Regulation of HuR by DNA damage response Kinases

Journal of Nucleic Acids

Volumn 2010, Issue , 2010, Pages

  Kim, Hyeon Ho ^a,b   Abdelmohsen, Kotb ^a   Gorospe, Myriam ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b Samsung Medical Center   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; ATR PROTEIN; CHECKPOINT KINASE 1; CHECKPOINT KINASE 2; CYCLIN DEPENDENT KINASE 1; DNA DAMAGE RESPONSE KINASE; HUR PROTEIN; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTEIN KINASE; PROTEIN KINASE C; UNCLASSIFIED DRUG;

CELL NUCLEUS; CELL PROLIFERATION; CELL SURVIVAL; CYTOPLASM; DNA DAMAGE; ENZYME PHOSPHORYLATION; GENE EXPRESSION; GENETIC TRANSCRIPTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN PROCESSING; PROTEIN TRANSPORT; REGULATORY MECHANISM; REVIEW; RNA STABILITY; STRESS;

ATAXIA TELANGIECTASIA;

EID: 80053986419     PISSN: 20900201     EISSN: 2090021X     Source Type: Journal    
DOI: 10.4061/2010/981487     Document Type: Review

References (77)

1. Svejstrup J. Q., Mechanisms of transcription-coupled DNA repair. Nature Reviews Molecular Cell Biology 2002 3 1 21 29 2-s2.0-0036363646 10.1038/nrm703 (Pubitemid 135709915)
2. Mitchell P., Tollervey D., mRNA stability in eukaryotes. Current Opinion in Genetics and Development 2000 10 2 193 198 2-s2.0-0034030583 10.1016/S0959-437X(00)00063-0 (Pubitemid 30182253)
3. Orphanides G., Reinberg D., A unified theory of gene expression. Cell 2002 108 4 439 451 2-s2.0-0037154982 10.1016/S0092-8674(02)00655-4 (Pubitemid 34260870)
4. Moore M. J., From birth to death: the complex lives of eukaryotic mRNAs. Science 2005 309 5740 1514 1518 2-s2.0-24644502657 10.1126/science.1111443 (Pubitemid 41266467)
5. Keene J. D., RNA regulons: coordination of post-transcriptional events. Nature Reviews Genetics 2007 8 7 533 543 2-s2.0-34250735674 10.1038/nrg2111 (Pubitemid 46955210)
6. Bartel D. P., MicroRNAs: target recognition and regulatory functions. Cell 2009 136 2 215 233 2-s2.0-58249088751 10.1016/j.cell.2009.01.002
7. Rieger K. E., Chu G., Portrait of transcriptional responses to ultraviolet and ionizing radiation in human cells. Nucleic Acids Research 2004 32 16 4786 4803 2-s2.0-4444236147 10.1093/nar/gkh783 (Pubitemid 39429683)
8. Haley B., Paunesku T., Protic M., Woloschak G. E., Response of heterogeneous ribonuclear proteins (hnRNP) to ionising radiation and their involvement in DNA damage repair. International Journal of Radiation Biology 2009 85 8 643 655 2-s2.0-68649126316 10.1080/09553000903009548
9. Lal A., Abdelmohsen K., Pullmann R., Kawai T., Galban S., Yang X., Brewer G., Gorospe M., Posttranscriptional derepression of GADD45 α by genotoxic stress. Molecular Cell 2006 22 1 117 128 2-s2.0-33645962172 10.1016/j.molcel.2006.03.016
10. Yang C., Maiguel D. A., Carrier F., Identification of nucleolin and nucleophosmin as genotoxic stress-responsive RNA-binding proteins. Nucleic Acids Research 2002 30 10 2251 2260 2-s2.0-0037052950 (Pubitemid 34567946)
11. Busà R., Geremia R., Sette C., Genotoxic stress causes the accumulation of the splicing regulator Sam68 in nuclear foci of transcriptionally active chromatin. Nucleic Acids Research 2010 38 9 3005 3018 10.1093/nar/gkq004
12. Hinman M. N., Lou H., Diverse molecular functions of Hu proteins. Cellular and Molecular Life Sciences 2008 65 20 3168 3181 2-s2.0-53849124668 10.1007/s00018-008-8252-6
13. Keene J. D., Why is Hu where? Shuttling of early-response-gene messenger RNA subsets. Proceedings of the National Academy of Sciences of the United States of America 1999 96 1 5 7 2-s2.0-0033524475 10.1073/pnas.96.1.5 (Pubitemid 29036041)
14. Brennan C. M., Steitz J. A., HuR and mRNA stability. Cellular and Molecular Life Sciences 2001 58 2 266 277 2-s2.0-0035099573 (Pubitemid 32217358)
15. Fan X. C., Steitz J. A., HNS, a nuclear-cytoplasmic shuttling sequence in HuR. Proceedings of the National Academy of Sciences of the United States of America 1998 95 26 15293 15298 2-s2.0-0032431026 10.1073/pnas.95.26.15293 (Pubitemid 29018692)
16. Güttinger S., Mühlhäusser P., Koller-Eichhorn R., Brennecke J., Kutay U., Transporting functions as importin and mediates nuclear import of HuR. Proceedings of the National Academy of Sciences of the United States of America 2004 101 9 2918 2923 2-s2.0-1542267816 10.1073/pnas.0400342101 (Pubitemid 38327711)
17. Gallouzi I.-E., Steitz J. A., Delineation of mRNA export pathways by the use of cell-permeable peptides. Science 2001 294 5548 1895 1901 2-s2.0-0035976612 10.1126/science.1064693 (Pubitemid 33101580)
18. Rebane A., Aab A., Steitz J. A., Transportins 1 and 2 are redundant nuclear import factors for hnRNP A1 and HuR. RNA 2004 10 4 590 599 2-s2.0-1642528962 10.1261/rna.5224304 (Pubitemid 38405937)
19. Levy N. S., Chung S., Furneaux H., Levy A. P., Hypoxic stabilization of vascular endothelial growth factor mRNA by the RNA-binding protein HuR. Journal of Biological Chemistry 1998 273 11 6417 6423 2-s2.0-0032513043 10.1074/jbc.273.11.6417 (Pubitemid 28144735)
20. Wang W., Furneaux H., Cheng H., Caldwell M. C., Hutter D., Liu Y., Holbrook N., Gorospe M., HuR regulates p21 mRNA stabilization by UV light. Molecular and Cellular Biology 2000 20 3 760 769 2-s2.0-0033959125 10.1128/MCB.20.3.760-769.2000 (Pubitemid 30044212)
21. Wang W., Caldwell M. C., Lin S., Furneaux H., Gorospe M., HuR regulates cyclin A and cyclin B1 mRNA stability during cell proliferation. EMBO Journal 2000 19 10 2340 2350 2-s2.0-0034657686 (Pubitemid 30259015)
22. Nabors L. B., Gillespie G. Y., Harkins L., King P. H., HuR, a RNA stability factor, is expressed in malignant brain tumors and binds to adenine- and uridine-rich elements within the 3′ untranslated regions of cytokine and angiogenic factor mRNAs. Cancer Research 2001 61 5 2154 2161 2-s2.0-0035266295 (Pubitemid 32692041)
23. Kullmann M., Göpfert U., Siewe B., Hengst L., ELAV/Hu proteins inhibit p27 translation via an IRES element in the p27 5′ UTR. Genes and Development 2002 16 23 3087 3099 2-s2.0-0036894711 10.1101/gad.248902 (Pubitemid 35424195)
24. Mazan-Mamczarz K., Galbán S., López de Silanes I., Martindale J. L., Atasoy U., Keene J. D., Gorospe M., RNA-binding protein HuR enhances p53 translation in response to ultraviolet light irradiation. Proceedings of the National Academy of Sciences of the United States of America 2003 100 14 8354 8359 2-s2.0-0038153919 10.1073/pnas.1432104100 (Pubitemid 36842549)
25. Lal A., Mazan-Mamczarz K., Kawai T., Yang X., Martindale J. L., Gorospe M., Concurrent versus individual binding of HuR and AUF1 to common labile target mRNAs. EMBO Journal 2004 23 15 3092 3102 2-s2.0-4143122397 10.1038/sj.emboj. 7600305 (Pubitemid 39093603)
26. Lal A., Kawai T., Yang X., Mazan-Mamczarz K., Gorospe M., Antiapoptotic function of RNA-binding protein HuR effected through prothymosin α EMBO Journal 2005 24 10 1852 1862 2-s2.0-20044366611 10.1038/sj.emboj.7600661 (Pubitemid 40769504)
27. Abdelmohsen K., Pullmann R. Jr., Lal A., Kim H. H., Galban S., Yang X., Blethrow J. D., Walker M., Shubert J., Gillespie D. A., Furneaux H., Gorospe M., Phosphorylation of HuR by Chk2 regulates SIRT1 expression. Molecular Cell 2007 25 4 543 557 2-s2.0-33847035824 10.1016/j.molcel.2007.01.011 (Pubitemid 46274441)
28. Abdelmohsen K., Lal A., Kim H. H., Gorospe M., Posttranscriptional orchestration of an anti-apoptotic program by HuR. Cell Cycle 2007 6 11 1288 1292 2-s2.0-34547651351 (Pubitemid 47327958)
29. Kim H. H., Abdelmohsen K., Lal A., Pullmann R. Jr., Yang X., Galban S., Srikantan S., Martindale J. L., Blethrow J., Shokat K. M., Gorospe M., Nuclear HuR accumulation through phosphorylation by Cdk1. Genes and Development 2008 22 13 1804 1815 2-s2.0-46249130717 10.1101/gad.1645808 (Pubitemid 351915505)
30. Kim H. H., Kuwano Y., Srikantan S., Lee E. K., Martindale J. L., Gorospe M., HuR recruits let-7/RISC to repress c-Myc expression. Genes and Development 2009 23 15 1743 1748 2-s2.0-68149165414 10.1101/gad.1812509
31. López de Silanes I., Zhan M., Lal A., Yang X., Gorospe M., Identification of a target RNA motif for RNA-binding protein HuR. Proceedings of the National Academy of Sciences of the United States of America 2004 101 9 2987 2992 2-s2.0-1542297742 10.1073/pnas.0306453101 (Pubitemid 38327723)
32. López de Silanes I., Fan J., Yang X., Zonderman A. B., Potapova O., Pizer E. S., Gorospe M., Role of the RNA-binding protein HuR in colon carcinogenesis. Oncogene 2003 22 46 7146 7154 2-s2.0-16744361844 10.1038/sj.onc.1206862 (Pubitemid 37378547)
33. Gorospe M., HuR in the mammalian genotoxic response: post-transcriptional multitasking. Cell Cycle 2003 2 5 412 414 2-s2.0-2342573011
34. Figueroa A., Cuadrado A., Fan J., Atasoy U., Muscat G. E., Muoz-Canoves P., Gorospe M., Muoz A., Role of HuR in skeletal myogenesis through coordinate regulation of muscle differentiation genes. Molecular and Cellular Biology 2003 23 14 4991 5004 2-s2.0-0038450334 10.1128/MCB.23.14.4991-5004.2003 (Pubitemid 36793344)
35. van der Giessen K., Di-Marco S., Clair E., Gallouzi I. E., RNAi-mediated HuR depletion leads to the inhibition of muscle cell differentiation. Journal of Biological Chemistry 2003 278 47 47119 47128 2-s2.0-0344875497 10.1074/jbc.M308889200 (Pubitemid 37452298)
36. Katsanou V., Papadaki O., Milatos S., Blackshear P. J., Anderson P., Kollias G., Kontoyiannis D. L., HuR as a negative posttranscriptional modulator in inflammation. Molecular Cell 2005 19 6 777 789 2-s2.0-24944468765 10.1016/j.molcel.2005.08.007 (Pubitemid 41316672)
37. Abdelmohsen K., Kuwano Y., Kim H. H., Gorospe M., Posttranscriptional gene regulation by RNA-binding proteins during oxidative stress: implications for cellular senescence. Biological Chemistry 2008 389 3 243 255 2-s2.0-40149096226 10.1515/BC.2008.022 (Pubitemid 351329020)
38. Abdelmohsen K., Srikantan S., Yang X., Lal A., Kim H. H., Kuwano Y., Galban S., Becker K. G., Kamara D., De Cabo R., Gorospe M., Ubiquitin-mediated proteolysis of HuR by heat shock. EMBO Journal 2009 28 9 1271 1282 2-s2.0-65649116886 10.1038/emboj.2009.67
39. Basu A., Involvement of protein kinase C- δ in DNA damage-induced apoptosis. Journal of Cellular and Molecular Medicine 2003 7 4 341 350 2-s2.0-1642263353 (Pubitemid 44151685)
40. Kim H. H., Yang X., Kuwano Y., Gorospe M., Modification at HuR(S242) alters HuR localization and proliferative influence. Cell Cycle 2008 7 21 3371 3377 2-s2.0-55849099956
41. Doller A., Huwiler A., Müller R., Radeke H. H., Pfeilschifter J., Eberhardt W., Protein kinase C α -dependent phosphorylation of the mRNA-stabilizing factor HuR: implications for posttranscriptional regulation of cyclooxygenase-2. Molecular Biology of the Cell 2007 18 6 2137 2148 2-s2.0-34250362729 10.1091/mbc.E06-09-0850 (Pubitemid 46911365)
42. Subbaramaiah K., Marmo T. P., Dixon D. A., Dannenberg A. J., Regulation of cyclooxgenase-2 mRNA stability by taxanes: evidence for involvement of p38, MAPKAPK-2, and HuR. Journal of Biological Chemistry 2003 278 39 37637 37647 2-s2.0-0141844522 10.1074/jbc.M301481200 (Pubitemid 37175287)
43. Kuwano Y., Kim H. H., Abdelmohsen K., Pullmann R. Jr., Martindale J. L., Yang X., Gorospe M., MKP-1 mRNA stabilization and translational control by RNA-binding proteins HuR and NF90. Molecular and Cellular Biology 2008 28 14 4562 4575 2-s2.0-47049116117 10.1128/MCB.00165-08 (Pubitemid 351977754)
44. Mazroui R., Di Marco S., Clair E., Von Roretz C., Tenenbaum S. A., Keene J. D., Saleh M., Gallouzi I.-E., Caspase-mediated cleavage of HuR in the cytoplasm contributes to pp32/PHAP-I regulation of apoptosis. Journal of Cell Biology 2008 180 1 113 127 2-s2.0-38349047829 10.1083/jcb.200709030
45. Niida H., Nakanishi M., DNA damage checkpoints in mammals. Mutagenesis 2006 21 1 3 9 2-s2.0-33344476097 10.1093/mutage/gei063 (Pubitemid 43288730)
46. Kastan M. B., Lim D.-S., The many substrates and functions of ATM. Nature Reviews Molecular Cell Biology 2000 1 3 179 186 2-s2.0-0034576494
47. Cliby W. A., Roberts C. J., Cimprich K. A., Stringer C. M., Lamb J. R., Schreiber S. L., Friend S. H., Overexpression of a kinase-inactive ATR protein causes sensitivity to DNA-damaging agents and defects in cell cycle checkpoints. EMBO Journal 1998 17 1 159 169 2-s2.0-0032472330 10.1093/emboj/17.1.159 (Pubitemid 28041057)
48. Tibbetts R. S., Brumbaugh K. M., Williams J. M., Sarkaria J. N., Cliby W. A., Shieh S.-Y., Taya Y., Prives C., Abraham R. T., A role for ATR in the DNA damage-induced phosphorylation of p53. Genes and Development 1999 13 2 152 157 2-s2.0-0033555260 (Pubitemid 29061945)
49. Shiotani B., Zou L., Single-stranded DNA orchestrates an ATM-to-ATR switch at DNA breaks. Molecular Cell 2009 33 5 547 558 2-s2.0-61649093808 10.1016/j.molcel.2009.01.024
50. Shiloh Y., Kastan M. B., ATM: genome stability, neuronal development, and cancer cross paths. Advances in Cancer Research 2001 83 209 254 2-s2.0-0034798285 10.1016/S0065-230X(01)83007-4 (Pubitemid 32959266)
51. Motoyama N., Naka K., DNA damage tumor suppressor genes and genomic instability. Current Opinion in Genetics and Development 2004 14 1 11 16 2-s2.0-0842287638 10.1016/j.gde.2003.12.003 (Pubitemid 38173005)
52. Zhao H., Piwnica-Worms H., ATR-mediated checkpoint pathways regulate phosphorylation and activation of human Chk1. Molecular and Cellular Biology 2001 21 13 4129 4139 2-s2.0-0034967556 10.1128/MCB.21.13.4129-4139.2001 (Pubitemid 32565295)
53. Jin J., Shirogane T., Xu L., Nalepa G., Qin J., Elledge S. J., Harper J. W., SCF β -TRCP links Chk1 signaling to degradation of the Cdc25A protein phosphatase. Genes and Development 2003 17 24 3062 3074 2-s2.0-0347361537 10.1101/gad.1157503 (Pubitemid 38040770)
54. Donzelli M., Draetta G. F., Regulating mammalian checkpoints through Cdc25 inactivation. EMBO Reports 2003 4 7 671 677 2-s2.0-0043066731 10.1038/sj.embor.embor887 (Pubitemid 36974751)
55. Lee J., Kumagai A., Dunphy W. G., Positive regulation of Wee1 by Chk1 and 14-3-3 proteins. Molecular Biology of the Cell 2001 12 3 551 563 2-s2.0-0035158899 (Pubitemid 33052011)
56. Enomoto M., Goto H., hgoto@aichi-cc.jp Tomoro Y., Kasahara K., Tsujimura K., Kiyono T., Inagaki M., minagaki@aichi-cc.jp Novel positive feedback loop between Cdk1 and Chk1 in the nucleus during G2/M transition. Journal of Biological Chemistry 2009 284 49 34223 34230 2-s2.0-67649576600 10.1074/jbc.C109.051540
57. Smits V. A. J., Reaper P. M., Jackson S. P., Rapid PIKK-dependent release of Chk1 from chromatin promotes the DNA-damage checkpoint response. Current Biology 2006 16 2 150 159 2-s2.0-30944435598 10.1016/j.cub.2005.11.066 (Pubitemid 43117429)
58. Doller A., Akool E.-S., Huwiler A., Müller R., Radeke H. H., Pfeilschifter J., Eberhardt W., Posttranslational modification of the AU-rich element binding protein HuR by protein kinase C δ elicits angiotensin II-induced stabilization and nuclear export of cyclooxygenase 2 mRNA. Molecular and Cellular Biology 2008 28 8 2608 2625 2-s2.0-42149150455 10.1128/MCB.01530-07 (Pubitemid 351542362)
59. Zhou B.-B. S., Elledge S. J., The DNA damage response: putting checkpoints in perspective. Nature 2000 408 6811 433 439 2-s2.0-0034707047 10.1038/35044005
60. Reinhardt H. C., Yaffe M. B., Kinases that control the cell cycle in response to DNA damage: Chk1, Chk2, and MK2. Current Opinion in Cell Biology 2009 21 2 245 255 2-s2.0-63749131243 10.1016/j.ceb.2009.01.018
61. Bartek J., Falck J., Lukas J., Chk2 kinase - a busy messenger. Nature Reviews Molecular Cell Biology 2001 2 12 877 886 2-s2.0-0035656415 10.1038/35103059 (Pubitemid 33674087)
62. Bell D. W., Varley J. M., Szydlo T. E., Kang D. H., Wahrer D. C. R., Shannon K. E., Lubratovich M., Verselis S. J., Isselbacher K. J., Fraumeni J. F., Birch J. M., Li F. P., Garber J. E., Haber D. A., Heterozygous germ line hCHK2 mutations in Li-Fraumeni syndrome. Science 1999 286 5449 2528 2531 2-s2.0-0033601346 10.1126/science.286.5449.2528 (Pubitemid 30026346)
63. Vahteristo P., Bartkova J., Eerola H., Syrjäkoski K., Ojala S., Kilpivaara O., Tamminen A., Kononen J., Aittomäki K., Heikkilä P., Holli K., Blomqvist C., Bartek J., Kallioniemi O.-P., Nevanlinna H., A CHEK2 genetic variant contributing to a substantial fraction of familial breast cancer. American Journal of Human Genetics 2002 71 2 432 438 2-s2.0-18444379055 10.1086/341943 (Pubitemid 34800260)
64. Wu X., Webster S. R., Chen J., Characterization of tumor-associated Chk2 mutations. Journal of Biological Chemistry 2001 276 4 2971 2974 2-s2.0-0035951809 10.1074/jbc.M009727200
65. Doller A., Schlepckow K., Schwalbe H., Pfeilschifter J., Eberhardt W., w.eberhardt@em.uni-frankfurt.de Tandem phosphorylation of serines 221 and 318 by protein kinase C δ coordinates mRNA binding and nucleocytoplasmic shuttling of HuR. Molecular and Cellular Biology 2010 30 6 1397 1410 2-s2.0-40149096226 10.1128/MCB.01373-09
66. Doller A., Pfeilschifter J., Eberhardt W., Signalling pathways regulating nucleo-cytoplasmic shuttling of the mRNA-binding protein HuR. Cellular Signalling 2008 20 12 2165 2173 2-s2.0-55049088775 10.1016/j.cellsig.2008.05.007
67. Yoshida K., Nuclear trafficking of pro-apoptotic kinases in response to DNA damage. Trends in Molecular Medicine 2008 14 7 305 313 2-s2.0-46049090743 10.1016/j.molmed.2008.05.003
68. Molnár Á., Theodoras A. M., Zon L. I., Kyriakis J. M., Cdc42Hs, but not Rac1, inhibits serum-stimulated cell cycle progression at G1/S through a mechanism requiring p38/RK. Journal of Biological Chemistry 1997 272 20 13229 13235 2-s2.0-0031009434 10.1074/jbc.272.20.13229 (Pubitemid 27216750)
69. Cuenda A., Rousseau S., p38 MAP-kinases pathway regulation, function and role in human diseases. Biochimica et Biophysica Acta 2007 1773 8 1358 1375 2-s2.0-34547154349 10.1016/j.bbamcr.2007.03.010 (Pubitemid 47125981)
70. Thornton T. M., Rincon M., Non-classical p38 map kinase functions: cell cycle checkpoints and survival. International Journal of Biological Sciences 2009 5 1 44 52 2-s2.0-60149093582
71. Lafarga V., Cuadrado A., López de Silanes I., Bengoechea R., Fernandez-Capetillo O., Nebreda A. R., p38 mitogen-activated protein kinase- and HuR-dependent stabilization of p21Cip1 mRNA mediates the G1/S checkpoint. Molecular and Cellular Biology 2009 29 16 4341 4351 2-s2.0-68949161769 10.1128/MCB.00210-09
72. Tran H., Maurer F., Nagamine Y., Stabilization of urokinase and urokinase receptor mRNAs by HuR is linked to its cytoplasmic accumulation induced by activated mitogen-activated protein kinase-activated protein kinase 2. Molecular and Cellular Biology 2003 23 20 7177 7188 2-s2.0-0141640857 10.1128/MCB.23.20.7177-7188.2003 (Pubitemid 37211000)
73. Wang W., Yang X., Kawai T., López de Silanes I., Mazan-Mamczarz K., Chen P., Yuh M. C., Quensel C., Köhler M., Gorospe M., AMP-activated protein kinase-regulated phosphorylation and acetylation of importin α 1: involvement in the nuclear import of RNA-binding protein HuR. Journal of Biological Chemistry 2004 279 46 48376 48388 2-s2.0-9144266386 10.1074/jbc.M409014200 (Pubitemid 39540994)
74. Kim H. H., Gorospe M., Phosphorylated HuR shuttles in cycles. Cell Cycle 2008 7 20 3124 3126 2-s2.0-54049111406
75. Abdelmohsen K., Srikantan S., Kuwano Y., Gorospe M., miR-519 reduces cell proliferation by lowering RNA-binding protein HuR levels. Proceedings of the National Academy of Sciences of the United States of America 2008 105 51 20297 20302 2-s2.0-58149511991 10.1073/pnas.0809376106
76. Abdelmohsen K., Kim M. M., Srikantan S., miR-519 suppresses tumor growth by reducing HuR levels. Cell Cycle 2010 9 7 1354 1359
77. Abdelmohsen K., Gorospe M., Post-transcriptional regulation of cancer traits by HuR. WIRES RNA. In press