Anti‑photoaging effect of fermented agricultural by‑products on ultraviolet B‑irradiated hairless mouse skin

Choi,Sun‑Il; Jung,Tae‑Dong; Cho,Bong‑Yeon; Choi,Seung‑Hyun; Sim,Wan‑Sup; Han,Xionggao; Lee,Sang   Jong; Kim,Young‑Cheul; Lee,Ok‑Hwan

doi:10.3892/ijmm.2019.4242

Anti‑photoaging effect of fermented agricultural by‑products on ultraviolet B‑irradiated hairless mouse skin

Authors:
- Sun‑Il Choi
- Tae‑Dong Jung
- Bong‑Yeon Cho
- Seung‑Hyun Choi
- Wan‑Sup Sim
- Xionggao Han
- Sang Jong Lee
- Young‑Cheul Kim
- Ok‑Hwan Lee
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Affiliations: Department of Food Science and Biotechnology, Kangwon National University, Chuncheon 24341, Republic of Korea, STR Biotech Co., Ltd., Chuncheon 24232, Republic of Korea, Department of Nutrition, University of Massachusetts, Amherst, MA 01003, USA
Published online on: June 12, 2019 https://doi.org/10.3892/ijmm.2019.4242
Pages: 559-568
Copyright: © Choi et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Processed products from agricultural produce generate a large number of agricultural by‑products that contain a number of functional substances. These are often discarded owing to the lack of suitable processing methods. The present study investigated the anti‑photoaging properties of fermented rice bran (FRB), soybean cake (FSB) and sesame seed cake (FSC) on ultraviolet B (UVB)‑irradiated hairless mouse skin. Results indicated that the oral administration of FRB, FSB and FSC effectively inhibited the UVB irradiation‑induced expression of matrix metalloproteinase (MMP)‑2, MMP‑9, MMP‑3 and MMP‑13. Reverse transcription‑quantitative polymerase chain reaction results also demonstrated that FRB, FSB and FSC significantly inhibited the UVB‑induced expression of the genes encoding tumor necrosis factor‑α, inducible nitric oxide synthase, interleukin (IL)‑6 and IL‑1β when compared with the UVB‑vehicle group (P<0.05). Additionally, collagen degradation and mast cell infiltration were reduced in hairless mouse skin. Furthermore, UVB‑induced wrinkle formation was also significantly reduced in mouse skin compared with the UVB‑vehicle group (P<0.05). These results reveal that fermented agricultural by‑products may serve as potential functional materials with anti‑photoaging activities.

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1	Schmalensee R: From 'Green Growth' to sound policies: An overview. Energy Econ. 34(Suppl 1): S2–S6. 2012. View Article : Google Scholar
2	Jänicke M: 'Green growth': From a growing eco-industry to economic sustainability. Energ Policy. 48:13–21. 2012. View Article : Google Scholar
3	Peschel W, Dieckmann W, Sonnenschein M and Plescher A: High antioxidant potential of pressing residues from evening primrose in comparison to other oilseed cakes and plant antioxidants. Ind Crop Prod. 25:44–54. 2007. View Article : Google Scholar
4	Asadullah M: Barriers of commercial power generation using biomass gasification gas: A review. Renew Sust Energ Rev. 24:201–215. 2013.
5	Iwata T: Biodegradable and bio-based polymers: Future prospects of eco-friendly plastics. Angew Chem Int Ed Engl. 54:3210–3215. 2015. View Article : Google Scholar : PubMed/NCBI
6	Perkins C, Siddiqui S, Puri M and Demain AL: Biotechnological applications of microbial bioconversions. Crit Rev Biotechnol. 36:1050–1065. 2016. View Article : Google Scholar
7	Cho YH, Cho JS and Lee GW: Antioxidant activity of wood vinegar by bioconversion. J Korea Acad Industr Coop Soc. 12:4434–4442. 2011. View Article : Google Scholar
8	Kiran EU, Trzcinski AP, NG WJ and Liu Y: Bioconversion of food waste to energy: A review. Fuel. 134:389–399. 2014. View Article : Google Scholar
9	Sanchez S and Demain AL: Enzymes and bioconversions of industrial, pharmaceutical, and biotechnological significance. Org Process Res Dev. 15:224–230. 2011. View Article : Google Scholar
10	Jung TD, Shin GH, Kim JM, Choi SI, Lee JH, Lee SJ, Park SJ, Woo KS, Oh SK and Lee OH: Comparative analysis of γ-oryzanol, β-glucan, total phenolic content and antioxidant activity in fermented rice bran of different varieties. Nutrients. 9:E5172017. View Article : Google Scholar
11	Jung TD, Shin GH, Kim JM, Oh JW, Choi SI, Lee JH, Lee SJ, Heo IY, Park SJ, Kim HT, et al: Assessment of validation method for bioactive contents of fermented soybean extracts by bioconversion and their antioxidant activities. J Korean Soc Food Sci Nutr. 45:680–689. 2016. View Article : Google Scholar
12	Jung TD, Choi SI, Choi SH, Cho BY, Sim WS, Han-Xionggao, Lee SJ, Park SJ, Kim DB, Kim YC, et al: Changes in the anti-allergic activities of sesame by bioconversion. Nutrients. 10:E2102018. View Article : Google Scholar : PubMed/NCBI
13	Kruk J and Duchnik E: Oxidative stress and skin diseases: Possible role of physical activity. Asian Pac J Cancer Prev. 15:561–568. 2014. View Article : Google Scholar : PubMed/NCBI
14	Webb AR and Engelsen O: Calculated ultraviolet exposure levels for a healthy vitamin D status. Photochem Photobiol. 82:1697–1703. 2006. View Article : Google Scholar : PubMed/NCBI
15	Taylor GJ, Bannister GC and Leeming JP: Wound disinfection with ultraviolet radiation. J Hosp Infect. 30:85–93. 1995. View Article : Google Scholar : PubMed/NCBI
16	Imokawa G: Mechanism of UVB-induced wrinkling of the skin: Paracrine cytokine linkage between keratinocytes and fibroblasts leading to the stimulation of elastase. J Investig Dermatol Symp Proc. 14:36–43. 2009. View Article : Google Scholar : PubMed/NCBI
17	Matts PJ: Solar ultraviolet radiation: Definitions and terminology. Dermatol Clin. 24:1–8. 2006. View Article : Google Scholar
18	Algaba I and Riva A: In vitro measurement of the ultraviolet protection factor of apparel textiles. Color Technol. 118:52–58. 2002. View Article : Google Scholar
19	Kim DB, Shin GH, Kim JM, Kim YH, Lee JH, Lee JS, Song HJ, Choe SY, Park IJ, Cho JH and Lee OH: Antioxidant and anti-ageing activities of citrus-based juice mixture. Food Chem. 194:920–927. 2016. View Article : Google Scholar
20	Afaq F and Mukhtar H: Botanical antioxidants in the prevention of photocarcinogenesis and photoaging. Exp Dermatol. 15:678–684. 2006. View Article : Google Scholar : PubMed/NCBI
21	Jurkiewicz BA, Bissett DL and Buettner GR: Effect of topically applied tocopherol on ultraviolet radiation-mediated free radical damage in skin. J Invest Dermatol. 104:484–488. 1995. View Article : Google Scholar : PubMed/NCBI
22	Weichenthal M, Godorr M, Altenhoff J, Neuber K and Breitbart EW: Effects of whole-body UVB irradiation on cytokine production by peripheral blood mononuclear cells from stage I melanoma patients. Arch Dermatol Res. 292:348–353. 2000. View Article : Google Scholar : PubMed/NCBI
23	Muthusamy V and Piva TJ: The UV response of the skin: A review of the MAPK, NFkappaB and TNFalpha signal transduction pathways. Arch Dermatol Res. 302:5–17. 2010. View Article : Google Scholar
24	Miyachi Y: Photoaging from an oxidative standpoint. J Dermatol Sci. 9:79–86. 1995. View Article : Google Scholar : PubMed/NCBI
25	Choi SH, Choi SI, Jung TD, Cho BY, Lee JH, Kim SH, Yoon SA, Ham YM, Yoon WJ, Cho JH and Lee OH: Anti-photoaging effect of jeju putgyul (unripe citrus) extracts on human dermal fibroblasts and ultraviolet B-induced hairless mouse skin. Int J Mol Sci. 18:E20522017. View Article : Google Scholar : PubMed/NCBI
26	Kumar S: Exploratory analysis of global cosmetic industry: Major players, technology and market trends. Technovation. 25:1263–1272. 2005. View Article : Google Scholar
27	Landriscina A, Rosen J and Friedman A: Nanotechnology, inflammation and the skin barrier: Innovative approaches for skin health and cosmesis. Cosmetics. 2:177–186. 2015. View Article : Google Scholar
28	Jeong SC, Park JH and Kim JH: The development trend of skin beauty food with skin protection effects from natural source. Asian J Beauty Cosmetol. 11:203–212. 2013.
29	Yaar M and Gilchrest BA: Aging versus photo aging: Postulated mechanisms and effectors. J Investing Dermatol Symp Proc. 3:47–51. 1998.
30	Bissett DL, Hannonand DP and Orr TV: An animal model of solar-aged skin: Histological, physical, and visible changes in UV-irradiated hairless mouse skin. Photochem Photobiol. 46:367–378. 1987. View Article : Google Scholar : PubMed/NCBI
31	Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) method. Methods. 25:402–408. 2001. View Article : Google Scholar
32	Kwon SB, Lee GT, Choi SJ, Lee NK, Park HW, Lee KS, Lee KK, Ahn KJ and An IS: The effect of glycerin, hyaluronic acid and silicone oil on the hydration, moisturization and transepidermal water loss in human skin. Asian J Beauty Cosmetol. 11:761–768. 2013.
33	Nasir A: Diseases associated with cutaneous barrier dysfunction: Basic science aspects and clinical perspectives. Toxicology of the Skin. Monteiro-Riviere NA: Informa Healthcare; New York: pp. 203–279. 2010
34	Kitatani K, Sheldon K, Rajagopalan V, Anelli V, Jenkins RW, Sun Y, Grabowski GA, Obeid LM and Hannun YA: Involvement of acid beta-glucosidase 1 in the salvage pathway of ceramide formation. J Biol Chem. 284:12972–12978. 2009. View Article : Google Scholar : PubMed/NCBI
35	Sirikudta W, Kulthanan K, Varothai S and Nuchkull P: Moisturizers for patients with atopic dermatitis: An overview. J Allergy Ther. 4:1–6. 2013. View Article : Google Scholar
36	Gkouveris I, Nikitakis N, Aseervatham J, Rao N and Ogbureke KUE: Matrix metalloproteinases in head and neck cancer: Current perspectives. Metalloproteinases Med. 4:47–61. 2017. View Article : Google Scholar
37	Chin JR, Murphy G and Werb Z: Stromelysin, a connective tissue-degrading metalloendopeptidase secreted by stimulated rabbit synovial fibroblasts in parallel with collage-nase. Biosynthesis, isolation, characterization, and substrates. J Biol Chem. 260:12367–12376. 1985.PubMed/NCBI
38	Sunami E, Tsuno N, Osada T, Saito S, Kitayama J, Tomozawa S, Tsuruo T, Shibata Y, Muto T and Nagawa H: MMP-1 is a prognostic marker for hematogenous metastasis of colorectal cancer. Oncologist. 5:108–114. 2000. View Article : Google Scholar : PubMed/NCBI
39	Fini ME and Girard MT: The pattern of metalloproteinase expression by corneal fibroblasts is altered by passage in cell culture. J Cell Sci. 97:373–383. 1990.PubMed/NCBI
40	Murphy G, Hembry RM, McGarrity AM, Reynolds JJ and Henderson B: Gelatinase (type IV collagenase) immunolocalization in cells and tissues: Use of an antiserum to rabbit bone gelatinase that identifies high and low Mr forms. J Cell Sci. 92:487–495. PubMed/NCBI
41	Meigel WN, Gay S and Weber L: Dermal architecture and collagen type distribution. Arch Dermatol Res. 259:1–10. 1977. View Article : Google Scholar : PubMed/NCBI
42	Robichaud TK, Steffensen B and Fields GB: Exosite interactions impact matrix metalloproteinase collagen specificities. J Biol Chem. 286:37535–37542. 2011. View Article : Google Scholar : PubMed/NCBI
43	Pillai S, Oresajo C and Hayward J: Ultraviolet radiation and skin aging: Roles of reactive oxygen species, inflammation and protease activation, and strategies for prevention of inflammation-induced matrix degradation-a review. Int J Cosmet Sci. 27:17–34. 2005. View Article : Google Scholar
44	Nichols JA and Katiyar SK: Skin photoprotection by natural polyphenols: Anti-inflammatory, antioxidant and DNA repair mechanisms. Arch Dermatol Res. 302:71–83. 2010. View Article : Google Scholar
45	Chen CC, Chiang AN, Liu HN and Chang YT: EGb-761 prevents ultraviolet B-induced photoaging via inactivation of mitogen-activated protein kinases and proinflammatory cytokine expression. J Dermatol Sci. 75:55–62. 2014. View Article : Google Scholar : PubMed/NCBI
46	Fo KY and Hameed BH: Utilization of rice husk ash as novel adsorbent: A judicious recycling of the colloidal agricultural waste. Adv Colloid Interfac Sci. 152:39–47. 2009. View Article : Google Scholar
47	Puglia C, Offerta A, Saija A, Trombetta D and Venera C: Protective effect of red orange extract supplementation against UV-induced skin damages: Photoaging and solar lentigines. J Cosmet Dermatol. 13:151–157. 2014. View Article : Google Scholar : PubMed/NCBI
48	Davies KJ: Protein damage and degradation by oxygen radical. I. general aspects. J Biol Chem. 262:9895–9901. 1987.PubMed/NCBI
49	Bissett DL, Chatterjee R and Hannon DP: Photoprotective effect of superoxide-scavenging antioxidants against ultraviolet radiation-induced chronic skin damage in the hairless mouse. Photodermatol Photoimmunol Photomed. 7:56–62. 1990.PubMed/NCBI
50	Korać RR and Khambholja KM: Potential of herbs in skin protection from ultraviolet radiation. Pharmacog Rev. 5:164–173. 2011. View Article : Google Scholar
51	Choi WH, Ann HS, Choi TY, Jin SY and Ahn RM: Effects of natural extracts on UVB-induced pigmentation and inflammation in C57BL/6 mouse skin. Korean J Environ Health Sci. 32:492–498. 2006.
52	Nanashima N, Horie K, Maeda H, Tomisawa T, Kitajima M and Nakamura T: Blackcurrant anthocyanins increase the levels of collagen, elastin and hyaluronic acid in human skin fibroblasts and ovariectomized rats. Nutrients. 10:E4952018. View Article : Google Scholar
53	Varani J, Schuger L, Dame MK, Leonard C, Fligiel SE, Kang S, Fisher GJ and Voorhees JJ: Reduced fibroblast interaction with intact collagen as a mechanism for depressed collagen synthesis in photodamaged skin. J Investig Dermatol. 122:1471–1479. 2004. View Article : Google Scholar : PubMed/NCBI
54	Frances C and Robert L: Elastin and elastic fibers in normal and pathologic skin. Int J Dermatol. 23:166–179. 1984. View Article : Google Scholar : PubMed/NCBI
55	Kligman LH and Kligman AM: The nature of photoaging: Its prevention and repair. Photodermatol. 3:215–227. 1986.PubMed/NCBI
56	Foote CS: Photosensitized oxidation and singlet oxygen; consequences in biological systems. Free Radicals in Biology. Pryor WA: Academic Press; New York: pp. 85–133. 1976, View Article : Google Scholar
57	Hwang BM, Noh EM, Kim JS, Kim JM, You YO, Hwang JK, Kwon KB and Lee YR: Curcumininhibits UVB-induced matrix metalloproteinase-1/3 expression by suppressing the MAPK-p38/JNK pathways in human dermal fibroblasts. Exp Dermatol. 22:371–374. 2013. View Article : Google Scholar : PubMed/NCBI