HuR maintains a replicative life span by repressing the ARF tumor suppressor

Molecular and Cellular Biology

Volumn 33, Issue 10, 2013, Pages 1886-1900

  Kawagishi, Hiroyuki ^a,c   Hashimoto, Michihiro ^a   Nakamura, Hideaki ^a   Tsugawa, Takayuki ^a   Watanabe, Atsushi ^a   Kontoyiannis, Dimitris L ^b   Sugimoto, Masataka ^a  

^a NATIONAL CENTER FOR GERIATRICS AND GERONTOLOGY   (Japan)

^b Institute of Immunology   (Greece)

^c NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARF PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR 2A; HUR PROTEIN; NUCLEOLIN; PROTEIN P19ARF; UNCLASSIFIED DRUG; CDKN2A PROTEIN, MOUSE; HU ANTIGEN; MESSENGER RNA; PHOSPHOPROTEIN; RNA BINDING PROTEIN; SMALL INTERFERING RNA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL AGING; CELL SURVIVAL; EMBRYO CELL; FIBROBLAST; GENE DELETION; GENE EXPRESSION; GENE LOCUS; HUMAN; HUMAN CELL; INSULIN SENSITIVITY; MOLECULAR STABILITY; MOUSE; NONHUMAN; NUCLEOLUS; PRIORITY JOURNAL; RIBOSOME; RNA REPLICATION; RNA TRANSLATION; 5' UNTRANSLATED REGION; ADIPOGENESIS; ANIMAL; CELL PROLIFERATION; CELL STRAIN 3T3; CELL STRAIN HEK293; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; INSULIN RESISTANCE; METABOLISM; MOUSE MUTANT; PHYSIOLOGY; PROTEIN BINDING; PROTEIN STABILITY; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; RNA STABILITY;

ANIMALIA;

5' UNTRANSLATED REGIONS; ADIPOGENESIS; ANIMALS; CELL AGING; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P16; FIBROBLASTS; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; HEK293 CELLS; HU PARANEOPLASTIC ENCEPHALOMYELITIS ANTIGENS; HUMANS; INSULIN RESISTANCE; MICE; MICE, KNOCKOUT; NIH 3T3 CELLS; PHOSPHOPROTEINS; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; PROTEIN STABILITY; PROTEIN TRANSPORT; RNA STABILITY; RNA, MESSENGER; RNA, SMALL INTERFERING; RNA-BINDING PROTEINS;

MLCS; MLOWN;

EID: 84878980875     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01277-12     Document Type: Article

References (61)

1. Hayflick L, Moorhead PS. 1961. The serial cultivation of human diploid cell strains. Exp. Cell Res. 25:585-621.
2. Dimri GP, Lee X, Basile G, Acosta M, Scott G, Roskelley C, Medrano EE, Linskens M, Rubelj I, Pereira-Smith O, Peacocke M, Campisi J. 1995. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc. Natl. Acad. Sci. U. S. A. 92:9363-9367.
3. Freund A, Orjalo AV, Desprez PY, Campisi J. 2010. Inflammatory networks during cellular senescence: causes and consequences. Trends Mol. Med. 16:238-246.
4. Ben-Porath I, Weinberg RA. 2005. The signals and pathways activating cellular senescence. Int. J. Biochem. Cell Biol. 37:961-976.
5. Sherr CJ. 2006. Divorcing ARF and p53: an unsettled case. Nat. Rev. Cancer 6:663-673.
6. Campisi Jand D, d'Adda F. 2007. Cellular senescence: when bad things happen to good cells. Nat. Rev. Mol. Cell Biol. 8:729-740.
7. Collado M, Blasco MA, Serrano M. 2007. Cellular senescence in cancer and aging. Cell 130:223-233.
8. Good PJ. 1995. A conserved family of elav-like genes in vertebrates. Proc. Natl. Acad. Sci. U. S. A. 92:4557-4561.
9. Ma WJ, Cheng S, Campbell C, Wright A, Furneaux H. 1996. Cloning and characterization of HuR, a ubiquitously expressed Elav-like protein. J. Biol. Chem. 271:8144-8151.
10. Katsanou V, Milatos S, Yiakouvaki A, Sgantzis N, Kotsoni A, Alexiou M, Harokopos V, Aidinis V, Hemberger M, Kontoyiannis DL. 2009. The RNA-binding protein Elavl1/HuR is essential for placental branching morphogenesis and embryonic development. Mol. Cell. Biol. 29:2762-2776.
11. Brennan CM, Steitz JA. 2001. HuR and mRNA stability. Cell. Mol. Life Sci. 58:266-277.
12. Doller A, Pfeilschifter J, Eberhardt W. 2008. Signalling pathways regulating nucleo-cytoplasmic shuttling of the mRNA-binding protein HuR. Cell. Signal. 20:2165-2173.
13. Abdelmohsen K, Lal A, Kim HH, Gorospe M. 2007. Posttranscriptional orchestration of an anti-apoptotic program by HuR. Cell Cycle 6:1288-1292.
14. Hinman MN, Lou H. 2008. Diverse molecular functions of Hu proteins. Cell. Mol. Life Sci. 65:3168-3181.
15. Dean JL, Wait R, Mahtani KR, Sully G, Clark AR, Saklatvala J. 2001. The 3' untranslated region of tumor necrosis factor alpha mRNA is a target of the mRNA-stabilizing factor HuR. Mol. Cell. Biol. 21:721-730.
16. Dormoy-Raclet V, Menard I, Clair E, Kurban G, Mazroui R, Di Marco S, von Roretz C, Pause A, Gallouzi IE. 2007. The RNA-binding protein HuR promotes cell migration and cell invasion by stabilizing the betaactin mRNA in a U-rich-element-dependent manner. Mol. Cell. Biol. 27: 5365-5380.
17. Levy NS, Chung S, Furneaux H, Levy AP. 1998. Hypoxic stabilization of vascular endothelial growth factor mRNA by the RNA-binding protein HuR. J. Biol. Chem. 273:6417-6423.
18. Lopez de Silanes I, Gorospe M, Taniguchi H, Abdelmohsen K, Srikantan S, Alaminos M, Berdasco M, Urdinguio RG, Fraga MF, Jacinto FV, Esteller M. 2009. The RNA-binding protein HuR regulates DNA methylation through stabilization of DNMT3b mRNA. Nucleic Acids Res. 37: 2658-2671.
19. 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.
20. 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.
21. Tominaga K, Srikantan S, Lee EK, Subaran SS, Martindale JL, Abdelmohsen K, Gorospe M. 2011. Competitive regulation of nucleolin expression by HuR and miR-494. Mol. Cell. Biol. 31:4219-4231.
22. Wang W, Yang X, Cristofalo VJ, Holbrook NJ, Gorospe M. 2001. Loss of HuR is linked to reduced expression of proliferative genes during replicative senescence. Mol. Cell. Biol. 21:5889-5898.
23. Abdelmohsen K, Srikantan S, Kuwano Y, Gorospe M. 2008. miR-519 reduces cell proliferation by lowering RNA-binding protein HuR levels. Proc. Natl. Acad. Sci. U. S. A. 105:20297-20302.
24. Marasa BS, Srikantan S, Martindale JL, Kim MM, Lee EK, Gorospe M, Abdelmohsen K. 2010. MicroRNA profiling in human diploid fibroblasts uncovers miR-519 role in replicative senescence. Aging (Albany, NY) 2:333-343.
25. Chang N, Yi J, Guo G, Liu X, Shang Y, Tong T, Cui Q, Zhan M, Gorospe M, Wang W. 2010. HuR uses AUF1 as a cofactor to promote p16INK4 mRNA decay. Mol. Cell. Biol. 30:3875-3886.
26. Mazan-Mamczarz K, Galban S, Lopez de Silanes I, Martindale JL, Atasoy U, Keene JD, Gorospe M. 2003. RNA-binding protein HuR enhances p53 translation in response to ultraviolet light irradiation. Proc. Natl. Acad. Sci. U. S. A. 100:8354-8359.
27. 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.
28. Krimpenfort P, Quon KC, Mooi WJ, Loonstra A, Berns A. 2001. Loss of p16Ink4a confers susceptibility to metastatic melanoma in mice. Nature 413:83-86.
29. Sharpless NE, Bardeesy N, Lee KH, Carrasco D, Castrillon DH, Aguirre AJ, Wu EA, Horner JW, DePinho RA. 2001. Loss of p16Ink4a with retention of p19ARF predisposes mice to tumorigenesis. Nature 413: 86-91.
30. Yamagishi M, Ishihama Y, Shirasaki Y, Kurama H, Funatsu T. 2009. Single-molecule imaging of beta-actin mRNAs in the cytoplasm of a living cell. Exp. Cell Res. 315:1142-1147.
31. Zindy F, Eischen CM, Randle DH, Kamijo T, Cleveland JL, Sherr CJ, Roussel MF. 1998. Myc signaling via the ARF tumor suppressor regulatesp53-dependent apoptosis and immortalization. Genes Dev. 12:2424-2433.
32. Heiman M, Schaefer A, Gong S, Peterson JD, Day M, Ramsey KE, Suarez-Farinas M, Schwarz C, Stephan DA, Surmeier DJ, Greengard P, Heintz N. 2008. A translational profiling approach for the molecular characterization of CNS cell types. Cell 135:738-748.
33. Nakamura H, Kawagishi H, Watanabe A, Sugimoto K, Maruyama M, Sugimoto M. 2011. Cooperative role of the RNA-binding proteins Hzf and HuR in p53 activation. Mol. Cell. Biol. 31:1997-2009.
34. Todaro GJ, Green H. 1963. Quantitative studies of the growth of mouse embryo cells in culture and their development into established lines. J. Cell Biol. 17:299-313.
35. Mu XC, Higgins PJ. 1995. Differential growth state-dependent regulation of plasminogen activator inhibitor type-1 expression in senescent IMR-90 human diploid fibroblasts. J. Cell. Physiol. 165:647-657.
36. Harvey M, Sands AT, Weiss RS, Hegi ME, Wiseman RW, Pantazis P, Giovanella BC, Tainsky MA, Bradley A, Donehower LA. 1993. In vitro growth characteristics of embryo fibroblasts isolated from p53-deficient mice. Oncogene 8:2457-2467.
37. Palmero I, Pantoja C, Serrano M. 1998. p19ARF links the tumour suppressor p53 to Ras. Nature 395:125-126.
38. Serrano M, Lin AW, McCurrach ME, Beach D, Lowe SW. 1997. Oncogenic ras provokes premature cell senescence associated with accumulation of p53 and p16INK4a. Cell 88:593-602.
39. Tsukada T, Tomooka Y, Takai S, Ueda Y, Nishikawa S, Yagi T, Tokunaga T, Takeda N, Suda Y, Abe S. 1993. Enhanced proliferative potential in culture of cells from p53-deficient mice. Oncogene 8:3313-3322.
40. Abdelmohsen K, Gorospe M. 2010. Posttranscriptional regulation of cancer traits by HuR. Wiley Interdiscip. Rev. RNA 1:214-229.
41. Sherr CJ. 2001. The INK4a/ARF network in tumour suppression. Nat. Rev. Mol. Cell Biol. 2:731-737.
42. Doyle JP, Dougherty JD, Heiman M, Schmidt EF, Stevens TR, Ma G, Bupp S, Shrestha P, Shah RD, Doughty ML, Gong S, Greengard P, Heintz N. 2008. Application of a translational profiling approach for the comparative analysis of CNS cell types. Cell 135:749-762.
43. Fusco D, Accornero N, Lavoie B, Shenoy SM, Blanchard JM, Singer RH, Bertrand E. 2003. Single mRNA molecules demonstrate probabilistic movement in living mammalian cells. Curr. Biol. 13:161-167.
44. Gajjar M, Candeias MM, Malbert-Colas L, Mazars A, Fujita J, Olivares-Illana V, Fahraeus R. 2012. The p53 mRNA-Mdm2 interaction controls Mdm2 nuclear trafficking and is required for p53 activation following DNA damage. Cancer Cell 21:25-35.
45. Abdelmohsen K, Tominaga K, Lee EK, Srikantan S, Kang MJ, Kim MM, Selimyan R, Martindale JL, Yang X, Carrier F, Zhan M, Becker KG, Gorospe M. 2011. Enhanced translation by Nucleolin via G-rich elements in coding and non-coding regions of target mRNAs. Nucleic Acids Res. 39:8513-8530.
46. Minamino T, Orimo M, Shimizu I, Kunieda T, Yokoyama M, Ito T, Nojima A, Nabetani A, Oike Y, Matsubara H, Ishikawa F, Komuro I. 2009. A crucial role for adipose tissue p53 in the regulation of insulin resistance. Nat. Med. 15:1082-1087.
47. Cherry J, Jones H, Karschner VA, Pekala PH. 2008. Post-transcriptional control of CCAAT/enhancer-binding protein beta (C/EBPbeta) expression: formation of a nuclear HuR-C/EBPbeta mRNA complex determines the amount of message reaching the cytosol. J. Biol. Chem. 283:30812-30820.
48. Krishnamurthy J, Torrice C, Ramsey MR, Kovalev GI, Al Regaiey K, Su L, Sharpless NE. 2004. Ink4a/ARF expression is a biomarker of aging. J. Clin. Invest. 114:1299-1307.
49. Kamijo T, Zindy F, Roussel MF, Quelle DE, Downing JR, Ashmun RA, Grosveld G, Sherr CJ. 1997. Tumor suppression at the mouse INK4a locus mediated by the alternative reading frame product p19ARF. Cell 91:649-659.
50. 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.
51. Yoon JH, Abdelmohsen K, Srikantan S, Yang X, Martindale JL, De S, Huarte M, Zhan M, Becker KG, Gorospe M. 2012. lincRNA-p21 suppresses target mRNA translation. Mol. Cell 47:648-655.
52. Mudhasani R, Zhu Z, Hutvagner G, Eischen CM, Lyle S, Hall LL, Lawrence JB, Imbalzano AN, Jones SN. 2008. Loss of miRNA biogenesis induces p19ARF-p53 signaling and senescence in primary cells. J. Cell Biol. 181:1055-1063.
53. Miceli AP, Saporita AJ, Weber JD. 2012. Hypergrowth mTORC1 signals translationally activate the ARF tumor suppressor checkpoint. Mol. Cell. Biol. 32:348-364.
54. Origanti S, Nowotarski SL, Carr TD, Sass-Kuhn S, Xiao L, Wang JY, Shantz LM. 2012. Ornithine decarboxylase mRNA is stabilized in an mTORC1-dependent manner in Ras-transformed cells. Biochem. J. 442: 199-207.
55. Gantt K, Cherry J, Tenney R, Karschner V, Pekala PH. 2005. An early event in adipogenesis, the nuclear selection of the CCAAT enhancerbinding protein β (C/EBPβ) mRNA by HuR and its translocation to the cytosol. J. Biol. Chem. 280:24768-24774.
56. Jones H, Carver M, Pekala PH. 2007. HuR binds to a single site on the C/EBPbeta mRNA of 3T3-L1 adipocytes. Biochem. Biophys. Res. Commun. 355:217-220.
57. Tanaka T, Yoshida N, Kishimoto T, Akira S. 1997. Defective adipocyte differentiation in mice lacking the C/EBPbeta and/or C/EBPdelta gene. EMBO J. 16:7432-7443.
58. Berberich SJ, Litteral V, Mayo LD, Tabesh D, Morris D. 1999. mdm-2 gene amplification in 3T3-L1 preadipocytes. Differentiation 64:205-212.
59. Saxena R, Voight BF, Lyssenko V, Burtt NP, de Bakker PI, Chen H, Roix JJ, Kathiresan S, Hirschhorn JN, Daly MJ, Hughes TE, Groop L, Altshuler D, Almgren P, Florez JC, Meyer J, Ardlie K, Bengtsson K, Isomaa B, Lettre G, Lindblad U, Lyon HN, Melander O, Newton-Cheh C, Nilsson P, Orho-Melander M, Rastam L, Speliotes EK, Taskinen MR, Tuomi T, Guiducci C, Berglund A, Carlson J, Gianniny L, Hackett R, Hall L, Holmkvist J, Laurila E, Sjogren M, Sterner M, Surti A, Svensson M, Svensson M, Tewhey R, Blumenstiel B, Parkin M, Defelice M, Barry R, Brodeur W, Camarata J, Chia N, Fava M, Gibbons J, Handsaker B, Healy C, Nguyen K, Gates C, Sougnez C, Gage D, Nizzari M, Gabriel SB, Chirn GW, Ma Q, Parikh H, Richardson D, Ricke D, Purcell S. 2007. Genome-wide association analysis identifies loci for type 2 diabetes and triglyceride levels. Science 316:1331-1336.
60. Scott LJ, Mohlke KL, Bonnycastle LL, Willer CJ, Li Y, Duren WL, Erdos MR, Stringham HM, Chines PS, Jackson AU, Prokunina-Olsson L, Ding CJ, Swift AJ, Narisu N, Hu T, Pruim R, Xiao R, Li XY, Conneely KN, Riebow NL, Sprau AG, Tong M, White PP, Hetrick KN, Barnhart MW, Bark CW, Goldstein JL, Watkins L, Xiang F, Saramies J, Buchanan TA, Watanabe RM, Valle TT, Kinnunen L, Abecasis GR, Pugh EW, Doheny KF, Bergman RN, Tuomilehto J, Collins FS, Boehnke M. 2007. A genome-wide association study of type 2 diabetes in Finns detects multiple susceptibility variants. Science 316:1341-1345.
61. Zeggini E, Weedon MN, Lindgren CM, Frayling TM, Elliott KS, Lango H, Timpson NJ, Perry JR, Rayner NW, Freathy RM, Barrett JC, Shields B, Morris AP, Ellard S, Groves CJ, Harries LW, Marchini JL, Owen KR, Knight B, Cardon LR, Walker M, Hitman GA, Morris AD, Doney AS, McCarthy MI, Hattersley AT. 2007. Replication of genome-wide association signals in U.K. samples reveals risk loci for type 2 diabetes. Science 316:1336-1341.