KRAS Engages AGO2 to Enhance Cellular Transformation

Cell Reports

Volumn 14, Issue 6, 2016, Pages 1448-1461

  Shankar, Sunita ^a   Pitchiaya, Sethuramasundaram ^a   Malik, Rohit ^a   Kothari, Vishal ^a   Hosono, Yasuyuki ^a   Yocum, Anastasia K ^a   Gundlapalli, Harika ^a   White, Yasmine ^b   Firestone, Ari ^b   Cao, Xuhong ^a   Dhanasekaran, Saravana M ^a   Stuckey, Jeanne A ^a   Bollag, Gideon ^c   Shannon, Kevin ^b   Walter, Nils G ^a   Kumar Sinha, Chandan ^a   Chinnaiyan, Arul M ^a  

^a UNIVERSITY OF MICHIGAN   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c PLEXXIKON INC   (United States)

Author keywords

Argonaute 2; Cancer; EIF2C2; KRAS; RNA silencing

Indexed keywords

ARGONAUTE 2 PROTEIN; K RAS PROTEIN; ARGONAUTE PROTEIN; CARBOXYPEPTIDASE; EIF2C2 PROTEIN, HUMAN; KRAS PROTEIN, HUMAN; MICRORNA; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN BINDING; PROTEIN P21; SCPEP1 PROTEIN, HUMAN; SMALL INTERFERING RNA;

3T3 CELL LINE; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CELL PROLIFERATION; CELL TRANSFORMATION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM; GENE SILENCING; IMMUNOPRECIPITATION; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PATHOLOGY; TRANSGENE;

ANIMALS; ARGONAUTE PROTEINS; BASE SEQUENCE; CARBOXYPEPTIDASES; CELL TRANSFORMATION, NEOPLASTIC; ENDOPLASMIC RETICULUM; GENE EXPRESSION REGULATION, NEOPLASTIC; GENE SILENCING; HUMANS; MICE; MICRORNAS; MOLECULAR SEQUENCE DATA; MUTATION; NIH 3T3 CELLS; PHOSPHATIDYLINOSITOL 3-KINASES; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS P21(RAS); RNA, SMALL INTERFERING; TRANSGENES;

EID: 84958125884     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2016.01.034     Document Type: Article

References (70)

1. Baines A.T., Xu D., Der C.J. Inhibition of Ras for cancer treatment: the search continues. Future Med. Chem. 2011, 3:1787-1808.
2. Balmain A., Pragnell I.B. Mouse skin carcinomas induced in vivo by chemical carcinogens have a transforming Harvey-ras oncogene. Nature 1983, 303:72-74.
3. Barceló C., Etchin J., Mansour M.R., Sanda T., Ginesta M.M., Sanchez-Arévalo Lobo V.J., Real F.X., Capellà G., Estanyol J.M., Jaumot M., et al. Ribonucleoprotein HNRNPA2B1 interacts with and regulates oncogenic KRAS in pancreatic ductal adenocarcinoma cells. Gastroenterology 2014, 147:882-892.e8.
4. Benhamed M., Herbig U., Ye T., Dejean A., Bischof O. Senescence is an endogenous trigger for microRNA-directed transcriptional gene silencing in human cells. Nat. Cell Biol. 2012, 14:266-275.
5. Bivona T.G., Quatela S.E., Bodemann B.O., Ahearn I.M., Soskis M.J., Mor A., Miura J., Wiener H.H., Wright L., Saba S.G., et al. PKC regulates a farnesyl-electrostatic switch on K-Ras that promotes its association with Bcl-XL on mitochondria and induces apoptosis. Mol. Cell 2006, 21:481-493.
6. Brenner J.C., Ateeq B., Li Y., Yocum A.K., Cao Q., Asangani I.A., Patel S., Wang X., Liang H., Yu J., et al. Mechanistic rationale for inhibition of poly(ADP-ribose) polymerase in ETS gene fusion-positive prostate cancer. Cancer Cell 2011, 19:664-678.
7. Broderick J.A., Salomon W.E., Ryder S.P., Aronin N., Zamore P.D. Argonaute protein identity and pairing geometry determine cooperativity in mammalian RNA silencing. RNA 2011, 17:1858-1869.
8. Burns M.C., Sun Q., Daniels R.N., Camper D., Kennedy J.P., Phan J., Olejniczak E.T., Lee T., Waterson A.G., Rossanese O.W., Fesik S.W. Approach for targeting Ras with small molecules that activate SOS-mediated nucleotide exchange. Proc. Natl. Acad. Sci. USA 2014, 111:3401-3406.
9. Cao Q., Wang X., Zhao M., Yang R., Malik R., Qiao Y., Poliakov A., Yocum A.K., Li Y., Chen W., et al. The central role of EED in the orchestration of polycomb group complexes. Nat. Commun. 2014, 5:3127.
10. Cheng C.M., Li H., Gasman S., Huang J., Schiff R., Chang E.C. Compartmentalized Ras proteins transform NIH 3T3 cells with different efficiencies. Mol. Cell. Biol. 2011, 31:983-997.
11. Cichowski K., Jacks T. NF1 tumor suppressor gene function: narrowing the GAP. Cell 2001, 104:593-604.
12. Catalog of Somatic Mutations in Cancer, COSMIC Release v66 2013, COSMIC, Wellcome Trust Sanger Institute.
13. Cox A.D., Der C.J. Ras history: The saga continues. Small GTPases 2010, 1:2-27.
14. Czech B., Hannon G.J. Small RNA sorting: matchmaking for Argonautes. Nat. Rev. Genet. 2011, 12:19-31.
15. DeFeo D., Gonda M.A., Young H.A., Chang E.H., Lowy D.R., Scolnick E.M., Ellis R.W. Analysis of two divergent rat genomic clones homologous to the transforming gene of Harvey murine sarcoma virus. Proc. Natl. Acad. Sci. USA 1981, 78:3328-3332.
16. Diederichs S., Haber D.A. Dual role for argonautes in microRNA processing and posttranscriptional regulation of microRNA expression. Cell 2007, 131:1097-1108.
17. Downward J. Targeting RAS signalling pathways in cancer therapy. Nat. Rev. Cancer 2003, 3:11-22.
18. Drosten M., Dhawahir A., Sum E.Y., Urosevic J., Lechuga C.G., Esteban L.M., Castellano E., Guerra C., Santos E., Barbacid M. Genetic analysis of Ras signalling pathways in cell proliferation, migration and survival. EMBO J. 2010, 29:1091-1104.
19. Dudley N.R., Goldstein B. RNA interference: silencing in the cytoplasm and nucleus. Curr. Opin. Mol. Ther. 2003, 5:113-117.
20. Gagnon K.T., Li L., Chu Y., Janowski B.A., Corey D.R. RNAi factors are present and active in human cell nuclei. Cell Rep. 2014, 6:211-221.
21. Goldfinger L.E., Ptak C., Jeffery E.D., Shabanowitz J., Han J., Haling J.R., Sherman N.E., Fox J.W., Hunt D.F., Ginsberg M.H. An experimentally derived database of candidate Ras-interacting proteins. J. Proteome Res. 2007, 6:1806-1811.
22. Gysin S., Salt M., Young A., McCormick F. Therapeutic strategies for targeting ras proteins. Genes Cancer 2011, 2:359-372.
23. Hand P.H., Thor A., Wunderlich D., Muraro R., Caruso A., Schlom J. Monoclonal antibodies of predefined specificity detect activated ras gene expression in human mammary and colon carcinomas. Proc. Natl. Acad. Sci. USA 1984, 81:5227-5231.
24. Höck J., Weinmann L., Ender C., Rüdel S., Kremmer E., Raabe M., Urlaub H., Meister G. Proteomic and functional analysis of Argonaute-containing mRNA-protein complexes in human cells. EMBO Rep. 2007, 8:1052-1060.
25. Horman S.R., Janas M.M., Litterst C., Wang B., MacRae I.J., Sever M.J., Morrissey D.V., Graves P., Luo B., Umesalma S., et al. Akt-mediated phosphorylation of argonaute 2 downregulates cleavage and upregulates translational repression of MicroRNA targets. Mol. Cell 2013, 50:356-367.
26. Jeng H.H., Taylor L.J., Bar-Sagi D. Sos-mediated cross-activation of wild-type Ras by oncogenic Ras is essential for tumorigenesis. Nat. Commun. 2012, 3:1168.
27. Johnson S.M., Grosshans H., Shingara J., Byrom M., Jarvis R., Cheng A., Labourier E., Reinert K.L., Brown D., Slack F.J. RAS is regulated by the let-microRNA family. Cell 2005, 120:635-647.
28. Karachaliou N., Mayo C., Costa C., Magrí I., Gimenez-Capitan A., Molina-Vila M.A., Rosell R. KRAS mutations in lung cancer. Clin. Lung Cancer 2013, 14:205-214.
29. Karnoub A.E., Weinberg R.A. Ras oncogenes: split personalities. Nat. Rev. Mol. Cell Biol. 2008, 9:517-531.
30. Kim Y.J., Maizel A., Chen X. Traffic into silence: endomembranes and post-transcriptional RNA silencing. EMBO J. 2014, 33:968-980.
31. Kwak P.B., Tomari Y. The N domain of Argonaute drives duplex unwinding during RISC assembly. Nat. Struct. Mol. Biol. 2012, 19:145-151.
32. Lampson B.L., Pershing N.L., Prinz J.A., Lacsina J.R., Marzluff W.F., Nicchitta C.V., MacAlpine D.M., Counter C.M. Rare codons regulate KRas oncogenesis. Curr. Biol. 2013, 23:70-75.
33. Lauchle J.O., Braun B.S., Loh M.L., Shannon K. Inherited predispositions and hyperactive Ras in myeloid leukemogenesis. Pediatr. Blood Cancer 2006, 46:579-585.
34. Lee Y.S., Dutta A. The tumor suppressor microRNA let-represses the HMGA2 oncogene. Genes Dev. 2007, 21:1025-1030.
35. Löhr M., Klöppel G., Maisonneuve P., Lowenfels A.B., Lüttges J. Frequency of K-ras mutations in pancreatic intraductal neoplasias associated with pancreatic ductal adenocarcinoma and chronic pancreatitis: a meta-analysis. Neoplasia 2005, 7:17-23.
36. Lu J., Getz G., Miska E.A., Alvarez-Saavedra E., Lamb J., Peck D., Sweet-Cordero A., Ebert B.L., Mak R.H., Ferrando A.A., et al. MicroRNA expression profiles classify human cancers. Nature 2005, 435:834-838.
37. MacRae I.J., Ma E., Zhou M., Robinson C.V., Doudna J.A. In vitro reconstitution of the human RISC-loading complex. Proc. Natl. Acad. Sci. USA 2008, 105:512-517.
38. Margarit S.M., Sondermann H., Hall B.E., Nagar B., Hoelz A., Pirruccello M., Bar-Sagi D., Kuriyan J. Structural evidence for feedback activation by Ras.GTP of the Ras-specific nucleotide exchange factor SOS. Cell 2003, 112:685-695.
39. McCarthy N. MicroRNA: lacking in maturity. Nat. Rev. Cancer 2013, 13:377.
40. Meister G., Landthaler M., Peters L., Chen P.Y., Urlaub H., Lührmann R., Tuschl T. Identification of novel argonaute-associated proteins. Curr. Biol. 2005, 15:2149-2155.
41. Ostrem J.M., Peters U., Sos M.L., Wells J.A., Shokat K.M. K-Ras(G12C) inhibitors allosterically control GTP affinity and effector interactions. Nature 2013, 503:548-551.
42. Paroo Z., Ye X., Chen S., Liu Q. Phosphorylation of the human microRNA-generating complex mediates MAPK/Erk signaling. Cell 2009, 139:112-122.
43. Pershing N.L., Lampson B.L., Belsky J.A., Kaltenbrun E., MacAlpine D.M., Counter C.M. Rare codons capacitate Kras-driven de novo tumorigenesis. J. Clin. Invest. 2015, 125:222-233.
44. Peters L., Meister G. Argonaute proteins: mediators of RNA silencing. Mol. Cell 2007, 26:611-623.
45. Pitchiaya S., Androsavich J.R., Walter N.G. Intracellular single molecule microscopy reveals two kinetically distinct pathways for microRNA assembly. EMBO Rep. 2012, 13:709-715.
46. Pitchiaya S., Krishnan V., Custer T.C., Walter N.G. Dissecting non-coding RNA mechanisms in cellulo by Single-molecule High-Resolution Localization and Counting. Methods 2013, 63:188-199.
47. Prior I.A., Hancock J.F. Ras trafficking, localization and compartmentalized signalling. Semin. Cell Dev. Biol. 2012, 23:145-153.
48. Pylayeva-Gupta Y., Grabocka E., Bar-Sagi D. RAS oncogenes: weaving a tumorigenic web. Nat. Rev. Cancer 2011, 11:761-774.
49. Qiu R.G., Chen J., Kirn D., McCormick F., Symons M. An essential role for Rac in Ras transformation. Nature 1995, 374:457-459.
50. Rakotondrafara A.M., Hentze M.W. An efficient factor-depleted mammalian in vitro translation system. Nat. Protoc. 2011, 6:563-571.
51. Ran F.A., Hsu P.D., Wright J., Agarwala V., Scott D.A., Zhang F. Genome engineering using the CRISPR-Cas9 system. Nat. Protoc. 2013, 8:2281-2308.
52. Rüdel S., Flatley A., Weinmann L., Kremmer E., Meister G. A multifunctional human Argonaute2-specific monoclonal antibody. RNA 2008, 14:1244-1253.
53. Rüdel S., Wang Y., Lenobel R., Körner R., Hsiao H.H., Urlaub H., Patel D., Meister G. Phosphorylation of human Argonaute proteins affects small RNA binding. Nucleic Acids Res. 2011, 39:2330-2343.
54. Schubbert S., Shannon K., Bollag G. Hyperactive Ras in developmental disorders and cancer. Nat. Rev. Cancer 2007, 7:295-308.
55. Shaw R.J., Cantley L.C. Ras, PI(3)K and mTOR signalling controls tumour cell growth. Nature 2006, 441:424-430.
56. Shen J., Xia W., Khotskaya Y.B., Huo L., Nakanishi K., Lim S.O., Du Y., Wang Y., Chang W.C., Chen C.H., et al. EGFR modulates microRNA maturation in response to hypoxia through phosphorylation of AGO2. Nature 2013, 497:383-387.
57. Shieh A., Ward A.F., Donlan K.L., Harding-Theobald E.R., Xu J., Mullighan C.G., Zhang C., Chen S.C., Su X., Downing J.R., et al. Defective K-Ras oncoproteins overcome impaired effector activation to initiate leukemia in vivo. Blood 2013, 121:4884-4893.
58. Shih C., Padhy L.C., Murray M., Weinberg R.A. Transforming genes of carcinomas and neuroblastomas introduced into mouse fibroblasts. Nature 1981, 290:261-264.
59. Spiegel J., Cromm P.M., Zimmermann G., Grossmann T.N., Waldmann H. Small-molecule modulation of Ras signaling. Nat. Chem. Biol. 2014, 10:613-622.
60. Stalder L., Heusermann W., Sokol L., Trojer D., Wirz J., Hean J., Fritzsche A., Aeschimann F., Pfanzagl V., Basselet P., et al. The rough endoplasmatic reticulum is a central nucleation site of siRNA-mediated RNA silencing. EMBO J. 2013, 32:1115-1127.
61. Stephen A.G., Esposito D., Bagni R.K., McCormick F. Dragging ras back in the ring. Cancer Cell 2014, 25:272-281.
62. Sun Q., Burke J.P., Phan J., Burns M.C., Olejniczak E.T., Waterson A.G., Lee T., Rossanese O.W., Fesik S.W. Discovery of small molecules that bind to K-Ras and inhibit Sos-mediated activation. Angew. Chem. Int. Ed. Engl. 2012, 51:6140-6143.
63. Sweet R.W., Yokoyama S., Kamata T., Feramisco J.R., Rosenberg M., Gross M. The product of ras is a GTPase and the T24 oncogenic mutant is deficient in this activity. Nature 1984, 311:273-275.
64. Symonds J.M., Ohm A.M., Carter C.J., Heasley L.E., Boyle T.A., Franklin W.A., Reyland M.E. Protein kinase C δ is a downstream effector of oncogenic K-ras in lung tumors. Cancer Res. 2011, 71:2087-2097.
65. Trahey M., McCormick F. A cytoplasmic protein stimulates normal N-ras p21 GTPase, but does not affect oncogenic mutants. Science 1987, 238:542-545.
66. Vasilescu J., Guo X., Kast J. Identification of protein-protein interactions using in vivo cross-linking and mass spectrometry. Proteomics 2004, 4:3845-3854.
67. Wang B., Li S., Qi H.H., Chowdhury D., Shi Y., Novina C.D. Distinct passenger strand and mRNA cleavage activities of human Argonaute proteins. Nat. Struct. Mol. Biol. 2009, 16:1259-1266.
68. Wilson R.C., Doudna J.A. Molecular mechanisms of RNA interference. Annu. Rev. Biophys. 2013, 42:217-239.
69. Yang M., Haase A.D., Huang F.K., Coulis G., Rivera K.D., Dickinson B.C., Chang C.J., Pappin D.J., Neubert T.A., Hannon G.J., et al. Dephosphorylation of tyrosine 393 in argonaute 2 by protein tyrosine phosphatase 1B regulates gene silencing in oncogenic RAS-induced senescence. Mol. Cell 2014, 55:782-790.
70. Zeng Y., Sankala H., Zhang X., Graves P.R. Phosphorylation of Argonaute 2 at serine-387 facilitates its localization to processing bodies. Biochem. J. 2008, 413:429-436.