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Relationship between Neutrophins and Gut Microbiome in Various Metabolic Types of Obesity

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Abstract

Obesity is associated with a gut microbiome imbalance and the risk of neurological complications. However, the risk of complications is determined by the metabolic type of obesity. The aim was to study the effect of intestinal microbiome taxa on the content of neurotrophins. 130 healthy non-obese donors and 104 obese patients were examined. Depending on the metabolic type of obesity, patients were divided into subgroups with metabolically healthy obesity (MHO, n = 40) and metabolically unhealthy obesity (MUHO, n = 55). Serum concentrations of neurotrophins were measured, and the gut microbiome qualitative assessment was determined by sequencing of the variable region of the 16S rRNA gene. Taxa with a positive correlation with brain-derived neurotrophic factor (BDNF) concentration were mainly represented by butyrate and/or GABA-producing microorganisms capable of degrading mucin. In healthy donors, a positive relationship was found between BDNF and S24-7. BDNF association with Bacteroides spp., Rikenellaceae, Oscillospira spp., [Barnesiellaceae], B. ovatus and Anaerostipes spp. was noted in MHO, while in MUHO with Bifidobacterium spp. and Coprococcus spp. Taxa negatively correlated with BDNF have also been identified, predominantly Gram-positive in obese patients. Nerve growth factor (NGF) concentration has been associated with the gut microbiome in obesity but not in healthy donors. A positive relationship with NGF has been noted for Odoribacter spp. in MHO patients and Slackia spp. in MUHO patients. H. parainfluenzae, Erysipelotrichaceae, Megamonas spp. and Clostridiaceae had a negative association on NGF level in MHO. In MUHO, a similar effect was shown by ML615J-287 and Clostridiales. Thus, obesity, regardless of metabolic type, is associated with the appearance of the “gut microbiome—NGF” relationship, which, apparently, is a consequence of increased intestinal permeability. The list of taxa that correlated with neurotrophins was unique for each group of patients. The obtained results indicate a significant effect ofinter-taxa interaction on the neurotrophin level.

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Funding

This work was performed under contract # 0373100122119000041 within the project “Creation of a bank of biosamples of blood serum and feces from healthy donors and patients with obesity, metabolic syndrome, type 2 diabetes mellitus, and impaired mucosal barrier of the gastrointestinal tract, in order to identify candidate species-nonspecific mediators of the quorum sensing microbiota systems of human, which modulate the endocrine and metabolic function of adipose tissue”.

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Authors and Affiliations

  1. Pirogov Russian National Research Medical University, Moscow, Russia

    I. M. Kolesnikova, S. A. Roumiantsev & A. V. Shestopalov

  2. Center for Digital and Translational Biomedicine, Center for Molecular Health, Moscow, Russia

    A. M. Gaponov, S. A. Roumiantsev & A. V. Shestopalov

  3. Rostov State Medical University, Rostov-on-Don, Russia

    A. M. Gaponov & N. I. Volkova

  4. V.A. Negovsky Research Institute of General Reanimatology, Federal Research and Clinical Center of Intensive Care Medicine and Rehabilitology, Moscow, Russia

    L. A. Ganenko

  5. Kazan (Volga Region) Federal University, Kazan, Russia

    T. V. Grigoryeva & A. V. Laikov

  6. Center for Strategic Planning and Management of Medical and Biological Health Risks, Moscow, Russia

    V. V. Makarov & S. M. Yudin

  7. Dmitry Rogachev National Medical Research Center of Pediatric Hematology, Oncology and Immunology, Moscow, Russia

    A. V. Shestopalov

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  1. I. M. Kolesnikova
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Contributions

Conceptualization (A.M.G., S.A.R., V.V.M., S.M.Yu., A.V.Sh.); experimental design (A.M.G., S.A.R., N.I.V., T.V.G., V.V.M., S.M.Yu., A.V.Sh.); data collection (L.A.G., N.I.V., T.V.G., A.V.L.); data processing (I.M.K., L.A.G., N.I.V., T.V.G., A.V.L.); writing the manuscript (I.M.K., A.V.Sh.); editing the manuscript A.M.G., S.A.R., V.V.M., S.M.Yu., A.V.Sh.).

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Correspondence to I. M. Kolesnikova.

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COMPLIANCE WITH ETHICAL STANDARDS

All experimental procedures that involved human subjects complied with the ethical standards of the National Research Ethics Committee and the 1964 Declaration of Helsinki with its subsequent modifications or comparable ethical standards. The conduct of the research was approved by Local Ethics Committee of Pirogov Russian National Research Medical University (protocol no. 186 dated 06/26/2019) and Ethics Committee of Rostov State Medical University (protocol no. 20/19 dated 12/12/2019). A voluntary informed consent was obtained from each of the participants included in the study.

CONFLICT OF INTEREST

The authors declare that they have neither evident nor potential conflict of interest related to the publication of this article.

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Translated by A. Polyanovsky

Russian Text © The Author(s), 2022, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2022, Vol. 58, No. 4, pp. 298–310https://doi.org/10.31857/S0044452922040076.

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Kolesnikova, I.M., Gaponov, A.M., Roumiantsev, S.A. et al. Relationship between Neutrophins and Gut Microbiome in Various Metabolic Types of Obesity. J Evol Biochem Phys 58, 986–1000 (2022). https://doi.org/10.1134/S0022093022040056

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