Cited by 376

The DOI matches its Crossref record; 5 of the 5 references it cites were found in a registry or an index.

Post-transcriptional control of cytokine production

Anderson, Paul·2008·Nature Immunology

Abstract

The cytokine-encoding messenger RNA (mRNA) molecules transcribed in the nucleus acquire a protein coat that facilitates nuclear export, influences cytoplasmic localization, and determines stability and translational competence. The composition of this coat is determined by sequence elements that recruit proteins that influence the rate of translation and/or mRNA decay. Some of these regulatory proteins direct their associated mRNA molecules to discrete cytoplasmic foci (stress granules and processing bodies) that are essential in 'programming' mRNA 'metabolism'. Studies have begun to identify how these various mechanisms are integrated and regulated to determine the amount of cytokine production in cells involved in immune responses. Understanding of these mechanisms has identified targets for the development of new classes of immunomodulatory drugs.

Overview

Integrity signals

Registry

Crossref · 10.1038/ni1584

Cites

5 of 5 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Verification

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Citations

Cites

Flagged first, then by citations

Show all 5 references

Research works printed but not linked: 102

  1. Stoecklin, G. & Anderson, P. Posttranscriptional mechanisms regulating the inflammatory response. Adv. Immunol. 89, 1–37 (2006). · DOI
  2. Hamilton, T.A. et al. Chemokine and chemoattractant receptor expression: post-transcriptional regulation. J. Leukoc. Biol. 82, 213–219 (2007). · DOI
  3. Khabar, K.S. Rapid transit in the immune cells: the role of mRNA turnover regulation. J. Leukoc. Biol. 81, 1335–1344 (2007). · DOI
  4. Caput, D. et al. Identification of a common nucleotide sequence in the 3′-untranslated region of mRNA molecules specifying inflammatory mediators. Proc. Natl. Acad. Sci. USA 83, 1670–1674 (1986). · DOI
  5. Shaw, G. & Kamen, R. A conserved AU sequence from the 3′ untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell 46, 659–667 (1986). · DOI
  6. Stoecklin, G. et al. Genome-wide analysis identifies interleukin-10 mRNA as target of tristetraprolin. J. Biol. Chem. published online 6 February 2008 (doi:10.1074/jbc.M709657200). · DOI
  7. Chen, C.Y.A., Xu, N. & Shyu, A.B. mRNA decay mediated by two distinct AU-rich elements from c-fos and granulocyte-macrophage colony-stimulating factor transcripts: Different deadenylation kinetics and uncoupling from translation. Mol. Cell. Biol. 15, 5777–5788 (1995). · DOI · Paper page
  8. Lagnado, C.A., Brown, C.Y. & Goodall, G.J. AUUUA is not sufficient to promote poly(A) shortening and degradation of an mRNA: the functional sequence within AU-rich elements may be UUAUUUA(U/A)(U/A). Mol. Cell. Biol. 14, 7984–7995 (1994).
  9. Zubiaga, A.M., Belasco, J.G. & Greenberg, M.E. The nonamer UUAUUUAUU is the key AU-rich sequence motif that mediates mRNA degradation. Mol. Cell. Biol. 15, 2219–2230 (1995). · DOI
  10. Blackshear, P.J. et al. 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 (2003). · DOI
  11. Worthington, M.T. et al. RNA binding properties of the AU-rich element-binding recombinant Nup475/TIS11/tristetraprolin protein. J. Biol. Chem. 277, 48558–48564 (2002). · DOI
  12. Lopez de Silanes, I. et al. Identification and functional outcome of mRNAs associated with RNA-binding protein TIA-1. Mol. Cell. Biol. 25, 9520–9531 (2005). · DOI
  13. Piecyk, M. et al. TIA-1 is a translational silencer that selectively regulates the expression of TNF-α. EMBO J. 19, 4154–4163 (2000). · DOI
  14. Garnon, J. et al. Fragile X-related protein FXR1P regulates proinflammatory cytokine tumor necrosis factor expression at the post-transcriptional level. J. Biol. Chem. 280, 5750–5763 (2005). · DOI
  15. Mukhopadhyay, D., Houchen, C.W., Kennedy, S., Dieckgraefe, B.K. & Anant, S. Coupled mRNA stabilization and translational silencing of cyclooxygenase-2 by a novel RNA binding protein, CUGBP2. Mol. Cell 11, 113–126 (2003). · DOI
  16. Carballo, E., Lai, W.S. & Blackshear, P.J. Feedback inhibition of macrophage tumor necrosis factor-α production by tristetraprolin. Science 281, 1001–1005 (1998). · DOI
  17. Stoecklin, G. et al. Functional cloning of BRF1, a regulator of ARE-dependent mRNA turnover. EMBO J. 21, 4709–4718 (2002). · DOI
  18. Chou, C.F. et al. Tethering KSRP, a decay-promoting AU-rich element-binding protein, to mRNAs elicits mRNA decay. Mol. Cell. Biol. 26, 3695–3706 (2006). · DOI
  19. Gherzi, R. et al. A KH domain RNA binding protein, KSRP, promotes ARE-directed mRNA turnover by recruiting the degradation machinery. Mol. Cell 14, 571–583 (2004). · DOI
  20. Laroia, G., Cuesta, R., Brewer, G. & Schneider, R.J. Control of mRNA decay by heat shock-ubiquitin-proteasome pathway. Science 284, 499–502 (1999). · DOI
  21. Lu, J.Y., Bergman, N., Sadri, N. & Schneider, R.J. Assembly of AUF1 with eIF4G-poly(A) binding protein complex suggests a translation function in AU-rich mRNA decay. RNA 12, 883–893 (2006). · DOI
  22. Lu, J.Y., Sadri, N. & Schneider, R.J. Endotoxic shock in AUF1 knockout mice mediated by failure to degrade proinflammatory cytokine mRNAs. Genes Dev. 20, 3174–3184 (2006). · DOI
  23. Sarkar, B., Xi, Q., He, C. & Schneider, R.J. Selective degradation of AU-rich mRNAs promoted by the p37 AUF1 protein isoform. Mol. Cell. Biol. 23, 6685–6693 (2003). · DOI
  24. Fan, X.C. & Steitz, J.A. Overexpression of HuR, a nuclear-cytoplasmic shuttling protein, increases the in vivo stability of ARE-containing mRNAs. EMBO J. 17, 3448–3460 (1998). · DOI · Paper page
  25. Peng, S.S., Chen, C.Y., Xu, N. & Shyu, A.B. RNA stabilization by the AU-rich element binding protein, HuR, an ELAV protein. EMBO J. 17, 3461–3470 (1998). · DOI
  26. Galban, S. et al. RNA-binding proteins HuR and PTB promote the translation of hypoxia-inducible factor-1α. Mol. Cell Biol. 28, 93–107 (2007). · DOI
  27. Katsanou, V. et al. HuR as a negative posttranscriptional modulator in inflammation. Mol. Cell 19, 777–789 (2005). · DOI
  28. Kawai, T. et al. Translational control of cytochrome c by RNA-binding proteins TIA-1 and HuR. Mol. Cell. Biol. 26, 3295–3307 (2006). · DOI
  29. Sureban, S.M. et al. Functional antagonism between RNA binding proteins HuR and CUGBP2 determines the fate of COX-2 mRNA translation. Gastroenterology 132, 1055–1065 (2007). · DOI
  30. Linker, K. et al. Involvement of KSRP in the post-transcriptional regulation of human iNOS expression-complex interplay of KSRP with TTP and HuR. Nucleic Acids Res. 33, 4813–4827 (2005). · DOI
  31. David, P.S., Tanveer, R. & Port, J.D. FRET-detectable interactions between the ARE binding proteins, HuR and p37AUF1. RNA 13, 1453–1468 (2007). · DOI · Paper page
  32. Pan, Y.X., Chen, H. & Kilberg, M.S. Interaction of RNA-binding proteins HuR and AUF1 with the human ATF3 mRNA 3′-untranslated region regulates its amino acid limitation-induced stabilization. J. Biol. Chem. 280, 34609–34616 (2005). · DOI
  33. Yamasaki, S., Stoecklin, G., Kedersha, N., Simarro, M. & Anderson, P. T-cell intracellular antigen-1 (TIA-1)-induced translational silencing promotes the decay of selected mRNAs. J. Biol. Chem. 282, 30070–30077 (2007). · DOI
  34. Rothe, F., Gueydan, C., Bellefroid, E., Huez, G. & Kruys, V. Identification of FUSE-binding proteins as interacting partners of TIA proteins. Biochem. Biophys. Res. Commun. 343, 57–68 (2006). · DOI
  35. Liao, B., Hu, Y. & Brewer, G. Competitive binding of AUF1 and TIAR to MYC mRNA controls its translation. Nat. Struct. Mol. Biol. 14, 511–518 (2007). · DOI
  36. Chrestensen, C.A. et al. MAPKAP kinase 2 phosphorylates tristetraprolin on in vivo sites including Ser178, a site required for 14–3-3 binding. J. Biol. Chem. 279, 10176–10184 (2004). · DOI
  37. Stoecklin, G., Stubbs, T., Kedersha, N., Blackwell, T.K. & Anderson, P. MK2-induced tristetraprolin:14–3-3 complexes prevent stress granule association and ARE-mRNA decay. EMBO J. 23, 1313–1324 (2004). · DOI · Paper page
  38. Sun, L. et al. Tristetraprolin (TTP)-14–3-3 complex formation protects TTP from dephosphorylation by protein phosphatase 2a and stabilizes tumor necrosis factor-alpha mRNA. J. Biol. Chem. 282, 3766–3777 (2007). · DOI
  39. Schmidlin, M. et al. The ARE-dependent mRNA-destabilizing activity of BRF1 is regulated by protein kinase B. EMBO J. 23, 4760–4769 (2004). · DOI
  40. Benjamin, D., Schmidlin, M., Min, L., Gross, B. & Moroni, C. BRF1 protein turnover and mRNA decay activity are regulated by protein kinase B at the same phosphorylation sites. Mol. Cell. Biol. 26, 9497–9507 (2006). · DOI
  41. Gherzi, R. et al. The RNA-binding protein KSRP promotes decay of β-catenin mRNA and is inactivated by PI3K-AKT signaling. PLoS Biol. 5, e5 (2006). · DOI
  42. He, C. & Schneider, R. 14–3-3sigma is a p37 AUF1-binding protein that facilitates AUF1 transport and AU-rich mRNA decay. EMBO J. 25, 3823–3831 (2006). · DOI
  43. Pyronnet, S. et al. Human eukaryotic translation initiation factor 4G (eIF4G) recruits Mnk1 to phosphorylate eIF4E. EMBO J. 18, 270–279 (1999). · DOI
  44. Waskiewicz, A.J. et al. Phosphorylation of the cap-binding protein eukaryotic translation initiation factor 4E by protein kinase Mnk1 in vivo. Mol. Cell. Biol. 19, 1871–1880 (1999). · DOI
  45. Buxade, M. et al. The Mnks are novel components in the control of TNFα biosynthesis and phosphorylate and regulate hnRNP A1. Immunity 23, 177–189 (2005). · DOI
  46. Esnault, S. et al. Pin1 modulates the type 1 immune response. PLoS ONE 2, e226 (2007). · DOI
  47. Shen, Z.J., Esnault, S. & Malter, J.S. The peptidyl-prolyl isomerase Pin1 regulates the stability of granulocyte-macrophage colony-stimulating factor mRNA in activated eosinophils. Nat. Immunol. 6, 1280–1287 (2005). · DOI
  48. Esnault, S. et al. A critical role for Pin1 in allergic pulmonary eosinophilia in rats. J. Allergy Clin. Immunol. 120, 1082–1088 (2007). · DOI
  49. Greenwald, R.J., Freeman, G.J. & Sharpe, A.H. The B7 family revisited. Annu. Rev. Immunol. 23, 515–548 (2005). · DOI · Paper page
  50. Sharpe, A.H., Wherry, E.J., Ahmed, R. & Freeman, G.J. The function of programmed cell death 1 and its ligands in regulating autoimmunity and infection. Nat. Immunol. 8, 239–245 (2007). · DOI
  51. Lindstein, T., June, C.H., Ledbetter, J.A., Stella, G. & Thompson, C.B. Regulation of lymphokine messenger RNA stability by a surface-mediated T cell activation pathway. Science 244, 339–343 (1989). · DOI
  52. Sanchez-Lockhart, M. & Miller, J. Engagement of CD28 outside of the immunological synapse results in up-regulation of IL-2 mRNA stability but not IL-2 transcription. J. Immunol. 176, 4778–4784 (2006). · DOI
  53. Mestas, J., Crampton, S.P., Hori, T. & Hughes, C.C. Endothelial cell co-stimulation through OX40 augments and prolongs T cell cytokine synthesis by stabilization of cytokine mRNA. Int. Immunol. 17, 737–747 (2005). · DOI
  54. Wang, J.G. et al. LFA-1-dependent HuR nuclear export and cytokine mRNA stabilization in T cell activation. J. Immunol. 176, 2105–2113 (2006). · DOI
  55. Stoecklin, G., Lu, M., Rattenbacher, B. & Moroni, C. A constitutive decay element promotes tumor necrosis factor α mRNA degradation via an AU-rich element-independent pathway. Mol. Cell. Biol. 23, 3506–3515 (2003). · DOI
  56. Brown, C.Y., Lagnado, C.A. & Goodall, G.J. A cytokine mRNA-destabilizing element that is structurally and functionally distinct from A+U-rich elements. Proc. Natl. Acad. Sci. USA 93, 13721–13725 (1996). · DOI
  57. Shim, J. & Lim, H. J, R.Y. & Karin, M. Nuclear export of NF90 is required for interleukin-2 mRNA stabilization. Mol. Cell 10, 1331–1344 (2002). · DOI
  58. Chen, C.Y. et al. Nucleolin and YB-1 are required for JNK-mediated interleukin-2 mRNA stabilization during T-cell activation. Genes Dev. 14, 1236–1248 (2000). · DOI
  59. Jing, Q. et al. Involvement of microRNA in AU-rich element-mediated mRNA instability. Cell 120, 623–634 (2005). · DOI
  60. Pillai, R.S., Artus, C.G. & Filipowicz, W. Tethering of human Ago proteins to mRNA mimics the miRNA-mediated repression of protein synthesis. RNA 10, 1518–1525 (2004). · DOI
  61. Vasudevan, S., Tong, Y. & Steitz, J.A. Switching from repression to activation: microRNAs can up-regulate translation. Science 318, 1931–1934 (2007). · DOI
  62. O'Connell, R.M., Taganov, K.D., Boldin, M.P., Cheng, G. & Baltimore, D. MicroRNA-155 is induced during the macrophage inflammatory response. Proc. Natl. Acad. Sci. USA 104, 1604–1609 (2007). · DOI · Paper page
  63. Thai, T.H. et al. Regulation of the germinal center response by microRNA-155. Science 316, 604–608 (2007). · DOI
  64. Vigorito, E. et al. MicroRNA-155 regulates the generation of immunoglobulin class-switched plasma cells. Immunity 27, 847–859 (2007). · DOI
  65. Leung, A.K., Calabrese, J.M. & Sharp, P.A. Quantitative analysis of Argonaute protein reveals microRNA-dependent localization to stress granules. Proc. Natl. Acad. Sci. USA 103, 18125–18130 (2006). · DOI
  66. Liu, J. et al. A role for the P-body component GW182 in microRNA function. Nat. Cell Biol. 7, 1161–1166 (2005). · DOI
  67. Liu, J., Valencia-Sanchez, M.A., Hannon, G.J. & Parker, R. MicroRNA-dependent localization of targeted mRNAs to mammalian P-bodies. Nat. Cell Biol. 7, 719–723 (2005). · DOI · Paper page
  68. Anderson, P. & Kedersha, N. Stress granules: the Tao of RNA triage. Trends Biochem. Sci. published online 19 February 2008 (doi:10.1016/j.tibs.2007.12.003). · DOI
  69. Parker, R. & Sheth, U. P bodies and the control of mRNA translation and degradation. Mol. Cell 25, 635–646 (2007). · DOI · Paper page
  70. Kedersha, N. et al. Stress granules and processing bodies are dynamically liked sites of mRNP remodeling. J. Cell Biol. 169, 871–884 (2005). · DOI
  71. Stohr, N. et al. ZBP1 regulates mRNA stability during cellular stress. J. Cell Biol. 175, 527–534 (2006). · DOI
  72. Franks, T.M. & Lykke-Andersen, J. TTP and BRF proteins nucleate processing body formation to silence mRNAs with AU-rich elements. Genes Dev. 21, 719–735 (2007). · DOI
  73. Stoecklin, G. & Anderson, P. In a tight spot: ARE-mRNAs at processing bodies. Genes Dev. 21, 627–631 (2007). · DOI
  74. Bhattacharyya, S.N., Habermacher, R., Martine, U., Closs, E.I. & Filipowicz, W. Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell 125, 1111–1124 (2006). · DOI
  75. Scheu, S. et al. Activation of the integrated stress response during T helper cell differentiation. Nat. Immunol. 7, 644–651 (2006). · DOI
  76. Yu, D. et al. Roquin represses autoimmunity by limiting inducible T-cell co-stimulator mRNA. Nature 450, 299–303 (2007). · DOI
  77. Munn, D.H. et al. GCN2 kinase in T cells mediates proliferative arrest and anergy induction in response to indoleamine 2,3-dioxygenase. Immunity 22, 633–642 (2005). · DOI
  78. MacKenzie, C.R., Heseler, K., Muller, A. & Daubener, W. Role of indoleamine 2,3-dioxygenase in antimicrobial defence and immuno-regulation: tryptophan depletion versus production of toxic kynurenines. Curr. Drug Metab. 8, 237–244 (2007). · DOI
  79. Munn, D.H. & Mellor, A.L. Indoleamine 2,3-dioxygenase and tumor-induced tolerance. J. Clin. Invest. 117, 1147–1154 (2007). · DOI
  80. Sedlmayr, P. Indoleamine 2,3-dioxygenase in materno-fetal interaction. Curr. Drug Metab. 8, 205–208 (2007). · DOI
  81. Gaestel, M., Mengel, A., Bothe, U. & Asadullah, K. Protein kinases as small molecule inhibitor targets in inflammation. Curr. Med. Chem. 14, 2214–2234 (2007). · DOI
  82. Schett, G., Zwerina, J. & Firestein, G. The p38 mitogen activated protein kinase (MAPK) pathway in rheumatoid arthritis. Ann. Rheum. Dis., published online 7 September 2007 (doi:10.1136/ard.2007.074278). · DOI
  83. Johansen, C. et al. Protein expression of TNF-α in psoriatic skin is regulated at a posttranscriptional level by MAPK-activated protein kinase 2. J. Immunol. 176, 1431–1438 (2006). · DOI
  84. Hegen, M., Gaestel, M., Nickerson-Nutter, C.L., Lin, L.L. & Telliez, J.B. MAPKAP kinase 2-deficient mice are resistant to collagen-induced arthritis. J. Immunol. 177, 1913–1917 (2006). · DOI
  85. Ding, C. Drug evaluation: VX-702, a MAP kinase inhibitor for rheumatoid arthritis and acute coronary syndrome. Curr. Opin. Investig. Drugs 7, 1020–1025 (2006).
  86. Schreiber, S. et al. Oral p38 mitogen-activated protein kinase inhibition with BIRB 796 for active Crohn's disease: a randomized, double-blind, placebo-controlled trial. Clin. Gastroenterol. Hepatol. 4, 325–334 (2006). · DOI
  87. Esnault, S., Shen, Z.J., Whitesel, E. & Malter, J.S. The peptidyl-prolyl isomerase Pin1 regulates granulocyte-macrophage colony-stimulating factor mRNA stability in T lymphocytes. J. Immunol. 177, 6999–7006 (2006). · DOI
  88. Chen, Y.L. et al. Differential regulation of ARE-mediated TNFα and IL-1β mRNA stability by lipopolysaccharide in RAW264.7 cells. Biochem. Biophys. Res. Commun. 346, 160–168 (2006). · DOI
  89. Bufler, P., Gamboni-Robertson, F., Azam, T., Kim, S.H. & Dinarello, C.A. Interleukin-1 homologues IL-1F7b and IL-18 contain functional mRNA instability elements within the coding region responsive to lipopolysaccharide. Biochem. J. 381, 503–510 (2004). · DOI
  90. Ogilvie, R.L. et al. Tristetraprolin down-regulates IL-2 gene expression through AU-rich element-mediated mRNA decay. J. Immunol. 174, 953–961 (2005). · DOI
  91. Shi, L., Godfrey, W., Lin, J., Zhao, G. & Kao, P. NF90 regulates inducible IL-2 gene expression in T cells. J. Exp. Med. 204, 971–977 (2007). · DOI
  92. Stoecklin, G., Ming, X.F., Looser, R. & Moroni, C. Somatic mRNA turnover mutants implicate tristetraprolin in the interleukin-3 mRNA degradation pathway. Mol. Cell. Biol. 20, 3753–3763 (2000). · DOI
  93. Yarovinsky, T.O., Butler, N.S., Monick, M.M. & Hunninghake, G.W. Early exposure to IL-4 stabilizes IL-4 mRNA in CD4+ T cells via RNA-binding protein HuR. J. Immunol. 177, 4426–4435 (2006). · DOI
  94. Neininger, A. et al. 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 (2002). · DOI
  95. Paschoud, S. et al. Destabilization of interleukin-6 mRNA requires a putative RNA stem-loop structure, an AU-rich element, and the RNA-binding protein AUF1. Mol. Cell. Biol. 26, 8228–8241 (2006). · DOI · Paper page
  96. Winzen, R. et al. Functional analysis of KSRP interaction with the AU-rich element of interleukin-8 and identification of inflammatory mRNA targets. Mol. Cell. Biol. 27, 8388–8400 (2007). · DOI
  97. Bamba, S. et al. Regulation of IL-11 expression in intestinal myofibroblasts: role of c-Jun AP-1- and MAPK-dependent pathways. Am. J. Physiol. Gastrointest. Liver Physiol. 285, G529–G538 (2003). · DOI
  98. Carballo, E., Lai, W.S. & Blackshear, P.J. Evidence that tristetraprolin is a physiological regulator of granulocyte-macrophage colony-stimulating factor messenger RNA deadenylation and stability. Blood 95, 1891–1899 (2000). · DOI
  99. Grosset, C. et al. In vivo studies of translational repression mediated by the granulocyte-macrophage colony-stimulating factor AU-rich element. J. Biol. Chem. 279, 13354–13362 (2004). · DOI
  100. Putland, R.A. et al. RNA destabilization by the granulocyte colony-stimulating factor stem-loop destabilizing element involves a single stem-loop that promotes deadenylation. Mol. Cell. Biol. 22, 1664–1673 (2002). · DOI
  101. Whittemore, L.A. & Maniatis, T. Postinduction turnoff of β-interferon gene expression. Mol. Cell. Biol. 10, 1329–1337 (1990).
  102. Mavropoulos, A., Sully, G., Cope, A.P. & Clark, A.R. Stabilization of IFN-γ mRNA by MAPK p38 in IL-12- and IL-18-stimulated human NK cells. Blood 105, 282–288 (2005). · DOI

Cited by

Sorted by citations

See all 376

Metadata

Authors
Anderson, P.
Venue
Nature Immunology
Published
2008-03-18
Volume
9
Issue
4
Pages
353-359
ISSN
  • 1529-2908
  • 1529-2916
Cited by
376
References
5
Language
en

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review