Browse > Article
http://dx.doi.org/10.14348/molcells.2014.0177

New Links between mRNA Polyadenylation and Diverse Nuclear Pathways  

Di Giammartino, Dafne Campigli (Columbia University, Department of Biological Sciences)
Manley, James L. (Columbia University, Department of Biological Sciences)
Publication Information
Molecules and Cells / v.37, no.9, 2014 , pp. 644-649 More about this Journal
Abstract
The 3' ends of most eukaryotic messenger RNAs must undergo a maturation step that includes an endonuc-leolytic cleavage followed by addition of a polyadenylate tail. While this reaction is catalyzed by the action of only two enzymes it is supported by an unexpectedly large number of proteins. This complexity reflects the necessity of coordinating this process with other nuclear events, and growing evidence indicates that even more factors than previously thought are necessary to connect 3' processing to additional cellular pathways. In this review we summarize the current understanding of the molecular machinery involved in this step of mRNA maturation, focusing on new core and auxiliary proteins that connect polyadenylation to splicing, DNA damage, transcription and cancer.
Keywords
3' end processing; cleavage; polyadenylation; pre-mRNA;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Zhao, W., and Manley, J.L. (1996). Complex alternative RNA processing generates an unexpected diversity of poly(A) polymerase isoforms. Mol. Cell. Biol. 16, 2378-2386.   DOI
2 Tian, B., and Manley, J.L. (2013). Alternative cleavage and polyadenylation: the long and short of it. Trends Biochem. Sci. 38, 312-320.   DOI   ScienceOn
3 Topalian, S.L., Kaneko, S., Gonzales, M.I., Bond, G.L., Ward, Y., and Manley, J.L. (2001). Identification and functional characterization of neo-poly(A) polymerase, an RNA processing enzyme overexpressed in human tumors. Mol. Cell. Biol. 21, 5614-5623.   DOI   ScienceOn
4 Vagner, S., Vagner, C., and Mattaj, I.W. (2000). The carboxyl terminus of vertebrate poly(A) polymerase interacts with U2AF 65 to couple 3'-end processing and splicing. Genes Dev. 14, 403-413.
5 Vethantham, V., Rao, N., and Manley, J.L. (2008). Sumoylation regulates multiple aspects of mammalian poly(A) polymerase function. Genes Dev. 22, 499-511.   DOI   ScienceOn
6 Vo, L.T., Minet, M., Schmitter, J.M., Lacroute, F., and 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.   DOI   ScienceOn
7 Wallace, A.M., Dass, B., Ravnik, S.E., Tonk, V., Jenkins, N.A., Gilbert, D.J., Copeland, N.G., and MacDonald, C.C. (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. USA 96, 6763-6768.   DOI
8 Xiang, K., Tong, L., and Manley, J.L. (2014). Delineating the structural blueprint of the pre-mRNA 3'-end processing machinery. Mol. Cell. Biol. 34, 1894-1910.   DOI   ScienceOn
9 Xu, C., and Min, J. (2011). Structure and function of WD40 domain proteins. Protein Cell 2, 202-214.   DOI   ScienceOn
10 Yang, Q., Nausch, L.W., Martin, G., Keller, W., and Doublie, S. (2014). Crystal structure of human poly(a) polymerase gamma reveals a conserved catalytic core for canonical poly(a) polymerases. J. Mol. Biol. 426, 43-50.   DOI   ScienceOn
11 Sakai, Y., Saijo, M., Coelho, K., Kishino, T., Niikawa, N., and 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.   DOI   ScienceOn
12 Simons, A., Melamed-Bessudo, C., Wolkowicz, R., Sperling, J., Sperling, R., Eisenbach, L., and Rotter, V. (1997). PACT: cloning and characterization of a cellular p53 binding protein that interacts with Rb. Oncogene 14, 145-155.   DOI
13 Sandberg, R., Neilson, J.R., Sarma, A., Sharp, P.A., and Burge, C.B. (2008). Proliferating cells express mRNAs with shortened 3' untranslated regions and fewer microRNA target sites. Science 320, 1643-1647.   DOI   ScienceOn
14 Shi, Y., Reddy, B., and Manley, J.L. (2006). PP1/PP2A phosphatases are required for the second step of Pre-mRNA splicing and target specific snRNP proteins. Mol. Cell 23, 819-829.   DOI   ScienceOn
15 Shi, Y., Di Giammartino, D.C., Taylor, D., Sarkeshik, A., Rice, W.J., Yates, J.R., 3rd, Frank, J., and Manley, J.L. (2009). Molecular architecture of the human pre-mRNA 3' processing complex. Mol. Cell 33, 365-376.   DOI   ScienceOn
16 Takagaki, Y., and Manley, J.L. (2000). Complex protein interactions within the human polyadenylation machinery identify a novel component. Mol. Cell. Biol. 20, 1515-1525.   DOI
17 Takagaki, Y., Ryner, L.C., and Manley, J.L. (1988). Separation and characterization of a poly(A) polymerase and a cleavage/specificity factor required for pre-mRNA polyadenylation. Cell 52, 731-742.   DOI   ScienceOn
18 Takata, H., Nishijima, H., Maeshima, K., and Shibahara, K. (2012). The integrator complex is required for integrity of Cajal bodies. J. Cell Sci. 125, 166-175.   DOI   ScienceOn
19 Nagaike, T., Logan, C., Hotta, I., Rozenblatt-Rosen, O., Meyerson, M., and Manley, J.L. (2011). Transcriptional activators enhance polyadenylation of mRNA precursors. Mol. Cell 41, 409-418.   DOI   ScienceOn
20 Ntini, E., Jarvelin, A.I., Bornholdt, J., Chen, Y., Boyd, M., Jorgensen, M., Andersson, R., Hoof, I., Schein, A., Andersen, P.R., et al. (2013). Polyadenylation site-induced decay of upstream transcripts enforces promoter directionality. Nat. Struct. Mol. Biol. 20, 923-928.   DOI   ScienceOn
21 Ohnacker, M., Barabino, S.M., Preker, P.J., and Keller, W. (2000). The WD-repeat protein pfs2p bridges two essential factors within the yeast pre-mRNA 3'-end-processing complex. EMBO J. 19, 37-47.   DOI   ScienceOn
22 Pashkova, N., Gakhar, L., Winistorfer, S.C., Yu, L., Ramaswamy, S., and Piper, R.C. (2010). WD40 repeat propellers define a ubiquitin-binding domain that regulates turnover of F box proteins. Mol. Cell 40, 433-443.   DOI   ScienceOn
23 Penheiter, K.L., Washburn, T.M., Porter, S.E., Hoffman, M.G., and Jaehning, J.A. (2005). A posttranscriptional role for the yeast Paf1-RNA polymerase II complex is revealed by identification of primary targets. Mol. Cell 20, 213-223.   DOI   ScienceOn
24 Proudfoot, N.J. (2011). Ending the message: poly(A) signals then and now. Genes Dev. 25, 1770-1782.   DOI   ScienceOn
25 Rozenblatt-Rosen, O., Nagaike, T., Francis, J.M., Kaneko, S., Glatt, K.A., Hughes, C.M., LaFramboise, T., Manley, J.L., and Meyerson, M. (2009). The tumor suppressor Cdc73 functionally associates with CPSF and CstF 3'mRNA processing factors. Proc. Natl. Acad. Sci. USA 106, 755-760.   DOI   ScienceOn
26 Ryan, K., and Bauer, D.L. (2008). Finishing touches: posttranslational modification of protein factors involved in mammalian pre-mRNA 3' end formation. Int. J. Biochem. Cell Biol. 40, 2384-2396.   DOI   ScienceOn
27 Li, W., Yeh, H.J., Shankarling, G.S., Ji, Z., Tian, B., and MacDonald, C.C. (2012). The tauCstF-64 polyadenylation protein controls genome expression in testis. PLoS One 7, e48373.   DOI   ScienceOn
28 Kleiman, F.E., and Manley, J.L. (1999). Functional interaction of BRCA1-associated BARD1 with polyadenylation factor CstF-50. Science 285, 1576-1579.   DOI   ScienceOn
29 Kleiman, F.E., and Manley, J.L. (2001). The BARD1-CstF-50 interaction links mRNA 3' end formation to DNA damage and tumor suppression. Cell 104, 743-753.   DOI   ScienceOn
30 Krishnakumar, R., and Kraus, W.L. (2010). The PARP side of the nucleus: molecular actions, physiological outcomes, and clinical targets. Mol. Cell 39, 8-24.   DOI   ScienceOn
31 Lubas, M., Christensen, M.S., Kristiansen, M.S., Domanski, M., Falkenby, L.G., Lykke-Andersen, S., Andersen, J.S., Dziembowski, A., and Jensen, T.H. (2011). Interaction profiling identifies the human nuclear exosome targeting complex. Mol. Cell 43, 624-637.
32 Mandel, C.R., Bai, Y., and Tong, L. (2008). Protein factors in premRNA 3'-end processing. Cell. Mol. Life Sci. 65, 1099-1122.   DOI   ScienceOn
33 Mayr, C., and Bartel, D.P. (2009). Widespread shortening of 3'UTRs by alternative cleavage and polyadenylation activates oncogenes in cancer cells. Cell 138, 673-684.   DOI   ScienceOn
34 Mbita, Z., Meyer, M., Skepu, A., Hosie, M., Rees, J., and Dlamini, Z. (2012). De-regulation of the RBBP6 isoform 3/DWNN in human cancers. Mol. Cell. Biochem. 362, 249-262.   DOI   ScienceOn
35 Meinhart, A., and Cramer, P. (2004). Recognition of RNA polymerase II carboxy-terminal domain by 3'-RNA-processing factors. Nature 430, 223-226.   DOI   ScienceOn
36 Hu, J., Lutz, C.S., Wilusz, J., and Tian, B. (2005). Bioinformatic identification of candidate cis-regulatory elements involved in human mRNA polyadenylation. RNA 11, 1485-1493.   DOI   ScienceOn
37 Mueller, C.L., Porter, S.E., Hoffman, M.G., and Jaehning, J.A. (2004). The Paf1 complex has functions independent of actively transcribing RNA polymerase II. Mol. Cell 14, 447-456.   DOI   ScienceOn
38 Gozani, O., Feld, R., and Reed, R. (1996). Evidence that sequenceindependent binding of highly conserved U2 snRNP proteins upstream of the branch site is required for assembly of spliceosomal complex A. Genes Dev. 10, 233-243.   DOI   ScienceOn
39 He, X., and Moore, C. (2005). Regulation of yeast mRNA 3' end processing by phosphorylation. Mol. Cell 19, 619-629.   DOI   ScienceOn
40 Ji, Z., and 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.   DOI   ScienceOn
41 Ji, Y., and Tulin, A.V. (2010). The roles of PARP1 in gene control and cell differentiation. Curr. Opin. Genet. Dev. 20, 512-518.   DOI   ScienceOn
42 Ji, Z., Lee, J.Y., Pan, Z., Jiang, B., and Tian, B. (2009). Progressive lengthening of 3' untranslated regions of mRNAs by alternative polyadenylation during mouse embryonic development. Proc. Natl. Acad. Sci. USA 106, 7028-7033.   DOI   ScienceOn
43 Jungmichel, S., Rosenthal, F., Altmeyer, M., Lukas, J., Hottiger, M.O., and Nielsen, M.L. (2013). Proteome-wide identification of poly(ADP-Ribosyl)ation targets in different genotoxic stress responses. Mol. Cell 52, 272-285.   DOI   ScienceOn
44 Baillat, D., Hakimi, M.A., Naar, A.M., Shilatifard, A., Cooch, N., and Shiekhattar, R. (2005). Integrator, a multiprotein mediator of small nuclear RNA processing, associates with the C-terminal repeat of RNA polymerase II. Cell 123, 265-276.   DOI   ScienceOn
45 Kapp, L.D., Abrams, E.W., Marlow, F.L., and Mullins, M.C. (2013). The integrator complex subunit 6 (Ints6) confines the dorsal organizer in vertebrate embryogenesis. PLoS Genet. 9, e1003822.   DOI   ScienceOn
46 Kim, Y.M., Watanabe, T., Allen, P.B., Kim, Y.M., Lee, S.J., Greengard, P., Nairn, A.C., and Kwon, Y.G. (2003). PNUTS, a protein phosphatase 1 (PP1) nuclear targeting subunit. Characterization of its PP1- and RNA-binding domains and regulation by phosphorylation. J. Biol. Chem. 278, 13819-13828   DOI   ScienceOn
47 Awasthi, S., and Alwine, J.C. (2003). Association of polyadenylation cleavage factor I with U1 snRNP. RNA 9, 1400-1409.   DOI
48 Berglund, J.A., Chua, K., Abovich, N., Reed, R., and Rosbash, M. (1997). The splicing factor BBP interacts specifically with the premRNA branchpoint sequence UACUAAC. Cell 89, 781-787.   DOI   ScienceOn
49 Cevher, M.A., Zhang, X., Fernandez, S., Kim, S., Baquero, J., Nilsson, P., Lee, S., Virtanen, A., and Kleiman, F.E. (2010). Nuclear deadenylation/polyadenylation factors regulate 3' processing in response to DNA damage. EMBO J. 29, 1674-1687.   DOI   ScienceOn
50 Colgan, D.F., Murthy, K.G., Prives, C., and Manley, J.L. (1996). Cellcycle related regulation of poly(A) polymerase by phosphorylation. Nature 384, 282-285.   DOI   ScienceOn
51 Collis, S.J., DeWeese, T.L., Jeggo, P.A., and Parker, A.R. (2005). The life and death of DNA-PK. Oncogene 24, 949-961.   DOI   ScienceOn
52 Gilbert, W., and Guthrie, C. (2004). The Glc7p nuclear phosphatase promotes mRNA export by facilitating association of Mex67p with mRNA. Mol. Cell 13, 201-212.   DOI   ScienceOn
53 Davidson, D., Amrein, L., Panasci, L., and Aloyz, R. (2013). Small molecules, inhibitors of DNA-PK, targeting DNA repair, and beyond. Front. Pharmacol. 4, 5.
54 Di Giammartino, D.C., Nishida, K., and Manley, J.L. (2011). Mechanisms and consequences of alternative polyadenylation. Mol. Cell 43, 853-866.   DOI   ScienceOn
55 Elkon, R., Ugalde, A.P., and Agami, R. (2013). Alternative cleavage and polyadenylation: extent, regulation and function. Nat. Rev. Genet. 14, 496-506.   DOI   ScienceOn
56 Zhang, F., Ma, T., and Yu, X. (2013). A core hSSB1-INTS complex participates in the DNA damage response. J. Cell Sci. 126, 4850-4855.   DOI   ScienceOn
57 Almada, A.E., Wu, X., Kriz, A.J., Burge, C.B., and Sharp, P.A. (2013). Promoter directionality is controlled by U1 snRNP and polyadenylation signals. Nature 499, 360-363.   DOI   ScienceOn
58 Ariumi, Y., Masutani, M., Copeland, T.D., Mimori, T., Sugimura, T., Shimotohno, K., Ueda, K., Hatanaka, M., and Noda, M. (1999). Suppression of the poly(ADP-ribose) polymerase activity by DNA-dependent protein kinase in vitro. Oncogene 18, 4616-4625.   DOI
59 Yao, C., Biesinger, J., Wan, J., Weng, L., Xing, Y., Xie, X., and Shi, Y. (2012). Transcriptome-wide analyses of CstF64-RNA interactions in global regulation of mRNA alternative polyadenylation. Proc. Natl. Acad. Sci. USA 109, 18773-18778.   DOI
60 Yao, C., Choi, E.A., Weng, L., Xie, X., Wan, J., Xing, Y., Moresco, J.J., Tu, P.G., Yates, J.R., 3rd, and Shi, Y. (2013). Overlapping and distinct functions of CstF64 and CstF64tau in mammalian mRNA 3' processing. RNA 19, 1781-1790.   DOI   ScienceOn
61 Di Giammartino, D.C., Shi, Y., and Manley, J.L. (2013). PARP1 represses PAP and inhibits polyadenylation during heat shock. Mol. Cell 49, 7-17.   DOI   ScienceOn
62 Weitzer, S., and Martinez, J. (2007). The human RNA kinase hClp1 is active on 3' transfer RNA exons and short interfering RNAs. Nature 447, 222-226.   DOI   ScienceOn
63 Stuparevic, I., Mosrin-Huaman, C., Hervouet-Coste, N., Remenaric, M., and Rahmouni, A.R. (2013). Cotranscriptional recruitment of RNA exosome cofactors Rrp47p and Mpp6p and two distinct Trf-Air-Mtr4 polyadenylation (TRAMP) complexes assists the exonuclease Rrp6p in the targeting and degradation of an aberrant messenger ribonucleoprotein particle (mRNP) in yeast. J. Biol. Chem. 288, 31816-31829.   DOI   ScienceOn
64 Nazeer, F.I., Devany, E., Mohammed, S., Fonseca, D., Akukwe, B., Taveras, C., and Kleiman, F.E. (2011). p53 inhibits mRNA 3' processing through its interaction with the CstF/BARD1 complex. Oncogene 30, 3073-3083.   DOI   ScienceOn
65 Lackford, B., Yao, C., Charles, G.M., Weng, L., Zheng, X., Choi, E.A., Xie, X., Wan, J., Xing, Y., Freudenberg, J.M., et al. (2014). Fip1 regulates mRNA alternative polyadenylation to promote stem cell self-renewal. EMBO J. 33, 878-889.   DOI   ScienceOn
66 Gunderson, S.I., Polycarpou-Schwarz, M., and Mattaj, I.W. (1998). U1 snRNP inhibits pre-mRNA polyadenylation through a direct interaction between U1 70K and poly(A) polymerase. Mol. Cell 1, 255-264.   DOI   ScienceOn
67 Reinhardt, H.C., and Yaffe, M.B. (2013). Phospho-Ser/Thr-binding domains: navigating the cell cycle and DNA damage response. Nat. Rev. Mol. Cell Biol. 14, 563-580.   DOI   ScienceOn