Nutlin-3 downregulates the expression of the oncogene TCL1 in primary B chronic lymphocytic leukemic cells

Clinical Cancer Research

Volumn 17, Issue 17, 2011, Pages 5649-5655

  Voltan, Rebecca ^a   Di Iasio, Maria Grazia ^a   Bosco, Raffaella ^a   Valeri, Nicola ^b   Pekarski, Yuri ^b   Tiribelli, Mario ^c   Secchiero, Paola ^a   Zauli, Giorgio ^d  

^a UNIVERSITY OF FERRARA   (Italy)

^b OHIO STATE UNIVERSITY   (United States)

^c UNIVERSITY HOSPITAL OF UDINE   (Italy)

^d INSTITUTE FOR MATERNAL AND CHILD HEALTH IRCCS BURLO GAROFOLO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; NUTLIN 3; ONCOPROTEIN; PROTEIN P53; T CELL LEUKEMIA LYMPHOMA 1 PROTEIN; UNCLASSIFIED DRUG;

ADULT; AGED; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; CELL SURVIVAL; CHRONIC LYMPHATIC LEUKEMIA; CLINICAL ARTICLE; CONTROLLED STUDY; DOWN REGULATION; EX VIVO STUDY; FEMALE; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; LEUKEMIA CELL; LEUKEMIA CELL LINE; LYMPHOBLASTOID CELL LINE; MALE; MDM2 GENE; ONCOGENE; PRIORITY JOURNAL; TCL1 GENE; UPREGULATION; WILD TYPE;

ADULT; AGED; AGED, 80 AND OVER; APOPTOSIS; B-LYMPHOCYTES; CELL LINE, TUMOR; CELL PROLIFERATION; DOWN-REGULATION; FEMALE; HUMANS; IMIDAZOLES; LEUKEMIA, LYMPHOCYTIC, CHRONIC, B-CELL; MALE; MIDDLE AGED; PIPERAZINES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-MDM2; RNA INTERFERENCE; RNA, MESSENGER; RNA, SMALL INTERFERING; TUMOR SUPPRESSOR PROTEIN P53;

EID: 80052426626     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-11-1064     Document Type: Article

References (33)

1. Virgilio L., Narducci M.G., Isobe M., Billips L.G., Cooper M.D., Croce C.M., et al. Identification of the TCL1 gene involved in T cell malignancies. Proc Natl Acad Sci U S A 1994;91:12530-12534
2. Bichi R., Shinton S.A., Martin E.S., Koval A., Calin G.A., Cesari R., et al. Human chronic lymphocytic leukemia modeled in mouse by targeted TCL1 expression. Proc Natl Acad Sci U S A 2002;99: 6955-6960 (Pubitemid 34526239)
3. Yan X.J., Albesiano E., Zanesi N., Yancopoulos S., Sawyer A., Romano E., et al. B cell receptors in TCL1 transgenic mice resemble those of aggressive, treatment-resistant human chronic lymphocytic leukemia. Proc Natl Acad Sci U S A 2006;103:11713-11718 (Pubitemid 44182516)
4. Pekarsky Y., Palamarchuk A., Maximov V., Efanov A., Nazaryan N., Santanam U., et al. Tcl1 functions as a transcriptional regulator and is directly involved in the pathogenesis of CLL. Proc Natl Acad Sci U S A 2008;105:19643-19648
5. Herling M., Patel K.A., Khalili J., Schlette E., Kobayashi R., Medeiros L.J., et al. TCL1 shows a regulated expression pattern in chronic lymphocytic leukemia that correlates with molecular subtypes and proliferative state. Leukemia 2006;20:280-285 (Pubitemid 43148666)
6. Aggarwal M., Villuendas R., Gomez G., Rodriguez-Pinilla S.M., Sanchez-Beato M., Alvarez D., et al. TCL1A expression delineates biological and clinical variability in B-cell lymphoma. Mod Pathol 2009;22:206-215
7. Herling M., Patel K.A., Weit N., Lilienthal N., Hallek M., Keating M.J., et al. High TCL1 levels are a marker of B-cell receptor pathway responsiveness and adverse outcome in chronic lymphocytic leukemia. Blood 2009;114:4675-4686
8. Laine J., Kunstle G., Obata T., Sha M., Noguchi M. The protooncogene TCL1 is an Akt kinase coactivator. Mol Cell 2000;6:395-407.
9. Pekarsky Y., Koval A., Hallas C., Bichi R., Tresini M., Malstrom S., et al. Tcl1 enhances Akt kinase activity and mediates its nuclear translocation. Proc Natl Acad Sci U S A 2000;97:3028-3033 (Pubitemid 30183249)
10. + leukemic cell populations in TCL1 transgenic mice show significantly increased proliferation and Akt phosphorylation. Leukemia 2010;24:970-975
11. Secchiero P., di Iasio M.G., Gonelli A., Zauli G. The MDM2 inhibitor Nutlins as an innovative therapeutic tool for the treatment of haematological malignancies. Curr Pharm Des 2008;14:2100-2110
12. Zenz T., Kröber A., Scherer K., Häbe S., Bühler A., Benner A., et al. Monoallelic TP53 inactivation is associated with poor prognosis in chronic lymphocytic leukemia: Results from a detailed genetic characterization with long-term follow-up. Blood 2008;112:3322-3329
13. Kojima K., Konopleva M., Samudio I.J., Shikami M., Cabreira-Hansen M., McQueen T., et al. MDM2 antagonists induce p53-dependent apoptosis in AML: Implications for leukemia therapy. Blood 2005;106: 3150-3159 (Pubitemid 41565913)
14. Secchiero P., Zerbinati C., di Iasio M.G., Melloni E., Tiribelli M., Grill V., et al. Synergistic cytotoxic activity of recombinant TRAIL plus the nongenotoxic activator of the p53 pathway nutlin-3 in acute myeloid leukemia cells. Curr Drug Metab 2007;8:395-403. (Pubitemid 46780067)
15. Secchiero P., Corallini F., Gonelli A., Dell'Eva R., Vitale M., Capitani S., et al. Antiangiogenic activity of the MDM2 antagonist nutlin-3. Circ Res 2007;100:61-69 (Pubitemid 46066774)
16. Kojima K., Konopleva M., McQueen T., O'Brien S., Plunkett W., Andreeff M. Mdm2 inhibitor Nutlin-3a induces p53-mediated apoptosis by transcription- dependent and transcription-independent mechanisms and may overcome Atm mediated resistance to fludarabine in chronic lymphocytic leukemia. Blood 2006;108:993-1000.
17. Secchiero P., Barbarotto E., Tiribelli M., Zerbinati C., di Iasio M.G., Gonelli A., et al. Functional integrity of the p53-mediated apoptotic pathway induced by the nongenotoxic agent nutlin-3 in B-cell chronic lymphocytic leukemia (B-CLL). Blood 2006;107:4122-4129 (Pubitemid 43726822)
18. Saddler C., Ouillette P., Kujawski L., Shangary S., Talpaz M., Kaminski M., et al. Comprehensive biomarker and genomic analysis identifies p53 status as the major determinant of response to MDM2 inhibitors in chronic lymphocytic leukemia. Blood 2008;111:1584-1593 (Pubitemid 351213449)
19. Zauli G., Voltan R., Bosco R.,Melloni E., Marmiroli S., RigolinG.M., et al. Dasatinib plus Nutlin-3 shows synergistic antileukemic activity in both p53 wild-type and p53 mutated B chronic lymphocytic leukemias by inhibiting the Akt pathway. Clin Cancer Res 2011;17: 762-770
20. Steele A.J., Prentice A.G., Hoffbrand A.V., Yogashangary B.C., Hart S.M., Nacheva E.P., et al. p53-mediated apoptosis of CLL cells: Evidence for a transcription-independent mechanism. Blood 2008;112: 3827-3834
21. Vaseva A.V., Marchenko N.D., Moll U.M. The transcription-independent mitochondrial p53 program is a major contributor to nutlin-induced apoptosis in tumor cells. Cell Cycle 2009;8:1711-1719
22. Saha M.N., Jiang H., Chang H. Molecular mechanisms of nutlin-induced apoptosis in multiple myeloma: Evidence for p53-transcription-dependentand -independent pathways. Cancer Biol Ther 2010;10: 567-578
23. Secchiero P., Melloni E., di Iasio M.G., Tiribelli M., Rimondi E., Corallini F., et al. Nutlin-3 upregulates the expression of Notch1 in both myeloid and lymphoid leukemic cells, as part of a negative feed-back antiapoptotic mechanism. Blood 2009;113:4300-4308
24. Zauli G., di Iasio M.G., Secchiero P., Dal Bo M., Marconi D., Bomben R., et al. Exposure of B cell chronic lymphocytic leukemia (B-CLL) cells to nutlin-3 induces a characteristic gene expression profile, which correlates with nutlin-3-mediated cytotoxicity. Curr Cancer Drug Targets 2009;9:510-518
25. +) cells purified from the bone marrow of AIDS patients are committed to apoptotic cell death in culture. AIDS 1993;7:1049-1055
26. Milani D., Zauli G., Rimondi E., Celeghini C., Marmiroli S., Narducci P., et al. Tumour necrosis factor-related apoptosis-inducing ligand sequentially activates pro-survival and pro-apoptotic pathways in SK-N-MC neuronal cells. J Neurochem 2003;86:126-135 (Pubitemid 36753853)
27. Secchiero P., Corallini F., di Iasio M.G., Gonelli A., Barbarotto E., Zauli G. TRAIL counteracts the proadhesive activity of inflammatory cytokines in endothelial cells by down-modulating CCL8 and CXCL10 chemokine expression and release. Blood 2005;105:3413-3419 (Pubitemid 40628180)
28. Secchiero P., Sun D., De Vico A.L., Crowley R.W., Reitz M.S. Jr, Zauli G., et al. Role of the extracellular domain of human herpesvirus 7 glycoprotein B in virus binding to cell surface heparan sulfate proteoglycans. J Virol 1997;71:4571-4580 (Pubitemid 27204150)
29. Pekarsky Y., Santanam U., Cimmino A., Palamarchuk A., Efanov A., Maximov V., et al. Tcl1 expression in chronic lymphocytic leukemia is regulated by miR-29 and miR-181. Cancer Res 2006;66:11590-11593 (Pubitemid 46094168)
30. Kojima K., Konopleva M., McQueen T., O'Brien S., Plunkett W., Andreeff M. Mdm2 inhibitor Nutlin-3a induces p53-mediated apoptosis by transcription- dependent and transcription-independent mechanisms and may overcome Atm-mediated resistance to fludarabine in chronic lymphocytic leukemia. Blood 2006;108:993-1000.
31. Valentine J.M., Kumar S., Moumen A. A p53-independent role for the MDM2 antagonist Nutlin-3 in DNA damage response initiation. BMC Cancer 2011;11:79.
32. Pekarsky Y., Croce C.M. Is miR-29 an oncogene or tumor suppressor in CLL?Oncotarget 2010;1:224-227
33. Harris S.L., Levine A.J. The p53 pathway: Positive and negative feedback loops. Oncogene 2005;24:2899-2908 (Pubitemid 40638098)