Skip to main content
SpringerLink
Log in

Tremella fuciformis polysaccharides alleviates UV-provoked skin cell damage via regulation of thioredoxin interacting protein and thioredoxin reductase 2

  • Original Papers
  • Published:
Photochemical & Photobiological Sciences Aims and scope Submit manuscript

Abstract

Introduction

Skin is exposed to a wide range of environmental risk factors including ultraviolet (UV) and all kinds of pollutants. Excessive UV exposure contributes to many disorders, such as photoaging, skin inflammation, and carcinogenesis. Previous studies have shown that Tremella fuciformis polysaccharides (TFPS) have protective effects on oxidative stress in cells, but the specific protective mechanism has not been clarified.

Methods

To determine the effects of TFPS on UV-irritated human skin, we conducted a variety of studies, including Cell Counting Kit-8 (CCK-8), trypan blue, Western blot, apoptosis assays, reactive oxygen species (ROS) detection in primary skin keratinocytes, and chronic UV-irradiated mouse model.

Results

We first determined that TFPS protects human skin keratinocytes against UV radiation-induced apoptosis and ROS production. Moreover, TFPS regulates thioredoxin interacting protein (TXNIP) and thioredoxin reductase 2 (TXNRD2) levels in primary skin keratinocytes for photoprotection. Last, we found that topical TFPS treatment could alleviate the UV-induced skin damage in chronic UV-irradiated mouse model.

Conclusion

Collectively, our work indicates the beneficial role of TFPS in UV-induced skin cell damage and provides a novel therapeutic reagent to prevent or alleviate the progress of photoaging and other UV-provoked skin diseases.

Graphical abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Breitkreutz, D., Mirancea, N., & Nischt, R. (2009). Basement membranes in skin: Unique matrix structures with diverse functions? Histochemistry and Cell Biology, 132(1), 1–10. https://doi.org/10.1007/s00418-009-0586-0

    Article  CAS  PubMed  Google Scholar 

  2. Iozzo, R. V. (2005). Basement membrane proteoglycans: From cellar to ceiling. Nature Reviews. Molecular Cell Biology, 6(8), 646–656. https://doi.org/10.1038/nrm1702

    Article  CAS  PubMed  Google Scholar 

  3. Heck, D. E., Vetrano, A. M., Mariano, T. M., et al. (2003). UVB light stimulates production of reactive oxygen species: Unexpected role for catalase. The Journal of Biological Chemistry, 278(25), 22432–22436. https://doi.org/10.1074/jbc.C300048200

    Article  CAS  PubMed  Google Scholar 

  4. Terra, V. A., Souza-Neto, F. P., Frade, M. A. C., et al. (2015). Genistein prevents ultraviolet B radiation-induced nitrosative skin injury and promotes cell proliferation. Journal of Photochemistry and Photobiology B: Biology, 144, 20–27. https://doi.org/10.1016/j.jphotobiol.2015.01.013

    Article  CAS  PubMed  Google Scholar 

  5. Li, H., & Hou, L. (2018). Regulation of melanocyte stem cell behavior by the niche microenvironment. Pigment Cell & Melanoma Research, 31(5), 556–569. https://doi.org/10.1111/pcmr.12701

    Article  Google Scholar 

  6. Yardman-Frank, J. M., & Fisher, D. E. (2021). Skin pigmentation and its control: From ultraviolet radiation to stem cells. Experimental Dermatology, 30(4), 560–571. https://doi.org/10.1111/exd.14260

    Article  CAS  PubMed  Google Scholar 

  7. Narayanan, D. L., Saladi, R. N., & Fox, J. L. (2010). Ultraviolet radiation and skin cancer. International Journal of Dermatology, 49(9), 978–986. https://doi.org/10.1111/j.1365-4632.2010.04474.x

    Article  PubMed  Google Scholar 

  8. Sime, S., & Reeve, V. E. (2004). Protection from inflammation, immunosuppression and carcinogenesis induced by UV radiation in mice by topical pycnogenol. Photochemistry and Photobiology, 79(2), 193–198. https://doi.org/10.1562/0031-8655(2004)079%3c0193:pfiiac%3e2.0.co;2

    Article  CAS  PubMed  Google Scholar 

  9. Yoshihara, E., Masaki, S., Matsuo, Y., et al. (2014). Thioredoxin/Txnip: Redoxisome, as a redox switch for the pathogenesis of diseases. Frontiers in Immunology, 4, 514. https://doi.org/10.3389/fimmu.2013.00514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Thioredoxin and thioredoxin target proteins: from molecular mechanisms to functional significance. Retrieved 15 Dec 2022 from https://pubmed.ncbi.nlm.nih.gov/22607099/.

  11. Karlenius, T. C., & Tonissen, K. F. (2010). Thioredoxin and cancer: A role for thioredoxin in all states of tumor oxygenation. Cancers, 2(2), 209–232. https://doi.org/10.3390/cancers2020209

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Mahmood, D. F. D., Abderrazak, A., el Hadri, K., et al. (2013). The thioredoxin system as a therapeutic target in human health and disease. Antioxidants & Redox Signaling, 19(11), 1266–1303. https://doi.org/10.1089/ars.2012.4757

    Article  CAS  Google Scholar 

  13. Gromer, S., Urig, S., & Becker, K. (2004). The thioredoxin system—From science to clinic. Medicinal Research Reviews, 24(1), 40–89. https://doi.org/10.1002/med.10051

    Article  CAS  PubMed  Google Scholar 

  14. Masutani, H., Ueda, S., & Yodoi, J. (2005). The thioredoxin system in retroviral infection and apoptosis. Cell Death and Differentiation, 12(Suppl 1), 991–998. https://doi.org/10.1038/sj.cdd.4401625

    Article  CAS  PubMed  Google Scholar 

  15. Baek, J., & Lee, M. G. (2016). Oxidative stress and antioxidant strategies in dermatology. Redox Report, 21(4), 164–169. https://doi.org/10.1179/1351000215Y.0000000015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Fu, H., You, S., Zhao, D., et al. (2021). Tremella fuciformis polysaccharides inhibit UVA-induced photodamage of human dermal fibroblast cells by activating up-regulating Nrf2/Keap1 pathways. Journal of Cosmetic Dermatology, 20(12), 4052–4059. https://doi.org/10.1111/jocd.14051

    Article  PubMed  Google Scholar 

  17. Tremella fuciformis polysaccharides alleviate induced atopic dermatitis in mice by regulating immune response and gut microbiota. Retrieved from 15 Dec 2022. https://pubmed.ncbi.nlm.nih.gov/36091780/.

  18. Ji, C., Huang, J. W., Xu, Q. Y., et al. (2016). Gremlin inhibits UV-induced skin cell damages via activating VEGFR2-Nrf2 signaling. Oncotarget, 7(51), 84748–84757. https://doi.org/10.18632/oncotarget.12454

    Article  PubMed  PubMed Central  Google Scholar 

  19. Ji, C., Yang, B., Yang, Y. L., et al. (2010). Exogenous cell-permeable C6 ceramide sensitizes multiple cancer cell lines to doxorubicin-induced apoptosis by promoting AMPK activation and mTORC1 inhibition. Oncogene, 29(50), 6557–6568. https://doi.org/10.1038/onc.2010.379

    Article  CAS  PubMed  Google Scholar 

  20. Ji, C., Yang, B., Yang, Z., et al. (2012). Ultra-violet B (UVB)-induced skin cell death occurs through a cyclophilin D intrinsic signaling pathway. Biochemical and Biophysical Research Communications, 425(4), 825–829. https://doi.org/10.1016/j.bbrc.2012.07.160

    Article  CAS  PubMed  Google Scholar 

  21. Ji, C., Yang, Y., Yang, B., et al. (2010). Trans-zeatin attenuates ultraviolet induced down-regulation of aquaporin-3 in cultured human skin keratinocytes. International Journal of Molecular Medicine, 26(2), 257–263. https://doi.org/10.3892/ijmm_00000460

    Article  CAS  PubMed  Google Scholar 

  22. Ji, C., Yang, Y. L., Yang, Z., et al. (2012). Perifosine sensitizes UVB-induced apoptosis in skin cells: new implication of skin cancer prevention? Cellular Signalling, 24(9), 1781–1789. https://doi.org/10.1016/j.cellsig.2012.05.003

    Article  CAS  PubMed  Google Scholar 

  23. Huang, J. W., Xu, Q. Y., Lin, M., et al. (2020). The extract from acidosasa longiligula alleviates in vitro UV-induced skin cell damage via positive regulation of thioredoxin 1. Clinical Interventions in Aging, 15, 897–905. https://doi.org/10.2147/CIA.S239920

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Ji, C., Yang, B., Huang, S. Y., et al. (2017). Salubrinal protects human skin fibroblasts against UVB-induced cell death by blocking endoplasmic reticulum (ER) stress and regulating calcium homeostasis. Biochemical and Biophysical Research Communications, 493(4), 1371–1376. https://doi.org/10.1016/j.bbrc.2017.10.012

    Article  CAS  PubMed  Google Scholar 

  25. Ichihashi, M., Ueda, M., Budiyanto, A., et al. (2003). UV-induced skin damage. Toxicology, 189(1–2), 21–39. https://doi.org/10.1016/s0300-483x(03)00150-1

    Article  CAS  PubMed  Google Scholar 

  26. Arnér, E. S., & Holmgren, A. (2000). Physiological functions of thioredoxin and thioredoxin reductase. European Journal of Biochemistry, 267(20), 6102–6109. https://doi.org/10.1046/j.1432-1327.2000.01701.x

    Article  PubMed  Google Scholar 

  27. Wen, L., Gao, Q., Ma, C. W., et al. (2016). Effect of polysaccharides from Tremella fuciformis on UV-induced photoaging. Journal of Functional Foods, 20, 400–410. https://doi.org/10.1016/j.jff.2015.11.014

    Article  CAS  Google Scholar 

  28. De Gruijl, F. R., Van Kranen, H. J., & Mullenders, L. H. (2001). UV-induced DNA damage, repair, mutations and oncogenic pathways in skin cancer. Journal of Photochemistry and Photobiology B: Biology, 63(1–3), 19–27. https://doi.org/10.1016/s1011-1344(01)00199-3

    Article  PubMed  Google Scholar 

  29. Shen, T., Duan, C., Chen, B., et al. (2017). Tremella fuciformis polysaccharide suppresses hydrogen peroxide-triggered injury of human skin fibroblasts via upregulation of SIRT1. Molecular Medicine Reports, 16(2), 1340–1346. https://doi.org/10.3892/mmr.2017.6754

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Matsui, M., Oshima, M., Oshima, H., et al. (1996). Early embryonic lethality caused by targeted disruption of the mouse thioredoxin gene. Developmental Biology, 178(1), 179–185. https://doi.org/10.1006/dbio.1996.0208

    Article  CAS  PubMed  Google Scholar 

  31. Gasdaska, P. Y., Oblong, J. E., Cotgreave, I. A., et al. (1994). The predicted amino acid sequence of human thioredoxin is identical to that of the autocrine growth factor human adult T-cell derived factor (ADF): Thioredoxin mRNA is elevated in some human tumors. Biochimica et Biophysica Acta, 1218(3), 292–296. https://doi.org/10.1016/0167-4781(94)90180-5

    Article  CAS  PubMed  Google Scholar 

  32. Berggren, M., Gallegos, A., Gasdaska, J. R., et al. (1996). Thioredoxin and thioredoxin reductase gene expression in human tumors and cell lines, and the effects of serum stimulation and hypoxia. Anticancer Research, 16(6B), 3459–3466.

    CAS  PubMed  Google Scholar 

  33. Grogan, T. M., Fenoglio-Prieser, C., Zeheb, R., et al. (2000). Thioredoxin, a putative oncogene product, is overexpressed in gastric carcinoma and associated with increased proliferation and increased cell survival. Human Pathology, 31(4), 475–481. https://doi.org/10.1053/hp.2000.6546

    Article  CAS  PubMed  Google Scholar 

  34. Ao, H., Li, H., Zhao, X., et al. (2021). TXNIP positively regulates the autophagy and apoptosis in the rat müller cell of diabetic retinopathy. Life Sciences, 267, 118988. https://doi.org/10.1016/j.lfs.2020.118988

    Article  CAS  PubMed  Google Scholar 

  35. Shi, D., Zhou, X., & Wang, H. (2021). S14G-humanin (HNG) protects retinal endothelial cells from UV-B-induced NLRP3 inflammation activation through inhibiting Egr-1. Inflammation Research: Official Journal of the European Histamine Research Society, 70(10–12), 1141–1150. https://doi.org/10.1007/s00011-021-01489-4

    Article  CAS  Google Scholar 

  36. Bu, L., Li, W., Ming, Z., et al. (2017). Inhibition of TrxR2 suppressed NSCLC cell proliferation, metabolism and induced cell apoptosis through decreasing antioxidant activity. Life sciences, 178, 35–41.

    Article  CAS  PubMed  Google Scholar 

  37. Essendoubi, M., Gobinet, C., Reynaud, R., et al. (2016). Human skin penetration of hyaluronic acid of different molecular weights as probed by Raman spectroscopy. Skin Research and Technology, 22(1), 55–62. https://doi.org/10.1111/srt.12228

    Article  CAS  PubMed  Google Scholar 

  38. Jenkins, G. (2002). Molecular mechanisms of skin ageing. Mechanisms of Ageing and Development, 123(7), 801–810. https://doi.org/10.1016/s0047-6374(01)00425-0

    Article  CAS  PubMed  Google Scholar 

  39. Davis, B. H., Chen, A., & Beno, D. W. (1996). Raf and mitogen-activated protein kinase regulate stellate cell collagen gene expression. The Journal of Biological Chemistry, 271(19), 11039–11042. https://doi.org/10.1074/jbc.271.19.11039

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

This work was supported by grants from Joint Funds for the Innovation of Science and Technology, Fujian Province (2021Y9150), Natural Science Foundation of Fujian Province (No. 2020J02053), and Natural Science Foundation of Fujian Province (No.2020J01966).

Author information

Author notes

  1. Mengting Lin, Chengbei Bao, and Lihong Chen have contributed equally to this work.

Authors and Affiliations

  1. Department of Dermatology, The First Affiliated Hospital of Fujian Medical University, 20 Chazhong Road, Fuzhou, Fujian, 350000, China

    Mengting Lin, Chengbei Bao, Lihong Chen, Shiling Geng, Haiqing Wang, Zhixun Xiao, Chao Ji & Bo Cheng

  2. Fujian Dermatology and Venereology Research Institute, The First Affiliated Hospital, Fujian Medical University, Fuzhou, China

    Mengting Lin, Chengbei Bao, Lihong Chen, Shiling Geng, Haiqing Wang, Zhixun Xiao, Chao Ji & Bo Cheng

  3. Key Laboratory of Skin Cancer of Fujian Higher Education Institutions, The First Affiliated Hospital, Fujian Medical University, Fuzhou, 350000, China

    Mengting Lin, Chengbei Bao, Lihong Chen, Shiling Geng, Haiqing Wang, Zhixun Xiao, Chao Ji & Bo Cheng

  4. Central Laboratory, The First Affiliated Hospital of Fujian Medical University, 20 Chazhong Road, Fuzhou, Fujian, 350000, China

    Ting Gong

Authors
  1. Mengting Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Chengbei Bao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lihong Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shiling Geng
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Haiqing Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zhixun Xiao
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ting Gong
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Chao Ji
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Bo Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Chao Ji or Bo Cheng.

Ethics declarations

Conflict of interest

On behalf of all authors, the corresponding author states that there is no conflict of interest.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lin, M., Bao, C., Chen, L. et al. Tremella fuciformis polysaccharides alleviates UV-provoked skin cell damage via regulation of thioredoxin interacting protein and thioredoxin reductase 2. Photochem Photobiol Sci 22, 2285–2296 (2023). https://doi.org/10.1007/s43630-023-00450-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s43630-023-00450-0

Keywords

Search

Navigation