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Cell Wall Mannan of Candida Attenuates Osteogenic Differentiation by Human Dental Pulp Cells

Published:December 28, 2022DOI:https://doi.org/10.1016/j.joen.2022.11.010

      Abstract

      Introduction

      Candida spp. has recently been introduced to interact with conventional carious bacteria, leading to dental caries progression and virulence ability. Evidence regarding the influence of Candida spp. on human dental pulp cell response remains unknown. This study aimed to investigate the effects of Candida albicans mannans on cytotoxicity, cell proliferation, osteogenic differentiation, and inflammatory-related gene expression in human dental pulp cells (hDPCs).

      Methods

      hDPCs were treated with cell wall mannans isolated from C. albicans, Candida krusei, Candida glabrata, Candida tropocalis, Candida parapsilosis, and Candida dubliniensis. Cell viability was performed using a 3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyl-2H-tetrazolium bromide assay. Osteogenic differentiation– and inflammatory-related gene expression were determined using a real-time polymerase chain reaction. Mineralization was examined using alizarin red S staining.

      Results

      The treatment of mannans isolated from C. albicans, C. krusei, C. glabrata, C. tropocalis, C. parapsilosis, and C. dubliniensis at concentrations ranging from 10–100 μg/mL did not affect cytotoxicity or cell proliferation. Mannans isolated from C. albicans, C. glabrata, and C. tropocalis significantly attenuated mineralization. However, cell wall mannans isolated from C. krusei, C. parapsilosis, and C. dubliniensis did not significantly influence mineral deposition in hDPCs. C. albicans cell wall mannans significantly attenuated osteogenic differentiation–related gene expression (RUNX2, ALP, and ENPP1). Interestingly, IL12 messenger RNA expression was significantly upregulated when treated with C. albicans cell wall mannans. The addition of recombinant IL12 significantly decreased mineralization in hDPCs.

      Conclusions

      C. albicans cell wall mannans attenuated osteogenic differentiation in hDPCs and up-regulated inflammatory-related gene IL12 expression.

      Key Words

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      References

        • Pereira D.
        • Seneviratne C.J.
        • Koga-Ito C.Y.
        • Samaranayake L.P.
        Is the oral fungal pathogen Candida albicans a cariogen?.
        Oral Dis. 2018; 24: 518-526
        • Lozano Moraga C.P.
        • Rodríguez Martínez G.A.
        • Lefimil Puente C.A.
        • et al.
        Prevalence of Candida albicans and carriage of Candida non-albicans in the saliva of preschool children, according to their caries status.
        Acta Odontol Scand. 2017; 75: 30-35
        • Caroline de Abreu Brandi T.
        • Portela M.B.
        • Lima P.M.
        • et al.
        Demineralizing potential of dental biofilm added with Candida albicans and Candida parapsilosis isolated from preschool children with and without caries.
        Microb Pathog. 2016; 100: 51-55
        • Thomas A.
        • Mhambrey S.
        • Chokshi K.
        • et al.
        Association of Oral Candida albicans with Severe Early Childhood Caries–A Pilot Study.
        J Clin Diagn Res. 2016; 10: Zc109-Zc112
        • Al-Ahmad A.
        • Auschill T.M.
        • Dakhel R.
        • et al.
        Prevalence of Candida albicans and Candida dubliniensis in caries-free and caries-active children in relation to the oral microbiota-a clinical study.
        Clin Oral Investig. 2016; 20: 1963-1971
        • Udayalaxmi J.
        • Shenoy N.
        Comparison between biofilm production, phospholipase and haemolytic activity of different species of Candida isolated from dental caries lesions in children.
        J Clin Diagn Res. 2016; 10: DC21-DC23
        • Hückelhoven R.
        Cell wall-associated mechanisms of disease resistance and susceptibility.
        Annu Rev Phytopathol. 2007; 45: 101-127
        • Gow N.A.
        • van de Veerdonk F.L.
        • Brown A.J.
        • Netea M.G.
        Candida albicans morphogenesis and host defence: discriminating invasion from colonization.
        Nat Rev Microbiol. 2011; 10: 112-122
        • Hall R.A.
        • Gow N.A.
        Mannosylation in Candida albicans: role in cell wall function and immune recognition.
        Mol Microbiol. 2013; 90: 1147-1161
        • Navarro-Arias M.J.
        • Defosse T.A.
        • Dementhon K.
        • et al.
        Disruption of protein mannosylation affects Candida guilliermondii cell wall, immune sensing, and virulence.
        Front Microbiol. 2016; 7: 1951
        • Estrada-Mata E.
        • Navarro-Arias M.J.
        • Pérez-García L.A.
        • et al.
        Members of the Candida parapsilosis complex and Candida albicans are differentially recognized by human peripheral blood mononuclear cells.
        Front Microbiol. 2015; 6: 1527
        • Podzorski R.P.
        • Herron M.J.
        • Fast D.J.
        • Nelson R.D.
        Pathogenesis of candidiasis. Immunosuppression by cell wall mannan catabolites.
        Arch Surg. 1989; 124: 1290-1294
        • Nelson R.D.
        • Shibata N.
        • Podzorski R.P.
        • Herron M.J.
        Candida mannan: chemistry, suppression of cell-mediated immunity, and possible mechanisms of action.
        Clin Microbiol Rev. 1991; 4: 1-19
        • Brown G.D.
        Innate antifungal immunity: the key role of phagocytes.
        Annu Rev Immunol. 2011; 29: 1-21
        • Brubaker S.W.
        • Bonham K.S.
        • Zanoni I.
        • Kagan J.C.
        Innate immune pattern recognition: a cell biological perspective.
        Annu Rev Immunol. 2015; 33: 257-290
        • Sancho D.
        • Reis e Sousa C.
        Signaling by myeloid C-type lectin receptors in immunity and homeostasis.
        Annu Rev Immunol. 2012; 30: 491-529
        • Kocourek J.
        • Ballou C.E.
        Method for fingerprinting yeast cell wall mannans.
        J Bacteriol. 1969; 100: 1175-1181
        • Nguyen T.N.Y.
        • Matangkasombut O.
        • Ritprajak P.
        Differential dendritic cell responses to cell wall mannan of Candida albicans, Candida parapsilosis, and Candida dubliniensis.
        J Oral Sci. 2018; 60: 557-566
        • Nguyen T.N.Y.
        • Padungros P.
        • Wongsrisupphakul P.
        • et al.
        Cell wall mannan of Candida krusei mediates dendritic cell apoptosis and orchestrates Th17 polarization via TLR-2/MyD88-dependent pathway.
        Sci Rep. 2018; 8: 17123
        • Masuko T.
        • Minami A.
        • Iwasaki N.
        • et al.
        Carbohydrate analysis by a phenol-sulfuric acid method in microplate format.
        Anal Biochem. 2005; 339: 69-72
        • Kim H.E.
        • Liu Y.
        • Dhall A.
        • et al.
        Synergism of Streptococcus mutans and Candida albicans reinforces biofilm maturation and acidogenicity in saliva: an In Vitro Study.
        Front Cell Infect Microbiol. 2020; 10: 623980
        • Liu Y.
        • Gao Y.
        • Zhan X.
        • et al.
        TLR4 activation by lipopolysaccharide and Streptococcus mutans induces differential regulation of proliferation and migration in human dental pulp stem cells.
        J Endod. 2014; 40: 1375-1381
        • Shayegan A.
        • Zucchi A.
        • De Swert K.
        • et al.
        Lipoteichoic acid stimulates the proliferation, migration and cytokine production of adult dental pulp stem cells without affecting osteogenic differentiation.
        Int Endod J. 2021; 54: 585-600
        • Cai S.
        • Zhang W.
        • Tribble G.
        • Chen W.
        Reactions of human dental pulp cells to capping agents in the presence or absence of bacterial exposure.
        J Oral Sci. 2017; 59: 621-627
        • Abe S.
        • Imaizumi M.
        • Mikami Y.
        • et al.
        Oral bacterial extracts facilitate early osteogenic/dentinogenic differentiation in human dental pulp-derived cells.
        Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2010; 109: 149-154
        • Diomede F.
        • Caputi S.
        • Merciaro I.
        • et al.
        Pro-inflammatory cytokine release and cell growth inhibition in primary human oral cells after exposure to endodontic sealer.
        Int Endod J. 2014; 47: 864-872
        • Egusa H.
        • Nikawa H.
        • Makihira S.
        • et al.
        In vitro mechanisms of interleukin-8-mediated responses of human gingival epithelial cells to Candida albicans infection.
        Int J Med Microbiol. 2006; 296: 301-311
        • Santos M.
        • Castro H.H.O.
        • Magalhaes L.M.D.
        • et al.
        Resinous adhesive systems differentially affect the expression of cytokines by human monocytes stimulated or not with Streptococcus mutans in vitro.
        Arch Oral Biol. 2020; 111: 104641
        • Neiva K.G.
        • Catalfamo D.L.
        • Holliday L.S.
        • et al.
        Propolis decreases lipopolysaccharide-induced inflammatory mediators in pulp cells and osteoclasts.
        Dent Traumatol. 2014; 30: 362-367
        • Colombini-Ishikiriama B.L.
        • Dionisio T.J.
        • Garbieri T.F.
        • et al.
        What is the response profile of deciduous pulp fibroblasts stimulated with E. coli LPS and E. faecalis LTA?.
        BMC Immunol. 2020; 21: 38
        • Nagata N.
        • Kitaura H.
        • Yoshida N.
        • Nakayama K.
        Inhibition of RANKL-induced osteoclast formation in mouse bone marrow cells by IL-12: involvement of IFN-gamma possibly induced from non-T cell population.
        Bone. 2003; 33: 721-732
        • Morita Y.
        • Kitaura H.
        • Yoshimatsu M.
        • et al.
        IL-18 inhibits TNF-alpha-induced osteoclastogenesis possibly via a T cell-independent mechanism in synergy with IL-12 in vivo.
        Calcif Tissue Int. 2010; 86: 242-248
        • Amarasekara D.S.
        • Kim S.
        • Rho J.
        Regulation of osteoblast differentiation by cytokine networks.
        Int J Mol Sci. 2021; 22: 2851
        • Xu J.
        • Wang Y.
        • Li J.
        • et al.
        IL-12p40 impairs mesenchymal stem cell-mediated bone regeneration via CD4(+) T cells.
        Cell Death Differ. 2016; 23: 1941-1951
        • Issaranggun Na Ayuthaya B.
        • Satravaha P.
        • Pavasant P.
        Interleukin-12 modulates the immunomodulatory properties of human periodontal ligament cells.
        J Periodontal Res. 2017; 52: 546-555