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Mediators of Inflammation
Volume 2017, Article ID 4786170, 10 pages
https://doi.org/10.1155/2017/4786170
Research Article

Role of Cathepsin S in Periodontal Inflammation and Infection

1Section of Experimental Dento-Maxillo-Facial Medicine, Center of Dento-Maxillo-Facial Medicine, University of Bonn, Bonn, Germany
2Department of Orthodontics, Center of Dento-Maxillo-Facial Medicine, University of Bonn, Bonn, Germany
3Department of Diagnosis and Surgery, School of Dentistry at Araraquara, Sao Paulo State University (UNESP), Araraquara, SP, Brazil
4Department of Periodontology, Laboratory for Oral Microbiology, School of Dental Medicine, University of Bern, Bern, Switzerland
5Discipline of Orthodontics, Faculty of Dentistry, University of Sydney, Sydney, NSW, Australia
6Institute of Reconstructive Neurobiology, Life & Brain Center, University of Bonn, Bonn, Germany
7Department of Periodontology, Operative and Preventive Dentistry, University of Bonn, Bonn, Germany
8Department of Biological Chemistry, Medical School, National and Kapodistrian University of Athens, Athens, Greece
9Noel Martin Visiting Chair, Faculty of Dentistry, University of Sydney, Sydney, NSW, Australia

Correspondence should be addressed to S. Memmert; ed.nnob-inu.bku@tremmem.ajnevs

Received 10 July 2017; Accepted 29 October 2017; Published 6 December 2017

Academic Editor: Settimio Rossi

Copyright © 2017 S. Memmert et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. G. Thornton-Evans, P. Eke, L. Wei et al., “Periodontitis among adults aged ≥30 years - United States, 2009-2010,” MMWR Supplements, vol. 62, no. 3, pp. 129–135, 2013. View at Google Scholar
  2. J. T. Marchesan, C. S. Scanlon, S. Soehren, M. Matsuo, and Y. L. Kapila, “Implications of cultured periodontal ligament cells for the clinical and experimental setting: a review,” Archives of Oral Biology, vol. 56, no. 10, pp. 933–943, 2011. View at Publisher · View at Google Scholar · View at Scopus
  3. A. Konermann, D. Stabenow, P. A. Knolle, S. A. E. Held, J. Deschner, and A. Jäger, “Regulatory role of periodontal ligament fibroblasts for innate immune cell function and differentiation,” Innate Immunity, vol. 18, no. 5, pp. 745–752, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. B. L. Pihlstrom, B. S. Michalowicz, and N. W. Johnson, “Periodontal diseases,” The Lancet, vol. 366, no. 9499, pp. 1809–1820, 2005. View at Publisher · View at Google Scholar · View at Scopus
  5. L. Sbordone and C. Bortolaia, “Oral microbial biofilms and plaque-related diseases: microbial communities and their role in the shift from oral health to disease,” Clinical Oral Investigations, vol. 7, no. 4, pp. 181–188, 2003. View at Publisher · View at Google Scholar
  6. D. N. Tatakis and P. S. Kumar, “Etiology and pathogenesis of periodontal diseases,” Dental Clinics of North America, vol. 49, no. 3, pp. 491–516, 2005. View at Publisher · View at Google Scholar · View at Scopus
  7. T. Yucel-Lindberg and T. Båge, “Inflammatory mediators in the pathogenesis of periodontitis,” Expert Reviews in Molecular Medicine, vol. 15, p. e7, 2013. View at Publisher · View at Google Scholar
  8. N. G. Chávarry, M. V. Vettore, C. Sansone, and A. Sheiham, “The relationship between diabetes mellitus and destructive periodontal disease: a meta-analysis,” Oral Health & Preventive Dentistry, vol. 7, no. 2, pp. 107–127, 2009. View at Google Scholar
  9. D. A. Chistiakov, A. N. Orekhov, and Y. V. Bobryshev, “Links between atherosclerotic and periodontal disease,” Experimental and Molecular Pathology, vol. 100, no. 1, pp. 220–235, 2016. View at Publisher · View at Google Scholar · View at Scopus
  10. G. Kroemer, G. Mariño, and B. Levine, “Autophagy and the integrated stress response,” Molecular Cell, vol. 40, no. 2, pp. 280–293, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. J. S. King, D. M. Veltman, and R. H. Insall, “The induction of autophagy by mechanical stress,” Autophagy, vol. 7, no. 12, pp. 1490–1499, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. Y. Ma, L. Galluzzi, L. Zitvogel, and G. Kroemer, “Autophagy and cellular immune responses,” Immunity, vol. 39, no. 2, pp. 211–227, 2013. View at Publisher · View at Google Scholar · View at Scopus
  13. G. Mariño, M. Niso-Santano, E. H. Baehrecke, and G. Kroemer, “Self-consumption: the interplay of autophagy and apoptosis,” Nature Reviews Molecular Cell Biology, vol. 15, no. 2, pp. 81–94, 2014. View at Publisher · View at Google Scholar · View at Scopus
  14. D. Glick, S. Barth, and K. F. Macleod, “Autophagy: cellular and molecular mechanisms,” The Journal of Pathology, vol. 221, no. 1, pp. 3–12, 2010. View at Publisher · View at Google Scholar · View at Scopus
  15. P. Lapaquette, J. Guzzo, L. Bretillon, and M. A. Bringer, “Cellular and molecular connections between autophagy and inflammation,” Mediators of Inflammation, vol. 2015, Article ID 398483, 13 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  16. W. Quan, Y. M. Lim, and M. S. Lee, “Role of autophagy in diabetes and endoplasmic reticulum stress of pancreatic β-cells,” Experimental & Molecular Medicine, vol. 44, no. 2, pp. 81–88, 2012. View at Publisher · View at Google Scholar · View at Scopus
  17. P. Bullon, M. D. Cordero, J. L. Quiles et al., “Autophagy in periodontitis patients and gingival fibroblasts: unraveling the link between chronic diseases and inflammation,” BMC Medicine, vol. 10, p. 122, 2012. View at Publisher · View at Google Scholar · View at Scopus
  18. W. P. Huang and D. J. Klionsky, “Autophagy in yeast: a review of the molecular machinery,” Cell Structure and Function, vol. 27, no. 6, pp. 409–420, 2002. View at Publisher · View at Google Scholar · View at Scopus
  19. S. Wesselborg and B. Stork, “Autophagy signal transduction by ATG proteins: from hierarchies to networks,” Cellular and Molecular Life Sciences, vol. 72, no. 24, pp. 4721–4757, 2015. View at Publisher · View at Google Scholar · View at Scopus
  20. C. C. Huang, C. C. Lee, H. H. Lin, M. C. Chen, C. C. Lin, and J. Y. Chang, “Autophagy-regulated ROS from xanthine oxidase acts as an early effector for triggering late mitochondria-dependent apoptosis in cathepsin S-targeted tumor cells,” PLoS One, vol. 10, no. 6, article e0128045, 2015. View at Publisher · View at Google Scholar · View at Scopus
  21. L. Zhang, H. Wang, J. Xu, J. Zhu, and K. Ding, “Inhibition of cathepsin S induces autophagy and apoptosis in human glioblastoma cell lines through ROS-mediated PI3K/AKT/mTOR/p70S6K and JNK signaling pathways,” Toxicology Letters, vol. 228, no. 3, pp. 248–259, 2014. View at Publisher · View at Google Scholar · View at Scopus
  22. G. P. Shi, A. C. Webb, K. E. Foster et al., “Human cathepsin S: chromosomal localization, gene structure, and tissue distribution,” Journal of Biological Chemistry, vol. 269, no. 15, pp. 11530–11536, 1994. View at Google Scholar
  23. S. Petanceska, P. Canoll, and L. A. Devi, “Expression of rat cathepsin S in phagocytic cells,” Journal of Biological Chemistry, vol. 271, no. 8, pp. 4403–4409, 1996. View at Publisher · View at Google Scholar · View at Scopus
  24. V. Zavanik-Bergant, A. Sekirnik, R. Golouh, V. Turk, and J. Kos, “Immunochemical localisation of cathepsin S, cathepsin L and MHC class II-associated p41 isoform of invariant chain in human lymph node tissue,” Biological Chemistry, vol. 382, no. 5, pp. 799–804, 2001. View at Publisher · View at Google Scholar · View at Scopus
  25. D. P. Dickinson, “Cysteine peptidases of mammals: their biological roles and potential effects in the oral cavity and other tissues in health and disease,” Critical Reviews in Oral Biology & Medicine, vol. 13, no. 3, pp. 238–275, 2002. View at Publisher · View at Google Scholar
  26. H. Nakanishi, “Microglial functions and proteases,” Molecular Neurobiology, vol. 27, no. 2, pp. 163–176, 2003. View at Publisher · View at Google Scholar · View at Scopus
  27. P. M. Andrault, S. A. Samsonov, G. Weber et al., “Antimicrobial peptide LL-37 is both a substrate of cathepsins S and K and a selective inhibitor of cathepsin L,” Biochemistry, vol. 54, no. 17, pp. 2785–2798, 2015. View at Publisher · View at Google Scholar · View at Scopus
  28. P. Pietschmann, U. Foger-Samwald, W. Sipos, and M. Rauner, “The role of cathepsins in osteoimmunology,” Critical Reviews in Eukaryotic Gene Expression, vol. 23, no. 1, pp. 11–26, 2013. View at Publisher · View at Google Scholar · View at Scopus
  29. G. Garg, A. R. Pradeep, and M. K. Thorat, “Effect of nonsurgical periodontal therapy on crevicular fluid levels of cathepsin K in periodontitis,” Archives of Oral Biology, vol. 54, no. 11, pp. 1046–1051, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. L. Song, J. Yao, Z. He, and B. Xu, “Genes related to inflammation and bone loss process in periodontitis suggested by bioinformatics methods,” BMC Oral Health, vol. 15, no. 1, p. 105, 2015. View at Publisher · View at Google Scholar · View at Scopus
  31. A. Mariotti and D. L. Cochran, “Characterization of fibroblasts derived from human periodontal ligament and gingiva,” Journal of Periodontology, vol. 61, no. 2, pp. 103–111, 1990. View at Publisher · View at Google Scholar
  32. E. K. Basdra and G. Komposch, “Osteoblast-like properties of human periodontal ligament cells: an in vitro analysis,” European Journal of Orthodontics, vol. 19, no. 6, pp. 615–621, 1997. View at Publisher · View at Google Scholar
  33. M. Nokhbehsaim, J. Winter, B. Rath, A. Jäger, S. Jepsen, and J. Deschner, “Effects of enamel matrix derivative on periodontal wound healing in an inflammatory environment in vitro,” Journal of Clinical Periodontology, vol. 38, no. 5, pp. 479–490, 2011. View at Publisher · View at Google Scholar · View at Scopus
  34. M. Nokhbehsaim, S. Eick, A. V. B. Nogueira et al., “Stimulation of MMP-1 and CCL2 by NAMPT in PDL cells,” Mediators of Inflammation, vol. 2013, Article ID 437123, 12 pages, 2013. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Nokhbehsaim, S. Keser, A. V. B. Nogueira et al., “Beneficial effects of adiponectin on periodontal ligament cells under normal and regenerative conditions,” Journal of Diabetes Research, vol. 2014, Article ID 796565, 11 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  36. M. Nokhbehsaim, S. Keser, A. V. Nogueira et al., “Leptin effects on the regenerative capacity of human periodontal cells,” International Journal of Endocrinology, vol. 2014, Article ID 180304, 13 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  37. A. Damanaki, M. Nokhbehsaim, S. Eick et al., “Regulation of NAMPT in human gingival fibroblasts and biopsies,” Mediators of Inflammation, vol. 2014, Article ID 912821, 10 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  38. A. V. B. Nogueira, M. Nokhbehsaim, S. Eick et al., “Regulation of visfatin by microbial and biomechanical signals in PDL cells,” Clinical Oral Investigations, vol. 18, no. 1, pp. 171–178, 2014. View at Publisher · View at Google Scholar · View at Scopus
  39. A. V. B. Nogueira, R. S. de Molon, M. Nokhbehsaim, J. Deschner, and J. A. Cirelli, “Contribution of biomechanical forces to inflammation-induced bone resorption,” Journal of Clinical Periodontology, vol. 44, no. 1, pp. 31–41, 2017. View at Publisher · View at Google Scholar
  40. L. C. Hsing and A. Y. Rudensky, “The lysosomal cysteine proteases in MHC class II antigen presentation,” Immunological Reviews, vol. 207, no. 1, pp. 229–241, 2005. View at Publisher · View at Google Scholar · View at Scopus
  41. W. S. Hou, W. Li, G. Keyszer et al., “Comparison of cathepsins K and S expression within the rheumatoid and osteoarthritic synovium,” Arthritis & Rheumatology, vol. 46, no. 3, pp. 663–674, 2002. View at Publisher · View at Google Scholar · View at Scopus
  42. M. Rauner, U. Föger-Samwald, M. F. Kurz et al., “Cathepsin S controls adipocytic and osteoblastic differentiation, bone turnover, and bone microarchitecture,” Bone, vol. 64, pp. 281–287, 2014. View at Publisher · View at Google Scholar · View at Scopus
  43. M. J. Hsieh, C. W. Lin, M. K. Chen et al., “Inhibition of cathepsin S confers sensitivity to methyl protodioscin in oral cancer cells via activation of p38 MAPK/JNK signaling pathways,” Scientific Reports, vol. 7, article 45039, 2017. View at Publisher · View at Google Scholar
  44. J. Arnlöv, “Cathepsin S as a biomarker: where are we now and what are the future challenges?” Biomarkers in Medicine, vol. 6, no. 1, pp. 9–11, 2012. View at Publisher · View at Google Scholar · View at Scopus
  45. E. Jobs, U. Risérus, E. Ingelsson et al., “Serum cathepsin S is associated with decreased insulin sensitivity and the development of type 2 diabetes in a community-based cohort of elderly men,” Diabetes Care, vol. 36, no. 1, pp. 163–165, 2013. View at Publisher · View at Google Scholar · View at Scopus
  46. N. R. Fuggle, T. O. Smith, A. Kaul, and N. Sofat, “Hand to mouth: a systematic review and meta-analysis of the association between rheumatoid arthritis and periodontitis,” Frontiers in Immunology, vol. 7, no. 80, 2016. View at Publisher · View at Google Scholar · View at Scopus
  47. S. N. Papageorgiou, C. Reichert, A. Jäger, and J. Deschner, “Effect of overweight/obesity on response to periodontal treatment: systematic review and a meta-analysis,” Journal of Clinical Periodontology, vol. 42, no. 3, pp. 247–261, 2015. View at Publisher · View at Google Scholar · View at Scopus
  48. B. Signat, C. Roques, P. Poulet, and D. Duffaut, “Fusobacterium nucleatum in periodontal health and disease,” Current Issues in Molecular Biology, vol. 13, no. 2, pp. 25–36, 2011. View at Publisher · View at Google Scholar
  49. J. He, W. Huang, Z. Pan et al., “Quantitative analysis of microbiota in saliva, supragingival, and subgingival plaque of Chinese adults with chronic periodontitis,” Clinical Oral Investigations, vol. 16, no. 6, pp. 1579–1588, 2011. View at Publisher · View at Google Scholar · View at Scopus
  50. C. Sina, S. Lipinski, O. Gavrilova et al., “Extracellular cathepsin K exerts antimicrobial activity and is protective against chronic intestinal inflammation in mice,” Gut, vol. 62, no. 4, pp. 520–530, 2012. View at Publisher · View at Google Scholar · View at Scopus
  51. S. Müller, A. Faulhaber, C. Sieber et al., “The endolysosomal cysteine cathepsins L and K are involved in macrophage-mediated clearance of Staphylococcus aureus and the concomitant cytokine induction,” The FASEB Journal, vol. 28, no. 1, pp. 162–175, 2014. View at Publisher · View at Google Scholar · View at Scopus
  52. G. Hajishengallis, “Periodontitis: from microbial immune subversion to systemic inflammation,” Nature Reviews Immunology, vol. 15, no. 1, pp. 30–44, 2015. View at Publisher · View at Google Scholar · View at Scopus
  53. O. A. Gonzalez, M. J. Novak, S. Kirakodu et al., “Comparative analysis of gingival tissue antigen presentation pathways in ageing and periodontitis,” Journal of Clinical Periodontology, vol. 41, no. 4, pp. 327–339, 2014. View at Publisher · View at Google Scholar · View at Scopus