The Conserved Intronic Cleavage and Polyadenylation Site of CstF-77 Gene Imparts Control of 3′ End Processing Activity through Feedback Autoregulation and by U1 snRNP

PLoS Genetics

Volumn 9, Issue 7, 2013, Pages

  Luo, Wenting ^a,b   Ji, Zhe ^a,b   Pan, Zhenhua ^a   You, Bei ^a   Hoque, Mainul ^a   Li, Wencheng ^a   Gunderson, Samuel I ^c   Tian, Bin ^a  

^a RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^b The State University of New Jersey   (United States)

^c RUTGERS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA PRECURSOR; SMALL NUCLEAR RIBONUCLEOPROTEIN; U1 SNRNP; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ANIMAL CELL; ARTICLE; AUTOREGULATION; CELL PROLIFERATION; CONTROLLED STUDY; CSTF 77 GENE; DIFFERENTIATION; GENE; GENE EXPRESSION; HUMAN; HUMAN CELL; INTRON; NEGATIVE FEEDBACK; NONHUMAN; POLYADENYLATION; RNA CLEAVAGE; RNA PROCESSING; RNA SEQUENCE; RNA SPLICING;

3' UNTRANSLATED REGIONS; CELL DIFFERENTIATION; CELL PROLIFERATION; CLEAVAGE STIMULATION FACTOR; EXONS; GENOME, HUMAN; HELA CELLS; HUMANS; INTRONS; POLYADENYLATION; RIBONUCLEOPROTEIN, U1 SMALL NUCLEAR; RNA SPLICE SITES; RNA, MESSENGER;

EID: 84880809596     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003613     Document Type: Article

References (47)

1. Zhao J, Hyman L, Moore C, (1999) Formation of mRNA 3′ ends in eukaryotes: mechanism, regulation, and interrelationships with other steps in mRNA synthesis. Microbiol Mol Biol Rev 63: 405-445.
2. Colgan DF, Manley JL, (1997) Mechanism and regulation of mRNA polyadenylation. Genes Dev 11: 2755-2766.
3. Tian B, Graber JH, (2011) Signals for pre-mRNA cleavage and polyadenylation. Wiley Interdiscip Rev RNA 3: 385-96.
4. Proudfoot NJ, (2011) Ending the message: poly(A) signals then and now. Genes Dev 25: 1770-1782.
5. Venkataraman K, Brown KM, Gilmartin GM, (2005) Analysis of a noncanonical poly(A) site reveals a tripartite mechanism for vertebrate poly(A) site recognition. Genes Dev 19: 1315-1327.
6. Tian B, Hu J, Zhang H, Lutz CS, (2005) A large-scale analysis of mRNA polyadenylation of human and mouse genes. Nucleic Acids Res 33: 201-212.
7. Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, et al. (2008) Alternative isoform regulation in human tissue transcriptomes. Nature 456: 470-476.
8. Hoque M, Ji Z, Zheng D, Luo W, Li W, et al. (2013) Analysis of alternative cleavage and polyadenylation by 3′ region extraction and deep sequencing. Nat Methods 10: 133-139.
9. Tian B, Pan Z, Lee JY, (2007) Widespread mRNA polyadenylation events in introns indicate dynamic interplay between polyadenylation and splicing. Genome Res 17: 156-165.
10. Takagaki Y, Seipelt RL, Peterson ML, Manley JL, (1996) The polyadenylation factor CstF-64 regulates alternative processing of IgM heavy chain pre-mRNA during B cell differentiation. Cell 87: 941-952.
11. Mandel CR, Bai Y, Tong L, (2008) Protein factors in pre-mRNA 3′-end processing. Cell Mol Life Sci 65: 1099-1122.
12. Shi Y, Di Giammartino DC, Taylor D, Sarkeshik A, Rice WJ, et al. (2009) Molecular architecture of the human pre-mRNA 3′ processing complex. Mol Cell 33: 365-376.
13. Hatton LS, Eloranta JJ, Figueiredo LM, Takagaki Y, Manley JL, et al. (2000) The Drosophila homologue of the 64 kDa subunit of cleavage stimulation factor interacts with the 77 kDa subunit encoded by the suppressor of forked gene. Nucleic Acids Res 28: 520-526.
14. Takagaki Y, Manley JL, (1994) A polyadenylation factor subunit is the human homologue of the Drosophila suppressor of forked protein. Nature 372: 471-474.
15. Bai Y, Auperin TC, Chou CY, Chang GG, Manley JL, et al. (2007) Crystal structure of murine CstF-77: dimeric association and implications for polyadenylation of mRNA precursors. Mol Cell 25: 863-875.
16. Legrand P, Pinaud N, Minvielle-Sebastia L, Fribourg S, (2007) The structure of the CstF-77 homodimer provides insights into CstF assembly. Nucleic Acids Res 35: 4515-4522.
17. Murthy KG, Manley JL, (1995) The 160-kD subunit of human cleavage-polyadenylation specificity factor coordinates pre-mRNA 3′-end formation. Genes Dev 9: 2672-2683.
18. McCracken S, Fong N, Yankulov K, Ballantyne S, Pan G, et al. (1997) The C-terminal domain of RNA polymerase II couples mRNA processing to transcription. Nature 385: 357-361.
19. Mitchelson A, Simonelig M, Williams C, O'Hare K, (1993) Homology with Saccharomyces cerevisiae RNA14 suggests that phenotypic suppression in Drosophila melanogaster by suppressor of forked occurs at the level of RNA stability. Genes Dev 7: 241-249.
20. Simonelig M, Elliott K, Mitchelson A, O'Hare K, (1996) Interallelic complementation at the suppressor of forked locus of Drosophila reveals complementation between suppressor of forked proteins mutated in different regions. Genetics 142: 1225-1235.
21. Audibert A, Simonelig M, (1998) Autoregulation at the level of mRNA 3′ end formation of the suppressor of forked gene of Drosophila melanogaster is conserved in Drosophila virilis. Proc Natl Acad Sci U S A 95: 14302-14307.
22. Juge F, Audibert A, Benoit B, Simonelig M, (2000) Tissue-specific autoregulation of Drosophila suppressor of forked by alternative poly(A) site utilization leads to accumulation of the suppressor of forked protein in mitotically active cells. RNA 6: 1529-1538.
23. Audibert A, Simonelig M, (1999) The suppressor of forked gene of Drosophila, which encodes a homologue of human CstF-77K involved in mRNA 3′-end processing, is required for progression through mitosis. Mech Dev 82: 41-50.
24. Benoit B, Juge F, Iral F, Audibert A, Simonelig M, (2002) Chimeric human CstF-77/Drosophila Suppressor of forked proteins rescue suppressor of forked mutant lethality and mRNA 3′ end processing in Drosophila. Proc Natl Acad Sci U S A 99: 10593-10598.
25. Pan Z, Zhang H, Hague LK, Lee JY, Lutz CS, et al. (2006) An intronic polyadenylation site in human and mouse CstF-77 genes suggests an evolutionarily conserved regulatory mechanism. Gene 366: 325-334.
26. Yeo G, Burge CB, (2004) Maximum entropy modeling of short sequence motifs with applications to RNA splicing signals. J Comput Biol 11: 377-394.
27. Siepel A, Bejerano G, Pedersen JS, Hinrichs AS, Hou M, et al. (2005) Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res 15: 1034-1050.
28. Robberson BL, Cote GJ, Berget SM, (1990) Exon definition may facilitate splice site selection in RNAs with multiple exons. Mol Cell Biol 10: 84-94.
29. Sheets MD, Ogg SC, Wickens MP, (1990) Point mutations in AAUAAA and the poly (A) addition site: effects on the accuracy and efficiency of cleavage and polyadenylation in vitro. Nucleic Acids Res 18: 5799-5805.
30. Ji Z, Tian B, (2009) Reprogramming of 3′ untranslated regions of mRNAs by alternative polyadenylation in generation of pluripotent stem cells from different cell types. PLoS One 4: e8419.
31. Ji Z, Lee JY, Pan Z, Jiang B, Tian B, (2009) Progressive lengthening of 3′ untranslated regions of mRNAs by alternative polyadenylation during mouse embryonic development. Proc Natl Acad Sci U S A 106: 7028-7033.
32. Gunderson SI, Polycarpou-Schwarz M, Mattaj IW, (1998) U1 snRNP inhibits pre-mRNA polyadenylation through a direct interaction between U1 70K and poly(A) polymerase. Mol Cell 1: 255-264.
33. Das BK, Xia L, Palandjian L, Gozani O, Chyung Y, et al. (1999) Characterization of a protein complex containing spliceosomal proteins SAPs 49, 130, 145, and 155. Mol Cell Biol 19: 6796-6802.
34. Valcarcel J, Gaur RK, Singh R, Green MR, (1996) Interaction of U2AF65 RS region with pre-mRNA branch point and promotion of base pairing with U2 snRNA [corrected]. Science 273: 1706-1709.
35. Goraczniak R, Behlke MA, Gunderson SI, (2009) Gene silencing by synthetic U1 adaptors. Nat Biotechnol 27: 257-263.
36. Berg MG, Singh LN, Younis I, Liu Q, Pinto AM, et al. (2012) U1 snRNP determines mRNA length and regulates isoform expression. Cell 150: 53-64.
37. Peterson ML, Perry RP, (1986) Regulated production of mu m and mu s mRNA requires linkage of the poly(A) addition sites and is dependent on the length of the mu s-mu m intron. Proc Natl Acad Sci U S A 83: 8883-8887.
38. Peterson ML, Perry RP, (1989) The regulated production of mu m and mu s mRNA is dependent on the relative efficiencies of mu s poly(A) site usage and the c mu 4-to-M1 splice. Mol Cell Biol 9: 726-738.
39. Phillips C, Pachikara N, Gunderson SI, (2004) U1A inhibits cleavage at the immunoglobulin M heavy-chain secretory poly(A) site by binding between the two downstream GU-rich regions. Mol Cell Biol 24: 6162-6171.
40. Martincic K, Alkan SA, Cheatle A, Borghesi L, Milcarek C, (2009) Transcription elongation factor ELL2 directs immunoglobulin secretion in plasma cells by stimulating altered RNA processing. Nat Immunol 10: 1102-1109.
41. Perez Canadillas JM, Varani G, (2003) Recognition of GU-rich polyadenylation regulatory elements by human CstF-64 protein. EMBO J 22: 2821-2830.
42. Yao C, Biesinger J, Wan J, Weng L, Xing Y, et al. (2012) Transcriptome-wide analyses of CstF64-RNA interactions in global regulation of mRNA alternative polyadenylation. Proc Natl Acad Sci U S A 109: 18773-18778.
43. Ji Z, Luo W, Li W, Hoque M, Pan Z, et al. (2011) Transcriptional activity regulates alternative cleavage and polyadenylation. Mol Syst Biol 7: 534.
44. Lee JY, Yeh I, Park JY, Tian B, (2007) PolyA_DB 2: mRNA polyadenylation sites in vertebrate genes. Nucleic Acids Res 35: D165-168.
45. Jurica MS, Moore MJ, (2003) Pre-mRNA splicing: awash in a sea of proteins. Mol Cell 12: 5-14.
46. Hofacker IL, (2003) Vienna RNA secondary structure server. Nucleic Acids Research 31: 3429-3431.
47. Huang da W, Sherman BT, Lempicki RA, (2009) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57.