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Cardiac hypertrophy that affects hyperthyroidism occurs independently of the NLRP3 inflammasome

  • Molecular and cellular mechanisms of disease
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Abstract

Cardiac hypertrophy (CH) is an adaptive response to maintain cardiac function; however, persistent stress responses lead to contractile dysfunction and heart failure. Although inflammation is involved in these processes, the mechanisms that control cardiac inflammation and hypertrophy still need to be clarified. The NLRP3 inflammasome is a cytosolic multiprotein complex that mediates IL-1β production. The priming step of NLRP3 is essential for increasing the expression of its components and occurs following NF-κB activation. Hyperthyroidism triggers CH, which can progress to maladaptive CH and even heart failure. We have shown in a previous study that thyroid hormone (TH)-induced CH is linked to the upregulation of S100A8, leading to NF-κB activation. Therefore, we aimed to investigate whether the NLRP3 inflammasome is involved in TH-induced CH and its potential role in CH pathophysiology. Hyperthyroidism was induced in NLRP3 knockout (NLRP3-KO), Caspase-1-KO and Wild Type (WT) male mice of the C57Bl/6J strain, aged 8–12 weeks, by triiodothyronine (7 μg/100 g BW, i.p.) administered daily for 14 days. Morphological and cardiac functional analysis besides molecular assays showed, for the first time, that TH-induced CH is accompanied by reduced NLRP3 expression in the heart and that it occurs independently of the NLRP3 inflammasome and caspase 1-related pathways. However, NLRP3 is important for the maintenance of basal cardiac function since NLRP3-KO mice had impaired diastolic function and reduced heart rate, ejection fraction, and fractional shortening compared with WT mice.

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Funding

This work was supported by the Foundation for the Support of Research in the State of São Paulo (FAPESP) [grant numbers 2019/17031–2 and 2021/06151–7], National Council of Technological and Scientific Development (CNPq) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) – Finance Code 001.

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Authors and Affiliations

  1. Department of Anatomy, Institute of Biomedical Sciences, University of Sao Paulo, Av. Prof. Lineu Prestes, 2415, Butanta, Sao Paulo, 05508-000, Brazil

    Aline Cristina Parletta, Gabriela Cavazza Cerri, Claudia Ribeiro Borba Gasparini, Karine Panico, Denival Nascimento Vieira-Junior, Larissa Maria Zacarias-Rodrigues, Nathalia Senger, Marina Fevereiro, Gabriela Placoná Diniz & Maria Luiza Morais Barreto-Chaves

  2. Department of Cardiopneumology, Heart Institute, Faculty of Medicine, University of Sao Paulo, Sao Paulo, Brazil

    Amanda de Almeida Silva & Maria Cláudia Costa Irigoyen

  3. Center for Regenerative Medicine, University of South Florida Health Heart Institute, Morsani School of Medicine, University of South Florida, Tampa, FL, USA

    Gabriela Placoná Diniz

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Contributions

Aline Cristina Parletta: Conceived and designed research, performed experiments, analyzed data, interpreted results of experiments, prepared figures and drafted manuscript. Gabriela Cavazza Cerri: Performed western blotting, edited, and revised manuscript. Claudia Ribeiro Borba Gasparini, Karine Panico, Denival Nascimento Vieira-Junior, and Larissa Maria Zacarias-Rodrigues: Performed experiments—treatment and euthanasia of animals and histology. Nathalia Senger: Edited and revised manuscript. Amanda de Almeida Silva: Performed experiments – echocardiography. Marina Fevereiro: Provided technical support for methodologies performed in the lab. Gabriela Placoná Diniz: Discussed the results and revised manuscript. Maria Cláudia Costa Irigoyen: Analyzed data and interpreted results of echocardiography. Maria Luiza Morais Barreto-Chaves: Conceived and designed research, edited and revised manuscript, approved final version of manuscript.

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Correspondence to Maria Luiza Morais Barreto-Chaves.

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All procedures were conducted according to the Brazilian law on the use of animals in science and approved by the Animal Ethics Committee of the Institute of Biomedical Sciences of the University of Sao Paulo (approval No 9768300119).

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424_2024_2965_MOESM1_ESM.tif

Supplementary file1 Figure S1. T3 treatment induced hyperthyroidism. A) Thyroxine (T4) circulating levels. B) Thyroid-stimulating hormone (TSH) circulating levels. C) Body weight gain. Data were analyzed by Student's t-test and are presented as mean ± SD. N=5 to 7 per group. (TIF 197 KB)

424_2024_2965_MOESM2_ESM.tif

Supplementary file2 Figure S2. Echocardiographic parameters. A) End diastolic volume (EDV). B) End systolic volume (ESV). C) Left ventricular internal diameter in diastole (LVIDd). D) Left ventricular diameter in systole (LVIDs). Data were analyzed by two-way ANOVA and are presented as mean ± SD. N=6 to 8 per group. (TIF 542 KB)

424_2024_2965_MOESM3_ESM.tif

Supplementary file3 Figure S3. NLRP3 deficiency prevented the increase in protein expression of TLR4 and NFκ-B as well as the increase in gene expression of IL-1β induced by T3. A) Representative Western Blotting image. B) Quantification of TLR4 protein expression. C) Quantification of NF-κB protein expression. Western blotting data were analyzed by two-way ANOVA and are presented as mean ± SD. N=3 to 6 per group. D) Quantitative PCR for IL-1β gene expression. PCR data were analyzed by Student's t-test and are presented as mean ± SD. N=5 to 6 per group. (TIF 670 KB)

Supplementary file4 (PDF 443 KB)

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Parletta, A.C., Cerri, G.C., Gasparini, C.R.B. et al. Cardiac hypertrophy that affects hyperthyroidism occurs independently of the NLRP3 inflammasome. Pflugers Arch - Eur J Physiol (2024). https://doi.org/10.1007/s00424-024-02965-6

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