Genome-wide analysis of mRNA decay in resting and activated primary human T lymphocytes

Nucleic Acids Research

Volumn 30, Issue 24, 2002, Pages 5529-5538

  Raghavan, Arvind ^a   Ogilvie, Rachel L ^a   Reilly, Cavan ^a   Abelson, Michelle L ^a   Raghavan, Shalini ^a   Vasdewani, Jayprakash ^a   Krathwohl, Mitchell ^b   Bohjanen, Paul R ^a,b  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD28 ANTIGEN; CD3 ANTIGEN; CELL SURFACE RECEPTOR; CYTOKINE; DACTINOMYCIN; MESSENGER RNA; PROTEIN ANTIBODY; REGULATOR PROTEIN; TRANSCRIPTION FACTOR;

APOPTOSIS; CELL CYCLE; CELL ISOLATION; CONTROLLED STUDY; CULTURE MEDIUM; DNA MICROARRAY; GENE CONTROL; GENE EXPRESSION; GENE REPRESSION; GENETIC CODE; GENOMICS; HALF LIFE TIME; HUMAN; HUMAN CELL; PERIPHERAL LYMPHOCYTE; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW; RNA DEGRADATION; RNA SEQUENCE; RNA TRANSCRIPTION; SIGNAL TRANSDUCTION; STEADY STATE; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; TRANSCRIPTION REGULATION; UNINDEXED SEQUENCE;

ANTIBODIES; ANTIGENS, CD28; ANTIGENS, CD3; BLOTTING, NORTHERN; GENOME, HUMAN; HALF-LIFE; HUMANS; LYMPHOCYTE ACTIVATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; T-LYMPHOCYTES; TRANSCRIPTION, GENETIC;

EID: 0037115826     PISSN: 03051048     EISSN: None     Source Type: Journal    
DOI: 10.1093/nar/gkf682     Document Type: Review

References (58)

1. Malter,J.S. (1998) Posttranscriptional regulation of mRNAs important in T cell function. Adv. Immunol., 68, 1-49.
2. Ross,J. (1995) mRNA stability in mammalian cells. Microbiol. Rev., 59, 423-450.
3. Pearson,P.L. and Van der Luijt,R.B. (1998) The genetic analysis of cancer. J. Intern. Med., 243, 413-417.
4. Raymond,V., Atwater,J.A. and Verma,I.M. (1989) Removal of an mRNA destabilizing element correlates with the increased oncogenicity of protooncogene fos. Oncogene Res., 5, 1-12.
5. Meijlink,F., Curran,T., Miller,A.D. and Verma,I.M. (1985) Removal of a 67-base-pair sequence in the noncoding region of protooncogene fos converts it to a transforming gene. Proc. Natl Acad. Sci. USA, 82, 4987-4991.
6. Aghib,D.F., Bishop,J.M., Ottolenghi,S., Guerrasio,A., Serra,A. and Saglio,G. (1990) A 3′ truncation of MYC caused by chromosomal translocation in a human T-cell leukemia increases mRNA stability. Oncogene, 5, 707-711.
7. Bernasconi,N.L., Wormhoudt,T.A. and Laird-Offringa,I.A. (2000) Post-transcriptional deregulation of myc genes in lung cancer cell lines. Am. J. Respir. Cell Mol. Biol., 23, 560-565.
8. Lindsten,T., June,C.H., Ledbetter,J.A., Stella,G. and Thompson,C.B. (1989) Regulation of lymphokine messenger RNA stability by a surface-mediated T cell activation pathway. Science, 244, 339-343.
9. Lam,L.T., Pickeral,O.K., Peng,A.C., Rosenwald,A., Hurt,E.M., Giltnane,J.M., Averett,L.M., Zhao,H., Davis,R.E., Sathyamoorthy,M. et al. (2001) Genomic-scale measurement of mRNA turnover and the mechanisms of action of the anti-cancer drug flavopiridol. Genome Biol., 2, RESEARCH0041.
10. Wang,Y., Liu,C.L., Storey,J.D., Tibshirani,R.J., Herschlag,D. and Brown,P.O. (2002) Precision and functional specificity in mRNA decay. Proc. Natl Acad. Sci. USA, 99, 5860-5865.
11. Raghavan,A., Robison,R.L., McNabb,J., Miller,C.R., Williams,D.A. and Bohjanen,P.R. (2001) HuA and tristetraprolin are induced following T cell activation and display distinct but overlapping RNA binding specificities. J. Biol. Chem., 276, 47958-47965.
12. Chen,C.Y. and Shyu,A.B. (1995) AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem. Sci., 20, 465-470.
13. Jacobson,A. and Peltz,S.W. (1996) Interrelationships of the pathways of mRNA decay and translation in eukaryotic cells. Annu. Rev. Biochem., 65, 693-739.
14. Shaw,G. and Kamen,R. (1986) A conserved AU sequence from the 3′ untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell, 46, 659-667.
15. Xu,N., Chen,C.Y. and Shyu,A.B. (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.
16. Bakheet,T., Frevel,M., Williams,B.R., Greer,W. and Khabar,K.S. (2001) ARED: human AU-rich element-containing mRNA database reveals an unexpectedly diverse functional repertoire of encoded proteins. Nucleic Acids Res., 29, 246-254.
17. Granucci,F., Castagnoli,P.R., Rogge,L. and Sinigaglia,F. (2001) Gene expression profiling in immune cells using microarray. Int. Arch. Allergy Immunol., 126, 257-266.
18. Ellisen,L.W., Palmer,R.E., Maki,R.G., Truong,V.B., Tamayo,P., Oliner,J.D. and Haber,D.A. (2001) Cascades of transcriptional induction during human lymphocyte activation. Eur. J. Cell Biol., 80, 321-328.
19. Ollila,J. and Vihinen,M. (1998) Stimulation of B and T cells activates expression of transcription and differentiation factors. Biochem. Biophys. Res. Commun. 249, 475-480.
20. Crabtree,G.R. 1989) Contingent genetic regulatory events in T lymphocyte activation. Science, 243, 355-361.
21. Ullman,K.S., Northrop,J.P., Verweij,C.L. and Crabtree,G.R. (1990) Transmission of signals from the T lymphocyte antigen receptor to the genes responsible for cell proliferation and immune function: the missing link. Annu. Rev. Immunol., 8, 421-452.
22. Borger,P., Kauffman,H.F., Vijgen,J.L., Postma,D.S. and Vellenga,E. (1996) Activation of the cAMP-dependent signaling pathway downregulates the expression of interleukin-3 and granulocyte-macrophage colony-stimulating factor in activated human T lymphocytes. Exp. Hematol., 24, 108-115.
23. Cerdan,C., Martin,Y., Courcoul,M., Mawas,C., Birg,F. and Olive,D. (1995) CD28 costimulation up-regulates long-term IL-2R beta expression in human T cells through combined transcriptional and posttranscriptional regulation. J. Immunol., 154, 1007-1013.
24. Geginat,J., Clissi,B., Moro,M., Dellabona,P., Bender,J.R. and Pardi,R. (2000) CD28 and LFA-1 contribute to cyclosporin A-resistant T cell growth by stabilizing the IL-2 mRNA through distinct signaling pathways. Eur. J. Immunol., 30, 1136-1144.
25. Lake,R.A., O'Hehir,R.E., Verhoef,A. and Lamb,J.R. (1993) CD28 mRNA rapidly decays when activated T cells are functionally anergized with specific peptide. Int. Immunol., 5, 461-466.
26. Malter,J.S., Reed,J.C. and Kamoun,M. (1988) Induction and regulation of CD2 mRNA in human lymphocytes. J. Immunol., 140, 3233-3236.
27. Santis,A.G., Lopez-Cabrera,M., Sanchez-Madrid,F. and Proudfoot,N. (1995) Expression of the early lymphocyte activation antigen CD69, a C-type lectin, is regulated by mRNA degradation associated with AU-rich sequence motifs. Eur. J. Immunol., 25, 2142-2146.
28. Umland,S.P., Razac,S., Shah,H., Nahrebne,D.K., Egan,R.W. and Billah,M.M. (1998) Interleukin-5 mRNA stability in human T cells is regulated differently than interleukin-2, interleukin-3, interleukin-4, granulocyte/macrophage colony-stimulating factor and interferon-gamma. Am. J. Respir. Cell Mol. Biol., 18, 631-642.
29. Wingett,D., Reeves,R. and Magnuson,N.S. (1991) Stability changes in pim-1 proto-oncogene mRNA after mitogen stimulation of normal lymphocytes. J. Immunol., 147, 3653-3659.
30. Ziegler,S.F., Ramsdell,F. and Alderson,M.R. (1994) The activation antigen CD69. Stem Cells, 12, 456-465.
31. Nichols,K.E., Koretzky,G.A. and June,C.H. (2001) SAP: natural inhibitor or grand SLAM of T cell activation? Nature Immunol., 2, 665-666.
32. Siegel,R.M., Chan,F.K., Chun,H.J. and Lenardo,M.J. (2000) The multifaceted role of Fas signaling in immune cell homeostasis and autoimmunity. Nature Immunol., 1, 469-474.
33. D'Souza,B., Rowe,M. and Walls,D. (2000) The bfl-1 gene is transcriptionally upregulated by the Epstein-Barr virus LMP1 and its expression promotes the survival of a Burkitt's lymphoma cell line. J. Virol., 74, 6652-6658.
34. Zong,W.X., Edelstein,L.C., Chen,C., Bash,J. and Gelinas,C. (1999) The prosurvival Bcl-2 homolog Bfl-1/A1 is a direct transcriptional target of NF-kappaB that blocks TNFalpha-induced apoptosis. Genes Dev., 13, 382-387.
35. Crabtree,G.R. and Clipstone,N.A. (1994) Signal transmission between the plasma membrane and nucleus of T lymphocytes. Annu. Rev. Biochem., 63, 1045-1083.
36. Thompson,C.B., Rathmell,J.C., Frauwirth,K.A., Lindsten,T., Rudin,C.M., Opferman,J.T., Ashton-Rickardt,P.G., Harris,M.H., Chandel,N.S., Schumacker,P.T. and Vander Heiden,M.G. (1999) What keeps a resting T cell alive? Cold Spring Harb. Symp. Quant. Biol., 64, 383-387.
37. Buckley,A.F., Kuo,C.T. and Leiden,J.M. (2001) Transcription factor LKLF is sufficient to program T cell quiescence via a c-Myc-dependent pathway. Nature Immunol., 2, 698-704.
38. Raab,M., Pfister,S. and Rudd,C.E. (2001) CD28 signaling via VAV/SLP-76 adaptors: regulation of cytokine transcription independent of TCR ligation. Immunity, 15, 921-933.
39. Bonecchi,R., Bianchi,G., Bordignon,P.P., D'Ambrosio,D., Lang,R., Borsatti,A., Sozzani,S., Allavena,P., Gray,P.A., Mantovani,A. and Sinigaglia,F. (1998) Differential expression of chemokine receptors and chemotactic responsiveness of type 1 T helper cells (Th1s) and Th2s. J. Exp. Med., 187, 129-134.
40. Epler,J.A., Liu,R. and Shimizu,Y. (2000) From the ECM to the cytoskeleton and back: how integrins orchestrate T cell action. Dev. Immunol., 7, 155-170.
41. Akdis,C.A. and Blaser,K. (2001) Mechanisms of interleukin-10-mediated immune suppression. Immunology, 103, 131-136.
42. Joss,A., Akdis,M., Faith,A., Blaser,K. and Akdis,C.A. (2000) IL-10 directly acts on T cells by specifically altering the CD28 co-stimulation pathway. Eur. J. Immunol., 30, 1683-1690.
43. Jenkins,M.K., Chen,C.A., Jung,G., Mueller,D.L. and Schwartz,R.H. (1990) Inhibition of antigen-specific proliferation of type 1 murine T cell clones after stimulation with immobilized anti-CD3 monoclonal antibody. J. Immunol., 144, 16-22.
44. Boise,L.H., Minn,A.J., Noel,P.J., June,C.H., Accavitti,M.A., Lindsten,T. and Thompson,C.B. (1995) CD28 costimulation can promote T cell survival by enhancing the expression of Bcl-XL. Immunity, 3, 87-98.
45. Norton,S.D., Zuckerman,L., Urdahl,K.B., Shefner,R., Miller,J. and Jenkins,M.K. (1992) The CD28 ligand, B7, enhances IL-2 production by providing a costimulatory signal to T cells. J. Immunol., 149, 1556-1561.
46. Jenkins,M.K., Taylor,P.S., Norton,S.D. and Urdahl,K.B. (1991) CD28 delivers a costimulatory signal involved in antigen-specific IL-2 production by human T cells. J. Immunol., 147, 2461-2466.
47. Fraser,J.D., Irving,B.A., Crabtree,G.R. and Weiss,A. (1991) Regulation of interleukin-2 gene enhancer activity by the T cell accessory molecule CD28. Science, 251, 313-316.
48. Bohjanen,P.R., Petryniak,B., June,C.H., Thompson,C.B. and Lindsten,T. (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.
49. Bohjanen,P.R., Petryniak,B., June,C.H., Thompson,C.B. and Lindsten,T. (1992) AU RNA-binding factors differ in their binding specificities and affinities. J. Biol. Chem., 267, 6302-6309.
50. 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.
51. 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.
52. Ford,L.P., Watson,J., Keene,J.D. and Wilusz,J. (1999) ELAV proteins stabilize deadenylated intermediates in a novel in vitro mRNA deadenylation/degradation system. Genes Dev., 13, 188-201.
53. Jain,R.G., Andrews,L.G., McGowan,K.M., Pekala,P.H. and Keene,J.D. (1997) Ectopic expression of Hel-N1, an RNA-binding protein, increases glucose transporter (GLUT1) expression in 3T3-L1 adipocytes. Mol. Cell. Biol., 17, 954-962.
54. Levy,N.S., Chung,S., Furneaux,H. and Levy,A.P. (1998) Hypoxic stabilization of vascular endothelial growth factor mRNA by the RNA-binding protein HuR. J. Biol. Chem., 273, 6417-6423.
55. Peng,S.S., Chen,C.Y., Xu,N. and Shyu,A.B. (1998) RNA stabilization by the AU-rich element binding protein, HuR, an ELAV protein. EMBO J., 17, 3461-3470.
56. Laroia,G., Cuesta,R., Brewer,G. and Schneider,R.J. (1999) Control of mRNA decay by heat shock-ubiquitin-proteasome pathway. Science, 284, 499-502.
57. 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.
58. Paillard,F. and Vaquero,C. (1991) Down-regulation of lck mRNA by T cell activation involves transcriptional and post-transcriptional mechanisms. Nucleic Acids Res., 19, 4655-4661.