Nitric oxide activation of Erk1/2 regulates the stability and translation of mRNA transcripts containing CU-rich elements

Nucleic Acids Research

Volumn 34, Issue 10, 2006, Pages 3044-3056

  Wang, Shuibang ^a   Zhang, Jianhua ^a   Theel, Stephanie ^a   Barb, Jennifer J ^a   Munson, Peter J ^a   Danner, Robert L ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 HYDROXYPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; DACTINOMYCIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; NITRIC OXIDE; CYTOSINE; HETEROGENEOUS NUCLEAR RIBONUCLEOPROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; URACIL;

3' UNTRANSLATED REGION; ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; ENZYME INHIBITION; GENE ACTIVATION; GENE LOCATION; GENE OVEREXPRESSION; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN MICROARRAY; REGULATORY MECHANISM; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA STABILITY; RNA TRANSLATION; UNINDEXED SEQUENCE; CELL LINE; CHEMISTRY; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; METABOLISM; PROTEIN SYNTHESIS; REGULATORY RNA SEQUENCE; REPORTER GENE;

3' UNTRANSLATED REGIONS; CELL LINE; CYTOSINE; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; GENE EXPRESSION REGULATION; GENES, REPORTER; HETEROGENEOUS-NUCLEAR RIBONUCLEOPROTEINS; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; NITRIC OXIDE; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN BIOSYNTHESIS; REGULATORY SEQUENCES, RIBONUCLEIC ACID; RNA STABILITY; RNA, MESSENGER; URACIL;

EID: 33745139539     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkl386     Document Type: Article

References (60)

1. Fan,J., Yang,X., Wang,W., Wood,W.H., IIIrd, Becker,K.G. and Gorospe,M. (2002) Global analysis of stress-regulated mRNA turnover by using cDNA arrays. Proc. Natl Acad. Sci. USA, 99, 10611-10616.
2. Kawai,T., Fan,J., Mazan-Mamczarz,K. and Gorospe,M. (2004) Global mRNA stabilization preferentially linked to translational repression during the endoplasmic reticulum stress response. Mol. Cell Biol., 24, 6773-6787.
3. Chen,C.Y. and Shyu,A.B. (1995) AU-rich elements: Characterization and importance in mRNA degradation. Trends Biochem. Sci., 20, 465-470.
4. Bakheet,T., Williams,B.R. and Khabar,K.S. (2003) ARED 2.0: An update of AU-rich element mRNA database. Nucleic Acids Res., 31, 421-423.
5. Shyu,A.B., Belasco,J.G. and Greenberg,M.E. (1991) Two distinct destabilizing elements in the c-fos message trigger deadenylation as a first step in rapid mRNA decay. Genes Dev., 5, 221-231.
6. Chen,C.Y., Gherzi,R., Ong,S.E., Chan,E.L., Raijmakers,R., Pruijn,G.J., Stoecklin,G., Moroni,C., Mann,M. and Karin,M. (2001) AU binding proteins recruit the exosome to degrade ARE-containing mRNAs. Cell, 107, 451-464.
7. Fan,X.C. and Steitz,J.A. (1998) Overexpression of HuR, a nuclear-cytoplasmic shuttling protein, increases the in vivo stability of ARE-containing mRNAs. EMBO J., 17, 3448-3460.
8. Carballo,E., Lai,W.S. and Blackshear,P.J. (1998) Feedback inhibition of macrophage tumor necrosis factor-alpha production by tristetraprolin. Science, 281, 1001-1005.
9. Lai,W.S., Carballo,E., Strum,J.R., Kennington,E.A., Phillips,R.S. and 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.
10. Raineri,I., Wegmueller,D., Gross,B., Certa,U. and Moroni,C. (2004) Roles of AUF1 isoforms, HuR and BRF1 in ARE-dependent mRNA turnover studied by RNA interference. Nucleic Acids Res., 32, 1279-1288.
11. Mukhopadhyay,D., Houchen,C.W., Kennedy,S., Dieckgraefe,B.K. and Anant,S. (2003) Coupled mRNA stabilization and translational silencing of cyclooxygenase-2 by a novel RNA binding protein, CUGBP2. Mol. Cell, 11, 113-126.
12. Ostareck,D.H., Ostareck-Lederer,A., Shatsky,I.N. and Hentze,M.W. (2001) Lipoxygenase mRNA silencing in erythroid differentiation: The 3′-UTR regulatory complex controls 60S ribosomal subunit joining. Cell, 104, 281-290.
13. Ostareck,D.H., Ostareck-Lederer,A., Wilm,M., Thiele,B.J., Mann,M. and Hentze,M.W. (1997) mRNA silencing in erythroid differentiation: HnRNP K and hnRNP E1 regulate 15-lipoxygenase translation from the 3′ end. Cell, 89, 597-606.
14. Holcik,M. and Liebhaber,S.A. (1997) Four highly stable eukaryotic mRNAs assemble 3′-untranslated region RNA-protein complexes sharing cis and trans components. Proc. Natl Acad. Sci. USA, 94, 2410-2414.
15. Skalweit,A., Doller,A., Huth,A., Kahne,T., Persson,P.B. and Thiele,B.J. (2003) Posttranscriptional control of renin synthesis: Identification of proteins interacting with renin mRNA 3′-untranslated region. Circ. Res., 92, 419-427.
16. Habelhah,H., Shah,K., Huang,L., Ostareck-Lederer,A., Burlingame,A.L., Shokat,K.M., Hentze,M.W. and Ronai,Z. (2001) ERK phosphorylation drives cytoplasmic accumulation of hnRNP-K and inhibition of mRNA translation. Nature Cell Biol., 3, 325-330.
17. Perrotti,D., Cesi,V., Trotta,R., Guerzoni,C., Santilli,G., Campbell,K., Iervolino,A., Condorelli,F., Gambacorti-Passerini,C., Caligiuri,M.A. et al. (2002) BCR-ABL suppresses C/EBPalpha expression through inhibitory action of hnRNP E2. Nature Genet., 30, 48-58.
18. Ostareck-Lederer,A., Ostareck,D.H., Cans,C., Neubauer,G., Bomsztyk,K., Superti-Furga,G. and Hentze,M.W. (2002) c-Src-mediated phosphorylation of hnRNP K drives translational activation of specifically silenced mRNAs. Mol. Cell Biol., 22, 4535-4543.
19. Mahtani,K.R., Brook,M., Dean,J.L., Sully,G., Saklatvala,J. and Clark,A.R. (2001) Mitogen-activated protein kinase p38 controls the expression and posttranslational modification of tristetraprolin, a regulator of tumor necrosis factor alpha mRNA stability. Mol. Cell Biol., 21, 6461-6469.
20. Carballo,E., Cao,H., Lai,W.S., Kennington,E.A., Campbell,D. and Blackshear,P.J. (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.
21. Ming,X.F., Stoecklin,G., Lu,M., Looser,R. and Moroni,C. (2001) Parallel and independent regulation of interleukin-3 mRNA turnover by phosphatidylinositol 3-kinase and p38 mitogen-activated protein kinase. Mol. Cell Biol., 21, 5778-5789.
22. Frevel,M.A., Bakheet,T., Silva,A.M., Hissong,J.G., Khabar,K.S. and Williams,B.R. (2003) p38 Mitogen-activated protein kinase-dependent and -independent signaling of mRNA stability of AU-rich element-containing transcripts. Mol. Cell Biol., 23, 425-436.
23. Lasa,M., Mahtani,K.-R., Finch,A., Brewer,G., Saklatvala,J. and Clark,A.R. (2000) Regulation of cyclooxygenase 2 mRNA stability by the mitogen-activated protein kinase p38 signaling cascade. Mol. Cell Biol., 20, 4265-4274.
24. Ma,P., Cui,X., Wang,S., Zhang,J., Nishanian,E.V., Wang,W., Wesley,R.A. and Danner,R.L. (2004) Nitric oxide post-transcriptionally up-regulates LPS-induced IL-8 expression through p38 MAPK activation. J. Leukoc. Biol., 76, 278-287.
25. Pages,G., Berra,E., Milanini,J., Levy,A.P. and Pouyssegur,J. (2000) Stress-activated protein kinases (JNK and p38/HOG) are essential for vascular endothelial growth factor mRNA stability. J. Biol. Chem., 275, 26484-26491.
26. Cui,X., Zhang,J., Ma,P., Myers,D., Goldberg,I.G., Sittler,K.J., Barb,J.J., Munson,P.J., Del Pilar Cintron,A., McCoy,J.P. et al. (2005) cGMP-independent nitric oxide signaling and regulation of the cell cycle. BMC Genomics, 6, 151.
27. Winzen,R., Kracht,M., Ritter,B., Wilhelm,A., Chen,C.Y., Shyu,A.B., Muller,M., Gaestel,M., Resch,K. and Holtmann,H. (1999) 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., 18, 4969-4980.
28. Zhang,J., Wang,S., Wesley,R.A. and Danner,R.L. (2003) Adjacent sequence controls the response polarity of nitric oxide-sensitive Sp factor binding sites. J. Biol. Chem., 278, 29192-29200.
29. Wang,S., Wang,W., Wesley,R.A. and Danner,R.L. (1999) A Sp1 binding site of the tumor necrosis factor alpha promoter functions as a nitric oxide response element. J. Biol. Chem., 274, 33190-33193.
30. Spiecker,M., Peng,H.B. and Liao,J.K. (1997) Inhibition of endothelial vascular cell adhesion molecule-1 expression by nitric oxide involves the induction and nuclear translocation of IkappaBalpha. J. Biol. Chem., 272, 30969-30974.
31. Pilz,R.B., Suhasini,M., Idriss,S., Meinkoth,J.L. and Boss,G.R. (1995) Nitric oxide and cGMP analogs activate transcription from AP-1-responsive promoters in mammalian cells. FASEB J., 9, 552-558.
32. Berendji,D., Kolb-Bachofen,V., Zipfel,P.F., Skerka,C., Carlberg,C. and Kroncke,K.D. (1999) Zinc finger transcription factors as molecular targets for nitric oxide-mediated immunosuppression: Inhibition of IL-2 gene expression in murine lymphocytes. Mol. Med., 5, 721-730.
33. Kimura,H., Weisz,A., Kurashima,Y., Hashimoto,K., Ogura,T., D'Acquisto,F., Addeo,R., Makuuchi,M. and Esumi,H. (2000) Hypoxia response element of the human vascular endothelial growth factor gene mediates transcriptional regulation by nitric oxide: Control of hypoxia-inducible factor-1 activity by nitric oxide. Blood, 95, 189-197.
34. Bouton,C. and Demple,B. (2000) Nitric oxide-inducible expression of heme oxygenase-1 in human cells. Translation-independent stabilization of the mRNA and evidence for direct action of nitric oxide. J. Biol. Chem., 275, 32688-32693.
35. Wei,J., Guo,H. and Kuo,P.C. (2002) Endotoxin-stimulated nitric oxide production inhibits expression of cytochrome c oxidase in ANA-1 murine macrophages. J. Immunol., 168, 4721-4727.
36. Ryu,S.D., Kang,J.H., Yi,H.G., Nahm,C.H. and Park,C.S. (2004) Hepatic flavin-containing monooxygenase activity attenuated by cGMP-independent nitric oxide-mediated mRNA destabilization. Biochem. Biophys. Res. Commun., 324, 409-416.
37. Abdelaziz,N., Colombo,F., Mercier,I. and Calderone,A. (2001) Nitric oxide attenuates the expression of transforming growth factor-beta(3) mRNA in rat cardiac fibroblasts via destabilization. Hypertension, 38, 261-266.
38. Akool,el,S., Kleinert,H., Hamada,F.M., Abdelwahab,M.H., Forstermann,U., Pfeilschifter,J. and Eberhardt,W. (2003) Nitric oxide increases the decay of matrix metalloproteinase 9 mRNA by inhibiting the expression of mRNA-stabilizing factor HuR. Mol. Cell Biol., 23, 4901-4916.
39. Yeo,S.J., Gravis,D., Yoon,J.G. and Yl,A.K. (2005) Myeloid differentiation factor 88-dependent transcriptional regulation of cyclooxygenase-2 expression by CpG DNA: Role of NF-kappaB and p38. J. Biol. Chem., 278, 22563-22573.
40. Benjamini,Y. and Hochberg,Y. (1995) Controlling the false discovery rate: A practical and powerful approach to multiple testing. J. R. Statist. Soc. B, 57, 289-300.
41. Seo,J. and Shneiderman,B. (2002) Understanding hierarchical clustering results by interactive exploration of dendrograms: A case study with genomic microarray data. IEEE Comput., 35, 80-86.
42. Mignone,F., Grillo,G., Licciulli,F., Iacono,M., Liuni,S., Kersey,P.J., Duarte,J., Saccone,C. and Pesole,G. (2005) UTRdb and UTRsite: A collection of sequences and regulatory motifs of the untranslated regions of eukaryotic mRNAs. Nucleic Acids Res., 33, D141-D146.
43. Brooks,S.A., Connolly,J.E. and Rigby,W.F. (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.
44. Esnault,S. and Malter,J.S. (2002) Extracellular signal-regulated kinase mediates granulocyte-macrophage colony-stimulating factor messenger RNA stabilization in tumor necrosis factor-alpha plus fibronectin-activated peripheral blood eosinophils. Blood, 99, 4048-4052.
45. Sullivan,D.E., Ferris,M., Pociask,D. and Brody,A.R. (2005) Tumor necrosis factor-alpha induces transforming growth factor-beta1 expression in lung fibroblasts through the extracellular signal-regulated kinase pathway. Am. J. Respir. Cell. Mol. Biol., 32, 342-349.
46. Lander,H.M., Hajjar,D.P., Hempstead,B.L., Mirza,U.A., Chait,B.T., Campbell,S. and Quilliam,L.A. (1997) A molecular redox switch on p21(ras). Structural basis for the nitric oxide-p21(ras) interaction. J. Biol. Chem., 272, 4323-4326.
47. Lander,H.M., Jacovina,A.T., Davis,R.J. and Tauras,J.M. (1996) Differential activation of mitogen-activated protein kinases by nitric oxide-related species. J. Biol. Chem., 271, 19705-19709.
48. Singh,R.P., Dhawan,P., Golden,C., Kapoor,G.S. and Mehta,K.D. (1999) One-way cross-talk between p38(MAPK) and p42/44(MAPK). Inhibition of p38(MAPK) induces low density lipoprotein receptor expression through activation of the p42/44(MAPK) cascade. J. Biol. Chem., 274, 19593-19600.
49. Zhang,H., Shi,X., Hampong,M., Blanis,L. and Pelech,S. (2001) Stress-induced inhibition of ERK1 and ERK2 by direct interaction with p38 MAP kinase. J. Biol. Chem., 276, 6905-6908.
50. Numazawa,S., Watabe,M., Nishimura,S., Kurosawa,M., Izuno,M. and Yoshida,T. (2003) Regulation of ERK-mediated signal transduction by p38 MAP kinase in human monocytic THP-1 cells. J. Biochem. (Tokyo), 133, 599-605.
51. Westmark,C.J. and Malter,J.S. (2001) Extracellular-regulated kinase controls beta-amyloid precursor protein mRNA decay. Brain Res. Mol. Brain Res., 90, 193-201.
52. Westmark,C.J. and Malter,J.S. (2001) Up-regulation of nucleolin mRNA and protein in peripheral blood mononuclear cells by extracellular-regulated kinase. J. Biol. Chem., 276, 1119-1126.
53. Lindquist,J.N., Parsons,C.J., Stefanovic,B. and Brenner,D.A. (2004) Regulation of alpha1(I) collagen messenger RNA decay by interactions with alphaCP at the 3′-untranslated region. J. Biol. Chem., 279, 23822-23829.
54. Kong,J., Ji,X. and Liebhaber,S.A. (2003) The KH-domain protein alpha CP has a direct role in mRNA stabilization independent of its cognate binding site. Mol. Cell Biol., 23, 1125-1134.
55. Wang,Z., Day,N., Trifillis,P. and Kiledjian,M. (1999) An mRNA stability complex functions with poly(A)-binding protein to stabilize mRNA in vitro. Mol. Cell Biol., 19, 4552-4560.
56. Ji,X., Kong,J. and Liebhaber,S.A. (2003) In vivo association of the stability control protein alphaCP with actively translating mRNAs. Mol. Cell Biol., 23, 899-907.
57. Weiss,I.M. and Liebhaber,S.A. (1995) Erythroid cell-specific mRNA stability elements in the alpha 2-globin 3′ nontranslated region. Mol. Cell Biol., 15, 2457-2465.
58. Reimann,I., Huth,A., Thiele,H. and Thiele,B.J. (2002) Suppression of 15-lipoxygenase synthesis by hnRNP E1 is dependent on repetitive nature of LOX mRNA 3′-UTR control element DICE. J. Mol. Biol., 315, 965-974.
59. Kedersha,N. and Anderson,P. (2002) Stress granules: Sites of mRNA triage that regulate mRNA stability and translatability. Biochem. Soc. Trans., 30, 963-969.
60. Katsanou,V., Papadaki,O., Milatos,S., Blackshear,P.J., Anderson,P., Kollias,G. and Kontoyiannis,D.L. (2005) HuR as a negative posttranscriptional modulator in inflammation. Mol. Cell, 19, 777-789.