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Treponema denticola increases MMP‐2 expression and activation in the periodontium via reversible DNA and histone modifications

dc.contributor.authorAteia, Islam M.
dc.contributor.authorSutthiboonyapan, Pimchanok
dc.contributor.authorKamarajan, Pachiyappan
dc.contributor.authorJin, Taocong
dc.contributor.authorGodovikova, Valentina
dc.contributor.authorKapila, Yvonne L.
dc.contributor.authorFenno, J. Christopher
dc.date.accessioned2018-04-04T18:51:17Z
dc.date.available2019-05-13T14:45:26Zen
dc.date.issued2018-04
dc.identifier.citationAteia, Islam M.; Sutthiboonyapan, Pimchanok; Kamarajan, Pachiyappan; Jin, Taocong; Godovikova, Valentina; Kapila, Yvonne L.; Fenno, J. Christopher (2018). "Treponema denticola increases MMP‐2 expression and activation in the periodontium via reversible DNA and histone modifications." Cellular Microbiology 20(4): n/a-n/a.
dc.identifier.issn1462-5814
dc.identifier.issn1462-5822
dc.identifier.urihttps://hdl.handle.net/2027.42/142926
dc.description.abstractHost‐derived matrix metalloproteinases (MMPs) and bacterial proteases mediate destruction of extracellular matrices and supporting alveolar bone in periodontitis. The Treponema denticola dentilisin protease induces MMP‐2 expression and activation in periodontal ligament (PDL) cells, and dentilisin‐mediated activation of pro‐MMP‐2 is required for cellular fibronectin degradation. Here, we report that T. denticola regulates MMP‐2 expression through epigenetic modifications in the periodontium. PDL cells were treated with epigenetic enzyme inhibitors before or after T. denticola challenge. Fibronectin fragmentation, MMP‐2 expression, and activation were assessed by immunoblot, zymography, and qRT‐PCR, respectively. Chromatin modification enzyme expression in T. denticola‐challenged PDL cells and periodontal tissues were evaluated using gene arrays. Several classes of epigenetic enzymes showed significant alterations in transcription in diseased tissue and T. denticola‐challenged PDL cells. T. denticola‐mediated MMP‐2 expression and activation were significantly reduced in PDL cells treated with inhibitors of aurora kinases and histone deacetylases. In contrast, DNA methyltransferase inhibitors had little effect, and inhibitors of histone acetyltransferases, methyltransferases, and demethylases exacerbated T. denticola‐mediated MMP‐2 expression and activation. Chronic epigenetic changes in periodontal tissues mediated by T. denticola or other oral microbes may contribute to the limited success of conventional treatment of chronic periodontitis and may be amenable to therapeutic reversal.
dc.publisherWiley Periodicals, Inc.
dc.titleTreponema denticola increases MMP‐2 expression and activation in the periodontium via reversible DNA and histone modifications
dc.typeArticleen_US
dc.rights.robotsIndexNoFollow
dc.subject.hlbsecondlevelMolecular, Cellular and Developmental Biology
dc.subject.hlbtoplevelHealth Sciences
dc.description.peerreviewedPeer Reviewed
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/142926/1/cmi12815.pdf
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/142926/2/cmi12815_am.pdf
dc.identifier.doi10.1111/cmi.12815
dc.identifier.sourceCellular Microbiology
dc.identifier.citedreferenceOffenbacher, S., Barros, S. P., & Beck, J. D. ( 2008 ). Rethinking periodontal inflammation. Journal of Periodontology, 79, 1577 – 1584.
dc.identifier.citedreferenceSimonson, L. G., Goodman, C. H., Bial, J. J., & Morton, H. E. ( 1988 ). Quantitative relationship of Treponema denticola to severity of periodontal disease. Infection and Immunity, 56, 726 – 728.
dc.identifier.citedreferenceSitholimela, C. S., & Shangase, L. S. ( 2013 ). The association between periodontitis and pre‐term birth and/or low birth weight: A literature review. SADJ, 68, 162 – 166.
dc.identifier.citedreferenceSocransky, S. S., Haffajee, A. D., Cugini, M. A., Smith, C., & Kent, R. L. Jr. ( 1998 ). Microbial complexes in subgingival plaque. Journal of Clinical Periodontology, 25, 134 – 144.
dc.identifier.citedreferenceSong, S. E., Choi, B. K., Kim, S. N., Yoo, Y. J., Kim, M. M., Park, S. K., … Kim, C. K. ( 2003 ). Inhibitory effect of procyanidin oligomer from elm cortex on the matrix metalloproteinases and proteases of periodontopathogens. Journal of Periodontal Research, 38, 282 – 289.
dc.identifier.citedreferenceStewart, R., & West, M. ( 2016 ). Increasing evidence for an association between periodontitis and cardiovascular disease. Circulation, 133, 549 – 551.
dc.identifier.citedreferenceStrongin, A. Y., Collier, I., Bannikov, G., Marmer, B. L., Grant, G. A., & Goldberg, G. I. ( 1995 ). Mechanism of cell surface activation of 72‐kDa type IV collagenase. Isolation of the activated form of the membrane metalloprotease. The Journal of Biological Chemistry, 270, 5331 – 5338.
dc.identifier.citedreferenceTafolla, E., Wang, S., Wong, B., Leong, J., & Kapila, Y. L. ( 2005 ). JNK1 and JNK2 oppositely regulate p53 in signaling linked to apoptosis triggered by an altered fibronectin matrix: JNK links FAK and p53. The Journal of Biological Chemistry, 280, 19992 – 19999.
dc.identifier.citedreferenceTalbert, P. B., & Henikoff, S. ( 2006 ). Spreading of silent chromatin: Inaction at a distance. Nature Reviews. Genetics, 7, 793 – 803.
dc.identifier.citedreferenceTanaka, K., Iwasaki, K., Feghali, K. E., Komaki, M., Ishikawa, I., & Izumi, Y. ( 2011 ). Comparison of characteristics of periodontal ligament cells obtained from outgrowth and enzyme‐digested culture methods. Archives of Oral Biology, 56, 380 – 388.
dc.identifier.citedreferenceUitto, V. J., Grenier, D., Chan, E. C., & McBride, B. C. ( 1988 ). Isolation of a chymotrypsinlike enzyme from Treponema denticola. Infection and Immunity, 56, 2717 – 2722.
dc.identifier.citedreferenceVeeraraghavan, J., Natarajan, M., Lagisetty, P., Awasthi, V., Herman, T. S., & Aravindan, N. ( 2011 ). Impact of curcumin, raspberry extract, and neem leaf extract on rel protein‐regulated cell death/radiosensitization in pancreatic cancer cells. Pancreas, 40, 1107 – 1119.
dc.identifier.citedreferenceWaddington, C. H. ( 2012 ). The epigenotype. 1942. International Journal of Epidemiology, 41, 10 – 13.
dc.identifier.citedreferenceWang, F., Qi, Y., Li, X., He, W., Fan, Q. X., & Zong, H. ( 2013 ). HDAC inhibitor trichostatin A suppresses esophageal squamous cell carcinoma metastasis through HADC2 reduced MMP‐2/9. Clinical and Investigative Medicine, 36, E87 – E94.
dc.identifier.citedreferenceWilliams, R. C., Barnett, A. H., Claffey, N., Davis, M., Gadsby, R., Kellett, M., … Thackray, S. ( 2008 ). The potential impact of periodontal disease on general health: A consensus view. Current Medical Research and Opinion, 24, 1635 – 1643.
dc.identifier.citedreferenceYin, L., & Chung, W. O. ( 2011 ). Epigenetic regulation of human beta‐defensin 2 and CC chemokine ligand 20 expression in gingival epithelial cells in response to oral bacteria. Mucosal Immunology, 4, 409 – 419.
dc.identifier.citedreferenceYoshida, A., Kawada, M., Suzuki, N., Nakano, Y., Oho, T., Saito, T., & Yamashita, Y. ( 2004 ). TaqMan real‐time polymerase chain reaction assay for the correlation of Treponema denticola numbers with the severity of periodontal disease. Oral Microbiology and Immunology, 19, 196 – 200.
dc.identifier.citedreferenceZhang, M., Xiao, X. Q., Jiang, Y. F., Liang, Y. S., Peng, M. Y., Xu, Y., & Gong, G. Z. ( 2011 ). DNA demethylation in PD‐1 gene promoter induced by 5‐azacytidine activates PD‐1 expression on Molt‐4 cells. Cellular Immunology, 271, 450 – 454.
dc.identifier.citedreferenceZhang, S., Barros, S. P., Niculescu, M. D., Moretti, A. J., Preisser, J. S., & Offenbacher, S. ( 2010 ). Alteration of PTGS2 promoter methylation in chronic periodontitis. Journal of Dental Research, 89, 133 – 137.
dc.identifier.citedreferenceZhang, Y., & Reinberg, D. ( 2001 ). Transcription regulation by histone methylation: Interplay between different covalent modifications of the core histone tails. Genes & Development, 15, 2343 – 2360.
dc.identifier.citedreferenceZucker, S., Pei, D., Cao, J., & Lopez‐Otin, C. ( 2003 ). Membrane type‐matrix metalloproteinases (MT‐MMP). Current Topics in Developmental Biology, 54, 1 – 74.
dc.identifier.citedreferenceAbdel Aziz, M. T., El‐Asmar, M. F., El‐Ibrashy, I. N., Rezq, A. M., Al‐Malki, A. L., Wassef, M. A., … Morsi, H. M. ( 2012 ). Effect of novel water soluble curcumin derivative on experimental type‐ 1 diabetes mellitus (short term study). Diabetology and Metabolic Syndrome, 4, 30.
dc.identifier.citedreferenceAchour, M., Mousli, M., Alhosin, M., Ibrahim, A., Peluso, J., Muller, C. D., … Bronner, C. ( 2013 ). Epigallocatechin‐3‐gallate up‐regulates tumor suppressor gene expression via a reactive oxygen species‐dependent down‐regulation of UHRF1. Biochemical and Biophysical Research Communications, 430, 208 – 212.
dc.identifier.citedreferenceAhn, M. Y., Kang, D. O., Na, Y. J., Yoon, S., Choi, W. S., Kang, K. W., … Kim, H. S. ( 2012 ). Histone deacetylase inhibitor, apicidin, inhibits human ovarian cancer cell migration via class II histone deacetylase 4 silencing. Cancer Letters, 325, 189 – 199.
dc.identifier.citedreferenceAilenberg, M., & Silverman, M. ( 2002 ). Trichostatin A—histone deacetylase inhibitor with clinical therapeutic potential—is also a selective and potent inhibitor of gelatinase A expression. Biochemical and Biophysical Research Communications, 298, 110 – 115.
dc.identifier.citedreferenceAndia, D. C., de Oliveira, N. F., Casarin, R. C., Casati, M. Z., Line, S. R., & de Souza, A. P. ( 2010 ). DNA methylation status of the IL8 gene promoter in aggressive periodontitis. Journal of Periodontology, 81, 1336 – 1341.
dc.identifier.citedreferenceAraki, Y., Tsuzuki Wada, T., Aizaki, Y., Sato, K., Yokota, K., Fujimoto, K., … Mimura, T. ( 2016 ). Histone methylation and STAT‐3 differentially regulate interleukin‐6‐induced matrix metalloproteinase gene activation in rheumatoid arthritis synovial fibroblasts. Arthritis & Rhematology, 68, 1111 – 1123.
dc.identifier.citedreferenceAresu, L., Benali, S., Garbisa, S., Gallo, E., & Castagnaro, M. ( 2011 ). Matrix metalloproteinases and their role in the renal epithelial mesenchymal transition. Histology and Histopathology, 26, 307 – 313.
dc.identifier.citedreferenceArmitage, G. C. ( 2004 ). Periodontal diagnoses and classification of periodontal diseases. Periodontology 2000, 34, 9 – 21.
dc.identifier.citedreferenceArmitage, G. C. ( 2008 ). Challenges in diagnosis and classification of periodontal diseases and conditions. Zhonghua Kou Qiang Yi Xue Za Zhi, 43, 260 – 263.
dc.identifier.citedreferenceAsai, Y., Jinno, T., Igarashi, H., Ohyama, Y., & Ogawa, T. ( 2002 ). Detection and quantification of oral treponemes in subgingival plaque by real‐time PCR. Journal of Clinical Microbiology, 40, 3334 – 3340.
dc.identifier.citedreferenceAzevedo, A., Prado, A. F., Antonio, R. C., Issa, J. P., & Gerlach, R. F. ( 2014 ). Matrix metalloproteinases are involved in cardiovascular diseases. Basic & Clinical Pharmacology & Toxicology, 115, 301 – 314.
dc.identifier.citedreferenceBakir, B., Yetkin Ay, Z., Buyukbayram, H. I., Kumbul Doguc, D., Bayram, D., Candan, I. A., & Uskun, E. ( 2016 ). The effect of curcumin treatment on systemic Th17 response; gingival expression of IL‐17 and retinoic acid receptor‐related orphan receptor γt; and alveolar bone loss in experimental periodontitis. Journal of Periodontology, 1 – 17.
dc.identifier.citedreferenceBalasubramanyam, K., Varier, R. A., Altaf, M., Swaminathan, V., Siddappa, N. B., Ranga, U., & Kundu, T. K. ( 2004 ). Curcumin, a novel p300/CREB‐binding protein‐specific inhibitor of acetyltransferase, represses the acetylation of histone/nonhistone proteins and histone acetyltransferase‐dependent chromatin transcription. The Journal of Biological Chemistry, 279, 51163 – 51171.
dc.identifier.citedreferenceBaliga, M. S., Joseph, N., Venkataranganna, M. V., Saxena, A., Ponemone, V., & Fayad, R. ( 2012 ). Curcumin, an active component of turmeric in the prevention and treatment of ulcerative colitis: Preclinical and clinical observations. Food & Function, 3, 1109 – 1117.
dc.identifier.citedreferenceBarros, S. P., & Offenbacher, S. ( 2009 ). Epigenetics: Connecting environment and genotype to phenotype and disease. Journal of Dental Research, 88, 400 – 408.
dc.identifier.citedreferenceBarros, S. P., & Offenbacher, S. ( 2014 ). Modifiable risk factors in periodontal disease: Epigenetic regulation of gene expression in the inflammatory response. Periodontology 2000, 64, 95 – 110.
dc.identifier.citedreferenceBarski, A., Cuddapah, S., Cui, K., Roh, T. Y., Schones, D. E., Wang, Z., … Zhao, K. ( 2007 ). High‐resolution profiling of histone methylations in the human genome. Cell, 129, 823 – 837.
dc.identifier.citedreferenceBauden, M., Tassidis, H., & Ansari, D. ( 2015 ). In vitro cytotoxicity evaluation of HDAC inhibitor apicidin in pancreatic carcinoma cells subsequent time and dose dependent treatment. Toxicology Letters, 236, 8 – 15.
dc.identifier.citedreferenceBayarsaihan, D. ( 2011 ). Epigenetic mechanisms in inflammation. Journal of Dental Research, 90, 9 – 17.
dc.identifier.citedreferenceBayarsaihan, D. ( 2016 ). Epigenetic mechanisms involved in modulation of inflammatory diseases. Current Opinion in Clinical Nutrition and Metabolic Care, 19, 263 – 269.
dc.identifier.citedreferenceBird, A. ( 2002 ). DNA methylation patterns and epigenetic memory. Genes & Development, 16, 6 – 21.
dc.identifier.citedreferenceBorkham‐Kamphorst, E., Alexi, P., Tihaa, L., Haas, U., & Weiskirchen, R. ( 2015 ). Platelet‐derived growth factor‐D modulates extracellular matrix homeostasis and remodeling through TIMP‐1 induction and attenuation of MMP‐2 and MMP‐9 gelatinase activities. Biochemical and Biophysical Research Communications, 457, 307 – 313.
dc.identifier.citedreferenceBrew, K., & Nagase, H. ( 2010 ). The tissue inhibitors of metalloproteinases (TIMPs): An ancient family with structural and functional diversity. Biochimica et Biophysica Acta, 1803, 55 – 71.
dc.identifier.citedreferenceButler, G. S., Butler, M. J., Atkinson, S. J., Will, H., Tamura, T., Schade van Westrum, S., … Murphy, G. ( 1998 ). The TIMP2 membrane type 1 metalloproteinase “receptor” regulates the concentration and efficient activation of progelatinase A. A kinetic study. The Journal of Biological Chemistry, 273, 871 – 880.
dc.identifier.citedreferenceCao, F., Liu, T., Xu, Y., Xu, D., & Feng, S. ( 2015 ). Curcumin inhibits cell proliferation and promotes apoptosis in human osteoclastoma cell through MMP‐9, NF‐kappaB and JNK signaling pathways. International Journal of Clinical and Experimental Pathology, 8, 6037 – 6045.
dc.identifier.citedreferenceChang, C. W., Hsieh, Y. H., Yang, W. E., Yang, S. F., Chen, Y., & Hu, D. N. ( 2014 ). Epigallocatechingallate inhibits migration of human uveal melanoma cells via downregulation of matrix metalloproteinase‐2 activity and ERK1/2 pathway. BioMed Research International, 2014, 141582.
dc.identifier.citedreferenceChang, H. W., Wang, H. C., Chen, C. Y., Hung, T. W., Hou, M. F., Yuan, S. S., … Tseng, C. N. ( 2014 ). 5‐azacytidine induces anoikis, inhibits mammosphere formation and reduces metalloproteinase 9 activity in MCF‐7 human breast cancer cells. Molecules, 19, 3149 – 3159.
dc.identifier.citedreferenceChang, J., Varghese, D. S., Gillam, M. C., Peyton, M., Modi, B., Schiltz, R. L., … Martinez, E. D. ( 2012 ). Differential response of cancer cells to HDAC inhibitors trichostatin A and depsipeptide. British Journal of Cancer, 106, 116 – 125.
dc.identifier.citedreferenceChang, Y. C., Yang, S. F., Lai, C. C., Liu, J. Y., & Hsieh, Y. S. ( 2002 ). Regulation of matrix metalloproteinase production by cytokines, pharmacological agents and periodontal pathogens in human periodontal ligament fibroblast cultures. Journal of Periodontal Research, 37, 196 – 203.
dc.identifier.citedreferenceCharitaki, E., Kastritis, E., Petraki, C., Liapis, K., Adamidis, K., Apostolou, T., … Dimopoulos, M. A. ( 2016 ). Glomerular expression of matrix metalloproteinases in AL‐amyloidosis and association with renal function at the time of kidney biopsy. Clinical Nephrology, 85, 44 – 54.
dc.identifier.citedreferenceChen, W. F., Huang, F., & Zha, J. ( 2012 ). The comparison of short‐term efficacies between decitabine and HA regimen for MDS/AML patients. Zhonghua Xue Ye Xue Za Zhi, 33, 143 – 144.
dc.identifier.citedreferenceChernov, A. V., Sounni, N. E., Remacle, A. G., & Strongin, A. Y. ( 2009 ). Epigenetic control of the invasion‐promoting MT1‐MMP/MMP‐2/TIMP‐2 axis in cancer cells. The Journal of Biological Chemistry, 284, 12727 – 12734.
dc.identifier.citedreferenceChi, B., Qi, M., & Kuramitsu, H. K. ( 2003 ). Role of dentilisin in Treponema denticola epithelial cell layer penetration. Research in Microbiology, 154, 637 – 643.
dc.identifier.citedreferenceChoi, B. K., Jung, J. H., Suh, H. Y., Yoo, Y. J., Cho, K. S., Chai, J. K., & Kim, C. K. ( 2001 ). Activation of matrix metalloproteinase‐2 by a novel oral spirochetal species Treponema lecithinolyticum. Journal of Periodontology, 72, 1594 – 1600.
dc.identifier.citedreferenceChoi, B. K., Paster, B. J., Dewhirst, F. E., & Gobel, U. B. ( 1994 ). Diversity of cultivable and uncultivable oral spirochetes from a patient with severe destructive periodontitis. Infection and Immunity, 62, 1889 – 1895.
dc.identifier.citedreferenceDai, R., Iwama, A., Wang, S., & Kapila, Y. L. ( 2005 ). Disease‐associated fibronectin matrix fragments trigger anoikis of human primary ligament cells: p53 and c‐myc are suppressed. Apoptosis, 10, 503 – 512.
dc.identifier.citedreferencede Camargo Pereira, G., Guimaraes, G. N., Planello, A. C., Santamaria, M. P., de Souza, A. P., Line, S. R., & Marques, M. R. ( 2013 ). Porphyromonas gingivalis LPS stimulation downregulates DNMT1, DNMT3a, and JMJD3 gene expression levels in human HaCaT keratinocytes. Clinical Oral Investigations, 17, 1279 – 1285.
dc.identifier.citedreferenceDing, Y., Haapasalo, M., Kerosuo, E., Lounatmaa, K., Kotiranta, A., & Sorsa, T. ( 1997 ). Release and activation of human neutrophil matrix metallo‐ and serine proteinases during phagocytosis of Fusobacterium nucleatum, Porphyromonas gingivalis and Treponema denticola. Journal of Clinical Periodontology, 24, 237 – 248.
dc.identifier.citedreferenceDu, A., Zhao, S., Wan, L., Liu, T., Peng, Z., Zhou, Z., … Fang, H. ( 2016 ). MicroRNA expression profile of human periodontal ligament cells under the influence of Porphyromonas gingivalis LPS. Journal of Cellular and Molecular Medicine, 20, 1329 – 1338.
dc.identifier.citedreferenceEjeil, A. L., Igondjo‐Tchen, S., Ghomrasseni, S., Pellat, B., Godeau, G., & Gogly, B. ( 2003 ). Expression of matrix metalloproteinases (MMPs) and tissue inhibitors of metalloproteinases (TIMPs) in healthy and diseased human gingiva. Journal of Periodontology, 74, 188 – 195.
dc.identifier.citedreferenceElburki, M. S., Moore, D. D., Terezakis, N. G., Zhang, Y., Lee, H. M., Johnson, F., & Golub, L. M. ( 2016 ). A novel chemically modified curcumin reduces inflammation‐mediated connective tissue breakdown in a rat model of diabetes: Periodontal and systemic effects. Journal of Periodontal Research.
dc.identifier.citedreferenceElburki, M. S., Rossa, C., Guimaraes, M. R., Goodenough, M., Lee, H. M., Curylofo, F. A., … Golub, L. M. ( 2014 ). A novel chemically modified curcumin reduces severity of experimental periodontal disease in rats: Initial observations. Mediators of Inflammation, 2014, 959471.
dc.identifier.citedreferenceEllen, R. P., Dawson, J. R., & Yang, P. F. ( 1994 ). Treponema denticola as a model for polar adhesion and cytopathogenicity of spirochetes. Trends in Microbiology, 2, 114 – 119.
dc.identifier.citedreferenceEllen, R. P., & Galimanas, V. B. ( 2005 ). Spirochetes at the forefront of periodontal infections. Periodontology 2000, 38, 13 – 32.
dc.identifier.citedreferenceEndres, M., Kneitz, S., Orth, M. F., Perera, R. K., Zernecke, A., & Butt, E. ( 2016 ). Regulation of matrix metalloproteinases (MMPs) expression and secretion in MDA‐MB‐231 breast cancer cells by LIM and SH3 protein 1 (LASP1). Oncotarget.
dc.identifier.citedreferenceFeng, Q., Su, Z., Song, S., Chiu, H., Zhang, B., Yi, L., … Wang, H. ( 2016 ). Histone deacetylase inhibitors suppress RSV infection and alleviate virus‐induced airway inflammation. Int J Mol Med.
dc.identifier.citedreferenceFenno, J.C. ( 2005 ). Laboratory maintenance of Treponema denticola. Curr Protoc Microbiol Chapter 12, Unit 12B 11.
dc.identifier.citedreferenceFenno, J. C., Hannam, P. M., Leung, W. K., Tamura, M., Uitto, V. J., & McBride, B. C. ( 1998 ). Cytopathic effects of the major surface protein and the chymotrypsinlike protease of Treponema denticola. Infection and Immunity, 66, 1869 – 1877.
dc.identifier.citedreferenceGarcia, D., Tarima, S., & Okunseri, C. ( 2015 ). Periodontitis and glycemic control in diabetes: NHANES 2009 to 2012. Journal of Periodontology, 86, 499 – 506.
dc.identifier.citedreferenceGhosh, A., Park, J. Y., Fenno, C., & Kapila, Y. L. ( 2008 ). Porphyromonas gingivalis, gamma interferon, and a proapoptotic fibronectin matrix form a synergistic trio that induces c‐Jun N‐terminal kinase 1‐mediated nitric oxide generation and cell death. Infection and Immunity, 76, 5514 – 5523.
dc.identifier.citedreferenceGoldberg, A. D., Allis, C. D., & Bernstein, E. ( 2007 ). Epigenetics: A landscape takes shape. Cell, 128, 635 – 638.
dc.identifier.citedreferenceGrenier, D., Uitto, V. J., & McBride, B. C. ( 1990 ). Cellular location of a T reponema denticola chymotrypsinlike protease and importance of the protease in migration through the basement membrane. Infection and Immunity, 58, 347 – 351.
dc.identifier.citedreferenceGuenther, M. G., Levine, S. S., Boyer, L. A., Jaenisch, R., & Young, R. A. ( 2007 ). A chromatin landmark and transcription initiation at most promoters in human cells. Cell, 130, 77 – 88.
dc.identifier.citedreferenceHaapasalo, M., Singh, U., McBride, B. C., & Uitto, V. J. ( 1991 ). Sulfhydryl‐dependent attachment of Treponema denticola to laminin and other proteins. Infection and Immunity, 59, 4230 – 4237.
dc.identifier.citedreferenceHassler, M. R., Klisaroska, A., Kollmann, K., Steiner, I., Bilban, M., Schiefer, A. I., … Egger, G. ( 2012 ). Antineoplastic activity of the DNA methyltransferase inhibitor 5‐aza‐2′‐deoxycytidine in anaplastic large cell lymphoma. Biochimie, 94, 2297 – 2307.
dc.identifier.citedreferenceHerceg, Z. ( 2016 ). Epigenetic mechanisms as an interface between the environment and genome. Advances in Experimental Medicine and Biology, 903, 3 – 15.
dc.identifier.citedreferenceHernandez‐Barrantes, S., Shimura, Y., Soloway, P. D., Sang, Q. A., & Fridman, R. ( 2001 ). Differential roles of TIMP‐4 and TIMP‐2 in pro‐MMP‐2 activation by MT1‐MMP. Biochemical and Biophysical Research Communications, 281, 126 – 130.
dc.identifier.citedreferenceHook, K. E., Garza, S. J., Lira, M. E., Ching, K. A., Lee, N. V., Cao, J., … Pavlicek, A. ( 2012 ). An integrated genomic approach to identify predictive biomarkers of response to the aurora kinase inhibitor PF‐03814735. Molecular Cancer Therapeutics, 11, 710 – 719.
dc.identifier.citedreferenceHuynh, Q. N., Wang, S., Tafolla, E., Gansky, S. A., Kapila, S., Armitage, G. C., & Kapila, Y. L. ( 2002 ). Specific fibronectin fragments as markers of periodontal disease status. Journal of Periodontology, 73, 1101 – 1110.
dc.identifier.citedreferenceInagaki, S., Kimizuka, R., Kokubu, E., Saito, A., & Ishihara, K. ( 2016 ). Treponema denticola invasion into human gingival epithelial cells. Microbial Pathogenesis, 94, 104 – 111.
dc.identifier.citedreferenceJani, J. P., Arcari, J., Bernardo, V., Bhattacharya, S. K., Briere, D., Cohen, B. D., … Jakubczak, J. L. ( 2010 ). PF‐03814735, an orally bioavailable small molecule aurora kinase inhibitor for cancer therapy. Molecular Cancer Therapeutics, 9, 883 – 894.
dc.identifier.citedreferenceJee, S. W., Wang, S., & Kapila, Y. L. ( 2004 ). Specific pro‐apoptotic fibronectin fragments modulate proteinase expression in periodontal ligament cells. Journal of Periodontology, 75, 523 – 530.
dc.identifier.citedreferenceJenuwein, T., & Allis, C. D. ( 2001 ). Translating the histone code. Science, 293, 1074 – 1080.
dc.identifier.citedreferenceJo, A. R., Baek, K. J., Shin, J. E., & Choi, Y. ( 2014 ). Mechanisms of IL‐8 suppression by Treponema denticola in gingival epithelial cells. Immunology and Cell Biology, 92, 139 – 147.
dc.identifier.citedreferenceJoo, N. E., Watanabe, T., Chen, C., Chekenya, M., Stallcup, W. B., & Kapila, Y. L. ( 2008 ). NG2, a novel proapoptotic receptor, opposes integrin alpha4 to mediate anoikis through PKCalpha‐dependent suppression of FAK phosphorylation. Cell Death and Differentiation, 15, 899 – 907.
dc.identifier.citedreferenceJoseph, J., Kapila, Y. L., Hayami, T., & Kapila, S. ( 2010 ). Disease‐associated extracellular matrix suppresses osteoblastic differentiation of human periodontal ligament cells via MMP‐1. Calcified Tissue International, 86, 154 – 162.
dc.identifier.citedreferenceKapila, Y. L., Kapila, S., & Johnson, P. W. ( 1996 ). Fibronectin and fibronectin fragments modulate the expression of proteinases and proteinase inhibitors in human periodontal ligament cells. Matrix Biology, 15, 251 – 261.
dc.identifier.citedreferenceKapila, Y. L., Lancero, H., & Johnson, P. W. ( 1998 ). The response of periodontal ligament cells to fibronectin. Journal of Periodontology, 69, 1008 – 1019.
dc.identifier.citedreferenceKapila, Y. L., Wang, S., Dazin, P., Tafolla, E., & Mass, M. J. ( 2002 ). The heparin‐binding domain and V region of fibronectin regulate apoptosis by suppression of p53 and c‐myc in human primary cells. The Journal of Biological Chemistry, 277, 8482 – 8491.
dc.identifier.citedreferenceKapila, Y. L., Wang, S., & Johnson, P. W. ( 1999 ). Mutations in the heparin binding domain of fibronectin in cooperation with the V region induce decreases in pp125(FAK) levels plus proteoglycan‐mediated apoptosis via caspases. The Journal of Biological Chemistry, 274, 30906 – 30913.
dc.identifier.citedreferenceKhansari, N., Shakiba, Y., & Mahmoudi, M. ( 2009 ). Chronic inflammation and oxidative stress as a major cause of age‐related diseases and cancer. Recent Patents on Inflammation & Allergy Drug Discovery, 3, 73 – 80.
dc.identifier.citedreferenceKim, M. S., Son, M. W., Kim, W. B., In Park, Y., & Moon, A. ( 2000 ). Apicidin, an inhibitor of histone deacetylase, prevents H‐ras‐induced invasive phenotype. Cancer Letters, 157, 23 – 30.
dc.identifier.citedreferenceKinoshita, T., Sato, H., Okada, A., Ohuchi, E., Imai, K., Okada, Y., & Seiki, M. ( 1998 ). TIMP‐2 promotes activation of progelatinase A by membrane‐type 1 matrix metalloproteinase immobilized on agarose beads. The Journal of Biological Chemistry, 273, 16098 – 16103.
dc.identifier.citedreferenceKoch, C. M., Andrews, R. M., Flicek, P., Dillon, S. C., Karaoz, U., Clelland, G. K., … Dunham, I. ( 2007 ). The landscape of histone modifications across 1% of the human genome in five human cell lines. Genome Research, 17, 691 – 707.
dc.identifier.citedreferenceKonermann, A., Deschner, J., Allam, J. P., Novak, N., Winter, J., Baader, S. L., … Jager, A. ( 2012 ). Antigen‐presenting cell marker expression and phagocytotic activity in periodontal ligament cells. Journal of Oral Pathology & Medicine, 41, 340 – 347.
dc.identifier.citedreferenceKouzarides, T. ( 2007 ). Chromatin modifications and their function. Cell, 128, 693 – 705.
dc.identifier.citedreferenceKubicek, S., O’Sullivan, R. J., August, E. M., Hickey, E. R., Zhang, Q., Teodoro, M. L., … Jenuwein, T. ( 2007 ). Reversal of H3K9me2 by a small‐molecule inhibitor for the G9a histone methyltransferase. Molecular Cell, 25, 473 – 481.
dc.identifier.citedreferenceLamont, R. J., Chan, A., Belton, C. M., Izutsu, K. T., Vasel, D., & Weinberg, A. ( 1995 ). Porphyromonas gingivalis invasion of gingival epithelial cells. Infection and Immunity, 63, 3878 – 3885.
dc.identifier.citedreferenceLee, A. Y., Fan, C. C., Chen, Y. A., Cheng, C. W., Sung, Y. J., Hsu, C. P., & Kao, T. Y. ( 2015 ). Curcumin inhibits invasiveness and epithelial‐mesenchymal transition in oral squamous cell carcinoma through reducing matrix metalloproteinase 2, 9 and modulating p53‐E‐cadherin pathway. Integrative Cancer Therapies, 14, 484 – 490.
dc.identifier.citedreferenceLeira, Y., Seoane, J., Blanco, M., Rodriguez‐Yanez, M., Takkouche, B., Blanco, J. and Castillo, J. ( 2016 ). Association between periodontitis and ischemic stroke: A systematic review and meta‐analysis. Eur J Epidemiol.
dc.identifier.citedreferenceLigi, D., & Mannello, F. ( 2016 ). Do matrix metalloproteinases represent reliable circulating biomarkers in colorectal cancer? British Journal of Cancer, 115, 633 – 634.
dc.identifier.citedreferenceLiu, C. C., Chang, T. C., Lin, Y. T., Yu, Y. L., Ko, B. S., Sung, L. Y., & Liou, J. Y. ( 2016 ). Paracrine regulation of matrix metalloproteinases contributes to cancer cell invasion by hepatocellular carcinoma‐secreted 14‐3‐3sigma. Oncotarget.
dc.identifier.citedreferenceLiu, W. H., Sang, M. X., Hou, S. Y., Zhang, C., & Shan, B. E. ( 2014 ). Low‐dose decitabine induces MAGE‐A expression and inhibits invasion via suppression of NF‐kappaB2 and MMP2 in Eca109 cells. Biomedicine & Pharmacotherapy, 68, 745 – 750.
dc.identifier.citedreferenceLiu, Z., Zhang, L., Ding, F., Li, J., Guo, M., Li, W., … Liu, Z. ( 2005 ). 5‐Aza‐2′‐deoxycytidine induces retinoic acid receptor‐beta(2) demethylation and growth inhibition in esophageal squamous carcinoma cells. Cancer Letters, 230, 271 – 283.
dc.identifier.citedreferenceLivak, K. J., & Schmittgen, T. D. ( 2001 ). Analysis of relative gene expression data using real‐time quantitative PCR and the 2 − ΔΔ C T method. Methods, 25, 402 – 408.
dc.identifier.citedreferenceLukaszewicz‐Zajac, M., Szmitkowski, M., Litman‐Zawadzka, A., & Mroczko, B. ( 2016 ). Matrix metalloproteinases and their tissue inhibitors in comparison to other inflammatory proteins in gastric cancer (GC). Cancer Investigation, 34, 305 – 312.
dc.identifier.citedreferenceMadsen, D. H., Jurgensen, H. J., Ingvarsen, S., Melander, M. C., Albrechtsen, R., Hald, A., … Engelholm, L. H. ( 2013 ). Differential actions of the endocytic collagen receptor uPARAP/Endo180 and the collagenase MMP‐2 in bone homeostasis. PLoS One, 8, e71261.
dc.identifier.citedreferenceMakinen, P. L., Makinen, K. K., & Syed, S. A. ( 1995 ). Role of the chymotrypsin‐like membrane‐associated proteinase from Treponema denticola ATCC 35405 in inactivation of bioactive peptides. Infection and Immunity, 63, 3567 – 3575.
dc.identifier.citedreferenceMani, S. K., Kern, C. B., Kimbrough, D., Addy, B., Kasiganesan, H., Rivers, W. T., … Menick, D. R. ( 2015 ). Inhibition of class I histone deacetylase activity represses matrix metalloproteinase‐2 and ‐9 expression and preserves LV function postmyocardial infarction. American Journal of Physiology. Heart and Circulatory Physiology, 308, H1391 – H1401.
dc.identifier.citedreferenceMartinez, J. A., Milagro, F. I., Claycombe, K. J., & Schalinske, K. L. ( 2014 ). Epigenetics in adipose tissue, obesity, weight loss, and diabetes. Advances in Nutrition, 5, 71 – 81.
dc.identifier.citedreferenceMathers, D. A., Leung, W. K., Fenno, J. C., Hong, Y., & McBride, B. C. ( 1996 ). The major surface protein complex of Treponema denticola depolarizes and induces ion channels in HeLa cell membranes. Infection and Immunity, 64, 2904 – 2910.
dc.identifier.citedreferenceMcDowell, J. V., Frederick, J., Miller, D. P., Goetting‐Minesky, M. P., Goodman, H., Fenno, J. C., & Marconi, R. T. ( 2011 ). Identification of the primary mechanism of complement evasion by the periodontal pathogen, Treponema denticola. Molecular Oral Microbiology, 26, 140 – 149.
dc.identifier.citedreferenceMcDowell, J. V., Huang, B., Fenno, J. C., & Marconi, R. T. ( 2009 ). Analysis of a unique interaction between the complement regulatory protein factor H and the periodontal pathogen Treponema denticola. Infection and Immunity, 77, 1417 – 1425.
dc.identifier.citedreferenceMedina, C., Santana, A., Quintero, E., Radomski, M. W., & Guarner, F. ( 2004 ). Matrix metalloproteinases in diseases of the gastrointestinal tract. Gastroenterología y Hepatología, 27, 491 – 497.
dc.identifier.citedreferenceMedzhitov, R., & Horng, T. ( 2009 ). Transcriptional control of the inflammatory response. Nature Reviews. Immunology, 9, 692 – 703.
dc.identifier.citedreferenceMiao, D., Fenno, J. C., Timm, J. C., Joo, N. E., & Kapila, Y. L. ( 2011 ). The Treponema denticola chymotrypsin‐like protease dentilisin induces matrix metalloproteinase‐2‐dependent fibronectin fragmentation in periodontal ligament cells. Infection and Immunity, 79, 806 – 811.
dc.identifier.citedreferenceMiao, D., Godovikova, V., Qian, X., Seshadrinathan, S., Kapila, Y. L., & Fenno, J. C. ( 2014 ). Treponema denticola upregulates MMP‐2 activation in periodontal ligament cells: Interplay between epigenetics and periodontal infection. Archives of Oral Biology, 59, 1056 – 1064.
dc.identifier.citedreferenceMirza, S., Sharma, G., Pandya, P., & Ralhan, R. ( 2010 ). Demethylating agent 5‐aza‐2‐deoxycytidine enhances susceptibility of breast cancer cells to anticancer agents. Molecular and Cellular Biochemistry, 342, 101 – 109.
dc.identifier.citedreferenceMittal, R., Patel, A. P., Debs, L. H., Nguyen, D., Patel, K., Grati, M., … Liu, X. Z. ( 2016 ). Intricate functions of matrix metalloproteinases in physiological and pathological conditions. Journal of Cellular Physiology, 231, 2599 – 2621.
dc.identifier.citedreferenceMogal, A., & Abdulkadir, S. A. ( 2006 ). Effects of histone deacetylase inhibitor (HDACi); Trichostatin‐A (TSA) on the expression of housekeeping genes. Molecular and Cellular Probes, 20, 81 – 86.
dc.identifier.citedreferenceMosig, R. A., & Martignetti, J. A. ( 2013 ). Loss of MMP‐2 in murine osteoblasts upregulates osteopontin and bone sialoprotein expression in a circuit regulating bone homeostasis. Disease Models & Mechanisms, 6, 397 – 403.
dc.identifier.citedreferenceMurphy, G., Stanton, H., Cowell, S., Butler, G., Knauper, V., Atkinson, S., & Gavrilovic, J. ( 1999 ). Mechanisms for pro matrix metalloproteinase activation. APMIS, 107, 38 – 44.
dc.identifier.citedreferenceNagaraju, G. P., Aliya, S., Zafar, S. F., Basha, R., Diaz, R., & El‐Rayes, B. F. ( 2012 ). The impact of curcumin on breast cancer. Integr Biol (Camb), 4, 996 – 1007.
dc.identifier.citedreferenceNagase, H. ( 1997 ). Activation mechanisms of matrix metalloproteinases. Biological Chemistry, 378, 151 – 160.
dc.identifier.citedreferenceNagase, H., Visse, R., & Murphy, G. ( 2006 ). Structure and function of matrix metalloproteinases and TIMPs. Cardiovascular Research, 69, 562 – 573.
dc.identifier.citedreferenceNagasri, M., Madhulatha, M., Musalaiah, S. V., Kumar, P. A., Krishna, C. H., & Kumar, P. M. ( 2015 ). Efficacy of curcumin as an adjunct to scaling and root planning in chronic periodontitis patients: A clinical and microbiological study. Journal of Pharmacy & Bioallied Sciences, 7, S554 – S558.
dc.identifier.citedreferenceNakayama, J., Rice, J. C., Strahl, B. D., Allis, C. D., & Grewal, S. I. ( 2001 ). Role of histone H3 lysine 9 methylation in epigenetic control of heterochromatin assembly. Science, 292, 110 – 113.
dc.identifier.citedreferenceNavratilova, Z., Kolek, V., & Petrek, M. ( 2016 ). Matrix metalloproteinases and their inhibitors in chronic obstructive pulmonary disease. Archivum Immunologiae et Therapiae Experimentalis (Warsz), 64, 177 – 193.
dc.identifier.citedreferenceNebbioso, A., Carafa, V., Benedetti, R., & Altucci, L. ( 2012 ). Trials with ’epigenetic’ drugs: An update. Molecular Oncology, 6, 657 – 682.
dc.identifier.citedreferenceNiller, H. H., Masa, R., Venkei, A., Meszaros, S., & Minarovits, J. ( 2017 ). Pathogenic mechanisms of intracellular bacteria. Current Opinion in Infectious Diseases, 30, 309 – 315.
dc.identifier.citedreferenceNissinen, L., & Kahari, V. M. ( 2014 ). Matrix metalloproteinases in inflammation. Biochimica et Biophysica Acta, 1840, 2571 – 2580.
dc.identifier.citedreferenceNowakowska, A., & Tarasiuk, J. ( 2016 ). Comparative effects of selected plant polyphenols, gallic acid and epigallocatechin gallate, on matrix metalloproteinases activity in multidrug resistant MCF7/DOX breast cancer cells. Acta Biochimica Polonica.
dc.identifier.citedreferenceOyarzun, A., Arancibia, R., Hidalgo, R., Penafiel, C., Caceres, M., Gonzalez, M. J., … Smith, P. C. ( 2010 ). Involvement of MT1‐MMP and TIMP‐2 in human periodontal disease. Oral Diseases, 16, 388 – 395.
dc.identifier.citedreferencePardo, A., Cabrera, S., Maldonado, M., & Selman, M. ( 2016 ). Role of matrix metalloproteinases in the pathogenesis of idiopathic pulmonary fibrosis. Respiratory Research, 17, 23.
dc.identifier.citedreferencePark, S. Y., Jun, J. A., Jeong, K. J., Heo, H. J., Sohn, J. S., Lee, H. Y., … Kang, J. ( 2011 ). Histone deacetylases 1, 6 and 8 are critical for invasion in breast cancer. Oncology Reports, 25, 1677 – 1681.
dc.identifier.citedreferencePasquier, J., Hoarau‐Vechot, J., Fakhro, K., Rafii, A., & Abi Khalil, C. ( 2015 ). Epigenetics and cardiovascular disease in diabetes. Current Diabetes Reports, 15, 108.
dc.identifier.citedreferencePereira, I. T., Ramos, E. A., Costa, E. T., Camargo, A. A., Manica, G. C., Klassen, L. M., … Klassen, G. ( 2014 ). Fibronectin affects transient MMP2 gene expression through DNA demethylation changes in non‐invasive breast cancer cell lines. PLoS One, 9, e105806.
dc.identifier.citedreferencePerkins, D. J., Patel, M. C., Blanco, J. C., & Vogel, S. N. ( 2016 ). Epigenetic mechanisms governing innate inflammatory responses. Journal of Interferon & Cytokine Research, 36, 454 – 461.
dc.identifier.citedreferencePietruszewska, W., Bojanowska‐Pozniak, K., & Kobos, J. ( 2016 ). Matrix metalloproteinases MMP1, MMP2, MMP9 and their tissue inhibitors TIMP1, TIMP2, TIMP3 in head and neck cancer: An immunohistochemical study. Otolaryngologia Polska, 70, 32 – 43.
dc.identifier.citedreferencePihlstrom, B. L., Michalowicz, B. S., & Johnson, N. W. ( 2005 ). Periodontal diseases. The Lancet, 366, 1809 – 1820.
dc.identifier.citedreferencePrasanna, S. J. ( 2011 ). Causal relationship between periodontitis and chronic obstructive pulmonary disease. J Indian Soc Periodontol, 15, 359 – 365.
dc.identifier.citedreferenceRazzouk, S., & Sarkis, R. ( 2013 ). Smoking and diabetes. Epigenetics involvement in osseointegration. The New York State Dental Journal, 79, 27 – 30.
dc.identifier.citedreferenceSafronova, O., & Morita, I. ( 2010 ). Transcriptome remodeling in hypoxic inflammation. Journal of Dental Research, 89, 430 – 444.
dc.identifier.citedreferenceSakamoto, M., Takeuchi, Y., Umeda, M., Ishikawa, I., & Benno, Y. ( 2001 ). Rapid detection and quantification of five periodontopathic bacteria by real‐time PCR. Microbiology and Immunology, 45, 39 – 44.
dc.identifier.citedreferenceSaldanha, S. N., Kala, R., & Tollefsbol, T. O. ( 2014 ). Molecular mechanisms for inhibition of colon cancer cells by combined epigenetic‐modulating epigallocatechin gallate and sodium butyrate. Experimental Cell Research, 324, 40 – 53.
dc.identifier.citedreferenceScanlon, C., Marchesan, J., Soehren, S., Matsuo, M., & Kapila, Y. ( 2011 ). Capturing the regenerative potential of periodontal ligament fibroblasts. J Stem Cells Regen Med, 7, 54 – 56.
dc.identifier.citedreferenceSchoffski, P., Jones, S. F., Dumez, H., Infante, J. R., Van Mieghem, E., Fowst, C., … Burris, H. A. ( 2011 ). Phase I, open‐label, multicentre, dose‐escalation, pharmacokinetic and pharmacodynamic trial of the oral aurora kinase inhibitor PF‐03814735 in advanced solid tumours. European Journal of Cancer, 47, 2256 – 2264.
dc.identifier.citedreferenceShin, J., & Choi, Y. ( 2012 ). The fate of Treponema denticola within human gingival epithelial cells. Molecular Oral Microbiology, 27, 471 – 482.
dc.identifier.citedreferenceShinkarenko, T. V., Rumiantsev, V. A., Egorova, E. N., & Eliseeva, T. I. ( 2013 ). Matrix metalloproteinases in periodontitis. Stomatologiia (Mosk), 92, 77 – 80.
dc.identifier.citedreferenceShofuda, K., Moriyama, K., Nishihashi, A., Higashi, S., Mizushima, H., Yasumitsu, H., … Miyazaki, K. ( 1998 ). Role of tissue inhibitor of metalloproteinases‐2 (TIMP‐2) in regulation of pro‐gelatinase a activation catalyzed by membrane‐type matrix metalloproteinase‐1 (MT1‐MMP) in human cancer cells. Journal of Biochemistry, 124, 462 – 470.
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