Skip to main content
Top
Published in: BMC Oral Health 1/2023

Open Access 01-12-2023 | Research

Molecular mechanism and diagnostic marker investigation of endoplasmic reticulum stress on periodontitis

Authors: Qianqian Sun, Enqiang Zhu

Published in: BMC Oral Health | Issue 1/2023

Login to get access

Abstract

Purpose

The aim of this study was to reveal the biological function of endoplasmic reticulum stress (ERS)-related genes (ERSGs) in periodontitis, and provide potential ERS diagnostic markers for clinical therapy of periodontitis.

Methods

The differentially expressed ERSGs (DE-ERSGs) were reveled based on periodontitis-related microarray dataset in Gene Expression Omnibus (GEO) database and 295 ERS in previous study, followed by a protein–protein interaction network construction. Then, the subtypes of periodontitis were explored, followed by validation with immune cell infiltration and gene set enrichment. Two machine learning algorithms were used to reveal potential ERS diagnostic markers of periodontitis. The diagnostic effect, target drug and immune correlation of these markers were further evaluated. Finally, a microRNA(miRNA)-gene interaction network was constructed.

Results

A total of 34 DE-ERSGs were revealed between periodontitis samples and control, followed by two subtypes investigated. There was a significant difference of ERS score, immune infiltration and Hallmark enrichment between two subtypes. Then, totally 7 ERS diagnostic markers including FCGR2B, XBP1, EDEM2, ATP2A3, ERLEC1, HYOU1 and YOD1 were explored, and the v the time-dependent ROC analysis showed a reliable result. In addition, a drug-gene network was constructed with 4 up-regulated ERS diagnostic markers and 24 drugs. Finally, based on 32 interactions, 5 diagnostic markers and 20 miRNAs, a miRNA-target network was constructed.

Conclusions

Up-regulated miR-671-5p might take part in the progression of periodontitis via stimulating the expression of ATP2A3. ERSGs including XBP1 and FCGR2B might be novel diagnostic marker for periodontitis.
Appendix
Available only for authorised users
Literature
1.
go back to reference Yan Y, Zhan Y, Wang X, Hou J. Clinical evaluation of ultrasonic subgingival debridement versus ultrasonic subgingival scaling combined with manual root planing in the treatment of periodontitis: study protocol for a randomized controlled trial. Trials. 2020;21:113.PubMedPubMedCentralCrossRef Yan Y, Zhan Y, Wang X, Hou J. Clinical evaluation of ultrasonic subgingival debridement versus ultrasonic subgingival scaling combined with manual root planing in the treatment of periodontitis: study protocol for a randomized controlled trial. Trials. 2020;21:113.PubMedPubMedCentralCrossRef
3.
go back to reference Dannewitz B, Holtfreter B, Eickholz P. Periodontitis-therapy of a widespread disease. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz. 2021;64:931–40.PubMedPubMedCentralCrossRef Dannewitz B, Holtfreter B, Eickholz P. Periodontitis-therapy of a widespread disease. Bundesgesundheitsblatt Gesundheitsforschung Gesundheitsschutz. 2021;64:931–40.PubMedPubMedCentralCrossRef
4.
go back to reference Slots J. Periodontitis: facts, fallacies and the future. Periodontol. 2000;2017(75):7–23. Slots J. Periodontitis: facts, fallacies and the future. Periodontol. 2000;2017(75):7–23.
5.
go back to reference Qasim SSB, Al-Otaibi D, Al-Jasser R, Gul SS, Zafar MS. An evidence-based update on the molecular mechanisms underlying periodontal diseases. Int J Mol Sci. 2020;21:66.CrossRef Qasim SSB, Al-Otaibi D, Al-Jasser R, Gul SS, Zafar MS. An evidence-based update on the molecular mechanisms underlying periodontal diseases. Int J Mol Sci. 2020;21:66.CrossRef
6.
go back to reference Isola G, Santonocito S, Distefano A, Polizzi A, Vaccaro M, Raciti G, et al. Impact of periodontitis on gingival crevicular fluid miRNAs profiles associated with cardiovascular disease risk. J Periodontal Res. 2023;58:165–74.PubMedCrossRef Isola G, Santonocito S, Distefano A, Polizzi A, Vaccaro M, Raciti G, et al. Impact of periodontitis on gingival crevicular fluid miRNAs profiles associated with cardiovascular disease risk. J Periodontal Res. 2023;58:165–74.PubMedCrossRef
7.
go back to reference Currò M, Matarese G, Isola G, Caccamo D, Ventura VP, Cornelius C, et al. Differential expression of transglutaminase genes in patients with chronic periodontitis. Oral Dis. 2014;20:616–23.PubMedCrossRef Currò M, Matarese G, Isola G, Caccamo D, Ventura VP, Cornelius C, et al. Differential expression of transglutaminase genes in patients with chronic periodontitis. Oral Dis. 2014;20:616–23.PubMedCrossRef
8.
go back to reference Song X, Li J, Jiao M, Chen Y, Pan K. Effect of endoplasmic reticulum stress-induced apoptosis in the role of periodontitis on vascular calcification in a rat model. J Mol Histol. 2021;52:1097–104.PubMedCrossRef Song X, Li J, Jiao M, Chen Y, Pan K. Effect of endoplasmic reticulum stress-induced apoptosis in the role of periodontitis on vascular calcification in a rat model. J Mol Histol. 2021;52:1097–104.PubMedCrossRef
9.
go back to reference Feng Y, Zhang R, Wang YR, Chen F, Luo Q, Cai C, et al. Inhibition of endoplasmic reticulum stress by 4-phenyl butyric acid presents therapeutic effects on periodontitis: experimental studies in vitro and in rats. Stem Cells Int. 2021;2021:6618943.PubMedPubMedCentralCrossRef Feng Y, Zhang R, Wang YR, Chen F, Luo Q, Cai C, et al. Inhibition of endoplasmic reticulum stress by 4-phenyl butyric acid presents therapeutic effects on periodontitis: experimental studies in vitro and in rats. Stem Cells Int. 2021;2021:6618943.PubMedPubMedCentralCrossRef
10.
go back to reference Zhang Q, Jiao Y, Ma N, Zhang L, Song Y. Identification of endoplasmic reticulum stress-related biomarkers of periodontitis based on machine learning: a bioinformatics analysis. Dis Markers. 2022;2022:8611755.PubMedPubMedCentral Zhang Q, Jiao Y, Ma N, Zhang L, Song Y. Identification of endoplasmic reticulum stress-related biomarkers of periodontitis based on machine learning: a bioinformatics analysis. Dis Markers. 2022;2022:8611755.PubMedPubMedCentral
11.
go back to reference Bettigole SE, Glimcher LH. Endoplasmic reticulum stress in immunity. Annu Rev Immunol. 2015;33:107–38.PubMedCrossRef Bettigole SE, Glimcher LH. Endoplasmic reticulum stress in immunity. Annu Rev Immunol. 2015;33:107–38.PubMedCrossRef
12.
go back to reference Cekici A, Kantarci A, Hasturk H, Van Dyke TE. Inflammatory and immune pathways in the pathogenesis of periodontal disease. Periodontol. 2000;2014(64):57–80. Cekici A, Kantarci A, Hasturk H, Van Dyke TE. Inflammatory and immune pathways in the pathogenesis of periodontal disease. Periodontol. 2000;2014(64):57–80.
13.
go back to reference Domon H, Takahashi N, Honda T, Nakajima T, Tabeta K, Abiko Y, et al. Up-regulation of the endoplasmic reticulum stress-response in periodontal disease. Clin Chim Acta. 2009;401:134–40.PubMedCrossRef Domon H, Takahashi N, Honda T, Nakajima T, Tabeta K, Abiko Y, et al. Up-regulation of the endoplasmic reticulum stress-response in periodontal disease. Clin Chim Acta. 2009;401:134–40.PubMedCrossRef
14.
go back to reference Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2002;30:207–10.PubMedPubMedCentralCrossRef Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res. 2002;30:207–10.PubMedPubMedCentralCrossRef
15.
go back to reference Zhang Y, Song Y, Dai J, Wang Z, Zeng Y, Chen F, et al. Endoplasmic reticulum stress-related signature predicts prognosis and drug response in clear cell renal cell carcinoma. Front Pharmacol. 2022;13: 909123.PubMedPubMedCentralCrossRef Zhang Y, Song Y, Dai J, Wang Z, Zeng Y, Chen F, et al. Endoplasmic reticulum stress-related signature predicts prognosis and drug response in clear cell renal cell carcinoma. Front Pharmacol. 2022;13: 909123.PubMedPubMedCentralCrossRef
16.
go back to reference Smyth GK. limma: linear models for microarray data. In: Gentleman R, Carey VJ, Huber W, Irizarry RA, Dudoit S, editors. Bioinformatics and Computational biology solutions using R and bioconductor. New York: Springer; 2005. p. 397–420. Smyth GK. limma: linear models for microarray data. In: Gentleman R, Carey VJ, Huber W, Irizarry RA, Dudoit S, editors. Bioinformatics and Computational biology solutions using R and bioconductor. New York: Springer; 2005. p. 397–420.
17.
go back to reference Szklarczyk D, Morris JH, Cook H, Kuhn M, Wyder S, Simonovic M, et al. The STRING database in 2017: quality-controlled protein-protein association networks, made broadly accessible. Nucleic Acids Res. 2017;45:D362–8.PubMedCrossRef Szklarczyk D, Morris JH, Cook H, Kuhn M, Wyder S, Simonovic M, et al. The STRING database in 2017: quality-controlled protein-protein association networks, made broadly accessible. Nucleic Acids Res. 2017;45:D362–8.PubMedCrossRef
18.
go back to reference Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003;13:2498–504.PubMedPubMedCentralCrossRef Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 2003;13:2498–504.PubMedPubMedCentralCrossRef
19.
20.
go back to reference Hänzelmann S, Castelo R, Guinney J. GSVA: gene set variation analysis for microarray and RNA-seq data. BMC Bioinform. 2013;14:7. CrossRef Hänzelmann S, Castelo R, Guinney J. GSVA: gene set variation analysis for microarray and RNA-seq data. BMC Bioinform. 2013;14:7. CrossRef
21.
22.
go back to reference Kawada JI, Takeuchi S, Imai H, Okumura T, Horiba K, Suzuki T, et al. Immune cell infiltration landscapes in pediatric acute myocarditis analyzed by CIBERSORT. J Cardiol. 2021;77:174–8.PubMedCrossRef Kawada JI, Takeuchi S, Imai H, Okumura T, Horiba K, Suzuki T, et al. Immune cell infiltration landscapes in pediatric acute myocarditis analyzed by CIBERSORT. J Cardiol. 2021;77:174–8.PubMedCrossRef
23.
go back to reference Liberzon A, Subramanian A, Pinchback R, Thorvaldsdóttir H, Tamayo P, Mesirov JP. Molecular signatures database (MSigDB) 3.0. Bioinformatics. 2011;27:1739–40.PubMedPubMedCentralCrossRef Liberzon A, Subramanian A, Pinchback R, Thorvaldsdóttir H, Tamayo P, Mesirov JP. Molecular signatures database (MSigDB) 3.0. Bioinformatics. 2011;27:1739–40.PubMedPubMedCentralCrossRef
24.
go back to reference Tibshirani R. The lasso method for variable selection in the Cox model. Stat Med. 1997;16:385–95.PubMedCrossRef Tibshirani R. The lasso method for variable selection in the Cox model. Stat Med. 1997;16:385–95.PubMedCrossRef
25.
go back to reference Alderden J, Pepper GA, Wilson A, Whitney JD, Richardson S, Butcher R, et al. Predicting pressure injury in critical care patients: a machine-learning model. Am J Crit Care. 2018;27:461–8.PubMedPubMedCentralCrossRef Alderden J, Pepper GA, Wilson A, Whitney JD, Richardson S, Butcher R, et al. Predicting pressure injury in critical care patients: a machine-learning model. Am J Crit Care. 2018;27:461–8.PubMedPubMedCentralCrossRef
26.
go back to reference Cotto KC, Wagner AH, Feng Y-Y, Kiwala S, Coffman AC, Spies G, et al. DGIdb 3.0: a redesign and expansion of the drug–gene interaction database. Nucleic Acids Res. 2017;46:D1068-73.PubMedCentralCrossRef Cotto KC, Wagner AH, Feng Y-Y, Kiwala S, Coffman AC, Spies G, et al. DGIdb 3.0: a redesign and expansion of the drug–gene interaction database. Nucleic Acids Res. 2017;46:D1068-73.PubMedCentralCrossRef
27.
go back to reference Dweep H, Gretz N. miRWalk2.0: a comprehensive atlas of microRNA-target interactions. Nat Methods. 2015;12:697.PubMedCrossRef Dweep H, Gretz N. miRWalk2.0: a comprehensive atlas of microRNA-target interactions. Nat Methods. 2015;12:697.PubMedCrossRef
28.
29.
30.
go back to reference Eieland AK, Normann KR, Sundaram AYM, Nyman TA, Øystese KAB, Lekva T, et al. Distinct pattern of endoplasmic reticulum protein processing and extracellular matrix proteins in functioning and silent corticotroph pituitary adenomas. Cancers. 2020;12:66.CrossRef Eieland AK, Normann KR, Sundaram AYM, Nyman TA, Øystese KAB, Lekva T, et al. Distinct pattern of endoplasmic reticulum protein processing and extracellular matrix proteins in functioning and silent corticotroph pituitary adenomas. Cancers. 2020;12:66.CrossRef
31.
go back to reference Urra H, Dufey E, Avril T, Chevet E, Hetz C. Endoplasmic reticulum stress and the hallmarks of cancer. Trends Cancer. 2016;2:252–62.PubMedCrossRef Urra H, Dufey E, Avril T, Chevet E, Hetz C. Endoplasmic reticulum stress and the hallmarks of cancer. Trends Cancer. 2016;2:252–62.PubMedCrossRef
32.
go back to reference Ren J, Bi Y, Sowers JR, Hetz C, Zhang Y. Endoplasmic reticulum stress and unfolded protein response in cardiovascular diseases. Nat Rev Cardiol. 2021;18:499–521.PubMedCrossRef Ren J, Bi Y, Sowers JR, Hetz C, Zhang Y. Endoplasmic reticulum stress and unfolded protein response in cardiovascular diseases. Nat Rev Cardiol. 2021;18:499–521.PubMedCrossRef
33.
go back to reference Griffin JB, Rodriguez-Melendez R, Dode L, Wuytack F, Zempleni J. Biotin supplementation decreases the expression of the SERCA3 gene (ATP2A3) in Jurkat cells, thus, triggering unfolded protein response. J Nutr Biochem. 2006;17:272–81.PubMedCrossRef Griffin JB, Rodriguez-Melendez R, Dode L, Wuytack F, Zempleni J. Biotin supplementation decreases the expression of the SERCA3 gene (ATP2A3) in Jurkat cells, thus, triggering unfolded protein response. J Nutr Biochem. 2006;17:272–81.PubMedCrossRef
34.
go back to reference Zhang Y, Li F, Liu L, Jiang H, Hu H, Du X, et al. Salinomycin triggers endoplasmic reticulum stress through ATP2A3 upregulation in PC-3 cells. BMC Cancer. 2019;19:381.PubMedPubMedCentralCrossRef Zhang Y, Li F, Liu L, Jiang H, Hu H, Du X, et al. Salinomycin triggers endoplasmic reticulum stress through ATP2A3 upregulation in PC-3 cells. BMC Cancer. 2019;19:381.PubMedPubMedCentralCrossRef
35.
go back to reference Izquierdo-Torres E, Hernández-Oliveras A, Meneses-Morales I, Rodríguez G, Fuentes-García G, Zarain-Herzberg Á. Resveratrol up-regulates ATP2A3 gene expression in breast cancer cell lines through epigenetic mechanisms. Int J Biochem Cell Biol. 2019;113:37–47.PubMedCrossRef Izquierdo-Torres E, Hernández-Oliveras A, Meneses-Morales I, Rodríguez G, Fuentes-García G, Zarain-Herzberg Á. Resveratrol up-regulates ATP2A3 gene expression in breast cancer cell lines through epigenetic mechanisms. Int J Biochem Cell Biol. 2019;113:37–47.PubMedCrossRef
36.
go back to reference Li S, Wang Y, Zhao H, He Y, Li J, Jiang G, et al. NF-kappa B-mediated inflammation correlates with calcium overload under arsenic trioxide-induced myocardial damage in Gallus gallus. Chemosphere. 2017;185:618–27.PubMedCrossRef Li S, Wang Y, Zhao H, He Y, Li J, Jiang G, et al. NF-kappa B-mediated inflammation correlates with calcium overload under arsenic trioxide-induced myocardial damage in Gallus gallus. Chemosphere. 2017;185:618–27.PubMedCrossRef
37.
go back to reference Ghosh S, Adhikary A, Chakraborty S, Nandi P, Mohanty S, Chakraborty S, et al. Nifetepimine, a dihydropyrimidone, ensures CD4+ T cell survival in a tumor microenvironment by maneuvering sarco(endo)plasmic reticulum Ca2+ ATPase (SERCA). J Biol Chem. 2012;287:32881–96.PubMedPubMedCentralCrossRef Ghosh S, Adhikary A, Chakraborty S, Nandi P, Mohanty S, Chakraborty S, et al. Nifetepimine, a dihydropyrimidone, ensures CD4+ T cell survival in a tumor microenvironment by maneuvering sarco(endo)plasmic reticulum Ca2+ ATPase (SERCA). J Biol Chem. 2012;287:32881–96.PubMedPubMedCentralCrossRef
38.
go back to reference Zhang Z, Zheng Y, Bian X, Jin M. Construction of potential periodontitis-related miRNA-mRNA regulatory network. 2020. Zhang Z, Zheng Y, Bian X, Jin M. Construction of potential periodontitis-related miRNA-mRNA regulatory network. 2020.
39.
go back to reference Uttamani JR, Naqvi AR, Estepa AMV, Kulkarni V, Brambila MF, Martínez G, et al. Downregulation of miRNA-26 in chronic periodontitis interferes with innate immune responses and cell migration by targeting phospholipase C beta 1. J Clin Periodontol. 2022;6:66. Uttamani JR, Naqvi AR, Estepa AMV, Kulkarni V, Brambila MF, Martínez G, et al. Downregulation of miRNA-26 in chronic periodontitis interferes with innate immune responses and cell migration by targeting phospholipase C beta 1. J Clin Periodontol. 2022;6:66.
40.
go back to reference Wu X, Yin S, Yan L, Liu Y, Shang L, Liu J. lncRNA DLEU1 modulates proliferation, inflammation, and extracellular matrix degradation of chondrocytes through regulating miR-671-5p. J Immunol Res. 2022;2022:1816217.PubMedPubMedCentralCrossRef Wu X, Yin S, Yan L, Liu Y, Shang L, Liu J. lncRNA DLEU1 modulates proliferation, inflammation, and extracellular matrix degradation of chondrocytes through regulating miR-671-5p. J Immunol Res. 2022;2022:1816217.PubMedPubMedCentralCrossRef
41.
go back to reference Lien GS, Liu JF, Chien MH, Hsu WT, Chang TH, Ku CC, et al. The ability to suppress macrophage-mediated inflammation in orbital fat stem cells is controlled by miR-671-5p. Stem Cell Res Ther. 2014;5:97.PubMedPubMedCentralCrossRef Lien GS, Liu JF, Chien MH, Hsu WT, Chang TH, Ku CC, et al. The ability to suppress macrophage-mediated inflammation in orbital fat stem cells is controlled by miR-671-5p. Stem Cell Res Ther. 2014;5:97.PubMedPubMedCentralCrossRef
42.
go back to reference Gao L, Dou ZC, Ren WH, Li SM, Liang X, Zhi KQ. CircCDR1as upregulates autophagy under hypoxia to promote tumor cell survival via AKT/ERK(½)/mTOR signaling pathways in oral squamous cell carcinomas. Cell Death Dis. 2019;10:745.PubMedPubMedCentralCrossRef Gao L, Dou ZC, Ren WH, Li SM, Liang X, Zhi KQ. CircCDR1as upregulates autophagy under hypoxia to promote tumor cell survival via AKT/ERK(½)/mTOR signaling pathways in oral squamous cell carcinomas. Cell Death Dis. 2019;10:745.PubMedPubMedCentralCrossRef
43.
go back to reference Hu Q, Zheng J, Xu XN, Gu C, Li W. Uranium induces kidney cells apoptosis via reactive oxygen species generation, endoplasmic reticulum stress and inhibition of PI3K/AKT/mTOR signaling in culture. Environ Toxicol. 2022;37:66.CrossRef Hu Q, Zheng J, Xu XN, Gu C, Li W. Uranium induces kidney cells apoptosis via reactive oxygen species generation, endoplasmic reticulum stress and inhibition of PI3K/AKT/mTOR signaling in culture. Environ Toxicol. 2022;37:66.CrossRef
44.
go back to reference Feng Y, Zhang R, Wang YR, Chen F, Xue P. Inhibition of endoplasmic reticulum stress by 4-phenyl butyric acid presents therapeutic effects on periodontitis: experimental studies in vitro and in rats. Stem Cells Int. 2021;66:18943. Feng Y, Zhang R, Wang YR, Chen F, Xue P. Inhibition of endoplasmic reticulum stress by 4-phenyl butyric acid presents therapeutic effects on periodontitis: experimental studies in vitro and in rats. Stem Cells Int. 2021;66:18943.
45.
go back to reference Zeng L, Zampetaki A, Margariti A, Pepe AE, Xu Q. Sustained activation of XBP1 splicing leads to endothelial apoptosis and atherosclerosis development in response to disturbed flow. Proc Natl Acad Sci. 2009;106:8326–31.PubMedPubMedCentralCrossRef Zeng L, Zampetaki A, Margariti A, Pepe AE, Xu Q. Sustained activation of XBP1 splicing leads to endothelial apoptosis and atherosclerosis development in response to disturbed flow. Proc Natl Acad Sci. 2009;106:8326–31.PubMedPubMedCentralCrossRef
46.
go back to reference Reimold AM, Iwakoshi NN, Manis J, Vallabhajosyula P, Szomolanyi-Tsuda E, Gravallese EM, et al. Plasma cell differentiation requires the transcription factor XBP-1. Nature. 2001;412:300–7.PubMedCrossRef Reimold AM, Iwakoshi NN, Manis J, Vallabhajosyula P, Szomolanyi-Tsuda E, Gravallese EM, et al. Plasma cell differentiation requires the transcription factor XBP-1. Nature. 2001;412:300–7.PubMedCrossRef
47.
go back to reference Lugea A, Gukovsky I, French S et al. T1834 role of XBP1 in the protective unfolded protein response to limit chronic ethanol-induced endoplasmic reticulum stress and damage in the pancreas. Gastroenterology. 2009;136:A-589. Lugea A, Gukovsky I, French S et al. T1834 role of XBP1 in the protective unfolded protein response to limit chronic ethanol-induced endoplasmic reticulum stress and damage in the pancreas. Gastroenterology. 2009;136:A-589.
48.
go back to reference Li LF, Wen Y, Jiang L, Zhu YQ. Study of endoplasmic reticulum stress response in osteogenic differentiation of human periodontal ligament cells. Shanghai Kou Qiang Yi Xue. 2017;26:577–81.PubMed Li LF, Wen Y, Jiang L, Zhu YQ. Study of endoplasmic reticulum stress response in osteogenic differentiation of human periodontal ligament cells. Shanghai Kou Qiang Yi Xue. 2017;26:577–81.PubMed
49.
go back to reference Ma X, Bi E, Lu Y, Su P, Huang C, Liu L, et al. Cholesterol induces CD8(+) T cell exhaustion in the tumor microenvironment. Cell Metab. 2019;30:143-56.e5.PubMedPubMedCentralCrossRef Ma X, Bi E, Lu Y, Su P, Huang C, Liu L, et al. Cholesterol induces CD8(+) T cell exhaustion in the tumor microenvironment. Cell Metab. 2019;30:143-56.e5.PubMedPubMedCentralCrossRef
50.
go back to reference Martinon F, Chen X, Lee AH, Glimcher LH. TLR activation of the transcription factor XBP1 regulates innate immune responses in macrophages. Nat Immunol. 2010;11:411–8.PubMedPubMedCentralCrossRef Martinon F, Chen X, Lee AH, Glimcher LH. TLR activation of the transcription factor XBP1 regulates innate immune responses in macrophages. Nat Immunol. 2010;11:411–8.PubMedPubMedCentralCrossRef
51.
go back to reference Polizzi A, Santonocito S, Lo Giudice A, Alibrandi A, De Pasquale R, Isola G. Analysis of the response to two pharmacological protocols in patients with oral lichen planus: a randomized clinical trial. Oral Dis. 2023;29:755–63.PubMedCrossRef Polizzi A, Santonocito S, Lo Giudice A, Alibrandi A, De Pasquale R, Isola G. Analysis of the response to two pharmacological protocols in patients with oral lichen planus: a randomized clinical trial. Oral Dis. 2023;29:755–63.PubMedCrossRef
52.
go back to reference Elli L, Bergamini CM, Bardella MT, Schuppan D. Transglutaminases in inflammation and fibrosis of the gastrointestinal tract and the liver. Dig Liver Dis. 2009;41:541–50.PubMedCrossRef Elli L, Bergamini CM, Bardella MT, Schuppan D. Transglutaminases in inflammation and fibrosis of the gastrointestinal tract and the liver. Dig Liver Dis. 2009;41:541–50.PubMedCrossRef
53.
go back to reference Shrestha S, Wiener HW, Olson AK, Edberg JC, Bowles NE, Patel H, et al. Functional FCGR2B gene variants influence intravenous immunoglobulin response in patients with Kawasaki disease. J Allergy Clin Immunol. 2011;128:677–80.PubMedPubMedCentralCrossRef Shrestha S, Wiener HW, Olson AK, Edberg JC, Bowles NE, Patel H, et al. Functional FCGR2B gene variants influence intravenous immunoglobulin response in patients with Kawasaki disease. J Allergy Clin Immunol. 2011;128:677–80.PubMedPubMedCentralCrossRef
54.
go back to reference Heikkinen AM, Kettunen K, Kovanen L, Haukka J, Elg J, Husu H, et al. Inflammatory mediator polymorphisms associate with initial periodontitis in adolescents. Clin Exp Dent Res. 2016;2:208–15.PubMedPubMedCentralCrossRef Heikkinen AM, Kettunen K, Kovanen L, Haukka J, Elg J, Husu H, et al. Inflammatory mediator polymorphisms associate with initial periodontitis in adolescents. Clin Exp Dent Res. 2016;2:208–15.PubMedPubMedCentralCrossRef
55.
go back to reference Nowicka M, Hilton LK, Ashton-Key M, Hargreaves CE, Lee C, Foxall R, et al. Prognostic significance of FCGR2B expression for the response of DLBCL patients to rituximab or obinutuzumab treatment. Blood Adv. 2021;5:2945–57.PubMedPubMedCentralCrossRef Nowicka M, Hilton LK, Ashton-Key M, Hargreaves CE, Lee C, Foxall R, et al. Prognostic significance of FCGR2B expression for the response of DLBCL patients to rituximab or obinutuzumab treatment. Blood Adv. 2021;5:2945–57.PubMedPubMedCentralCrossRef
Metadata
Title
Molecular mechanism and diagnostic marker investigation of endoplasmic reticulum stress on periodontitis
Authors
Qianqian Sun
Enqiang Zhu
Publication date
01-12-2023
Publisher
BioMed Central
Published in
BMC Oral Health / Issue 1/2023
Electronic ISSN: 1472-6831
DOI
https://doi.org/10.1186/s12903-023-02822-5

Other articles of this Issue 1/2023

BMC Oral Health 1/2023 Go to the issue