Bal1/artd9 represses the anti-proliferative and pro-apoptotic IFNγ-STAT1-IRF1-p53 axis indiffuse large B-cell lymphoma

Journal of Cell Science

Volumn 126, Issue 9, 2013, Pages 1969-1980

  Camicia, Rosalba ^a   Bachmann, Samia B ^a   Winkler, Hans C ^a   Beer, Marc ^b   Tinguely, Marianne ^b   Haralambieva, Eugenia ^b   Hassa, Paul O ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

ADP ribosylation; BAL1 ARTD9; Diffuse large B cell lymphoma; IFN STAT1 signaling; IRF1; Macrodomains; P53; Survival

Indexed keywords

ADP RIBOSYLTRANSFERASE 9; B AGGRESSIVE LYMPHOMA 1 PROTEIN; GAMMA INTERFERON; INTERFERON REGULATORY FACTOR 1; INTERFERON REGULATORY FACTOR 2; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; ONCOPROTEIN; PROTEIN BCL 6; PROTEIN P53; STAT1 ALPHA PROTEIN; STAT1 BETA PROTEIN; STAT1 PROTEIN; UNCLASSIFIED DRUG;

ADENOSINE DIPHOSPHATE RIBOSYLATION; ANTIPROLIFERATIVE ACTIVITY; APOPTOSIS; ARTICLE; CANCER RESISTANCE; CELL NUCLEUS; CELL PROLIFERATION; CELL SURVIVAL; COMPLEX FORMATION; CONTROLLED STUDY; GENE EXPRESSION; HIGH RISK PATIENT; HUMAN; HUMAN CELL; LARGE CELL LYMPHOMA; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTO ONCOGENE; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR GENE;

ADP-RIBOSYLATION; BAL1/ARTD9; DIFFUSE LARGE B-CELL LYMPHOMA; IFNΓ-STAT1-SIGNALING; IRF1; MACRODOMAINS; P53; SURVIVAL;

APOPTOSIS; CELL LINE, TUMOR; CELL PROLIFERATION; DRUG RESISTANCE, NEOPLASM; GENE EXPRESSION REGULATION, NEOPLASTIC; HEK293 CELLS; HUMANS; INTERFERON REGULATORY FACTOR-1; INTERFERON REGULATORY FACTOR-2; INTERFERON-GAMMA; LYMPHOMA, LARGE B-CELL, DIFFUSE; NEOPLASM PROTEINS; PROTEIN ISOFORMS; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84878644504     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.118174     Document Type: Article

References (59)

1. Abramson, J. S. and Shipp, M. A. (2005). Advances in the biology and therapy of diffuse large B-cell lymphoma: moving toward a molecularly targeted approach. Blood 106, 1164-1174.
2. Aguiar, R. C., Yakushijin, Y., Kharbanda, S., Salgia, R., Fletcher, J. A. and Shipp, M. A. (2000). BAL is a novel risk-related gene in diffuse large B-cell lymphomas that enhances cellular migration. Blood 96, 4328-4334.
3. Aguiar, R. C., Takeyama, K., He, C., Kreinbrink, K. and Shipp, M. A. (2005). Baggressive lymphoma family proteins have unique domains that modulate transcription and exhibit poly(ADP-ribose) polymerase activity. J. Biol. Chem. 280, 33756-33765.
4. Aho, T. L., Sandholm, J., Peltola, K. J., Mankonen, H. P., Lilly, M. and Koskinen, P. J. (2004). Pim-1 kinase promotes inactivation of the pro-apoptotic Bad protein by phosphorylating it on the Ser112 gatekeeper site. FEBS Lett. 571, 43-49.
5. Baran-Marszak, F., Feuillard, J., Najjar, I., Le Clorennec, C., Béchet, J. M., Dusanter-Fourt, I., Bornkamm, G. W., Raphaël, M. and Fagard, R. (2004).Differential roles of STAT1alpha and STAT1beta in fludarabine-induced cell cycle arrest and apoptosis in human B cells. Blood 104, 2475-2483.
6. Barbarulo, A., Iansante, V., Chaidos, A., Naresh, K., Rahemtulla, A., Franzoso, G., Karadimitris, A., Haskard, D. O., Papa, S. and Bubici, C. (2012). Poly(ADPribose) polymerase family member 14 (PARP14) is a novel effector of the JNK2- dependent pro-survival signal in multiple myeloma. Oncogene [Epub ahead of print] doi:10.1038/onc.2012.448.
7. Chen, J. L., Limnander, A. and Rothman, P. B. (2008). Pim-1 and Pim-2 kinases are required for efficient pre-B-cell transformation by v-Abl oncogene. Blood 111, 1677- 1685.
8. Cho, S. H., Goenka, S., Henttinen, T., Gudapati, P., Reinikainen, A., Eischen, C. M., Lahesmaa, R. and Boothby, M. (2009a). PARP-14, a member of the B aggressive lymphoma (BAL) family, transduces survival signals in primary B cells. Blood. 113, 2416-2425.
9. Cho, S. H., Goenka, S., Henttinen, T., Gudapati, P., Reinikainen, A., Eischen, C. M., Lahesmaa, R. and Boothby, M. (2009b). PARP-14, a member of the B aggressive lymphoma family, transduces survival signals in primary B cells. Blood 113, 2416- 2425.
10. Choo, A., Palladinetti, P., Passioura, T., Shen, S., Lock, R., Symonds, G. and Dolnikov, A. (2006). The role of IRF1 and IRF2 transcription factors in leukaemogenesis. Curr. Gene Ther. 6, 543-550.
11. Chung, K. H., Hart, C. C., Al-Bassam, S., Avery, A., Taylor, J., Patel, P. D., Vojtek, A. B. and Turner, D. L. (2006). Polycistronic RNA polymerase II expression vectors for RNA interference based on BIC/miR-155. Nucleic Acids Res. 34, e53.
12. Covic, M., Hassa, P. O., Saccani, S., Buerki, C., Meier, N. I., Lombardi, C., Imhof, R., Bedford, M. T., Natoli, G. and Hottiger, M. O. (2005). Arginine methyltransferase CARM1 is a promoter-specific regulator of NF-kappaB-dependent gene expression. EMBO J. 24, 85-96.
13. Cunningham, O., Andolfo, A., Santovito, M. L., Iuzzolino, L., Blasi, F. and Sidenius, N. (2003). Dimerization controls the lipid raft partitioning of uPAR/CD87 and regulates its biological functions. EMBO J. 22, 5994-6003.
14. Darnell, J. E., Jr, Kerr, I. M. and Stark, G. R. (1994). Jak-STAT pathways and transcriptional activation in response to IFNs and other extracellular signaling proteins. Science 264, 1415-1421.
15. Davis, R. E., Ngo, V. N., Lenz, G., Tolar, P., Young, R. M., Romesser, P. B., Kohlhammer, H., Lamy, L., Zhao, H., Yang, Y. et al. (2010). Chronic active Bcell- receptor signalling in diffuse large B-cell lymphoma. Nature 463, 88-92.
16. Decker, T. and Kovarik, P. (2000). Serine phosphorylation of STATs. Oncogene 19, 2628-2637.
17. Dignam, J. D., Martin, P. L., Shastry, B. S. and Roeder, R. G. (1983). Eukaryotic gene transcription with purified components. Methods Enzymol. 101, 582-598.
18. Duan, S., Cermak, L., Pagan, J. K., Rossi, M., Martinengo, C., di Celle, P. F., Chapuy, B., Shipp, M., Chiarle, R. and Pagano, M. (2012). FBXO11 targets BCL6 for degradation and is inactivated in diffuse large B-cell lymphomas. Nature 481, 90- 93.
19. Dunn, G. P., Koebel, C. M. and Schreiber, R. D. (2006). Interferons, immunity and cancer immunoediting. Nat. Rev. Immunol. 6, 836-848.
20. Goenka, S. and Boothby, M. (2006). Selective potentiation of Stat-dependent gene expression by collaborator of Stat6 (CoaSt6), a transcriptional cofactor. Proc. Natl. Acad. Sci. USA 103, 4210-4215.
21. Goenka, S., Cho, S. H. and Boothby, M. (2007). Collaborator of Stat6 (CoaSt6)- associated poly(ADP-ribose) polymerase activity modulates Stat6-dependent gene transcription. J. Biol. Chem. 282, 18732-18739.
22. Green, W. B., Slovak, M. L., Chen, I. M., Pallavicini, M., Hecht, J. L. and Willman, C. L. (1999). Lack of IRF-1 expression in acute promyelocytic leukemia and in a subset of acute myeloid leukemias with del(5)(q31). Leukemia 13, 1960-1971.
23. Guetg, C., Scheifele, F., Rosenthal, F., Hottiger, M. O. and Santoro, R. (2012). Inheritance of silent rDNA chromatin is mediated by PARP1 via noncoding RNA. Mol. Cell 45, 790-800.
24. Hassa, P. O., Haenni, S. S., Buerki, C., Meier, N. I., Lane, W. S., Owen, H., Gersbach, M., Imhof, R. and Hottiger, M. O. (2005). Acetylation of poly(ADPribose) polymerase-1 by p300/CREB-binding protein regulates coactivation of NFkappaB- dependent transcription. J. Biol. Chem. 280, 40450-40464.
25. Hottiger, M. O., Hassa, P. O., Lüscher, B., Schüler, H. and Koch-Nolte, F. (2010). Toward a unified nomenclature for mammalian ADP-ribosyltransferases. Trends Biochem. Sci. 35, 208-219.
26. Juszczynski, P., Kutok, J. L., Li, C., Mitra, J., Aguiar, R. C. and Shipp, M. A. (2006). BAL1 and BBAP are regulated by a gamma interferon-responsive bidirectional promoter and are overexpressed in diffuse large B-cell lymphomas with a prominent inflammatory infiltrate. Mol. Cell. Biol. 26, 5348-5359.
27. Juszczyński, P., Nowak, J. and Warzocha, K. (2008). Host immune response in B-cell lymphomas: friend or foe? Arch. Immunol. Ther. Exp. (Warsz.) 56, 245-255.
28. Khodarev, N. N., Beckett, M., Labay, E., Darga, T., Roizman, B. and Weichselbaum, R. R. (2004). STAT1 is overexpressed in tumors selected for radioresistance and confers protection from radiation in transduced sensitive cells. Proc. Natl. Acad. Sci. USA 101, 1714-1719.
29. Khodarev, N. N., Roach, P., Pitroda, S. P., Golden, D. W., Bhayani, M., Shao, M. Y., Darga, T. E., Beveridge, M. G., Sood, R. F., Sutton, H. G. et al. (2009). STAT1 pathway mediates amplification of metastatic potential and resistance to therapy. PLoS ONE 4, e5821.
30. Khodarev, N. N., Roizman, B. and Weichselbaum, R. R. (2012). Molecular pathways: interferon/stat1 pathway: role in the tumor resistance to genotoxic stress and aggressive growth. Clin. Cancer Res. 18, 3015-3021.
31. Lukacher, A. E. (2002). IFN-gamma suspends the killing license of anti-tumor CTLs. J. Clin. Invest. 110, 1407-1409.
32. Meyer, T., Marg, A., Lemke, P., Wiesner, B. and Vinkemeier, U. (2003). DNA binding controls inactivation and nuclear accumulation of the transcription factor Stat1. Genes Dev. 17, 1992-2005.
33. Monti, S., Savage, K. J., Kutok, J. L., Feuerhake, F., Kurtin, P., Mihm, M., Wu, B., Pasqualucci, L., Neuberg, D., Aguiar, R. C. et al. (2005). Molecular profiling of diffuse large B-cell lymphoma identifies robust subtypes including one characterized by host inflammatory response. Blood 105, 1851-1861.
34. Mowen, K. and David, M. (2000). Regulation of STAT1 nuclear export by Jak1. Mol. Cell. Biol. 20, 7273-7281.
35. Moyle, P. M. and Muir, T. W. (2010). Method for the synthesis of mono-ADP-ribose conjugated peptides. J. Am. Chem. Soc. 132, 15878-15880.
36. Ngo, V. N., Young, R. M., Schmitz, R., Jhavar, S., Xiao, W., Lim, K. H., Kohlhammer, H., Xu, W., Yang, Y., Zhao, H. et al. (2011). Oncogenically active MYD88 mutations in human lymphoma. Nature 470, 115-119.
37. Nozawa, H., Oda, E., Nakao, K., Ishihara, M., Ueda, S., Yokochi, T., Ogasawara, K., Nakatsuru, Y., Shimizu, S., Ohira, Y. et al. (1999). Loss of transcription factor IRF- 1 affects tumor susceptibility in mice carrying the Ha-ras transgene or nullizygosity for p53. Genes Dev. 13, 1240-1245.
38. Okada, S., Yamada, E., Saito, T., Ohshima, K., Hashimoto, K., Yamada, M., Uehara, Y., Tsuchiya, T., Shimizu, H., Tatei, K. et al. (2008). CDK5-dependent phosphorylation of the Rho family GTPase TC10(alpha) regulates insulin-stimulated GLUT4 translocation. J. Biol. Chem. 283, 35455-35463.
39. Owen, H. R., Quadroni, M., Bienvenut, W., Buerki, C. and Hottiger, M. O. (2005). Identification of novel and cell type enriched cofactors of the transcription activation domain of RelA (p65 NF-kappaB). J. Proteome Res. 4, 1381-1390.
40. Phan, R. T. and Dalla-Favera, R. (2004). The BCL6 proto-oncogene suppresses p53 expression in germinal-centre B cells. Nature 432, 635-639.
41. Rosenwald, A., Wright, G., Chan, W. C., Connors, J. M., Campo, E., Fisher, R. I., Gascoyne, R. D., Muller-Hermelink, H. K., Smeland, E. B., Giltnane, J. M. et al.; Lymphoma/Leukemia Molecular Profiling Project (2002). The use of molecular profiling to predict survival after chemotherapy for diffuse large-B-cell lymphoma. N. Engl. J. Med. 346, 1937-1947.
42. Saito, M., Gao, J., Basso, K., Kitagawa, Y., Smith, P. M., Bhagat, G., Pernis, A., Pasqualucci, L. and Dalla-Favera, R. (2007). A signaling pathway mediating downregulation of BCL6 in germinal center B cells is blocked by BCL6 gene alterations in B cell lymphoma. Cancer Cell 12, 280-292.
43. Saito, M., Novak, U., Piovan, E., Basso, K., Sumazin, P., Schneider, C., Crespo, M., Shen, Q., Bhagat, G., Califano, A. et al. (2009). BCL6 suppression of BCL2 via Miz1 and its disruption in diffuse large B cell lymphoma. Proc. Natl. Acad. Sci. USA 106, 11294-11299.
44. Schwartz, J. L., Shajahan, A. N. and Clarke, R. (2011). The Role of Interferon Regulatory Factor-1 (IRF1) in Overcoming Antiestrogen Resistance in the Treatment of Breast Cancer. Int. J. Breast Cancer 2011, 912102.
45. Sen, S., Roy, K., Mukherjee, S., Mukhopadhyay, R. and Roy, S. (2011). Restoration of IFNγR subunit assembly, IFNγ signaling and parasite clearance in Leishmania donovani infected macrophages: role of membrane cholesterol. PLoS Pathog. 7, e1002229.
46. Shaffer, A. L., III, Young, R. M. and Staudt, L. M. (2012). Pathogenesis of Human B Cell Lymphomas. Annu. Rev. Immunol. 30, 565-610.
47. Shi, L., Perin, J. C., Leipzig, J., Zhang, Z. and Sullivan, K. E. (2011). Genome-wide analysis of interferon regulatory factor I binding in primary human monocytes. Gene 487, 21-28.
48. Shipp, M. A., Ross, K. N., Tamayo, P., Weng, A. P., Kutok, J. L., Aguiar, R. C., Gaasenbeek, M., Angelo, M., Reich, M., Pinkus, G. S. et al. (2002). Diffuse large B-cell lymphoma outcome prediction by gene-expression profiling and supervised machine learning. Nat. Med. 8, 68-74.
49. Stang, M. T., Armstrong, M. J., Watson, G. A., Sung, K. Y., Liu, Y., Ren, B. and Yim, J. H. (2007). Interferon regulatory factor-1-induced apoptosis mediated by a ligand-independent fas-associated death domain pathway in breast cancer cells. Oncogene 26, 6420-6430.
50. Stefancikova, L., Moulis, M., Fabian, P., Vasova, I., Zedek, F., Ravcukova, B., Muzik, J., Kuglik, P., Vranova, V., Falkova, I. et al. (2011). Prognostic impact of p53 aberrations for R-CHOP-treated patients with diffuse large B-cell lymphoma. Int. J. Oncol. 39, 1413-1420.
51. Stronach, E. A., Alfraidi, A., Rama, N., Datler, C., Studd, J. B., Agarwal, R., Guney, T. G., Gourley, C., Hennessy, B. T., Mills, G. B. et al. (2011). HDAC4-regulated STAT1 activation mediates platinum resistance in ovarian cancer. Cancer Res. 71, 4412-4422.
52. Taniguchi, T., Ogasawara, K., Takaoka, A. and Tanaka, N. (2001). IRF family of transcription factors as regulators of host defense. Annu. Rev. Immunol. 19, 623-655.
53. Timinszky, G., Till, S., Hassa, P. O., Hothorn, M., Kustatscher, G., Nijmeijer, B., Colombelli, J., Altmeyer, M., Stelzer, E. H., Scheffzek, K. et al. (2009). A macrodomain-containing histone rearranges chromatin upon sensing PARP1 activation. Nat. Struct. Mol. Biol. 16, 923-929.
54. Townsend, P. A., Scarabelli, T. M., Davidson, S. M., Knight, R. A., Latchman, D. S. and Stephanou, A. (2004). STAT-1 interacts with p53 to enhance DNA damageinduced apoptosis. J. Biol. Chem. 279, 5811-5820.
55. Wahlberg, E., Karlberg, T., Kouznetsova, E., Markova, N., Macchiarulo, A., Thorsell, A. G., Pol, E., Frostell, A., Ekblad, T., Öncü , D. et al. (2012). Familywide chemical profiling and structural analysis of PARP and tankyrase inhibitors. Nat. Biotechnol. 30, 283-288.
56. Weichselbaum, R. R., Ishwaran, H., Yoon, T., Nuyten, D. S., Baker, S. W., Khodarev, N., Su, A. W., Shaikh, A. Y., Roach, P., Kreike, B. et al. (2008). An interferon-related gene signature for DNA damage resistance is a predictive marker for chemotherapy and radiation for breast cancer. Proc. Natl. Acad. Sci. USA 105, 18490-18495.
57. Yan, B., Zemskova, M., Holder, S., Chin, V., Kraft, A., Koskinen, P. J. and Lilly, M. (2003). The PIM-2 kinase phosphorylates BAD on serine 112 and reverses BADinduced cell death. J. Biol. Chem. 278, 45358-45367.
58. Yanagawa, T., Funasaka, T., Tsutsumi, S., Hu, H., Watanabe, H. and Raz, A. (2007). Regulation of phosphoglucose isomerase/autocrine motility factor activities by the poly(ADP-ribose) polymerase family-14. Cancer Res. 67, 8682-8689.
59. Zakharova, N., Lymar, E. S., Yang, E., Malik, S., Zhang, J. J., Roeder, R. G. and Darnell, J. E., Jr (2003). Distinct transcriptional activation functions of STAT1alpha and STAT1beta on DNA and chromatin templates. J. Biol. Chem. 278, 43067-43073.