Inhibiting CARD11 translation during BCR activation by targeting the eIF4A RNA helicase

Blood

Volumn 124, Issue 25, 2014, Pages 3758-3767

  Steinhardt, James J ^a   Peroutka, Raymond J ^a   Mazan Mamczarz, Krystyna ^a   Chen, Qing ^a   Houng, Simone ^a   Robles, Carol ^a   Barth, Rolf N ^b   DuBose, Joseph ^b   Bruns, Brandon ^b   Tesoriero, Ronald ^b   Stein, Deborah ^b   Fang, Raymond ^b   Hanna, Nader ^b   Pasley, Jason ^b   Rodriguez, Carlos ^b   Kligman, Mark D ^b   Bradley, Matthew ^b   Rabin, Joseph ^b   Shackelford, Stacy ^b   Dai, Bojie ^a   Landon, Ari L ^a   Scalea, Thomas ^b   Livak, Ferenc ^a   Gartenhaus, Ronald B ^a,c   more..

^a UNIVERSITY OF MARYLAND MEDICAL CENTER   (United States)

^b R ADAMS COWLEY SHOCK TRAUMA CENTER   (United States)

^c BALTIMORE VA MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B LYMPHOCYTE ANTIGEN; B LYMPHOCYTE RECEPTOR; IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; INITIATION FACTOR 4A; RNA HELICASE; S6 KINASE; 5' UNTRANSLATED REGION; APOPTOSIS REGULATORY PROTEIN; BCL10 PROTEIN, HUMAN; CARD11 PROTEIN, HUMAN; CASPASE; CASPASE RECRUITMENT DOMAIN SIGNALING PROTEIN; DEAD BOX PROTEIN; GUANYLATE CYCLASE; LYMPHOCYTE ANTIGEN RECEPTOR; MALT1 PROTEIN, HUMAN; PDCD4 PROTEIN, HUMAN; RNA BINDING PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN; SILVESTROL; TRITERPENE; TUMOR PROTEIN;

5' UNTRANSLATED REGION; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IN VITRO STUDY; LARGE CELL LYMPHOMA; ONCOGEN MALT 1; ONCOGENE; ONCOGENE BCL 10; ONCOGENE CARD 11; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; RNA TRANSLATION; UPREGULATION; ADULT; AGED; ANTAGONISTS AND INHIBITORS; B LYMPHOCYTE; CELL CULTURE; DRUG EFFECTS; GENETICS; METABOLISM; MIDDLE AGED; PATHOLOGY; PROTEIN SYNTHESIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TUMOR CELL LINE; VERY ELDERLY; WESTERN BLOTTING;

5' UNTRANSLATED REGIONS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADULT; AGED; AGED, 80 AND OVER; APOPTOSIS REGULATORY PROTEINS; B-LYMPHOCYTES; BLOTTING, WESTERN; CARD SIGNALING ADAPTOR PROTEINS; CASPASES; CELL LINE, TUMOR; CELLS, CULTURED; DEAD-BOX RNA HELICASES; EUKARYOTIC INITIATION FACTOR-4A; GUANYLATE CYCLASE; HUMANS; LYMPHOMA, LARGE B-CELL, DIFFUSE; MIDDLE AGED; NEOPLASM PROTEINS; PROTEIN BIOSYNTHESIS; RECEPTORS, ANTIGEN, B-CELL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RIBOSOMAL PROTEIN S6 KINASES, 70-KDA; RNA-BINDING PROTEINS; SIGNAL TRANSDUCTION; TRITERPENES;

EID: 84919628705     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2014-07-589689     Document Type: Article

References (54)

1. Wakabayashi C, Adachi T, Wienands J, Tsubata T. A distinct signaling pathway used by the IgG-containing B cell antigen receptor. Science. 2002;298(5602):2392-2395.
2. Dogan I, Bertocci B, Vilmont V, et al. Multiple layers of B cell memory with different effector functions. Nat Immunol. 2009;10(12):1292-1299.
3. Kehry MR. CD40-mediated signaling in B cells. Balancing cell survival, growth, and death. J Immunol. 1996;156(7):2345-2348.
4. Monroe JG. ITAM-mediated tonic signalling through pre-BCR and BCR complexes. Nat Rev Immunol. 2006;6(4):283-294.
5. Horikawa K, Martin SW, Pogue SL, et al. Enhancement and suppression of signaling by the conserved tail of IgG memory-type B cell antigen receptors. J Exp Med. 2007;204(4):759-769.
6. Alizadeh AA, Eisen MB, Davis RE, et al. Distinct types of diffuse large B-cell lymphoma identified by gene expression profiling. Nature. 2000;403(6769):503-511.
7. Young RM, Staudt LM. Targeting pathological B cell receptor signalling in lymphoid malignancies. Nat Rev Drug Discov. 2013;12(3):229-243.
8. Blenk S, Engelmann J, Weniger M, et al. Germinal center B cell-like (GCB) and activated B cell-like (ABC) type of diffuse large B cell lymphoma (DLBCL): analysis of molecular predictors, signatures, cell cycle state and patient survival. Cancer Inform. 2007;3:399-420.
9. Gauld SB, Dal Porto JM, Cambier JC. B cell antigen receptor signaling: roles in cell development and disease. Science. 2002;296(5573):1641-1642.
10. Li HL, Forman MS, Kurosaki T, Puré E. Syk is required for BCR-mediated activation of p90Rsk, but not p70S6k, via a mitogen-activated protein kinase-independent pathway in B cells. J Biol Chem. 1997;272(29):18200-18208.
11. Gingras AC, Raught B, Sonenberg N. eIF4 initiation factors: effectors of mRNA recruitment to ribosomes and regulators of translation. Annu Rev Biochem. 1999;68:913-963.
12. Bi X, Ren J, Goss DJ. Wheat germ translation initiation factor eIF4B affects eIF4A and eIFiso4F helicase activity by increasing the ATP binding affinity of eIF4A. Biochemistry. 2000;39(19):5758-5765.
13. Dennis MD, Jefferson LS, Kimball SR. Role of p70S6K1-mediated phosphorylation of eIF4B and PDCD4 proteins in the regulation of protein synthesis. J Biol Chem. 2012;287(51):42890-42899.
14. Rogers GWJ Jr, Richter NJ, Merrick WC. Biochemical and kinetic characterization of the RNA helicase activity of eukaryotic initiation factor 4A. J Biol Chem. 1999;274(18):12236-12244.
15. Yang HS, Jansen AP, Komar AA, et al. The transformation suppressor Pdcd4 is a novel eukaryotic translation initiation factor 4A binding protein that inhibits translation. Mol Cell Biol. 2003;23(1):26-37.
16. Dorrello NV, Peschiaroli A, Guardavaccaro D, Colburn NH, Sherman NE, Pagano M. S6K1- and betaTRCP-mediated degradation of PDCD4 promotes protein translation and cell growth. Science. 2006;314(5798):467-471.
17. Hilliard A, Hilliard B, Zheng SJ, et al. Translational regulation of autoimmune inflammation and lymphoma genesis by programmed cell death 4. J Immunol. 2006;177(11):8095-8102.
18. Shen Y, Iqbal J, Xiao L, et al. Distinct gene expression profiles in different B-cell compartments in human peripheral lymphoid organs. BMC Immunol. 2004;5(20):20.
19. Horvilleur E, Sbarrato T, Hill K, et al. A role for eukaryotic initiation factor 4B overexpression in the pathogenesis of diffuse large B-cell lymphoma. Leukemia. 2014;28(5):1092-1102.
20. Hwang BY, Su BN, Chai H, et al. Silvestrol and episilvestrol, potential anticancer rocaglate derivatives from Aglaia silvestris. J Org Chem. 2004;69(10):3350-3358.
21. Bordeleau ME, Mori A, Oberer M, et al. Functional characterization of IRESes by an inhibitor of the RNA helicase eIF4A. Nat Chem Biol. 2006;2(4):213-220.
22. Lucas DM, Edwards RB, Lozanski G, et al. The novel plant-derived agent silvestrol has B-cell selective activity in chronic lymphocytic leukemia and acute lymphoblastic leukemia in vitro and in vivo. Blood. 2009;113(19):4656-4666.
23. Markham NR, Zuker M. DINAMelt web server for nucleic acid melting prediction. Nucleic Acids Res. 2005;33(Web Server Issue):W577-W581.
24. Willis AE. Translational control of growth factor and proto-oncogene expression. Int J Biochem Cell Biol. 1999;31(1):73-86.
25. Thome M. CARMA1, BCL-10 and MALT1 in lymphocyte development and activation. Nat Rev Immunol. 2004;4(5):348-359.
26. Lenz G, Davis RE, Ngo VN, et al. Oncogenic CARD11 mutations in human diffuse large B cell lymphoma. Science. 2008;319(5870):1676-1679.
27. Davis RE, Ngo VN, Lenz G, et al. Chronic active B-cell-receptor signalling in diffuse large B-cell lymphoma. Nature. 2010;463(7277):88-92.
28. Rawlings DJ, Sommer K, Moreno-García ME. The CARMA1 signalosome links the signalling machinery of adaptive and innate immunity in lymphocytes. Nat Rev Immunol. 2006;6(11):799-812.
29. Petersen CP, Bordeleau ME, Pelletier J, Sharp PA. Short RNAs repress translation after initiation in mammalian cells. Mol Cell. 2006;21(4):533-542.
30. Kutner RH, Zhang XY, Reiser J. Production, concentration and titration of pseudotyped HIV-1-based lentiviral vectors. Nat Protoc. 2009;4(4):495-505.
31. Mazan-Mamczarz K, Zhao XF, Dai B, et al. Downregulation of eIF4GII by miR-520c-3p represses diffuse large B cell lymphoma development. PLoS Genet. 2014;10(1):e1004105.
32. Mazan-Mamczarz K, Lal A, Martindale JL, Kawai T, Gorospe M. Translational repression by RNA-binding protein TIAR. Mol Cell Biol. 2006;26(7):2716-2727.
33. Wang J, Zhong C, Wang F, Qu F, Ding J. Crystal structures of S6K1 provide insights into the regulation mechanism of S6K1 by the hydrophobic motif. Biochem J. 2013;454(1):39-47.
34. Mizuno T, Rothstein TL. B cell receptor (BCR) cross-talk: CD40 engagement enhances BCR-induced ERK activation. J Immunol. 2005;174(6):3369-3376.
35. Sánchez-Mateos P, Cebrián M, Acevedo A, López-Botet M, De Landázuri MO, Sánchez-Madrid F. Expression of a gp33/27,000 MW activation inducer molecule (AIM) on human lymphoid tissues. Induction of cell proliferation on thymocytes and B lymphocytes by anti-AIM antibodies. Immunology. 1989;68(1):72-79.
36. Bjur E, Larsson O, Yurchenko E, et al. Distinct translational control in CD4+ T cell subsets. PLoS Genet. 2013;9(5):e1003494.
37. Jin C, Rajabi H, Rodrigo CM, Porco JAJ Jr, Kufe D. Targeting the eIF4A RNA helicase blocks translation of the MUC1-C oncoprotein. Oncogene. 2013;32(17):2179-2188.
38. Pestova TV, Shatsky IN, Fletcher SP, Jackson RJ, Hellen CU. A prokaryotic-like mode of cytoplasmic eukaryotic ribosome binding to the initiation codon during internal translation initiation of hepatitis C and classical swine fever virus RNAs. Genes Dev. 1998;12(1):67-83.
39. Svitkin YV, Pause A, Haghighat A, et al. The requirement for eukaryotic initiation factor 4A (elF4A) in translation is in direct proportion to the degree of mRNA 5′ secondary structure. RNA. 2001;7(3):382-394.
40. Schatz JH, Oricchio E, Wolfe AL, et al. Targeting cap-dependent translation blocks converging survival signals by AKT and PIM kinases in lymphoma. J Exp Med. 2011;208(9):1799-1807.
41. Sonenberg N. eIF4E, the mRNA cap-binding protein: from basic discovery to translational research. Biochem Cell Biol. 2008;86(2):178-183.
42. Ruggero D. Translational control in cancer etiology. Cold Spring Harb Perspect Biol. 2013;5(2):a012336.
43. Boussemart L, Malka-Mahieu H, Girault I, et al. eIF4F is a nexus of resistance to anti-BRAF and anti-MEK cancer therapies. Nature. 2014;513(7516):105-109.
44. Monks A, Scudiero D, Skehan P, et al. Feasibility of a high-flux anticancer drug screen using a diverse panel of cultured human tumor cell lines. J Natl Cancer Inst. 1991;83(11):757-766.
45. Saradhi UV, Gupta SV, Chiu M, et al. Characterization of silvestrol pharmacokinetics in mice using liquid chromatography-tandem mass spectrometry. AAPS J. 2011;13(3):347-356.
46. National Cancer Institute. COMPARE methodology. http://dtp.nci.nih.gov/docs/compare/compare-methodology.html. Accessed April 12, 2014.
47. Wolfe AL, Singh K, Zhong Y, et al. RNA G-quadruplexes cause eIF4A-dependent oncogene translation in cancer. Nature. 2014;513(7516):65-70.
48. Gu L, Song G, Chen L, et al. Inhibition of miR-21 induces biological and behavioral alterations in diffuse large B-cell lymphoma. Acta Haematol. 2013;130(2):87-94.
49. Lam KP, Kühn R, Rajewsky K. In vivo ablation of surface immunoglobulin on mature B cells by inducible gene targeting results in rapid cell death. Cell. 1997;90(6):1073-1083.
50. Pasparakis M, Schmidt-Supprian M, Rajewsky K. IkappaB kinase signaling is essential for maintenance of mature B cells. J Exp Med. 2002;196(6):743-752.
51. Egawa T, Albrecht B, Favier B, et al. Requirement for CARMA1 in antigen receptor-induced NF-kappa B activation and lymphocyte proliferation. Curr Biol. 2003;13(14):1252-1258.
52. Hara H, Wada T, Bakal C, et al. The MAGUK family protein CARD11 is essential for lymphocyte activation. Immunity. 2003;18(6):763-775.
53. Jun JE, Wilson LE, Vinuesa CG, et al. Identifying the MAGUK protein Carma-1 as a central regulator of humoral immune responses and atopy by genome-wide mouse mutagenesis. Immunity. 2003;18(6):751-762.
54. Newton K, Dixit VM. Mice lacking the CARD of CARMA1 exhibit defective B lymphocyte development and impaired proliferation of their B and T lymphocytes. Curr Biol. 2003;13(14):1247-1251.