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In Vitro Evaluation of the Photoprotective Potential of Quinolinic Alkaloids Isolated from the Antarctic Marine Fungus Penicillium echinulatum for Topical Use

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Abstract

Marine-derived fungi proved to be a rich source of biologically active compounds. The genus Penicillium has been extensively studied regarding their secondary metabolites and biological applications. However, the photoprotective effects of these metabolites remain underexplored. Herein, the photoprotective potential of Penicillium echinulatum, an Antarctic alga-associated fungus, was assessed by UV absorption, photostability study, and protection from UVA-induced ROS generation assay on human immortalized keratinocytes (HaCaT) and reconstructed human skin (RHS). The photosafety was evaluated by the photoreactivity (OECD TG 495) and phototoxicity assays, performed by 3T3 neutral red uptake (3T3 NRU PT, OECD TG 432) and by the RHS model. Through a bio-guided purification approach, four known alkaloids, (-)-cyclopenin (1), dehydrocyclopeptine (2), viridicatin (3), and viridicatol (4), were isolated. Compounds 3 and 4 presented absorption in UVB and UVA-II regions and were considered photostable after UVA irradiation. Despite compounds 3 and 4 showed phototoxic potential in 3T3 NRU PT, no phototoxicity was observed in the RHS model (reduction of cell viability < 30%), which indicates their very low acute photoirritation and high photosafety potential in humans. Viridicatin was considered weakly photoreactive, while viridicatol showed no photoreactivity; both compounds inhibited UVA-induced ROS generation in HaCaT cells, although viridicatol was not able to protect the RHS model against UVA-induced ROS production. Thus, the results highlighted the photoprotective and antioxidant potential of metabolites produced by P. echinulatum which can be considered a new class of molecules for photoprotection, since their photosafety and non-cytotoxicity were predicted using recommended in vitro methods for topical use.

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Acknowledgements

The authors are thankful to University of São Paulo for providing access to necessary resources, the financial and fellowship support from the Brazilian research funding agencies Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) and Conselho Nacional de desenvolvimento Científico e Tecnológico (CNPq). The Department of Biomolecular Sciences and the Núcleo de Pesquisas em Produtos Naturais e Sintéticos – NPPNS are acknowledged.

Funding

This study had financial and logistic support from the Brazilian Antarctic Program (PROANTAR/MCTI/CNPq N°64/2013), Brazilian Marine Force, National Institute of Science and Technology (INCT: BioNat), Grant #465637/2014-0, and the State of São Paulo Research Foundation (FAPESP), Grant #2014/50926-0 and 2017/03552-5.

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  1. Department of Biomolecular Sciences, School of Pharmaceutical Sciences of Ribeirão Preto, University of São Paulo, Ribeirão Preto, SP, Brazil

    Thaiz Rodrigues Teixeira, Gustavo Souza dos Santos & Hosana Maria Debonsi

  2. Department of Pharmaceutical Sciences, School of Pharmaceutical Sciences of Ribeirão Preto, University of São Paulo, Ribeirão Preto, SP, Brazil

    Karen Cristina Rangel, Renata Spagolla Napoleão Tavares, Camila Martins Kawakami & Lorena Rigo Gaspar

  3. Department of Clinical and Toxicological Analysis, School of Pharmaceutical Sciences, University of São Paulo, São Paulo, SP, Brazil

    Silvya Stuchi Maria-Engler

  4. Department of Biochemistry, Chemistry Institute, University of São Paulo, São Paulo, SP, Brazil

    Pio Colepicolo

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  1. Thaiz Rodrigues Teixeira
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Contributions

TRT prepared the design, conducted experiments, analyzed data, wrote, discussed, reviewed, and edited the manuscript. KCR, RSNT, CMK, and GSS conducted experiments, analyzed data, and contributed to the discussion part. SSME and PC edited and supervised the entire work. PC, LRG, and HMD designed, edited, supervised, and funded the project. All authors read and approved the manuscript.

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Correspondence to Hosana Maria Debonsi.

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All experimental procedures involving humans were performed in accordance with the principles of the Declaration of Helsinki and were approved by the Human Research Ethics Committee of Faculty of Pharmaceutical Sciences of Ribeirão Preto, São Paulo, Brazil (CAAE no. 96779018.1.0000.5403). The written informed consent was signed by all the donors or their parents or legal guardian.

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Teixeira, T.R., Rangel, K.C., Tavares, R.S.N. et al. In Vitro Evaluation of the Photoprotective Potential of Quinolinic Alkaloids Isolated from the Antarctic Marine Fungus Penicillium echinulatum for Topical Use. Mar Biotechnol 23, 357–372 (2021). https://doi.org/10.1007/s10126-021-10030-x

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  • DOI: https://doi.org/10.1007/s10126-021-10030-x

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