Staufen2 functions in Staufen1-mediated mRNA decay by binding to itself and its paralog and promoting UPF1 helicase but not ATPase activity

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 2, 2013, Pages 405-412

  Park, Eonyoung ^a,b   Gleghorn, Michael L ^a,b   Maquat, Lynne E ^a,b  

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

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

Protein protein interactions; Protein RNA interactions

Indexed keywords

ADENOSINE TRIPHOSPHATASE; MESSENGER RNA; RNA BINDING PROTEIN; SMALL INTERFERING RNA; STAUFEN1 PROTEIN; STAUFEN2 PROTEIN; UNCLASSIFIED DRUG; UPF1 HELICASE;

3' UNTRANSLATED REGION; ARTICLE; CELL STRAIN HEK293; CONFORMATIONAL TRANSITION; ENZYME ACTIVITY; FEMALE; HELA CELL; HUMAN; HUMAN CELL; HYDROLYSIS; IN VITRO STUDY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION;

3' UNTRANSLATED REGIONS; ADENOSINE TRIPHOSPHATASES; BLOTTING, WESTERN; CYTOSKELETAL PROTEINS; DNA PRIMERS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; HEK293 CELLS; HELA CELLS; HUMANS; IMMUNOPRECIPITATION; NERVE TISSUE PROTEINS; PLASMIDS; PROTEIN BINDING; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA STABILITY; RNA-BINDING PROTEINS; TRANS-ACTIVATORS;

MAMMALIA;

EID: 84872195078     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1213508110     Document Type: Article

References (46)

1. Duchaîne TF, et al. (2002) Staufen2 isoforms localize to the somatodendritic domain of neurons and interact with different organelles. J Cell Sci 115(Pt 16):3285-3295.
2. 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(3):2220-2230.
3. Monshausen M, Gehring NH, Kosik KS (2004) The mammalian RNA-binding protein Staufen2 links nuclear and cytoplasmic RNA processing pathways in neurons. Neuromolecular Med 6(2-3):127-144.
4. Kanai Y, Dohmae N, Hirokawa N (2004) Kinesin transports RNA: Isolation and characterization of an RNA-transporting granule. Neuron 43(4):513-525.
5. Kiebler MA, et al. (1999) The mammalian staufen protein localizes to the somatodendritic domain of cultured hippocampal neurons: Implications for its involvement in mRNA transport. J Neurosci 19(1):288-297.
6. Thomas MG, et al. (2005) Staufen recruitment into stress granules does not affect early mRNA transport in oligodendrocytes. Mol Biol Cell 16(1):405-420.
7. Vessey JP, et al. (2008) A loss of function allele for murine Staufen1 leads to impairment of dendritic Staufen1-RNP delivery and dendritic spine morphogenesis. Proc Natl Acad Sci USA 105(42):16374-16379.
8. Tang SJ, Meulemans D, Vazquez L, Colaco N, Schuman E (2001) A role for a rat homolog of staufen in the transport of RNA to neuronal dendrites. Neuron 32(3):463-475.
9. Goetze B, et al. (2006) The brain-specific double-stranded RNA-binding protein Staufen2 is required for dendritic spine morphogenesis. J Cell Biol 172(2):221-231.
10. Lebeau G, et al. (2008) Staufen1 regulation of protein synthesis-dependent long-term potentiation and synaptic function in hippocampal pyramidal cells. Mol Cell Biol 28(9):2896-2907.
11. Lebeau G, DesGroseillers L, Sossin W, Lacaille JC (2011) mRNA binding protein staufen 1-dependent regulation of pyramidal cell spine morphology via NMDA receptor-mediated synaptic plasticity. Mol Brain 4:22.
12. Lebeau G, et al. (2011) Staufen 2 regulates mGluR long-term depression and Map1b mRNA distribution in hippocampal neurons. Learn Mem 18(5):314-326.
13. 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(2):195-208.
14. Kim YK, et al. (2007) Staufen1 regulates diverse classes of mammalian transcripts. EMBO J 26(11):2670-2681.
15. Miki T, et al. (2011) Cell type-dependent gene regulation by Staufen2 in conjunction with Upf1. BMC Mol Biol 12:48.
16. 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(1):54-66.
17. Gong C, Maquat LE (2011) IncRNAs transactivate STAU1-mediated mRNA decay by duplexing with 3′ UTRs via Alu elements. Nature 470(7333):284-288.
18. Cho H, et al. (2012) Staufen1-mediated mRNA decay functions in adipogenesis. Mol Cell 46(4):495-506.
19. Gautrey H, McConnell J, Lako M, Hall J, Hesketh J (2008) Staufen1 is expressed in preimplantation mouse embryos and is required for embryonic stem cell differentiation. Biochim Biophys Acta 1783(10):1935-1942.
20. Furic L, Maher-Laporte M, DesGroseillers L (2008) A genome-wide approach identifies distinct but overlapping subsets of cellular mRNAs associated with Staufen1- and Staufen2-containing ribonucleoprotein complexes. RNA 14(2):324-335.
21. Allison R, et al. (2004) Two distinct Staufen isoforms in Xenopus are vegetally localized during oogenesis. RNA 10(11):1751-1763.
22. Martel C, et al. (2010) Multimerization of Staufen1 in live cells. RNA 16(3):585-597.
23. Pal M, Ishigaki Y, Nagy E, Maquat LE (2001) Evidence that phosphorylation of human Upfl protein varies with intracellular location and is mediated by a wortmannin-sensitive and rapamycin-sensitive PI 3-kinase-related kinase signaling pathway. RNA 7(1):5-15.
24. Hwang J, Sato H, Tang Y, Matsuda D, Maquat LE (2010) UPF1 association with the capbinding protein, CBP80, promotes nonsense-mediated mRNA decay at two distinct steps. Mol Cell 39(3):396-409.
25. Hosoda N, Kim YK, Lejeune F, Maquat LE (2005) CBP80 promotes interaction of Upf1 with Upf2 during nonsense-mediated mRNA decay in mammalian cells. Nat Struct Mol Biol 12(10):893-901.
26. Maher-Laporte M, et al. (2010) Molecular composition of staufen2-containing ribonucleoproteins in embryonic rat brain. PLoS ONE 5(6):e11350.
27. Chakrabarti S, et al. (2011) Molecular mechanisms for the RNA-dependent ATPase activity of Upf1 and its regulation by Upf2. Mol Cell 41(6):693-703.
28. Chamieh H, Ballut L, Bonneau F, Le Hir H (2008) NMD factors UPF2 and UPF3 bridge UPF1 to the exon junction complex and stimulate its RNA helicase activity. Nat Struct Mol Biol 15(1):85-93.
29. Isken O, Maquat LE (2008) The multiple lives of NMD factors: Balancing roles in gene and genome regulation. Nat Rev Genet 9(9):699-712.
30. Bhattacharya A, et al. (2000) Characterization of the biochemical properties of the human Upf1 gene product that is involved in nonsense-mediated mRNA decay. RNA 6(9):1226-1235.
31. Cheng Z, Muhlrad D, Lim MK, Parker R, Song H (2007) Structural and functional insights into the human Upf1 helicase core. EMBO J 26(1):253-264.
32. Gu M, Rice CM (2010) Three conformational snapshots of the hepatitis C virus NS3 helicase reveal a ratchet translocation mechanism. Proc Natl Acad Sci USA 107(2):521-528.
33. Lindquist RN, Lynn JL, Jr., Lienhard GE (1973) Possible transition-state analogs for ribonuclease. The complexes of uridine with oxovanadium(IV) ion and vanadium(V) ion. J Am Chem Soc 95(26):8762-8768.
34. Westheimer FH (1987) Why nature chose phosphates. Science 235(4793):1173-1178.
35. Goodno CC (1979) Inhibition of myosin ATPase by vanadate ion. Proc Natl Acad Sci USA 76(6):2620-2624.
36. Goodno CC, Taylor EW (1982) Inhibition of actomyosin ATPase by vanadate. Proc Natl Acad Sci USA 79(1):21-25.
37. Yamasaki K, Yamamoto T (1991) Existence of high- and low-affinity vanadate-binding sites on Ca(2+)-ATPase of the sarcoplasmic reticulum. J Biochem 110(6):915-921.
38. Krovat BC, Jantsch MF (1996) Comparative mutational analysis of the double-stranded RNA binding domains of Xenopus laevis RNA-binding protein A. J Biol Chem 271(45):28112-28119.
39. Ivanov KA, Ziebuhr J (2004) Human coronavirus 229E nonstructural protein 13: Characterization of duplex-unwinding, nucleoside triphosphatase, and RNA 5′-triphosphatase activities. J Virol 78(14):7833-7838.
40. Tanaka N, Aronova A, Schwer B (2007) Ntr1 activates the Prp43 helicase to trigger release of lariat-intron from the spliceosome. Genes Dev 21(18):2312-2325.
41. Tsai RT, et al. (2005) Spliceosome disassembly catalyzed by Prp43 and its associated components Ntr1 and Ntr2. Genes Dev 19(24):2991-3003.
42. Ha T, et al. (2002) Initiation and re-initiation of DNA unwinding by the Escherichia coli Rep helicase. Nature 419(6907):638-641.
43. Yarranton GT, Gefter ML (1979) Enzyme-catalyzed DNA unwinding: studies on Escherichia coli rep protein. Proc Natl Acad Sci USA 76(4):1658-1662.
44. Kaygun H, Marzluff WF (2005) Regulated degradation of replication-dependent histone mRNAs requires both ATR and Upf1. Nat Struct Mol Biol 12(9):794-800.
45. Franks TM, Singh G, Lykke-Andersen J (2010) Upf1 ATPase-dependent mRNP disassembly is required for completion of nonsense- mediated mRNA decay. Cell 143(6):938-950.
46. Shigeoka T, Kato S, Kawaichi M, Ishida Y (2012) Evidence that the Upf1-related molecular motor scans the 3′-UTR to ensure mRNA integrity. Nucleic Acids Res 40(14):6887-6897.