Garbled messages and corrupted translations

Nature Chemical Biology

Volumn 6, Issue 3, 2010, Pages 189-198

  Schneider Poetsch, Tilman ^a   Usui, Takeo ^b   Kaida, Daisuke ^c   Yoshida, Minoru ^a,d  

^a RIKEN   (Japan)

^b UNIVERSITY OF TSUKUBA   (Japan)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

13 DEOXYTEDANOLIDE; BIFLAVONOID; CAPPED RNA; CYCLOHEXIMIDE; DIDEMNIN B; ELONGATION FACTOR; FR 901463; FR 901464; FR 901465; HIPPURISTANOL; HOMOHARRINGTONINE; INITIATION FACTOR; ISOGINKGETIN; ISOMIGRASTATIN; LACTIMIDOMYCIN; MEAYAMYCIN; MESSENGER RNA; MESSENGER RNA PRECURSOR; MYCALAMIDE A; NATURAL PRODUCT; PATEAMINE; PATEAMINE A; PEDERIN; PLADIENOLIDE; PLADIENOLIDE B; POLYPYRIMIDINE TRACT BINDING PROTEIN; REVEROMYCIN A; SMALL NUCLEAR RIBONUCLEOPROTEIN; SPLICEOSTATIN A; UNCLASSIFIED DRUG; UNINDEXED DRUG;

CYTOPLASM; EUKARYOTE; HUMAN; NONHUMAN; NUCLEOTIDE SEQUENCE; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REVIEW; RIBOSOME; RNA INTERFERENCE; RNA TRANSLATION; SPLICEOSOME;

EUKARYOTA;

EID: 77249147933     PISSN: 15524450     EISSN: 15524469     Source Type: Journal    
DOI: 10.1038/nchembio.326     Document Type: Review

References (97)

1. Staley, J.P. & Woolford, J.L. Jr. Assembly of ribosomes and spliceosomes: complex ribonucleoprotein machines. Curr. Opin. Cell Biol. 21, 109-118 (2009).
2. Wahl, M.C., Will, C.L. & Lührmann, R. The spliceosome: design principles of a dynamic RNP machine. Cell 136, 701-718 (2009).
3. Nakajima, H. et al. New antitumor substances, FR901463, FR901464 and FR901465. I. Taxonomy, fermentation, isolation, physico-chemical properties and biological activities. J. Antibiot. (Tokyo) 49, 1196-1203 (1996).
4. Nakajima, H. et al. New antitumor substances, FR901463, FR901464 and FR901465. II. Activities against experimental tumors in mice and mechanism of action. J. Antibiot. (Tokyo) 49, 1204-1211 (1996).
5. Nakajima, H., Kim, Y.B., Terano, H., Yoshida, M. & Horinouchi, S. FR901228, a potent antitumor antibiotic, is a novel histone deacetylase inhibitor. Exp. Cell Res. 241, 126-133 (1998).
6. Kaida, D. et al. Spliceostatin A targets SF3b and inhibits both splicing and nuclear retention of pre-mRNA. Nat. Chem. Biol. 3, 576-583 (2007). (Pubitemid 47294395)
7. Horigome, M., Motoyoshi, H., Watanabe, H. & Kitahara, T. A synthesis of FR901464. Tetrahedr. Lett. 42, 8207-8210 (2001).
8. Thompson, C.F., Jamison, T.F. & Jacobsen, E.N. FR901464: total synthesis, proof of structure, and evaluation of synthetic analogues. J. Am. Chem. Soc. 123, 9974-9983 (2001).
9. Albert, B.J., Sivaramakrishnan, A., Naka, T., Czaicki, N.L. & Koide, K. Total syntheses, fragmentation studies, and antitumor/antiproliferative activities of FR901464 and its low picomolar analogue. J. Am. Chem. Soc. 129, 2648-2659 (2007).
10. Albert, B.J. et al. Meayamycin inhibits pre-messenger RNA splicing and exhibits picomolar activity against multidrug-resistant cells. Mol. Cancer Ther. 8, 2308-2318 (2009).
11. Sakai, T. et al. Pladienolides, new substances from culture of Streptomyces platensis Mer-11107. I. Taxonomy, fermentation, isolation and screening. J. Antibiot. (Tokyo) 57, 173-179 (2004). (Pubitemid 38489675)
12. Sakai, T., Asai, N., Okuda, A., Kawamura, N. & Mizui, Y. Pladienolides, new substances from culture of Streptomyces platensis Mer-11107. II. Physico-chemical properties and structure elucidation. J. Antibiot. (Tokyo) 57, 180-187 (2004). (Pubitemid 38489676)
13. Kotake, Y. et al. Splicing factor SF3b as a target of the antitumor natural product pladienolide. Nat. Chem. Biol. 3, 570-575 (2007).
14. O'Brien, K., Matlin, A.J., Lowell, A.M. & Moore, M.J. The biflavonoid isoginkgetin is a general inhibitor of Pre-mRNA splicing. J. Biol. Chem. 283, 33147-33154 (2008).
15. Soret, J. et al. Selective modification of alternative splicing by indole derivatives that target serine-arginine-rich protein splicing factors. Proc. Natl. Acad. Sci. USA 102, 8764-8769 (2005).
16. Stoilov, P., Lin, C.H., Damoiseaux, R., Nikolic, J. & Black, D.L. A high-throughput screening strategy identifies cardiotonic steroids as alternative splicing modulators. Proc. Natl. Acad. Sci. USA 105, 11218-11223 (2008).
17. Hagiwara, M. Alternative splicing: a new drug target of the post-genome era. Biochim. Biophys. Acta 1754, 324-331 (2005).
18. Martinez, E. et al. Human STAGA complex is a chromatin-acetylating transcription coactivator that interacts with pre-mRNA splicing and DNA damage-binding factors in vivo. Mol. Cell. Biol. 21, 6782-6795 (2001).
19. Choudhary, C. et al. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325, 834-840 (2009).
20. Kuhn, A.N., van Santen, M.A., Schwienhorst, A., Urlaub, H. & Luhrmann, R. Stalling of spliceosome assembly at distinct stages by small-molecule inhibitors of protein acetylation and deacetylation. RNA 15, 153-175 (2009).
21. Balasubramanyam, K., Swaminathan, V., Ranganathan, A. & Kundu, T.K. Small molecule modulators of histone acetyltransferase p300. J. Biol. Chem. 278, 19134-19140 (2003).
22. Balasubramanyam, K. et al. Polyisoprenylated benzophenone, garcinol, a natural histone acetyltransferase inhibitor, represses chromatin transcription and alters global gene expression. J. Biol. Chem. 279, 33716-33726 (2004).
23. Ban, N., Nissen, P., Hansen, J., Moore, P.B. & Steitz, T.A. The complete atomic structure of the large ribosomal subunit at 2.4 A resolution. Science 289, 905-920 (2000).
24. Brodersen, D.E. et al. The structural basis for the action of the antibiotics tetracycline, pactamycin, and hygromycin B on the 30S ribosomal subunit. Cell 103, 1143-1154 (2000).
25. Wimberly, B.T. et al. Structure of the 30S ribosomal subunit. Nature 407, 327-339 (2000).
26. Tu, D., Blaha, G., Moore, P.B. & Steitz, T.A. Structures of MLSBK antibiotics bound to mutated large ribosomal subunits provide a structural explanation for resistance. Cell 121, 257-270 (2005).
27. Schroeder, S.J., Blaha, G., Tirado-Rives, J., Steitz, T.A. & Moore, P.B. The structures of antibiotics bound to the E site region of the 50 S ribosomal subunit of Haloarcula marismortui: 13-deoxytedanolide and girodazole. J. Mol. Biol. 367, 1471-1479 (2007).
28. Lecompte, O., Ripp, R., Thierry, J.C., Moras, D. & Poch, O. Comparative analysis of ribosomal proteins in complete genomes: an example of reductive evolution at the domain scale. Nucleic Acids Res. 30, 5382-5390 (2002).
29. Hermann, T. Drugs targeting the ribosome. Curr. Opin. Struct. Biol. 15, 355-366 (2005).
30. Sutcliffe, J.A. Improving on nature: antibiotics that target the ribosome. Curr. Opin. Microbiol. 8, 534-542 (2005).
31. Schroeder, R., Waldsich, C. & Wank, H. Modulation of RNA function by aminoglycoside antibiotics. EMBO J. 19, 1-9 (2000).
32. Chopra, I. & Roberts, M. Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol. Mol. Biol. Rev. 65, 232-260 (2001).
33. Nierhaus, D. & Nierhaus, K.H. Identification of the chloramphenicol-binding protein in Escherichia coli ribosomes by partial reconstitution. Proc. Natl. Acad. Sci. USA 70, 2224-2228 (1973).
34. Bashan, A. et al. Structural basis of the ribosomal machinery for peptide bond formation, translocation, and nascent chain progression. Mol. Cell 11, 91-102 (2003).
35. Tenson, T., Lovmar, M. & Ehrenberg, M. The mechanism of action of macrolides, lincosamides and streptogramin B reveals the nascent peptide exit path in the ribosome. J. Mol. Biol. 330, 1005-1014 (2003).
36. Hurdle, J.G., O'Neill, A.J. & Chopra, I. Prospects for aminoacyl-tRNA synthetase inhibitors as new antimicrobial agents. Antimicrob. Agents Chemother. 49, 4821-4833 (2005).
37. Rodnina, M.V. et al. Thiostrepton inhibits the turnover but not the GTPase of elongation factor G on the ribosome. Proc. Natl. Acad. Sci. USA 96, 9586-9590 (1999).
38. Heffron, S.E. & Jurnak, F. Structure of an EF-Tu complex with a thiazolyl peptide antibiotic determined at 2.35 A resolution: atomic basis for GE2270A inhibition of EF-Tu. Biochemistry 39, 37-45 (2000).
39. Eustice, D.C. & Wilhelm, J.M. Mechanisms of action of aminoglycoside antibiotics in eucaryotic protein synthesis. Antimicrob. Agents Chemother. 26, 53-60 (1984).
40. Nathans, D. Puromycin inhibition of protein synthesis: incorporation of puromycin into peptide chains. Proc. Natl. Acad. Sci. USA 51, 585-592 (1964).
41. Justice, M.C. et al. Elongation factor 2 as a novel target for selective inhibition of fungal protein synthesis. J. Biol. Chem. 273, 3148-3151 (1998).
42. Ahuja, D. et al. Inhibition of protein synthesis by didemnin B: how EF-1alpha mediates inhibition of translocation. Biochemistry 39, 4339-4346 (2000).
43. Gomez-Lorenzo, M.G. et al. Three-dimensional cryo-electron microscopy localization of EF2 in the Saccharomyces cerevisiae 80S ribosome at 17.5 A resolution. EMBO J. 19, 2710-2718 (2000).
44. Jorgensen, R. et al. Two crystal structures demonstrate large conformational changes in the eukaryotic ribosomal translocase. Nat. Struct. Biol. 10, 379-385 (2003).
45. Vazquez, D. Inhibitors of protein biosynthesis. Mol. Biol. Biochem. Biophys. 30, i-x, 1-312 (1979).
46. Takahashi, H. et al. Reveromycins, new inhibitors of eukaryotic cell growth. II. Biological activities. J. Antibiot. (Tokyo) 45, 1414-1419 (1992).
47. Miyamoto, Y. et al. Identification of Saccharomyces cerevisiae isoleucyl-tRNA synthetase as a target of the G1-specific inhibitor Reveromycin A. J. Biol. Chem. 277, 28810-28814 (2002).
48. Hood, K.A., West, L.M., Northcote, P.T., Berridge, M.V. & Miller, J.H. Induction of apoptosis by the marine sponge (Mycale) metabolites, mycalamide A and pateamine. Apoptosis 6, 207-219 (2001).
49. Sugawara, K. et al. Lactimidomycin, a new glutarimide group antibiotic. Production, isolation, structure and biological activity. J. Antibiot. (Tokyo) 45, 1433-1441 (1992).
50. Lee, K.H. et al. Inhibition of protein synthesis and activation of stress-activated protein kinases by onnamide A and theopederin B, antitumor marine natural products. Cancer Sci. 96, 357-364 (2005).
51. Chan, J., Khan, S.N., Harvey, I., Merrick, W. & Pelletier, J. Eukaryotic protein synthesis inhibitors identified by comparison of cytotoxicity profiles. RNA 10, 528-543 (2004).
52. Kapp, L.D. & Lorsch, J.R. The molecular mechanics of eukaryotic translation. Annu. Rev. Biochem. 73, 657-704 (2004).
53. Rogers, G.W. Jr., Richter, N.J., Lima, W.F. & Merrick, W.C. Modulation of the helicase activity of eIF4A by eIF4B, eIF4H, and eIF4F. J. Biol. Chem. 276, 30914-30922 (2001).
54. Palacios, I.M., Gatfield, D., St Johnston, D. & Izaurralde, E. An eIF4AIIIcontaining complex required for mRNA localization and nonsense-mediated mRNA decay. Nature 427, 753-757 (2004).
55. Northcote, P.T., Blunt, J.W. & Munro, M.H.G. Pateamine: a potent cytotoxin from the New Zealand marine sponge Mycale sp. Tetrahedr. Lett. 32, 6411-6414 (1991).
56. Rzasa, R.M., Shea, H.A. & Romo, D. Total synthesis of the novel, immunosuppressive agent (-)-pateamine A from Mycale sp. employing a ?-lactam-based macrocyclization. J. Am. Chem. Soc. 120, 591-592 (1998). (Pubitemid 28067830)
57. Low, W.K. et al. Inhibition of eukaryotic translation initiation by the marine natural product pateamine A. Mol. Cell 20, 709-722 (2005).
58. Bordeleau, M.E. et al. Stimulation of mammalian translation initiation factor eIF4A activity by a small molecule inhibitor of eukaryotic translation. Proc. Natl. Acad. Sci. USA 102, 10460-10465 (2005).
59. Bordeleau, M.E. et al. RNA-mediated sequestration of the RNA helicase eIF4A by pateamine A inhibits translation initiation. Chem. Biol. 13, 1287-1295 (2006).
60. Dang, Y. et al. Eukaryotic initiation factor 2?-independent pathway of stress granule induction by the natural product pateamine A. J. Biol. Chem. 281, 32870-32878 (2006).
61. Mazroui, R. et al. Inhibition of ribosome recruitment induces stress granule formation independently of eukaryotic initiation factor 2phosphorylation. Mol. Biol. Cell 17, 4212-4219 (2006).
62. Kedersha, N. & Anderson, P. Stress granules: sites of mRNA triage that regulate mRNA stability and translatability. Biochem. Soc. Trans. 30, 963-969 (2002).
63. Dang, Y. et al. Inhibition of nonsense-mediated mRNA decay by the natural product pateamine A through eukaryotic initiation factor 4AIII. J. Biol. Chem. 284, 23613-23621 (2009).
64. Kuznetsov, G. et al. Potent in vitro and in vivo anticancer activities of desmethyl, des-amino pateamine A, a synthetic analogue of marine natural product pateamine A. Mol. Cancer Ther. 8, 1250-1260 (2009).
65. Bordeleau, M.E. et al. Functional characterization of IRESes by an inhibitor of the RNA helicase eIF4A. Nat. Chem. Biol. 2, 213-220 (2006).
66. Lindqvist, L. et al. Selective pharmacological targeting of a DEAD box RNA helicase. PLoS One 3, e1583 (2008).
67. Obrig, T.G., Culp, W.J., McKeehan, W.L. & Hardesty, B. The mechanism by which cycloheximide and related glutarimide antibiotics inhibit peptide synthesis on reticulocyte ribosomes. J. Biol. Chem. 246, 174-181 (1971).
68. Pestova, T.V. & Hellen, C.U. Translation elongation after assembly of ribosomes on the Cricket paralysis virus internal ribosomal entry site without initiation factors or initiator tRNA. Genes Dev. 17, 181-186 (2003).
69. Schneider-Poetsch, T. et al. Inhibition of translation elongation by cycloheximide and lactimidomycin. Nat. Chem. Biol. 6, xxx-yyy (2010).
70. Nakae, K. et al. Migrastatin, a new inhibitor of tumor cell migration from Streptomyces sp. MK929-43F1. Taxonomy, fermentation, isolation and biological activities. J. Antibiot. (Tokyo) 53, 1130-1136 (2000).
71. Woo, E.J. et al. Migrastatin and a new compound, isomigrastatin, from Streptomyces platensis. J. Antibiot. (Tokyo) 55, 141-146 (2002).
72. Takemoto, Y., Tashiro, E. & Imoto, M. Suppression of multidrug resistance by migrastatin. J. Antibiot. (Tokyo) 59, 435-438 (2006).
73. Shan, D. et al. Synthetic analogues of migrastatin that inhibit mammary tumor metastasis in mice. Proc. Natl. Acad. Sci. USA 102, 3772-3776 (2005).
74. Ju, J., Lim, S.K., Jiang, H. & Shen, B. Migrastatin and dorrigocins are shunt metabolites of iso-migrastatin. J. Am. Chem. Soc. 127, 1622-1623 (2005).
75. Ju, J. et al. Lactimidomycin, iso-migrastatin and related glutarimidecontaining 12-membered macrolides are extremely potent inhibitors of cell migration. J. Am. Chem. Soc. 131, 1370-1371 (2009).
76. Gurel, G., Blaha, G., Steitz, T.A. & Moore, P.B. The structures of triacetyloleandomycin and mycalamide A bound to the large ribosomal subunit of Haloarcula marismortui. Antimicrob. Agents Chemother. 53, 5010-5014 (2009).
77. Nishimura, S. et al. 13-Deoxytedanolide, a marine sponge-derived antitumor macrolide, binds to the 60S large ribosomal subunit. Bioorg. Med. Chem. 13, 449-454 (2005).
78. Fresno, M., Jimenez, A. & Vazquez, D. Inhibition of translation in eukaryotic systems by harringtonine. Eur. J. Biochem. 72, 323-330 (1977).
79. Gurel, G., Blaha, G., Moore, P.B. & Steitz, T.A. U2504 determines the species specificity of the A-site cleft antibiotics: the structures of tiamulin, homoharringtonine, and bruceantin bound to the ribosome. J. Mol. Biol. 389, 146-156 (2009).
80. Quintas-Cardama, A., Kantarjian, H. & Cortes, J. Homoharringtonine, omacetaxine mepesuccinate, and chronic myeloid leukemia circa 2009. Cancer 115, 5382-5393 (2009).
81. Kucuk, O. et al. Phase II trail of didemnin B in previously treated non- Hodgkin's lymphoma: an Eastern Cooperative Oncology Group (ECOG) study. Am. J. Clin. Oncol. 23, 273-277 (2000).
82. Le Tourneau, C. et al. Reports of clinical benefit of plitidepsin (Aplidine), a new marine-derived anticancer agent, in patients with advanced medullary thyroid carcinoma. Am. J. Clin. Oncol. (2009).
83. Ocio, E.M., Mateos, M.V., Maiso, P., Pandiella, A. & San-Miguel, J.F. New drugs in multiple myeloma: mechanisms of action and phase I/II clinical findings. Lancet Oncol. 9, 1157-1165 (2008).
84. Robert, F. et al. Altering chemosensitivity by modulating translation elongation. PLoS One 4, e5428 (2009).
85. Beretta, L., Gingras, A.C., Svitkin, Y.V., Hall, M.N. & Sonenberg, N. Rapamycin blocks the phosphorylation of 4E-BP1 and inhibits cap-dependent initiation of translation. EMBO J. 15, 658-664 (1996).
86. Averous, J. & Proud, C.G. When translation meets transformation: the mTOR story. Oncogene 25, 6423-6435 (2006).
87. Woo, J.T. et al. Reveromycin A, an agent for osteoporosis, inhibits bone resorption by inducing apoptosis specifically in osteoclasts. Proc. Natl. Acad. Sci. USA 103, 4729-4734 (2006).
88. Hiraoka, K. et al. Inhibition of bone and muscle metastases of lung cancer cells by a decrease in the number of monocytes/macrophages. Cancer Sci. 99, 1595-1602 (2008).
89. Faustino, N.A. & Cooper, T.A. Pre-mRNA splicing and human disease. Genes Dev. 17, 419-437 (2003).
90. Ng, B. et al. Increased noncanonical splicing of autoantigen transcripts provides the structural basis for expression of untolerized epitopes. J. Allergy Clin. Immunol. 114, 1463-1470 (2004).
91. Wang, G.S. & Cooper, T.A. Splicing in disease: disruption of the splicing code and the decoding machinery. Nat. Rev. Genet. 8, 749-761 (2007).
92. Blencowe, B.J. Alternative splicing: new insights from global analyses. Cell 126, 37-47 (2006).
93. Kim, Y.K. & Kim, V.N. Processing of intronic microRNAs. EMBO J. 26, 775-783 (2007).
94. Bayne, E.H. et al. Splicing factors facilitate RNAi-directed silencing in fission yeast. Science 322, 602-606 (2008).
95. Hirose, T., Shu, M.D. & Steitz, J.A. Splicing-dependent and -independent modes of assembly for intron-encoded box C/D snoRNPs in mammalian cells. Mol. Cell 12, 113-123 (2003).
96. Kataoka, N., Fujita, M. & Ohno, M. Functional association of the Microprocessor complex with the spliceosome. Mol. Cell. Biol. 29, 3243-3254 (2009).
97. Lee, K.H. et al. Induction of a ribotoxic stress response that stimulates stress-activated protein kinases by 13-deoxytedanolide, an antitumor marine macrolide. Biosci. Biotechnol. Biochem. 70, 161-171 (2006).