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Article

Vesicular Messages from Dental Biofilms for Neutrophils

by
Ljubomir Vitkov
1,2,3,
Jelena Krunić
1,
Johanna Dudek
2,
Madhusudhan Reddy Bobbili
4,5,
Johannes Grillari
4,5,
Bernhard Hausegger
3,
Irena Mladenović
6,7,
Nikola Stojanović
6,7,
Wolf Dietrich Krautgartner
3,
Hannah Oberthaler
3,
Christine Schauer
8,9,
Martin Herrmann
8,9,
Jeeshan Singh
8,9,
Bernd Minnich
3,† and
Matthias Hannig
2,*,†
1
Department of Dental Pathology, Faculty of Medicine, University of East Sarajevo, 73300 Foča, Bosnia and Herzegovina
2
Clinic of Operative Dentistry, Periodontology and Preventive Dentistry, Saarland University, 664241 Homburg, Germany
3
Department of Environment & Biodiversity, University of Salzburg, 5020 Salzburg, Austria
4
Ludwig Boltzmann Institute for Traumatology, Research Center in Cooperation with AUVA, 1200 Vienna, Austria
5
Department of Biotechnology, Institute of Molecular Biotechnology, University of Natural Resources and Life Sciences (BOKU University), 1190 Vienna, Austria
6
Department of Oral Rehabilitation, Faculty of Medicine, University of East Sarajevo, 73300 Foča, Bosnia and Herzegovina
7
Center for Biomedical Science, Faculty of Medicine, University of East Sarajevo, 73300 Foča, Bosnia and Herzegovina
8
Department of Internal Medicine 3—Rheumatology and Immunology, Universitätsklinikum Erlangen, Friedrich-Alexander-University Erlangen-Nürnberg (FAU), 91054 Erlangen, Germany
9
Deutsches Zentrum für Immuntherapie (DZI), Universitätsklinikum Erlangen, Friedrich-Alexander-University Erlangen-Nürnberg (FAU), 91054 Erlangen, Germany
*
Author to whom correspondence should be addressed.
†
B.M. and M.H. (Matthias Hannig) share senior authorship.
Int. J. Mol. Sci. 2024, 25(6), 3314; https://doi.org/10.3390/ijms25063314
Submission received: 5 February 2024 / Revised: 9 March 2024 / Accepted: 12 March 2024 / Published: 14 March 2024
(This article belongs to the Special Issue Neutrophil Extracellular Traps (NETs) in Immunity and Diseases: 2nd Edition)
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Abstract

The encounter between dental biofilm and neutrophils in periodontitis remains elusive, although it apparently plays a crucial role in the periodontal pathology and constitutes a key topic of periodontology. Dental biofilm and neutrophils were isolated from orally healthy persons and patients with periodontitis. We investigated biofilm and its particle-shedding phenomenon with electron microscopy and nanoparticle tracking analysis (NTA); biofilm shedding–neutrophil interactions were examined ex vivo with epi-fluorescence microscopy. For this purpose, we used acellular dental biofilm shedding, purified lipopolysaccharide (LPS), and phorbol 12-myristate 13-acetate (PMA) as activators, and the interleukin 8 receptor beta (CXCR2) inhibitor and the anti-interleukin 8 receptor alpha (CXCR1) antibody as modulators. The shedding of acellular dental biofilms overwhelmingly consists of bacterial extracellular vesicles (BEVs). The latter induced the moderate formation of neutrophil extracellular traps (NETs) in orally healthy subjects and a strong formation in patients with periodontitis. A CXCR2 inhibitor and an anti-CXCR1 antibody had a minor effect on NET formation. Neutrophils from patients with periodontitis exhibited NET hyper-responsiveness. BEVs were stronger inducers of NET formation than purified LPS and PMA. A plateau of neutrophil responsiveness is reached above the age of 40 years, indicating the abrupt switch of maladaptive trained immunity (TI) into the activated modus. Our results suggest that dental biofilms consist of and disseminate immense amounts of outer membrane vesicles (OMVs), which initiate NET formation via a non-canonical cytosolic LPS/caspase-4/11/Gasdermin D pathway. This modus of NET formation is independent of neutrophil elastase (NE), myeloperoxidase (MPO), peptidylarginine deiminase 4 (PAD4), and toll-like receptors (TLR). In periodontitis, the hyper-responsiveness of neutrophils to BEVs and the increased NET formation appear to be a consequence of TI.
Keywords: periodontitis; dental biofilm; bacterial extracellular vesicles; outer membrane vesicles; caspase 4; trained immunity periodontitis; dental biofilm; bacterial extracellular vesicles; outer membrane vesicles; caspase 4; trained immunity

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MDPI and ACS Style

Vitkov, L.; Krunić, J.; Dudek, J.; Bobbili, M.R.; Grillari, J.; Hausegger, B.; Mladenović, I.; Stojanović, N.; Krautgartner, W.D.; Oberthaler, H.; et al. Vesicular Messages from Dental Biofilms for Neutrophils. Int. J. Mol. Sci. 2024, 25, 3314. https://doi.org/10.3390/ijms25063314

AMA Style

Vitkov L, Krunić J, Dudek J, Bobbili MR, Grillari J, Hausegger B, Mladenović I, Stojanović N, Krautgartner WD, Oberthaler H, et al. Vesicular Messages from Dental Biofilms for Neutrophils. International Journal of Molecular Sciences. 2024; 25(6):3314. https://doi.org/10.3390/ijms25063314

Chicago/Turabian Style

Vitkov, Ljubomir, Jelena Krunić, Johanna Dudek, Madhusudhan Reddy Bobbili, Johannes Grillari, Bernhard Hausegger, Irena Mladenović, Nikola Stojanović, Wolf Dietrich Krautgartner, Hannah Oberthaler, and et al. 2024. "Vesicular Messages from Dental Biofilms for Neutrophils" International Journal of Molecular Sciences 25, no. 6: 3314. https://doi.org/10.3390/ijms25063314

APA Style

Vitkov, L., Krunić, J., Dudek, J., Bobbili, M. R., Grillari, J., Hausegger, B., Mladenović, I., Stojanović, N., Krautgartner, W. D., Oberthaler, H., Schauer, C., Herrmann, M., Singh, J., Minnich, B., & Hannig, M. (2024). Vesicular Messages from Dental Biofilms for Neutrophils. International Journal of Molecular Sciences, 25(6), 3314. https://doi.org/10.3390/ijms25063314

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