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Research article

Food Microbiology and Biotechnology (FMB)  |  Bioactive Compounds and Functional Foods

Antimelanogenic and Antioxidant Effects of Postbioics of Lactobacillus Strains in α-MSH-Induced B16F10 Melanoma Cells via CREB/MITF and MAPKs Signaling Pathway

Hye-Won Lee, Yu-Rim Lee, Kyung-Min Park, Na-Kyoung Lee, and Hyun-Dong Paik*

Department of Food Science and Biotechnology of Animal Resources, Konkuk University, Seoul 05029, Republic of Korea

Correspondence to:
Hyun-Dong Paik,        hdpaik@konkuk.ac.kr
Received: August 9, 2024; Revised: September 6, 2024; Accepted: September 16, 2024

J. Microbiol. Biotechnol. 2024; 34(11): 2279-2289

Published November 28, 2024 https://doi.org/10.4014/jmb.2408.08015

Copyright © The Korean Society for Microbiology and Biotechnology.

Abstract

Abnormal melanin synthesis can lead to severe skin problems. This study investigated the anti-melanogenic effects on α-melanocyte stimulating hormone (α-MSH)-induced B16F10 cells using cell-free supernatants of Lactiplantibacillus plantarum WB326 and Levilactobacillus brevis WB2810. Samples were prepared using 1 mg/ml freeze-dried culture supernatant. Cell viability was assessed using B16F10 cells and MTT assay. Tyrosinase inhibition and melanin content decreased in the samples compared to those treated with α-MSH. This effect was also observed when L-DOPA staining was used under a microscope. Moreover, the mRNA expression levels of microphthalmia-associated transcription factor (MITF), tyrosinase, tyrosinase-related protein (TRP)-1, and TRP-2 decreased in the sample-treated group. Protein expression of the CREB/MITF/MAPK signaling pathway was also reduced. Using HPLC analysis, lactic and acetic acids were detected in the culture supernatants. Finally, the antioxidant effects of the samples were confirmed by comparison with those of Trolox and arbutin. According to the experimental results, their utilization is possible in the fields of functional materials and cosmetic ingredients.

Keywords

Lactobacillus, antimelanogenic, antioxidant, CREB/MITF signaling pathway, MAPK signaling pathway

Graphical Abstract


References

  1. Han JH, Kim HS. 2024. Skin deep: the potential of microbiome cosmetics. J. Microbiol. 62: 181-199.
    Pubmed
  2. Duarte M, Oliveira AL, Oliveira C, Pintado M, Amaro A, Madureira AR. 2022. Current postbiotics in the cosmetic market - An update and development opportunities. Appl. Microbiol. Biotechnol. 106: 5879-5891.
    Pubmed
  3. Dou J, Feng N, Guo F, Chen Z, Liang J, Wang T, et al. 2023. Applications of probiotic constituents in cosmetics. Molecules 28: 6765.
    Pubmed PMC
  4. Huang HC, Wang SS, Tsai TC, Ko WP, Chang TM. 2020. Phoenix dactylifera L. seed extract exhibits antioxidant effects and attenuates melanogenesis in B16F10 murine melanoma cells by downregulating PKA signaling. Antioxidants 9: 1270.
    Pubmed PMC
  5. Chen YM, Su WC, Li C, Shi Y, Chen QX, Zheng J, et al. 2019. Anti-melanogenesis of novel kojic acid derivatives in B16F10 cells and zebrafish. Int. J. Biol. Macromol. 123: 723-731.
    Pubmed
  6. Ribeiro HM, Allegro M, Marto J, Pedras B, Oliveira NG, Paiva A, et al. 2018. Converting spent coffee grounds into bioactive extracts with potential skin antiaging and lightening effects. ACS Sustain. Chem. Eng. 6: 6289-6295.
  7. Wang L, Oh JY, Jayawardena TU, Jeon YJ, Ryu B. 2020. Anti-inflammatory and anti-melanogenesis activities of sulfated polysaccharides isolated from Hizikia fusiforme. Int. J. Biol. Macromol. 142: 545-550.
    Pubmed
  8. Choi H, Yoon JH, Youn K, Jun M. 2022. Decursin prevents melanogenesis by suppressing MITF expression through the regulation of PKA/CREB, MAPKs, and PI3K/Akt/GSK-3β cascades. Biomed. Pharmacother. 147: 112651.
    Pubmed
  9. Choi MH, Jo HG, Yang JH, Ki SH, Shin HJ. 2018. Antioxidative and anti-melanogenic activities of bamboo stems (Phyllostachys nigra variety henosis) via PKA/CREB-mediated MITF downregulation in B16F10 melanoma cells. Int. J. Mol. Sci. 19: 409.
    Pubmed PMC
  10. Meng Z, Oh S. 2021. Antioxidant and antimelanogenic activities of kimchi-derived Limosilactobacillus fermentum JNU532 in B16F10 melanoma cells. J. Microbiol. Biotechnol. 31: 990-998.
    Pubmed PMC
  11. Sangkaew O, Yompakdee C. 2020. Fermented unpolished black rice (Oryza sativa L.) inhibits melanogenesis via ERK, p38, and AKT phosphorylation in B16F10 melanoma cells. J. Microbiol. Biotechnol. 30: 1184.
    Pubmed PMC
  12. Goelzer Neto CF, do Nascimento P, da Silveira VC, de Mattos ABN, Bertol CD. 2022. Natural sources of melanogenic inhibitors: a systematic review. Int. J. Cosmet. Sci. 44: 143-153.
    Pubmed
  13. Lee JE, An BJ, Jo C, Min B, Paik HD, Ahn DU. 2023. The elastase and melanogenesis inhibitory and anti-inflammatory activities of phosvitin phosphopeptides produced using high-temperature and mild-pressure (HTMP) pretreatment and enzyme hydrolysis combinations. Poult. Sci. 102: 102680.
    Pubmed PMC
  14. Park JY, Song MW, Kim KT, Paik HD. 2022. Improved antioxidative, anti-inflammatory, and antimelanogenic effects of fermented hydroponic ginseng with Bacillus strains. Antioxidants 11: 1848.
    Pubmed PMC
  15. Park EH, Bae WY, Kim JY, Kim KT, Paik HD. 2017. Antimelanogenic effects of Inula britannica flower petal extract fermented by Lactobacillus plantarum KCCM 11613P. J. Zhejiang Univ. Sci. B 18: 816.
    PMC
  16. Jung HS, Lee HW, Kim KT, Lee NK, Paik HD. 2023. Anti-inflammatory, antioxidant effects, and antimicrobial effect of Bacillus subtilis P223. Food Sci. Biotechnol. 33: 2179-2187.
    Pubmed PMC
  17. Yu HS, Jang HJ, Lee NK, Paik HD. 2019. Evaluation of the probiotic characteristics and prophylactic potential of Weissella cibaria strains isolated from kimchi. LWT-Food Sci. Technol. 112: 108229.
  18. Bock HJ, Lee NK, Paik HD. 2023. Neuroprotective effects of heat-killed Levilactobacillus brevis KU15152 on H2O2-induced oxidative stress. J. Microbiol. Biotechnol. 33: 1189-1196.
    Pubmed PMC
  19. Cao D, Gong S, Yang J, Li W, Ge Y, Wei Y. 2018. Melanin deposition ruled out as cause of color changes in the red-eared sliders (Trachemys scripta elegans). Comp. Biochem. Physiol. B Biochem. Mol. Biol. 217: 79-85.
    Pubmed
  20. Jiang L, Huang J, Hu Y, Lei L, Ouyang Y, Long Y, et al. 2021. Identification of the ceRNA networks in α-MSH-induced melanogenesis of melanocytes. Aging 13: 2700.
    Pubmed PMC
  21. Wen SY, Wu YS, Liu H, Ng SC, Padma VV, Huang CY, et al. 2023. Paeoniflorin found in Paeonia lactiflora root extract inhibits melanogenesis by regulating melanin‐related signal transduction in B16F10 cells. J. Cosmet. Dermatol. 22: 2824-2830.
    Pubmed
  22. Kamilijiang M, Zang D, Abudukelimu N, Aidarhan N, Liu G, Aisa HA. 2022. Anti-melanogenesis effect of polysaccharide from Saussurea involucrata on forskolin-induced melanogenesis in B16F10 melanoma cells. Nutrients 14: 5044.
    Pubmed PMC
  23. Lee CJ, Park SK, Kang JY, Kim JM, Yoo SK, Han HJ, et al. 2019. Melanogenesis regulatory activity of the ethyl acetate fraction from Arctium lappa L. leaf on α-MSH-induced B16/F10 melanoma cells. Ind. Crops Prod. 138: 111581.
  24. Shin S, Kim M, Song N, Sun S, Choi J, Park K. 2022. Antioxidant and anti-melanogenesis effects of colloidal gold Camellia sinensis L. extracts. Molecules 27: 5593.
    Pubmed PMC
  25. Byun EB, Song HY, Mushtaq S, Kim HM, Kang JA, Yang MS, et al. 2017. Gamma-irradiated luteolin inhibits 3-isobutyl-1methylxanthine-induced melanogenesis through the regulation of CREB/MITF, PI3K/Akt, and ERK pathways in B16BL6 melanoma cells. J. Med. Food 20: 812-819.
    Pubmed
  26. Merecz-Sadowska A, Sitarek P, Kowalczyk T, Zajdel K, Kucharska E, Zajdel R. 2022. The modulation of melanogenesis in B16 cells upon treatment with plant extracts and isolated plant compounds. Molecules 27: 4360.
    Pubmed PMC
  27. Zhou X, Oh JH, Karadeniz F, Yang J, Lee H, Seo Y, et al. 2022. Anti-melanogenesis effect of Rosa rugosa on α-MSH-induced B16F10 cells via PKA/CREB pathway activation. Appl. Sci. 13: 184.
  28. Chung YC, Kim MJ, Kang EY, Kim YB, Kim BS, Park SM, et al. 2019. Anti-melanogenic effects of hydroxyectoine via MITF inhibition by jnk, p38, and akt pathways in B16F10 melanoma cells. Nat. Prod. Commun. 14. doi:10.1177/1934578X19858523.
  29. Park JU, Yang SY, Guo RH, Li HX, Kim YH, Kim YR. 2020. Anti-melanogenic effect of Dendropanax morbiferus and its active components via protein kinase A/Cyclic adenosine monophosphate-responsive binding protein-and p38 mitogen-activated protein kinase-mediated microphthalmia - associated transcription factor downregulation. Front. Pharmacol. 11: 504554.
    Pubmed PMC
  30. Lee MS, Chung YC, Moon SH, Hyun CG. 2021. Lincomycin induces melanogenesis through the activation of MITF via p38 MAPK, AKT, and PKA signaling pathways. J. Appl. Biol. Chem. 64: 323-331.
  31. Pillaiyar T, Manickam M, Jung SH. 2017. Downregulation of melanogenesis: drug discovery and therapeutic options. Drug Discov. Today 22: 282-298.
    Pubmed
  32. Lew LC, Liong MT. 2013. Bioactives from probiotics for dermal health: functions and benefits. J. Appl. Microbiol. 114: 1241-1253.
    Pubmed
  33. Halstead FD, Rauf M, Moiemen NS, Bamford A, Wearn CM, Fraise AP, et al. 2015. The antibacterial activity of acetic acid against biofilm-producing pathogens of relevance to burns patients. PLoS One 10: e0136190.
    Pubmed PMC
  34. Bayazid AB, Jang YA, Jeong SA, Lim BO. 2022. Cypress tree (Chamaecyparis obtusa) Bark extract inhibits melanogenesis through repressing CREB and MITF signaling pathways in α-MSH-stimulated B16F10 cells. Food Agric. Immunol. 33: 498-510.
  35. Hu CH, Ren LQ, Zhou Y, Ye BC. 2019. Characterization of antimicrobial activity of three Lactobacillus plantarum strains isolated from Chinese traditional dairy food. Food Sci. Nutr. 7: 1997-2005.
    Pubmed PMC
  36. Seo HJ, Park AR, Kim S, Yeon J, Yu NH, Ha S, et al. 2019. Biological control of root-knot nematodes by organic acid-producing Lactobacillus brevis WiKim0069 isolated from Kimchi. Plant Pathol. J. 35: 662
    Pubmed PMC

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Article

Research article

J. Microbiol. Biotechnol. 2024; 34(11): 2279-2289

Published online November 28, 2024 https://doi.org/10.4014/jmb.2408.08015

Copyright © The Korean Society for Microbiology and Biotechnology.

Antimelanogenic and Antioxidant Effects of Postbioics of Lactobacillus Strains in α-MSH-Induced B16F10 Melanoma Cells via CREB/MITF and MAPKs Signaling Pathway

Hye-Won Lee, Yu-Rim Lee, Kyung-Min Park, Na-Kyoung Lee, and Hyun-Dong Paik*

Department of Food Science and Biotechnology of Animal Resources, Konkuk University, Seoul 05029, Republic of Korea

Correspondence to:Hyun-Dong Paik,        hdpaik@konkuk.ac.kr

Received: August 9, 2024; Revised: September 6, 2024; Accepted: September 16, 2024

Abstract

Abnormal melanin synthesis can lead to severe skin problems. This study investigated the anti-melanogenic effects on α-melanocyte stimulating hormone (α-MSH)-induced B16F10 cells using cell-free supernatants of Lactiplantibacillus plantarum WB326 and Levilactobacillus brevis WB2810. Samples were prepared using 1 mg/ml freeze-dried culture supernatant. Cell viability was assessed using B16F10 cells and MTT assay. Tyrosinase inhibition and melanin content decreased in the samples compared to those treated with α-MSH. This effect was also observed when L-DOPA staining was used under a microscope. Moreover, the mRNA expression levels of microphthalmia-associated transcription factor (MITF), tyrosinase, tyrosinase-related protein (TRP)-1, and TRP-2 decreased in the sample-treated group. Protein expression of the CREB/MITF/MAPK signaling pathway was also reduced. Using HPLC analysis, lactic and acetic acids were detected in the culture supernatants. Finally, the antioxidant effects of the samples were confirmed by comparison with those of Trolox and arbutin. According to the experimental results, their utilization is possible in the fields of functional materials and cosmetic ingredients.

Keywords: Lactobacillus, antimelanogenic, antioxidant, CREB/MITF signaling pathway, MAPK signaling pathway

References

  1. Han JH, Kim HS. 2024. Skin deep: the potential of microbiome cosmetics. J. Microbiol. 62: 181-199.
    Pubmed
  2. Duarte M, Oliveira AL, Oliveira C, Pintado M, Amaro A, Madureira AR. 2022. Current postbiotics in the cosmetic market - An update and development opportunities. Appl. Microbiol. Biotechnol. 106: 5879-5891.
    Pubmed
  3. Dou J, Feng N, Guo F, Chen Z, Liang J, Wang T, et al. 2023. Applications of probiotic constituents in cosmetics. Molecules 28: 6765.
    Pubmed KoreaMed
  4. Huang HC, Wang SS, Tsai TC, Ko WP, Chang TM. 2020. Phoenix dactylifera L. seed extract exhibits antioxidant effects and attenuates melanogenesis in B16F10 murine melanoma cells by downregulating PKA signaling. Antioxidants 9: 1270.
    Pubmed KoreaMed
  5. Chen YM, Su WC, Li C, Shi Y, Chen QX, Zheng J, et al. 2019. Anti-melanogenesis of novel kojic acid derivatives in B16F10 cells and zebrafish. Int. J. Biol. Macromol. 123: 723-731.
    Pubmed
  6. Ribeiro HM, Allegro M, Marto J, Pedras B, Oliveira NG, Paiva A, et al. 2018. Converting spent coffee grounds into bioactive extracts with potential skin antiaging and lightening effects. ACS Sustain. Chem. Eng. 6: 6289-6295.
  7. Wang L, Oh JY, Jayawardena TU, Jeon YJ, Ryu B. 2020. Anti-inflammatory and anti-melanogenesis activities of sulfated polysaccharides isolated from Hizikia fusiforme. Int. J. Biol. Macromol. 142: 545-550.
    Pubmed
  8. Choi H, Yoon JH, Youn K, Jun M. 2022. Decursin prevents melanogenesis by suppressing MITF expression through the regulation of PKA/CREB, MAPKs, and PI3K/Akt/GSK-3β cascades. Biomed. Pharmacother. 147: 112651.
    Pubmed
  9. Choi MH, Jo HG, Yang JH, Ki SH, Shin HJ. 2018. Antioxidative and anti-melanogenic activities of bamboo stems (Phyllostachys nigra variety henosis) via PKA/CREB-mediated MITF downregulation in B16F10 melanoma cells. Int. J. Mol. Sci. 19: 409.
    Pubmed KoreaMed
  10. Meng Z, Oh S. 2021. Antioxidant and antimelanogenic activities of kimchi-derived Limosilactobacillus fermentum JNU532 in B16F10 melanoma cells. J. Microbiol. Biotechnol. 31: 990-998.
    Pubmed KoreaMed
  11. Sangkaew O, Yompakdee C. 2020. Fermented unpolished black rice (Oryza sativa L.) inhibits melanogenesis via ERK, p38, and AKT phosphorylation in B16F10 melanoma cells. J. Microbiol. Biotechnol. 30: 1184.
    Pubmed KoreaMed
  12. Goelzer Neto CF, do Nascimento P, da Silveira VC, de Mattos ABN, Bertol CD. 2022. Natural sources of melanogenic inhibitors: a systematic review. Int. J. Cosmet. Sci. 44: 143-153.
    Pubmed
  13. Lee JE, An BJ, Jo C, Min B, Paik HD, Ahn DU. 2023. The elastase and melanogenesis inhibitory and anti-inflammatory activities of phosvitin phosphopeptides produced using high-temperature and mild-pressure (HTMP) pretreatment and enzyme hydrolysis combinations. Poult. Sci. 102: 102680.
    Pubmed KoreaMed
  14. Park JY, Song MW, Kim KT, Paik HD. 2022. Improved antioxidative, anti-inflammatory, and antimelanogenic effects of fermented hydroponic ginseng with Bacillus strains. Antioxidants 11: 1848.
    Pubmed KoreaMed
  15. Park EH, Bae WY, Kim JY, Kim KT, Paik HD. 2017. Antimelanogenic effects of Inula britannica flower petal extract fermented by Lactobacillus plantarum KCCM 11613P. J. Zhejiang Univ. Sci. B 18: 816.
    KoreaMed
  16. Jung HS, Lee HW, Kim KT, Lee NK, Paik HD. 2023. Anti-inflammatory, antioxidant effects, and antimicrobial effect of Bacillus subtilis P223. Food Sci. Biotechnol. 33: 2179-2187.
    Pubmed KoreaMed
  17. Yu HS, Jang HJ, Lee NK, Paik HD. 2019. Evaluation of the probiotic characteristics and prophylactic potential of Weissella cibaria strains isolated from kimchi. LWT-Food Sci. Technol. 112: 108229.
  18. Bock HJ, Lee NK, Paik HD. 2023. Neuroprotective effects of heat-killed Levilactobacillus brevis KU15152 on H2O2-induced oxidative stress. J. Microbiol. Biotechnol. 33: 1189-1196.
    Pubmed KoreaMed
  19. Cao D, Gong S, Yang J, Li W, Ge Y, Wei Y. 2018. Melanin deposition ruled out as cause of color changes in the red-eared sliders (Trachemys scripta elegans). Comp. Biochem. Physiol. B Biochem. Mol. Biol. 217: 79-85.
    Pubmed
  20. Jiang L, Huang J, Hu Y, Lei L, Ouyang Y, Long Y, et al. 2021. Identification of the ceRNA networks in α-MSH-induced melanogenesis of melanocytes. Aging 13: 2700.
    Pubmed KoreaMed
  21. Wen SY, Wu YS, Liu H, Ng SC, Padma VV, Huang CY, et al. 2023. Paeoniflorin found in Paeonia lactiflora root extract inhibits melanogenesis by regulating melanin‐related signal transduction in B16F10 cells. J. Cosmet. Dermatol. 22: 2824-2830.
    Pubmed
  22. Kamilijiang M, Zang D, Abudukelimu N, Aidarhan N, Liu G, Aisa HA. 2022. Anti-melanogenesis effect of polysaccharide from Saussurea involucrata on forskolin-induced melanogenesis in B16F10 melanoma cells. Nutrients 14: 5044.
    Pubmed KoreaMed
  23. Lee CJ, Park SK, Kang JY, Kim JM, Yoo SK, Han HJ, et al. 2019. Melanogenesis regulatory activity of the ethyl acetate fraction from Arctium lappa L. leaf on α-MSH-induced B16/F10 melanoma cells. Ind. Crops Prod. 138: 111581.
  24. Shin S, Kim M, Song N, Sun S, Choi J, Park K. 2022. Antioxidant and anti-melanogenesis effects of colloidal gold Camellia sinensis L. extracts. Molecules 27: 5593.
    Pubmed KoreaMed
  25. Byun EB, Song HY, Mushtaq S, Kim HM, Kang JA, Yang MS, et al. 2017. Gamma-irradiated luteolin inhibits 3-isobutyl-1methylxanthine-induced melanogenesis through the regulation of CREB/MITF, PI3K/Akt, and ERK pathways in B16BL6 melanoma cells. J. Med. Food 20: 812-819.
    Pubmed
  26. Merecz-Sadowska A, Sitarek P, Kowalczyk T, Zajdel K, Kucharska E, Zajdel R. 2022. The modulation of melanogenesis in B16 cells upon treatment with plant extracts and isolated plant compounds. Molecules 27: 4360.
    Pubmed KoreaMed
  27. Zhou X, Oh JH, Karadeniz F, Yang J, Lee H, Seo Y, et al. 2022. Anti-melanogenesis effect of Rosa rugosa on α-MSH-induced B16F10 cells via PKA/CREB pathway activation. Appl. Sci. 13: 184.
  28. Chung YC, Kim MJ, Kang EY, Kim YB, Kim BS, Park SM, et al. 2019. Anti-melanogenic effects of hydroxyectoine via MITF inhibition by jnk, p38, and akt pathways in B16F10 melanoma cells. Nat. Prod. Commun. 14. doi:10.1177/1934578X19858523.
  29. Park JU, Yang SY, Guo RH, Li HX, Kim YH, Kim YR. 2020. Anti-melanogenic effect of Dendropanax morbiferus and its active components via protein kinase A/Cyclic adenosine monophosphate-responsive binding protein-and p38 mitogen-activated protein kinase-mediated microphthalmia - associated transcription factor downregulation. Front. Pharmacol. 11: 504554.
    Pubmed KoreaMed
  30. Lee MS, Chung YC, Moon SH, Hyun CG. 2021. Lincomycin induces melanogenesis through the activation of MITF via p38 MAPK, AKT, and PKA signaling pathways. J. Appl. Biol. Chem. 64: 323-331.
  31. Pillaiyar T, Manickam M, Jung SH. 2017. Downregulation of melanogenesis: drug discovery and therapeutic options. Drug Discov. Today 22: 282-298.
    Pubmed
  32. Lew LC, Liong MT. 2013. Bioactives from probiotics for dermal health: functions and benefits. J. Appl. Microbiol. 114: 1241-1253.
    Pubmed
  33. Halstead FD, Rauf M, Moiemen NS, Bamford A, Wearn CM, Fraise AP, et al. 2015. The antibacterial activity of acetic acid against biofilm-producing pathogens of relevance to burns patients. PLoS One 10: e0136190.
    Pubmed KoreaMed
  34. Bayazid AB, Jang YA, Jeong SA, Lim BO. 2022. Cypress tree (Chamaecyparis obtusa) Bark extract inhibits melanogenesis through repressing CREB and MITF signaling pathways in α-MSH-stimulated B16F10 cells. Food Agric. Immunol. 33: 498-510.
  35. Hu CH, Ren LQ, Zhou Y, Ye BC. 2019. Characterization of antimicrobial activity of three Lactobacillus plantarum strains isolated from Chinese traditional dairy food. Food Sci. Nutr. 7: 1997-2005.
    Pubmed KoreaMed
  36. Seo HJ, Park AR, Kim S, Yeon J, Yu NH, Ha S, et al. 2019. Biological control of root-knot nematodes by organic acid-producing Lactobacillus brevis WiKim0069 isolated from Kimchi. Plant Pathol. J. 35: 662
    Pubmed KoreaMed