STAU1 binding 3′ UTR IRAlus complements nuclear retention to protect cells from PKR-mediated translational shutdown

Genes and Development

Volumn 27, Issue 13, 2013, Pages 1495-1510

  Elbarbary, Reyad A ^a,b   Li, Wencheng ^c,d   Tian, Bin ^c,d   Maquat, Lynne E ^a,b  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^c University of Medicine   (United States)

^d RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

Author keywords

Inverted repeat Alu elements; Myogenesis; Nuclear export; p54nrb; PKR; STAU1; Translation

Indexed keywords

BINDING PROTEIN; INITIATION FACTOR 2ALPHA; MESSENGER RNA; PROTEIN KINASE R; PROTEIN P54; STAU1 PROTEIN; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ALU SEQUENCE; ARTICLE; CELL PROTECTION; CONTROLLED STUDY; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MUSCLE DEVELOPMENT; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN RNA BINDING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA SEQUENCE; RNA TRANSLATION; WESTERN BLOTTING;

INVERTED REPEAT ALU ELEMENTS; MYOGENESIS; NUCLEAR EXPORT; P54NRB; PKR; STAU1; TRANSLATION;

3' UNTRANSLATED REGIONS; ALU ELEMENTS; CELL NUCLEUS; CELLS, CULTURED; CYTOSKELETAL PROTEINS; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; PROTEIN BINDING; RNA TRANSPORT; RNA, MESSENGER; RNA-BINDING PROTEINS;

EUKARYOTA;

EID: 84879745156     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.220962.113     Document Type: Article

References (54)

1. Athanasiadis A, Rich A, Maas S. 2004. Widespread A-to-I RNA editing of Alu-containing mRNAs in the human transcriptome. PLoS Biol 2: e391.
2. Bass BL. 2002. RNA editing by adenosine deaminases that act on RNA. Annu Rev Biochem 71: 817-846.
3. Ben-Asouli Y, Banai Y, Pel-Or Y, Shir A, Kaempfer R. 2002. Human interferon-g mRNA autoregulates its translation through a pseudoknot that activates the interferon-inducible protein kinase PKR. Cell 108: 221-232.
4. Berger A, Strub K. 2011. Multiple roles of Alu-related noncoding RNAs. Prog Mol Subcell Biol 51: 119-146.
5. Bond CS, Fox AH. 2009. Paraspeckles: Nuclear bodies built on long noncoding RNA. J Cell Biol 186: 637-644.
6. Campbell RE, Tour O, Palmer AE, Steinbach PA, Baird GS, Zacharias DA, Tsien RY. 2002. A monomeric red fluorescent protein. Proc Natl Acad Sci 99: 7877-7882.
7. Capshew CR, Dusenbury KL, Hundley HA. 2012. Inverted Alu dsRNA structures do not affect localization but can alter translation efficiency of human mRNAs independent of RNA editing. Nucleic Acids Res 40: 8637-8645.
8. Chen LL, Carmichael GG. 2008. Gene regulation by SINES and inosines: Biological consequences of A-to-I editing of Alu element inverted repeats. Cell Cycle 7: 3294-3301.
9. Chen LL, Carmichael GG. 2009. Altered nuclear retention of mRNAs containing inverted repeats in human embryonic stem cells: Functional role of a nuclear noncoding RNA. Mol Cell 35: 467-478.
10. Chen LL, DeCerbo JN, Carmichael GG. 2008. Alu elementmediated gene silencing. EMBO J 27: 1694-1705.
11. Chen LL, Yang L, Carmichael GG. 2010. Molecular basis for an attenuated cytoplasmic dsRNA response in human embryonic stem cells. Cell Cycle 9: 3552-3564.
12. Cohen-Chalamish S, Hasson A, Weinberg D, Namer LS, Banai Y, Osman F, Kaempfer R. 2009. Dynamic refolding of IFN-g mRNA enables it to function as PKR activator and translation template. Nat Chem Biol 5: 896-903.
13. Deininger P. 2011. Alu elements: Know the SINEs. Genome Biol 12: 236.
14. Dugré-Brisson S, Elvira G, Boulay K, Chatel-Chaix L, Mouland AJ, DesGroseillers L. 2005. Interaction of Staufen1 with the 59 end of mRNA facilitates translation of these RNAs. Nucleic Acids Res 33: 4797-4812.
15. Fitzpatrick T, Huang S. 2012. 3′-UTR-located inverted Alu repeats facilitate mRNA translational repression and stress granule accumulation. Nucleus 3: 359-369.
16. Furic L, Maher-Laporte M, DesGroseillers L. 2008. A genomewide approach identifies distinct but overlapping subsets of cellular mRNAs associated with Staufen1- and Staufen2- containing ribonucleoprotein complexes. RNA 14: 324-335.
17. Gerlitz G, Jagus R, Elroy-Stein O. 2002. Phosphorylation of initiation factor-2a is required for activation of internal translation initiation during cell differentiation. Eur J Biochem 269: 2810-2819.
18. Gleghorn ML, Gong C, Kielkopf CL, Maquat LE. 2013. Staufen1 dimerizes through a conserved motif and a degenerate dsRNA-binding domain to promote mRNA decay. Nat Struct Mol Biol 20: 515-524.
19. Gong C, Maquat LE. 2011. lncRNAs transactivate STAU1- mediated mRNA decay by duplexing with 3′ UTRs via Alu elements. Nature 470: 284-288.
20. Gong C, Kim YK, Woeller CF, Tang Y, Maquat LE. 2009. SMD and NMD are competitive pathways that contribute to myogenesis: Effects on PAX3 and myogenin mRNAs. Genes & Dev 23: 54-66.
21. Heo I, Joo C, Cho J, Ha M, Han J, Kim VN. 2008. Lin28 mediates the terminal uridylation of let-7 precursor microRNA. Mol Cell 32: 276-284.
22. Huichalaf C, Sakai K, Jin B, Jones K, Wang GL, Schoser B, Schneider-Gold C, Sarkar P, Pereira-Smith OM, Timchenko N, et al. 2010. Expansion of CUG RNA repeats causes stress and inhibition of translation in myotonic dystrophy 1 (DM1) cells. FASEB J 24: 3706-3719.
23. Hundley HA, Bass BL. 2010. ADAR editing in double-stranded UTRs and other noncoding RNA sequences. Trends Biochem Sci 35: 377-383.
24. Kim DD, Kim TT, Walsh T, Kobayashi Y, Matise TC, Buyske S, Gabriel A. 2004. Widespread RNA editing of embedded alu elements in the human transcriptome. Genome Res 14: 1719-1725.
25. Kim YK, Furic L, DesGroseillers L, Maquat LE. 2005. Mammalian Staufen1 recruits Upf1 to specific mRNA 3′UTRs so as to elicit mRNA decay. Cell 120: 195-208.
26. Kim YK, Furic L, Parisien M, Major F, DesGroseillers L, Maquat LE. 2007. Staufen1 regulates diverse classes of mammalian transcripts. EMBO J 26: 2670-2681.
27. Koromilas AE, Roy S, Barber GN, Katze MG, Sonenberg N. 1992. Malignant transformation by a mutant of the IFNinducible dsRNA-dependent protein kinase. Science 257: 1685-1689.
28. Krayev AS, Markusheva TV, Kramerov DA, Ryskov AP, Skryabin KG, Bayev AA, Georgiev GP. 1982. Ubiquitous transposonlike repeats B1 and B2 of the mouse genome: B2 sequencing. Nucleic Acids Res 10: 7461-7475.
29. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, Devon K, Dewar K, Doyle M, FitzHugh W, et al. 2001. Initial sequencing and analysis of the human genome. Nature 409: 860-921.
30. Levanon EY, Eisenberg E, Yelin R, Nemzer S, Hallegger M, Shemesh R, Fligelman ZY, Shoshan A, Pollock SR, Sztybel D, et al. 2004. Systematic identification of abundant A-to-I editing sites in the human transcriptome. Nat Biotechnol 22: 1001-1005.
31. Manche L, Green SR, Schmedt C, Mathews MB. 1992. Interactions between double-stranded RNA regulators and the protein kinase DAI. Mol Cell Biol 12: 5238-5248.
32. Martel C, Macchi P, Furic L, Kiebler MA, DesGroseillers L. 2006. Staufen1 is imported into the nucleolus via a bipartite nuclear localization signal and several modulatory determinants. Biochem J 393: 245-254.
33. Martel C, Dugre-Brisson S, Boulay K, Breton B, Lapointe G, Armando S, Trepanier V, Duchaîne T, Bouvier M, DesGroseillers L. 2010. Multimerization of Staufen1 in live cells. RNA 16: 585-597.
34. Neeman Y, Levanon EY, Jantsch MF, Eisenberg E. 2006. RNA editing level in the mouse is determined by the genomic repeat repertoire. RNA 12: 1802-1809.
35. Nussbaum JM, Gunnery S, Mathews MB. 2002. The 39- untranslated regions of cytoskeletal muscle mRNAs inhibit translation by activating the double-stranded RNA-dependent protein kinase PKR. Nucleic Acids Res 30: 1205-1212.
36. Park E, Gleghorn ML, Maquat LE. 2013. Staufen2 functions in Staufen1-mediated mRNA decay by binding to itself and its paralog and promoting UPF1 helicase but not ATPase activity. Proc Natl Acad Sci 110: 405-412.
37. Pfaller CK, Li Z, George CX, Samuel CE. 2011. Protein kinase PKR and RNA adenosine deaminase ADAR1: New roles for old players as modulators of the interferon response. Curr Opin Immunol 23: 573-582.
38. Polesskaya A, Cuvellier S, Naguibneva I, Duquet A, Moss EG, Harel-Bellan A. 2007. Lin-28 binds IGF-2 mRNA and participates in skeletal myogenesis by increasing translation efficiency. Genes & Dev 21: 1125-1138.
39. Prasanth KV, Spector DL. 2007. Eukaryotic regulatory RNAs: An answer to the 'genome complexity' conundrum. Genes & Dev 21: 11-42.
40. Prasanth KV, Prasanth SG, Xuan Z, Hearn S, Freier SM, Bennett CF, Zhang MQ, Spector DL. 2005. Regulating gene expression through RNA nuclear retention. Cell 123: 249-263.
41. Ravel-Chapuis A, Belanger G, Yadava RS, Mahadevan MS, DesGroseillers L, Cote J, Jasmin BJ. 2012. The RNA-binding protein Staufen1 is increased in DM1 skeletal muscle and promotes alternative pre-mRNA splicing. J Cell Biol 196: 699-712.
42. Scheuner D, Song B, McEwen E, Liu C, Laybutt R, Gillespie P, Saunders T, Bonner-Weir S, Kaufman RJ. 2001. Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol Cell 7: 1165-1176.
43. Sefton BM. 2005. Labeling cultured cells with 32Pi and preparing cell lysates for immunoprecipitation. Cur Protocols Mol Biol 40: 18.2.1-18.2.8.
44. Sen SK, Han K, Wang J, Lee J, Wang H, Callinan PA, Dyer M, Cordaux R, Liang P, Batzer MA. 2006. Human genomic deletions mediated by recombination between Alu elements. Am J Hum Genet 79: 41-53.
45. Shav-Tal Y, Zipori D. 2002. PSF and p54(nrb)/NonO-multifunctional nuclear proteins. FEBS Lett 531: 109-114.
46. Shcherbo D, Merzlyak EM, Chepurnykh TV, Fradkov AF, Ermakova GV, Solovieva EA, Lukyanov KA, Bogdanova EA, Zaraisky AG, Lukyanov S, et al. 2007. Bright far-red fluorescent protein for whole-body imaging. Nat Methods 4: 741-746.
47. Sonenberg N, Hinnebusch AG. 2009. Regulation of translation initiation in eukaryotes: Mechanisms and biological targets. Cell 136: 731-745.
48. Stefl R, Oberstrass FC, Hood JL, Jourdan M, Zimmermann M, Skrisovska L, Maris C, Peng L, Hofr C, Emeson RB, et al. 2010. The solution structure of the ADAR2 dsRBM-RNA complex reveals a sequence-specific readout of the minor groove. Cell 143: 225-237.
49. Thornton JE, Gregory RI. 2012. How does Lin28 let-7 control development and disease? Trends Cell Biol 22: 474-482.
50. Tian B, White RJ, Xia T, Welle S, Turner DH, Mathews MB, Thornton CA. 2000. Expanded CUG repeat RNAs form hairpins that activate the double-stranded RNA-dependent protein kinase PKR. RNA 6: 79-87.
51. Walters RD, Kugel JF, Goodrich JA. 2009. InvAluable junk: The cellular impact and function of Alu and B2 RNAs. IUBMB Life 61: 831-837.
52. Wang J, Gong C, Maquat LE. 2013. Control of myogenesis by rodent SINE-containing lncRNAs. Genes & Dev 27: 793-804.
53. Wickham L, Duchaîne T, Luo M, Nabi IR, DesGroseillers L. 1999. Mammalian staufen is a double-stranded-RNA- and tubulin-binding protein which localizes to the rough endoplasmic reticulum. Mol Cell Biol 19: 2220-2230.
54. Zhang Z, Carmichael GG. 2001. The fate of dsRNA in the nucleus: A p54(nrb)-containing complex mediates the nuclear retention of promiscuously A-to-I edited RNAs. Cell 106: 465-475.