Advertisement

In vitro anti-inflammatory effects of curcumin on mast cell-mediated allergic responses via inhibiting FcεRI protein expression and protein kinase C delta translocation

  • Zwe-Ling KongEmail author
  • Sabri Sudirman
  • Huey-Jun Lin
  • Wei-Ning Chen
Original Article

Abstract

Allergy is a hypersensitivity reaction when exposed to certain environmental substances. It shows high relation between immunoglobulin E (IgE) binding to a specific receptor (FcεRI), pro-inflammatory cytokines, and mediators with allergic inflammation responses. Curcumin is a yellow pigment isolated from the turmeric. Curcumin possesses antioxidant and anti-inflammatory properties as well as exhibits significant chemopreventive activity. This study was aimed to investigate the in vitro assessment of the regulation of curcumin on allergic inflammatory responses on rat basophil leukemia (RBL)-2H3 and human pre-basophils (KU812) cell lines. Curcumin showed the activity against histamine and β-hexosaminidase releases from both IgE-mediated and A23187-induced cells degranulation. The morphological observation also confirmed that curcumin inhibits cells degranulation. IgE-mediated allergic responses and significantly induced mast cells intracellular reactive oxygen species (ROS) production. Curcumin reduced ROS production from IgE-mediated or A23187-induced cells degranulation. Curcumin also successfully reduced FcεRI expressions and some pro-inflammatory cytokines, such as interleukin (IL)-4 and IL-13. Furthermore, curcumin inhibited protein kinase C (PKC)-δ translocation from cytosolic to particulate. These results suggested that curcumin can alleviate both the IgE-mediated and calcium ionosphere A23187-stimulated allergic responses through reducing the release of the allergic mediators.

Keywords

Allergic responses Curcumin Degranulation Immunoglobulin E Protein kinase C 

Notes

Author contributions

Z-LK conceived and designed the experiments. H-JL and W-NC performed analyses. H-JL and SS wrote the manuscript.

Funding

This research received no external funding.

Compliance with ethical standards

Conflicts of interest

The authors declare that they have no conflict of interest.

References

  1. Ak T, Gülçin İ (2008) Antioxidant and radical scavenging properties of curcumin. Chem Biol Interact 174:27–37.  https://doi.org/10.1016/j.cbi.2008.05.003 CrossRefPubMedGoogle Scholar
  2. Akizawa Y (2003) Regulation of human FcepsilonRI beta chain gene expression by Oct-1. Int Immunol 15:549–556.  https://doi.org/10.1093/intimm/dxg055 CrossRefPubMedGoogle Scholar
  3. Bao K, Reinhardt RL (2015) The differential expression of IL-4 and IL-13 and its impact on type-2 immunity. Cytokine 75:25–37.  https://doi.org/10.1016/j.cyto.2015.05.008 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Basnet P, Skalko-Basnet N (2011) Curcumin: an anti-inflammatory molecule from a curry spice on the path to cancer treatment. Molecules 16:4567–4598.  https://doi.org/10.3390/molecules16064567 CrossRefPubMedPubMedCentralGoogle Scholar
  5. Bohn A, König W (1982) Generation of monoclonal murine anti-DNP-IgE, IgM and IgG1 antibodies: biochemical and biological characterization. Immunology 47:297–311PubMedPubMedCentralGoogle Scholar
  6. Bohn A, König W (1985) Monoclonal murine anti-DNP IgE:in vitro histamine release of rat mast cells in the presence of reaginic rat and mouse sera. Agents Actions 16:485–490.  https://doi.org/10.1007/bf01983651 CrossRefPubMedGoogle Scholar
  7. Broide DH (2001) Molecular and cellular mechanisms of allergic disease. J Allergy Clin Immunol 108:S65–S71.  https://doi.org/10.1067/mai.2001.116436 CrossRefPubMedGoogle Scholar
  8. Buhrmann C, Mobasheri A, Busch F, Aldinger C, Stahlmann R, Montaseri A, Shakibaei M (2011) Curcumin modulates nuclear factor κB (NF-κB)-mediated inflammation in human tenocytesin vitro. J Biol Chem 286:28556–28566.  https://doi.org/10.1074/jbc.M111.256180 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Chainani-Wu N (2003) Safety and anti-inflammatory activity of curcumin: a component of tumeric (Curcuma longa). J Altern Complement Med 9:161–168.  https://doi.org/10.1089/107555303321223035 CrossRefPubMedGoogle Scholar
  10. Chen X-J, Lycke N, Enerback L (2001) Surface and gene expression of immunoglobulin E receptors on mast cells and mast-cell numbers in interleukin-4-gene knockout mice. Immunology 96:544–550.  https://doi.org/10.1046/j.1365-2567.1999.00727.x CrossRefGoogle Scholar
  11. Chen H-J, Shih C-K, Hsu H-Y, Chiang W (2010) Mast cell-dependent allergic responses are inhibited by ethanolic extract of adlay (Coix lachryma-jobi L. var.ma-yuen Stapf) testa. J Agric Food Chem 58:2596–2601.  https://doi.org/10.1021/jf904356q CrossRefPubMedGoogle Scholar
  12. Cho SH, You HJ, Woo CH, Yoo YJ, Kim JH (2004) Rac and protein kinase C-regulate ERKs and cytosolic phospholipase A2 in Fc RI signaling to cysteinyl leukotriene synthesis in mast cells. J Immunol 173:624–631.  https://doi.org/10.4049/jimmunol.173.1.624 CrossRefPubMedGoogle Scholar
  13. Choi Y, Kim MS, Hwang JK (2012) Inhibitory effects of panduratin A on allergy-related mediator production in rat basophilic leukemia mast cells. Inflammation 35:1904–1915.  https://doi.org/10.1007/s10753-012-9513-y CrossRefPubMedGoogle Scholar
  14. Choi YH, Jin GY, Lc Li, Yan GH (2013) Inhibition of protein kinase C delta attenuates allergic airway inflammation through suppression of PI3K/Akt/mTOR/HIF-1 alpha/VEGF pathway. PLoS ONE.  https://doi.org/10.1371/journal.pone.0081773 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Chong L et al (2014) Protective effect of curcumin on acute airway inflammation of allergic asthma in mice through Notch1–GATA3 signaling pathway. Inflammation 37:1476–1485.  https://doi.org/10.1007/s10753-014-9873-6 CrossRefPubMedPubMedCentralGoogle Scholar
  16. Claramunt RM, Bouissane L, Cabildo MP, Cornago MP, Elguero J, Radziwon A, Medina C (2009) Synthesis and biological evaluation of curcuminoid pyrazoles as new therapeutic agents in inflammatory bowel disease: effect on matrix metalloproteinases. Bioorg Med Chem 17:1290–1296.  https://doi.org/10.1016/j.bmc.2008.12.029 CrossRefPubMedGoogle Scholar
  17. Das J, Ramani R, Suraju MO (2016) Polyphenol compounds and PKC signaling. Biochimica et Biophysica Acta Gen Subj 1860:2107–2121.  https://doi.org/10.1016/j.bbagen.2016.06.022 CrossRefGoogle Scholar
  18. Feldmesser M, Alphonse MP, Saffar AS, Shan L, HayGlass KT, Simons FER, Gounni AS (2008) Regulation of the high affinity IgE receptor (FcεRI) in human neutrophils: role of seasonal allergen exposure and Th-2 cytokines. PLoS ONE.  https://doi.org/10.1371/journal.pone.0001921 CrossRefGoogle Scholar
  19. Galli SJ, Tsai M, Piliponsky AM (2008) The development of allergic inflammation. Nature 454:445–454.  https://doi.org/10.1038/nature07204 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Gazave E et al (2009) Origin and evolution of the Notch signalling pathway: an overview from eukaryotic genomes. BMC Evol Biol.  https://doi.org/10.1186/1471-2148-9-249 CrossRefPubMedPubMedCentralGoogle Scholar
  21. Gupta S et al (2011) Fluctuations in total antioxidant capacity, catalase activity and hydrogen peroxide levels of follicular fluid during bovine folliculogenesis. Reprod Fertil Dev.  https://doi.org/10.1071/rd10270 CrossRefPubMedPubMedCentralGoogle Scholar
  22. Gupta SC, Patchva S, Aggarwal BB (2012) Therapeutic roles of curcumin: lessons learned from clinical trials. AAPS J 15:195–218.  https://doi.org/10.1208/s12248-012-9432-8 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Hara T, Yamada K, Tachibana H (1998) Basophilic differentiation of the human leukemia cell line KU812 upon treatment with interleukin-4. Biochem Biophys Res Commun 247:542–548.  https://doi.org/10.1006/bbrc.1998.8816 CrossRefPubMedGoogle Scholar
  24. Hatcher H, Planalp R, Cho J, Torti FM, Torti SV (2008) Curcumin: from ancient medicine to current clinical trials. Cell Mol Life Sci 65:1631–1652.  https://doi.org/10.1007/s00018-008-7452-4 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Hong S, Son DK, Lim WR, Kim SH, Kim H, Yum HY, Kwon H (2012) The prevalence of atopic dermatitis, asthma, and allergic rhinitis and the comorbidity of allergic diseases in children. Environ Health Toxicol.  https://doi.org/10.5620/eht.2012.27.e2012006 CrossRefPubMedPubMedCentralGoogle Scholar
  26. Hosoki K, Gandhe R, Boldogh I, Sur S (2014) Reactive oxygen species (ROS) and allergic responses. In: Systems biology of free radicals and antioxidants, pp 3239–3266.  https://doi.org/10.1007/978-3-642-30018-9_145 CrossRefGoogle Scholar
  27. Inoue T, Suzuki Y, Yoshimaru T, Ra C (2008) Reactive oxygen species produced up- or downstream of calcium influx regulate proinflammatory mediator release from mast cells: role of NADPH oxidase and mitochondria. Biochim Biophys Acta 1783:789–802.  https://doi.org/10.1016/j.bbamcr.2007.12.004 CrossRefPubMedGoogle Scholar
  28. Juckmeta T, Thongdeeying P, Itharat A (2014) Inhibitory effect on β-hexosaminidase release from RBL-2H3 cells of extracts and some pure constituents of benchalokawichian, a Thai herbal remedy used for allergic disorders. Evid Based Complement Alternat Med 2014:1–8.  https://doi.org/10.1155/2014/828760 CrossRefGoogle Scholar
  29. Kao N-J, Hu J-Y, Wu C-S, Kong Z-L (2016) Curcumin represses the activity of inhibitor-κB kinase in dextran sulfate sodium-induced colitis by S-nitrosylation. Int Immunopharmacol 38:1–7.  https://doi.org/10.1016/j.intimp.2016.05.015 CrossRefPubMedGoogle Scholar
  30. Kim CJ et al (2002) Histamine release by hydrochloric acid is mediated via reactive oxygen species generation and phospholipase D in RBL-2H3 mast cells. Arch Pharmacal Res 25:675–680.  https://doi.org/10.1007/bf02976943 CrossRefGoogle Scholar
  31. Kobayashi S, Tanabe S (2006) Evaluation of the anti-allergic activity of Citrus unshiu using rat basophilic leukemia RBL-2H3 cells as well as basophils of patients with seasonal allergic rhinitis to pollen. Int J Mol Med.  https://doi.org/10.3892/ijmm.17.3.511 CrossRefPubMedGoogle Scholar
  32. Kurup VP, Barrios CS (2008) Immunomodulatory effects of curcumin in allergy. Mol Nutr Food Res 52:1031–1039.  https://doi.org/10.1002/mnfr.200700293 CrossRefPubMedGoogle Scholar
  33. Lee JH et al (2008) Curcumin, a constituent of curry, suppresses IgE-mediated allergic response and mast cell activation at the level of Syk. J Allergy Clin Immunol 121:1225–1231.  https://doi.org/10.1016/j.jaci.2007.12.1160 CrossRefPubMedGoogle Scholar
  34. Liao E-C, Chang C-Y, Hsieh C-W, Yu S-J, Yin S-C, Tsai J-J (2015) An exploratory pilot study of genetic marker for IgE-mediated allergic diseases with expressions of FcεR1α and Cε. Int J Mol Sci 16:9504–9519.  https://doi.org/10.3390/ijms16059504 CrossRefPubMedPubMedCentralGoogle Scholar
  35. Lora JM et al (2003) FcεRI-dependent gene expression in human mast cells is differentially controlled by T helper type 2 cytokines. J Allergy Clin Immunol 112:1119–1126.  https://doi.org/10.1016/j.jaci.2003.08.042 CrossRefPubMedGoogle Scholar
  36. Lowry OH, Rosenbrough NJ, Farr A, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275PubMedPubMedCentralGoogle Scholar
  37. Lu ZG, Liu H, Yamaguchi T, Miki Y, Yoshida K (2009) Protein kinase C activates RelA/p65 and nuclear factor-B signaling in response to tumor necrosis factor. Cancer Res 69:5927–5935.  https://doi.org/10.1158/0008-5472.Can-08-4786 CrossRefPubMedGoogle Scholar
  38. Majhi A, Rahman GM, Panchal S, Das J (2010) Binding of curcumin and its long chain derivatives to the activator binding domain of novel protein kinase C. Bioorg Med Chem 18:1591–1598.  https://doi.org/10.1016/j.bmc.2009.12.075 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Matsuda H, Tewtrakul S, Morikawa T, Nakamura A, Yoshikawa M (2004) Anti-allergic principles from Thai zedoary: structural requirements of curcuminoids for inhibition of degranulation and effect on the release of TNF-α and IL-4 in RBL-2H3 cells. Bioorg Med Chem 12:5891–5898.  https://doi.org/10.1016/j.bmc.2004.08.027 CrossRefPubMedGoogle Scholar
  40. Matsui T et al (2000) Diphenyleneiodonium prevents reactive oxygen species generation, tyrosine phosphorylation, and histamine release in RBL-2H3 mast cells. Biochem Biophys Res Commun 276:742–748.  https://doi.org/10.1006/bbrc.2000.3545 CrossRefPubMedGoogle Scholar
  41. Menon VP, Sudheer AR (2007) Antioxidant and anti-inflammatory properties of curcumin. In: The molecular targets and therapeutic uses of curcumin in health and disease. Advances in experimental medicine and biology, pp 105–125.  https://doi.org/10.1007/978-0-387-46401-5_3
  42. Metzger H, Alcaraz G, Hohman R, Kinet JP, Pribluda V, Quarto R (1986) The receptor with high affinity for immunoglobulin E. Annu Rev Immunol 4:419–470.  https://doi.org/10.1146/annurev.iy.04.040186.002223 CrossRefPubMedGoogle Scholar
  43. Nugroho AE, Sardjiman S, Maeyama K (2010) Comparison of cytotoxic and antiproliferative effects of benzylidenecyclopentanone analogues of curcumin on RBL-2H3 Cells. Indones J Biotechnol 15:64–71.  https://doi.org/10.22146/ijbiotech.7822 CrossRefGoogle Scholar
  44. Ozawa K, Yamada K, Kazanietz MG, Blumberg PM, Beaven MA (1993) Different isozymes of protein kinase C mediate feedback inhibition of phospholipase C and stimulatory signals for exocytosis in rat RBL-2H3 cells. J Biol Chem 268:2280–2283PubMedGoogle Scholar
  45. Pan M-H, Huang T-M, Lin J-K (1999) Biotransformation of curcumin through reduction and glucuronidation in mice. Drug Metab Dispos 27:486–494PubMedGoogle Scholar
  46. Pan M-H, Chen J-W, Kong Z-L, Wu J-C, Ho C-T, Lai C-S (2018) Attenuation by tetrahydrocurcumin of adiposity and hepatic steatosis in mice with high-fat-diet-induced obesity. J Agric Food Chem 66:12685–12695.  https://doi.org/10.1021/acs.jafc.8b04624 CrossRefPubMedGoogle Scholar
  47. Qu J, Li Y, Zhong W, Gao P, Hu C (2017) Recent developments in the role of reactive oxygen species in allergic asthma. J Thorac Dis 9:E32–E43.  https://doi.org/10.21037/jtd.2017.01.05 CrossRefPubMedPubMedCentralGoogle Scholar
  48. Ren J et al (2014) Protein kinase C-δ (PKCδ) regulates proinflammatory chemokine expression through cytosolic interaction with the NF-κB subunit p65 in vascular smooth muscle cells. J Biol Chem 289:9013–9026.  https://doi.org/10.1074/jbc.M113.515957 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Rivera J, Gilfillan A (2006) Molecular regulation of mast cell activation. J Allergy Clin Immunol 117:1214–1225.  https://doi.org/10.1016/j.jaci.2006.04.015 CrossRefPubMedGoogle Scholar
  50. Rosenwasser LJ (2011) Mechanisms of IgE inflammation. Curr Allergy Asthma Rep 11:178–183.  https://doi.org/10.1007/s11882-011-0179-6 CrossRefPubMedGoogle Scholar
  51. Shim S-Y et al (2002) Construction of an in vitro allergy reaction evaluation system using human leukemia cell lines. Cytotechnology 40:75–83.  https://doi.org/10.1023/a:1023918206060 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Shim J-U, Oh P-S, Lim K-T (2009) Anti-inflammatory activity of ethanol extract from Geranium sibiricum Linne. J Ethnopharmacol 126:90–95.  https://doi.org/10.1016/j.jep.2009.08.004 CrossRefPubMedGoogle Scholar
  53. Soudamini KK, Kuttan R (1989) Inhibition of chemical carcinogenesis by curcumin. J Ethnopharmacol 27:227–233.  https://doi.org/10.1016/0378-8741(89)90094-9 CrossRefPubMedGoogle Scholar
  54. Suzuki Y, Yoshimaru T, Matsui T, Inoue T, Niide O, Nunomura S, Ra C (2003) Fc RI signaling of mast cells activates intracellular production of hydrogen peroxide: role in the regulation of calcium signals. J Immunol 171:6119–6127.  https://doi.org/10.4049/jimmunol.171.11.6119 CrossRefPubMedGoogle Scholar
  55. Swindle EJ, Metcalfe DD (2007) The role of reactive oxygen species and nitric oxide in mast cell-dependent inflammatory processes. Immunol Rev 217:186–205.  https://doi.org/10.1111/j.1600-065X.2007.00513.x CrossRefPubMedGoogle Scholar
  56. Tagen M, Elorza A, Kempuraj D, Boucher W, Kepley CL, Shirihai OS, Theoharides TC (2009) Mitochondrial uncoupling protein 2 inhibits mast cell activation and reduces histamine content. J Immunol 183:6313–6319.  https://doi.org/10.4049/jimmunol.0803422 CrossRefPubMedPubMedCentralGoogle Scholar
  57. Takahashi K, Ra C (2005) The high affinity IgE receptor (FcεRI) as a target for anti-allergic agents. Allergol Int 54:1–5.  https://doi.org/10.2332/allergolint.54.1 CrossRefGoogle Scholar
  58. Tang J-M, Liu J, Wu W (2012) Studies on the degranulation of RBL-2H3 cells induced by traditional Chinese medicine injections. Chin Med 03:200–208.  https://doi.org/10.4236/cm.2012.34029 CrossRefGoogle Scholar
  59. van Rijt L, Utsch L, Lutter R, van Ree R (2017) Oxidative stress: promoter of allergic sensitization to protease allergens? Int J Mol Sci.  https://doi.org/10.3390/ijms18061112 CrossRefPubMedPubMedCentralGoogle Scholar
  60. Vercelli D, Gozdz J, von Mutius E (2014) Innate lymphoid cells in asthma. Curr Opin Allergy Clin Immunol 14:29–34.  https://doi.org/10.1097/aci.0000000000000023 CrossRefPubMedGoogle Scholar
  61. Wang Y-J, Pan M-H, Cheng A-L, Lin L-I, Ho Y-S, Hsieh C-Y, Lin J-K (1997) Stability of curcumin in buffer solutions and characterization of its degradation products. J Pharm Biomed Anal 15:1867–1876.  https://doi.org/10.1016/s0731-7085(96)02024-9 CrossRefPubMedGoogle Scholar
  62. Wills-Karp M, Luyimbazi J, Xu X, Schofield B, Neben TY, Karp CL, Donaldson DD (1998) Interleukin-13: central mediator of allergic asthma. Science 282:2258–2261.  https://doi.org/10.1126/science.282.5397.2258 CrossRefPubMedGoogle Scholar
  63. Zhao ZZ, Sugerman PB, Walsh LJ, Savage NW (2001) A fluorometric microassay for histamine release from human gingival mast cells. J Periodontal Res 36:233–236.  https://doi.org/10.1034/j.1600-0765.2001.036004233.x CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Department of Food ScienceNational Taiwan Ocean UniversityKeelung CityTaiwan

Personalised recommendations