PRMT5 is required for lymphomagenesis triggered by multiple oncogenic drivers

Cancer Discovery

Volumn 5, Issue 3, 2015, Pages 288-303

  Li, Yan ^a,d   Chitnis, Nilesh ^a   Nakagawa, Hiroshi ^b   Kita, Yoshiaki ^c   Natsugoe, Shoji ^c   Yang, Yi ^d   Li, Zihai ^d   Wasik, Mariusz ^b,e   Klein Szanto, Andres J P ^f   Rustgi, Anil K ^b   Alan Diehl, J ^a,d  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c KAGOSHIMA UNIVERSITY   (Japan)

^d MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

^e UNIVERSITY OF PENNSYLVANIA   (United States)

^f FOX CHASE CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN D1; CYCLIN DEPENDENT KINASE 4; NOTCH1 RECEPTOR; PROTEIN ARGININE METHYLTRANSFERASE; PROTEIN ARGININE METHYLTRANSFERASE 5; PROTEIN P53; UNCLASSIFIED DRUG; ARGININE; MEP50 PROTEIN, HUMAN; PRMT5 PROTEIN, HUMAN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

3T3 CELL LINE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE MARROW TRANSPLANTATION; CANCER INHIBITION; CARCINOGENESIS; CELL PROLIFERATION; CELL RENEWAL; CELL TRANSFORMATION; CONTROLLED STUDY; FLUORESCENCE ACTIVATED CELL SORTING; GENE MUTATION; GENE OVEREXPRESSION; HEK293 CELL LINE; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; LEUKEMIA; LYMPHOMA; LYMPHOMAGENESIS; METHYLATION; MOUSE; NONHUMAN; ONCOGENE; PLASMID; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RETROVIRUS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SITE DIRECTED MUTAGENESIS; T CELL LYMPHOMA; TRANSIENT TRANSFECTION; WESTERN BLOTTING; AMINO ACID SUBSTITUTION; ANIMAL; APOPTOSIS; CLUSTER ANALYSIS; ENZYME ACTIVATION; GENE EXPRESSION PROFILING; GENETICS; METABOLISM; MUTATION; PATHOLOGY; PHOSPHORYLATION; T CELL LEUKEMIA;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID SUBSTITUTION; ANIMALS; APOPTOSIS; ARGININE; CELL TRANSFORMATION, NEOPLASTIC; CLUSTER ANALYSIS; CYCLIN D1; CYCLIN-DEPENDENT KINASE 4; ENZYME ACTIVATION; GENE EXPRESSION PROFILING; HUMANS; LEUKEMIA, T-CELL; LYMPHOMA; LYMPHOMA, T-CELL; METHYLATION; MICE; MUTATION; ONCOGENES; PHOSPHORYLATION; PROTEIN-ARGININE N-METHYLTRANSFERASES; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84925302177     PISSN: 21598274     EISSN: 21598290     Source Type: Journal    
DOI: 10.1158/2159-8290.CD-14-0625     Document Type: Article

References (48)

1. Bedford MT, Clarke SG. Protein arginine methylation in mammals: who, what, and why. Mol Cell 2009;33:1-13.
2. Bedford MT, Richard S. Arginine methylation an emerging regulator of protein function. Mol Cell 2005;18:263-72.
3. Wang L, Pal S, Sif S. Protein arginine methyltransferase 5 suppresses the transcription of the RB family of tumor suppressors in leukemia and lymphoma cells. Mol Cell Biol 2008;28:6262-77.
4. Yang Y, McBride KM, Hensley S, Lu Y, Chedin F, Bedford MT. Arginine methylation facilitates the recruitment of TOP3B to chro-matin to prevent R loop accumulation. Mol Cell 2014;53:484-97.
5. Aggarwal P, Vaites LP, Kim JK, Mellert H, Gurung B, Nakagawa H, et al. Nuclear cyclin D1/CDK4 kinase regulates CUL4 expression and triggers neoplastic growth via activation of the PRMT5 methyltrans-ferase. Cancer Cell 2010;18:329-40.
6. Pal S, Vishwanath SN, Erdjument-Bromage H, Tempst P, Sif S. Human SWI/SNF-associated PRMT5 methylates histone H3 arginine 8 and negatively regulates expression of ST7 and NM23 tumor suppressor genes. Mol Cell Biol 2004;24:9630-45.
7. Zhao Q, Rank G, Tan YT, Li H, Moritz RL, Simpson RJ, et al. PRMT5-mediated methylation of histone H4R3 recruits DNMT3A, coupling histone and DNA methylation in gene silencing. Nat Struct Mol Biol 2009;16:304-11.
8. Vagin VV, Wohlschlegel J, Qu J, Jonsson Z, Huang X, Chuma S, et al. Proteomic analysis of murine Piwi proteins reveals a role for arginine methylation in specifying interaction with Tudor family members. Genes Dev 2009;23:1749-62.
9. Kirino Y, Kim N, de Planell-Saguer M, Khandros E, Chiorean S, Klein PS, et al. Arginine methylation of Piwi proteins catalysed by dPRMT5 is required for Ago3 and Aub stability. Nat Cell Biol 2009;11:652-8.
10. Wei H, Wang B, Miyagi M, She Y, Gopalan B, Huang DB, et al. PRMT5 dimethylates R30 of the p65 subunit to activate NF-kappaB. Proc Natl Acad Sci U S A 2013;110:13516-21.
11. Hsu JM, Chen CT, Chou CK, Kuo HP, Li LY, Lin CY, et al. Crosstalk between Arg 1175 methylation and Tyr 1173 phosphorylation negatively modulates EGFR-mediated ERK activation. Nat Cell Biol 2011;13:174-81.
12. Zheng S, Moehlenbrink J, Lu YC, Zalmas LP, Sagum CA, Carr S, et al. Arginine methylation-dependent reader-writer interplay governs growth control by E2F-1. Mol Cell 2013; 52: 37-51.
13. Jansson M, Durant ST, Cho EC, Sheahan S, Edelmann M, Kessler B, et al. Arginine methylation regulates the p53 response. Nat Cell Biol 2008;10:1431-9.
14. Sherr CJ, Roberts JM. Living with or without cyclins and cyclin-dependent kinases. Genes Dev 2004;18:2699-711.
15. Alt JR, Cleveland JL, Hannink M, Diehl JA. Phosphorylation-dependent regulation of cyclin D1 nuclear export and cyclin D1-dependent cellular transformation. Genes Dev 2000;14:3102-14.
16. Gladden AB, Woolery R, Aggarwal P, Wasik MA, Diehl JA. Expression of constitutively nuclear cyclin D1 in murine lymphocytes induces B-cell lymphoma. Oncogene 2006;25:998-1007.
17. Lin DI, Barbash O, Kumar KG, Weber JD, Harper JW, Klein-Szanto AJ, et al. Phosphorylation-dependent ubiquitination of cyclin D1 by the SCF(FBX4-alphaB crystallin) complex. Mol Cell 2006;24:355-66.
18. Jares P, Colomer D, Campo E. Molecular pathogenesis of mantle cell lymphoma. J Clin Invest 2012;122:3416-23.
19. Aggarwal P, Lessie MD, Lin DI, Pontano L, Gladden AB, Nuskey B, et al. Nuclear accumulation of cyclin D1 during S phase inhibits Cul4-dependent Cdt1 proteolysis and triggers p53-dependent DNA rereplication. Genes Dev 2007;21:2908-22.
20. Vaites LP, Lian Z, Lee EK, Yin B, DeMicco A, Bassing CH, et al. ATM defi ciency augments constitutively nuclear cyclin D1-driven genomic instability and lymphomagenesis. Oncogene 2014;33:129-33.
21. Benzeno S, Lu F, Guo M, Barbash O, Zhang F, Herman JG, et al. Identifi cation of mutations that disrupt phosphorylation-dependent nuclear export of cyclin D1. Oncogene 2006;25:6291-303.
22. Moreno-Bueno G, Rodriguez-Perales S, Sanchez-Estevez C, Hardis-son D, Sarrio D, Prat J, et al. Cyclin D1 gene (CCND1) mutations in endometrial cancer. Oncogene 2003;22:6115-8.
23. Halazonetis TD, Gorgoulis VG, Bartek J. An oncogene-induced DNA damage model for cancer development. Science 2008;319:1352-5.
24. Brady CA, Jiang D, Mello SS, Johnson TM, Jarvis LA, Kozak MM, et al. Distinct p53 transcriptional programs dictate acute DNA-damage responses and tumor suppression. Cell 2011;145:571-83.
25. Sperka T, Wang J, Rudolph KL. DNA damage checkpoints in stem cells, ageing and cancer. Nat Rev Mol Cell Biol 2012;13:579-90.
26. Vousden KH, Prives C. Blinded by the light: the growing complexity of p53. Cell 2009;137:413-31.
27. Chipuk JE, Kuwana T, Bouchier-Hayes L, Droin NM, Newmeyer DD, Schuler M, et al. Direct activation of Bax by p53 mediates mitochondrial membrane permeabilization and apoptosis. Science 2004;303:1010-4.
28. Muller PA, Vousden KH. Mutant p53 in cancer: new functions and therapeutic opportunities. Cancer Cell 2014;25:304-17.
29. Xu-Monette ZY, Medeiros LJ, Li Y, Orlowski RZ, Andreeff M, Bueso-Ramos CE, et al. Dysfunction of the TP53 tumor suppressor gene in lymphoid malignancies. Blood 2012;119:3668-83.
30. Peller S, Rotter V. TP53 in hematological cancer: low incidence of mutations with significant clinical relevance. Hum Mutat 2003; 21:277-84.
31. Cheung KJ, Horsman DE, Gascoyne RD. The signifi cance of TP53 in lymphoid malignancies: mutation prevalence, regulation, prognostic impact and potential as a therapeutic target. Br J Haematol 2009;146:257-69.
32. Branscombe TL, Frankel A, Lee JH, Cook JR, Yang Z, Pestka S, et al. PRMT5 (Janus kinase-binding protein 1) catalyzes the formation of symmetric dimethylarginine residues in proteins. J Biol Chem 2001;276:32971-6.
33. Sykes SM, Stanek TJ, Frank A, Murphy ME, McMahon SB. Acetyla-tion of the DNA binding domain regulates transcription-independent apoptosis by p53. J Biol Chem 2009;284:20197-205.
34. Cho EC, Zheng S, Munro S, Liu G, Carr SM, Moehlenbrink J, et al. Arginine methylation controls growth regulation by E2F-1. EMBO J 2012;31:1785-97.
35. Okano J, Snyder L, Rustgi AK. Genetic alterations in esophageal cancer. Methods Mol Biol 2003;222:131-45.
36. Karkhanis V, Hu YJ, Baiocchi RA, Imbalzano AN, Sif S. Versatility of PRMT5-induced methylation in growth control and development. Trends Biochem Sci 2011;36:633-41.
37. Xiong Y, Connolly T, Futcher B, Beach D. Human D-type cyclin. Cell 1991;65:691-9.
38. Motokura T, Bloom T, Kim HG, Juppner H, Ruderman JV, Kronen-berg HM, et al. A novel cyclin encoded by a bcl1-linked candidate oncogene. Nature 1991;350:512-5.
39. Blow JJ, Gillespie PJ. Replication licensing and cancer—a fatal entanglement? Nat Rev Cancer 2008;8:799-806.
40. Meek DW. Tumour suppression by p53: a role for the DNA damage response? Nat Rev Cancer 2009;9:714-23.
41. Wade M, Li YC, Wahl GM. MDM2, MDMX and p53 in oncogenesis and cancer therapy. Nat Rev Cancer 2013;13:83-96.
42. Eischen CM, Weber JD, Roussel MF, Sherr CJ, Cleveland JL. Disruption of the ARF-Mdm2-p53 tumor suppressor pathway in Myc-induced lymphomagenesis. Genes Dev 1999;13:2658-69.
43. McBride KA, Ballinger ML, Killick E, Kirk J, Tattersall MH, Eeles RA, et al. Li-Fraumeni syndrome: cancer risk assessment and clinical management. Nat Rev Clin Oncol 2014;11:260-71.
44. Ribeiro RC, Sandrini F, Figueiredo B, Zambetti GP, Michalkiewicz E, Lafferty AR, et al. An inherited p53 mutation that contributes in a tissue-specifi c manner to pediatric adrenal cortical carcinoma. Proc Natl Acad Sci U S A 2001;98:9330-5.
45. Chung J, Karkhanis V, Tae S, Yan F, Smith P, Ayers LW, et al. Protein arginine methyltransferase 5 (PRMT5) inhibition induces lymphoma cell death through reactivation of the retinoblastoma tumor suppressor pathway and polycomb repressor complex 2 (PRC2) silencing. J Biol Chem 2013;288:35534-47
46. Yan F, Alinari L, Lustberg ME, Katherine Martin L, Cordero-Nieves HM, Banasavadi-Siddegowda Y, et al. Genetic validation of the protein arginine methyltransferase PRMT5 as a candidate therapeutic target in glioblastoma. Cancer Res 2014;74:1752-65.
47. Chiang MY, Shestova O, Xu L, Aster JC, Pear WS. Divergent effects of supraphysiologic Notch signals on leukemia stem cells and hemat-opoietic stem cells. Blood 2013;121:905-17.
48. Xu K, Shimelis H, Linn DE, Jiang R, Yang X, Sun F , et al. Regulation of androgen receptor transcriptional activity and specificity by RNF6-induced ubiquitination. Cancer Cell 2009;15:270-82.