Activation of receptor-interacting protein 3-mediated necroptosis accelerates periodontitis in mice.
MLKL
RIP3
necroptosis
periodontitis
Journal
Oral diseases
ISSN: 1601-0825
Titre abrégé: Oral Dis
Pays: Denmark
ID NLM: 9508565
Informations de publication
Date de publication:
30 Jul 2023
30 Jul 2023
Historique:
revised:
09
07
2023
received:
02
11
2022
accepted:
14
07
2023
medline:
31
7
2023
pubmed:
31
7
2023
entrez:
31
7
2023
Statut:
aheadofprint
Résumé
To investigate the involvement and role of receptor-interacting protein 3 (RIP3)-mediated necroptosis in periodontitis. A periodontitis murine model was established by oral infection with Porphyromonas gingivalis, and activation of necroptosis pathway was identified by immunohistochemistry. Adeno-associated virus was used to knock down Rip3 and the effect of Rip3 knockdown on periodontal inflammation was examined by Micro-CT, qRT-PCR and histological staining. In vitro, P. gingivalis-LPS was used to infect fibroblast cell line L929 and siRNA was used to knock down Rip3. Necroptosis pathway signalling and inflammation in cells were detected by cell viability and death assay, Western Blot, qRT-PCR and immunofluorescence analysis. Phosphorylation of RIP3 and mixed lineage kinase domain-like protein (MLKL) was increased in the periodontal ligament of mice infected with P. gingivalis. RIP3 knockdown reduced osteoclastogenesis and inflammatory cytokines in the periodontal area, and alleviated alveolar bone loss in vivo. In vitro, P. gingivalis-LPS-induced RIP3-mediated necroptosis in L929 cells, and knockdown of RIP3 by siRNA decreased the expression of inflammatory cytokines. RIP3-mediated necroptosis is activated in periodontitis and blocking necroptosis alleviates disease progression, indicating that RIP3 may be a potential target for periodontitis treatment.
Types de publication
Journal Article
Langues
eng
Subventions
Organisme : National Natural Science Foundation of China
ID : 82001060
Organisme : National Natural Science Foundation of China
ID : 81991500
Organisme : National Natural Science Foundation of China
ID : 81991502
Organisme : West China School/Hospital of Stomatology, Sichuan University
ID : RCDWJS2021-11
Organisme : Sichuan Provincial Science and Technology Foundation
ID : 2023YFS0081
Organisme : Sichuan Provincial Science and Technology Foundation
ID : 2022YFS0286
Organisme : Sichuan Provincial Science and Technology Foundation
ID : 2020YFQ0008
Informations de copyright
© 2023 Wiley Periodicals LLC.
Références
Abusleme, L., Dupuy, A. K., Dutzan, N., Silva, N., Burleson, J. A., Strausbaugh, L. D., Gamonal, J., & Diaz, P. I. (2013). The subgingival microbiome in health and periodontitis and its relationship with community biomass and inflammation. The ISME Journal, 7(5), 1016-1025.
Afonso, M. B., Rodrigues, P. M., Simão, A. L., Ofengeim, D., Carvalho, T., Amaral, J. D., Gaspar, M. M., Cortez-Pinto, H., Castro, R. E., Yuan, J., & Rodrigues, C. M. P. (2016). Activation of necroptosis in human and experimental cholestasis. Cell Death & Disease, 7(9), e2390.
American Academy of Periodontology. (2000). Parameter on chronic periodontitis with slight to moderate loss of periodontal support. Journal of Periodontology, 71(5 Suppl), 853-855.
Carrouel, F., Staquet, M. J., Keller, J. F., Baudouin, C., Msika, P., Bleicher, F., Alliot-Licht, B., & Farges, J. C. (2013). Lipopolysaccharide-binding protein inhibits toll-like receptor 2 activation by lipoteichoic acid in human odontoblast-like cells. Journal of Endodontia, 39(8), 1008-1014.
Challa, S., & Chan, F. K. (2010). Going up in flames: Necrotic cell injury and inflammatory diseases. Cellular and Molecular Life Sciences, 67(19), 3241-3253.
Chen, Q., Liu, X., Wang, D., Zheng, J., Chen, L., Xie, Q., Liu, X., Niu, S., Qu, G., Lan, J., Li, J., Yang, C., & Zou, D. (2021). Periodontal inflammation-triggered by periodontal ligament stem cell pyroptosis exacerbates periodontitis. Frontiers in Cell and Development Biology, 9, 663037.
Christgen, S., Zheng, M., Kesavardhana, S., Karki, R., Malireddi, R. K. S., Banoth, B., Place, D. E., Briard, B., Sharma, B. R., Tuladhar, S., Samir, P., Burton, A., & Kanneganti, T. D. (2020). Identification of the PANoptosome: A molecular platform triggering Pyroptosis, apoptosis, and necroptosis (PANoptosis). Frontiers in Cellular and Infection Microbiology, 10, 237.
Gaba, A., Xu, F., Lu, Y., Park, H. S., Liu, G. Q., & Zhou, Y. (2019). The NS1 protein of influenza a virus participates in necroptosis by interacting with MLKL and increasing its oligomerization and membrane translocation. Journal of Virology, 93(2), 10-128.
Galluzzi, L., Vitale, I., Aaronson, S. A., Abrams, J. M., Adam, D., Agostinis, P., Alnemri, E. S., Altucci, L., Amelio, I., Andrews, D. W., Annicchiarico-Petruzzelli, M., Antonov, A. V., Arama, E., Baehrecke, E. H., Barlev, N. A., Bazan, N. G., Bernassola, F., Bertrand, M. J. M., Bianchi, K., … Kroemer, G. (2018). Molecular mechanisms of cell death: Recommendations of the nomenclature committee on cell death 2018. Cell Death and Differentiation, 25(3), 486-541.
Green, D. R. (2019). The coming decade of cell death research: Five riddles. Cell, 177(5), 1094-1107.
Hajishengallis, G. (2014). Immunomicrobial pathogenesis of periodontitis: Keystones, pathobionts, and host response. Trends in Immunology, 35(1), 3-11.
Hajishengallis, G., & Korostoff, J. M. (2017). Revisiting the Page & Schroeder model: The good, the bad and the unknowns in the periodontal host response 40 years later. Periodontology 2000, 75(1), 116-151.
Hao, M., Han, X., Yao, Z., Zhang, H., Zhao, M., Peng, M., Wang, K., Shan, Q., Sang, X., Wu, X., Wang, L., Lv, Q., Yang, Q., Bao, Y., Kuang, H., Zhang, H., & Cao, G. (2022). The pathogenesis of organ fibrosis: Focus on necroptosis. British Journal of Pharmacology, https://doi.org/10.1111/bph.15952
Hienz, S. A., Paliwal, S., & Ivanovski, S. (2015). Mechanisms of bone resorption in periodontitis. Journal of Immunology Research, 2015, 615486.
Ito, Y., Bhawal, U. K., Sasahira, T., Toyama, T., Sato, T., Matsuda, D., Nishikiori, H., Kobayashi, M., Sugiyama, M., Hamada, N., Arakawa, H., & Kuniyasu, H. (2012). Involvement of HMGB1 and RAGE in IL-1beta-induced gingival inflammation. Archives of Oral Biology, 57(1), 73-80.
Karki, R., Sharma, B. R., Tuladhar, S., Williams, E. P., Zalduondo, L., Samir, P., Zheng, M., Sundaram, B., Banoth, B., Malireddi, R. K. S., Schreiner, P., Neale, G., Vogel, P., Webby, R., Jonsson, C. B., & Kanneganti, T. D. (2021). Synergism of TNF-alpha and IFN-gamma triggers inflammatory cell death, tissue damage, and mortality in SARS-CoV-2 infection and cytokine shock syndromes. Cell, 184(1), 149-168.e17.
Ke, X., Lei, L., Li, H., Li, H., & Yan, F. (2016). Manipulation of necroptosis by Porphyromonas gingivalis in periodontitis development. Molecular Immunology, 77, 8-13.
Kearney, C. J., & Martin, S. J. (2017). An inflammatory perspective on necroptosis. Molecular Cell, 65(6), 965-973.
Kesavardhana, S., Malireddi, R. K. S., & Kanneganti, T. D. (2020). Caspases in cell death, inflammation, and Pyroptosis. Annual Review of Immunology, 38, 567-595.
Khoury, M. K., Gupta, K., Franco, S. R., & Liu, B. (2020). Necroptosis in the pathophysiology of disease. The American Journal of Pathology, 190(2), 272-285.
Kim, S. J., & Li, J. (2013). Caspase blockade induces RIP3-mediated programmed necrosis in toll-like receptor-activated microglia. Cell Death & Disease, 4(7), e716.
Kornman, K. S., Page, R. C., & Tonetti, M. S. (1997). The host response to the microbial challenge in periodontitis: Assembling the players. Periodontology 2000, 14, 33-53.
Kurita-Ochiai, T., Seto, S., Suzuki, N., Yamamoto, M., Otsuka, K., Abe, K., & Ochiai, K. (2008). Butyric acid induces apoptosis in inflamed fibroblasts. Journal of Dental Research, 87(1), 51-55.
Lee, S., Karki, R., Wang, Y., Nguyen, L. N., Kalathur, R. C., & Kanneganti, T. D. (2021). AIM2 forms a complex with pyrin and ZBP1 to drive PANoptosis and host defence. Nature, 597(7876), 415-419.
Li, Y. Y., Cai, Q., Li, B. S., Qiao, S. W., Jiang, J. Y., Wang, D., du, X. C., & Meng, W. Y. (2021). The effect of Porphyromonas gingivalis lipopolysaccharide on the Pyroptosis of gingival fibroblasts. Inflammation, 44(3), 846-858.
Liu, Y. Z., Maney, P., Puri, J., Zhou, Y., Baddoo, M., Strong, M., Wang, Y. P., Flemington, E., & Deng, H. W. (2016). RNA-sequencing study of peripheral blood monocytes in chronic periodontitis. Gene, 581(2), 152-160.
Maeda, A., & Fadeel, B. (2014). Mitochondria released by cells undergoing TNF-alpha-induced necroptosis act as danger signals. Cell Death & Disease, 5, e1312.
Malireddi, R. K. S., Kesavardhana, S., Karki, R., Kancharana, B., Burton, A. R., & Kanneganti, T. D. (2020). RIPK1 distinctly regulates Yersinia-induced inflammatory cell death, PANoptosis. Immunohorizons, 4(12), 789-796.
Morimoto, Y., Kawahara, K. I., Tancharoen, S., Kikuchi, K., Matsuyama, T., Hashiguchi, T., Izumi, Y., & Maruyama, I. (2008). Tumor necrosis factor-alpha stimulates gingival epithelial cells to release high mobility-group box 1. Journal of Periodontal Research, 43(1), 76-83.
Moriwaki, K., Bertin, J., Gough, P. J., Orlowski, G. M., & Chan, F. K. M. (2015). Differential roles of RIPK1 and RIPK3 in TNF-induced necroptosis and chemotherapeutic agent-induced cell death. Cell Death & Disease, 6, e1636.
Nagata, S., & Tanaka, M. (2017). Programmed cell death and the immune system. Nature Reviews. Immunology, 17(5), 333-340.
Palaiologou, A. A., Yukna, R. A., Moses, R., & Lallier, T. E. (2001). Gingival, dermal, and periodontal ligament fibroblasts express different extracellular matrix receptors. Journal of Periodontology, 72(6), 798-807.
Pan, W., Yin, W., Yang, L., Xue, L., Ren, J., Wei, W., Lu, Q., Ding, H., Liu, Z., Nabar, N. R., Wang, M., & Hao, L. (2019). Inhibition of Ctsk alleviates periodontitis and comorbid rheumatoid arthritis via downregulation of the TLR9 signalling pathway. Journal of Clinical Periodontology, 46(3), 286-296.
Pasparakis, M., & Vandenabeele, P. (2015). Necroptosis and its role in inflammation. Nature, 517(7534), 311-320.
Peres, M. A., Daly, B., Guarnizo-Herreño, C. C., Benzian, H., & Watt, R. G. (2020). Oral diseases: A global public health challenge-Authors' reply. Lancet, 395(10219), 186-187.
Place, D. E., Lee, S., & Kanneganti, T. D. (2021). PANoptosis in microbial infection. Current Opinion in Microbiology, 59, 42-49.
Qing, D. Y., Conegliano, D., Shashaty, M. G. S., Seo, J., Reilly, J. P., Worthen, G. S., Huh, D., Meyer, N. J., & Mangalmurti, N. S. (2014). Red blood cells induce necroptosis of lung endothelial cells and increase susceptibility to lung inflammation. American Journal of Respiratory and Critical Care Medicine, 190(11), 1243-1254.
Said-Sadier, N., & Ojcius, D. M. (2012). Alarmins, inflammasomes and immunity. Biomedical Journal, 35(6), 437-449.
Shi, J., Li, J., Su, W., Zhao, S., Li, H., & Lei, L. (2019). Loss of periodontal ligament fibroblasts by RIPK3-MLKL-mediated necroptosis in the progress of chronic periodontitis. Scientific Reports, 9(1), 2902.
Son, S., Yoon, S. H., Chae, B. J., Hwang, I., Shim, D. W., Choe, Y. H., Hyun, Y. M., & Yu, J. W. (2021). Neutrophils facilitate prolonged inflammasome response in the DAMP-rich inflammatory milieu. Frontiers in Immunology, 12, 746032.
Tsuda, H., Ning, Z., Yamaguchi, Y., & Suzuki, N. (2012). Programmed cell death and its possible relationship with periodontal disease. Journal of Oral Science, 54(2), 137-149.
Wang, H., Sun, L., Su, L., Rizo, J., Liu, L., Wang, L. F., Wang, F. S., & Wang, X. (2014). Mixed lineage kinase domain-like protein MLKL causes necrotic membrane disruption upon phosphorylation by RIP3. Molecular Cell, 54(1), 133-146.
Wang, Y., & Kanneganti, T. D. (2021). From pyroptosis, apoptosis and necroptosis to PANoptosis: A mechanistic compendium of programmed cell death pathways. Computational and Structural Biotechnology Journal, 19, 4641-4657.
Weber, K., Roelandt, R., Bruggeman, I., Estornes, Y., & Vandenabeele, P. (2018). Nuclear RIPK3 and MLKL contribute to cytosolic necrosome formation and necroptosis. Communications Biology, 1, 6.
Wei, W., Xiao, X., Li, J., Ding, H., Pan, W., Deng, S., Yin, W., Xue, L., Lu, Q., Yue, Y., Tian, Y., Wang, M., & Hao, L. (2019). Activation of the STAT1 pathway accelerates periodontitis in Nos3(−/−) mice. Journal of Dental Research, 98(9), 1027-1036.
Wei, W., Xue, L., Tan, L., Liu, J., Yang, Q., Wang, J., Yan, B., Cai, Q., Yang, L., Yue, Y., Hao, L., Wang, M., & Li, J. (2021). Inhibition of yes-associated protein dephosphorylation prevents aggravated periodontitis with occlusal trauma. Journal of Periodontology, 92(7), 1036-1048.
Yang, Y., Wang, L., Zhang, H., & Luo, L. (2022). Mixed lineage kinase domain-like pseudokinase-mediated necroptosis aggravates periodontitis progression. Journal of Molecular Medicine (Berlin, Germany), 100(1), 77-86.
Yoon, S., Bogdanov, K., Kovalenko, A., & Wallach, D. (2016). Necroptosis is preceded by nuclear translocation of the signaling proteins that induce it. Cell Death and Differentiation, 23(2), 253-260.
Yoshihara-Hirata, C., Yamashiro, K., Yamamoto, T., Aoyagi, H., Ideguchi, H., Kawamura, M., Suzuki, R., Ono, M., Wake, H., Nishibori, M., & Takashiba, S. (2018). Anti-HMGB1 neutralizing antibody attenuates periodontal inflammation and bone resorption in a murine periodontitis model. Infection and Immunity, 86(5), e00111-18.
Zhang, Y., Chen, X., Gueydan, C., & Han, J. (2018). Plasma membrane changes during programmed cell deaths. Cell Research, 28(1), 9-21.
Zheng, M., Williams, E. P., Malireddi, R. K. S., Karki, R., Banoth, B., Burton, A., Webby, R., Channappanavar, R., Jonsson, C. B., & Kanneganti, T. D. (2020). Impaired NLRP3 inflammasome activation/pyroptosis leads to robust inflammatory cell death via caspase-8/RIPK3 during coronavirus infection. The Journal of Biological Chemistry, 295(41), 14040-14052.
Geng, F., Liu, J., Yin, C., Zhang, S., Pan, Y., & Sun, H. (2022). Porphyromonas gingivalis lipopolysaccharide induced RIPK3/MLKL-mediated necroptosis of oral epithelial cells and the further regulation in macrophage activation. Journal of Oral Microbiology, 14(1), 2041790.