Alternative polyadenylation: Another foe in cancer

Molecular Cancer Research

Volumn 14, Issue 6, 2016, Pages 507-517

  Erson Bensan, Ayse Elif ^a   Can, Tolga ^a  

^a MIDDLE EAST TECHNICAL UNIVERSITY   (Turkey)

Author keywords

[No Author keywords available]

Indexed keywords

CLEAVAGE AND POLYADENYLATION SPECIFICITY FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; ESTROGEN RECEPTOR; MESSENGER RNA; MICRORNA; POLYADENYLIC ACID; PROTEIN TYROSINE KINASE; RNA ISOFORM; SIGNAL PEPTIDE; TRANSCRIPTOME; ISOPROTEIN;

3' UNTRANSLATED REGION; BREAST CANCER; CANCER CELL; CANCER PROGNOSIS; CANCER RESEARCH; CELLULAR DISTRIBUTION; DISEASE COURSE; GENE CONTROL; GENE EXPRESSION REGULATION; GENE MUTATION; HUMAN; MOLECULAR INTERACTION; NONHUMAN; POLYADENYLATION; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTO ONCOGENE; REVIEW; RNA SEQUENCE; ANIMAL; GENETICS; METABOLISM; NEOPLASM;

ANIMALS; GENE EXPRESSION REGULATION; HUMANS; NEOPLASMS; POLYADENYLATION; PROTEIN ISOFORMS;

EID: 84975091249     PISSN: 15417786     EISSN: 15573125     Source Type: Journal    
DOI: 10.1158/1541-7786.MCR-15-0489     Document Type: Review

References (102)

1. Marzluff WF, Wagner EJ, Duronio RJ. Metabolism and regulation of canonical histone mRNAs: life without a poly(A) tail. Nat Rev Genet 2008;9:843-54.
2. Proudfoot N. Poly(A) signals. Cell 1991;64:671-4.
3. Colgan DF,Manley JL. Mechanism and regulation of mRNA polyadenylation. Genes Dev 1997;11:2755-66.
4. Derti A, Garrett-Engele P, Macisaac KD, Stevens RC, SriramS, Chen R, et al. A quantitative atlas of polyadenylation in five mammals. Genome Res 2012;22:1173-83.
5. Millevoi S, Vagner S. Molecular mechanisms of eukaryotic pre-mRNA 30 end processing regulation. Nucleic Acids Res 2010;38:2757-74.
6. Tian B, Graber JH. Signals for pre-mRNA cleavage and polyadenylation. Wiley Interdiscip Rev RNA 2012;3:385-96.
7. Zarudnaya MI, Kolomiets IM, Potyahaylo AL, Hovorun DM. Downstream elements of mammalian pre-mRNA polyadenylation signals: primary, secondary and higher-order structures. Nucleic Acids Res 2003;31:1375-86.
8. Kuhn RM, Karolchik D, Zweig AS, Wang T, Smith KE, Rosenbloom KR, et al. The UCSC Genome Browser Database: update 2009. Nucleic Acids Res 2009;37:D755-61.
9. Kaufmann I, Martin G, Friedlein A, Langen H, Keller W. Human Fip1 is a subunit of CPSF that binds to U-rich RNA elements and stimulates poly (A) polymerase. EMBO J 2004;23:616-26.
10. Mandel CR, Bai Y, Tong L. Protein factors in pre-mRNA 30-end processing. Cell Mol Life Sci 2008;65:1099-122.
11. Chan SL, Huppertz I, Yao C, Weng L, Moresco JJ, Yates JR, et al. CPSF30 and Wdr33 directly bind to AAUAAA inmammalianmRNA30 processing. Genes Dev 2014;28:2370-80.
12. Schönemann L, Kühn U, Martin G, Schäfer P, Gruber AR, Keller W, et al. Reconstitution of CPSF active in polyadenylation: recognition of the polyadenylation signal by WDR33. Genes Dev 2014;28:2381-93.
13. Mandel CR, Kaneko S, Zhang H, Gebauer D, Vethantham V, Manley JL, et al. Polyadenylation factor CPSF-73 is the pre-mRNA 30-end-processing endonuclease. Nature 2006;444:953-6.
14. Dantonel JC, Murthy KG, Manley JL, Tora L. Transcription factor TFIID recruits factor CPSF for formation of 30 end of mRNA. Nature 1997;389: 399-402.
15. Nag A, Narsinh K, Martinson HG. The poly(A)-dependent transcriptional pause is mediated by CPSF acting on the body of the polymerase. Nat Struct Mol Biol 2007;14:662-9.
16. Glover-Cutter K, Kim S, Espinosa J, Bentley DL. RNA polymerase II pauses and associates with pre-mRNA processing factors at both ends of genes. Nat Struct Mol Biol 2008;15:71-8.
17. Kwon C, Tak H, Rho M, Chang HR, Kim YH, Kim KT, et al. Detection of PIWI and piRNAs in the mitochondria of mammalian cancer cells. Biochem Biophys Res Commun 2014;446:218-23.
18. 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;14:6647-54.
19. 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;10:6397-407.
20. Takagaki Y, Manley JL. Complex protein interactions within the human polyadenylation machinery identify a novel component. Mol Cell Biol 2000;20:1515-25.
21. Yao Y, Song L, Katz Y, Galili G. Cloning and characterization of Arabidopsis homologues of the animal CstF complex that regulates 30 mRNA cleavage and polyadenylation. J Exp Bot 2002;53:2277-8.
22. CevherMA, Kleiman FE. Connections between 30-end processing and DNA damage response. Wiley Interdiscip Rev RNA 2010;1:193-9.
23. Brown KM, Gilmartin GM. A mechanism for the regulation of premRNA 30 processing by human cleavage factor Im. Mol Cell 2003;12: 1467-76.
24. Venkataraman K, Brown KM, Gilmartin GM. Analysis of a noncanonical poly(A) site reveals a tripartite mechanism for vertebrate poly(A) site recognition. Genes Dev 2005;19:1315-27.
25. Coseno M, Martin G, Berger C, Gilmartin G, Keller W, Doublie S. Crystal structure of the 25 kDa subunit of human cleavage factor Im. Nucleic Acids Res 2008;36:3474-83.
26. Yang Q, Gilmartin GM, Doublie S. Structural basis of UGUA recognition by the Nudix protein CFI(m)25 and implications for a regulatory role in mRNA 30 processing. Proc Natl Acad Sci U S A 2010;107: 10062-7.
27. Li H, Tong S, Li X, Shi H, Ying Z, Gao Y, et al. Structural basis of pre-mRNA recognition by the human cleavage factor Im complex. Cell Res 2011; 21:1039-51.
28. Yang Q, Doublie S. Structural biology of poly(A) site definition. Wiley Interdiscip Rev RNA 2011;2:732-47.
29. Birse CE, Minvielle-Sebastia L, Lee BA, Keller W, Proudfoot NJ. Coupling termination of transcription to messenger RNA maturation in yeast. Science 1998;280:298-301.
30. Proudfoot NJ. Ending the message: poly(A) signals then and now. Genes Dev 2011;25:1770-82.
31. Scorilas A. Polyadenylate polymerase (PAP) and 30 end pre-mRNA processing: function, assays, and association with disease. Crit Rev Clin Lab Sci 2002;39:193-224.
32. Eckmann CR, Rammelt C, Wahle E. Control of poly(A) tail length. Wiley Interdiscip Rev RNA 2011;2:348-61.
33. Lutz CS, Moreira A. Alternative mRNA polyadenylation in eukaryotes: an effective regulator of gene expression. Wiley Interdiscip Rev RNA 2011; 2:23-31.
34. Subtelny AO, Eichhorn SW, Chen GR, Sive H, Bartel DP. Poly(A)-tail profiling reveals an embryonic switch in translational control. Nature 2014;508:66-71.
35. Wang L, Eckmann CR, Kadyk LC, Wickens M, Kimble J. A regulatory cytoplasmic poly(A) polymerase in Caenorhabditis elegans. Nature 2002;419:312-6.
36. Saitoh S, Chabes A,McDonaldWH,Thelander L, Yates JR, Russell P. Cid13 is a cytoplasmic poly(A) polymerase that regulates ribonucleotide reductase mRNA. Cell 2002;109:563-73.
37. Rouhana L, Wang L, Buter N, Kwak JE, Schiltz CA, Gonzalez T, et al. Vertebrate GLD2 poly(A) polymerases in the germline and the brain. RNA 2005;11:1117-30.
38. Charlesworth A, Meijer HA, deMoor CH. Specificity factors in cytoplasmic polyadenylation. Wiley Interdiscip Rev RNA 2013;4:437-61.
39. Bava FA, Eliscovich C, Ferreira PG, Minana B, Ben-Dov C, Guigo R, et al. CPEB1 coordinates alternative 30-UTR formation with translational regulation. Nature 2013;495:121-5.
40. Batra R, Charizanis K, Manchanda M, Mohan A, LiM, FinnDJ, et al. Loss of MBNL leads to disruption of developmentally regulated alternative polyadenylation in RNA-mediated disease. Mol Cell 2014;56:311-22.
41. Hilgers V, Lemke SB, Levine M. ELAV mediates 30 UTR extension in the Drosophila nervous system. Genes Dev 2012;26:2259-64.
42. Dai W, Zhang G, Makeyev EV. RNA-binding protein HuR autoregulates its expression by promoting alternative polyadenylation site usage. Nucleic Acids Res 2012;40:787-800.
43. Zhu H, Zhou HL, Hasman RA, Lou H. Hu proteins regulate polyadenylation by blocking sites containing U-rich sequences. J Biol Chem 2007; 282:2203-10.
44. Licatalosi DD, Mele A, Fak JJ, Ule J, Kayikci M, Chi SW, et al. HITS-CLIP yields genome-wide insights into brain alternative RNA processing. Nature 2008;456:464-9.
45. Hu W, Liu Y, Yan J. Microarray meta-Analysis of RNA-binding protein functions in alternative polyadenylation. PLoS One 2014;9:e90774.
46. Akman HB, Erson-Bensan AE. Alternative polyadenylation and its impact on cellular processes. Microrna 2014;3:2-9.
47. Tian B, Hu J, Zhang H, Lutz CS. A large-scale analysis of mRNA polyadenylation of human and mouse genes. Nucleic Acids Res 2005; 33:201-12.
48. Ni T, Yang Y, Hafez D, Yang W, Kiesewetter K, Wakabayashi Y, et al. Distinct polyadenylation landscapes of diverse human tissues revealed by a modified PA-seq strategy. BMC Genomics 2013;14:615.
49. Zhang H, Lee JY, Tian B. Biased alternative polyadenylation in human tissues. Genome Biol 2005;6:R100.
50. Sandberg R, Neilson JR, Sarma A, Sharp PA, Burge CB. Proliferating cells express mRNAs with shortened 30 untranslated regions and fewer micro-RNA target sites. Science 2008;320:1643-7.
51. Ji Z, Lee JY, Pan Z, Jiang B, Tian B. Progressive lengthening of 30 untranslated regions of mRNAs by alternative polyadenylation during mouse embryonic development. Proc Natl Acad Sci U S A 2009;106: 7028-33.
52. Kleppe L, Edvardsen RB, Kuhl H, Malde K, Furmanek T, Drivenes O, et al. Maternal 30UTRs: from egg to onset of zygotic transcription in Atlantic cod. BMC Genomics 2012;13:443.
53. Velten L, Anders S, Pekowska A, Järvelin AI, Huber W, Pelechano V, et al. Single-cell polyadenylation site mapping reveals 30 isoform choice variability. Mol Syst Biol 2015;11:812.
54. Lackford B, Yao C, Charles GM, Weng L, Zheng X, Choi EA, et al. Fip1 regulates mRNA alternative polyadenylation to promote stem cell selfrenewal. EMBO J 2014;33:878-89.
55. Hoque M, Ji Z, Zheng D, Luo W, Li W, You B, et al. Analysis of alternative cleavage and polyadenylation by 30 region extraction and deep sequencing. Nat Methods 2013;10:133-9.
56. Zhang S, Han J, Zhong D, Liu R, Zheng J. Genome-wide identification and predictive modeling of lincRNAs polyadenylation in cancer genome. Comput Biol Chem 2014;52:1-8.
57. Prasanth KV, Prasanth SG, Xuan Z, Hearn S, Freier SM, Bennett CF, et al. Regulating gene expression through RNA nuclear retention. Cell 2005; 123:249-63.
58. Naganuma T, Nakagawa S, Tanigawa A, Sasaki YF, Goshima N, Hirose T. Alternative 30-end processing of long noncoding RNA initiates construction of nuclear paraspeckles. EMBO J 2012;31:4020-34.
59. Yao CG, Biesinger J,Wan J, Weng LJ, Xing Y, Xie XH, et al. Transcriptomewide analyses of CstF64-RNA interactions in global regulation of mRNA alternative polyadenylation. Proc Natl Acad Sci U S A 2012;109:18773.
60. Youngblood BA, Grozdanov PN, MacDonald CC. CstF-64 supports pluripotency and regulates cell cycle progression in embryonic stem cells through histone 30 end processing. Nucleic Acids Res 2014;42: 8330-42.
61. Akman BH, Can T, Erson-Bensan AE. Estrogen-induced upregulation and 30-UTR shortening of CDC6. Nucleic Acids Res 2012;40:10679-88.
62. Akman HB, Oyken M, Tuncer T, Can T, Erson-Bensan AE. 30UTR shortening and EGF signaling: implications for breast cancer. Hum Mol Genet 2015;24:6910-20.
63. Elkon R, Drost J, van Haaften G, Jenal M, Schrier M, Oude Vrielink JA, et al. E2F mediates enhanced alternative polyadenylation in proliferation. Genome Biol 2012;13:R59.
64. Gruber AR, Martin G, Keller W, Zavolan M. Cleavage factor Im is a key regulator of 30 UTR length. RNA Biol 2012;9:1405-12.
65. Martin G, Gruber AR, Keller W, Zavolan M. Genome-wide analysis of premRNA 30 end processing reveals a decisive role of human cleavage factor I in the regulation of 30 UTR length. Cell Rep 2012;1:753-63.
66. Masamha CP, Xia Z, Yang J, Albrecht TR, Li M, Shyu AB, et al. CFIm25 links alternative polyadenylation to glioblastoma tumour suppression. Nature 2014;510:412-6.
67. Zhu ZH, Yu YP, Shi YK, Nelson JB, Luo JH. CSR1 induces cell death through inactivation of CPSF3. Oncogene 2009;28:41-51.
68. Proudfoot NJ, Furger A, Dye MJ. Integrating mRNA processing with transcription. Cell 2002;108:501-12.
69. Elkon R, Ugalde AP, Agami R. Alternative cleavage and polyadenylation: extent, regulation and function. Nat Rev Genet 2013;14:496-506.
70. Oktaba K, Zhang W, Lotz TS, Jun DJ, Lemke SB, Ng SP, et al. ELAV links paused Pol II to alternative polyadenylation in the Drosophila nervous system. Mol Cell 2015;57:341-8.
71. Mansfield KD, Keene JD. Neuron-specific ELAV/Hu proteins suppress HuR mRNA during neuronal differentiation by alternative polyadenylation. Nucleic Acids Res 2012;40:2734-46.
72. Spraggon L, Cartegni L. U1 snRNP-dependent suppression of polyadenylation: physiological role and therapeutic opportunities in cancer. Int J Cell Biol 2013;2013:846510.
73. Wang ET, Sandberg R, Luo S, Khrebtukova I, Zhang L, Mayr C, et al. Alternative isoform regulation in human tissue transcriptomes. Nature 2008;456:470-6.
74. Orkin SH, Cheng TC, Antonarakis SE, Kazazian HH. Thalassemia due to a mutation in the cleavage-polyadenylation signal of the human betaglobin gene. EMBO J 1985;4:453-6.
75. Stacey SN, Sulem P, Jonasdottir A, Masson G, Gudmundsson J, Gudbjartsson DF, et al. A germline variant in the TP53 polyadenylation signal confers cancer susceptibility. Nat Genet 2011;43:1098-103.
76. Diskin SJ, Capasso M, Diamond M, Oldridge DA, Conkrite K, Bosse KR, et al. Rare variants in TP53 and susceptibility to neuroblastoma. J Natl Cancer Inst 2014;106:dju047.
77. Thomas LF, Saetrom P. Single nucleotide polymorphisms can create alternative polyadenylation signals and affect gene expression through loss of microRNA-regulation. PLoS Comput Biol 2012;8: e1002621.
78. Huang H, Liu H, Sun X. Nucleosome distribution near the 30 ends of genes in the human genome. Biosci Biotechnol Biochem 2013;77: 2051-5.
79. Lemmon MA, Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell 2010;141:1117-34.
80. Vorlova S, Rocco G, Lefave CV, Jodelka FM, Hess K, Hastings ML, et al. Induction of antagonistic soluble decoy receptor tyrosine kinases by intronic polyA activation. Mol Cell 2011;43:927-39.
81. Rosenwald A, Wright G, Wiestner A, Chan WC, Connors JM, Campo E, et al. The proliferation gene expression signature is a quantitative integrator of oncogenic events that predicts survival in mantle cell lymphoma. Cancer Cell 2003;3:185-97.
82. Mayr C, Bartel DP. Widespread shortening of 30UTRs by alternative cleavage and polyadenylation activates oncogenes in cancer cells. Cell 2009;138:673-84.
83. Gruber AR,Martin G, Müller P, Schmidt A, Gruber AJ, Gumienny R, et al. Global 30 UTR shortening has a limited effect on protein abundance in proliferating T cells. Nat Commun 2014;5:5465.
84. Mingle LA, Okuhama NN, Shi J, Singer RH, Condeelis J, Liu G. Localization of all seven messenger RNAs for the actin-polymerization nucleator Arp2/3 complex in the protrusions of fibroblasts. J Cell Sci 2005;118: 2425-33.
85. Lau AG, Irier HA, Gu J, Tian D, Ku L, Liu G, et al. Distinct 30UTRs differentially regulate activity-dependent translation of brain-derived neurotrophic factor (BDNF). Proc Natl Acad Sci U S A 2010;107: 15945-50.
86. Berkovits BD, Mayr C. Alternative 30 UTRs act as scaffolds to regulate membrane protein localization. Nature 2015;522:363-7.
87. Meola G, Cardani R.Myotonic dystrophies: An update on clinical aspects, genetic, pathology, and molecular pathomechanisms. Biochim Biophys Acta 2015;1852:594-606.
88. Creemers EE, Bawazeer A, Ugalde AP, van Deutekom HW, van der Made I, de Groot NE, et al. Genome-wide polyadenylation maps reveal dynamic mRNA 30-end formation in the failing human heart. Circ Res 2016; 118:433-8.
89. Singh P, Alley TL, Wright SM, Kamdar S, Schott W, Wilpan RY, et al. Global changes in processing of mRNA 30 untranslated regions characterize clinically distinct cancer subtypes. Cancer Res 2009;69:9422-30.
90. Fu Y, Sun Y, Li Y, Li J, Rao X, Chen C, et al. Differential genome-wide profiling of tandem 30 UTRs among human breast cancer and normal cells by high-throughput sequencing. Genome Res 2011;21:741-7.
91. Xia Z, Donehower LA, Cooper TA, Neilson JR, Wheeler DA, Wagner EJ, et al. Dynamic analyses of alternative polyadenylation from RNA-seq reveal a 30-UTR landscape across seven tumour types. Nat Commun 2014;5:5274.
92. Morris AR, Bos A, Diosdado B, Rooijers K, Elkon R, Bolijn AS, et al. Alternative cleavage and polyadenylation during colorectal cancer development. Clin Cancer Res 2012;18:5256-66.
93. Gautheret D, Poirot O, Lopez F, Audic S, Claverie JM. Alternate polyadenylation in human mRNAs: a large-scale analysis by EST clustering. Genome Res 1998;8:524-30.
94. Wang Z, Gerstein M, Snyder M. RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet 2009;10:57-63.
95. Sun Y, Fu Y, Li Y, Xu A. Genome-wide alternative polyadenylation in animals: insights from high-throughput technologies. J Mol Cell Biol 2012;4:352-61.
96. Shepard PJ, Choi EA, Lu J, Flanagan LA, Hertel KJ, Shi Y. Complex and dynamic landscape of RNA polyadenylation revealed by PAS-Seq. RNA 2011;17:761-72.
97. Jan CH, Friedman RC, Ruby JG, Bartel DP. Formation, regulation and evolution of Caenorhabditis elegans 30UTRs. Nature 2011;469:97-101.
98. Hafner M, Renwick N, Brown M, Mihailovic A, Holoch D, Lin C, et al. RNA-ligase-dependent biases in miRNA representation in deepsequenced small RNA cDNA libraries. RNA 2011;17:1697-712.
99. Nussbacher JK, Batra R, Lagier-Tourenne C, Yeo GW. RNA-binding proteins in neurodegeneration: Seq and you shall receive. Trends Neurosci 2015;38:226-36.
100. Le Pera L, Mazzapioda M, Tramontano A. 3USS: a web server for detecting alternative 30UTRs from RNA-seq experiments. Bioinformatics 2015;31: 1845-7.
101. Katz Y, Wang ET, Airoldi EM, Burge CB. Analysis and design of RNA sequencing experiments for identifying isoformregulation. NatMethods 2010;7:1009-15.
102. Lembo A, Di Cunto F, Provero P. Shortening of 30UTRs correlates with poor prognosis in breast and lung cancer. PLoS One 2012;7:e31129.