Intra- and intermolecular regulatory interactions in Upf1, the RNA helicase central to nonsense-mediated mRNA decay in yeast

Molecular and Cellular Biology

Volumn 33, Issue 23, 2013, Pages 4672-4684

  He, Feng ^a   Ganesan, Robin ^a   Jacobson, Allan ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA FRAGMENT; MESSENGER RNA; MESSENGER RNA PRECURSOR; PROTEIN UPF1; PROTEIN UPF2; PROTEIN UPF3; REGULATOR PROTEIN; RNA HELICASE; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATASE; FUNGAL RNA; NAM7 PROTEIN, S CEREVISIAE; NMD2 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ARTICLE; ENZYME REGULATION; MOLECULAR INTERACTION; NONHUMAN; NONSENSE MEDIATED MRNA DECAY; PLASMID; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN PROTEIN INTERACTION; RNA BINDING; RNA METABOLISM; RNA TRANSLATION; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION REGULATION; TWO HYBRID SYSTEM; YEAST; AMINO ACID SUBSTITUTION; CHEMISTRY; ENZYMOLOGY; GENETICS; METABOLISM; PHYSIOLOGY; PROTEIN DOMAIN; RNA STABILITY; SITE DIRECTED MUTAGENESIS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ADENOSINE TRIPHOSPHATASES; AMINO ACID SUBSTITUTION; MUTAGENESIS, SITE-DIRECTED; PEPTIDE CHAIN TERMINATION, TRANSLATIONAL; PROTEIN INTERACTION DOMAINS AND MOTIFS; RNA HELICASES; RNA STABILITY; RNA, FUNGAL; RNA, MESSENGER; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 84891709077     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01136-13     Document Type: Article

References (57)

1. Isken O, Maquat LE. 2007. Quality control of eukaryotic mRNA: safeguarding cells from abnormal mRNA function. Genes Dev. 21:1833-1856.
2. Parker R. 2012. RNA degradation in Saccharomyces cerevisiae. Genetics 191:671-702.
3. Shoemaker CJ, Green R. 2012. Translation drives mRNA quality control. Nat. Struct. Mol. Biol. 19:594-601.
4. Kervestin S, Jacobson A. 2012. NMD: a multifaceted response to premature translational termination. Nat. Rev. Mol. Cell Biol. 13:700-712.
5. Pulak R, Anderson P. 1993. mRNA surveillance by the Caenorhabditis elegans smg genes. Genes Dev. 7:1885-1897.
6. - mutant. Proc. Natl. Acad. Sci. U. S. A. 90:7034-7038.
7. Nicholson P, Yepiskoposyan H, Metze S, Zamudio Orozco R, Kleinschmidt N, Muhlemann O. 2010. Nonsense-mediated mRNA decay in human cells: mechanistic insights, functions beyond quality control and the double-life of NMD factors. Cell. Mol. Life Sci. 67:677-700.
8. Rehwinkel J, Raes J, Izaurralde E. 2006. Nonsense-mediated mRNA decay: target genes and functional diversification of effectors. Trends Biochem. Sci. 31:639-646.
9. He F, Li X, Spatrick P, Casillo R, Dong S, Jacobson A. 2003. Genomewide analysis of mRNAs regulated by the nonsense-mediated and 5' to 3' mRNA decay pathways in yeast. Mol. Cell 12:1439-1452.
10. 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. 15:85-93.
11. He F, Brown AH, Jacobson A. 1997. Upf1p, Nmd2p, and Upf3p are interacting components of the yeast nonsense-mediated mRNA decay pathway. Mol. Cell. Biol. 17:1580-1594.
12. Serin G, Gersappe A, Black JD, Aronoff R, Maquat LE. 2001. Identification and characterization of human orthologues to Saccharomyces cerevisiae Upf2 protein and Upf3 protein (Caenorhabditis elegans SMG-4). Mol. Cell. Biol. 21:209-223.
13. Lykke-Andersen J, Shu MD, Steitz JA. 2000. Human Upf proteins target an mRNA for nonsense-mediated decay when bound downstream of a termination codon. Cell 103:1121-1131.
14. Page MF, Carr B, Anders KR, Grimson A, Anderson P. 1999. SMG-2 is a phosphorylated protein required for mRNA surveillance in Caenorhabditis elegans and related to Upf1p of yeast. Mol. Cell. Biol. 19:5943-5951.
15. Gatfield D, Unterholzner L, Ciccarelli FD, Bork P, Izaurralde E. 2003. Nonsense-mediated mRNA decay in Drosophila: at the intersection of the yeast and mammalian pathways. EMBO J. 22:3960-3970.
16. Isken O, Kim YK, Hosoda N, Mayeur GL, Hershey JW, Maquat LE. 2008. Upf1 phosphorylation triggers translational repression during nonsense-mediated mRNA decay. Cell 133:314-327.
17. Okada-Katsuhata Y, Yamashita A, Kutsuzawa K, Izumi N, Hirahara F, Ohno S. 2012. N- and C-terminal Upf1 phosphorylations create binding platforms for SMG-6 and SMG-5:SMG-7 during NMD. Nucleic Acids Res. 40:1251-1266.
18. Lai T, Cho H, Liu Z, Bowler MW, Piao S, Parker R, Kim YK, Song H. 2012. Structural basis of the PNRC2-mediated link between mRNA surveillance and decapping. Structure 20:2025-2037.
19. Cho H, Kim KM, Kim YK. 2009. Human proline-rich nuclear receptor coregulatory protein 2 mediates an interaction between mRNA surveillance machinery and decapping complex. Mol. Cell 33:75-86.
20. Weng Y, Czaplinski K, Peltz SW. 1996. Identification and characterization of mutations in the UPF1 gene that affect nonsense suppression and the formation of the Upf protein complex but not mRNA turnover. Mol. Cell. Biol. 16:5491-5506.
21. Keeling KM, Lanier J, Du M, Salas-Marco J, Gao L, Kaenjak-Angeletti A, Bedwell DM. 2004. Leaky termination at premature stop codons antagonizes nonsense-mediated mRNA decay in S. cerevisiae. RNA 10:691-703.
22. Wang W, Czaplinski K, Rao Y, Peltz SW. 2001. The role of Upf proteins in modulating the translation read-through of nonsense-containing transcripts. EMBO J. 20:880-890.
23. Maderazo AB, He F, Mangus DA, Jacobson A. 2000. Upf1p control of nonsense mRNA translation is regulated by Nmd2p and Upf3p. Mol. Cell. Biol. 20:4591-4603.
24. Bidou L, Stahl G, Hatin I, Namy O, Rousset JP, Farabaugh PJ. 2000. Nonsense-mediated decay mutants do not affect programmed-1 frameshifting. RNA 6:952-961.
25. Johansson MJ, Jacobson A. 2010. Nonsense-mediated mRNA decay maintains translational fidelity by limiting magnesium uptake. Genes Dev. 24:1491-1495.
26. Leeds P, Wood JM, Lee BS, Culbertson MR. 1992. Gene products that promote mRNA turnover in Saccharomyces cerevisiae. Mol. Cell. Biol. 12:2165-2177.
27. Altamura N, Groudinsky O, Dujardin G, Slonimski PP. 1992. NAM7 nuclear gene encodes a novel member of a family of helicases with a Znligand motif and is involved in mitochondrial functions in Saccharomyces cerevisiae. J. Mol. Biol. 224:575-587.
28. Koonin E. 1992. A new group of putative RNA helicases. Trends Biochem. Sci. 17:495-497.
29. Chakrabarti S, Jayachandran U, Bonneau F, Fiorini F, Basquin C, Domcke S, Le Hir H, Conti E. 2011. Molecular mechanisms for the RNA-dependent ATPase activity of Upf1 and its regulation by Upf2. Mol. Cell 41:693-703.
30. Clerici M, Mourao A, Gutsche I, Gehring NH, Hentze MW, Kulozik A, Kadlec J, Sattler M, Cusack S. 2009. Unusual bipartite mode of interaction between the nonsense-mediated decay factors, UPF1 and UPF2. EMBO J. 28:2293-2306.
31. Kadlec J, Guilligay D, Ravelli RB, Cusack S. 2006. Crystal structure of the UPF2-interacting domain of nonsense-mediated mRNA decay factor UPF1. RNA 12:1817-1824.
32. Cheng Z, Muhlrad D, Lim MK, Parker R, Song H. 2007. Structural and functional insights into the human Upf1 helicase core. EMBO J. 26:253-264.
33. Czaplinski K, Weng Y, Hagan KW, Peltz SW. 1995. Purification and characterization of the Upf1 protein: a factor involved in translation and mRNA degradation. RNA 1:610-623.
34. Bhattacharya A, Czaplinski K, Trifillis P, He F, Jacobson A, Peltz SW. 2000. Characterization of the biochemical properties of the human Upf1 gene product that is involved in nonsense-mediated mRNA decay. RNA 6:1226-1235.
35. Weng Y, Czaplinski K, Peltz SW. 1996. Genetic and biochemical characterization of mutations in the ATPase and helicase regions of the Upf1 protein. Mol. Cell. Biol. 16:5477-5490.
36. Ghosh S, Ganesan R, Amrani N, Jacobson A. 2010. Translational competence of ribosomes released from a premature termination codon is modulated by NMD factors. RNA 16:1832-1847.
37. Franks TM, Singh G, Lykke-Andersen J. 2010. Upf1 ATPase-dependent mRNP disassembly is required for completion of nonsense-mediated mRNA decay. Cell 143:938-950.
38. He F, Jacobson A. 1995. Identification of a novel component of the nonsense-mediated mRNA decay pathway by use of an interacting protein screen. Genes Dev. 9:437-454.
39. He F, Brown AH, Jacobson A. 1996. Interaction between Nmd2p and Upf1p is required for activity but not for dominant-negative inhibition of the nonsense-mediated mRNA decay pathway in yeast. RNA 2:153-170.
40. Czaplinski K, Ruiz-Echevarria MJ, Paushkin SV, Han X, Weng Y, Perlick HA, Dietz HC, Ter-Avanesyan MD, Peltz SW. 1998. The surveillance complex interacts with the translation release factors to enhance termination and degrade aberrant mRNAs. Genes Dev. 12:1665-1677.
41. Ivanov PV, Gehring NH, Kunz JB, Hentze MW, Kulozik AE. 2008. Interactions between UPF1, eRFs, PABP and the exon junction complex suggest an integrated model for mammalian NMD pathways. EMBO J. 27:736-747.
42. Lykke-Andersen J. 2002. Identification of a human decapping complex associated with hUpf proteins in nonsense-mediated decay. Mol. Cell. Biol. 22:8114-8121.
43. Lejeune F, Li X, Maquat LE. 2003. Nonsense-mediated mRNA decay in mammalian cells involves decapping, deadenylating, and exonucleolytic activities. Mol. Cell 12:675-687.
44. Kadlec J, Izaurralde E, Cusack S. 2004. The structural basis for the interaction between nonsense-mediated mRNA decay factors UPF2 and UPF3. Nat. Struct. Mol. Biol. 11:330-337.
45. Dong S, Jacobson A, He F. 2010. Degradation of YRA1 pre-mRNA in the cytoplasm requires translational repression, multiple modular intronic elements, Edc3p, and Mex67p. PLoS Biol. 8:e1000360. doi:10.1371/journal.pbio.1000360.
46. Fields S, Song O. 1989. A novel genetic system to detect protein-protein interactions. Nature 340:245-246.
47. Cui Y, Dinman JD, Peltz SW. 1996. Mof4-1 is an allele of the UPF1/IFS2 gene which affects both mRNA turnover and-1 ribosomal frameshifting efficiency. EMBO J. 15:5726-5736.
48. Fairman-Williams ME, Guenther UP, Jankowsky E. 2010. SF1 and SF2 helicases: family matters. Curr. Opin. Struct. Biol. 20:313-324.
49. He F, Jacobson A. 2001. Upf1p, Nmd2p, and Upf3p regulate the decapping and exonucleolytic degradation of both nonsense-containing mRNAs and wild-type mRNAs. Mol. Cell. Biol. 21:1515-1530.
50. Amrani N, Sachs MS, Jacobson A. 2006. Early nonsense: mRNA decay solves a translational problem. Nat. Rev. Mol. Cell Biol. 7:415-425.
51. Weng Y, Czaplinski K, Peltz SW. 1998. ATP is a cofactor of the Upf1 protein that modulates its translation termination and RNA binding activities. RNA 4:205-214.
52. Cheng W, Hsieh J, Brendza KM, Lohman TM. 2001. E. coli Rep oligomers are required to initiate DNA unwinding in vitro. J. Mol. Biol. 310:327-350.
53. Levin MK, Patel SS. 1999. The helicase from hepatitis C virus is active as an oligomer. J. Biol. Chem. 274:31839-31846.
54. Maluf NK, Ali JA, Lohman TM. 2003. Kinetic mechanism for formation of the active, dimeric UvrD helicase-DNA complex. J. Biol. Chem. 278:31930-31940.
55. Serebrov V, Pyle AM. 2004. Periodic cycles of RNA unwinding and pausing by hepatitis C virus NS3 helicase. Nature 430:476-480.
56. Klostermeier D, Rudolph MG. 2009. A novel dimerization motif in the C-terminal domain of the Thermus thermophilus DEAD box helicase Hera confers substantial flexibility. Nucleic Acids Res. 37:421-430.
57. Min EE, Roy B, Amrani N, He F, Jacobson A. 2013. Yeast Upf1 CH domain interacts with Rps26 of the 40S ribosomal subunit. RNA 19:1105-1115.