Evaluation of apoptosis and hypoxia-related factors in gingival tissues of smoker and non-smoker periodontitis patients.
Apoptosis
Basic Helix-Loop-Helix Transcription Factors
Case-Control Studies
Caspase 3
Fibroblasts
Gingiva
/ pathology
Gingival Crevicular Fluid
Humans
Hypoxia
Matrix Metalloproteinase 8
Non-Smokers
Periodontitis
/ physiopathology
Proto-Oncogene Proteins c-bcl-2
Smokers
Tissue Inhibitor of Metalloproteinase-1
Vascular Endothelial Growth Factor A
bcl-2-Associated X Protein
apoptosis
hypoxia
smoking
Journal
Journal of periodontal research
ISSN: 1600-0765
Titre abrégé: J Periodontal Res
Pays: United States
ID NLM: 0055107
Informations de publication
Date de publication:
Jun 2020
Jun 2020
Historique:
received:
06
09
2018
revised:
01
11
2019
accepted:
25
11
2019
pubmed:
20
12
2019
medline:
17
9
2020
entrez:
20
12
2019
Statut:
ppublish
Résumé
Smoking causes pathological changes in all tissues, including gingiva and alveolar bone. The aim of present study was to evaluate apoptotic tissue alterations and tissue destruction in smoker and non-smoker periodontitis patients and healthy individuals. Gingival biopsy samples from 15 systemically and orally healthy individuals (Group 1), 15 systemically healthy periodontitis patients (Group 2), 15 systemically and orally healthy smokers (Group 3), and 15 systemically healthy smoker periodontitis patients (Group 4) were enrolled in the present study. Clinical periodontal measurements as plaque index (PI), gingival index (GI), and clinical attachment levels (CAL) were recorded, and gingival biopsies were obtained. Biopsy samples were fixed in formalin solution and embedded in paraffin. Fibroblast and inflammatory cell counts were determined via histomorphometrically. Hypoxia-inducible factor alpha (HIF-1α), vascular endothelial growth factor(VEGF), tissue inhibitor of matrix metalloproteinase-1(TIMP-1), matrix metalloproteinases-8(MMP-8) expressions, Bax, Bcl-2, and caspase-3 expressions were evaluated via immunohistochemistry. Demographic data of the study groups were similar. Smoking levels of the smokers were also similar. The highest fibroblast cell counts were observed in healthy controls and the counts were similar in other groups. The highest inflammatory cell counts were found in smoker periodontitis group, and the lowest counts were found in healthy control groups. The differences were statistically significant. HIF-1α and Bax expressions were elevated and Bcl-2 decreased in smoker periodontitis patients compared with healthy individuals. However, there were no differences in VEGF, MMP-8, and TIMP-1 expressions. Within limits of present study, it can be suggested that both smoking and periodontitis caused similar decrease in fibroblast counts while causing a dramatic increase in inflammatory cell counts. Increased apoptosis and hypoxia also accompanied to the increased inflammation.
Substances chimiques
BAX protein, human
0
BCL2 protein, human
0
Basic Helix-Loop-Helix Transcription Factors
0
Proto-Oncogene Proteins c-bcl-2
0
TIMP1 protein, human
0
Tissue Inhibitor of Metalloproteinase-1
0
VEGFA protein, human
0
Vascular Endothelial Growth Factor A
0
bcl-2-Associated X Protein
0
endothelial PAS domain-containing protein 1
1B37H0967P
CASP3 protein, human
EC 3.4.22.-
Caspase 3
EC 3.4.22.-
MMP8 protein, human
EC 3.4.24.34
Matrix Metalloproteinase 8
EC 3.4.24.34
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
392-399Informations de copyright
© 2019 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd.
Références
Page RC, Kornman KS. The pathogenesis of human periodontitis: an introduction. Periodontol 2000. 1997;14(1):9-11.
Cekici A, Kantarci A, Hasturk H, Van Dyke TE. Inflammatory and immune pathways in the pathogenesis of periodontal disease. Periodontol 2000. 2014;64(1):57-80.
Adler L, Modin C, Friskopp J, Jansson L. Relationship between smoking and periodontal probing pocket depth profile. Swed Dent J. 2008;32(4):157-163.
White PC, Hirschfeld J, Milward MR, et al. Cigarette smoke modifies neutrophil chemotaxis, neutrophil extracellular trap formation and inflammatory response-related gene expression. J Periodontal Res. 2018;53(4):525-535.
Centers for Disease Control and Prevention. How tobacco smoke causes disease: the biology and behavioral basis for smoking-attributable disease: a report of the surgeon general; 2010.
Horinouchi T, Higashi T, Mazaki Y, Miwa S. Carbonyl compounds in the gas phase of cigarette mainstream smoke and their pharmacological properties. Biol Pharm Bull. 2016;39(6):909-914.
Lu X, Cai J, Kong H, et al. Analysis of cigarette smoke condensates by comprehensive two-dimensional gas chromatography/time-of-flight mass spectrometry I acidic fraction. Anal Chem. 2003;75(17):4441-4451.
Kang SW, Park HJ, Ban JY, Chung JH, Chun GS, Cho JO. Effects of nicotine on apoptosis in human gingival fibroblasts. Arch Oral Biol. 2011;56(10):1091-1097.
Gutiérrez-Venegas G, Guadarrama-Solís A, Muñoz-Seca C, Arreguín-Cano JA. Hydrogen peroxide-induced apoptosis in human gingival fibroblasts. Int J Clin Exp Pathol. 2015;8(12):15563.
Kashiwagi Y, Yanagita M, Kojima Y, Shimabukuro Y, Murakami S. Nicotine up-regulates IL-8 expression in human gingival epithelial cells following stimulation with IL-1β or P gingivalis lipopolysaccharide via nicotinic acetylcholine receptor signalling. Arch Oral Biol. 2012;57(5):483-490.
Liu Y-F, Ge X, Wen L-Y, Wang X-J. Targeting nicotinic acetylcholine receptor to treat smoking-related periodontitis. Med Hypotheses. 2011;76(2):244-245.
Alamri A, Semlali A, Jacques É, et al. Long-term exposure of human gingival fibroblasts to cigarette smoke condensate reduces cell growth by modulating B ax, c aspase-3 and p 53 expression. J Periodontal Res. 2015;50(4):423-433.
Mehta H, Nazzal K, Sadikot RT. Cigarette smoking and innate immunity. Inflamm Res. 2008;57(11):497-503.
Sato Y. Molecular mechanism of angiogenesis transcription factors and their therapeutic relevance. Pharmacol Therapeut. 2000;87(1):51-60.
Hirota K, Fukamizu A. Transcriptional regulation of energy metabolism in the liver. J Recept Signal Transduct Res. 2010;30(6):403-409.
Greijer A, Van der Wall E. The role of hypoxia inducible factor 1 (HIF-1) in hypoxia induced apoptosis. J Clin Pathol. 2004;57(10):1009-1014.
Das A, Chakrabarty S, Choudhury D, Chakrabarti G. 1, 4-Benzoquinone (PBQ) induced toxicity in lung epithelial cells is mediated by the disruption of the microtubule network and activation of caspase-3. Chem Res Toxicol. 2010;23(6):1054-1066.
Carmeliet P, Dor Y, Herbert J-M, et al. Role of HIF-1α in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. Nature. 1998;394(6692):485.
Laxman VK, Annaji S. Tobacco use and its effects on the periodontium and periodontal therapy. J Contemp Dent Pract. 2008;9(7):97-107.
Cáceres M, Oyarzun A, Smith P. Defective wound-healing in aging gingival tissue. J Dent Res. 2014;93(7):691-697.
Lekic P, Pender N, McCulloch C. Is fibroblast heterogeneity relevant to the health, diseases, and treatments of periodontal tissues? Crit Rev Oral Biol Med. 1997;8(3):253-268.
Caton JG, Armitage G, Berglundh T, et al. classification. J Periodontol. 1999;2018(89):S1-S8.
Glavind L, Löe H. Errors in the clinical assessment of periodontal destruction. J Periodontal Res. 1967;2(3):180-184.
Silness J, Loe H. Periodontal disease in pregnancy. Ii. Correlation between oral hygiene and periodontal condtion. Acta Odontol Scand. 1964;22:121-135.
Loe H, Silness J. Periodontal disease in pregnancy. I. Prevalence and severity. Acta Odontol Scand. 1963;21:533-551.
Fawcett DW, Bloom W, Raviola E. A Textbook of Histology (Vol. 530). Philadelphia, PA: Saunders; 1986.
Häkkinen L, Larjava H, Fournier BP. Distinct phenotype and therapeutic potential of gingival fibroblasts. Cytotherapy. 2014;16(9):1171-1186.
Fournier BP, Larjava H, Häkkinen L. Gingiva as a source of stem cells with therapeutic potential. Stem Cell Develop. 2013;22(24):3157-3177.
Balci Yuce H, Lektemur Alpan A, Gevrek F, Toker H. Investigation of the effect of astaxanthin on alveolar bone loss in experimental periodontitis. J Periodontal Res. 2018;53(1):131-138.
Toker H, Balci Yuce H, Lektemur Alpan A, Gevrek F, Elmastas M. Morphometric and histopathological evaluation of the effect of grape seed proanthocyanidin on alveolar bone loss in experimental diabetes and periodontitis. J Periodontal Res. 2018;53(3):478-486.
Xing T, Wang Y, Ding W-J, et al. Thrombospondin-1 production regulates the inflammatory cytokine secretion in THP-1 cells through NF-κB signaling pathway. Inflammation. 2017;40(5):1606-1621.
Balci Yuce H, Akbulut N, Ocakli S, Kayir O, Elmastas M. The effect of commercial conjugated linoleic acid products on experimental periodontitis and diabetes mellitus in Wistar rats. Acta Odontol Scand. 2017;75(1):21-29.
Lazăr L, Loghin A, Bud E-S, Cerghizan D, Horváth E, Nagy EE. Cyclooxygenase-2 and matrix metalloproteinase-9 expressions correlate with tissue inflammation degree in periodontal disease. Rom J Morphol Embryol. 2015;56(4):1441-1446.
Dong W, Xiang J, Li C, Cao Z, Huang Z. Increased expression of extracellular matrix metalloproteinase inducer is associated with matrix metalloproteinase-1 and-2 in gingival tissues from patients with periodontitis. J Periodontal Res. 2009;44(1):125-132.
Sánchez-Hernández P, Zamora-Perez A, Fuentes-Lerma M, Robles-Gómez C, Mariaud-Schmidt R, Guerrero-Velázquez C. IL-12 and IL-18 levels in serum and gingival tissue in aggressive and chronic periodontitis. Oral Dis. 2011;17(5):522-529.
Kannan K, Jain SK. Oxidative stress and apoptosis. Pathophysiology. 2000;7(3):153-163.
de Groot H, Littauer A. Hypoxia, reactive oxygen, and cell injury. Free Radic Biol Med. 1989;6(5):541-551.
Lee H, Park J-R, Kim E-J, et al. Cigarette smoke-mediated oxidative stress induces apoptosis via the MAPKs/STAT1 pathway in mouse lung fibroblasts. Toxicol Lett. 2016;240(1):140-148.
Sancilio S, Gallorini M, Cataldi A, di Giacomo V. Cytotoxicity and apoptosis induction by e-cigarette fluids in human gingival fibroblasts. Clin Oral Invest. 2016;20(3):477-483.
Elmore S. Apoptosis: a review of programmed cell death. Toxicol Pathol. 2007;35(4):495-516.
Gorman D, Drewry A, Huang YL, Sames C. The clinical toxicology of carbon monoxide. Toxicology. 2003;187(1):25-38.
Nemr R, Lasserre B, Chahine R. Effects of nicotine on thromboxane/prostacyclin balance in myocardial ischemia. Prostaglandins Leukot Essent Fatty Acids. 2003;68(3):191-195.
Ziello JE, Jovin IS, Huang Y. Hypoxia-Inducible Factor (HIF)-1 regulatory pathway and its potential for therapeutic intervention in malignancy and ischemia. Yale J Biol Med. 2007;80(2):51-60.
Kim YS, Shin SI, Kang KL, et al. Nicotine and lipopolysaccharide stimulate the production of MMPs and prostaglandin E2 by hypoxia-inducible factor-1alpha up-regulation in human periodontal ligament cells. J Periodontal Res. 2012;47(6):719-728.
Guan R, Wang J, Li Z, et al. Sodium Tanshinone IIA sulfonate decreases cigarette smoke-induced inflammation and oxidative stress via blocking the activation of MAPK/HIF-1alpha signaling pathway. Front Pharmacol. 2018;9:263.
Franco C, Patricia HR, Timo S, Claudia B, Marcela H. Matrix Metalloproteinases as Regulators of Periodontal Inflammation. Int J Mol Sci. 2017;18:440.
Golz L, Memmert S, Rath-Deschner B, et al. gingivalis synergistically induce HIF-1 and NF-kappaB activation in PDL cells and periodontal diseases. Mediators Inflamm. 2015;2015:438085.
Teasdale JE, Hazell GGJ, Peachey AMG, et al. Cigarette smoke extract profoundly suppresses TNFα-mediated proinflammatory gene expression through upregulation of ATF3 in human coronary artery endothelial cells. Scientific Rep. 2017;7:39945.
Higuchi T, Omata F, Tsuchihashi K, Higashioka K, Koyamada R, Okada S. Current cigarette smoking is a reversible cause of elevated white blood cell count: Cross-sectional and longitudinal studies. Prev Med Rep. 2016;4:417-422.