Nucleolin stabilizes Bcl-XL messenger RNA in response to UVA irradiation

Cancer Research

Volumn 68, Issue 4, 2008, Pages 1046-1054

  Zhang, Jack ^a   Tsaprailis, George ^b   Bowden, G Tim ^a  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; NUCLEOLIN; POLYADENYLIC ACID BINDING PROTEIN; PROTEIN BCL XL; RIBONUCLEOPROTEIN; RNA BINDING PROTEIN; SMALL INTERFERING RNA;

3' UNTRANSLATED REGION; ARTICLE; CONTROLLED STUDY; ENZYME DEGRADATION; HELA CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; LIQUID CHROMATOGRAPHY; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; TANDEM MASS SPECTROMETRY; ULTRAVIOLET A RADIATION;

3' UNTRANSLATED REGIONS; BCL-X PROTEIN; HELA CELLS; HUMANS; KERATINOCYTES; PHOSPHOPROTEINS; POLY(A)-BINDING PROTEINS; PROTEIN BINDING; RNA, MESSENGER; RNA-BINDING PROTEINS; TRANSFECTION; ULTRAVIOLET RAYS;

EID: 39449125605     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-07-1927     Document Type: Article

References (59)

1. Bode AM, Dong Z. Mitogen-activated protein kinase activation in UV-induced signal transduction. Sci STKE 2003;2003:RE2.
2. Bowden GT. Prevention of non-melanoma skin cancer by targeting ultraviolet-B-light signalling. Nat Rev Cancer 2004;4:23-35.
3. Mitchell D. Revisiting the photochemistry of solar UVA in human skin. Proc Natl Acad Sci U S A 2006;103:13567-8.
4. de Gruijl FR. Photocarcinogenesis: UVA vs UVB. Methods Enzymol 2000;319:359-66.
5. de Laat JM, de Gruijl FR. The role of UVA in the aetiology of non-melanoma skin cancer. Cancer Surv 1996;26:173-91.
6. He YY, Pi J, Huang JL, Diwan BA, Waalkes MP, Chignell CF. Chronic UVA irradiation of human HaCaT keratinocytes induces malignant transformation associated with acquired apoptotic resistance. Oncogene 2006;25:3680-8.
7. Moan J, Dahlback A, Setlow RB. Epidemiological support for an hypothesis for melanoma induction indicating a role for UVA radiation. Photochem Photobiol 1999;70:243-7.
8. van Kranen HJ, de Laat A, van de Ven J, et al. Low incidence of p53 mutations in UVA (365-nm)-induced skin tumors in hairless mice. Cancer Res 1997;57:1238-40.
9. de Laat A, van der Leun JC, de Gruijl FR. Carcinogenesis induced by UVA (365-nm) radiation: the dose-time dependence of tumor formation in hairless mice. Carcinogenesis 1997;18:1013-20.
10. Mouret S, Baudouin C, Charveron M, Favier A, Cadet J, Douki T. Cyclobutane pyrimidine dimers are predominant DNA lesions in whole human skin exposed to UVA radiation. Proc Natl Acad Sci U S A 2006;103:13765-70.
11. Bachelor MA, Bowden GT. UVA-mediated activation of signaling pathways involved in skin tumor promotion and progression. Semin Cancer Biol 2004;14:131-8.
12. Zhang Y, Ma WY, Kaji A, Bode AM, Dong Z. Requirement of ATM in UVA-induced signaling and apoptosis. J Biol Chem 2002;277:3124-31.
13. Grad JM, Zeng XR, Boise LH. Regulation of Bcl-xL: a little bit of this and a little bit of STAT. Curr Opin Oncol 2000;12:543-9.
14. Kim R. Unknotting the roles of Bcl-2 and Bcl-xL in cell death. Biochem Biophys Res Commun 2005;333:336-43.
15. Motoyama N, Wang F, Roth KA, et al. Massive cell death of immature hematopoietic cells and neurons in Bcl-x-deficient mice. Science 1995;267:1506-10.
16. Wu LX, La Rose J, Chen L, et al. CD28 regulates the translation of Bcl-xL via the phosphatidylinositol 3-kinase/mammalian target of rapamycin pathway. J Immunol 2005;174:180-94.
17. Kirkin V, Joos S, Zornig M. The role of Bcl-2 family members in tumorigenesis. Biochim Biophys Acta 2004;1644:229-49.
18. Jost M, Class R, Kari C, Jensen PJ, Rodeck U. A central role of Bcl-X(L) in the regulation of keratinocyte survival by autocrine EGFR ligands. J Invest Dermatol 1999;112:443-9.
19. Pena JC, Rudin CM, Thompson CB. A Bcl-xL transgene promotes malignant conversion of chemically initiated skin papillomas. Cancer Res 1998;58:2111-6.
20. Chun E, Lee KY. Bcl-2 and Bcl-xL are important for the induction of paclitaxel resistance in human hepatocellular carcinoma cells. Biochem Biophys Res Commun 2004;315:771-9.
21. Minn AJ, Rudin CM, Boise LH, Thompson CB. Expression of bcl-xL can confer a multidrug resistance phenotype. Blood 1995;86:1903-10.
22. Schoop RA, Kooistra K, Baatenburg De Jong RJ, Noteborn MH. Bcl-xL inhibits p53- but not apoptin-induced apoptosis in head and neck squamous cell carcinoma cell line. Int J Cancer 2004;109:38-42.
23. Reed JC. Proapoptotic multidomain Bcl-2/Bax-family proteins: mechanisms, physiological roles, and therapeutic opportunities. Cell Death Differ 2006;13:1378-86.
24. Pecci A, Viegas LR, Baranao JL, Beato M. Promoter choice influences alternative splicing and determines the balance of isoforms expressed from the mouse bcl-X gene. J Biol Chem 2001;276:21062-9.
25. Viegas LR, Vicent GP, Baranao JL, Beato M, Pecci A. Steroid hormones induce bcl-X gene expression through direct activation of distal promoter P4. J Biol Chem 2004;279:9831-9.
26. Bachelor MA, Bowden GT. Ultraviolet A-induced modulation of Bcl-XL by p38 MAPK in human keratinocytes: posttranscriptional regulation through the 3′-untranslated region. J Biol Chem 2004;279:42658-68.
27. Grzybowska EA, Wilczynska A, Siedlecki JA. Regulatory functions of 3′UTRs. Biochem Biophys Res Commun 2001;288:291-5.
28. Shim J, Karin M. The control of mRNA stability in response to extracellular stimuli. Mol Cells 2002;14:323-31.
29. Audic Y, Hartley RS. Post-transcriptional regulation in cancer. Biol Cell 2004;96:479-98.
30. Chen CY, Chen TM, Shyu AB. Interplay of two functionally and structurally distinct domains of the c-fos AU-rich element specifies its mRNA-destabilizing function. Mol Cell Biol 1994;14:416-26.
31. Meyer S, Temme C, Wahle E. Messenger RNA turnover in eukaryotes: pathways and enzymes. Crit Rev Biochem Mol Biol 2004;39:197-216.
32. Mukherjee D, Gao M, O'Connor JP, et al. The mammalian exosome mediates the efficient degradation of mRNAs that contain AU-rich elements. EMBO J 2002;21:165-74.
33. Stoecklin G, Mayo T, Anderson P. ARE-mRNA degradation requires the 5′-3′ decay pathway. EMBO Rep 2006;7:72-7.
34. Barreau C, Paillard L, Osborne HB. AU-rich elements and associated factors: are there unifying principles? Nucleic Acids Res 2005;33:7138-50.
35. Chou CF, Mulky A, Maitra S, et al. Tethering KSRP, a decay-promoting AU-rich element-binding protein, to mRNAs elicits mRNA decay. Mol Cell Biol 2006;26:3695-706.
36. Pan YX, Chen H, Kilberg MS. Interaction of RNA-binding proteins HuR and AUF1 with the human ATF3 mRNA 3′-untranslated region regulates its amino acid limitation-induced stabilization. J Biol Chem 2005;280:34609-16.
37. Sengupta TK, Bandyopadhyay S, Fernandes DJ, Spicer EK. Identification of nucleolin as an AU-rich element binding protein involved in bcl-2 mRNA stabilization. J Biol Chem 2004;279:10855-63.
38. Zhang Y, Bhatia D, Xia H, Castranova V, Shi X, Chen F. Nucleolin links to arsenic-induced stabilization of GADD45α mRNA. Nucleic Acids Res 2006;34:485-95.
39. Rajagopalan LE, Westmark CJ, Jarzembowski JA, Malter JS. hnRNP C increases amyloid precursor protein (APP) production by stabilizing APP mRNA. Nucleic Acids Res 1998;26:3418-23.
40. Nagaoka K, Suzuki T, Kawano T, Imakawa K, Sakai S. Stability of casein mRNA is ensured by structural interactions between the 3′-untranslated region and poly(A) tail via the HuR and poly(A)-binding protein complex. Biochim Biophys Acta 2006;1759:132-40.
41. Chen CY, Gherzi R, Andersen JS, et al. Nucleolin and YB-1 are required for JNK-mediated interleukin-2 mRNA stabilization during T-cell activation. Genes Dev 2000;14:1236-48.
42. Hanakahi LA, Dempsey LA, Li MJ, Maizels N. Nucleolin is one component of the B cell-specific transcription factor and switch region binding protein, LR1. Proc Natl Acad Sci U S A 1997;94:3605-10.
43. Hanakahi LA, Sun H, Maizels N. High affinity interactions of nucleolin with G-G-paired rDNA. J Biol Chem 1999;274:15908-12.
44. Wang Z, Day N, Trifillis P, Kiledjian M. An mRNA stability complex functions with poly(A)-binding protein to stabilize mRNA in vitro. Mol Cell Biol 1999;19:4552-60.
45. Cok SJ, Acton SJ, Sexton AE, Morrison AR. Identification of RNA-binding proteins in RAW 264.7 cells that recognize a lipopolysaccharide-responsive element in the 3-untranslated region of the murine cyclooxygenase-2 mRNA. J Biol Chem 2004;279:8196-205.
46. Shevchenko A, Wilm M, Vorm O, Mann M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 1996;68:850-8.
47. Andon NL, Hollingworth S, Koller A, Greenland AJ, Yates JR III, Haynes PA. Proteomic characterization of wheat amyloplasts using identification of proteins by tandem mass spectrometry. Proteomics 2002;2:1156-68.
48. Yates JR III, Eng JK, McCormack AL, Schieltz D. Method to correlate tandem mass spectra of modified peptides to amino acid sequences in the protein database. Anal Chem 1995;67:1426-36.
49. Cooper B, Eckert D, Andon NL, Yates JR, Haynes PA. Investigative proteomics: identification of an unknown plant virus from infected plants using mass spectrometry. J Am Soc Mass Spectrom 2003;14:736-41.
50. Conne B, Stutz A, Vassalli JD. The 3′ untranslated region of messenger RNA: a molecular 'hotspot' for pathology? Nat Med 2000;6:637-41.
51. Yang C, Maiguel DA, Carrier F. Identification of nucleolin and nucleophosmin as genotoxic stress-responsive RNA-binding proteins. Nucleic Acids Res 2002;30:2251-60.
52. Navaratnam N, Shah R, Patel D, Fay V, Scott J. Apolipoprotein B mRNA editing is associated with UV crosslinking of proteins to the editing site. Proc Natl Acad Sci U S A 1993;90:222-6.
53. Hieronymus H, Silver PA. Genome-wide analysis of RNA-protein interactions illustrates specificity of the mRNA export machinery. Nat Genet 2003;33:155-61.
54. Hurt E, Luo MJ, Rother S, Reed R, Strasser K. Cotranscriptional recruitment of the serine-arginine-rich (SR)-like proteins Gbp2 and Hrb1 to nascent mRNA via the TREX complex. Proc Natl Acad Sci U S A 2004;101:1858-62.
55. Bouvet P, Diaz JJ, Kindbeiter K, Madjar JJ, Amalric F. Nucleolin interacts with several ribosomal proteins through its RGG domain. J Biol Chem 1998;273:19025-9.
56. Krajewska M, Moss SF, Krajewski S, Song K, Holt PR, Reed JC. Elevated expression of Bcl-X and reduced Bak in primary colorectal adenocarcinomas. Cancer Res 1996;56:2422-7.
57. Skalweit A, Doller A, Huth A, Kahne T, Persson PB, Thiele BJ. Posttranscriptional control of renin synthesis: identification of proteins interacting with renin mRNA 3′-untranslated region. Circ Res 2003;92:419-27.
58. Srivastava M, Pollard HB. Molecular dissection of nucleolin's role in growth and cell proliferation: new insights. FASEB J 1999;13:1911-22.
59. Saxena A, Rorie CJ, Dimitrova D, Daniely Y, Borowiec JA. Nucleolin inhibits Hdm2 by multiple pathways leading to p53 stabilization. Oncogene 2006;25:7274-88.