Prevotella melaninogenica disrupted oral epithelial barrier function via myosin light chain kinase.
Prevotella melaninogenica
RNA‐seq
myosin light chain kinase
oral lichen planus
Journal
Oral diseases
ISSN: 1601-0825
Titre abrégé: Oral Dis
Pays: Denmark
ID NLM: 9508565
Informations de publication
Date de publication:
08 May 2024
08 May 2024
Historique:
revised:
04
11
2023
received:
15
06
2023
accepted:
22
04
2024
medline:
9
5
2024
pubmed:
9
5
2024
entrez:
9
5
2024
Statut:
aheadofprint
Résumé
Our previous studies have found that the composition ratio of Prevotella melaninogenica (Pm) on buccal mucosa surface of oral lichen planus (OLP) patients increased significantly compared with control. Furthermore, Pm could invade the epithelium of OLP patients. This study aimed to further explore the impact of Pm on oral keratinocytes. The Pm-human oral keratinocyte (HOK) co-culture model was established to detect monolayer permeability, zona occludens-1 (ZO-1) expression, and intracellular survival of Pm. We performed RNA-seq followed by identification of differentially expressed genes (DEGs) and Gene Ontology (GO) analysis, with a particular focus on myosin light chain kinase (MLCK). An MLCK inhibitor ML-7 was utilized in Pm-HOK co-culture model to assess its effects on monolayer permeability and ZO-1 expression. HOK monolayer permeability was increased, and ZO-1 expression was decreased after co-culture (p < 0.05). Pm could survive in HOK cells. RNA-seq revealed MLCK was an upregulated common DEG. The expression of MLCK in the Pm-HOK co-culture model was upregulated. Inhibition of MLCK rescued the increased epithelial permeability, and ZO-1 expression was upregulated (p < 0.05). MLCK may be involved in disrupting epithelial barrier function by Pm.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : National Natural Science Foundation of China
Informations de copyright
© 2024 Wiley Periodicals LLC.
Références
Aas, J. A., Paster, B. J., Stokes, L. N., Olsen, I., & Dewhirst, F. E. (2005). Defining the normal bacterial flora of the oral cavity. Journal of Clinical Microbiology, 43(11), 5721–5732. https://doi.org/10.1128/JCM.43.11.5721‐5732.2005
Blair, S. A., Kane, S. V., Clayburgh, D. R., & Turner, J. R. (2006). Epithelial myosin light chain kinase expression and activity are upregulated in inflammatory bowel disease. Laboratory Investigation, 86(2), 191–201. https://doi.org/10.1038/labinvest.3700373
Choi, Y. S., Kim, Y., Yoon, H.‐J., Baek, K. J., Alam, J., Park, H. K., & Choi, Y. (2016). The presence of bacteria within tissue provides insights into the pathogenesis of oral lichen planus. Scientific Reports, 6(1), 29186. https://doi.org/10.1038/srep29186
Cong, X., & Kong, W. (2020). Endothelial tight junctions and their regulatory signaling pathways in vascular homeostasis and disease. Cellular Signalling, 66, 109485. https://doi.org/10.1016/j.cellsig.2019.109485
Du, G.‐H., Wang, Y.‐F., Chen, J.‐J., Deng, Y.‐W., Han, X.‐Z., & Tang, G.‐Y. (2020). Potential association between Fusobacterium nucleatum enrichment on oral mucosal surface and oral lichen planus. Oral Diseases, 26(1), 122–130. https://doi.org/10.1111/odi.13232
Eutamene, H., Theodorou, V., Schmidlin, F., Tondereau, V., Garcia‐Villar, R., Salvador‐Cartier, C., Chovet, M., Bertrand, C., & Bueno, L. (2005). LPS‐induced lung inflammation is linked to increased epithelial permeability: Role of MLCK. European Respiratory Journal, 25(5), 789–796. https://doi.org/10.1183/09031936.05.00064704
Ghaisas, S., Maher, J., & Kanthasamy, A. (2016). Gut microbiome in health and disease: Linking the microbiome‐gut‐brain axis and environmental factors in the pathogenesis of systemic and neurodegenerative diseases. Pharmacology & Therapeutics, 158, 52–62. https://doi.org/10.1016/j.pharmthera.2015.11.012
Groeger, S. E., & Meyle, J. (2015). Epithelial barrier and oral bacterial infection. Periodontology 2000, 69(1), 46–67. https://doi.org/10.1111/prd.12094
Guhathakurta, P., Prochniewicz, E., & Thomas, D. D. (2018). Actin‐myosin interaction: Structure, function and drug discovery. International Journal of Molecular Sciences, 19(9), 2628. https://doi.org/10.3390/ijms19092628
Guo, S., Chen, S., Ma, J., Ma, Y., Zhu, J., Ma, Y., Liu, Y., Wang, P., & Pan, Y. (2019). Escherichia coli Nissle 1917 protects intestinal barrier function by inhibiting NF‐κB‐mediated activation of the MLCK‐P‐MLC signaling pathway. Mediators of Inflammation, 2019, 1–13. https://doi.org/10.1155/2019/5796491
Guo, Y., Han, W., Xu, P., Shao, R., & He, Y. (2022). (2022) transcriptome analysis of primary human oral keratinocytes stimulated with Prevotella melaninogenica. Journal of Prevention and Treatment for Stomatological Diseases, 30(9), 620–629. https://doi.org/10.12016/j.issn.2096‐1456.2022.09.002
Haas, A. J., Zihni, C., Ruppel, A., Hartmann, C., Ebnet, K., Tada, M., Balda, M. S., & Matter, K. (2020). Interplay between extracellular matrix stiffness and JAM‐A regulates mechanical load on ZO‐1 and tight junction assembly. Cell Reports, 32(3), 107924. https://doi.org/10.1016/j.celrep.2020.107924
Hämäläinen, L., Soini, Y., Pasonen‐Seppänen, S., & Siponen, M. (2019). Alterations in the expression of EMT‐related proteins claudin‐1, claudin‐4 and claudin‐7, E‐cadherin, TWIST1 and ZEB1 in oral lichen planus. Journal of Oral Pathology & Medicine, 48(8), 735–744. https://doi.org/10.1111/jop.12917
He, W.‐Q., Wang, J., Sheng, J.‐Y., Zha, J.‐M., Graham, W. V., & Turner, J. R. (2020). Contributions of myosin light chain kinase to regulation of epithelial Paracellular permeability and mucosal homeostasis. International Journal of Molecular Sciences, 21(3), 993. https://doi.org/10.3390/ijms21030993
He, Y., Gong, D., Shi, C., Shao, F., Shi, J., & Fei, J. (2017). Dysbiosis of oral buccal mucosa microbiota in patients with oral lichen planus. Oral Diseases, 23(5), 674–682. https://doi.org/10.1111/odi.12657
Hooper, L. V., Littman, D. R., & Macpherson, A. J. (2012). Interactions between the microbiota and the immune system. Science, 336(6086), 1268–1273. https://doi.org/10.1126/science.1223490
Ivanov, A. I., Parkos, C. A., & Nusrat, A. (2010). Cytoskeletal regulation of epithelial barrier function during inflammation. The American Journal of Pathology, 177(2), 512–524. https://doi.org/10.2353/ajpath.2010.100168
Johansson, M. E. V., Gustafsson, J. K., Holmén‐Larsson, J., Jabbar, K. S., Xia, L., Xu, H., Ghishan, F. K., Carvalho, F. A., Gewirtz, A. T., Sjövall, H., & Hansson, G. C. (2014). Bacteria penetrate the normally impenetrable inner colon mucus layer in both murine colitis models and patients with ulcerative colitis. Gut, 63(2), 281–291. https://doi.org/10.1136/gutjnl‐2012‐303207
Kamaguchi, M., Iwata, H., Miyauchi, T., Ujiie, H., Ujiie, I., Nomura, T., Ohga, N., Shimizu, H., & Kitagawa, Y. (2019). The identification of autoantigens in mucous membrane pemphigoid using immortalized oral mucosal keratinocytes. Journal of Oral Pathology & Medicine, 48(1), 60–67. https://doi.org/10.1111/jop.12780
Kim, M., Lee, S.‐W., Kim, J., Shin, Y., Chang, F., Kim, J. M., Cong, X., Yu, G.‐Y., & Park, K. (2021). LPS‐induced epithelial barrier disruption via hyperactivation of CACC and ENaC. American Journal of Physiology, 320, C448–C461. https://doi.org/10.1152/ajpcell.00295.2020
Kuehl, C. J., Dragoi, A.‐M., Talman, A., & Agaisse, H. (2015). Bacterial spread from cell to cell: Beyond Actin‐based motility. Trends in Microbiology, 23(9), 558–566. https://doi.org/10.1016/j.tim.2015.04.010
Lathrop, S. K., Bloom, S. M., Rao, S. M., Nutsch, K., Lio, C.‐W., Santacruz, N., Peterson, D. A., Stappenbeck, T. S., & Hsieh, C.‐S. (2011). Peripheral education of the immune system by colonic commensal microbiota. Nature, 478(7368), 250–254. https://doi.org/10.1038/nature10434
Li, Y., Li, X., Geng, C., Guo, Y., & Wang, C. (2021). Somatostatin receptor 5 is critical for protecting intestinal barrier function in vivo and in vitro. Molecular and Cellular Endocrinology, 535, 111390. https://doi.org/10.1016/j.mce.2021.111390
Li, Y., Wang, K., Zhang, B., Tu, Q., Yao, Y., Cui, B., Ren, B., He, J., Shen, X., Van Nostrand, J. D., Zhou, J., Shi, W., Xiao, L., Lu, C., & Zhou, X. (2019). Salivary mycobiome dysbiosis and its potential impact on bacteriome shifts and host immunity in oral lichen planus. International Journal of Oral Science, 11(2), 13. https://doi.org/10.1038/s41368‐019‐0045‐2
Ma, K., Lv, P., & Li, G. (2015). Relationship between black‐pigmented bacteria and dental pulp infections. Chinese Journal of Nosocomiology, 2015(22), 5234–5235+5246.
Mager, D. L., Haffajee, A. D., Devlin, P. M., Norris, C. M., Posner, M. R., & Goodson, J. M. (2005). The salivary microbiota as a diagnostic indicator of oral cancer: A descriptive, non‐randomized study of cancer‐free and oral squamous cell carcinoma subjects. Journal of Translational Medicine, 3, 27. https://doi.org/10.1186/1479‐5876‐3‐27
Mager, D. L., Ximenez‐Fyvie, L. A., Haffajee, A. D., & Socransky, S. S. (2003). Distribution of selected bacterial species on intraoral surfaces. Journal of Clinical Periodontology, 30(7), 644–654. https://doi.org/10.1034/j.1600‐051x.2003.00376.x
Martens, E. C., Neumann, M., & Desai, M. S. (2018). Interactions of commensal and pathogenic microorganisms with the intestinal mucosal barrier. Nature Reviews. Microbiology, 16(8), 457–470. https://doi.org/10.1038/s41579‐018‐0036‐x
Matsuda, G. (1983). The light chains of muscle myosin: Its structure, function, and evolution. Advances in Biophysics, 16, 185–218. https://doi.org/10.1016/0065‐227x(83)90009‐6
Monack, D. M., & Theriot, J. A. (2001). Actin‐based motility is sufficient for bacterial membrane protrusion formation and host cell uptake. Cellular Microbiology, 3(9), 633–647. https://doi.org/10.1046/j.1462‐5822.2001.00143.x
Oda, D., & Watson, E. (1990). Human oral epithelial cell culture I. Improved conditions for reproducible culture in serum‐free medium. In Vitro Cellular & Developmental Biology, 26(6), 589–595. https://doi.org/10.1007/BF02624208
Pai, Y.‐C., Weng, L.‐T., Wei, S.‐C., Wu, L.‐L., Shih, D. Q., Targan, S. R., Turner, J. R., & Yu, L. C.‐H. (2020). Gut microbial transcytosis induced by tumor necrosis factor‐like 1A‐dependent activation of a myosin light chain kinase splice variant contributes to IBD. Journal of Crohn's & Colitis, jjaa165, 258–272. https://doi.org/10.1093/ecco‐jcc/jjaa165
Roopashree, M. R., Gondhalekar, R. V., Shashikanth, M. C., George, J., Thippeswamy, S. H., & Shukla, A. (2010). Pathogenesis of oral lichen planus – A review. Journal of Oral Pathology & Medicine, 39(10), 729–734. https://doi.org/10.1111/j.1600‐0714.2010.00946.x
Rottner, K., Faix, J., Bogdan, S., Linder, S., & Kerkhoff, E. (2017). Actin assembly mechanisms at a glance. Journal of Cell Science, 130(20), 3427–3435. https://doi.org/10.1242/jcs.206433
Sayoc‐Becerra, A., Krishnan, M., Fan, S., Jimenez, J., Hernandez, R., Gibson, K., Preciado, R., Butt, G., & McCole, D. F. (2020). The JAK‐inhibitor Tofacitinib rescues human intestinal epithelial cells and Colonoids from cytokine‐induced barrier dysfunction. Inflammatory Bowel Diseases, 26(3), 407–422. https://doi.org/10.1093/ibd/izz266
Schmidt, B. L., Kuczynski, J., Bhattacharya, A., Huey, B., Corby, P. M., Queiroz, E. L. S., Nightingale, K., Kerr, A. R., DeLacure, M. D., Veeramachaneni, R., Olshen, A. B., Albertson, D. G., & Teh, M.‐T. (2014). Changes in abundance of Oral microbiota associated with Oral cancer. PLoS One, 9(6), e98741. https://doi.org/10.1371/journal.pone.0098741
Shen, L. (2012). Tight junctions on the move: Molecular mechanisms for epithelial barrier regulation. Annals of the New York Academy of Sciences, 1258(1), 9–18. https://doi.org/10.1111/j.1749‐6632.2012.06613.x
Su, L., Nalle, S. C., Shen, L., Turner, E. S., Singh, G., Breskin, L. A., Khramtsova, E. A., Khramtsova, G., Tsai, P.‐Y., Fu, Y.‐X., Abraham, C., & Turner, J. R. (2013). TNFR2 activates MLCK‐dependent tight junction dysregulation to cause apoptosis‐mediated barrier loss and experimental colitis. Gastroenterology, 145(2), 407–415. https://doi.org/10.1053/j.gastro.2013.04.011
Sugerman, P. B., Savage, N. W., Walsh, L. J., Zhao, Z. Z., Zhou, X. J., Khan, A., Seymour, G. J., & Bigby, M. (2002). The pathogenesis of oral lichen planus. Critical Reviews in Oral Biology and Medicine: An Official Publication of the American Association of Oral Biologists, 13(4), 350–365. https://doi.org/10.1177/154411130201300405
Svitkina, T. (2018). The Actin cytoskeleton and Actin‐based motility. Cold Spring Harbor Perspectives in Biology, 10(1), a018267. https://doi.org/10.1101/cshperspect.a018267
Tan, Z., Xu, P., Guo, Y., & He, Y. (2021). Prevotella melaninogenica impairs oral epithelial barrier through inhibiting tight junction proteins as mechanism of pathogenesis of oral lichen planus. Journal of Tongji University (Medical Science), 04, 459–466. https://doi.org/10.12289/j.issn.1008‐0392.21048
Theriot, J. A. (1995). The cell biology of infection by intracellular bacterial pathogens. Annual Review of Cell and Developmental Biology, 11, 213–239. https://doi.org/10.1146/annurev.cb.11.110195.001241
Wang, K., Lu, W., Tu, Q., Ge, Y., He, J., Zhou, Y., Gou, Y., Van Nostrand, J. D., Qin, Y., Li, J., Zhou, J., Li, Y., Xiao, L., & Zhou, X. (2016). Preliminary analysis of salivary microbiome and their potential roles in oral lichen planus. Scientific Reports, 6(1), 22943. https://doi.org/10.1038/srep22943
Wang, X., Zhao, Z., Tang, N., Zhao, Y., Xu, J., Li, L., Qian, L., Zhang, J., & Fan, Y. (2020). Microbial community analysis of saliva and biopsies in patients with Oral lichen planus. Frontiers in Microbiology, 11, 629. https://doi.org/10.3389/fmicb.2020.00629
Xu, M. (2014). Antibiotic resistance of Prevotella species and virulence analysis of Prevotella Nigrescens isolated from chronic periodontitis [PhD Thesis]. Fudan University. https://kns.cnki.net/KCMS/detail/detail.aspx?dbname=CMFD201602&filename=1015428543.nh
Yi, H., Wang, L., Xiong, Y., Wang, Z., Qiu, Y., Wen, X., Jiang, Z., Yang, X., & Ma, X. (2018). Lactobacillus reuteri LR1 improved expression of genes of tight junction proteins via the MLCK pathway in IPEC‐1 cells during infection with Enterotoxigenic Escherichia coli K88. Mediators of Inflammation, 2018, e6434910. https://doi.org/10.1155/2018/6434910
Yu, D., Marchiando, A. M., Weber, C. R., Raleigh, D. R., Wang, Y., Shen, L., & Turner, J. R. (2010). MLCK‐dependent exchange and Actin binding region‐dependent anchoring of ZO‐1 regulate tight junction barrier function. Proceedings of the National Academy of Sciences, 107(18), 8237–8241. https://doi.org/10.1073/pnas.0908869107
Yu, F. Y., Wang, Q. Q., Li, M., Cheng, Y.‐H., Cheng, Y.‐S. L., Zhou, Y., Yang, X., Zhang, F., Ge, X., Zhao, B., & Ren, X. Y. (2020). Dysbiosis of saliva microbiome in patients with oral lichen planus. BMC Microbiology, 20(1), 75. https://doi.org/10.1186/s12866‐020‐01733‐7
Zheng, S., Xu, P., Cai, L., Tan, Z., Guo, Y., Zhu, R., & He, Y. (2021). The presence of Prevotella melaninogenica within tissue and preliminary study on its role in the pathogenesis of oral lichen planus. Oral Diseases, 28(6), 1580–1590. https://doi.org/10.1111/odi.13862