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Neuroprotective Effect of Exogenous Galectin-1 in Status Epilepticus

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Abstract

Intrahippocampal pilocarpine microinjection (H-PILO) induces status epilepticus (SE) that can lead to spontaneous recurrent seizures (SRS) and neurodegeneration in rodents. Studies using animal models have indicated that lectins mediate a variety of biological activities with neuronal benefits, especially galectin-1 (GAL-1), which has been identified as an effective neuroprotective compound. GAL-1 is associated with the regulation of cell adhesion, proliferation, programmed cell death, and immune responses, as well as attenuating neuroinflammation. Here, we administrated GAL-1 to Wistar rats and evaluated the severity of the SE, neurodegenerative and inflammatory patterns in the hippocampal formation. Administration of GAL-1 caused a reduction in the number of class 2 and 4 seizures, indicating a decrease in seizure severity. Furthermore, we observed a reduction in inflammation and neurodegeneration 24 h and 15 days after SE. Overall, these results suggest that GAL-1 has a neuroprotective effect in the early stage of epileptogenesis and provides new insights into the roles of exogenous lectins in temporal lobe epilepsy (TLE).

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Data Availability

The datasets generated during and/or analyzed during the current study are available from the corresponding author upon reasonable request.

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Acknowledgements

This research was supported by a grant from CAPES/CNPq (#458143/2014) and FAPEMIG; Melo IS was a recipient of a FAPEAL fellowship. We would like to thank our collaborators at the Dental Research Center in Biomechanics, Biomaterials, and Cell Biology (CPbio). N.G.C., D.G.L.G., M.D.B (grant number 312606/2019-2), and OWC (grant number 304175/2021-8) were supported by the Research Productivity Scholarship Program in Brazilian National Council for Scientific and Technological Development (CNPq). We thank CAPES-Brazil for the PhD Research Fellowship to I.S.M., Y.M.O.S., A.L.D.P., and M.A.C. Finally, would like to thank Lilian Cataldi Rodrigues, Juliana da Silva Oliveira Faccio, Edite Santos Siqueira and Suélen Santos Alves for technical support.

Funding

This project was supported by FAPEAL, CNPq, and CAPES.

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Author notes

  1. Amanda Larissa Dias Pacheco and Igor Santana de Melo contributed equally to this work.

Authors and Affiliations

  1. Institute of Biological Sciences and Health, Federal University of Alagoas (UFAL), Av. Lourival de Melo Mota, km 14, Campus A. C. Simões, Cidade Universitária, Maceió, AL, CEP 57072-970, Brazil

    Amanda Larissa Dias Pacheco, Igor Santana de Melo, Maisa de Araujo Costa, Mariah Morais Celestino Amaral, Nívea Karla de Gusmão Taveiros Silva, Yngrid Mickaelli Oliveira Santos, Daniel Leite Góes Gitaí, Marcelo Duzzioni, Alexandre Urban Borbely & Olagide Wagner de Castro

  2. Department of Physiology, Institute of Biomedical Sciences, Federal University of Uberlândia (UFU), Uberlândia, MG, Brazil

    Robinson Sabino Silva

  3. Department of Physiology, Medical School of Ribeirão Preto, University of São Paulo (USP), Ribeirão Preto, São Paulo, Brazil

    Ana Luiza Ferreira Donatti & Norberto Garcia-Cairasco

  4. Department of Neuroscience and Behavioral Sciences, University of São Paulo, Ribeirão Preto, São Paulo, Brazil

    Ana Luiza Ferreira Donatti & Norberto Garcia-Cairasco

  5. Department of Clinical Analyses, Toxicology, and Food Sciences, School of Pharmaceutical Sciences of Ribeirão Preto, University of São Paulo (USP), Ribeirão Preto, São Paulo, Brazil

    Luisa Mestriner, Carlos Alessandro Fuzo & Marcelo Dias-Baruffi

  6. Beth Israel Deaconess Medical Center, Department of Surgery, Harvard Glycomics Center, Harvard Medical School, CLS 11087 - 3 Blackfan Circle, Boston, MA, 02115, USA

    Richard D. Cummings

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  1. Amanda Larissa Dias Pacheco
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Contributions

Conceptualization, A.L.D.P., M.D.B., and O.W.C.; methodology, I.S.M., Y.M.O.S., A.L.D.P., M.M.C.A., N.K.G.T.S., M.A.C., R.S.S., L.M., C.A.F., M.D.B., and O.W.C.; investigation, A.L.D.P.,C.A.F., L.M., I.S.M., A.U.B., R.S.S., and O.W.C.; formal analysis, A.L.D.P., I.S.M., R.S.S. M.D.B., and O.W.C.; supervision and fund acquisition, M.D.B., and O.W.C.; writing—review and editing, A.L.D.P., I.S.M., D.G.L.G., C.A.F., A.L.F.D., A.U.B., R.S.S., R.D.C., M.D.B., and O.W.C.; resources, A.U.B., R.D.C., N.G.C., M.D.B., and O.W.C.

Corresponding authors

Correspondence to Marcelo Dias-Baruffi or Olagide Wagner de Castro.

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Ethics Approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Experiments were performed in accordance with the NIH guidelines for the care and use of laboratory animals and with the approval of the Federal University of Alagoas Animal Use Ethics Committee.

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Supplementary Information

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Supplementary Fig. 1

Pilocarpine microinjection into the hippocampus. Note the cannula tract with artefacts. inset shows uncharacteristic anatomical detail of pyramidal neurons. calibration bar 20 μm. (PNG 1680 kb)

High resolution image (TIF 26034 kb)

Supplementary Fig. 2

Multiple alignment and similarity among GAL-1 from different organisms. (A) Multiple sequence alignment of galectin-1 sequences from Human, Rat, Conger myriaster (congerin-1 and -2), and Cinachyrella sp obtained with MAFFT. Chemical similarity color scheme and conservation logos are depicted at the top of the graphical representation constructed with the msa R package. (B) Distance matrix from multiple sequence alignment that depicts dissimilarity index for GAL-1 sequence pairs calculated using R package. (PNG 696 kb)

High resolution image (TIFF 1054 kb)

Supplementary Fig. 3

Total seizures number and time of Racine´s classes 3 and 5 during SE. GAL-1+PILO group presented a tendency to increase the number of class 5 seizures compared VEH+PILO (A), as well as pre-treatment with GAL-1 decreased seizures time in class 3 (C and D). We analyzed the number at classes 3 and 5 of Racine’s scale for window (10 min) in VEH + PILO and GAL-1 + PILO to observe the severity of seizures with more details. P < 0.05. *, ** and *** compared with VEH + PILO; unpaired t test or two-way ANOVA with Tukey’s post-hoc test (PNG 744 kb)

High resolution image (TIF 1100 kb)

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Pacheco, A.L.D., de Melo, I.S., de Araujo Costa, M. et al. Neuroprotective Effect of Exogenous Galectin-1 in Status Epilepticus. Mol Neurobiol 59, 7354–7369 (2022). https://doi.org/10.1007/s12035-022-03038-4

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