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Proteomics Reveals Long-Term Alterations in Signaling and Metabolic Pathways Following Both Myocardial Infarction and Chemically Induced Denervation

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Abstract

Myocardial infraction (MI) is the principal risk factor for the onset of heart failure (HF). Investigations regarding the physiopathology of MI progression to HF have revealed the concerted engagement of other tissues, such as the autonomic nervous system and the medulla oblongata (MO), giving rise to systemic effects, important in the regulation of heart function. Cardiac sympathetic afferent denervation following application of resiniferatoxin (RTX) attenuates cardiac remodelling and restores cardiac function following MI. While the physiological responses are well documented in numerous species, the underlying molecular responses during the initiation and progression from MI to HF remains unclear. We obtained multi-tissue time course proteomics with a murine model of HF induced by MI in conjunction with RTX application. We isolated tissue sections from the left ventricle (LV), MO, cervical spinal cord and cervical vagal nerves at four time points over a 12-week study. Bioinformatic analyses consistently revealed a high statistical enrichment for metabolic pathways in all tissues and treatments, implicating a central role of mitochondria in the tissue-cellular response to both MI and RTX. In fact, the additional functional pathways found to be enriched in these tissues, involving the cytoskeleton, vesicles and signal transduction, could be downstream of responses initiated by mitochondria due to changes in neuronal pulse frequency after a shock such as MI or the modification of such frequency communication from the heart to the brain after RTX application. Development of future experiments, based on our proteomic results, should enable the dissection of more precise mechanisms whereby metabolic changes in neuronal and cardiac tissues can effectively ameliorate the negative physiological effects of MI via RTX application.

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Data availability

The data that support the findings from this study are available from the corresponding author upon reasonable request.

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Acknowledgements

We acknowledge core support from Animal facility ANEXPLO, CREFRE US006 Rangueil, and in particular Xavier Sudre for his expertise. This work was funded by the Foundation de France Grant Number RAF18002BBA awarded to Dina N. Arvanitis. The proteomic investigations were funded by the National Sciences and Engineering Research Council of Canada (F. Beaudry discovery Grant No. RGPIN-2020-05228). Laboratory equipment was funded by the Canadian Foundation for Innovation (CFI) and the Fonds de Recherche du Québec (FRQ), the Government of Quebec (F. Beaudry CFI John R. Evans Leaders Grant No. 36706). F. Beaudry is the holder of the Canada Research Chair in metrology of bioactive molecule and target discovery (Grant No. CRC-2021-00160). This research was undertaken, partly, thanks to funding from the Canada Research Chairs Program. Ph.D. scholarships were awarded to J. Ben Salem from the Fonds de Recherche du Québec—Santé (Scholarship No. 302490) and from the Université de Montréal.

Funding

This work was supported by Foundation de France (Grant No. RAF18002BBA), National Sciences and Engineering Research Council of Canada (Grant No. RGPIN-2020-05228), Canadian Foundation for Innovation (Grant No. 36706), Canada Research Chairs (Grant No. CRC-2021-00160).

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Author notes

  1. Jennifer Ben Salem and Jason S. Iacovoni are co-first authors and they have contributed equally to this work.

Authors and Affiliations

  1. INSERM DR Midi-Pyrénées Limousin, Institut des Maladies Métaboliques et Cardiovasculaires (I2MC) UMR1297, Université de Toulouse III, Toulouse, France

    Jennifer Ben Salem, Jason S. Iacovoni & Dina N. Arvanitis

  2. Département de Biomédecine Vétérinaire, Faculté de Médecine Vétérinaire, Université de Montréal, 3200 Sicotte, Saint-Hyacinthe, QC, J2S 2M2, Canada

    Jennifer Ben Salem & Francis Beaudry

  3. Centre de recherche sur le cerveau et l’apprentissage (CIRCA), Université de Montréal, Montréal, QC, Canada

    Jennifer Ben Salem & Francis Beaudry

  4. INSERM DR Midi-Pyrénées Limousin, Centre Régional d’Exploration Fonctionnelle et Ressources Expérimentales Service Microchirurgie, (CREFRE- US06, Rangueil), Toulouse, France

    Denis Calise

  5. Institut des Maladies Métaboliques et Cardiovasculaires (I2MC) UMR INSERM 1297 - Équipe 10, 1 Avenue Jean Poulhès, BP 84225, 31432, Toulouse Cedex, France

    Dina N. Arvanitis

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  1. Jennifer Ben Salem
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Salem, J.B., Iacovoni, J.S., Calise, D. et al. Proteomics Reveals Long-Term Alterations in Signaling and Metabolic Pathways Following Both Myocardial Infarction and Chemically Induced Denervation. Neurochem Res 47, 2416–2430 (2022). https://doi.org/10.1007/s11064-022-03636-7

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