DOI QR코드

DOI QR Code

Anti-Inflammatory Effects of Bee Venom on Phthalic Anhydride-Induced Atopic Dermatitis

  • Oh, Myung Jin (Department of Acupuncture and Moxibustion Medicine, College of Korean Medicine, Gachon University) ;
  • Song, Ho-Sueb (Department of Acupuncture and Moxibustion Medicine, College of Korean Medicine, Gachon University)
  • 투고 : 2019.03.21
  • 심사 : 2019.06.14
  • 발행 : 2020.02.28

초록

Background: Atopic dermatitis (AD) is a chronic inflammatory condition which can be studied using phthalic anhydride (PA) to induce AD. Anti-inflammatory properties of bee venom (BV) wereinvestigated to determine whether it may be a useful treatment for AD. Methods: AD was induced by applying to pical PA to 8-week-old HR-1 mice (N = 50), then treating with (0.1, 0.25, and 0.5 ㎍) or without topical BV. Body weight, ear thickness histology, enzyme-linked immune sorbent assay (serum IgE concentrations), Western blot analysis [inducible nitric oxide synthase, cyclooxygenase-2, IκB-α, phospho-IκB-α, c-Jun N-terminal kinase (JNK), phospho-JNK, p38, phospho-p38, extra cellular signal-regulated kinase (ERK), and phospho-ERK], and the pull down assay for immunoblotting (p50), were used to measure inflammatory mediators. Results: PA + BV (0.1, 0.25, and 0.5 ㎍) significantly decreased ear thickness without altering body weight. IgE concentrations decreased in the PA + BV (0.5 ㎍)-treated groups compared with PAtreatment. Tumor necrosis factor-α, interleukin-1β, inducible nitric oxide synthase, cyclooxygenase-2, phospho-IκB-α, phospho-JNK, p38, phospho-p38, and phospho-ERK, all decreased following treatment with PA + BV compared with the PA-treatment alone. p50 was upregulated in the PA + BV-treated groups compared with the PA-treated group. Furthermore, the number of mast cells decreased in the PA + BV-treated groups compared with the PA-treated group. Epidermal thickness was significantly lower in the PA + BV-treated group compared with PA treatment alone. Conclusion: BV maybe a useful anti-inflammatory treatment for AD.

키워드

참고문헌

  1. Leung DYM, Bieber T. Atopic dermatitis. Lancet 2003;361:151-160. https://doi.org/10.1016/S0140-6736(03)12193-9
  2. Sehra S, Krishnamurthy P, Koh B, Zhou HM, Seymour L, Akhtar N et al. Increased Th2 activity and diminished skin barrier function cooperate in allergic skin inflammation. Eur J Immunol 2016;46:2609-2613. https://doi.org/10.1002/eji.201646421
  3. Lee DY, Hwang CJ, Choi JY, Park MH, Song MJ, Oh KW et al. Inhibitory effect of carnosol on phthalic anhydride-induced atopic dermatitis via inhibition of STAT3. Biomol Ther 2017;25:535-544. https://doi.org/10.4062/biomolther.2017.006
  4. Thomsen SF. Atopic dermatitis: natural history, diagnosis, and treatment. ISRN Allergy 2014;2014:354250. https://doi.org/10.1155/2014/354250
  5. Williams HC. Atopic dermatitis. N Engl J Med 2005;352:2314-2324. https://doi.org/10.1056/NEJMcp042803
  6. Saeki H, Furue M, Furukawa F, Hide M, Ohtsuki M, Katayama I et al. Guidelines for management of atopic dermatitis. J Dermatol 2009;36:563-577. https://doi.org/10.1111/j.1346-8138.2009.00706.x
  7. Katayama I, Aihara M, Ohya Y, Saeki H, Shimojo N, Shoji S et al. Japanese guidelines for atopic dermatitis 2017. Allergol Int 2017;66:230-247. https://doi.org/10.1016/j.alit.2016.12.003
  8. Sidbury R, Hanifin JM. Systemic therapy of atopic dermatitis. Clin Exp Dermatol 2000;25:559-566. https://doi.org/10.1046/j.1365-2230.2000.00697.x
  9. Kirchhof MG, Landells I, Lynde CW, Gooderham MJ, Hong CH. Approach to the assessment and management of adult patients with atopic dermatitis: aconsensus document. Section I: Pathophysiology of atopic dermatitis and implications for systemic therapy. J Cutan Med Surg 2018;22:6S-9S. https://doi.org/10.1177/1203475418803626
  10. Cabanillas B, Brehler AC, Novak N. Atopic dermatitis phenotypes and the need for personalized medicine. Curr Opin Allergy Clin Immunol 2017;17:309-315. https://doi.org/10.1097/ACI.0000000000000376
  11. Kempuraj D, Castellani ML, Petrarca C, Frydas S, Conti P, Theoharides TC et al. Inhibitory effect of quercetin on tryptase and interleukin-6 release, and histidine decarboxylase mRNA transcription by human mast cell-1 cell line. Clin Exp Med 2006;6:150-156. https://doi.org/10.1007/s10238-006-0114-7
  12. Leung DYM, Boguniewicz M, Howell MD, Nomura I, Hamid QA. New insights into atopic dermatitis. J Clin Invest 2004;113:651-657. https://doi.org/10.1172/JCI21060
  13. Kee JY, Jeon YD, Kim DS, Han YH, Park J, Youn DH et al. Korean red ginseng improves atopic dermatitis-like skin lesions by suppressing expression of proinflammatory cytokines and chemokines in vivo and in vitro. J Ginseng Res 2017;41:134-143. https://doi.org/10.1016/j.jgr.2016.02.003
  14. Lim HS, Kim YJ, Seo CS, Yoo SR, Jin SE, Shin HK et al. Chungsimyeonjaeum inhibits inflammatory responses in RAW 264.7 macrophages and HaCaT keratinocytes. BMC Complement Altern Med 2015;15:371. https://doi.org/10.1186/s12906-015-0902-2
  15. Seo WY, Youn GS, Choi SY, Park J. Butein, a tetrahydroxychalcone, suppresses pro-inflammatory responses in HaCaT keratinocytes. BMB Rep 2015;48:495-500. https://doi.org/10.5483/BMBRep.2015.48.9.259
  16. Yang JH, Hwang YH, Gu MJ, Cho WK, Ma JY. Ethanol extracts of Sanguisorba officinalis L. suppress TNF-alpha/IFN-gamma-induced proinflammatory chemokine production in HaCaT cells. Phytomedicine 2015;22:1262-1268. https://doi.org/10.1016/j.phymed.2015.09.006
  17. Kasraie S, Werfel T. Role of macrophages in the pathogenesis of atopic dermatitis. Mediators Inflamm 2013;2013:942375.
  18. Bogdanov S [Internet]. Bee venom: composition, health, medicine: areview. Swiss: Bee Product Science. [cited 11 Apr 2016]. Available from: http://www.bee-hexagon.net/files/file/fileE/Health/VenomBookReview.pdf.
  19. Kwon YB, Yoon SY, Kim HW, Roh DH, Kang SY, Ryu YH et al. Substantial role of locus coeruleus-noradrenergic activation and capsaicin-insensitive primary afferent fibers in bee venom's anti-inflammatory effect. Neurosci Res 2006;55:197-203. https://doi.org/10.1016/j.neures.2006.03.003
  20. Nam KW, Je KH, Lee JH, Han HJ, Lee HJ, Kang SK et al. Inhibition of COX-2 activity and proinflammatory cytokines ($TNF-{\alpha}$ and IL-$1{\beta}$) production by water-soluble sub-fractionated parts from bee (Apis mellifera) venom. Arch Pharm Res 2003;26:383-388. https://doi.org/10.1007/BF02976695
  21. Lee KG, Cho HJ, Bae YS, Park KK, Choe JY, Chung IK et al. Bee venom suppresses LPS-mediated NO/iNOS induction through inhibition of PKCalpha expression. J Ethnopharmacol 2009;123:15-21. https://doi.org/10.1016/j.jep.2009.02.044
  22. Kim SJ, Park JH, Kim KH, Lee WR, Chang YC, Park KK et al. Bee venom inhibits hepatic fibrosis through suppression of pro-fibrogenic cytokine expression. Am J Chin Med 2010;38:921-935. https://doi.org/10.1142/S0192415X10008354
  23. Yoon SY, Kwon YB, Kim HW, Roh DH, Seo HS, Han HJ et al. Peripheral bee venom's anti-inflammatory effect involves activation of the coeruleospinal pathway and sympathetic preganglionic neurons. Neurosci Res 2007;59:51-59. https://doi.org/10.1016/j.neures.2007.05.008
  24. Weidinger S, Novak N. Atopic dermatitis. Lancet 2016;387:1109-1122. https://doi.org/10.1016/S0140-6736(15)00149-X
  25. Egawa G, Kabashima, K. Multifactorial skin barrier deficiency and atopic dermatitis: Essential topics to prevent the atopic march. J Allergy Clin Immunol 2016;138:350-358. https://doi.org/10.1016/j.jaci.2016.06.002
  26. Dearman RJ, Kimber I. Divergent immune response to respiratory and contact chemical allergens: antibody elicited by phthalic anhydride and oxazolone. Clin Exp Allergy 1992;22:241-250. https://doi.org/10.1111/j.1365-2222.1992.tb03079.x
  27. Towae FK, Enke W, Jackh R, Bhargava N. Phthalic acid and derivatives. In: Elvers B, Hawkins S, Schulz G, eds, Ullmann's Encyclopedia of Industrial Chemistry, Vol. A20, 5th rev. ed. New York (NY): VCH Publishers; 1992. p. 181-211.
  28. Keren RA. Asthma and allergic rhinitis due to sensitization to phthalic anhydride. J Allergy 1939;10:164-165. https://doi.org/10.1016/S0021-8707(39)90050-X
  29. Venables KM. Low molecular weight chemicals, hypersensitivity and direct toxicity: acid anhydrides. Br J Ind Med 1989;46:222-232.
  30. Ban M, Hettich D. Effect of Th2 cytokine antagonist treatments on chemical-induced allergic response in mice. J Appl Toxicol 2005;25:239-247. https://doi.org/10.1002/jat.1062
  31. Bae CJ, Lee JW, Bae HS, Shim SB, Jee SW, Lee SH et al. Detection of allergenic compounds using an IL-4/Luciferase/CNS-1 transgenic mice model. Toxicol Sci 2011;120:349-359. https://doi.org/10.1093/toxsci/kfr004
  32. Moller DR, Gallagher JS, Bernstein DI, Wilcox TG, Burroughs HE, Bernstein IL. Detection of IgE-mediated respiratory sensitization in workers exposed to hexahydrophthalic anhydride. J Allergy Clin Immunol 1985;75:663-672. https://doi.org/10.1016/0091-6749(85)90091-0
  33. Pakarinen M, Koivuluhta M, Kalkkinen N, Keskinen H, Nordman H, Estlander T et al. Phthalic anhydride allergy: development and characterization of optimized hapten-carrier conjugates for improved diagnosis. Allergy. 2002;57:894-899. https://doi.org/10.1034/j.1398-9995.2002.23579.x
  34. Lee YJ, Kim JE, Kwak MH, Go J, Kim DS, Son H et al. Quantitative evaluation of the therapeutic effect of fermented soybean products containing a high concentration of GABA on phthalic anhydride-induced atopic dermatitis in IL-4/Luc/CNS-1 Tg mice. Int J Mol Med 2014;33:1185-1194. https://doi.org/10.3892/ijmm.2014.1685
  35. Mok JY, Jeon IH, Cho JK, Park JM, Kim HS, Kang HJ et al. Effect of persimmon leaf extract on phthalic anhydride-induced allergic response in mice. Prev Nutr Food Sci 2012;17:14-21. https://doi.org/10.3746/pnf.2012.17.1.014
  36. Barnes PJ, Karin M. Nuclear factor-kappaB: a pivotal transcription factor in chronic inflammatory diseases. N Engl J Med 1997;336:1066-1071. https://doi.org/10.1056/NEJM199704103361506
  37. Jeong HJ, Koo HN, Na HJ, Kim MS, Hong SH, Eom JW et al. Inhibition of TNF-alpha and IL-6 production by Aucubin through blockade of NFkappaB activation RBL-2H3 mast cells. Cytokine 2002;18:252-259. https://doi.org/10.1006/cyto.2002.0894
  38. Marquardt DL, Walker LL. Dependence of mast cell IgE-mediated cytokine production on nuclear factor-kappaB activity. J Allergy Clin Immunol 2000;105:500-505. https://doi.org/10.1067/mai.2000.104942
  39. Matsumoto M, Yamada T, Yoshinaga SK, Boone T, Horan T, Fujita S, et al. Essential role of NF-kappa B-inducing kinase in T cell activation through the TCR/CD3 pathway. J Immunol 2002;169:1151-1158. https://doi.org/10.4049/jimmunol.169.3.1151
  40. Park JH, Kim MS, Jeong GS, Yoon J. Xanthii fructus extract inhibits $TNF-{\alpha}$/IFN-${\gamma}$-induced Th2-chemokines production via blockade of $NF-{\kappa}B$, STAT1 and p38-MAPK activation in human epidermal keratinocytes. J Ethnopharmacol 2015;171:85-93. https://doi.org/10.1016/j.jep.2015.05.039
  41. Wullaert A, Bonnet MC, Pasparakis M. $NF-{\kappa}B$ in the regulation of epithelial homeostasis and inflammation. Cell Res 2011;21:146-158. https://doi.org/10.1038/cr.2010.175
  42. Chang WA, Hung JY, Jian SF, Lin YS, Wu CY, Hsu YL et al. Laricitrin ameliorates lung cancer-mediated dendritic cell suppression by inhibiting signal transducer and activator of transcription 3. Oncotarget 2016;7:85220-85234. https://doi.org/10.18632/oncotarget.13240
  43. Tyagi A, Agarwal C, Dwyer-Nield LD, Singh RP, Malkinson AM, Agarwal R. Silibinin modulates$TNF-{\alpha}$ and IFN-${\gamma}$ mediated signaling to regulate COX2 and iNOS expression in tumorigenic mouse lung epithelial LM2 cells. Mol Carcinog 2012;51:832-842. https://doi.org/10.1002/mc.20851
  44. Park JH, Yeo IJ, Han JH, Suh JW, Lee HP, Hong JT. Anti-inflammatory effect of astaxanthin in phthalic anhydride-induced atopic dermatitis animal model. Exp Dermatol 2018;27:378-385. https://doi.org/10.1111/exd.13437
  45. Cargnello M, Roux PP. Activation and function of the MAPKs and their substrates, the MAPK-activated protein kinases. Microbiol Mol Biol Rev 2011;75:50-83. https://doi.org/10.1128/MMBR.00031-10
  46. Moy JK, Khoutorsky A, Asiedu MN, Black BJ, Kuhn JL, Barragan-Iglesias P et al. The MNK-eIF4E signaling axis contributes to injury-induced nociceptive plasticity and the development of chronic pain. J Neurosci 2017;37:7481-7499. https://doi.org/10.1523/JNEUROSCI.0220-17.2017
  47. Wang Z, Ma W, Chabot JG, Quirion R. Cell-type specific activation of p38 and ERK mediates calcitonin gene-related peptide involvement in tolerance to morphine-induced analgesia. FASEB J 2009;23:2576-2586. https://doi.org/10.1096/fj.08-128348
  48. Kim EK, Choi EJ. Compromised MAPK signaling in human diseases: an update. Arch Toxicol 2015;89:867-882. https://doi.org/10.1007/s00204-015-1472-2
  49. Obata K, Yamanaka H, Dai Y, Tachibana T, Fukuoka T, Tokunaga A et al. Differential activation of extracellular signal-regulated protein kinase in primary afferent neurons regulates brain-derived neurotrophic factor expression after peripheral inflammation and nerve injury. J Neurosci 2003;23:4117-4126. https://doi.org/10.1523/jneurosci.23-10-04117.2003
  50. Manassero G, Repetto IE, Cobianchi S, Valsecchi V, Bonny C, Rossi F et al. Role of JNK isoforms in the development of neuropathic pain following sciatic nerve transection in the mouse. Mol Pain 2012;8:39.
  51. Peluso I, Yarla NS, Ambra R, Pastore G, Perry G. MAPK signalling pathway in cancers: Olive products as cancer preventive and therapeutic agents. Semin Cancer Biol 2019;56:185-195. https://doi.org/10.1016/j.semcancer.2017.09.002
  52. Moon DO, Park SY, Lee KJ, Heo MS, Kim KC, Kim MO et al. Bee venom and melittin reduce proinflammatory mediators in lipopolysaccharidestimulated BV2 microglia. Int Immunopharmacol 2007;7:1092-1101. https://doi.org/10.1016/j.intimp.2007.04.005
  53. Lariviere WR, Melzack R. The bee venom test: a new tonic-pain test. Pain 1996;66:271-277. https://doi.org/10.1016/0304-3959(96)03075-8
  54. Kwon YB, Kang MS, Kim HW, Ham TW, Yim YK, Jeong SH et al. Antinociceptive effects of bee venom acupuncture (apipuncture) in rodent animal models: a comparative study of acupoint versus non-acupoint stimulation. Acupunct Electrother Res 2001;26:59-68. https://doi.org/10.3727/036012901816356054
  55. Wang C, Chen T, Zhang N, Yang M, Li B, Lu X et al. Melittin, a major component of bee venom, sensitizes human hepatocellular carcinoma cells to tumor necrosis factor-related apoptosis-inducing ligand (TRAIL)-induced apoptosis by activating CaMKII-TAK1-JNK/p38 and inhibiting IkappaBalpha kinase-NFkappaB. J Biol Chem 2009;284:3804-3813. https://doi.org/10.1074/jbc.M807191200
  56. Sur B, Lee B, Yeom M, Hong JH, Kwon S, Kim ST et al. Bee venom acupuncture alleviates trimellitic anhydride-induced atopic dermatitis-like skin lesions in mice. BMC Complement Altern Med 2016;16:38.

피인용 문헌

  1. Cosmetic Applications of Bee Venom vol.13, pp.11, 2021, https://doi.org/10.3390/toxins13110810