Regulated degradation of replication-dependent histone mRNAs requires both ATR and Upf1

Nature Structural and Molecular Biology

Volumn 12, Issue 9, 2005, Pages 794-800

  Kaygun, Handan ^a   Marzluff, William F ^a,b  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATR PROTEIN; HISTONE; MESSENGER RNA; PROTEIN; PROTEIN UPF1; UNCLASSIFIED DRUG; ATR PROTEIN, HUMAN; CAFFEINE; CELL CYCLE PROTEIN; HYDROXYUREA; LYSINE; PROTEIN SERINE THREONINE KINASE; RENT1 PROTEIN, HUMAN; SMALL INTERFERING RNA; TRANSACTIVATOR PROTEIN;

ARTICLE; CONTROLLED STUDY; DNA DAMAGE; DNA REPLICATION; FEMALE; HELA CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; RNA DEGRADATION; STRESS; DRUG EFFECT; GENETICS; METABOLISM; PROTEIN BINDING; RNA STABILITY;

EUKARYOTA; MAMMALIA; METAZOA;

CAFFEINE; CELL CYCLE PROTEINS; DNA REPLICATION; HELA CELLS; HISTONES; HUMANS; HYDROXYUREA; LYSINE; PROTEIN BINDING; PROTEIN-SERINE-THREONINE KINASES; RNA STABILITY; RNA, MESSENGER; RNA, SMALL INTERFERING; TRANS-ACTIVATORS;

EID: 26944503146     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb972     Document Type: Article

References (43)

1. Nelson, D.M. et al. Coupling of DNA synthesis and histone synthesis in S-phase independent of cyclin/cdk2 activity. Mol. Cell. Biol. 22, 7459-7472 (2002).
2. Ye, X. et al. Defective S phase chromatin assembly causes DNA damage, activation of the S phase checkpoint, and S phase arrest. Mol. Cell 11, 341-351 (2003).
3. Sancar, A., Lindsey-Boltz, L.A., Unsal-Kacmaz, K. & Linn, S. Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu. Rev. Biochem. 73, 39-85 (2004).
4. Sittman, D.B., Graves, R.A. & Marzluff, W.F. Histone mRNA concentrations are regulated at the level of transcription and mRNA degradation. Proc. Natl. Acad. Sci. USA 80, 1849-1853 (1983).
5. Dominski, Z. & Marzluff, W.F. Formation of the 3′ end of histone mRNA. Gene 239, 1-14 (1999).
6. Dominski, Z., Zheng, L.-X., Sanchez, R. & Marzluff, W.F. The stem-loop binding protein facilitates 3′ end formation by stabilizing 117 snRNP binding to the histone pre-mRNA. Mol. Cell. Biol. 19, 3561-3570 (1999).
7. Sanchez, R. & Marzluff, W.F. The stem-loop binding protein is required for efficient translation of histone mRNA in vivo and in vitro. Mol. Cell. Biol. 22, 7093-7104 (2002).
8. Pandey, N.B. & Marzluff, W.F. The stem-loop structure at the 3′ end of histone mRNA is necessary and sufficient for regulation of histone mRNA stability. Mol. Cell. Biol. 7, 4557-4559 (1987).
9. Harris, M.E. et al. Regulation of histone mRNA in the unperturbed cell cycle: evidence suggesting control at two posttranscriptional steps. Mol. Cell. Biol. 11, 2416-2424 (1991).
10. Maquat, L.E. Nonsense-mediated mRNA decay: splicing, translation and mRNP dynamics. Nat. Rev. Mol. Cell Biol. 5, 89-99 (2004).
11. Lykke-Andersen, J., Shu, M.D. & Steitz, J.A. Human Upf proteins target an mRNA for nonsense-mediated decay when bound downstream of a termination codon. Cell 103, 1121-1131 (2000).
12. Kim, V.N., Kataoka, N. & Dreyfuss, G. Role of the nonsense-mediated decay factor hUpf3 in the splicing-dependent exon-exon junction complex. Science 293, 1832-1836 (2001).
13. Graves, R.A., Pandey, N.B., Chodchoy, N. & Marzluff, W.F. Translation is required for regulation of histone mRNA degradation. Cell 48, 615-626 (1987).
14. Kaygun, H. & Marzluff, W.F. Translation termination is involved in histone mRNA degradation when DNA replication is inhibited. Mol. Cell. Biol. 25, 6879-6888 (2005).
15. Wells, D. & Kedes, L. Structure of a human histone cDNA: evidence that basally expressed histone genes have intervening sequences and encode polyadenylated mRNAs. Proc. Natl. Acad. Sci. USA 82, 2834-2838 (1985).
16. Brush, D., Dodgson, J.B., Choi, O.R., Stevens, P.W. & Engel, J.D. Replacement variant histone genes contain intervening sequences. Mol. Cell. Biol. 5, 1307-1317 (1985).
17. Czaplinski, K., Weng, Y., Hagan, K.W. & Peltz, S.W. Purification and characterization of the Upf1 protein: a factor involved in translation and mRNA degradation. RNA 1, 610-623 (1995).
18. Sun, X., Perlick, H.A., Dietz, H.C. & Maquat, L.E. A mutated human homologue to yeast Upf1 protein has a dominant-negative effect on the decay of nonsense-containing mRNAs in mammalian cells. Proc. Natl. Acad. Sci. USA 95, 10009-10014 (1998).
19. Leeds, P., Wood, J.M., Lee, B.-S. & Culbertson, M.R. Gene products that promote mRNA turnover in Saccharomyces cerevisiae. Mol. Cell. Biol. 12, 2165-2177 (1992).
20. Perlick, H.A., Medghalchi, S.M., Spencer, F.A., Kendzior, R.J., Jr. & Dietz, H.C. Mammalian orthologues of a yeast regulator of nonsense transcript stability. Proc. Natl. Acad. Sci. USA 93, 10928-10932 (1996).
21. Weng, Y., Czaplinski, K. & Peltz, S.W. Genetic and biochemical characterization of mutations in the ATPase and helicase regions of the Upf1 protein. Mol. Cell. Biol. 16, 5477-5490 (1996).
22. Whitfield, M.L. et al. Stem-loop binding protein, the protein that binds the 3′ end of histone mRNA, is cell cycle regulated by both translational and posttranslational mechanisms. Mol. Cell. Biol. 20, 4188-4198 (2000).
23. Zheng, L. et al. Phosphorylation of SLBP on two threonines triggers degradation of SLBP, the sole cell-cycle regulated factor required for regulation of histone mRNA processing, at the end of S-phase. Mol. Cell. Biol. 23, 1590-1601 (2003).
24. Whitfield, M.L. et al. SLBP is associated with histone mRNA on polyribosomes as a component of histone mRNP. Nucleic Adds Res. 32, 4833-4842 (2004).
25. He, F. & Jacobson, A. Identification of a novel component of the nonsense-mediated mRNA decay pathway by use of an interacting protein screen. Genes Dev. 9, 437-454 (1995).
26. Schell, T. et al. Complexes between the nonsense-mediated mRNA decay pathway factor human upf1 (up-frameshift protein 1) and essential nonsense-mediated mRNA decay factors in HeLa cells. Biochem. J. 373, 775-783 (2003).
27. Nghiem, P., Park, P.K., Kim, Y., Vaziri, C. & Schreiber, S.L. ATR inhibition selectively sensitizes G1 checkpoint-deficient cells to lethal premature chromatin condensation. Proc. Natl. Acad. Sci. USA 98, 9092-9097 (2001).
28. Amrani, N. et al. A faux 3′-UTR promotes aberrant termination and triggers nonsense-mediated mRNA decay. Nature 432, 112-118 (2004).
29. Maquat, L.E. & Li, X.J. Mammalian heat shock p70 and histone H4 transcripts, which derive from naturally intronless genes, are immune to nonsense-mediated decay. RNA 7, 445-456 (2001).
30. Le Hir, H., Moore, M.J. & Maquat, L.E. Pre-mRNA splicing alters mRNP composition: evidence for stable association of proteins at exon-exon junctions. Genes Dev. 14, 1098-1108 (2000).
31. Le Hir, H., Izaurralde, E., Maquat, L.E. & Moore, M.J. The spliceosome deposits multiple proteins 20-24 nucleotides upstream of mRNA exon-exon junctions. EMBO J. 19, 6860-6869 (2000).
32. Ishigaki, Y., Li, X.J., Serin, G. & Maquat, L.E. Evidence for a pioneer round of mRNA translation: mRNAs subject to nonsense-mediated decay in mammalian cells are bound by CBP80 and CBP20. Cell 106, 607-617 (2001).
33. Marzluff, W.F., Gongidi, P., Woods, K.R., Jin, J.P. & Maltais, L. The human and mouse replication-dependent histone genes. Genomics 80, 487-498 (2002).
34. Yamashita, A., Ohnishi, T., Kashima, I., Taya, Y. & Ohno, S. Human SMG-1, a novel phosphatidylinositol 3-kinase-related protein kinase, associates with components of the mRNA surveillance complex and is involved in the regulation of nonsense-mediated mRNA decay. Genes Dev. 15, 2215-2228 (2001).
35. Ohnishi, T. et al. Phosphorylation of hUPF1 induces formation of mRNA surveillance complexes containing hSMG-5 and hSMG-7. Mol. Cell 12, 1187-1200 (2003).
36. Pal, M., Ishigaki, Y., Nagy, E. & Maquat, L.E. Evidence that phosphorylation of human Upf1 protein varies with intracellular location and is mediated by a wortmannin-sensitive and rapamycin-sensitive PI 3-kinase-related kinase signaling pathway. RNA 7, 5-15 (2001).
37. Lejeune, F., Li, X. & Maquat, L.E. Nonsense-mediated mRNA decay in mammalian cells involves decapping, deadenylating, and exonucleolytic activities. Mol. Cell 12, 675-687 (2003).
38. Brumbaugh, K.M. et al. The mRNA surveillance protein hSMG-1 functions in genotoxic stress response pathways in mammalian cells. Mol. Cell 14, 585-598 (2004).
39. Nabatiyan, A. & Krude, T. Silencing of chromatin assembly factor 1 in human cells leads to cell death and loss of chromatin assembly during DNA synthesis. Mol. Cell. Biol. 24, 2853-2862 (2004).
40. Kim, Y.K., Furic, L., LesGroseillers, L. & Maquat, L.E. Mammalian Staufen1 recruits Upf1 to specific mRNA 3′UTRs so as to elicit mRNA decay. Cell 120, 195-208 (2005).
41. Wellman, S.E., Casano, P.J., Pilch, D.R., Marzluff, W.F. & Sittman, D.B. Characterization of mouse H3.3-like histone genes. Gene 59, 29-39 (1987).
42. Wagner, E.J. & Garcia-Blanco, M.A. RNAi-mediated PTB depletion leads to enhanced exon definition. Mol. Cell 10, 943-949 (2002).
43. Mendell, J.T., ap Rhys, C.M. & Dietz, H.C. Separable roles for rent1/hUpf1 in altered splicing and decay of nonsense transcripts. Science 298, 419-422 (2002).