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The Protective Effect of Lithium Against Rotenone may be Evolutionarily Conserved: Evidence from Eisenia fetida, a Primitive Animal with a Ganglionic Brain

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Abstract

Chronic exposure to stress is a non-adaptive situation that is associated with mitochondrial dysfunction and the accumulation of reactive oxygen species (ROS), especially superoxide anion (SA). This accumulation of ROS produces damage-associated molecular patterns (DAMPs), which activate chronic inflammatory states and behavioral changes found in several mood disorders. In a previous study, we observed that an imbalance of SA triggered by rotenone (Ro) exposure caused evolutionarily conserved oxi-inflammatory disturbances and behavioral changes in Eisenia fetida earthworms. These results supported our hypothesis that SA imbalance triggered by Ro exposure could be attenuated by lithium carbonate (LC), which has anti-inflammatory properties. The initial protocol exposed earthworms to Ro (30 nM) and four different LC concentrations. LC at a concentration of 12.85 mg/L decreased SA and nitric oxide (NO) levels and was chosen to perform complementary assays: (1) neuromuscular damage evaluated by optical and scanning electron microscopy (SEM), (2) innate immune inefficiency by analysis of Eisenia spp. extracellular neutrophil traps (eNETs), and (3) behavioral changes. Gene expression was also evaluated involving mitochondrial (COII, ND1), inflammatory (EaTLR, AMP), and neuronal transmission (nAchR α5). LC attenuated the high melanized deposits in the circular musculature, fiber disarrangement, destruction of secretory glands, immune inefficiency, and impulsive behavior pattern triggered by Ro exposure. However, the effects of LC and Ro on gene expression were more heterogeneous. In summary, SA imbalance, potentially associated with mitochondrial dysfunction, appears to be an evolutionary component triggering oxidative, inflammatory, and behavioral changes observed in psychiatric disorders that are inhibited by LC exposure.

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Data Availability

All data generated regarding this study are available in this manuscript. Data and related evaluations that supported the entire research will be available in the University library (UFSM) of the corresponding author from 2024, respecting the 12 months agreed upon between the institution and the author. Any inquiries related to the data of this study can be requested from the corresponding author with a reasonable explanation.

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Acknowledgements

The authors are thankful to the funding sources Conselho Nacional de Desenvolvimento Científico (CNPq), Fundação de Amparo à Pesquisa do Rio Grande do Sul (FAPERGS), and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Capes). They also express gratitude to laboratory technician Marina de Souza Vencato and the members of the laboratory of the Technology Center, Graduate Program in Mechanical Engineering at UFSM, Juliana Silva and Professor Natália Daudt.

Funding

This work was supported by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Capes), which was received by the author M.H.M., and by the Conselho Nacional de Desenvolvimento Científico (CNPq) and Fundação de Amparo à Pesquisa do Rio Grande do Sul (FAPERGS), which were received by the author I.B.M.C.

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Authors and Affiliations

  1. Graduate Program of Pharmacology, Health Sciences Center, Federal University of Santa Maria, Santa Maria, Rio Grande do Sul, Brazil

    Moisés Henrique Mastella, Bárbara Osmarin Turra, Nathália Cardoso de Afonso Bonotto, Cibele Ferreira Teixeira, Fernanda Barbisan & Ivana Beatrice Mânica da Cruz

  2. Biogenomics Lab, Health Sciences Center, Federal University of Santa Maria, Santa Maria, Rio Grande do Sul, Av. Roraima 1000, Building 19, 97105-900, Brazil

    Moisés Henrique Mastella, Isabel Roggia, Bárbara Osmarin Turra, Nathália Cardoso de Afonso Bonotto, Cibele Ferreira Teixeira, Débora Luisa Filipetto Pulcinelli, Graziela Moro Meira, Fernanda Barbisan & Ivana Beatrice Mânica da Cruz

  3. Center for Research, Teaching and Technological Development (Gerontec/FUnATI), Manaus, Amazonas, Brazil

    Verônica Farina Azzolin

  4. Anatomical Design Laboratory, Morphology Department, Federal University of Santa Maria, Santa Maria, Rio Grande do Sul, Brazil

    Luciano de Morais-Pinto

  5. Graduate Program of Gerontology, Center for Physical Education and Sports, Federal University of Santa Maria, Santa Maria, Rio Grande do Sul, Brazil

    Verônica Farina Azzolin, Fernanda Barbisan & Ivana Beatrice Mânica da Cruz

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  1. Moisés Henrique Mastella
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Contributions

Authors M.H.M. and I.B.M.C. contributed to the study conception and design, material preparation, data collection, analysis, the first draft of the manuscript, and funding acquisition. Author I.R. contributed to conceptualization, supervision, data collection, and the writing/review process. Authors B.O.T., N.C.A.B., C.F.T., D.L.F.P., G.M.M., V.F.A., L.M.P., and F.B. contributed to the material preparation and analysis. All authors have read and approved the final manuscript.

Corresponding author

Correspondence to Moisés Henrique Mastella.

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Ethics approval and consent to participate

According to Brazilian legislation, which governs the study’s location, the use of invertebrates, including those used in this study, does not require approval from an ethics committee. Nevertheless, all experiments were conducted following the guidelines for animal experimentation established by the European Parliament and the Council of the European Union in 2010.

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The authors declare that they have no known competing financial interests or personal relationships that could have influenced the work reported in this paper.

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Mastella, M.H., Roggia, I., Turra, B.O. et al. The Protective Effect of Lithium Against Rotenone may be Evolutionarily Conserved: Evidence from Eisenia fetida, a Primitive Animal with a Ganglionic Brain. Neurochem Res 48, 3538–3559 (2023). https://doi.org/10.1007/s11064-023-04001-y

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