Skip to main content
Top
Published in: BMC Complementary Medicine and Therapies 1/2015

Open Access 01-12-2015 | Research article

Protective effect of diet supplemented with rice prolamin extract against DNCB-induced atopic dermatitis in BALB/c mice

Authors: Hyun-Joong Yoon, Mi-Sun Jang, Hyun-Woo Kim, Dong-Up Song, Kwang-Il Nam, Choon-Sang Bae, Seong-Jin Kim, Seung-Rock Lee, Chang-Sub Ku, Dong-Il Jang, Bong-Whan Ahn

Published in: BMC Complementary Medicine and Therapies | Issue 1/2015

Login to get access

Abstract

Background

Rice prolamin has been reported to possess antioxidative, anti-inflammatory and immune-promoting properties. This study is aimed to examine the protective effects of dietary rice prolamin extract (RPE) against dinitrochlorobenzene (DNCB)-induced atopic dermatitis (AD)-like skin lesions in mice.

Methods

BALB/c mice were fed diet supplemented with 0–0.1 % RPE for 6 weeks. For the last 2 weeks, 1 % or 0.2 % DNCB was applied repeatedly to the back skin of mice to induce AD-like lesions. Following AD induction, the severity of skin lesions was examined macroscopically and histologically. In addition, the serum levels of IgE, IgG1 and IgG2a were determined by ELISA, and the mRNA expression of IL-4 and IFN-γ in the skin was determined by real-time PCR.

Results

Dietary RPE suppressed the clinical symptoms of DNCB-induced dermatitis as well as its associated histopathological changes such as epidermal hyperplasia and infiltration of mast cells and eosinophils in the dermis. RPE treatment also suppressed the DNCB-induced increase in transepidermal water loss. Dietary RPE inhibited the DNCB-induced enhancement of serum IgE and IgG1 levels, whereas it increased the serum IgG2a level in DNCB-treated mice. In addition, dietary RPE upregulated the IFN-γ mRNA expression and downregulated the IL-4 mRNA expression in the skin of DNCB-treated mice.

Conclusions

The above results suggest that dietary RPE exerts a protective effect against DNCB-induced AD in mice via upregulation of Th1 immunity and that RPE may be useful for the treatment of AD.
Literature
1.
go back to reference Weston S, Halbert A, Richmond P, Prescott SL. Effects of probiotics on atopic dermatitis: a randomised controlled trial. Arch Dis Child. 2005;90(9):892–7.CrossRefPubMedPubMedCentral Weston S, Halbert A, Richmond P, Prescott SL. Effects of probiotics on atopic dermatitis: a randomised controlled trial. Arch Dis Child. 2005;90(9):892–7.CrossRefPubMedPubMedCentral
2.
go back to reference Bogfuniewicz M, Schmid-Grendelmeier P, Leung DY. Atopic dermatitis. J Allergy Clin Immunol. 2006;118(1):40–3.CrossRef Bogfuniewicz M, Schmid-Grendelmeier P, Leung DY. Atopic dermatitis. J Allergy Clin Immunol. 2006;118(1):40–3.CrossRef
3.
go back to reference Liu FT, Goodarzi H, Chen HY. IgE, mast cells, and eosinophils in atopic dermatitis. Clin Rev Allergy Immunol. 2011;41(3):298–310.CrossRefPubMed Liu FT, Goodarzi H, Chen HY. IgE, mast cells, and eosinophils in atopic dermatitis. Clin Rev Allergy Immunol. 2011;41(3):298–310.CrossRefPubMed
4.
go back to reference Chan LS, Robinson N, 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. 2001;117(4):977–83.CrossRefPubMed Chan LS, Robinson N, 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. 2001;117(4):977–83.CrossRefPubMed
6.
go back to reference Hattori K, Nishikawa M, Watcharanurak K, Ikoma A, Kabashima K, Toyota H, et al. Sustained exogenous expression of therapeutic levels of IFN-gamma ameliorates atopic dermatitis in NC/Nga mice via Th1 polarization. J Immunol. 2010;184(5):2729–35.CrossRefPubMed Hattori K, Nishikawa M, Watcharanurak K, Ikoma A, Kabashima K, Toyota H, et al. Sustained exogenous expression of therapeutic levels of IFN-gamma ameliorates atopic dermatitis in NC/Nga mice via Th1 polarization. J Immunol. 2010;184(5):2729–35.CrossRefPubMed
7.
go back to reference Won TJ, Kim B, Lim YT, Song DS, Park SY, Park ES, et al. Oral administration of Lactobacillus strains from Kimchi inhibits atopic dermatitis in NC/Nga mice. J Appl Microbiol. 2011;110(5):1195–202. Won TJ, Kim B, Lim YT, Song DS, Park SY, Park ES, et al. Oral administration of Lactobacillus strains from Kimchi inhibits atopic dermatitis in NC/Nga mice. J Appl Microbiol. 2011;110(5):1195–202.
8.
go back to reference Özdemir Ö. The role of probiotics in atopic dermatitis prevention and therapy. In: Esparza-Gordillo J, Dekio I, editors. Atopic Dermatitis - Disease Etiology and Clinical Management. Rijeka: Intech; 2012. p. 353–86. Özdemir Ö. The role of probiotics in atopic dermatitis prevention and therapy. In: Esparza-Gordillo J, Dekio I, editors. Atopic Dermatitis - Disease Etiology and Clinical Management. Rijeka: Intech; 2012. p. 353–86.
9.
go back to reference West CE, Hammarström ML, Hernell O. Probiotics during weaning reduce the incidence of eczema. Pediatr Allergy Immunol. 2009;20(5):430–7.CrossRefPubMed West CE, Hammarström ML, Hernell O. Probiotics during weaning reduce the incidence of eczema. Pediatr Allergy Immunol. 2009;20(5):430–7.CrossRefPubMed
10.
go back to reference Sistek D, Kelly R, Wickens K, Stanley T, Fitzharris P, Crane J. Is the effect of probiotics on atopic dermatitis confined to food sensitized children? Clin Exp Allergy. 2006;36(5):629–33.CrossRefPubMed Sistek D, Kelly R, Wickens K, Stanley T, Fitzharris P, Crane J. Is the effect of probiotics on atopic dermatitis confined to food sensitized children? Clin Exp Allergy. 2006;36(5):629–33.CrossRefPubMed
11.
go back to reference Pohjavuori E, Viljanen M, Korpela R, Kuitunen M, Tiittanen M, Vaarala O, et al. Lactobacillus GG effect in increasing IFN-gamma production in infants with cow’s milk allergy. J Allergy Clin Immunol. 2004;114(1):131–6. Pohjavuori E, Viljanen M, Korpela R, Kuitunen M, Tiittanen M, Vaarala O, et al. Lactobacillus GG effect in increasing IFN-gamma production in infants with cow’s milk allergy. J Allergy Clin Immunol. 2004;114(1):131–6.
12.
go back to reference Juliano BO. RICE Chemistry and Technology. 2nd ed. Minnesota: The American Association of Cereal Chemists; 1985. Juliano BO. RICE Chemistry and Technology. 2nd ed. Minnesota: The American Association of Cereal Chemists; 1985.
13.
go back to reference Qureshi AA, Sami SA, Salser WA, Khan FA. Dose-dependent suppression of serum cholesterol by tocotrienol-rich fraction (TRF25) of rice bran in hypercholesterolemic humans. Atherosclerosis. 2002;161(1):199–207. Qureshi AA, Sami SA, Salser WA, Khan FA. Dose-dependent suppression of serum cholesterol by tocotrienol-rich fraction (TRF25) of rice bran in hypercholesterolemic humans. Atherosclerosis. 2002;161(1):199–207.
14.
go back to reference Yang L, Kumagai T, Kawamura H, Watanabe T, Kubota M, Fujimura S, et al. Effects of rice proteins from two cultivars, Koshihikari and Shunyo, on cholesterol and triglyceride metabolism in growing and adult rats. Biosci Biotechnol Biochem. 2007;71(3):694–703. Yang L, Kumagai T, Kawamura H, Watanabe T, Kubota M, Fujimura S, et al. Effects of rice proteins from two cultivars, Koshihikari and Shunyo, on cholesterol and triglyceride metabolism in growing and adult rats. Biosci Biotechnol Biochem. 2007;71(3):694–703.
15.
go back to reference Katayama M, Sugie S, Yoshimi N, Yamada Y, Sakata K, Qiao Z, et al. Preventive effect of fermented brown rice and rice bran on diethylnitrosoamine and phenobarbital-induced hepatocarcinogenesis in male F344 rats. Oncol Rep. 2003;10(4):875–80. Katayama M, Sugie S, Yoshimi N, Yamada Y, Sakata K, Qiao Z, et al. Preventive effect of fermented brown rice and rice bran on diethylnitrosoamine and phenobarbital-induced hepatocarcinogenesis in male F344 rats. Oncol Rep. 2003;10(4):875–80.
16.
go back to reference Shibata T, Nagayasu H, Kitajo H, Arisue M, Yamashita T, Hatakeyama D, et al. Inhibitory effects of fermented brown rice and rice bran on the development of acute hepatitis in Long-Evans Cinnamon rats. Oncol Rep. 2006;15(4):869–74. Shibata T, Nagayasu H, Kitajo H, Arisue M, Yamashita T, Hatakeyama D, et al. Inhibitory effects of fermented brown rice and rice bran on the development of acute hepatitis in Long-Evans Cinnamon rats. Oncol Rep. 2006;15(4):869–74.
17.
go back to reference Yamazaki K, Murray JA, Kita H. Innate immunomodulatory effects of cereal grains through induction of IL-10. J Allergy Clin Immunol. 2008;121(1):172–8.CrossRefPubMed Yamazaki K, Murray JA, Kita H. Innate immunomodulatory effects of cereal grains through induction of IL-10. J Allergy Clin Immunol. 2008;121(1):172–8.CrossRefPubMed
18.
go back to reference Islam MS, Murata T, Fujisawa M, Nagasaka R, Ushio H, Bari AM, et al. Anti-inflammatory effects of phytosteryl ferulates in colitis induced by dextran sulphate sodium in mice. Br J Pharmacol. 2008;154(4):812–24. Islam MS, Murata T, Fujisawa M, Nagasaka R, Ushio H, Bari AM, et al. Anti-inflammatory effects of phytosteryl ferulates in colitis induced by dextran sulphate sodium in mice. Br J Pharmacol. 2008;154(4):812–24.
19.
go back to reference Murakami M, Ota H, Sugiyama A, Ishizone S, Maruta F, Akita N, et al. Suppressive effect of rice extract on Helicobacter pylori infection in a Mongolian gerbil model. J Gastroenterol. 2005;40(5):459–66. Murakami M, Ota H, Sugiyama A, Ishizone S, Maruta F, Akita N, et al. Suppressive effect of rice extract on Helicobacter pylori infection in a Mongolian gerbil model. J Gastroenterol. 2005;40(5):459–66.
20.
go back to reference Song DU, Jang MS, Kim HW, Yoon HJ, Chay KO, Joo YE, et al. Gastroprotective effects of glutinous rice extract against ethanol-, indomethacin-, and stress-induced ulcers in rats. Chonnam Med J. 2014;50(1):6–14. Song DU, Jang MS, Kim HW, Yoon HJ, Chay KO, Joo YE, et al. Gastroprotective effects of glutinous rice extract against ethanol-, indomethacin-, and stress-induced ulcers in rats. Chonnam Med J. 2014;50(1):6–14.
21.
go back to reference Shewry PR, Halford NG. Cereal seed storage proteins: structures, properties and role in grain utilization. J Exp Bot. 2002;53(370):947–58.CrossRefPubMed Shewry PR, Halford NG. Cereal seed storage proteins: structures, properties and role in grain utilization. J Exp Bot. 2002;53(370):947–58.CrossRefPubMed
22.
go back to reference Kawase SI, Matsumura Y, Murakami H, Mori T. Comparison of antioxidative activity among three types of prolamin subunits. J Cereal Sci. 1998;28(1):33–41.CrossRef Kawase SI, Matsumura Y, Murakami H, Mori T. Comparison of antioxidative activity among three types of prolamin subunits. J Cereal Sci. 1998;28(1):33–41.CrossRef
23.
go back to reference Chung CY, Park YL, Kim N, Oh HH, Myung DS, Kim JS, et al. Rice prolamin extract ameliorates acute murine colitis by inhibiting nuclear factor-kappa B and modulating intestinal apoptosis and cell proliferation. Clin Exp Immunol. 2014;178(3):537–47. Chung CY, Park YL, Kim N, Oh HH, Myung DS, Kim JS, et al. Rice prolamin extract ameliorates acute murine colitis by inhibiting nuclear factor-kappa B and modulating intestinal apoptosis and cell proliferation. Clin Exp Immunol. 2014;178(3):537–47.
24.
go back to reference Chen YJ, Chen YY, Wu CT, Yu CC, Liao HF. Prolamin, a rice protein, augments anti-leukaemia immune response. J Cereal Sci. 2010;51(2):189–97.CrossRef Chen YJ, Chen YY, Wu CT, Yu CC, Liao HF. Prolamin, a rice protein, augments anti-leukaemia immune response. J Cereal Sci. 2010;51(2):189–97.CrossRef
25.
go back to reference Liao HF, Chen YY, Yang YC, Wang CS, Chen YJ. Rice (Oryza sativa L.) inhibits growth and induces differentiation of human leukemic U937 cells through activation of peripheral blood mononuclear cells. Food Chem Toxicol. 2006;44(10):1724–9.CrossRefPubMed Liao HF, Chen YY, Yang YC, Wang CS, Chen YJ. Rice (Oryza sativa L.) inhibits growth and induces differentiation of human leukemic U937 cells through activation of peripheral blood mononuclear cells. Food Chem Toxicol. 2006;44(10):1724–9.CrossRefPubMed
26.
go back to reference Kubota M, Saito Y, Masumura T, Kumagai T, Watanabe R, Fujimura S, et al. Improvement in the in vivo digestibility of rice protein by alkali extraction is due to structural changes in prolamin/protein body-I particle. Biosci Biotechnol Biochem. 2010;74(3):614–9. Kubota M, Saito Y, Masumura T, Kumagai T, Watanabe R, Fujimura S, et al. Improvement in the in vivo digestibility of rice protein by alkali extraction is due to structural changes in prolamin/protein body-I particle. Biosci Biotechnol Biochem. 2010;74(3):614–9.
27.
go back to reference Ju ZY, Hettiarachchy NS, Rath N. Extraction, denaturation and hydrophobic properties of rice flour protein. J Food Sci. 2001;66(2):229–32.CrossRef Ju ZY, Hettiarachchy NS, Rath N. Extraction, denaturation and hydrophobic properties of rice flour protein. J Food Sci. 2001;66(2):229–32.CrossRef
28.
go back to reference Lee KS, Jeong ES, Heo SH, Seo JH, Jeong DG, Choi YK. A novel model for human atopic dermatitis: application of repeated DNCB patch in BALB/c mice, in comparison with NC/Nga mice. Lab Anim Res. 2010;26(1):95–102.CrossRef Lee KS, Jeong ES, Heo SH, Seo JH, Jeong DG, Choi YK. A novel model for human atopic dermatitis: application of repeated DNCB patch in BALB/c mice, in comparison with NC/Nga mice. Lab Anim Res. 2010;26(1):95–102.CrossRef
29.
go back to reference Matsuda H, Watanabe N, Geba GP, Sperl J, Tsudzuki M, Hiroi J, et al. Development of atopic dermatitis-like skin lesion with IgE hyperproduction in NC/Nga mice. Int Immunol. 1997;9(3):461–6. Matsuda H, Watanabe N, Geba GP, Sperl J, Tsudzuki M, Hiroi J, et al. Development of atopic dermatitis-like skin lesion with IgE hyperproduction in NC/Nga mice. Int Immunol. 1997;9(3):461–6.
30.
go back to reference Kim EC, Lee HS, Kim SK, Choi MS, Lee S, Han JB, et al. The bark of Betula platyphylla var. japonica inhibits the development of atopic dermatitis-like skin lesions in NC/Nga mice. J Ethnopharmacol. 2008;116(2):270–8. Kim EC, Lee HS, Kim SK, Choi MS, Lee S, Han JB, et al. The bark of Betula platyphylla var. japonica inhibits the development of atopic dermatitis-like skin lesions in NC/Nga mice. J Ethnopharmacol. 2008;116(2):270–8.
31.
go back to reference Snapper CM, Paul WE. Interferon-gamma and B cell stimulatory factor-1 reciprocally regulate Ig isotype production. Science. 1987;236(4804):944–7.CrossRefPubMed Snapper CM, Paul WE. Interferon-gamma and B cell stimulatory factor-1 reciprocally regulate Ig isotype production. Science. 1987;236(4804):944–7.CrossRefPubMed
32.
go back to reference Stone KD, Prussin C, Metcalfe DD. IgE, mast cells, basophils, and eosinophils. J Allergy Clin Immunol. 2010;125(25):73–80.CrossRef Stone KD, Prussin C, Metcalfe DD. IgE, mast cells, basophils, and eosinophils. J Allergy Clin Immunol. 2010;125(25):73–80.CrossRef
33.
go back to reference Kidd P. Th1/Th2 balance: the hypothesis, its limitations, and implications for health and disease. Altern Med Rev. 2003;8(3):223–46.PubMed Kidd P. Th1/Th2 balance: the hypothesis, its limitations, and implications for health and disease. Altern Med Rev. 2003;8(3):223–46.PubMed
34.
go back to reference Amsen D, Blander JM, Lee GR, Tanigaki K, Honjo T, Flavell RA. Instruction of distinct CD4 T helper cell fates by different notch ligands on antigen-presenting cells. Cell. 2004;117(4):515–26.CrossRefPubMed Amsen D, Blander JM, Lee GR, Tanigaki K, Honjo T, Flavell RA. Instruction of distinct CD4 T helper cell fates by different notch ligands on antigen-presenting cells. Cell. 2004;117(4):515–26.CrossRefPubMed
35.
go back to reference Mazmanian SK, Liu CH, Tzianabos AO, Kasper DL. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell. 2005;122(1):107–18.CrossRefPubMed Mazmanian SK, Liu CH, Tzianabos AO, Kasper DL. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell. 2005;122(1):107–18.CrossRefPubMed
36.
go back to reference Biedermann T, Röcken M, Carballido JM. TH1 and TH2 lymphocyte development and regulation of TH cell-mediated immune responses of the skin. J Investig Dermatol Symp Proc. 2004;9(1):5–14.CrossRefPubMed Biedermann T, Röcken M, Carballido JM. TH1 and TH2 lymphocyte development and regulation of TH cell-mediated immune responses of the skin. J Investig Dermatol Symp Proc. 2004;9(1):5–14.CrossRefPubMed
37.
go back to reference Wang G, Savinko T, Wolff H, Dieu-Nosjean MC, Kemeny L, Homey B, et al. Repeated epicutaneous exposures to ovalbumin progressively induce atopic dermatitis-like skin lesions in mice. Clin Exp Allergy. 2007;37(1):151–61. Wang G, Savinko T, Wolff H, Dieu-Nosjean MC, Kemeny L, Homey B, et al. Repeated epicutaneous exposures to ovalbumin progressively induce atopic dermatitis-like skin lesions in mice. Clin Exp Allergy. 2007;37(1):151–61.
39.
go back to reference Hatano Y, Terashi H, Arakawa S, Katagiri K. Interleukin-4 suppresses the enhancement of ceramide synthesis and cutaneous permeability barrier functions induced by tumor necrosis factor-alpha and interferon-gamma in human epidermis. J Invest Dermatol. 2005;124(4):786–92.CrossRefPubMed Hatano Y, Terashi H, Arakawa S, Katagiri K. Interleukin-4 suppresses the enhancement of ceramide synthesis and cutaneous permeability barrier functions induced by tumor necrosis factor-alpha and interferon-gamma in human epidermis. J Invest Dermatol. 2005;124(4):786–92.CrossRefPubMed
40.
go back to reference Rescigno M, Rotta G, Valzasina B, Ricciardi-Castagnoli P. Dendritic cells shuttle microbes across gut epithelial monolayers. Immunobiology. 2001;204(5):572–81.CrossRefPubMed Rescigno M, Rotta G, Valzasina B, Ricciardi-Castagnoli P. Dendritic cells shuttle microbes across gut epithelial monolayers. Immunobiology. 2001;204(5):572–81.CrossRefPubMed
41.
go back to reference Mowat AM. Anatomical basis of tolerance and immunity to intestinal antigens. Nat Rev Immunol. 2003;3(4):331–41.CrossRefPubMed Mowat AM. Anatomical basis of tolerance and immunity to intestinal antigens. Nat Rev Immunol. 2003;3(4):331–41.CrossRefPubMed
42.
go back to reference Morelli AE, Thomson AW. Dendritic cells: regulators of alloimmunity and opportunities for tolerance induction. Immunol Rev. 2003;196(1):125–46.CrossRefPubMed Morelli AE, Thomson AW. Dendritic cells: regulators of alloimmunity and opportunities for tolerance induction. Immunol Rev. 2003;196(1):125–46.CrossRefPubMed
Metadata
Title
Protective effect of diet supplemented with rice prolamin extract against DNCB-induced atopic dermatitis in BALB/c mice
Authors
Hyun-Joong Yoon
Mi-Sun Jang
Hyun-Woo Kim
Dong-Up Song
Kwang-Il Nam
Choon-Sang Bae
Seong-Jin Kim
Seung-Rock Lee
Chang-Sub Ku
Dong-Il Jang
Bong-Whan Ahn
Publication date
01-12-2015
Publisher
BioMed Central
Published in
BMC Complementary Medicine and Therapies / Issue 1/2015
Electronic ISSN: 2662-7671
DOI
https://doi.org/10.1186/s12906-015-0892-0

Other articles of this Issue 1/2015

BMC Complementary Medicine and Therapies 1/2015 Go to the issue