Identification of a long non-coding RNA-associated RNP complex regulating metastasis at the translational step

EMBO Journal

Volumn 32, Issue 20, 2013, Pages 2672-2684

  Gumireddy, Kiranmai ^a   Li, Anping ^a   Yan, Jinchun ^b   Setoyama, Tetsuro ^c   Johannes, Gregg J ^d   Ørom, Ulf A ^e   Tchou, Julia ^f   Liu, Qin ^a   Zhang, Lin ^f   Speicher, David W ^a   Calin, George A ^c   Huang, Qihong ^a  

^a WISTAR INSTITUTE   (United States)

^b UNIVERSITY OF WASHINGTON MEDICAL CENTER   (United States)

^c UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

^d DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

^e MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

^f UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

metastasis; non coding RNA; translation

Indexed keywords

LONG UNTRANSLATED RNA; MESSENGER RNA; RIBONUCLEOPROTEIN; RNA BINDING PROTEIN; UVOMORULIN;

3' UNTRANSLATED REGION; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BREAST CANCER; DOWN REGULATION; GENETIC ASSOCIATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LYMPH NODE METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROCESSING; RNA ANALYSIS; RNA TRANSLATION; TRANSLATION REGULATION; TUMOR INVASION; UPREGULATION;

ANIMALS; FEMALE; GENE EXPRESSION REGULATION, NEOPLASTIC; HEK293 CELLS; HUMANS; MICE; MICE, INBRED NOD; MICE, SCID; MULTIPROTEIN COMPLEXES; NEOPLASM METASTASIS; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; RIBONUCLEOPROTEINS; RNA, LONG NONCODING; TUMOR CELLS, CULTURED;

EID: 84885852048     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2013.188     Document Type: Article

References (92)

1. Azzalin CM, Reichenbach P, Khoriauli L, Giulotto E, Lingner J (2007) Telomeric repeat containing RNA and RNA surveillance factors at mammalian chromosome ends. Science 318: 798-801
2. Banfei B, Jia H, Khatun J, Wood E, Risk B, Gundling Jr WE, Kundaje A, Gunawardena HP, Yu Y, Xie L, Krajewski K, Strahl BD, Che X, Bickle P, Giddings MC, Brown JB, Lipovich L (2012) Long noncoding RNAs are rarely translated in two human cell lines. Genome Res 22: 1646-1657
3. Bartel DP (2009) MicroRNAs: Target recognition and regulatory functions. Cell 136: 215-233
4. Bellucci M, Agostini F, Masin M, Tartaglia GG (2011) Predicting protein associations with long noncoding RNAs. Nat Methods 8: 444-445
5. Beltran M, Puig I, Pena C, Garcia JM, Alvarez AB, Pena R, Bonilla F, de Herreros AG (2008) A natural antisense transcript regulates Zeb2/Sip1 gene expression during Snail1-induced epithelial-mesenchymal transition. Genes Dev 22: 756-769
6. Benetatos L, Hatzimichael E, Dasoula A, Dranitsaris G, Tsiara S, Syrrou M, Georgiou I, Bourantas KL (2010) CpG methylation analysis of theMEG3 and SNRPN imprinted genes in acute myeloid leukemia and myelodysplastic syndromes. Leuk Res 34: 148-153
7. Bernard D, Prasanth KV, Tripathi V, Colasse S, Nakamura T, Xuan Z, Zhang MQ, Sedel F, Jourdren L, Coulpier F, Triller A, Spector DL, Bessis A (2010) A long nuclear-retained non-coding RNA regulates synaptogenesis by modulating gene expression. EMBO J 29: 3082-3093
8. Bomsztyk K, Denisenko O, Ostrowski J (2004) hnRNP K: One protein multiple processes. Bioessays 26: 629-638
9. Cabili MN, Trapnell C, Goff L, Koziol M, Tazon-Vega B, Regev A, Rinn JL (2011) Integrative annotation of human large intergenic noncoding RNAs reveals global properties and specific subclasses. Genes Dev 25: 1915-1927
10. Calin GA, Croce CM (2006) MicroRNA signatures in human cancers. Nat Rev Cancer 6: 857-866
11. Calin GA, Liu CG, Ferracin M, Hyslop T, Spizzo R, Sevignani C, Fabbri M, Cimmino A, Lee EJ, Wojcik SE, Shimizu M, Tili E, Rossi S, Taccioli C, Pichiorri F, Liu X, Zupo S, Herlea V, Gramantieri L, Lanza G et al (2007) Ultraconserved regions encoding ncRNAs are altered in human leukemias and carcinomas. Cancer Cell 12: 215-229
12. Ceman S, Brown V, Warren ST (1999) Isolation of an FMRPassociated messenger ribonucleoprotein particle and identification of nucleolin and the fragile X-related proteins as components of the complex. Mol Cell Biol 19: 7925-7932
13. Cesana M, Cacchiarelli D, Legnini I, Santini T, Sthandier O, Chinappi M, Tramontano A, Bozzoni I (2011) A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell 147: 358-369
14. Chang XB, Mengos A, Hou YX, Cui L, Jensen TJ, Aleksandrov A, Riordan JR, Gentzsch M (2008) Role of N-linked oligosaccharides in the biosynthetic processing of the cystic fibrosis membrane conductance regulator. J Cell Sci 121: 2814-2823
15. Chaudhury A, Hussey GS, Ray PS, Jin G, Fox PL, Howe PH (2010) TGF-beta-mediated phosphorylation of hnRNP E1 induces EMT via transcript-selective translational induction of Dab2 and ILEI. Nat Cell Biol 12: 286-293
16. Cook LM, Hurst DR, Welch DR (2011) Metastasis suppressors and the tumor microenvironment. Semin Cancer Biol 21: 113-122
17. Corsini L, Hothorn M, Stier G, Rybin V, Scheffzek K, Gibson TJ, Sattler M (2009) Dimerization and protein binding specificity of the U2AF homology motif of the splicing factor Puf60. J Biol Chem 284: 630-639
18. Ebert MS, Sharp PA (2010) Emerging roles for natural microRNA sponges. Curr Biol 20: R858-R861.
19. Eiring AM, Harb JG, Neviani P, Garton C, Oaks JJ, Spizzo R, Liu S, Schwind S, Santhanam R, Hickey CJ, Becker H, Chandler JC, Andino R, Cortes J, Hokland P, Huettner CS, Bhatia R, Roy DC, Liebhaber SA, Caligiuri MA et al (2010) miR-328 functions as an RNA decoy to modulate hnRNP E2 regulation of mRNA translation in leukemic blasts. Cell 140: 652-665
20. Evdokimova V, Ruzanov P, Imataka H, Raught B, Svitkin Y, Ovchinnikov LP, Sonenberg N (2001) The major mRNA-associated protein YB-1 is a potent 50 cap-dependent mRNA stabilizer. EMBO J 20: 5491-5502
21. Faghihi MA, Modarresi F, Khalil AM, Wood DE, Sahagan BG, Morgan TE, Finch St CE, Laurent 3rd G, Kenny PJ, Wahlestedt C (2008) Expression of a noncoding RNA is elevated in Alzheimers disease and drives rapid feed-forward regulation of beta-secretase. Nat Med 14: 723-730
22. Filipowicz W, Bhattacharyya SN, Sonenberg N (2008) Mechanisms of post-transcriptional regulation by microRNAs: Are the answers in sight Nat Rev Genet 9: 102-114
23. Flynn RL, Centore RC, OSullivan RJ, Rai R, Tse A, Songyang Z, Chang S, Karlseder J, Zou L (2011) TERRA and hnRNPA1 orchestrate an RPA-to-POT1 switch on telomeric single-stranded DNA. Nature 471: 532-536
24. Friend K, Campbell ZT, Cooke A, Kroll-Conner P, Wickens MP, Kimble J (2012) A conserved PUF-Ago-eEF1A complex attenuates translation elongation. Nat Struct Mol Biol 19: 176-183
25. Fukaya T, Tomari Y (2012) MicroRNAs mediate gene silencing via multiple different pathways in drosophila. Mol Cell 48: 825-836
26. Gebauer F, Hentze MW (2004) Molecular mechanisms of translational control. Nat Rev Mol Cell Biol 5: 827-835
27. Glisovic T, Bachorik JL, Yong J, Dreyfuss G (2008) RNA-binding proteins and post-transcriptional gene regulation. FEBS Lett 582: 1977-1986
28. Gong C, Maquat LE (2011) lncRNAs transactivate STAU1-mediated mRNA decay by duplexing with 30 UTRs via Alu elements. Nature 470: 284-288
29. Gumireddy K, Li A, Gimotty PA, Klein-Szanto AJ, Showe LC, Katsaros D, Coukos G, Zhang L, Huang Q (2009) KLF17 is a negative regulator of epithelial-mesenchymal transition and metastasis in breast cancer. Nat Cell Biol 11: 1297-1304
30. Guo H, Ingolia NT, Weissman JS, Bartel DP (2010) Mammalian microRNAs predominantly act to decrease target mRNA level. Nature 466: 835-840
31. Gupta RA, Shah N, Wang KC, Kim J, Horlings HM, Wong DJ, Tsai MC, Hung T, Argani P, Rinn JL, Wang Y, Brzoska P, Kong B, Li R, West RB, van de Vijver MJ, Sukumar S, Chang HY (2010) Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 464: 1071-1076
32. GuttmanM, Donaghey J, Carey BW, GarberM, Grenier JK, Munson G, Young G, Lucas AB, Ach R, Bruhn L, Yang X, Amit I, Meissner A, Regev A, Rinn JL, Root DE, Lander ES (2011) lincRNAs act in the circuitry controlling pluripotency and differentiation. Nature 477: 295-300
33. Guttman M, Russell P, Ingolia NT, Weissman JS, Lander ES (2013) Ribosome profiling provides evidence that large noncoding RNAs do not code proteins. Cell 154: 240-251
34. Harismendy O, Notani D, Song X, Rahim NG, Tanasa B, Heintzman N, Ren B, Fu XD, Topol EJ, Rosenfeld MG, Frazer KA (2011) 9p21 DNA variants associated with coronary artery disease impair interferongamma signalling response. Nature 470: 264-268
35. He L, He X, Lowe SW, Hannon GJ (2007) microRNAs join the p53 network-another piece in the tumour-suppression puzzle. Nat Rev Cancer 7: 819-822
36. Heo JB, Sung S (2011) Vernalization-mediated epigenetic silencing by a long intronic noncoding RNA. Science 331: 76-79
37. Hoogeveen AT, Willemsen R, Oostra BA (2002) Fragile X syndrome, the Fragile X related proteins, and animal models. Microsc Res Tech 57: 148-155
38. Huarte M, Guttman M, Feldser D, Garber M, Koziol MJ, Kenzelmann-Broz D, Khalil AM, Zuk O, Amit I, Rabani M, Attardi LD, Regev A, Lander ES, Jacks T, Rinn JL (2010) A large intergenic noncoding RNA induced by p53 mediates global gene repression in the p53 response. Cell 142: 409-419
39. Hussey GS, Chaudhury A, Dawson AE, Lindner DJ, Knudsen CR, Wilce MC, Merrick WC, Howe PH (2011) Identification of an mRNP complex regulating tumorigenesis at the translational elongation step. Mol Cell 41: 419-431
40. Jackson RJ, Hellen CU, Pestova TV (2010) The mechanism of eukaryotic translation initiation and principles of its regulation. Nat Rev Mol Cell Biol 11: 113-127
41. Jin P, Warren ST (2000) Understanding the molecular basis of fragile X syndrome. Hum Mol Genet 9: 901-908
42. Johannes G, Sarnow P (1998) Cap-independent polysomal association of natural mRNAs encoding c-myc, BiP, and eIF4G conferred by internal ribosome entry sites. RNA 4: 1500-1513
43. Kedde M, van Kouwenhove M, Zwart W, Oude Vrielink JA, Elkon R, Agami R (2010) A Pumilio-induced RNA structure switch in p27- 30 UTR controls miR-221 and miR-222 accessibility. Nat Cell Biol 12: 1014-1020
44. Khalil AM, Guttman M, Huarte M, Garber M, Raj A, RiveaMorales D, Thomas K, Presser A, Bernstein BE, van Oudenaarden A, Regev A, Lander ES, Rinn JL (2009) Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proc Natl Acad Sci USA 106: 11667-11672
45. Khalil AM, Rinn JL (2011) RNA-protein interactions in human health and disease. Semin Cell Dev Biol 22: 359-365
46. Kielkopf CL, Lucke S, Green MR (2004) U2AF homology motifs: Protein ecognition in the RRM world. Genes Dev 18: 1513-1526.
47. Kim JH, Hahm B, Kim YK, Choi M, Jang SK (2000) Protein-protein interaction among hnRNPs shuttling between nucleus and cytoplasm. J Mol Biol 298: 395-405
48. Kim TK, Hemberg M, Gray JM, Costa AM, Bear DM, Wu J, Harmin DA, Laptewicz M, Barbara-Haley K, Kuersten S, Markenscoff-Papadimitriou E, Kuhl D, Bito H, Worley PF, Kreiman G, Greenberg ME (2010) Widespread transcription at neuronal activity-regulated enhancers. Nature 465: 182-187
49. Kino T, Hurt DE, Ichijo T, Nader N, Chrousos GP (2010) Noncoding RNA gas5 is a growth arrest- and starvation-associated repressor of the glucocorticoid receptor. Sci Signal 3: ra8.
50. Kotake Y, Nakagawa T, Kitagawa K, Suzuki S, Liu N, Kitagawa M, Xiong Y (2011) Long non-coding RNA ANRIL is required for the PRC2 recruitment to and silencing of p15(INK4B) tumor suppressor gene. Oncogene 30: 1956-1962
51. Li L, Feng T, Lian Y, Zhang G, Garen A, Song X (2009) Role of human noncoding RNAs in the control of tumorigenesis. Proc Natl Acad Sci USA 106: 12956-12961
52. Liu F, Marquardt S, Lister C, Swiezewski S, Dean C (2010) Targeted 30 processing of antisense transcripts triggers Arabidopsis FLC chromatin silencing. Science 327: 94-97
53. Luo MJ, Reed R (2003) Identification of RNA binding proteins by UV cross-linking. Curr Protoc Mol Biol Chapter 27: Unit 27
54. Maison C, Bailly D, Roche D, Montes de Oca R, Probst AV, Vassias I, Dingli F, Lombard B, Loew D, Quivy JP, Almouzni G (2011) SUMOylation promotes de novo targeting of HP1alpha to pericentric heterochromatin. Nat Genet 43: 220-227
55. Mancini-Dinardo D, Steele SJ, Levorse JM, Ingram RS, Tilghman SM (2006) Elongation of the Kcnq1ot1 transcript is required for genomic imprinting of neighboring genes. Genes Dev 20: 1268-1282
56. Martianov I, Ramadass A, Serra Barros A, Chow N, Akoulitchev A (2007) Repression of the human dihydrofolate reductase gene by a non-coding interfering transcript. Nature 445: 666-670
57. Mattick JS (2009) The genetic signatures of noncoding RNAs. PLoS Genet 5: E1000459
58. Meijer HA, Kong YW, Lu WT, Wilczynska A, Spriggs RV, Robinson SW, Godfrey JD, Willis AE, Bushell M (2013) Translational repression and eIF4A2 activity are critical for microRNA-mediated gene regulation. Science 340: 82-85
59. Mercer TR, Dinger ME, Mattick JS (2009) Long non-coding RNAs: Insights into functions. Nat Rev Genet 10: 155-159
60. Mourtada-Maarabouni M, Pickard MR, Hedge VL, Farzaneh F, Williams GT (2009) GAS5, a non-protein-coding RNA, controls apoptosis and is downregulated in breast cancer. Oncogene 28: 195-208
61. Nagano T, Mitchell JA, Sanz LA, Pauler FM, Ferguson-Smith AC, Feil R, Fraser P (2008) The Air noncoding RNA epigenetically silences transcription by targeting G9a to chromatin. Science 322: 1717-1720
62. Orom UA, Derrien T, Beringer M, Gumireddy K, Gardini A, Bussotti G, Lai F, Zytnicki M, Notredame C, Huang Q, Guigo R, Shiekhattar R (2010) Long noncoding RNAs with enhancer-like function in human cells. Cell 143: 46-58
63. Ostareck DH, Ostareck-Lederer A, Wilm M, Thiele BJ, Mann M, Hentze MW (1997) mRNA silencing in erythroid differentiation: hnRNP K and hnRNP E1 regulate 15-lipoxygenase translation from the 30 end. Cell 89: 597-606
64. Ostareck-Lederer A, Ostareck DH, Cans C, Neubauer G, Bomsztyk K, Superti-Furga G, Hentze MW (2002) c-Src-mediated phosphorylation of hnRNP K drives translational activation of specifically silenced mRNAs. Mol Cell Biol 22: 4535-4543
65. Ostareck-Lederer A, Ostareck DH, Hentze MW (1998) Cytoplasmic regulatory functions of the KH-domain proteins hnRNPs K and E1/E2. Trends Biochem Sci 23: 409-411
66. Ostrowski J, Kawata Y, Schullery DS, Denisenko ON, Bomsztyk K (2003) Transient recruitment of the hnRNP K protein to inducibly transcribed gene loci. Nucleic Acids Res 31: 3954-3962
67. Perez DS, Hoage TR, Pritchett JR, Ducharme-Smith AL, Halling ML, Ganapathiraju SC, Streng PS, Smith DI (2008) Long, abundantly expressed non-coding transcripts are altered in cancer. Hum Mol Genet 17: 642-655
68. Petrovics G, Zhang W, Makarem M, Street JP, Connelly R, Sun L, Sesterhenn IA, Srikantan V, Moul JW, Srivastava S (2004) Elevated expression of PCGEM1, a prostate-specific gene with cell growth-promoting function, is associated with high-risk prostate cancer patients. Oncogene 23: 605-611
69. Poliseno L, Salmena L, Zhang J, Carver B, Haveman WJ, Pandolfi PP (2010) A coding-independent function of gene and pseudogene mRNAs regulates tumour biology. Nature 465: 1033-1038
70. Ponting CP, Oliver PL, Reik W (2009) Evolution and functions of long noncoding RNAs. Cell 136: 629-641
71. Prigge JR, Iverson SV, Siders AM, Schmidt EE (2009) Interactome for auxiliary splicing factor U2AF(65) suggests diverse roles. Biochim Biophys Acta 1789: 487-492
72. Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, Goodnough LH, Helms JA, Farnham PJ, Segal E, Chang HY (2007) Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129: 1311-1323
73. Schmitz KM, Mayer C, Postepska A, Grummt I (2010) Interaction of noncoding RNA with the rDNA promoter mediates recruitment of DNMT3b and silencing of rRNA genes. Genes Dev 24: 2264-2269
74. Shnyreva M, Schullery DS, Suzuki H, Higaki Y, Bomsztyk K (2000) Interaction of two multifunctional proteins. Heterogeneous nuclear ribonucleoprotein K and Y-box-binding protein. J Biol Chem 275: 15498-15503
75. Silvera D, Formenti SC, Schneider RJ (2010) Translational control in cancer. Nat Rev Cancer 10: 254-266
76. Sonenberg N, Dever TE (2003) Eukaryotic translation initiation factors and regulators. Curr Opin Struct Biol 13: 56-63
77. Sonenberg N, Hinnebusch AG (2009) Regulation of translation initiation in eukaryotes: Mechanisms and biological targets. Cell 136: 731-745
78. Steeg PS (2006) Tumor metastasis: Mechanistic insights and clinical challenges. Nat Med 12: 895-904
79. Tian D, Sun S, Lee JT (2010) The long noncoding RNA, Jpx, is a molecular switch for X chromosome inactivation. Cell 143: 390-403
80. Tomonaga T, Levens D (1995) Heterogeneous nuclear ribonucleoprotein K is a DNA-binding transactivator. J Biol Chem 270: 4875-4881
81. Tripathi V, Ellis JD, Shen Z, Song DY, Pan Q, Watt AT, Freier SM, Bennett CF, Sharma A, Bubulya PA, Blencowe BJ, Prasanth SG, Prasanth KV (2010) The nuclear-retained noncoding RNA MALAT1 regulates alternative splicing by modulating SR splicing factor phosphorylation. Mol Cell 39: 925-938
82. Tsai MC, Manor O, Wan Y, Mosammaparast N, Wang JK, Lan F, Shi Y, Segal E, Chang HY (2010) Long noncoding RNA as modular scaffold of histone modification complexes. Science 329: 689-693
83. Ule J, Jensen K, Mele A, Darnell RB (2005) CLIP: A method for identifying protein-RNA interaction sites in living cells. Methods 37: 376-386
84. Valastyan S, Weinberg RA (2011) Tumor metastasis: Molecular insights and evolving paradigms. Cell 147: 275-292
85. Valverde R, Edwards L, Regan L (2008) Structure and function of KH domains. FEBS J 275: 2712-2726
86. van Kouwenhove M, Kedde M, Agami R (2011) MicroRNA regulation by RNA-binding proteins and its implications for cancer. Nat Rev Cancer 11: 644-656
87. Vasudevan S, Steitz JA (2007) AU-rich-element-mediated upregulation of translation by FXR1 and Argonaute 2. Cell 128: 1105-1118
88. Wang KC, Chang HY (2011) Molecular mechanisms of long noncoding RNAs. Mol Cell 43: 904-914
89. Wang X, Arai S, Song X, Reichart D, Du K, Pascual G, Tempst P, Rosenfeld MG, Glass CK, Kurokawa R (2008) Induced ncRNAs allosterically modify RNA-binding proteins in cis to inhibit transcription. Nature 454: 126-130
90. Wapinski O, Chang HY (2011) Long noncoding RNAs and human disease. Trends Cell Biol 21: 354-361
91. Yap KL, Li S, Munoz-Cabello AM, Raguz S, Zeng L, Mujtaba S, Gil J, Walsh MJ, Zhou MM (2010) Molecular interplay of the noncoding RNA ANRIL and methylated histone H3 lysine 27 by polycomb CBX7 in transcriptional silencing of INK4a. Mol Cell 38: 662-674
92. Yoon JH, Abdelmohsen K, Srikantan S, Yang X, Martindale JL, De S, Huarte M, Zhan M, Becker KG, Gorospe M (2012) LincRNA-p21 suppresses target mRNA translation. Mol Cell 47: 648-655.