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Combinatorial Chemistry & High Throughput Screening

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ISSN (Print): 1386-2073
ISSN (Online): 1875-5402

Research Article

Expression Levels of A Disintegrin-like Metalloproteinase with Thrombospondin Motifs-4 and -5 (ADAMTS-4 and ADAMTS-5) in Inflamed and Healthy Gingival Tissues

Author(s): Mahmure A. Tayman*, İsmail Koyuncu and Nimet Ö. Köklü

Volume 23, Issue 2, 2020

Page: [168 - 176] Pages: 9

DOI: 10.2174/1386207323666200218113000

Price: $65

Abstract

Background: ADAMTS (A disintegrin-like metalloproteinase with thrombospondin motifs) is a group of 19 zinc-dependent metalloproteases known to function in many pathological and physiological processes, such as adhesion, cell fusion, signaling, proteolysis and ECM degradation.

Objectives: The aim of this study was to demonstrate the levels of ADAMTS-4 and -5 in gingival tissues with Stage III-Grade B generalized periodontitis (SIII-GB), Stage III-Grade C generalized periodontitis (SIII-GC) and healthy-control (C) groups.

Methods: The clinical measurements were recorded for each patient. A total of 63 gingival biopsy specimens were obtained from the C (n:20), SIII-GB (n:23) and SIII-GC (n:20) groups. Polymerase chain reaction (Rt-PCR) and immunohistochemical (IHC) examinations were used to determine gene and protein levels.

Results: According to the results of all methods, ADAMTS-4 and -5 expressions existed in periodontitis and C groups (P> 0.05). Immunostaining for ADAMTS-4 was found to be higher in patients with periodontitis than for ADAMTS-5 (P>0.05). Gene expression levels for ADAMTS-4 and -5 seemed to be up-regulated in subjects diagnosed with periodontitis, but the results were not statistically significant (P>0.05). A positive correlation was observed between PPD and ADAMTS-4 mRNA in SIII-GC (p=0.035) and SIII-GB (p=0.015). A positive correlation was determined between ADAMTS-4 mRNA and ADAMTS-5 mRNA in SIII-GC (p=0.037) and SIII-GB (p=0.00).

Conclusion: ADAMTS expression may take part in both pathological and physiological processes in the periodontal tissues, and periodontal destruction may be the result of a complex interaction of several pathways with many participants, such as ADAMTS-4 and -5, thus facilitating the exaggeration of periodontal disease.

Keywords: Matrix metalloproteinase, ADAMTS-4, ADAMTS-5, periodontal disease, inflammation, generalized periodontitis.

[1]
Armitage, G.C. Development of a classification system for periodontal diseases and conditions. Ann. Periodontol., 1999, 4(1), 1-6.
[http://dx.doi.org/10.1902/annals.1999.4.1.1] [PMID: 10863370]
[2]
Sorsa, T.; Tjäderhane, L.; Konttinen, Y.T.; Lauhio, A.; Salo, T.; Lee, H.M.; Golub, L.M.; Brown, D.L.; Mäntylä, P. Matrix metalloproteinases: contribution to pathogenesis, diagnosis and treatment of periodontal inflammation. Ann. Med., 2006, 38(5), 306-321.
[http://dx.doi.org/10.1080/07853890600800103] [PMID: 16938801]
[3]
Porter, S.; Clark, I.M.; Kevorkian, L.; Edwards, D.R. The ADAMTS metalloproteinases. Biochem. J., 2005, 386(Pt 1), 15-27.
[http://dx.doi.org/10.1042/BJ20040424] [PMID: 15554875]
[4]
Kelwick, R.; Desanlis, I.; Wheeler, G.N.; Edwards, D.R. The ADAMTS (A Disintegrin and Metalloproteinase with Thrombospondin motifs) family. Genome Biol., 2015, 16, 113.
[http://dx.doi.org/10.1186/s13059-015-0676-3] [PMID: 26025392]
[5]
Tortorella, M.D.; Burn, T.C.; Pratta, M.A.; Abbaszade, I.; Hollis, J.M.; Liu, R.; Rosenfeld, S.A.; Copeland, R.A.; Decicco, C.P.; Wynn, R.; Rockwell, A.; Yang, F.; Duke, J.L.; Solomon, K.; George, H.; Bruckner, R.; Nagase, H.; Itoh, Y.; Ellis, D.M.; Ross, H.; Wiswall, B.H.; Murphy, K.; Hillman, M.C., Jr; Hollis, G.F.; Newton, R.C.; Magolda, R.L.; Trzaskos, J.M.; Arner, E.C. Purification and cloning of aggrecanase-1: a member of the ADAMTS family of proteins. Science, 1999, 284(5420), 1664-1666.
[http://dx.doi.org/10.1126/science.284.5420.1664] [PMID: 10356395]
[6]
Bostanci, N.; Emingil, G.; Afacan, B.; Han, B.; Ilgenli, T.; Atilla, G.; Hughes, F.J.; Belibasakis, G.N. Tumor necrosis factor-alpha-converting enzyme (TACE) levels in periodontal diseases. J. Dent. Res., 2008, 87(3), 273-277.
[http://dx.doi.org/10.1177/154405910808700311] [PMID: 18296613]
[7]
Khongkhunthian, S.; Techasatian, P.; Supanchart, C.; Bandhaya, P.; Montreekachon, P.; Thawanaphong, S.; Krisanaprakornkit, S. Elevated levels of a disintegrin and metalloproteinase 8 in gingival crevicular fluid of patients with periodontal diseases. J. Periodontol., 2013, 84(4), 520-528.
[http://dx.doi.org/10.1902/jop.2012.120262] [PMID: 22612366]
[8]
Nimcharoen, T.; Aung, W.P.P.; Makeudom, A.; Sastraruji, T.; Khongkhunthian, S.; Sirinirund, B.; Krisanaprakornkit, S.; Montreekachon, P. Reduced ADAM8 levels upon non-surgical periodontal therapy in patients with chronic periodontitis. Arch. Oral Biol., 2019, 97, 137-143.
[http://dx.doi.org/10.1016/j.archoralbio.2018.10.021] [PMID: 30384155 ]
[9]
Aung, W.P.P.; Chotjumlong, P.; Pata, S.; Montreekachon, P.; Supanchart, C.; Khongkhunthian, S.; Sastraruji, T.; Krisanaprakornkit, S. Inducible expression of A Disintegrin and Metalloproteinase 8 in chronic periodontitis and gingival epithelial cells. J. Periodontal Res., 2017, 52(3), 582-593.
[http://dx.doi.org/10.1111/jre.12426] [PMID: 27859260]
[10]
Tayman, M.A.; Kurgan, Ş.; Önder, C.; Güney, Z.; Serdar, M.A.; Kantarcı, A.; Günhan, M. 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. J. Periodontol., 2019, 90(10), 1182-1189.
[http://dx.doi.org/10.1002/JPER.18-0195] [PMID: 31020669]
[11]
Pockert, A.J.; Richardson, S.M.; Le Maitre, C.L.; Lyon, M.; Deakin, J.A.; Buttle, D.J.; Freemont, A.J.; Hoyland, J.A. Modified expression of the ADAMTS enzymes and tissue inhibitor of metalloproteinases 3 during human intervertebral disc degeneration. Arthritis Rheum., 2009, 60(2), 482-491.
[http://dx.doi.org/10.1002/art.24291] [PMID: 19180493]
[12]
Mwale, F.; Masuda, K.; Pichika, R.; Epure, L.M.; Yoshikawa, T.; Hemmad, A.; Roughley, P.J.; Antoniou, J. The efficacy of Link N as a mediator of repair in a rabbit model of intervertebral disc degeneration. Arthritis Res. Ther., 2011, 13(4), R120.
[http://dx.doi.org/10.1186/ar3423] [PMID: 21787415]
[13]
Wang, J.; Markova, D.; Anderson, D.G.; Zheng, Z.; Shapiro, I.M.; Risbud, M.V. TNF-α and IL-1β promote a disintegrin-like and metalloprotease with thrombospondin type I motif-5-mediated aggrecan degradation through syndecan-4 in intervertebral disc. J. Biol. Chem., 2011, 286(46), 39738-39749.
[http://dx.doi.org/10.1074/jbc.M111.264549] [PMID: 21949132]
[14]
Troeberg, L.; Nagase, H. Proteases involved in cartilage matrix degradation in osteoarthritis. Biochim. Biophys. Acta, 2012, 1824(1), 133-145.
[http://dx.doi.org/10.1016/j.bbapap.2011.06.020] [PMID: 21777704]
[15]
Chen, X.; Zhang, C.; Wang, X.; Huo, S. Juglanin inhibits IL-1β-induced inflammation in human chondrocytes. Artif. Cells Nanomed. Biotechnol., 2019, 47(1), 3614-3620.
[http://dx.doi.org/10.1080/21691401.2019.1657877] [PMID: 31468982]
[16]
Demircan, K.; Yonezawa, T.; Takigawa, T.; Topcu, V.; Erdogan, S.; Ucar, F.; Armutcu, F.; Yigitoglu, M.R.; Ninomiya, Y.; Hirohata, S. ADAMTS1, ADAMTS5, ADAMTS9 and aggrecanase-generated proteoglycan fragments are induced following spinal cord injury in mouse. Neurosci. Lett., 2013, 544, 25-30.
[http://dx.doi.org/10.1016/j.neulet.2013.02.064] [PMID: 23562508]
[17]
Ashlin, T.G.; Kwan, A.P.; Ramji, D.P. Regulation of ADAMTS-1, -4 and -5 expression in human macrophages: differential regulation by key cytokines implicated in atherosclerosis and novel synergism between TL1A and IL-17. Cytokine, 2013, 64(1), 234-242.
[http://dx.doi.org/10.1016/j.cyto.2013.06.315] [PMID: 23859810]
[18]
Wågsäter, D.; Björk, H.; Zhu, C.; Björkegren, J.; Valen, G.; Hamsten, A.; Eriksson, P. ADAMTS-4 and -8 are inflammatory regulated enzymes expressed in macrophage-rich areas of human atherosclerotic plaques. Atherosclerosis, 2008, 196(2), 514-522.
[http://dx.doi.org/10.1016/j.atherosclerosis.2007.05.018] [PMID: 17606262]
[19]
Melekoglu, R.; Ciftci, O.; Celik, E.; Yilmaz, E.; Bastemur, A.G. Evaluation of second trimester amniotic fluid ADAMTS4, ADAMTS5, interleukin-6 and tumor necrosis factor-α levels in patients with gestational diabetes mellitus. J. Obstet. Gynaecol. Res., 2019, 45(4), 824-829.
[http://dx.doi.org/10.1111/jog.13914] [PMID: 30623540]
[20]
Song, R.H.; Tortorella, M.D.; Malfait, A.M.; Alston, J.T.; Yang, Z.; Arner, E.C.; Griggs, D.W. Aggrecan degradation in human articular cartilage explants is mediated by both ADAMTS-4 and ADAMTS-5. Arthritis Rheum., 2007, 56(2), 575-585.
[http://dx.doi.org/10.1002/art.22334] [PMID: 17265492]
[21]
Stanton, H.; Rogerson, F.M.; East, C.J.; Golub, S.B.; Lawlor, K.E.; Meeker, C.T.; Little, C.B.; Last, K.; Farmer, P.J.; Campbell, I.K.; Fourie, A.M.; Fosang, A.J. ADAMTS5 is the major aggrecanase in mouse cartilage in vivo and in vitro. Nature, 2005, 434(7033), 648-652.
[http://dx.doi.org/10.1038/nature03417] [PMID: 15800625]
[22]
East, C.J.; Stanton, H.; Golub, S.B.; Rogerson, F.M.; Fosang, A.J. ADAMTS-5 deficiency does not block aggrecanolysis at preferred cleavage sites in the chondroitin sulfate-rich region of aggrecan. J. Biol. Chem., 2007, 282(12), 8632-8640.
[http://dx.doi.org/10.1074/jbc.M605750200] [PMID: 17255106]
[23]
Ilic, M.Z.; East, C.J.; Rogerson, F.M.; Fosang, A.J.; Handley, C.J. Distinguishing aggrecan loss from aggrecan proteolysis in ADAMTS-4 and ADAMTS-5 single and double deficient mice. J. Biol. Chem., 2007, 282(52), 37420-37428.
[http://dx.doi.org/10.1074/jbc.M703184200] [PMID: 17938173]
[24]
Velasco, J.; Li, J.; DiPietro, L.; Stepp, M.A.; Sandy, J.D.; Plaas, A. Adamts5 deletion blocks murine dermal repair through CD44-mediated aggrecan accumulation and modulation of transforming growth factor β1 (TGFβ1) signaling. J. Biol. Chem., 2011, 286(29), 26016-26027.
[http://dx.doi.org/10.1074/jbc.M110.208694] [PMID: 21566131]
[25]
Dupuis, L.E.; Nelson, E.L.; Hozik, B.; Porto, S.C.; Rogers-DeCotes, A.; Fosang, A.; Kern, C.B. Adamts5-/- mice exhibit altered aggrecan proteolytic profiles that correlate with ascending aortic anomalies. Arterioscler. Thromb. Vasc. Biol., 2019, 39(10), 2067-2081.
[http://dx.doi.org/10.1161/ATVBAHA.119.313077] [PMID: 31366218]
[26]
Tonetti, M.S.; Greenwell, H.; Kornman, K.S. Staging and grading of periodontitis: Framework and proposal of a new classification and case definition. J. Periodontol., 2018, 89(Suppl. 1), S159-S172.
[http://dx.doi.org/10.1002/JPER.18-0006] [PMID: 29926952]
[27]
Uysal, S.; Ünal, Z.N.; Erdoğan, S.; Akyol, S.; Ramazan Yiğitoğlu, M.; Hirohata, S.; Işık, B.; Demircan, K. Augmentation of ADAMTS9 gene expression by IL-1β is reversed by NFκB and MAPK inhibitors, but not PI3 kinase inhibitors. Cell Biochem. Funct., 2013, 31(7), 539-544.
[PMID: 23175174 ]
[28]
Laurie, C.C.; Doheny, K.F.; Mirel, D.B.; Pugh, E.W.; Bierut, L.J.; Bhangale, T.; Boehm, F.; Caporaso, N.E.; Cornelis, M.C.; Edenberg, H.J.; Gabriel, S.B.; Harris, E.L.; Hu, F.B.; Jacobs, K.B.; Kraft, P.; Landi, M.T.; Lumley, T.; Manolio, T.A.; McHugh, C.; Painter, I.; Paschall, J.; Rice, J.P.; Rice, K.M.; Zheng, X.; Weir, B.S. Quality control and quality assurance in genotypic data for genome-wide association studies. Genet. Epidemiol., 2010, 34(6), 591-602.
[http://dx.doi.org/10.1002/gepi.20516] [PMID: 20718045]
[29]
Bartold, P.M.; Narayanan, A.S. Molecular and cell biology of healthy and diseased periodontal tissues. Periodontol. 2000, 2006, 40(40), 29-49.
[http://dx.doi.org/10.1111/j.1600-0757.2005.00140.x] [PMID: 16398684]
[30]
Sorsa, T.; Tjäderhane, L.; Salo, T. Matrix metalloproteinases (MMPs) in oral diseases. Oral Dis., 2004, 10(6), 311-318.
[http://dx.doi.org/10.1111/j.1601-0825.2004.01038.x] [PMID: 15533204]
[31]
McCawley, L.J.; Matrisian, L.M. Matrix metalloproteinases: they’re not just for matrix anymore! Curr. Opin. Cell Biol., 2001, 13(5), 534-540.
[http://dx.doi.org/10.1016/S0955-0674(00)00248-9] [PMID: 11544020]
[32]
Page, R.C. The role of inflammatory mediators in the pathogenesis of periodontal disease. J. Periodontal Res., 1991, 26(3 Pt 2), 230-242.
[http://dx.doi.org/10.1111/j.1600-0765.1991.tb01649.x] [PMID: 1679130]
[33]
Glowacki, A.J.; Gottardi, R.; Yoshizawa, S.; Cavalla, F.; Garlet, G.P.; Sfeir, C.; Little, S.R. Strategies to direct the enrichment, expansion, and recruitment of regulatory cells for the treatment of disease. Ann. Biomed. Eng., 2015, 43(3), 593-602.
[http://dx.doi.org/10.1007/s10439-014-1125-2] [PMID: 25245220]
[34]
Koshy, P.J.; Lundy, C.J.; Rowan, A.D.; Porter, S.; Edwards, D.R.; Hogan, A.; Clark, I.M.; Cawston, T.E. The modulation of matrix metalloproteinase and ADAM gene expression in human chondrocytes by interleukin-1 and oncostatin M: a time-course study using real-time quantitative reverse transcription-polymerase chain reaction. Arthritis Rheum., 2002, 46(4), 961-967.
[http://dx.doi.org/10.1002/art.10212] [PMID: 11953973]
[35]
Lazăr, L.; Loghin, A.; Bud, E.S.; Cerghizan, D.; Horváth, E.; Nagy, E.E. Cyclooxygenase-2 and matrix metalloproteinase-9 expressions correlate with tissue inflammation degree in periodontal disease. Rom. J. Morphol. Embryol., 2015, 56(4), 1441-1446.
[PMID: 26743292]
[36]
van der Zee, E.; Everts, V.; Beertsen, W. Cytokines modulate routes of collagen breakdown. Review with special emphasis on mechanisms of collagen degradation in the periodontium and the burst hypothesis of periodontal disease progression. J. Clin. Periodontol., 1997, 24(5), 297-305.
[http://dx.doi.org/10.1111/j.1600-051X.1997.tb00761.x] [PMID: 9178108]
[37]
Le Maitre, C.L.; Freemont, A.J.; Hoyland, J.A. The role of interleukin-1 in the pathogenesis of human intervertebral disc degeneration. Arthritis Res. Ther., 2005, 7(4), R732-R745.
[http://dx.doi.org/10.1186/ar1732] [PMID: 15987475 ]
[38]
Lee, S.; Moon, C.S.; Sul, D.; Lee, J.; Bae, M.; Hong, Y.; Lee, M.; Choi, S.; Derby, R.; Kim, B.J.; Kim, J.; Yoon, J.S.; Wolfer, L.; Kim, J.; Wang, J.; Hwang, S.W.; Lee, S.H. Comparison of growth factor and cytokine expression in patients with degenerated disc disease and herniated nucleus pulposus. Clin. Biochem., 2009, 42(15), 1504-1511.
[http://dx.doi.org/10.1016/j.clinbiochem.2009.06.017] [PMID: 19563795]
[39]
Setton, L.A.; Chen, J. Mechanobiology of the intervertebral disc and relevance to disc degeneration. J. Bone Joint Surg. Am., 2006, 88(Suppl. 2), 52-57.
[PMID: 16595444]
[40]
Millward-Sadler, S.J.; Costello, P.W.; Freemont, A.J.; Hoyland, J.A. Regulation of catabolic gene expression in normal and degenerate human intervertebral disc cells: implications for the pathogenesis of intervertebral disc degeneration. Arthritis Res. Ther., 2009, 11(3), R65.
[http://dx.doi.org/10.1186/ar2693] [PMID: 19435506]
[41]
Tian, Y.; Yuan, W.; Fujita, N.; Wang, J.; Wang, H.; Shapiro, I.M.; Risbud, M.V. Inflammatory cytokines associated with degenerative disc disease control aggrecanase-1 (ADAMTS-4) expression in nucleus pulposus cells through MAPK and NF-κB. Am. J. Pathol., 2013, 182(6), 2310-2321.
[http://dx.doi.org/10.1016/j.ajpath.2013.02.037] [PMID: 23602832 ]
[42]
Didangelos, A.; Mayr, U.; Monaco, C.; Mayr, M. Novel role of ADAMTS-5 protein in proteoglycan turnover and lipoprotein retention in atherosclerosis. J. Biol. Chem., 2012, 287(23), 19341-19345.
[http://dx.doi.org/10.1074/jbc.C112.350785] [PMID: 22493487]
[43]
Birkedal-Hansen, H. Role of matrix metalloproteinases in human periodontal diseases. J. Periodontol., 1993, 64, 474-484.
[44]
Teumer, A.; Holtfreter, B.; Völker, U.; Petersmann, A.; Nauck, M.; Biffar, R.; Völzke, H.; Kroemer, H.K.; Meisel, P.; Homuth, G.; Kocher, T. Genome-wide association study of chronic periodontitis in a general German population. J. Clin. Periodontol., 2013, 40(11), 977-985.
[http://dx.doi.org/10.1111/jcpe.12154] [PMID: 24024966]
[45]
Divaris, K.; Monda, K.L.; North, K.E.; Olshan, A.F.; Reynolds, L.M.; Hsueh, W.C.; Lange, E.M.; Moss, K.; Barros, S.P.; Weyant, R.J.; Liu, Y.; Newman, A.B.; Beck, J.D.; Offenbacher, S. Exploring the genetic basis of chronic periodontitis: a genome-wide association study. Hum. Mol. Genet., 2013, 22(11), 2312-2324.
[http://dx.doi.org/10.1093/hmg/ddt065] [PMID: 23459936]
[46]
Divaris, K.; Monda, K.L.; North, K.E.; Olshan, A.F.; Reynolds, L.M.; Hsueh, W.C.; Lange, E.M.; Moss, K.; Barros, S.P.; Weyant, R.J.; Liu, Y.; Newman, A.B.; Beck, J.D.; Offenbacher, S. Exploring the genetic basis of chronic periodontitis: A genomewide association study. Hum. Mol. Genet., 2013, 22, 2312-2324.
[http://dx.doi.org/10.1093/hmg/ddt065] [PMID: 23459936]

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