Extract of Bletilla formosana callus elevates cellular antioxidative activity via Nrf2/HO-1 signaling pathway and inhibits melanogenesis in zebrafish
Tóm tắt
Bletilla species are endangered terrestrial orchids used in natural skin care formulas in Asia for a long history. In order to explore the bioactivity potential of Bletilla species as a cosmetic ingredient in a sustainable resource manner, the callus of Bletilla formosana (Hayata) Schltr. was established and extracted by an eco-friendly supercritical fluid CO2 extraction (SFE-CO2) method. The intracellular reactive oxygen species (ROS) scavenging activity and antioxidation-related gene expression of the callus extract were evaluated in both Hs68 fibroblast cells and HaCaT keratinocytes. The melanogenesis-inhibitory effect was investigated in B16F10 melanoma cells and in an in vivo zebrafish model. The calli of B. formosana were propagated for 10–15 generations with a consistent yellow friable appearance and then subjected to SFE-CO2 extraction to obtain a yellow pasty extract. Obvious intracellular ROS scavenging activity of the extract was detected in both Hs68 and HaCaT cells with 64.30 ± 8.27% and 32.50 ± 4.05% reduction at the concentration of 250 μg/mL. Moreover, marked expression levels of heme oxygenase-1 (HO-1) and (NAD(P)H) quinone oxidoreductase-1 (NQO1) genes were detected after 6-h and 24-h treatments. These results indicate the cellular antioxidative activity of B. formosana callus extract was probably activated via the nuclear factor erythroid 2-related factor 2 (Nrf2)/HO-1 signaling pathway. Melanogenesis-inhibitory effect of the extract was observed in α-MSH stimuli-inducing B16F10 cells with 28.46% inhibition of intracellular melanin content at the concentration of 50 μg/ml. The effect was confirmed with in vivo zebrafish embryos that showed a relative pigmentation density of 80.27 ± 7.98% at the concentration of 100 μg/mL without toxicity. Our results shed light on a sustainable utilization of Bletilla species as a potential ingredient for skin.
Tài liệu tham khảo
He X, Wang X, Fang J, Zhao Z, Huang L, Guo H, Zheng X (2017) Bletilla striata: Medicinal uses, phytochemistry and pharmacological activities. J Ethnopharmacol 195:20–38. https://doi.org/10.1016/j.jep.2016.11.026
Ko C-Y, Chao J, Chen P-Y, Su S-Y, Maeda T, Lin C-Y, Chiang H-C, Huang S-S (2021) Ethnobotanical survey on skin whitening prescriptions of traditional Chinese medicine in Taiwan. Front Pharmacol 12:736370. https://doi.org/10.3389/fphar.2021.736370
Jiang S, Wang M, Jiang L, Xie Q, Yuan H, Yang Y, Zafar S, Liu Y, Jian Y, Li B, Wang W (2021) The medicinal uses of the genus Bletilla in traditional Chinese medicine: a phytochemical and pharmacological review. J Ethnopharmacol 280:114263. https://doi.org/10.1016/j.jep.2021.114263
Li J-Y, Kuang M-T, Yang L, Kong Q-H, Hou B, Liu Z-H, Chi X-Q, Yuan M-Y, Hu J-M, Zhou J (2018) Stilbenes with anti-inflammatory and cytotoxic activity from the rhizomes of Bletilla ochracea Schltr. Fitoterapia 127:74–80. https://doi.org/10.1016/j.fitote.2018.02.007
Zhang M, Shao Q, Xu E, Wang Z, Wang Z, Yin L (2019) Bletilla striata: a review of seedling propagation and cultivation modes. Physiol Mol Biol Plants 25:601–609. https://doi.org/10.1007/s12298-019-00644-w
Sugiura N (1995) The pollination ecology of Bletilla striata (Orchidaceae). Ecol Res 10:171–177. https://doi.org/10.1007/BF02347939
Chung MY, Chung MG (2005) Pollination biology and breeding systems in the terrestrial orchid Bletilla striata. Plant Syst Evol 252:1–9. https://doi.org/10.1007/s00606-004-0256-6
Ribeiro A, Estanqueiro M, Oliveira M, Sousa Lobo J (2015) Main benefits and applicability of plant extracts in skin care products. Cosmetics 2:48–65. https://doi.org/10.3390/cosmetics2020048
Park D, Adhikari D, Pangeni R, Panthi V, Kim H, Park J (2018) Preparation and characterization of callus extract from Pyrus pyrifolia and investigation of its effects on skin regeneration. Cosmetics 5:71. https://doi.org/10.3390/cosmetics5040071
Gomes C, Silva AC, Marques AC, Sousa Lobo J, Amaral MH (2020) Biotechnology applied to cosmetics and aesthetic medicines. Cosmetics 7:33. https://doi.org/10.3390/cosmetics7020033
Sotelo CG, Blanco M, Ramos P, Vázquez JA, Perez-Martin RI (2021) Sustainable sources from aquatic organisms for cosmeceuticals ingredients. Cosmetics 8:48. https://doi.org/10.3390/cosmetics8020048
Barbulova A, Apone F, Colucci G (2014) Plant cell cultures as source of cosmetic active ingredients. Cosmetics 1:94–104. https://doi.org/10.3390/cosmetics1020094
Georgiev V, Slavov A, Vasileva I, Pavlov A (2018) Plant cell culture as emerging technology for production of active cosmetic ingredients. Eng Life Sci 18:779–798. https://doi.org/10.1002/elsc.201800066
Miastkowska M, Sikora E (2018) Anti-aging properties of plant stem cell extracts. Cosmetics 5:55. https://doi.org/10.3390/cosmetics5040055
Tito A, Carola A, Bimonte M, Barbulova A, Arciello S, de Laurentiis F, Monoli I, Hill J, Gibertoni S, Colucci G, Apone F (2011) A tomato stem cell extract, containing antioxidant compounds and metal chelating factors, protects skin cells from heavy metal-induced damages: a tomato cell extract protects skin from heavy metals. Int J Cosmet Sci 33:543–552. https://doi.org/10.1111/j.1468-2494.2011.00668.x
Apone F, Tito A, Carola A, Arciello S, Tortora A, Filippini L, Monoli I, Cucchiara M, Gibertoni S, Chrispeels MJ, Colucci G (2010) A mixture of peptides and sugars derived from plant cell walls increases plant defense responses to stress and attenuates ageing-associated molecular changes in cultured skin cells. J Biotechnol 145:367–376. https://doi.org/10.1016/j.jbiotec.2009.11.021
Pressi G, Bertaiola O, Guarnerio C, Barbieri E, Rigillo G, Governa P, Biagi M, Guzzo F, Semenzato A (2022) In vitro cell culture of Rhus coriaria L.: a standardized phytocomplex rich of gallic acid derivatives with antioxidant and skin repair activity. Cosmetics 9:12. https://doi.org/10.3390/cosmetics9010012
Kim H-R, Kim S, Jie EY, Kim SJ, Ahn WS, Jeong S-I, Yu K-Y, Kim SW, Kim S-Y (2021) Effects of Tiarella polyphylla D. Don callus extract on photoaging in human foreskin fibroblasts Hs68 cells. Natural Product Communications 16:1934578X2110169. https://doi.org/10.1177/1934578X211016970
Pan Y, Li L, Xiao S, Chen Z, Sarsaiya S, Zhang S, ShangGuan Y, Liu H, Xu D (2020) Callus growth kinetics and accumulation of secondary metabolites of Bletilla striata Rchb.f. using a callus suspension culture. PLoS ONE 15:e0220084. https://doi.org/10.1371/journal.pone.0220084
Gamborg OL, Miller RA, Ojima K (1968) Nutrient requirements of suspension cultures of soybean root cells. Exp Cell Res 50:151–158. https://doi.org/10.1016/0014-4827(68)90403-5
Jia Z, Tang M, Wu J (1999) The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chem 64:555–559. https://doi.org/10.1016/S0308-8146(98)00102-2
Braga TM, Rocha L, Chung TY, Oliveira RF, Pinho C, Oliveira AI, Morgado J, Cruz A (2020) Biological activities of gedunin—a limonoid from the Meliaceae family. Molecules 25:493. https://doi.org/10.3390/molecules25030493
Zhang G-M, Deng M-T, Lei Z-H, Wan Y-J, Nie H-T, Wang Z-Y, Fan Y-X, Wang F, Zhang Y-L (2017) Effects of NRF1 on steroidogenesis and apoptosis in goat luteinized granulosa cells. Reproduction 154:111–122. https://doi.org/10.1530/REP-16-0583
Wang P, Liu J, Li Y, Wu S, Luo J, Yang H, Subbiah R, Chatham J, Zhelyabovska O, Yang Q (2010) Peroxisome proliferator-activated receptor δ is an essential transcriptional regulator for mitochondrial protection and biogenesis in adult heart. Circ Res 106:911–919. https://doi.org/10.1161/CIRCRESAHA.109.206185
Rong X, Qiu X, Jiang Y, Li D, Xu J, Zhang Y, Lu Y (2016) Effects of histone acetylation on superoxide dismutase 1 gene expression in the pathogenesis of senile cataract. Sci Rep 6:34704. https://doi.org/10.1038/srep34704
Tsuboi T, Kondoh H, Hiratsuka J, Mishima Y (1998) Enhanced melanogenesis induced by tyrosinase gene-transfer increases boron-uptake and killing effect of boron neutron capture therapy for amelanotic melanoma. Pigment Cell Res 11:275–282. https://doi.org/10.1111/j.1600-0749.1998.tb00736.x
Choi T-Y, Kim J-H, Ko DH, Kim C-H, Hwang J-S, Ahn S, Kim SY, Kim C-D, Lee J-H, Yoon T-J (2007) Zebrafish as a new model for phenotype-based screening of melanogenic regulatory compounds. Pigment Cell Res 20:120–127. https://doi.org/10.1111/j.1600-0749.2007.00365.x
Ziyada AK, Elhussien SA (2008) Physical and chemical characteristics of Citrullus lanatus Var. Colocynthoide seed oil. J Phys Sci 19(2):69–75
Suryawanshi B, Mohanty B (2018) Application of an artificial neural network model for the supercritical fluid extraction of seed oil from Argemone mexicana (L.) seeds. Ind Crops Prod 123:64–74. https://doi.org/10.1016/j.indcrop.2018.06.057
Hu W, Zhang L, Li P, Wang X, Zhang Q, Xu B, Sun X, Ma F, Ding X (2014) Characterization of volatile components in four vegetable oils by headspace two-dimensional comprehensive chromatography time-of-flight mass spectrometry. Talanta 129:629–635. https://doi.org/10.1016/j.talanta.2014.06.010
Ighodaro OM, Akinloye OA (2018) First line defence antioxidants-superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPX): Their fundamental role in the entire antioxidant defence grid. Alexandria J Med 54:287–293. https://doi.org/10.1016/j.ajme.2017.09.001
Ross D, Siegel D (2021) The diverse functionality of NQO1 and its roles in redox control. Redox Biology 41:101950. https://doi.org/10.1016/j.redox.2021.101950
Nguyen T, Sherratt PJ, Nioi P, Yang CS, Pickett CB (2005) Nrf2 controls constitutive and inducible expression of ARE-driven genes through a dynamic pathway involving nucleocytoplasmic shuttling by Keap1. J Biol Chem 280:32485–32492. https://doi.org/10.1074/jbc.M503074200
Loboda A, Damulewicz M, Pyza E, Jozkowicz A, Dulak J (2016) Role of Nrf2/HO-1 system in development, oxidative stress response and diseases: an evolutionarily conserved mechanism. Cell Mol Life Sci 73:3221–3247. https://doi.org/10.1007/s00018-016-2223-0
Ross D, Siegel D (2017) Functions of NQO1 in cellular protection and CoQ10 metabolism and its potential role as a redox sensitive molecular switch. Front Physiol 8:595. https://doi.org/10.3389/fphys.2017.00595
Vasiliou V, Theurer MJ, Puga A, Reuter SF, Nebert DW (1994) Mouse dioxin-inducible NAD(P)H: menadione oxidoreductase. Pharmacogenetics 4:341–348. https://doi.org/10.1097/00008571-199412000-00007
Jaiswal AK (2000) Regulation of genes encoding NAD(P)H:quinone oxidoreductases. Free Radical Biol Med 29:254–262. https://doi.org/10.1016/S0891-5849(00)00306-3
Wahyudi LD, Jeong J, Yang H, Kim J-H (2018) Amentoflavone-induced oxidative stress activates NF-E2-related factor 2 via the p38 MAP kinase-AKT pathway in human keratinocytes. Int J Biochem Cell Biol 99:100–108. https://doi.org/10.1016/j.biocel.2018.04.006
Jiang J (2017) Consideration on development of Bletillae striata based on whitening theory in traditional Chinese medicine. Chinese Traditional and Herbal Drugs 2313–2320
Välimaa A-L, Raitanen J-E, Tienaho J, Sarjala T, Nakayama E, Korpinen R, Mäkinen S, Eklund P, Willför S, Jyske T (2020) Enhancement of Norway spruce bark side-streams: modification of bioactive and protective properties of stilbenoid-rich extracts by UVA-irradiation. Industrial Crops and Products 145:112150. https://doi.org/10.1016/j.indcrop.2020.112150
Luo Y, Wang J, Li S, Wu Y, Wang Z, Chen S, Chen H (2022) Discovery and identification of potential anti-melanogenic active constituents of Bletilla striata by zebrafish model and molecular docking. BMC Complement Med Ther 22:9. https://doi.org/10.1186/s12906-021-03492-y
Gharehmatrossian S, Popov Y, Ghorbanli M, Safaeian S, Iranbakhsh A (2016) Phytochemical and morphological evidences for shikonin production by plant cell cultures of Onosma sericeum Willd. Braz Arch Biol Technol 59:. https://doi.org/10.1590/1678-4324-2016160235
Kamrani Rad SZ, Rameshrad M, Hosseinzadeh H (2017) Toxicology effects of Berberis vulgaris (barberry) and its active constituent, berberine: a review. Iranian Journal of Basic Medical Sciences 20:. https://doi.org/10.22038/ijbms.2017.8676