A bacterial metabolite ameliorates periodontal pathogen-induced gingival epithelial barrier disruption via GPR40 signaling

Scientific Reports

Volumn 8, Issue 1, 2018, Pages

  Yamada, Miki ^a   Takahashi, Naoki ^a   Matsuda, Yumi ^a   Sato, Keisuke ^a   Yokoji, Mai ^a   Sulijaya, Benso ^a   Maekawa, Tomoki ^a   Ushiki, Tatsuo ^a   Mikami, Yoshikazu ^a   Hayatsu, Manabu ^a   Mizutani, Yusuke ^a   Kishino, Shigenobu ^b   Ogawa, Jun ^b   Arita, Makoto ^c   Tabeta, Koichi ^d   Maeda, Takeyasu ^a   Yamazaki, Kazuhisa ^a  

^a NIIGATA UNIVERSITY GRADUATE SCHOOL OF MEDICAL AND DENTAL SCIENCES   (Japan)

^b KYOTO UNIVERSITY   (Japan)

^c Institute of Physical and Chemical Research   (Japan)

^d NIIGATA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

10-HYDROXY-12-OCTADECENOIC ACID; CADHERIN; CYTOKINE; FFAR1 PROTEIN, HUMAN; G PROTEIN COUPLED RECEPTOR; OLEIC ACID;

ANIMAL; BACTERIUM; C57BL MOUSE; CACO-2 CELL LINE; CELL LINE; DRUG EFFECT; EPITHELIUM CELL; GENE EXPRESSION; GENETICS; GINGIVA; HUMAN; MALE; METABOLISM; MICROBIOLOGY; PATHOLOGY; PERIODONTAL DISEASE; PERIODONTITIS; PHYSIOLOGY; PORPHYROMONAS GINGIVALIS; SIGNAL TRANSDUCTION;

ANIMALS; BACTERIA; CACO-2 CELLS; CADHERINS; CELL LINE; CYTOKINES; EPITHELIAL CELLS; GENE EXPRESSION; GINGIVA; HUMANS; MALE; MICE, INBRED C57BL; OLEIC ACIDS; PERIODONTAL DISEASES; PERIODONTITIS; PORPHYROMONAS GINGIVALIS; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION;

EID: 85048546466     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/s41598-018-27408-y     Document Type: Article

References (62)

1. Sonnenburg, J. L. & Backhed, F. Diet-microbiota interactions as moderators of human metabolism. Nature 535, 56-64, https://doi.org/10.1038/nature18846 (2016).
2. Levy, M., Thaiss, C. A. & Elinav, E. Metabolites: messengers between the microbiota and the immune system. Genes Dev. 30, 1589-1597, https://doi.org/10.1101/gad.284091.116 (2016).
3. Sharon, G. et al. Specialized metabolites from the microbiome in health and disease. Cell Metab 20, 719-730, https://doi.org/10.1016/j.cmet.2014.10.016 (2014).
4. Kishino, S. et al. Polyunsaturated fatty acid saturation by gut lactic acid bacteria affecting host lipid composition. Proc. Natl. Acad. Sci. USA 110, 17808-17813, https://doi.org/10.1073/pnas.1312937110 (2013).
5. Goto, T. et al. 10-oxo-12(Z)-octadecenoic acid, a linoleic acid metabolite produced by gut lactic acid bacteria, potently activates PPARgamma and stimulates adipogenesis. Biochem. Biophys. Res. Commun. 459, 597-603, https://doi.org/10.1016/j. bbrc.2015.02.154 (2015).
6. Bergamo, P. et al. Immunomodulatory activity of a gut microbial metabolite of dietary linoleic acid, 10-hydroxy-cis-12-octadecenoic acid, associated with improved antioxidant/detoxifying defences. Journal of Functional Foods 11, 192-202, https://doi.org/10.1016/j.jff.2014.10.007 (2014).
7. Miyamoto, J. et al. A gut microbial metabolite of linoleic acid, 10-hydroxy-cis-12-octadecenoic acid, ameliorates intestinal epithelial barrier impairment partially via GPR40-MEK-ERK pathway. J. Biol. Chem. 290, 2902-2918, https://doi.org/10.1074/jbc. M114.610733 (2015).
8. Itoh, Y. et al. Free fatty acids regulate insulin secretion from pancreatic beta cells through GPR40. Nature 422, 173-176, https://doi.org/10.1038/nature01478 (2003).
9. Ma, S. K. et al. Activation of G-protein-coupled receptor 40 attenuates the cisplatin-induced apoptosis of human renal proximal tubule epithelial cells. Int. J. Mol. Med. 34, 1117-1123, https://doi.org/10.3892/ijmm.2014.1874 (2014).
10. Gras, D. et al. Thiazolidinediones induce proliferation of human bronchial epithelial cells through the GPR40 receptor. Am. J. Physiol. Lung Cell Mol. Physiol. 296, L970-978, https://doi.org/10.1152/ajplung.90219.2008 (2009).
11. Paster, B. J. et al. Bacterial diversity in human subgingival plaque. J. Bacteriol. 183, 3770-3783, https://doi.org/10.1128/JB.183.12.3770-3783.2001 (2001).
12. Badet, C. & Thebaud, N. B. Ecology of lactobacilli in the oral cavity: a review of literature. Open Microbiol J 2, 38-48, https://doi.org/10.2174/1874285800802010038 (2008).
13. Amano, A., Takeuchi, H. & Furuta, N. Outer membrane vesicles function as offensive weapons in host-parasite interactions. Microbes Infect 12, 791-798, https://doi.org/10.1016/j.micinf.2010.05.008 (2010).
14. Nagano, K., Hasegawa, Y., Yoshida, Y. & Yoshimura, F. A Major Fimbrilin Variant of Mfa1 Fimbriae in Porphyromonas gingivalis. J. Dent. Res. 94, 1143-1148, https://doi.org/10.1177/0022034515588275 (2015).
15. Takahashi, N. et al. Interleukin-1 receptor-associated kinase-M in gingival epithelial cells attenuates the inflammatory response elicited by Porphyromonas gingivalis. J. Periodontal Res. 45, 512-519, https://doi.org/10.1111/j.1600-0765.2009.01266.x (2010).
16. Ogawa, T. & Yagi, T. Bioactive mechanism of Porphyromonas gingivalis lipid A. Periodontol. 2000 54, 71-77, https://doi.org/10.1111/j.1600-0757.2009.00343.x (2010).
17. Laine, M. L., Appelmelk, B. J. & van Winkelhoff, A. J. Prevalence and distribution of six capsular serotypes of Porphyromonas gingivalis in periodontitis patients. J. Dent. Res. 76, 1840-1844, https://doi.org/10.1177/00220345970760120601 (1997).
18. Singh, A. et al. The capsule of Porphyromonas gingivalis leads to a reduction in the host inflammatory response, evasion of phagocytosis, and increase in virulence. Infect. Immun. 79, 4533-4542, https://doi.org/10.1128/IAI.05016-11 (2011).
19. de Diego, I. et al. Structure and mechanism of cysteine peptidase gingipain K (Kgp), a major virulence factor of Porphyromonas gingivalis in periodontitis. J. Biol. Chem. 289, 32291-32302, https://doi.org/10.1074/jbc.M114.602052 (2014).
20. Dubin, G., Koziel, J., Pyrc, K., Wladyka, B. & Potempa, J. Bacterial proteases in disease-role in intracellular survival, evasion of coagulation/fibrinolysis innate defenses, toxicoses and viral infections. Curr. Pharm. Des. 19, 1090-1113 (2013).
21. Potempa, J., Banbula, A. & Travis, J. Role of bacterial proteinases in matrix destruction and modulation of host responses. Periodontol. 2000(24), 153-192 (2000).
22. Katz, J. Hydrolysis of Epithelial Junctional Proteins by Porphyromonas gingivalis Gingipains. Infect. Immun. 70, 2512-2518, https://doi.org/10.1128/iai.70.5.2512-2518.2002 (2002).
23. Katz, J., Sambandam, V., Wu, J. H., Michalek, S. M. & Balkovetz, D. F. Characterization of Porphyromonas gingivalis-induced degradation of epithelial cell junctional complexes. Infect. Immun. 68, 1441-1449 (2000).
24. DiRienzo, J. M. Breaking the Gingival Epithelial Barrier: Role of the Aggregatibacter actinomycetemcomitans Cytolethal Distending Toxin in Oral Infectious Disease. Cells 3, 476-499, https://doi.org/10.3390/cells3020476 (2014).
25. Moens, E. & Veldhoen, M. Epithelial barrier biology: good fences make good neighbours. Immunology 135, 1-8, https://doi.org/10.1111/j.1365-2567.2011.03506.x (2012).
26. Tian, X. et al. E-cadherin/beta-catenin complex and the epithelial barrier. J Biomed Biotechnol 2011, 567305, https://doi.org/10.1155/2011/567305 (2011).
27. Brooke, M. A., Nitoiu, D. & Kelsell, D. P. Cell-cell connectivity: desmosomes and disease. J. Pathol. 226, 158-171, https://doi.org/10.1002/path.3027 (2012).
28. Nagarakanti, S., Ramya, S., Babu, P., Arun, K. V. & Sudarsan, S. Differential expression of E-cadherin and cytokeratin 19 and net proliferative rate of gingival keratinocytes in oral epithelium in periodontal health and disease. J. Periodontol. 78, 2197-2202, https://doi.org/10.1902/jop.2007.070070 (2007).
29. Ye, P., Chapple, C. C., Kumar, R. K. & Hunter, N. Expression patterns of E-cadherin, involucrin, and connexin gap junction proteins in the lining epithelia of inflamed gingiva. J. Pathol. 192, 58-66, https://doi.org/10.1002/1096-9896(2000)9999:9999::AIDPATH6733.0.CO;2-T (2000).
30. Whitmarsh, A. J. Regulation of gene transcription by mitogen-activated protein kinase signaling pathways. Biochim. Biophys. Acta 1773, 1285-1298, https://doi.org/10.1016/j.bbamcr.2006.11.011 (2007).
31. Chu, Z. G. et al. p38 MAP kinase mediates burn serum-induced endothelial barrier dysfunction: involvement of F-actin rearrangement and L-caldesmon phosphorylation. Shock 34, 222-228, https://doi.org/10.1097/SHK.0b013e3181d75a66 (2010).
32. Li, L. et al. P38/MAPK contributes to endothelial barrier dysfunction via MAP4 phosphorylation-dependent microtubule disassembly in inflammation-induced acute lung injury. Sci. Rep. 5, 8895, https://doi.org/10.1038/srep08895 (2015).
33. Birukova, A. A. et al. MAP kinases in lung endothelial permeability induced by microtubule disassembly. Am. J. Physiol. Lung Cell Mol. Physiol. 289, L75-84, https://doi.org/10.1152/ajplung.00447.2004 (2005).
34. Lee, W. J. & Hase, K. Gut microbiota-generated metabolites in animal health and disease. Nat. Chem. Biol. 10, 416-424, https://doi.org/10.1038/nchembio.1535 (2014).
35. Fasano, A. & Shea-Donohue, T. Mechanisms of disease: the role of intestinal barrier function in the pathogenesis of gastrointestinal autoimmune diseases. Nat. Clin. Pract. Gastroenterol. Hepatol. 2, 416-422, https://doi.org/10.1038/ncpgasthep0259 (2005).
36. de Jong, P. R., Gonzalez-Navajas, J. M. & Jansen, N. J. The digestive tract as the origin of systemic inflammation. Crit. Care 20, 279, https://doi.org/10.1186/s13054-016-1458-3 (2016).
37. Bansal, T., Alaniz, R. C., Wood, T. K. & Jayaraman, A. The bacterial signal indole increases epithelial-cell tight-junction resistance and attenuates indicators of inflammation. Proc. Natl. Acad. Sci. USA 107, 228-233, https://doi.org/10.1073/pnas.0906112107 (2010).
38. Shimada, Y. et al. Commensal bacteria-dependent indole production enhances epithelial barrier function in the colon. PLoS One 8, e80604, https://doi.org/10.1371/journal.pone.0080604 (2013).
39. Fukuda, S. et al. Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature 469, 543-547, https://doi.org/10.1038/nature09646 (2011).
40. Wang, H. B., Wang, P. Y., Wang, X., Wan, Y. L. & Liu, Y. C. Butyrate enhances intestinal epithelial barrier function via up-regulation of tight junction protein Claudin-1 transcription. Dig. Dis. Sci. 57, 3126-3135, https://doi.org/10.1007/s10620-012-2259-4 (2012).
41. Sakanaka, A. et al. Distinct signatures of dental plaque metabolic byproducts dictated by periodontal inflammatory status. Sci. Rep. 7, 42818, https://doi.org/10.1038/srep42818 (2017).
42. Kuboniwa, M. et al. Prediction of Periodontal Inflammation via Metabolic Profiling of Saliva. J. Dent. Res. 95, 1381-1386, https://doi.org/10.1177/0022034516661142 (2016).
43. Viskupicova, J., Danihelova, M., Majekova, M., Liptaj, T. & Sturdik, E. Polyphenol fatty acid esters as serine protease inhibitors: a quantum-chemical QSAR analysis. J. Enzyme Inhib. Med. Chem. 27, 800-809, https://doi.org/10.3109/14756366.2010.616860 (2012).
44. Choi, J.-S. The antibacterial activity of various saturated and unsaturated fatty acids against several oral pathogens. J. Environ. Biol. (2012).
45. Uehara, A., Sugawara, S., Tamai, R. & Takada, H. Contrasting responses of human gingival and colonic epithelial cells to lipopolysaccharides, lipoteichoic acids and peptidoglycans in the presence of soluble CD14. Med. Microbiol. Immunol. 189, 185-192 (2001).
46. Offermanns, S. Free fatty acid (FFA) and hydroxy carboxylic acid (HCA) receptors. Annu. Rev. Pharmacol. Toxicol. 54, 407-434, https://doi.org/10.1146/annurev-pharmtox-011613-135945 (2014).
47. Karve, T. M. & Cheema, A. K. Small changes huge impact: the role of protein posttranslational modifications in cellular homeostasis and disease. J Amino Acids 2011, 207691, https://doi.org/10.4061/2011/207691 (2011).
48. Ribet, D. & Cossart, P. Post-translational modifications in host cells during bacterial infection. FEBS Lett. 584, 2748-2758, https://doi.org/10.1016/j.febslet.2010.05.012 (2010).
49. McEwen, A. E., Maher, M. T., Mo, R. & Gottardi, C. J. E-cadherin phosphorylation occurs during its biosynthesis to promote its cell surface stability and adhesion. Mol. Biol. Cell 25, 2365-2374, https://doi.org/10.1091/mbc.E14-01-0690 (2014).
50. Vargas, D. A., Sun, M., Sadykov, K., Kukuruzinska, M. A. & Zaman, M. H. The Integrated Role of Wnt/beta-Catenin, N-Glycosylation, and E-Cadherin-Mediated Adhesion in Network Dynamics. PLoS Comput. Biol. 12, e1005007, https://doi.org/10.1371/journal.pcbi.1005007 (2016).
51. Liwosz, A., Lei, T. & Kukuruzinska, M. A. N-glycosylation affects the molecular organization and stability of E-cadherin junctions. J. Biol. Chem. 281, 23138-23149, https://doi.org/10.1074/jbc.M512621200 (2006).
52. Hayashi, H. & Yamashita, Y. Role of N-glycosylation in cell surface expression and protection against proteolysis of the intestinal anion exchanger SLC26A3. Am. J. Physiol. Cell Physiol. 302, C781-795, https://doi.org/10.1152/ajpcell.00165.2011 (2012).
53. Varki, A. Biological roles of oligosaccharides: all of the theories are correct. Glycobiology 3, 97-130 (1993).
54. Lis, H. & Sharon, N. Protein glycosylation. Structural and functional aspects. Eur. J. Biochem. 218, 1-27 (1993).
55. Takahashi, N., Okui, T., Tabeta, K. & Yamazaki, K. Effect of interleukin-17 on the expression of chemokines in gingival epithelial cells. Eur. J. Oral Sci. 119, 339-344, https://doi.org/10.1111/j.1600-0722.2011.00842.x (2011).
56. Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT Method. Methods 25, 402-408, https://doi.org/10.1006/meth.2001.1262 (2001).
57. Takahashi, N. et al. Epithelial TRPV1 Signaling Accelerates Gingival Epithelial Cell Proliferation. J. Dent. Res. 93, 1141-1147, https://doi.org/10.1177/0022034514552826 (2014).
58. Vergauwen, H. et al. Trolox and ascorbic acid reduce direct and indirect oxidative stress in the IPEC-J2 cells, an in vitro model for the porcine gastrointestinal tract. PLoS One 10, e0120485, https://doi.org/10.1371/journal.pone.0120485 (2015).
59. Carrasco-Pozo, C., Morales, P. & Gotteland, M. Polyphenols protect the epithelial barrier function of Caco-2 cells exposed to indomethacin through the modulation of occludin and zonula occludens-1 expression. J. Agric. Food Chem. 61, 5291-5297, https://doi.org/10.1021/jf400150p (2013).
60. Hollander, M. R. et al. Dissecting the Effects of Ischemia and Reperfusion on the Coronary Microcirculation in a Rat Model of Acute Myocardial Infarction. PLoS One 11, e0157233, https://doi.org/10.1371/journal.pone.0157233 (2016).
61. Rajasekaran, S. A. et al. Na,K-ATPase inhibition alters tight junction structure and permeability in human retinal pigment epithelial cells. Am. J. Physiol. Cell Physiol. 284, C1497-1507, https://doi.org/10.1152/ajpcell.00355.2002 (2003).
62. Takahashi, N. et al. Neuronal TRPV1 activation regulates alveolar bone resorption by suppressing osteoclastogenesis via CGRP. Sci. Rep. 6, 29294, https://doi.org/10.1038/srep29294 (2016).