Modulation of host cell signaling pathways as a therapeutic approach in periodontal disease

Journal of Applied Oral Science

Volumn 20, Issue 2, 2012, Pages 128-138

  de Souza, João Antonio Chaves ^a   Rossa Junior, Carlos ^a   Garlet, Gustavo Pompermaier ^b   Nogueira, Andressa Vilas Boas ^a   Cirelli, Joni Augusto ^a  

^a SÃO PAULO STATE UNIVERSITY UNESP   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Janus kinases; Mitogen activated protein kinases; NF kappa B; Periodontitis; Signal transduction; STAT transcription factors

Indexed keywords

EID: 84862727906     PISSN: 16787757     EISSN: 16787765     Source Type: Journal    
DOI: 10.1590/S1678-77572012000200002     Document Type: Article

References (92)

1. Albandar JM. Global risk factors and risk indicators for periodontal diseases. Periodontol 2000. 2002;29:177-206.
2. Alexander MB, Damoulis PD. The role of cytokines in the pathogenesis of periodontal disease. Curr Opin Periodontol. 1994:39-53.
3. Ambili R, Santhi WS, Janam P, Nandakumar K, Pillai MR. Expression of activated transcription factor nuclear factor-kappaB in periodontally diseased tissues. J Periodontol. 2005;76:1148-1153.
4. Badger AM, Griswold DE, Kapadia R, Blake S, Swift BA, Hoffman SJ, et al. Disease-modifying activity of SB 242235, a selective inhibitor of p38 mitogen-activated protein kinase, in rat adjuvant-induced arthritis. Arthritis Rheum. 2000;43:175-183.
5. Baeuerle PA, Baichwal VR. NF-kappa B as a frequent target for immunosuppressive and anti-inflammatory molecules. Adv Immunol. 1997;65:111-137.
6. Baker PJ. The role of immune responses in bone loss during periodontal disease. Microbes Infect. 2000;2:1181-1192.
7. Baldassare JJ, Bi Y, Bellone CJ. The role of p38 mitogen-activated protein kinase in IL-1 beta transcription. J Immunol. 1999;162:5367-5373.
8. Berglundh T, Donati M. Aspects of adaptive host response in periodontitis. J Clin Periodontol. 2005;32:87-107.
9. Bondeson J, Foxwell B, Brennan F, Feldmann M. Defining therapeutic targets by using adenovirus: blocking NF-kappaB inhibits both inflammatory and destructive mechanisms in rheumatoid synovium but spares anti-inflammatory mediators. Proc Natl Acad Sci USA. 1999;96:5668-5673.
10. Brown LJ, Löe H. Prevalence, extent, severity and progression of periodontal disease. Periodontol 2000. 1993;2:57-71.
11. Cho H, Lee KH, Colquhoun AN, Evans SA. Invasive ora aspergillosis in a patient with acute myeloid leukaemia. Aust Dent J. 2010;55:214-218.
12. Chopra P, Kulkarni O, Gupta S, Bajpai M, Kanoje V, Banerjee M, et al. Pharmacological profile of AW-814141, a novel, potent, selective and orally active inhibitor of p38 MAP kinase. Int Immunopharmacol. 2010;10:467-473.
13. Ciesielski CJ, Andreakos E, Foxwell BM, Feldmann M. TNFalpha-induced macrophage chemokine secretion is more dependent on NF-kappaB expression than lipopolysaccharides-induced macrophage chemokine secretion. Eur J Immunol. 2002;32:2037-2045.
14. Cohen P. Targeting protein kinases for the development of anti-inflammatory drugs. Curr Opin Cell Biol. 2009;21:317-324.
15. Damjanov N, Kauffman RS, Spencer-Green GT Efficacy, pharmacodynamics, and safety of VX-702, a novel p38 MAPK inhibitor, in rheumatoid arthritis: results of two randomized, double-blind, placebo-controlled clinical studies. Arthritis Rheum. 2009;60:1232-1241.
16. De Repentigny L, Lewandowski D, Aumont F, Hanna Z, Jolicoeur P. Oral mucosal cell response to Candida albicans in transgenic mice expressing HIV-1. Methods Mol Biol. 2009;470:359-368.
17. Dhasmana DJ, Dheda K, Ravn P, Wilkinson RJ, Meintjes G. Immune reconstitution inflammatory syndrome in HIV-infected patients receiving antiretroviral therapy: pathogenesis, clinica manifestations and management. Drugs. 2008;68:191-208.
18. Dinarello CA. Therapeutic strategies to reduce IL-1 activity in treating local and systemic inflammation. Curr Opin Pharmacol. 2004;4:378-385.
19. Gamonal J, Acevedo A, Bascones A, Jorge O, Silva A. Levels of interleukin-1 beta, -8, and -10 and RANTES in gingival crevicular fluid and cell populations in adult periodontitis patients and the effect of periodontal treatment. J Periodontol. 2000;71:1535-1545.
20. Garcia de Aquino S, Manzolli Leite FR, Stach-Machado DR, Francisco da Silva JA, Spolidorio LC, Rossa C Jr. Signaling pathways associated with the expression of inflammatory mediators activated during the course of two models of experimenta periodontitis. Life Sci. 2009;84:745-754.
21. Garlet GP, Cardoso CR, Campanelli AP, Martins W Jr., Silva JS. Expression of suppressors of cytokine signaling in diseased periodontal tissues: a stop signal for disease progression? J Periodontal Res. 2006;41:580-584.
22. Garlet GP, Martins W Jr, Fonseca BA, Ferreira BR, Silva JS. Matrix metalloproteinases, their physiological inhibitors and osteoclast factors are differentially regulated by the cytokine profile in human periodontal disease. J Clin Periodontol. 2004;31:671-679.
23. Gemmell E, Seymour GJ. Immunoregulatory control of Th1/ Th2 cytokine profiles in periodontal disease. Periodontol 2000. 2004;35:21-41.
24. Ghosh S, May MJ, Kopp EB. NF-kappa B and Rel proteins: evolutionarily conserved mediators of immune responses. Annu Rev Immunol. 1998;16:225-260.
25. Gilroy DW, Lawrence T, Perretti M, Rossi AG. Inflammatory resolution: new opportunities for drug discovery. Nat Rev Drug Discov. 2004;3:401-416.
26. Gilston V, Jones HW, Soo CC, Coumbe A, Blades S, Kaltschmidt C, et al. NF-kappa B activation in human knee-joint synovial tissue during the early stage of joint inflammation. Biochem Soc Trans. 1997;25:518S.
27. Goldstein DM, Gabriel T. Pathway to the clinic: inhibition of P38 MAP kinase. A review of ten chemotypes selected for development. Curr Top Med Chem. 2005;5:1017-1029.
28. Golub LM, McNamara TF, Ryan ME, Kohut B, Blieden T, Payonk G, et al. Adjunctive treatment with subantimicrobia doses of doxycycline: effects on gingival fluid collagenase activity and attachment loss in adult periodontitis. J Clin Periodontol. 2001;28:146-156.
29. Graves D. Cytokines that promote periodontal tissue destruction. J Periodontol. 2008;79:1585-1591.
30. Haddad JJ. Cytokines and related receptor-mediated signaling pathways. Biochem Biophys Res Commun. 2002;297:700-713.
31. Haddad JJ. VX-745. Vertex Pharmaceuticals. Curr Opin Investig Drugs. 2001;2:1070-1076.
32. Han Z, Boyle DL, Chang L, Bennett B, Karin M, Yang L, et al. c-Jun N-terminal kinase is required for metalloproteinase expression and joint destruction in inflammatory arthritis. J Clin Invest. 2001;108:73-81.
33. Hitti E, Iakovleva T, Brook M, Deppenmeier S, Gruber AD, Radzioch D, et al. Mitogen-activated protein kinase-activated protein kinase 2 regulates tumor necrosis factor mRNA stability and translation mainly by altering tristetraprolin expression, stability, and binding to adenine/uridine-rich element. Mol Cel Biol. 2006;26:2399-2407.
34. Ihle JN, Kerr IM. Jaks and Stats in signaling by the cytokine receptor superfamily. Trends Genet. 1995;11:69-74.
35. Kasperkovitz PV, Verbeet NL, Smeets TJ, van Rietschoten JG, Kraan MC, van der Pouw Kraan TC, et al. Activation of the STAT1 pathway in rheumatoid arthritis. Ann Rheum Dis. 2004;63:233-239.
36. Kirkwood KL, Li F, Rogers JE, Otremba J, Coatney DD, Kreider JM, et al. A p38alpha selective mitogen-activated protein kinase inhibitor prevents periodontal bone loss. J Pharmacol Exp Ther. 2007;320:56-63.
37. Kirkwood KL, Rossa C Jr. The potential of p38 MAPK inhibitors to modulate periodontal infections. Curr Drug Metab. 2009;10:55-67.
38. Kortylewski M, Yu H. Stat3 as a potential target for cancer immunotherapy. J Immunother. 2007;30:131-139.
39. Krause A, Scaletta N, Ji JD, Ivashkiv LB. Rheumatoid arthritis synoviocyte survival is dependent on Stat3. J Immunol. 2002;169:6610-6616.
40. Kuo LC, Poison AM, Kang T. Associations between periodonta diseases and systemic diseases: a review of the inter-relationships and interactions with diabetes, respiratory diseases, cardiovascular diseases and osteoporosis. Public Health. 2008;122:417-433.
41. Kyriakis JM, Avruch J. Mammalian mitogen-activated protein kinase signal transduction pathways activated by stress and inflammation. Physiol Rev. 2001;81:807-869.
42. Lane N, Armitage GC, Loomer P, Hsieh S, Majumdar S, Wang HY, et al. Bisphosphonate therapy improves the outcome of conventional periodontal treatment: results of a 12-month, randomized, placebo-controlled study. J Periodontol. 2005;76:1113-1122.
43. Lee JC, Laydon JT, McDonnell PC, Gallagher TF, Kumar S, Green D, et al. A protein kinase involved in the regulation of inflammatory cytokine biosynthesis. Nature. 1994;372:739-746.
44. Leitao RF, Ribeiro RA, Chaves HV, Rocha FA, Lima V, Brito GA. Nitric oxide synthase inhibition prevents alveolar bone resorption in experimental periodontitis in rats. J Periodontol. 2005;76:956-963.
45. Li Q, Lu Q, Bottero V, Estepa G, Morrison L, Mercurio F, et al. Enhanced NF-kappaB activation and cellular function in macrophages lacking IkappaB kinase 1 (IKK1). Proc Natl Acad Sci USA. 2005;102:12425-12430.
46. Liu D, Xu JK, Figliomeni L, Huang L, Pavlos NJ, Rogers M, et al. Expression of RANKL and OPG mRNA in periodonta disease: possible involvement in bone destruction. Int J Mol Med. 2003;11:17-21.
47. Lu YC, Yeh WC, Ohashi PS. LPS/TLR4 signal transduction pathway. Cytokine. 2008;42:145-151.
48. Maeda S, Chang L, Li ZW, Luo JL, Leffert H, Karin M. IKKbeta is required for prevention of apoptosis mediated by cell-bound but not by circulating TNFalpha. Immunity. 2003;19:725-737.
49. Mbalaviele G, Anderson G, Jones A, De Ciechi P, Settle S, Mnich S, et al. Inhibition of p38 mitogen-activated protein kinase prevents inflammatory bone destruction. J Pharmacol Exp Ther. 2006;317:1044-1053.
50. McIntyre KW, Shuster DJ, Gillooly KM, Dambach DM, Pattoli MA, Lu P, et al. A highly selective inhibitor of I kappa B kinase, BMS-345541, blocks both joint inflammation and destruction in collagen-induced arthritis in mice. Arthritis Rheum. 2003;48:2652-2659.
51. Medicherla S, Ma JY, Mangadu R, Jiang Y, Zhao JJ, Almirez R, et al. A selective p38 alpha mitogen-activated protein kinase inhibitor reverses cartilage and bone destruction in mice with collagen-induced arthritis. J Pharmacol Exp Ther. 2006;318:132-141.
52. Medzhitov R, Janeway CA Jr. Innate immunity: the virtues of a nonclonal system of recognition. Cell. 1997;91:295-298.
53. Miagkov AV, Kovalenko DV, Brown CE, Didsbury JR, Cogswel JP, Stimpson SA, et al. NF-kappaB activation provides the potentia ink between inflammation and hyperplasia in the arthritic joint. Proc Natl Acad Sci USA. 1998;95:13859-13864.
54. Nishimoto N, Yoshizaki K, Miyasaka N, Yamamoto K, Kawai S, Takeuchi T, et al. Treatment of rheumatoid arthritis with humanized anti-interleukin-6 receptor antibody: a multicenter, double-blind, placebo-controlled trial. Arthritis Rheum. 2004;50:1761-1769.
55. O'Shea JJ, Gadina M, Schreiber RD. Cytokine signaling in 2002: new surprises in the Jak/Stat pathway. Cell. 2002;109:S121-S131.
56. Ohori M. ERK inhibitors as a potential new therapy for rheumatoid arthritis. Drug News Perspect. 2008;21:245-250.
57. Page RC. The role of inflammatory mediators in the pathogenesis of periodontal disease. J Periodontal Res. 1991;26:230-242.
58. Parganas E, Wang D, Stravopodis D, Topham DJ, Marine JC, Teglund S, et al. Jak2 is essential for signaling through a variety of cytokine receptors. Cell. 1998;93:385-395.
59. Pargellis C, Regan J. Inhibitors of p38 mitogen-activated protein kinase for the treatment of rheumatoid arthritis. Curr Opin Investig Drugs. 2003;4:566-571.
60. Patil C, Rossa C Jr, Kirkwood KL. Actinobacillus actinomycetemcomitans lipopolysaccharide induces interleukin-6 expression through multiple mitogen-activated protein kinase pathways in periodontal ligament fibroblasts. Oral Microbio Immunol. 2006;21:392-398.
61. Patil C, Zhu X, Rossa C Jr, Kim YJ, Kirkwood KL. p38 MAPK regulates IL-1beta induced IL-6 expression through mRNA stability in osteoblasts. Immunol Invest. 2004;33:213-233.
62. Patil CS, Kirkwood KL. p38 MAPK signaling in oral-related diseases. J Dent Res. 2007;86:812-825.
63. Pearson G, Robinson F, Beers Gibson T, Xu BE, Karandikar M, Berman K, et al. Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions. Endocr Rev. 2001;22:153-183.
64. Perdiguero E, Ruiz-Bonilla V, Serrano AL, Muñoz-Cánoves P. Genetic deficiency of p38alpha reveals its critical role in myoblast cell cycle exit: the p38alpha-JNK connection. Cell Cycle. 2007;6:1298-1303.
65. Reddy MS, Geurs NC, Gunsolley JC. Periodontal host modulation with antiproteinase, anti-inflammatory, and bone-sparing agents. A systematic review. Ann Periodontol. 2003;8:12-37.
66. Roberts FA, McCaffery KA, Michalek SM. Profile of cytokine mRNA expression in chronic adult periodontitis. J Dent Res. 1997;76:1833-1839.
67. Robinson MJ, Cobb MH. Mitogen-activated protein kinase pathways. Curr Opin Cell Biol. 1997;9:180-186.
68. Rodig SJ, Meraz MA, White JM, Lampe PA, Riley JK, Arthur CD, et al. Disruption of the Jak1 gene demonstrates obligatory and nonredundant roles of the Jaks in cytokine-induced biologic responses. Cell. 1998;93:373-383.
69. Rogers JE, Li F, Coatney DD, Otremba J, Kriegl JM, Protter TA, et al. A p38 mitogen-activated protein kinase inhibitor arrests active alveolar bone loss in a rat periodontitis model. J Periodontol. 2007;78:1992-1998.
70. Rossa C Jr, Liu M, Kirkwood KL. A dominant function of p38 mitogen-activated protein kinase signaling in receptor activator of nuclear factor-kappaB ligand expression and osteoclastogenesis induction by Aggregatibacter actinomycetemcomitans and Escherichia coli lipopolysaccharide. J Periodontal Res. 2008;43:201-211.
71. Ryan ME. Clinical applications for host modulatory therapy. Compend Contin Educ Dent. 2002;23:1071-6,1079-1082.
72. Saklatvala J, Dean J, Clark A. Control of the expression of inflammatory response genes. Biochem Soc Symp. 2003:95-106.
73. Schindler CW. Series introduction. JAK-STAT signaling in human disease. J Clin Invest. 2002;109:1133-1137.
74. Sen R, Baltimore D. Inducibility of kappa immunoglobulin enhancer-binding protein Nf-kappa B by a posttranslationa mechanism. Cell. 1986;47:921-928.
75. Shaw MH, Boyartchuk V, Wong S, Karaghiosoff M, Ragimbeau J, Pellegrini S, et al. A natural mutation in the Tyk2 pseudokinase domain underlies altered susceptibility of B10.Q/J mice to infection and autoimmunity. Proc Natl Acad Sci USA. 2003;100:11594-11599.
76. Smith RJ. Therapies for rheumatoid arthritis: hope springs eternal. Drug Discov Today. 2005;10:1598-1606.
77. Starr R, Hilton DJ. Negative regulation of the JAK/STAT pathway. Bioessays. 1999;21:47-52.
78. Sugita N, Kimura A, Matsuki Y, Yamamoto T, Yoshie H, Hara K. Activation of transcription factors and IL-8 expression in neutrophils stimulated with lipopolysaccharide from Porphyromonas gingivalis. Inflammation. 1998;22:253-267.
79. Sweeney SE, Firestein GS. Mitogen activated protein kinase inhibitors: where are we now and where are we going? Ann Rheum Dis. 2006;65:iii83-iii88.
80. Sweeney SE, Firestein GS. Primer: signal transduction in rheumatic disease - a clinician's guide. Nat Clin Pract Rheumatol. 2007;3:651-660.
81. Tak PP, Firestein GS. NF-kappaB: a key role in inflammatory diseases. J Clin Invest. 2001;107:7-11.
82. Tan AE. Periodontal maintenance. Aust Dent J. 2009;54:S110-S117.
83. Thalhamer T, McGrath MA, Harnett MM. MAPKs and their relevance to arthritis and inflammation. Rheumatology (Oxford). 2008;47:409-414.
84. Velazquez L, Fellous M, Stark GR, Pellegrini S. A protein tyrosine kinase in the interferon alpha/beta signaling pathway. Cell. 1992;70:313-322.
85. Walker JG, Ahern MJ, Coleman M, Weedon H, Papangelis V, Beroukas D, et al. Expression of Jak3, STAT1, STAT4, and STAT6 in inflammatory arthritis: unique Jak3 and STAT4 expression in dendritic cells in seropositive rheumatoid arthritis. Ann Rheum Dis. 2006;65:149-156.
86. Wang Z, Yang H, Tachado SD, Capó-Aponte JE, Bildin VN, Koziel H, et al. Phosphatase-mediated crosstalk control of ERK and p38 MAPK signaling in corneal epithelial cells. Invest Ophthalmol Vis Sci. 2006;47:5267-5275.
87. Weisman MH. What are the risks of biologic therapy in rheumatoid arthritis? An update on safety. J Rheumatol Suppl. 2002;65:33-38.
88. West K. CP-690550, a JAK3 inhibitor as an immunosuppressant for the treatment of rheumatoid arthritis, transplant rejection, psoriasis and other immune-mediated disorders. Curr Opin Investig Drugs. 2009;10:491-504.
89. Williams DH, Wilkinson SE, Purton T, Lamont A, Flotow H, Murray EJ. Ro 09-2210 exhibits potent anti-proliferative effects on activated T cells by selectively blocking MKK activity. Biochemistry. 1998;37:9579-9585.
90. Williams RC, Beck JD, Offenbacher SN. The impact of new technologies to diagnose and treat periodontal disease. A look to the future. J Clin Periodontol. 1996;23:299-305.
91. Winzen R, Kracht M, Ritter B, Wilhelm A, Chen CY, Shyu AB, et al. The p38 MAP kinase pathway signals for cytokine-induced mRNA stabilization via MAP kinase-activated protein kinase 2 and an AU-rich region-targeted mechanism. EMBO J. 1999;18:4969-4980.
92. Yong HY, Koh MS, Moon A. The p38 MAPK inhibitors for the treatment of inflammatory diseases and cancer. Expert Opin Investig Drugs. 2009;18:1893-1905.