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Characterization of macrophage polarization in periodontal disease

dc.contributor.authorGaraicoa‐pazmino, Carlos
dc.contributor.authorFretwurst, Tobias
dc.contributor.authorSquarize, Cristiane H.
dc.contributor.authorBerglundh, Tord
dc.contributor.authorGiannobile, William V.
dc.contributor.authorLarsson, Lena
dc.contributor.authorCastilho, Rogerio M.
dc.date.accessioned2019-08-09T17:12:55Z
dc.date.availableWITHHELD_13_MONTHS
dc.date.available2019-08-09T17:12:55Z
dc.date.issued2019-08
dc.identifier.citationGaraicoa‐pazmino, Carlos ; Fretwurst, Tobias; Squarize, Cristiane H.; Berglundh, Tord; Giannobile, William V.; Larsson, Lena; Castilho, Rogerio M. (2019). "Characterization of macrophage polarization in periodontal disease." Journal of Clinical Periodontology 46(8): 830-839.
dc.identifier.issn0303-6979
dc.identifier.issn1600-051X
dc.identifier.urihttps://hdl.handle.net/2027.42/150506
dc.description.abstractAimTo explore the M1/M2 status of macrophage polarization from healthy, gingivitis, and periodontitis patient samples.Materials and methodsGingival biopsies were collected from 42 individuals (14 gingivitis, 18 periodontitis, and 10 healthy samples) receiving periodontal therapy. Histomorphology analysis was performed with haematoxylin and eosin staining. Immunofluorescence was performed using a combination of CD68 (macrophages), iNOS (M1), and CD206 (M2) in order to acquire changes in macrophage polarization at a singleâ cell resolution. Macrophages were quantified under microscopy using narrow wavelength filters to detect Alexa 488, Alexa 568, Alexa 633 fluorophores, and Hoechst 33342 to identify cellular DNA content.ResultsGingivitis and periodontitis samples showed higher levels of macrophages compared with healthy samples. Unexpectedly, periodontitis samples displayed lower levels of macrophages dispersed in the stromal tissues compared with gingivitis samples; however, it remained higher than healthy tissues. The polarization of macrophages appears to be reduced in periodontitis and showed similar levels to those observed in healthy tissues.ConclusionsOur study found that gingivitis and periodontitis differ from each other by the levels of macrophage infiltrate, but not by changes in macrophage polarization.
dc.publisherWiley Periodicals, Inc.
dc.subject.otherperiodontitis
dc.subject.othergingivitis
dc.subject.otherallergy and immunology
dc.subject.otherimmunohistochemistry
dc.subject.otherimmunologic factors
dc.subject.otherinflammation
dc.titleCharacterization of macrophage polarization in periodontal disease
dc.typeArticle
dc.rights.robotsIndexNoFollow
dc.subject.hlbsecondlevelDentistry
dc.subject.hlbtoplevelHealth Sciences
dc.description.peerreviewedPeer Reviewed
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/150506/1/jcpe13156_am.pdf
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/150506/2/jcpe13156.pdf
dc.identifier.doi10.1111/jcpe.13156
dc.identifier.sourceJournal of Clinical Periodontology
dc.identifier.citedreferenceNavarrete, M., Garcia, J., Dutzan, N., Henriquez, L., Puente, J., Carvajal, P., â ¦ Gamonal, J. ( 2014 ). Interferonâ gamma, interleukinsâ 6 and â 4, and factor xiiiâ a as indirect markers of the classical and alternative macrophage activation pathways in chronic periodontitis. Journal of Periodontology, 85 ( 5 ), 751 â 760.
dc.identifier.citedreferenceHolden, J. A., Attard, T. J., Laughton, K. M., Mansell, A., O’Brienâ Simpson, N. M., & Reynolds, E. C. ( 2014 ). Porphyromonas gingivalis lipopolysaccharide weakly activates m1 and m2 polarized mouse macrophages but induces inflammatory cytokines. Infection and Immunity, 82 ( 10 ), 4190 â 4203. https://doi.org/10.1128/IAI.02325-14
dc.identifier.citedreferenceHugoson, A., Sjodin, B., & Norderyd, O. ( 2008 ). Trends over 30 years, 1973â 2003, in the prevalence and severity of periodontal disease. Journal of Clinical Periodontology, 35 ( 5 ), 405 â 414. https://doi.org/10.1111/j.1600-051X.2008.01225.x
dc.identifier.citedreferenceHussain, Q. A., McKay, I. J., Gonzalesâ Marin, C., & Allaker, R. P. ( 2016 ). Detection of adrenomedullin and nitric oxide in different forms of periodontal disease. Journal of Periodontal Research, 51 ( 1 ), 16 â 25. https://doi.org/10.1111/jre.12273
dc.identifier.citedreferenceJeffcoat, M. K., & Reddy, M. S. ( 1991 ). Progression of probing attachment loss in adult periodontitis. Journal of Periodontology, 62 ( 3 ), 185 â 189. https://doi.org/10.1902/jop.1991.62.3.185
dc.identifier.citedreferenceKassebaum, N. J., Bernabe, E., Dahiya, M., Bhandari, B., Murray, C. J., & Marcenes, W. ( 2014 ). Global burden of severe tooth loss: A systematic review and metaâ analysis. Journal of Dental Research, 93 ( 7 Suppl ), 20S â 28S. https://doi.org/10.1177/0022034514537828
dc.identifier.citedreferenceKinane, D., Bouchard, P., & Group E of European Workshop on Periodontology ( 2008 ). Periodontal diseases and health: Consensus report of the sixth European workshop on periodontology. Journal of Clinical Periodontology, 35 ( 8 Suppl ), 333 â 337. https://doi.org/10.1111/j.1600-051X.2008.01278.x
dc.identifier.citedreferenceLam, R. S., O’Brienâ Simpson, N. M., Lenzo, J. C., Holden, J. A., Brammar, G. C., Walsh, K. A., â ¦ Reynolds, E. C. ( 2014 ). Macrophage depletion abates porphyromonas gingivalisâ induced alveolar bone resorption in mice. Journal of Immunology, 193 ( 5 ), 2349 â 2362.
dc.identifier.citedreferenceLappin, D. F., Kjeldsen, M., Sander, L., & Kinane, D. F. ( 2000 ). Inducible nitric oxide synthase expression in periodontitis. Journal of Periodontal Research, 35 ( 6 ), 369 â 373. https://doi.org/10.1034/j.1600-0765.2000.035006369.x
dc.identifier.citedreferenceLins, R. D. A. U., Figueiredo, C. R. L. V., Queiroz, L. M. G., Silveira, E. J. D. D., Godoy, G. P., & Freitas, R. D. A. ( 2008 ). Immunohistochemical evaluation of the inflammatory response in periodontal disease. Brazilian Dental Journal, 19 ( 1 ), 9 â 14. https://doi.org/10.1590/S0103-64402008000100002
dc.identifier.citedreferenceLoe, H., Anerud, A., Boysen, H., & Morrison, E. ( 1986 ). Natural history of periodontal disease in man. Rapid, moderate and no loss of attachment in sri lankan laborers 14 to 46 years of age. Journal of Clinical Periodontology, 13 ( 5 ), 431 â 445. https://doi.org/10.1111/j.1600-051X.1986.tb01487.x
dc.identifier.citedreferenceLoe, H., Theilade, E., & Jensen, S. B. ( 1965 ). Experimental gingivitis in man. Journal of Periodontology, 36, 177 â 187. https://doi.org/10.1902/jop.1965.36.3.177
dc.identifier.citedreferenceMartinez, F. O., & Gordon, S. ( 2014 ). The M1 and M2 paradigm of macrophage activation: Time for reassessment. F1000Prime Reports, 6, 13. https://doi.org/10.12703/P6-13
dc.identifier.citedreferenceMartins, M. D., Jiao, Y., Larsson, L., Almeida, L. O., Garaicoaâ Pazmino, C., Le, J. M., â ¦ Castilho, R. M. ( 2016 ). Epigenetic modifications of histones in periodontal disease. Journal of Dental Research, 95 ( 2 ), 215 â 222. https://doi.org/10.1177/0022034515611876
dc.identifier.citedreferenceMills, C. D., Kincaid, K., Alt, J. M., Heilman, M. J., & Hill, A. M. ( 2000 ). Mâ 1/mâ 2 macrophages and the th1/th2 paradigm. Journal of Immunology, 164 ( 12 ), 6166 â 6173.
dc.identifier.citedreferenceMills, C. D., & Ley, K. ( 2014 ). M1 and m2 macrophages: The chicken and the egg of immunity. Journal of Innate Immunity, 6 ( 6 ), 716 â 726. https://doi.org/10.1159/000364945
dc.identifier.citedreferenceBerglundh, T., Zitzmann, N. U., & Donati, M. ( 2011 ). Are periâ implantitis lesions different from periodontitis lesions? Journal of Clinical Periodontology, 38 ( Suppl 11 ), 188 â 202.
dc.identifier.citedreferenceOzmeric, N., Elgun, S., & Uraz, A. ( 2000 ). Salivary arginase in patients with adult periodontitis. Clinical Oral Investigations, 4 ( 1 ), 21 â 24. https://doi.org/10.1007/s007840050108
dc.identifier.citedreferencePage, R. C., & Schroeder, H. E. ( 1976 ). Pathogenesis of inflammatory periodontal disease. A Summary of Current Work. Laboratory Investigation, 34 ( 3 ), 235 â 249.
dc.identifier.citedreferenceSeeley, J. J., & Ghosh, S. ( 2017 ). Molecular mechanisms of innate memory and tolerance to lps. Journal of Leukocyte Biology, 101 ( 1 ), 107 â 119.
dc.identifier.citedreferenceSeymour, G. J., Powell, R. N., & Aitken, J. F. ( 1983 ). Experimental gingivitis in humans. A clinical and histologic investigation. Journal of Periodontology, 54 ( 9 ), 522 â 528. https://doi.org/10.1902/jop.1983.54.9.522
dc.identifier.citedreferenceSima, C., & Glogauer, M. ( 2013 ). Macrophage subsets and Osteoimmunology: Tuning of the immunological recognition and effector systems that maintain alveolar bone. Periodontology 2000, 63 ( 1 ), 80 â 101. https://doi.org/10.1111/prd.12032.
dc.identifier.citedreferenceSocransky, S. S., Haffajee, A. D., Goodson, J. M., & Lindhe, J. ( 1984 ). New concepts of destructive periodontal disease. Journal of Clinical Periodontology, 11 ( 1 ), 21 â 32. https://doi.org/10.1111/j.1600-051X.1984.tb01305.x
dc.identifier.citedreferenceTeles, R., Benecha, H. K., Preisser, J. S., Moss, K., Starr, J. R., Corby, P., â ¦ Cugini, M. A. ( 2016 ). Modelling changes in clinical attachment loss to classify periodontal disease progression. Journal of Clinical Periodontology, 43 ( 5 ), 426 â 434. https://doi.org/10.1111/jcpe.12539
dc.identifier.citedreferenceThorbertâ Mros, S., Larsson, L., & Berglundh, T. ( 2015 ). Cellular composition of longâ standing gingivitis and periodontitis lesions. Journal of Periodontal Research, 50 ( 4 ), 535 â 543. https://doi.org/10.1111/jre.12236
dc.identifier.citedreferenceViniegra, A., Goldberg, H., Ã il, Ã ., Fine, N., Sheikh, Z., Galli, M., â ¦ Sima, C. ( 2018 ). Resolving macrophages counter osteolysis by anabolic actions on bone cells. Journal of Dental Research, 97 ( 10 ), 1160 â 1169. https://doi.org/10.1177/0022034518777973
dc.identifier.citedreferenceYu, T., Zhao, L., Huang, X., Ma, C., Wang, Y., Zhang, J., & Xuan, D. ( 2016 ). Enhanced activity of the macrophage m1/m2 phenotypes and phenotypic switch to m1 in periodontal infection. Journal of Periodontology, 87 ( 9 ), 1092 â 1102. https://doi.org/10.1902/jop.2016.160081
dc.identifier.citedreferenceZhang, S., Barros, S. P., Moretti, A. J., Yu, N., Zhou, J., Preisser, J. S., â ¦ Offenbacher, S. ( 2013 ). Epigenetic regulation of tnfa expression in periodontal disease. Journal of Periodontology, 84 ( 11 ), 1606 â 1616.
dc.identifier.citedreferenceBerglundh, T., & Donati, M. ( 2005 ). Aspects of adaptive host response in periodontitis. Journal of Clinical Periodontology, 32 ( Suppl 6 ), 87 â 107. https://doi.org/10.1111/j.1600-051X.2005.00820.x
dc.identifier.citedreferenceCarcuac, O., & Berglundh, T. ( 2014 ). Composition of human periâ implantitis and periodontitis lesions. Journal of Dental Research, 93 ( 11 ), 1083 â 1088. https://doi.org/10.1177/0022034514551754
dc.identifier.citedreferenceChapple, C. C., Srivastava, M., & Hunter, N. ( 1998 ). Failure of macrophage activation in destructive periodontal disease. The Journal of Pathology, 186 ( 3 ), 281 â 286.
dc.identifier.citedreferenceDas, A., Sinha, M., Datta, S., Abas, M., Chaffee, S., Sen, C. K., & Roy, S. ( 2015 ). Monocyte and macrophage plasticity in tissue repair and regeneration. The American Journal of Pathology, 185 ( 10 ), 2596 â 2606.
dc.identifier.citedreferenceDi Paola, R., Mazzon, E., Maiere, D., Zito, D., Britti, D., De Majo, M., â ¦ Cuzzocrea, S. ( 2006 ). Rosiglitazone reduces the evolution of experimental periodontitis in the rat. Journal of Dental Research, 85 ( 2 ), 156 â 161. https://doi.org/10.1177/154405910608500208
dc.identifier.citedreferenceDivaris, K., Monda, K. L., North, K. E., Olshan, A. F., Reynolds, L. M., Hsueh, W.â C., â ¦ Offenbacher, S. ( 2013 ). Exploring the genetic basis of chronic periodontitis: A genomeâ wide association study. Human Molecular Genetics, 22 ( 11 ), 2312 â 2324. https://doi.org/10.1093/hmg/ddt065
dc.identifier.citedreferenceEke, P. I., Dye, B. A., Wei, L., Slade, G. D., Thorntonâ Evans, G. O., Borgnakke, W. S., â ¦ Genco, R. J. ( 2015 ). Update on prevalence of periodontitis in adults in the United States: Nhanes 2009 to 2012. Journal of Periodontology, 86 ( 5 ), 611 â 622. https://doi.org/10.1902/jop.2015.140520
dc.identifier.citedreferenceEke, P. I., Wei, L., Thorntonâ Evans, G. O., Borrell, L. N., Borgnakke, W. S., Dye, B., & Genco, R. J. ( 2016 ). Risk indicators for periodontitis in us adults: Nhanes 2009 to 2012. Journal of Periodontology, 87 ( 10 ), 1174 â 1185. https://doi.org/10.1902/jop.2016.160013
dc.identifier.citedreferenceGarlet, G. P., & Giannobile, W. V. ( 2018 ). Macrophages: The bridge between inflammation resolution and tissue repair? Journal of Dental Research, 97 ( 10 ), 1079 â 1081. https://doi.org/10.1177/0022034518785857
dc.identifier.citedreferenceGheren, L. W., Cortelli, J. R., Rodrigues, E., Holzhausen, M., & Saad, W. A. ( 2008 ). Periodontal therapy reduces arginase activity in saliva of patients with chronic periodontitis. Clinical Oral Investigations, 12 ( 1 ), 67 â 72. https://doi.org/10.1007/s00784-007-0146-8
dc.identifier.citedreferenceGorska, R., Gregorek, H., Kowalski, J., Laskusâ Perendyk, A., Syczewska, M., & Madalinski, K. ( 2003 ). Relationship between clinical parameters and cytokine profiles in inflamed gingival tissue and serum samples from patients with chronic periodontitis. Journal of Clinical Periodontology, 30 ( 12 ), 1046 â 1052. https://doi.org/10.1046/j.0303-6979.2003.00425.x
dc.identifier.citedreferenceGullu, C., Ozmeric, N., Tokman, B., Elgun, S., & Balos, K. ( 2005 ). Effectiveness of scaling and root planing versus modified widman flap on nitric oxide synthase and arginase activity in patients with chronic periodontitis. Journal of Periodontal Research, 40 ( 2 ), 168 â 175. https://doi.org/10.1111/j.1600-0765.2005.00784.x
dc.identifier.citedreferenceHassumi, M. Y., Silvaâ Filho, V. J., Camposâ Junior, J. C., Vieira, S. M., Cunha, F. Q., Alves, P. M., â ¦ Napimoga, M. H. ( 2009 ). Pparâ gamma agonist rosiglitazone prevents inflammatory periodontal bone loss by inhibiting osteoclastogenesis. International Immunopharmacology, 9 ( 10 ), 1150 â 1158.
dc.owningcollnameInterdisciplinary and Peer-Reviewed


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