A multiprotein occupancy map of the mRNP on the 3′ end of histone mRNAs

RNA

Volumn 21, Issue 11, 2015, Pages 1943-1965

  Brooks, Lionel ^a   Lyons, Shawn M ^b   Mahoney, J Matthew ^a   Welch, Joshua D ^b   Liu, Zhongle ^a   Marzluff, William F ^b   Whitfield, Michael L ^a  

^a DARTMOUTH MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

3HExo; CIMS; CLIP seq; H2A.X; H2AFX; Histone mRNA; HITS CLIP; RBPome; RIP chip; RIP seq; RNP; SLBP; UPF1

Indexed keywords

HISTONE; MESSENGER RNA; CLEAVAGE AND POLYADENYLATION SPECIFICITY FACTOR; NUCLEAR PROTEIN; PROTEIN BINDING; RNA BINDING PROTEIN;

3' UNTRANSLATED REGION; AFFINITY CHROMATOGRAPHY; ARTICLE; BINDING SITE; CHROMOSOME REPLICATION; CONTROLLED STUDY; CORRELATION ANALYSIS; CROSS HYBRIDIZATION; CROSS LINKING; DNA REPLICATION; ELECTROPHORETIC MOBILITY; GEL MOBILITY SHIFT ASSAY; HELA CELL LINE; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN CELL; IN VITRO STUDY; INDUCED MUTATION; MOLECULAR WEIGHT; PRIORITY JOURNAL; PROTEIN RNA BINDING; RNA BINDING; SECONDARY ANALYSIS; ANIMAL; CELL LINE; GENETICS; TUMOR CELL LINE;

ANIMALS; BINDING SITES; CELL LINE; CELL LINE, TUMOR; DNA REPLICATION; HELA CELLS; HISTONES; HUMANS; MRNA CLEAVAGE AND POLYADENYLATION FACTORS; NUCLEAR PROTEINS; PROTEIN BINDING; RNA, MESSENGER; RNA-BINDING PROTEINS;

EID: 84944768767     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.053389.115     Document Type: Article

References (64)

1. Amrani N, Sachs MS, Jacobson A. 2006. Early nonsense: mRNA decay solves a translational problem. Nat Rev Mol Cell Biol 7: 415-425.
2. ÄnköML, Müller-McNicoll M, Brandl H, Curk T, Gorup C, Henry I, Ule J, Neugebauer KM. 2012. The RNA-b inding landscapes of two SR proteins reveal unique functions and binding to diverse RNA classes. Genome Biol 13: R17.
3. Battle DJ, Doudna JA. 2001. The stem-loop binding protein forms a highly stable and specific complex with the 3? stem-loop of histone mRNAs. RNA 7: 123-132.
4. Bonner WM, Mannironi C, Orr A, Pilch DR, Hatch CL. 1993. Histone H2A.X gene transcription is regulated differently than transcription of o ther replication-linked histone genes. Mol Cell Biol 13: 984-992.
5. Braastad CD, Hovhannisyan H, van Wijnen AJ, Stein JL, Stein GS. 2004. Functional characterization of a human histone gene cluster duplication. Gene 342: 35-40.
6. Cakmakci N G,Lerner RS,Wagner EJ,Zheng L,Marzluff WF. 2008 SLIP1, a factor required for activation of histone mRNA translation by the stem-loop binding protein Mol Cell Biol, 28, 1182-1194.
7. Cox MP, Pe terson DA, Biggs PJ. 2010. SolexaQA: at-a-glance quality assessment of Illumina second-generation sequencing data. BMC Bioinform 11: 485.
8. Dávila Ló pez M, Samuelsson T. 2008. Early evolution of histone mRNA 3? end processing. RNA 14: 1-10.
9. Dickey JS, Redon CE, Nakamura AJ, Baird BJ, Sedelnikova OA, Bonner WM. 2009. H2AX: functional roles and potential applications. Chromosoma 118: 683-692.
10. Djebali S, Davis CA, Merkel A, Dobin A, Lassmann T, Mortazavi A, Tanzer A, Lagarde J, Lin W, Schlesinger F, et al. 2012. Landscape of transcription in human cells. Natu re 489: 101-108.
11. Dominski Z, Zheng LX, Sanchez R, Marzluff WF. 1999. Stem-loop binding protein facilitates 3?-end formation by stabilizing U7 snRNP binding to histone pre-mRNA. Mol Cell Biol 19: 3561-3570.
12. Dominski Z, Yang X, Kaygun H, Marzluff WF. 2003. A 3? exonuclease that specifically interacts with the 3? end of histone mRNA. Mol Cell 12: 295-305.
13. Erkmann JA, Sánch ez R, Treichel N, Marzluff WF, Kutay U. 2005. Nuclear export of metazoan replication-dependent histone mRNAs is dependent on RNA length and is mediated by TAP. RNA 11: 45-58.
14. Gorgoni B, Andrews S, Schaller A, Schümperli D, Gray NK, Müller B. 2005. The stem-loop binding protein stimulates histone translation at an early step in the initiation pathway. RNA 11: 1030-1042.
15. Hanson RJ, Sun J, Willis DG, Marzluff WF. 1996. Efficient extraction and partial purification of the polyribosome-associated stem-loop binding protein bound to the 3? end of histone mRNA. Biochemistry 35: 2146-2156.
16. Harris ME, Böhni R, Schneiderman MH, Ramamurthy L, Schümperli D, Marzluff WF. 1991. Regulation of histone mRNA in the unperturbed cell cycle: evidence suggesting control at two posttranscriptional steps. Mol Cell Biol 11: 2416-2424.
17. Hoefig KP, Rath N, Heinz GA, Wolf C, Dameris J, Schepers A, Kremmer E, Ansel KM, Heissmeyer V. 2013. Eri1 degrades the stem-loop of oligouridylated histone mRNAs to induce replication-depen dent decay. Nat Struct Mol Biol 20: 73-81.
18. Holmes WF, Braastad CD, Mitra P, Hampe C, Doenecke D, Albig W, Stein JL, van Wijnen AJ, Stein GS. 2005. Coordinate control and selective expression o f the full complement of replication-dependent histone H4 genes in normal and cancer cells. J Biol Chem 280: 37400-37407.
19. Hsu F, Kent WJ, Clawson H, Kuhn RM, Diekhans M, Haussler D. 2006. The UCSC known genes. Bioinformatics 22: 1036-1046.
20. Isken O, Maquat LE. 2008. The multiple lives ofNMDfactors: balancing roles in gene and genome regulation. Nat Rev Genet 9: 699-712.
21. Kaygun H, Marzluff WF. 2005. Regulated degradation of replication-dependent histone mRNAs requires both ATR and Upf1. Nat Struct Mol Biol 12: 794-800.
22. Kryzwinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA. 2009. Circos: an information aesthetic for comparative genomics. Genome Res 19: 163 9-1645.
23. Langmead B, Trapnell C, Pop M, Salzberg SL. 2009. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10: R25.
24. Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25: 1754-1760.
25. Licatalosi DD, Mele A, Fak JJ, Ule J, Kayikci M, Chi SW, Clark TA, Schweitzer AC, Blume JE, Wang X, et al. 2008. HITS-CLIP yields genome-wide insights into brain alternative RNA processing. Nature 456: 464-469.
26. Mannironi C, Bonner WM, Hatch CL. 1989. H2A.X. a histon e isoprotein with a conserved C-terminal sequence, is encoded by a novel mRNA with both DNA replication type and polyA 3? processing signals. Nucleic Acids Res 17: 9113-9126.
27. Mariñ o-Ramirez L, Levine KM, Morales M, Zhang S, Moreland RT, Baxevanis AD, Landsman D. 2011. The Histone Database: an integrated resource for histones and histone fold-containing proteins. Database (Oxford) 2011: bar048.
28. Martin L,Meier M,Lyons SM,Sit RV,Marzluff WF,Quake SR,Chang HY. 2012 Systematic reconstruction of RNA functional motifs with high-throughput microfluidics Nat Methods 9 1192-1194.
29. Marzluff WF, Gongidi P, Woods KR, Jin J, Maltais LJ. 2002. The human and mouse replication-dependent histone genes. Genomics 80: 487-498.
30. Marzluff WF, Duronio RJ, Wagner EJ. 2008. Metabolism and regulation of canonical histone mRNAs: life without a poly(A) tail. Nat Rev Genet 9: 843-854.
31. Meyer LR, Zweig AS, Hinrichs AS, Karolchik D, Kuhn RM, Wong M, Sloan CA, Rosenbloom KR, Roe G, Rhead B, et al. 2013. The UCSC Genome Browser database: extensions and updates 2013. Nucleic Acids Res 41: D64-D69.
32. Mili S, Steitz JA. 2004. Evidence for reassociation of RNA-binding proteins after cell lysis: implications for the interpretation of immunoprecipitation analyses. RNA 10: 1692-1694.
33. Milligan JF, Groebe DR, Wither ell GW, Uhlenbeck OC. 1987. Oligoribonucleotide synthesis using T7 RNA polymerase and synthetic DNA templates. Nucleic Acids Res 15: 8783-8798.
34. Pandey NB, Marzluff WF. 1987. 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.
35. Pandey NB, Sun J-H, Marzluff WF. 1991. Different complexes are formed on the 3? end of histone mRNA in nuclear and polysomal proteins. Nucleic Acids Res 19: 5653-5659.
36. Perlick HA, Medghalchi SM, Spencer FA, Kendzior RJ, Dietz HC. 1996. Mammalian orthologues of a yeast regula tor of nonsense transcript stability. Proc Natl Acad Sci 93: 10928-10932.
37. Pollard KS, Hubisz MJ, Rosenbloom KR, Siepel A. 2010. Detection of nonneutral substitution rates on mammalian phylogenies. Genome Res 20: 110-121.
38. Pruitt KD, Tatusova T, Brown GR, Maglott DR. 2012. NCBI Reference Sequences (RefSeq): current status, new features and genome annotation policy. Nucleic Acids Res 40: D130-D135.
39. Quinlan AR, Hall IM. 2010. BEDTools: a flexible suite of utilities for comparing genomic features. Bioinformatics 26: 841-842.
40. Robinson MD, McCarthy DJ, Smyth GK. 2010. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26: 139-140.
41. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM. 1998. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273: 5858-5868.
42. Sánchez R, Marzluff WF. 2002. The stem-loop binding protein is required for efficient translation of histone mRNA in vivo and in vitro. Mol Cell Biol 22: 7093-7104.
43. Slevin MK, Meaux S, Welch JD, Bigler R, de Marval PLM, Su W, Prins JF, Rhoads RE, Marzluff WF. 2014. Deep sequencing shows multi ple oligouridylations are required for 3? to 5? degradation of histone mRNAs on polyribosomes. Mol Cell 53: 1020-1030.
44. Sullivan KD, Mullen TE, Marzluff WF, Wagner EJ. 2009. Knockdown of SLBP results in nuclear retention of histone mRNA. RNA 15: 459-472.
45. Sun X, Perlick HA, Dietz HC, Maquat LE. 1998. 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 95: 10009-10014.
46. Tan D, Marzluff WF, Dominski Z, Tong L. 2013. Structure of histone mRNA stem-loop, human stem-loop binding protein, and 3?hExo ternary complex. Science 339: 318-321.
47. Townley-Tilson WH, Pendergrass SA, Marzluff WF, Whitfield ML. 2006. Genome-wide analysis of mRNAs bound to the histone stem-loop binding protein. RNA 12: 1853-1867.
48. Tusher VG, Tibshirani R, Chu G. 2001. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci 98: 5116-5121.
49. Ule J,Jensen KB,Ruggiu M,Mele A,Ule A,Darnell RB. 2003 CLIP identifies Nova-regulated RNA networks in the brain Science 302 1212-1215.
50. 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.
51. von Moeller H, Lerner R, Ricciardi A, Basquin C, Marzluff WF, Conti E. 2013. Structural and biochemical studies of SLIP1-SLBP identify DBP5 and eIF3g as SLIP1-binding proteins. Nucleic Acids Res 14: 79 60-7971.
52. Wang ZF, Whitfield ML, Ingledue TC, Dominski Z, Marzluff WF. 1996. The protein that binds the 3? end of histone mRNA: a novel RNAbinding protein required for histone pre-mRNA processing. Genes Dev 10: 3028-3040.
53. Welch JD, Slevin MK, Tatomer DC, Duronio RJ, Prins JF, Marzluff WF. 2015. EnD-Seq and AppEnD: sequencing 3? ends to identify nontemplated tails and degradation intermediates. RNA 21: 1375-1389.
54. West MHP, Bonner WM. 1980. Histone 2A, a heteromorphous family of eight protein species. Biochemistry 19: 3238-3245.
55. Whitfield ML, Zheng LX, Baldwin A, Ohta T, Hurt MM, Marzluff WF. 2000. 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.
56. Whitfield ML, Kaygun H, Erkmann JA, Townley-Tilson WHD, Dominski Z, Marzluff WF. 2004. SLBP is associated with histone mRNA on polyribosomes as a component of the histone mRNP. Nucleic Acids Res 32: 4 833-4842.
57. Williams AS, Marzluff WF. 1995. The sequence of the stem and flanking sequences at the 3? end of histone mRNA are critical determinants for the binding of the stem-loop binding protein. Nucleic Acids Res 23: 654-662.
58. Yang XC, Purdy M, Marzluff WF, Dominski Z. 2006. Characterization of 3?hExo, a 3? exonuclease specifically interacting with the 3? end of histone mRNA. J Biol Chem 281: 30447-30454.
59. Yang XC, Torres MP, Marzluff WF, Dominski Z. 2009. Three proteins of the U7-specific Sm ring function as the molecular ruler to determine the site of 3?-end processing in mammalian histone pre-mRNA. Mol Cell Biol 29: 4045-4056.
60. Yang L, Duff MO, Graveley BR, Carmichael GG, Chen LL. 2011. Genomewide characterization of non-polyadenylated RNAs. Genome Biol 12: R16.
61. Yeo GW, Coufal NG, Liang TY, Peng GE, Fu XD, Gage FH. 2009. An RNA code for the FOX2 splicing regulator revealed by mapping RNA-protein interactions in stem cells. Nat Struct Mol Biol 16: 130-137.
62. Zhang C, Darnell RB. 2011. Mapping in vivo protein-RNA interactions at single-nucleotide resolution from HITS-CLIP data. Nat Biotechnol 29: 607-614.
63. Zheng L, Dominski Z, Yang X-C, Elms P , Raska CS, Borchers CH, Marzluff WF. 2003. Phosphorylation of stem-loop binding protein (SLBP) on two threonines triggers degradation of SLBP, the sole cell cycle-regulated factor required for regulation of histone mRNA processing, a t the end of S phase. Mol Cell Biol 23: 1590-1601.
64. Zünd D, Gruber AR, Zavolan M, Mühlemann O. 2013. Translation-dependent displacement of UPF1 from coding sequences causes its enrichment in 3? UTRs. Nat Struct Mol Biol 20: 936-943.