Targeting Mcl-1 for multiple myeloma (MM) therapy: Drug-induced generation of Mcl-1 fragment Mcl-1128-350 triggers MM cell death via c-Jun upregulation

Cancer Letters

Volumn 343, Issue 2, 2014, Pages 286-294

  Fan, Fengjuan ^a   Tonon, Giovanni ^b   Bashari, Muhammad Hasan ^a   Vallet, Sonia ^a   Antonini, Elena ^b   Goldschmidt, Hartmut ^d   Schulze Bergkamen, Henning ^a   Opferman, Joseph T ^e   Sattler, Martin ^c   Anderson, Kenneth C ^c   Jäger, Dirk ^a   Podar, Klaus ^a  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b SAN RAFFAELE HOSPITAL   (Italy)

^c HARVARD MEDICAL SCHOOL   (United States)

^d UNIVERSITY OF HEIDELBERG   (Germany)

^e ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

Apoptosis; C Jun; Glioblastoma; Mcl 1; MEFs; Multiple myeloma

Indexed keywords

ADAPHOSTIN; ALANINE; ASPARTIC ACID; BORTEZOMIB; CARFILZOMIB; CASPASE; IXAZOMIB CITRATE; MESSENGER RNA; PROTEIN AP 1; PROTEIN C JUN; PROTEIN MCL 1; STAUROSPORINE; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; DOWNSTREAM PROCESSING; DRUG TARGETING; EMBRYO; ENZYME METABOLISM; FIBROBLAST; HUMAN; HUMAN CELL; MOUSE; MULTIPLE MYELOMA; NONHUMAN; POINT MUTATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS INHIBITION; UPREGULATION;

MURINAE;

APOPTOSIS; C-JUN; GLIOBLASTOMA; MCL-1; MEFS; MULTIPLE MYELOMA;

ANIMALS; ANTINEOPLASTIC AGENTS; APOPTOSIS; CELL LINE, TUMOR; DRUG DELIVERY SYSTEMS; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; MICE; MULTIPLE MYELOMA; MYELOID CELL LEUKEMIA SEQUENCE 1 PROTEIN; OLIGOPEPTIDES; PEPTIDE FRAGMENTS; PROTO-ONCOGENE PROTEINS C-JUN; REAL-TIME POLYMERASE CHAIN REACTION; UP-REGULATION;

EID: 84891827277     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2013.09.042     Document Type: Article

References (48)

1. Perciavalle R.M., Opferman J.T. Delving deeper: MCL-1's contributions to normal and cancer biology. Trends Cell Biol. 2013, 23:22-29.
2. Kozopas K.M., Yang T., Buchan H.L., Zhou P., Craig R.W. MCL1, a gene expressed in programmed myeloid cell differentiation, has sequence similarity to BCL2. Proc. Natl. Acad. Sci. USA 1993, 90:3516-3520.
3. Opferman J.T., Iwasaki H., Ong C.C., Suh H., Mizuno S., Akashi K., Korsmeyer S.J. Obligate role of anti-apoptotic MCL-1 in the survival of hematopoietic stem cells. Science 2005, 307:1101-1104.
4. Opferman J.T., Letai A., Beard C., Sorcinelli M.D., Ong C.C., Korsmeyer S.J. Development and maintenance of B and T lymphocytes requires antiapoptotic MCL-1. Nature 2003, 426:671-676.
5. Peperzak V., Vikstrom I., Walker J., Glaser S.P., LePage M., Coquery C.M., Erickson L.D., Fairfax K., Mackay F., Strasser A., Nutt S.L., Tarlinton D.M. Mcl-1 is essential for the survival of plasma cells. Nat. Immunol. 2013, 14:290-297.
6. Thomas L.W., Lam C., Edwards S.W. Mcl-1; the molecular regulation of protein function. FEBS Lett. 2010, 584:2981-2989.
7. Clohessy J.G., Zhuang J., Brady H.J. Characterisation of Mcl-1 cleavage during apoptosis of haematopoietic cells. Br. J. Haematol. 2004, 125:655-665.
8. Han J., Goldstein L.A., Gastman B.R., Froelich C.J., Yin X.M., Rabinowich H. Degradation of Mcl-1 by granzyme B: implications for Bim-mediated mitochondrial apoptotic events. J. Biol. Chem. 2004, 279:22020-22029.
9. Herrant M., Jacquel A., Marchetti S., Belhacene N., Colosetti P., Luciano F., Auberger P. Cleavage of Mcl-1 by caspases impaired its ability to counteract Bim-induced apoptosis. Oncogene 2004, 23:7863-7873.
10. Michels J., O'Neill J.W., Dallman C.L., Mouzakiti A., Habens F., Brimmell M., Zhang K.Y., Craig R.W., Marcusson E.G., Johnson P.W., Packham G. Mcl-1 is required for Akata6 B-lymphoma cell survival and is converted to a cell death molecule by efficient caspase-mediated cleavage. Oncogene 2004, 23:4818-4827.
11. Podar K., Gouill S.L., Zhang J., Opferman J.T., Zorn E., Tai Y.T., Hideshima T., Amiot M., Chauhan D., Harousseau J.L., Anderson K.C. A pivotal role for Mcl-1 in Bortezomib-induced apoptosis. Oncogene 2008, 27:721-731.
12. Quinn B.A., Dash R., Azab B., Sarkar S., Das S.K., Kumar S., Oyesanya R.A., Dasgupta S., Dent P., Grant S., Rahmani M., Curiel D.T., Dmitriev I., Hedvat M., Wei J., Wu B., Stebbins J.L., Reed J.C., Pellecchia M., Sarkar D., Fisher P.B. Targeting Mcl-1 for the therapy of cancer. Expert Opin. Investig. Drugs 2011, 20:1397-1411.
13. Puthier D., Bataille R., Amiot M. IL-6 up-regulates mcl-1 in human myeloma cells through JAK/STAT rather than ras/MAP kinase pathway. Eur. J. Immunol. 1999, 29:3945-3950.
14. Derenne S., Monia B., Dean N.M., Taylor J.K., Rapp M.J., Harousseau J.L., Bataille R., Amiot M. Antisense strategy shows that Mcl-1 rather than Bcl-2 or Bcl-x(L) is an essential survival protein of human myeloma cells. Blood 2002, 100:194-199.
15. Jourdan M., Veyrune J.L., De Vos J., Redal N., Couderc G., Klein B. A major role for Mcl-1 antiapoptotic protein in the IL-6-induced survival of human myeloma cells. Oncogene 2003, 22:2950-2959.
16. Le Gouill S., Podar K., Amiot M., Hideshima T., Chauhan D., Ishitsuka K., Kumar S., Raje N., Richardson P.G., Harousseau J.L., Anderson K.C. VEGF induces Mcl-1 up-regulation and protects multiple myeloma cells against apoptosis. Blood 2004, 104:2886-2892.
17. Wuilleme-Toumi S., Robillard N., Gomez P., Moreau P., Le Gouill S., Avet-Loiseau H., Harousseau J.L., Amiot M., Bataille R. Mcl-1 is overexpressed in multiple myeloma and associated with relapse and shorter survival. Leukemia 2005, 19:1248-1252.
18. Munshi N.C., Hideshima T., Carrasco D., Shammas M., Auclair D., Davies F., Mitsiades N., Mitsiades C., Kim R.S., Li C., Rajkumar S.V., Fonseca R., Bergsagel L., Chauhan D., Anderson K.C. Identification of genes modulated in multiple myeloma using genetically identical twin samples. Blood 2004, 103:1799-1806.
19. Le Gouill S., Podar K., Harousseau J.L., Anderson K.C. Mcl-1 regulation and its role in multiple myeloma. Cell Cycle 2004, 3:1259-1262.
20. Gomez-Bougie P., Menoret E., Juin P., Dousset C., Pellat-Deceunynck C., Amiot M. Noxa controls Mule-dependent Mcl-1 ubiquitination through the regulation of the Mcl-1/USP9X interaction. Biochem. Biophys. Res. Commun. 2011, 413:460-464.
21. Trudel S., Li Z.H., Rauw J., Tiedemann R.E., Wen X.Y., Stewart A.K. Preclinical studies of the pan-Bcl inhibitor obatoclax (GX015-070) in multiple myeloma. Blood 2007, 109:5430-5438.
22. Streetly M.J., Maharaj L., Joel S., Schey S.A., Gribben J.G., Cotter F.E. GCS-100, a novel galectin-3 antagonist, modulates MCL-1, NOXA, and cell cycle to induce myeloma cell death. Blood 2010, 115:3939-3948.
23. Mott J.L., Kobayashi S., Bronk S.F., Gores G.J. Mir-29 regulates Mcl-1 protein expression and apoptosis. Oncogene 2007, 26:6133-6140.
24. Zhang Y.K., Wang H., Leng Y., Li Z.L., Yang Y.F., Xiao F.J., Li Q.F., Chen X.Q., Wang L.S. Overexpression of microRNA-29b induces apoptosis of multiple myeloma cells through down regulating Mcl-1. Biochem. Biophys. Res. Commun. 2011, 414:233-239.
25. Gomez-Bougie P., Wuilleme-Toumi S., Menoret E., Trichet V., Robillard N., Philippe M., Bataille R., Amiot M. Noxa up-regulation and Mcl-1 cleavage are associated to apoptosis induction by bortezomib in multiple myeloma. Cancer Res. 2007, 67:5418-5424.
26. Menoret E., Gomez-Bougie P., Surget S., Trichet V., Oliver L., Pellat-Deceunynck C., Amiot M. Mcl-1(128-350) fragment induces apoptosis through direct interaction with Bax. FEBS Lett. 2010, 584:487-492.
27. Morel C., Carlson S.M., White F.M., Davis R.J. Mcl-1 integrates the opposing actions of signaling pathways that mediate survival and apoptosis. Mol. Cell. Biol. 2009, 29:3845-3852.
28. Vasanwala F.H., Kusam S., Toney L.M., Dent A.L. Repression of AP-1 function: a mechanism for the regulation of Blimp-1 expression and B lymphocyte differentiation by the B cell lymphoma-6 protooncogene. J. Immunol. 2002, 169:1922-1929.
29. Podar K., Raab M.S., Tonon G., Sattler M., Barila D., Zhang J., Tai Y.T., Yasui H., Raje N., DePinho R.A., Hideshima T., Chauhan D., Anderson K.C. Up-regulation of c-Jun inhibits proliferation and induces apoptosis via caspase-triggered c-Abl cleavage in human multiple myeloma. Cancer Res. 2007, 67:1680-1688.
30. Hagenbuchner J., Ausserlechner M.J., Porto V., David R., Meister B., Bodner M., Villunger A., Geiger K., Obexer P. The anti-apoptotic protein BCL2L1/Bcl-xL is neutralized by pro-apoptotic PMAIP1/Noxa in neuroblastoma, thereby determining bortezomib sensitivity independent of prosurvival MCL1 expression. J. Biol. Chem. 2010, 285:6904-6912.
31. Beroukhim R., Mermel C.H., Porter D., Wei G., Raychaudhuri S., Donovan J., Barretina J., Boehm J.S., Dobson J., Urashima M., Mc Henry K.T., Pinchback R.M., Ligon A.H., Cho Y.J., Haery L., Greulich H., Reich M., Winckler W., Lawrence M.S., Weir B.A., Tanaka K.E., Chiang D.Y., Bass A.J., Loo A., Hoffman C., Prensner J., Liefeld T., Gao Q., Yecies D., Signoretti S., Maher E., Kaye F.J., Sasaki H., Tepper J.E., Fletcher J.A., Tabernero J., Baselga J., Tsao M.S., Demichelis F., Rubin M.A., Janne P.A., Daly M.J., Nucera C., Levine R.L., Ebert B.L., Gabriel S., Rustgi A.K., Antonescu C.R., Ladanyi M., Letai A., Garraway L.A., Loda M., Beer D.G., True L.D., Okamoto A., Pomeroy S.L., Singer S., Golub T.R., Lander E.S., Getz G., Sellers W.R., Meyerson M. The landscape of somatic copy-number alteration across human cancers. Nature 2010, 463:899-905.
32. Sheng Z., Li L., Zhu L.J., Smith T.W., Demers A., Ross A.H., Moser R.P., Green M.R. A genome-wide RNA interference screen reveals an essential CREB3L2-ATF5-MCL1 survival pathway in malignant glioma with therapeutic implications. Nat. Med. 2010, 16:671-677.
33. Jane E.P., Premkumar D.R., Pollack I.F. Bortezomib sensitizes malignant human glioma cells to TRAIL, mediated by inhibition of the NF-{kappa}B signaling pathway. Mol. Cancer Ther. 2011, 10:198-208.
34. Wei G., Margolin A.A., Haery L., Brown E., Cucolo L., Julian B., Shehata S., Kung A.L., Beroukhim R., Golub T.R. Chemical genomics identifies small-molecule MCL1 repressors and BCL-xL as a predictor of MCL1 dependency. Cancer Cell 2012, 21:547-562.
35. Wei G., Twomey D., Lamb J., Schlis K., Agarwal J., Stam R.W., Opferman J.T., Sallan S.E., den Boer M.L., Pieters R., Golub T.R., Armstrong S.A. Gene expression-based chemical genomics identifies rapamycin as a modulator of MCL1 and glucocorticoid resistance. Cancer Cell 2006, 10:331-342.
36. Zhong Q., Gao W., Du F., Wang X. Mule/ARF-BP1, a BH3-only E3 ubiquitin ligase, catalyzes the polyubiquitination of Mcl-1 and regulates apoptosis. Cell 2005, 121:1085-1095.
37. Schwickart M., Huang X., Lill J.R., Liu J., Ferrando R., French D.M., Maecker H., O'Rourke K., Bazan F., Eastham-Anderson J., Yue P., Dornan D., Huang D.C., Dixit V.M. Deubiquitinase USP9X stabilizes MCL1 and promotes tumour cell survival. Nature 2010, 463:103-107.
38. Ding Q., He X., Hsu J.M., Xia W., Chen C.T., Li L.Y., Lee D.F., Liu J.C., Zhong Q., Wang X., Hung M.C. Degradation of Mcl-1 by beta-TrCP mediates glycogen synthase kinase 3-induced tumor suppression and chemosensitization. Mol. Cell Biol. 2007, 27:4006-4017.
39. Wertz I.E., Kusam S., Lam C., Okamoto T., Sandoval W., Anderson D.J., Helgason E., Ernst J.A., Eby M., Liu J., Belmont L.D., Kaminker J.S., O'Rourke K.M., Pujara K., Kohli P.B., Johnson A.R., Chiu M.L., Lill J.R., Jackson P.K., Fairbrother W.J., Seshagiri S., Ludlam M.J., Leong K.G., Dueber E.C., Maecker H., Huang D.C., Dixit V.M. Sensitivity to antitubulin chemotherapeutics is regulated by MCL1 and FBW7. Nature 2011, 471:110-114.
40. Chapman M.A., Lawrence M.S., Keats J.J., Cibulskis K., Sougnez C., Schinzel A.C., Harview C.L., Brunet J.P., Ahmann G.J., Adli M., Anderson K.C., Ardlie K.G., Auclair D., Baker A., Bergsagel P.L., Bernstein B.E., Drier Y., Fonseca R., Gabriel S.B., Hofmeister C.C., Jagannath S., Jakubowiak A.J., Krishnan A., Levy J., Liefeld T., Lonial S., Mahan S., Mfuko B., Monti S., Perkins L.M., Onofrio R., Pugh T.J., Rajkumar S.V., Ramos A.H., Siegel D.S., Sivachenko A., Stewart A.K., Trudel S., Vij R., Voet D., Winckler W., Zimmerman T., Carpten J., Trent J., Hahn W.C., Garraway L.A., Meyerson M., Lander E.S., Getz G., Golub T.R. Initial genome sequencing and analysis of multiple myeloma. Nature 2011, 471:467-472.
41. Perciavalle R.M., Stewart D.P., Koss B., Lynch J., Milasta S., Bathina M., Temirov J., Cleland M.M., Pelletier S., Schuetz J.D., Youle R.J., Green D.R., Opferman J.T. Anti-apoptotic MCL-1 localizes to the mitochondrial matrix and couples mitochondrial fusion to respiration. Nat. Cell Biol. 2012, 14:575-583.
42. Rost B., Liu J. The PredictProtein server. Nucleic Acids Res. 2003, 31:3300-3304.
43. Briesemeister S., Rahnenfuhrer J., Kohlbacher O. YLoc-an interpretable web server for predicting subcellular localization. Nucleic Acids Res. 2010, 38:W497-502.
44. la Cour T., Kiemer L., Molgaard A., Gupta R., Skriver K., Brunak S. Analysis and prediction of leucine-rich nuclear export signals. Protein Eng. Des. Sel. 2004, 17:527-536.
45. Szilagyi A., Skolnick J. Efficient prediction of nucleic acid binding function from low-resolution protein structures. J. Mol. Biol. 2006, 358:922-933.
46. Shaulian E. AP-1 - The Jun proteins: oncogenes or tumor suppressors in disguise?. Cell Signal 2010, 22:894-899.
47. Ferraris S.E., Isoniemi K., Torvaldson E., Anckar J., Westermarck J., Eriksson J.E. Nucleolar AATF regulates c-Jun-mediated apoptosis. Mol. Biol. Cell 2012, 23:4323-4332.
48. Hartley P.S., Bayne R.A., Robinson L.L., Fulton N., Anderson R.A. Developmental changes in expression of myeloid cell leukemia-1 in human germ cells during oogenesis and early folliculogenesis. J. Clin. Endocrinol. Metab. 2002, 87:3417-3427.