Postage for the messenger: Designating routes for nuclear mRNA export

Trends in Cell Biology

Volumn 23, Issue 8, 2013, Pages 365-373

  Natalizio, Barbara J ^a   Wente, Susan R ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Exportin; Lamin; MRNA export; Nuclear envelope; Nuclear pore complex; Transport

Indexed keywords

CIS ACTING ELEMENT; MESSENGER RNA; RNA BINDING PROTEIN; RNA POLYMERASE II; TRANS ACTING FACTOR;

CELL NUCLEUS MEMBRANE; CONFORMATIONAL TRANSITION; ENVIRONMENTAL FACTOR; NONHUMAN; NUCLEAR EXPORT SIGNAL; NUCLEAR PORE COMPLEX; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; RNA PROCESSING; RNA SEQUENCE; RNA TRANSCRIPTION; RNA TRANSPORT; SACCHAROMYCES CEREVISIAE; SIGNAL TRANSDUCTION;

EXPORTIN; LAMIN; MRNA EXPORT; NUCLEAR ENVELOPE; NUCLEAR PORE COMPLEX; TRANSPORT;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL NUCLEUS; DISEASE; HUMANS; RNA TRANSPORT; RNA, MESSENGER; STRESS, PHYSIOLOGICAL;

EID: 84880964277     PISSN: 09628924     EISSN: 18793088     Source Type: Journal    
DOI: 10.1016/j.tcb.2013.03.006     Document Type: Review

References (90)

1. Hetzer M.W. The nuclear envelope. Cold Spring Harb. Perspect. Biol. 2010, 2:a000539.
2. Hocine S., et al. RNA processing and export. Cold Spring Harb. Perspect. Biol. 2010, 2:a000752.
3. Moore M.J., Proudfoot N.J. Pre-mRNA processing reaches back to transcription and ahead to translation. Cell 2009, 136:688-700.
4. Van de Vosse D.W., et al. Role of the nuclear envelope in genome organization and gene expression. Wiley Interdiscip. Rev. Syst. Biol. Med. 2011, 3:147-166.
5. Antonin W., et al. Traversing the NPC along the pore membrane: targeting of membrane proteins to the INM. Nucleus 2011, 2:87-91.
6. Guttinger S., et al. Orchestrating nuclear envelope disassembly and reassembly during mitosis. Nat. Rev. Mol. Cell Biol. 2009, 10:178-191.
7. Starr D.A., Fridolfsson H.N. Interactions between nuclei and the cytoskeleton are mediated by SUN-KASH nuclear-envelope bridges. Annu. Rev. Cell Dev. Biol. 2010, 26:421-444.
8. Dechat T., et al. Nuclear lamins. Cold Spring Harb. Perspect. Biol. 2010, 2:a000547.
9. Gerace L., Huber M.D. Nuclear lamina at the crossroads of the cytoplasm and nucleus. J. Struct. Biol. 2012, 177:24-31.
10. Capelson M., et al. Nuclear pore complexes: guardians of the nuclear genome. Cold Spring Harb. Symp. Quant. Biol. 2010, 75:585-597.
11. Aitchison J.D., Rout M.P. The yeast nuclear pore complex and transport through it. Genetics 2012, 190:855-883.
12. Grossman E., et al. Functional architecture of the nuclear pore complex. Annu. Rev. Biophys. 2012, 41:557-584.
13. Guttler T., Gorlich D. Ran-dependent nuclear export mediators: a structural perspective. EMBO J. 2011, 30:3457-3474.
14. Speese S.D., et al. Nuclear envelope budding enables large ribonucleoprotein particle export during synaptic Wnt signaling. Cell 2012, 149:832-846.
15. Rodriguez-Navarro S., Hurt E. Linking gene regulation to mRNA production and export. Curr. Opin. Cell Biol. 2011, 23:302-309.
16. Kelly S.M., Corbett A.H. Messenger RNA export from the nucleus: a series of molecular wardrobe changes. Traffic 2009, 10:1199-1208.
17. Fornerod M., et al. CRM1 is an export receptor for leucine-rich nuclear export signals. Cell 1997, 90:1051-1060.
18. Stade K., et al. Exportin 1 (Crm1p) is an essential nuclear export factor. Cell 1997, 90:1041-1050.
19. Gruter P., et al. TAP, the human homolog of Mex67p, mediates CTE-dependent RNA export from the nucleus. Mol. Cell 1998, 1:649-659.
20. Segref A., et al. Mex67p, a novel factor for nuclear mRNA export, binds to both poly(A)+ RNA and nuclear pores. EMBO J. 1997, 16:3256-3271.
21. Hutten S., Kehlenbach R.H. CRM1-mediated nuclear export: to the pore and beyond. Trends Cell Biol. 2007, 17:193-201.
22. Galy V., et al. Nuclear retention of unspliced mRNAs in yeast is mediated by perinuclear Mlp1. Cell 2004, 116:63-73.
23. Iglesias N., et al. Ubiquitin-mediated mRNP dynamics and surveillance prior to budding yeast mRNA export. Genes Dev. 2010, 24:1927-1938.
24. Stutz F., et al. REF, an evolutionary conserved family of hnRNP-like proteins, interacts with TAP/Mex67p and participates in mRNA nuclear export. RNA 2000, 6:638-650.
25. Strasser K., Hurt E. Yra1p, a conserved nuclear RNA-binding protein, interacts directly with Mex67p and is required for mRNA export. EMBO J. 2000, 19:410-420.
26. Zenklusen D., et al. The yeast hnRNP-Like proteins Yra1p and Yra2p participate in mRNA export through interaction with Mex67p. Mol. Cell. Biol. 2001, 21:4219-4232.
27. Cullen B.R. Nuclear mRNA export: insights from virology. Trends Biochem. Sci. 2003, 28:419-424.
28. Terry L.J., Wente S.R. Nuclear mRNA export requires specific FG nucleoporins for translocation through the nuclear pore complex. J. Cell Biol. 2007, 178:1121-1132.
29. Strasser K., et al. Binding of the Mex67p/Mtr2p heterodimer to FXFG, GLFG, and FG repeat nucleoporins is essential for nuclear mRNA export. J. Cell Biol. 2000, 150:695-706.
30. Strawn L.A., et al. The GLFG regions of Nup116p and Nup100p serve as binding sites for both Kap95p and Mex67p at the nuclear pore complex. J. Biol. Chem. 2001, 276:6445-6452.
31. Oka M., et al. The mobile FG nucleoporin Nup98 is a cofactor for Crm1-dependent protein export. Mol. Biol. Cell 2010, 21:1885-1896.
32. Terry L.J., Wente S.R. Flexible gates: dynamic topologies and functions for FG nucleoporins in nucleocytoplasmic transport. Eukaryot. Cell 2009, 8:1814-1827.
33. Mor A., et al. Dynamics of single mRNP nucleocytoplasmic transport and export through the nuclear pore in living cells. Nat. Cell Biol. 2010, 12:543-552.
34. Grunwald D., Singer R.H. In vivo imaging of labelled endogenous beta-actin mRNA during nucleocytoplasmic transport. Nature 2010, 467:604-607.
35. Folkmann A.W., et al. Dbp5, Gle1-IP6 and Nup159: a working model for mRNP export. Nucleus 2011, 2:540-548.
36. Alcazar-Roman A.R., et al. Inositol hexakisphosphate and Gle1 activate the DEAD-box protein Dbp5 for nuclear mRNA export. Nat. Cell Biol. 2006, 8:711-716.
37. Weirich C.S., et al. Activation of the DExD/H-box protein Dbp5 by the nuclear-pore protein Gle1 and its coactivator InsP6 is required for mRNA export. Nat. Cell Biol. 2006, 8:668-676.
38. Snay-Hodge C.A., et al. Dbp5p/Rat8p is a yeast nuclear pore-associated DEAD-box protein essential for RNA export. EMBO J. 1998, 17:2663-2676.
39. Schmitt C., et al. Dbp5, a DEAD-box protein required for mRNA export, is recruited to the cytoplasmic fibrils of nuclear pore complex via a conserved interaction with CAN/Nup159p. EMBO J. 1999, 18:4332-4347.
40. Montpetit B., et al. A conserved mechanism of DEAD-box ATPase activation by nucleoporins and InsP6 in mRNA export. Nature 2011, 472:238-242.
41. Noble K.N., et al. 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. 2011, 25:1065-1077.
42. Hodge C.A., et al. 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.
43. Tran E.J., et al. The DEAD-box protein Dbp5 controls mRNA export by triggering specific RNA:protein remodeling events. Mol. Cell 2007, 28:850-859.
44. Bernad R., et al. Nup358/RanBP2 attaches to the nuclear pore complex via association with Nup88 and Nup214/CAN and plays a supporting role in CRM1-mediated nuclear protein export. Mol. Cell. Biol. 2004, 24:2373-2384.
45. Bachi A., et al. The C-terminal domain of TAP interacts with the nuclear pore complex and promotes export of specific CTE-bearing RNA substrates. RNA 2000, 6:136-158.
46. Cook A.G., et al. Structures of the tRNA export factor in the nuclear and cytosolic states. Nature 2009, 461:60-65.
47. Okada C., et al. A high-resolution structure of the pre-microRNA nuclear export machinery. Science 2009, 326:1275-1279.
48. Topisirovic I., et al. Molecular dissection of the eukaryotic initiation factor 4E (eIF4E) export-competent RNP. EMBO J. 2009, 28:1087-1098.
49. Culjkovic B., et al. eIF4E is a central node of an RNA regulon that governs cellular proliferation. J. Cell Biol. 2006, 175:415-426.
50. Brennan C.M., et al. Protein ligands to HuR modulate its interaction with target mRNAs in vivo. J. Cell Biol. 2000, 151:1-14.
51. Yang J., et al. Two closely related human nuclear export factors utilize entirely distinct export pathways. Mol. Cell 2001, 8:397-406.
52. Carmody S.R., et al. The mitogen-activated protein kinase Slt2 regulates nuclear retention of non-heat shock mRNAs during heat shock-induced stress. Mol. Cell. Biol. 2010, 30:5168-5179.
53. Strasser K., Hurt E. Splicing factor Sub2p is required for nuclear mRNA export through its interaction with Yra1p. Nature 2001, 413:648-652.
54. Lee M.S., et al. A protein that shuttles between the nucleus and the cytoplasm is an important mediator of RNA export. Genes Dev. 1996, 10:1233-1246.
55. Tutucci E., Stutz F. Keeping mRNPs in check during assembly and nuclear export. Nat. Rev. Mol. Cell Biol. 2011, 12:377-384.
56. Viphakone N., et al. TREX exposes the RNA-binding domain of Nxf1 to enable mRNA export. Nat. Commun. 2012, 3:1006.
57. Gilbert W., Guthrie C. The Glc7p nuclear phosphatase promotes mRNA export by facilitating association of Mex67p with mRNA. Mol. Cell 2004, 13:201-212.
58. Gilbert W., et al. Phosphorylation by Sky1p promotes Npl3p shuttling and mRNA dissociation. RNA 2001, 7:302-313.
59. Neville M., et al. The importin-beta family member Crm1p bridges the interaction between Rev and the nuclear pore complex during nuclear export. Curr. Biol. 1997, 7:767-775.
60. Verma D., et al. Epstein-Barr Virus SM protein utilizes cellular splicing factor SRp20 to mediate alternative splicing. J. Virol. 2010, 84:11781-11789.
61. Lindtner S., et al. RNA-binding motif protein 15 binds to the RNA transport element RTE and provides a direct link to the NXF1 export pathway. J. Biol. Chem. 2006, 281:36915-36928.
62. Legiewicz M., et al. The RNA transport element of the murine musD retrotransposon requires long-range intramolecular interactions for function. J. Biol. Chem. 2010, 285:42097-42104.
63. Palazzo A.F., Akef A. Nuclear export as a key arbiter of "mRNA identity" in eukaryotes. Biochim. Biophys. Acta 2012, 1819:566-577.
64. Saavedra C., et al. Regulation of mRNA export in response to stress in Saccharomyces cerevisiae. Genes Dev. 1996, 10:1608-1620.
65. McCloskey A., et al. hnRNP C tetramer measures RNA length to classify RNA polymerase II transcripts for export. Science 2012, 335:1643-1646.
66. Kohler A., Hurt E. Exporting RNA from the nucleus to the cytoplasm. Nat. Rev. Mol. Cell Biol. 2007, 8:761-773.
67. Ohno M., et al. PHAX, a mediator of U snRNA nuclear export whose activity is regulated by phosphorylation. Cell 2000, 101:187-198.
68. Mettenleiter T.C., et al. The way out: what we know and do not know about herpesvirus nuclear egress. Cell. Microbiol. 2012, 15:170-178.
69. Johnson D.C., Baines J.D. Herpesviruses remodel host membranes for virus egress. Nat. Rev. Microbiol. 2011, 9:382-394.
70. Morano K.A., et al. The response to heat shock and oxidative stress in Saccharomyces cerevisiae. Genetics 2012, 190:1157-1195.
71. Saavedra C.A., et al. Yeast heat shock mRNAs are exported through a distinct pathway defined by Rip1p. Genes Dev. 1997, 11:2845-2856.
72. Kendirgi F., et al. Interaction between the shuttling mRNA export factor Gle1 and the nucleoporin hCG1: a conserved mechanism in the export of Hsp70 mRNA. Mol. Biol. Cell 2005, 16:4304-4315.
73. Stutz F., et al. The yeast nucleoporin rip1p contributes to multiple export pathways with no essential role for its FG-repeat region. Genes Dev. 1997, 11:2857-2868.
74. Krebber H., et al. Uncoupling of the hnRNP Npl3p from mRNAs during the stress-induced block in mRNA export. Genes Dev. 1999, 13:1994-2004.
75. Rollenhagen C., et al. Following temperature stress, export of heat shock mRNA occurs efficiently in cells with mutations in genes normally important for mRNA export. Eukaryot. Cell 2007, 6:505-513.
76. von Roretz C., et al. Turnover of AU-rich-containing mRNAs during stress: a matter of survival. Wiley Interdiscip. Rev. RNA 2011, 2:336-347.
77. Siddiqui N., Borden K.L. mRNA export and cancer. Wiley Interdiscip. Rev. RNA 2012, 3:13-25.
78. Kohler A., Hurt E. Gene regulation by nucleoporins and links to cancer. Mol. Cell 2010, 38:6-15.
79. Borden K.L., Culjkovic-Kraljacic B. Ribavirin as an anti-cancer therapy: acute myeloid leukemia and beyond?. Leuk. Lymphoma 2010, 51:1805-1815.
80. Culjkovic-Kraljacic B., et al. The oncogene eIF4E reprograms the nuclear pore complex to promote mRNA export and oncogenic transformation. Cell Rep. 2012, 2:207-215.
81. Jao L.E., et al. A zebrafish model of lethal congenital contracture syndrome 1 reveals Gle1 function in spinal neural precursor survival and motor axon arborization. Development 2012, 139:1316-1326.
82. Santos-Rosa H., et al. Nuclear mRNA export requires complex formation between Mex67p and Mtr2p at the nuclear pores. Mol. Cell. Biol. 1998, 18:6826-6838.
83. Guzik B.W., et al. NXT1 (p15) is a crucial cellular cofactor in TAP-dependent export of intron-containing RNA in mammalian cells. Mol. Cell. Biol. 2001, 21:2545-2554.
84. Murphy R., Wente S.R. An RNA-export mediator with an essential nuclear export signal. Nature 1996, 383:357-360.
85. Hodge C.A., et al. Rat8p/Dbp5p is a shuttling transport factor that interacts with Rat7p/Nup159p and Gle1p and suppresses the mRNA export defect of xpo1-1 cells. EMBO J. 1999, 18:5778-5788.
86. Kraemer D.M., et al. The essential yeast nucleoporin NUP159 is located on the cytoplasmic side of the nuclear pore complex and serves in karyopherin-mediated binding of transport substrate. J. Biol. Chem. 1995, 270:19017-19021.
87. Tseng S.S., et al. Dbp5p, a cytosolic RNA helicase, is required for poly(A)+ RNA export. EMBO J. 1998, 17:2651-2662.
88. Hutten S., Kehlenbach R.H. Nup214 is required for CRM1-dependent nuclear protein export in vivo. Mol. Cell. Biol. 2006, 26:6772-6785.
89. Ataman B., et al. Rapid activity-dependent modifications in synaptic structure and function require bidirectional Wnt signaling. Neuron 2008, 57:705-718.
90. Mathew D., et al. Wingless signaling at synapses is through cleavage and nuclear import of receptor DFrizzled2. Science 2005, 310:1344-1347.