Tristetraprolin (TTP) coordinately regulates primary and secondary cellular responses to proinflammatory stimuli

Journal of Leukocyte Biology

Volumn 97, Issue 4, 2015, Pages 723-736

  Qiu, Lian Qun ^a   Lai, Wi S ^a   Bradbury, Alyce ^a   Zeldin, Darryl C ^a   Blackshear, Perry J ^a,b  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

AU rich elements; Mouse embryonic fibroblasts; mRNA decay; Tumor necrosis factor

Indexed keywords

CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; MESSENGER RNA; TRISTETRAPROLIN; 3' UNTRANSLATED REGION; CXCL1 PROTEIN, MOUSE; CXCL2 PROTEIN, MOUSE; CYCLOOXYGENASE 2; HYBRID PROTEIN; IEX-1 PROTEIN, MOUSE; IMMEDIATE EARLY PROTEIN; LEUKEMIA INHIBITORY FACTOR; LIF PROTEIN, MOUSE; LIPOPOLYSACCHARIDE; LIPOPOLYSACCHARIDE, E COLI O55-B5; PTGS2 PROTEIN, MOUSE; TOLL LIKE RECEPTOR; TUMOR NECROSIS FACTOR; ZFP36 PROTEIN, MOUSE;

3' UNTRANSLATED REGION; ANIMAL CELL; ARTICLE; BINDING SITE; CELLULAR IMMUNITY; CONTROLLED STUDY; EARLY RESPONSE GENE; EMBRYO; FIBROBLAST; GENETIC TRANSCRIPTION; INFLAMMATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN RNA BINDING; RNA SEQUENCE; AGONISTS; ANIMAL; AU RICH ELEMENT; BIOSYNTHESIS; C57BL MOUSE; CELL CULTURE; DEFICIENCY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HUMAN; KNOCKOUT MOUSE; MACROPHAGE; METABOLISM; NEUTROPHIL CHEMOTAXIS; PATHOPHYSIOLOGY; PHYSIOLOGY; RNA STABILITY;

MUS;

3' UNTRANSLATED REGIONS; ANIMALS; AU RICH ELEMENTS; BINDING SITES; CELLS, CULTURED; CHEMOKINE CXCL1; CHEMOKINE CXCL2; CHEMOTAXIS, LEUKOCYTE; CYCLOOXYGENASE 2; FIBROBLASTS; GENE EXPRESSION REGULATION; HUMANS; IMMEDIATE-EARLY PROTEINS; INFLAMMATION; LEUKEMIA INHIBITORY FACTOR; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECOMBINANT FUSION PROTEINS; RNA STABILITY; RNA, MESSENGER; TOLL-LIKE RECEPTORS; TRANSCRIPTION, GENETIC; TRISTETRAPROLIN; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84929191328     PISSN: 07415400     EISSN: 19383673     Source Type: Journal    
DOI: 10.1189/jlb.3A0214-106R     Document Type: Article

References (44)

1. Lai, W. S., Parker, J. S., Grissom, S. F., Stumpo, D. J., Blackshear, P. J. (2006) Novel mRNA targets for tristetraprolin (TTP) identified by global analysis of stabilized transcripts in TTP-deficient fibroblasts. Mol. Cell. Biol. 26, 9196–9208.
2. Blackshear, P. J., Phillips, R. S., Ghosh, S., Ramos, S. B., Richfield, E. K., Lai, W. S. (2005) Zfp36l3, a rodent X chromosome gene encoding a placenta-specific member of the tristetraprolin family of CCCH tandem zinc finger proteins. Biol. Reprod. 73, 297–307.
3. Carrick, D. M., Lai, W. S., Blackshear, P. J. (2004) The tandem CCCH zinc finger protein tristetraprolin and its relevance to cytokine mRNA turnover and arthritis. Arthritis Res. Ther. 6, 248–264.
4. Brooks, S. A., Blackshear, P. J. (2013) Tristetraprolin (TTP): interactions with mRNA and proteins, and current thoughts on mechanisms of action. Biochim. Biophys. Acta 1829, 666–679.
5. Taylor, G. A., Carballo, E., Lee, D. M., Lai, W. S., Thompson, M. J., Patel, D. D., Schenkman, D. I., Gilkeson, G. S., Broxmeyer, H. E., Haynes, B. F., Blackshear, P. J. (1996) A pathogenetic role for TNF alpha in the syndrome of cachexia, arthritis, and autoimmunity resulting from tristetraprolin (TTP) deficiency. Immunity 4, 445–454.
6. Carballo, E., Lai, W. S., Blackshear, P. J. (1998) Feedback inhibition of macrophage tumor necrosis factor-alpha production by tristetraprolin. Science 281, 1001–1005.
7. Lai, W. S., Carballo, E., Strum, J. R., Kennington, E. A., Phillips, R. S., Blackshear, P. J. (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.
8. Carballo, E., Blackshear, P. J. (2001) Roles of tumor necrosis factor-alpha receptor subtypes in the pathogenesis of the tristetraprolin-deficiency syndrome. Blood 98, 2389–2395.
9. Ghosh, S., Hoenerhoff, M. J., Clayton, N., Myers, P., Stumpo, D. J., Maronpot, R. R., Blackshear, P. J. (2010) Left-sided cardiac valvulitis in tristetraprolin-deficient mice: the role of tumor necrosis factor alpha. Am. J. Pathol. 176, 1484–1493.
10. Flavell, S. J., Hou, T. Z., Lax, S., Filer, A. D., Salmon, M., Buckley, C. D. (2008) Fibroblasts as novel therapeutic targets in chronic inflammation. Br. J. Pharmacol. 153 (Suppl 1), S241–S246.
11. Hao, S., Baltimore, D. (2009) The stability of mRNA influences the temporal order of the induction of genes encoding inflammatory molecules. Nat. Immunol. 10, 281–288.
12. Horner, T. J., Lai, W. S., Stumpo, D. J., Blackshear, P. J. (2009) Stimulation of polo-like kinase 3 mRNA decay by tristetraprolin. Mol. Cell. Biol. 29, 1999–2010.
13. Carballo, E., Gilkeson, G. S., Blackshear, P. J. (1997) Bone marrow transplantation reproduces the tristetraprolin-deficiency syndrome in recombination activating gene-2 (2/2) mice. Evidence that monocyte/ macrophage progenitors may be responsible for TNFalpha overproduction. J. Clin. Invest. 100, 986–995.
14. Qiu, L. Q., Stumpo, D. J., Blackshear, P. J. (2012) Myeloid-specific tristetraprolin deficiency in mice results in extreme lipopolysaccharide sensitivity in an otherwise minimal phenotype. J. Immunol. 188, 5150–5159.
15. Pfaffl, M. W. (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45.
16. Lai, W. S., Carrick, D. M., Blackshear, P. J. (2005) Influence of nonameric AU-rich tristetraprolin-binding sites on mRNA deadenylation and turnover. J. Biol. Chem. 280, 34365–34377.
17. Cao, H., Tuttle, J. S., Blackshear, P. J. (2004) Immunological characterization of tristetraprolin as a low abundance, inducible, stable cytosolic protein. J. Biol. Chem. 279, 21489–21499.
18. Cao, H., Deterding, L. J., Venable, J. D., Kennington, E. A., Yates III J. R., Tomer, K. B., Blackshear, P. J. (2006) Identification of the antiinflammatory protein tristetraprolin as a hyperphosphorylated protein by mass spectrometry and site-directed mutagenesis. Biochem. J. 394, 285–297.
19. Ciais, D., Cherradi, N., Feige, J. J. (2013) Multiple functions of tristetraprolin/TIS11 RNA-binding proteins in the regulation of mRNA biogenesis and degradation. Cell. Mol. Life Sci. 70, 2031–2044.
20. Sanduja, S., Blanco, F. F., Young, L. E., Kaza, V., Dixon, D. A. (2012) The role of tristetraprolin in cancer and inflammation. Front Biosci (Landmark Ed) 17, 174–188.
21. Parsonage, G., Falciani, F., Burman, A., Filer, A., Ross, E., Bofill, M., Martin, S., Salmon, M., Buckley, C. D. (2003) Global gene expression profiles in fibroblasts from synovial, skin and lymphoid tissue reveals distinct cytokine and chemokine expression patterns. Thromb. Haemost. 90, 688–697.
22. Parsonage, G., Filer, A. D., Haworth, O., Nash, G. B., Rainger, G. E., Salmon, M., Buckley, C. D. (2005) A stromal address code defined by fibroblasts. Trends Immunol. 26, 150–156.
23. Jelaska, A., Strehlow, D., Korn, J. H. (1999) Fibroblast heterogeneity in physiological conditions and fibrotic disease. Springer Semin. Immunopathol. 21, 385–395.
24. Datta, S., Biswas, R., Novotny, M., Pavicic, Jr., P. G., Herjan, T., Mandal, P., Hamilton, T. A. (2008) Tristetraprolin regulates CXCL1 (KC) mRNA stability. J. Immunol. 180, 2545–2552.
25. Boisvert, W. A., Rose, D. M., Johnson, K. A., Fuentes, M. E., Lira, S. A., Curtiss, L. K., Terkeltaub, R. A. (2006) Up-regulated expression of the CXCR2 ligand KC/GRO-alpha in atherosclerotic lesions plays a central role in macrophage accumulation and lesion progression. Am. J. Pathol. 168, 1385–1395.
26. Zaja-Milatovic, S., Richmond, A. (2008) CXC chemokines and their receptors: a case for a significant biological role in cutaneous wound healing. Histol. Histopathol. 23, 1399–1407.
27. Koch, A. E. (2005) Chemokines and their receptors in rheumatoid arthritis: future targets? Arthritis Rheum. 52, 710–721.
28. Kratochvill, F., Machacek, C., Vogl, C., Ebner, F., Sedlyarov, V., Gruber, A. R., Hartweger, H., Vielnascher, R., Karaghiosoff, M., Rülicke, T., Müller, M., Hofacker, I., Lang, R., Kovarik, P. (2011) Tristetraprolin-driven regulatory circuit controls quality and timing of mRNA decay in inflammation. Mol. Syst. Biol. 7, 560.
29. Sadik, C. D., Kim, N. D., Luster, A. D. (2011) Neutrophils cascading their way to inflammation. Trends Immunol. 32, 452–460.
30. Beider, K., Abraham, M., Peled, A. (2008) Chemokines and chemokine receptors in stem cell circulation. Front. Biosci. 13, 6820–6833.
31. Dhawan, P., Richmond, A. (2002) Role of CXCL1 in tumorigenesis of melanoma. J. Leukoc. Biol. 72, 9–18.
32. Sawaoka, H., Dixon, D. A., Oates, J. A., Boutaud, O. (2003) Tristetraprolin binds to the 39-untranslated region of cyclooxygenase-2 mRNA. A polyadenylation variant in a cancer cell line lacks the binding site. J. Biol. Chem. 278, 13928–13935.
33. Arlt, A., Schäfer, H. (2011) Role of the immediate early response 3 (IER3) gene in cellular stress response, inflammation and tumorigenesis. Eur. J. Cell Biol. 90, 545–552.
34. Zhu, M., Oishi, K., Lee, S. C., Patterson, P. H. (2001) Studies using leukemia inhibitory factor (LIF) knockout mice and a LIF adenoviral vector demonstrate a key anti-inflammatory role for this cytokine in cutaneous inflammation. J. Immunol. 166, 2049–2054.
35. Young, L. E., Sanduja, S., Bemis-Standoli, K., Pena, E. A., Price, R. L., Dixon, D. A. (2009) The mRNA binding proteins HuR and tristetraprolin regulate cyclooxygenase 2 expression during colon carcinogenesis. Gastroenterology 136, 1669–1679.
36. Sully, G., Dean, J. L., Wait, R., Rawlinson, L., Santalucia, T., Saklatvala, J., Clark, A. R. (2004) Structural and functional dissection of a conserved destabilizing element of cyclo-oxygenase-2 mRNA: evidence against the involvement of AUF-1 [AU-rich element/poly(U)-binding/degradation factor-1], AUF-2, tristetraprolin, HuR (Hu antigen R) or FBP1 (farupstream- sequence-element-binding protein 1). Biochem. J. 377, 629–639.
37. Stoecklin, G., Anderson, P. (2006) Posttranscriptional mechanisms regulating the inflammatory response. Adv. Immunol. 89, 1–37.
38. Eberhardt, W., Doller, A., Akool, el-S., Pfeilschifter, J. (2007) Modulation of mRNA stability as a novel therapeutic approach. Pharmacol. Ther. 114, 56–73.
39. Carballo, E., Lai, W. S., Blackshear, P. J. (2000) Evidence that tristetraprolin is a physiological regulator of granulocyte-macrophage colony-stimulating factor messenger RNA deadenylation and stability. Blood 95, 1891–1899.
40. Armaka, M., Apostolaki, M., Jacques, P., Kontoyiannis, D. L., Elewaut, D., Kollias, G. (2008) Mesenchymal cell targeting by TNF as a common pathogenic principle in chronic inflammatory joint and intestinal diseases. J. Exp. Med. 205, 331–337.
41. Kontoyiannis, D., Pasparakis, M., Pizarro, T. T., Cominelli, F., Kollias, G. (1999) Impaired on/off regulation of TNF biosynthesis in mice lacking TNF AU-rich elements: implications for joint and gut-associated immunopathologies. Immunity 10, 387–398.
42. Tiedje, C., Ronkina, N., Tehrani, M., Dhamija, S., Laass, K., Holtmann, H., Kotlyarov, A., Gaestel, M. (2012) The p38/MK2-driven exchange between tristetraprolin and HuR regulates AU-rich element-dependent translation. PLoS Genet. 8, e1002977.
43. Qi, M. Y., Wang, Z. Z., Zhang, Z., Shao, Q., Zeng, A., Li, X. Q., Li, W. Q., Wang, C., Tian, F. J., Li, Q., Zou, J., Qin, Y. W., Brewer, G., Huang, S., Jing, Q. (2012) AU-rich-element-dependent translation repression requires the cooperation of tristetraprolin and RCK/P 54. Mol. Cell. Biol. 32, 913–928.
44. Rousseau, S., Morrice, N., Peggie, M., Campbell, D. G., Gaestel, M., Cohen, P. (2002) Inhibition of SAPK2a/p38 prevents hnRNP A0 phosphorylation by MAPKAP-K2 and its interaction with cytokine mRNAs. EMBO J. 21, 6505–6514.