Global dissociation of HuR-mRNA complexes promotes cell survival after ionizing radiation

EMBO Journal

Volumn 30, Issue 6, 2011, Pages 1040-1053

  Masuda, Kiyoshi ^a   Abdelmohsen, Kotb ^a   Kim, Mihee M ^a   Srikantan, Subramanya ^a   Lee, Eun Kyung ^a   Tominaga, Kumiko ^a   Selimyan, Roza ^a   Martindale, Jennifer L ^a   Yang, Xiaoling ^a   Lehrmann, Elin ^a   Zhang, Yongqing ^a   Becker, Kevin G ^a   Wang, Jian Ying ^b   Kim, Hyeon Ho ^c   Gorospe, Myriam ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b BALTIMORE VA MEDICAL CENTER   (United States)

^c Samsung Medical Center   (South Korea)

Author keywords

Chk2; HuR phosphorylation; radiotherapy; ribonucleoprotein complex; RNA binding protein

Indexed keywords

CHECKPOINT KINASE 2; HUR PROTEIN; K RAS PROTEIN; MESSENGER RNA; PROTEIN BAX; PROTEIN MDM2;

APOPTOSIS; ARTICLE; CARCINOMA CELL; CELL SURVIVAL; COLORECTAL CARCINOMA; CONTROLLED STUDY; DISSOCIATION; HUMAN; HUMAN CELL; IONIZING RADIATION; MICROARRAY ANALYSIS; MUTANT; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PHOSPHORYLATION; RNA TRANSLATION; TRANSCRIPTION REGULATION;

ANTIGENS, SURFACE; CELL LINE; CELL SURVIVAL; EPITHELIAL CELLS; GENE EXPRESSION REGULATION; GENE KNOCKOUT TECHNIQUES; HUMANS; PROTEIN-SERINE-THREONINE KINASES; RADIATION, IONIZING; RNA, MESSENGER; RNA-BINDING PROTEINS;

EID: 79952754428     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2011.24     Document Type: Article

References (65)

1. Abdelmohsen K, Gorospe M (2010) Posttranscriptional regulation of cancer traits by HuR. WIRES RNA 1: 214-229
2. Abdelmohsen K, Kuwano Y, Kim HH, Gorospe M (2008) Posttranscriptional gene regulation by RNA-binding proteins during oxidative stress: implications for cellular senescence. Biol Chem 389: 243-255 (Pubitemid 351329020)
3. Abdelmohsen K, Pullmann Jr R, Lal A, Kim HH, Galban S, Yang X, Blethrow JD, Walker M, Shubert J, Gillespie DA, Furneaux H, Gorospe M (2007) Phosphorylation of HuR by Chk2 regulates SIRT1 expression. Mol Cell 25: 543-557 (Pubitemid 46274441)
4. Ahn J, Urist M, Prives C (2004) The Chk2 protein kinase. DNA Repair 3: 1039-1047 (Pubitemid 38997946)
5. Antoni L, Sodha N, Collins I, Garrett MD (2007) CHK2 kinase: cancer susceptibility and cancer therapy-two sides of the same coin? Nat Rev Cancer 7: 925-936 (Pubitemid 350165855)
6. Bartek J, Lukas J (2003) Chk1 and Chk2 kinases in checkpoint control and cancer. Cancer Cell 3: 421-429 (Pubitemid 38340288)
7. Bhattacharyya SN, Habermacher R, Martine U, Closs EI, Filipowicz W (2006) Relief of microRNA-mediated translational repression in human cells subjected to stress. Cell 125: 1111-1124 (Pubitemid 43866197)
8. Bouska A, Eischen CM (2009) Murine double minute 2: p53-independent roads lead to genome instability or death. Trends Biochem Sci 34: 279-286
9. Brennan P, McKay J, Moore L, Zaridze D, Mukeria A, Szeszenia-Dabrowska N, Lissowska J, Rudnai P, Fabianova E, Mates D, Bencko V, Foretova L, Janout V, Chow WH, Rothman N, Chabrier A, Gaborieau V, Odefrey F, Southey M, Hashibe M, Hall J, Boffetta P, Peto J, Peto R, Hung RJ (2007) Uncommon CHEK2 mis-sense variant and reduced risk of tobacco-related cancers: case control study. Hum Mol Genet 16: 1794-1801 (Pubitemid 47244527)
10. Cory S, Adams JM (2002) The Bcl2 family: regulators of the cellular life-or-death switch. Nat Rev Cancer 2: 647-656 (Pubitemid 37328916)
11. Doller A, Akool el-S, Huwiler A, Müller R, Radeke HH, Pfeilschifter J, Eberhardt W (2008b) Posttranslational modification of the AU-rich element binding protein HuR by protein kinase Cdelta elicits angiotensin II-induced stabilization and nuclear export of cyclooxygenase 2 mRNA. Mol Cell Biol 28: 2608-2625 (Pubitemid 351542362)
12. Doller A, Huwiler A, Müller R, Radeke HH, Pfeilschifter J, Eberhardt W (2007) Protein kinase Ca-dependent phosphoryla-tion of the mRNA-stabilizing factor HuR: implications for post-transcriptional regulation of cyclooxygenase-2. Mol Biol Cell 18: 2137-2148 (Pubitemid 46911365)
13. Doller A, Pfeilschifter J, Eberhardt W (2008a) Signalling pathways regulating nucleo-cytoplasmic shuttling of the mRNA-binding protein HuR. Cell Signal 20: 2165-2173
14. Fanning AS, Anderson JM (2009) Zonula occludens-1 and -2 are cytosolic scaffolds that regulate the assembly of cellular junctions. Ann NYAcad Sci 1165: 113-120
15. Foster JW, Dominguez-Steglich MA, Guioli S, Kwok C, Weller PA, Stev M, Weissenbach J, Mansour S, Young ID, Goodfellow PN, Brook JD, Schafer AJ (1994) Campomelic dysplasia and auto-somal sex reversal caused by mutations in an SRY-related gene. Nature 372: 525-530 (Pubitemid 24368528)
16. Freiberg RA, Hammond EM, Dorie MJ, Welford SM, Giaccia AJ (2006) DNA damage during reoxygenation elicits a Chk2-depen-dent checkpoint response. Mol Cell Biol 26: 1598-1609
17. Gallouzi IE, Steitz JA (2001) Delineation of mRNA export pathways by the use of cell-permeable peptides. Science 294: 1895-1901 (Pubitemid 33101580)
18. Ghosh JC, Dohi T, Raskett CM, Kowalik TF, Altieri DC (2006) Activated checkpoint kinase 2 provides a survival signal for tumor cells. Cancer Res 66: 11576-11579 (Pubitemid 46094165)
19. Ghosh M, Aguila HL, Michaud J, Ai Y, Wu MT, Hemmes A, Ristimaki A, Guo C, Furneaux H, Hla T (2009) Essential role of the RNA-binding protein HuR in progenitor cell survival in mice. J Clin Invest 119: 3530-3543
20. Gibson SL, Bindra RS, Glazer PM (2005) Hypoxia-induced phosphorylation of Chk2 in an ataxia telangiectasia mutated-dependent manner. Cancer Res 65: 10734-10741 (Pubitemid 41713341)
21. Gorospe M, de Cabo R (2008) AsSIRTing the DNA damage response. Trends Cell Biol 18: 77-83
22. Guttinger S, Muhlhausser P, Koller-Eichhorn R, Brennecke J, Kutay U (2004) Transportin2 functions as importin and mediates nuclear import of HuR. Proc Natl Acad Sci USA 101: 2918-2923 (Pubitemid 38327711)
23. Harper JW, Elledge SJ (2007) The DNA damage response: ten years after. Mol Cell 28: 739-745 (Pubitemid 350217064)
24. Hinman MN, Lou H (2008) Diverse molecular functions of Hu proteins. Cell Mol Life Sci 65: 3168-3181
25. Hur EH, Hur W, Choi JY, Kim IK, Kim HY, Yoon SK, Rhim H (2004) Functional identification of the pro-apoptotic effector domain in human Sox4. Biochem Biophys Res Commun 325: 59-67 (Pubitemid 39441160)
26. Jackson SP, Bartek J (2009) The DNA-damage response in human biology and disease. Nature 461: 1071-1078
27. Jallepalli PV, Lengauer C, Vogelstein B, Bunz F (2003) The Chk2 tumor suppressor is not required for p53 responses in human cancer cells. J Biol Chem 278: 20475-20479 (Pubitemid 36806343)
28. Kastan MB, Lim DS (2000) The many substrates and functions of ATM. Nat Rev Mol Cell Biol 1: 179-186
29. Kawai T, Lal A, Yang X, Galban S, Mazan-Mamczarz K, Gorospe M (2006) Translational control of cytochrome c by RNA-binding proteins TIA-1 and HuR. Mol Cell Biol 26: 3295-3307
30. Keene JD (1999) Why is Hu where? Shuttling of early-response-gene messenger RNA subsets. Proc Natl Acad Sci USA 96: 5-7 (Pubitemid 29036041)
31. Kim HH, Abdelmohsen K, Lal A, Pullmann Jr R, Yang X, Galban S, Srikantan S, Martindale JL, Blethrow J, Shokat KM, Gorospe M (2008b) Nuclear HuR accumulation through phosphorylation by Cdk1. Genes Dev 22: 1804-1815 (Pubitemid 351915505)
32. Kim HH, Gorospe M (2008) Phosphorylated HuR shuttles in cycles. Cell Cycle 7: 3124-3126
33. Kim HH, Kuwano Y, Srikantan S, Lee EK, Martindale JL, Gorospe M (2009) HuR recruits let-7/RISC to repress c-Myc expression. Genes Dev 23: 1743-1748
34. Kim HH, Yang X, Kuwano Y, Gorospe M (2008a) Modification at HuR(S242) alters HuR localization and proliferative influence. Cell Cycle 7: 3371-3377
35. 0UTR. Genes Dev 16: 3087-3099 (Pubitemid 35424195)
36. Kuwano Y, Pullmann Jr R, Marasa BS, Abdelmohsen K, Lee EK, Yang X, Martindale JL, Zhan M, Gorospe M (2010) NF90 selectively represses the translation of target mRNAs bearing an AU-rich signature motif. Nucleic Acids Res 38: 225-238
37. Kwok C, Weller PA, Guioli S, Foster JW, Mansour S, Zuffardi O, Punnett HH, Dominguez-Steglich MA, Brook JD, Young ID, Goodfellow PN, Schafer AJ (1995) Mutations in SOX9, the gene responsible for Campomelic dysplasia and autosomal sex reversal. Am J Hum Genet 57: 1028-1036
38. Lafarga V, Cuadrado A, Lopez de Silanes I, Bengoechea R, Fernandez-Capetillo O, Nebreda AR (2009) p38 Mitogen-activated protein kinase- and HuR-dependent stabilization of p21(Cip1) mRNA mediates the G(1)/S checkpoint. Mol Cell Biol 29: 4341-4351
39. Lal A, Abdelmohsen K, Pullmann R, Kawai T, Galban S, Yang X, Brewer G, Gorospe M (2006) Posttranscriptional derepression of GADD45alpha by genotoxic stress. Mol Cell 22: 117-128
40. Lal A, Mazan-Mamczarz K, Kawai T, Yang X, Martindale JL, Gorospe M (2004) Concurrent versus individual binding of HuR and AUF1 to common labile target mRNAs. EMBO J 23: 3092-3102 (Pubitemid 39093603)
41. Liu P, Ramachandran S, Ali Seyed M, Scharer CD, Laycock N, Dalton WB, Williams H, Karanam S, Datta MW, Jaye DL, Moreno CS (2006) Sex-determining region Y box 4 is a transforming oncogene in human prostate cancer cells. Cancer Res 66: 4011-4019
42. López de Silanes I, Zhan M, Lal A, Yang X, Gorospe M (2004) Identification of a target RNA motif for RNA-binding protein HuR. Proc Natl Acad Sci USA 101 : 2987-2992 (Pubitemid 38327723)
43. Malumbres M, Barbacid M (2003) RAS oncogenes: the first 30 years. Nat Rev Cancer 3: 459-465 (Pubitemid 37328850)
44. Manfredi JJ (2010) The Mdm2-p53 relationship evolves: Mdm2 swings both ways as an oncogene and a tumor suppressor. Genes Dev 24: 1580-1589
45. Matsuoka S, Huang M, Elledge SJ (1998) Linkage of ATM to cell cycle regulation by the Chk2 protein kinase. Science 282: 1893-1897 (Pubitemid 28555269)
46. Melchionna R, Chen XB, Blasina A, McGowan CH (2000) Threonine 68 is required for radiation-induced phosphorylation and activation of Cds1. Nat Cell Biol 2: 762-765
47. Meng Z, Jackson NL, Choi H, King PH, Emanuel PD, Blume SW (2008) Alterations in RNA-binding activities of IRES-regulatory proteins as a mechanism for physiological variability and pathological dysregulation of IGF-IR translational control in human breast tumor cells. J Cell Physiol 217: 172-183
48. Murakami H, Okayama H (1995) A kinase from fission yeast responsible for blocking mitosis in S phase. Nature 374: 817-819
49. Passeron T, Valencia JC, Namiki T, Vieira WD, Passeron H, Miyamura Y, Hearing VJ (2009) Upregulation of SOX9 inhibits the growth of human and mouse melanomas and restores their sensitivity to retinoic acid. J Clin Invest 119: 954-963
50. Perona R, Moncho-Amor V, Machado-Pinilla R, Belda-Iniesta C, Sánchez Pérez I (2008) Role of CHK2 in cancer development. Clin Transl Oncol 10: 538-542
51. Pothof J, Verkaik NS, van IJcken W, Wiemer EA, Ta VT, van der Horst GT, Jaspers NG, van Gent DC, Hoeijmakers JH, Persengiev SP (2009) MicroRNA-mediated gene silencing modulates the UV-induced DNA-damage response. EMBO J 28: 2090-2099
52. Rebane A, Aab A, Steitz JA (2004) Transportins 1 and 2 are redundant nuclear import factors for hnRNP A1 and HuR. RNA 10: 590-599 (Pubitemid 38405937)
53. Samuels-Lev Y, O'Connor DJ, Bergamaschi D, Trigiante G, Hsieh JK, Zhong S, Campargue I, Naumovski L, Crook T, Lu X (2001) ASPP proteins specifically stimulate the apoptotic function of p53. Mol Cell 8: 781-794 (Pubitemid 33030212)
54. Siddiqui AD, Piperdi B (2010) KRAS mutation in colon cancer: a marker of resistance to EGFR-I therapy. Ann Surg Oncol 17: 1168-1176
55. Sodha N, Mantoni TS, Tavtigian SV, Eeles R, Garrett MD (2006) Rare germ line CHEK2 variants identified in breast cancer families encode proteins that show impaired activation. Cancer Res 66: 8966-8970 (Pubitemid 44521112)
56. Stevens C, Smith L, La Thangue NB (2003) Chk2 activates E2F-1 in response to DNA damage. Nat Cell Biol 5: 401-409 (Pubitemid 36592262)
57. Stoecklin G, Stubbs T, Kedersha N, Wax S, Rigby WF, Blackwell TK, Anderson P (2004) MK2-induced tristetraprolin: 14-3-3 complexes prevent stress granule association and ARE-mRNA decay. EMBO J 23: 1313-1324 (Pubitemid 38525003)
58. Takai H, Naka K, Okada Y, Watanabe M, Harada N, Saito S, Anderson CW, Appella E, Nakanishi M, Suzuki H, Nagashima K, Sawa H, Ikeda K, Motoyama N (2002) Chk2-deficient mice exhibit radioresistance and defective p53-mediated transcription. EMBO J 21: 5195-5205
59. Tsukita S, Itoh M, Nagafuchi A, Yonemura S, Tsukita S (1993) Submembranous junctional plaque proteins include potential tumor suppressor molecules. J Cell Biol 123: 1049-1053 (Pubitemid 23352416)
60. Wagner-Ecker M, Schwager C, Wirkner U, Abdollahi A, Huber PE (2010) MicroRNA expression after ionizing radiation in human endothelial cells. Radiat Oncol 5: 25
61. Wang W, Furneaux H, Cheng H, Caldwell MC, Hutter D, Liu Y, Holbrook N, Gorospe M (2000) HuR regulates p21 mRNA stabilization by UV light. Mol Cell Biol 20: 760-769 (Pubitemid 30044212)
62. Wang W, Yang X, Kawai T, López de Silanes I, Mazan-Mamczarz K, Chen P, Chook YM, Quensel C, Köhler M, Gorospe M (2004) AMP-activated protein kinase-regulated phosphorylation and acetylation of importin alpha1: involvement in the nuclear import of RNA-binding protein HuR. J Biol Chem 279: 48376-48388 (Pubitemid 39540994)
63. Wilusz CJ, Wilusz J (2007) HuR-SIRT: the hairy world of posttran-scriptional control. Mol Cell 25: 485-487 (Pubitemid 46274450)
64. Yang S, Kuo C, Bisi JE, Kim MK (2002) PML-dependent apoptosis after DNA damage is regulated by the checkpoint kinase hCds1/ Chk2. Nat Cell Biol 4: 865-870 (Pubitemid 35331361)
65. Yu Q, La Rose J, Zhang H, Takemura H, Kohn KW, Pommier Y (2002) UCN-01 inhibits p53 up-regulation and abrogates gamma-radiation-induced G(2)-M checkpoint independently of p53 by targeting both of the checkpoint kinases, Chk2 and Chk1. Cancer Res 62: 5743-5748 (Pubitemid 35204730)