Mucosal-associated invariant T cells and oral microbiome in persistent apical periodontitis

Haleh Davanian , Rogier Aäron Gaiser , Mikael Silfverberg , Luisa W. Hugerth , Michał J. Sobkowiak , Liyan Lu , Katie Healy , Johan K. Sandberg , Peggy Näsman , Jörgen Karlsson , Leif Jansson , Lars Engstrand , Margaret Sällberg Chen

International Journal of Oral Science ›› 2019, Vol. 11 ›› Issue (2) : 16

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International Journal of Oral Science ›› 2019, Vol. 11 ›› Issue (2) : 16 DOI: 10.1038/s41368-019-0049-y
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Mucosal-associated invariant T cells and oral microbiome in persistent apical periodontitis

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Abstract

Opportunistic bacteria in apical periodontitis (AP) may pose a risk for systemic dissemination. Mucosal-associated invariant T (MAIT) cells are innate-like T cells with a broad and potent antimicrobial activity important for gut mucosal integrity. It was recently shown that MAIT cells are present in the oral mucosal tissue, but the involvement of MAIT cells in AP is unknown. Here, comparison of surgically resected AP and gingival tissues demonstrated that AP tissues express significantly higher levels of Vα7.2-Jα33, Vα7.2-Jα20, Vα7.2-Jα12, Cα and tumour necrosis factor (TNF), interferon (IFN)-γ and interleukin (IL)-17A transcripts, resembling a MAIT cell signature. Moreover, in AP tissues the MR1-restricted MAIT cells positive for MR1–5-OP-RU tetramer staining appeared to be of similar levels as in peripheral blood but consisted mainly of CD4+ subset. Unlike gingival tissues, the AP microbiome was quantitatively impacted by factors like fistula and high patient age and had a prominent riboflavin-expressing bacterial feature. When merged in an integrated view, the examined immune and microbiome data in the sparse partial least squares discriminant analysis could identify bacterial relative abundances that negatively correlated with Vα7.2-Jα33, Cα, and IL-17A transcript expressions in AP, implying that MAIT cells could play a role in the local defence at the oral tissue barrier. In conclusion, we describe the presence of MAIT cells at the oral site where translocation of oral microbiota could take place. These findings have implications for understanding the immune sensing of polymicrobial-related oral diseases.

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Haleh Davanian, Rogier Aäron Gaiser, Mikael Silfverberg, Luisa W. Hugerth, Michał J. Sobkowiak, Liyan Lu, Katie Healy, Johan K. Sandberg, Peggy Näsman, Jörgen Karlsson, Leif Jansson, Lars Engstrand, Margaret Sällberg Chen. Mucosal-associated invariant T cells and oral microbiome in persistent apical periodontitis. International Journal of Oral Science, 2019, 11(2): 16 DOI:10.1038/s41368-019-0049-y

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References

[1]

Huumonen S, Vehkalahti MM, Nordblad A. Radiographic assessments on prevalence and technical quality of endodontically-treated teeth in the Finnish population, aged 30 years and older. Acta Odontol. Scand., 2012, 70: 234-240.

[2]

Dutta A, Smith-Jack F, Saunders WP. Prevalence of periradicular periodontitis in a Scottish subpopulation found on CBCT images. Int. Endod. J., 2014, 47: 854-863.

[3]

Pak JG, Fayazi S, White SN. Prevalence of periapical radiolucency and root canal treatment: a systematic review of cross-sectional studies. J. Endod., 2012, 38: 1170-1176.

[4]

Huumonen S, Suominen AL, Vehkalahti MM. Prevalence of apical periodontitis in root filled teeth: findings from a nationwide survey in Finland. Int. Endod. J., 2017, 50: 229-236.

[5]

van der Waal SV, Lappin DF, Crielaard W. Does apical periodontitis have systemic consequences? The need for well-planned and carefully conducted clinical studies. Br. Dent. J., 2015, 218: 513-516.

[6]

Siqueira JF Jr., Rocas IN. Microbiology and treatment of acute apical abscesses. Clin. Microbiol. Rev., 2013, 26: 255-273.

[7]

Pessi T, . Bacterial signatures in thrombus aspirates of patients with myocardial infarction. Circulation, 2013, 127: 1219-1228. e1211-1216

[8]

Cotti E, Dessi C, Piras A, Mercuro G. Can a chronic dental infection be considered a cause of cardiovascular disease? A review of the literature. Int. J. Cardiol., 2011, 148: 4-10.

[9]

Treiner E, . Selection of evolutionarily conserved mucosal-associated invariant T cells by MR1. Nature, 2003, 422: 164-169.

[10]

Corbett AJ, . T-cell activation by transitory neo-antigens derived from distinct microbial pathways. Nature, 2014, 509: 361-365.

[11]

Kjer-Nielsen L, . MR1 presents microbial vitamin B metabolites to MAIT cells. Nature, 2012, 491: 717-723.

[12]

Ussher JE, Klenerman P, Willberg CB. Mucosal-associated invariant T-cells: new players in anti-bacterial immunity. Front. Immunol., 2014, 5: 450.

[13]

Mondot S, Boudinot P, Lantz O. MAIT, MR1, microbes and riboflavin: a paradigm for the co-evolution of invariant TCRs and restricting MHCI-like molecules?. Immunogenetics, 2016, 68: 537-548.

[14]

Salou M, Franciszkiewicz K, Lantz O. MAIT cells in infectious diseases. Curr. Opin. Immunol., 2017, 48: 7-14.

[15]

Sobkowiak MJ, . Tissue-resident MAIT cell populations in human oral mucosa exhibit an activated profile and produce IL-17. Eur. J. Immunol., 2018, 49: 133-143.

[16]

Berkson JD, Prlic M. The MAIT conundrum - how human MAIT cells distinguish bacterial colonization from infection in mucosal barrier tissues. Immunol. Lett., 2017, 192: 7-11.

[17]

Dias J, Leeansyah E, Sandberg JK. Multiple layers of heterogeneity and subset diversity in human MAIT cell responses to distinct microorganisms and to innate cytokines. Proc. Natl Acad. Sci. USA, 2017, 114: E5434-E5443.

[18]

Le Bourhis L, . Antimicrobial activity of mucosal-associated invariant T cells. Nat. Immunol., 2010, 11: 701-708.

[19]

Segata N, . Metagenomic biomarker discovery and explanation. Genome Biol., 2011, 12

[20]

Garcia-Angulo VA. Overlapping riboflavin supply pathways in bacteria. Crit. Rev. Microbiol., 2017, 43: 196-209.

[21]

Langille MG, . Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat. Biotechnol., 2013, 31: 814-821.

[22]

Le Cao KA, Boitard S, Besse P, Sparse PLS. Discriminant analysis: biologically relevant feature selection and graphical displays for multiclass problems. BMC Bioinforma., 2011, 12

[23]

Colic M, . Regulatory T-cells in periapical lesions. J. Dent. Res., 2009, 88: 997-1002.

[24]

He M, Song G, Yu Y, Jin Q, Bian Z. LPS-miR-34a-CCL22 axis contributes to regulatory T cell recruitment in periapical lesions. Biochem. Biophys. Res. Commun., 2015, 460: 733-740.

[25]

AlShwaimi E, . IL-17 receptor A signaling is protective in infection-stimulated periapical bone destruction. J. Immunol., 2013, 191: 1785-1791.

[26]

de Vries TJ, Andreotta S, Loos BG, Nicu EA. Genes critical for developing periodontitis: Lessons from mouse models. Front. Immunol., 2017, 8: 1395.

[27]

Konkel JE, Moutsopoulos NM. Unique tailoring of Th17 at the gingival oral mucosal barrier. J. Dent. Res., 2018, 97: 128-131.

[28]

Weaver CT, Elson CO, Fouser LA, Kolls JK. The Th17 pathway and inflammatory diseases of the intestines, lungs, and skin. Annu. Rev. Pathol., 2013, 8: 477-512.

[29]

Walker LJ, . Human MAIT and CD8alphaalpha cells develop from a pool of type-17 precommitted CD8 + T cells. Blood, 2012, 119: 422-433.

[30]

Leeansyah E, . Activation, exhaustion, and persistent decline of the antimicrobial MR1-restricted MAIT-cell population in chronic HIV-1 infection. Blood, 2013, 121: 1124-1135.

[31]

Leeansyah E, Loh L, Nixon DF, Sandberg JK. Acquisition of innate-like microbial reactivity in mucosal tissues during human fetal MAIT-cell development. Nat. Commun., 2014, 5

[32]

Meierovics A, Yankelevich WJ, Cowley SC. MAIT cells are critical for optimal mucosal immune responses during in vivo pulmonary bacterial infection. Proc. Natl Acad. Sci. USA, 2013, 110: E3119-E3128.

[33]

Siqueira Jr José F., Rôças Isabela N.. Distinctive features of the microbiota associated with different forms of apical periodontitis. Journal of Oral Microbiology, 2009, 1(1): 2009.

[34]

Siqueira JF Jr., Rocas IN, Ricucci D, Hulsmann M. Causes and management of post-treatment apical periodontitis. Br. Dent. J., 2014, 216: 305-312.

[35]

Zakaria MN, . Microbial community in persistent apical periodontitis: a 16S rRNA gene clone library analysis. Int. Endod. J., 2015, 48: 717-728.

[36]

Siqueira JF Jr., Antunes HS, Rocas IN, Rachid CT, Alves FR. Microbiome in the apical root canal system of teeth with post-treatment apical periodontitis. PLoS ONE, 2016, 11

[37]

Glass RT, Bullard JW, Hadley CS, Mix EW, Conrad RS. Partial spectrum of microorganisms found in dentures and possible disease implications. J. Am. Osteopath. Assoc., 2001, 101: 92-94.

[38]

Subramanian K, Mickel AK. Molecular analysis of persistent periradicular lesions and root ends reveals a diverse microbial profile. J. Endod., 2009, 35: 950-957.

[39]

Diaz PI, . Transplantation-associated long-term immunosuppression promotes oral colonization by potentially opportunistic pathogens without impacting other members of the salivary bacteriome. Clin. Vaccin. Immunol., 2013, 20: 920-930.

[40]

Scales BS, Dickson RP, LiPuma JJ, Huffnagle GB. Microbiology, genomics, and clinical significance of the Pseudomonas fluorescens species complex, an unappreciated colonizer of humans. Clin. Microbiol. Rev., 2014, 27: 927-948.

[41]

Provenzano JC, . Host-bacterial interactions in post-treatment apical periodontitis: A metaproteome analysis. J. Endod., 2016, 42: 880-885.

[42]

Nonnenmacher C, Dalpke A, Mutters R, Heeg K. Quantitative detection of periodontopathogens by real-time PCR. J. Microbiol Methods, 2004, 59: 117-125.

[43]

Herlemann DP, . Transitions in bacterial communities along the 2000 km salinity gradient of the Baltic Sea. ISME J., 2011, 5: 1571-1579.

[44]

Edgar RC, Flyvbjerg H. Error filtering, pair assembly and error correction for next-generation sequencing reads. Bioinformatics, 2015, 31: 3476-3482.

[45]

DeSantis TZ, . Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl. Environ. Microbiol., 2006, 72: 5069-5072.

[46]

Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics, 2010, 26: 2460-2461.

[47]

Chen T, . The Human Oral Microbiome Database: a web accessible resource for investigating oral microbe taxonomic and genomic information. Database (Oxf.)., 2010, 2010: baq013.

[48]

Pruesse E, Peplies J, Glockner FO. SINA: accurate high-throughput multiple sequence alignment of ribosomal RNA genes. Bioinformatics, 2012, 28: 1823-1829.

[49]

Quast C, . The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucl. Acids Res., 2013, 41: D590-D596.

[50]

Oksanen, J. et al. The Vegan Package (Community ecology package) Version 2.4-1 https://github.com/vegandevs/vegan R-Forge. (2016).

[51]

Rohart F, Gautier B, Singh A, Le Cao K. A. mixOmics: An R package for ‘omics feature selection and multiple data integration. PLoS Comput. Biol., 2017, 13

[52]

Magnusdottir S, Ravcheev D, de Crecy-Lagard V, Thiele I. Systematic genome assessment of B-vitamin biosynthesis suggests co-operation among gut microbes. Front. Genet., 2015, 6: 148.

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