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Photosensitizers attenuate LPS-induced inflammation: implications in dentistry and general health

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Abstract

Antimicrobial photodynamic therapy (aPDT) is a complementary therapeutic modality for periodontal and endodontic diseases, in which Gram-negative bacteria are directly involved. Currently, there are few evidences regarding the effects of aPDT on bacterial components such as lipopolysaccharide (LPS) and it would represent a major step forward in the clinical use of this therapy. In this context, this study aimed to evaluate the efficacy of different photosensitizers (PSs) used in aPDT in LPS inhibition. Four PSs were used in this study: methylene blue (MB), toluidine blue (TBO), new methylene blue (NMB), and curcumin (CUR). Different approaches to evaluate LPS interaction with PSs were used, such as spectrophotometry, Limulus amebocyte lysate (LAL) test, functional assays using mouse macrophages, and an in vivo model of LPS injection. Spectrophotometry showed that LPS decreased the absorbance of all PSs used, indicating interactions between the two species. LAL assay revealed significant differences in LPS concentrations upon pre-incubation with the different PSs. Interestingly, the inflammatory potential of LPS decreased after previous treatment with the four PSs, resulting in decreased secretion of inflammatory cytokines by macrophages. In vivo, pre-incubating curcumin with LPS prevented animals from undergoing septic shock within the established time. Using relevant models to study the inflammatory activity of LPS, we found that all PSs used in this work decreased LPS-induced inflammation, with a more striking effect observed for NMB and curcumin. These data advance the understanding of the mechanisms of LPS inhibition by PSs.

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Acknowledgments

We are thankful to Prof. Dr. Dario Simões Zamboni for providing reagents and important resources for the development of this work. We also thank Izaíra Ticani Brandão and Nilza Letícia Magalhães for their technical support for this study in LAL Assays. Finally, we are grateful for Prof. Dr. Zeki Naal, Profa. Dra. Lúcia Helena Faccioli, and their lab members for the lab and equipment availability.

Funding

This work was supported by grants from the Coordination for the Improvement of Higher Education Personnel - Academic Excellence Program (CAPES-PROEX process 23038.000712/2018-34) and São Paulo Research Foundation (FAPESP process 2016/113386-5).

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  1. Renan Villanova Homem de Carvalho

    Present address: Laboratory of Lymphocyte Dynamics, The Rockefeller University, 1230 York Ave, NY, 10065, New York, USA

Authors and Affiliations

  1. Departamento de Clínica Infantil, Faculdade de Odontologia de Ribeirão Preto, Universidade de São Paulo, Av. do Café, s/n, Monte Alegre, 14040-904, Ribeirão Preto, São Paulo, Brazil

    Ana Carolina Fernandes Couto, Raquel Assed Bezerra da Silva, Paulo Nelson-Filho, Francisco Wanderley Garcia Paula-Silva & Maria Cristina Borsatto

  2. Departamento de Biologia Celular, Molecular e Bioagentes Patogênicos, Faculdade de Medicina de Ribeirão Preto, Universidade de São Paulo, Av. Bandeirantes, 3900, Monte Alegre, 14049-900, Ribeirão Preto, São Paulo, Brazil

    Renan Villanova Homem de Carvalho

  3. Departamento de Análises Clínicas, Toxicológicas e Bromatológicas, Faculdade de Ciências Farmacêuticas de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto, Brazil

    Guilherme Thomaz Pereira Brancini, Fernando Grine Martins, Carlos Arterio Sorgi & Gilberto Úbida Leite Braga

  4. Departamento de Cirurgia e Traumatologia Buco-Maxilo-Facial e Periodontia, Faculdade de Odontologia de Ribeirão Preto, Universidade de São Paulo, Av. do Café, s/n, Monte Alegre, 14040-904, Ribeirão Preto, São Paulo, Brazil

    Arthur Belém Novaes Júnior

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Contributions

A.C.F.C. and R.V.H.C. designed, generated figures, wrote, and performed experiments. G.U.L.B., M.C.B., and R.A.B.S. provided reagents and tools. A.C.F.C., R.V.H.C., G.T.P.B., F.G.M., C.A.S., R.A.B.S., P.N.F., F.W.G.P.S., G.U.L.B., M.C.B., and A.B.N.J. analyzed the data, discussed hypotheses, and revised the manuscript.

Corresponding authors

Correspondence to Ana Carolina Fernandes Couto, Renan Villanova Homem de Carvalho or Arthur Belém Novaes Júnior.

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Conflict of interest

The authors declare that they have no conflict of interest.

Role of funding source

Grants from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-Programa de Excelência Acadêmica (CAPES-PROEX process 23,038.000712/2018-34) and Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP process 2016/113386-5) were crucial for the development of this work.

Ethical approval

The research project was approved by the Ethics Committee on the Use of Animals of the Faculty of Dentistry of Ribeirão Preto, University of São Paulo (process 2019.1.173.58.4) and was carried out following international standards for experimentation on live animals and the rules of the National Council for the Control of Animal Experimentation (CONCEA).

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Ana Carolina Fernandes Couto and Renan Villanova Homem de Carvalho are joint first authors

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Couto, A.C.F., de Carvalho, R.V.H., Brancini, G.T.P. et al. Photosensitizers attenuate LPS-induced inflammation: implications in dentistry and general health. Lasers Med Sci 36, 913–926 (2021). https://doi.org/10.1007/s10103-020-03180-2

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