Identification of Y-box binding protein 1 as a core regulator of MEK/ERK pathway-dependent gene signatures in colorectal cancer cells

PLoS Genetics

Volumn 6, Issue 12, 2010, Pages 1-19

  Jürchott, Karsten ^a   Kuban, Ralf Jürgen ^a   Krech, Till ^a   Blüthgen, Nils ^b   Stein, Ulrike ^c   Walther, Wolfgang ^c   Friese, Christian ^a   Kiełbasa, Szymon M ^b,d   Ungethüm, Ute ^a   Lund, Per ^a   Knösel, Thomas ^e   Kemmner, Wolfgang ^a,c   Morkel, Markus ^c,d   Fritzmann, Johannes ^a   Schlag, Peter M ^a   Birchmeier, Walter ^c   Krueger, Tammo ^d   Sperling, Silke ^d   Sers, Christine ^a   Royer, Hans Dieter ^f,g   Herzel, Hanspeter ^b   Schäfer, Reinhold ^a   more..

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b HUMBOLDT UNIVERSITY   (Germany)

^c MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^d MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^e FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^f CENTER OF ADVANCED EUROPEAN STUDIES AND RESEARCH CAESAR   (Germany)

^g HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; NUCLEAR FACTOR Y; PROTEIN TYROSINE KINASE; RAS PROTEIN; REGULATOR PROTEIN; TRANSCRIPTION FACTOR E2F; TRANSCRIPTOME; Y BOX BINDING PROTEIN 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE;

ARTICLE; BINDING SITE; CANCER CELL; CELL STRAIN HCT116; CELL STRAIN HT29; CHROMATIN IMMUNOPRECIPITATION; COLORECTAL CANCER; CONTROLLED STUDY; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENE TARGETING; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; NUCLEOTIDE SEQUENCE; PROGNOSIS; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN MOTIF; REGULATORY MECHANISM; REGULATORY SEQUENCE; REPORTER GENE; VALIDATION PROCESS; COLORECTAL TUMOR; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; REGULATOR GENE; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

CELL LINE, TUMOR; COLORECTAL NEOPLASMS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; GENES, REGULATOR; HUMANS; MAP KINASE SIGNALING SYSTEM; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; Y-BOX-BINDING PROTEIN 1;

EID: 78650697735     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1001231     Document Type: Article

References (81)

1. Weigelt B, Baehner FL, Reis-Filho JS (2010) The contribution of gene expression profiling to breast cancer classification, prognostication and prediction: a retrospective of the last decade. J Pathol 220: 263-280.
2. Walther A, Johnstone E, Swanton C, Midgley R, Tomlinson I, et al. (2009) Genetic prognostic and predictive markers in colorectal cancer. Nat Rev Cancer 9: 489-499.
3. Sotiriou C, Piccart MJ (2007) Taking gene-expression profiling to the clinic: when will molecular signatures become relevant to patient care? Nat Rev Cancer 7: 545-553.
4. Tullai JW, Schaffer ME, Mullenbrock S, Sholder G, Kasif S, et al. (2007) Immediate-early and delayed primary response genes are distinct in function and genomic architecture. J Biol Chem 282: 23981-23995.
5. Tullai JW, Schaffer ME, Mullenbrock S, Kasif S, Cooper GM (2004) Identification of transcription factor binding sites upstream of human genes regulated by the phosphatidylinositol 3-kinase and MEK/ERK signaling pathways. J Biol Chem 279: 20167-20177.
6. Adler AS, Lin M, Horlings H, Nuyten DSA, van de Vijver MJ, et al. (2006) Genetic regulators of large-scale transcriptional signatures in cancer. Nat Genet 38: 421-430.
7. Zuber J, Tchernitsa OI, Hinzmann B, Schmitz AC, Grips M, et al. (2000) A genome-wide survey of RAS transformation targets. Nat Genet 24: 144-152.
8. Tchernitsa OI, Sers C, Zuber J, Hinzmann B, Grips M, et al. (2004) Transcriptional basis of KRAS oncogene-mediated cellular transformation in ovarian epithelial cells. Oncogene 23: 4536-4555.
9. Chang JT, Carvalho C, Mori S, Bild AH, Gatza ML, Wang Q, et al. (2009) A genomic strategy to elucidate modules of oncogenic pathway signaling networks. Mol Cell 34: 104-114.
10. Bild AH, Yao G, Chang JT, Wang Q, Potti A, et al. (2006) Oncogenic pathway signatures in human cancers as a guide to targeted therapies. Nature 439: 353-357.
11. UlküAS, Der CJ (2003) Ras signaling, deregulation of gene expression and oncogenesis. Cancer Treat Res 115: 189-208.
12. Malumbres M, Barbacid M (2003) RAS oncogenes: the first 30 years. Nat Rev Cancer 3: 459-465.
13. Karnoub AE, Weinberg RA (2008) Ras oncogenes: split personalities. Nat Rev Mol Cell Biol 9: 517-531.
14. Mitin N, Rossman KL, Der CJ (2005) Signaling interplay in Ras superfamily function. Curr Biol 15: R563-74.
15. Hamad NM, Elconin JH, Karnoub AE, Bai W, Rich JN, et al. (2002) Distinct requirements for Ras oncogenesis in human versus mouse cells. Genes Dev 16: 2045-2057.
16. Downward J (1998) Ras signalling and apoptosis. Curr Opin Genet Dev 8: 49-54.
17. Brem R, Certa U, Neeb M, Nair AP, Moroni C (2001) Global analysis of differential gene expression after transformation with the v-H-ras oncogene in a murine tumor model. Oncogene 20: 2854-2858.
18. Linardou H, Dahabreh IJ, Kanaloupiti D, Siannis F, Bafaloukos D, et al. (2008) Assessment of somatic k-RAS mutations as a mechanism associated with resistance to EGFR-targeted agents: a systematic review and meta-analysis of studies in advanced non-small-cell lung cancer and metastatic colorectal cancer. Lancet Oncol 9: 962-972.
19. Fearon ER, Vogelstein B (1990) A genetic model for colorectal tumorigenesis. Cell 61: 759-767.
20. Kinzler KW, Vogelstein B (1996) Lessons from hereditary colorectal cancer. Cell 87: 159-170.
21. Gayet J, Zhou XP, Duval A, Rolland S, Hoang JM, et al. (2001) Extensive characterization of genetic alterations in a series of human colorectal cancer cell lines. Oncogene 20: 5025-5032.
22. Davies H, Bignell GR, Cox C, Stephens P, Edkins S, et al. (2002) Mutations of the BRAF gene in human cancer. Nature 417: 949-954.
23. Osherov N, Levitzki A (1994) Epidermal-growth-factor-dependent activation of the src-family kinases. Eur J Biochem 225: 1047-1053.
24. Rice PL, Goldberg RJ, Ray EC, Driggers LJ, Ahnen DJ (2001) Inhibition of extracellular signal-regulated kinase 1/2 phosphorylation and induction of apoptosis by sulindac metabolites. Cancer Res 61: 1541-1547.
25. Dudley DT, Pang L, Decker SJ, Bridges AJ, Saltiel AR (1995) A synthetic inhibitor of the mitogen-activated protein kinase cascade. Proc Natl Acad Sci U S A 92: 7686-7689.
26. Favata MF, Horiuchi KY, Manos EJ, Daulerio AJ, Stradley DA, et al. (1998) Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J Biol Chem 273: 18623-18632.
27. Shirasawa S, Furuse M, Yokoyama N, Sasazuki T (1993) Altered growth of human colon cancer cell lines disrupted at activated Ki-ras. Science 260: 85-88.
28. Pretlow TP, Pretlow TG (2005) Mutant KRAS in aberrant crypt foci (ACF): initiation of colorectal cancer? Biochim Biophys Acta 1756: 83-96.
29. Blüthgen N, Kiełbasa SM, Herzel H (2005) Inferring combinatorial regulation of transcription in silico. Nucleic Acids Res 33: 272-279.
30. Blum R, Nakdimon I, Goldberg L, Elkon R, Shamir R, et al. (2006) E2F1 identified by promoter and biochemical analysis as a central target of glioblastoma cell-cycle arrest in response to Ras inhibition. Int J Cancer 119: 527-538.
31. Katula KS, Wright KL, Paul H, Surman DR, Nuckolls FJ, et al. (1997) Cyclindependent kinase activation and S-phase induction of the cyclin B1 gene are linked through the CCAAT elements. Cell Growth Differ 8: 811-820.
32. Farina A, Manni I, Fontemaggi G, Tiainen M, Cenciarelli C, et al. (1999) Down-regulation of cyclin B1 gene transcription in terminally differentiated skeletal muscle cells is associated with loss of functional CCAAT-binding NF-Y complex. Oncogene 18: 2818-2827.
33. Manni I, Mazzaro G, Gurtner A, Mantovani R, Haugwitz U, et al. (2001) NF-Y mediates the transcriptional inhibition of the cyclin B1, cyclin B2, and cdc25C promoters upon induced G2 arrest. J Biol Chem 276: 5570-5576.
34. Jurchott K, Bergmann S, Stein U, Walther W, Janz M, et al. (2003) YB-1 as a cell cycle-regulated transcription factor facilitating cyclin A and cyclin B1 gene expression. J Biol Chem 278: 27988-27996.
35. Chatterjee M, Rancso C, Stühmer T, Eckstein N, Andrulis M, et al. (2008) The Y-box binding protein YB-1 is associated with progressive disease and mediates survival and drug resistance in multiple myeloma. Blood 111: 3714-3722.
36. Basaki Y, Taguchi K, Izumi H, Murakami Y, Kubo T, et al. (2010) Y-box binding protein-1 (YB-1) promotes cell cycle progression through CDC6- dependent pathway in human cancer cells. Eur J Cancer 46: 954-965.
37. Finkbeiner MR, Astanehe A, To K, Fotovati A, Davies AH, et al. (2009) Profiling YB-1 target genes uncovers a new mechanism for MET receptor regulation in normal and malignant human mammary cells. Oncogene 28: 1421-1431.
38. Fritzmann J, Morkel M, Besser D, Budczies J, Kosel F, et al. (2009) A colorectal cancer expression profile that includes transforming growth factor beta inhibitor BAMBI predicts metastatic potential. Gastroenterology 137: 165-175.
39. Shibahara K, Sugio K, Osaki T, Uchiumi T, Maehara Y, et al. (2001) Nuclear expression of the Y-box binding protein, YB-1, as a novel marker of disease progression in non-small cell lung cancer. Clin Cancer Res 7: 3151-3155.
40. Oda Y, Ohishi Y, Saito T, Hinoshita E, Uchiumi T, et al. (2003) Nuclear expression of Y-box-binding protein-1 correlates with P-glycoprotein and topoisomerase II alpha expression, and with poor prognosis in synovial sarcoma. J Pathol 199: 251-258.
41. Kamura T, Yahata H, Amada S, Ogawa S, Sonoda T, et al. (1999) Is nuclear expression of Y box-binding protein-1 a new prognostic factor in ovarian serous adenocarcinoma? Cancer 85: 2450-2454.
42. Janz M, Harbeck N, Dettmar P, Berger U, Schmidt A, et al. (2002) Y-box factor YB-1 predicts drug resistance and patient outcome in breast cancer independent of clinically relevant tumor biologic factors HER2, uPA and PAI-1. Int J Cancer 97: 278-282.
43. Huang X, Ushijima K, Komai K, Takemoto Y, Motoshima S, et al. (2004) Coexpression of Y box-binding protein-1 and P-glycoprotein as a prognostic marker for survival in epithelial ovarian cancer. Gynecol Oncol 93: 287-291.
44. Gessner C, Woischwill C, Schumacher A, Liebers U, Kuhn H, et al. (2004) Nuclear YB-1 expression as a negative prognostic marker in nonsmall cell lung cancer. Eur Respir J 23: 14-19.
45. Knösel T, Emde A, Schlüns K, Chen Y, Jürchott K, et al. (2005) Immunoprofiles of 11 biomarkers using tissue microarrays identify prognostic subgroups in colorectal cancer. Neoplasia 7: 741-747.
46. Evdokimova V, Tognon C, Ng T, Ruzanov P, Melnyk N, et al. (2009) Translational activation of snail1 and other developmentally regulated transcription factors by YB-1 promotes an epithelial-mesenchymal transition. Cancer Cell 15: 402-415.
47. Chen H, Tsai S, Leone G (2009) Emerging roles of E2Fs in cancer: an exit from cell cycle control. Nat Rev Cancer 9: 785-797.
48. Mantovani R (1998) A survey of 178 NF-Y binding CCAAT boxes. Nucleic Acids Res 26: 1135-1143.
49. Kohno K, Izumi H, Uchiumi T, Ashizuka M, Kuwano M (2003) The pleiotropic functions of the Y-box-binding protein, YB-1. Bioessays 25: 691-698.
50. Duh JL, Zhu H, Shertzer HG, Nebert DW, Puga A (1995) The Y-box motif mediates redox-dependent transcriptional activation in mouse cells. J Biol Chem 270: 30499-30507.
51. Evdokimova V, Ruzanov P, Anglesio MS, Sorokin AV, Ovchinnikov LP, et al. (2006) Akt-mediated YB-1 phosphorylation activates translation of silent mRNA species. Mol Cell Biol 26: 277-292.
52. Marenstein DR, Ocampo MT, Chan MK, Altamirano A, Basu AK, et al. (2001) Stimulation of human endonuclease III by Y box-binding protein 1 (DNAbinding protein B). Interaction between a base excision repair enzyme and a transcription factor. J Biol Chem 276: 21242-21249.
53. Bargou RC, Jürchott K, Wagener C, Bergmann S, Metzner S, et al. (1997) Nuclear localization and increased levels of transcription factor YB-1 in primary human breast cancers are associated with intrinsic MDR1 gene expression. Nat Med 3: 447-450.
54. Astanehe A, Finkbeiner MR, Hojabrpour P, To K, Fotovati A, et al. (2009) The transcriptional induction of PIK3CA in tumor cells is dependent on the oncoprotein Y-box binding protein-1. Oncogene 28: 2406-2418.
55. Stein U, Jürchott K, Walther W, Bergmann S, Schlag PM, et al. (2001) Hyperthermia-induced nuclear translocation of transcription factor YB-1 leads to enhanced expression of multidrug resistance-related ABC transporters. J Biol Chem 276: 28562-28569.
56. Berquin IM, Pang B, Dziubinski ML, Scott LM, Chen YQ, et al. (2005) Y-boxbinding protein 1 confers EGF independence to human mammary epithelial cells. Oncogene 24: 3177-3186.
57. Swamynathan SK, Varma BR, Weber KT, Guntaka RV (2002) Targeted disruption of one allele of the Y-box protein gene, Chk-YB-1b, in DT40 cells results in major defects in cell cycle. Biochem Biophys Res Commun 296: 451-457.
58. Lu ZH, Books JT, Ley TJ (2005) YB-1 is important for late-stage embryonic development, optimal cellular stress responses, and the prevention of premature senescence. Mol Cell Biol 25: 4625-4637.
59. Bergmann S, Royer-Pokora B, Fietze E, Jürchott K, Hildebrandt B, et al. (2005) YB-1 provokes breast cancer through the induction of chromosomal instability that emerges from mitotic failure and centrosome amplification. Cancer Res 65: 4078-4087.
60. Giménez-Bonafé P, Fedoruk MN, Whitmore TG, Akbari M, Ralph JL, et al. (2004) YB-1 is upregulated during prostate cancer tumor progression and increases P-glycoprotein activity. Prostate 59: 337-349.
61. Shibao K, Takano H, Nakayama Y, Okazaki K, Nagata N, et al. (1999) Enhanced coexpression of YB-1 and DNA topoisomerase II alpha genes in human colorectal carcinomas. Int J Cancer 83: 732-737.
62. Blüthgen N, Legewie S, Kielbasa SM, Schramme A, Tchernitsa O, et al. (2009) A systems biological approach suggests that transcriptional feedback regulation by dual-specificity phosphatase 6 shapes extracellular signal-related kinase activity in RAS-transformed fibroblasts. FEBS J 276: 1024-1035.
63. Sutherland BW, Kucab J, Wu J, Lee C, Cheang MCU, et al. (2005) Akt phosphorylates the Y-box binding protein 1 at Ser102 located in the cold shock domain and affects the anchorage-independent growth of breast cancer cells. Oncogene 24: 4281-4292.
64. Stratford AL, Fry CJ, Desilets C, Davies AH, Cho YY, et al. (2008) Y-box binding protein-1 serine 102 is a downstream target of p90 ribosomal S6 kinase in basal-like breast cancer cells. Breast Cancer Res 10: R99.
65. Coles LS, Lambrusco L, Burrows J, Hunter J, Diamond P, et al. (2005) Phosphorylation of cold shock domain/Y-box proteins by ERK2 and GSK3beta and repression of the human VEGF promoter. FEBS Lett 579: 5372-5378.
66. Lee C, Dhillon J, Wang MYC, Gao Y, Hu K, et al. (2008) Targeting YB-1 in HER- 2 overexpressing breast cancer cells induces apoptosis via the mTOR/STAT3 pathway and suppresses tumor growth in mice. Cancer Res 68: 8661-8666.
67. Blum R, Elkon R, Yaari S, Zundelevich A, Jacob-Hirsch J, et al. (2007) Gene expression signature of human cancer cell lines treated with the ras inhibitor salirasib (S-farnesylthiosalicylic acid). Cancer Res 67: 3320-3328.
68. Blüthgen N, Kiełbasa SM, Cajavec B, Herzel H (2004) HOMGL-comparing genelists across species and with different accession numbers. Bioinformatics 20: 125-126.
69. Blüthgen N, Brand K, Cajavec B, Swat M, Herzel H, et al. (2005) Biological profiling of gene groups utilizing Gene Ontology. Genome Inform 16: 106-115.
70. Hubbard TJP, Aken BL, Beal K, Ballester B, Caccamo M, et al. (2007) Ensembl 2007. Nucleic Acids Res 35: D610-7.
71. Matys V, Kel-Margoulis OV, Fricke E, Liebich I, Land S, Barre-Dirrie A, et al. (2006) TRANSFAC and its module TRANSCompel: transcriptional gene regulation in eukaryotes. Nucleic Acids Res 34: D108-10.
72. Rahmann S, Müller T, Vingron M (2003) On the power of profiles for transcription factor binding site detection. Stat Appl Genet Mol Biol 2: Article 7.
73. Wasner M, Haugwitz U, Reinhard W, Tschöp K, Spiesbach K, et al. (2003) Three CCAAT-boxes and a single cell cycle genes homology region (CHR) are the major regulating sites for transcription from the human cyclin B2 promoter. Gene 312: 225-237.
74. Ohga T, Koike K, Ono M, Makino Y, Itagaki Y, et al. (1996) Role of the human Y box-binding protein YB-1 in cellular sensitivity to the DNA-damaging agents cisplatin, mitomycin C, and ultraviolet light. Cancer Res 56: 4224-4228.
75. Iyer VR, Horak CE, Scafe CS, Botstein D, Snyder M, et al. (2001) Genomic binding sites of the yeast cell-cycle transcription factors SBF and MBF. Nature 409: 533-538.
76. Huber W, Boer JM, von Heydebreck A, Gunawan B, Vingron M, et al. (2002) Transcription profiling of renal cell carcinoma. Verh Dtsch Ges Pathol 86: 153-164.
77. Tusher VG, Tibshirani R, Chu G (2001) Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 98: 5116-5121.
78. Tibshirani R, Chu G, Hastie T, Narasimhan B Samr: SAM: Significance Analysis of Microarrays. http://www.bioconductor.org.
79. R Development Core Team (2009) R: A Language and Environment for Statistical Computing. http://www.r-project.org.
80. Therneau T LT survival: Survival analysis, including penalised likelihood. http://www.r-project.org.
81. Testa A, Donati G, Yan P, Romani F, Huang TH, et al. (2005) Chromatin immunoprecipitation (ChIP) on chip experiments uncover a widespread distribution of NF-Y binding CCAAT sites outside of core promoters. J Biol Chem 280: 13606-13615.