Restricted accessResearch articleFirst published online 2015-10
Protective Effect of Super-Critical Carbon Dioxide Fluid Extract from Flowers and Buds of Chrysanthemum indicum Linnén Against Ultraviolet-Induced Photo-Aging in Mice
It is known that solar ultraviolet (UV) radiation to human skin causes photo-aging, including increases in skin thickness and wrinkle formation and reduction in skin elasticity. UV radiation induces damage to skin mainly by superfluous reactive oxygen species and chronic low-grade inflammation, which eventually up-regulate the expression of matrix metalloproteinases (MMPs). In this study, the super-critical carbon dioxide extract from flowers and buds of Chrysanthemum indicum Linnén (CISCFE), which has been reported to possess free radical scavenging and anti-inflammatory properties, was investigated for its photo-protective effect by topical application on the skin of mice. Moreover, CISCFE effectively suppressed the UV-induced increase in skin thickness and wrinkle grading in a dose-dependent manner, which was correlated with the inhibition of loss of collagen fiber content and epidermal thickening. Furthermore, we observed that CISCFE could obviously decrease UV-induced skin inflammation by inhibiting the production of inflammatory cytokines (interleukin-1β [IL-1β, IL-6, IL-10, tumor necrosis factor-α), alleviate the abnormal changes of anti-oxidative indicators (superoxide dismutase, catalase, and glutathione peroxidase), and down-regulate the levels of MMP-1 and MMP-3. The results indicated that CISCFE was a novel photo-protective agent from natural resources against UV irradiation.
Get full access to this article
View all access options for this article.
References
1.
SerafiniMR, DetoniCB, Menezes PdosP, Pereira FilhoRN, FortesVS, VieiraMJ, GuterresSS, Cavalcanti de Albuquerque JuniorRL, AraujoAA. UVA-UVB photoprotective activity of topical formulations containing Morinda citrifolia extract. Biomed Res Int, 2014; 2014:587819.
2.
ChungJH. Photoaging in Asians. Photodermatol Photoimmunol Photomed, 2003; 19:109–121.
3.
PillaiS, OresajoC, HaywardJ. 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, 2005; 27:17–34.
4.
MasakiH. Role of antioxidants in the skin: Anti-aging effects. J Dermatol Sci, 2010; 58:85–90.
5.
KondoS. The roles of cytokines in photoaging. J Dermatol Sci, 2000; 23(Suppl 1):S30–S36.
6.
ShahH, MahajanSR. Screening of topical gel containing lycopene and dexamethasone against UV radiation induced photoaging in mice. Biomed Aging Pathol, 2014; 4:303–308.
7.
HallidayGM. Inflammation, gene mutation and photoimmunosuppression in response to UVR-induced oxidative damage contributes to photocarcinogenesis. Mutat Res, 2005; 571:107–120.
8.
Perez-SanchezA, Barrajon-CatalanE, CaturlaN, CastilloJ, Benavente-GarciaO, AlcarazM, MicolV. Protective effects of citrus and rosemary extracts on UV-induced damage in skin cell model and human volunteers. J Photochem Photobiol B, 2014; 136:12–18.
9.
PoddaM, TraberMG, WeberC, YanLJ, PackerL. UV-irradiation depletes antioxidants and causes oxidative damage in a model of human skin. Free Radic Biol Med, 1998; 24:55–65.
10.
SharmaSD, MeeranSM, KatiyarSK. Dietary grape seed proanthocyanidins inhibit UVB-induced oxidative stress and activation of mitogen-activated protein kinases and nuclear factor-kappaB signaling in in vivo SKH-1 hairless mice. Mol Cancer Ther, 2007; 6:995–1005.
11.
Djavaheri-MergnyM, MergnyJL, BertrandF, SantusR, MaziereC, DubertretL, MaziereJC. Ultraviolet-A induces activation of AP-1 in cultured human keratinocytes. FEBS Lett, 1996; 384:92–96.
FisherGJ, VoorheesJJ. Molecular mechanisms of photoaging and its prevention by retinoic acid: Ultraviolet irradiation induces MAP kinase signal transduction cascades that induce Ap-1-regulated matrix metalloproteinases that degrade human skin in vivo. J Investig Dermatol Symp Proc, 1998; 3:61–68.
14.
ZhangJY, ZhangL, JinY, ChengWM, GuoL, ZouYH, PengL, ZhangQ, LiJ. The anti-inflammatory effects of total flavonoids of chrysanthemum indicum and its partial mechanism. Acta Universitis Medicinalis Nahui, 2005; 5:004.
15.
ZhuSY, YangY, YuHD, YuY, ZouGL. Chemical composition and antimicrobial activity of the essential oils of Chrysanthemum indicum. J Ethnopharmacol, 2005; 96:151–158.
16.
ChengW, LiJ, YouT, HuC. Anti-inflammatory and immunomodulatory activities of the extracts from the inflorescence of Chrysanthemum indicum Linne. J Ethnopharmacol, 2005; 101:334–337.
17.
DebnathT, JinHL, HasnatMA, KimY, SamadNB, ParkPJ, LimBO. Antioxidant potential and oxidative dna damage preventive activity of chrysanthemum indicum extracts. J Food Biochem, 2013; 37:440–448.
18.
YoshikawaM, MorikawaT, ToguchidaI, HarimaS, MatsudaH. Medicinal flowers. II. Inhibitors of nitric oxide production and absolute stereostructures of five new germacrane-type sesquiterpenes, kikkanols D, D monoacetate, E, F, and F monoacetate from the flowers of Chrysanthemum indicum L. Chem Pharmaceut Bull Tokyo, 2000; 48:651–656.
19.
CheonMS, YoonT, Lee doY, ChoiG, MoonBC, LeeAY, ChooBK, KimHK. Chrysanthemum indicum Linne extract inhibits the inflammatory response by suppressing NF-kappaB and MAPKs activation in lipopolysaccharide-induced RAW 264.7 macrophages. J Ethnopharmacol, 2009; 122:473–477.
20.
WuXL, LiCW, ChenHM, SuZQ, ZhaoXN, ChenJN, LaiXP, ZhangXJ, SuZR. Anti-inflammatory effect of supercritical-carbon dioxide fluid extract from flowers and buds of Chrysanthemum indicum Linnen. Evid Based Complement Alternat Med, 2013; 2013:413237.
21.
WuXL, FengXX, LiCW, ZhangXJ, ChenZW, ChenJN, LaiXP, ZhangSX, LiYC, SuZR. The protective effects of the supercritical-carbon dioxide fluid extract of Chrysanthemum indicum against lipopolysaccharide-induced acute lung injury in mice via modulating Toll-like receptor 4 signaling pathway. Mediators Inflamm, 2014; 2014:246407.
22.
BissettDL, HannonDP, OrrTV. An animal model of solar-aged skin: Histological, physical, and visible changes in UV-irradiated hairless mouse skin. Photochem Photobiol, 1987; 46:367–378.
23.
TsukaharaK, MoriwakiS, HottaM, FujimuraT, Sugiyama-NakagiriY, SugawaraS, KitaharaT, TakemaY. The effect of sunscreen on skin elastase activity induced by ultraviolet-A irradiation. Biol Pharmaceut Bull, 2005; 28:2302–2307.
24.
IbbotsonSH, MoranMN, NashJF, KochevarIE. The effects of radicals compared with UVB as initiating species for the induction of chronic cutaneous photodamage. J Invest Dermatol, 1999; 112:933–938.
25.
WuYY, TianQ, LiLH, KhanMN, YangXQ, ZhangZM, HuX, ChenSJ. Inhibitory effect of antioxidant peptides derived from Pinctada fucata protein on ultraviolet-induced photoaging in mice. J Funct Foods, 2013; 5; 527–538.
26.
BernsteinEF, LeeJ, BrownDB, YuR, Van ScottE. Glycolic acid treatment increases type I collagen mRNA and hyaluronic acid content of human skin. Dermatol Surg, 2001; 27:429–433.
27.
KongSZ, ShiXG, FengXX, LiWJ, LiuWH, ChenZW, XieJH, LaiXP, ZhangSX, ZhangXJ. Inhibitory effect of hydroxysafflor yellow a on mouse skin photoaging induced by ultraviolet irradiation. Rejuvenation Res, 2013; 16:404–413.
28.
NeumanRE, LoganMA. The determination of collagen and elastin in tissues. J Biol Chem, 1950; 186:549–556.
29.
BaumannL. Skin ageing and its treatment. J Pathol, 2007; 211:241–251.
30.
SerafiniMR, GuimaraesAG, QuintansJS, AraujoAA, NunesPS, Quintans-JuniorLJ. Natural compounds for solar photoprotection: A patent review. Expert Opin Ther Pat, 2015; 1-12.
31.
WarrenR, GartsteinV, KligmanAM, MontagnaW, AllendorfRA, RidderGM. Age, sunlight, and facial skin: A histologic and quantitative study. J Am Acad Dermatol, 1991; 25:751–760.
32.
AgachePG, MonneurC, LevequeJL, De RigalJ. Mechanical properties and Young's modulus of human skin in vivo. Arch Dermatol Res, 1980; 269:221–232.
KimMS, KimYK, ChoKH, ChungJH. Regulation of type I procollagen and MMP-1 expression after single or repeated exposure to infrared radiation in human skin. Mech Ageing Dev, 2006; 127:875–882.
35.
SongKC, ChangTS, LeeH, KimJ, ParkJH, HwangGS. Processed Panax ginseng, Sun Ginseng increases type i collagen by regulating MMP-1 and TIMP-1 expression in human dermal fibroblasts. J Ginseng Res, 2012; 36:61–67.
36.
ChiangHM, ChenHC, LinTJ, ShihIC, WenKC. Michelia alba extract attenuates UVB-induced expression of matrix metalloproteinases via MAP kinase pathway in human dermal fibroblasts. Food Chem Toxicol, 2012; 50:4260–4269.
37.
BlokhinaO, VirolainenE, FagerstedtKV. Antioxidants, oxidative damage and oxygen deprivation stress: A review. Ann Bot, 2003; 91:179–194.
38.
SunS, JiangP, SuW, XiangY, LiJ, ZengL, YangS. Wild chrysanthemum extract prevents UVB radiation-induced acute cell death and photoaging. Cytotechnology, 2014; Jul23. [Epub ahead of print]
39.
FisherGJ, DattaSC, TalwarHS, WangZQ, VaraniJ, KangS, VoorheesJJ. Molecular basis of sun-induced premature skin ageing and retinoid antagonism. Nature, 1996; 379:335–339.
40.
YamamotoY, GaynorRB. Therapeutic potential of inhibition of the NF-kappaB pathway in the treatment of inflammation and cancer. J Clin Invest, 2001; 107:135–142.
41.
BragaPC, Dal SassoM, CuliciM, BianchiT, BordoniL, MarabiniL. Anti-inflammatory activity of thymol: Inhibitory effect on the release of human neutrophil elastase. Pharmacology, 2006; 77:130–136.
42.
JuergensUR, EngelenT, RackeK, StoberM, GillissenA, VetterH. Inhibitory activity of 1,8-cineol (eucalyptol) on cytokine production in cultured human lymphocytes and monocytes. Pulm Pharmacol Ther, 2004; 17:281–287.
43.
WenKC, ChiuHH, FanPC, ChenCW, WuSM, ChangJH, ChiangHM. Antioxidant activity of Ixora parviflora in a cell/cell-free system and in UV-exposed human fibroblasts. Molecules, 2011; 16:5735–5752.
44.
HwangYP, OhKN, YunHJ, JeongHG. The flavonoids apigenin and luteolin suppress ultraviolet A-induced matrix metalloproteinase-1 expression via MAPKs and AP-1-dependent signaling in HaCaT cells. J Dermatol Sci, 2011; 61:23–31.
Supplementary Material
Please find the following supplemental material available below.
For Open Access articles published under a Creative Commons License, all supplemental material carries the same license as the article it is associated with.
For non-Open Access articles published, all supplemental material carries a non-exclusive license, and permission requests for re-use of supplemental material or any part of supplemental material shall be sent directly to the copyright owner as specified in the copyright notice associated with the article.
