mRNA polyadenylation. 1. 3\'-end formation of vertebrates\' mRNAs

Zarudnaya, M. I.

doi:10.7124/bc.0005A2

Biopolym. Cell. 2001; 17(2):93-108.

http://dx.doi.org/10.7124/bc.0005A2

Reviews

mRNA polyadenylation. 1. 3'-end formation of vertebrates' mRNAs

1Zarudnaya M. I.

Institute of Molecular Biology and Genetics, NAS of Ukraine
150, Akademika Zabolotnoho Str., Kyiv, Ukraine, 03680

Abstract

In this review the contemporary understanding of a process of the 3'-end formation of vertebrates' mRNAs is summarized. The protein factors taking part in the reaction, and the signal sequences in pre-mRNAs guiding the process are characterized. The process of polyadenylation complex formation is analyzed. The relation between polyadenylation, on one hand, and transcription and splicing, on the other hand, is considered. The examples of the regulation of the polyadenylation reaction are given. The author proposes more strict definition of downstream signal than that available in literature.

Full text: (PDF, in Russian)

References

[1] Chen Z, Li Y, Krug RM. Influenza A virus NS1 protein targets poly(A)-binding protein II of the cellular 3'-end processing machinery. EMBO J. 1999;18(8):2273-83.

[2] Wang Z, Day N, Trifillis P, Kiledjian M. An mRNA stability complex functions with poly(A)-binding protein to stabilize mRNA in vitro. Mol Cell Biol. 1999;19(7):4552-60.

[3] Decker CJ, Parker R. A turnover pathway for both stable and unstable mRNAs in yeast: evidence for a requirement for deadenylation. Genes Dev. 1993;7(8):1632-43.

[4] Craig AW, Haghighat A, Yu AT, Sonenberg N. Interaction of polyadenylate-binding protein with the eIF4G homologue PAIP enhances translation. Nature. 1998;392(6675):520-3.

[5] Taneja KL, Lifshitz LM, Fay FS, Singer RH. Poly(A) RNA codistribution with microfilaments: evaluation by in situ hybridization and quantitative digital imaging microscopy. J Cell Biol. 1992;119(5):1245-60.

[6] Manley JL. Messenger RNA polyadenylylation: a universal modification. Proc Natl Acad Sci U S A. 1995;92(6):1800-1.

[7] Dominski Z, Zheng LX, Sanchez R, Marzluff WF. Stem-loop binding protein facilitates 3'-end formation by stabilizing U7 snRNP binding to histone pre-mRNA. Mol Cell Biol. 1999;19(5):3561-70.

[8] Williams AS, Ingledue TC 3rd, Kay BK, Marzluff WF. Changes in the stem-loop at the 3' terminus of histone mRNA affects its nucleocytoplasmic transport and cytoplasmic regulation. Nucleic Acids Res. 1994;22(22):4660-6.

[9] Pandey NB, Marzluff WF. The stem-loop structure at the 3' end of histone mRNA is necessary and sufficient for regulation of histone mRNA stability. Mol Cell Biol. 1987;7(12):4557-9.

[10] Sun J, Pilch DR, Marzluff WF. The histone mRNA 3' end is required for localization of histone mRNA to polyribosomes. Nucleic Acids Res. 1992;20(22):6057-66.

[11] Wahle E. 3'-end cleavage and polyadenylation of mRNA precursors. Biochim Biophys Acta. 1995;1261(2):183-94.

[12] Colgan DF, Manley JL. Mechanism and regulation of mRNA polyadenylation. Genes Dev. 1997;11(21):2755-66.

[13] Gilmartin GM, Fleming ES, Oetjen J, Graveley BR. CPSF recognition of an HIV-1 mRNA 3'-processing enhancer: multiple sequence contacts involved in poly(A) site definition. Genes Dev. 1995;9(1):72-83.

[14] Preker PJ, Keller W. The HAT helix, a repetitive motif implicated in RNA processing. Trends Biochem Sci. 1998;23(1):15-6.

[15] R?egsegger U, Blank D, Keller W. Human pre-mRNA cleavage factor Im is related to spliceosomal SR proteins and can be reconstituted in vitro from recombinant subunits. Mol Cell. 1998;1(2):243-53.

[16] Wahle E, R?egsegger U. 3'-End processing of pre-mRNA in eukaryotes. FEMS Microbiol Rev. 1999;23(3):277-95.

[17] Raabe T, Murthy KG, Manley JL. Poly(A) polymerase contains multiple functional domains. Mol Cell Biol. 1994;14(5):2946-57.

[18] Martin G, Keller W. Mutational analysis of mammalian poly(A) polymerase identifies a region for primer binding and catalytic domain, homologous to the family X polymerases, and to other nucleotidyltransferases. EMBO J. 1996;15(10):2593-603.

[19] Nemeth A, Krause S, Blank D, Jenny A, Jen? P, Lustig A, Wahle E. Isolation of genomic and cDNA clones encoding bovine poly(A) binding protein II. Nucleic Acids Res. 1995;23(20):4034-41.

[20] Wahle E, Lustig A, Jen? P, Maurer P. Mammalian poly(A)-binding protein II. Physical properties and binding to polynucleotides. J Biol Chem. 1993;268(4):2937-45.

[21] Burd CG, Dreyfuss G. Conserved structures and diversity of functions of RNA-binding proteins. Science. 1994;265(5172):615-21.

[22] Neer EJ, Schmidt CJ, Nambudripad R, Smith TF. The ancient regulatory-protein family of WD-repeat proteins. Nature. 1994;371(6495):297-300.

[23] Zhao W, Manley JL. Complex alternative RNA processing generates an unexpected diversity of poly(A) polymerase isoforms. Mol Cell Biol. 1996;16(5):2378-86.

[24] Beyer K, Dandekar T, Keller W. RNA ligands selected by cleavage stimulation factor contain distinct sequence motifs that function as downstream elements in 3'-end processing of pre-mRNA. J Biol Chem. 1997;272(42):26769-79.

[25] Wallace AM, Dass B, Ravnik SE, Tonk V, Jenkins NA, Gilbert DJ, Copeland NG, MacDonald CC. Two distinct forms of the 64,000 Mr protein of the cleavage stimulation factor are expressed in mouse male germ cells. Proc Natl Acad Sci U S A. 1999;96(12):6763-8.

[26] Birnstiel ML, Busslinger M, Strub K. Transcription termination and 3' processing: the end is in site! Cell. 1985;41(2):349-59.

[27] Graber JH, Cantor CR, Mohr SC, Smith TF. In silico detection of control signals: mRNA 3'-end-processing sequences in diverse species. Proc Natl Acad Sci U S A. 1999;96(24):14055-60.

[28] Wilusz J, Shenk T. A uridylate tract mediates efficient heterogeneous nuclear ribonucleoprotein C protein-RNA cross-linking and functionally substitutes for the downstream element of the polyadenylation signal. Mol Cell Biol. 1990;10(12):6397-407.

[29] MacDonald CC, Wilusz J, Shenk T. The 64-kilodalton subunit of the CstF polyadenylation factor binds to pre-mRNAs downstream of the cleavage site and influences cleavage site location. Mol Cell Biol. 1994;14(10):6647-54.

[30] Chou ZF, Chen F, Wilusz J. Sequence and position requirements for uridylate-rich downstream elements of polyadenylation signals. Nucleic Acids Res. 1994;22(13):2525-31.

[31] Chen F, MacDonald CC, Wilusz J. Cleavage site determinants in the mammalian polyadenylation signal. Nucleic Acids Res. 1995;23(14):2614-20.

[32] McLauchlan J, Gaffney D, Whitton JL, Clements JB. The consensus sequence YGTGTTYY located downstream from the AATAAA signal is required for efficient formation of mRNA 3' termini. Nucleic Acids Res. 1985;13(4):1347-68.

[33] Gil A, Proudfoot NJ. Position-dependent sequence elements downstream of AAUAAA are required for efficient rabbit beta-globin mRNA 3' end formation. Cell. 1987;49(3):399-406.

[34] Chen JS, Nordstrom JL. Bipartite structure of the downstream element of the mouse beta globin (major) poly(A) signal. Nucleic Acids Res. 1992;20(10):2565-72.

[35] McDevitt MA, Hart RP, Wong WW, Nevins JR. Sequences capable of restoring poly(A) site function define two distinct downstream elements. EMBO J. 1986;5(11):2907-13.

[36] Zhang F, Denome RM, Cole CN. Fine-structure analysis of the processing and polyadenylation region of the herpes simplex virus type 1 thymidine kinase gene by using linker scanning, internal deletion, and insertion mutations. Mol Cell Biol. 1986;6(12):4611-23.

[37] Renan MJ. Conserved 12-bp element downstream from mRNA polyadenylation sites. Gene. 1987;60(2-3):245-54.

[38] Edwalds-Gilbert G, Prescott J, Falck-Pedersen E. 3' RNA processing efficiency plays a primary role in generating termination-competent RNA polymerase II elongation complexes. Mol Cell Biol. 1993;13(6):3472-80.

[39] Lutz CS, Alwine JC. Direct interaction of the U1 snRNP-A protein with the upstream efficiency element of the SV40 late polyadenylation signal. Genes Dev. 1994;8(5):576-86.

[40] Bagga PS, Ford LP, Chen F, Wilusz J. The G-rich auxiliary downstream element has distinct sequence and position requirements and mediates efficient 3' end pre-mRNA processing through a trans-acting factor. Nucleic Acids Res. 1995;23(9):1625-31.

[41] Wassarman KM, Steitz JA. Association with terminal exons in pre-mRNAs: a new role for the U1 snRNP? Genes Dev. 1993;7(4):647-59.

[42] Takagaki Y, Manley JL. RNA recognition by the human polyadenylation factor CstF. Mol Cell Biol. 1997;17(7):3907-14.

[43] Benoit B, Nemeth A, Aulner N, K?hn U, Simonelig M, Wahle E, Bourbon HM. The Drosophila poly(A)-binding protein II is ubiquitous throughout Drosophila development and has the same function in mRNA polyadenylation as its bovine homolog in vitro. Nucleic Acids Res. 1999;27(19):3771-8.

[44] Proudfoot N. Poly(A) signals. Cell. 1991;64(4):671-4.

[45] Sittler A, Gallinaro H, Jacob M. Upstream and downstream cis-acting elements for cleavage at the L4 polyadenylation site of adenovirus-2. Nucleic Acids Res. 1994;22(2):222-31.

[46] Bagga PS, Arhin GK, Wilusz J. DSEF-1 is a member of the hnRNP H family of RNA-binding proteins and stimulates pre-mRNA cleavage and polyadenylation in vitro. Nucleic Acids Res. 1998;26(23):5343-50.

[47] Williamson JR, Raghuraman MK, Cech TR. Monovalent cation-induced structure of telomeric DNA: the G-quartet model. Cell. 1989;59(5):871-80.

[48] Sadofsky M, Connelly S, Manley JL, Alwine JC. Identification of a sequence element on the 3' side of AAUAAA which is necessary for simian virus 40 late mRNA 3'-end processing. Mol Cell Biol. 1985;5(10):2713-9.

[49] Hirose Y, Manley JL. Creatine phosphate, not ATP, is required for 3' end cleavage of mammalian pre-mRNA in vitro. J Biol Chem. 1997;272(47):29636-42.

[50] Chao LC, Jamil A, Kim SJ, Huang L, Martinson HG. Assembly of the cleavage and polyadenylation apparatus requires about 10 seconds in vivo and is faster for strong than for weak poly(A) sites. Mol Cell Biol. 1999;19(8):5588-600.

[51] Flaherty SM, Fortes P, Izaurralde E, Mattaj IW, Gilmartin GM. Participation of the nuclear cap binding complex in pre-mRNA 3' processing. Proc Natl Acad Sci U S A. 1997;94(22):11893-8.

[52] McCracken S, Fong N, Yankulov K, Ballantyne S, Pan G, Greenblatt J, Patterson SD, Wickens M, Bentley DL. The C-terminal domain of RNA polymerase II couples mRNA processing to transcription. Nature. 1997;385(6614):357-61.

[53] Dantonel JC, Murthy KG, Manley JL, Tora L. Transcription factor TFIID recruits factor CPSF for formation of 3' end of mRNA. Nature. 1997;389(6649):399-402.

[54] Hirose Y, Manley JL. RNA polymerase II is an essential mRNA polyadenylation factor. Nature. 1998;395(6697):93-6.

[55] Baur?n G, Belikov S, Wieslander L. Transcriptional termination in the Balbiani ring 1 gene is closely coupled to 3'-end formation and excision of the 3'-terminal intron. Genes Dev. 1998;12(17):2759-69.

[56] Yeung G, Choi LM, Chao LC, Park NJ, Liu D, Jamil A, Martinson HG. Poly(A)-driven and poly(A)-assisted termination: two different modes of poly(A)-dependent transcription termination. Mol Cell Biol. 1998;18(1):276-89.

[57] Stumpf G, Goppelt A, Domdey H. Pre-mRNA topology is important for 3'-end formation in Saccharomyces cerevisiae and mammals. Mol Cell Biol. 1996;16(5):2204-13.

[58] Wahle E, K?hn U. The mechanism of 3' cleavage and polyadenylation of eukaryotic pre-mRNA. Prog Nucleic Acid Res Mol Biol. 1997;57:41-71.

[59] Wahle E. Poly(A) tail length control is caused by termination of processive synthesis. J Biol Chem. 1995;270(6):2800-8.

[60] Zarudna MI, Hovorun DM. Structural transitions in poliadeniloviy acid: possible molecular mechanisms of the functioning of mRNA poly (A) tails. Dopovidi Nats Akad Nauk Ukrainy. 1998;(12):155-60.

[61] Zarudnaya MI, Hovorun DM. Structural transitions in polyadenylic acid and hypothesis on biological role of its double-stranded forms. Ukr Biokhim Zh. 1999;71(4):15-20. Review.

[62] Zarudnaya MI, Zheltovsky NV. Affinity electrophoresis study on the interaction between homopolyribonucleotides and divalent lysine complex. Mol Biol (Mosk). 1992; 26(1):110-7.

[63] Zarudnaia MI, ZHeltovskiĭ NV. Electrophoretic study of conformational transitions in poly(A) at acid pHs. Mol Biol (Mosk). 1995;29(5):1040-7.

[64] Zarudnaia MI. Study of conformational transitions in poly(A) using the buffer capacity method. Mol Biol (Mosk). 1998;32(3):508-14.

[65] Schul W, van Driel R, de Jong L. A subset of poly(A) polymerase is concentrated at sites of RNA synthesis and is associated with domains enriched in splicing factors and poly(A) RNA. Exp Cell Res. 1998;238(1):1-12.

[66] Prescott J, Falck-Pedersen E. Sequence elements upstream of the 3' cleavage site confer substrate strength to the adenovirus L1 and L3 polyadenylation sites. Mol Cell Biol. 1994;14(7):4682-93.

[67] Furth PA, Choe WT, Rex JH, Byrne JC, Baker CC. Sequences homologous to 5' splice sites are required for the inhibitory activity of papillomavirus late 3' untranslated regions. Mol Cell Biol. 1994;14(8):5278-89.

[68] Gunderson SI, Polycarpou-Schwarz M, Mattaj IW. U1 snRNP inhibits pre-mRNA polyadenylation through a direct interaction between U1 70K and poly(A) polymerase. Mol Cell. 1998;1(2):255-64.

[69] Gunderson SI, Vagner S, Polycarpou-Schwarz M, Mattaj IW. Involvement of the carboxyl terminus of vertebrate poly(A) polymerase in U1A autoregulation and in the coupling of splicing and polyadenylation. Genes Dev. 1997;11(6):761-73.

[70] Lutz CS, Murthy KG, Schek N, O'Connor JP, Manley JL, Alwine JC. Interaction between the U1 snRNP-A protein and the 160-kD subunit of cleavage-polyadenylation specificity factor increases polyadenylation efficiency in vitro. Genes Dev. 1996;10(3):325-37.

[71] Klein Gunnewiek JM, Hussein RI, van Aarssen Y, Palacios D, de Jong R, van Venrooij WJ, Gunderson SI. Fourteen residues of the U1 snRNP-specific U1A protein are required for homodimerization, cooperative RNA binding, and inhibition of polyadenylation. Mol Cell Biol. 2000;20(6):2209-17.

[72] Wahle E, Martin G, Schiltz E, Keller W. Isolation and expression of cDNA clones encoding mammalian poly(A) polymerase. EMBO J. 1991;10(13):4251-7.

[73] Carswell S, Alwine JC. Efficiency of utilization of the simian virus 40 late polyadenylation site: effects of upstream sequences. Mol Cell Biol. 1989;9(10):4248-58.

[74] Moreira A, Takagaki Y, Brackenridge S, Wollerton M, Manley JL, Proudfoot NJ. The upstream sequence element of the C2 complement poly(A) signal activates mRNA 3' end formation by two distinct mechanisms. Genes Dev. 1998;12(16):2522-34.

[75] Brackenridge S, Ashe HL, Giacca M, Proudfoot NJ. Transcription and polyadenylation in a short human intergenic region. Nucleic Acids Res. 1997;25(12):2326-36.

[76] Lou H, Gagel RF, Berget SM. An intron enhancer recognized by splicing factors activates polyadenylation. Genes Dev. 1996;10(2):208-19.

[77] Lou H, Neugebauer KM, Gagel RF, Berget SM. Regulation of alternative polyadenylation by U1 snRNPs and SRp20. Mol Cell Biol. 1998;18(9):4977-85.

[78] Ashe MP, Pearson LH, Proudfoot NJ. The HIV-1 5' LTR poly(A) site is inactivated by U1 snRNP interaction with the downstream major splice donor site. EMBO J. 1997;16(18):5752-63.

[79] Vagner S, R?egsegger U, Gunderson SI, Keller W, Mattaj IW. Position-dependent inhibition of the cleavage step of pre-mRNA 3'-end processing by U1 snRNP. RNA. 2000;6(2):178-88.

[80] Ashe MP, Furger A, Proudfoot NJ. Stem-loop 1 of the U1 snRNP plays a critical role in the suppression of HIV-1 polyadenylation. RNA. 2000;6(2):170-7.

[81] Das AT, Klaver B, Klasens BI, van Wamel JL, Berkhout B. A conserved hairpin motif in the R-U5 region of the human immunodeficiency virus type 1 RNA genome is essential for replication. J Virol. 1997;71(3):2346-56.

[82] Valsamakis A, Zeichner S, Carswell S, Alwine JC. The human immunodeficiency virus type 1 polyadenylylation signal: a 3' long terminal repeat element upstream of the AAUAAA necessary for efficient polyadenylylation. Proc Natl Acad Sci U S A. 1991;88(6):2108-12.

[83] Das AT, Klaver B, Berkhout B. A hairpin structure in the R region of the human immunodeficiency virus type 1 RNA genome is instrumental in polyadenylation site selection. J Virol. 1999;73(1):81-91.

[84] Klasens BI, Thiesen M, Virtanen A, Berkhout B. The ability of the HIV-1 AAUAAA signal to bind polyadenylation factors is controlled by local RNA structure. Nucleic Acids Res. 1999;27(2):446-54.

[85] Cooke C, Hans H, Alwine JC. Utilization of splicing elements and polyadenylation signal elements in the coupling of polyadenylation and last-intron removal. Mol Cell Biol. 1999;19(7):4971-9.

[86] Vagner S, Vagner C, Mattaj IW. The carboxyl terminus of vertebrate poly(A) polymerase interacts with U2AF 65 to couple 3'-end processing and splicing. Genes Dev. 2000;14(4):403-13.

[87] Das Gupta J, Gu H, Chernokalskaya E, Gao X, Schoenberg DR. Identification of two cis-acting elements that independently regulate the length of poly(A) on Xenopus albumin pre-mRNA. RNA. 1998;4(7):766-76.

[88] Gu H, Das Gupta J, Schoenberg DR. The poly(A)-limiting element is a conserved cis-acting sequence that regulates poly(A) tail length on nuclear pre-mRNAs. Proc Natl Acad Sci U S A. 1999;96(16):8943-8.

[89] Edwalds-Gilbert G, Veraldi KL, Milcarek C. Alternative poly(A) site selection in complex transcription units: means to an end? Nucleic Acids Res. 1997;25(13):2547-61.