi K, Matsushita K, Yoshimoto T (2014) The role of basophils and proallergic cytokines, TSLP and IL-33, in cutaneously sensitized food allergy. Int Immunol 26:539–549

    Article  CAS  PubMed  Google Scholar 

  52. Navas TA, Baldwin DT, Stewart TA (1999) RIP2 is a Raf1-activated mitogen-activated protein kinase kinase. J Biol Chem 274:33684–333690

    Article  CAS  PubMed  Google Scholar 

  53. Neal B (2014) Dietary salt is a public health hazard that requires vigorous attack. Can J Cardiol 30:502–506

    Article  PubMed  Google Scholar 

  54. Oeckinghaus A, Ghosh S (2009) The NF-kappaB family of transcription factors and its regulation. Cold Spring Harb Perspect Biol 1:a000034

    Article  PubMed Central  PubMed  Google Scholar 

  55. Oh HA, Seo JY, Jeong HJ, Kim HM (2013) Ginsenoside Rg1 inhibits the TSLP production in allergic rhinitis mice. Immunopharmacol Immunotoxicol 35:678–686

    Article  CAS  PubMed  Google Scholar 

  56. Parcell S (2002) Sulfur in human nutrition and applications in medicine. Altern Med Rev 7:22–44

    PubMed  Google Scholar 

  57. Prasad AS (2009) Zinc: role in immunity, oxidative stress and chronic inflammation. Curr Opin Clin Nutr Metab Care 12:646–652

    Article  CAS  PubMed  Google Scholar 

  58. Redhu NS, Saleh A, Halayko AJ, Ali AS, Gounni AS (2011) Essential role of NF-κB and AP-1 transcription factors in TNF-α-induced TSLP expression in human airway smooth muscle cells. Am J Physiol Lung Cell Mol Physiol 300:L479–L485

    Article  CAS  PubMed  Google Scholar 

  59. Roan F, Bell BD, Stoklasek TA, Kitajima M, Han H, Ziegler SF (2012) The multiple facets of thymic stromal lymphopoietin (TSLP) during allergic inflammation and beyond. J Leukoc Biol 91:877–886

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  60. Ruefli-Brasse AA, Lee WP, Hurst S, Dixit VM (2004) Rip2 participates in Bcl10 signaling and T-cell receptor-mediated NF-kappaB activation. J Biol Chem 279:1570–1574

    Article  CAS  PubMed  Google Scholar 

  61. Sarkar A, Duncan M, Hart J, Hertlein E, Guttridge DC, Wewers MD (2006) ASC directs NF-kappaB activation by regulating receptor interacting protein-2 (RIP2) caspase-1 interactions. J Immunol 176:4979–4986

    Article  CAS  PubMed  Google Scholar 

  62. Shin JH, Park HR, Kim SW, Park CS, Cho JH, Park YJ, Kim SW (2012) The effect of topical FK506 (tacrolimus) in a mouse model of allergic rhinitis. Am J Rhinol Allergy 26:e71–e75

    Article  PubMed  Google Scholar 

  63. Singhal P, Bal LM, Satya S, Sudhakar P, Naik SN (2013) Bamboo shoots: a novel source of nutrition and medicine. Crit Rev Food Sci Nutr 53:517–534

    Article  PubMed  Google Scholar 

  64. Staal J, Bekaert T, Beyaert R (2011) Regulation of NF-κB signaling by caspases and MALT1 paracaspase. Cell Res 21:40–54

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  65. Sundström M, Vliagoftis H, Karlberg P, Butterfield JH, Nilsson K, Metcalfe DD, Nilsson G (2003) Functional and phenotypic studies of two variants of a human mast cell line with a distinct set of mutations in the c-kit proto-oncogene. Immunology 108:89–97

    Article  PubMed Central  PubMed  Google Scholar 

  66. Suzuki R, Leach S, Liu W, Ralston E, Scheffel J, Zhang W, Lowell CA, Rivera J (2014) Molecular editing of cellular responses by the high-affinity receptor for IgE. Science 343:1021–1025

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  67. Tornatore L, Thotakura AK, Bennett J, Moretti M, Franzoso G (2012) The nuclear factor kappa B signaling pathway: integrating metabolism with inflammation. Trends Cell Biol 22:557–566

    Article  CAS  PubMed  Google Scholar 

  68. Verhoog NJ, Du Toit A, Avenant C, Hapgood JP (2011) Glucocorticoid-independent repression of tumor necrosis factor (TNF) alpha-stimulated interleukin (IL)-6 expression by the glucocorticoid receptor: a potential mechanism for protection against an excessive inflammatory response. J Biol Chem 286:19297–19310

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  69. Wang G, Bowman BA (2013) Recent economic evaluations of interventions to prevent cardiovascular disease by reducing sodium intake. Curr Atheroscler Rep 15:349

    Article  PubMed Central  PubMed  Google Scholar 

  70. Wang R (2012) Physiological implications of hydrogen sulfide: a whiff exploration that blossomed. Physiol Rev 92:791–896

    Article  CAS  PubMed  Google Scholar 

  71. Wang W, Soltero L, Zhang P, Huang XR, Lan HY, Adrogue HJ (2007) Renal inflammation is modulated by potassium in chronic kidney disease: possible role of Smad7. Am J Physiol Renal Physiol 293:F1123–F1130

    Article  CAS  PubMed  Google Scholar 

  72. Wedi B, Elsner J, Czech W, Butterfield JH, Kapp A (1996) Modulation of intercellular adhesion molecule 1 (ICAM-1) expression on the human mast-cell line (HMC)-1 by inflammatory mediators. Allergy 51:676–684

    Article  CAS  PubMed  Google Scholar 

  73. Xu S, Liu Z, Liu P (2014) Targeting hydrogen sulfide as a promising therapeutic strategy for atherosclerosis. Int J Cardiol 172:313–317

    Article  PubMed  Google Scholar 

  74. Zhang G, Wang P, Yang G, Cao Q, Wang R (2013) The inhibitory role of hydrogen sulfide in airway hyperresponsiveness and inflammation in a mouse model of asthma. Am J Pathol 182:1188–1195

    Article  CAS  PubMed  Google Scholar 

  75. Zhao X, Deng X, Park KY, Qiu L, Pang L (2013) Purple bamboo salt has anticancer activity in TCA8113 cells in vitro and preventive effects on buccal mucosa cancer in mice in vivo. Exp Ther Med 5:549–554

    PubMed Central  PubMed  Google Scholar 

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Acknowledgments

This work was supported by Grant PJT200599 to Solar Salt Research Center from Ministry of Oceans and Fisheries of Korea.

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    1. Department of Pharmacology, College of Korean Medicine, Kyung Hee University, 1 Hoegi-dong, Dongdaemun-gu, Seoul, 130-701, Republic of Korea

      Na-Ra Han, Phil-Dong Moon & Hyung-Min Kim

    2. Department of Food Technology and Biochip Research Center, Hoseo University, 165, Sechul-ri, Asan, Chungnam, 336-795, Republic of Korea

      Hyun-Ja Jeong

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    H.-J. Jeong and H.-M. Kim contributed equally to this work.

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    Han, NR., Moon, PD., Jeong, HJ. et al. Hydrogen sulfide diminishes the levels of thymic stromal lymphopoietin in activated mast cells. Arch Dermatol Res 308, 103–113 (2016). https://doi.org/10.1007/s00403-016-1619-x

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