Targeting mRNA stability arrests inflammatory bone loss

Molecular Therapy

Volumn 16, Issue 10, 2008, Pages 1657-1664

  Patil, Chetan S ^a,b   Liu, Min ^b   Zhao, Wenpu ^b   Coatney, Derek D ^b   Li, Fei ^b   VanTubergen, Elizabeth A ^b   D'Silva, Nisha J ^b,c   Kirkwood, Keith L ^b  

^a UNIVERSITY AT BUFFALO   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE PHOSPHATE; ADENOVIRUS VECTOR; BACTERIUM LIPOPOLYSACCHARIDE; CYTOKINE; INTERLEUKIN 6; LUCIFERASE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; PROSTAGLANDIN E2; RNA BINDING PROTEIN; TRISTETRAPROLIN; TUMOR NECROSIS FACTOR ALPHA; URIDINE PHOSPHATE;

3' UNTRANSLATED REGION; ACTINOBACILLUS ACTINOMYCETEMCOMITANS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DRUG TARGETING; EXPERIMENTAL MODEL; FEMALE; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATORY INFILTRATE; NONHUMAN; OSTEOLYSIS; PERIODONTITIS; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; REPORTER GENE; RNA DEGRADATION; RNA STABILITY; SIGNAL TRANSDUCTION; VIRAL GENE DELIVERY SYSTEM;

ADENOVIRIDAE; ANIMALS; BONE DISEASES, METABOLIC; CELL LINE; DINOPROSTONE; GENE THERAPY; HELA CELLS; HUMANS; INFLAMMATION; INTERLEUKIN-6; MICE; RATS; RNA STABILITY; TRISTETRAPROLIN; TUMOR NECROSIS FACTOR-ALPHA;

ANIMALIA;

EID: 54849162300     PISSN: 15250016     EISSN: 15250024     Source Type: Journal    
DOI: 10.1038/mt.2008.163     Document Type: Article

References (50)

1. Teng, YT (2003). The role of acquired immunity and periodontal disease progression. Crit Rev Oral Biol Med 14: 237-252.
2. Teng, YT (2002). Mixed periodontal Th1-Th2 cytokine profile in Actinobacillus actinomycetemcomitans-specitic osteoprotegerin ligand (or RANK-L)-mediated alveolar bone destruction in vivo. Infect Immun 70: 5269-5273.
3. Patil, CS and Kirkwood, KL (2007). p38 MAPK signaling in oral-related diseases. J Dent Res 86: 812-825.
4. Hamilton, TA, Novotny, M, Datta, S, Mandal, P, Hartupee, J, Tebo, J et al. (2007). Chemokine and chemoattractant receptor expression: post-transcriptional regulation. J Leukoc Biol 82: 213-219.
5. Hamilton, TA, Ohmori, Y and Tebo, J (2002). Regulation of chemokine expression by antiinflammatory cytokines. Immunol Res 25: 229-245.
6. Patil, C, Rossa, C Jr. and Kirkwood, KL (2006). Actinobocillus actinomycetemcomitans lipopolysaccharide induces interleukin-6 expression through multiple mitogen-activated protein kinase pathways in periodontal ligament fibroblasts. Oral Microbiol Immunol 21: 392-398.
7. Rossa, C, Ehmann, K, Liu, M, Patil, C and Kirkwood, KL (2006). MKK3/ 6-p38 MAPK signaling is required for IL-1 beta and TNF-alpha-induced RANKL expression in bone marrow stromal cells. J Interferon Cytokine Res 26: 719-729.
8. Hirose, K, Isogai, E, Miura, H and Ueda, I (1997). Levels of Porphyromonas gingivalis Fimbriae and inflammatory cytokines in gingival crevicular fluid from adult human subjects. Microbiol Immunol 41: 21-26.
9. Geivelis, M, Turner, DW, Pederson, ED and Lamberts, BL (1993). Measurements of interleukin-6 in gingival crevicular fluid from adults with destructive periodontal disease. J Periodontol 64: 980-983.
10. Takeichi, O, Saito, I, Tsurumachi, T, Moro, I and Saito, T (1996). Expression of inflammatory cytokine genes in vivo by human alveolar bone-derived polymorphonuclear leukocytes isolated from chronically inflamed sites of bone resorption. Calcif Tissue Int 58: 244-248.
11. Takeichi, O, Saito, I, Tsurumachi, T, Saito, T and Moro, I (1994). Human polymorphonuclear leukocytes derived from chronically inflamed tissue express inflammatory cytokines in vivo. Cell Immunol 156: 296-309.
12. Gutierrez-Venegas, G, Maldonado-Frias, S, Ontiveros-Granados, A and Kawasaki-Cardenas, P (2005). Role of p38 in nitric oxide synthase and cyclooxygenase expression, and nitric oxide and PGE2 synthesis in human gingival fibroblasts stimulated with lipopolysaccharides. Life Sci 77: 60-73.
13. Nassar, CA, Nassar, PO, Nassar, PM and Spolidorio, LC (2005). Selective cyclooxygenase-2 inhibition prevents bone resorption. Braz Oral Res 19: 36-40.
14. Assuma, R, Oates, T Cochran, D, Amar, S and Graves, DT (1998). IL-1 and TNF antagonists inhibit the inflammatory response and bone loss in experimental periodontitis. J Immunol 160: 403-409.
15. Kirkwood, KL, Li, F, Rogers, JE, Otremba, I, Coatney, DD, Kreider, JM et al. (2007). A p38alpha selective mitogen-activated protein kinase inhibitor prevents periodontal bone loss. J Phormocol Exp Ther 320: 56-63.
16. Rogers, JE, Li, F, Coatney, DD, Otremba, J, Kriegl, JM, Protter, TA et al. (2007). A p38 mitogen-activated protein kinase inhibitor arrests active alveolar bone loss in a rat periodontitis model. J Periodontol 78: 1992-1998.
17. Mahtani, KR, Brook, M, Dean, JL, Sully, G, Saklatvala, J and Clark, AR (2001). Mitogen-activated protein kinase p3B controls the expression and posttranslational modification of tristetraprolin, a regulator of tumor necrosis factor alpha mRNA stability. Mol Cell Biol 21: 6461-6469.
18. Stoecklin, G, Stoeckle, P, Lu, M, Muehlemann, O and Moroni, C (2001). Cellular mutants define a common mRNA degradation pathway targeting cytokine AU-rich elements. RNA 7:1578-1588.
19. Kotlyarov, A, Neininger, A, Schubert, C, Eckert, R, Birchmeier, C, Volk, HD et al. (1999), MAPKAP kinase 2 is essential for LPS-incluced TNF-alpha biosynthesis. Nat Cell Biol 1: 94-97.
20. Neininger, A, Kontoyiannis, D, Kotlyarov, A, Winzen, R, Eckert, R, Volk, HD et al. (2002). MK2 targets AU-rich elements and regulates biosynthesis of tumor necrosis factor and interleukin-6 independently at different post-transcriptional levels. J Biol Chem 277: 3065-3068.
21. Winzen, R, Kracht, M, Ritter, B, Wilhelm, A, Chen, CY, Shyu, AB et al. (1999). The p38 MAP kinase pathway signals for cytokine-incluced mRNA stabilization via MAP kinase-activated protein kinase 2 and an AU-rich region-targeted mechanism. EMBO J 18: 4969-4980.
22. Wang, JG, Collinge, M, Ramgolam, V et al. (2006). LFA-1-dependent HuR nuclear export and cytokine mRNA stabilization in T cell activation. J Immunol 176: 2105-2113.
23. Varnum, BC, Ma, QF, Chi, TH, Fletcher, B and Herschman, HR (1991). The TIS11 primary response gene is a member of a gene family that encodes proteins with a highly conserved sequence containing an unusual Cys-His repeat. Mol Cell Biol 11: 1754-1758.
24. Taylor, GA, Carballo, E, Lee, DM, Lai, WS, Thompson, MJ, Patel, DD et al. (1996). A pathogenetic role for TNF alpha in the syndrome of cachexia, arthritis, and autoimmunity resulting from tristetraprolin (TTP) deficiency. Immunity 4: 445-454.
25. Carballo, E, Lai, WS and Blackshear, PJ (1998). Feedback inhibition of macrophage tumor necrosis factor-alpha production by tristetraprolin. Science 281: 1001-1005.
26. Carballo, E, Lai, WS and Blackshear, PJ (2000). Evidence that tristetraprolin is a physiological regulator of granulocyte-macrophage colony-stimulating factor messenger RNA cleadenylation and stability. Blood 95: 1891-1899.
27. Rigby, WF, Roy, K, Collins, J, Rigby, 5, Connolly, JE, Bloch, DB et al. (2005). Structure/function analysis of tristetraprolin (TTP): p38 stress-activated protein kinase and lipopolysaccharide stimulation do not alter TTP function. J Immunol 174: 7883-7893.
28. Rogers, JE, Li, F, Coatney, DD, Rossa, C, Bronson, P, Krieder, JM et al. (2007). Actinobocillus octinomycetemcomitans lipopolysaccharide-mediated experimental bone loss model for aggressive periodontitis. J Periodontol 79: 550-558.
29. Blackshear, PJ, Lai, WS, Kennington, EA, Brewer, G, Wilson, GM, Guan, X et al. (2003). Characteristics of the interaction of a synthetic human tristetraprolin tandem zinc finger peptide with AU-rich element-containing RNA substrates. J Biol Chem 278 19947-19955.
30. Tchen, CR, Brook, M, Saklatvala, J and Clark, AR (2004). The stability of tristetraprolin mRNA is regulated by mitogen-activated protein kinase p38 and by tristetraprolin itself. J Biol Chem 279: 32393-32400.
31. Boutaud, O, Dixon, DA, Oates, JA and Sawaoka, H (2003). Tristetraprolin binds to the COX-2 mRNA 3′ untranslated region in cancer cells. Adv Exp Med Biol 525: 157-160.
32. Hau, HH, Walsh, RJ, Ogilvie, RL, Williams, DA, Reilly, CS and Bohjanen, PR (2007). Tristetraprolin recruits functional mRNA decay complexes to ARE sequences. J Cell Biochem 100: 1477-1492.
33. Chrestensen, CA, Schroeder, MJ, Shabanowitz, J, Hunt, DF, Pelo, JW, Worthington, MT et al. (2004). MAPKAP kinase 2 phosphorylates tristetraprolin on in vivo sites including Ser1 78, a site required for 14-3-3 binding. J Biol Chem 279: 10176-10184.
34. Stoecklin, G, Stubbs, T, Kedersha, N, Wax, S, Rigby, WF, Blackwell, TK et al. (2004). MK2-induced tristetraprolin:14-3-3 complexes prevent stress granule association and ARE-mRNA decay. EMBO J 23: 1313-1324.
35. Stoecklin, G, Mayo, T and Anderson, P (2006). ARE-mRNA degradation requires the 5′-3′ decay pathway. EMBO Rep 7: 72-77.
36. Lai, WS, Carballo, E, Strum, JR, Kennington, EA, Phillips, RS and Blackshear, PJ (1999). Evidence that tristetraprolin binds to AU-rich elements and promotes the deadenylation and destabilization of tumor necrosis factor alpha mRNA. Mol Cell Biol 19: 4311-4323.
37. Sun, L, Stoecklin, G, Van Way, S, Hinkovska-Galcheva, V, Guo, RF, Anderson, P et al. (2007). Tristetraprolin (TTP)-l4-3-3 complex formation protects TTP from dephosphorylation by protein phosphatase 2a and stabilizes tumor necrosis factor-alpha mRNA. J Biol Chem 282: 3766-3777.
38. Fairhurst, M, Connolly, JE, Hintz, KA, Goulding, NJ, Rassias, AJ, Yeager, MP et al. (2003). Regulation and localization of endogenous human tristetraprolin. Arthritis Res Ther 5: 11214-11225.
39. Brook, M, Tchen, CR, Santalucia, T, McIlrath, J, Arthur, JS, Salklatvala, J et al. (2006). Posttranslational regulation of tristetraprolin subcellular localization and protein stability by p38 mitogen-activated protein kinase and extracellular signal-regulated kinase pathways. Mol Cell Biol 26: 2408-2418.
40. Deleault, KM, Skinner, SJ and Brooks, SA (2008). Tristetraprolin regulates TNF TNF-alpha mRNA stability via a proteasome dependent mechanism involving the combined action of the ERK and p38 pathways. Mol Immunol 45: 13-24.
41. Lang, R, Hammer, M and Mages, J (2006). DUSP meet immunology: Dual specificity MAPK phosphatases in control of the inflammatory response. J Immunol 177: 7497-7504.
42. Lasa, M, Mahtani, KR, Finch, A, Brewer, G, Saklatvala, J and Clark, AR (2000). Regulation of cyclooxygenase 2 mRNA stability by the mitogen-activated protein kinase p38 signaling cascade. Mol Cell Biol 20: 4265-4274.
43. Jalonen, U, Nieminen, R, Vuolteenaho, K, Kankaanranta, H and Moilanen, E (2006). Down-regulation of tristetraprolin expression results in enhanced IL-12 and MIP-2 production and reduced MIP-3alpha synthesis in activated macrophages. Mediators Inflamm 2006: 40691.
44. Yu, Y, Fan, J, Chen, XS, Wang, D, Klein-Szanto, AJ, Campbell, RL et al. (2006). Genetic model of selective COX2 inhibition reveals novel heterodimer signaling. Nat Med 12: 699-704.
45. Yu, Y and Funk, CD (2007). A novel genetic model of selective COX-2 inhibition: Comparison with COX-2 null mice. Prostaglandins Other Lipid Mediat 82: 77-84.
46. Reddy, ST and Herschman, HR (1994). Ligand-induced prostaglandin synthesis requires expression of the TIS10/PGS-2 prostaglandin synthase gene in murine fibroblasts and macrophages. J Biol Chem 269: 15473-15480.
47. Nishida, E, Hara, Y, Kaneko, T, Ikeda, Y, Ukai, T and Kato, I(2001). Bone resorption and local interleukin-1 alpha and interleukin-1beta synthesis induced by Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis lipopolysaccharide. J Periodontal Res 36: 1-8.
48. Smith, BJ, Lerner, MR, Bu, SY, Lucas, EA, Hanas, JS, Lightfoot, SA et al. (2006). Systemic bone loss and induction of coronary vessel disease in a rat model of chronic inflammation. Bone 38: 378-386.
49. Rehemtulla, A, Stegman, LID, Cardozo, SJ, Gupta, S, Hall, DE, Contag, CH et al. (2000). Rapid and quantitative assessment of cancer treatment response using in vivo bioluminescence imaging. Neoplasia 2: 491-495.
50. Henson, B, Li, F, Coatney, DD, Carey, TE, Mitra, RS, Kirkwood, KL et al. (2007). An orthotopic floor-of-mouth model for locoregional growth and spread of human squamous cell carcinoma. J Oral Pothol Med 36: 363-370.