Ganoderma lucidum polysaccharides protect fibroblasts against UVB-induced photoaging

Zeng,Qinghai; Zhou,Fang; Lei,Li; Chen,Jing; Lu,Jianyun; Zhou,Jianda; Cao,Ke; Gao,Lihua; Xia,Fang; Ding,Shu; Huang,Lihua; Xiang,Hong; Wang,Jingjing; Xiao,Yangfan; Xiao,Rong; Huang,Jinhua

doi:10.3892/mmr.2016.6026

Ganoderma lucidum polysaccharides protect fibroblasts against UVB-induced photoaging

Authors:
- Qinghai Zeng
- Fang Zhou
- Li Lei
- Jing Chen
- Jianyun Lu
- Jianda Zhou
- Ke Cao
- Lihua Gao
- Fang Xia
- Shu Ding
- Lihua Huang
- Hong Xiang
- Jingjing Wang
- Yangfan Xiao
- Rong Xiao
- Jinhua Huang
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Affiliations: Department of Dermatology, Third Xiangya Hospital, Central South University, Changsha, Hunan 410013, P.R. China, Department of Burn and Plastic Surgery, Third Xiangya Hospital, Central South University, Changsha, Hunan 410013, P.R. China, Department of Oncology, Third Xiangya Hospital, Central South University, Changsha, Hunan 410013, P.R. China, The Central Laboratory, Third Xiangya Hospital, Central South University, Changsha, Hunan 410013, P.R. China, Department of Dermatology, Second Xiangya Hospital, Central South University, Changsha, Hunan 410013, P.R. China
Published online on: December 12, 2016 https://doi.org/10.3892/mmr.2016.6026
Pages: 111-116
Copyright: © Zeng et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

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Abstract

Ganoderma lucidum has featured in traditional Chinese medicine for >1,000 years. Ganoderma polysaccharides (GL-PS), a major active ingredient in Ganoderma, confer immune regulation, antitumor effects and significant antioxidant effects. The aim of the present study was to investigate the efficacy and mechanism of GL‑PS‑associated inhibition of ultraviolet B (UVB)‑induced photoaging in human fibroblasts in vitro. Primary human skin fibroblasts were cultured, and a fibroblast photoaging model was built through exposure to UVB. Cell viability was measured by MTT assay. Aged cells were stained using a senescence‑associated β-galactosidase staining (SA‑β‑gal) kit. ELISA kits were used to analyze matrix metalloproteinase (MMP) ‑1 and C‑telopeptides of Type I collagen (CICP) protein levels in cellular supernatant. ROS levels were quantified by flow cytometry. Cells exposed to UVB had decreased cell viability, increased aged cells, decreased CICP protein expression, increased MMP‑1 protein expression, and increased cellular ROS levels compared with non‑exposed cells. However, cells exposed to UVB and treated with 10, 20 and 40 µg/ml GL‑PS demonstrated increased cell viability, decreased aged cells, increased CICP protein expression, decreased MMP‑1 protein expression, and decreased cellular ROS levels compared with UVB exposed/GL‑PS untreated cells. These results demonstrate that GL‑PS protects fibroblasts against photoaging by eliminating UVB‑induced ROS. This finding indicates GL‑PS treatment may serve as a novel strategy for antiphotoaging.

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1	Han A, Chien AL and Kang S: Photoaging. Dermatol Clin. 32291–299. (vii)2014.PubMed/NCBI
2	Fisher GJ, Kang S, Varani J, Bata-Csorgo Z, Wan Y, Datta S and Voorhees JJ: Mechanisms of photoaging and chronological skin aging. Arch Dermatol. 138:1462–1470. 2002.PubMed/NCBI
3	Sjerobabski Masnec I and Poduje S: Photoaging. Coll Antropol. 32:(Suppl 2). S177–S180. 2008.
4	Hwang E, Park SY, Lee HJ, Lee TY, Sun ZW and Yi TH: Gallic acid regulates skin photoaging in UVB-exposed fibroblast and hairless mice. Phytother Res. 28:1778–1788. 2014. View Article : Google Scholar : PubMed/NCBI
5	Williams JD, Bermudez Y, Park SL, Stratton SP, Uchida K, Hurst CA and Wondrak GT: Malondialdehyde-derived epitopes in human skin result from acute exposure to solar UV and occur in nonmelanoma skin cancer tissue. J Photochem Photobiol B. 132:56–65. 2014. View Article : Google Scholar : PubMed/NCBI
6	Rittié L and Fisher GJ: UV-light-induced signal cascades and skin aging. Ageing Res Rev. 1:705–720. 2002. View Article : Google Scholar : PubMed/NCBI
7	Valencia A and Kochevar IE: Nox1-based NADPH oxidase is the major source of UVA-induced reactive oxygen species in human keratinocytes. J Invest Dermatol. 128:214–222. 2008. View Article : Google Scholar : PubMed/NCBI
8	Emri G, Horkay I and Remenyik E: The role of free radicals in the UV-induced skin damage. Photo-aging. Orv Hetil. 147:731–735. 2006.(In Hungarian).
9	Van Laethem A, Nys K, Van Kelst S, Claerhout S, Ichijo H, Vandenheede JR, Garmyn M and Agostinis P: Apoptosis signal regulating kinase-1 connects reactive oxygen species to p38 MAPK-induced mitochondrial apoptosis in UVB-irradiated human keratinocytes. Free Radic Biol Med. 41:1361–1371. 2006. View Article : Google Scholar : PubMed/NCBI
10	Watanabe H, Shimizu T, Nishihira J, Abe R, Nakayama T, Taniguchi M, Sabe H, Ishibashi T and Shimizu H: Ultraviolet A-induced production of matrix metalloproteinase-1 is mediated by macrophage migration inhibitory factor (MIF) in human dermal fibroblasts. J Biol Chem. 279:1676–1683. 2004. View Article : Google Scholar : PubMed/NCBI
11	Quan T, He T, Voorhees JJ and Fisher GJ: Ultraviolet irradiation induces Smad7 via induction of transcription factor AP-1 in human skin fibroblasts. J Biol Chem. 280:8079–8085. 2005. View Article : Google Scholar : PubMed/NCBI
12	Brennan M, Bhatti H, Nerusu KC, Bhagavathula N, Kang S, Fisher GJ, Varani J and Voorhees JJ: Matrix metalloproteinase-1 is the major collagenolytic enzyme responsible for collagen damage in UV-irradiated human skin. Photochem Photobiol. 78:43–48. 2003. View Article : Google Scholar : PubMed/NCBI
13	Visse R and Nagase H: Matrix metalloproteinases and tissue inhibitors of metalloproteinases: Structure, function, and biochemistry. Circ Res. 92:827–839. 2003. View Article : Google Scholar : PubMed/NCBI
14	Gambichler T, Skrygan M, Tomi NS, Breuksch S, Altmeyer P and Kreuter A: Significant downregulation of transforming growth factor-beta signal transducers in human skin following ultraviolet-A1 irradiation. Br J Dermatol. 156:951–956. 2007. View Article : Google Scholar : PubMed/NCBI
15	Imokawa G: Recent advances in characterizing biological mechanisms underlying UV-induced wrinkles: A pivotal role of fibrobrast-derived elastase. Arch Dermatol Res. 300:(Suppl 1). S7–S20. 2008. View Article : Google Scholar : PubMed/NCBI
16	Quan T, Qin Z, Xia W, Shao Y, Voorhees JJ and Fisher GJ: Matrix-degrading metalloproteinases in photoaging. J Investig Dermatol Symp Proc. 14:20–24. 2009. View Article : Google Scholar : PubMed/NCBI
17	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
18	Katiyar SK: UV-induced immune suppression and photocarcinogenesis: Chemoprevention by dietary botanical agents. Cancer Lett. 255:1–11. 2007. View Article : Google Scholar : PubMed/NCBI
19	Huang J, Luo X, Lu J, Chen J, Zuo C, Xiang Y, Yang S, Tan L, Kang J and Bi Z: IPL irradiation rejuvenates skin collagen via the bidirectional regulation of MMP-1 and TGF-β1 mediated by MAPKs in fibroblasts. Lasers Med Sci. 26:381–387. 2011. View Article : Google Scholar : PubMed/NCBI
20	Matsui MS, Hsia A, Miller JD, Hanneman K, Scull H, Cooper KD and Baron E: Non-sunscreen photoprotection: Antioxidants add value to a sunscreen. J Investig Dermatol Symp Proc. 14:56–59. 2009. View Article : Google Scholar : PubMed/NCBI
21	Sun S, Jiang P, Su W, Xiang Y, Li J, Zeng L and Yang S: Wild chrysanthemum extract prevents UVB radiation-induced acute cell death and photoaging. Cytotechnology. 68:229–240. 2016. View Article : Google Scholar : PubMed/NCBI
22	Lee KE, Mun S, Pyun HB, Kim MS and Hwang JK: Effects of macelignan isolated from Myristica fragrans (Nutmeg) on expression of matrix metalloproteinase-1 and type I procollagen in UVB-irradiated human skin fibroblasts. Biol Pharm Bull. 35:1669–1675. 2012. View Article : Google Scholar : PubMed/NCBI
23	Yun TK: Update from Asia. Asian studies on cancer chemoprevention. Ann N Y Acad Sci. 889:157–192. 1999. View Article : Google Scholar : PubMed/NCBI
24	Sliva D: Cellular and physiological effects of Ganoderma lucidum (Reishi). Mini Rev Med Chem. 4:873–879. 2004. View Article : Google Scholar : PubMed/NCBI
25	Dudhgaonkar S, Thyagarajan A and Sliva D: Suppression of the inflammatory response by triterpenes isolated from the mushroom Ganoderma lucidum. Int Immunopharmacol. 9:1272–1280. 2009. View Article : Google Scholar : PubMed/NCBI
26	XiaoPing C, Yan C, ShuiBing L, YouGuo C, JianYun L and LanPing L: Free radical scavenging of Ganoderma lucidum polysaccharides and its effect on antioxidant enzymes and immunity activities in cervical carcinoma rats. Carbohydr Polym. 77:389–393. 2009. View Article : Google Scholar
27	Xu Z, Chen X, Zhong Z, Chen L and Wang Y: Ganoderma lucidum polysaccharides: Immunomodulation and potential anti-tumor activities. Am J Chin Med. 39:15–27. 2011. View Article : Google Scholar : PubMed/NCBI
28	Shi M, Zhang Z and Yang Y: Antioxidant and immunoregulatory activity of Ganoderma lucidum polysaccharide (GLP). Carbohydr Polym. 95:200–206. 2013. View Article : Google Scholar : PubMed/NCBI
29	Zhao Z, Zheng X and Fang F: Ganoderma lucidum polysaccharides supplementation attenuates exercise-induced oxidative stress in skeletal muscle of mice. Saudi J Biol Sci. 21:119–123. 2014. View Article : Google Scholar : PubMed/NCBI
30	Yuen JW and Gohel MD: Anticancer effects of Ganoderma lucidum: A review of scientific evidence. Nutr Cancer. 53:11–17. 2005. View Article : Google Scholar : PubMed/NCBI
31	Lin ZB and Zhang HN: Anti-tumor and immunoregulatory activities of Ganoderma lucidum and its possible mechanisms. Acta Pharmacol Sin. 25:1387–1395. 2004.PubMed/NCBI
32	Yen GC and Wu JY: Antioxidant and radical scavenging properties of extracts from Ganoderma tsugae. Food Chem. 65:375–379. 1999. View Article : Google Scholar
33	Kim DH, Shim SB, Kim NJ and Jang IS: Beta-glucuronidase-inhibitory activity and hepatoprotective effect of Ganoderma lucidum. Biol Pharm Bull. 22:162–164. 1999. View Article : Google Scholar : PubMed/NCBI
34	Seto SW, Lam TY, Tam HL, Au AL, Chan SW, Wu JH, Yu PH, Leung GP, Ngai SM, Yeung JH, et al: Novel hypoglycemic effects of Ganoderma lucidum water-extract in obese/diabetic (+db/+db) mice. Phytomedicine. 16:426–436. 2009. View Article : Google Scholar : PubMed/NCBI
35	Nie S, Zhang H, Li W and Xie M: Current development of polysaccharides from Ganoderma: Isolation, structure and bioactivities. Bioactive Carbohydrates and Dietary Fibre. 1:10–20. 2013. View Article : Google Scholar
36	Zheng J, Yang B, Yu Y, Chen Q, Huang T and Li D: Ganoderma lucidum polysaccharides exert anti-hyperglycemic effect on streptozotocin-induced diabetic rats through affecting β-cells. Comb Chem High Throughput Screen. 15:542–550. 2012. View Article : Google Scholar : PubMed/NCBI
37	Gilchrest BA: Photoaging. J Invest Dermatol. 133:E2–E6. 2013. View Article : Google Scholar
38	Wang XY and Bi ZG: UVB-irradiated human keratinocytes and interleukin-1alpha indirectly increase MAP kinase/AP-1 activation and MMP-1 production in UVA-irradiated dermal fibroblasts. Chin Med J (Engl). 119:827–831. 2006.PubMed/NCBI
39	Kao PF, Wang SH, Hung WT, Liao YH, Lin CM and Yang WB: Structural characterization and antioxidative activity of low-molecular-weights beta-1,3-glucan from the residue of extracted Ganoderma lucidum fruiting bodies. J Biomed Biotechnol. 2012:6737642012.PubMed/NCBI
40	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