A disintegrin-like and metalloproteinase with thrombospondin-1 (ADAMTS-1) levels in gingival crevicular fluid correlate with vascular endothelial growth factor-A, hypoxia-inducible factor-1α, and clinical parameters in patients with advanced periodontitis.


Journal

Journal of periodontology
ISSN: 1943-3670
Titre abrégé: J Periodontol
Pays: United States
ID NLM: 8000345

Informations de publication

Date de publication:
10 2019
Historique:
received: 26 03 2018
revised: 14 12 2018
accepted: 22 02 2019
pubmed: 26 4 2019
medline: 9 4 2020
entrez: 26 4 2019
Statut: ppublish

Résumé

ADAMTS (a disintegrin-like and metalloproteinase with thrombospondin) are a family of proteinases that are structurally similar to the family of matrix metalloproteinases with critical roles in damage and repair of the extracellular matrix. Their functions are closely related to inflammation, hypoxia, and vascularization. Our aim was to determine levels of ADAMTS-1 in gingival crevicular fluid (GCF) in patients with advanced periodontal diseases and identify their association with hypoxia-inducible factor-1alpha (HIF-1α), vascular endothelial growth factor (VEGF-A), and clinical parameters of periodontitis. The study consisted of three groups: healthy individuals (control; n = 20), generalized chronic periodontitis (CP; n = 21), and generalized aggressive periodontitis (GAgP; n = 20). Clinical parameters were measured. Levels of ADAMTS-1, VEGF-A, and HIF-1α in GCF and serum were quantified by enzyme-linked immunosorbent assay (ELISA) and reported as total amounts and concentration. ADAMTS-1 total amount in GCF were significantly higher in patients with CP and GAgP compared with healthy individuals (P < 0.05). HIF-1α total amount in GCF were also higher in periodontitis groups compared with the control group (P < 0.05). GCF total VEGF-A content was significantly higher in the GAgP group compared with the CP and the controls (respectively; P = 0.023, P = 0.003). There was a significant correlation between ADAMTS-1, VEGF-A, and HIF-1α levels in the GCF and clinical periodontal parameters (probing depth [PD], bleeding on probing [BOP], and clinical attachment loss (CAL); P < 0.05). ADAMTS-1 may play a role in advanced periodontal disease pathogenesis in correlation with tissue hypoxia and vascularization.

Sections du résumé

BACKGROUND
ADAMTS (a disintegrin-like and metalloproteinase with thrombospondin) are a family of proteinases that are structurally similar to the family of matrix metalloproteinases with critical roles in damage and repair of the extracellular matrix. Their functions are closely related to inflammation, hypoxia, and vascularization. Our aim was to determine levels of ADAMTS-1 in gingival crevicular fluid (GCF) in patients with advanced periodontal diseases and identify their association with hypoxia-inducible factor-1alpha (HIF-1α), vascular endothelial growth factor (VEGF-A), and clinical parameters of periodontitis.
METHODS
The study consisted of three groups: healthy individuals (control; n = 20), generalized chronic periodontitis (CP; n = 21), and generalized aggressive periodontitis (GAgP; n = 20). Clinical parameters were measured. Levels of ADAMTS-1, VEGF-A, and HIF-1α in GCF and serum were quantified by enzyme-linked immunosorbent assay (ELISA) and reported as total amounts and concentration.
RESULTS
ADAMTS-1 total amount in GCF were significantly higher in patients with CP and GAgP compared with healthy individuals (P < 0.05). HIF-1α total amount in GCF were also higher in periodontitis groups compared with the control group (P < 0.05). GCF total VEGF-A content was significantly higher in the GAgP group compared with the CP and the controls (respectively; P = 0.023, P = 0.003). There was a significant correlation between ADAMTS-1, VEGF-A, and HIF-1α levels in the GCF and clinical periodontal parameters (probing depth [PD], bleeding on probing [BOP], and clinical attachment loss (CAL); P < 0.05).
CONCLUSION
ADAMTS-1 may play a role in advanced periodontal disease pathogenesis in correlation with tissue hypoxia and vascularization.

Identifiants

pubmed: 31020669
doi: 10.1002/JPER.18-0195
doi:

Substances chimiques

Disintegrins 0
Hypoxia-Inducible Factor 1, alpha Subunit 0
Thrombospondin 1 0
Vascular Endothelial Growth Factor A 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

1182-1189

Informations de copyright

© 2019 American Academy of Periodontology.

Références

Demircan K, Akyol S, Armutçu F. A multi-functional gene family from arthritis to cancer: A disintegrin-like metalloproteinase with thrombospondin type-1 motif (ADAMTS). J Clin Anal Med. 2013;4:429-434.
Gao S, De Geyter C, Kossowska K, Zhang H. FSH stimulates the expression of the ADAMTS-16 protease in mature human ovarian follicles. Mol Hum Reprod. 2007;13:465-471.
Kuno K, Iizasa H, Ohno S, Matsushima K. The exon/intron organization and chromosomal mapping of the mouse ADAMTS-1 gene encoding an ADAM family protein with TSP motifs. Genomics. 1997;46:466-471.
Chen Y, Huang J, Tang C, et al. Small molecule therapeutics for inflammation-associated chronic musculoskeletal degenerative diseases: past, present and future. Exp Cell Res. 2017;359(1):1-9.
Höpfl G, Ogunshola O, Gassmann MG. HIFs and tumors-causes and consequences. Am J Physiol Regul Integr Comp Physiol. 2004;286(4):608-623.
Hatipoglu OF, Hirohata S, Cilek MZ, et al. ADAMTS1 is a unique hypoxi cearly response gene expressed by endothelial cells. J Biol Chem. 2009;284(24):16325-16333.
Ng YH, Zhu H, Pallen CJ, Leung PC, MacCalman CD. Differential effects of interleukin-1beta and transforming growth factor-beta1 on the expression of the inflammation-associated protein, ADAMTS-1, in human decidual stromal cells in vitro. Hum Reprod. 2006;21(8):1990-1999.
Bevitt DJ, Mohamed J, Catterall JB, et al. Expression of ADAMTS metalloproteinases in the retinal pigment epithelium derived cell line ARPE-19: transcriptional regulation by TNFalpha. Biochim Biophys Acta. 2003;1626(1-3):83-91.
Cross AK, Haddock G, Stock CJ, et al. ADAMTS-1 and -4 are up-regulated following transient middle cerebral artery occlusion in the rat and their expression is modulated by TNF in cultured astrocytes. Brain Res. 2006;1088(1):19-30.
Krampert M, Kuenzle S, Thai SN, Lee N, Iruela-Arispe ML, Werner S. ADAMTS1 proteinase is up-regulated in wounded skin and regulates migration of fibroblasts and endothelial cells. J Biol Chem. 2005;280(25):23844-23852.
Iruela-Arispe ML, Carpizo D, Luque A. ADAMTS1: a matrix metalloprotease with angio inhibitory properties. Ann N Y Acad Sci. 2003;995:183-190.
Luque A, Carpizo DR, Iruela-Arispe ML. ADAMTS1/METH1 inhibits endothelial cell proliferation by direct binding and sequestration of VEGF165. J Biol Chem. 2003;278:23656-23665.
Rodriguez-Manzaneque JC, Milchanowski AB, Dufour EK, Leduc R, Iruela-Arispe ML. Characterization of METH-1/ADAMTS1 processing reveals two distinct active forms. J Biol Chem. 2000;275(43):33471-33479.
Lee NV, Sato M, Annis DS, et al. ADAMTS1 mediates the release of antiangiogenic polypeptides from TSP1 and 2. EMBO J. 2006;25(22):5270-5283.
Dawson DW, Pearce SF, Zhong R, Silverstein RL, Frazier WA, Bouck NP. CD36 mediates the In vitro inhibitory effects of thrombospondin-1 on endothelial cells. J Cell Biol. 1997;138(3):707-717.
Cetinkaya BO, Keles GC, Ayas B, Sakallioglu EE, Acikgoz G. The expression of vascular endothelial growth factor in a rat model at destruction and healing stages of periodontal disease. J Periodontol. 2007;78:1129-1135.
Pradeep AR, Prapulla DV, Sharma A, Sujatha PB. Gingival crevicular fluid and serum vascular endothelial growth factor: their relationship in periodontal health, disease and after treatment. Cytokine. 2011;54:200-204.
Keles GC, Cetinkaya BO, Eroglu C, Simsek SB, Kahraman H. Vascular endothelial growth factor expression levels of gingiva in gingivitis and periodontitis patients with/without diabetes mellitus. Inflamm Res. 2010;59:543-549.
Van Dyke TE, Lester MA, Shapira L. The role of the host response in periodontal disease progression: implications for future treatment strategies. J Periodontol. 1993;64(8):792-806.
Page RC. The role of inflammatory mediators in the pathogenesis of periodontal disease. J Periodontal Res. 1991;26:230-242.
Prapulla DV, Sujatha PB, Pradeep AR. Gingival crevicular fluid VEGF levels in periodontal health and disease. J Periodontol. 2007;78:1783-1787.
Johnson RB, Serio FG, Dai X. Vascular endothelial growth factor and progression of periodontal disease. J Periodontol. 1998;70:848-852.
Ng KT, Li JP, Ng KM, Tipoe GL, Leung WK, Fung ML. Expressionof hypoxia-inducible factor-1α in human periodontal tissue. J Periodontol. 2011;82:136-141.
Li JP, Li FY, Xu A, et al. Lipopolysaccharide and hypoxia-Induced HIF-1 activation in human gingival fibroblasts. J Periodontol. 2012;83:816-824.
Schofield CJ, Ratcliffe PJ. Oxygen sensing by HIF hydroxylases. Nat Rev Mol Cell Biol. 2004;5:343-354.
Armitage GC. Development of a classification system for periodontal diseases and conditions. Ann Periodontol. 1999;4:1-6.
Alpagot T, Wolff LF, Smith QT, Tran SD. Risk indicators for periodontal disease in a racially diverse urban population. J Clin Periodontol. 1996;23(11):982-988.
Koromantzos PA, Makrilakis K, Dereka X, et al. Effect of non-surgical periodontal therapy on C reactive protein, oxidative stress, and Matrix Metalloproteinase (MMP)-9 and MMP-2 levels in patients with type 2 diabetes: A randomized controlled study. J Periodontol. 2012;83(1):3-10.
Loe H, Holm-Pedersen P. Absence and presence of fluid from normal and inflamed gingivae. Periodontics. 1965;3:171-177.
Kurgan Ş, Fentoğlu Ö, Önder C, Serdar M, et al. The effects of periodontal therapy on gingival crevicular fluid matrix metalloproteinase-8, interleukin-6 and prostaglandin-E2 levels in patients with rheumatoid arthritis. J Periodontal Res. 2016;51:586-595.
Chapple IL, Matthews JB, Thorpe GHG, Glenwright HD, Smith JM, Saxby M. A new ultrasensitive chemiluminescent assay for the site-specific quantification of alkaline phosphatase in gingival crevicular fluid. J Periodontal Res. 1993;28(4):266-273.
Lin SJ, Chen YL, Kuo MY, Li CL, Lu HK. Measurement of gp130 cytokines oncostatin M and IL-6 in gingival crevicular fluid of patients with chronic periodontitis. Cytokine. 2005;30(4):160-167.
Lamster IB, Oshrain RL, Fiorello LA, Celenti RS, Gordon JM. A comparison of 4 methods of data presentation for lysosomal enzyme activity in gingival crevicular fluid. J Clin Periodontol. 1988;15(6):347-352.
Wågsäter D, Björk H, Zhu C, et al. ADAMTS-4 and -8 are inflammatory regulated enzymes expressed in macrophage-rich areas of human atherosclerotic plaques. Atherosclerosis. 2008;196:514-522.
Jonsson-Rylander AC, Nilsson T, Fritsche-Danielson R, Hammarstrom A, Behrendt M, Andersson JO, et al. Role of ADAMTS-1 in atherosclerosis: remodeling of carotid artery, immunohistochemistry, and proteolysis of versican. Arterioscler Thromb Vasc Biol. 2005;25:180-185.
Kuno K, Kanada N, Nakashima E, Fujiki F, Ichimura F, Matsushima K. Molecular cloning of a gene encoding a new type of metalloproteinase-disintegrin family protein with thrombospondin motifs as an inflammation associated gene. J Biol Chem. 1997;272:556-562.
Oveland E, Karlsen TV, Haslene-Hox H, et al. Proteomic evaluation of inflammatory proteins in rat spleen interstitial fluid and lymph during LPS-induced systemic inflammation reveals increased levels of ADAMST1. J Proteome Res. 2012;11(11):5338-5349.
Rapraeger AC. Syndecan-regulated receptor signaling. J Cell Biol. 2000;149(5):995-998.
Dvorak HF, Brown LF, Detmar M, Dvorak AM. Vascular permeability factor/vascular endothelial growth factor, microvascular hyperpermeability, and angiogenesis. Am J Pathol. 1995;146:1029-1039.
Booth V, Young S, Cruchley A, Taichman NS, Paleolog E. Vascular endothelial growth factor in human periodontal disease. J Periodontal Res. 1998 Nov;33(8):491-499.
Önder C, Kurgan Ş, Balci N, et al. Vascular Endothelial Growth Factor Levels (VEGF) in gingival biopsies of patients with chronic or aggressive periodontitis. Ponte. 2016;72(7). https://10.21506/j.ponte.2016.7.19
Ben-Av P, Crofford LJ, Wilder RL, Hla T. Induction of vascular endothelial growth factor expression in synovial fibroblasts by prostaglandin E and interleukin-1: a potential mechanism for inflammatory angiogenesis. FEBS Lett. 1995;372(1):83-87.
Booth V, Young S, Cruchley A, Taichman NS, Paleolog E. Vascular endothelial growth factor in human periodontal disease. J Periodontal Res. 1998;33(8):491-499.
Gölz L, Memmert S, Rath-Deschner B, et al. LPS from P. gingivalis and hypoxia increases oxidative stress in periodontal ligament fibroblasts and contributes to periodontitis. Mediators Inflamm. 2014;2014:986264. https://0.1155/2014/986264
Frede S, Freitag P, Otto T, Heilmaier C, Fandrey J. The proinflammatory cytokine interleukin 1beta and hypoxia cooperatively induce the expression of adrenomedullin in ovarian carcinoma cells through hypoxia inducible factor 1 activation. Cancer Res. 2005;65(11):4690-4697.
Frede S, Stockmann C, Freitag P, Fandrey J. Bacterial lipopolysaccharide induces HIF-1 activation in human monocytes via p44/42 MAPK and NF-kappaB. Biochem J. 2006;396(3):517-527.
Bonello S, Zähringer C, BelAiba RS, et al. Reactive oxygen species activate the HIF-1alpha promoter via a functional NF-kappaB site. Arterioscler Thromb Vasc Biol. 2007;27(4):755-761.
Imtiyaz HZ, Simon MC. Hypoxia-inducible factors as essential regulators of inflammation. Curr Top Microbiol Immunol. 2010;345:105-120.
Albina JE, Mastrofrancesco B, Vessella JA, Louis CA, Henry WL, Jr, Reichner JS. HIF-1 expression in healing wounds: hIF-1alpha induction in primary inflammatory cells by TNF-alpha. Am J Physiol Cell Physiol. 2001;281(6):1971-1977.
Peng J, Gong L, Si K, Bai X, Du G. Fluorescence resonance energy transfer assay for high-throughput screening of ADAMTS1 inhibitors. Molecules. 2011;16(12):10709-10721.

Auteurs

Mahmure Ayşe Tayman (MA)

Department of Periodontology, Faculty of Dentistry, Ankara University, Ankara, Turkey.

Şivge Kurgan (Ş)

Department of Periodontology, Faculty of Dentistry, Ankara University, Ankara, Turkey.

Canan Önder (C)

Department of Periodontology, Faculty of Dentistry, Ankara University, Ankara, Turkey.

Zeliha Güney (Z)

Department of Periodontology, Faculty of Dentistry, Ankara University, Ankara, Turkey.

Muhittin A Serdar (MA)

Department of Medical Biochemistry, School of Medicine, Acibadem University, Ankara, Turkey.

Alpdoğan Kantarcı (A)

Forsyth Institute, Department of Applied Oral Sciences, Center for Periodontology, Cambridge, MA, USA.

Meral Günhan (M)

Department of Periodontology, Faculty of Dentistry, Ankara University, Ankara, Turkey.

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