Multilevel regulation of HIF-1 signaling by TTP

Molecular Biology of the Cell

Volumn 23, Issue 20, 2012, Pages 4129-4141

  Fähling, Michael ^a   Persson, Anja Bondke ^a   Klinger, Bertram ^a,b   Benko, Edgar ^a   Steege, Andreas ^c   Kasim, Mumtaz ^a   Patzak, Andreas ^a   Persson, Pontus B ^a   Wolf, Gunter ^d   Blüthgen, Nils ^a,b   Mrowka, Ralf ^a,d  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b HUMBOLDT UNIVERSITY   (Germany)

^c UNIVERSITY HOSPITAL REGENSBURG   (Germany)

^d JENA UNIVERSITY HOSPITAL   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HYPOXIA INDUCIBLE FACTOR 1; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; TRISTETRAPROLIN;

3' UNTRANSLATED REGION; ARTICLE; CELL DIFFERENTIATION; CELL MIGRATION; CONTROLLED STUDY; GENE EXPRESSION; GENOME; HUMAN; HUMAN CELL; HYPOXIA; MACROPHAGE; MATHEMATICAL MODEL; MONOCYTE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION;

3' UNTRANSLATED REGIONS; ANIMALS; AU RICH ELEMENTS; CELL DIFFERENTIATION; CONSERVED SEQUENCE; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MACROPHAGES; MICE; MODELS, BIOLOGICAL; MONOCYTES; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PROTEIN BINDING; RNA, MESSENGER; SIGNAL TRANSDUCTION; TETRADECANOYLPHORBOL ACETATE; TRISTETRAPROLIN;

EID: 84867467818     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-11-0949     Document Type: Article

References (53)

1. Al Souhibani N, Al Ahmadi W, Hesketh JE, Blackshear PJ, Khabar KS (2010). The RNA-binding zinc-finger protein tristetraprolin regulates AU-rich mRNAs involved in breast cancer-related processes. Oncogene 29, 4205-4215.
2. Auwerx J (1991). The human leukemia cell line, THP-1: a multifacetted model for the study of monocyte-macrophage differentiation. Experientia 47, 22-31.
3. Bakheet T, Frevel M, Williams BR, Greer W, Khabar KS (2001). ARED: human AU-rich element-containing mRNA database reveals an unexpectedly diverse functional repertoire of encoded proteins. Nucleic Acids Res 29, 246-254. (Pubitemid 32054460)
4. Barreau C, Paillard L, Osborne HB (2005). AU-rich elements and associated factors: are there unifying principles? Nucleic Acids Res 33, 7138-7150. (Pubitemid 43125082)
5. Bermudez O, Jouandin P, Rottier J, Bourcier C, Pagès G, Gimond C (2011). Post-transcriptional regulation of the DUSP6/MKP-3 phosphatase by MEK/ERK signaling and hypoxia. J Cell Physiol 226, 276-84.
6. Bevilacqua A, Ceriani MC, Capaccioli S, Nicolin A (2003). Post-transcriptional regulation of gene expression by degradation of messenger RNAs. J Cell Physiol 195, 356-372. (Pubitemid 36529864)
7. Brook M, Tchen CR, Santalucia T, McIlrath J, Arthur JS, Saklatvala J, Clark AR (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. (Pubitemid 43346939)
8. Brooks SA, Connolly JE, Rigby WF (2004). The role of mRNA turnover in the regulation of tristetraprolin expression: evidence for an extracellular signal-regulated kinase-specific, AU-rich element-dependent, autoregulatory pathway. J Immunol 172, 7263-7271. (Pubitemid 38747585)
9. Bruggeman FJ, Westerhoff HV, Hoek JB, Kholodenko BN (2002). Modular response analysis of cellular regulatory networks. J Theor Biol 218, 507-520. (Pubitemid 35286349)
10. Cao H, Deterding LJ, Venable JD, Kennington EA, Yates JR III, Tomer KB, Blackshear PJ (2006). Identification of the anti-inflammatory protein tristetraprolin as a hyperphosphorylated protein by mass spectrometry and site-directed mutagenesis. Biochem J 394, 285-297. (Pubitemid 43259679)
11. Carballo E, Cao H, Lai WS, Kennington EA, Campbell D, Blackshear PJ (2001). Decreased sensitivity of tristetraprolin-deficient cells to p38 inhibitors suggests the involvement of tristetraprolin in the p38 signaling pathway. J Biol Chem 276, 42580-42587.
12. Carballo E, Lai WS, Blackshear PJ (1998). Feedback inhibition of macrophage tumor necrosis factor-alpha production by tristetraprolin. Science 281, 1001-1005. (Pubitemid 28399252)
13. Carmeliet P (2005). Angiogenesis in life, disease and medicine. Nature 438, 932-936.
14. Castrop H, Kurtz A (2010). Functional evidence confirmed by histological localization: overlapping expression of erythropoietin and HIF-2alpha in interstitial fibroblasts of the renal cortex. Kidney Int 77, 269-271.
15. Chamboredon S, Ciais D, Desroches-Castan A, Savi P, Bono F, Feige JJ, Cherradi N (2011). Hypoxia-inducible factor-1{alpha} mRNA: a new target for destabilization by tristetraprolin in endothelial cells. Mol Biol Cell 22, 3366-3378.
16. Clement SL, Scheckel C, Stoecklin G, Lykke-Andersen J (2011). Phosphorylation of tristetraprolin by MK2 impairs AU-rich element mRNA decay by preventing deadenylase recruitment. Mol Cell Biol 31, 256-266.
17. Cramer T et al. (2003). HIF-1alpha is essential for myeloid cell-mediated inflammation. Cell 112, 645-657. (Pubitemid 36331777)
18. Demeter J et al. (2007). The Stanford Microarray Database: implementation of new analysis tools and open source release of software. Nucleic Acids Res 35, D766-D770. (Pubitemid 46056307)
19. Eltzschig HK, Carmeliet P (2011). Hypoxia and inflammation. N Engl J Med 364, 656-665.
20. Fähling M, Mrowka R, Steege A, Martinka P, Persson PB, Thiele BJ (2006a). Heterogeneous nuclear ribonucleoprotein-A2/B1 modulate collagen prolyl 4-hydroxylase, {alpha} (I) mRNA stability. J Biol Chem 281, 9279-9286. (Pubitemid 43864643)
21. Fähling M, Mrowka R, Steege A, Nebrich G, Perlewitz A, Persson PB, Thiele BJ (2006b). Translational control of collagen prolyl 4-hydroxylase- alpha(I) gene expression under hypoxia. J Biol Chem. 281, 26089-26101. (Pubitemid 44401815)
22. Frede S, Berchner-Pfannschmidt U, Fandrey J (2007). Regulation of hypoxia-inducible factors during inflammation. Methods Enzymol 435, 405-419.
23. Galban S, Gorospe M (2009). Factors interacting with HIF-1alpha mRNA: novel therapeutic targets. Curr Pharm Des 15, 3853-3860.
24. Gorospe M, Tominaga K, Wu X, Fähling M, Ivan M (2011). Post-transcriptional control of the hypoxic response by RNA-binding proteins and microRNAs. Front Mol Neurosci 4, 7.
25. Hitti E, Iakovleva T, Brook M, Deppenmeier S, Gruber AD, Radzioch D, Clark AR, Blackshear PJ, Kotlyarov A, Gaestel M (2006). Mitogen-activated protein kinase-activated protein kinase 2 regulates tumor necrosis factor mRNA stability and translation mainly by altering tristetraprolin expression, stability, binding to adenine/uridine-rich element. Mol Cell Biol 26, 2399-2407. (Pubitemid 43346938)
26. Johnson BA, Stehn JR, Yaffe MB, Blackwell TK (2002). Cytoplasmic localization of tristetraprolin involves 14-3-3-dependent and -independent mechanisms. J Biol Chem 277, 18029-18036. (Pubitemid 34967615)
27. Kappert K et al. (2009). Chronic treatment with losartan results in sufficient serum levels of the metabolite EXP3179 for PPARgamma activation. Hypertension 54, 738-743.
28. Kholodenko BN, Kiyatkin A, Bruggeman FJ, Sontag E, Westerhoff HV, Hoek JB (2002). Untangling the wires: a strategy to trace functional interactions in signaling and gene networks. Proc Natl Acad Sci USA 99, 12841-12846.
29. Kim TW, Yim S, Choi BJ, Jang Y, Lee JJ, Sohn BH, Yoo HS, Yeom YI, Park KC (2010). Tristetraprolin regulates the stability of HIF-1alpha mRNA during prolonged hypoxia. Biochem Biophys Res Commun 391, 963-968.
30. Kuersten S, Goodwin EB (2003). The power of the 3′ UTR: translational control and development. Nat Rev Genet 4, 626-637. (Pubitemid 36917504)
31. Kuschel A, Simon P, Tug S (2012). Functional regulation of HIF-1α under normoxia-is there more than post-translational regulation? J Cell Physiol 227, 514-24.
32. Lai WS, Parker JS, Grissom SF, Stumpo DJ, Blackshear PJ (2006). Novel mRNA targets for tristetraprolin (TTP) identified by global analysis of stabilized transcripts in TTP-deficient fibroblasts. Mol Cell Biol 26, 9196-9208. (Pubitemid 44904416)
33. Mrowka R, Bluthgen N, Fähling M (2008). Seed-based systematic discovery of specific transcription factor target genes. FEBS J 275, 3178-3192. (Pubitemid 351743593)
34. Niranjanakumari S, Lasda E, Brazas R, Garcia-Blanco MA (2002). Reversible cross-linking combined with immunoprecipitation to study RNA-protein interactions in vivo. Methods 26, 182-190. (Pubitemid 34969580)
35. Oda T et al. (2006). Activation of hypoxia-inducible factor 1 during macrophage differentiation. Am J Physiol Cell Physiol 291, C104-C113.
36. Ono M (2008). Molecular links between tumor angiogenesis and inflammation: inflammatory stimuli of macrophages and cancer cells as targets for therapeutic strategy. Cancer Sci 99, 1501-1506.
37. Rossignol F, Vache C, Clottes E (2002). Natural antisense transcripts of hypoxia-inducible factor 1alpha are detected in different normal and tumour human tissues. Gene 299, 135-140. (Pubitemid 35379835)
38. Sandler H, Stoecklin G (2008). Control of mRNA decay by phosphorylation of tristetraprolin. Biochem Soc Trans 36, 491-496. (Pubitemid 351839361)
39. Schreiber E, Matthias P, Muller MM, Schaffner W (1989). Rapid detection of octamer binding proteins with 'mini-extracts', prepared from a small number of cells. Nucleic Acids Res 17, 6419. (Pubitemid 19198635)
40. Schnoor M, Buers I, Sietmann A, Brodde MF, Hofnagel O, Robenek H, Lorkowski S (2009). Efficient non-viral transfection of THP-1 cells. J Immunol Methods 344, 109-115.
41. Semenza GL (2003). Targeting HIF-1 for cancer therapy. Nat Rev Cancer 3, 721-732.
42. Semenza GL (2007). Hypoxia-inducible factor 1 (HIF-1) pathway. Sci STKE 2007, cm8.
43. Shabalina SA, Ogurtsov AY, Lipman DJ, Kondrashov AS (2003). Patterns in interspecies similarity correlate with nucleotide composition in mammalian 3′ UTRs. Nucleic Acids Res 31, 5433-5439. (Pubitemid 37441912)
44. Sheflin LG, Zou AP, Spaulding SW (2004). Androgens regulate the binding of endogenous HuR to the AU-rich 3′ UTRs of HIF-1alpha and EGF mRNA. Biochem Biophys Res Commun 322, 644-651. (Pubitemid 39490351)
45. Siepel A et al. (2005). Evolutionarily conserved elements in vertebrate, insect, worm, yeast genomes. Genome Res 15, 1034-1050. (Pubitemid 41126859)
46. Stoecklin G, Stubbs T, Kedersha N, Wax S, Rigby WF, Blackwell TK, Anderson P (2004). MK2-induced tristetraprolin:14-3-3 complexes prevent stress granule association and ARE-mRNA decay. EMBO J 23, 1313-1324. (Pubitemid 38525003)
47. Stoecklin G, Tenenbaum SA, Mayo T, Chittur SV, George AD, Baroni TE, Blackshear PJ, Anderson P (2008). Genome-wide analysis identifies interleukin-10 mRNA as target of tristetraprolin. J Biol Chem 283, 11689-11699.
48. Stuart JM, Segal E, Koller D, Kim SK (2003). A gene-coexpression network for global discovery of conserved genetic modules. Science 302, 249-255. (Pubitemid 37248749)
49. Taylor GA et al. (1996). A pathogenetic role for TNF alpha in the syndrome of cachexia, arthritis, autoimmunity resulting from tristetraprolin (TTP) deficiency. Immunity 4, 445-454. (Pubitemid 26354654)
50. Tiedje C, Kotlyarov A, Gaestel M (2010). Molecular mechanisms of phosphorylation-regulated TTP (tristetraprolin) action and screening for further TTP-interacting proteins. Biochem Soc Trans 38, 1632-1637.
51. Tudor C, Marchese FP, Hitti E, Aubareda A, Rawlinson L, Gaestel M, Blackshear PJ, Clark AR, Saklatvala J, Dean JL (2009). The p38 MAPK pathway inhibits tristetraprolin-directed decay of interleukin-10 and pro-inflammatory mediator mRNAs in murine macrophages. FEBS Lett 583, 1933-1938.
52. Zhang T, Kruys V, Huez G, Gueydan C (2002). AU-rich element-mediated translational control: complexity and multiple activities of trans-activating factors. Biochem Soc Trans 30, 952-958. (Pubitemid 36002387)
53. Zhao W, Liu M, D'Silva NJ, Kirkwood KL (2011). Tristetraprolin regulates interleukin-6 expression through p38 MAPK-dependent affinity changes with mRNA 3′ untranslated region. J Interferon Cytokine Res 31, 629-637.