Journal of Microbiology and Biotechnology

The Korean Society for Microbiology and Biotechnology (한국미생물·생명공학회)
권호 표지
DOI QR코드

DOI QR Code

Protective Effects of the Postbiotic Levilactobacillus brevis BK3 against H2O2-Induced Oxidative Damage in Skin Cells

  • Young-Sun Lee (Department of Biomedicine and Pharmaceutics, Dong-Eui University) ;
  • Su-Jeong Lee (Department of Biomedicine and Pharmaceutics, Dong-Eui University) ;
  • Won Je Jang (Department of Biomedicine and Pharmaceutics, Dong-Eui University) ;
  • Eun-Woo Lee (Department of Biomedicine and Pharmaceutics, Dong-Eui University)
  • Received : 2024.03.07
  • Accepted : 2024.05.04
  • Published : 2024.07.28
Download PDF
⟨ Previous Next ⟩

Abstract

Postbiotics have various functional effects, such as antioxidant, anti-inflammatory, and anti-obesity. Levilactobacillus brevis BK3, the subject of this study, was derived from lactic acid bacteria isolated from Kimchi, a traditional Korean fermented food. The antioxidant activity of BK3 was confirmed through the measurements of 2,2-diphenyl-1-picryl-hydrazyl (DPPH), 2,2'-azino-bis (3-ethylbenzothiazoline-6-sulfonic acid) (ABTS), and total antioxidant capacity (TAC). The wrinkle improvement effect was validated by assessing elastase inhibitory activity and collagenase inhibitory activity. The intracellular activity was confirmed using human keratinocytes (HaCaT) and human fibroblasts (HFF-1). BK3 protects skin cells from oxidative stress induced by H2O2 and reduces intracellular reactive oxygen species (ROS) production. In addition, the expressions of the antioxidant genes superoxide dismutase (SOD), catalase (CAT), and glutathione peroxidase (GPx) were upregulated. Meanwhile, matrix metalloproteinase-1 (MMP-1) and collagen type I alpha 1 (COL1A1), involved in collagen degradation and synthesis, were significantly regulated. These results suggest the possibility of utilizing BK3 as a functional ingredient with antioxidant and wrinkle-improving effects.

Keywords

References

  1. Salminen S, Collado MC, Endo A, Hill C, Lebeer S, Quigley EMM, et al. 2021. The international scientific association of probiotics and prebiotics (ISAPP) consensus statement on the definition and scope of postbiotics. Nat. Rev. Gastroenterol. Hepatol. 18: 649-667.a  https://doi.org/10.1038/s41575-021-00440-6
  2. Aggarwal S, Sabharwal V, Kaushik P, Joshi A, Aayushi A, Suri M. 2022. Postbiotics: from emerging concept to application. Front. Sustain. Food Syst. 6. https://doi.org/10.3389/fsufs.2022.887642 
  3. Wegh CAM, Geerlings SY, Knol J, Roeselers G, Belzer C. 2019. Postbiotics and their potential applications in early life nutrition and beyond. Int. J. Mol. Sci. 20: 4673. 
  4. Zolkiewicz J, Marzec A, Ruszczynski M, Feleszko W. 2020. Postbiotics-a step beyond pre- and probiotics. Nutrients 12: 2189. 
  5. Im AR, Lee B, Kang DJ, Chae S. 2019. Protective effects of tyndallized Lactobacillus acidophilus IDCC 3302 against UVB-induced photodamage to epidermal keratinocytes cells. Int. J. Mol. Med. 43: 2499-2506.  https://doi.org/10.3892/ijmm.2019.4161
  6. Choi WS. 2013. Whitening effects of Lactobacillus rhamnosus associated with its antioxidative activities. Microbiol. Biotechnol. Lett. 41: 183-189.  https://doi.org/10.4014/kjmb.1302.02006
  7. Tsai WH, Chou CH, Chiang YJ, Lin CG, Lee CH. 2021. Regulatory effects of Lactobacillus plantarum-GMNL6 on human skin health by improving skin microbiome. Int. J. Med. Sci. 18: 1114-1120.  https://doi.org/10.7150/ijms.51545
  8. Kim JY, Park BK, Park HJ, Park YH, Kim BO, Pyo S. 2013. Atopic dermatitis-mitigating effects of new Lactobacillus strain, Lactobacillus sakei probio 65 isolated from Kimchi. J. Appl. Microbiol. 115: 517-526.  https://doi.org/10.1111/jam.12229
  9. Ogawa M, Saiki A, Matsui Y, Tsuchimoto N, Nakakita Y, Takata Y, et al. 2016. Effects of oral intake of heat-killed Lactobacillus brevis SBC8803 (SBL88) on dry skin conditions: a randomized, double-blind, placebo-controlled study. Exp. Ther. Med. 12: 3863-3872.  https://doi.org/10.3892/etm.2016.3862
  10. Brandi J, Cheri S, Manfredi M, Di Carlo C, Vita Vanella V, Federici F, et al. 2020. Exploring the wound healing, anti-inflammatory, anti-pathogenic and proteomic effects of lactic acid bacteria on keratinocytes. Sci. Rep. 10: 11572. 
  11. Walters KA, Michael SR. 2002. The structure and function of skin. Dermatol. Transdermal formulations. 
  12. De Almeida CV, Antiga E, Lulli M. 2023. Oral and topical probiotics and postbiotics in skincare and dermatological therapy: a concise review. Microorganisms 11: 1420. 
  13. Dabrowska AK, Spano F, Derler S, Adlhart C, Spencer ND, Rossi RM. 2018. The relationship between skin function, barrier properties, and body-dependent factors. Skin Res. Technol. 24: 165-174.  https://doi.org/10.1111/srt.12424
  14. He YL, Lin L, Zheng H, Mo Y, Zhou C, Sun S, et al. 2022. Potential anti-skin aging effect of a peptide AYAPE isolated from Isochrysis zhanjiangensis on UVB-induced HaCaT cells and H2O2-induced BJ cells. J. Photochem. Photobiol. B. 233: 112481. 
  15. Rinnerthaler M, Bischof J, Streubel MK, Trost A, Richter K. 2015. Oxidative stress in aging human skin. Biomolecules 5: 545-589.  https://doi.org/10.3390/biom5020545
  16. Lee H, Yeom M, Shin S, Jeon K, Park D, Jung E. 2019. Protective effects of aqueous extract of Mentha suaveolens against oxidative stress-induced damages in human keratinocyte HaCaT cells. Evid Based Complement. Alternat. Med. 2019: 5045491. 
  17. Kim G, Han DW, Lee JH. 2023. The cytoprotective effects of baicalein on H2O2-induced ROS by maintaining mitochondrial homeostasis and cellular tight junction in HaCaT keratinocytes. Antioxidants (Basel) 12: 902. 
  18. Nakai K, Tsuruta D. 2021. What are reactive oxygen species, free radicals, and oxidative stress in skin diseases? Int. J. Mol. Sci. 22: 10799. 
  19. Park C, Lee H, Noh JS, Jin CY, Kim GY, Hyun JW, et al. 2020. Hemistepsin A protects human keratinocytes against hydrogen peroxide-induced oxidative stress through activation of the Nrf2/HO-1 signaling pathway. Arch. Biochem. Biophys. 691: 108512. 
  20. Papaccio F, A DA, Caputo S, Bellei B. 2022. Focus on the contribution of oxidative stress in skin aging. Antioxidants (Basel) 11: 1121. 
  21. Das D, Goyal A. 2015. Antioxidant activity and γ-aminobutyric acid (GABA) producing ability of probiotic Lactobacillus plantarum DM5 isolated from Marcha of Sikkim. LWT Food Sci. Technol. 61: 263-268.  https://doi.org/10.1016/j.lwt.2014.11.013
  22. Afify AEMM, Romeilah RM, Shaimaa IM, Hussein MM. 2012. Antioxidant activity and biological evaluations of probiotic bacteria strains. Int. J. Acad. Res. 4: 124-137.  https://doi.org/10.7813/2075-4124.2012/4-6/A.19
  23. Shirzad M, Hamedi J, Motevaseli E, Modarressi MH. 2018. Anti-elastase and anti-collagenase potential of Lactobacilli exopolysaccharides on human fibroblast. Artif. Cells Nanomed. Biotechnol. 46: 1051-1061.  https://doi.org/10.1080/21691401.2018.1443274
  24. Xu J, Feng Y, Song G, Gong Q, Yin L, Hu Y, et al. 2018. Tacrolimus reverses UVB irradiation-induced epidermal langerhans cell reduction by inhibiting TNF-alpha secretion in keratinocytes via regulation of NF-kappaB/p65. Front. Pharmacol. 9: 67. 
  25. Chaiprasongsuk A, Janjetovic Z, Kim TK, Jarrett SG, D'Orazio JA, Holick MF, et al. 2019. Protective effects of novel derivatives of vitamin D3 and lumisterol against UVB-induced damage in human keratinocytes involve activation of Nrf2 and p53 defense mechanisms. Redox Biol. 24: 101206. 
  26. Camillo L, Grossini E, Farruggio S, Marotta P, Gironi LC, Zavattaro E, et al. 2022. Alpha-tocopherol protects human dermal fibroblasts by modulating nitric oxide release, mitochondrial function, redox status, and inflammation. Skin Pharmacol. Physiol. 35: 1-12.  https://doi.org/10.1159/000517204
  27. Cheng W, An Q, Zhang J, Shi X, Wang C, Li M, et al. 2022. Protective effect of ectoin on UVA/H2O2-induced oxidative damage in human skin fibroblast cells. Appl. Sci. 12: 8531. 
  28. Zi Y, Zhang B, Jiang B, Yang X, Liang Z, Liu W, et al. 2018. Antioxidant action and protective and reparative effects of lentinan on oxidative damage in HaCaT cells. J. Cosmet. Dermatol. 17: 1108-1114.  https://doi.org/10.1111/jocd.12488
  29. Kim H, Jeon B, Kim WJ, Chung DK. 2020. Effect of paraprobiotic prepared from Kimchi-derived Lactobacillus plantarum K8 on skin moisturizing activity in human keratinocyte. J. Funct. Foods 75: 104244. 
  30. Jung YO, Jeong H, Cho Y, Lee EO, Jang HW, Kim J, et al. 2019. Lysates of a probiotic, Lactobacillus rhamnosus, can improve skin barrier function in a reconstructed human epidermis model. Int. J. Mol. Sci. 20: 4289. 
  31. Wu J, Zhang F, Yu H, Qi S, Wu Y, Xiao W. 2023. Anti-melanogenic and antioxidant activity of Bifidobacterium longum strain ZJ1 extracts, isolated from a Chinese Centenarian. Int. J. Mol. Sci. 24: 12810. 
  32. Song MW, Jang HJ, Kim KT, Paik HD. 2019. Probiotic and antioxidant properties of novel Lactobacillus brevis KCCM 12203P isolated from Kimchi and evaluation of immune-stimulating activities of its heat-killed cells in RAW 264.7 cells. J. Microbiol. Biotechnol. 29: 1894-1903.  https://doi.org/10.4014/jmb.1907.07081
  33. Njus D, Kelley PM, Tu YJ, Schlegel HB. 2020. Ascorbic acid: the chemistry underlying its antioxidant properties. Free Radic. Biol. Med. 159: 37-43.  https://doi.org/10.1016/j.freeradbiomed.2020.07.013
  34. Oehlke K, Heins A, Stockmann H, Sonnichsen F, Schwarz K. 2011. New insights into the antioxidant activity of Trolox in o/w emulsions. Food Chem. 124: 781-787.  https://doi.org/10.1016/j.foodchem.2010.06.095
  35. Lee W, Im HC, Lee YB, Choi J. 2024. Protective effect of soy germ-fermented postbiotics derived from Lacticaseibacillus paracasei DCF0429 (SGPB-DCF0429) in human reconstituted skin. J. Funct. Foods 113. https://doi.org/10.1016/j.jff.2024.106023. 
  36. Merzza HA, Idris AM, Chwen LT, Ling FH. 2021. Antioxidant activities of postbiotics produced by several lactobacillus plantarum strains using reconstituted media. Sci. J. Univ. Benghazi. 34: 150-153.  https://doi.org/10.37376/sjuob.v34i2.3224
  37. Zuliani T, Denis V, Noblesse E, Schnebert S, Andre P, Dumas M, et al. 2005. Hydrogen peroxide-induced cell death in normal human keratinocytes is differentiation dependent. Free Radic. Biol. Med. 38: 307-316.  https://doi.org/10.1016/j.freeradbiomed.2004.09.021
  38. Barbouti A, Nousis L, Tenopoulou M, Galaris D. 2002. DNA damage and apoptosis in hydrogen peroxide-exposed Jurkat cells: bolus addition versus continuous generation of H2O2. Free Radic. Biol. Med. 33: 691-702.  https://doi.org/10.1016/S0891-5849(02)00967-X
  39. Yang Y, Cheng JZ, Singhal SS, Saini M, Pandya U, Awasthi S, et al. 2001. Role of glutathione S-transferases in protection against lipid peroxidation. Overexpression of hGSTA2-2 in K562 cells protects against hydrogen peroxide-induced apoptosis and inhibits JNK and caspase 3 activation. J. Biol. Chem. 276: 19220-19230.  https://doi.org/10.1074/jbc.M100551200
  40. Letsiou S, Kalliampakou K, Gardikis K, Mantecon L, Infante C, Chatzikonstantinou M, et al. 2017. Skin protective effects of Nannochloropsis gaditana extract on H2O2-stressed human dermal fibroblasts. Front. Mar. Sci. 4. doi.org/10.3389/fmars.2017.00221. 
  41. Pillai S, Oresajo C, Hayward J. 2005. 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. 27: 17-34.  https://doi.org/10.1111/j.1467-2494.2004.00241.x
  42. Masaki H. 2010. Role of antioxidants in the skin: anti-aging effects. J. Dermatol. Sci. 58: 85-90.  https://doi.org/10.1016/j.jdermsci.2010.03.003
  43. Godic A, Poljsak B, Adamic M, Dahmane R. 2014. The role of antioxidants in skin cancer prevention and treatment. Oxid. Med. Cell Longev. 2014: 860479. 
  44. Oresajo C, Pillai S, Manco M, Yatskayer M, McDaniel D. 2012. Antioxidants and the skin: understanding formulation and efficacy. Dermatol. Ther. 25: 252-259.  https://doi.org/10.1111/j.1529-8019.2012.01505.x
  45. Ighodaro OM, Akinloye OA. 2019. 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
  46. Md Jaffri J. 2023. Reactive oxygen species and antioxidant system in selected skin disorders. Malays J. Med. Sci. 30: 7-20.  https://doi.org/10.21315/mjms2023.30.1.2
  47. Glorieux C, Calderon PB. 2017. Catalase, a remarkable enzyme: targeting the oldest antioxidant enzyme to find a new cancer treatment approach. Biol. Chem. 398: 1095-1108.  https://doi.org/10.1515/hsz-2017-0131
  48. Lubos E, Loscalzo J, Handy DE. 2011. Glutathione peroxidase-1 in health and disease: from molecular mechanisms to therapeutic opportunities. Antioxid. Redox Signal. 15: 1957-1997.  https://doi.org/10.1089/ars.2010.3586
  49. Xu J, Zhang X, Song Y, Zheng B, Wen Z, Gong M, et al. 2022. Heat-killed Lacticaseibacillus paracasei ameliorated UVB-induced oxidative damage and photoaging and its underlying mechanisms. Antioxidants (Basel) 11: 1875. 
  50. Ahn SH, Lee GW, Kwon DS, Shin HJ, Cho YH. 2021. Anti-aging effects of black ginseng extract via H2O2-induced oxidative stress regulation in human keratinocytes. J. Korean Soc. Food Sci. Nutr. 50: 1019-1029.  https://doi.org/10.3746/jkfn.2021.50.10.1019
  51. Kar S, Subbaram S, Carrico PM, Melendez JA. 2010. Redox-control of matrix metalloproteinase-1: a critical link between free radicals, matrix remodeling and degenerative disease. Respir. Physiol. Neurobiol. 174: 299-306.  https://doi.org/10.1016/j.resp.2010.08.019
  52. da Silva Vale A, de Melo Pereira GV, de Oliveira AC, de Carvalho Neto DP, Herrmann LW, Karp SG, et al. 2023. Production, formulation, and application of postbiotics in the treatment of skin conditions. Fermentation 9: 264. 
  53. Cui H, Guo C, Wang Q, Feng C, Duan Z. 2022. A pilot study on the efficacy of topical lotion containing anti-acne postbiotic in subjects with mild -to -moderate acne. Front. Med (Lausanne) 9: 1064460. 
  54. Majeed M, Majeed S, Nagabhushanam K, Mundkur L, Rajalakshmi H, Shah K, et al. 2020. Nove topical application of a postbiotic, LactoSporin, in mild to moderate acne: A randomized, comparative clinical study to evaluate its efficacy, tolerability and safety. Cosmetics 7: 70.