RNA Regulation by Poly(ADP-Ribose) Polymerases

Molecular Cell

Volumn 58, Issue 6, 2015, Pages 959-969

  Bock, Florian J ^a   Todorova, Tanya T ^a   Chang, Paul ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE RIBOSE; MICRORNA; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; REGULATOR PROTEIN; RNA BINDING PROTEIN; TRANSCRIPTOME; POLY(ADENOSINE DIPHOSPHATE RIBOSE); RNA;

ADENOSINE DIPHOSPHATE RIBOSYLATION; APOPTOSIS; CELL STRESS; ENDOPLASMIC RETICULUM; EXOSOME; GENE EXPRESSION; IMMUNOPRECIPITATION; MOLECULAR MODEL; NONHUMAN; OXIDATIVE STRESS; PROTEIN BINDING; REVIEW; RNA BINDING; RNA METABOLISM; RNA PROCESSING; RNA SPLICING; STRESS; WASTE; ZINC FINGER MOTIF; ANIMAL; BIOLOGICAL MODEL; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; PROTEIN PROCESSING;

ADENOSINE DIPHOSPHATE RIBOSE; ANIMALS; GENE EXPRESSION REGULATION; HUMANS; MODELS, GENETIC; POLY ADENOSINE DIPHOSPHATE RIBOSE; POLY(ADP-RIBOSE) POLYMERASES; PROTEIN PROCESSING, POST-TRANSLATIONAL; RNA; RNA-BINDING PROTEINS;

EID: 84937622587     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.01.037     Document Type: Review

References (107)

1. Anderson P. Post-transcriptional control of cytokine production. Nat. Immunol. 2008, 9:353-359.
2. Anderson P., Kedersha N. Stress granules: the Tao of RNA triage. Trends Biochem. Sci. 2008, 33:141-150.
3. Atasheva S., Akhrymuk M., Frolova E.I., Frolov I. New PARP gene with an anti-alphavirus function. J. Virol. 2012, 86:8147-8160.
4. Atasheva S., Frolova E.I., Frolov I. Interferon-stimulated poly(ADP-Ribose) polymerases are potent inhibitors of cellular translation and virus replication. J. Virol. 2014, 88:2116-2130.
5. Barreau C., Paillard L., Osborne H.B. AU-rich elements and associated factors: are there unifying principles?. Nucleic Acids Res. 2005, 33:7138-7150.
6. Bartel D.P. MicroRNAs: target recognition and regulatory functions. Cell 2009, 136:215-233.
7. Bick M.J., Carroll J.-W.N., Gao G., Goff S.P., Rice C.M., MacDonald M.R. Expression of the zinc-finger antiviral protein inhibits alphavirus replication. J. Virol. 2003, 77:11555-11562.
8. Black D.L. Mechanisms of alternative pre-messenger RNA splicing. Annu. Rev. Biochem. 2003, 72:291-336.
9. Boamah E.K., Kotova E., Garabedian M., Jarnik M., Tulin A.V. Poly(ADP-Ribose) polymerase 1 (PARP-1) regulates ribosomal biogenesis in Drosophila nucleoli. PLoS Genet. 2012, 8:e1002442.
10. Boisvert F.-M., van Koningsbruggen S., Navascués J., Lamond A.I. The multifunctional nucleolus. Nat. Rev. Mol. Cell Biol. 2007, 8:574-585.
11. Bürkle A. Poly(ADP-ribose). The most elaborate metabolite of NAD+. FEBS J. 2005, 272:4576-4589.
12. Castello A., Fischer B., Eichelbaum K., Horos R., Beckmann B.M., Strein C., Davey N.E., Humphreys D.T., Preiss T., Steinmetz L.M., et al. Insights into RNA biology from an atlas of mammalian mRNA-binding proteins. Cell 2012, 149:1393-1406.
13. Chambon P., Weill J.D., Mandel P. Nicotinamide mononucleotide activation of new DNA-dependent polyadenylic acid synthesizing nuclear enzyme. Biochem. Biophys. Res. Commun. 1963, 11:39-43.
14. Chaudhury A., Chander P., Howe P.H. Heterogeneous nuclear ribonucleoproteins (hnRNPs) in cellular processes: Focus on hnRNP E1's multifunctional regulatory roles. RNA 2010, 16:1449-1462.
15. Chen K.C., Xie H., Cai Y. Modes of action of ADP-ribosylated elongation factor 2 in inhibiting the polypeptide elongation cycle: a modeling study. PLoS ONE 2012, 8:e66446. 10.1371/journal.pone.0066446.
16. Chen S., Xu Y., Zhang K., Wang X., Sun J., Gao G., Liu Y. Structure of N-terminal domain of ZAP indicates how a zinc-finger protein recognizes complex RNA. Nat. Struct. Mol. Biol. 2012, 19:430-435.
17. Coller J., Parker R. Eukaryotic mRNA decapping. Annu. Rev. Biochem. 2004, 73:861-890.
18. Daniels C.M., Ong S.E., Leung A.K.L. Phosphoproteomic approach to characterize protein mono- and poly(ADP-ribosyl)ation sites from cells. J. Proteome Res. 2014, 13:3510-3522.
19. Daubner G.M., Cléry A., Allain F.H.T. RRM-RNA recognition: NMR or crystallography. and new findings. Curr. Opin. Struct. Biol. 2013, 23:100-108.
20. Di Giammartino D.C., Shi Y., Manley J.L. PARP1 represses PAP and inhibits polyadenylation during heat shock. Mol. Cell 2013, 49:7-17.
21. Fabian M.R., Sonenberg N. The mechanics of miRNA-mediated gene silencing: a look under the hood of miRISC. Nat. Struct. Mol. Biol. 2012, 19:586-593.
22. Gagné J.-P., Hunter J.M., Labrecque B., Chabot B., Poirier G.G. A proteomic approach to the identification of heterogeneous nuclear ribonucleoproteins as a new family of poly(ADP-ribose)-binding proteins. Biochem. J. 2003, 371:331-340.
23. Gagné J.P., Isabelle M., Lo K.S., Bourassa S., Hendzel M.J., Dawson V.L., Dawson T.M., Poirier G.G. Proteome-wide identification of poly(ADP-ribose) binding proteins and poly(ADP-ribose)-associated protein complexes. Nucleic Acids Res. 2008, 36:6959-6976.
24. Gao G., Guo X., Goff S.P. Inhibition of retroviral RNA production by ZAP, a CCCH-type zinc finger protein. Science 2002, 297:1703-1706.
25. Garneau N.L., Wilusz J., Wilusz C.J. The highways and byways of mRNA decay. Nat. Rev. Mol. Cell Biol. 2007, 8:113-126.
26. Gibson B.A., Kraus W.L. New insights into the molecular and cellular functions of poly(ADP-ribose) and PARPs. Nat. Rev. Mol. Cell Biol. 2012, 13:411-424.
27. Glisovic T., Bachorik J.L., Yong J., Dreyfuss G. RNA-binding proteins and post-transcriptional gene regulation. FEBS Lett. 2008, 582:1977-1986.
28. Guetg C., Scheifele F., Rosenthal F., Hottiger M.O., Santoro R. Inheritance of silent rDNA chromatin is mediated by PARP1 via noncoding RNA. Mol. Cell 2012, 45:790-800.
29. Guo X., Carroll J.-W.N., Macdonald M.R., Goff S.P., Gao G. The zinc finger antiviral protein directly binds to specific viral mRNAs through the CCCH zinc finger motifs. J. Virol. 2004, 78:12781-12787.
30. Guo X., Ma J., Sun J., Gao G. The zinc-finger antiviral protein recruits the RNA processing exosome to degrade the target mRNA. Proc. Natl. Acad. Sci. USA 2007, 104:151-156.
31. Hafner M., Landthaler M., Burger L., Khorshid M., Hausser J., Berninger P., Rothballer A., Ascano M., Jungkamp A.C., Munschauer M., et al. Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 2010, 141:129-141.
32. Hall T.M.T. Multiple modes of RNA recognition by zinc finger proteins. Curr. Opin. Struct. Biol. 2005, 15:367-373.
33. Hayakawa S., Shiratori S., Yamato H., Kameyama T., Kitatsuji C., Kashigi F., Goto S., Kameoka S., Fujikura D., Yamada T., et al. ZAPS is a potent stimulator of signaling mediated by the RNA helicase RIG-I during antiviral responses. Nat. Immunol. 2011, 12:37-44.
34. Hellen C.U.T., Sarnow P. Internal ribosome entry sites in eukaryotic mRNA molecules. Genes Dev. 2001, 15:1593-1612.
35. Herzog N., Hartkamp J.D.H., Verheugd P., Treude F., Forst A.H., Feijs K.L.H., Lippok B.E., Kremmer E., Kleine H., Lüscher B. Caspase-dependent cleavage of the mono-ADP-ribosyltransferase ARTD10 interferes with its pro-apoptotic function. FEBS J. 2013, 280:1330-1343.
36. Hocine S., Singer R.H., Grünwald D. RNA processing and export. Cold Spring Harb. Perspect. Biol. 2010, 2:a000752.
37. Hsu P.D., Lander E.S., Zhang F. Development and applications of CRISPR-Cas9 for genome engineering. Cell 2014, 157:1262-1278.
38. Huang Y., Carmichael G.G. Role of polyadenylation in nucleocytoplasmic transport of mRNA. Mol. Cell. Biol. 1996, 16:1534-1542.
39. Iglewski W.J., Lee H., Muller P. ADP-ribosyltransferase from beef liver which ADP-ribosylates elongation factor-2. FEBS Lett. 1984, 173:113-118.
40. Iqbal M.B., Johns M., Cao J., Liu Y., Yu S.-C., Hyde G.D., Laffan M.A., Marchese F.P., Cho S.H., Clark A.R., et al. PARP-14 combines with tristetraprolin in the selective post-transcriptional control of macrophage tissue factor expression. Blood 2014, 124:3646-3655.
41. Isabelle M., Moreel X., Gagné J.-P., Rouleau M., Ethier C., Gagné P., Hendzel M.J., Poirier G.G. Investigation of PARP-1, PARP-2, and PARG interactomes by affinity-purification mass spectrometry. Proteome Sci. 2010, 8:22.
42. Isabelle M., Gagné J.-P., Gallouzi I.-E., Poirier G.G. Quantitative proteomics and dynamic imaging reveal that G3BP-mediated stress granule assembly is poly(ADP-ribose)-dependent following exposure to MNNG-induced DNA alkylation. J. Cell Sci. 2012, 125:4555-4566.
43. Jackson R.J., Hellen C.U.T., Pestova T.V. The mechanism of eukaryotic translation initiation and principles of its regulation. Nat. Rev. Mol. Cell Biol. 2010, 11:113-127.
44. Jäger D., Werdan K., Müller-Werdan U. Endogenous ADP-ribosylation of elongation factor-2 by interleukin-1β. Mol. Cell. Biochem. 2011, 348:125-128.
45. Ji Y., Tulin A.V. Poly(ADP-ribosyl)ation of heterogeneous nuclear ribonucleoproteins modulates splicing. Nucleic Acids Res. 2009, 37:3501-3513.
46. Ji Y., Tulin A.V. Poly(ADP-ribose) controls DE-cadherin-dependent stem cell maintenance and oocyte localization. Nat. Commun. 2012, 3:760.
47. Ji Y., Tulin A.V. Post-transcriptional regulation by poly(ADP-ribosyl)ation of the RNA-binding proteins. Int. J. Mol. Sci. 2013, 14:16168-16183.
48. Jiang H., Kim J.H., Frizzell K.M., Kraus W.L., Lin H. Clickable NAD analogues for labeling substrate proteins of poly(ADP-ribose) polymerases. J. Am. Chem. Soc. 2010, 132:9363-9372.
49. Jungmichel S., Rosenthal F., Altmeyer M., Lukas J., Hottiger M.O., Nielsen M.L. Proteome-wide identification of poly(ADP-Ribosyl)ation targets in different genotoxic stress responses. Mol. Cell 2013, 52:272-285.
50. Kato M., Han T.W., Xie S., Shi K., Du X., Wu L.C., Mirzaei H., Goldsmith E.J., Longgood J., Pei J., et al. Cell-free formation of RNA granules: low complexity sequence domains form dynamic fibers within hydrogels. Cell 2012, 149:753-767.
51. Kawashima K., Izawa M. Poly(ADP-ribose) synthesis in nucleoli and ADP-ribosylation of nucleolar proteins in mouse ascites tumor cells in vitro. J. Biochem. 1981, 89:1889-1901.
52. Kedersha N., Ivanov P., Anderson P. Stress granules and cell signaling: more than just a passing phase?. Trends Biochem. Sci. 2013, 38:494-506.
53. Kim D.H., Langlois M.A., Lee K.B., Riggs A.D., Puymirat J., Rossi J.J. HnRNP H inhibits nuclear export of mRNA containing expanded CUG repeats and a distal branch point sequence. Nucleic Acids Res. 2005, 33:3866-3874.
54. Kostka G., Schweiger A. ADP-ribosylation of proteins associated with heterogeneous nuclear RNA in rat liver nuclei. Biochim. Biophys. Acta 1982, 696:139-144.
55. Kotova E., Jarnik M., Tulin A.V. Poly (ADP-ribose) polymerase 1 is required for protein localization to Cajal body. PLoS Genet. 2009, 5:e1000387.
56. Koyama Y., Katagiri S., Hanai S., Uchida K., Miwa M. Poly(ADP-ribose) polymerase interacts with novel Drosophila ribosomal proteins, L22 and l23a, with unique histone-like amino-terminal extensions. Gene 1999, 226:339-345.
57. LeBlanc H.N., Ashkenazi A. Apo2L/TRAIL and its death and decoy receptors. Cell Death Differ. 2003, 10:66-75.
58. Lee H., Iglewski W.J. Cellular ADP-ribosyltransferase with the same mechanism of action as diphtheria toxin and Pseudomonas toxin A. Proc. Natl. Acad. Sci. USA 1984, 81:2703-2707.
59. Lee H., Komano J., Saitoh Y., Yamaoka S., Kozaki T., Misawa T., Takahama M., Satoh T., Takeuchi O., Yamamoto N., et al. Zinc-finger antiviral protein mediates retinoic acid inducible gene I-like receptor-independent antiviral response to murine leukemia virus. Proc. Natl. Acad. Sci. USA 2013, 110:12379-12384.
60. Léger K., Bär D., Savić N., Santoro R., Hottiger M.O. ARTD2 activity is stimulated by RNA. Nucleic Acids Res. 2014, 42:5072-5082.
61. Leitinger N., Wesierska-Gadek J. ADP-ribosylation of nucleolar proteins in HeLa tumor cells. J. Cell. Biochem. 1993, 52:153-158.
62. Leung A.K.L. Poly(ADP-ribose): an organizer of cellular architecture. J. Cell Biol. 2014, 205:613-619.
63. Leung A.K.L., Vyas S., Rood J.E., Bhutkar A., Sharp P.A., Chang P. Poly(ADP-ribose) regulates stress responses and microRNA activity in the cytoplasm. Mol. Cell 2011, 42:489-499.
64. Libri D., Dower K., Boulay J., Thomsen R., Rosbash M., Jensen T.H. Interactions between mRNA export commitment, 3'-end quality control, and nuclear degradation. Mol. Cell. Biol. 2002, 22:8254-8266.
65. Licatalosi D.D., Mele A., Fak J.J., Ule J., Kayikci M., Chi S.W., Clark T.A., Schweitzer A.C., Blume J.E., Wang X., et al. HITS-CLIP yields genome-wide insights into brain alternative RNA processing. Nature 2008, 456:464-469.
66. Lloyd R.E. Regulation of stress granules and P-bodies during RNA virus infection. Wiley Interdiscip. Rev. RNA 2013, 4:317-331.
67. Lord C.J., Tutt A.N.J., Ashworth A. Synthetic lethality and cancer therapy: lessons learned from the development of PARP inhibitors. Annu. Rev. Med. 2015, 66:455-470.
68. Malanga M., Czubaty A., Girstun A., Staron K., Althaus F.R. Poly(ADP-ribose) binds to the splicing factor ASF/SF2 and regulates its phosphorylation by DNA topoisomerase I. J. Biol. Chem. 2008, 283:19991-19998.
69. Manley J.L. Nuclear coupling: RNA processing reaches back to transcription. Nat. Struct. Biol. 2002, 9:790-791.
70. Mao R., Nie H., Cai D., Zhang J., Liu H., Yan R., Cuconati A., Block T.M., Guo J.T., Guo H. Inhibition of hepatitis B virus replication by the host zinc finger antiviral protein. PLoS Pathog. 2013, 9:e1003494.
71. Meder V.S., Boeglin M., de Murcia G., Schreiber V. PARP-1 and PARP-2 interact with nucleophosmin/B23 and accumulate in transcriptionally active nucleoli. J. Cell Sci. 2005, 118:211-222.
72. Meister G. Argonaute proteins: functional insights and emerging roles. Nat. Rev. Genet. 2013, 14:447-459.
73. Mérino D., Lalaoui N., Morizot A., Schneider P., Solary E., Micheau O. Differential inhibition of TRAIL-mediated DR5-DISC formation by decoy receptors 1 and 2. Mol. Cell. Biol. 2006, 26:7046-7055.
74. Messner S., Hottiger M.O. Histone ADP-ribosylation in DNA repair, replication and transcription. Trends Cell Biol. 2011, 21:534-542.
75. Moore M.J., Proudfoot N.J. Pre-mRNA processing reaches back to transcription and ahead to translation. Cell 2009, 136:688-700.
76. Müller S., Möller P., Bick M.J., Wurr S., Becker S., Günther S., Kümmerer B.M. Inhibition of filovirus replication by the zinc finger antiviral protein. J. Virol. 2007, 81:2391-2400.
77. Nakielny S., Dreyfuss G. The hnRNP C proteins contain a nuclear retention sequence that can override nuclear export signals. J. Cell Biol. 1996, 134:1365-1373.
78. Onomoto K., Yoneyama M., Fung G., Kato H., Fujita T. Antiviral innate immunity and stress granule responses. Trends Immunol. 2014, 35:420-428.
79. Pérez I., McAfee J.G., Patton J.G. Multiple RRMs contribute to RNA binding specificity and affinity for polypyrimidine tract binding protein. Biochemistry 1997, 36:11881-11890.
80. Prasad S., Walent J., Dritschilo A. ADP-ribosylation of heterogeneous ribonucleoproteins in HeLa cells. Biochem. Biophys. Res. Commun. 1994, 204:772-779.
81. Proudfoot N.J., Furger A., Dye M.J. Integrating mRNA processing with transcription. Cell 2002, 108:501-512.
82. Rancourt A., Satoh M.S. Delocalization of nucleolar poly(ADP-ribose) polymerase-1 to the nucleoplasm and its novel link to cellular sensitivity to DNA damage. DNA Repair (Amst.) 2009, 8:286-297.
83. Richter K., Haslbeck M., Buchner J. The heat shock response: life on the verge of death. Mol. Cell 2010, 40:253-266.
84. Roy B., Jacobson A. The intimate relationships of mRNA decay and translation. Trends Genet. 2013, 29:691-699.
85. Rozelle D.K., Filone C.M., Kedersha N., Connor J.H. Activation of stress response pathways promotes formation of antiviral granules and restricts virus replication. Mol. Cell. Biol. 2014, 34:2003-2016.
86. Saavedra C., Tung K.S., Amberg D.C., Hopper A.K., Cole C.N. Regulation of mRNA export in response to stress in Saccharomyces cerevisiae. Genes Dev. 1996, 10:1608-1620.
87. Schoenberg D.R., Maquat L.E. Regulation of cytoplasmic mRNA decay. Nat. Rev. Genet. 2012, 13:246-259.
88. Seo G.J., Kincaid R.P., Phanaksri T., Burke J.M., Pare J.M., Cox J.E., Hsiang T.-Y.Y., Krug R.M., Sullivan C.S. Reciprocal inhibition between intracellular antiviral signaling and the RNAi machinery in mammalian cells. Cell Host Microbe 2013, 14:435-445.
89. Sitikov A.S., Davydova E.K., Ovchinnikov L.P. Endogenous ADP-ribosylation of elongation factor 2 in polyribosome fraction of rabbit reticulocytes. FEBS Lett. 1984, 176:261-263.
90. Sitikov A.S., Davydova E.K., Bezlepkina T.A., Ovchinnikov L.P., Spirin A.S. Eukaryotic elongation factor 2 loses its non-specific affinity for RNA and leaves polyribosomes as a result of ADP-ribosylation. FEBS Lett. 1984, 176:406-410.
91. Song D., Sakamoto S., Taniguchi T. Inhibition of poly(ADP-ribose) polymerase activity by Bcl-2 in association with the ribosomal protein S3a. Biochemistry 2002, 41:929-934.
92. Spriggs K.A., Bushell M., Willis A.E. Translational regulation of gene expression during conditions of cell stress. Mol. Cell 2010, 40:228-237.
93. Thomas M.F., L'Etoile N.D., Ansel K.M. Eri1: a conserved enzyme at the crossroads of multiple RNA-processing pathways. Trends Genet. 2014, 30:298-307.
94. Todorova T., Bock F.J., Chang P. PARP13 regulates cellular mRNA post-transcriptionally and functions as a pro-apoptotic factor by destabilizing TRAILR4 transcript. Nat. Commun. 2014, 5:5362.
95. Tschochner H., Hurt E. Pre-ribosomes on the road from the nucleolus to the cytoplasm. Trends Cell Biol. 2003, 13:255-263.
96. Vinciguerra P., Stutz F. mRNA export: an assembly line from genes to nuclear pores. Curr. Opin. Cell Biol. 2004, 16:285-292.
97. Vivelo C.A., Leung A.K.L. Proteomics approaches to identify mono-(ADP-ribosyl)ated and poly(ADP-ribosyl)ated proteins. Proteomics 2015, 15:203-217.
98. Vyas S., Chang P. New PARP targets for cancer therapy. Nat. Rev. Cancer 2014, 14:502-509.
99. Vyas S., Melissa C.-C., Todorova T., Huang Y.-H.H., Chang P. A systematic analysis of the PARP protein family identifies new functions critical for cell physiology. Nat. Commun. 2012, 4:2240.
100. Vyas S., Matic I., Uchima L., Rood J., Zaja R., Hay R.T., Ahel I., Chang P. Family-wide analysis of poly(ADP-ribose) polymerase activity. Nat. Commun. 2014, 5:4426.
101. Welsby I., Hutin D., Gueydan C., Kruys V., Rongvaux A., Leo O. PARP12, an interferon-stimulated gene involved in the control of protein translation and inflammation. J. Biol. Chem. 2014, 289:26642-26657.
102. Wilson R.C., Doudna J.A. Molecular mechanisms of RNA interference. Annu. Rev. Biophys. 2013, 42:217-239.
103. Wolfe S.A., Nekludova L., Pabo C.O. DNA recognition by Cys2His2 zinc finger proteins. Annu. Rev. Biophys. Biomol. Struct. 2000, 29:183-212.
104. Yang X.C., Purdy M., Marzluff W.F., Dominski Z. Characterization of 3'hExo, a 3' exonuclease specifically interacting with the 3' end of histone mRNA. J. Biol. Chem. 2006, 281:30447-30454.
105. Yu M., Schreek S., Cerni C., Schamberger C., Lesniewicz K., Poreba E., Vervoorts J., Walsemann G., Grötzinger J., Kremmer E., et al. PARP-10, a novel Myc-interacting protein with poly(ADP-ribose) polymerase activity, inhibits transformation. Oncogene 2005, 24:1982-1993.
106. Zhang Y., Wang J., Ding M., Yu Y. Site-specific characterization of the Asp- and Glu-ADP-ribosylated proteome. Nat. Methods 2013, 10:981-984.
107. Zhu Y., Chen G., Lv F., Wang X., Ji X., Xu Y., Sun J., Wu L., Zheng Y.-T., Gao G. Zinc-finger antiviral protein inhibits HIV-1 infection by selectively targeting multiply spliced viral mRNAs for degradation. Proc. Natl. Acad. Sci. USA 2011, 108:15834-15839.