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


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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.

Objective: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.

About the authors

Suriya Chaiwong

Department of Pharmacognosy and Pharmaceutical Botanynd Pharmaceutical Botany, Faculty of Pharmaceutical Sciences, Prince of Songkla University

Email: info@benthamscience.net

Somporn Sretrirutchai

Immunology Uni, Songklanagarind Hospital

Email: info@benthamscience.net

Jong-Hyuk Sung

College of Pharmacy, Yonsei University

Email: info@benthamscience.net

Sireewan Kaewsuwan

Department of Pharmacognosy and Pharmaceutical Botany, Faculty of Pharmaceutical Sciences, Prince of Songkla University

Author for correspondence.
Email: info@benthamscience.net

References

  1. Toyoda, M.; Morohashi, M. Pathogenesis of acne. Med. Electron Microsc., 2001, 34(1), 29-40. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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 structureâ€"activity relationships. Phytother. Res., 2010, 24(1), 101-106. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 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. doi: 10.1007/s13213-012-0559-8

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