Nucleolin enhances internal ribosomal entry site (IRES)-mediated translation of Sp1 in tumorigenesis

Biochimica et Biophysica Acta - Molecular Cell Research

Volumn 1843, Issue 12, 2014, Pages 2843-2854

  Hung, Chia Yang ^a   Yang, Wen Bin ^b   Wang, Shao An ^b   Hsu, Tsung I ^a,b   Chang, Wen Chang ^c   Hung, Jan Jong ^a,b,c  

^a NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^b NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^c TAIPEI MEDICAL UNIVERSITY   (Taiwan)

Author keywords

EGFR; IRES; Nucleolin; Phosphorylation; Sp1

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; 8 [4 (1 AMINOCYCLOBUTYL)PHENYL] 9 PHENYL 1,2,4 TRIAZOLO[3,4 F][1,6]NAPHTHYRIDIN 3(2H) ONE; EPITHELIAL GROWTH FACTOR RECEPTOR; GEFITINIB; GROWTH FACTOR RECEPTOR; MESSENGER RNA; NUCLEOLIN; TRANSCRIPTION FACTOR SP1; UNCLASSIFIED DRUG;

5' UNTRANSLATED REGION; ARTICLE; CONTROLLED STUDY; DRUG INHIBITION; FEMALE; GENE SILENCING; HELA CELL LINE; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; INTERNAL RIBOSOME ENTRY SITE; LUNG CANCER CELL LINE; LUNG CARCINOGENESIS; MOUSE; NONHUMAN; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; RNA TRANSLATION; SIGNAL TRANSDUCTION;

EID: 84907462374     PISSN: 01674889     EISSN: 18792596     Source Type: Journal    
DOI: 10.1016/j.bbamcr.2014.08.009     Document Type: Article

References (63)

1. Li L., Davie J.R. The role of Sp1 and Sp3 in normal and cancer cell biology. Ann. Anat. 2010, 192:275-283.
2. Suske G., Bruford E., Philipsen S. Mammalian SP/KLF transcription factors: bring in the family. Genomics 2005, 85:551-556.
3. Lagger G., Doetzlhofer A., Schuettengruber B., Haidweger E., Simboeck E., Tischler J., Chiocca S., Suske G., Rotheneder H., Wintersberger E., Seiser C. The tumor suppressor p53 and histone deacetylase 1 are antagonistic regulators of the cyclin-dependent kinase inhibitor p21/WAF1/CIP1 gene. Mol. Cell. Biol. 2003, 23:2669-2679.
4. Wang S.A., Chuang J.Y., Yeh S.H., Wang Y.T., Liu Y.W., Chang W.C., Hung J.J. Heat shock protein 90 is important for Sp1 stability during mitosis. J. Mol. Biol. 2009, 387:1106-1119.
5. Opitz O.G., Rustgi A.K. Interaction between Sp1 and cell cycle regulatory proteins is important in transactivation of a differentiation-related gene. Cancer Res. 2000, 60:2825-2830.
6. Kong L.M., Liao C.G., Fei F., Guo X., Xing J.L., Chen Z.N. Transcription factor Sp1 regulates expression of cancer-associated molecule CD147 in human lung cancer. Cancer Sci. 2010, 101:1463-1470.
7. Chuang C.W., Pan M.R., Hou M.F., Hung W.C. Cyclooxygenase-2 up-regulates CCR7 expression via AKT-mediated phosphorylation and activation of Sp1 in breast cancer cells. J. Cell. Physiol. 2013, 228:341-348.
8. Yue L., Li L., Liu F., Hu N., Zhang W., Bai X., Li Y., Zhang Y., Fu L., Zhang X., Ye L. The oncoprotein HBXIP activates transcriptional coregulatory protein LMO4 via Sp1 to promote proliferation of breast cancer cells. Carcinogenesis 2013, 34:927-935.
9. Bonofiglio D., Qi H., Gabriele S., Catalano S., Aquila S., Belmonte M., Ando S. Peroxisome proliferator-activated receptor gamma inhibits follicular and anaplastic thyroid carcinoma cells growth by upregulating p21Cip1/WAF1 gene in a Sp1-dependent manner. Endocr. Relat. Cancer 2008, 15:545-557.
10. Yuan J.H., Yang F., Chen B.F., Lu Z., Huo X.S., Zhou W.P., Wang F., Sun S.H. The histone deacetylase 4/SP1/microrna-200a regulatory network contributes to aberrant histone acetylation in hepatocellular carcinoma. Hepatology 2011, 54:2025-2035.
11. Yin P., Zhao C., Li Z., Mei C., Yao W., Liu Y., Li N., Qi J., Wang L., Shi Y., Qiu S., Fan J., Zha X. Sp1 is involved in regulation of cystathionine gamma-lyase gene expression and biological function by PI3K/Akt pathway in human hepatocellular carcinoma cell lines. Cell. Signal. 2012, 24:1229-1240.
12. Huang C., Xie K. Crosstalk of Sp1 and Stat3 signaling in pancreatic cancer pathogenesis. Cytokine Growth Factor Rev. 2012, 23:25-35.
13. Pathi S., Jutooru I., Chadalapaka G., Nair V., Lee S.O., Safe S. Aspirin inhibits colon cancer cell and tumor growth and downregulates specificity protein (Sp) transcription factors. PLoS ONE 2012, 7:e48208.
14. Xu Y., Zhao F., Wang Z., Song Y., Luo Y., Zhang X., Jiang L., Sun Z., Miao Z., Xu H. MicroRNA-335 acts as a metastasis suppressor in gastric cancer by targeting Bcl-w and specificity protein 1. Oncogene 2012, 31:1398-1407.
15. Wang L., Guan X., Zhang J., Jia Z., Wei D., Li Q., Yao J., Xie K. Targeted inhibition of Sp1-mediated transcription for antiangiogenic therapy of metastatic human gastric cancer in orthotopic nude mouse models. Int. J. Oncol. 2008, 33:161-167.
16. Wang Y.T., Chuang J.Y., Shen M.R., Yang W.B., Chang W.C., Hung J.J. Sumoylation of specificity protein 1 augments its degradation by changing the localization and increasing the specificity protein 1 proteolytic process. J. Mol. Biol. 2008, 380:869-885.
17. Hsu T.I., Wang M.C., Chen S.Y., Yeh Y.M., Su W.C., Chang W.C., Hung J.J. Sp1 expression regulates lung tumor progression. Oncogene 2012, 31:3973-3988.
18. Trisciuoglio D., Iervolino A., Candiloro A., Fibbi G., Fanciulli M., Zangemeister-Wittke U., Zupi G., Del Bufalo D. bcl-2 induction of urokinase plasminogen activator receptor expression in human cancer cells through Sp1 activation: involvement of ERK1/ERK2 activity. J. Biol. Chem. 2004, 279:6737-6745.
19. De Siervi A., Marinissen M., Diggs J., Wang X.F., Pages G., Senderowicz A. Transcriptional activation of p21(waf1/cip1) by alkylphospholipids: role of the mitogen-activated protein kinase pathway in the transactivation of the human p21(waf1/cip1) promoter by Sp1. Cancer Res. 2004, 64:743-750.
20. Chuang J.Y., Wang Y.T., Yeh S.H., Liu Y.W., Chang W.C., Hung J.J. Phosphorylation by c-Jun NH2-terminal kinase 1 regulates the stability of transcription factor Sp1 during mitosis. Mol. Biol. Cell 2008, 19:1139-1151.
21. Wang Y.T., Yang W.B., Chang W.C., Hung J.J. Interplay of posttranslational modifications in Sp1 mediates Sp1 stability during cell cycle progression. J. Mol. Biol. 2011, 414:1-14.
22. Yeh S.H., Yang W.B., Gean P.W., Hsu C.Y., Tseng J.T., Su T.P., Chang W.C., Hung J.J. Translational and transcriptional control of Sp1 against ischaemia through a hydrogen peroxide-activated internal ribosomal entry site pathway. Nucleic Acids Res. 2011, 39:5412-5423.
23. Gonzalez-Herrera I.G., Prado-Lourenco L., Pileur F., Conte C., Morin A., Cabon F., Prats H., Vagner S., Bayard F., Audigier S., Prats A.C. Testosterone regulates FGF-2 expression during testis maturation by an IRES-dependent translational mechanism. FASEB J. 2006, 20:476-478.
24. Fox J.T., Shin W.K., Caudill M.A., Stover P.J. A UV-responsive internal ribosome entry site enhances serine hydroxymethyltransferase 1 expression for DNA damage repair. J. Biol. Chem. 2009, 284:31097-31108.
25. Jang S.K., Krausslich H.G., Nicklin M.J., Duke G.M., Palmenberg A.C., Wimmer E. A segment of the 5' nontranslated region of encephalomyocarditis virus RNA directs internal entry of ribosomes during in vitro translation. J. Virol. 1988, 62:2636-2643.
26. Chen L.L., Kung Y.A., Weng K.F., Lin J.Y., Horng J.T., Shih S.R. Enterovirus 71 infection cleaves a negative regulator for viral internal ribosomal entry site-driven translation. J. Virol. 2013, 87:3828-3838.
27. Redondo N., Sanz M.A., Steinberger J., Skern T., Kusov Y., Carrasco L. Translation directed by hepatitis A virus IRES in the absence of active eIF4F complex and eIF2. PLoS ONE 2012, 7:e52065.
28. Shi Y., Sharma A., Wu H., Lichtenstein A., Gera J. Cyclin D1 and c-myc internal ribosome entry site (IRES)-dependent translation is regulated by AKT activity and enhanced by rapamycin through a p38 MAPK- and ERK-dependent pathway. J. Biol. Chem. 2005, 280:10964-10973.
29. Graber T.E., Baird S.D., Kao P.N., Mathews M.B., Holcik M. NF45 functions as an IRES trans-acting factor that is required for translation of cIAP1 during the unfolded protein response. Cell Death Differ. 2010, 17:719-729.
30. Parsyan A., Shahbazian D., Martineau Y., Petroulakis E., Alain T., Larsson O., Mathonnet G., Tettweiler G., Hellen C.U., Pestova T.V., Svitkin Y.V., Sonenberg N. The helicase protein DHX29 promotes translation initiation, cell proliferation, and tumorigenesis. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:22217-22222.
31. Shatsky I.N., Dmitriev S.E., Terenin I.M., Andreev D.E. Cap- and IRES-independent scanning mechanism of translation initiation as an alternative to the concept of cellular IRESs. Mol. Cells 2010, 30:285-293.
32. Pestova T.V., de Breyne S., Pisarev A.V., Abaeva I.S., Hellen C.U. eIF2-dependent and eIF2-independent modes of initiation on the CSFV IRES: a common role of domain II. EMBO J. 2008, 27:1060-1072.
33. Dmitriev S.E., Terenin I.M., Andreev D.E., Ivanov P.A., Dunaevsky J.E., Merrick W.C., Shatsky I.N. GTP-independent tRNA delivery to the ribosomal P-site by a novel eukaryotic translation factor. J. Biol. Chem. 2010, 285:26779-26787.
34. Thakor N., Holcik M. IRES-mediated translation of cellular messenger RNA operates in eIF2alpha-independent manner during stress. Nucleic Acids Res. 2012, 40:541-552.
35. Robert F., Kapp L.D., Khan S.N., Acker M.G., Kolitz S., Kazemi S., Kaufman R.J., Merrick W.C., Koromilas A.E., Lorsch J.R., Pelletier J. Initiation of protein synthesis by hepatitis C virus is refractory to reduced eIF2.GTP.Met-tRNA(i)(Met) ternary complex availability. Mol. Biol. Cell 2006, 17:4632-4644.
36. Ventoso I., Sanz M.A., Molina S., Berlanga J.J., Carrasco L., Esteban M. Translational resistance of late alphavirus mRNA to eIF2alpha phosphorylation: a strategy to overcome the antiviral effect of protein kinase PKR. Genes Dev. 2006, 20:87-100.
37. Kim J.H., Park S.M., Park J.H., Keum S.J., Jang S.K. eIF2A mediates translation of hepatitis C viral mRNA under stress conditions. EMBO J. 2011, 30:2454-2464.
38. Komar A.A., Hatzoglou M. Cellular IRES-mediated translation: the war of ITAFs in pathophysiological states. Cell Cycle 2011, 10:229-240.
39. Semler B.L., Waterman M.L. IRES-mediated pathways to polysomes: nuclear versus cytoplasmic routes. Trends Microbiol. 2008, 16:1-5.
40. Gerbasi V.R., Link A.J. The myotonic dystrophy type 2 protein ZNF9 is part of an ITAF complex that promotes cap-independent translation. Mol. Cell. Proteomics 2007, 6:1049-1058.
41. Lewis S.M., Holcik M. For IRES trans-acting factors, it is all about location. Oncogene 2008, 27:1033-1035.
42. Arguelles S., Camandola S., Cutler R.G., Ayala A., Mattson M.P. Elongation factor 2 diphthamide is critical for translation of two IRES-dependent protein targets, XIAP and FGF2, under oxidative stress conditions. Free Radic. Biol. Med. 2014, 67:131-138.
43. Dobson T., Chen J., Krushel L.A. Dysregulating IRES-dependent translation contributes to overexpression of oncogenic Aurora A Kinase. Mol. Cancer Res. 2013, 11:887-900.
44. Antonucci L., D'Amico D., Di Magno L., Coni S., Di Marcotullio L., Cardinali B., Gulino A., Ciapponi L., Canettieri G. CNBP regulates wing development in Drosophila melanogaster by promoting IRES-dependent translation of dMyc. Cell Cycle 2014, 13:434-439.
45. Damiano F., Rochira A., Tocci R., Alemanno S., Gnoni A., Siculella L. hnRNP A1 mediates the activation of the IRES-dependent SREBP-1a mRNA translation in response to endoplasmic reticulum stress. Biochem. J. 2013, 449:543-553.
46. Leon K., Boulo T., Musnier A., Morales J., Gauthier C., Dupuy L., Heyne S., Backofen R., Poupon A., Cormier P., Reiter E., Crepieux P. Activation of a GPCR leads to eIF4G phosphorylation at the 5' cap and to IRES-dependent translation. J. Mol. Endocrinol. 2014, 52:373-382.
47. Sharathchandra A., Lal R., Khan D., Das S. Annexin A2 and PSF proteins interact with p53 IRES and regulate translation of p53 mRNA. RNA Biol. 2012, 9:1429-1439.
48. Abdelmohsen K., Gorospe M. RNA-binding protein nucleolin in disease. RNA Biol. 2012, 9:799-808.
49. Abdelmohsen K., Tominaga K., Lee E.K., Srikantan S., Kang M.J., Kim M.M., Selimyan R., Martindale J.L., Yang X., Carrier F., Zhan M., Becker K.G., Gorospe M. Enhanced translation by Nucleolin via G-rich elements in coding and non-coding regions of target mRNAs. Nucleic Acids Res. 2011, 39:8513-8530.
50. Tajrishi M.M., Tuteja R., Tuteja N. Nucleolin: the most abundant multifunctional phosphoprotein of nucleolus. Commun. Integr. Biol. 2011, 4:267-275.
51. Bouvet P., Diaz J.J., Kindbeiter K., Madjar J.J., Amalric F. Nucleolin interacts with several ribosomal proteins through its RGG domain. J. Biol. Chem. 1998, 273:19025-19029.
52. Stoneley M., Willis A.E. Cellular internal ribosome entry segments: structures, trans-acting factors and regulation of gene expression. Oncogene 2004, 23:3200-3207.
53. Komar A.A., Hatzoglou M. Internal ribosome entry sites in cellular mRNAs: mystery of their existence. J. Biol. Chem. 2005, 280:23425-23428.
54. Chang W.C., Hung J.J. Functional role of post-translational modifications of Sp1 in tumorigenesis. J. Biomed. Sci. 2012, 19:94.
55. Ishikawa F., Matunis M.J., Dreyfuss G., Cech T.R. Nuclear proteins that bind the pre-mRNA 3' splice site sequence r(UUAG/G) and the human telomeric DNA sequence d(TTAGGG)n. Mol. Cell. Biol. 1993, 13:4301-4310.
56. Dickinson L.A., Kohwi-Shigematsu T. Nucleolin is a matrix attachment region DNA-binding protein that specifically recognizes a region with high base-unpairing potential. Mol. Cell. Biol. 1995, 15:456-465.
57. Wang S.A., Li H.Y., Hsu T.I., Chen S.H., Wu C.J., Chang W.C., Hung J.J. Heat shock protein 90 stabilizes nucleolin to increase mRNA stability in mitosis. J. Biol. Chem. 2011, 286:43816-43829.
58. Bonello M.R., Khachigian L.M. Fibroblast growth factor-2 represses platelet-derived growth factor receptor-alpha (PDGFR-alpha) transcription via ERK1/2-dependent Sp1 phosphorylation and an atypical cis-acting element in the proximal PDGFR-alpha promoter. J. Biol. Chem. 2004, 279:2377-2382.
59. Milanini-Mongiat J., Pouyssegur J., Pages G. Identification of two Sp1 phosphorylation sites for p42/p44 mitogen-activated protein kinases: their implication in vascular endothelial growth factor gene transcription. J. Biol. Chem. 2002, 277:20631-20639.
60. Cobbold L.C., Wilson L.A., Sawicka K., King H.A., Kondrashov A.V., Spriggs K.A., Bushell M., Willis A.E. Upregulated c-myc expression in multiple myeloma by internal ribosome entry results from increased interactions with and expression of PTB-1 and YB-1. Oncogene 2010, 29:2884-2891.
61. Shi Y., Frost P.J., Hoang B.Q., Benavides A., Sharma S., Gera J.F., Lichtenstein A.K. IL-6-induced stimulation of c-myc translation in multiple myeloma cells is mediated by myc internal ribosome entry site function and the RNA-binding protein, hnRNP A1. Cancer Res. 2008, 68:10215-10222.
62. Grover R., Candeias M.M., Fahraeus R., Das S. p53 and little brother p53/47: linking IRES activities with protein functions. Oncogene 2009, 28:2766-2772.
63. Ghisolfi L., Kharrat A., Joseph G., Amalric F., Erard M. Concerted activities of the RNA recognition and the glycine-rich C-terminal domains of nucleolin are required for efficient complex formation with pre-ribosomal RNA. Eur. J. Biochem. 1992, 209:541-548.