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Photoactivated resveratrol controls intradermal infection by Staphylococcus aureus in mice: a pilot study

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Abstract

Staphylococcus aureus is one of the main causative agent of infections acquired in both community and hospital environment. In this context, photodynamic therapy (PDT) consists in using a photosensitizer that, activated by light, evokes the formation of reactive oxygen species (ROS), which lead to the death of microorganisms due to oxidative damage; it is useful tool since this action, harmful to pathogens, does not significantly injure human cells. In view of this, this work proposes a more in-depth study on the use of resveratrol (RSV) as a possible photosensitizer. It was observed, in the intradermal infection model in animals’ ear dermis, that photoactivated resveratrol promotes an increase in myeloperoxidase expression with reduced bacterial load in the draining lymph node. Besides that, the draining lymph node of the animals treated with photoactivated RSV controls inflammation through IL-10 production. These are pioneers data and this work being a pilot study; then, other works must be conducted with the objective of elucidate the photoactivated resveratrol mechanism of action.

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References

  1. Islam T, Kubra K, Hassan Chowdhury MM (2018) Prevalence of methicillin-resistant Staphylococcus aureus in hospitals in Chittagong, Bangladesh: a threat of nosocomial infection. J Microsc Ultrastruct 6(4):188–191. https://doi.org/10.4103/JMAU.JMAU_33_18

    Article  PubMed  PubMed Central  Google Scholar 

  2. Dos Santos DP, Muniz IPR, Queiroz AF, Pereira IS, Souza MPA, Lima LJ, Sousa LRO, Ribeiro IS, Galantini MPL, Marques LM, Figueiredo TB, da Silva RAA (2018) Individual variation is the key to the development of a vaccine against Staphylococcus aureus: a comparative study between mice lineages. Braz J Med Biol Res 51(5):e6773. https://doi.org/10.1590/1414-431X20186773

    Article  PubMed  PubMed Central  Google Scholar 

  3. Ryu S, Song PI, Seo CH, Cheong H, Park Y (2014) Colonization and infection of the skin by S. aureus: immune system evasion and the response to cationic antimicrobial peptides. Int J Mol Sci 15(5):8753–8772. https://doi.org/10.3390/ijms15058753

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Sukumaran V, Senanayake S (2016) Bacterial skin and soft tissue infections. Aust Prescr 39(5):159–163. https://doi.org/10.18773/austprescr.2016.058

    Article  PubMed  PubMed Central  Google Scholar 

  5. Tarai B, Das P, Kumar D (2013) Recurrent challenges for clinicians: emergence of methicillin-resistant Staphylococcus aureus, vancomycin resistance, and current treatment options. J Lab Physicians 5(2):71–78. https://doi.org/10.4103/0974-2727.119843

    Article  PubMed  PubMed Central  Google Scholar 

  6. Ding H, Yu H, Dong Y, Tian R, Huang G, Boothman DA, Sumer BD, Gao J (2011) Photoactivation switch from type II to type I reactions by electron-rich micelles for improved photodynamic therapy of cancer cells under hypoxia. J Control Release 156(3):276–280. https://doi.org/10.1016/j.jconrel.2011.08.019

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Dos Santos DP, Lopes DPS, de Melo Calado SP, Goncalves CV, Muniz IPR, Ribeiro IS, Galantini MPL, da Silva RAA (2019) Efficacy of photoactivated Myrciaria cauliflora extract against Staphylococcus aureus infection - a pilot study. J Photochem Photobiol B 191:107–115. https://doi.org/10.1016/j.jphotobiol.2018.12.011

    Article  CAS  PubMed  Google Scholar 

  8. Guzel Tunccan O, Kalkanci A, Unal EA, Abdulmajed O, Erdogan M, Dizbay M, Caglar K (2018) The in vitro effect of antimicrobial photodynamic therapy on Candida and Staphylococcus biofilms. Turk J Med Sci 48(4):873–879. https://doi.org/10.3906/sag-1803-44

    Article  CAS  PubMed  Google Scholar 

  9. Madani L, Sarkisians E, Kiomarsi N, Kharazifard MJ, Chiniforush N (2018) Effect of antimicrobial photodynamic therapy on microleakage of class cavities restored with composite resin. Photodiagn Photodyn Ther 23:78–82. https://doi.org/10.1016/j.pdpdt.2018.06.010

    Article  CAS  Google Scholar 

  10. Mahmoudi H, Pourhajibagher M, Alikhani MY, Bahador A (2019) The effect of antimicrobial photodynamic therapy on the expression of biofilm associated genes in Staphylococcus aureus strains isolated from wound infections in burn patients. Photodiagn Photodyn Ther. https://doi.org/10.1016/j.pdpdt.2019.01.028

  11. Lopez-Miranda V, Soto-Montenegro ML, Vera G, Herradon E, Desco M, Abalo R (2012) Resveratrol: a neuroprotective polyphenol in the Mediterranean diet. Rev Neurol 54(6):349–356

    PubMed  Google Scholar 

  12. Akilov OE, Kosaka S, O'Riordan K, Hasan T (2007) Photodynamic therapy for cutaneous leishmaniasis: the effectiveness of topical phenothiaziniums in parasite eradication and Th1 immune response stimulation. Photochem Photobiol Sci 6(10):1067–1075. https://doi.org/10.1039/b703521g

    Article  CAS  PubMed  Google Scholar 

  13. Almeida PP, Pereira IS, Rodrigues KB, Leal LS, Marques AS, Rosa LP, da Silva FC, da Silva RAA (2017) Photodynamic therapy controls of Staphylococcus aureus intradermal infection in mice. Lasers Med Sci 32(6):1337–1342. https://doi.org/10.1007/s10103-017-2247-1

    Article  PubMed  Google Scholar 

  14. Rodriguez-Cabo T, Rodriguez I, Ramil M, Cela R (2015) Comprehensive evaluation of the photo-transformation routes of trans-resveratrol. J Chromatogr A 1410:129–139. https://doi.org/10.1016/j.chroma.2015.07.088

    Article  CAS  PubMed  Google Scholar 

  15. Uesugia D, Hamada H, Shimoda K (2016) Glycosylation of trans-resveratrol by cultured plant cells under illumination of LEDs. Nat Prod Commun 11(2):199–200

    PubMed  Google Scholar 

  16. Yang I, Kim E, Kang J, Han H, Sul S, Park SB, Kim SK (2012) Photochemical generation of a new, highly fluorescent compound from non-fluorescent resveratrol. Chem Commun 48(32):3839–3841. https://doi.org/10.1039/c2cc30940h

    Article  CAS  Google Scholar 

  17. Dos Santos DP, Soares Lopes DP, de Moraes RCJ, Vieira Goncalves C, Pereira Rosa L, da Silva Rosa FC, da Silva RAA (2019) Photoactivated resveratrol against Staphylococcus aureus infection in mice. Photodiagn Photodyn Ther. https://doi.org/10.1016/j.pdpdt.2019.01.005

  18. Davies MJ (2011) Myeloperoxidase-derived oxidation: mechanisms of biological damage and its prevention. J Clin Biochem Nutr 48(1):8–19. https://doi.org/10.3164/jcbn.11-006FR

    Article  CAS  PubMed  Google Scholar 

  19. Malle E, Furtmuller PG, Sattler W, Obinger C (2007) Myeloperoxidase: a target for new drug development? Br J Pharmacol 152(6):838–854. https://doi.org/10.1038/sj.bjp.0707358

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Reeves EP, Nagl M, Godovac-Zimmermann J, Segal AW (2003) Reassessment of the microbicidal activity of reactive oxygen species and hypochlorous acid with reference to the phagocytic vacuole of the neutrophil granulocyte. J Med Microbiol 52(Pt 8):643–651. https://doi.org/10.1099/jmm.0.05181-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Klebanoff SJ, Kettle AJ, Rosen H, Winterbourn CC, Nauseef WM (2013) Myeloperoxidase: a front-line defender against phagocytosed microorganisms. J Leukoc Biol 93(2):185–198. https://doi.org/10.1189/jlb.0712349

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Domingues-Ferreira M, Levy A, Barros NC, Bertolini DL, Vasconcelos DM (2017) Case report of myeloperoxidase deficiency associated with disseminated paracoccidioidomycosis and peritoneal tuberculosis. Rev Soc Bras Med Trop 50(4):568–570. https://doi.org/10.1590/0037-8682-0462-2016

    Article  PubMed  Google Scholar 

  23. Vandenesch F, Lina G, Henry T (2012) Staphylococcus aureus hemolysins, bi-component leukocidins, and cytolytic peptides: a redundant arsenal of membrane-damaging virulence factors? Front Cell Infect Microbiol 2:12. https://doi.org/10.3389/fcimb.2012.00012

    Article  PubMed  PubMed Central  Google Scholar 

  24. Arango Duque G, Descoteaux A (2014) Macrophage cytokines: involvement in immunity and infectious diseases. Front Immunol 5:491. https://doi.org/10.3389/fimmu.2014.00491

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Golic M, Luft FC, Dechend R (2016) Tumor necrosis factor-alpha, uterine natural killer cells, and pregnancy. Hypertension 68(5):1108–1109. https://doi.org/10.1161/HYPERTENSIONAHA.116.08028

    Article  CAS  PubMed  Google Scholar 

  26. Biedermann T, Kneilling M, Mailhammer R, Maier K, Sander CA, Kollias G, Kunkel SL, Hultner L, Rocken M (2000) Mast cells control neutrophil recruitment during T cell-mediated delayed-type hypersensitivity reactions through tumor necrosis factor and macrophage inflammatory protein 2. J Exp Med 192(10):1441–1452

    Article  CAS  Google Scholar 

  27. Torre-Amione G, Bozkurt B, Deswal A, Mann DL (1999) An overview of tumor necrosis factor alpha and the failing human heart. Curr Opin Cardiol 14(3):206–210

    Article  CAS  Google Scholar 

  28. Turner MD, Nedjai B, Hurst T, Pennington DJ (2014) Cytokines and chemokines: at the crossroads of cell signalling and inflammatory disease. Biochim Biophys Acta 1843(11):2563–2582. https://doi.org/10.1016/j.bbamcr.2014.05.014

    Article  CAS  PubMed  Google Scholar 

  29. Chen L, Deng H, Cui H, Fang J, Zuo Z, Deng J, Li Y, Wang X, Zhao L (2018) Inflammatory responses and inflammation-associated diseases in organs. Oncotarget 9(6):7204–7218. https://doi.org/10.18632/oncotarget.23208

    Article  PubMed  Google Scholar 

  30. Rock KL, Lai JJ, Kono H (2011) Innate and adaptive immune responses to cell death. Immunol Rev 243(1):191–205. https://doi.org/10.1111/j.1600-065X.2011.01040.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Gu C, Wu L, Li X (2013) IL-17 family: cytokines, receptors and signaling. Cytokine 64(2):477–485. https://doi.org/10.1016/j.cyto.2013.07.022

    Article  CAS  PubMed  Google Scholar 

  32. Schmitz JM, Tonkonogy SL, Dogan B, Leblond A, Whitehead KJ, Kim SC, Simpson KW, Sartor RB (2018) Murine adherent and Invasive E. coli induces chronic inflammation and immune responses in the small and large intestines of monoassociated IL-10−/− mice independent of long polar fimbriae adhesin a. Inflamm Bowel Dis. https://doi.org/10.1093/ibd/izy386

  33. Wang X, Coradin T, Helary C (2018) Modulating inflammation in a cutaneous chronic wound model by IL-10 released from collagen-silica nanocomposites via gene delivery. Biomater Sci 6(2):398–406. https://doi.org/10.1039/c7bm01024a

    Article  CAS  PubMed  Google Scholar 

  34. Sharma P, Shahabi K, Spitzer R, Farrugia M, Kaul R, Yudin M (2018) Cervico-vaginal inflammatory cytokine alterations after intrauterine contraceptive device insertion: a pilot study. PLoS One 13(12):e0207266. https://doi.org/10.1371/journal.pone.0207266

    Article  PubMed  PubMed Central  Google Scholar 

  35. Li YP, Stashenko P (1992) Proinflammatory cytokines tumor necrosis factor-alpha and IL-6, but not IL-1, down-regulate the osteocalcin gene promoter. J Immunol 148(3):788–794

    CAS  PubMed  Google Scholar 

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Funding

This study was funded by CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior), for the Institutional Program of Scientific Initiation of Federal University of Bahia and by the Research Center in Optics and Photonics (CePOF) for the equipment to the development of this work.

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Authors and Affiliations

  1. Anísio Teixeira Campus, Multidisciplinary Institute in Health, Federal University of Bahia, 58 Rio de Contas Street, 17 Block, 58 Lot, Candeias, Vitória da Conquista, Bahia, 45029-094, Brazil

    Denisar Palmito dos Santos, Maria Poliana Leite Galantini, Israel Souza Ribeiro, Igor Pereira Ribeiro Muniz, Italo Sousa Pereira & Robson Amaro Augusto da Silva

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  1. Denisar Palmito dos Santos
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  2. Maria Poliana Leite Galantini
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  3. Israel Souza Ribeiro
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  5. Italo Sousa Pereira
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  6. Robson Amaro Augusto da Silva
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Correspondence to Robson Amaro Augusto da Silva.

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Ethical approval

The study followed the guidelines of the Animal Experimentation Code of Ethics of the Brazilian College of Animal Experimentation and was approved by the Ethics Committee on the use of animals (CEUA, Universidade Federal da Bahia, Instituto Multidisciplinar em Saúde, Campus Anísio Teixeira) at which the studies were conducted, under protocol number 042/2017.

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dos Santos, D.P., Galantini, M.P.L., Ribeiro, I.S. et al. Photoactivated resveratrol controls intradermal infection by Staphylococcus aureus in mice: a pilot study. Lasers Med Sci 35, 1341–1347 (2020). https://doi.org/10.1007/s10103-019-02942-x

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  • DOI: https://doi.org/10.1007/s10103-019-02942-x

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