Poly(A)-specific ribonuclease (PARN): An allosterically regulated, processive and mRNA cap-interacting deadenylase

Critical Reviews in Biochemistry and Molecular Biology

Volumn 48, Issue 2, 2013, Pages 192-209

  Virtanen, Anders ^a   Henriksson, Niklas ^a,b   Nilsson, Per ^a,c,d   Nissbeck, Mikael ^a  

^a UPPSALA UNIVERSITY   (Sweden)

^b UPPSALA UNIVERSITY HOSPITAL   (Sweden)

^c RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

^d KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Deadenylase; MRNA degradation; MRNA poly(A) tail degradation; MRNA turnover; Ribonuclease

Indexed keywords

ADENINE; EXORIBONUCLEASE; HYDROLASE; INITIATION FACTOR 4E; INITIATION FACTOR 4F; INITIATION FACTOR 4G; MESSENGER RNA; POLY(A) RIBONUCLEASE; POLYADENYLATED RNA; POLYNUCLEOTIDE ADENYLYLTRANSFERASE; RIBOSE; UNCLASSIFIED DRUG;

ALLOSTERISM; AMINO ACID SEQUENCE; CELL FUNCTION; ENZYME SPECIFICITY; ENZYME SUBSTRATE; GENE CONTROL; GENETIC CONSERVATION; HUMAN; MAMMAL CELL; MOLECULAR WEIGHT; NUCLEAR LOCALIZATION SIGNAL; PRIORITY JOURNAL; PROTEIN HYDROLYSIS; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; REACTION ANALYSIS; REGULATORY MECHANISM; REVIEW; RIBOSOME; RIBOSOME SUBUNIT; RNA DEGRADATION; RNA INTERFERENCE;

ADENINE; ANIMALS; EVOLUTION, MOLECULAR; EXORIBONUCLEASES; HUMANS; MODELS, MOLECULAR; POLY A; PROTEIN CONFORMATION; RIBOSE; RNA CAPS; RNA, MESSENGER; SUBSTRATE SPECIFICITY;

EUKARYOTA;

EID: 84875618805     PISSN: 10409238     EISSN: 15497798     Source Type: Journal    
DOI: 10.3109/10409238.2013.771132     Document Type: Review

References (154)

1. Abraham AK, Jacob ST. (1978). Hydrolysis of poly(A) to adenine nucleotides by purified poly(A) polymerase. Proc Natl Acad Sci USA 75:2085-7
2. Amblar M, Barbas A, Fialho AM, Arraiano CM. (2006). Characterization of the functional domains of Escherichia coli RNase II. J Mol Biol 360:921-33
3. Amrani N, Ghosh S, Mangus DA, Jacobson A. (2008). Translation factors promote the formation of two states of the closed-loop mRNP. Nature 453:1276-80
4. Andersen KR, Jonstrup AT, Van LB, Brodersen DE. (2009). The activity and selectivity of fission yeast Pop2p are affected by a high affinity for Zn2 and Mn2in the active site. RNA 15:850-61
5. Astrom J, Astrom A, Virtanen A. (1991). In vitro deadenylation of mammalian mRNA by a HeLa cell 30 exonuclease. EMBO J 10:3067-71
6. Astrom J, Astrom A, Virtanen A. (1992). Properties of a HeLa cell 30 exonuclease specific for degrading poly(A) tails of mammalian mRNA. J Biol Chem 267:18154-9
7. Baker TA, Bell SP. (1998). Polymerases and the replisome: machines within machines. Cell 92:295-305
8. Balatsos NA, Maragozidis P, Anastasakis D, Stathopoulos C. (2012). Modulation of poly(A)-specific ribonuclease (PARN): current knowledge and perspectives. Curr Med Chem 19:4838-49
9. Balatsos NA, Nilsson P, Mazza C, et al. (2006). Inhibition of mRNA deadenylation by the nuclear cap binding complex (CBC). J Biol Chem 281:4517-22
10. Barnard EA, Stein WD. (1958). The roles of imidazole in biological systems. Adv Enzymol Relat Subj Biochem 20:51-110
11. Beese LS, Steitz TA. (1991). Structural basis for the 30-50 exonuclease activity of Escherichia coli DNA polymerase I: a two metal ion mechanism. Embo J 10:25-33
12. Behm-Ansmant I, Rehwinkel J, Doerks T, et al. (2006). mRNA degradation by miRNAs and GW182 requires both CCR4:NOT deadenylase and DCP1:DCP2 decapping complexes. Genes Dev 20:1885-98
13. Bernad A, Blanco L, Lazaro JM, et al. (1989). A conserved 30-50 exonuclease active site in prokaryotic and eukaryotic DNA polymerases. Cell 59:219-28
14. Berndt H, Harnisch C, Rammelt C, et al. (2012). Maturation of mammalian H/ACA box snoRNAs: PAPD5-dependent adenylation and PARN-dependent trimming. RNA 18:958-72
15. Bernstein P, Peltz SW, Ross J. (1989). The poly(A)-poly(A)-binding protein complex is a major determinant of mRNA stability in vitro. Mol Cell Biol 9:659-70
16. Bianchin C, Mauxion F, Sentis S, et al. (2005). Conservation of the deadenylase activity of proteins of the Caf1 family in human. RNA 11:487-94
17. Boeck R, Tarun S, Rieger M, et al. (1996). The yeast Pan2 protein is required for poly(A)-binding protein-stimulated poly(A)-nuclease activity. J Biol Chem 271:432-8
18. Brautigam CA, Steitz TA. (1998). Structural principles for the inhibition of the 30-50 exonuclease activity of Escherichia coli DNA polymerase I by phosphorothioates. J Mol Biol 277:363-77
19. Bregman A, Avraham-Kelbert M, Barkai O, et al. (2011). Promoter elements regulate cytoplasmic mRNA decay. Cell 147:1473-83
20. Brewer G, Ross J. (1988). Poly(A) shortening and degradation of the 30 AU-rich sequences of human c-myc mRNA in a cell-free system. Mol Cell Biol 8:1697-708
21. Brown CE, Tarun Jr SZ, Boeck R, Sachs AB. (1996). PAN3 encodes a subunit of the Pab1p-dependent poly(A) nuclease in Saccharomyces cerevisiae. Mol Cell Biol 16:5744-53
22. Buiting K, Korner C, Ulrich B, Wahle E, Horsthemke B. (1999). The human gene for the poly(A)-specific ribonuclease (PARN) maps to 16p13 and has a truncated copy in the Prader-Willi/ Angelman syndrome region on 15q11-4q13. Cytogenet Cell Genet 87:125-31
23. Calero G, Wilson KF, LY T, et al. (2002). Structural basis of m7GpppG binding to the nuclear cap-binding protein complex. Nat Struct Biol 9:912-7
24. Cannistraro VJ, Kennell D. (1994). The processive reaction mechanism of ribonuclease II. J Mol Biol 243:930-43
25. Cevher MA, Zhang X, Fernandez S, et al. (2010). Nuclear deadenylation/ polyadenylation factors regulate 30 processing in response to DNA damage. EMBO J 29:1674-87
26. Chen CY, Zheng D, Xia Z, Shyu AB. (2009). Ago-TNRC6 triggers microRNA-mediated decay by promoting two deadenylation steps. Nat Struct Mol Biol 16:1160-6
27. Chiba Y, Johnson MA, Lidder P, et al. (2004). AtPARN is an essential poly(A) ribonuclease in Arabidopsis. Gene 328:95-102
28. Chou CF, Mulky A, Maitra S, et al. (2006). Tethering KSRP, a decaypromoting AU-rich element-binding protein, to mRNAs elicits mRNA decay. Mol Cell Biol 26:3695-706
29. Copeland PR, Wormington M. (2001). The mechanism and regulation of deadenylation: identification and characterization of Xenopus PARN. RNA 7:875-86
30. Cui Q, Karplus M. (2008). Allostery and cooperativity revisited. Protein Sci 17:1295-307
31. Dasgupta T, Ladd AN. (2012). The importance of CELF control: molecular and biological roles of the CUG-BP, Elav-like family of RNA-binding proteins. Wiley Interdiscip Rev RNA 3:104-21
32. Dehlin E, Wormington M, Ko?rner CG, Wahle E. (2000). Cap-dependent deadenylation of mRNA. Embo J 19:1079-86
33. Eckmann CR, Rammelt C, Wahle E. (2011). Control of poly(A) tail length. Wiley Interdiscip Rev RNA 2:348-61
34. Ernoult-Lange M, Wilczynska A, Harper M, et al. (2009). Nucleocytoplasmic traffic of CPEB1 and accumulation in Crm1 nucleolar bodies. Mol Biol Cell 20:176-87
35. Eulalio A, Huntzinger E, Nishihara T, et al. (2009). Deadenylation is a widespread effect of miRNA regulation. RNA 15:21-32
36. Fabian MR, Mathonnet G, Sundermeier T, et al. (2009). Mammalian miRNA RISC recruits CAF1 and PABP to affect PABP-dependent deadenylation. Mol Cell 35:868-80
37. Flicek P, Amode MR, Barrell D, et al. (2012). Ensembl 2012. Nucleic Acids Res 40:D84-90
38. Ford LP, Watson J, Keene JD, Wilusz J. (1999). ELAV proteins stabilize deadenylated intermediates in a novel in vitro mRNA deadenylation/ degradation system. Genes Dev 13:188-201
39. Ford LP, Wilusz J. (1999). An in vitro system using HeLa cytoplasmic extracts that reproduces regulated mRNA stability. Methods 17:21-7
40. Frazao C, Mcvey CE, Amblar M, et al. (2006). Unravelling the dynamics of RNA degradation by ribonuclease II and its RNA-bound complex. Nature 443:110-14
41. Freemont PS, Friedman JM, Beese LS, et al. (1988). Cocrystal structure of an editing complex of Klenow fragment with DNA. Proc Natl Acad Sci USA 85:8924-8
42. Gao M, Fritz DT, Ford LP, Wilusz J. (2000). Interaction between a poly(A)-specific ribonuclease and the 50 cap influences mRNA deadenylation rates in vitro. Mol Cell 5:479-88
43. Garneau NL, Wilusz J, Wilusz CJ. (2007). The highways and byways of mRNA decay. Nat Rev Mol Cell Biol 8:113-26
44. Geer LY, Marchler-Bauer A, Geer RC, et al. (2010). The NCBI BioSystems database. Nucleic Acids Res 38:D492-6
45. Gherzi R, Lee KY, Briata P, et al. (2004). A KH domain RNA binding protein, KSRP, promotes ARE-directed mRNA turnover by recruiting the degradation machinery. Mol Cell 14:571-83
46. Goldstrohm AC, Wickens M. (2008). Multifunctional deadenylase complexes diversify mRNA control. Nat Rev Mol Cell Biol 9:337-44
47. Gruber AR, Fallmann J, Kratochvill F, et al. (2011). AREsite: a database for the comprehensive investigation of AU-rich elements. Nucleic Acids Res 39:D66-9
48. Guilligay D, Tarendeau F, Resa-Infante P, et al. (2008). The structural basis for cap binding by influenza virus polymerase subunit PB2. Nat Struct Mol Biol 15:500-6
49. Henriksson N, Nilsson P, Wu M, et al. (2010). Recognition of adenosine residues by the active site of poly(A)-specific ribonuclease. J Biol Chem 285:163-70
50. Hinnebusch AG, Lorsch Jr. (2012). The mechanism of eukaryotic translation initiation: new insights and challenges. Cold Spring Harb Perspect Biol 4:a011544
51. Hodel AE, Gershon PD, Quiocho FA. (1998). Structural basis for sequence-nonspecific recognition of 50-capped mRNA by a cap-modifying enzyme. Mol Cell 1:443-7
52. Hu G, Tsai AL, Quiocho FA. (2003). Insertion of an N7-methylguanine mRNA cap between two coplanar aromatic residues of a cap-binding protein is fast and selective for a positively charged cap. J Biol Chem 278:51515-20
53. Izaurralde E, Lewis J, Mcguigan C, et al. (1994). A nuclear cap binding protein complex involved in pre-mRNA splicing. Cell 78:657-68
54. Januszyk K, Liu Q, Lima CD. (2011). Activities of human RRP6 and structure of the human RRP6 catalytic domain. RNA 17:1566-77
55. Jonstrup AT, Andersen KR, Van LB, Brodersen DE. (2007). The 1. 4-A crystal structure of the S. pombe Pop2p deadenylase subunit unveils the configuration of an active enzyme. Nucleic Acids Res 35:3153-64
56. Kim JH, Richter JD. (2006). Opposing polymerase-deadenylase activities regulate cytoplasmic polyadenylation. Mol Cell 24:173-83
57. Kim JH, Richter JD. (2007). RINGO/cdk1 and CPEB mediate poly(A) tail stabilization and translational regulation by ePAB. Genes Dev 21:2571-9
58. Kim EE, Wyckoff HW. (1991). Reaction mechanism of alkaline phosphatase based on crystal structures. Two-metal ion catalysis. J Mol Biol 218:449-64
59. Kiss T, Fayet-Lebaron E, Jady BE. (2010). Box H/ACA small ribonucleoproteins. Mol Cell 37:597-606
60. Kleiman FE, Manley JL. (1999). Functional interaction of BRCA1- associated BARD1 with polyadenylation factor CstF-50. Science 285:1576-9
61. Kleiman FE, Manley JL. (2001). The BARD1-CstF-50 interaction links mRNA 30 end formation to DNA damage and tumor suppression. Cell 104:743-53
62. Kleiman FE, Wu-Baer F, Fonseca D, et al. (2005). BRCA1/BARD1 inhibition of mRNA 30 processing involves targeted degradation of RNA polymerase II. Genes Dev 19:1227-37
63. Korner CG, Wahle E. (1997). Poly(A) tail shortening by a mammalian poly(A)-specific 30- exoribonuclease. J Biol Chem 272:10448-56
64. Korner CG, Wormington M, Muckenthaler M, et al. (1998). The deadenylating nuclease (DAN) is involved in poly(A) tail removal during the meiotic maturation of Xenopus oocytes. Embo J 17:5427-37
65. Kuhn U, Wahle E. (2004). Structure and function of poly(A) binding proteins. Biochim Biophys Acta 1678:67-84
66. Lai WS, Carballo E, Strum JR, et al. (1999). Evidence that tristetraprolin binds to AU-rich elements and promotes the deadenylation and destabilization of tumor necrosis factor alpha mRNA. Mol Cell Biol 19:4311-23
67. Lai WS, Carballo E, Thorn JM, et al. (2000). Interactions of CCCH zinc finger proteins with mRNA. Binding of tristetraprolin-related zinc finger proteins to Au-rich elements and destabilization of mRNA. J Biol Chem 275:17827-37
68. Lai WS, Kennington EA, Blackshear PJ. (2003). Tristetraprolin and its family members can promote the cell-free deadenylation of AU-rich element-containing mRNAs by poly(A) ribonuclease. Mol Cell Biol 23:3798-812
69. Lau NC, Kolkman A, Van Schaik FM, et al. (2009). Human Ccr4-Not complexes contain variable deadenylase subunits. Biochem J 422:443-53
70. Lazarus HM, Sporn MB. (1967). Purification and properties of a nuclear exoribonuclease from ehrlich ascites tumor cells. Proc Natl Acad Sci USA 57:1386-93
71. Lee JE, Lee JY, Trembly J, et al. (2012). The PARN deadenylase targets a discrete set of mRNAs for decay and regulates cell motility in mouse myoblasts. PLoS Genet 8:e1002901
72. Lee JE, Lee JY, Wilusz J, et al. (2010). Systematic analysis of ciselements in unstable mRNAs demonstrates that CUGBP1 is a key regulator of mRNA decay in muscle cells. PLoS One 5:e11201
73. Lejeune F, Li X, Maquat LE. (2003). Nonsense-mediated mRNA decay in mammalian cells involves decapping, deadenylating, and exonucleolytic activities. Mol Cell 12:675-87
74. Lin CL, Evans V, Shen S, et al. (2010). The nuclear experience of CPEB: implications for RNA processing and translational control. RNA 16:338-48
75. Liu WF, Zhang A, Cheng Y, et al. (2007). Effect of magnesium ions on the thermal stability of human poly(A)-specific ribonuclease. FEBS Lett 581:1047-52
76. Lykke-Andersen J, Wagner E. (2005). Recruitment and activation of mRNA decay enzymes by two ARE-mediated decay activation domains in the proteins TTP and BRF-1. Genes Dev 19:351-61
77. Mangus DA, Evans MC, Jacobson A. (2003). Poly(A)-binding proteins: multifunctional scaffolds for the post-transcriptional control of gene expression. Genome Biol 4:223.1-223.14
78. Maragozidis P, Karangeli M, Labrou M, et al. (2012). Alterations of deadenylase expression in acute leukemias: evidence for poly(a)- specific ribonuclease as a potential biomarker. Acta Haematol 128:39-46
79. Marchese FP, Aubareda A, Tudor C, et al. (2010). MAPKAP kinase 2 blocks tristetraprolin-directed mRNA decay by inhibiting CAF1 deadenylase recruitment. J Biol Chem 285:27590-600
80. Marchler-Bauer A, Lu S, Anderson JB, et al. (2011). CDD: a conserved domain database for the functional annotation of proteins. Nucleic Acids Res 39:D225-9
81. Marcotrigiano J, Gingras AC, Sonenberg N, Burley SK. (1997). Cocrystal structure of the messenger RNA 50 cap-binding protein (eIF4E) bound to 7-methyl-GDP. Cell 89:951-61
82. Martinez J, Ren YG, Nilsson P, et al. (2001). The mRNA cap structure stimulates rate of poly(A) removal and amplifies processivity of degradation. J Biol Chem 276:27923-9
83. Martinez J, Ren YG, Thuresson AC, et al. (2000). A 54-kDa fragment of the poly(A)-specific ribonuclease is an oligomeric, processive, and cap-interacting poly(A)-specific 30 exonuclease. J Biol Chem 275:24222-30
84. Matera, AG, Terns RM, Terns MP. (2007). Non-coding RNAs: lessons from the small nuclear and small nucleolar RNAs. Nat Rev Mol Cell Biol 8:209-20
85. Mazza C, Ohno M, Segref A, et al. (2001). Crystal structure of the human nuclear cap binding complex. Mol Cell 8:383-96
86. Mazza C, Segref A, Mattaj IW, Cusack S. (2002). Large-scale induced fit recognition of an m(7)GpppG cap analogue by the human nuclear capbinding complex. Embo J 21:5548-57
87. Meyer S, Temme C, Wahle E. (2004). Messenger RNA turnover in eukaryotes: pathways and enzymes. Crit Rev Biochem Mol Biol 39:197-216
88. Mian IS. (1997). Comparative sequence analysis of ribonucleases HII, III, II PH and D. Nucleic Acids Res 25:3187-95
89. Midtgaard SF, Assenholt J, Jonstrup AT, et al. (2006). Structure of the nuclear exosome component Rrp6p reveals an interplay between the active site and the HRDC domain. Proc Natl Acad Sci USA 103:11898-903
90. Minshall N, Reiter MH, Weil D, Standart N. (2007). CPEB interacts with an ovary-specific eIF4E and 4E-T in early Xenopus oocytes. J Biol Chem 282:37389-401
91. Mirkin N, Fonseca D, Mohammed S, et al. (2008). The 30 processing factor CstF functions in the DNA repair response. Nucleic Acids Res 36:1792-804
92. Monecke T, Schell S, Dickmanns A, Ficner R. (2008). Crystal structure of the RRM domain of poly(A)-specific ribonuclease reveals a novel m(7)G-cap-binding mode. J Mol Biol 382:827-34
93. Monod J, Changeux JP, Jacob F. (1963). Allosteric proteins and cellular control systems. J Mol Biol 6:306-29
94. Monod J, Jacob F. (1961). Teleonomic mechanisms in cellular metabolism, growth, and differentiation. Cold Spring Harb Symp Quant Biol 26:389-401
95. Moraes KC, Wilusz CJ, Wilusz J. (2006). CUG-BP binds to RNA substrates and recruits PARN deadenylase. RNA 12:1084-91
96. Moser MJ, Holley WR, Chatterjee A, Mian IS. (1997). The proofreading domain of Escherichia coli DNA polymerase I and other DNA and/or RNA exonuclease domains. Nucleic Acids Res 25:5110-18
97. Muller WEG, Arendes J, Zahn RK, Schro?der HC. (1978). Control of enzymic hydrolysis of polyadenylate segment of messenger RNA: role of polyadenylate-associated proteins. Eur J Biochem 86:283-90
98. Nagata T, Suzuki S, Endo R, et al. (2008). The RRM domain of poly(A)- specific ribonuclease has a noncanonical binding site for mRNA cap analog recognition. Nucleic Acids Res 36:4754-67
99. Nakamura T, Zhao Y, Yamagata Y, et al. (2012). Watching DNA polymerase eta make a phosphodiester bond. Nature 487:196-201
100. Niedzwiecka A, Lekka M, Nilsson P, Virtanen A. (2011). Global architecture of human poly(A)-specific ribonuclease by atomic force microscopy in liquid and dynamic light scattering. Biophys Chem 158:141-9
101. Niedzwiecka A, Marcotrigiano J, Stepinski J, et al. (2002). Biophysical studies of eIF4E cap-binding protein: recognition of mRNA 50 cap structure and synthetic fragments of eIF4G and 4E-BP1 proteins. J Mol Biol 319:615-35
102. Nilsson P, Henriksson N, Niedzwiecka A, et al. (2007). A multifunctional RNA recognition motif in poly(A)-specific ribonuclease with cap and poly(A) binding properties. J Biol Chem 282:32902-11
103. Nishimura N, Kitahata N, Seki M, et al. (2005). Analysis of ABA hypersensitive germination2 revealed the pivotal functions of PARN in stress response in Arabidopsis. Plant J 44:972-84
104. Nossal NG, Singer MF. (1968). The processive degradation of individual polyribonucleotide chains. I. Escherichia coli ribonuclease II. J Biol Chem 243:913-22
105. Opyrchal M, Anderson JR, Sokoloski KJ, et al. (2005). A cell-free mRNA stability assay reveals conservation of the enzymes and mechanisms of mRNA decay between mosquito and mammalian cell lines. Insect Biochem Mol Biol 35:1321-34
106. Ota R, Kotani T, Yamashita M. (2011). Biochemical characterization of Pumilio1 and Pumilio2 in Xenopus oocytes. J Biol Chem 286:2853-63
107. Parker R, Song H. (2004). The enzymes and control of eukaryotic mRNA turnover. Nat Struct Mol Biol 11:121-7
108. Pomerantz RT, O'donnell M. (2007). Replisome mechanics: insights into a twin DNA polymerase machine. Trends Microbiol 15:156-64
109. Quiocho FA, Hu G, Gershon PD. (2000). Structural basis of mRNA cap recognition by proteins [see comments]. Curr Opin Struct Biol 10:78-86
110. Reinhardt HC, Hasskamp P, Schmedding I, et al. (2010). DNA damage activates a spatially distinct late cytoplasmic cell-cycle checkpoint network controlled by MK2-mediated RNA stabilization. Mol Cell 40:34-49
111. Ren YG, Kirsebom LA, Virtanen A. (2004). Coordination of divalent metal ions in the active site of poly(A)-specific ribonuclease. J Biol Chem 279:48702-6
112. Ren YG, Martinez J, Kirsebom LA, Virtanen A. (2002a). Inhibition of Klenow DNA polymerase and poly(A)-specific ribonuclease by aminoglycosides. RNA 8:1393-400
113. Ren YG, Martinez J, Virtanen A. (2002b). Identification of the active site of poly(A)-specific ribonuclease by site-directed mutagenesis and Fe(2)-mediated cleavage. J Biol Chem 277:5982-7
114. Reverdatto SV, Dutko JA, Chekanova JA, et al. (2004). mRNA deadenylation by PARN is essential for embryogenesis in higher plants. RNA 10:1200-14
115. Richter JD. (2007). CPEB: a life in translation. Trends Biochem Sci 32:279-85
116. Richter JD, Lasko P. (2011). Translational control in oocyte development. Cold Spring Harb Perspect Biol 3:a002758
117. Ross J. (1995). mRNA stability in mammalian cells. Microbiol Rev 59:423-50
118. Rouget C, Papin C, Mandart E. (2006). Cytoplasmic CstF-77 protein belongs to a masking complex with cytoplasmic polyadenylation element-binding protein in Xenopus oocytes. J Biol Chem 281: 28687-98
119. Sachs AB, Varani G. (2000). Eukaryotic translation initiation: there are (at least) two sides to every story. Nat Struct Biol 7:356-61
120. Schoenberg DR, Maquat LE. (2012). Regulation of cytoplasmic mRNA decay. Nat Rev Genet 13:246-59
121. Schroder HC, Zahn RK, Dose K, Mu?ller WEG. (1980). Purification and characterization of a poly(A)-specific exoribonuclease from calf Thymus. J Biol Chem 255:4535-8
122. Seal R, Temperley R, Wilusz J, et al. (2005). Serum-deprivation stimulates cap-binding by PARN at the expense of eIF4E, consistent with the observed decrease in mRNA stability. Nucleic Acids Res 33:376-87
123. Shatkin AJ, Manley JL. (2000). The ends of the affair: capping and polyadenylation. Nat Struct Biol 7:838-42
124. Shaw G, Kamen R. (1986). A conserved AU sequence from the 30 untranslated region of GM-CSF mRNA mediates selective mRNA degradation. Cell 46:659-67
125. Siddiqui N, Mangus DA, Chang TC, et al. (2007). Poly(A) nuclease interacts with the C-terminal domain of polyadenylate-binding protein domain from poly(A)-binding protein. J Biol Chem 282:25067-75
126. Sonenberg N, Dever TE. (2003). Eukaryotic translation initiation factors and regulators. Curr Opin Struct Biol 13:56-63
127. Steitz TA, Steitz JA. (1993). A general two-metal-ion mechanism for catalytic RNA. Proc Natl Acad Sci USA 90:6498-502
128. Tarun Jr SZ, Sachs AB. (1996). Association of the yeast poly(A) tail binding protein with translation initiation factor eIF-4G. Embo J 15:7168-77
129. Temme C, Zaessinger S, Meyer S, et al. (2004). A complex containing the CCR4 and CAF1 proteins is involved in mRNA deadenylation in Drosophila. Embo J 23:2862-71
130. Tran H, Schilling M, Wirbelauer C, et al. (2004). Facilitation of mRNA deadenylation and decay by the exosome-bound, DExH protein RHAU. Mol Cell 13:101-11
131. Trcek T, Larson DR, Moldon A, et al. (2011). Single-molecule mRNA decay measurements reveal promoter- regulated mRNA stability in yeast. Cell 147:1484-97
132. Tucker M, Valencia-Sanchez MA, Staples RR, et al. (2001). The transcription factor associated Ccr4 and Caf1 proteins are components of the major cytoplasmic mRNA deadenylase in Saccharomyces cerevisiae. Cell 104:377-86
133. Uchida N, Hoshino S, Katada T. (2004). Identification of a human cytoplasmic poly(A) nuclease complex stimulated by poly(A)-binding protein. J Biol Chem 279:1383-91
134. Uhlen M, Oksvold P, Fagerberg L, et al. (2010). Towards a knowledgebased human protein atlas. Nat Biotechnol 28:1248-50
135. Varnum SM, Hurney CA, Wormington WM. (1992). Maturation-specific deadenylation in Xenopus oocytes requires nuclear and cytoplasmic factors. Dev Biol 153:283-90
136. Vlasova IA, Tahoe NM, Fan D, et al. (2008). Conserved GU-rich elements mediate mRNA decay by binding to CUG-binding protein 1. Mol Cell 29:263-70
137. Wagner E, Clement SL, Lykke-Andersen J. (2007). An unconventional human Ccr4-Caf1 deadenylase complex in nuclear cajal bodies. Mol Cell Biol 27:1686-95
138. Wells SE, Hillner PE, Vale RD, Sachs AB. (1998). Circularization of mRNA by eukaryotic translation initiation factors. Mol Cell 2:135-40
139. Wickens M. (1990). In the beginning is the end: regulation of poly(A) addition and removal during early development. Trends Biochem Sci 15:320-4
140. Wilusz CJ, Wormington M, Peltz SW. (2001). The cap-to-tail guide to mRNA turnover. Nat Rev Mol Cell Biol 2:237-46
141. Worch R, Niedzwiecka A, Stepinski J, et al. (2005). Specificity of recognition of mRNA 50 cap by human nuclear cap-binding complex. RNA 11:1355-63
142. Wormington M. (1993). Poly(A) and translation: development control. Curr Opin Cell Biol 5:950-4
143. Wormington M, Searfoss AM, Hurney CA. (1996). Overexpression of poly(A) binding protein prevents maturation-specific deadenylation and translational inactivation in Xenopus oocytes. EMBO J 15:900-9
144. Wu M, Nilsson P, Henriksson N, et al. (2009). Structural basis of m(7)GpppG binding to poly(A)-specific ribonuclease. Structure 17:276-86
145. Wu M, Reuter M, Lilie H, et al. (2005). Structural insight into poly(A) binding and catalytic mechanism of human PARN. Embo J 24:4082-93
146. Wu X, Brewer G. (2012). The regulation of mRNA stability in mammalian cells: 2. 0. Gene 500:10-21
147. Yamashita A, Chang TC, Yamashita Y, et al. (2005). Concerted action of poly(A) nucleases and decapping enzyme in mammalian mRNA turnover. Nat Struct Mol Biol 12:1054-63
148. Yang W. (2011). Nucleases: diversity of structure, function and mechanism. Q Rev Biophys 44:1-93
149. Yang W, Lee JY, Nowotny M. (2006). Making and breaking nucleic acids: two-Mg2-ion catalysis and substrate specificity. Mol Cell 22:5-13
150. Zhang L, Lee JE, Wilusz J, Wilusz CJ. (2008). The RNA-binding protein CUGBP1 regulates stability of tumor necrosis factor mRNA in muscle cells: implications for myotonic dystrophy. J Biol Chem 283:22457-63
151. Zhang A, Liu WF, Yan YB. (2007). Role of the RRM domain in the activity, structure and stability of poly(A)-specific ribonuclease. Arch Biochem Biophys 461:255-62
152. Zhang X, Virtanen A, Kleiman FE. (2010). To polyadenylate or to deadenylate: that is the question. Cell Cycle 9:4437-49
153. Zhu Y, Chen G, Lv F, et al. (2011). Zinc-finger antiviral protein inhibits HIV-1 infection by selectively targeting multiply spliced viral mRNAs for degradation. Proc Natl Acad Sci USA 108: 15834-9
154. Zuo Y, Deutscher MP. (2001). Exoribonuclease superfamilies: structural analysis and phylogenetic distribution. Nucleic Acids Res 29:1017-26