Roles of helicases in translation initiation: A mechanistic view

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1829, Issue 8, 2013, Pages 799-809

  Marintchev, Assen ^a  

^a BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

DEAD box; DExH box; RNA helicase; Translation; Translation initiation factor

Indexed keywords

ADENOSINE TRIPHOSPHATE; DDX3 PROTEIN; DED1 PROTEIN; DHX29 PROTEIN; GUANOSINE TRIPHOSPHATE; HELICASE; INITIATION FACTOR 4A; INITIATION FACTOR 4B; MESSENGER RNA; UBIQUITIN; UNCLASSIFIED DRUG; VASA PROTEIN;

5' UNTRANSLATED REGION; HYDROLYSIS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; REGULATORY MECHANISM; REVIEW; RNA BINDING; RNA STRUCTURE; RNA TRANSLATION; TRANSLATION INITIATION; YEAST;

ANIMALS; EUKARYOTIC INITIATION FACTOR-4A; EUKARYOTIC INITIATION FACTOR-4F; HUMANS; PEPTIDE CHAIN INITIATION, TRANSLATIONAL; PROTEIN BIOSYNTHESIS; RNA HELICASES; RNA, MESSENGER; YEASTS;

EID: 84877923058     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2013.01.005     Document Type: Review

References (100)

1. Hinnebusch A.G., Lorsch J.R. The mechanism of eukaryotic translation initiation: new insights and challenges. Cold Spring Harb. Perspect. Biol. 2012, 4. (Epub ahead of print).
2. Jackson R.J., Hellen C.U., Pestova T.V. The mechanism of eukaryotic translation initiation and principles of its regulation. Nat. Rev. Mol. Cell Biol. 2010, 11:113-127.
3. Marintchev A., Wagner G. Translation initiation: structures, mechanisms and evolution. Q. Rev. Biophys. 2004, 37:197-284.
4. Sonenberg N., Hinnebusch A.G. Regulation of translation initiation in eukaryotes: mechanisms and biological targets. Cell 2009, 136:731-745.
5. Berthelot K., Muldoon M., Rajkowitsch L., Hughes J., McCarthy J.E. Dynamics and processivity of 40S ribosome scanning on mRNA in yeast. Mol. Microbiol. 2004, 51:987-1001.
6. Abaeva I.S., Marintchev A., Pisareva V.P., Hellen C.U., Pestova T.V. Bypassing of stems versus linear base-by-base inspection of mammalian mRNAs during ribosomal scanning. EMBO J. 2011, 30:115-129.
7. Parsyan A., Shahbazian D., Martineau Y., Petroulakis E., Alain T., Larsson O., Mathonnet G., Tettweiler G., Hellen C.U., Pestova T.V., Svitkin Y.V., Sonenberg N. The helicase protein DHX29 promotes translation initiation, cell proliferation, and tumorigenesis. Proc. Natl. Acad. Sci. U. S. A. 2009, 106:22217-22222.
8. Pisareva V.P., Pisarev A.V., Komar A.A., Hellen C.U., Pestova T.V. Translation initiation on mammalian mRNAs with structured 5'UTRs requires DExH-box protein DHX29. Cell 2008, 135:1237-1250.
9. Parsyan A., Svitkin Y., Shahbazian D., Gkogkas C., Lasko P., Merrick W.C., Sonenberg N. mRNA helicases: the tacticians of translational control. Nat. Rev. Mol. Cell Biol. 2011, 12:235-245.
10. Linder P., Jankowsky E. From unwinding to clamping - the DEAD box RNA helicase family. Nat. Rev. Mol. Cell Biol. 2011, 12:505-516.
11. Andreou A.Z., Klostermeier D. The DEAD-box helicase eIF4A: paradigm or the odd one out?. RNA Biol. 2012, 10. (Epub ahead of print).
12. Minshall N., Kress M., Weil D., Standart N. Role of p54 RNA helicase activity and its C-terminal domain in translational repression, P-body localization and assembly. Mol. Biol. Cell 2009, 20:2464-2472.
13. Coller J., Parker R. General translational repression by activators of mRNA decapping. Cell 2005, 122:875-886.
14. Fischer N., Weis K. The DEAD box protein Dhh1 stimulates the decapping enzyme Dcp1. EMBO J. 2002, 21:2788-2797.
15. Carrera P., Johnstone O., Nakamura A., Casanova J., Jackle H., Lasko P. VASA mediates translation through interaction with a Drosophila yIF2 homolog. Mol. Cell 2000, 5:181-187.
16. Johnstone O., Lasko P. Interaction with eIF5B is essential for Vasa function during development. Development 2004, 131:4167-4178.
17. Liang L., Diehl-Jones W., Lasko P. Localization of Vasa protein to the Drosophila pole plasm is independent of its RNA-binding and helicase activities. Development 1994, 120:1201-1211.
18. Liu N., Han H., Lasko P. Vasa promotes Drosophila germline stem cell differentiation by activating mei-P26 translation by directly interacting with a (U)-rich motif in its 3' UTR. Genes Dev. 2009, 23:2742-2752.
19. Bolinger C., Sharma A., Singh D., Yu L., Boris-Lawrie K. RNA helicase A modulates translation of HIV-1 and infectivity of progeny virions. Nucleic Acids Res. 2010, 38:1686-1696.
20. Ranji A., Shkriabai N., Kvaratskhelia M., Musier-Forsyth K., Boris-Lawrie K. Features of double-stranded RNA-binding domains of RNA helicase A are necessary for selective recognition and translation of complex mRNAs. J. Biol. Chem. 2011, 286:5328-5337.
21. Short J.D., Pfarr C.M. Translational regulation of the JunD messenger RNA. J. Biol. Chem. 2002, 277:32697-32705.
22. Hartman T.R., Qian S., Bolinger C., Fernandez S., Schoenberg D.R., Boris-Lawrie K. RNA helicase A is necessary for translation of selected messenger RNAs. Nat. Struct. Mol. Biol. 2006, 13:509-516.
23. Leroy P., Alzari P., Sassoon D., Wolgemuth D., Fellous M. The protein encoded by a murine male germ cell-specific transcript is a putative ATP-dependent RNA helicase. Cell 1989, 57:549-559.
24. Chuang R.Y., Weaver P.L., Liu Z., Chang T.H. Requirement of the DEAD-Box protein ded1p for messenger RNA translation. Science 1997, 275:1468-1471.
25. de la Cruz J., Iost I., Kressler D., Linder P. The p20 and Ded1 proteins have antagonistic roles in eIF4E-dependent translation in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:5201-5206.
26. Iost I., Dreyfus M., Linder P. Ded1p, a DEAD-box protein required for translation initiation in Saccharomyces cerevisiae, is an RNA helicase. J. Biol. Chem. 1999, 274:17677-17683.
27. Lai M.C., Lee Y.H., Tarn W.Y. The DEAD-box RNA helicase DDX3 associates with export messenger ribonucleoproteins as well as tip-associated protein and participates in translational control. Mol. Biol. Cell 2008, 19:3847-3858.
28. Lee C.S., Dias A.P., Jedrychowski M., Patel A.H., Hsu J.L., Reed R. Human DDX3 functions in translation and interacts with the translation initiation factor eIF3. Nucleic Acids Res. 2008, 36:4708-4718.
29. Shih J.W., Tsai T.Y., Chao C.H., Lee Y.H.Wu. Candidate tumor suppressor DDX3 RNA helicase specifically represses cap-dependent translation by acting as an eIF4E inhibitory protein. Oncogene 2008, 27:700-714.
30. Hilliker A., Gao Z., Jankowsky E., Parker R. The DEAD-box protein Ded1 modulates translation by the formation and resolution of an eIF4F-mRNA complex. Mol. Cell 2011, 43:962-972.
31. Nakajima T., Uchida C., Anderson S.F., Lee C.G., Hurwitz J., Parvin J.D., Montminy M. RNA helicase A mediates association of CBP with RNA polymerase II. Cell 1997, 90:1107-1112.
32. Anderson S.F., Schlegel B.P., Nakajima T., Wolpin E.S., Parvin J.D. BRCA1 protein is linked to the RNA polymerase II holoenzyme complex via RNA helicase A. Nat. Genet. 1998, 19:254-256.
33. Gatfield D., Le Hir H., Schmitt C., Braun I.C., Kocher T., Wilm M., Izaurralde E. The DExH/D box protein HEL/UAP56 is essential for mRNA nuclear export in Drosophila. Curr. Biol. 2001, 11:1716-1721.
34. Yedavalli V.S., Neuveut C., Chi Y.H., Kleiman L., Jeang K.T. Requirement of DDX3 DEAD box RNA helicase for HIV-1 Rev-RRE export function. Cell 2004, 119:381-392.
35. Schroder M., Baran M., Bowie A.G. Viral targeting of DEAD box protein 3 reveals its role in TBK1/IKKepsilon-mediated IRF activation. EMBO J. 2008, 27:2147-2157.
36. Yajima M., Wessel G.M. The multiple hats of Vasa: its functions in the germline and in cell cycle progression. Mol. Reprod. Dev. 2011, 78:861-867.
37. Henn A., Bradley M.J., De La Cruz E.M. ATP utilization and RNA conformational rearrangement by DEAD-box proteins. Annu. Rev. Biophys. 2012, 41:247-267.
38. Byrd A.K., Raney K.D. Superfamily 2 helicases. Front. Biosci. 2012, 17:2070-2088.
39. Gorbalenya A.E., Koonin E.V., Donchenko A.P., Blinov V.M. Two related superfamilies of putative helicases involved in replication, recombination, repair and expression of DNA and RNA genomes. Nucleic Acids Res. 1989, 17:4713-4730.
40. Linder P., Lasko P.F., Ashburner M., Leroy P., Nielsen P.J., Nishi K., Schnier J., Slonimski P.P. Birth of the D-E-A-D box. Nature 1989, 337:121-122.
41. Rogers G.W., Richter N.J., Merrick W.C. Biochemical and kinetic characterization of the RNA helicase activity of eukaryotic initiation factor 4A. J. Biol. Chem. 1999, 274:12236-12244.
42. Sengoku T., Nureki O., Nakamura A., Kobayashi S., Yokoyama S. Structural basis for RNA unwinding by the DEAD-box protein Drosophila Vasa. Cell 2006, 125:287-300.
43. Yang Q., Del Campo M., Lambowitz A.M., Jankowsky E. DEAD-box proteins unwind duplexes by local strand separation. Mol. Cell 2007, 28:253-263.
44. Yang Q., Jankowsky E. The DEAD-box protein Ded1 unwinds RNA duplexes by a mode distinct from translocating helicases. Nat. Struct. Mol. Biol. 2006, 13:981-986.
45. Chen Y., Potratz J.P., Tijerina P., Del Campo M., Lambowitz A.M., Russell R. DEAD-box proteins can completely separate an RNA duplex using a single ATP. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:20203-20208.
46. Liu F., Putnam A., Jankowsky E. ATP hydrolysis is required for DEAD-box protein recycling but not for duplex unwinding. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:20209-20214.
47. Henn A., Cao W., Licciardello N., Heitkamp S.E., Hackney D.D., De La Cruz E.M. Pathway of ATP utilization and duplex rRNA unwinding by the DEAD-box helicase, DbpA. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:4046-4050.
48. Oberer M., Marintchev A., Wagner G. Structural basis for the enhancement of eIF4A helicase activity by eIF4G. Genes Dev. 2005, 19:2212-2223.
49. Abramson R.D., Dever T.E., Lawson T.G., Ray B.K., Thach R.E., Merrick W.C. The ATP-dependent interaction of eukaryotic initiation factors with mRNA. J. Biol. Chem. 1987, 262:3826-3832.
50. Abramson R.D., Dever T.E., Merrick W.C. Biochemical evidence supporting a mechanism for cap-independent and internal initiation of eukaryotic mRNA. J. Biol. Chem. 1988, 263:6016-6019.
51. Bi X., Ren J., Goss D.J. Wheat germ translation initiation factor eIF4B affects eIF4A and eIFiso4F helicase activity by increasing the ATP binding affinity of eIF4A. Biochemistry 2000, 39:5758-5765.
52. Marintchev A., Edmonds K.A., Marintcheva B., Hendrickson E., Oberer M., Suzuki C., Herdy B., Sonenberg N., Wagner G. Topology and regulation of the human eIF4A/4G/4H helicase complex in translation initiation. Cell 2009, 136:447-460.
53. Nielsen K.H., Behrens M.A., He Y., Oliveira C.L., Jensen L.S., Hoffmann S.V., Pedersen J.S., Andersen G.R. Synergistic activation of eIF4A by eIF4B and eIF4G. Nucleic Acids Res. 2011, 39:2678-2689.
54. Rozovsky N., Butterworth A.C., Moore M.J. Interactions between eIF4AI and its accessory factors eIF4B and eIF4H. RNA 2008, 14:2136-2148.
55. Loh P.G., Yang H.S., Walsh M.A., Wang Q., Wang X., Cheng Z., Liu D., Song H. Structural basis for translational inhibition by the tumour suppressor Pdcd4. EMBO J. 2009, 28:274-285.
56. Suzuki C., Garces R.G., Edmonds K.A., Hiller S., Hyberts S.G., Marintchev A., Wagner G. PDCD4 inhibits translation initiation by binding to eIF4A using both its MA3 domains. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:3274-3279.
57. Mayberry L.K., Allen M.L., Dennis M.D., Browning K.S. Evidence for variation in the optimal translation initiation complex: plant eIF4B, eIF4F, and eIF(iso)4F differentially promote translation of mRNAs. Plant Physiol. 2009, 150:1844-1854.
58. Rajagopal V., Park E.H., Hinnebusch A.G., Lorsch J.R. Specific domains in yeast translation initiation factor eIF4G strongly bias RNA unwinding activity of the eIF4F complex toward duplexes with 5'-overhangs. J. Biol. Chem. 2012, 287:20301-20312.
59. Sun Y., Atas E., Lindqvist L., Sonenberg N., Pelletier J., Meller A. The eukaryotic initiation factor eIF4H facilitates loop-binding, repetitive RNA unwinding by the eIF4A DEAD-box helicase. Nucleic Acids Res. 2012, 40:6199-6207.
60. Chase J.W., Williams K.R. Single-stranded DNA binding proteins required for DNA replication. Annu. Rev. Biochem. 1986, 55:103-136.
61. Darnell J.C., Jensen K.B., Jin P., Brown V., Warren S.T., Darnell R.B. Fragile X mental retardation protein targets G quartet mRNAs important for neuronal function. Cell 2001, 107:489-499.
62. Zanotti K.J., Lackey P.E., Evans G.L., Mihailescu M.R. Thermodynamics of the fragile X mental retardation protein RGG box interactions with G quartet forming RNA. Biochemistry 2006, 45:8319-8330.
63. Dhote V., Sweeney T.R., Kim N., Hellen C.U., Pestova T.V. Roles of individual domains in the function of DHX29, an essential factor required for translation of structured mammalian mRNAs. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:E3150-E3159.
64. Hodge C.A., Tran E.J., Noble K.N., Alcazar-Roman A.R., Ben-Yishay R., Scarcelli J.J., Folkmann A.W., Shav-Tal Y., Wente S.R., Cole C.N. The Dbp5 cycle at the nuclear pore complex during mRNA export I: dbp5 mutants with defects in RNA binding and ATP hydrolysis define key steps for Nup159 and Gle1. Genes Dev. 2011, 25:1052-1064.
65. Montpetit B., Thomsen N.D., Helmke K.J., Seeliger M.A., Berger J.M., Weis K. A conserved mechanism of DEAD-box ATPase activation by nucleoporins and InsP6 in mRNA export. Nature 2011, 472:238-242.
66. Noble K.N., Tran E.J., Alcazar-Roman A.R., Hodge C.A., Cole C.N., Wente S.R. The Dbp5 cycle at the nuclear pore complex during mRNA export II: nucleotide cycling and mRNP remodeling by Dbp5 are controlled by Nup159 and Gle1. Genes Dev. 2012, 25:1065-1077.
67. Hilbert M., Kebbel F., Gubaev A., Klostermeier D. eIF4G stimulates the activity of the DEAD box protein eIF4A by a conformational guidance mechanism. Nucleic Acids Res. 2011, 39:2260-2270.
68. Ballut L., Marchadier B., Baguet A., Tomasetto C., Seraphin B., Le Hir H. The exon junction core complex is locked onto RNA by inhibition of eIF4AIII ATPase activity. Nat. Struct. Mol. Biol. 2005, 12:861-869.
69. Le Hir H., Izaurralde E., Maquat L.E., Moore M.J. The spliceosome deposits multiple proteins 20-24 nucleotides upstream of mRNA exon-exon junctions. EMBO J. 2000, 19:6860-6869.
70. Lorsch J.R., Herschlag D. The DEAD box protein eIF4A. 1. A minimal kinetic and thermodynamic framework reveals coupled binding of RNA and nucleotide. Biochemistry 1998, 37:2180-2193.
71. Rozen F., Edery I., Meerovitch K., Dever T.E., Merrick W.C., Sonenberg N. Bidirectional RNA helicase activity of eucaryotic translation initiation factors 4A and 4F. Mol. Cell. Biol. 1990, 10:1134-1144.
72. Soto-Rifo R., Rubilar P.S., Limousin T., de Breyne S., Decimo D., Ohlmann T. DEAD-box protein DDX3 associates with eIF4F to promote translation of selected mRNAs. EMBO J. 2012, 31:3745-3756.
73. Siridechadilok B., Fraser C.S., Hall R.J., Doudna J.A., Nogales E. Structural roles for human translation factor eIF3 in initiation of protein synthesis. Science 2005, 310:1513-1515.
74. Spirin A.S. How does a scanning ribosomal particle move along the 5'-untranslated region of eukaryotic mRNA? Brownian ratchet model. Biochemistry 2009, 48:10688-10692.
75. Walker S.E., Zhou F., Mitchell S.F., Larson V.S., Valasek L., Hinnebusch A.G., Lorsch J.R. Yeast eIF4B binds to the head of the 40S ribosomal subunit and promotes mRNA recruitment through its N-terminal and internal repeat domains. RNA 2013, 19:191-207.
76. Methot N., Pickett G., Keene J.D., Sonenberg N. In vitro RNA selection identifies RNA ligands that specifically bind to eukaryotic translation initiation factor 4B: the role of the RNA remotif. RNA 1996, 2:38-50.
77. Jin J., Jing W., Lei X.X., Feng C., Peng S., Boris-Lawrie K., Huang Y. Evidence that Lin28 stimulates translation by recruiting RNA helicase A to polysomes. Nucleic Acids Res. 2011, 39:3724-3734.
78. Manojlovic Z., Stefanovic B. A novel role of RNA helicase A in regulation of translation of type I collagen mRNAs. RNA 2012, 18:321-334.
79. Gibson T.J., Thompson J.D. Detection of dsRNA-binding domains in RNA helicase A and Drosophila maleless: implications for monomeric RNA helicases. Nucleic Acids Res. 1994, 22:2552-2556.
80. Styhler S., Nakamura A., Swan A., Suter B., Lasko P. Vasa is required for GURKEN accumulation in the oocyte, and is involved in oocyte differentiation and germline cyst development. Development 1998, 125:1569-1578.
81. Breitwieser W., Markussen F.H., Horstmann H., Ephrussi A. Oskar protein interaction with Vasa represents an essential step in polar granule assembly. Genes Dev. 1996, 10:2179-2188.
82. Beckham C., Hilliker A., Cziko A.M., Noueiry A., Ramaswami M., Parker R. The DEAD-box RNA helicase Ded1p affects and accumulates in Saccharomyces cerevisiae P-bodies. Mol. Biol. Cell 2008, 19:984-993.
83. Geissler R., Golbik R.P., Behrens S.E. The DEAD-box helicase DDX3 supports the assembly of functional 80S ribosomes. Nucleic Acids Res. 2012, 40:4998-5011.
84. Jamieson D.J., Beggs J.D. A suppressor of yeast spp 81/ded1 mutations encodes a very similar putative ATP-dependent RNA helicase. Mol. Microbiol. 1991, 5:805-812.
85. von der Haar T., McCarthy J.E. Intracellular translation initiation factor levels in Saccharomyces cerevisiae and their role in cap-complex function. Mol. Microbiol. 2002, 46:531-544.
86. Hinnebusch A.G. Molecular mechanism of scanning and start codon selection in eukaryotes. Microbiol. Mol. Biol. Rev. 2011, 75:434-467.
87. Choi S.K., Lee J.H., Zoll W.L., Merrick W.C., Dever T.E. Promotion of met-tRNAiMet binding to ribosomes by yIF2, a bacterial IF2 homolog in yeast. Science 1998, 280:1757-1760.
88. Pestova T.V., Kolupaeva V.G. The roles of individual eukaryotic translation initiation factors in ribosomal scanning and initiation codon selection. Genes Dev. 2002, 16:2906-2922.
89. Ariumi Y., Kuroki M., Abe K., Dansako H., Ikeda M., Wakita T., Kato N. DDX3 DEAD-box RNA helicase is required for hepatitis C virus RNA replication. J. Virol. 2007, 81:13922-13926.
90. Noueiry A.O., Chen J., Ahlquist P. A mutant allele of essential, general translation initiation factor DED1 selectively inhibits translation of a viral mRNA. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:12985-12990.
91. Randall G., Panis M., Cooper J.D., Tellinghuisen T.L., Sukhodolets K.E., Pfeffer S., Landthaler M., Landgraf P., Kan S., Lindenbach B.D., Chien M., Weir D.B., Russo J.J., Ju J., Brownstein M.J., Sheridan R., Sander C., Zavolan M., Tuschl T., Rice C.M. Cellular cofactors affecting hepatitis C virus infection and replication. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:12884-12889.
92. Thoreen C.C., Chantranupong L., Keys H.R., Wang T., Gray N.S., Sabatini D.M. A unifying model for mTORC1-mediated regulation of mRNA translation. Nature 2012, 485:109-113.
93. Pisarev A.V., Unbehaun A., Hellen C.U., Pestova T.V. Assembly and analysis of eukaryotic translation initiation complexes. Methods Enzymol. 2007, 430:147-177.
94. Yoder-Hill J., Pause A., Sonenberg N., Merrick W.C. The p46 subunit of eukaryotic initiation factor (eIF)-4F exchanges with eIF-4A. J. Biol. Chem. 1993, 268:5566-5573.
95. Pause A., Methot N., Svitkin Y., Merrick W.C., Sonenberg N. Dominant negative mutants of mammalian translation initiation factor eIF-4A define a critical role for eIF-4F in cap-dependent and cap-independent initiation of translation. EMBO J. 1994, 13:1205-1215.
96. Ivanov I.P., Loughran G., Sachs M.S., Atkins J.F. Initiation context modulates autoregulation of eukaryotic translation initiation factor 1 (eIF1). Proc. Natl. Acad. Sci. U. S. A. 2010, 107:18056-18060.
97. Loughran G., Sachs M.S., Atkins J.F., Ivanov I.P. Stringency of start codon selection modulates autoregulation of translation initiation factor eIF5. Nucleic Acids Res. 2012, 40:2898-2906.
98. Martin-Marcos P., Cheung Y.N., Hinnebusch A.G. Functional elements in initiation factors 1, 1A, and 2beta discriminate against poor AUG context and non-AUG start codons. Mol. Cell. Biol. 2011, 31:4814-4831.
99. Petrelli D., LaTeana A., Garofalo C., Spurio R., Pon C.L., Gualerzi C.O. Translation initiation factor IF3: two domains, five functions, one mechanism?. EMBO J. 2001, 20:4560-4569.
100. Yu Y., Abaeva I.S., Marintchev A., Pestova T.V., Hellen C.U. Common conformational changes induced in type 2 picornavirus IRESs by cognate trans-acting factors. Nucleic Acids Res. 2011, 39:4851-4865.