Correlation of the expression of tumor necrosis factor-alpha in chronic periapical lesions with the expression of bacterial chaperonin 60
Abstract
Background/Aim. Chronic microbial infections of the root canal are a common issue. This process very often causes an immune reaction in the root canal system that results in forming of chronic periapical lesions (PLs). The aim of this study was to determine the quantitative expression of the bacterial heat shock protein (HSP), chaperonin 60 (cpn60), and the pro-inflammatory and anti-inflammatory cytokines in periapical tissue obtained from individuals with chronic PLs and to determine if there is a correlation between the expression of the bacterial HSP and the expression of these cytokines. Methods. The study was performed on 18 PLs and 6 control samples of healthy periapical tissue, taken at the Department of Dentistry, Faculty of Medicine, University of Priština/Kosovska Mitrovica. The levels of messenger ribonucleic acid (mRNA) expression of pro- and anti-inflammatory cytokines and bacterial HSP were determined by quantitative real-time polymerase chain reaction (RT-PCR) and quantified by comparing to the internal control gene for glyceraldehyde 3-phosphate dehydrogenase (GAPDH). Results. Analysis revealed significantly higher mRNA levels of tumor necrosis factor-alpha (TNF-a) and cpn60 in the tissue of PLs compared with normal periapical tissue (p < 0.05). Contrary to these results, the mRNA expression of anti-inflammatory interleukin-10 (IL-10) was significantly higher in the samples of normal periapical tissue compared with the mRNA levels of this cytokine in the tissue of PLs (p < 0.001). Expression of cpn60 is in strong correlation with TNF-a expression in PLs. Conclusion. cpn60 released from bacteria in periapical tissue could be a strong stimulator of inflammatory response and one of the important players in the pathogenesis of PLs.
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1. Sasaki H, Hirai K, Martins CM, Furusho H, Battaglino R, Hashimoto K. Interrelationship Between Periapical Lesion and Systemic Metabolic Disorders. Curr Pharm Des 2016; 22(15): 2204‒15.
2. Stashenko P, Teles R, D'Souza R. Periapical inflammatory responses and their modulation. Crit Rev Oral Biol Med 1998; 9(4): 498‒521.
3. Bouillaguet S, Manoil D, Girard M, Louis J, Gaïa N, Leo S, et al. Root Microbiota in Primary and Secondary Apical Periodontitis. Front Microbiol 2018; 9: 2374.
4. Gomes BPFA, Herrera DR. Etiologic role of root canal infection in apical periodontitis and its relationship with clinical symptomatology. Braz Oral Res 2018; 32(Suppl 1): e69.
5. Chen B, Feder ME, Kang L. Evolution of heat-shock protein expression underlying adaptive responses to environmental stress. Mol Ecol 2018; 27(15): 3040‒54.
6. Tabeta K, Yamazaki K, Hotokezaka H, Yoshie H, Hara K. Elevated humoral immune response to heat shock protein 60 (hsp60) family in periodontitis patients. Clin Exp Immunol 2000; 120(2): 285‒93.
7. Chen Q, Wu G, Chen H, Li H, Li S, Zhang C, et al. Quantification of Human Oral and Fecal Streptococcus parasanguinis by Use of Quantitative Real-Time PCR Targeting the groEL Gene. Front Microbiol 2019; 10: 2910.
8. Links MG, Dumonceaux TJ, Hemmingsen SM, Hill JE. The chaperonin-60 universal target is a barcode for bacteria that enables de novo assembly of metagenomic sequence data. PLoS One 2012; 7(11): e49755.
9. Bansal A, Paliwal PK, Sagi SS, Sairam M. Effect of adjuvants on immune response and protective immunity elicited by recombinant Hsp60 (GroEL) of Salmonella typhi against S. typhi infection. Mol Cell Biochem 2010; 337(1‒2): 213‒21.
10. Gholizadeh P, Pormohammad A, Eslami H, Shokouhi B, Fakhrzadeh V, Kafil HS. Oral pathogenesis of Aggregatibacter actinomycetemcomitans. Microb Pathog 2017; 113: 303‒11.
11. Colić M, Gazivoda D, Vucević D, Vasilijić S, Rudolf R, Lukić A. Proinflammatory and immunoregulatory mechanisms in periapical lesions. Mol Immunol 2009; 47(1): 101‒13.
12. Velickovic M, Pejnovic N, Petrovic R, Mitrovic S, Jeftic I, Kanjevac T, et al. Expression of interleukin-33 and its receptor ST2 in periapical granulomas and radicular cysts. J Oral Pathol Med 2016; 45(1): 70‒6.
13. Álvares PR, de Arruda JAA, Oliveira Silva LV, da Silva LP, do Nascimento GJF, da Silveira MMF, et al. Immunohistochemical Analysis of Cyclooxygenase-2 and Tumor Necrosis Factor Alpha in Periapical Lesions. J Endod 2018; 44(12): 1783‒7.
14. Maia LM, Espaladori MC, Diniz JMB, Tavares WLF, de Brito LCN, Vieira LQ, et al. Clinical endodontic procedures modulate periapical cytokine and chemokine gene expressions. Clin Oral Investig 2020; 24(10): 3691‒7.
15. Walker KF, Lappin DF, Takahashi K, Hope J, Macdonald DG, Kinane DF. Cytokine expression in periapical granulation tissue as assessed by immunohistochemistry. Eur J Oral Sci 2000; 108(3): 195‒201.
16. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 2001; 25(4): 402‒8.
17. Dreier J, Störmer M, Kleesiek K. Two novel real-time reverse transcriptase PCR assays for rapid detection of bacterial contamination in platelet concentrates. J Clin Microbiol 2004; 42(10): 4759‒64.
18. Goh SH, Potter S, Wood JO, Hemmingsen SM, Reynolds RP, Chow AW. HSP60 gene sequences as universal targets for microbial species identification: studies with coagulase-negative staphylococci. J Clin Microbiol 1996; 34(4): 818‒23.
19. Brousseau R, Hill JE, Préfontaine G, Goh SH, Harel J, Hemmingsen SM. Streptococcus suis serotypes characterized by analysis of chaperonin 60 gene sequences. Appl Environ Microbiol 2001; 67(10): 4828‒33.
20. Márton IJ, Kiss C. Overlapping protective and destructive regulatory pathways in apical periodontitis. J Endod 2014; 40(2): 155‒63.
21. Goodman SC, Letra A, Dorn S, Araujo-Pires AC, Vieira AE, Chaves de Souza L, et al. Expression of heat shock proteins in periapical granulomas. J Endod 2014; 40(6): 830‒6.
22. Andisheh-Tadbir A, Fakharian M. HSP70 expression in dentigerous cyst, odontogenic keratocyst, and ameloblastoma. Oral Maxillofac Surg 2015; 19(3): 287‒91.
23. Leonardi R, Villari L, Caltabiano M, Travali S. Heat shock protein 27 expression in the epithelium of periapical lesions. J Endod 2001; 27(2): 89‒92.
24. Suzuki T, Kumamoto H, Ooya K. Expression of inducible nitric oxide synthase and heat shock proteins in periapical inflammatory lesions. J Oral Pathol Med 2002; 31(8): 488‒93.
25. Maheshwari K, Silva RM, Guajardo-Morales L, Garlet GP, Vieira AR, Letra A. Heat Shock 70 Protein Genes and Genetic Susceptibility to Apical Periodontitis. J Endod 2016; 42(10): 1467‒71.
26. Paju S, Goulhen F, Asikainen S, Grenier D, Mayrand D, Uitto V. Localization of heat shock proteins in clinical Actinobacillus actinomycetemcomitans strains and their effects on epithelial cell proliferation. FEMS Microbiol Lett 2000; 182(2): 231‒5.
27. Honda T, Domon H, Okui T, Kajita K, Amanuma R, Yamazaki K. Balance of inflammatory response in stable gingivitis and progressive periodontitis lesions. Clin Exp Immunol 2006; 144(1): 35‒40.
28. Hasan A, Sadoh D, Palmer R, Foo M, Marber M, Lehner T. The immune responses to human and microbial heat shock proteins in periodontal disease with and without coronary heart disease. Clin Exp Immunol 2005; 142(3): 585‒94.
29. Yamazaki K, Ohsawa Y, Tabeta K, Ito H, Ueki K, Oda T, et al. Accumulation of human heat shock protein 60-reactive T cells in the gingival tissues of periodontitis patients. Infect Immun 2002; 70(5): 2492‒501.
30. Nalbant A, Saygılı T. IL12, IL10, IFNγ and TNFα Expression in Human Primary Monocytes Stimulated with Bacterial Heat Shock GroEL (Hsp64) Protein. PLoS One 2016; 11(4): e0154085.
31. Saygılı T, Akıncılar SC, Akgül B, Nalbant A. Aggregatibacter actinomycetemcomitans GroEL protein promotes conversion of human CD4+ T cells into IFNγ IL10 producing Tbet+ Th1 cells. PLoS One 2012; 7(11): e49252.
32. Torres-Huerta A, Villaseñor T, Flores-Alcantar A, Parada C, Alemán-Navarro E, Espitia C, et al. Interaction of the CD43 Sialomucin with the Mycobacterium tuberculosis Cpn60.2 Chaperonin Leads to Tumor Necrosis Factor Alpha Production. Infect Immun 2017; 85(3): e00915-16.
33. Cehovin A, Coates AR, Hu Y, Riffo-Vasquez Y, Tormay P, Botanch C, et al. Comparison of the moonlighting actions of the two highly homologous chaperonin 60 proteins of Mycobacterium tuberculosis. Infect Immun 2010; 78(7): 3196‒206.
34. Hienz SA, Paliwal S, Ivanovski S. Mechanisms of Bone Resorption in Periodontitis. J Immunol Res 2015; 2015: 615486.
35. Nair SP, Meghji S, Wilson M, Reddi K, White P, Henderson B. Bacterially induced bone destruction: mechanisms and misconceptions. Infect Immun 1996; 64(7): 2371‒80.
36. Parveen N, Varman R, Nair S, Das G, Ghosh S, Mukhopadhyay S. Endocytosis of Mycobacterium tuberculosis heat shock protein 60 is required to induce interleukin-10 production in macrophages. J Biol Chem 2013; 288(34): 24956‒71.
37. Zhang Q, Chen B, Yan F, Guo J, Zhu X, Ma S, et al. Interleukin-10 inhibits bone resorption: a potential therapeutic strategy in periodontitis and other bone loss diseases. Biomed Res Int 2014; 2014: 284836.
38. Marcatili A, de I'Ero GC, Galdiero M, Folgore A, Petrillo G. TNF-alpha, IL-1 alpha, IL-6 and ICAM-1 expression in human keratinocytes stimulated in vitro with Escherichia coli heat-shock proteins. Microbiology (Reading) 1997; 143(Pt 1): 45‒53.
39. Graham GM, Farrar MD, Cruse-Sawyer JE, Holland KT, Ingham E. Proinflammatory cytokine production by human keratinocytes stimulated with Propionibacterium acnes and P. acnes GroEL. Br J Dermatol 2004; 150(3): 421‒8.