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Current Pharmaceutical Biotechnology

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ISSN (Print): 1389-2010
ISSN (Online): 1873-4316

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Research Article

Antioxidative and Anti-photooxidative Potential of Interruptins from the Edible Fern Cyclosorus terminans in Human Skin Cells

Author(s): Suriya Chaiwong, Somporn Sretrirutchai, Jong-Hyuk Sung and Sireewan Kaewsuwan*

Volume 25, Issue 4, 2024

Published on: 26 June, 2023

Page: [468 - 476] Pages: 9

DOI: 10.2174/1389201024666230614162152

Price: $65

Abstract

Background: Human skin is exposed daily to oxidative stress factors such as UV light, chemical pollutants, and invading organisms. Reactive oxygen species (ROS) are intermediate molecules that cause cellular oxidative stress. In order to survive in an oxygen-rich environment, all aerobic organisms, including mammals, have evolved enzymatic and non-enzymatic defence systems. The interruptins from an edible fern Cyclosorus terminans possess antioxidative properties and can scavenge intracellular ROS in adipose-derived stem cells.

Objectives: This study aimed to evaluate the antioxidative efficacy of interruptins A, B, and C in cultured human dermal fibroblasts (HDFs) and epidermal keratinocytes (HEKs). Moreover, the anti-photooxidative activity of interruptins in ultraviolet (UV)-exposed skin cells was investigated.

Methods: The intracellular ROS scavenging capacity of interruptins in skin cells was measured by flow cytometry. Their induction effects on gene expression of the endogenous antioxidant enzymes was monitored using real-time polymerase chain reaction.

Results: Interruptins A and B, but not interruptin C, were highly effective in ROS scavenging, particularly in HDFs. Interruptins A and B upregulated gene expression of superoxide dismutase (SOD)1, SOD2, catalase (CAT), and glutathione peroxidase (GPx) in HEKs, but they only induced SOD1, SOD2, and GPx gene expression in HDFs. Additionally, interruptins A and B efficiently suppressed UVA- and UVB-induced ROS generation in both HEKs and HDFs.

Conclusion: The results suggest that these naturally occurring interruptins A and B are potent natural antioxidants and therefore may have the potential in the future of inclusion in antiaging cosmeceutical products.

Keywords: Antioxidant enzyme, coumarin, natural antioxidant, ROS, skin, ultraviolet radiation.

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[1]
Toyoda, M.; Morohashi, M. Pathogenesis of acne. Med. Electron Microsc., 2001, 34(1), 29-40.
[http://dx.doi.org/10.1007/s007950100002] [PMID: 11479771]
[2]
Shah, H.; Rawal Mahajan, S. Photoaging: New insights into its stimulators, complications, biochemical changes and therapeutic interventions. Biomed. Aging Pathol., 2013, 3(3), 161-169.
[http://dx.doi.org/10.1016/j.biomag.2013.05.003]
[3]
Yoshikawa, T.; Naito, Y. What is oxidative stress? Japan Med. Assoc. J., 2002, 45, 271-276.
[PMID: 12147265]
[4]
Valko, M.; Leibfritz, D.; Moncol, J.; Cronin, M.T.D.; Mazur, M.; Telser, J. Free radicals and antioxidants in normal physiological functions and human disease. Int. J. Biochem. Cell Biol., 2007, 39(1), 44-84.
[http://dx.doi.org/10.1016/j.biocel.2006.07.001] [PMID: 16978905]
[5]
MatÉs, J.M.; Pérez-Gómez, C.; De Castro, I.N. Antioxidant enzymes and human diseases. Clin. Biochem., 1999, 32(8), 595-603.
[http://dx.doi.org/10.1016/S0009-9120(99)00075-2] [PMID: 10638941]
[6]
Matés, M. Effects of antioxidant enzymes in the molecular control of reactive oxygen species toxicology. Toxicology, 2000, 153(1-3), 83-104.
[http://dx.doi.org/10.1016/S0300-483X(00)00306-1] [PMID: 11090949]
[7]
Kaewsuwan, S.; Yuenyongsawad, S.; Plubrukarn, A.; Kaewchoothong, A.; Raksawong, A.; Puttarak, P.; Apirug, C. Bioactive interruptins A and B from Cyclosorus terminans: antibacterial, anticancer, stem cell proliferation and ROS scavenging activities. Songklanakarin J. Sci. Technol., 2015, 37, 309-317.
[8]
Chaiwong, S.; Puttaruk, P.; Kaewsuwan, S. Anti Propionibacterium acnes activity, HPLC method validation for simultaneous analysis and extraction of coumarins from the fern Cyclosorus terminans. Lat. Am. J. Pharm., 2018, 31, 1791-1797.
[9]
Chaiwong, S.; Puttarak, P.; Sretrirutchai, S.; Kaewsuwan, S. In vitro anti-inflammatory and antioxidative activities of isolated interruptins from Cyclosorus terminans. Lat. Am. J. Pharm., 2019, 38, 1677-1682.
[10]
Ibbotson, S.H.; Moran, M.N.; Kochevar, I.E.; Nash, J.F. The effects of radicals compared with UVB as initiating species for the induction of chronic cutaneous photodamage. J. Invest. Dermatol., 1999, 112(6), 933-938.
[http://dx.doi.org/10.1046/j.1523-1747.1999.00591.x] [PMID: 10383741]
[11]
Lange, R.W.; Germolec, D.R.; Foley, J.F.; Luster, M.I. Antioxidants attenuate anthralin-induced skin inflammation in BALB/c mice: role of specific proinflammatory cytokines. J. Leukoc. Biol., 1998, 64(2), 170-176.
[http://dx.doi.org/10.1002/jlb.64.2.170] [PMID: 9715255]
[12]
Eruslanov, E.; Kusmartsev, S. Identification of ROS using oxidized DCFDA and flow-cytometry. Methods Mol. Biol., 2010, 594, 57-72.
[http://dx.doi.org/10.1007/978-1-60761-411-1_4] [PMID: 20072909]
[13]
Kim, J.H.; Song, S.Y.; Park, S.G.; Song, S.U.; Xia, Y.; Sung, J.H. Primary involvement of NADPH oxidase 4 in hypoxia-induced generation of reactive oxygen species in adipose-derived stem cells. Stem Cells Dev., 2012, 21(12), 2212-2221.
[http://dx.doi.org/10.1089/scd.2011.0561] [PMID: 22181007]
[14]
ISO 10993-5. Biological evaluation of medical devices-Part 5: tests for in vitro cytotoxicity; 3rd ed; ISO: Geneva, Switzerland, 2009.
[http://dx.doi.org/10.1089/scd.2011.0561] [PMID: 22181007]
[15]
López-García, J.; Lehocký, M. Humpolíček, P.; Sáha, P. HaCaT keratinocytes response on antimicrobial atelocollagen substrates: extent of cytotoxicity, cell viability and proliferation. J. Funct. Biomater., 2014, 5(2), 43-57.
[http://dx.doi.org/10.3390/jfb5020043] [PMID: 24956439]
[16]
Ekanayake-Mudiyanselage, S.; Jensen, J-M.; Proksch, E.; Aschauer, H.; Schmook, F.P.; Meingassner, J.G. Expression of epidermal keratins and the cornified envelope protein involucrin is influenced by permeability barrier disruption. J. Invest. Dermatol., 1998, 111(3), 517-523.
[http://dx.doi.org/10.1046/j.1523-1747.1998.00318.x] [PMID: 9740250]
[17]
Schäfer, M.; Werner, S. The cornified envelope: a first line of defense against reactive oxygen species. J. Invest. Dermatol., 2011, 131(7), 1409-1411.
[http://dx.doi.org/10.1038/jid.2011.119] [PMID: 21673710]
[18]
Akram, N.A.; Shafiq, F.; Ashraf, M. Ascorbic acid-A potential oxidant scavenger and its role in plant development and abiotic stress tolerance. Front. Plant Sci., 2017, 8, 613.
[http://dx.doi.org/10.3389/fpls.2017.00613] [PMID: 28491070]
[19]
Gęgotek, A.; Skrzydlewska, E. Antioxidative and anti-inflammatory activity of ascorbic acid. Antioxidants, 2022, 11(10), 1993.
[http://dx.doi.org/10.3390/antiox11101993] [PMID: 36290716]
[20]
Feidantsis, K.; Georgoulis, I.; Giantsis, I.A.; Michaelidis, B. Treatment with ascorbic acid normalizes the aerobic capacity, antioxidant defence, and cell death pathways in thermally stressed Mytilus galloprovincialis. Comp. Biochem. Physiol. B Biochem. Mol. Biol., 2021, 255, 110611.
[http://dx.doi.org/10.1016/j.cbpb.2021.110611] [PMID: 33965617]
[21]
Oh, C.W.; Li, M.; Kim, E.H.; Park, J.S.; Lee, J.C.; Ham, S.W. Antioxidant and radical scavenging activities of ascorbic acid derivatives conjugated with organogermanium. Bull. Korean Chem. Soc., 2010, 31(12), 3513-3514.
[http://dx.doi.org/10.5012/bkcs.2010.31.12.3513]
[22]
Sharma, O.P.; Bhat, T.K. DPPH antioxidant assay revisited. Food Chem., 2009, 113(4), 1202-1205.
[http://dx.doi.org/10.1016/j.foodchem.2008.08.008]
[23]
Bubols, G.B. Vianna, Dda.R.; Medina-Remon, A.; von Poser, G.; Lamuela-Raventos, R.M.; Eifler-Lima, V.L.; Garcia, S.C. The antioxidant activity of coumarins and flavonoids. Mini Rev. Med. Chem., 2013, 13(3), 318-334.
[PMID: 22876957]
[24]
Foti, M.; Piattelli, M.; Baratta, M.T.; Ruberto, G. Flavonoids, coumarins, and cinnamic acids as antioxidants in a micellar system. Structure-activity relationship. J. Agric. Food Chem., 1996, 44(2), 497-501.
[http://dx.doi.org/10.1021/jf950378u]
[25]
Thuong, P.T.; Hung, T.M.; Ngoc, T.M.; Ha, D.T.; Min, B.S.; Kwack, S.J.; Kang, T.S.; Choi, J.S.; Bae, K. Antioxidant activities of coumarins from Korean medicinal plants and their structure–activity relationships. Phytother. Res., 2010, 24(1), 101-106.
[http://dx.doi.org/10.1002/ptr.2890] [PMID: 19468986]
[26]
Trachootham, D.; Alexandre, J.; Huang, P. Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach? Nat. Rev. Drug Discov., 2009, 8(7), 579-591.
[http://dx.doi.org/10.1038/nrd2803] [PMID: 19478820]
[27]
Ma, Q. Role of nrf2 in oxidative stress and toxicity. Annu. Rev. Pharmacol. Toxicol., 2013, 53(1), 401-426.
[http://dx.doi.org/10.1146/annurev-pharmtox-011112-140320] [PMID: 23294312]
[28]
Shindo, Y.; Witt, E.; Han, D.; Epstein, W.; Packer, L. Enzymic and non-enzymic antioxidants in epidermis and dermis of human skin. J. Invest. Dermatol., 1994, 102(1), 122-124.
[http://dx.doi.org/10.1111/1523-1747.ep12371744] [PMID: 8288904]
[29]
Tan, M.; Li, S.; Swaroop, M.; Guan, K.; Oberley, L.W.; Sun, Y. Transcriptional activation of the human glutathione peroxidase promoter by p53. J. Biol. Chem., 1999, 274(17), 12061-12066.
[http://dx.doi.org/10.1074/jbc.274.17.12061] [PMID: 10207030]
[30]
Wassmann, S.; Wassmann, K.; Nickenig, G. Modulation of oxidant and antioxidant enzyme expression and function in vascular cells. Hypertension, 2004, 44(4), 381-386.
[http://dx.doi.org/10.1161/01.HYP.0000142232.29764.a7] [PMID: 15337734]
[31]
Comhair, S.A.A.; Erzurum, S.C. The regulation and role of extracellular glutathione peroxidase. Antioxid. Redox Signal., 2005, 7(1-2), 72-79.
[http://dx.doi.org/10.1089/ars.2005.7.72] [PMID: 15650397]
[32]
Na, H.K. Kim, E.H.; Jung, J.H.; Lee, H.H.; Hyun, J.W.; Surh, Y.J. (−)-Epigallocatechin gallate induces Nrf2-mediated antioxidant enzyme expression via activation of PI3K and ERK in human mammary epithelial cells. Arch. Biochem. Biophys., 2008, 476(2), 171-177.
[http://dx.doi.org/10.1016/j.abb.2008.04.003] [PMID: 18424257]
[33]
Milani, P.; Gagliardi, S.; Cova, E.; Cereda, C. SOD1 transcriptional and posttranscriptional regulation and its potential implications in ALS. Neurol. Res. Int., 2011, 2011, 1-9.
[http://dx.doi.org/10.1155/2011/458427] [PMID: 21603028]
[34]
Glorieux, C.; Zamocky, M.; Sandoval, J.M.; Verrax, J.; Calderon, P.B. Regulation of catalase expression in healthy and cancerous cells. Free Radic. Biol. Med., 2015, 87, 84-97.
[http://dx.doi.org/10.1016/j.freeradbiomed.2015.06.017] [PMID: 26117330]
[35]
Kaewsuwan, S.; Plubrukarn, A.; Utsintong, M.; Kim, S.H.; Jeong, J.H.; Cho, J.G.; Park, S.G.; Sung, J.H. Interruptin B induces brown adipocyte differentiation and glucose consumption in adipose-derived stem cells. Mol. Med. Rep., 2016, 13(3), 2078-2086.
[http://dx.doi.org/10.3892/mmr.2016.4758] [PMID: 26781331]
[36]
Dai, T.; Fuchs, B.B.; Coleman, J.J.; Prates, R.A.; Astrakas, C.; St Denis, T.G.; Ribeiro, M.S.; Mylonakis, E.; Hamblin, M.R.; Tegos, G.P. Concepts and principles of photodynamic therapy as an alternative antifungal discovery platform. Front. Microbiol., 2012, 3, 120.
[http://dx.doi.org/10.3389/fmicb.2012.00120] [PMID: 22514547]
[37]
Smith, H.L.; Howland, M.C.; Szmodis, A.W.; Li, Q.; Daemen, L.L.; Parikh, A.N.; Majewski, J. Early stages of oxidative stress-induced membrane permeabilization: a neutron reflectometry study. J. Am. Chem. Soc., 2009, 131(10), 3631-3638.
[http://dx.doi.org/10.1021/ja807680m] [PMID: 19275260]
[38]
Yeo, S.K.; Liong, M.T. Effects and applications of sub-lethal ultrasound, electroporation and UV radiations in bioprocessing. Ann. Microbiol., 2013, 63(3), 813-824.
[http://dx.doi.org/10.1007/s13213-012-0559-8]

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