Generation of Histone MRNA 3' Ends by Endonucleolytic Cleavage of the Pre-mRNA in a SnRNP-dependent in Vitro Reaction

Overview

Journal EMBO J

Specialties Biotechnology
Molecular Biology

Date 1986 Jun 1

PMID 3015597

Citations 86

Authors

O Gick

A Kramer

W Keller

M L Birnstiel

Affiliations

Soon will be listed here.

Abstract

Incubation of SP6 generated mouse histone H4 mRNA precursors in nuclear extracts of HeLa cells yields processed mRNA species which end on the 3' adenosine of the conserved terminal ACCA sequence not unlike ten different histone mRNAs isolated from sea urchin embryos which end either on the 3' C or A. In the presence of 20 mM EDTA, the cleaved off 3' spacer portions of the RNA transcripts are readily detected, hence the 3' ends of histone mRNAs arise as a consequence of endonucleolytic cleavage(s) of the precursor RNA. The in vitro cleavage reaction is specifically inhibited by human antisera of the Sm-serotype, but not by control sera and can be rescued by the addition of a preparation of partially purified small nuclear RNPs to the antibody-depleted extract. Interestingly, the snRNP preparation is sufficient to elicit 3' processing of pre-mRNA in the absence of added nuclear extract.

Citing Articles

Xrn2 substrate mapping identifies torpedo loading sites and extensive premature termination of RNA pol II transcription.

Cortazar M, Erickson B, Fong N, Pradhan S, Ntini E, Bentley D Genes Dev. 2022; 36(19-20):1062-1078.

PMID: 36396340 PMC: 9744234. DOI: 10.1101/gad.350004.122.

U7 deciphered: the mechanism that forms the unusual 3' end of metazoan replication-dependent histone mRNAs.

Dominski Z, Tong L Biochem Soc Trans. 2021; 49(5):2229-2240.

PMID: 34351387 PMC: 8563397. DOI: 10.1042/BST20210323.

Reconstitution and biochemical assays of an active human histone pre-mRNA 3'-end processing machinery.

Sun Y, Aik W, Yang X, Marzluff W, Dominski Z, Tong L Methods Enzymol. 2021; 655:291-324.

PMID: 34183127 PMC: 8724919. DOI: 10.1016/bs.mie.2021.03.021.

A subset of replication-dependent histone mRNAs are expressed as polyadenylated RNAs in terminally differentiated tissues.

Lyons S, Cunningham C, Welch J, Groh B, Guo A, Wei B Nucleic Acids Res. 2016; 44(19):9190-9205.

PMID: 27402160 PMC: 5100578. DOI: 10.1093/nar/gkw620.

Motif types, motif locations and base composition patterns around the RNA polyadenylation site in microorganisms, plants and animals.

Li X, Du D BMC Evol Biol. 2014; 14:162.

PMID: 25052519 PMC: 4360255. DOI: 10.1186/s12862-014-0162-7.

References

Zaug A, Cech T . The intervening sequence excised from the ribosomal RNA precursor of Tetrahymena contains a 5-terminal guanosine residue not encoded by the DNA. Nucleic Acids Res. 1982; 10(9):2823-38. PMC: 320658. DOI: 10.1093/nar/10.9.2823. View

Birchmeier C, Grosschedl R, Birnstiel M . Generation of authentic 3' termini of an H2A mRNA in vivo is dependent on a short inverted DNA repeat and on spacer sequences. Cell. 1982; 28(4):739-45. DOI: 10.1016/0092-8674(82)90053-8. View

Stunnenberg H, Birnstiel M . Bioassay for components regulating eukaryotic gene expression: a chromosomal factor involved in the generation of histone mRNA 3' termini. Proc Natl Acad Sci U S A. 1982; 79(20):6201-4. PMC: 347087. DOI: 10.1073/pnas.79.20.6201. View

Contreras R, Cheroutre H, Degrave W, Fiers W . Simple, efficient in vitro synthesis of capped RNA useful for direct expression of cloned eukaryotic genes. Nucleic Acids Res. 1982; 10(20):6353-62. PMC: 326924. DOI: 10.1093/nar/10.20.6353. View

Dignam J, Lebovitz R, Roeder R . Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 1983; 11(5):1475-89. PMC: 325809. DOI: 10.1093/nar/11.5.1475. View

Green M, Maniatis T, Melton D . Human beta-globin pre-mRNA synthesized in vitro is accurately spliced in Xenopus oocyte nuclei. Cell. 1983; 32(3):681-94. DOI: 10.1016/0092-8674(83)90054-5. View

Galli G, Hofstetter H, Stunnenberg H, Birnstiel M . Biochemical complementation with RNA in the Xenopus oocyte: a small RNA is required for the generation of 3' histone mRNA termini. Cell. 1983; 34(3):823-8. DOI: 10.1016/0092-8674(83)90539-1. View

Birchmeier C, Folk W, Birnstiel M . The terminal RNA stem-loop structure and 80 bp of spacer DNA are required for the formation of 3' termini of sea urchin H2A mRNA. Cell. 1983; 35(2 Pt 1):433-40. DOI: 10.1016/0092-8674(83)90176-9. View

Altman S . Aspects of biochemical catalysis. Cell. 1984; 36(2):237-9. DOI: 10.1016/0092-8674(84)90216-2. View

10.

Maxson R, Cohn R, Kedes L, Mohun T . Expression and organization of histone genes. Annu Rev Genet. 1983; 17:239-77. DOI: 10.1146/annurev.ge.17.120183.001323. View

11.

Moore C, Sharp P . Site-specific polyadenylation in a cell-free reaction. Cell. 1984; 36(3):581-91. DOI: 10.1016/0092-8674(84)90337-4. View

12.

Birchmeier C, Schumperli D, Sconzo G, Birnstiel M . 3' editing of mRNAs: sequence requirements and involvement of a 60-nucleotide RNA in maturation of histone mRNA precursors. Proc Natl Acad Sci U S A. 1984; 81(4):1057-61. PMC: 344763. DOI: 10.1073/pnas.81.4.1057. View

13.

Kramer A, Keller W, Appel B, Luhrmann R . The 5' terminus of the RNA moiety of U1 small nuclear ribonucleoprotein particles is required for the splicing of messenger RNA precursors. Cell. 1984; 38(1):299-307. DOI: 10.1016/0092-8674(84)90551-8. View

14.

Price D, Parker C . The 3' end of drosophila histone H3 mRNA is produced by a processing activity in vitro. Cell. 1984; 38(2):423-9. DOI: 10.1016/0092-8674(84)90497-5. View

15.

Georgiev O, Mous J, Birnstiel M . Processing and nucleo-cytoplasmic transport of histone gene transcripts. Nucleic Acids Res. 1984; 12(22):8539-51. PMC: 320397. DOI: 10.1093/nar/12.22.8539. View

16.

Strub K, Galli G, Busslinger M, Birnstiel M . The cDNA sequences of the sea urchin U7 small nuclear RNA suggest specific contacts between histone mRNA precursor and U7 RNA during RNA processing. EMBO J. 1984; 3(12):2801-7. PMC: 557769. DOI: 10.1002/j.1460-2075.1984.tb02212.x. View

17.

Hanly S, Bleecker G, Heintz N . Identification of promoter elements necessary for transcriptional regulation of a human histone H4 gene in vitro. Mol Cell Biol. 1985; 5(2):380-9. PMC: 366721. DOI: 10.1128/mcb.5.2.380-389.1985. View

18.

Birnstiel M, Busslinger M, Strub K . Transcription termination and 3' processing: the end is in site!. Cell. 1985; 41(2):349-59. DOI: 10.1016/s0092-8674(85)80007-6. View

19.

Conway L, Wickens M . A sequence downstream of A-A-U-A-A-A is required for formation of simian virus 40 late mRNA 3' termini in frog oocytes. Proc Natl Acad Sci U S A. 1985; 82(12):3949-53. PMC: 397911. DOI: 10.1073/pnas.82.12.3949. View

20.

Moore C, Sharp P . Accurate cleavage and polyadenylation of exogenous RNA substrate. Cell. 1985; 41(3):845-55. DOI: 10.1016/s0092-8674(85)80065-9. View