Phosphorylation of HuR by Chk2 Regulates SIRT1 Expression

Molecular Cell

Volumn 25, Issue 4, 2007, Pages 543-557

  Abdelmohsen, Kotb ^a   Pullmann Jr , Rudolf ^a   Lal, Ashish ^a   Kim, Hyeon Ho ^a   Galban, Stefanie ^a   Yang, Xiaoling ^a   Blethrow, Justin D ^b   Walker, Mark ^c   Shubert, Jonathan ^d   Gillespie, David A ^c   Furneaux, Henry ^d   Gorospe, Myriam ^a  

^a NATIONAL INSTITUTE ON AGING   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c BEATSON INSTITUTE FOR CANCER RESEARCH   (United Kingdom)

^d UNIVERSITY OF CONNECTICUT SCHOOL OF MEDICINE   (United States)

Author keywords

RNA

Indexed keywords

CHECKPOINT KINASE 2; HEAT SHOCK PROTEIN; HUR PROTEIN; HYDROGEN PEROXIDE; MESSENGER RNA; MUTANT PROTEIN; PROTEIN SIRT1; SERINE; SIRTUIN; THREONINE; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ARTICLE; CELL SURVIVAL; COMPLEX FORMATION; CONTROLLED STUDY; GENE EXPRESSION REGULATION; GENE MUTATION; HUMAN; HUMAN CELL; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; REGULATORY MECHANISM; RNA DEGRADATION; RNA STABILITY;

ANTIGENS, SURFACE; BASE SEQUENCE; CELL AGING; FIBROBLASTS; GENE EXPRESSION REGULATION; HELA CELLS; HUMANS; HYDROGEN PEROXIDE; MOLECULAR SEQUENCE DATA; OXIDATIVE STRESS; PHOSPHORYLATION; POINT MUTATION; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; RIBONUCLEOPROTEINS; RNA STABILITY; RNA, MESSENGER; RNA-BINDING PROTEINS; SIRTUINS; SUBSTRATE SPECIFICITY;

EID: 33847035824     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molcel.2007.01.011     Document Type: Article

References (54)

1. Astrom S.U., Cline T.W., and Rine J. The Drosophila melanogaster sir2+ gene is nonessential and has only minor effects on position-effect variegation. Genetics 163 (2003) 931-937
2. Bartek J., and Lukas J. Chk1 and Chk2 kinases in checkpoint control and cancer. Cancer Cell 3 (2003) 421-429
3. Bevilacqua A., Ceriani M.C., Capaccioli S., and Nicolin A. Post-transcriptional regulation of gene expression by degradation of messenger RNAs. J. Cell. Physiol. 195 (2003) 356-372
4. Bhattacharyya S.N., Habermacher R., Martine U., Closs E.I., and Filipowicz W. Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell 125 (2006) 1111-1124
5. Blander G., and Guarente L. The Sir2 family of protein deacetylases. Annu. Rev. Biochem. 73 (2004) 417-435
6. Brennan C.M., and Steitz J.A. HuR and mRNA stability. Cell. Mol. Life Sci. 58 (2001) 266-277
7. Brunet A., Sweeney L.B., Sturgill J.F., Chua K.F., Greer P.L., Lin Y., Tran H., Ross S.E., Mostoslavsky R., Cohen H.Y., et al. Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science 303 (2004) 2011-2015
8. Buscemi B., Perego P., Carenini N., Nakanishi M., Chessa L., Chen J., Khanna K., and Delia D. Activation of ATM and Chk2 kinases in relation to the amount of DNA strand breaks. Oncogene 23 (2004) 7691-7700
9. Carballo E., Lai W.S., and Blackshear P.J. Feedback inhibition of macrophage tumor necrosis factor-α production by tristetraprolin. Science 281 (1998) 1001-1005
10. Cheadle C., Fan J., Cho-Chung Y.S., Werner T., Ray J., Do L., Gorospe M., and Becker K.G. Stability regulation of mRNA and the control of gene expression. Ann. N Y Acad. Sci. 1058 (2005) 196-204
11. Chen C.Y., and Shyu A.-B. AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem. Sci. 20 (1995) 465-470
12. Chen W.Y., Wang D.H., Yen R.C., Luo J., Gu W., and Baylin S.B. Tumor suppressor HIC1 directly regulates SIRT1 to modulate p53-dependent DNA-damage responses. Cell 123 (2005) 437-448
13. Chua K.F., Mostoslavsky R., Lombard D.B., Pang W.W., Saito S., Franco S., Kaushal D., Cheng H.L., Fischer M.R., Stokes N., et al. Mammalian SIRT1 limits replicative life span in response to chronic genotoxic stress. Cell Metab. 2 (2005) 67-76
14. Cohen H.Y., Lavu S., Bitterman K.J., Hekking B., Imahiyerobo T.A., Miller C., Frye R., Ploegh H., Kessler B.M., and Sinclair D.A. Acetylation of the C terminus of Ku70 by CBP and PCAF controls Bax-mediated apoptosis. Mol. Cell 13 (2004) 627-638
15. Cohen H.Y., Miller C., Bitterman K.J., Wall N.R., Hekking B., Kessler B., Howitz K.T., Gorospe M., de Cabo R., and Sinclair D.A. Calorie restriction promotes mammalian cell survival by inducing the SIRT1 deacetylase. Science 305 (2004) 390-392
16. d' Adda di Fagagna F., Reaper P.M., Clay-Farrace L., Fiegler H., Carr P., Von Zglinicki T., Saretzki G., Carter N.P., and Jackson S.P. A DNA damage checkpoint response in telomere-initiated senescence. Nature 426 (2003) 194-198
17. Dimri G.P., Lee X., Basile G., Acosta M., Scott G., Roskelley C., Medrano E.E., Linskens M., Rubelj I., Pereira-Smith O., et al. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc. Natl. Acad. Sci. USA 92 (1995) 9363-9367
18. Frye R.A. Phylogenetic classification of prokaryotic and eukaryotic Sir2-like proteins. Biochem. Biophys. Res. Commun. 273 (2000) 793-798
19. Garcia-Martinez J., Aranda A., and Perez-Ortin J.E. Genomic run-on evaluates transcription rates for all yeast genes and identifies gene regulatory mechanisms. Mol. Cell 15 (2004) 303-313
20. Gherzi R., Lee K.Y., Briata P., Wegmuller D., Moroni C., Karin M., and Chen C.Y. A KH domain RNA binding protein, KSRP, promotes ARE-directed mRNA turnover by recruiting the degradation machinery. Mol. Cell 14 (2004) 571-583
21. Gire V., Roux P., Wynford-Thomas D., Brondello J.M., and Dulic V. DNA damage checkpoint kinase Chk2 triggers replicative senescence. EMBO J. 23 (2004) 2554-2563
22. 2-mediated apoptosis of human colorectal carcinoma cells. Mol. Cell. Biol. 16 (1996) 6654-6660
23. Hirao A., Kong Y.Y., Matsuoka S., Wakeham A., Ruland J., Yoshida H., Liu D., Elledge S.J., and Mak T.W. DNA damage-induced activation of p53 by the checkpoint kinase Chk2. Science 287 (2000) 1824-1827
24. Kawai T., Lal A., Yang X., Galban S., Mazan-Mamczarz K., and Gorospe M. Translational control of cytochrome c by RNA-binding proteins TIA-1 and HuR. Mol. Cell. Biol. 26 (2006) 3295-3307
25. Kedersha N., Stoecklin G., Ayodele M., Yacono P., Lykke-Andersen J., Fitzler M.J., Scheuner D., Kaufman R.J., Golan D.E., and Anderson P. Stress granules and processing bodies are dynamically linked sites of mRNP remodeling. J. Cell Biol. 169 (2005) 871-884
26. Keene J.D. Why is Hu where? Shuttling of early-response-gene messenger RNA subsets. Proc. Natl. Acad. Sci. USA 96 (1999) 5-7
27. Keene J.D. Ribonucleoprotein infrastructure regulating the flow of genetic information between the genome and the proteome. Proc. Natl. Acad. Sci. USA 98 (2001) 7018-7024
28. Kullmann M., Gopfert U., Siewe B., and Hengst L. ELAV/Hu proteins inhibit p27 translation via an IRES element in the p27 5′UTR. Genes Dev. 16 (2002) 3087-3099
29. Lal A., Mazan-Mamczarz K., Kawai T., Yang X., Martindale J.L., and Gorospe M. Concurrent versus individual binding of HuR and AUF1 to common labile target mRNAs. EMBO J. 23 (2004) 3092-3102
30. Lal A., Kawai T., Yang X., Mazan-Mamczarz K., and Gorospe M. Antiapoptotic function of RNA-binding protein HuR effected through prothymosin alpha. EMBO J. 24 (2005) 1852-1862
31. Lal A., Abdelmohsen K., Pullmann R., Kawai T., Yang X., Galban S., Brewer G., and Gorospe M. Posttranscriptional derepression of GADD45α by genotoxic stress. Mol. Cell 22 (2006) 117-128
32. Laroia G., Cuesta R., Brewer G., and Schneider R.J. Control of mRNA decay by heat shock-ubiquitin-proteasome pathway. Science 284 (1999) 499-502
33. Leroy C., Mann C., and Marsolier M.C. Silent repair accounts for cell cycle specificity in the signaling of oxidative DNA lesions. EMBO J. 20 (2001) 2896-2906
34. Lin S.J., Defossez P.A., and Guarente L. Requirement of NAD and SIR2 for life-span extension by calorie restriction in Saccharomyces cerevisiae. Science 289 (2000) 2126-2128
35. López de Silanes I., Fan J., Yang X., Zonderman A.B., Potapova O., Pizer E.S., and Gorospe M. Role of the RNA-binding protein HuR in colon carcinogenesis. Oncogene 22 (2003) 7146-7154
36. López de Silanes I., Lal A., and Gorospe M. HuR: post-transcriptional paths to malignancy. RNA Biology 1 (2004) 135-137
37. López de Silanes I., Zhan M., Lal A., Yang X., and Gorospe M. Identification of a target RNA motif for RNA-binding protein HuR. Proc. Natl. Acad. Sci. USA 101 (2004) 2987-2992
38. Luo J., Nikolaev A.Y., Imai S., Chen D., Su F., Shiloh A., Guarente L., and Gu W. Negative control of p53 by Sir2alpha promotes cell survival under stress. Cell 107 (2001) 137-148
39. Mazan-Mamczarz K., Galban S., López de Silanes I., Martindale J.L., Atasoy U., Keene J.D., and Gorospe M. RNA-binding protein HuR enhances p53 translation in response to ultraviolet light irradiation. Proc. Natl. Acad. Sci. USA 100 (2003) 8354-8359
40. Melchionna R., Chen X.B., Blasina A., and McGowan C.H. Threonine 68 is required for radiation-induced phosphorylation and activation of Cds1. Nat. Cell Biol. 2 (2000) 762-765
41. Moore M.J. From birth to death: the complex lives of eukaryotic mRNAs. Science 309 (2005) 1514-1518
42. Motta M.C., Divecha N., Lemieux M., Kamel C., Chen D., Gu W., Bultsma Y., McBurney M., and Guarente L. Mammalian SIRT1 represses forkhead transcription factors. Cell 116 (2004) 551-563
43. Murakami H., and Okayama H. A kinase from fission yeast responsible for blocking mitosis in S phase. Nature 374 (1995) 817-819
44. Nemoto S., Fergusson M.M., and Finkel T. Nutrient availability regulates SIRT1 through a forkhead-dependent pathway. Science 306 (2004) 2105-2108
45. North B.J., and Verdin E. Sirtuins: Sir2-related NAD-dependent protein deacetylases. Genome Biol. 5 (2004) 224 10.1186/gb-2004-5-5-224 Published online April 28, 2004
46. O'Neill T., Giarratani L., Chen P., Iyer L., Lee C.H., Bobiak M., Kanai F., Zhou B.B., Chung J.H., and Rathbun G.A. Determination of substrate motifs for human Chk1 and hCds1/Chk2 by the oriented peptide library approach. J. Biol. Chem. 277 (2002) 16102-16115
47. Prives C., and Manley J.L. Why is p53 acetylated?. Cell 107 (2001) 815-818
48. Rogina B., and Helfand S.L. Sir2 mediates longevity in the fly through a pathway related to calorie restriction. Proc. Natl. Acad. Sci. USA 101 (2004) 15998-16003
49. Sinclair D.A., and Guarente L. Extrachromosomal rDNA circles-a cause of aging in yeast. Cell 91 (1997) 1033-1042
50. Vaziri H., Dessain S.K., Ng Eaton E., Imai S.I., Frye R.A., Pandita T.K., Guarente L., and Weinberg R.A. hSIR2(SIRT1) functions as an NAD-dependent p53 deacetylase. Cell 107 (2001) 149-159
51. Wang W., Furneaux H., Cheng H., Caldwell M.C., Hutter D., Liu Y., Holbrook N., and Gorospe M. HuR regulates p21 mRNA stabilization by UV light. Mol. Cell. Biol. 20 (2000) 760-769
52. Wang W., Yang X., Cristofalo V.J., Holbrook N.J., and Gorospe M. Loss of HuR influences gene expression during replicative senescence. Mol. Cell. Biol. 21 (2001) 5889-5898
53. Wilusz C.J., and Wilusz J. Bringing the role of mRNA decay in the control of gene expression into focus. Trends Genet. 20 (2004) 491-497
54. Wood J.G., Rogina B., Lavu S., Howitz K., Helfand S.L., Tatar M., and Sinclair D. Sirtuin activators mimic caloric restriction and delay ageing in metazoans. Nature 430 (2004) 686-689