Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Brief Communication
  • Published:

Mass spectrometry-guided isolation of thiodiketopiperazines from an EtOAc-extract of Setosphaeria rostrata culture medium and their anti-skin aging effects on TNF-α-induced human dermal fibroblasts

The Journal of Antibiotics volume 77, pages 257–263 (2024)Cite this article

Subjects

Abstract

Using mass spectrometry (MS)-guided isolation methods, a new thiodiketopiperazine derivative (1) and exserohilone (2) were isolated from an EtOAc-extract of Setosphaeria rostrata culture medium. The chemical structure of the new compound was elucidated by MS and NMR spectroscopy, and the absolute configurations were established by the quantum mechanical calculations of electronic circular dichroism. All isolated compounds were examined for their effects on reactive oxygen species (ROS) production, matrix metalloproteinase 1 (MMP-1) secretion, and procollagen type I α1 secretion in tumor necrosis factor (TNF)-α-induced human dermal fibroblasts. Compound 1 and exserohilone (2) exhibited the inhibition of TNF-α-induced ROS generation and MMP-1 secretion. Additionally, compound 1 and exserohilone (2) increased the procollagen type I α1 secretion. Compound 1 docked computationally into the active site of MMP-1 (−6.0 kcal/mol).

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

References

  1. McGINNIS MR, Rinaldi MG, Winn RE. Emerging agents of phaeohyphomycosis: pathogenic species of Bipolaris and Exserohilum. J Clin Microbiol. 1986;24:250–9. https://doi.org/10.1128/jcm.24.2.250-259.1986

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Mideros SX, Chung C-L, Wiesner-Hanks T, Poland JA, Wu D, Fialko AA, et al. Determinants of virulence and in vitro development colocalize on a genetic map of Setosphaeria turcica. Phytopathology. 2018;108:254–63. https://doi.org/10.1094/PHYTO-01-17-0021-R

    Article  PubMed  Google Scholar 

  3. Wu D, Turgeon BG. Setosphaeria rostrata: Insights from the sequenced genome of Setosphaeria turcica. Fungal Genet Biol. 2013;61:158–63. https://doi.org/10.1016/j.fgb.2013.08.015

    Article  CAS  PubMed  Google Scholar 

  4. Gu SQ, Li P, Wu M, Hao ZM, Gong XD, Zhang XY, et al. StSTE12 is required for the pathogenicity of Setosphaeria turcica by regulating appressorium development and penetration. Microbiol Res. 2014;169:817–23. https://doi.org/10.1016/j.micres.2014.04.001

    Article  CAS  PubMed  Google Scholar 

  5. Pang X, Lin X, Yang J, Zhou X, Yang B, Wang J, et al. Spiro-phthalides and isocoumarins isolated from the marine-sponge-derived fungus Setosphaeria sp. SCSIO41009. J Nat Prod. 2018;81:1860–8. https://doi.org/10.1021/acs.jnatprod.8b00345

    Article  CAS  PubMed  Google Scholar 

  6. Sugawara K, Sugawara F, Strobel GA, Fu Y, Cun-Heng H, Clardy J. Exserohilone: A novel phytotoxin produced by Exserohilum holmii. J Org Chem. 1985;50:5631–3. https://doi.org/10.1021/jo00350a040

    Article  CAS  Google Scholar 

  7. Park MY, Park SJ, Kim J-J, Lee DH, Kim BS. Inhibitory effect of Moriniafungin produced by Setosphaeria Rostrata F3736 on the development of Rhizopus Rot. Plant Pathol. J. 2020;36:570. https://doi.org/10.5423/PPJ.OA.09.2020.0176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Huertas ACM, Schmelzer CE, Hoehenwarter W, Heyroth F, Heinz A. Molecular-level insights into aging processes of skin elastin. Biochim. 2016;128:163–73. https://doi.org/10.1016/j.biochi.2016.08.010

    Article  CAS  Google Scholar 

  9. Parrado C, Mercado-Saenz S, Perez-Davo A, Gilaberte Y, Gonzalez S, Juarranz AJ. Environmental stressors on skin aging. Mechanistic insights. Front. Pharmacol. 2019;10:759. https://doi.org/10.3389/fphar.2019.00759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Jeon S, Choi M. Anti-inflammatory andanti-aging effects of hydroxytyrosol on human dermal fibroblasts (HDFs). Biomed Dermatol. 2018;2:1–8. https://doi.org/10.1186/s41702-018-0031-x

  11. Chen S, He Z, Xu J. Application of adipose-derived stem cells in photoaging: basic science and literature review. Stem Cell Res Ther. 2020;11:1–15. https://doi.org/10.1186/s13287-020-01994-z

    Article  Google Scholar 

  12. Wang M, Carver JJ, Phelan VV, Sanchez LM, Garg N, Peng Y, et al. Sharing and community curation of mass spectrometry data with Global Natural Products Social Molecular Networking. Nat Biotechnol. 2016;34:828–37. https://doi.org/10.1038/nbt.3597

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Kwon H, Nguyen QN, Ryu SM, Kwon J, Park S, Guo Y, et al. Chemical constituents from Neopestalotiopsis clavispora culture medium with estrogenic effects in MCF-7 cells. Phytochem Lett. 2022;52:134–7. https://doi.org/10.1016/j.phytol.2022.10.008

    Article  CAS  Google Scholar 

  14. Guo C-J, Yeh H-H, Chiang Y-M, Sanchez JF, Chang S-L, Bruno KS, et al. Biosynthetic pathway for the epipolythiodioxopiperazine acetylaranotin in Aspergillus terreus revealed by genome-based deletion analysis. J Am Chem Soc. 2013;135:7205–13. https://doi.org/10.1021/ja3123653

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Tan RX, Jensen PR, Williams PG, Fenical W. Isolation and structure assignments of rostratins A−D, cytotoxic disulfides produced by the marine-derived fungus Exserohilum rostratum. J Nat Prod. 2004;67:1374–82. https://doi.org/10.1021/np049920b

    Article  CAS  PubMed  Google Scholar 

  16. Zhang Y, Liu S, Che Y, Liu X. Epicoccins A–D, epipolythiodioxopiperazines from a Cordyceps-colonizing isolate of Epicoccum nigrum. J Nat Prod. 2007;70:1522–5. https://doi.org/10.1021/np070239u

    Article  CAS  PubMed  Google Scholar 

  17. Tu Y, Quan T. Oxidative stress and human skin connective tissue aging. Cosmetics. 2016;3:28. https://doi.org/10.3390/cosmetics3030028

    Article  CAS  Google Scholar 

  18. Marcos‐Garcés V, Molina Aguilar P, Bea Serrano C, García Bustos V, Benavent Seguí J, Ferrández Izquierdo A, et al. Age‐related dermal collagen changes during development, maturation and ageing–a morphometric and comparative study. J Anat. 2014;225:98–108. https://doi.org/10.1111/joa.12186

    Article  PubMed  PubMed Central  Google Scholar 

  19. Freitas-Rodriguez S, Folgueras AR, Lopez-Otin C. The role of matrix metalloproteinases in aging: Tissue remodeling and beyond. Biochim Biophys Acta Mol Cell Res. 2017;1864:2015–25. https://doi.org/10.1016/j.bbamcr.2017.05.007

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This research was supported by the Korea University, Korea Polar Research Institute (Grant: PE23150), and the National Research Foundation of Korea (NRF-2019R1A2C1006226 and NRF-2022R1A4A3022401).

Author information

Authors and Affiliations

  1. Department of Plant Biotechnology, College of Life Sciences and Biotechnology, Korea University, Seoul, 02841, Republic of Korea

    Haeun Kwon, Sojung Park & Dongho Lee

  2. Department of Life Science, Gachon University, Seongnam, 13120, Republic of Korea

    Hee Woon Ann & Sullim Lee

  3. Natural Product Informatics Research Center, Korea Institute of Science and Technology (KIST) Gangneung Institute, Gangneung, 25451, Republic of Korea

    Jaeyoung Kwon & Keunwan Park

  4. Herbal Medicine Resources Center, Korea Institute of Oriental Medicine, Naju, 58245, Republic of Korea

    Seung Mok Ryu

  5. State Key Laboratory of Medicinal Chemical Biology, College of Pharmacy, and Tianjin Key Laboratory of Molecular Drug Research, Nankai University, Tianjin, 300350, People’s Republic of China

    Yuanqiang Guo

  6. Division of Environmental Science and Ecological Engineering, College of Life Sciences and Biotechnology, Korea University, Seoul, 02841, Republic of Korea

    Jae-Jin Kim

  7. Division of Life Sciences, Korea Polar Research Institute, Incheon, 21990, Republic of Korea

    Joung Han Yim & Il-Chan Kim

  8. Natural Products Research Institute, College of Pharmacy, Seoul National University, Seoul, 08826, Republic of Korea

    Sang Hee Shim

Authors
  1. Haeun Kwon
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Hee Woon Ann
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sojung Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jaeyoung Kwon
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Keunwan Park
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Seung Mok Ryu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yuanqiang Guo
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jae-Jin Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Joung Han Yim
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Il-Chan Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Sang Hee Shim
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Sullim Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Dongho Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Sullim Lee or Dongho Lee.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kwon, H., Ann, H.W., Park, S. et al. Mass spectrometry-guided isolation of thiodiketopiperazines from an EtOAc-extract of Setosphaeria rostrata culture medium and their anti-skin aging effects on TNF-α-induced human dermal fibroblasts. J Antibiot 77, 257–263 (2024). https://doi.org/10.1038/s41429-023-00702-2

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41429-023-00702-2

Search

Advanced search

Quick links