Regulation of c-Myc ubiquitination controls chronic myelogenous leukemia initiation and progression

Cancer Cell

Volumn 23, Issue 3, 2013, Pages 362-375

  Reavie, Linsey ^a   Buckley, Shannon M ^a   Loizou, Evangelia ^a   Takeishi, Shoichiro ^b   Aranda Orgilles, Beatriz ^a   Ndiaye Lobry, Delphine ^a   Abdel Wahab, Omar ^c   Ibrahim, Sherif ^a   Nakayama, Keiichi I ^b   Aifantis, Iannis ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b KYUSHU UNIVERSITY   (Japan)

^c MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN P53; UBIQUITIN PROTEIN LIGASE;

APOPTOSIS; ARTICLE; CANCER GROWTH; CHRONIC MYELOID LEUKEMIA; DISEASE COURSE; HUMAN; HUMAN CELL; MOLECULAR MECHANICS; ONCOGENE C MYC; PRIORITY JOURNAL; PROTEIN EXPRESSION; UBIQUITINATION;

EID: 84876434253     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccr.2013.01.025     Document Type: Article

References (56)

1. Aghajan M., Jonai N., Flick K., Fu F., Luo M., Cai X., Ouni I., Pierce N., Tang X., Lomenick B., et al. Chemical genetics screen for enhancers of rapamycin identifies a specific inhibitor of an SCF family E3 ubiquitin ligase. Nat. Biotechnol. 2010, 28:738-742.
2. Bartram C.R., de Klein A., Hagemeijer A., van Agthoven T., Geurts van Kessel A., Bootsma D., Grosveld G., Ferguson-Smith M.A., Davies T., Stone M., et al. Translocation of c-ab1 oncogene correlates with the presence of a Philadelphia chromosome in chronic myelocytic leukaemia. Nature 1983, 306:277-280.
3. Bhatia R., Holtz M., Niu N., Gray R., Snyder D.S., Sawyers C.L., Arber D.A., Slovak M.L., Forman S.J. Persistence of malignant hematopoietic progenitors in chronic myelogenous leukemia patients in complete cytogenetic remission following imatinib mesylate treatment. Blood 2003, 101:4701-4707.
4. Bonnet D., Dick J.E. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat. Med. 1997, 3:730-737.
5. Bric A., Miething C., Bialucha C.U., Scuoppo C., Zender L., Krasnitz A., Xuan Z., Zuber J., Wigler M., Hicks J., et al. Functional identification of tumor-suppressor genes through an in vivo RNA interference screen in a mouse lymphoma model. Cancer Cell 2009, 16:324-335.
6. Cleveland J.L., Dean M., Rosenberg N., Wang J.Y., Rapp U.R. Tyrosine kinase oncogenes abrogate interleukin-3 dependence of murine myeloid cells through signaling pathways involving c-myc: conditional regulation of c-myc transcription by temperature-sensitive v-abl. Mol. Cell. Biol. 1989, 9:5685-5695.
7. Corbin A.S., Agarwal A., Loriaux M., Cortes J., Deininger M.W., Druker B.J. Human chronic myeloid leukemia stem cells are insensitive to imatinib despite inhibition of BCR-ABL activity. J. Clin. Invest. 2011, 121:396-409.
8. Daley G.Q., Van Etten R.A., Baltimore D. Induction of chronic myelogenous leukemia in mice by the P210bcr/abl gene of the Philadelphia chromosome. Science 1990, 247:824-830.
9. de Alboran I.M., O'Hagan R.C., Gärtner F., Malynn B., Davidson L., Rickert R., Rajewsky K., DePinho R.A., Alt F.W. Analysis of C-MYC function in normal cells via conditional gene-targeted mutation. Immunity 2001, 14:45-55.
10. de Lavallade H., Apperley J.F., Khorashad J.S., Milojkovic D., Reid A.G., Bua M., Szydlo R., Olavarria E., Kaeda J., Goldman J.M., Marin D. Imatinib for newly diagnosed patients with chronic myeloid leukemia: incidence of sustained responses in an intention-to-treat analysis. J. Clin. Oncol. 2008, 26:3358-3363.
11. Delmore J.E., Issa G.C., Lemieux M.E., Rahl P.B., Shi J., Jacobs H.M., Kastritis E., Gilpatrick T., Paranal R.M., Qi J., et al. BET bromodomain inhibition as a therapeutic strategy to target c-Myc. Cell 2011, 146:904-917.
12. Druker B.J., Guilhot F., O'Brien S.G., Gathmann I., Kantarjian H., Gattermann N., Deininger M.W., Silver R.T., Goldman J.M., Stone R.M., et al. Five-year follow-up of patients receiving imatinib for chronic myeloid leukemia. N. Engl. J. Med. 2006, 355:2408-2417. IRIS Investigators.
13. Gorre M.E., Mohammed M., Ellwood K., Hsu N., Paquette R., Rao P.N., Sawyers C.L. Clinical resistance to STI-571 cancer therapy caused by BCR-ABL gene mutation or amplification. Science 2001, 293:876-880.
14. Gregory M.A., Qi Y., Hann S.R. Phosphorylation by glycogen synthase kinase-3 controls c-myc proteolysis and subnuclear localization. J. Biol. Chem. 2003, 278:51606-51612.
15. Gupta-Rossi N., Le Bail O., Gonen H., Brou C., Logeat F., Six E., Ciechanover A., Israël A. Functional interaction between SEL-10, an F-box protein, and the nuclear form of activated Notch1 receptor. J. Biol. Chem. 2001, 276:34371-34378.
16. Heidel F.H., Bullinger L., Feng Z., Wang Z., Neff T.A., Stein L., Kalaitzidis D., Lane S.W., Armstrong S.A. Genetic and pharmacologic inhibition of β-catenin targets imatinib-resistant leukemia stem cells in CML. Cell Stem Cell 2012, 10:412-424.
17. Heisterkamp N., Jenster G., ten Hoeve J., Zovich D., Pattengale P.K., Groffen J. Acute leukaemia in bcr/abl transgenic mice. Nature 1990, 344:251-253.
18. Hochhaus A., O'Brien S.G., Guilhot F., Druker B.J., Branford S., Foroni L., Goldman J.M., Müller M.C., Radich J.P., Rudoltz M., et al. Six-year follow-up of patients receiving imatinib for the first-line treatment of chronic myeloid leukemia. Leukemia 2009, 23:1054-1061. IRIS Investigators.
19. Huang C.Y., Bredemeyer A.L., Walker L.M., Bassing C.H., Sleckman B.P. Dynamic regulation of c-Myc proto-oncogene expression during lymphocyte development revealed by a GFP-c-Myc knock-in mouse. Eur. J. Immunol. 2008, 38:342-349.
20. Huntly B.J., Gilliland D.G. Leukaemia stem cells and the evolution of cancer-stem-cell research. Nat. Rev. Cancer 2005, 5:311-321.
21. Ito T., Kwon H.Y., Zimdahl B., Congdon K.L., Blum J., Lento W.E., Zhao C., Lagoo A., Gerrard G., Foroni L., et al. Regulation of myeloid leukaemia by the cell-fate determinant Musashi. Nature 2010, 466:765-768.
22. Jamieson C.H., Ailles L.E., Dylla S.J., Muijtjens M., Jones C., Zehnder J.L., Gotlib J., Li K., Manz M.G., Keating A., et al. Granulocyte-macrophage progenitors as candidate leukemic stem cells in blast-crisis CML. N. Engl. J. Med. 2004, 351:657-667.
23. Jankowska A.M., Szpurka H., Tiu R.V., Makishima H., Afable M., Huh J., O'Keefe C.L., Ganetzky R., McDevitt M.A., Maciejewski J.P. Loss of heterozygosity 4q24 and TET2 mutations associated with myelodysplastic/myeloproliferative neoplasms. Blood 2009, 113:6403-6410.
24. Kelman Z., Prokocimer M., Peller S., Kahn Y., Rechavi G., Manor Y., Cohen A., Rotter V. Rearrangements in the p53 gene in Philadelphia chromosome positive chronic myelogenous leukemia. Blood 1989, 74:2318-2324.
25. Koepp D.M., Schaefer L.K., Ye X., Keyomarsi K., Chu C., Harper J.W., Elledge S.J. Phosphorylation-dependent ubiquitination of cyclin E by the SCFFbw7 ubiquitin ligase. Science 2001, 294:173-177.
26. Lapidot T., Sirard C., Vormoor J., Murdoch B., Hoang T., Caceres-Cortes J., Minden M., Paterson B., Caligiuri M.A., Dick J.E. A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 1994, 367:645-648.
27. le Coutre P., Tassi E., Varella-Garcia M., Barni R., Mologni L., Cabrita G., Marchesi E., Supino R., Gambacorti-Passerini C. Induction of resistance to the Abelson inhibitor STI571 in human leukemic cells through gene amplification. Blood 2000, 95:1758-1766.
28. Martinez A., Gil C., Perez D.I. Glycogen synthase kinase 3 inhibitors in the next horizon for Alzheimer's disease treatment. Int. J. Alzheimers Dis. 2011, 2011:280502.
29. Matsuoka S., Oike Y., Onoyama I., Iwama A., Arai F., Takubo K., Mashimo Y., Oguro H., Nitta E., Ito K., et al. Fbxw7 acts as a critical fail-safe against premature loss of hematopoietic stem cells and development of T-ALL. Genes Dev. 2008, 22:986-991.
30. Michor F., Hughes T.P., Iwasa Y., Branford S., Shah N.P., Sawyers C.L., Nowak M.A. Dynamics of chronic myeloid leukaemia. Nature 2005, 435:1267-1270.
31. Nakamura S., Yokota D., Tan L., Nagata Y., Takemura T., Hirano I., Shigeno K., Shibata K., Fujisawa S., Ohnishi K. Down-regulation of Thanatos-associated protein 11 by BCR-ABL promotes CML cell proliferation through c-Myc expression. Int. J. Cancer. 2012, 130:1046-1059.
32. Neering S.J., Bushnell T., Sozer S., Ashton J., Rossi R.M., Wang P.Y., Bell D.R., Heinrich D., Bottaro A., Jordan C.T. Leukemia stem cells in a genetically defined murine model of blast-crisis CML. Blood 2007, 110:2578-2585.
33. Nowell P.C., Hungerford D.A. Chromosome studies on normal and leukemic human leukocytes. J. Natl. Cancer Inst. 1960, 25:85-109.
34. O'Hare T., Corbin A.S., Druker B.J. Targeted CML therapy: controlling drug resistance, seeking cure. Curr. Opin. Genet. Dev. 2006, 16:92-99.
35. O'Neil J., Grim J., Strack P., Rao S., Tibbitts D., Winter C., Hardwick J., Welcker M., Meijerink J.P., Pieters R., et al. FBW7 mutations in leukemic cells mediate NOTCH pathway activation and resistance to gamma-secretase inhibitors. J. Exp. Med. 2007, 204:1813-1824.
36. Orlicky S., Tang X., Neduva V., Elowe N., Brown E.D., Sicheri F., Tyers M. An allosteric inhibitor of substrate recognition by the SCF(Cdc4) ubiquitin ligase. Nat. Biotechnol. 2010, 28:733-737.
37. Pear W.S., Miller J.P., Xu L., Pui J.C., Soffer B., Quackenbush R.C., Pendergast A.M., Bronson R., Aster J.C., Scott M.L., Baltimore D. Efficient and rapid induction of a chronic myelogenous leukemia-like myeloproliferative disease in mice receiving P210 bcr/abl-transduced bone marrow. Blood 1998, 92:3780-3792.
38. Reavie L., Della Gatta G., Crusio K., Aranda-Orgilles B., Buckley S.M., Thompson B., Lee E., Gao J., Bredemeyer A.L., Helmink B.A., et al. Regulation of hematopoietic stem cell differentiation by a single ubiquitin ligase-substrate complex. Nat. Immunol. 2010, 11:207-215.
39. Reynaud D., Pietras E., Barry-Holson K., Mir A., Binnewies M., Jeanne M., Sala-Torra O., Radich J.P., Passegué E. IL-6 controls leukemic multipotent progenitor cell fate and contributes to chronic myelogenous leukemia development. Cancer Cell 2011, 20:661-673.
40. Rowley J.D. Letter: A new consistent chromosomal abnormality in chronic myelogenous leukaemia identified by quinacrine fluorescence and Giemsa staining. Nature 1973, 243:290-293.
41. Sawyers C.L., Callahan W., Witte O.N. Dominant negative MYC blocks transformation by ABL oncogenes. Cell 1992, 70:901-910.
42. Shah N.P., Nicoll J.M., Nagar B., Gorre M.E., Paquette R.L., Kuriyan J., Sawyers C.L. Multiple BCR-ABL kinase domain mutations confer polyclonal resistance to the tyrosine kinase inhibitor imatinib (STI571) in chronic phase and blast crisis chronic myeloid leukemia. Cancer Cell 2002, 2:117-125.
43. Sirard C., Lapidot T., Vormoor J., Cashman J.D., Doedens M., Murdoch B., Jamal N., Messner H., Addey L., Minden M., et al. Normal and leukemic SCID-repopulating cells (SRC) coexist in the bone marrow and peripheral blood from CML patients in chronic phase, whereas leukemic SRC are detected in blast crisis. Blood 1996, 87:1539-1548.
44. Stadtfeld M., Graf T. Assessing the role of hematopoietic plasticity for endothelial and hepatocyte development by non-invasive lineage tracing. Development 2005, 132:203-213.
45. Takeishi S., Matsumoto A., Onoyama I., Naka K., Hirao A., Nakayama K.I. Ablation of Fbw7 eliminates leukemia-intiating cells by preventing quiescence. Cancer Cell 2013, 23:347-361. this issue.
46. Thompson B.J., Buonamici S., Sulis M.L., Palomero T., Vilimas T., Basso G., Ferrando A., Aifantis I. The SCFFBW7 ubiquitin ligase complex as a tumor suppressor in T cell leukemia. J. Exp. Med. 2007, 204:1825-1835.
47. Thompson B.J., Jankovic V., Gao J., Buonamici S., Vest A., Lee J.M., Zavadil J., Nimer S.D., Aifantis I. Control of hematopoietic stem cell quiescence by the E3 ubiquitin ligase Fbw7. J. Exp. Med. 2008, 205:1395-1408.
48. Wang J.C., Lapidot T., Cashman J.D., Doedens M., Addy L., Sutherland D.R., Nayar R., Laraya P., Minden M., Keating A., et al. High level engraftment of NOD/SCID mice by primitive normal and leukemic hematopoietic cells from patients with chronic myeloid leukemia in chronic phase. Blood 1998, 91:2406-2414.
49. Wang Z., Smith K.S., Murphy M., Piloto O., Somervaille T.C., Cleary M.L. Glycogen synthase kinase 3 in MLL leukaemia maintenance and targeted therapy. Nature 2008, 455:1205-1209.
50. Welcker M., Orian A., Jin J., Grim J.E., Harper J.W., Eisenman R.N., Clurman B.E. The Fbw7 tumor suppressor regulates glycogen synthase kinase 3 phosphorylation-dependent c-Myc protein degradation. Proc. Natl. Acad. Sci. USA 2004, 101:9085-9090.
51. Wendel H.G., de Stanchina E., Cepero E., Ray S., Emig M., Fridman J.S., Veach D.R., Bornmann W.G., Clarkson B., McCombie W.R., et al. Loss of p53 impedes the antileukemic response to BCR-ABL inhibition. Proc. Natl. Acad. Sci. USA 2006, 103:7444-7449.
52. Wertheim J.A., Forsythe K., Druker B.J., Hammer D., Boettiger D., Pear W.S. BCR-ABL-induced adhesion defects are tyrosine kinase-independent. Blood 2002, 99:4122-4130.
53. Xie S., Lin H., Sun T., Arlinghaus R.B. Jak2 is involved in c-Myc induction by Bcr-Abl. Oncogene 2002, 21:7137-7146.
54. Yada M., Hatakeyama S., Kamura T., Nishiyama M., Tsunematsu R., Imaki H., Ishida N., Okumura F., Nakayama K., Nakayama K.I. Phosphorylation-dependent degradation of c-Myc is mediated by the F-box protein Fbw7. EMBO J. 2004, 23:2116-2125.
55. Zhao C., Blum J., Chen A., Kwon H.Y., Jung S.H., Cook J.M., Lagoo A., Reya T. Loss of beta-catenin impairs the renewal of normal and CML stem cells in vivo. Cancer Cell 2007, 12:528-541.
56. Zhao C., Chen A., Jamieson C.H., Fereshteh M., Abrahamsson A., Blum J., Kwon H.Y., Kim J., Chute J.P., Rizzieri D., et al. Hedgehog signalling is essential for maintenance of cancer stem cells in myeloid leukaemia. Nature 2009, 458:776-779.