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Published in: BMC Oral Health 1/2015

Open Access 01-12-2015 | Research article

Periodontal CD14 mRNA expression is downregulated in patients with chronic periodontitis and type 2 diabetes

Authors: Dustin C. Hedgpeth, Xiaoming Zhang, Junfei Jin, Renata S. Leite, Joe W. Krayer, Yan Huang

Published in: BMC Oral Health | Issue 1/2015

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Abstract

Background

Patients with type 2 diabetes mellitus (T2DM) have increased severity of periodontitis. Toll-like receptor (TLR)4, its co-receptors CD14 and MD-2, and adaptor MyD88 play pivotal roles in lipopolysaccharide (LPS)-triggered tissue inflammation and periodontitis. This study investigated the effects of T2DM and periodontitis on TLR4, CD14, MD-2 and MyD88 mRNA expression in surgically removed periodontal tissues.

Methods

Periodontal tissue specimens were collected from 14 patients without periodontitis and T2DM (Group 1), 15 patients with periodontitis alone (Group 2), and 7 patients with both periodontitis and T2DM (Group 3). The mRNA of TLR4, CD14, MD-2 and MyD88 was quantified using real-time PCR and compared between the groups.

Results

Statistical analysis showed that periodontal expression of CD14 mRNA was significantly reduced across Groups 1, 2 and 3 (p = 0.02) whereas the mRNA expression of TLR4, MD-2 and MyD88 was not significantly different among the groups. Furthermore, when patients in Groups 1 and 2 were combined (n = 22), the CD14 mRNA expression was significantly lower than that in patients of Group 1 (p = 0.04).

Conclusions

CD14 mRNA expression was downregulated across patients with neither periodontitis nor T2DM, patients with periodontitis alone and patients with both diseases, suggesting that CD14 mRNA expression is associated with a favorable host response or subjected to a negative feedback regulation.
Literature
1.
go back to reference Page RC. The pathobiology of periodontal diseases may affect systemic diseases: inversion of a paradigm. Ann Periodontol. 1998;3(1):108–20.PubMedCrossRef Page RC. The pathobiology of periodontal diseases may affect systemic diseases: inversion of a paradigm. Ann Periodontol. 1998;3(1):108–20.PubMedCrossRef
2.
go back to reference Page RC, Offenbacher S, Schroeder HE, Seymour GJ, Kornman KS. Advances in the pathogenesis of periodontitis: summary of developments, clinical implications and future directions. Periodontol 2000. 1997;14:216–48.PubMedCrossRef Page RC, Offenbacher S, Schroeder HE, Seymour GJ, Kornman KS. Advances in the pathogenesis of periodontitis: summary of developments, clinical implications and future directions. Periodontol 2000. 1997;14:216–48.PubMedCrossRef
3.
go back to reference Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C, Du X, et al. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science. 1998;282(5396):2085–8.PubMedCrossRef Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C, Du X, et al. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science. 1998;282(5396):2085–8.PubMedCrossRef
4.
go back to reference Gu Y, Lee HM, Sorsa T, Salminen A, Ryan ME, Slepian MJ, et al. Non-antibacterial tetracyclines modulate mediators of periodontitis and atherosclerotic cardiovascular disease: a mechanistic link between local and systemic inflammation. Pharmacol Res. 2011;64(6):573–9.PubMedCrossRef Gu Y, Lee HM, Sorsa T, Salminen A, Ryan ME, Slepian MJ, et al. Non-antibacterial tetracyclines modulate mediators of periodontitis and atherosclerotic cardiovascular disease: a mechanistic link between local and systemic inflammation. Pharmacol Res. 2011;64(6):573–9.PubMedCrossRef
5.
go back to reference Peri F, Piazza M. Therapeutic targeting of innate immunity with Toll-like receptor 4 (TLR4) antagonists. Biotechnol Adv. 2012;30(1):251–60.PubMedCrossRef Peri F, Piazza M. Therapeutic targeting of innate immunity with Toll-like receptor 4 (TLR4) antagonists. Biotechnol Adv. 2012;30(1):251–60.PubMedCrossRef
6.
go back to reference Stoll LL, Denning GM, Weintraub NL. Endotoxin, TLR4 signaling and vascular inflammation: potential therapeutic targets in cardiovascular disease. Curr Pharm Des. 2006;12(32):4229–45.PubMedCrossRef Stoll LL, Denning GM, Weintraub NL. Endotoxin, TLR4 signaling and vascular inflammation: potential therapeutic targets in cardiovascular disease. Curr Pharm Des. 2006;12(32):4229–45.PubMedCrossRef
7.
go back to reference Christiansen D, Brekke OL, Stenvik J, Lambris JD, Espevik T, Mollnes TE. Differential effect of inhibiting MD-2 and CD14 on LPS- versus whole E. coli bacteria-induced cytokine responses in human blood. Adv Exp Med Biol. 2012;946:237–51.PubMedCrossRef Christiansen D, Brekke OL, Stenvik J, Lambris JD, Espevik T, Mollnes TE. Differential effect of inhibiting MD-2 and CD14 on LPS- versus whole E. coli bacteria-induced cytokine responses in human blood. Adv Exp Med Biol. 2012;946:237–51.PubMedCrossRef
8.
go back to reference O'Neill LA, Dunne A, Edjeback M, Gray P, Jefferies C, Wietek C. Mal and MyD88: adapter proteins involved in signal transduction by Toll-like receptors. J Endotoxin Res. 2003;9(1):55–9.PubMedCrossRef O'Neill LA, Dunne A, Edjeback M, Gray P, Jefferies C, Wietek C. Mal and MyD88: adapter proteins involved in signal transduction by Toll-like receptors. J Endotoxin Res. 2003;9(1):55–9.PubMedCrossRef
9.
go back to reference Preshaw PM, Alba AL, Herrera D, Jepsen S, Konstantinidis A, Makrilakis K, et al. Periodontitis and diabetes: a two-way relationship. Diabetologia. 2012;55(1):21–31.PubMedCrossRef Preshaw PM, Alba AL, Herrera D, Jepsen S, Konstantinidis A, Makrilakis K, et al. Periodontitis and diabetes: a two-way relationship. Diabetologia. 2012;55(1):21–31.PubMedCrossRef
10.
go back to reference Lalla E, Papapanou PN. Diabetes mellitus and periodontitis: a tale of two common interrelated diseases. Nat Rev Endocrinol. 2011;7(12):738–48.PubMedCrossRef Lalla E, Papapanou PN. Diabetes mellitus and periodontitis: a tale of two common interrelated diseases. Nat Rev Endocrinol. 2011;7(12):738–48.PubMedCrossRef
11.
go back to reference Lalla E, Lamster IB, Drury S, Fu C, Schmidt AM. Hyperglycemia, glycoxidation and receptor for advanced glycation endproducts: potential mechanisms underlying diabetic complications, including diabetes-associated periodontitis. Periodontol 2000. 2000;23:50–62.PubMedCrossRef Lalla E, Lamster IB, Drury S, Fu C, Schmidt AM. Hyperglycemia, glycoxidation and receptor for advanced glycation endproducts: potential mechanisms underlying diabetic complications, including diabetes-associated periodontitis. Periodontol 2000. 2000;23:50–62.PubMedCrossRef
12.
go back to reference Ross JH, Hardy DC, Schuyler CA, Slate EH, Mize TW, Huang Y. Expression of periodontal interleukin-6 protein is increased across patients with neither periodontal disease nor diabetes, patients with periodontal disease alone and patients with both diseases. J Periodontal Res. 2010;45(5):688–94.PubMedPubMedCentralCrossRef Ross JH, Hardy DC, Schuyler CA, Slate EH, Mize TW, Huang Y. Expression of periodontal interleukin-6 protein is increased across patients with neither periodontal disease nor diabetes, patients with periodontal disease alone and patients with both diseases. J Periodontal Res. 2010;45(5):688–94.PubMedPubMedCentralCrossRef
13.
go back to reference Cole CM, Sundararaj KP, Leite RS, Nareika A, Slate EH, Sanders JJ, et al. A trend of increase in periodontal interleukin-6 expression across patients with neither diabetes nor periodontal disease, patients with periodontal disease alone, and patients with both diseases. J Periodontal Res. 2008;43(6):717–22.PubMedCrossRef Cole CM, Sundararaj KP, Leite RS, Nareika A, Slate EH, Sanders JJ, et al. A trend of increase in periodontal interleukin-6 expression across patients with neither diabetes nor periodontal disease, patients with periodontal disease alone, and patients with both diseases. J Periodontal Res. 2008;43(6):717–22.PubMedCrossRef
14.
go back to reference Hardy DC, Ross JH, Schuyler CA, Leite RS, Slate EH, Huang Y. Matrix metalloproteinase-8 expression in periodontal tissues surgically removed from diabetic and non-diabetic patients with periodontal disease. J Clin Periodontol. 2012;39(3):249–55.PubMedCrossRef Hardy DC, Ross JH, Schuyler CA, Leite RS, Slate EH, Huang Y. Matrix metalloproteinase-8 expression in periodontal tissues surgically removed from diabetic and non-diabetic patients with periodontal disease. J Clin Periodontol. 2012;39(3):249–55.PubMedCrossRef
15.
go back to reference Li Y, Samuvel DJ, Sundararaj KP, Lopes-Virella MF, Huang Y. IL-6 and high glucose synergistically upregulate MMP-1 expression by U937 mononuclear phagocytes via ERK1/2 and JNK pathways and c-Jun. J Cell Biochem. 2010;110(1):248–59.PubMedPubMedCentral Li Y, Samuvel DJ, Sundararaj KP, Lopes-Virella MF, Huang Y. IL-6 and high glucose synergistically upregulate MMP-1 expression by U937 mononuclear phagocytes via ERK1/2 and JNK pathways and c-Jun. J Cell Biochem. 2010;110(1):248–59.PubMedPubMedCentral
16.
go back to reference Maldonado A, He L, Game BA, Nareika A, Sanders JJ, London SD, et al. Pre-exposure to high glucose augments lipopolysaccharide-stimulated matrix metalloproteinase-1 expression by human U937 histiocytes. J Periodontal Res. 2004;39(6):415–23.PubMedCrossRef Maldonado A, He L, Game BA, Nareika A, Sanders JJ, London SD, et al. Pre-exposure to high glucose augments lipopolysaccharide-stimulated matrix metalloproteinase-1 expression by human U937 histiocytes. J Periodontal Res. 2004;39(6):415–23.PubMedCrossRef
17.
go back to reference Nareika A, Im YB, Game BA, Slate EH, Sanders JJ, London SD, et al. High glucose enhances lipopolysaccharide-stimulated CD14 expression in U937 mononuclear cells by increasing nuclear factor kappaB and AP-1 activities. J Endocrinol. 2008;196(1):45–55.PubMedCrossRef Nareika A, Im YB, Game BA, Slate EH, Sanders JJ, London SD, et al. High glucose enhances lipopolysaccharide-stimulated CD14 expression in U937 mononuclear cells by increasing nuclear factor kappaB and AP-1 activities. J Endocrinol. 2008;196(1):45–55.PubMedCrossRef
18.
go back to reference Nareika A, Maldonado A, He L, Game BA, Slate EH, Sanders JJ, et al. High glucose-boosted inflammatory responses to lipopolysaccharide are suppressed by statin. J Periodontal Res. 2007;42(1):31–8.PubMedCrossRef Nareika A, Maldonado A, He L, Game BA, Slate EH, Sanders JJ, et al. High glucose-boosted inflammatory responses to lipopolysaccharide are suppressed by statin. J Periodontal Res. 2007;42(1):31–8.PubMedCrossRef
19.
go back to reference Sundararaj KP, Samuvel DJ, Li Y, Sanders JJ, Lopes-Virella MF, Huang Y. Interleukin-6 released from fibroblasts is essential for up-regulation of matrix metalloproteinase-1 expression by U937 macrophages in coculture: cross-talking between fibroblasts and U937 macrophages exposed to high glucose. J Biol Chem. 2009;284(20):13714–24.PubMedPubMedCentralCrossRef Sundararaj KP, Samuvel DJ, Li Y, Sanders JJ, Lopes-Virella MF, Huang Y. Interleukin-6 released from fibroblasts is essential for up-regulation of matrix metalloproteinase-1 expression by U937 macrophages in coculture: cross-talking between fibroblasts and U937 macrophages exposed to high glucose. J Biol Chem. 2009;284(20):13714–24.PubMedPubMedCentralCrossRef
20.
go back to reference Jialal I, Huet BA, Kaur H, Chien A, Devaraj S. Increased toll-like receptor activity in patients with metabolic syndrome. Diabetes Care. 2012;35(4):900–4.PubMedPubMedCentralCrossRef Jialal I, Huet BA, Kaur H, Chien A, Devaraj S. Increased toll-like receptor activity in patients with metabolic syndrome. Diabetes Care. 2012;35(4):900–4.PubMedPubMedCentralCrossRef
21.
go back to reference Dasu MR, Devaraj S, Park S, Jialal I. Increased toll-like receptor (TLR) activation and TLR ligands in recently diagnosed type 2 diabetic subjects. Diabetes Care. 2010;33(4):861–8.PubMedPubMedCentralCrossRef Dasu MR, Devaraj S, Park S, Jialal I. Increased toll-like receptor (TLR) activation and TLR ligands in recently diagnosed type 2 diabetic subjects. Diabetes Care. 2010;33(4):861–8.PubMedPubMedCentralCrossRef
23.
go back to reference Taylor GW. Exploring interrelationships between diabetes and periodontal disease in African Americans. Compend Contin Educ Dent. 2001;22(3 Spec No):42–8.PubMed Taylor GW. Exploring interrelationships between diabetes and periodontal disease in African Americans. Compend Contin Educ Dent. 2001;22(3 Spec No):42–8.PubMed
24.
go back to reference Haber J. Smoking is a major risk factor for periodontitis. Curr Opin Periodontol. 1994:12-18. Haber J. Smoking is a major risk factor for periodontitis. Curr Opin Periodontol. 1994:12-18.
25.
go back to reference Jin L, Ren L, Leung WK, Darveau RP. The in vivo expression of membrane-bound CD14 in periodontal health and disease. J Periodontol. 2004;75(4):578–85.PubMedCrossRef Jin L, Ren L, Leung WK, Darveau RP. The in vivo expression of membrane-bound CD14 in periodontal health and disease. J Periodontol. 2004;75(4):578–85.PubMedCrossRef
26.
go back to reference Jin L, Darveau RP. Soluble CD14 levels in gingival crevicular fluid of subjects with untreated adult periodontitis. J Periodontol. 2001;72(5):634–40.PubMedCrossRef Jin L, Darveau RP. Soluble CD14 levels in gingival crevicular fluid of subjects with untreated adult periodontitis. J Periodontol. 2001;72(5):634–40.PubMedCrossRef
27.
go back to reference Nichols TC, Fischer TH, Deliargyris EN, Baldwin Jr AS. Role of nuclear factor-kappa B (NF-kappa B) in inflammation, periodontitis, and atherogenesis. Ann Periodontol. 2001;6(1):20–9.PubMedCrossRef Nichols TC, Fischer TH, Deliargyris EN, Baldwin Jr AS. Role of nuclear factor-kappa B (NF-kappa B) in inflammation, periodontitis, and atherogenesis. Ann Periodontol. 2001;6(1):20–9.PubMedCrossRef
28.
go back to reference Dietel M, Johrens K, Laffert M, Hummel M, Blaker H, Muller BM, et al. Predictive molecular pathology and its role in targeted cancer therapy: a review focussing on clinical relevance. Cancer Gene Ther. 2013;20(4):211–21.PubMedCrossRef Dietel M, Johrens K, Laffert M, Hummel M, Blaker H, Muller BM, et al. Predictive molecular pathology and its role in targeted cancer therapy: a review focussing on clinical relevance. Cancer Gene Ther. 2013;20(4):211–21.PubMedCrossRef
29.
go back to reference Promsudthi A, Poomsawat S, Limsricharoen W. The role of Toll-like receptor 2 and 4 in gingival tissues of chronic periodontitis subjects with type 2 diabetes. J Periodontal Res. 2014;49(3):346–54.PubMedCrossRef Promsudthi A, Poomsawat S, Limsricharoen W. The role of Toll-like receptor 2 and 4 in gingival tissues of chronic periodontitis subjects with type 2 diabetes. J Periodontal Res. 2014;49(3):346–54.PubMedCrossRef
30.
go back to reference Rojo-Botello NR, Garcia-Hernandez AL, Moreno-Fierros L. Expression of toll-like receptors 2, 4 and 9 is increased in gingival tissue from patients with type 2 diabetes and chronic periodontitis. J Periodontal Res. 2012;47(1):62–73.PubMedCrossRef Rojo-Botello NR, Garcia-Hernandez AL, Moreno-Fierros L. Expression of toll-like receptors 2, 4 and 9 is increased in gingival tissue from patients with type 2 diabetes and chronic periodontitis. J Periodontal Res. 2012;47(1):62–73.PubMedCrossRef
31.
go back to reference Wright SD. CD14 and innate recognition of bacteria. J Immunol. 1995;155(1):6–8.PubMed Wright SD. CD14 and innate recognition of bacteria. J Immunol. 1995;155(1):6–8.PubMed
32.
go back to reference Wright SD, Ramos RA, Tobias PS, Ulevitch RJ, Mathison JC. CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science. 1990;249(4975):1431–3.PubMedCrossRef Wright SD, Ramos RA, Tobias PS, Ulevitch RJ, Mathison JC. CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science. 1990;249(4975):1431–3.PubMedCrossRef
33.
go back to reference Tapping RI, Tobias PS. Soluble CD14-mediated cellular responses to lipopolysaccharide. Chem Immunol. 2000;74:108–21.PubMedCrossRef Tapping RI, Tobias PS. Soluble CD14-mediated cellular responses to lipopolysaccharide. Chem Immunol. 2000;74:108–21.PubMedCrossRef
34.
go back to reference Beutler B, Rietschel ET. Innate immune sensing and its roots: the story of endotoxin. Nat Rev Immunol. 2003;3(2):169–76.PubMedCrossRef Beutler B, Rietschel ET. Innate immune sensing and its roots: the story of endotoxin. Nat Rev Immunol. 2003;3(2):169–76.PubMedCrossRef
35.
go back to reference Ranoa DR, Kelley SL, Tapping RI. Human lipopolysaccharide-binding protein (LBP) and CD14 independently deliver triacylated lipoproteins to Toll-like receptor 1 (TLR1) and TLR2 and enhance formation of the ternary signaling complex. J Biol Chem. 2013;288(14):9729–41.PubMedPubMedCentralCrossRef Ranoa DR, Kelley SL, Tapping RI. Human lipopolysaccharide-binding protein (LBP) and CD14 independently deliver triacylated lipoproteins to Toll-like receptor 1 (TLR1) and TLR2 and enhance formation of the ternary signaling complex. J Biol Chem. 2013;288(14):9729–41.PubMedPubMedCentralCrossRef
36.
go back to reference Heumann D, Lauener R, Ryffel B. The dual role of LBP and CD14 in response to Gram-negative bacteria or Gram-negative compounds. J Endotoxin Res. 2003;9(6):381–4.PubMedCrossRef Heumann D, Lauener R, Ryffel B. The dual role of LBP and CD14 in response to Gram-negative bacteria or Gram-negative compounds. J Endotoxin Res. 2003;9(6):381–4.PubMedCrossRef
37.
go back to reference Schimke J, Mathison J, Morgiewicz J, Ulevitch RJ. Anti-CD14 mAb treatment provides therapeutic benefit after in vivo exposure to endotoxin. Proc Natl Acad Sci U S A. 1998;95(23):13875–80.PubMedPubMedCentralCrossRef Schimke J, Mathison J, Morgiewicz J, Ulevitch RJ. Anti-CD14 mAb treatment provides therapeutic benefit after in vivo exposure to endotoxin. Proc Natl Acad Sci U S A. 1998;95(23):13875–80.PubMedPubMedCentralCrossRef
38.
go back to reference Wenneras C, Ave P, Huerre M, Arondel J, Ulevitch RJ, Mathison JC, et al. Blockade of CD14 increases Shigella-mediated invasion and tissue destruction. J Immunol. 2000;164(6):3214–21.PubMedCrossRef Wenneras C, Ave P, Huerre M, Arondel J, Ulevitch RJ, Mathison JC, et al. Blockade of CD14 increases Shigella-mediated invasion and tissue destruction. J Immunol. 2000;164(6):3214–21.PubMedCrossRef
39.
go back to reference Patino R, Ibarra J, Rodriguez A, Yague MR, Pintor E, Fernandez-Cruz A, et al. Circulating monocytes in patients with diabetes mellitus, arterial disease, and increased CD14 expression. Am J Cardiol. 2000;85(11):1288–91.PubMedCrossRef Patino R, Ibarra J, Rodriguez A, Yague MR, Pintor E, Fernandez-Cruz A, et al. Circulating monocytes in patients with diabetes mellitus, arterial disease, and increased CD14 expression. Am J Cardiol. 2000;85(11):1288–91.PubMedCrossRef
40.
go back to reference Fernandez-Real JM, Perez Del Pulgar S, Luche E, Moreno-Navarrete JM, Waget A, Serino M, et al. CD14 modulates inflammation-driven insulin resistance. Diabetes. 2011;60(8):2179–86.PubMedPubMedCentralCrossRef Fernandez-Real JM, Perez Del Pulgar S, Luche E, Moreno-Navarrete JM, Waget A, Serino M, et al. CD14 modulates inflammation-driven insulin resistance. Diabetes. 2011;60(8):2179–86.PubMedPubMedCentralCrossRef
41.
go back to reference Young JL, Mora A, Cerny A, Czech MP, Woda B, Kurt-Jones EA, et al. CD14 deficiency impacts glucose homeostasis in mice through altered adrenal tone. PLoS One. 2012;7(1):e29688.PubMedPubMedCentralCrossRef Young JL, Mora A, Cerny A, Czech MP, Woda B, Kurt-Jones EA, et al. CD14 deficiency impacts glucose homeostasis in mice through altered adrenal tone. PLoS One. 2012;7(1):e29688.PubMedPubMedCentralCrossRef
42.
go back to reference Nemoto E, Sugawara S, Tada H, Takada H, Shimauchi H, Horiuchi H. Cleavage of CD14 on human gingival fibroblasts cocultured with activated neutrophils is mediated by human leukocyte elastase resulting in down-regulation of lipopolysaccharide-induced IL-8 production. J Immunol. 2000;165(10):5807–13.PubMedCrossRef Nemoto E, Sugawara S, Tada H, Takada H, Shimauchi H, Horiuchi H. Cleavage of CD14 on human gingival fibroblasts cocultured with activated neutrophils is mediated by human leukocyte elastase resulting in down-regulation of lipopolysaccharide-induced IL-8 production. J Immunol. 2000;165(10):5807–13.PubMedCrossRef
43.
go back to reference Liu S, Khemlani LS, Shapiro RA, Johnson ML, Liu K, Geller DA, et al. Expression of CD14 by hepatocytes: upregulation by cytokines during endotoxemia. Infect Immun. 1998;66(11):5089–98.PubMedPubMedCentral Liu S, Khemlani LS, Shapiro RA, Johnson ML, Liu K, Geller DA, et al. Expression of CD14 by hepatocytes: upregulation by cytokines during endotoxemia. Infect Immun. 1998;66(11):5089–98.PubMedPubMedCentral
44.
go back to reference Matsuura K, Ishida T, Setoguchi M, Higuchi Y, Akizuki S, Yamamoto S. Upregulation of mouse CD14 expression in Kupffer cells by lipopolysaccharide. J Exp Med. 1994;179(5):1671–6.PubMedCrossRef Matsuura K, Ishida T, Setoguchi M, Higuchi Y, Akizuki S, Yamamoto S. Upregulation of mouse CD14 expression in Kupffer cells by lipopolysaccharide. J Exp Med. 1994;179(5):1671–6.PubMedCrossRef
45.
go back to reference Parajuli B, Sonobe Y, Kawanokuchi J, Doi Y, Noda M, Takeuchi H, et al. GM-CSF increases LPS-induced production of proinflammatory mediators via upregulation of TLR4 and CD14 in murine microglia. J Neuroinflammation. 2012;9:268.PubMedPubMedCentralCrossRef Parajuli B, Sonobe Y, Kawanokuchi J, Doi Y, Noda M, Takeuchi H, et al. GM-CSF increases LPS-induced production of proinflammatory mediators via upregulation of TLR4 and CD14 in murine microglia. J Neuroinflammation. 2012;9:268.PubMedPubMedCentralCrossRef
46.
go back to reference Imai K, Takeshita A, Hanazawa S. Transforming growth factor-beta inhibits lipopolysaccharide-stimulated expression of inflammatory cytokines in mouse macrophages through downregulation of activation protein 1 and CD14 receptor expression. Infect Immun. 2000;68(5):2418–23.PubMedPubMedCentralCrossRef Imai K, Takeshita A, Hanazawa S. Transforming growth factor-beta inhibits lipopolysaccharide-stimulated expression of inflammatory cytokines in mouse macrophages through downregulation of activation protein 1 and CD14 receptor expression. Infect Immun. 2000;68(5):2418–23.PubMedPubMedCentralCrossRef
47.
go back to reference Mize TW, Sundararaj KP, Leite RS, Huang Y. Increased and correlated expression of connective tissue growth factor and transforming growth factor beta 1 in surgically removed periodontal tissues with chronic periodontitis. J Periodontal Res. 2015;50(3):315–9.PubMedCrossRef Mize TW, Sundararaj KP, Leite RS, Huang Y. Increased and correlated expression of connective tissue growth factor and transforming growth factor beta 1 in surgically removed periodontal tissues with chronic periodontitis. J Periodontal Res. 2015;50(3):315–9.PubMedCrossRef
Metadata
Title
Periodontal CD14 mRNA expression is downregulated in patients with chronic periodontitis and type 2 diabetes
Authors
Dustin C. Hedgpeth
Xiaoming Zhang
Junfei Jin
Renata S. Leite
Joe W. Krayer
Yan Huang
Publication date
01-12-2015
Publisher
BioMed Central
Published in
BMC Oral Health / Issue 1/2015
Electronic ISSN: 1472-6831
DOI
https://doi.org/10.1186/s12903-015-0118-3

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