ARF and p53 Coordinate Tumor Suppression of an Oncogenic IFN-β-STAT1-ISG15 Signaling Axis

Cell Reports

Volumn 7, Issue 2, 2014, Pages 514-526

  Forys, Jason T ^a   Kuzmicki, Catherine E ^a   Saporita, Anthony J ^a   Winkeler, Crystal L ^a   Maggi, Leonard B ^a   Weber, Jason D ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSYLATION FACTOR; BETA INTERFERON; MESSENGER RNA; PROTEIN P53; STAT1 PROTEIN; STAT2 PROTEIN; CYTOKINE; ISG15 PROTEIN, HUMAN; UBIQUITIN;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BREAST CANCER; CANCER INHIBITION; CARCINOGENICITY; CELL CYCLE S PHASE; CELL PROLIFERATION; CYTOKINE PRODUCTION; FEMALE; IMMUNE RESPONSE; INNATE IMMUNITY; LIGAND BINDING; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; UPREGULATION; ANIMAL; BREAST TUMOR; CELL CULTURE; CELL LINE; GENETICS; HUMAN; METABOLISM; MUTATION; SIGNAL TRANSDUCTION;

ADP-RIBOSYLATION FACTORS; ANIMALS; BREAST NEOPLASMS; CELL LINE; CELL PROLIFERATION; CELLS, CULTURED; CYTOKINES; FEMALE; HUMANS; INTERFERON-BETA; MICE; MUTATION; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; TUMOR SUPPRESSOR PROTEIN P53; UBIQUITINS;

EID: 84899629693     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.03.026     Document Type: Article

References (45)

1. Apicelli A.J., Maggi L.B., Hirbe A.C., Miceli A.P., Olanich M.E., Schulte-Winkeler C.L., Saporita A.J., Kuchenreuther M., Sanchez J., Weilbaecher K., Weber J.D. A non-tumor suppressor role for basal p19ARF in maintaining nucleolar structure and function. Mol. Cell. Biol. 2008, 28:1068-1080.
2. Buess M., Nuyten D.S., Hastie T., Nielsen T., Pesich R., Brown P.O. Characterization of heterotypic interaction effects invitro to deconvolute global gene expression profiles in cancer. Genome Biol. 2007, 8:R191.
3. Burks J., Reed R.E., Desai S.D. ISGylation governs the oncogenic function of Ki-Ras in breast cancer. Oncogene 2014, 33:794-803.
4. Comprehensive genomic characterization of squamous cell lung cancers. Nature 2012, 489:519-525. Cancer Genome Atlas Research Network.
5. Chan S.R., Vermi W., Luo J., Lucini L., Rickert C., Fowler A.M., Lonardi S., Arthur C., Young L.J., Levy D.E., et al. STAT1-deficient mice spontaneously develop estrogen receptor α-positive luminal mammary carcinomas. Breast Cancer Res. 2012, 14:R16.
6. Cheon H., Holvey-Bates E.G., Schoggins J.W., Forster S., Hertzog P., Imanaka N., Rice C.M., Jackson M.W., Junk D.J., Stark G.R. IFNβ-dependent increases in STAT1, STAT2, and IRF9 mediate resistance to viruses and DNA damage. EMBO J. 2013, 32:2751-2763.
7. Chiappinelli K.B., Haynes B.C., Brent M.R., Goodfellow P.J. Reduced DICER1 elicits an interferon response in endometrial cancer cells. Mol. Cancer Res. 2012, 10:316-325.
8. Duarte C.W., Willey C.D., Zhi D., Cui X., Harris J.J., Vaughan L.K., Mehta T., McCubrey R.O., Khodarev N.N., Weichselbaum R.R., Gillespie G.Y. Expression signature of IFN/STAT1 signaling genes predicts poor survival outcome in glioblastoma multiforme in a subtype-specific manner. PLoS ONE 2012, 7:e29653.
9. Dunn G.P., Koebel C.M., Schreiber R.D. Interferons, immunity and cancer immunoediting. Nat. Rev. Immunol. 2006, 6:836-848.
10. Durbin J.E., Hackenmiller R., Simon M.C., Levy D.E. Targeted disruption of the mouse Stat1 gene results in compromised innate immunity to viral disease. Cell 1996, 84:443-450.
11. Ellis M.J., Perou C.M. The genomic landscape of breast cancer as a therapeutic roadmap. Cancer Discov. 2013, 3:27-34.
12. Jonkers J., Meuwissen R., van der Gulden H., Peterse H., van der Valk M., Berns A. Synergistic tumor suppressor activity of BRCA2 and p53 in a conditional mouse model for breast cancer. Nat. Genet. 2001, 29:418-425.
13. Kamijo T., Zindy F., Roussel M.F., Quelle D.E., Downing J.R., Ashmun R.A., Grosveld G., Sherr C.J. Tumor suppression at the mouse INK4a locus mediated by the alternative reading frame product p19ARF. Cell 1997, 91:649-659.
14. Kawagishi H., Nakamura H., Maruyama M., Mizutani S., Sugimoto K., Takagi M., Sugimoto M. ARF suppresses tumor angiogenesis through translational control of VEGFA mRNA. Cancer Res. 2010, 70:4749-4758.
15. Kuchenreuther M.J., Weber J.D. The ARF tumor-suppressor controls Drosha translation to prevent Ras-driven transformation. Oncogene 2014, 33:300-307.
16. Kuo M.L., den Besten W., Thomas M.C., Sherr C.J. Arf-induced turnover of the nucleolar nucleophosmin-associated SUMO-2/3 protease Senp3. Cell Cycle 2008, 7:3378-3387.
17. Leonova K.I., Brodsky L., Lipchick B., Pal M., Novototskaya L., Chenchik A.A., Sen G.C., Komarova E.A., Gudkov A.V. p53 cooperates with DNA methylation and a suicidal interferon response to maintain epigenetic silencing of repeats and noncoding RNAs. Proc. Natl. Acad. Sci. USA 2013, 110:E89-E98.
18. - stem cell-like breast cancer cells in human tumors. J.Clin. Invest. 2011, 121:2723-2735.
19. Miceli A.P., Saporita A.J., Weber J.D. Hypergrowth mTORC1 signals translationally activate the ARF tumor suppressor checkpoint. Mol. Cell. Biol. 2012, 32:348-364.
20. O'Dell M.R., Huang J.L., Whitney-Miller C.L., Deshpande V., Rothberg P., Grose V., Rossi R.M., Zhu A.X., Land H., Bardeesy N., Hezel A.F. Kras(G12D) and p53 mutation cause primary intrahepatic cholangiocarcinoma. Cancer Res. 2012, 72:1557-1567.
21. Osiak A., Utermöhlen O., Niendorf S., Horak I., Knobeloch K.P. ISG15, an interferon-stimulated ubiquitin-like protein, is not essential for STAT1 signaling and responses against vesicular stomatitis and lymphocytic choriomeningitis virus. Mol. Cell. Biol. 2005, 25:6338-6345.
22. Perou C.M., Jeffrey S.S., van de Rijn M., Rees C.A., Eisen M.B., Ross D.T., Pergamenschikov A., Williams C.F., Zhu S.X., Lee J.C., et al. Distinctive gene expression patterns in human mammary epithelial cells and breast cancers. Proc. Natl. Acad. Sci. USA 1999, 96:9212-9217.
23. Platanias L.C. Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat. Rev. Immunol. 2005, 5:375-386.
24. Qi Y., Gregory M.A., Li Z., Brousal J.P., West K., Hann S.R. p19ARF directly and differentially controls the functions of c-Myc independently of p53. Nature 2004, 431:712-717.
25. Quelle D.E., Zindy F., Ashmun R.A., Sherr C.J. Alternative reading frames of the INK4a tumor suppressor gene encode two unrelated proteins capable of inducing cell cycle arrest. Cell 1995, 83:993-1000.
26. Ramana C.V., Chatterjee-Kishore M., Nguyen H., Stark G.R. Complex roles of Stat1 in regulating gene expression. Oncogene 2000, 19:2619-2627.
27. Riley T., Sontag E., Chen P., Levine A. Transcriptional control of human p53-regulated genes. Nat. Rev. Mol. Cell Biol. 2008, 9:402-412.
28. Roussel M.F. The INK4 family of cell cycle inhibitors in cancer. Oncogene 1999, 18:5311-5317.
29. Rozenblum E., Schutte M., Goggins M., Hahn S.A., Panzer S., Zahurak M., Goodman S.N., Sohn T.A., Hruban R.H., Yeo C.J., Kern S.E. Tumor-suppressive pathways in pancreatic carcinoma. Cancer Res. 1997, 57:1731-1734.
30. Sadler A.J., Williams B.R. Interferon-inducible antiviral effectors. Nat. Rev. Immunol. 2008, 8:559-568.
31. Sanchez-Cespedes M., Reed A.L., Buta M., Wu L., Westra W.H., Herman J.G., Yang S.C., Jen J., Sidransky D. Inactivation of the INK4A/ARF locus frequently coexists with TP53 mutations in non-small cell lung cancer. Oncogene 1999, 18:5843-5849.
32. Saporita A.J., Maggi L.B., Apicelli A.J., Weber J.D. Therapeutic targets in the ARF tumor suppressor pathway. Curr. Med. Chem. 2007, 14:1815-1827.
33. Selbert S., Bentley D.J., Melton D.W., Rannie D., Lourenço P., Watson C.J., Clarke A.R. Efficient BLG-Cre mediated gene deletion in the mammary gland. Transgenic Res. 1998, 7:387-396.
34. Sherr C.J. The INK4a/ARF network in tumour suppression. Nat. Rev. Mol. Cell Biol. 2001, 2:731-737.
35. Sherr C.J. Divorcing ARF and p53: an unsettled case. Nat. Rev. Cancer 2006, 6:663-673.
36. Sherr C.J., Bertwistle D., DEN Besten W., Kuo M.L., Sugimoto M., Tago K., Williams R.T., Zindy F., Roussel M.F. p53-dependent and -independent functions of the Arf tumor suppressor. Cold Spring Harb. Symp. Quant. Biol. 2005, 70:129-137.
37. Stott F.J., Bates S., James M.C., McConnell B.B., Starborg M., Brookes S., Palmero I., Ryan K., Hara E., Vousden K.H., Peters G. The alternative product from the human CDKN2A locus, p14(ARF), participates in a regulatory feedback loop with p53 and MDM2. EMBO J. 1998, 17:5001-5014.
38. Sugimoto M., Kuo M.L., Roussel M.F., Sherr C.J. Nucleolar Arftumor suppressor inhibits ribosomal RNA processing. Mol. Cell 2003, 11:415-424.
39. Tsai Y.C., Pestka S., Wang L.H., Runnels L.W., Wan S., Lyu Y.L., Liu L.F. Interferon-β signaling contributes to Ras transformation. PLoS ONE 2011, 6:e24291.
40. Weber J.D., Jeffers J.R., Rehg J.E., Randle D.H., Lozano G., Roussel M.F., Sherr C.J., Zambetti G.P. p53-independent functions of the p19(ARF) tumor suppressor. Genes Dev. 2000, 14:2358-2365.
41. Yu H., Pardoll D., Jove R. STATs in cancer inflammation and immunity: a leading role for STAT3. Nat. Rev. Cancer 2009, 9:798-809.
42. Zeng Y., Kotake Y., Pei X.H., Smith M.D., Xiong Y. p53 binds to and is required for the repression of Arf tumor suppressor by HDAC and polycomb. Cancer Res. 2011, 71:2781-2792.
43. Zimmerman M.A., Rahman N.T., Yang D., Lahat G., Lazar A.J., Pollock R.E., Lev D., Liu K. Unphosphorylated STAT1 promotes sarcoma development through repressing expression of Fas and bad and conferring apoptotic resistance. Cancer Res. 2012, 72:4724-4732.
44. Zindy F., Quelle D.E., Roussel M.F., Sherr C.J. Expression of the p16INK4a tumor suppressor versus other INK4 family members during mouse development and aging. Oncogene 1997, 15:203-211.
45. Zindy F., Eischen C.M., Randle D.H., Kamijo T., Cleveland J.L., Sherr C.J., Roussel M.F. Myc signaling via the ARF tumor suppressor regulates p53-dependent apoptosis and immortalization. Genes Dev. 1998, 12:2424-2433.