Nucleolin and YB-1 are required for JNK-mediated interleukin-2 mRNA stabilization during T-cell activation

Genes and Development

Volumn 14, Issue 10, 2000, Pages 1236-1248

  Chen, Ching Yi ^a   Gherzi, Roberto ^a   Andersen, Jens S ^b   Gaietta, Guido ^a   Jürchott, Karsten ^c   Royer, Hans Dieter ^c   Mann, Matthias ^b   Karin, Michael ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF SOUTHERN DENMARK   (Denmark)

^c MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

Author keywords

JNK; Nucleolin; Stabilization; T cell activation; Trans acting factors

Indexed keywords

INTERLEUKIN 2; JANUS KINASE; MESSENGER RNA; NUCLEOLIN; RNA BINDING PROTEIN; TRANS ACTING FACTOR; UNCLASSIFIED DRUG; Y BOX BINDING PROTEIN 1;

5' UNTRANSLATED REGION; ARTICLE; CELL FREE SYSTEM; CONTROLLED STUDY; DNA RESPONSIVE ELEMENT; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; LEUKEMIA CELL LINE; PRIORITY JOURNAL; REPORTER GENE; RNA DEGRADATION; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION;

AMINO ACID SEQUENCE; BASE SEQUENCE; CCAAT-ENHANCER-BINDING PROTEINS; CYTOPLASM; DNA-BINDING PROTEINS; ENZYME ACTIVATION; GENE EXPRESSION REGULATION; HALF-LIFE; HUMANS; INTERLEUKIN-2; JNK MITOGEN-ACTIVATED PROTEIN KINASES; JURKAT CELLS; LYMPHOCYTE ACTIVATION; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; MITOGEN-ACTIVATED PROTEIN KINASES; MOLECULAR SEQUENCE DATA; MUTATION; NFI TRANSCRIPTION FACTORS; PHOSPHOPROTEINS; PRECIPITIN TESTS; PROTEIN BINDING; RESPONSE ELEMENTS; RNA STABILITY; RNA, MESSENGER; RNA-BINDING PROTEINS; T-LYMPHOCYTES; TRANSCRIPTION FACTORS; Y-BOX-BINDING PROTEIN 1;

JANUS;

EID: 0034657357     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (64)

1. Bohjanen, P.R., B. Petryniak, C.H. June, C.B. Thompson, and T. Lindsten. 1991. An inducible cytoplasmic factor (AU-B) binds selectively to AUUUA multimers in the 3′ untranslated region of lymphokine mRNA. Mol. Cell. Biol. 11: 3288-3295.
2. Bouvet, P., K. Matsumoto, and A.P. Wolffe. 1995. Sequence-specific RNA recognition by the Xenopus Y-box proteins. An essential role for the cold shock domain. J. Biol. Chem. 270: 28297-28303.
3. Brewer, G. 1991. An A + U-rich element RNA-binding factor regulates c-myc mRNA stability in vitro. Mol. Cell. Biol. 11: 2460-2466.
4. Brewer, G. and J. Ross. 1990. Messenger RNA turnover in cell-free extracts. Methods Enzymol. 181: 202-209.
5. Brown, C.Y., C.A. Lagnado, and G.J. Goodall. 1996. A cytokine mRNA-destabilizing element that is structurally and functionally distinct from A+U-rich elements. Proc. Natl. Acad. Sci. 93: 13721-13725.
6. Burd, G.G. and G. Dreyfuss. 1994. Conserved structures and diversity of functions of RNA-binding proteins. Science 265: 615-621.
7. Caput, D., B. Beutler, K. Hartog, R. Thayer, S. Brown-Shimer, and A. Cerami. 1986. Identification of a common nucleotide sequence in the 3′-untranslated region of mRNA molecules specifying inflammatory mediators. Proc. Natl. Acad. Sci. 83: 1670-1674.
8. Carballo, E., W.S. Lai, and P.J. Blackshear. 1998. Feedback inhibition of macrophage tumor necrosis factor-alpha production by tristetraprolin. Science 281: 1001-1005.
9. Chen, C.Y. and A.B. Shyu. 1995. AU-rich elements: Characterization and importance in mRNA degradation. Trends Biochem. Sci. 20: 465-470.
10. Chen, C.Y., F. Del Gatto-Konczak, Z. Wu, and M. Karin. 1998. Stabilization of interleukin-2 mRNA by the c-Jun NH2-terminal kinase pathway. Science 280: 1945-1949.
11. Dibbens, J.A., D.L. Miller, A. Damert, W. Risau, M.A. Vadas, and G.J. Goodall. 1999. Hypoxic regulation of vascular endothelial growth factor mRNA stability requires the cooperation of multiple RNA elements. Mol. Biol. Cell 10: 907-919.
12. Didier, D.K., J. Schiffenbauer, S.L. Woulfe, M. Zacheis, and B.D. Schwartz. 1988. Characterization of the cDNA encoding a protein binding to the major histocompatibility complex class II Y box. Proc. Natl. Acad. Sci. 85: 7322-7326.
13. Evdokimova, V.M. and L.P. Ovchinnikov. 1999. Translational regulation by Y-box transcription factor: Involvement of the major mRNA-associated protein, p50. Int. J. Biochem. Cell Biol. 31: 139-149.
14. Evdokimova, V.M., C.L. Wei, A.S. Sitikov, P.N. Simonenko, O.A. Lazarev, K.S. Vasilenko, V.A. Ustinov, J.W. Hershey, and L.P. Ovchinnikov. 1995. The major protein of messenger ribonucleoprotein particles in somatic cells is a member of the Y-box binding transcription factor family. J. Biol. Chem. 270: 3186-3192.
15. Fan, X.C. and J.A. Steitz. 1998. Overexpression of HuR, a nuclear-cytoplasmic shuttling protein, increases the in vivo stability of ARE-containing mRNAs. EMBO J. 17: 3448-3460.
16. Ford, L.P., J. Watson, J.D. Keene, and J. Wilusz. 1999. ELAV proteins stabilize deadenylated intermediates in a novel in vitro mRNA deadenylation/degradation system. Genes & Dev. 13: 188-201.
17. Ghisolfi-Nieto, L., G. Joseph, F. Puvion-Dutilleul, F. Amalric, and P. Bouvet. 1996. Nucleolin is a sequence-specific RNA-binding protein: Characterization of targets on pre-ribosomal RNA. J. Mol. Biol. 260: 34-53.
18. Ginisty, H., F. Amalric, and P. Bouvet. 1998. Nucleolin functions in the first step of ribosomal RNA processing. EMBO J. 17: 1476-1486.
19. Ginisty, H., H. Sicard, B. Roger, and P. Bouvet. 1999. Structure and functions of nucleolin. J. Cell Sci. 112: 761-772.
20. Hamilton, B.J., E. Nagy, J.S. Malter, B.A. Arrick, and W.F. Rigby. 1993. Association of heterogeneous nuclear ribonucleoprotein A1 and C proteins with reiterated AUUUA sequences. J. Biol. Chem. 268: 8881-8887.
21. Hanakahi, L.A., L.A. Dempsey, M.J. Li, and N. Maizels. 1997. Nucleolin is one component of the B cell-specific transcription factor and switch region binding protein, LR1. Proc. Natl. Acad. Sci. 94: 3605-3610.
22. Hill, C.S. and R. Treisman. 1995. Transcriptional regulation by extracellular signals: Mechanisms and specificity. Cell 80: 199-211.
23. Hunter, T. and M. Karin. 1992. The regulation of transcription by phosphorylation. Cell 70: 375-387.
24. Iwai, Y., M. Bickel, D.H. Pluznik, and R.B. Cohen. 1991. Identification of sequences within the murine granulocyte-macrophage colony-stimulating factor mRNA 3′-untranslated region that mediate mRNA stabilization induced by mitogen treatment of EL-4 thymoma cells. J. Biol. Chem. 266: 17959-17965.
25. Iwai, Y., K. Akahane, D.H. Pluznik, and R.B. Cohen. 1993. Ca2+ ionophore A23187-dependent stabilization of granulocyte-macrophage colony-stimulating factor messenger RNA in murine thymoma EL-4 cells is mediated through two distinct regions in the 3′-untranslated region. J. Immunol. 150: 4386-4394.
26. Jiang, Y., C. Chen, Z. Li, W. Guo, J.A. Gegner, S. Lin, and J. Han. 1996. Characterization of the structure and function of a new mitogen-activated protein kinase (p38beta). J. Biol. Chem. 271: 17920-17926.
27. Karin, M. and T. Hunter. 1995. Transcriptional control by protein phosphorylation: signal transmission from the cell surface to the nucleus. Curr. Biol. 5: 747-757.
28. Kishore, R., J.M. Tebo, M. Kolosov, and T.A. Hamilton. 1999. Cutting edge: Clustered AU-rich elements are the target of IL-10-mediated mRNA destabilization in mouse macrophages. J. Immunol. 162: 2457-2461.
29. Lagnado, C.A., C.Y. Brown, and G.J. Goodall. 1994. 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.
30. Lai, W.S., E. Carballo, J.R. Strum, E.A. Kennington, R.S. Phillips, and P.J. Blackshear. 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: 4311-1323.
31. Laroia, G., R. Cuesta, G. Brewer, and R.J. Schneider. 1999. Control of mRNA decay by heat shock-ubiquitin-proteasome pathway. Science 284: 499-502.
32. Li, W.W., Y. Hsiung, V. Wong, K. Galvin, Y. Zhou, Y. Shi, and A.S. Lee. 1997. Suppression of grp78 core promoter element-mediated stress induction by the dbpA and dbpB (YB-1) cold shock domain proteins. Mol. Cell. Biol. 17: 61-68.
33. Lindsten, T., C.H. June, J.A. Ledbetter, G. Stella, and C.B. Thompson. 1989. Regulation of lymphokine messenger RNA stability by a surface-mediated T cell activation pathway. Science 244: 339-343.
34. Loflin, P., C.Y. Chen, and A.B. Shyu. 1999. Unraveling a cytoplasmic role for hnRNP D in the in vivo mRNA destabilization directed by the AU-rich element. Genes & Dev. 13: 1884-1897.
35. Mansour, S.J., W.T. Matten, A.S. Hermann, J.M. Candia, S. Rong, K. Fukasawa, G.F. Vande Woude, and N.G. Ahn. 1994. Transformation of mammalian cells by constitutively active MAP kinase kinase. Science 265: 966-970.
36. Myer, V.E., X.C. Fan, and J.A. Steitz. 1997. Identification of HuR as a protein implicated in AUUUA-mediated mRNA decay. EMBO J. 16: 2130-2139.
37. Nagy, E. and W.F. Rigby. 1995. Glyceraldehyde-3-phosphate dehydrogenase selectively binds AU-rich RNA in the NAD(+)-binding region (Rossmann fold). J. Biol. Chem. 270: 2755-2763.
38. Nakagawa, J., H. Waldner, S. Meyer-Monard, J. Hofsteenge, P. Jenö, and C. Moroni. 1995. AUH, a gene encoding an AU-specific RNA binding protein with intrinsic enoyl-CoA hydratase activity. Proc. Natl. Acad. Sci. 92: 2051-2055.
39. Peng, S.S., C.Y. Chen, and A.B. Shyu. 1996. Functional characterization of a non-AUUUA AU-rich element from the c-jun proto-oncogene mRNA: Evidence for a novel class of AU-rich elements. Mol. Cell. Biol. 16: 1490-1499.
40. Peng, S.S., C.Y. Chen, N. Xu, and A.B. Shyu. 1998. RNA stabilization by the AU-rich element binding protein, HuR, an ELAV protein. EMBO J. 17: 3461-3470.
41. Pruijn, G.J.M., J.P.H. Thijssen, P.R. Smith, D.G. Williams, and W.J. Van Venrooij. 1995. Anti-La monoclonal antibodies recognizing epitopes within the RNA-binding domain of the La protein show differential capacities to immunoprecipitate RNA-associated La protein. Eur. J. Biochem. 232: 611-619.
42. Ragheb, J.A., M. Deen, and R.H. Schwartz. 1999. CD28-Mediated regulation of mRNA stability requires sequences within the coding region of the IL-2 mRNA. J. Immunol. 163: 120-129.
43. Ranjan, M., S.R. Tafuri, and A.P. Wolffe. 1993. Masking mRNA from translation in somatic cells. Genes & Dev. 7: 1725-1736.
44. Ross, J. 1995. mRNA stability in mammalian cells. Microbiol. Rev. 59: 423-450.
45. Sachs, A.B. 1993. Messenger RNA degradation in eukaryotes. Cell 74: 413-421.
46. Schuler, G.D. and M.D. Cole. 1988. GM-CSF and oncogene mRNA stabilities are independently regulated in trans in a mouse monocytic tumor. Cell 55: 1115-1122.
47. Serin, G., G. Joseph, L. Ghisolfi, M. Bauzan, M. Erard, F. Amalric, and P. Bouvet. 1997. Two RNA-binding domains determine the RNA-binding specificity of nucleolin. J. Biol. Chem. 272: 13109-13116.
48. Shaw, G. and R. Kamen. 1986. A conserved AU sequence from the 3′ untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell 46: 659-667.
49. Shyu, A.B., M.E. Greenberg, and J.G. Belasco. 1989. The c-fos transcript is targeted for rapid decay by two distinct mRNA degradation pathways. Genes & Dev. 3: 60-72.
50. Shyu, A.B., J.G. Belasco, and M.E. Greenberg. 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.
51. Srivastava, M., P.J. Fleming, H.B. Pollard, and A.L. Burns. 1989. Cloning and sequencing of the human nucleolin cDNA. FEBS Lett. 250: 99-105.
52. Stoecklin, G., S. Hahn, and C. Moroni. 1994. Functional hierarchy of AUUUA motifs in mediating rapid interleukin-3 mRNA decay. J. Biol. Chem. 269: 28591-28597.
53. Valdez, B.C., D. Henning, R.K. Busch, M. Srivastava, and H. Busch. 1995. Immunodominant RNA recognition motifs of human nucleolin/C23. Mol. Immunol. 32: 1207-1213.
54. Wilm, M., A. Shevchenko, T. Houthaeve, S. Breit, L. Schweigerer, T. Fotsis, and M. Mann. 1996. Femtomole sequencing of proteins from polyacrylamide gels by nano-electrospray mass spectrometry. Nature 379: 466-469.
55. Wisdom, R. and W. Lee. 1991. The protein-coding region of c-myc mRNA contains a sequence that specifies rapid mRNA turnover and induction by protein synthesis inhibitors. Genes & Dev. 5: 232-243.
56. Wolffe, A.P., S. Tafuri, M. Ranjan, and M. Familari. 1992. The Y-box factors: A family of nucleic acid binding proteins conserved from Escherichia coli to man. New Biologist 4: 290-298.
57. Wu, Z., J. Wu, E. Jacinto, and M. Karin. 1997. Molecular cloning and characterization of human JNKK2, a novel Jun NH2-terminal kinase-specific kinase. Mol. Cell. Biol. 17: 7407-7416.
58. Xu, N., C.Y. Chen, and A.B. Shyu. 1997. Modulation of the fate of cytoplasmic mRNA by AU-rich elements: Key sequence features controlling mRNA deadenylation and decay. Mol. Cell. Biol. 17: 4611-4621.
59. Yang, L., C.N. Steussy, D.K. Fuhrer, J. Hamilton, and Y.C. Yang. 1996. Interleukin-11 mRNA stabilization in phorbol ester-stimulated primate bone marrow stromal cells. Mol. Cell. Biol. 16: 3300-3307.
60. Yang, T.H., W.H. Tsai, Y.M. Lee, H.Y. Lei, M.Y. Lai, D.S. Chen, N.H. Yen, and S.C. Lee. 1994. Purification and characterization of nucleolin and its identification as a transcription repressor. Mol. Cell. Biol. 14: 6068-6074.
61. Zaidi, S.H. and J.S. Malter. 1995. Nucleolin and heterogeneous nuclear ribonucleoprotein C proteins specifically interact with the 3′-untranslated region of amyloid protein precursor mRNA. J. Biol. Chem. 270: 17292-17298.
62. Zaidi, S.H., R. Denman, and J.S. Malter. 1994. Multiple proteins interact at a unique cis-element in the 3′-untranslated region of amyloid precursor protein mRNA. J. Biol. Chem. 269: 24000-24006.
63. Zhang, W., B.J. Wagner, K. Ehrenman, A.W. Schaefer, C.T. DeMaria, D. Crater, K. DeHaven, L. Long, and G. Brewer. 1993. Purification, characterization, and cDNA cloning of an AU-rich element RNA-binding protein, AUF1. Mol. Cell. Biol. 13: 7652-7665.
64. Zuhiaga, A.M., J.G. Belasco, and M.E. Greenberg. 1995. The nonamer UUAUUUAUU is the key AU-rich sequence motif that mediates mRNA degradation. Mol. Cell. Biol. 15: 2219-2230.