HuR, a key post-transcriptional regulator, and its implication in progression of breast cancer

Histology and Histopathology

Volumn 25, Issue 10, 2010, Pages 1331-1340

  Yuan, Zhu ^a,b   Sanders, Andrew J ^a   Ye, Lin ^a   Jiang, Wen G ^a  

^a CARDIFF UNIVERSITY SCHOOL OF MEDICINE   (United Kingdom)

^b CAPITAL MEDICAL UNIVERSITY   (China)

Author keywords

AU and U rich elements (AREs); Breast cancer; Carcinogenesis; HuR; Nucleo cytoplasmic shuttling

Indexed keywords

ELAV-LIKE PROTEIN 1; HUR PROTEIN; MEMBRANE ANTIGEN; MESSENGER RNA; RNA BINDING PROTEIN;

ANIMAL; BREAST TUMOR; FEMALE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; PATHOLOGY; REVIEW; RNA PROCESSING; RNA STABILITY; SIGNAL TRANSDUCTION;

ANIMALS; ANTIGENS, SURFACE; BREAST NEOPLASMS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA STABILITY; RNA, MESSENGER; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION;

EID: 79952022055     PISSN: 02133911     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (101)

1. Anderson K.D., Morin M.A., Beckel-Mitchener A., Mobarak C.D., Neve R.L., Furneaux H.M., Burry R. and Perrone-Bizzozero N.I. (2000). Overexpression of HuD, but not of its truncated form HuD I+II, promotes GAP-43 gene expression and neurite outgrowth in PC12 cells in the absence of nerve growth factor. J. Neurochem. 75, 1103-1114.
2. Antic D. and Keene J.D. (1997). Embryonic lethal abnormal visual RNAbinding proteins involved in growth, differentiation, and posttranscriptional gene expression. Am. J. Hum. Genet. 61, 273-278.
3. 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.
4. Bakheet T., Williams B.R. and Khabar K.S. (2003). ARED 2.0: an update of AU-rich element mRNA database. Nucleic Acids Res. 31, 421-423.
5. Barreau C., Paillard L. and Osborne H.B. (2005). AU-rich elements and associated factors: are there unifying principles? Nucleic Acids Res. 33, 7138-7150.
6. Beckel-Mitchener A.C., Miera A., Keller R. and Perrone-Bizzozero N.I. (2002). Poly(A) tail length-dependent stabilization of GAP-43 mRNA by the RNA-binding protein HuD. J. Biol. Chem. 277, 27996-28002.
7. Bolster D.R., Crozier S.J., Kimball S.R. and Jefferson L.S. (2002). AMPactivated protein kinase suppresses protein synthesis in rat skeletal muscle through down-regulated mammalian target of rapamycin (mTOR) signaling. J. Biol. Chem. 277, 23977-23980.
8. Brennan C.M. and Steitz J.A. (2001). HuR and mRNA stability. Cell. Mol. Life Sci. 58, 266-277.
9. Brennan C.M., Gallouzi I.E. and Steitz J.A. (2000). Protein ligands to HuR modulate its interaction with target mRNAs in vivo. J. Cell Biol. 151, 1-14.
10. Chen C.Y. and Shyu A.B. (1995). AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem. Sci. 20, 465-470.
11. Chen C.Y., Xu N. and Shyu A.B. (2002). Highly selective actions of HuR in antagonizing AU-rich element-mediated mRNA destabilization. Mol. Cell Biol. 22, 7268-7278.
12. Claus E.B., Schildkraut J.M., Thompson W.D. and Risch N.J. (1996). The genetic attributable risk of breast and ovarian cancer. Cancer 77, 2318-2324.
13. David P.S., Tanveer R. and Port J.D. (2007). FRET-detectable interactions between the ARE binding proteins, HuR and p37AUF1. RNA 13, 1453-1468.
14. Dean J.L., Wait R., Mahtani K.R., Sully G., Clark A.R. and Saklatvala J. (2001). The 3' untranslated region of tumour necrosis factor alpha mRNA is a target of the mRNA-stabilizing factor HuR. Mol. Cell Biol. 21, 721-730.
15. Dean J.L., Sully G., Clark A.R. and Saklatvala J. (2004). The involvement of AU-rich element-binding proteins in p38 mitogenactivated protein kinase pathway-mediated mRNA stabilisation. Cell Signal. 16, 1113-1121.
16. Denkert C., Weichert W., Pest S., Koch I., Licht D., Kobel M., Reles A., Sehouli J., Dietel M. and Hauptmann S. (2004a). Overexpression of the embryonic-lethal abnormal vision-like protein HuR in ovarian carcinoma is a prognostic factor and is associated with increased cyclooxygenase 2 expression. Cancer Res. 64, 189-195.
17. Denkert C., Weichert W., Winzer K.J., Muller B.M., Noske A., Niesporek S., Kristiansen G., Guski H., Dietel M. and Hauptmann S. (2004b). Expression of the ELAV-like protein HuR is associated with higher tumour grade and increased cyclooxygenase-2 expression in human breast carcinoma. Clin. Cancer Res. 10, 5580-5586.
18. Deschenes-Furry J., Perrone-Bizzozero N. and Jasmin B.J. (2006). The RNA-binding protein HuD: a regulator of neuronal differentiation, maintenance and plasticity. Bioessays 28, 822-833.
19. Dixon D.A., Tolley N.D., King P.H., Nabors L.B., McIntyre T.M., Zimmerman G.A. and Prescott S.M. (2001). Altered expression of the mRNA stability factor HuR promotes cyclooxygenase-2 expression in colon cancer cells. J. Clin. Invest. 108, 1657-1665.
20. Doller A., Akool el S., Huwiler A., Muller R., Radeke H.H., Pfeilschifter J. and Eberhardt W. (2008). Posttranslational modification of the AUrich 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.
21. Doller A., Huwiler A., Muller R., Radeke H.H., Pfeilschifter J. and Eberhardt W. (2007). Protein kinase C alpha-dependent phosphorylation of the mRNA-stabilizing factor HuR: implications for posttranscriptional regulation of cyclooxygenase-2. Mol. Biol. Cell. 18, 2137-2148.
22. Doller A., Pfeilschifter J. and Eberhardt W. (2008). Signalling pathways regulating nucleo-cytoplasmic shuttling of the mRNA-binding protein HuR. Cell Signal. 20, 2165-2173.
23. el-Kabbani O., Chang C.H., Tiede D., Norris J. and Schiffer M. (1991). Comparison of reaction centers from Rhodobacter sphaeroides and Rhodopseudomonas viridis: overall architecture and protein-pigment interactions. Biochemistry 30, 5361-5369.
24. Erkinheimo T.L., Lassus H., Sivula A., Sengupta S., Furneaux H., Hla T., Haglund C., Butzow R. and Ristimaki A. (2003). Cytoplasmic HuR expression correlates with poor outcome and with cyclooxygenase 2 expression in serous ovarian carcinoma. Cancer Res. 63, 7591-7594.
25. Esnault S. and Malter J.S. (2003). Hyaluronic acid or TNF-alpha plus fibronectin triggers granulocyte macrophage-colony-stimulating factor mRNA stabilization in eosinophils yet engages differential intracellular pathways and mRNA binding proteins. J. Immunol. 171, 6780-6787.
26. Fan X.C. and Steitz J.A. (1998). HNS, a nuclear-cytoplasmic shuttling sequence in HuR. Proc. Natl. Acad. Sci. USA 95, 15293-15298.
27. Galban S., Kuwano Y., Pullmann R. Jr, Martindale J.L., Kim H.H., Lal A., Abdelmohsen K., Yang X., Dang Y., Liu J.O., Lewis S.M., Holcik M. and Gorospe M. (2008). RNA-binding proteins HuR and PTB promote the translation of hypoxia-inducible factor 1alpha. Mol. Cell Biol. 28, 93-107.
28. Ghosh M., Aguila H.L., Michaud J., Ai Y., Wu M.T., Hemmes A., Ristimaki A., Guo C., Furneaux H. and Hla T. (2009). Essential role of the RNA-binding protein HuR in progenitor cell survival in mice. J. Clin. Invest. 119, 3530-3543.
29. Guhaniyogi J. and Brewer G. (2001). Regulation of mRNA stability in mammalian cells. Gene 265, 11-23.
30. Guo X. and Hartley R.S. (2006). HuR contributes to cyclin E1 deregulation in MCF-7 breast cancer cells. Cancer Res. 66, 7948-7956.
31. Guo X., Wu Y. and Hartley R.S. (2009). MicroRNA-125a represses cell growth by targeting HuR in breast cancer. RNA Biol. 6, 575-583.
32. Hanahan D. and Weinberg R.A. (2000). The hallmarks of cancer. Cell 100, 57-70.
33. Heinonen M., Bono P., Narko K., Chang S.H., Lundin J., Joensuu H., Furneaux H., Hla T., Haglund C. and Ristimaki A. (2005). Cytoplasmic HuR expression is a prognostic factor in invasive ductal breast carcinoma. Cancer Res. 65, 2157-2161.
34. Heinonen M., Fagerholm R., Aaltonen K., Kilpivaara O., Aittomaki K., Blomqvist C., Heikkila P., Haglund C., Nevanlinna H. and Ristimaki A. (2007). Prognostic role of HuR in hereditary breast cancer. Clin. Cancer Res. 13, 6959-6963.
35. Hinman M.N. and Lou H. (2008). Diverse molecular functions of Hu proteins. Cell. Mol. Life Sci. 65, 3168-3181.
36. Hostetter C., Licata L.A., Witkiewicz A., Costantino C.L., Yeo C.J., Brody J.R. and Keen J.C. (2008). Cytoplasmic accumulation of the RNA binding protein HuR is central to tamoxifen resistance in estrogen receptor positive breast cancer cells. Cancer Biol. Ther. 7, 1496-1506.
37. Huwiler A., Akool el S., Aschrafi A., Hamada F.M., Pfeilschifter J. and Eberhardt W. (2003). ATP potentiates interleukin-1 beta-induced MMP-9 expression in mesangial cells via recruitment of the ELAV protein HuR. J. Biol. Chem. 278, 51758-51769.
38. Ide H., Seligson D.B., Memarzadeh S., Xin L., Horvath S., Dubey P., Flick M.B., Kacinski B.M., Palotie A. and Witte O.N. (2002). Expression of colony-stimulating factor 1 receptor during prostate development and prostate cancer progression. Proc. Natl. Acad. Sci. USA 99, 14404-14409.
39. Inoue M., Muto Y., Sakamoto H. and Yokoyama S. (2000). NMR studies on functional structures of the AU-rich element-binding domains of Hu antigen C. Nucleic Acids Res. 28, 1743-1750.
40. Jaiyesimi I.A., Buzdar A.U., Decker D.A. and Hortobagyi G.N. (1995). Use of tamoxifen for breast cancer: twenty-eight years later. J. Clin. Oncol. 13, 513-529.
41. Jin S.H., Kim T.I., Yang K.M. and Kim W.H. (2007). Thalidomide destabilizes cyclooxygenase-2 mRNA by inhibiting p38 mitogenactivated protein kinase and cytoplasmic shuttling of HuR. Eur. J. Pharmacol. 558, 14-20.
42. Katsanou V., Milatos S., Yiakouvaki A., Sgantzis N., Kotsoni A., Alexiou M., Harokopos V., Aidinis V., Hemberger M. and Kontoyiannis D.L. (2009). The RNA-binding protein Elavl1/HuR is essential for placental branching morphogenesis and embryonic development. Mol. Cell Biol. 29, 2762-2776.
43. Kluger H.M., Dolled-Filhart M., Rodov S., Kacinski B.M., Camp R.L. and Rimm D.L. (2004). Macrophage colony-stimulating factor-1 receptor expression is associated with poor outcome in breast cancer by large cohort tissue microarray analysis. Clin. Cancer Res. 10, 173-177.
44. Lafarga V., Cuadrado A., Lopez de Silanes I., Bengoechea R., Fernandez-Capetillo O. and Nebreda A.R. (2009). p38 Mitogenactivated protein kinase- and HuR-dependent stabilization of p21(Cip1) mRNA mediates the G(1)/S checkpoint. Mol. Cell Biol. 29, 4341-4351.
45. Lafon I., Carballes F., Brewer G., Poiret M. and Morello D. (1998). Developmental expression of AUF1 and HuR, two c-myc mRNA binding proteins. Oncogene 16, 3413-3421.
46. Lai W.S. and Blackshear P.J. (2001). Interactions of CCCH zinc finger proteins with mRNA: tristetraprolin-mediated AU-rich elementdependent mRNA degradation can occur in the absence of a poly(A) tail. J. Biol. Chem. 276, 23144-23154.
47. Lal A., Mazan-Mamczarz K., Kawai T., Yang X., Martindale J.L. and Gorospe M. (2004). Concurrent versus individual binding of HuR and AUF1 to common labile target mRNAs. EMBO J. 23, 3092-3102.
48. Lal A., Kawai T., Yang X., Mazan-Mamczarz K. and Gorospe M. (2005). Antiapoptotic function of RNA-binding protein HuR effected through prothymosin alpha. EMBO J. 24, 1852-1862.
49. Lasa M., Mahtani K.R., Finch A., Brewer G., Saklatvala J. and Clark A.R. (2000). Regulation of cyclooxygenase 2 mRNA stability by the mitogen-activated protein kinase p38 signaling cascade. Mol. Cell Biol. 20, 4265-4274.
50. Lazarova D.L., Spengler B.A., Biedler J.L. and Ross R.A. (1999). HuD, a neuronal-specific RNA-binding protein, is a putative regulator of Nmyc pre-mRNA processing/stability in malignant human neuroblasts. Oncogene 18, 2703-2710.
51. 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.
52. Li M., Makkinje A. and Damuni Z. (1996). Molecular identification of I1PP2A, a novel potent heat-stable inhibitor protein of protein phosphatase 2A. Biochemistry 35, 6998-7002.
53. Lopez de Silanes I., Fan J., Yang X., Zonderman A.B., Potapova O., Pizer E.S. and Gorospe M. (2003). Role of the RNA-binding protein HuR in colon carcinogenesis. Oncogene 22, 7146-7154.
54. Lopez de Silanes I., Fan J., Galban C.J., Spencer R.G., Becker K.G. and Gorospe M. (2004a). Global analysis of HuR-regulated gene expression in colon cancer systems of reducing complexity. Gene Expr. 12, 49-59.
55. Lopez de Silanes I., Zhan M., Lal A., Yang X. and Gorospe M. (2004b). Identification of a target RNA motif for RNA-binding protein HuR. Proc. Natl. Acad. Sci. USA 101, 2987-2992.
56. Lopez de Silanes I., Lal A. and Gorospe M. (2005). HuR: posttranscriptional paths to malignancy. RNA Biol. 2, 11-13.
57. Lykke-Andersen J. and Wagner E. (2005). Recruitment and activation of mRNA decay enzymes by two ARE-mediated decay activation domains in the proteins TTP and BRF-1. Genes Dev. 19, 351-361.
58. Ma W.J. and Furneaux H. (1997). Localization of the human HuR gene to chromosome 19p13.2. Hum. Genet. 99, 32-33.
59. Ma W.J., Cheng S., Campbell C., Wright A. and Furneaux H. (1996). Cloning and characterization of HuR, a ubiquitously expressed Elavlike protein. J. Biol. Chem. 271, 8144-8151.
60. Ma W.J., Chung S. and Furneaux H. (1997). The Elav-like proteins bind to AU-rich elements and to the poly(A) tail of mRNA. Nucleic Acids Res. 25, 3564-3569.
61. Malek S.N., Katumuluwa A.I. and Pasternack G.R. (1990). Identification and preliminary characterization of two related proliferationassociated nuclear phosphoproteins. J. Biol. Chem. 265, 13400-13409.
62. Matsumoto K., Nagata K., Ui M. and Hanaoka F. (1993). Template activating factor I, a novel host factor required to stimulate the adenovirus core DNA replication. J. Biol. Chem. 268, 10582-10587.
63. Mazan-Mamczarz K., Galban S., Lopez de Silanes I., Martindale J.L., Atasoy U., Keene J.D. and Gorospe M. (2003). RNA-binding protein HuR enhances p53 translation in response to ultraviolet light irradiation. Proc. Natl. Acad. Sci. USA 100, 8354-8359.
64. Mazan-Mamczarz K., Hagner P.R., Corl S., Srikantan S., Wood W.H., Becker K.G., Gorospe M., Keene J.D., Levenson A.S. and Gartenhaus R.B. (2008). Post-transcriptional gene regulation by HuR promotes a more tumourigenic phenotype. Oncogene 27, 6151-6163.
65. Meng Z., Jackson N.L., Choi H., King P.H., Emanuel P.D. and Blume S.W. (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 tumour cells. J. Cell Physiol. 217, 172-183.
66. Miki Y., Swensen J., Shattuck-Eidens D., Futreal P.A., Harshman K., Tavtigian S., Liu Q., Cochran C., Bennett L.M., Ding W., Bell R., Rosenthal J., Hussey C., Tran T., McClure M., Frye C., Hattier T., Phelps R., Haugenstrano A., Katcher H., Yakumo K., Gholami Z., Shaffer D., Stone S., Bayer S., Wray C., Bogden R., Dayananth P., Ward J., Tonin P., Narod S., Bristow P.K., Norris F.H., Helvering L., Morrison P., Rosteck P., Lai M., Barret J.C., Lewis C., Neuhausen S., Cannonalbright L., Goldgar D., Wiseman R., Kamb A. and Skolnick M.H. (1994). A strong candidate for the breast and ovarian cancer susceptibility gene BRCA1. Science 266, 66-71.
67. Mili S. and Steitz J.A. (2004). Evidence for reassociation of RNA-binding proteins after cell lysis: implications for the interpretation of immunoprecipitation analyses. RNA 10, 1692-1694.
68. Ming X.F., Stoecklin G., Lu M., Looser R. and Moroni C. (2001). Parallel and independent regulation of interleukin-3 mRNA turnover by phosphatidylinositol 3-kinase and p38 mitogen-activated protein kinase. Mol. Cell. Biol. 21, 5778-5789.
69. Mrena J., Wiksten J.P., Thiel A., Kokkola A., Pohjola L., Lundin J., Nordling S., Ristimaki A. and Haglund C. (2005). Cyclooxygenase-2 is an independent prognostic factor in gastric cancer and its expression is regulated by the messenger RNA stability factor HuR. Clin. Cancer Res. 11, 7362-7368.
70. Myer V.E., Fan X.C. and Steitz J.A. (1997). Identification of HuR as a protein implicated in AUUUA-mediated mRNA decay. EMBO J. 16, 2130-2139.
71. Nabors L.B., Gillespie G.Y., Harkins L. and King P.H. (2001). HuR, a RNA stability factor, is expressed in malignant brain tumours and binds to adenine- and uridine-rich elements within the 3' untranslated regions of cytokine and angiogenic factor mRNAs. Cancer Res. 61, 2154-2161.
72. Okano H.J. and Darnell R.B. (1997). A hierarchy of Hu RNA binding proteins in developing and adult neurons. J. Neurosci. 17, 3024-3037.
73. Ortega A.D., Sala S., Espinosa E., Gonzalez-Baron M. and Cuezva J.M. (2008). HuR and the bioenergetic signature of breast cancer: a low tumour expression of the RNA-binding protein predicts a higher risk of disease recurrence. Carcinogenesis 29, 2053-2061.
74. Osborne C.K. (1998). Tamoxifen in the treatment of breast cancer. N. Engl. J. Med. 339, 1609-1618.
75. 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.
76. Pryzbylkowski P., Obajimi O. and Keen J.C. (2008). Trichostatin A and 5 Aza-2' deoxycytidine decrease estrogen receptor mRNA stability in ER positive MCF7 cells through modulation of HuR. Breast Cancer Res. Treat. 111, 15-25.
77. Rice J.C. and Futscher B.W. (2000). Transcriptional repression of BRCA1 by aberrant cytosine methylation, histone hypoacetylation and chromatin condensation of the BRCA1 promoter. Nucleic Acids Res. 28, 3233-3239.
78. Saito S., Miyaji-Yamaguchi M., Shimoyama T. and Nagata K. (1999). Functional domains of template-activating factor-I as a protein phosphatase 2A inhibitor. Biochem. Biophys. Res. Commun. 259, 471-475.
79. Sapi E., Flick M.B., Rodov S., Gilmore-Hebert M., Kelley M., Rockwell S. and Kacinski B.M. (1996). Independent regulation of invasion and anchorage-independent growth by different autophosphorylation sites of the macrophage colony-stimulating factor 1 receptor. Cancer Res. 56, 5704-5712.
80. Saunus J.M., French J.D., Edwards S.L., Beveridge D.J., Hatchell E.C., Wagner S.A., Stein S.R., Davidson A., Simpson K.J., Francis G.D., Leedman P.J. and Brown M.A. (2008). Posttranscriptional regulation of the breast cancer susceptibility gene BRCA1 by the RNA binding protein HuR. Cancer Res. 68, 9469-9478.
81. Shao W. and Brown M. (2004). Advances in estrogen receptor biology: prospects for improvements in targeted breast cancer therapy. Breast Cancer Res. 6, 39-52.
82. Sheflin L.G., Zou A.P. and Spaulding S.W. (2004). Androgens regulate the binding of endogenous HuR to the AU-rich 3'UTRs of HIF-1alpha and EGF mRNA. Biochem. Biophys. Res. Commun. 322, 644-651.
83. Standart N. and Jackson R.J. (1994). Regulation of translation by specific protein/mRNA interactions. Biochimie 76, 867-879.
84. Subbaramaiah K., Marmo T.P., Dixon D.A. and Dannenberg A.J. (2003). Regulation of cyclooxgenase-2 mRNA stability by taxanes: evidence for involvement of p38, MAPKAPK-2, and HuR. J. Biol. Chem. 278, 37637-37647.
85. Szabo A., Dalmau J., Manley G., Rosenfeld M., Wong E., Henson J., Posner J.B. and Furneaux H.M. (1991). HuD, a paraneoplastic encephalomyelitis antigen, contains RNA-binding domains and is homologous to Elav and Sex-lethal. Cell 67, 325-333.
86. Toy E.P., Bonafe N., Savlu A., Zeiss C., Zheng W., Flick M. and Chambers S.K. (2005). Correlation of tumour phenotype with c-fms proto-oncogene expression in an in vivo intraperitoneal model for experimental human breast cancer metastasis. Clin. Exp. Metastasis 22, 1-9.
87. Tran H., Maurer F. and Nagamine Y. (2003). Stabilization of urokinase and urokinase receptor mRNAs by HuR is linked to its cytoplasmic accumulation induced by activated mitogen-activated protein kinaseactivated protein kinase 2. Mol. Cell. Biol. 23, 7177-7188.
88. Vogelstein B. and Kinzler K.W. (2004). Cancer genes and the pathways they control. Nat. Med. 10, 789-799.
89. von Lindern M., van Baal S., Wiegant J., Raap A., Hagemeijer A. and Grosveld G. (1992). Can, a putative oncogene associated with myeloid leukemogenesis, may be activated by fusion of its 3' half to different genes: characterization of the set gene. Mol. Cell Biol. 12, 3346-3355.
90. Wang W., Caldwell M.C., Lin S., Furneaux H. and Gorospe M. (2000a). HuR regulates cyclin A and cyclin B1 mRNA stability during cell proliferation. EMBO J. 19, 2340-2350.
91. Wang W., Furneaux H., Cheng H., Caldwell M.C., Hutter D., Liu Y., Holbrook N. and Gorospe M. (2000b). HuR regulates p21 mRNA stabilization by UV light. Mol. Cell Biol. 20, 760-769.
92. Wang W., Yang X., Cristofalo V.J., Holbrook N.J. and Gorospe M. (2001). Loss of HuR is linked to reduced expression of proliferative genes during replicative senescence. Mol. Cell Biol. 21, 5889-5898.
93. Wang W., Fan J., Yang X., Furer-Galban S., Lopez de Silanes I., von Kobbe C., Guo J., Georas S.N., Foufelle F., Hardie D.G., Carling D. and Gorospe M. (2002). AMP-activated kinase regulates cytoplasmic HuR. Mol. Cell Biol. 22, 3425-3436.
94. Wang W., Yang X., Lopez de Silanes I., Carling D. and Gorospe M. (2003). Increased AMP:ATP ratio and AMP-activated protein kinase activity during cellular senescence linked to reduced HuR function. J. Biol. Chem. 278, 27016-27023.
95. Winzen R., Kracht M., Ritter B., Wilhelm A., Chen C.Y., Shyu A.B., Muller M., Gaestel M., Resch K. and Holtmann H. (1999). The p38 MAP kinase pathway signals for cytokine-induced mRNA stabilization via MAP kinase-activated protein kinase 2 and an AUrich region-targeted mechanism. EMBO J. 18, 4969-4980.
96. Winzen R., Gowrishankar G., Bollig F., Redich N., Resch K. and Holtmann H. (2004). Distinct domains of AU-rich elements exert different functions in mRNA destabilization and stabilization by p38 mitogen-activated protein kinase or HuR. Mol. Cell Biol. 24, 4835-4847.
97. Woo H.H., Zhou Y., Yi X., David C.L., Zheng W., Gilmore-Hebert M., Kluger H.M., Ulukus E.C., Baker T., Stoffer J.B. and Chambers S.K. (2009). Regulation of non-AU-rich element containing c-fms protooncogene expression by HuR in breast cancer. Oncogene 28, 1176-1186.
98. Wooster R., Bignell G., Lancaster J., Swift S., Seal S., Mangion J., Collins N., Gregory S., Gumbs C. and Micklem G. (1995). Identification of the breast cancer susceptibility gene BRCA2. Nature 378, 789-792.
99. Yao K.M., Samson M.L., Reeves R. and White K. (1993). Gene elav of Drosophila melanogaster: a prototype for neuronal-specific RNA binding protein gene family that is conserved in flies and humans. J. Neurobiol. 24, 723-739.
100. Zhang W., Wagner B.J., Ehrenman K., Schaefer A.W., DeMaria C.T., Crater D., DeHaven K., Long L. and Brewer G. (1993). Purification, characterization, and cDNA cloning of an AU-rich element RNAbinding protein, AUF1. Mol. Cell Biol. 13, 7652-7665.
101. Zheng D., MacLean P.S., Pohnert S.C., Knight J.B., Olson A.L., Winder W.W. and Dohm G.L. (2001). Regulation of muscle GLUT-4 transcription by AMP-activated protein kinase. J. Appl. Physiol. 91, 1073-1083.