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

Lee,Young Ju; Kim,Ji Eun; Kwak,Moon Hwa; Go,Jun; Kim,Dong Seob; Son,Hong Joo; Hwang,Dae Youn

doi:10.3892/ijmm.2014.1685

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

Authors:
- Young Ju Lee
- Ji Eun Kim
- Moon Hwa Kwak
- Jun Go
- Dong Seob Kim
- Hong Joo Son
- Dae Youn Hwang
View Affiliations

Affiliations: Department of Biomaterials Science, College of Natural Resources and Life Science/Life and Industry Convergence Research Institute, Pusan National University, Gyeongsangnam-do 627-706, Republic of Korea, Department of Food Science and Technology, College of Natural Resources and Life Science/Life and Industry Convergence Research Institute, Pusan National University, Gyeongsangnam-do 627-706, Republic of Korea, Department of Life Science and Environment Biochemistry, College of Natural Resources and Life Science/Life and Industry Convergence Research Institute, Pusan National University, Gyeongsangnam-do 627-706, Republic of Korea
Published online on: March 6, 2014 https://doi.org/10.3892/ijmm.2014.1685
Pages: 1185-1194

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Cheonggukjang (CKJ) is a fermented soybean product that exhibits diverse biological and pharmacological activities, including anti-obesity, anti-diabetic, and anti‑inflammatory effects on human chronic diseases. In this study, the effects of the aqueous extract of CKJ containing a high concentration of GABA on atopic dermatitis (AD) were quantified using the luciferase reporter system in IL-4/Luc/CNS-1 transgenic (Tg) mice. Alterations of the luciferase signal and phenotypes of AD were quantified in the IL-4/Luc/CNS-1 Tg mice co-treated with phthalic anhydride (PA) and CKJ for 4 weeks using the IVIS imaging system. A strong luciferase signal was detected in the abdominal region of IL-4/Luc/CNS-1 Tg mice treated with PA alone. However, this signal was significantly reduced in IL-4/Luc/CNS-1 Tg mice co-treated with PA and CKJ. The thymus showed the greatest decrease in luciferase following CKJ treatment, but the level increased after PA treatment. Furthermore, the CKJ-treated group showed improvement of common allergic responses including decreased ear thickness, dermis thickness, auricular lymph node (ALN) weight and infiltrating mast cells. However, IgE concentration and epidermis thickness were maintained a constant level. These results indicated that the luciferase signal may successfully reflect the therapeutic effects of CKJ in IL-4/Luc/CNS-1 Tg mice. The results also suggested that CKJ may be considered an effective substance for the treatment of AD.

View Figures

View References

1	Hanifin JM and Rajka G: Diagnostic features of atopic dermatitis. Acta Derm Venereol Suppl (Stockh). 92:44–47. 1980.
2	Leung DY and Bieber T: Atopic dermatitis. Lancet. 361:151–160. 2003. View Article : Google Scholar
3	Kay AB: Overview of ‘allergy and allergic diseases: with a view to the future’. Br Med Bull. 56:843–864. 2000.
4	Kay AB: Allergy and allergic diseases. First of two parts. N Engl J Med. 344:30–37. 2001. View Article : Google Scholar
5	Jin H, He R, Oyoshi M and Geha RS: Animal models of atopic dermatitis. J Invest Dermatol. 129:31–40. 2009. View Article : Google Scholar
6	Spergel JM and Paller AS: Atopic dermatitis and the atopic march. J Allergy Clin Immunol. 112(Suppl 6): S118–S127. 2003. View Article : Google Scholar : PubMed/NCBI
7	Turner KJ, Stewart GA, Sharp AH and Czarny D: Standardization of allergen extracts by inhibition of RAST, skin test, and chemical composition. Clin Allergy. 10:441–450. 1980. View Article : Google Scholar : PubMed/NCBI
8	Johansson SG: ImmunoCAP specific IgE test: an objective tool for research and routine allergy diagnosis. Expert Rev Mol Diagn. 4:273–279. 2004. View Article : Google Scholar : PubMed/NCBI
9	Petersen AB, Gudmann P, Milvang-Grønager P, Mørkeberg R, Bøgestrand S, Linneberg A and Johansen N: Performance evaluation of a specific IgE assay developed for the ADVIA centaur immunoassay system. Clin Biochem. 37:882–892. 2004. View Article : Google Scholar
10	Bae CJ, Lee JW, Bae HS, Shim SB, Jee SW, Lee SH, Lee CK, Hong JT and Hwang DY: Detection of allergenic compounds using an IL-4/luciferase/CNS-1 transgenic mice model. Toxicol Sci. 120:349–359. 2011. View Article : Google Scholar : PubMed/NCBI
11	Kwak MH, Kim JE, Hwang IS, Lee YJ, An BS, Hong JT, Lee SH and Hwang DY: Quantitative evaluation of therapeutic effect of Liriope platyphylla on phthalic anhydride-induced atopic dermatitis in IL-4/Luc/CNS-1 Tg mice. J Ethnopharmacol. 148:880–889. 2013.PubMed/NCBI
12	Lee JJ, Lee DS and Kim HB: Fermentation patterns of chungkookjang and Kanjang by Bacillus licheniformis B1. Korean J Microbiol. 35:296–301. 1999.
13	Nakajima N, Nozaki N, Ishihara K, Ishikawa A and Tsuji H: Analysis of isoflavone content in tempeh, a fermented soybean, and preparation of a new isoflavone-enriched tempeh. J Biosci Bioeng. 100:685–687. 2005. View Article : Google Scholar : PubMed/NCBI
14	Kwon DY, Jang JS, Lee JE, Kim YS, Shin DH and Park S: The isoflavonoid aglycone-rich fractions of Chungkookjang, fermented unsalted soybean, enhance insulin signaling and peroxisome proliferator-activated receptor-gamma activity in vitro. Biofactors. 26:245–258. 2006. View Article : Google Scholar
15	Su CL, Wu CJ, Chen FN, Wang BJ, Shen SR and Won SJ: Supernatant of bacterial fermented soybean induces apoptosis of human hepatocellular carcinoma Hep 3B cells via activation of caspase-8 and mitochondria. Food Chem Toxicol. 45:303–314. 2007. View Article : Google Scholar
16	Kim MH, Kim SY, Ko JM, Jeong DY and Kim YS: Biological activities of cheonggukjang prepared with several soybean cultivars. Food Sci Biotechnol. 21:475–483. 2012. View Article : Google Scholar
17	Kwon EY, Jung KO, Moon SH and Park KY: Studies on enhancing chemopreventive effect of chungkookjangs-antimutagenic activity of chungkookjangs prepared with the different varieties of soybean and starter. J Korean Assoc Cancer Prev. 7:200–209. 2002.
18	Choi J, Kwon SH, Park KY, Yu BP, Kim ND, Jung JH and Chung HY: The anti-inflammatory action of fermented soybean products in kidney of high-fat-fed rats. J Med Food. 14:232–239. 2011. View Article : Google Scholar : PubMed/NCBI
19	Jalin AMA, Lee CK, Lee CY, Kang AR, Park CM, Cha J, Kim JH, Lee SW, Song YS, Lee JT and Kang SG: Thrombolytic activity of cheonggukjang kinase in recovery from brain damage in a rat cerebral embolic stroke model. Neural Regen Res. 5:1875–1882. 2010.
20	Ko JA, Koo SY and Park HJ: Effects of alginate microencapsulation on the fibrinolytic activity of fermented soybean paste (cheonggukjang) extract. Food Chem. 111:921–924. 2008. View Article : Google Scholar
21	Matsuda A, Tanaka A, Pan W, Okamoto N, Oida K, Kingyo N, Amagai Y, Xia Y, Jang H, Nishikawa S, Kajiwara N, Ahn G, Ohmori K and Matsuda H: Supplementation of the fermented soy product ImmuBalance™ effectively reduces itching behavior of atopic NC/Tnd mice. J Dermatol Sci. 67:130–139. 2012.
22	Jang SN, Kim KL, Yun MY and Kang SM: The effect of γ-PGA on NC/Nga mice, a mouse model for mite antigen-induced atopic dermatitis. Korean J Microbiol Biotechnol. 38:53–63. 2010.(In Korean).
23	Choi YH, Lim H, Heo MY, Kwon DY and Kim HP: Anti-inflammatory activity of the ethanol extract of chungkukjang, Korean fermented bean: 5-lipoxygenase inhibition. J Med Food. 11:539–543. 2008. View Article : Google Scholar : PubMed/NCBI
24	Hwang IS, Kim JE, Lee YJ, Kwak MH, Lee HG, Kim HS, Lee HS and Hwang DY: Growth sensitivity in the epiphyseal growth plate, liver and muscle of SD rats is significantly enhanced by treatment with a fermented soybean product (cheonggukjang) through stimulation of growth hormone secretion. Mol Med Rep. 9:166–172. 2014.
25	Lee YJ, Kim JE, Kwak MH, Go J, Son HJ, Kim DS and Hwang DY: In vitro and in vivo study of effects of fermented soybean product (chungkookjang) on NGF secretion ability and NGF receptor signaling pathway. Lab Anim Res. 29:113–126. 2013. View Article : Google Scholar : PubMed/NCBI
26	Zhang G and Brown AW: The rapid determination of gamma-aminobutyric acid. Phytochemistry. 44:1007–1009. 1997. View Article : Google Scholar
27	Kim JE, Lee YK, Nam SH, Choi SI, Goo JS, Jang MJ, Lee HS, Son HJ, Lee CY and Hwang DY: The symptoms of atopic dermatitis in NC/Nga mice were significantly relieved by the water extract of Liriope platyphylla. Lab Anim Res. 26:377–384. 2010. View Article : Google Scholar
28	Stahlmann R, Wegner M, Riecke K, Kruse M and Platzek T: Sensitising potential of four textile dyes and some of their metabolites in a modified local lymph node assay. Toxicology. 219:113–123. 2006. View Article : Google Scholar : PubMed/NCBI
29	Bae CJ, Shim SB, Jee SW, Lee SH, Kim MR, Lee JW, Lee CK and Hwang DY: IL-6, VEGF, KC and RANTES are a major cause of a high irritant dermatitis to phthalic anhydride in C57BL/6 inbred mice. Allergol Int. 59:389–397. 2010. View Article : Google Scholar : PubMed/NCBI
30	Prussin C and Metcalfe DD: 4. IgE, mast cells, basophils, and eosinophils. J Allergy Clin Immunol. 111(Suppl 2): S486–S494. 2003. View Article : Google Scholar : PubMed/NCBI
31	Spergel JM, Mizoguchi E, Brewer JP, Martin TR, Bhan AK and Geha RS: Epicutaneous sensitization with protein antigen induces localized allergic dermatitis and hyperresponsiveness to methacholine after single exposure to aerosolized antigen in mice. J Clin Invest. 101:1614–1622. 1998. View Article : Google Scholar
32	Kimura M, Tsuruta S and Yoshida T: Correlation of house dust mite-specific lymphocyte proliferation with IL-5 production, eosinophilia, and the severity of symptoms in infants with atopic dermatitis. J Allergy Clin Immunol. 101:84–89. 1998. View Article : Google Scholar
33	Man MQ, Hatano Y, Lee SH, Man M, Chang S, Feingold KR, Leung DY, Holleran W, Uchida Y and Elias PM: Characterization of a hapten-induced, murine model with multiple features of atopic dermatitis: structural, immunologic, and biochemical changes following single versus multiple oxazolone challenges. J Invest Dermatol. 128:79–86. 2008. View Article : Google Scholar
34	Laouini D, Kawamoto S, Yalcindag A, Bryce P, Mizoguchi E, Oettgen H and Geha RS: Epicutaneous sensitization with superantigen induces allergic skin inflammation. J Allergy Clin Immunol. 112:981–987. 2003. View Article : Google Scholar : PubMed/NCBI
35	Chan LS, Robinson N and Xu L: Expression of interleukin-4 in the epidermis of transgenic mice results in a pruritic inflammatory skin disease: an experimental animal model to study atopic dermatitis. J Invest Dermatol. 117:977–983. 2001. View Article : Google Scholar
36	Dillon SR, Sprecher C, Hammond A, et al: Interleukin 31, a cytokine produced by activated T cells, induces dermatitis in mice. Nat Immunol. 5:752–760. 2004. View Article : Google Scholar : PubMed/NCBI
37	Soumelis V, Reche PA, Kanzler H, et al: Human epithelial cells trigger dendritic cell mediated allergic inflammation by producing TSLP. Nat Immunol. 3:673–680. 2002.PubMed/NCBI
38	Kim E, Lee JE, Namkung JH, Park JH, Kim S, Shin ES, Cho EY and Yang JM: Association of the single-nucleotide polymorphism and haplotype of the interleukin 18 gene with atopic dermatitis in Koreans. Clin Exp Allergy. 37:865–871. 2007. View Article : Google Scholar : PubMed/NCBI
39	Weih F, Warr G, Yang H and Bravo R: Multifocal defects in immune responses in RelB-deficient mice. J Immunol. 158:5211–5218. 1997.PubMed/NCBI
40	Tsukuba T, Okamoto K, Okamoto Y, Yanagawa M, Kohmura K, Yasuda Y, Uchi H, Nakahara T, Furue M, Nakayama K, Kadowaki T, Yamamoto K and Nakayama KI: Association of cathepsin E deficiency with development of atopic dermatitis. J Biochem. 134:893–902. 2003. View Article : Google Scholar : PubMed/NCBI
41	Watanabe O, Natori K, Tamari M, Shiomoto Y, Kubo S and Nakamura Y: Significantly elevated expression of PF4 (platelet factor 4) and eotaxin in the NOA mouse, a model for atopic dermatitis. J Hum Genet. 44:173–176. 1999. View Article : Google Scholar
42	Hikita I, Yoshioka T, Mizoguchi T, Tsukahara K, Tsuru K, Nagai H, Hirasawa T, Tsuruta Y, Suzuki R, Ichihashi M and Horikawa T: Characterization of dermatitis arising spontaneously in DS-Nh mice maintained under conventional conditions: another possible model for atopic dermatitis. J Dermatol Sci. 30:142–153. 2002. View Article : Google Scholar
43	Kim JE, Hwang IS, Goo JS, Nam SH, Choi SI, Lee HR, Lee YJ, Kim YH, Park SJ, Kim NS, Choi YH and Hwang DY: LP9M80-H isolated from Liriope platyphylla could help alleviate diabetic symptoms via the regulation of glucose and lipid concentration. J Life Sci. 22:634–641. 2012.
44	Kawakami T, Ando T, Kimura M, Wilson BS and Kawakami Y: Mast cells in atopic dermatitis. Curr Opin Immunol. 21:666–678. 2009. View Article : Google Scholar
45	Galli SJ: Mast cells and basophils. Curr Opin Hematol. 7:32–39. 2000. View Article : Google Scholar
46	Gao XK, Nakamura N, Fuseda K, Tanaka H, Inagaki N and Nagai H: Establishment of allergic dermatitis in NC/Nga mice as a model for severe atopic dermatitis. Biol Pharm Bull. 27:1376–1381. 2004. View Article : Google Scholar : PubMed/NCBI
47	Dearman RJ, Skinner RA, Humphreys NE and Kimber I: Methods for the identification of chemical respiratory allergens in rodents: comparisons of cytokine profiling with induced changes in serum IgE. J Appl Toxicol. 23:199–207. 2003. View Article : Google Scholar