Journal of Microbiology and Biotechnology

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

DOI QR Code

Effects of Hahella chejuensis-Derived Prodigiosin on UV-Induced ROS Production, Inflammation and Cytotoxicity in HaCaT Human Skin Keratinocytes

  • Lee, Jieun (Environmental Diseases Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB)) ;
  • Kim, Hyun Ju (Department of Systems Biotechnology, Chung-Ang University) ;
  • Lee, Sang Jun (Department of Systems Biotechnology, Chung-Ang University) ;
  • Lee, Moo-Seung (Environmental Diseases Research Center, Korea Research Institute of Bioscience and Biotechnology (KRIBB))
  • Received : 2020.11.16
  • Accepted : 2020.12.20
  • Published : 2021.03.28
Download PDF
⟨ Previous Next ⟩

Abstract

Prodigiosins, which are natural tripyrrole red pigments and synthetic derivatives, reportedly have multiple biological effects mainly on various types of cancer cells. However, the effects of bacterial prodigiosin on non-cancerous HaCaT human skin keratinocytes have not been reported. Therefore, the present study aimed to investigate the functional activities of prodigiosin derived from cultures of the bacterium Hahella chejuensis in HaCaT cells. Cell viability, the cell proliferation rate, and reactive oxygen species (ROS) production in vitro were assayed following treatment of HaCaT cells with prodigiosin. Prodigiosin did not cause cytotoxicity and notably increased proliferation of HaCaT cells. Furthermore, prodigiosin reduced ultraviolet (UV) irradiation-induced ROS production and the inflammatory response in HaCaT cells. More importantly, prodigiosin reduced matrix metalloproteinase-9 expression and increased collagen synthesis in UV-irradiated HaCaT cells, demonstrating that it elicits anti-aging effects. In conclusion, our results reveal that H. chejuensis-derived prodigiosin is a potential natural product to develop functional cosmetic ingredients.

Keywords

References

  1. Demain AL. 1992. Microbial secondary metabolism: a new theoretical frontier for academia, a new opportunity for industry. Ciba Found Symp. 171: 3-16; discussion 16-23.
  2. Singh BP, Rateb ME, Rodriguez-Couto S, Polizeli M, Li WJ. 2019. Editorial: microbial secondary metabolites: recent developments and technological challenges. Front. Microbiol. 10: 914. https://doi.org/10.3389/fmicb.2019.00914
  3. Sekurova ON, Schneider O, Zotchev SB. 2019. Novel bioactive natural products from bacteria via bioprospecting, genome mining and metabolic engineering. Microb. Biotechnol. 12: 828-844. https://doi.org/10.1111/1751-7915.13398
  4. Darshan N, Manonmani HK. 2015. Prodigiosin and its potential applications. J. Food Sci. Technol. 52: 5393-5407. https://doi.org/10.1007/s13197-015-1740-4
  5. Lee HK, Chun J, Moon EY, Ko SH, Lee DS, Lee HS, et al. 2001. Hahella chejuensis gen. nov., sp. nov., an extracellular-polysaccharide-producing marine bacterium. Int. J. Syst. Evol. Microbiol. 51(Pt 2): 661-666. https://doi.org/10.1099/00207713-51-2-661
  6. Abbas AK, Lichtman AH, Pillai S. 2014. Cellular and Molecular Immunology, pp. 285, 305-308. 8th Ed. Elsevier, Philadelphia, Pennsylvania. USA.
  7. Zhu X, Li N, Wang Y, Ding L, Chen H, Yu Y, et al. 2017. Protective effects of quercetin on UVB irradiation induced cytotoxicity through ROS clearance in keratinocyte cells. Oncol. Rep. 37: 209-218. https://doi.org/10.3892/or.2016.5217
  8. D'Orazio J, Jarrett S, Amaro-Ortiz A, Scott T. 2013. UV radiation and the skin. Int. J. Mol. Sci. 14: 12222-12248. https://doi.org/10.3390/ijms140612222
  9. Suryawanshi RK, Patil CD, Borase HP, Narkhede CP, Stevenson A, Hallsworth JE, et al. 2015. Towards an understanding of bacterial metabolites prodigiosin and violacein and their potential for use in commercial sunscreens. Int. J. Cosmet. Sci. 37: 98-107. https://doi.org/10.1111/ics.12175
  10. Lin TK, Zhong L, Santiago JL. 2017. Anti-inflammatory and skin barrier repair effects of topical application of some plant oils. Int. J. Mol. Sci. 19: 70. https://doi.org/10.3390/ijms19010070
  11. Wilson VG. 2014. Growth and differentiation of HaCaT keratinocytes. Methods Mol. Biol. 1195: 33-41. https://doi.org/10.1007/7651_2013_42
  12. Peyrat LA, Tsafantakis N, Georgousaki K, Ouazzani J, Genilloud O, Trougakos IP, et al. 2019. Terrestrial microorganisms: cell factories of bioactive molecules with skin protecting applications. Molecules 24: 1836. https://doi.org/10.3390/molecules24091836
  13. Jeong H, Yim JH, Lee C, Choi SH, Park YK, Yoon SH, et al. 2005. Genomic blueprint of Hahella chejuensis, a marine microbe producing an algicidal agent. Nucleic Acids Res. 33: 7066-7073. https://doi.org/10.1093/nar/gki1016
  14. Tyagi N, Bhardwaj A, Srivastava SK, Arora S, Marimuthu S, Deshmukh SK, et al. 2015. Development and characterization of a novel in vitro progression model for UVB-induced skin carcinogenesis. Sci. Rep. 5: 13894. https://doi.org/10.1038/srep13894
  15. Gazel A, Ramphal P, Rosdy M, De Wever B, Tornier C, Hosein N, et al. 2003. Transcriptional profiling of epidermal keratinocytes: comparison of genes expressed in skin, cultured keratinocytes, and reconstituted epidermis, using large DNA microarrays. J. Invest. Dermatol. 121: 1459-1468. https://doi.org/10.1111/j.1523-1747.2003.12611.x
  16. Ando K, Ajchenbaum-Cymbalista F, Griffin JD. 1993. Regulation of G1/S transition by cyclins D2 and D3 in hematopoietic cells. Proc. Natl. Acad. Sci. USA 90: 9571-9575. https://doi.org/10.1073/pnas.90.20.9571
  17. Cooper GM, Hausman RE. 2009. The Cell: A Molecular Approach, pp. 653-659. 5th Ed. Sinauer Associates, Inc., Sunderland, Pennsylvania. USA.
  18. Montaner B, Navarro S, Pique M, Vilaseca M, Martinell M, Giralt E, et al. 2000. Prodigiosin from the supernatant of Serratia marcescens induces apoptosis in haematopoietic cancer cell lines. Br. J. Pharmacol. 131: 585-593. https://doi.org/10.1038/sj.bjp.0703614
  19. Hsieh HY, Shieh JJ, Chen CJ, Pan MY, Yang SY, Lin SC, et al. 2012. Prodigiosin down-regulates SKP2 to induce p27(KIP1) stabilization and antiproliferation in human lung adenocarcinoma cells. Br. J. Pharmacol. 166: 2095-2108. https://doi.org/10.1111/j.1476-5381.2012.01921.x
  20. Li D, Liu J, Wang X, Kong D, Du W, Li H, et al. 2018. Biological potential and mechanism of prodigiosin from Serratia marcescens Subsp. lawsoniana in human choriocarcinoma and prostate cancer cell lines. Int. J. Mol. Sci. 19: 3465. https://doi.org/10.3390/ijms19113465
  21. Dunaway S, Odin R, Zhou L, Ji L, Zhang Y, Kadekaro AL. 2018. Natural antioxidants: multiple mechanisms to protect skin from solar radiation. Front. Pharmacol. 9: 392. https://doi.org/10.3389/fphar.2018.00392
  22. Braun S, Hanselmann C, Gassmann MG, auf dem Keller U, Born-Berclaz C, Chan K, et al. 2002. Nrf2 transcription factor, a novel target of keratinocyte growth factor action which regulates gene expression and inflammation in the healing skin wound. Mol. Cell. Biol. 22: 5492-5505. https://doi.org/10.1128/MCB.22.15.5492-5505.2002
  23. Ma Q. 2013. Role of nrf2 in oxidative stress and toxicity. Annu. Rev. Pharmacol. Toxicol. 53: 401-426. https://doi.org/10.1146/annurev-pharmtox-011112-140320
  24. Edgar S, Hopley B, Genovese L, Sibilla S, Laight D, Shute J. 2018. Effects of collagen-derived bioactive peptides and natural antioxidant compounds on proliferation and matrix protein synthesis by cultured normal human dermal fibroblasts. Sci. Rep. 8: 10474. https://doi.org/10.1038/s41598-018-28492-w
  25. Rittie L, Fisher GJ. 2002. UV-light-induced signal cascades and skin aging. Ageing Res. Rev. 1: 705-720. https://doi.org/10.1016/S1568-1637(02)00024-7
  26. Pittayapruek P, Meephansan J, Prapapan O, Komine M, Ohtsuki M. 2016. Role of matrix metalloproteinases in photoaging and photocarcinogenesis. Int. J. Mol. Sci. 17: 868. https://doi.org/10.3390/ijms17060868
  27. Freitas-Rodriguez S, Folgueras AR, Lopez-Otin C. 2017. The role of matrix metalloproteinases in aging: Tissue remodeling and beyond. Biochim. Biophys. Acta. Mol. Cell. Res. 1864 (11 Pt A): 2015-2025. https://doi.org/10.1016/j.bbamcr.2017.05.007
  28. Noske K. 2018. Secreted immunoregulatory proteins in the skin. J. Dermatol. Sci. 89: 3-10. https://doi.org/10.1016/j.jdermsci.2017.10.008
  29. Nedoszytko B, Sokolowska-Wojdylo M, Ruckemann-Dziurdzinska K, Roszkiewicz J, Nowicki RJ. 2014. Chemokines and cytokines network in the pathogenesis of the inflammatory skin diseases: atopic dermatitis, psoriasis and skin mastocytosis. Postepy. Dermatol. Alergol. 31: 84-91.
  30. Altmeyer P, Hoffmann K, Stucker M. 1997. Skin Cancer and UV Radiation, pp. 219-226. 1st Ed. Springer, Berlin, Heidelberg.
  31. Collier AE, Spandau DF, Wek RC. 2018. Translational control of a human CDKN1A mRNA splice variant regulates the fate of UVB-irradiated human keratinocytes. Mol. Biol. Cell. 29: 29-41. https://doi.org/10.1091/mbc.E17-06-0362

Cited by

  1. Comparative study of the photo‑protective and anti‑melanogenic properties of gomisin D, J and O vol.25, pp.1, 2021, https://doi.org/10.3892/mmr.2021.12524