Immunometabolic capacities of nutritional fatty acids in regulation of inflammatory bone cell interaction and systemic impact of periodontal infection

Frontiers in Immunology · 12 authors, 7 centres

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TL;DR

In a mouse model, a diet enriched with palmitic acid (PA) reduced systemic bone microarchitecture and increased osteoclasts, effects which were reversed by substituting PA with oleic acid (OA).

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This preclinical study used C57BL/6 mice and in vitro bone cell cultures to investigate how dietary fatty acids modulate systemic bone responses to oral infection with Porphyromonas gingivalis. Mice were fed diets enriched with oleic acid (OA), palmitic acid (PA), or a mixture for 16 weeks before oral infection. Results showed that a PA-enriched diet reduced systemic bone microarchitecture, increased lipotoxic PA-containing metabolites in bone, and increased femoral osteoclast numbers after infection. Substituting PA with OA reversed these effects, improving bone parameters and increasing the stress-reducing lipokine PI(18:1/18:1). In vitro, OA counteracted PA-induced osteoblast inflammation and impaired mineralization.

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other

SPECIALTY

nutrition

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ORIGINAL PAPER

PMC10509849

Immunometabolic capacities of nutritional fatty acids in regulation of inflammatory bone cell interaction and systemic impact of periodontal infection

Frontiers in Immunology

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ABSTRACT

Abstract Introduction Novel preventive strategies in periodontal disease target the bacterial-induced inflammatory host response to reduce associated tissue destruction. Strategies focus on the modulation of tissue-destroying inflammatory host response, particularly the reduction of inflammation and promotion of resolution. Thereby, nutrition is a potent immunometabolic non-pharmacological intervention. Human studies have demonstrated the benefit of olive oil-containing Mediterranean-style diets (MDs), the main component of which being mono-unsaturated fatty acid (FA) oleic acid (OA (C18:1)). Hence, nutritional OA strengthened the microarchitecture of alveolar trabecular bone and increased circulating pro-resolving lipid mediators following bacterial inoculation with periodontal pathogen Porphyromonas gingivalis , contrary to saturated FA palmitic acid (PA (C16:0)), which is abundant in Western-style diets. Additionally, the generalized distribution of inflammatory pathway mediators can occur in response to bacterial infection and compromise systemic tissue metabolism and bone homeostasis distant from the side of infection. Whether specific FA-enriched nutrition and periodontal inoculation are factors in systemic pathology that can be immune-modulatory targeted through dietary substitution is unknown and of clinical relevance. Methods Normal-weight C57BL/6-mice received OA-or PA-enriched diets (PA-ED, OA-ED, PA/OA-ED) or a normal-standard diet (n=12/group) for 16 weeks and were orally infected with P. gingivalis /placebo to induce periodontal disease. Using histomorphometry and LC-MS/MS, systemic bone morphology, incorporated immunometabolic FA-species, serological markers of bone metabolism, and stress response were determined in addition to bone cell inflammation and interaction in vitro . Results In contrast to OA-ED, PA-ED reduced systemic bone microarchitecture paralleled by increased lipotoxic PA-containing metabolite accumulation in bone. Substitution with OA reversed the bone-destructive impact of PA, which was accompanied by reduced diacylglycerols (DAG) and saturated ceramide levels. Further, PA-associated reduction in mineralization activity and concomitant pro-inflammatory activation of primary osteoblasts were diminished in cultures where PA was replaced with OA, which impacted cellular interaction with osteoclasts. Additionally, PA-ED increased osteoclast numbers in femurs in response to oral P. gingivalis infection, whereas OA-ED reduced osteoclast occurrence, which was paralleled by serologically increased levels of the stress-reducing lipokine PI(18:1/18:1). Conclusion OA substitution reverses the bone-destructive and pro-inflammatory effects of PA and eliminates incorporated lipotoxic PA metabolites. This supports Mediterranean-style OA-based diets as a preventive intervention to target the accumulation of PA-associated lipotoxic metabolites and thereby supports systemic bone tissue resilience after oral bacterial P. gingivalis infection. Keywords: bone remodeling, regeneration, lipids, inflammation, nutrition, bone loss, periodontal disease

CITATION EXPORT

Annika Döding, Svenja Zimmermann, Ahmed Maghames et al.. Immunometabolic capacities of nutritional fatty acids in regulation of inflammatory bone cell interaction and systemic impact of periodontal infection. Frontiers in Immunology. (2023). https://doi.org/10.3389/fimmu.2023.1213026

AUTHORS

12 · 7 CENTRES

Annika Döding, Svenja Zimmermann, Ahmed Maghames, Michael Reimann, Judit Symmank, Maria Thürmer, Markus H Gräler, Michael Wolf, Collin Jacobs, Andreas Koeberle, Bernd Sigusch, Ulrike Schulze-Späte

1 Section of Geriodontics, Department of Conservative Dentistry and Periodontics, University Hospital Jena, Jena, Germany
2 Department of Orthodontics, University Hospital Jena, Jena, Germany
3 Chair of Pharmaceutical and Medicinal Chemistry, Institute of Pharmacy, Friedrich-Schiller-University Jena, Jena, Germany
4 Department of Anesthesiology and Intensive Care Medicine, Center for Molecular Biomedicine (CMB) and Center for Sepsis Control and Care (CSCC), Jena University Hospital, Jena, Germany
5 Department of Orthodontics, University Hospital RWTH Aachen, Aachen, Germany
6 Michael Popp Institute and Center for Molecular Biosciences Innsbruck (CMBI), University of Innsbruck, Innsbruck, Austria
7 Department of Conservative Dentistry and Periodontics, University Hospital Jena, Jena, Germany