The relationship between matrix metalloproteinases (MMP-3, -8, -9) in serum and peripheral lymphocytes (CD8+, CD56+) in Down syndrome children with gingivitis

Background and Objective Altered immune response may be a major contributor to periodontal disease in Down syndrome. This study investigated the relationship between peripheral lymphocytes and matrix metalloproteinases (MMPs) in serum in Down syndrome children with gingivitis. Material and Methods C...

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Vydané v:Journal of periodontal research Ročník 49; číslo 6; s. 742 - 750
Hlavní autori: Tsilingaridis, G., Yucel-Lindberg, T., Concha Quezada, H., Modéer, T.
Médium: Journal Article
Jazyk:English
Vydavateľské údaje: United States Blackwell Publishing Ltd 01.12.2014
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ISSN:0022-3484, 1600-0765, 1600-0765
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Abstract Background and Objective Altered immune response may be a major contributor to periodontal disease in Down syndrome. This study investigated the relationship between peripheral lymphocytes and matrix metalloproteinases (MMPs) in serum in Down syndrome children with gingivitis. Material and Methods Children with Down syndrome (n = 10) and healthy controls (n = 10) were clinically and radiographically examined during dental treatment under general anaesthesia. Peripheral blood and gingival crevicular fluid were collected from each subject and concentrations were determined: serum MMP‐2, ‐3, ‐8 and ‐9; serum tissue inhibitors of metalloproteinases (TIMP) ‐1, ‐2 and ‐3; and gingival crevicular fluid. Leukocytes were isolated from peripheral blood and the relative amounts (%) of the various cell phenotypes were analysed using flow cytometry. In addition, peripheral blood cells were treated with Porphyromonas gingivalis lipopolysaccharide and levels of MMPs and TIMPs measured. Results Concentrations of MMP‐3, MMP‐8 and TIMP‐1 in serum were significantly higher (p < 0.05) in the Down syndrome group compared to the controls. When peripheral blood leukocytes were cultured in the presence or absence of P. gingivalis lipopolysaccharide, MMP‐8 levels were significantly (p < 0.05) higher in the Down syndrome group compared to controls. Children with Down syndrome exhibited significant positive correlations between CD8+ T cells and MMP‐8 (r = 0.630; p = 0.050), between CD8+ T cells and MMP‐9 (r = 0.648; p = 0.043), and between CD56+ NK cells and MMP‐3 (r = 0.828; p = 0.003) compared to controls. Conclusions The positive relationship of serum MMP‐3, ‐8 and ‐9 with immune cells in children with Down syndrome may facilitate migration of CD8+ T cells and CD56+ NK cells into the periodontal tissue, which may contribute to the increased degradation of periodontal tissue in individuals with Down syndrome.
AbstractList Altered immune response may be a major contributor to periodontal disease in Down syndrome. This study investigated the relationship between peripheral lymphocytes and matrix metalloproteinases (MMPs) in serum in Down syndrome children with gingivitis.BACKGROUND AND OBJECTIVEAltered immune response may be a major contributor to periodontal disease in Down syndrome. This study investigated the relationship between peripheral lymphocytes and matrix metalloproteinases (MMPs) in serum in Down syndrome children with gingivitis.Children with Down syndrome (n = 10) and healthy controls (n = 10) were clinically and radiographically examined during dental treatment under general anaesthesia. Peripheral blood and gingival crevicular fluid were collected from each subject and concentrations were determined: serum MMP-2, -3, -8 and -9; serum tissue inhibitors of metalloproteinases (TIMP) -1, -2 and -3; and gingival crevicular fluid. Leukocytes were isolated from peripheral blood and the relative amounts (%) of the various cell phenotypes were analysed using flow cytometry. In addition, peripheral blood cells were treated with Porphyromonas gingivalis lipopolysaccharide and levels of MMPs and TIMPs measured.MATERIAL AND METHODSChildren with Down syndrome (n = 10) and healthy controls (n = 10) were clinically and radiographically examined during dental treatment under general anaesthesia. Peripheral blood and gingival crevicular fluid were collected from each subject and concentrations were determined: serum MMP-2, -3, -8 and -9; serum tissue inhibitors of metalloproteinases (TIMP) -1, -2 and -3; and gingival crevicular fluid. Leukocytes were isolated from peripheral blood and the relative amounts (%) of the various cell phenotypes were analysed using flow cytometry. In addition, peripheral blood cells were treated with Porphyromonas gingivalis lipopolysaccharide and levels of MMPs and TIMPs measured.Concentrations of MMP-3, MMP-8 and TIMP-1 in serum were significantly higher (p < 0.05) in the Down syndrome group compared to the controls. When peripheral blood leukocytes were cultured in the presence or absence of P. gingivalis lipopolysaccharide, MMP-8 levels were significantly (p < 0.05) higher in the Down syndrome group compared to controls. Children with Down syndrome exhibited significant positive correlations between CD8(+) T cells and MMP-8 (r = 0.630; p = 0.050), between CD8(+) T cells and MMP-9 (r = 0.648; p = 0.043), and between CD56(+) NK cells and MMP-3 (r = 0.828; p = 0.003) compared to controls.RESULTSConcentrations of MMP-3, MMP-8 and TIMP-1 in serum were significantly higher (p < 0.05) in the Down syndrome group compared to the controls. When peripheral blood leukocytes were cultured in the presence or absence of P. gingivalis lipopolysaccharide, MMP-8 levels were significantly (p < 0.05) higher in the Down syndrome group compared to controls. Children with Down syndrome exhibited significant positive correlations between CD8(+) T cells and MMP-8 (r = 0.630; p = 0.050), between CD8(+) T cells and MMP-9 (r = 0.648; p = 0.043), and between CD56(+) NK cells and MMP-3 (r = 0.828; p = 0.003) compared to controls.The positive relationship of serum MMP-3, -8 and -9 with immune cells in children with Down syndrome may facilitate migration of CD8(+) T cells and CD56(+) NK cells into the periodontal tissue, which may contribute to the increased degradation of periodontal tissue in individuals with Down syndrome.CONCLUSIONSThe positive relationship of serum MMP-3, -8 and -9 with immune cells in children with Down syndrome may facilitate migration of CD8(+) T cells and CD56(+) NK cells into the periodontal tissue, which may contribute to the increased degradation of periodontal tissue in individuals with Down syndrome.
Background and Objective Altered immune response may be a major contributor to periodontal disease in Down syndrome. This study investigated the relationship between peripheral lymphocytes and matrix metalloproteinases (MMPs) in serum in Down syndrome children with gingivitis. Material and Methods Children with Down syndrome (n = 10) and healthy controls (n = 10) were clinically and radiographically examined during dental treatment under general anaesthesia. Peripheral blood and gingival crevicular fluid were collected from each subject and concentrations were determined: serum MMP‐2, ‐3, ‐8 and ‐9; serum tissue inhibitors of metalloproteinases (TIMP) ‐1, ‐2 and ‐3; and gingival crevicular fluid. Leukocytes were isolated from peripheral blood and the relative amounts (%) of the various cell phenotypes were analysed using flow cytometry. In addition, peripheral blood cells were treated with Porphyromonas gingivalis lipopolysaccharide and levels of MMPs and TIMPs measured. Results Concentrations of MMP‐3, MMP‐8 and TIMP‐1 in serum were significantly higher (p < 0.05) in the Down syndrome group compared to the controls. When peripheral blood leukocytes were cultured in the presence or absence of P. gingivalis lipopolysaccharide, MMP‐8 levels were significantly (p < 0.05) higher in the Down syndrome group compared to controls. Children with Down syndrome exhibited significant positive correlations between CD8+ T cells and MMP‐8 (r = 0.630; p = 0.050), between CD8+ T cells and MMP‐9 (r = 0.648; p = 0.043), and between CD56+ NK cells and MMP‐3 (r = 0.828; p = 0.003) compared to controls. Conclusions The positive relationship of serum MMP‐3, ‐8 and ‐9 with immune cells in children with Down syndrome may facilitate migration of CD8+ T cells and CD56+ NK cells into the periodontal tissue, which may contribute to the increased degradation of periodontal tissue in individuals with Down syndrome.
Altered immune response may be a major contributor to periodontal disease in Down syndrome. This study investigated the relationship between peripheral lymphocytes and matrix metalloproteinases (MMPs) in serum in Down syndrome children with gingivitis. Children with Down syndrome (n = 10) and healthy controls (n = 10) were clinically and radiographically examined during dental treatment under general anaesthesia. Peripheral blood and gingival crevicular fluid were collected from each subject and concentrations were determined: serum MMP-2, -3, -8 and -9; serum tissue inhibitors of metalloproteinases (TIMP) -1, -2 and -3; and gingival crevicular fluid. Leukocytes were isolated from peripheral blood and the relative amounts (%) of the various cell phenotypes were analysed using flow cytometry. In addition, peripheral blood cells were treated with Porphyromonas gingivalis lipopolysaccharide and levels of MMPs and TIMPs measured. Concentrations of MMP-3, MMP-8 and TIMP-1 in serum were significantly higher (p<0.05) in the Down syndrome group compared to the controls. When peripheral blood leukocytes were cultured in the presence or absence of P. gingivalis lipopolysaccharide, MMP-8 levels were significantly (p<0.05) higher in the Down syndrome group compared to controls. Children with Down syndrome exhibited significant positive correlations between CD8+ T cells and MMP-8 (r = 0.630; p=0.050), between CD8+ T cells and MMP-9 (r = 0.648; p=0.043), and between CD56+NK cells and MMP-3 (r = 0.828; p =0.003) compared to controls. The positive relationship of serum MMP-3, -8 and -9 with immune cells in children with Down syndrome may facilitate migration of CD8+ T cells and CD56+NK cells into the periodontal tissue, which may contribute to the increased degradation of periodontal tissue in individuals with Down syndrome.
Altered immune response may be a major contributor to periodontal disease in Down syndrome. This study investigated the relationship between peripheral lymphocytes and matrix metalloproteinases (MMPs) in serum in Down syndrome children with gingivitis. Children with Down syndrome (n = 10) and healthy controls (n = 10) were clinically and radiographically examined during dental treatment under general anaesthesia. Peripheral blood and gingival crevicular fluid were collected from each subject and concentrations were determined: serum MMP-2, -3, -8 and -9; serum tissue inhibitors of metalloproteinases (TIMP) -1, -2 and -3; and gingival crevicular fluid. Leukocytes were isolated from peripheral blood and the relative amounts (%) of the various cell phenotypes were analysed using flow cytometry. In addition, peripheral blood cells were treated with Porphyromonas gingivalis lipopolysaccharide and levels of MMPs and TIMPs measured. Concentrations of MMP-3, MMP-8 and TIMP-1 in serum were significantly higher (p < 0.05) in the Down syndrome group compared to the controls. When peripheral blood leukocytes were cultured in the presence or absence of P. gingivalis lipopolysaccharide, MMP-8 levels were significantly (p < 0.05) higher in the Down syndrome group compared to controls. Children with Down syndrome exhibited significant positive correlations between CD8(+) T cells and MMP-8 (r = 0.630; p = 0.050), between CD8(+) T cells and MMP-9 (r = 0.648; p = 0.043), and between CD56(+) NK cells and MMP-3 (r = 0.828; p = 0.003) compared to controls. The positive relationship of serum MMP-3, -8 and -9 with immune cells in children with Down syndrome may facilitate migration of CD8(+) T cells and CD56(+) NK cells into the periodontal tissue, which may contribute to the increased degradation of periodontal tissue in individuals with Down syndrome.
Author Concha Quezada, H.
Yucel-Lindberg, T.
Modéer, T.
Tsilingaridis, G.
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Keywords crevicular fluid
Down syndrome
T cells
serum
matrix metalloproteinases
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Pueschel SM, Anneren G, Durlach R, Flores J, Sustrova M, Verma IC. Guidelines for optimal medical care of persons with Down syndrome. International League of Societies for Persons with Mental Handicap (ILSMH). Acta Paediatr 1995;84:823-827.
Page RC, Schroeder HE. Pathogenesis of inflammatory periodontal disease. A summary of current work. Lab Invest 1976;34:235-249.
Cossarizza A, Monti D, Montagnani G et al. Precocious aging of the immune system in Down syndrome: alteration of B lymphocytes, T-lymphocyte subsets, and cells with natural killer markers. Am J Med Genet Suppl 1990;7:213-218.
Baker AH, Edwards DR, Murphy G. Metalloproteinase inhibitors: biological actions and therapeutic opportunities. J Cell Sci 2002;115:3719-3727.
Kinane DF, Johnston FA, Evans CW. Depressed helper-to-suppressor T-cell ratios in early-onset forms of periodontal disease. J Periodontal Res 1989;24:161-164.
Colombo ML, Girardo E, Saitta M, Ricci BM, Maina D. [The immunological profile of children with Down's syndrome]. Minerva Pediatr 1989;41:1-4.
Nespoli L, Burgio GR, Ugazio AG, Maccario R. Immunological features of Down's syndrome: a review. J Intellect Disabil Res 1993;6:543-551.
Zeng L, An S, Goetzl EJ. Selective regulation of RNK-16 cell matrix metalloproteinases by the EP4 subtype of prostaglandin E2 receptor. Biochemistry 1996;35:7159-7164.
Pussinen PJ, Sarna S, Puolakkainen M, Ohlin H, Sorsa T, Pesonen E. The balance of serum matrix metalloproteinase-8 and its tissue inhibitor in acute coronary syndrome and its recurrence. Int J Cardiol 2013;167:362-368.
Seguier S, Godeau G, Brousse N. Collagen fibers and inflammatory cells in healthy and diseased human gingival tissues: a comparative and quantitative study by immunohistochemistry and automated image analysis. J Periodontol 2000;71:1079-1085.
Lejeune J, Turpin R, Gautier M. [Mongolism; a chromosomal disease (trisomy)]. Bull Acad Natl Med 1959;143:256-265.
Domeij H, Yucel-Lindberg T, Modeer T. Signal pathways involved in the production of MMP-1 and MMP-3 in human gingival fibroblasts. Eur J Oral Sci 2002;110:302-306.
Kawai T, Eisen-Lev R, Seki M, Eastcott JW, Wilson ME, Taubman MA. Requirement of B7 costimulation for Th1-mediated inflammatory bone resorption in experimental periodontal disease. J Immunol 2000;164:2102-2109.
Chaves ES, Wood RC, Jones AA, Newbold DA, Manwell MA, Kornman KS. Relationship of "bleeding on probing" and "gingival index bleeding" as clinical parameters of gingival inflammation. J Clin Periodontol 1993;20:139-143.
Halinen S, Sorsa T, Ding Y et al. Characterization of matrix metalloproteinase (MMP-8 and -9) activities in the saliva and in gingival crevicular fluid of children with Down's syndrome. J Periodontol 1996;67:748-754.
Verstappen J, Von den Hoff JW. Tissue inhibitors of metalloproteinases (TIMPs): their biological functions and involvement in oral disease. J Dent Res 2006;85:1074-1084.
Johnatty RN, Taub DD, Reeder SP et al. Cytokine and chemokine regulation of proMMP-9 and TIMP-1 production by human peripheral blood lymphocytes. J Immunol 1997;158:2327-2333.
Zhou H, Bernhard EJ, Fox FE, Billings PC. Induction of metalloproteinase activity in human T-lymphocytes. Biochim Biophys Acta 1993;1177:174-178.
Kallestal C, Matsson L. Criteria for assessment of interproximal bone loss on bite-wing radiographs in adolescents. J Clin Periodontol 1989;16:300-304.
Barkin RM, Weston WL, Humbert JR, Sunada K. Phagocytic function in Down syndrome - II. Bactericidal activity and phagocytosis. J Ment Defic Res 1980;4:251-256.
Mazzoni A, Mannello F, Tay FR et al. Zymographic analysis and characterization of MMP-2 and -9 forms in human sound dentin. J Dent Res 2007;86:436-440.
Barr-Agholme M, Krekmanova L, Yucel-Lindberg T, Shinoda K, Modeer T. Prostaglandin E2 level in gingival crevicular fluid from patients with Down syndrome. Acta Odontol Scand 1997;55:101-105.
Sorsa T, Tervahartiala T, Leppilahti J et al. Collagenase-2 (MMP-8) as a point-of-care biomarker in periodontitis and cardiovascular diseases. Therapeutic response to non-antimicrobial properties of tetracyclines. Pharmacol Res 2011;63:108-113.
Barkin RM, Weston WL, Humbert JR, Maire F. Phagocytic function in Down syndrome - I. Chemotaxis. J Ment Defic Res 1980;4:243-249.
Ugazio AG, Maccario R, Notarangelo LD, Burgio GR. Immunology of Down syndrome: a review. Am J Med Genet Suppl 1990;7:204-212.
Licastro F, Mariani RA, Faldella G et al. Immune-endocrine status and coeliac disease in children with Down's syndrome: relationships with zinc and cognitive efficiency. Brain Res Bull 2001;55:313-317.
Hannas AR, Pereira JC, Granjeiro JM, Tjaderhane L. The role of matrix metalloproteinases in the oral environment. Acta Odontol Scand 2007;65:1-13.
Goetzl EJ, Banda MJ, Leppert D. Matrix metalloproteinases in immunity. J Immunol 1996;156:1-4.
Sakellari D, Arapostathis KN, Konstantinidis A. Periodontal conditions and subgingival microflora in Down syndrome patients. A case-control study. J Clin Periodontol 2005;32:684-690.
Mosmann TR, Kobie JJ, Lee FE, Quataert SA. T helper cytokine patterns: defined subsets, random expression, and external modulation. Immunol Res 2009;45:173-184.
Seguier S, Gogly B, Bodineau A, Godeau G, Brousse N. Is collagen breakdown during periodontitis linked to inflammatory cells and expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases in human gingival tissue? J Periodontol 2001;72:1398-1406.
Tsilingaridis G, Yucel-Lindberg T, Modeer T. Altered relationship between MMP-8 and TIMP-2 in gingival crevicular fluid in adolescents with Down's syndrome. J Periodontal Res 2013;48:553-562.
Yamazaki-Kubota T, Miyamoto M, Sano Y et al. Analysis of matrix metalloproteinase (MMP-8 and MMP-2) activity in gingival crevicular fluid from children with Down's syndrome. J Periodontal Res 2010;45:170-176.
Levin S. The immune system and susceptibility to infections in Down's syndrome. Prog Clin Biol Res 1987;246:143-162.
Korn T, Bettelli E, Oukka M, Kuchroo VK. IL-17 and Th17 Cells. Annu Rev Immunol 2009;27:485-517.
Weeks BS. The role of HIV-1 activated leukocyte adhesion mechanisms and matrix metalloproteinase secretion in AIDS pathogenesis (Review). Int J Mol Med 1998;1:361-366.
Reuland-Bosma W, van Dijk J. Periodontal disease in Down's syndrome: a review. J Clin Periodontol 1986;13:64-73.
Sorsa T, Tjaderhane L, Konttinen YT et al. Matrix metalloproteinases: contribution to pathogenesis, diagnosis and treatment of periodontal inflammation. Ann Med 2006;38:306-321.
Karttunen R, Nurmi T, Ilonen J, Surcel HM. Cell-mediated immunodeficiency in Down's syndrome: normal IL-2 production but inverted ratio of T cell subsets. Clin Exp Immunol 1984;55:257-263.
Nagase H, Visse R, Murphy G. Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc Res 2006;69:562-573.
Leppert D, Hauser SL, Kishiyama JL, An S, Zeng L, Goetzl EJ. Stimulation of matrix metalloproteinase-dependent migration of T cells by eicosanoids. FASEB J 1995;9:1473-1481.
Restaino CG, Chaparro A, Valenzuela MA et al. Stimulatory response of neutrophils from periodontitis patients with periodontal pathogens. Oral Dis 2007;13:474-481.
Xia M, Leppert D, Hauser SL et al. Stimulus specificity of matrix metalloproteinase dependence of human T cell migration through a model basement membrane. J Immunol 1996;156:160-167.
Modeer T, Barr M, Dahllof G. Periodontal disease in children with Down's syndrome. Scand J Dent Res 1990;98:228-234.
Murphy M, Lempert MJ, Epstein LB. Decreased level of T cell receptor expression by Down syndrome (trisomy 21) thymocytes. Am J Med Genet Suppl 1990;7:234-237.
de Hingh YC, van der Vossen PW, Gemen EF et al. Intrinsic abnormalities of lymphocyte counts in children with Down syndrome. J Pediatr 2005;147:744-747.
Reynolds JJ, Meikle MC. Mechanisms of connective tissue matrix destruction in periodontitis. Periodontol 2000 1997;14:144-157.
Reeves AF, Rees JM, Schiff M, Hujoel P. Total body weight and waist circumference associated with chronic periodontitis among adolescents in the United States. Arch Pediatr Adolesc Med 2006;160:894-899.
Barnett ML, Press KP, Friedman D, Sonnenberg EM. The prevalence of periodontitis
2009; 45
1989; 41
1997; 158
1990; 98
2002; 110
2006; 38
1993; 20
2013; 167
2002; 115
2012; 16
1996; 35
1996; 103
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1992; 7
1976; 34
2003; 92
1997; 55
2005; 147
1984; 55
1997; 14
2006; 69
2011; 64
2011; 63
2005; 32
2000; 164
2006; 160
2001; 55
2008; 112
2007; 65
1998; 10
1996; 67
1995; 9
2001; 72
2013; 48
2010; 37
1959; 143
1987; 246
1986; 13
1986; 57
1992; 149
1993; 1177
2000; 71
1989; 24
2009; 27
2007; 13
2010; 45
1995; 84
2006; 85
1980; 4
1998; 1
2007; 86
2003; 61
1993; 157
1989; 16
1996; 156
1990; 7
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References_xml – reference: Cossarizza A, Monti D, Montagnani G et al. Precocious aging of the immune system in Down syndrome: alteration of B lymphocytes, T-lymphocyte subsets, and cells with natural killer markers. Am J Med Genet Suppl 1990;7:213-218.
– reference: Yamazaki-Kubota T, Miyamoto M, Sano Y et al. Analysis of matrix metalloproteinase (MMP-8 and MMP-2) activity in gingival crevicular fluid from children with Down's syndrome. J Periodontal Res 2010;45:170-176.
– reference: Sorsa T, Tervahartiala T, Leppilahti J et al. Collagenase-2 (MMP-8) as a point-of-care biomarker in periodontitis and cardiovascular diseases. Therapeutic response to non-antimicrobial properties of tetracyclines. Pharmacol Res 2011;63:108-113.
– reference: Murphy M, Friend DS, Pike-Nobile L, Epstein LB. Tumor necrosis factor-alpha and IFN-gamma expression in human thymus. Localization and overexpression in Down syndrome (trisomy 21). J Immunol 1992;149:2506-2512.
– reference: Reynolds JJ, Meikle MC. Mechanisms of connective tissue matrix destruction in periodontitis. Periodontol 2000 1997;14:144-157.
– reference: Zeng L, An S, Goetzl EJ. Selective regulation of RNK-16 cell matrix metalloproteinases by the EP4 subtype of prostaglandin E2 receptor. Biochemistry 1996;35:7159-7164.
– reference: Tsilingaridis G, Yucel-Lindberg T, Modeer T. T-helper-related cytokines in gingival crevicular fluid from adolescents with Down syndrome. Clin Oral Investig 2012;16:267-273.
– reference: Nagase H, Visse R, Murphy G. Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc Res 2006;69:562-573.
– reference: Barnett ML, Press KP, Friedman D, Sonnenberg EM. The prevalence of periodontitis and dental caries in a Down's syndrome population. J Periodontol 1986;57:288-293.
– reference: Pussinen PJ, Sarna S, Puolakkainen M, Ohlin H, Sorsa T, Pesonen E. The balance of serum matrix metalloproteinase-8 and its tissue inhibitor in acute coronary syndrome and its recurrence. Int J Cardiol 2013;167:362-368.
– reference: Nespoli L, Burgio GR, Ugazio AG, Maccario R. Immunological features of Down's syndrome: a review. J Intellect Disabil Res 1993;6:543-551.
– reference: Barkin RM, Weston WL, Humbert JR, Maire F. Phagocytic function in Down syndrome - I. Chemotaxis. J Ment Defic Res 1980;4:243-249.
– reference: Mosmann TR, Kobie JJ, Lee FE, Quataert SA. T helper cytokine patterns: defined subsets, random expression, and external modulation. Immunol Res 2009;45:173-184.
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– reference: Levin S. The immune system and susceptibility to infections in Down's syndrome. Prog Clin Biol Res 1987;246:143-162.
– reference: Mazzoni A, Mannello F, Tay FR et al. Zymographic analysis and characterization of MMP-2 and -9 forms in human sound dentin. J Dent Res 2007;86:436-440.
– reference: Lejeune J, Turpin R, Gautier M. [Mongolism; a chromosomal disease (trisomy)]. Bull Acad Natl Med 1959;143:256-265.
– reference: Weeks BS. The role of HIV-1 activated leukocyte adhesion mechanisms and matrix metalloproteinase secretion in AIDS pathogenesis (Review). Int J Mol Med 1998;1:361-366.
– reference: Weeks BS, Schnaper HW, Handy M, Holloway E, Kleinman HK. Human T lymphocytes synthesize the 92 kDa type IV collagenase (gelatinase B). J Cell Physiol 1993;157:644-649.
– reference: Verstappen J, Von den Hoff JW. Tissue inhibitors of metalloproteinases (TIMPs): their biological functions and involvement in oral disease. J Dent Res 2006;85:1074-1084.
– reference: Kawai T, Eisen-Lev R, Seki M, Eastcott JW, Wilson ME, Taubman MA. Requirement of B7 costimulation for Th1-mediated inflammatory bone resorption in experimental periodontal disease. J Immunol 2000;164:2102-2109.
– reference: de Hingh YC, van der Vossen PW, Gemen EF et al. Intrinsic abnormalities of lymphocyte counts in children with Down syndrome. J Pediatr 2005;147:744-747.
– reference: Seguier S, Gogly B, Bodineau A, Godeau G, Brousse N. Is collagen breakdown during periodontitis linked to inflammatory cells and expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases in human gingival tissue? J Periodontol 2001;72:1398-1406.
– reference: Ugazio AG, Maccario R, Notarangelo LD, Burgio GR. Immunology of Down syndrome: a review. Am J Med Genet Suppl 1990;7:204-212.
– reference: Lauhio A, Hastbacka J, Pettila V et al. Serum MMP-8, -9 and TIMP-1 in sepsis: high serum levels of MMP-8 and TIMP-1 are associated with fatal outcome in a multicentre, prospective cohort study. Hypothetical impact of tetracyclines. Pharmacol Res 2011;64:590-594.
– reference: Kinane DF, Johnston FA, Evans CW. Depressed helper-to-suppressor T-cell ratios in early-onset forms of periodontal disease. J Periodontal Res 1989;24:161-164.
– reference: Pueschel SM, Anneren G, Durlach R, Flores J, Sustrova M, Verma IC. Guidelines for optimal medical care of persons with Down syndrome. International League of Societies for Persons with Mental Handicap (ILSMH). Acta Paediatr 1995;84:823-827.
– reference: Sakellari D, Arapostathis KN, Konstantinidis A. Periodontal conditions and subgingival microflora in Down syndrome patients. A case-control study. J Clin Periodontol 2005;32:684-690.
– reference: Halinen S, Sorsa T, Ding Y et al. Characterization of matrix metalloproteinase (MMP-8 and -9) activities in the saliva and in gingival crevicular fluid of children with Down's syndrome. J Periodontol 1996;67:748-754.
– reference: Hannas AR, Pereira JC, Granjeiro JM, Tjaderhane L. The role of matrix metalloproteinases in the oral environment. Acta Odontol Scand 2007;65:1-13.
– reference: Baker AH, Edwards DR, Murphy G. Metalloproteinase inhibitors: biological actions and therapeutic opportunities. J Cell Sci 2002;115:3719-3727.
– reference: Xia M, Leppert D, Hauser SL et al. Stimulus specificity of matrix metalloproteinase dependence of human T cell migration through a model basement membrane. J Immunol 1996;156:160-167.
– reference: Barr-Agholme M, Krekmanova L, Yucel-Lindberg T, Shinoda K, Modeer T. Prostaglandin E2 level in gingival crevicular fluid from patients with Down syndrome. Acta Odontol Scand 1997;55:101-105.
– reference: Goetzl EJ, Banda MJ, Leppert D. Matrix metalloproteinases in immunity. J Immunol 1996;156:1-4.
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– reference: Kallestal C, Matsson L. Criteria for assessment of interproximal bone loss on bite-wing radiographs in adolescents. J Clin Periodontol 1989;16:300-304.
– reference: Colombo ML, Girardo E, Saitta M, Ricci BM, Maina D. [The immunological profile of children with Down's syndrome]. Minerva Pediatr 1989;41:1-4.
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– reference: Reeves AF, Rees JM, Schiff M, Hujoel P. Total body weight and waist circumference associated with chronic periodontitis among adolescents in the United States. Arch Pediatr Adolesc Med 2006;160:894-899.
– reference: Leppert D, Hauser SL, Kishiyama JL, An S, Zeng L, Goetzl EJ. Stimulation of matrix metalloproteinase-dependent migration of T cells by eicosanoids. FASEB J 1995;9:1473-1481.
– reference: Domeij H, Yucel-Lindberg T, Modeer T. Signal pathways involved in the production of MMP-1 and MMP-3 in human gingival fibroblasts. Eur J Oral Sci 2002;110:302-306.
– reference: Page RC, Schroeder HE. Pathogenesis of inflammatory periodontal disease. A summary of current work. Lab Invest 1976;34:235-249.
– reference: Licastro F, Mariani RA, Faldella G et al. Immune-endocrine status and coeliac disease in children with Down's syndrome: relationships with zinc and cognitive efficiency. Brain Res Bull 2001;55:313-317.
– reference: Shresta S, Pham CT, Thomas DA, Graubert TA, Ley TJ. How do cytotoxic lymphocytes kill their targets? Curr Opin Immunol 1998;10:581-587.
– reference: Sorsa T, Tjaderhane L, Konttinen YT et al. Matrix metalloproteinases: contribution to pathogenesis, diagnosis and treatment of periodontal inflammation. Ann Med 2006;38:306-321.
– reference: Barr-Agholme M, Dahllof G, Linder L, Modeer T. Actinobacillus actinomycetemcomitans, Capnocytophaga and Porphyromonas gingivalis in subgingival plaque of adolescents with Down's syndrome. Oral Microbiol Immunol 1992;7:244-248.
– reference: Barkin RM, Weston WL, Humbert JR, Sunada K. Phagocytic function in Down syndrome - II. Bactericidal activity and phagocytosis. J Ment Defic Res 1980;4:251-256.
– reference: Tsilingaridis G, Yucel-Lindberg T, Modeer T. Altered relationship between MMP-8 and TIMP-2 in gingival crevicular fluid in adolescents with Down's syndrome. J Periodontal Res 2013;48:553-562.
– reference: Karttunen R, Nurmi T, Ilonen J, Surcel HM. Cell-mediated immunodeficiency in Down's syndrome: normal IL-2 production but inverted ratio of T cell subsets. Clin Exp Immunol 1984;55:257-263.
– reference: Tsilingaridis G, Yucel-Lindberg T, Modeer T. Enhanced levels of prostaglandin E2, leukotriene B4, and matrix metalloproteinase-9 in gingival crevicular fluid from patients with Down syndrome. Acta Odontol Scand 2003;61:154-158.
– reference: Modeer T, Barr M, Dahllof G. Periodontal disease in children with Down's syndrome. Scand J Dent Res 1990;98:228-234.
– reference: Restaino CG, Chaparro A, Valenzuela MA et al. Stimulatory response of neutrophils from periodontitis patients with periodontal pathogens. Oral Dis 2007;13:474-481.
– reference: Johnatty RN, Taub DD, Reeder SP et al. Cytokine and chemokine regulation of proMMP-9 and TIMP-1 production by human peripheral blood lymphocytes. J Immunol 1997;158:2327-2333.
– reference: Seguier S, Godeau G, Brousse N. Collagen fibers and inflammatory cells in healthy and diseased human gingival tissues: a comparative and quantitative study by immunohistochemistry and automated image analysis. J Periodontol 2000;71:1079-1085.
– reference: Reuland-Bosma W, van Dijk J. Periodontal disease in Down's syndrome: a review. J Clin Periodontol 1986;13:64-73.
– reference: Murphy M, Lempert MJ, Epstein LB. Decreased level of T cell receptor expression by Down syndrome (trisomy 21) thymocytes. Am J Med Genet Suppl 1990;7:234-237.
– reference: Zhou H, Bernhard EJ, Fox FE, Billings PC. Induction of metalloproteinase activity in human T-lymphocytes. Biochim Biophys Acta 1993;1177:174-178.
– volume: 45
  start-page: 173
  year: 2009
  end-page: 184
  article-title: T helper cytokine patterns: defined subsets, random expression, and external modulation
  publication-title: Immunol Res
– volume: 64
  start-page: 590
  year: 2011
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  article-title: Serum MMP‐8, ‐9 and TIMP‐1 in sepsis: high serum levels of MMP‐8 and TIMP‐1 are associated with fatal outcome in a multicentre, prospective cohort study. Hypothetical impact of tetracyclines
  publication-title: Pharmacol Res
– volume: 65
  start-page: 1
  year: 2007
  end-page: 13
  article-title: The role of matrix metalloproteinases in the oral environment
  publication-title: Acta Odontol Scand
– volume: 72
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  year: 2001
  end-page: 1406
  article-title: Is collagen breakdown during periodontitis linked to inflammatory cells and expression of matrix metalloproteinases and tissue inhibitors of metalloproteinases in human gingival tissue?
  publication-title: J Periodontol
– volume: 85
  start-page: 1074
  year: 2006
  end-page: 1084
  article-title: Tissue inhibitors of metalloproteinases (TIMPs): their biological functions and involvement in oral disease
  publication-title: J Dent Res
– volume: 156
  start-page: 160
  year: 1996
  end-page: 167
  article-title: Stimulus specificity of matrix metalloproteinase dependence of human T cell migration through a model basement membrane
  publication-title: J Immunol
– volume: 86
  start-page: 436
  year: 2007
  end-page: 440
  article-title: Zymographic analysis and characterization of MMP‐2 and ‐9 forms in human sound dentin
  publication-title: J Dent Res
– volume: 98
  start-page: 228
  year: 1990
  end-page: 234
  article-title: Periodontal disease in children with Down's syndrome
  publication-title: Scand J Dent Res
– volume: 157
  start-page: 644
  year: 1993
  end-page: 649
  article-title: Human T lymphocytes synthesize the 92 kDa type IV collagenase (gelatinase B)
  publication-title: J Cell Physiol
– volume: 55
  start-page: 101
  year: 1997
  end-page: 105
  article-title: Prostaglandin E2 level in gingival crevicular fluid from patients with Down syndrome
  publication-title: Acta Odontol Scand
– volume: 10
  start-page: 581
  year: 1998
  end-page: 587
  article-title: How do cytotoxic lymphocytes kill their targets?
  publication-title: Curr Opin Immunol
– volume: 84
  start-page: 823
  year: 1995
  end-page: 827
  article-title: Guidelines for optimal medical care of persons with Down syndrome. International League of Societies for Persons with Mental Handicap (ILSMH)
  publication-title: Acta Paediatr
– volume: 55
  start-page: 257
  year: 1984
  end-page: 263
  article-title: Cell‐mediated immunodeficiency in Down's syndrome: normal IL‐2 production but inverted ratio of T cell subsets
  publication-title: Clin Exp Immunol
– volume: 13
  start-page: 474
  year: 2007
  end-page: 481
  article-title: Stimulatory response of neutrophils from periodontitis patients with periodontal pathogens
  publication-title: Oral Dis
– volume: 6
  start-page: 543
  year: 1993
  end-page: 551
  article-title: Immunological features of Down's syndrome: a review
  publication-title: J Intellect Disabil Res
– volume: 110
  start-page: 302
  year: 2002
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Snippet Background and Objective Altered immune response may be a major contributor to periodontal disease in Down syndrome. This study investigated the relationship...
Altered immune response may be a major contributor to periodontal disease in Down syndrome. This study investigated the relationship between peripheral...
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SubjectTerms Adolescent
CD56 Antigen - analysis
CD8 Antigens - analysis
CD8-Positive T-Lymphocytes - immunology
Child
crevicular fluid
Cross-Sectional Studies
Down syndrome
Down Syndrome - blood
Down Syndrome - enzymology
Down Syndrome - immunology
Female
Gingival Crevicular Fluid - enzymology
Gingival Crevicular Fluid - immunology
Gingivitis - blood
Gingivitis - enzymology
Gingivitis - immunology
Humans
Killer Cells, Natural - immunology
Lipopolysaccharides - pharmacology
Male
Matrix Metalloproteinase 3 - blood
Matrix Metalloproteinase 8 - blood
Matrix Metalloproteinase 9 - blood
matrix metalloproteinases
Pilot Projects
Porphyromonas gingivalis
serum
T cells
Tissue Inhibitor of Metalloproteinase-1 - blood
Tissue Inhibitor of Metalloproteinase-2 - blood
Tissue Inhibitor of Metalloproteinase-3 - blood
Young Adult
Title The relationship between matrix metalloproteinases (MMP-3, -8, -9) in serum and peripheral lymphocytes (CD8+, CD56+) in Down syndrome children with gingivitis
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https://www.ncbi.nlm.nih.gov/pubmed/24372339
https://www.proquest.com/docview/1622064132
https://www.proquest.com/docview/1654684570
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Volume 49
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