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Mediterranean diet enriched in extra-virgin olive oil or nuts modulates circulating exosomal non-coding RNAs

  • Original Contribution
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European Journal of Nutrition Aims and scope Submit manuscript

Abstract

Purpose

Exosomes are extracellular vesicles secreted by cells, which can transport different molecules, including nucleic acids. Dietary habits may induce gene regulation through the modulation of exosomal RNAs. We aimed at characterizing exosomal lncRNAs, mRNA and miRNAs modulation after a 1-year adherence to a low-fat diet (LFD) or to Mediterranean-based diets enriched in extra-virgin olive oil (MedDiet + EVOO) or in a mixture of nuts (MedDiet + Nuts).

Methods

Plasma samples were collected, at baseline and after 1 year of dietary interventions, from 150 participants included in the PREDIMED study (Reus Center). LncRNAs, mRNAs and miRNAs were isolated from plasma exosomes and screened. RT-qPCR validation was performed for miRNAs.

Results

Compared with LFD, 413 lncRNAs and 188 mRNAs, and 476 lncRNAs and 235 mRNAs were differentially modulated in response to the MedDiet + EVOO and MedDiet + Nuts interventions, respectively. In addition, after 1 year of dietary interventions, 26 circulating miRNAs were identified as differentially expressed between groups. After 1 year of intervention, 11 miRNAs significantly changed in LFD group, while 8 and 21 were modulated in response to the MedDiet enriched with EVOO or nuts, respectively. Bioinformatic analyses of differentially expressed miRNAs and their validated target genes suggest certain metabolic pathways are modulated by LFD (PI3K-Akt and AMPK), MedDiet + EVOO (PI3K-Akt, NF-kappa B, HIF-1, and insulin resistance), and MedDiet-Nuts (FoxO, PI3K-Akt, AMPK, p53 and HIF-1) interventions.

Conclusion

Results show that 1-year MedDiet + Nuts and MedDiet + EVOO dietary interventions modulate exosomal RNA content, with the former affecting a higher number of miRNAs. The modulation of exosomal RNAs could help explain how the adherence to a Mediterranean diet may lead to beneficial effects and deserves further investigation.

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Abbreviations

CVD:

Cardiovascular disease

c-miRNAs:

Circulating miRNAs

lncRNAs:

Long non-coding RNAs

MedDiet:

Mediterranean Diet

miRNAs/miR:

MicroRNAs

mRNA:

Messenger RNA

RBP:

RNA-binding proteins

RT-qPCR:

Quantitative reverse transcription polymerase chain reaction

PUFAs:

Poly-unsaturated fatty acids

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Acknowledgements

We are grateful to all the volunteers who participate in this study. DCM-E is a fellow of “Centro de Estudios Interdisciplinarios Básicos y Aplicados” (CEIBA), Colombia, through the program “Bolívar Gana con Ciencia”. M.C.L.H and L.D.P. were recipients of contracts supported by Consejería de Educación, Juventud y Deporte de la Comunidad de Madrid, Fondo Social Europeo, and Iniciativa de Empleo Juvenil YEI (PEJD‐2016/BIO‐2781 and PEJD-2017-PRE/BIO-5100, respectively). JS-S is partially supported by ICREA under the ICREA Academy programme. 

Funding

This research was funded by grants from the Fundación Ramón Areces (CIVP18A3888) to AD, JTC, MCC, RMH, JS-S and MB; and by the Spanish “Agencia Estatal de Investigación” and European FEDER Funds to AD and RMH (AGL2016-78922-R and PID2019-109369RB-I00), to MCLH (RTI2018-093873-A-I00) and “NutriEpigen” Network to AD, MCLH and MB (AGL2017-90623-REDT). PREDIMED study was granted by the official funding agency for biomedical research of the Spanish government, Instituto de Salud Carlos III, through grants provided to research networks specifically developed for the trial (RTIC G03/140 and RTIC RD 06/0045) and through Centro de Investigación Biomédica The Fundación Patrimonio Comunal Olivarero and Hojiblanca (Malaga, Spain), California Walnut Commission (Sacramento, California), Borges (Reus, Spain), and Morella Nuts (Reus, Spain) donated the olive oil, walnuts, almonds and hazelnuts, respectively, used in the study.

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Author notes

  1. Diana C. Mantilla-Escalante and María-Carmen López de las Hazas have contribute equally to this work.

Authors and Affiliations

  1. Laboratory of Epigenetics of Lipid Metabolism, Madrid Institute for Advanced Studies (IMDEA)-Food, IMDEA Food Institute, CEI UAM + CSIC, Ctra. De Cantoblanco 8, 28049, Madrid, Spain

    Diana C. Mantilla-Escalante, María-Carmen López de las Hazas , Lorena del Pozo-Acebo & Alberto Dávalos

  2. Laboratory of Functional Foods, Madrid Institute for Advanced Studies (IMDEA)-Food, CEI UAM + CSIC, 28049, Madrid, Spain

    M. Carmen Crespo & Joao Tomé-Carneiro

  3. Bioinformatics and Biostatistics Unit, IMDEA Food Institute, CEI UAM+CSIC, Ctra. De Canto Blanco 8, 28049, Madrid, Spain

    Roberto Martín-Hernández

  4. Institut d’Investigació Sanitària Pere Virgili, 43204, Reus, Spain

    Jordi Salas-Salvadó & Mónica Bulló

  5. Departament de Bioquímica i Biotecnologia, Universitat Rovira i Virgili, 43201, Reus, Spain

    Jordi Salas-Salvadó & Mónica Bulló

  6. CIBER Fisiopatología de la Obesidad y Nutrición (CIBEROBN), Instituto de Salud Carlos III, 28029, Madrid, Spain

    Jordi Salas-Salvadó & Mónica Bulló

  7. Nutrition Unit, University Hospital of Sant Joan de Reus, 43204, Reus, Spain

    Jordi Salas-Salvadó

Authors
  1. Diana C. Mantilla-Escalante
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  2. María-Carmen López de las Hazas
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  3. M. Carmen Crespo
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  6. Lorena del Pozo-Acebo
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  9. Alberto Dávalos
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Contributions

AD, MB and JS-S conceived the idea. DCM-E, MCLH, MCC, JTC and L.D.P. performed experiments. RM-H performed bioinformatic analysis. DCM-E, MCLH, MCC, JTC, RM-H and AD wrote the manuscript. AD, MB and JS-S revised and edited the manuscript. All authors revised the manuscript before submission.

Corresponding author

Correspondence to Alberto Dávalos.

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Conflict of interest

Prof. Jordi Salas-Salvadó reports serving on the board of the International Nut and Dried Fruit Council, and the Eroski Foundation and receiving grant support from these entities through his institution. He also reports serving on the Executive Committee of the Instituto Danone Spain. He reports receiving consulting fees or travel expenses from Danone; the California Walnut Commission, the Eroski Foundation, the Instituto Danone—Spain, Nestlé, Abbot Laboratories, and Font Vella Lanjarón. Dr. Salas-Salvadó reports non-financial support from California Walnut Commission, Sacramento CA, USA, non-financial support from Patrimonio Comunal Olivarero, Spain, non-financial support from La Morella Nuts, Spain, non-financial support from Borges S.A., Spain, during the conduct of the study. All the other authors have no conflicts of interest to declare.

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Mantilla-Escalante, D.C., López de las Hazas , MC., Crespo, M.C. et al. Mediterranean diet enriched in extra-virgin olive oil or nuts modulates circulating exosomal non-coding RNAs. Eur J Nutr 60, 4279–4293 (2021). https://doi.org/10.1007/s00394-021-02594-0

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