IMiD immunomodulatory compounds block C/EBPβ translation through eIF4E down-regulation resulting in inhibition of MM

Blood

Volumn 117, Issue 19, 2011, Pages 5157-5165

  Li, Shirong ^a   Pal, Rekha ^a   Monaghan, Sara A ^b   Schafer, Peter ^c   Ouyang, Hongjiao ^a,d   Mapara, Markus ^a   Galson, Deborah L ^a,d   Lentzsch, Suzanne ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^c CELGENE CORPORATION   (United States)

^d VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CCAAT ENHANCER BINDING PROTEIN BETA; INITIATION FACTOR 4E; INTERFERON REGULATORY FACTOR 4; LENALIDOMIDE; POMALIDOMIDE; THALIDOMIDE DERIVATIVE;

ARTICLE; CELL PROLIFERATION; DRUG MECHANISM; HUMAN; HUMAN CELL; IMMUNOMODULATION; MULTIPLE MYELOMA; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING;

EID: 79955969732     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-10-314278     Document Type: Article

References (50)

1. Lentzsch S, LeBlanc R, Podar K, et al. Immunomodulatory analogs of thalidomide inhibit growth of Hs Sultan cells and angiogenesis in vivo. Leukemia. 2003;17(1):41-44. (Pubitemid 36175886)
2. Lentzsch S, Rogers MS, LeBlanc R, et al. S-3-Amino-phthalimido- glutarimide inhibits angiogenesis and growth of B-cell neoplasias in mice. Cancer Res. 2002;62(8):2300-2305. (Pubitemid 34411708)
3. Quach H, Ritchie D, Stewart AK, et al. Mechanism of action of immunomodulatory drugs (IMiDS) in multiple myeloma. Leukemia. 2010; 24(1):22-32.
4. Escoubet-Lozach L, Lin IL, Jensen-Pergakes K, et al. Pomalidomide and lenalidomide induce p21 WAF-1 expression in both lymphoma and multiple myeloma through a LSD1-mediated epigenetic mechanism. Cancer Res. 2009;69(18):7347-7356.
5. Gandhi AK, Kang J, Capone L, et al. Dexamethasone synergizes with lenalidomide to inhibit multiple myeloma tumor growth, but reduces lenalidomide-induced immunomodulation of T and NK cell function. Curr Cancer Drug Targets. 2010; 10(2):155-167.
6. Xu Y, Li J, Ferguson GD, et al. Immunomodulatory drugs reorganize cytoskeleton by modulating Rho GTPases. Blood. 2009;114(2):338-345.
7. Ramji DP, Foka P. CCAAT/enhancer-binding proteins: structure, function and regulation. Biochem J. 2002;365(3):561-575. (Pubitemid 34864439)
8. Tsukada J, Saito K, Waterman WR, Webb AC, Auron PE. Transcription factors NF-IL6 and CREB recognize a common essential site in the human prointerleukin 1 beta gene. Mol Cell Biol. 1994;14(11):7285-7297. (Pubitemid 24326393)
9. Choy L, Derynck R. Transforming growth factor-beta inhibits adipocyte differentiation by Smad3 interacting with CCAAT/enhancer-binding protein (C/EBP) and repressing C/EBP transactivation function. J Biol Chem. 2003;278(11):9609-9619. (Pubitemid 36800456)
10. Heckman CA, Wheeler MA, Boxer LM. Regulation of Bcl-2 expression by C/EBP in t(14;18) lymphoma cells. Oncogene. 2003;22(39):7891-7899. (Pubitemid 37175853)
11. Oya M, Horiguchi A, Mizuno R, Marumo K, Murai M. Increased activation of CCAAT/enhancer binding protein-beta correlates with the invasiveness of renal cell carcinoma. Clin Cancer Res. 2003;9(3):1021-1027. (Pubitemid 36323706)
12. Calkhoven CF, Muller C, Leutz A. Translational control of C/EBPalpha and C/EBPbeta isoform expression. Genes Dev. 2000;14(15):1920-1932. (Pubitemid 30639525)
13. Chen X, Liu W, Ambrosino C, et al. Impaired generation of bone marrow B lymphocytes in mice deficient in C/EBPbeta. Blood. 1997;90(1):156-164. (Pubitemid 27276558)
14. Akira S, Isshiki H, Sugita T, et al. A nuclear factor for IL-6 expression (NF-IL-6) is a member of the C/EBP family. EMBO. 1990;9:1897-1906.
15. Pal R, Janz M, Galson DL, et al. C/EBPbeta regulates transcription factors critical for proliferation and survival of multiple myeloma cells. Blood. 2009;114(18):3890-3898.
16. Klein U, Casola S, Cattoretti G, et al. Transcription factor IRF4 controls plasma cell differentiation and class-switch recombination. Nat Immunol. 2006;7(7):773-782. (Pubitemid 43905877)
17. Mittrucker HW, Matsuyama T, Grossman A, et al. Requirement for the transcription factor LSIRF/ IRF4 for mature B and T lymphocyte function. Science. 1997;275(5299):540-543. (Pubitemid 27051911)
18. Sciammas R, Shaffer AL, Schatz JH, Zhao H, Staudt LM, Singh H. Graded expression of interferon regulatory factor-4 coordinates isotype switching with plasma cell differentiation. Immunity. 2006;25(2):225-236. (Pubitemid 44224149)
19. Shaffer AL, Emre NC, Lamy L, et al. IRF4 addiction in multiple myeloma. Nature. 2008; 454(7201):226-231. (Pubitemid 351969894)
20. Kim MH, Fields J. Translationally regulated C/EBP beta isoform expression upregulates metastatic genes in hormone-independent prostate cancer cells. Prostate. 2008;68(12):1362-1371.
21. Rau M, Ohlmann T, Morley SJ, Pain VM. A reevaluation of the cap-binding protein, eIF4E, as a rate-limiting factor for initiation of translation in reticulocyte lysate. J Biol Chem. 1996;271(15): 8983-8990. (Pubitemid 26123327)
22. Sonenberg N. Translation factors as effectors of cell growth and tumorigenesis. Curr Opin Cell Biol. 1993;5(6):955-960. (Pubitemid 23340500)
23. Richter JD, Sonenberg N. Regulation of cap-dependent translation by eIF4E inhibitory proteins. Nature. 2005;433(7025):477-480. (Pubitemid 40204297)
24. Graff JR, Konicek BW, Vincent TM, et al. Therapeutic suppression of translation initiation factor eIF4E expression reduces tumor growth without toxicity. J Clin Invest. 2007;117(9):2638-2648. (Pubitemid 47494364)
25. Kevil CG, De Benedetti A, Payne DK, Coe LL, Laroux FS, Alexander JS. Translational regulation of vascular permeability factor by eukaryotic initiation factor 4E: implications for tumor angiogenesis. Int J Cancer. 1996;65(6):785-790. (Pubitemid 26127753)
26. Mezquita P, Parghi SS, Brandvold KA, Ruddell A. Myc regulates VEGF production in B cells by stimulating initiation of VEGF mRNA translation. Oncogene. 2005;24(5):889-901. (Pubitemid 40216097)
27. Feng R, Ma H, Hassig CA, et al. KD5170, a novel mercaptoketone-based histone deacetylase inhibitor, exerts antimyeloma effects by DNA damage and mitochondrial signaling. Mol Cancer Ther. 2008;7(6):1494-1505.
28. Lentzsch S, Gries M, Janz M, Bargou R, Dorken B, Mapara MY. Macrophage inflammatory protein 1-alpha (MIP-1 alpha) triggers migration and signaling cascades mediating survival and proliferation in multiple myeloma (MM) cells. Blood. 2003;101(9):3568-3573. (Pubitemid 36857943)
29. Feng R, Oton A, Mapara MY, Anderson G, Belani C, Lentzsch S. The histone deacetylase inhibitor, PXD101, potentiates bortezomib-induced anti-multiple myeloma effect by induction of oxidative stress and DNAdamage. Br J Haematol. 2007;139(3):385-397. (Pubitemid 47512171)
30. Feng R, Anderson G, Xiao G, et al. SDX-308, a nonsteroidal anti-inflammatory agent, inhibits NF-kappaB activity, resulting in strong inhibition of osteoclast formation/activity and multiple myeloma cell growth. Blood. 2007;109(5):2130-2138. (Pubitemid 46348215)
31. Andrei MA, Ingelfinger D, Heintzmann R, Achsel T, Rivera-Pomar R, Luhrmann R.Arole for eIF4E and eIF4E-transporter in targeting mRNPs to mammalian processing bodies. Rna. 2005;11(5):717-727. (Pubitemid 40594337)
32. De Benedetti A, Graff JR. eIF-4E expression and its role in malignancies and metastases. Oncogene. 2004;23(18):3189-3199. (Pubitemid 38638830)
33. Li S, Gill N, Lentzsch S. Recent advances of IMiDs in cancer therapy. Curr Opin Oncol. 2010; 22(6):579-585.
34. Weber DM, Chen C, Niesvizky R, et al. Lenalidomide plus dexamethasone for relapsed multiple myeloma in North America. N Engl J Med. 2007; 357(21):2133-2142. (Pubitemid 350146108)
35. Richardson PG, Blood E, Mitsiades CS, et al. A randomized phase 2 study of lenalidomide therapy for patients with relapsed or relapsed and refractory multiple myeloma. Blood. 2006; 108(10):3458-3464.
36. Lacy MQ, Hayman SR, Gertz MA, et al. Pomalidomide (CC4047) plus low-dose dexamethasone as therapy for relapsed multiple myeloma. J Clin Oncol. 2009;27(30):5008-5014.
37. Dimopoulos M, Spencer A, Attal M, et al. Lenalidomide plus dexamethasone for relapsed or refractory multiple myeloma. N Engl J Med. 2007; 357(21):2123-2132. (Pubitemid 350146107)
38. Ferrajoli A, Lee BN, Schlette EJ, et al. Lenalidomide induces complete and partial remissions in patients with relapsed and refractory chronic lymphocytic leukemia. Blood. 2008;111(11):5291-5297.
39. Witzig TE, Wiernik PH, Moore T, et al. Lenalidomide oral monotherapy produces durable responses in relapsed or refractory indolent non-Hodgkin's lymphoma. J Clin Oncol. 2009;27(32): 5404-5409.
40. Hideshima T, Chauhan D, Shima Y, et al. Thalidomide and its analogs overcome drug resistance of human multiple myeloma cells to conventional therapy. Blood. 2000;96(9):2943-2950.
41. Iida S, Rao PH, Butler M, et al. Deregulation of MUM1/IRF4 by chromosomal translocation in multiple myeloma. Nat Genet. 1997;17(2):226-230.
42. Falini B, Fizzotti M, Pucciarini A, et al. A monoclonal antibody (MUM1p) detects expression of the MUM1/IRF4 protein in a subset of germinal center B cells, plasma cells, and activated T cells. Blood. 2000;95(6):2084-2092. (Pubitemid 30151649)
43. Heintel D, Zojer N, Schreder M, et al. Expression of MUM1/IRF4 mRNA as a prognostic marker in patients with multiple myeloma. Leukemia. 2008; 22(2):441-445. (Pubitemid 351250556)
44. Podar K, Anderson KC. Inhibition of VEGF signaling pathways in multiple myeloma and other malignancies. Cell Cycle. 2007;6(5):538-542. (Pubitemid 46440425)
45. Gupta D, Treon SP, Shima Y, et al. Adherence of multiple myeloma cells to bone marrow stromal cells upregulates vascular endothelial growth factor secretion: therapeutic applications. Leukemia. 2001;15(12):1950-1961. (Pubitemid 33115003)
46. Lopez-Girona A, Mendy D, Gaidarova S, et al. Lenalidomide inhibits the multiple myeloma cell survival factor IRF4/MUM1. Clin Lymph Myeloma. 2009;(suppl 1):s122.
47. Koh KR, Janz M, Mapara MY, et al. Immunomodulatory derivative of thalidomide (IMiD CC-4047) induces a shift in lineage commitment by suppressing erythropoiesis and promoting myelopoiesis. Blood. 2005;105(10):3833-3840. (Pubitemid 40656125)
48. Pal R, Monaghan SA, Hassett AC, et al. Immunomodulatory derivatives induce PU.1 down-regulation, myeloid maturation arrest, and neutropenia. Blood. 2010;115(3):605-614.
49. Hagner PR, Schneider A, Gartenhaus RB. Targeting the translational machinery as a novel treatment strategy for hematologic malignancies. Blood. 2010;115(11):2127-2135.
50. Raje N, Kumar S, Hideshima T, et al. Combination of the mTOR inhibitor rapamycin and CC-5013 has synergistic activity in multiple myeloma. Blood. 2004;104(13):4188-4193. (Pubitemid 39620173)