BIM Is the Primary Mediator of MYC-Induced Apoptosis in Multiple Solid Tissues

Cell Reports

Volumn 8, Issue 5, 2014, Pages 1347-1353

  Muthalagu, Nathiya ^a   Junttila, Melissa R ^b,e   Wiese, Katrin E ^c   Wolf, Elmar ^c   Morton, Jennifer ^a   Bauer, Barbara ^c   Evan, Gerard I ^b,f   Eilers, Martin ^c   Murphy, Daniel J ^a,c,d  

^a BEATSON INSTITUTE FOR CANCER RESEARCH   (United Kingdom)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF WÜRZBURG   (Germany)

^d UNIVERSITY OF GLASGOW   (United Kingdom)

^e Genetech Corp   (United States)

^f UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ARF PROTEIN; BH3 PROTEIN; BIM PROTEIN; DOXORUBICIN; PROTEIN NOXA; PROTEIN P19; PROTEIN P53; PUMA PROTEIN; TAMOXIFEN; ANTINEOPLASTIC AGENT; APOPTOSIS REGULATORY PROTEIN; BCL-2-LIKE PROTEIN 11; CDKN2A PROTEIN, MOUSE; CYCLIN DEPENDENT KINASE INHIBITOR 2A; MEMBRANE PROTEIN; MYC PROTEIN; ONCOPROTEIN; PUMA PROTEIN, MOUSE; TUMOR SUPPRESSOR PROTEIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CARCINOGENICITY; CELL PROLIFERATION; CELLS BY BODY ANATOMY; CONTROLLED STUDY; DRUG SENSITIZATION; GENE OVEREXPRESSION; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; ONCOGENE MYC; PROTEIN FUNCTION; PROTEIN INDUCTION; ANIMAL; C57BL MOUSE; DRUG EFFECTS; GENETICS; INTESTINE; LIVER; METABOLISM; PANCREAS ISLET; PATHOLOGY;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; APOPTOSIS REGULATORY PROTEINS; CYCLIN-DEPENDENT KINASE INHIBITOR P16; DOXORUBICIN; INTESTINES; ISLETS OF LANGERHANS; LIVER; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-MYC; TUMOR SUPPRESSOR PROTEINS;

EID: 84922519100     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.07.057     Document Type: Article

References (47)

1. Askew D.S., Ashmun R.A., Simmons B.C., Cleveland J.L. Constitutive c-myc expression in an IL-3-dependent myeloid cell line suppresses cell cycle arrest and accelerates apoptosis. Oncogene 1991, 6:1915-1922.
2. Bissonnette R.P., Echeverri F., Mahboubi A., Green D.R. Apoptotic cell death induced by c-myc is inhibited by bcl-2. Nature 1992, 359:552-554.
3. Blyth K., Stewart M., Bell M., James C., Evan G., Neil J.C., Cameron E.R. Sensitivity to myc-induced apoptosis is retained in spontaneous and transplanted lymphomas of CD2-mycER mice. Oncogene 2000, 19:773-782.
4. Bouillet P., Metcalf D., Huang D.C., Tarlinton D.M., Kay T.W., Köntgen F., Adams J.M., Strasser A. Proapoptotic Bcl-2 relative Bim required for certain apoptotic responses, leukocyte homeostasis, and to preclude autoimmunity. Science 1999, 286:1735-1738.
5. Campone M., Noël B., Couriaud C., Grau M., Guillemin Y., Gautier F., Gouraud W., Charbonnel C., Campion L., Jézéquel P., et al. c-Myc dependent expression of pro-apoptotic Bim renders HER2-overexpressing breast cancer cells dependent on anti-apoptotic Mcl-1. Mol. Cancer 2011, 10:110.
6. Czabotar P.E., Lessene G., Strasser A., Adams J.M. Control of apoptosis by the BCL-2 protein family: implications for physiology and therapy. Nat. Rev. Mol. Cell Biol. 2014, 15:49-63.
7. Dansen T.B., Whitfield J., Rostker F., Brown-Swigart L., Evan G.I. Specific requirement for Bax, not Bak, in Myc-induced apoptosis and tumor suppression invivo. J.Biol. Chem. 2006, 281:10890-10895.
8. Egle A., Harris A.W., Bouillet P., Cory S. Bim is a suppressor of Myc-induced mouse B cell leukemia. Proc. Natl. Acad. Sci. USA 2004, 101:6164-6169.
9. Eischen C.M., Weber J.D., Roussel M.F., Sherr C.J., Cleveland J.L. Disruption of the ARF-Mdm2-p53 tumor suppressor pathway in Myc-induced lymphomagenesis. Genes Dev. 1999, 13:2658-2669.
10. Eischen C.M., Woo D., Roussel M.F., Cleveland J.L. Apoptosis triggered by Myc-induced suppression of Bcl-X(L) or Bcl-2 is bypassed during lymphomagenesis. Mol. Cell. Biol. 2001, 21:5063-5070.
11. Evan G.I., Wyllie A.H., Gilbert C.S., Littlewood T.D., Land H., Brooks M., Waters C.M., Penn L.Z., Hancock D.C. Induction of apoptosis in fibroblasts by c-myc protein. Cell 1992, 69:119-128.
12. Evan G.I., Christophorou M., Lawlor E.A., Ringshausen I., Prescott J., Dansen T., Finch A., Martins C., Murphy D. Oncogene-dependent tumor suppression: using the dark side of the force for cancer therapy. Cold Spring Harb. Symp. Quant. Biol. 2005, 70:263-273.
13. Fanidi A., Harrington E.A., Evan G.I. Cooperative interaction between c-myc and bcl-2 proto-oncogenes. Nature 1992, 359:554-556.
14. Finch A., Prescott J., Shchors K., Hunt A., Soucek L., Dansen T.B., Swigart L.B., Evan G.I. Bcl-xL gain of function and p19 ARF loss of function cooperate oncogenically with Myc invivo by distinct mechanisms. Cancer Cell 2006, 10:113-120.
15. Goga A., Yang D., Tward A.D., Morgan D.O., Bishop J.M. Inhibition of CDK1 as a potential therapy for tumors over-expressing MYC. Nat. Med. 2007, 13:820-827.
16. Hemann M.T., Bric A., Teruya-Feldstein J., Herbst A., Nilsson J.A., Cordon-Cardo C., Cleveland J.L., Tansey W.P., Lowe S.W. Evasion of the p53 tumour surveillance network by tumour-derived MYC mutants. Nature 2005, 436:807-811.
17. Hsu B., Marin M.C., el-Naggar A.K., Stephens L.C., Brisbay S., McDonnell T.J. Evidence that c-myc mediated apoptosis does not require wild-type p53 during lymphomagenesis. Oncogene 1995, 11:175-179.
18. Hueber A.O., Zörnig M., Lyon D., Suda T., Nagata S., Evan G.I. Requirement for the CD95 receptor-ligand pathway in c-Myc-induced apoptosis. Science 1997, 278:1305-1309.
19. Juin P., Hueber A.O., Littlewood T., Evan G. c-Myc-induced sensitization to apoptosis is mediated through cytochrome c release. Genes Dev. 1999, 13:1367-1381.
20. Juin P., Hunt A., Littlewood T., Griffiths B., Swigart L.B., Korsmeyer S., Evan G. c-Myc functionally cooperates with Bax to induce apoptosis. Mol. Cell. Biol. 2002, 22:6158-6169.
21. Kamijo T., Weber J.D., Zambetti G., Zindy F., Roussel M.F., Sherr C.J. Functional and physical interactions of the ARF tumor suppressor with p53 and Mdm2. Proc. Natl. Acad. Sci. USA 1998, 95:8292-8297.
22. Kelly P.N., Grabow S., Delbridge A.R., Adams J.M., Strasser A. Prophylactic treatment with the BH3 mimetic ABT-737 impedes Myc-driven lymphomagenesis in mice. Cell Death Differ. 2013, 20:57-63.
23. Kelly G.L., Grabow S., Glaser S.P., Fitzsimmons L., Aubrey B.J., Okamoto T., Valente L.J., Robati M., Tai L., Fairlie W.D., et al. Targeting of MCL-1 kills MYC-driven mouse and human lymphomas even when they bear mutations in p53. Genes Dev. 2014, 28:58-70.
24. Kemp C.J., Grandori C. Functional genomics to identify unforeseen cancer drug targets. Future Oncol. 2013, 9:473-476.
25. Lee Y.Y., Moujalled D., Doerflinger M., Gangoda L., Weston R., Rahimi A., de Alboran I., Herold M., Bouillet P., Xu Q., et al. CREB-binding protein (CBP) regulates β-adrenoceptor (β-AR)-mediated apoptosis. Cell Death Differ. 2013, 20:941-952.
26. Li T., Kon N., Jiang L., Tan M., Ludwig T., Zhao Y., Baer R., Gu W. Tumor suppression in the absence of p53-mediated cell-cycle arrest, apoptosis, and senescence. Cell 2012, 149:1269-1283.
27. Liu L., Ulbrich J., Müller J., Wüstefeld T., Aeberhard L., Kress T.R., Muthalagu N., Rycak L., Rudalska R., Moll R., et al. Deregulated MYC expression induces dependence upon AMPK-related kinase 5. Nature 2012, 483:608-612.
28. Llambi F., Moldoveanu T., Tait S.W., Bouchier-Hayes L., Temirov J., McCormick L.L., Dillon C.P., Green D.R. A unified model of mammalian BCL-2 protein family interactions at the mitochondria. Mol. Cell 2011, 44:517-531.
29. Maclean K.H., Keller U.B., Rodriguez-Galindo C., Nilsson J.A., Cleveland J.L. c-Myc augments gamma irradiation-induced apoptosis by suppressing Bcl-XL. Mol. Cell. Biol. 2003, 23:7256-7270.
30. Michalak E.M., Jansen E.S., Happo L., Cragg M.S., Tai L., Smyth G.K., Strasser A., Adams J.M., Scott C.L. Puma and to a lesser extent Noxa are suppressors of Myc-induced lymphomagenesis. Cell Death Differ. 2009, 16:684-696.
31. Morton J.P., Timpson P., Karim S.A., Ridgway R.A., Athineos D., Doyle B., Jamieson N.B., Oien K.A., Lowy A.M., Brunton V.G., et al. Mutant p53 drives metastasis and overcomes growth arrest/senescence in pancreatic cancer. Proc. Natl. Acad. Sci. USA 2010, 107:246-251.
32. Murphy D.J., Junttila M.R., Pouyet L., Karnezis A., Shchors K., Bui D.A., Brown-Swigart L., Johnson L., Evan G.I. Distinct thresholds govern Myc's biological output invivo. Cancer Cell 2008, 14:447-457.
33. Nakano K., Vousden K.H. PUMA, a novel proapoptotic gene, is induced by p53. Mol. Cell 2001, 7:683-694.
34. Ni Chonghaile T., Sarosiek K.A., Vo T.T., Ryan J.A., Tammareddi A., Moore Vdel.G., Deng J., Anderson K.C., Richardson P., Tai Y.T., et al. Pretreatment mitochondrial priming correlates with clinical response to cytotoxic chemotherapy. Science 2011, 334:1129-1133.
35. Pelengaris S., Khan M., Evan G.I. Suppression of Myc-induced apoptosis in beta cells exposes multiple oncogenic properties of Myc and triggers carcinogenic progression. Cell 2002, 109:321-334.
36. Popov N., Schülein C., Jaenicke L.A., Eilers M. Ubiquitylation of the amino terminus of Myc by SCF(β-TrCP) antagonizes SCF(Fbw7)-mediated turnover. Nat. Cell Biol. 2010, 12:973-981.
37. Sarosiek K.A., Chi X., Bachman J.A., Sims J.J., Montero J., Patel L., Flanagan A., Andrews D.W., Sorger P., Letai A. BID preferentially activates BAK while BIM preferentially activates BAX, affecting chemotherapy response. Mol. Cell 2013, 51:751-765.
38. Sarosiek K.A., Ni Chonghaile T., Letai A. Mitochondria: gatekeepers of response to chemotherapy. Trends Cell Biol. 2013, 23:612-619.
39. Schmitt C.A., McCurrach M.E., de Stanchina E., Wallace-Brodeur R.R., Lowe S.W. INK4a/ARF mutations accelerate lymphomagenesis and promote chemoresistance by disabling p53. Genes Dev. 1999, 13:2670-2677.
40. Soucek L., Whitfield J., Martins C.P., Finch A.J., Murphy D.J., Sodir N.M., Karnezis A.N., Swigart L.B., Nasi S., Evan G.I. Modelling Myc inhibition as a cancer therapy. Nature 2008, 455:679-683.
41. Stott F.J., Bates S., James M.C., McConnell B.B., Starborg M., Brookes S., Palmero I., Ryan K., Hara E., Vousden K.H., Peters G. The alternative product from the human CDKN2A locus, p14(ARF), participates in a regulatory feedback loop with p53 and MDM2. EMBO J. 1998, 17:5001-5014.
42. Strasser A., Harris A.W., Bath M.L., Cory S. Novel primitive lymphoid tumours induced in transgenic mice by cooperation between myc and bcl-2. Nature 1990, 348:331-333.
43. Villunger A., Michalak E.M., Coultas L., Müllauer F., Böck G., Ausserlechner M.J., Adams J.M., Strasser A. p53- and drug-induced apoptotic responses mediated by BH3-only proteins puma and noxa. Science 2003, 302:1036-1038.
44. Yu J., Wang Z., Kinzler K.W., Vogelstein B., Zhang L. PUMA mediates the apoptotic response to p53 in colorectal cancer cells. Proc. Natl. Acad. Sci. USA 2003, 100:1931-1936.
45. Zindy F., Eischen C.M., Randle D.H., Kamijo T., Cleveland J.L., Sherr C.J., Roussel M.F. Myc signaling via the ARF tumor suppressor regulates p53-dependent apoptosis and immortalization. Genes Dev. 1998, 12:2424-2433.
46. Zindy F., Williams R.T., Baudino T.A., Rehg J.E., Skapek S.X., Cleveland J.L., Roussel M.F., Sherr C.J. Arf tumor suppressor promoter monitors latent oncogenic signals invivo. Proc. Natl. Acad. Sci. USA 2003, 100:15930-15935.
47. Zuber J., Shi J., Wang E., Rappaport A.R., Herrmann H., Sison E.A., Magoon D., Qi J., Blatt K., Wunderlich M., et al. RNAi screen identifies Brd4 as a therapeutic target in acute myeloid leukaemia. Nature 2011, 478:524-528.