Ink4a and Arf are crucial factors in the determination of the cell of origin and the therapeutic sensitivity of Myc-induced mouse lymphoid tumor

Oncogene

Volumn 31, Issue 23, 2012, Pages 2849-2861

  Sugihara, E ^a,b   Shimizu, T ^a,b   Kojima, K ^c   Onishi, N ^a   Kai, K ^a   Ishizawa, J ^a   Nagata, K ^d   Hashimoto, N ^a   Honda, H ^e   Kanno, M ^e   Miwa, M ^f   Okada, S ^g   Andreeff, M ^c   Saya, H ^a,b  

^a KEIO UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

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

^d KYOWA HAKKO KOGYO CO LTD   (Japan)

^e HIROSHIMA UNIVERSITY   (Japan)

^f NAGAHAMA INSTITUTE OF BIO SCIENCE AND TECHNOLOGY   (Japan)

^g KUMAMOTO UNIVERSITY   (Japan)

Author keywords

Arf; cell of origin; Ink4a; Mdm2 inhibitor; Myc; pre B ALL LBL

Indexed keywords

ARF PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR 2A; CYTARABINE; MYC PROTEIN; NUTLIN 3; PROTEIN MDM2; RETROVIRUS VECTOR;

ACUTE LYMPHOBLASTIC LEUKEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; BONE MARROW CELL; CANCER CELL CULTURE; CANCER RELAPSE; CANCER SUSCEPTIBILITY; CONTROLLED STUDY; GENETIC SUSCEPTIBILITY; GENETIC TRANSDUCTION; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; LYMPHOBLASTOMA; LYMPHOID PROGENITOR CELL; MOUSE; MYELOID PROGENITOR CELL; NONHUMAN; PRE B LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TUMOR CELL; TUMOR GROWTH;

ANIMALS; ANTIMETABOLITES, ANTINEOPLASTIC; APOPTOSIS; BLOTTING, WESTERN; BONE MARROW CELLS; BONE MARROW TRANSPLANTATION; CELLS, CULTURED; CYCLIN-DEPENDENT KINASE INHIBITOR P16; CYTARABINE; DISEASE MODELS, ANIMAL; FLOW CYTOMETRY; GENES, MYC; HEMATOPOIETIC STEM CELLS; HUMANS; IMIDAZOLES; MICE; MICE, KNOCKOUT; PIPERAZINES; PRECURSOR B-CELL LYMPHOBLASTIC LEUKEMIA-LYMPHOMA; PRECURSOR CELLS, B-LYMPHOID; TUMOR SUPPRESSOR PROTEIN P14ARF;

EID: 84861994671     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2011.462     Document Type: Article

References (40)

1. Adams JM, Harris AW, Pinkert CA, Corcoran LM, Alexander WS, Cory S et al. (1985). The c-myc oncogene driven by immunoglobulin enhancers induces lymphoid malignancy in transgenic mice. Nature 318: 533-538. (Pubitemid 16173038)
2. Ausserlechner MJ, Obexer P, Wiegers GJ, Hartmann BL, Geley S, Kofler R. (2001). The cell cycle inhibitor p16(INK4A) sensitizes lymphoblastic leukemia cells to apoptosis by physiologic glucocorticoid levels. J Biol Chem 276: 10984-10989. (Pubitemid 38089278)
3. Calabretta B, Perrotti D. (2004). The biology of CML blast crisis. Blood 103: 4010-4022. (Pubitemid 38685338)
4. Cano F, Pannel R, Follows GA, Rabbitts TH. (2008). Preclinical modeling of cytosine arabinoside response in Mll-Enl translocator mouse leukemias. Mol Cancer Ther 7: 730-735. (Pubitemid 351482156)
5. Cardone M, Kandilci A, Carella C, Nilsson JA, Brennan JA, Sirma S et al. (2005). The novel ETS factor TEL2 cooperates with Myc in B lymphomagenesis. Mol Cell Biol 25: 2395-2405. (Pubitemid 40354633)
6. Castor A, Nilsson L, Astrand-Grundstrom I, Buitenhuis M, Ramirez C, Anderson K et al. (2005). Distinct patterns of hematopoietic stem cell involvement in acute lymphoblastic leukemia. Nat Med 11: 630-637. (Pubitemid 40868303)
7. Cobaleda C, Gutierrez-Cianca N, Perez-Losada J, Flores T, Garcia-Sanz R, Gonzalez M et al. (2000). A primitive hematopoietic cell is the target for the leukemic transformation in human Philadelphiapositive acute lymphoblastic leukemia. Blood 95: 1007-1013. (Pubitemid 30062725)
8. Cobaleda C, Sanchez-Garcia I. (2009). B-cell acute lymphoblastic leukaemia: towards understanding its cellular origin. Bioessays 31: 600-609.
9. Cox CV, Evely RS, Oakhill A, Pamphilon DH, Goulden NJ, Blair A. (2004). Characterization of acute lymphoblastic leukemia progenitor cells. Blood 104: 2919-2925. (Pubitemid 39434980)
10. Eischen CM, Weber JD, Roussel MF, Sherr CJ, Cleveland JL. (1999). Disruption of the ARF-Mdm2-p53 tumor suppressor pathway in Myc-induced lymphomagenesis. Genes Dev 13: 2658-2669. (Pubitemid 29508553)
11. Gu L, Zhu N, Findley HW, Zhou M. (2008). MDM2 antagonist nutlin-3 is a potent inducer of apoptosis in pediatric acute lymphoblastic leukemia cells with wild-type p53 and overexpression of MDM2. Leukemia 22: 730-739. (Pubitemid 351552622)
12. Hemann MT, Bric A, Teruya-Feldstein J, Herbst A, Nilsson JA, Cordon-Cardo C et al. (2005). Evasion of the p53 tumour surveillance network by tumour-derived MYC mutants. Nature 436: 807-811. (Pubitemid 41160633)
13. Hong D, Gupta R, Ancliff P, Atzberger A, Brown J, Soneji S et al. (2008). Initiating and cancer-propagating cells in TEL-AML1-associated childhood leukemia. Science 319: 336-339.
14. Hotfilder M, Rottgers S, Rosemann A, Schrauder A, Schrappe M, Pieters R et al. (2005). Leukemic stem cells in childhood high-risk ALL/t(9;22) and t(4;11) are present in primitive lymphoid-restricted CD34+CD19-cells. Cancer Res 65: 1442-1449. (Pubitemid 40270173)
15. Hu Y, Smyth GK. (2009). ELDA: extreme limiting dilution analysis for comparing depleted and enriched populations in stem cell and other assays. J Immunol Methods 347: 70-78.
16. Iwama A, Oguro H, Negishi M, Kato Y, Morita Y, Tsukui H et al. (2004). Enhanced self-renewal of hematopoietic stem cells mediated by the polycomb gene product Bmi-1. Immunity 21: 843-851. (Pubitemid 39626674)
17. Jacobs JJ, Scheijen B, Voncken JW, Kieboom K, Berns A, van Lohuizen M. (1999). Bmi-1 collaborates with c-Myc in tumorigenesis by inhibiting c-Myc-induced apoptosis via INK4a/ARF. Genes Dev 13: 2678-2690. (Pubitemid 29508555)
18. Kamijo T, Zindy F, Roussel MF, Quelle DE, Downing JR, Ashmun RA et al. (1997). Tumor suppression at the mouse INK4a locus mediated by the alternative reading frame product p19ARF. Cell 91: 649-659. (Pubitemid 27513656)
19. Kawagoe H, Kandilci A, Kranenburg TA, Grosveld GC. (2007). Overexpression of N-Myc rapidly causes acute myeloid leukemia in mice. Cancer Res 67: 10677-10685. (Pubitemid 350145893)
20. Kojima K, Konopleva M, McQueen T, O'Brien S, Plunkett W, Andreeff M. (2006). 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 108: 993-1000. (Pubitemid 44154636)
21. Kojima K, KonoplevaM, Samudio IJ, Shikami M, Cabreira-HansenM, McQueen T et al. (2005). MDM2 antagonists induce p53-dependent apoptosis in AML: implications for leukemia therapy. Blood 106: 3150-3159. (Pubitemid 41565913)
22. le Viseur C, Hotfilder M, Bomken S, Wilson K, Rottgers S, Schrauder A et al. (2008). In childhood acute lymphoblastic leukemia, blasts at different stages of immunophenotypic maturation have stem cell properties. Cancer Cell 14: 47-58. (Pubitemid 351885495)
23. Luo H, Li Q, O'Neal J, Kreisel F, Le Beau MM, Tomasson MH. (2005). c-Myc rapidly induces acute myeloid leukemia in mice without evidence of lymphoma-associated antiapoptotic mutations. Blood 106: 2452-2461. (Pubitemid 41510820)
24. Meyer N, Penn LZ. (2008). Reflecting on 25 years with MYC. Nat Rev Cancer 8: 976-990.
25. Morita S, Kojima T, Kitamura T. (2000). Plat-E: an efficient and stable system for transient packaging of retroviruses. Gene Ther 7: 1063-1066. (Pubitemid 30398356)
26. Morse III HC, Anver MR, Fredrickson TN, Haines DC, Harris AW, Harris NL et al. (2002). Bethesda proposals for classification of lymphoid neoplasms in mice. Blood 100: 246-258. (Pubitemid 35177454)
27. Mullighan CG, Phillips LA, Su X, Ma J, Miller CB, Shurtleff SA et al. (2008a). Genomic analysis of the clonal origins of relapsed acute lymphoblastic leukemia. Science 322: 1377-1380. (Pubitemid 352775249)
28. Mullighan CG, Williams RT, Downing JR, Sherr CJ. (2008b). Failure of CDKN2A/B (INK4A/B-ARF)-mediated tumor suppression and resistance to targeted therapy in acute lymphoblastic leukemia induced by BCR-ABL. Genes Dev 22: 1411-1415. (Pubitemid 351793074)
29. Park IK, Qian D, Kiel M, Becker MW, Pihalja M, Weissman IL et al. (2003). Bmi-1 is required for maintenance of adult self-renewing haematopoietic stem cells. Nature 423: 302-305. (Pubitemid 40852701)
30. Schmitt CA, Fridman JS, Yang M, Lee S, Baranov E, Hoffman RM et al. (2002). A senescence program controlled by p53 and p16INK4a contributes to the outcome of cancer therapy. Cell 109: 335-346. (Pubitemid 34606876)
31. Schmitt CA, McCurrach ME, de Stanchina E, Wallace-Brodeur RR, Lowe SW. (1999). INK4a/ARF mutations accelerate lymphomagenesis and promote chemoresistance by disabling p53. Genes Dev 13: 2670-2677. (Pubitemid 29508554)
32. Shimizu T, Ishikawa T, Sugihara E, Kuninaka S, Miyamoto T, Mabuchi Y et al. (2010). c-MYC overexpression with loss of Ink4a/Arf transforms bone marrow stromal cells into osteosarcoma accompanied by loss of adipogenesis. Oncogene 29: 5687-5699.
33. Sugihara E, Kanai M, Saito S, Nitta T, Toyoshima H, Nakayama K et al. (2006). Suppression of centrosome amplification after DNA damage depends on p27 accumulation. Cancer Res 66: 4020-4029.
34. Tsuji K, Mizumoto K, Sudo H, Kouyama K, Ogata E, Matsuoka M. (2002). p53-independent apoptosis is induced by the p19ARF tumor suppressor. Biochem Biophys Res Commun 295: 621-629. (Pubitemid 34756894)
35. Vassilev LT, Vu BT, Graves B, Carvajal D, Podlaski F, Filipovic Z et al. (2004). In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science 303: 844-848. (Pubitemid 38174664)
36. Visvader JE. (2011). Cells of origin in cancer. Nature 469: 314-322.
37. Wade M, Wang YV, Wahl GM. (2010). The p53 orchestra: Mdm2 and Mdmx set the tone. Trends Cell Biol 20: 299-309.
38. Wang PY, Young F, Chen CY, Stevens BM, Neering SJ, Rossi RM et al. (2008). The biologic properties of leukemias arising from BCR/ABL-mediated transformation vary as a function of developmental origin and activity of the p19ARF gene. Blood 112: 4184-4192.
39. Wilson A, Murphy MJ, Oskarsson T, Kaloulis K, Bettess MD, Oser GM et al. (2004). c-Myc controls the balance between hematopoietic stem cell self-renewal and differentiation. Genes Dev 18: 2747-2763. (Pubitemid 39507768)
40. Yasuda T, Sanjo H, Pages G, Kawano Y, Karasuyama H, Pouyssegur J et al. (2008). Erk kinases link pre-B cell receptor signaling to transcriptional events required for early B cell expansion. Immunity 28: 499-508.