Plasma Levels of Endocannabinoids and Their Analogues Are Related to Specific Fecal Bacterial Genera in Young Adults: Role in Gut Barrier Integrity

Lourdes Ortiz-Alvarez, Huiwen Xu, Xinyu Di, Isabelle Kohler, Francisco J. Osuna-Prieto, Francisco M. Acosta, Ramiro Vilchez-Vargas, Alexander Link, Julio Plaza-Díaz, Mario van der Stelt, Thomas Hankemeier, Mercedes Clemente-Postigo, Francisco J. Tinahones, Angel Gil, Patrick C.N. Rensen, Jonatan R. Ruiz*, Borja Martinez-Tellez

*Corresponding author for this work

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

Objective: To investigate the association of plasma levels of endocannabinoids with fecal microbiota. Methods: Plasma levels of endocannabinoids, anandamide (AEA) and 2-arachidonoylglycerol (2-AG), as well as their eleven analogues, and arachidonic acid (AA), were measured using liquid chromatography-tandem mass spectrometry in 92 young adults. DNA extracted from stool samples was analyzed using 16S rRNA gene sequencing. Lipopolysaccharide levels were measured in plasma samples. Results: Plasma levels of endocannabinoids and their analogues were not related to beta or alpha diversity indexes. Plasma levels of AEA and related N-acylethanolamines correlated positively with the relative abundance of Faecalibacterium genus (all rho ≥ 0.26, p ≤ 0.012) and Akkermansia genus (all rho ≥ 0.22, p ≤ 0.036), and negatively with the relative abundance of Bilophila genus (all rho ≤ −0.23, p ≤ 0.031). Moreover, plasma levels of 2-AG and other acylglycerols correlated positively with the relative abundance of Parasutterella (all rho ≥ 0.24, p ≤ 0.020) and Odoribacter genera (all rho ≥ 0.27, p ≤ 0.011), and negatively with the relative abundance of Prevotella genus (all rho ≤ −0.24, p ≤ 0.023). In participants with high lipopolysaccharide values, the plasma levels of AEA and related N-acylethanolamines, as well as AA and 2-AG, were negatively correlated with plasma levels of lipopolysaccharide (all rho ≤ −0.24, p ≤ 0.020). Conclusion: Plasma levels of endocannabinoids and their analogues are correlated to specific fecal bacterial genera involved in maintaining gut barrier integrity in young adults. This suggests that plasma levels of endocannabinoids and their analogues may play a role in the gut barrier integrity in young adults.

Original languageEnglish
Article number2143
Pages (from-to)1-19
Number of pages19
JournalNutrients
Volume14
Issue number10
DOIs
Publication statusPublished - 2 May 2022

Bibliographical note

Special Issue: Dietary Bioactives, Gut Microbiota, and Human Health.

Funding Information:
Funding: The study was supported by the Spanish Ministry of Economy and Competitiveness via Fondo de Investigación Sanitaria del Instituto de Salud Carlos III (PI13/01393) and PTA 12264-I, Retos de la Sociedad (DEP2016-79512-R), and European Regional Development Funds (ERDF), by the Spanish Ministry of Education (FPU16/05159, FPU16/02828 and FPU17/01523), the Fundación Iberoamericana de Nutrición (FINUT), the Redes Temáticas De Investigación Cooperativa RETIC (Red SAMID RD16/0022), the Chinese Scholarship Council (CSC, No. 201707060012 to XD), InFLAMES Flagship Programme of the Academy of Finland (decision number: 337530), Fundación Alfonso Martin Escudero and Maria Zambrano fellowship by the Ministerio de Universidades y la Unión Europea—NextGenerationEU (RR_C_2021_04). AstraZeneca HealthCare Foundation, the University of Granada Plan Propio de Investigación 2016-Excellence actions: Unit of Excellence on Exercise and Health (UCEES), and by the Junta de Andalucía, Consejería de Economía, Conocimiento, Empresas y Universidad (ref. P18-RT-4455). AL and RVV are supported by the funds of European Commission through the “European funds for regional development” (EFRE) as well as by the regional Ministry of Economy, Science and Digitalization of Saxony-Anhalt as part of the “Autonomy in old Age“ (AiA) research group for “LiLife” Project (Project ID: ZS/2018/11/95324). M.C-P was recipient of a postdoctoral grant (DOC_00448) from the Consejeria de Economía, Industria, Conocimiento y Universidades (PAIDI 2020, Junta de Andalucía), Spain, cofunded by the Fondo Europeo de Desarrollo Regional (FEDER). We would like to thank the team of Data Integration Center of University Medicine Magdeburg for local data-analysis solutions; they are supported by MIRACUM and funded by the German Federal Ministry of Education and Research (BMBF) within the “Medical Informatics Funding Scheme” (FKZ 01ZZ1801H).

Publisher Copyright:
© 2022 by the authors. Licensee MDPI, Basel, Switzerland.

Funding

Funding: The study was supported by the Spanish Ministry of Economy and Competitiveness via Fondo de Investigación Sanitaria del Instituto de Salud Carlos III (PI13/01393) and PTA 12264-I, Retos de la Sociedad (DEP2016-79512-R), and European Regional Development Funds (ERDF), by the Spanish Ministry of Education (FPU16/05159, FPU16/02828 and FPU17/01523), the Fundación Iberoamericana de Nutrición (FINUT), the Redes Temáticas De Investigación Cooperativa RETIC (Red SAMID RD16/0022), the Chinese Scholarship Council (CSC, No. 201707060012 to XD), InFLAMES Flagship Programme of the Academy of Finland (decision number: 337530), Fundación Alfonso Martin Escudero and Maria Zambrano fellowship by the Ministerio de Universidades y la Unión Europea—NextGenerationEU (RR_C_2021_04). AstraZeneca HealthCare Foundation, the University of Granada Plan Propio de Investigación 2016-Excellence actions: Unit of Excellence on Exercise and Health (UCEES), and by the Junta de Andalucía, Consejería de Economía, Conocimiento, Empresas y Universidad (ref. P18-RT-4455). AL and RVV are supported by the funds of European Commission through the “European funds for regional development” (EFRE) as well as by the regional Ministry of Economy, Science and Digitalization of Saxony-Anhalt as part of the “Autonomy in old Age“ (AiA) research group for “LiLife” Project (Project ID: ZS/2018/11/95324). M.C-P was recipient of a postdoctoral grant (DOC_00448) from the Consejeria de Economía, Industria, Conocimiento y Universidades (PAIDI 2020, Junta de Andalucía), Spain, cofunded by the Fondo Europeo de Desarrollo Regional (FEDER). We would like to thank the team of Data Integration Center of University Medicine Magdeburg for local data-analysis solutions; they are supported by MIRACUM and funded by the German Federal Ministry of Education and Research (BMBF) within the “Medical Informatics Funding Scheme” (FKZ 01ZZ1801H).

FundersFunder number
Consejeria de Economía, Industria, Conocimiento y Universidades
MIRACUM
Ministerio de Universidades y la Unión EuropeaRR_C_2021_04
Ministry of Economy, Science and Digitalization of Saxony-Anhalt
PAIDI 2020, Junta de Andalucía
University of Granada Plan Propio de Investigación
Fundación Alfonso Martín Escudero
Consejería de Economía, Conocimiento, Empresas y Universidad, Junta de AndalucíaP18-RT-4455
Consejería de Economía, Conocimiento, Empresas y Universidad, Junta de Andalucía
AstraZeneca HealthCare Foundation
Fundación Iberoamericana de NutriciónRD16/0022
Fundación Iberoamericana de Nutrición
Anglo-Israel AssociationDOC_00448, ZS/2018/11/95324
Anglo-Israel Association
European Commission
Academy of Finland337530
Academy of Finland
Bundesministerium für Bildung und ForschungFKZ 01ZZ1801H
Bundesministerium für Bildung und Forschung
Ministerio de Educación, Cultura y DeporteFPU16/05159, FPU16/02828, FPU17/01523
Ministerio de Educación, Cultura y Deporte
Ministerio de Economía y Competitividad
China Scholarship Council201707060012
China Scholarship Council
Instituto de Salud Carlos IIIPI13/01393, DEP2016-79512-R, PTA 12264-I
Instituto de Salud Carlos III
European Regional Development Fund

    Keywords

    • endocannabinoid system
    • gastrointestinal microbiome
    • gut barrier
    • inflammation
    • short-chain fatty acids

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