IKKα Activation of NOTCH Links Tumorigenesis via FOXA2 Suppression

Molecular Cell

Volumn 45, Issue 2, 2012, Pages 171-184

  Liu, Mo ^a,b   Lee, Dung Fang ^a,b   Chen, Chun Te ^a,b   Yen, Chia Jui ^e   Li, Long Yuan ^c   Lee, Hong Jen ^a,b   Chang, Chun Ju ^a   Chang, Wei Chao ^c,d   Hsu, Jung Mao ^a,b   Kuo, Hsu Ping ^a,b   Xia, Weiya ^a   Wei, Yongkun ^a   Chiu, Pei Chun ^c   Chou, Chao Kai ^a,b   Du, Yi ^a,b   Dhar, Debanjan ^f   Karin, Michael ^f,g   Chen, Chung Hsuan ^d   Hung, Mien Chie ^a,b,c  

^a UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^b UNIVERSITY OF TEXAS   (United States)

^c CHINA MEDICAL UNIVERSITY   (Taiwan)

^d GENOMICS RESEARCH CENTER   (Taiwan)

^e NATIONAL CHENG KUNG UNIVERSITY   (Taiwan)

^f University of California San Diego   (United States)

^g UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEPATOCYTE NUCLEAR FACTOR 3BETA; I KAPPA B KINASE ALPHA; NOTCH RECEPTOR; NOTCH1 RECEPTOR; NUMB PROTEIN; PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CARCINOGENESIS; CELL PROLIFERATION; ENZYME PHOSPHORYLATION; HUMAN; HUMAN CELL; HUMAN TISSUE; LIVER; LIVER CELL CARCINOMA; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; TRANSCRIPTION TERMINATION;

ANIMALS; CARCINOMA, HEPATOCELLULAR; CELL PROLIFERATION; CELL TRANSFORMATION, NEOPLASTIC; GENE EXPRESSION REGULATION, NEOPLASTIC; HEPATOCYTE NUCLEAR FACTOR 3-BETA; HUMANS; I-KAPPA B KINASE; LIVER NEOPLASMS; LIVER NEOPLASMS, EXPERIMENTAL; MEMBRANE PROTEINS; MICE; MODELS, BIOLOGICAL; NERVE TISSUE PROTEINS; PHOSPHORYLATION; RECEPTOR, NOTCH1; SIGNAL TRANSDUCTION; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84856264859     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2011.11.018     Document Type: Article

References (43)

1. Allavena P., Garlanda C., Borrello M.G., Sica A., Mantovani A. Pathways connecting inflammation and cancer. Curr. Opin. Genet. Dev. 2008, 18:3-10.
2. Anest V., Hanson J.L., Cogswell P.C., Steinbrecher K.A., Strahl B.D., Baldwin A.S. A nucleosomal function for IkappaB kinase-alpha in NF-kappaB-dependent gene expression. Nature 2003, 423:659-663.
3. Balkwill F., Mantovani A. Inflammation and cancer: back to Virchow?. Lancet 2001, 357:539-545.
4. Bochkis I.M., Rubins N.E., White P., Furth E.E., Friedman J.R., Kaestner K.H. Hepatocyte-specific ablation of Foxa2 alters bile acid homeostasis and results in endoplasmic reticulum stress. Nat. Med. 2008, 14:828-836.
5. Cantarini M.C., de la Monte S.M., Pang M., Tong M., D'Errico A., Trevisani F., Wands J.R. Aspartyl-asparagyl beta hydroxylase over-expression in human hepatoma is linked to activation of insulin-like growth factor and notch signaling mechanisms. Hepatology 2006, 44:446-457.
6. Carayol N., Wang C.Y. IKKalpha stabilizes cytosolic beta-catenin by inhibiting both canonical and non-canonical degradation pathways. Cell. Signal. 2006, 18:1941-1946.
7. Carroll K.D., Bu W., Palmeri D., Spadavecchia S., Lynch S.J., Marras S.A., Tyagi S., Lukac D.M. Kaposi's Sarcoma-associated herpesvirus lytic switch protein stimulates DNA binding of RBP-Jk/CSL to activate the Notch pathway. J.Virol. 2006, 80:9697-9709.
8. Castello G., Scala S., Palmieri G., Curley S.A., Izzo F. HCV-related hepatocellular carcinoma: from chronic inflammation to cancer. Clin. Immunol. 2010, 134:237-250.
9. Danese S., Mantovani A. Inflammatory bowel disease and intestinal cancer: a paradigm of the Yin-Yang interplay between inflammation and cancer. Oncogene 2010, 29:3313-3323.
10. Farre D., Roset R., Huerta M., Adsuara J.E., Rosello L., Alba M.M., Messeguer X. Identification of patterns in biological sequences at the ALGGEN server: PROMO and MALGEN. Nucleic Acids Res. 2003, 31:3651-3653.
11. Gramantieri L., Giovannini C., Lanzi A., Chieco P., Ravaioli M., Venturi A., Grazi G.L., Bolondi L. Aberrant Notch3 and Notch4 expression in human hepatocellular carcinoma. Liver Int. 2007, 27:997-1007.
12. Hayashi Y., Wang W., Ninomiya T., Nagano H., Ohta K., Itoh H. Liver enriched transcription factors and differentiation of hepatocellular carcinoma. Mol. Pathol. 1999, 52:19-24.
13. Hsieh J.J., Henkel T., Salmon P., Robey E., Peterson M.G., Hayward S.D. Truncated mammalian Notch1 activates CBF1/RBPJk-repressed genes by a mechanism resembling that of Epstein-Barr virus EBNA2. Mol. Cell. Biol. 1996, 16:952-959.
14. Hu M.C., Lee D.F., Xia W., Golfman L.S., Ou-Yang F., Yang J.Y., Zou Y., Bao S., Hanada N., Saso H., et al. IkappaB kinase promotes tumorigenesis through inhibition of forkhead FOXO3a. Cell 2004, 117:225-237.
15. Huang W.C., Ju T.K., Hung M.C., Chen C.C. Phosphorylation of CBP by IKKalpha promotes cell growth by switching the binding preference of CBP from p53 to NF-kappaB. Mol. Cell 2007, 26:75-87.
16. Iso T., Kedes L., Hamamori Y. HES and HERP families: multiple effectors of the Notch signaling pathway. J.Cell. Physiol. 2003, 194:237-255.
17. Karaczyn A., Bani-Yaghoub M., Tremblay R., Kubu C., Cowling R., Adams T.L., Prudovsky I., Spicer D., Friesel R., Vary C., Verdi J.M. Two novel human NUMB isoforms provide a potential link between development and cancer. Neural Develop. 2010, 5:31. 10.1186/1749-8104-5-31.
18. Karin M. The IkappaB kinase-a bridge between inflammation and cancer. Cell Res. 2008, 18:334-342.
19. Kimble J., Crittenden S.L. Controls of germline stem cells, entry into meiosis, and the sperm/oocyte decision in Caenorhabditis elegans. Annu. Rev. Cell Dev. Biol. 2007, 23:405-433.
20. Lee D.F., Hung M.C. Advances in targeting IKK and IKK-related kinases for cancer therapy. Clin. Cancer Res. 2008, 14:5656-5662.
21. Lee C.S., Sund N.J., Behr R., Herrera P.L., Kaestner K.H. Foxa2 is required for the differentiation of pancreatic alpha-cells. Dev. Biol. 2005, 278:484-495.
22. Lee D.F., Kuo H.P., Chen C.T., Hsu J.M., Chou C.K., Wei Y., Sun H.L., Li L.Y., Ping B., Huang W.C., et al. IKK beta suppression of TSC1 links inflammation and tumor angiogenesis via the mTOR pathway. Cell 2007, 130:440-455.
23. Lehner F., Kulik U., Klempnauer J., Borlak J. The hepatocyte nuclear factor 6 (HNF6) and FOXA2 are key regulators in colorectal liver metastases. FASEB J. 2007, 21:1445-1462.
24. Luo J.L., Tan W., Ricono J.M., Korchynskyi O., Zhang M., Gonias S.L., Cheresh D.A., Karin M. Nuclear cytokine-activated IKKalpha controls prostate cancer metastasis by repressing Maspin. Nature 2007, 446:690-694.
25. Ma C., Wang J., Luo J. Exposure to asphalt fumes activates activator protein-1 through the phosphatidylinositol 3-kinase/Akt signaling pathway in mouse epidermal cells. J.Biol. Chem. 2003, 278:44265-44272.
26. Maeda S., Yoshida H., Ogura K., Mitsuno Y., Hirata Y., Yamaji Y., Akanuma M., Shiratori Y., Omata M. H.pylori activates NF-kappaB through a signaling pathway involving IkappaB kinases, NF-kappaB-inducing kinase, TRAF2, and TRAF6 in gastric cancer cells. Gastroenterology 2000, 119:97-108.
27. McGill M.A., McGlade C.J. Mammalian numb proteins promote Notch1 receptor ubiquitination and degradation of the Notch1 intracellular domain. J.Biol. Chem. 2003, 278:23196-23203.
28. Medyouf H., Gao X., Armstrong F., Gusscott S., Liu Q., Gedman A.L., Matherly L.H., Schultz K.R., Pflumio F., You M.J., Weng A.P. Acute T-cell leukemias remain dependent on Notch signaling despite PTEN and INK4A/ARF loss. Blood 2010, 115:1175-1184.
29. Messeguer X., Escudero R., Farre D., Nunez O., Martinez J., Alba M.M. PROMO: detection of known transcription regulatory elements using species-tailored searches. Bioinformatics 2002, 18:333-334.
30. Ning L., Wentworth L., Chen H., Weber S.M. Down-regulation of Notch1 signaling inhibits tumor growth in human hepatocellular carcinoma. Am. J. Transl. Res. 2009, 1:358-366.
31. Pui C.H. T cell acute lymphoblastic leukemia: NOTCHing the way toward a better treatment outcome. Cancer Cell 2009, 15:85-87.
32. Qi R., An H., Yu Y., Zhang M., Liu S., Xu H., Guo Z., Cheng T., Cao X. Notch1 signaling inhibits growth of human hepatocellular carcinoma through induction of cell cycle arrest and apoptosis. Cancer Res. 2003, 63:8323-8329.
33. Song L.L., Peng Y., Yun J., Rizzo P., Chaturvedi V., Weijzen S., Kast W.M., Stone P.J., Santos L., Loredo A., et al. Notch-1 associates with IKKalpha and regulates IKK activity in cervical cancer cells. Oncogene 2008, 27:5833-5844.
34. Tanigaki K., Honjo T. Regulation of lymphocyte development by Notch signaling. Nat. Immunol. 2007, 8:451-456.
35. Wederell E.D., Bilenky M., Cullum R., Thiessen N., Dagpinar M., Delaney A., Varhol R., Zhao Y., Zeng T., Bernier B., et al. Global analysis of invivo Foxa2-binding sites in mouse adult liver using massively parallel sequencing. Nucleic Acids Res. 2008, 36:4549-4564.
36. Westhoff B., Colaluca I.N., D'Ario G., Donzelli M., Tosoni D., Volorio S., Pelosi G., Spaggiari L., Mazzarol G., Viale G., et al. Alterations of the Notch pathway in lung cancer. Proc. Natl. Acad. Sci. USA 2009, 106:22293-22298.
37. Whitsett J.A., Haitchi H.M., Maeda Y. Intersections between pulmonary development and disease. Am. J. Resp. Crit. Care Med. 2011, 184:401-406.
38. Wolfrum C., Shih D.Q., Kuwajima S., Norris A.W., Kahn C.R., Stoffel M. Role of Foxa-2 in adipocyte metabolism and differentiation. J.Clin. Invest. 2003, 112:345-356.
39. Xiong W., Ren Z.G., Qiu S.J., Sun H.C., Wang L., Liu B.B., Li Q.S., Zhang W., Zhu X.D., Liu L., et al. Residual hepatocellular carcinoma after oxaliplatin treatment has increased metastatic potential in a nude mouse model and is attenuated by Songyou Yin. BMC Cancer 2010, 10:219. 10.1186/1471-2407-10-219.
40. Yaguchi S., Fukui Y., Koshimizu I., Yoshimi H., Matsuno T., Gouda H., Hirono S., Yamazaki K., Yamori T. Antitumor activity of ZSTK474, a new phosphatidylinositol 3-kinase inhibitor. J.Natl. Cancer Inst. 2006, 98:545-556.
41. Yamamoto Y., Verma U.N., Prajapati S., Kwak Y.T., Gaynor R.B. Histone H3 phosphorylation by IKK-alpha is critical for cytokine-induced gene expression. Nature 2003, 423:655-659.
42. Yang J.Y., Zong C.S., Xia W., Yamaguchi H., Ding Q., Xie X., Lang J.Y., Lai C.C., Chang C.J., Huang W.C., et al. ERK promotes tumorigenesis by inhibiting FOXO3a via MDM2-mediated degradation. Nat. Cell Biol. 2008, 10:138-148.
43. Zardawi S.J., Zardawi I., McNeil C.M., Millar E.K., McLeod D., Morey A.L., Crea P., Murphy N.C., Pinese M., Lopez-Knowles E., et al. High Notch1 protein expression is an early event in breast cancer development and is associated with the HER-2 molecular subtype. Histopathology 2010, 56:286-296.