MTAP Deletions in Cancer Create Vulnerability to Targeting of the MAT2A/PRMT5/RIOK1 Axis

Cell Reports

Volumn 15, Issue 3, 2016, Pages 574-587

  Marjon, Katya ^a   Cameron, Michael J ^a   Quang, Phong ^a   Clasquin, Michelle F ^a   Mandley, Everton ^a   Kunii, Kaiko ^a,c   McVay, Michael ^a   Choe, Sung ^a   Kernytsky, Andrew ^a,b   Gross, Stefan ^a   Konteatis, Zenon ^a   Murtie, Joshua ^a   Blake, Michelle L ^a,d   Travins, Jeremy ^a   Dorsch, Marion ^a   Biller, Scott A ^a   Marks, Kevin M ^a  

^a AGIOS PHARMACEUTICALS   (United States)

^b CRISPR THERAPEUTICS   (United States)

^c EISAI INC   (United States)

^d SEATTLE GENETICS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

METHIONINE ADENOSYLTRANSFERASE II ALPHA; ONCOPROTEIN; PROTEIN PRMT5; PROTEIN RIOK1; S ADENOSYLMETHIONINE; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; 2-METHYLTHIOADENOSINE; 5'-METHYLTHIOADENOSINE PHOSPHORYLASE; AD034 ANTIGEN, HUMAN; ADENOSINE; MAT2A PROTEIN, HUMAN; METHIONINE ADENOSYLTRANSFERASE; MULTIPROTEIN COMPLEX; NUCLEOSIDE; PRMT5 PROTEIN, HUMAN; PROTEIN ARGININE METHYLTRANSFERASE; PROTEIN SERINE THREONINE KINASE; PURINE NUCLEOSIDE PHOSPHORYLASE; SMALL INTERFERING RNA; TUMOR ANTIGEN;

ARTICLE; BIOCHEMICAL COMPOSITION; CONTROLLED STUDY; ENZYME ACTIVITY; GENE DELETION; GENETIC SCREENING; LETHALITY; METABOLITE; METABOLOMICS; MTAP GENE; NEOPLASM; ONCOGENE; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN METHYLATION; PROTEIN TARGETING; SENSITIVITY ANALYSIS; ANALOGS AND DERIVATIVES; DEFICIENCY; ENZYMOLOGY; GENOMICS; HCT 116 CELL LINE; HUMAN; METABOLISM; SIGNAL TRANSDUCTION;

ADENOSINE; ANTIGENS, NEOPLASM; GENE DELETION; GENOMICS; HCT116 CELLS; HUMANS; METHIONINE ADENOSYLTRANSFERASE; MULTIPROTEIN COMPLEXES; NEOPLASMS; PROTEIN-ARGININE N-METHYLTRANSFERASES; PROTEIN-SERINE-THREONINE KINASES; PURINE-NUCLEOSIDE PHOSPHORYLASE; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; THIONUCLEOSIDES;

EID: 84962689154     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.03.043     Document Type: Article

References (49)

1. Andreu-Pérez P., Esteve-Puig R., de Torre-Minguela C., López-Fauqued M., Bech-Serra J.J., Tenbaum S., García-Trevijano E.R., Canals F., Merlino G., Avila M.A., Recio J.A. Protein arginine methyltransferase 5 regulates ERK1/2 signal transduction amplitude and cell fate through CRAF. Sci. Signal. 2011, 4:ra58.
2. Angermayr M., Roidl A., Bandlow W. Yeast Rio1p is the founding member of a novel subfamily of protein serine kinases involved in the control of cell cycle progression. Mol. Microbiol. 2002, 44:309-324.
3. Antonysamy S., Bonday Z., Campbell R.M., Doyle B., Druzina Z., Gheyi T., Han B., Jungheim L.N., Qian Y., Rauch C., et al. Crystal structure of the human PRMT5:MEP50 complex. Proc. Natl. Acad. Sci. USA 2012, 109:17960-17965.
4. Arrowsmith C.H., Bountra C., Fish P.V., Lee K., Schapira M. Epigenetic protein families: a new frontier for drug discovery. Nat. Rev. Drug Discov. 2012, 11:384-400.
5. Basu I., Locker J., Cassera M.B., Belbin T.J., Merino E.F., Dong X., Hemeon I., Evans G.B., Guha C., Schramm V.L. Growth and metastases of human lung cancer are inhibited in mouse xenografts by a transition state analogue of 5'-methylthioadenosine phosphorylase. J. Biol. Chem. 2011, 286:4902-4911.
6. Beroukhim R., Mermel C.H., Porter D., Wei G., Raychaudhuri S., Donovan J., Barretina J., Boehm J.S., Dobson J., Urashima M., et al. The landscape of somatic copy-number alteration across human cancers. Nature 2010, 463:899-905.
7. Bezzi M., Teo S.X., Muller J., Mok W.C., Sahu S.K., Vardy L.A., Bonday Z.Q., Guccione E. Regulation of constitutive and alternative splicing by PRMT5 reveals a role for Mdm4 pre-mRNA in sensing defects in the spliceosomal machinery. Genes Dev. 2013, 27:1903-1916.
8. Breitinger H.-G. Drug synergy-mechanisms and methods of analysis. Toxicity and Drug Testing 2012, InTech. http://www.intechopen.com/books/toxicity-and-drug-testing/drug-synergy-mechanisms-and-methods-of-analysis, W. Acree (Ed.).
9. Chan-Penebre E., Kuplast K.G., Majer C.R., Boriack-Sjodin P.A., Wigle T.J., Johnston L.D., Rioux N., Munchhof M.J., Jin L., Jacques S.L., et al. A selective inhibitor of PRMT5 with in vivo and in vitro potency in MCL models. Nat. Chem. Biol. 2015, 11:432-437.
10. Chilcote R.R., Brown E., Rowley J.D. Lymphoblastic leukemia with lymphomatous features associated with abnormalities of the short arm of chromosome 9. N. Engl. J. Med. 1985, 313:286-291.
11. Chung J., Karkhanis V., Tae S., Yan F., Smith P., Ayers L.W., Agostinelli C., Pileri S., Denis G.V., Baiocchi R.A., Sif S. 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, 288:35534-35547.
12. Enouf J., Lawrence F., Tempete C., Robert-Gero M., Lederer E. Relationship between inhibition of protein methylase I and inhibition of Rous sarcoma virus-induced cell transformation. Cancer Res. 1979, 39:4497-4502.
13. Frezza C., Zheng L., Folger O., Rajagopalan K.N., MacKenzie E.D., Jerby L., Micaroni M., Chaneton B., Adam J., Hedley A., et al. Haem oxygenase is synthetically lethal with the tumour suppressor fumarate hydratase. Nature 2011, 477:225-228.
14. Friesen W.J., Paushkin S., Wyce A., Massenet S., Pesiridis G.S., Van Duyne G., Rappsilber J., Mann M., Dreyfuss G. The methylosome, a 20S complex containing JBP1 and pICln, produces dimethylarginine-modified Sm proteins. Mol. Cell. Biol. 2001, 21:8289-8300.
15. Gu Z., Gao S., Zhang F., Wang Z., Ma W., Davis R.E., Wang Z. Protein arginine methyltransferase 5 is essential for growth of lung cancer cells. Biochem. J. 2012, 446:235-241.
16. Guderian G., Peter C., Wiesner J., Sickmann A., Schulze-Osthoff K., Fischer U., Grimmler M. RioK1, a new interactor of protein arginine methyltransferase 5 (PRMT5), competes with pICln for binding and modulates PRMT5 complex composition and substrate specificity. J. Biol. Chem. 2011, 286:1976-1986.
17. Hsu J.M., Chen C.T., Chou C.K., Kuo H.P., Li L.Y., Lin C.Y., Lee H.J., Wang Y.N., Liu M., Liao H.W., et al. Crosstalk between Arg 1175 methylation and Tyr 1173 phosphorylation negatively modulates EGFR-mediated ERK activation. Nat. Cell Biol. 2011, 13:174-181.
18. Kamijo T., Zindy F., Roussel M.F., Quelle D.E., Downing J.R., Ashmun R.A., Grosveld G., Sherr C.J. Tumor suppression at the mouse INK4a locus mediated by the alternative reading frame product p19ARF. Cell 1997, 91:649-659.
19. Kryukov G.V., Wilson F.H., Ruth J.R., Paulk J., Tsherniak A., Marlow S.E., Vazquez F., Weir B.A., Fitzgerald M.E., Tanaka M., et al. MTAP deletion confers enhanced dependency on the PRMT5 arginine methyltransferase in cancer cells. Science 2016, 351:1214-1218.
20. Lacroix M., El Messaoudi S., Rodier G., Le Cam A., Sardet C., Fabbrizio E. The histone-binding protein COPR5 is required for nuclear functions of the protein arginine methyltransferase PRMT5. EMBO Rep. 2008, 9:452-458.
21. Li W., Su D., Mizobuchi H., Martin D.S., Gu B., Gorlick R., Cole P., Bertino J.R. Status of methylthioadenosine phosphorylase and its impact on cellular response to L-alanosine and methylmercaptopurine riboside in human soft tissue sarcoma cells. Oncol. Res. 2004, 14:373-379.
22. Liu F., Cheng G., Hamard P.J., Greenblatt S., Wang L., Man N., Perna F., Xu H., Tadi M., Luciani L., Nimer S.D. Arginine methyltransferase PRMT5 is essential for sustaining normal adult hematopoiesis. J. Clin. Invest. 2015, 125:3532-3544.
23. Longshaw A.I., Adanitsch F., Gutierrez J.A., Evans G.B., Tyler P.C., Schramm V.L. Design and synthesis of potent "sulfur-free" transition state analogue inhibitors of 5'-methylthioadenosine nucleosidase and 5'-methylthioadenosine phosphorylase. J. Med. Chem. 2010, 53:6730-6746.
24. Lord C.J., Tutt A.N., Ashworth A. Synthetic lethality and cancer therapy: lessons learned from the development of PARP inhibitors. Annu. Rev. Med. 2015, 66:455-470.
25. Mavrakis K.J., McDonald E.R., Schlabach M.R., Billy E., Hoffman G.R., deWeck A., Ruddy D.A., Venkatesan K., Yu J., McAllister G., et al. Disordered methionine metabolism in MTAP/CDKN2A-deleted cancers leads to dependence on PRMT5. Science 2016, 351:1208-1213.
26. Meister G., Eggert C., Bühler D., Brahms H., Kambach C., Fischer U. Methylation of Sm proteins by a complex containing PRMT5 and the putative U snRNP assembly factor pICln. Curr. Biol. 2001, 11:1990-1994.
27. Muller F.L., Colla S., Aquilanti E., Manzo V.E., Genovese G., Lee J., Eisenson D., Narurkar R., Deng P., Nezi L., et al. Passenger deletions generate therapeutic vulnerabilities in cancer. Nature 2012, 488:337-342.
28. Muller F.L., Aquilanti E.A., DePinho R.A. Collateral lethality: a new therapeutic strategy in oncology. Trends Cancer 2015, 1:161-173.
29. Pagliarini D.J., Calvo S.E., Chang B., Sheth S.A., Vafai S.B., Ong S.E., Walford G.A., Sugiana C., Boneh A., Chen W.K., et al. A mitochondrial protein compendium elucidates complex I disease biology. Cell 2008, 134:112-123.
30. Parsons D.W., Jones S., Zhang X., Lin J.C., Leary R.J., Angenendt P., Mankoo P., Carter H., Siu I.M., Gallia G.L., et al. An integrated genomic analysis of human glioblastoma multiforme. Science 2008, 321:1807-1812.
31. Pesiridis G.S., Diamond E., Van Duyne G.D. Role of pICLn in methylation of Sm proteins by PRMT5. J. Biol. Chem. 2009, 284:21347-21359.
32. Pollack B.P., Kotenko S.V., He W., Izotova L.S., Barnoski B.L., Pestka S. The human homologue of the yeast proteins Skb1 and Hsl7p interacts with Jak kinases and contains protein methyltransferase activity. J. Biol. Chem. 1999, 274:31531-31542.
33. Ren J., Wang Y., Liang Y., Zhang Y., Bao S., Xu Z. Methylation of ribosomal protein S10 by protein-arginine methyltransferase 5 regulates ribosome biogenesis. J. Biol. Chem. 2010, 285:12695-12705.
34. Richon V.M., Johnston D., Sneeringer C.J., Jin L., Majer C.R., Elliston K., Jerva L.F., Scott M.P., Copeland R.A. Chemogenetic analysis of human protein methyltransferases. Chem. Biol. Drug Des. 2011, 78:199-210.
35. Ruefli-Brasse A., Sakamoto D., Orf J., Rong M., Shi J., Carlson T., Quon K., Kamb A., Wickramasinghe D. Methylthioadenosine (MTA) rescues methylthioadenosine phosphorylase (MTAP)-deficient tumors from purine synthesis inhibition in vivo via non-autonomous adenine supply. J. Cancer Ther. 2011, 2:523-534.
36. Serrano M., Hannon G.J., Beach D. A new regulatory motif in cell-cycle control causing specific inhibition of cyclin D/CDK4. Nature 1993, 366:704-707.
37. Stevens A.P., Dettmer K., Kirovski G., Samejima K., Hellerbrand C., Bosserhoff A.K., Oefner P.J. Quantification of intermediates of the methionine and polyamine metabolism by liquid chromatography-tandem mass spectrometry in cultured tumor cells and liver biopsies. J. Chromatogr. A 2010, 1217:3282-3288.
38. Sun L., Wang M., Lv Z., Yang N., Liu Y., Bao S., Gong W., Xu R.M. Structural insights into protein arginine symmetric dimethylation by PRMT5. Proc. Natl. Acad. Sci. USA 2011, 108:20538-20543.
39. Tee W.W., Pardo M., Theunissen T.W., Yu L., Choudhary J.S., Hajkova P., Surani M.A. Prmt5 is essential for early mouse development and acts in the cytoplasm to maintain ES cell pluripotency. Genes Dev. 2010, 24:2772-2777.
40. Thiele I., Swainston N., Fleming R.M., Hoppe A., Sahoo S., Aurich M.K., Haraldsdottir H., Mo M.L., Rolfsson O., Stobbe M.D., et al. A community-driven global reconstruction of human metabolism. Nat. Biotechnol. 2013, 31:419-425.
41. Vance D.E., Walkey C.J., Cui Z. Phosphatidylethanolamine N-methyltransferase from liver. Biochim. Biophys. Acta 1997, 1348:142-150.
42. Widmann B., Wandrey F., Badertscher L., Wyler E., Pfannstiel J., Zemp I., Kutay U. The kinase activity of human Rio1 is required for final steps of cytoplasmic maturation of 40S subunits. Mol. Biol. Cell 2012, 23:22-35.
43. Wiederschain D., Wee S., Chen L., Loo A., Yang G., Huang A., Chen Y., Caponigro G., Yao Y.M., Lengauer C., et al. Single-vector inducible lentiviral RNAi system for oncology target validation. Cell Cycle 2009, 8:498-504.
44. Wilczek C., Chitta R., Woo E., Shabanowitz J., Chait B.T., Hunt D.F., Shechter D. Protein arginine methyltransferase Prmt5-Mep50 methylates histones H2A and H4 and the histone chaperone nucleoplasmin in Xenopus laevis eggs. J. Biol. Chem. 2011, 286:42221-42231.
45. Williams K.T., Schalinske K.L. New insights into the regulation of methyl group and homocysteine metabolism. J. Nutr. 2007, 137:311-314.
46. Yan F., Alinari L., Lustberg M.E., Martin L.K., Cordero-Nieves H.M., Banasavadi-Siddegowda Y., Virk S., Barnholtz-Sloan J., Bell E.H., Wojton J., et al. Genetic validation of the protein arginine methyltransferase PRMT5 as a candidate therapeutic target in glioblastoma. Cancer Res. 2014, 74:1752-1765.
47. Zappia V., Della Ragione F., Pontoni G., Gragnaniello V., Cartenì-Farina M. Human 5'-deoxy-5'-methylthioadenosine phosphorylase: kinetic studies and catalytic mechanism. Adv. Exp. Med. Biol. 1988, 250:165-177.
48. Zhang H., Chen Z.H., Savarese T.M. Codeletion of the genes for p16INK4, methylthioadenosine phosphorylase, interferon-alpha1, interferon-beta1, and other 9p21 markers in human malignant cell lines. Cancer Genet. Cytogenet. 1996, 86:22-28.
49. Zhang T., Günther S., Looso M., Künne C., Krüger M., Kim J., Zhou Y., Braun T. Prmt5 is a regulator of muscle stem cell expansion in adult mice. Nat. Commun. 2015, 6:7140.