Ribonuclease L and metal-ion-independent endoribonuclease cleavage sites in host and viral RNAs

Nucleic Acids Research

Volumn 42, Issue 8, 2014, Pages 5202-5216

  Cooper, Daphne A ^a   Jha, Babal K ^b   Silverman, Robert H ^b   Hesselberth, Jay R ^a   Barton, David J ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b LERNER RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2,3' CYCLIC PHOSPHATE; COMPLEMENTARY DNA; PHOSPHATE; RIBONUCLEASE; RIBONUCLEASE L; RNA; RNA 5S; SMALL NUCLEAR RNA; U6 SMALL NUCLEAR RNA; UNCLASSIFIED DRUG; VIRUS RNA;

ARTICLE; CONTROLLED STUDY; DNA LIBRARY; DNA SYNTHESIS; ENZYME ISOLATION; ENZYME LOCALIZATION; ENZYME SYNTHESIS; HELA CELL LINE; HEPATITIS C VIRUS; NONHUMAN; NUCLEOTIDE SEQUENCE; POLIOMYELITIS; PRIORITY JOURNAL; PROCESS OPTIMIZATION; PROTEIN CLEAVAGE; RNA ANALYSIS; RNA CLEAVAGE; RNA SEQUENCE; SEQUENCE ANALYSIS; VIRUS GENOME;

ENDORIBONUCLEASES; HELA CELLS; HEPACIVIRUS; HUMANS; POLIOVIRUS; RIBONUCLEASE, PANCREATIC; RNA CLEAVAGE; RNA, RIBOSOMAL; RNA, SMALL NUCLEAR; RNA, VIRAL;

EID: 84899862908     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku118     Document Type: Article

References (76)

1. Yang, W. (2011) Nucleases: diversity of structure, function and mechanism. Q. Rev. Biophys., 44, 1-93.
2. Zhou, A.M., Paranjape, J., Brown, T.L., Nie, H.Q., Naik, S., Dong, B.H., Chang, A.S., Trapp, B., Fairchild, R., Colmenares, C. et al. (1997) Interferon action and apoptosis are defective in mice devoid of 2′, 5′-oligoadenylate-dependent RNase L. EMBO J., 16, 6355-6363.
3. Tuck, A.C. and Tollervey, D. (2011) RNA in pieces. Trends Genet., 27, 422-432.
4. Yamasaki, S., Ivanov, P., Hu, G.F. and Anderson, P. (2009) Angiogenin cleaves tRNA and promotes stress-induced translational repression. J. Cell Biol., 185, 35-42.
5. Luhtala, N. and Parker, R. (2010) T2 Family ribonucleases: ancient enzymes with diverse roles. Trends Biochem. Sci., 35, 253-259.
6. Mroczek, S., Krwawicz, J., Kutner, J., Lazniewski, M., Kucinski, I., Ginalski, K. and Dziembowski, A. (2012) C16orf57, a gene mutated in poikiloderma with neutropenia, encodes a putative phosphodiesterase responsible for the U6 snRNA 3′ end modification. Genes Dev., 26, 1911-1925.
7. Shchepachev, V., Wischnewski, H., Missiaglia, E., Soneson, C. and Azzalin, C.M. (2012) Mpn1, mutated in poikiloderma with neutropenia protein 1, is a conserved 3′-to-5′ RNA exonuclease processing U6 small nuclear RNA. Cell Rep., 2, 855-865.
8. Shchepachev, V. and Azzalin, C.M. (2013) The Mpn1 RNA exonuclease: cellular functions and implication in disease. FEBS Lett., 587, 1858-1862.
9. Sidrauski, C. and Walter, P. (1997) The transmembrane kinase Ire1p is a site-specific endonuclease that initiates mRNA splicing in the unfolded protein response. Cell, 90, 1031-1039.
10. Cho, H., Stanzione, F., LaMarca, R., Sum, A.K. and Chan, C. (2013) Computational and experimental analyses of the transmembrane domain dimerization of IRE1 alpha protein. Biophys. J., 104, 406A.
11. Laneve, P., Gioia, U., Ragno, R., Altieri, F., Di Franco, C., Santini, T., Arceci, M., Bozzoni, I. and Caffarelli, E. (2008) The tumor marker human placental protein 11 is an endoribonuclease. J. Biol. Chem., 283, 34712-34719.
12. Esakova, O. and Krasilnikov, A.S. (2010) Of proteins and RNA: the RNase P/MRP family. RNA, 16, 1725-1747.
13. Lee, H.H., Kim, Y.S., Kim, K.H., Heo, I., Kim, S.K., Kim, O., Kim, H.K., Yoon, J.Y., Kim, H.S., Kim, D.J. et al. (2007) Structural and functional insights into Dom34, a key component of no-go mRNA decay. Mol. Cell, 27, 938-950.
14. Cole, S.E., LaRiviere, F.J., Merrikh, C.N. and Moore, M.J. (2009) A convergence of rRNA and mRNA quality control pathways revealed by mechanistic analysis of nonfunctional rRNA decay. Mol. Cell, 34, 440-450.
15. Schoenberg, D.R. (2011) Mechanisms of endonuclease-mediated mRNA decay. Wiley Interdiscip. Rev. RNA, 2, 582-600.
16. Ivanov, K.A., Hertzig, T., Rozanov, M., Bayer, S., Thiel, V., Gorbalenya, A.E. and Ziebuhr, J. (2004) Major genetic marker of nidoviruses encodes a replicative endoribonuclease. Proc. Natl Acad. Sci. USA, 101, 12694-12699.
17. Nedialkova, D.D., Ulferts, R., van den Born, E., Lauber, C., Gorbalenya, A.E., Ziebuhr, J. and Snijder, E.J. (2009) Biochemical characterization of arterivirus nonstructural protein 11 reveals the nidovirus-wide conservation of a replicative endoribonuclease. J. Virol., 83, 5671-5682.
18. Andersen, J.B., Li, X.L., Judge, C.S., Zhou, A., Jha, B.K., Shelby, S., Zhou, L., Silverman, R.H. and Hassel, B.A. (2007) Role of 2-5A-dependent RNase-L in senescence and longevity. Oncogene, 26, 3081-3088.
19. Long, T.M., Chakrabarti, A., Ezelle, H.J., Brennan-Laun, S.E., Raufman, J.P., Polyakova, I., Silverman, R.H. and Hassel, B.A. (2013) RNase-L deficiency exacerbates experimental colitis and colitis-associated cancer. Inflamm. Bowel Dis., 19, 1295-1305.
20. Silverman, R.H. (2003) Implications for RNase L in prostate cancer biology. Biochemistry, 42, 1805-1812.
21. Li, X.L., Ezelle, H.J., Kang, T.J., Zhang, L., Shirey, K.A., Harro, J., Hasday, J.D., Mohapatra, S.K., Crasta, O.R., Vogel, S.N. et al. (2008) An essential role for the antiviral endoribonuclease, RNase-L, in antibacterial immunity. Proc. Natl Acad. Sci. USA, 105, 20816-20821.
22. Zhou, A., Hassel, B.A. and Silverman, R.H. (1993) Expression cloning of 2-5A-dependent RNAase: a uniquely regulated mediator of interferon action. Cell, 72, 753-765.
23. Silverman, R.H. (2007) Viral encounters with 2′, 5′-oligoadenylate synthetase and RNase L during the interferon antiviral response. J. Virol., 81, 12720-12729.
24. Dong, B., Niwa, M., Walter, P. and Silverman, R.H. (2001) Basis for regulated RNA cleavage by functional analysis of RNase L and Ire1p. RNA, 7, 361-373.
25. Gonzalez, T.N., Sidrauski, C., Dorfler, S. and Walter, P. (1999) Mechanism of non-spliceosomal mRNA splicing in the unfolded protein response pathway. EMBO J., 18, 3119-3132.
26. Wreschner, D.H., McCauley, J.W., Skehel, J.J. and Kerr, I.M. (1981) Interferon action-sequence specificity of the ppp(A2′p)nA-dependent ribonuclease. Nature, 289, 414-417.
27. Han, J.Q., Wroblewski, G., Xu, Z., Silverman, R.H. and Barton, D.J. (2004) Sensitivity of hepatitis C virus RNA to the antiviral enzyme ribonuclease L is determined by a subset of efficient cleavage sites. J. Interferon Cytokine Res., 24, 664-676.
28. Malathi, K., Dong, B., Gale, M. Jr and Silverman, R.H. (2007) Small self-RNA generated by RNase L amplifies antiviral innate immunity. Nature, 448, 816-819.
29. Malathi, K., Saito, T., Crochet, N., Barton, D.J., Gale, M. Jr and Silverman, R.H. (2010) RNase L releases a small RNA from HCV RNA that refolds into a potent PAMP. RNA, 16, 2108-2119.
30. Han, J.Q., Townsend, H.L., Jha, B.K., Paranjape, J.M., Silverman, R.H. and Barton, D.J. (2007) A phylogenetically conserved RNA structure in the poliovirus open reading frame inhibits the antiviral endoribonuclease RNase L. J. Virol., 81, 5561-5572.
31. Keel, A.Y., Jha, B.K. and Kieft, J.S. (2012) Structural architecture of an RNA that competitively inhibits RNase L. RNA, 18, 88-99.
32. Townsend, H.L., Jha, B.K., Han, J.Q., Maluf, N.K., Silverman, R.H. and Barton, D.J. (2008) A viral RNA competitively inhibits the antiviral endoribonuclease domain of RNase L. RNA, 14, 1026-1036.
33. Townsend, H.L., Jha, B.K., Silverman, R.H. and Barton, D.J. (2008) A putative loop E motif and an H-H kissing loop interaction are conserved and functional features in a group C enterovirus RNA that inhibits ribonuclease L. RNA Biol., 5, 263-272.
34. Zhang, R., Jha, B.K., Ogden, K.M., Dong, B., Zhao, L., Elliott, R., Patton, J.T., Silverman, R.H. and Weiss, S.R. (2013) Homologous 2′, 5′-phosphodiesterases from disparate RNA viruses antagonize antiviral innate immunity. Proc. Natl Acad. Sci. USA, 110, 13114-13119.
35. Zhao, L., Jha, B.K., Wu, A., Elliott, R., Ziebuhr, J., Gorbalenya, A.E., Silverman, R.H. and Weiss, S.R. (2012) Antagonism of the interferon-induced OAS-RNase L pathway by murine coronavirus ns2 protein is required for virus replication and liver pathology. Cell Host Microbe, 11, 607-616.
36. Sorgeloos, F., Jha, B.K., Silverman, R.H. and Michiels, T. (2013) Evasion of antiviral innate immunity by Theiler's virus L* protein through direct inhibition of RNase L. PLoS Pathog., 9, e1003474.
37. Wreschner, D.H., James, T.C., Silverman, R.H. and Kerr, I.M. (1981) Ribosomal RNA cleavage, nuclease activation and 2-5A(ppp(A2′p)nA) in interferon-treated cells. Nucleic Acids Res., 9, 1571-1581.
38. Banerjee, S., An, S., Zhou, A., Silverman, R.H. and Makino, S. (2000) RNase L-independent specific 28S rRNA cleavage in murine coronavirus-infected cells. J. Virol., 74, 8793-8802.
39. Kwon, Y.C., Kang, J.I., Hwang, S.B. and Ahn, B.Y. (2013) The ribonuclease L-dependent antiviral roles of human 2′, 5′-oligoadenylate synthetase family members against hepatitis C virus. FEBS Lett., 587, 156-164.
40. Washenberger, C.L., Han, J.Q., Kechris, K.J., Jha, B.K., Silverman, R.H. and Barton, D.J. (2007) Hepatitis C virus RNA: dinucleotide frequencies and cleavage by RNase L. Virus Res., 130, 85-95.
41. Schutz, K., Hesselberth, J.R. and Fields, S. (2010) Capture and sequence analysis of RNAs with terminal 2′, 3′-cyclic phosphates. RNA, 16, 621-631.
42. Anger, A.M., Armache, J.P., Berninghausen, O., Habeck, M., Subklewe, M., Wilson, D.N. and Beckmann, R. (2013) Structures of the human and Drosophila 80S ribosome. Nature, 497, 80-85.
43. Barton, D.J., O'Donnell, B.J. and Flanegan, J.B. (2001) 5′ cloverleaf in poliovirus RNA is a cis-acting replication element required for negative-strand synthesis. EMBO J., 20, 1439-1448.
44. Kolykhalov, A.A., Agapov, E.V., Blight, K.J., Mihalik, K., Feinstone, S.M. and Rice, C.M. (1997) Transmission of hepatitis C by intrahepatic inoculation with transcribed RNA. Science, 277, 570-574.
45. Rusch, L., Dong, B. and Silverman, R.H. (2001) Monitoring activation of ribonuclease L by 2′, 5′-oligoadenylates using purified recombinant enzyme and intact malignant glioma cells. Methods Enzymol., 342, 10-20.
46. Silverman, R.H., Dong, B., Maitra, R.K., Player, M.R. and Torrence, P.F. (2000) Selective RNA cleavage by isolated RNase L activated with 2-5A antisense chimeric oligonucleotides. Methods Enzymol., 313, 522-533.
47. Dong, B. and Silverman, R.H. (1995) 2-5A-dependent RNase molecules dimerize during activation by 2-5A. J. Biol. Chem., 270, 4133-4137.
48. Langmead, B., Trapnell, C., Pop, M. and Salzberg, S.L. (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol., 10, R25.
49. Kivioja, T., Vaharautio, A., Karlsson, K., Bonke, M., Enge, M., Linnarsson, S. and Taipale, J. (2012) Counting absolute numbers of molecules using unique molecular identifiers. Nat. Methods, 9, 72-74.
50. R Development Core Team. (2008) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
51. Barrett, T., Wilhite, S.E., Ledoux, P., Evangelista, C., Kim, I.F., Tomashevsky, M., Marshall, K.A., Phillippy, K.H., Sherman, P.M., Holko, M. et al. (2013) NCBI GEO: archive for functional genomics data sets-update. Nucleic Acids Res., 41, D991-D995.
52. Richards, F.M. and Wykoff, H.W. (1971) Bovine Pancreatic Ribonuclease. In: Boyer, P.D. (ed.), The Enzymes, Vol. 4, 3rd edn. Academic Press Inc., Elsevier B.V., Amsterdam, pp. 647-656.
53. Forconi, M. and Herschlag, D. (2009) Metal ion-based RNA cleavage as a structural probe. Methods Enzymol., 468, 91-106.
54. Polacek, N. and Barta, A. (1998) Metal ion probing of rRNAs: evidence for evolutionarily conserved divalent cation binding pockets. RNA, 4, 1282-1294.
55. Palmenberg, A.C. and Sgro, J.Y. (1997) Topological organization of picornaviral genomes: statistical prediction of RNA structural signals. Semin. Virol., 8, 231-241.
56. Davis, M., Sagan, S.M., Pezacki, J.P., Evans, D.J. and Simmonds, P. (2008) Bioinformatic and physical characterizations of genome-scale ordered RNA structure in mammalian RNA viruses. J. Virol., 82, 11824-11836.
57. Kuznetsov, Y.G., Daijogo, S., Zhou, J., Semler, B.L. and McPherson, A. (2005) Atomic force microscopy analysis of icosahedral virus RNA. J. Mol. Biol., 347, 41-52.
58. Page, G.S., Mosser, A.G., Hogle, J.M., Filman, D.J., Rueckert, R.R. and Chow, M. (1988) 3-Dimensional structure of poliovirus serotype-1 neutralizing determinants. J. Virol., 62, 1781-1794.
59. Fiore, L., Ridolfi, B., Genovese, D., Buttinelli, G., Lucioli, S., Lahm, A. and Ruggeri, F.M. (1997) Poliovirus Sabin type 1 neutralization epitopes recognized immunoglobulin A monoclonal antibodies. J. Virol, 71, 6905-6912.
60. Iordanov, M.S., Paranjape, J.M., Zhou, A.M., Wong, J., Williams, B.R.G., Meurs, E.F., Silverman, R.H. and Magun, B.E. (2000) Activation of p38 mitogen-activated protein kinase and c-Jun NH2-terminal kinase by double-stranded RNA and encephalomyocarditis virus: involvement of RNase L, protein kinase R, and alternative pathways. Mol. Cell. Biol., 20, 617-627.
61. Houge, G., Robaye, B., Eikhom, T.S., Golstein, J., Mellgren, G., Gjertsen, B.T., Lanotte, M. and Doskeland, S.O. (1995) Fine mapping of 28s ribosomal-RNA sites specifically cleaved in cells undergoing apoptosis. Mol. Cell. Biol., 15, 2051-2062.
62. Benjamini, Y. and Speed, T.P. (2012) Summarizing and correcting the GC content bias in high-throughput sequencing. Nucleic Acids Res., 40, e72.
63. Johnson, G.D., Sendler, E., Lalancette, C., Hauser, R., Diamond, M.P. and Krawetz, S.A. (2011) Cleavage of rRNA ensures translational cessation in sperm at fertilization. Mol. Hum. Reprod., 17, 721-726.
64. Iwawaki, T., Hosoda, A., Okuda, T., Kamigori, Y., Nomura-Furuwatari, C., Kimata, Y., Tsuru, A. and Kohno, K. (2001) Translational control by the ER transmembrane kinase/ribonuclease IRE1 under ER stress. Nat. Cell Biol., 3, 158-164.
65. Samali, A., Gilje, B., Doskeland, S.O., Cotter, T.G. and Houge, G. (1997) The ability to cleave 28S ribosomal RNA during apoptosis is a cell-type dependent trait unrelated to DNA fragmentation. Cell Death Differ., 4, 289-293.
66. Mroczek, S. and Kufel, J. (2008) Apoptotic signals induce specific degradation of ribosomal RNA in yeast. Nucleic Acids Res., 36, 2874-2888.
67. Parker, R. (2012) RNA degradation in Saccharomyces cerevisae. Genetics, 191, 671-702.
68. Lafontaine, D.L.J. (2010) A 'garbage can' for ribosomes: how eukaryotes degrade their ribosomes. Trends Biochem. Sci., 35, 267-277.
69. Hillwig, M.S., Contento, A.L., Meyer, A., Ebany, D., Bassham, D.C. and Macintosh, G.C. (2011) RNS2, a conserved member of the RNase T2 family, is necessary for ribosomal RNA decay in plants. Proc. Natl Acad. Sci. USA, 108, 1093-1098.
70. Haud, N., Kara, F., Diekmann, S., Henneke, M., Willer, J.R., Hillwig, M.S., Gregg, R.G., Macintosh, G.C., Gartner, J., Alia, A. et al. (2011) rnaset2 mutant zebrafish model familial cystic leukoencephalopathy and reveal a role for RNase T2 in degrading ribosomal RNA. Proc. Natl Acad. Sci. USA, 108, 1099-1103.
71. Gu, J., Shumyatsky, G., Makan, N. and Reddy, R. (1997) Formation of 2′, 3′-cyclic phosphates at the 3′ end of human U6 small nuclear RNA in vitro. Identification of 2′, 3′-cyclic phosphates at the 3′ ends of human signal recognition particle and mitochondrial RNA processing RNAs. J. Biol. Chem., 272, 21989-21993.
72. Li, M.Y. and Gu, W. (2011) A critical role for noncoding 5S rRNA in regulating Mdmx stability. Mol. Cell, 43, 1023-1032.
73. Piper, P.W., Bellatin, J.A. and Lockheart, A. (1983) Altered maturation of sequences at the 3′ terminus of 5S gene transcripts in a Saccharomyces cerevisiae mutant that lacks a RNA processing endonuclease. EMBO J., 2, 353-359.
74. van Hoof, A., Lennertz, P. and Parker, R. (2000) Three conserved members of the RNase D family have unique and overlapping functions in the processing of 5S, 5.8S, U4, U5, RNase MRP and RNase P RNAs in yeast. EMBO J., 19, 1357-1365.
75. Licht, K., Medenbach, J., Luhrmann, R., Kambach, C. and Bindereif, A. (2008) 3′-cyclic phosphorylation of U6 snRNA leads to recruitment of recycling factor p110 through LSm proteins. RNA, 14, 1532-1538.
76. Kufel, J., Allmang, C., Petfalski, E., Beggs, J. and Tollervey, D. (2003) Lsm proteins are required for normal processing and stability of ribosomal RNAs. J. Biol. Chem., 278, 2147-2156.