The end of the message: Multiple protein–RNA interactions define the mRNA polyadenylation site

Genes and Development

Volumn 29, Issue 9, 2015, Pages 889-897

  Shi, Yongsheng ^a   Manley, James L ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Och Spine at New York Presbyterian Hospitals   (United States)

Author keywords

Gene expression; mRNA processing; Poly(A) site recognition

Indexed keywords

CLEAVAGE AND POLYADENYLATION SPECIFICITY FACTOR; MESSENGER RNA; MESSENGER RNA PRECURSOR; SERINE ARGININE RICH PROTEIN; PROTEIN BINDING; RNA PRECURSOR;

ARTICLE; CELLS BY BODY ANATOMY; DNA DAMAGE; GENE EXPRESSION; HUMAN; MOLECULAR RECOGNITION; POLYADENYLATION; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; REGULATORY MECHANISM; RNA BINDING; RNA SEQUENCE; STEREOSPECIFICITY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; NUCLEOTIDE SEQUENCE; PROTEIN MOTIF;

AMINO ACID MOTIFS; CLEAVAGE AND POLYADENYLATION SPECIFICITY FACTOR; CONSERVED SEQUENCE; GENE EXPRESSION REGULATION; POLYADENYLATION; PROTEIN BINDING; RNA PRECURSORS; RNA, MESSENGER;

EID: 84929453434     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.261974.115     Document Type: Article

References (108)

1. Avendano-Vazquez SE, Dhir A, Bembich S, Buratti E, Proudfoot N, Baralle FE. 2012. Autoregulation of TDP-43 mRNA levels involves interplay between transcription, splicing, and alternative polyA site selection. Genes Dev 26: 1679–1684.
2. Bai Y, Auperin TC, Chou CY, Chang GG, Manley JL, Tong L. 2007. Crystal structure of murine CstF-77: dimeric association and implications for polyadenylation of mRNA precursors. Mol Cell 25: 863–875.
3. Barabino SM, Hubner W, Jenny A, Minvielle-Sebastia L, Keller W. 1997. The 30-kD subunit of mammalian cleavage and polyadenylation specificity factor and its yeast homolog are RNAbinding zinc finger proteins. Genes Dev 11: 1703–1716.
4. Batra R, Charizanis K, Manchanda M, Mohan A, Li M, Finn DJ, Goodwin M, Zhang C, Sobczak K, Thornton CA, et al. 2014. Loss of MBNL leads to disruption of developmentally regulated alternative polyadenylation in RNA-mediated disease. Mol Cell 56: 311–322.
5. Bava FA, Eliscovich C, Ferreira PG, Minana B, Ben-Dov C, Guigo R, Valcarcel J, Mendez R. 2013. CPEB1 coordinates alternative 3′-UTR formation with translational regulation. Nature 495: 121–125.
6. Beaudoing E, Freier S, Wyatt JR, Claverie JM, Gautheret D. 2000. Patterns of variant polyadenylation signal usage in human genes. Genome Res 10: 1001–1010.
7. Bentley DL. 2005. Rules of engagement: co-transcriptional recruitment of pre-mRNA processing factors. Curr Opin Cell Biol 17: 251–256.
8. Berg MG, Singh LN, Younis I, Liu Q, Pinto AM, Kaida D, Zhang Z, Cho S, Sherrill-Mix S, Wan L, et al. 2012. U1 snRNP determines mRNA length and regulates isoform expression. Cell 150: 53–64.
9. Bienroth S, Wahle E, Suter-Crazzolara C, Keller W. 1991. Purification of the cleavage and polyadenylation factor involved in the 3′-processing of messenger RNA precursors. J Biol Chem 266: 19768–19776.
10. Brass AL, Huang IC, Benita Y, John SP, Krishnan MN, Feeley EM, Ryan BJ, Weyer JL, van derWeyden L, Fikrig E, et al. 2009. The IFITM proteins mediate cellular resistance to influenza A H1N1 virus, West Nile virus, and dengue virus. Cell 139: 1243–1254.
11. Brown KM, Gilmartin GM. 2003.Amechanism for the regulation of pre-mRNA 3′ processing by human cleavage factor Im. Mol Cell 12: 1467–1476.
12. Castelo-Branco P, Furger A, Wollerton M, Smith C, Moreira A, Proudfoot N. 2004. Polypyrimidine tract binding protein modulates efficiency of polyadenylation. Mol Cell Biol 24: 4174–4183.
13. Chan S, Choi EA, Shi Y. 2011. Pre-mRNA 3′-end processing complex assembly and function. Wiley Interdiscip Rev RNA 2: 321–335.
14. Chan S, Huppertz I, Yao C, Weng L, Moresco J, Yates JR, Ule J, Manley J, Shi Y. 2014. CPSF30 and Wdr33 directly bind to AAUAAA in mammalian mRNA 3′ processing. Genes Dev 28: 2370–2380.
15. Chen J, Tang H, Wu Z, Zhou C, Jiang T, Xue Y, Huang G, Yan D, Peng Z. 2013. Overexpression of RBBP6, alone or combined with mutant TP53, is predictive of poor prognosis in colon cancer. PLoS One 8: e66524.
16. Christofori G, Keller W. 1988. 3′ cleavage and polyadenylation of mRNA precursors in vitro requires a poly(A) polymerase, a cleavage factor, and a snRNP. Cell 54: 875–889.
17. Cler E, Papai G, Schultz P, Davidson I. 2009. Recent advances in understanding the structure and function of general transcription factor TFIID. Cell Mol Life Sci 66: 2123–2134.
18. Colgan DF, Manley JL. 1997. Mechanism and regulation of mRNA polyadenylation. Genes Dev 11: 2755–2766.
19. Cooke C, Alwine JC. 1996. The cap and the 3′ splice site similarly affect polyadenylation efficiency. Mol Cell Biol 16: 2579–2584.
20. Decorsiere A, Cayrel A, Vagner S, Millevoi S. 2011. Essential role for the interaction between hnRNP H/F and aGquadruplex in maintaining p53 pre-mRNA 3′-end processing and function during DNA damage. Genes Dev 25: 220–225.
21. Dichtl B, Blank D, Sadowski M, Hubner W, Weiser S, Keller W. 2002. Yhh1p/Cft1p directly links poly(A) site recognition and RNA polymerase II transcription termination. EMBO J 21: 4125–4135.
22. Di Giammartino DC, Nishida K, Manley JL. 2011. Mechanisms and consequences of alternative polyadenylation. Mol Cell 43: 853–866.
23. Di Giammartino DC, Li W, Ogami K, Yashinskie JJ, Hoque M, Tian B, Manley JL. 2014. RBBP6 isoforms regulate the human polyadenylation machinery and modulate expression of mRNAs with AU-rich 3′ UTRs. Genes Dev 28: 2248–2260.
24. Elkon R, Ugalde AP, Agami R. 2013. Alternative cleavage and polyadenylation: extent, regulation and function. Nat Rev Genet 14: 496–506.
25. Erkelenz S, Mueller WF, Evans MS, Busch A, Schoneweis K, Hertel KJ, Schaal H. 2013. Position-dependent splicing activation and repression by SR and hnRNP proteins rely on common mechanisms. RNA 19: 96–102.
26. Flaherty SM, Fortes P, Izaurralde E, Mattaj IW, Gilmartin GM. 1997. Participation of the nuclear cap binding complex in pre-mRNA 3′ processing. Proc Natl Acad Sci 94: 11893–11898.
27. Flavell SW, Kim TK, Gray JM, Harmin DA, Hemberg M, Hong EJ, Markenscoff-Papadimitriou E, Bear DM, Greenberg ME. 2008. Genome-wide analysis of MEF2 transcriptional program reveals synaptic target genes and neuronal activity-dependent polyadenylation site selection. Neuron 60: 1022–1038.
28. Fu XD, Ares M Jr. 2014. Context-dependent control of alternative splicing by RNA-binding proteins. Nat Rev Genet 15: 689–701.
29. Gawande B, Robida MD, Rahn A, Singh R. 2006. Drosophila sexlethal protein mediates polyadenylation switching in the female germline. EMBO J 25: 1263–1272.
30. Gilmartin GM, Nevins JR. 1991. Molecular analyses of two poly (A) site-processing factors that determine the recognition and efficiency of cleavage of the pre-mRNA. Mol Cell Biol 11: 2432–2438.
31. Gomes NP, Bjerke G, Llorente B, Szostek SA, Emerson BM, Espinosa JM. 2006. Gene-specific requirement for P-TEFb activity and RNA polymerase II phosphorylation within the p53 transcriptional program. Genes Dev 20: 601–612.
32. Graber JH, Nazeer FI, Yeh PC, Kuehner JN, Borikar S, Hoskinson D, Moore CL. 2013. DNA damage induces targeted, genomewide variation of poly(A) sites in budding yeast. Genome Res 23: 1690–1703.
33. Gruber AR, Martin G, Keller W, Zavolan M. 2012. Cleavage factor Im is a key regulator of 3′ UTR length. RNA Biol 9: 1405–1412.
34. Gunderson SI, Vagner S, Polycarpou-Schwarz M, Mattaj IW. 1997. Involvement of the carboxyl terminus of vertebrate poly(A) polymerase in U1A autoregulation and in the coupling of splicing and polyadenylation. Genes Dev 11: 761–773.
35. 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.
36. Hirose Y, Manley JL. 2000. RNA polymerase II and the integration of nuclear events. Genes Dev 14: 1415–1429.
37. Hu J, Lutz CS, Wilusz J, Tian B. 2005. Bioinformatic identification of candidate cis-regulatory elements involved in human mRNA polyadenylation. RNA 11: 1485–1493.
38. Hudson BP, Martinez-Yamout MA, Dyson HJ, Wright PE. 2004. Recognition of the mRNAAU-rich element by the zinc finger domain of TIS11d. Nat Struct Mol Biol 11: 257–264.
39. Jenal M, Elkon R, Loayza-Puch F, van Haaften G, Kuhn U, Menzies FM, Oude Vrielink JA, Bos AJ, Drost J, Rooijers K, et al. 2012. The poly(A)-binding protein nuclear 1 suppresses alternative cleavage and polyadenylation sites. Cell 149: 538–553.
40. Jensen KB, Dredge BK, Stefani G, Zhong R, Buckanovich RJ, Okano HJ, Yang YY, Darnell RB. 2000. Nova-1 regulates neuron- specific alternative splicing and is essential for neuronal viability. Neuron 25: 359–371.
41. Ji Z, Lee JY, Pan Z, Jiang B, Tian B. 2009. Progressive lengthening of 3′ untranslated regions ofmRNAsby alternative polyadenylation during mouse embryonic development. Proc Natl Acad Sci 106: 7028–7033.
42. Kaida D, Berg MG, Younis I, Kasim M, Singh LN,Wan L, Dreyfuss G. 2010. U1 snRNP protects pre-mRNAs from premature cleavage and polyadenylation. Nature 468: 664–668.
43. Kaufmann I, Martin G, Friedlein A, Langen H, Keller W. 2004. Human Fip1 is a subunit of CPSF that binds to U-rich RNA elements and stimulates poly(A) polymerase. EMBO J 23: 616–626.
44. Keller W, Bienroth S, Lang KM, Christofori G. 1991. Cleavage and polyadenylation factor CPF specifically interacts with the premRNA 3′ processing signal AAUAAA. EMBO J 10: 4241–4249.
45. Kleiman FE, Manley JL. 2001. The BARD1–CstF-50 interaction linksmRNA3′ end formation toDNAdamage and tumor suppression. Cell 104: 743–753.
46. Kyburz A, Friedlein A, Langen H, Keller W. 2006. Direct interactions between subunits of CPSF and the U2 snRNP contribute to the coupling of pre-mRNA 3′ end processing and splicing. Mol Cell 23: 195–205.
47. Lackford B, Yao C, Charles GM, Weng L, Zheng X, Choi EA, Xie X, Wan J, Xing Y, Freudenberg JM, et al. 2014. Fip1 regulates mRNA alternative polyadenylation to promote stem cell self-renewal. EMBO J 33: 878–889.
48. Lau CK, Bachorik JL, Dreyfuss G. 2009. Gemin5-snRNA interaction reveals an RNA binding function forWDrepeat domains. Nat Struct Mol Biol 16: 486–491.
49. Lee SD, Moore CL. 2014. Efficient mRNA polyadenylation requires a ubiquitin-like domain, a zinc knuckle, and a RING finger domain, all contained in the Mpe1 protein. Mol Cell Biol 34: 3955–3967.
50. Li L, Deng B, Xing G, Teng Y, Tian C, Cheng X, Yin X, Yang J, Gao X, Zhu Y, et al. 2007. PACT is a negative regulator of p53 and essential for cell growth and embryonic development. Proc Natl Acad Sci 104: 7951–7956.
51. Licatalosi DD, Mele A, Fak JJ, Ule J, Kayikci M, Chi SW, Clark TA, Schweitzer AC, Blume JE, Wang X, et al. 2008. HITSCLIP yields genome-wide insights into brain alternative RNA processing. Nature 456: 464–469.
52. MacDonald CC, Wilusz J, Shenk T. 1994. 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 14: 6647–6654.
53. Martin G, Gruber AR, Keller W, Zavolan M. 2012. Genome-wide analysis of pre-mRNA3′ end processing reveals a decisive role of human cleavage factor I in the regulation of 3′ UTR length. Cell Rep 1: 753–763.
54. Marzluff WF, Wagner EJ, Duronio RJ. 2008. Metabolism and regulation of canonical histone mRNAs: life without a poly(A) tail. Nat Rev Genet 9: 843–854.
55. Masamha CP, Xia Z, Yang J, Albrecht TR, Li M, Shyu AB, Li W, Wagner EJ. 2014. CFIm25 links alternative polyadenylation to glioblastoma tumour suppression. Nature 510: 412–416.
56. Mayr C, Bartel DP. 2009.Widespread shortening of 3′UTRs by alternative cleavage and polyadenylation activates oncogenes in cancer cells. Cell 138: 673–684.
57. Mbita Z, Meyer M, Skepu A, Hosie M, Rees J, Dlamini Z. 2012. De-regulation of the RBBP6 isoform 3/DWNN in human cancers. Mol Cell Biochem 362: 249–262.
58. Millevoi S, Geraghty F, Idowu B, Tam JL, Antoniou M, Vagner S. 2002. A novel function for the U2AF 65 splicing factor in promoting pre-mRNA 3′-end processing. EMBO Rep 3: 869–874.
59. Millevoi S, Loulergue C, Dettwiler S, Karaa SZ, Keller W, Antoniou M, Vagner S. 2006. An interaction between U2AF 65 and CF I(m) links the splicing and 3′ end processing machineries. EMBO J 25: 4854–4864.
60. Miotto B, Chibi M, Xie P, Koundrioukoff S, Moolman-Smook H, Pugh D, Debatisse M, He F, Zhang L, Defossez PA. 2014. The RBBP6/ZBTB38/MCM10 axis regulates DNA replication and common fragile site stability. Cell Rep 7: 575–587.
61. Monarez RR, MacDonald CC, Dass B. 2007. Polyadenylation proteins CstF-64 and τCstF-64 exhibit differential binding affinities for RNA polymers. Biochem J 401: 651–658.
62. Moreno-Morcillo M, Minvielle-Sebastia L, Mackereth C, Fribourg S. 2011. Hexameric architecture of CstF supported by CstF-50 homodimerization domain structure. RNA 17: 412–418.
63. Mueller AA, Cheung TH, Rando TA. 2013. All’s well that ends well: alternative polyadenylation and its implications for stem cell biology. Curr Opin Cell Biol 25: 222–232.
64. Muller F, Zaucker A, Tora L. 2010. Developmental regulation of transcription initiation: more than just changing the actors. Curr Opin Genet Dev 20: 533–540.
65. Murthy KG, Manley JL. 1992. Characterization of the multisubunit cleavage-polyadenylation specificity factor from calf thymus. J Biol Chem 267: 14804–14811.
66. Murthy KG, Manley JL. 1995. The 160-kD subunit of human cleavage-polyadenylation specificity factor coordinates premRNA 3′-end formation. Genes Dev 9: 2672–2683.
67. Nemeroff ME, Barabino SM, Li Y, Keller W, Krug RM. 1998. Influenza virus NS1 protein interacts with the cellular 30 kDa subunit of CPSF and inhibits 3′end formation of cellular premRNAs. Mol Cell 1: 991–1000.
68. Oktaba K, Zhang W, Lotz TS, Jun DJ, Lemke SB, Ng SP, Esposito E, Levine M, Hilgers V. 2015. ELAV links paused Pol II to alternative polyadenylation in the Drosophila nervous system. Mol Cell 57: 341–348.
69. Perez Canadillas JM, Varani G. 2003. Recognition of GU-rich polyadenylation regulatory elements by human CstF-64 protein. EMBO J 22: 2821–2830.
70. Proudfoot NJ. 2011. Ending the message: poly(A) signals then and now. Genes Dev 25: 1770–1782.
71. Proudfoot NJ, Furger A, Dye MJ. 2002. Integrating mRNA processing with transcription. Cell 108: 501–512.
72. Rappsilber J, Ryder U, Lamond AI, Mann M. 2002. Large-scale proteomic analysis of the human spliceosome. Genome Res 12: 1231–1245.
73. Ruegsegger U, Beyer K, Keller W. 1996. Purification and characterization of human cleavage factor Im involved in the 3′ end processing of messenger RNA precursors. J Biol Chem 271: 6107–6113.
74. Ruegsegger U, Blank D, Keller W. 1998. Human pre-mRNAcleavage factor Im is related to spliceosomal SR proteins and can be reconstituted in vitro from recombinant subunits. Mol Cell 1: 243–253.
75. Saijo M, Sakai Y, Kishino T, Niikawa N, Matsuura Y, Morino K, Tamai K, Taya Y. 1995. Molecular cloning of a human protein that binds to the retinoblastoma protein and chromosomal mapping. Genomics 27: 511–519.
76. Sakai Y, Saijo M, Coelho K, Kishino T, Niikawa N, Taya Y. 1995. cDNA sequence and chromosomal localization of a novel human protein, RBQ-1 (RBBP6), that binds to the retinoblastoma gene product. Genomics 30: 98–101.
77. Sandberg R, Neilson JR, Sarma A, Sharp PA, Burge CB. 2008. Proliferating cells expressmRNAswith shortened 3′ untranslated regions and fewer microRNA target sites. Science 320: 1643–1647.
78. Schonemann L, Kuhn U, Martin G, Schafer P, Gruber AR, Keller W, Zavolan M, Wahle E. 2014. Reconstitution of CPSF active in polyadenylation: recognition of the polyadenylation signal by WDR33. Genes Dev 28: 2381–2393.
79. Shankarling GS, Coates PW, Dass B, Macdonald CC. 2009.Afamily of splice variants of CstF-64 expressed in vertebrate nervous systems. BMC Mol Biol 10: 22.
80. Shepard PJ, Choi EA, Lu J, Flanagan LA, Hertel KJ, Shi Y. 2011. Complex and dynamic landscape of RNA polyadenylation revealed by PAS-Seq. RNA 17: 761–772.
81. Shi Y. 2012. Alternative polyadenylation: new insights from global analyses. RNA 18: 2105–2117.
82. Shi Y, Di Giammartino DC, Taylor D, Sarkeshik A, Rice WJ, Yates JR III, Frank J, Manley JL. 2009. Molecular architecture of the human pre-mRNA 3′ processing complex. Mol Cell 33: 365–376.
83. Simons A, Melamed-Bessudo C, Wolkowicz R, Sperling J, Sperling R, Eisenbach L, Rotter V. 1997. PACT: cloning and characterization of a cellular p53 binding protein that interacts with Rb. Oncogene 14: 145–155.
84. Sullivan KD, Steiniger M, Marzluff WF. 2009. A core complex of CPSF73, CPSF100, and Symplekin may form two different cleavage factors for processing of poly(A) and histone mRNAs. Mol Cell 34: 322–332.
85. Tacahashi Y, Helmling S, Moore CL. 2003. Functional dissection of the zinc finger and flanking domains of the Yth1 cleavage/ polyadenylation factor. Nucleic Acids Res 31: 1744–1752.
86. Tacke R, Manley JL. 1996. SR proteins and splicing control. Genes Dev 10: 1569–1579.
87. Takagaki Y, Manley JL. 1997. RNA recognition by the human polyadenylation factor CstF. Mol Cell Biol 17: 3907–3914.
88. Takagaki Y, Manley JL. 2000. Complex protein interactions within the human polyadenylation machinery identify a novel component. Mol Cell Biol 20: 1515–1525.
89. Takagaki Y, Ryner LC, Manley JL. 1989. Four factors are required for 3′-end cleavage of pre-mRNAs. Genes Dev 3: 1711–1724.
90. Takagaki Y, Manley JL, MacDonald CC, Wilusz J, Shenk T. 1990. A multisubunit factor, CstF, is required for polyadenylation of mammalian pre-mRNAs. Genes Dev 4: 2112–2120.
91. Thomas MC, Chiang CM. 2006. The general transcription machinery and general cofactors. Crit Rev Biochem Mol Biol 41: 105–178.
92. Tian B, Graber JH. 2012. Signals for pre-mRNA cleavage and polyadenylation. Wiley Interdiscip Rev RNA 3: 385–396.
93. Tian B, Manley JL. 2013. Alternative cleavage and polyadenylation: the long and short of it. Trends Biochem Sci 38: 312–320.
94. Twu KY, Noah DL, Rao P, Kuo RL, Krug RM. 2006. The CPSF30 binding site on the NS1A protein of influenza A virus is a potential antiviral target. J Virol 80: 3957–3965.
95. Vo LT, Minet M, Schmitter JM, Lacroute F, Wyers F. 2001. Mpe1, a zinc knuckle protein, is an essential component of yeast cleavage and polyadenylation factor required for the cleavage and polyadenylation of mRNA. Mol Cell Biol 21: 8346–8356.
96. Wahl MC, Will CL, Luhrmann R. 2009. The spliceosome: design principles of a dynamic RNP machine. Cell 136: 701–718.
97. Wallace AM, Dass B, Ravnik SE, Tonk V, Jenkins NA, Gilbert DJ, Copeland NG, MacDonald CC. 1999. 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 96: 6763–6768.
98. Wang Y, Ma M, Xiao X, Wang Z. 2012. Intronic splicing enhancers, cognate splicing factors and context-dependent regulation rules. Nat Struct Mol Biol 19: 1044–1052.
99. Yang Q, Coseno M, Gilmartin GM, Doublie S. 2010a. Crystal structure of a human cleavage factor CFI(m)25/CFI(m)68/ RNA complex provides an insight into poly(A) site recognition and RNA looping. Structure 19: 368–377.
100. Yang Q, Gilmartin GM, Doublie S. 2010b. Structural basis of UGUA recognition by the Nudix protein CFI(m)25 and implications for a regulatory role inmRNA3′ processing. Proc Natl Acad Sci 107: 10062–10067.
101. Yang Q, Gilmartin GM, Doublie S. 2011. The structure of human cleavage factor I(m) hints at functions beyond UGUA-specific RNA binding: a role in alternative polyadenylation and a potential link to 5′ capping and splicing. RNA Biol 8: 748–753.
102. Yao C, Biesinger J, Wan J, Weng L, Xing Y, Xie X, Shi Y. 2012. Transcriptome-wide analyses of CstF64-RNA interactions in global regulation of mRNA alternative polyadenylation. Proc Natl Acad Sci 109: 18773–18778.
103. Yao C, Choi EA, Weng L, Xie X, Wan J, Xing Y, Moresco JJ, Tu PG, Yates JR III, Shi Y. 2013. Overlapping and distinct functions of CstF64 and CstF64τ in mammalian mRNA 3′ processing. RNA 19: 1781–1790.
104. Zarudnaya MI, Kolomiets IM, Potyahaylo AL, Hovorun DM. 2003. Downstream elements of mammalian pre-mRNA polyadenylation signals: primary, secondary and higher-order structures. Nucleic Acids Res 31: 1375–1386.
105. Zhao J, Kessler MM, Moore CL. 1997. Cleavage factor II of Saccharomyces cerevisiae contains homologues to subunits of the mammalian cleavage/polyadenylation specificity factor and exhibits sequence-specific, ATP-dependent interaction with precursor RNA. J Biol Chem 272: 10831–10838.
106. 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.
107. Zhou Z, Licklider LJ, Gygi SP, Reed R. 2002. Comprehensive proteomic analysis of the human spliceosome. Nature 419: 182–185.
108. Zhu H, Zhou HL, Hasman RA, Lou H. 2007. Hu proteins regulate polyadenylation by blocking sites containing U-rich sequences. J Biol Chem 282: 2203–2210.