Insights into mRNA export-linked molecular mechanisms of human disease through a Gle1 structure-function analysis

Advances in Biological Regulation

Volumn 54, Issue 1, 2014, Pages 74-91

  Folkmann, Andrew W ^a   Dawson, T Renee ^a   Wente, Susan R ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLE1 PROTEIN, HUMAN; MESSENGER RNA; NUCLEOCYTOPLASMIC TRANSPORT PROTEIN;

ANIMAL; ARTHROGRYPOSIS; ARTICLE; CELL NUCLEUS; CHEMISTRY; GENETICS; HUMAN; METABOLISM; MOTOR NEURON DISEASE; RNA TRANSPORT;

ANIMALS; ARTHROGRYPOSIS; CELL NUCLEUS; HUMANS; MOTOR NEURON DISEASE; NUCLEOCYTOPLASMIC TRANSPORT PROTEINS; RNA TRANSPORT; RNA, MESSENGER;

EID: 84893385652     PISSN: 22124926     EISSN: None     Source Type: Book Series    
DOI: 10.1016/j.jbior.2013.10.002     Document Type: Article

References (57)

1. Al-Qattan M.M., Shamseldin H.E., Alkuraya F.S. Familial dorsalization of the skin of the proximal palm and the instep of the sole of the foot. Gene 2012, 500:216-219.
2. Alcazar-Roman A.R., Bolger T.A., Wente S.R. Control of mRNA export and translation termination by inositol hexakisphosphate requires specific interaction with Gle1. JBiol Chem 2010, 285:16683-16692.
3. Alcazar-Roman A.R., Tran E.J., Guo S., Wente S.R. Inositol hexakisphosphate and Gle1 activate the DEAD-box protein Dbp5 for nuclear mRNA export. Nat Cell Biol 2006, 8:711-716.
4. Ashkenazy H., Erez E., Martz E., Pupko T., Ben-Tal N. ConSurf 2010: calculating evolutionary conservation in sequence and structure of proteins and nucleic acids. Nucleic Acids Res 2010, 38:W529-W533.
5. 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.
6. Bolger T.A., Folkmann A.W., Tran E.J., Wente S.R. The mRNA export factor Gle1 and inositol hexakisphosphate regulate distinct stages of translation. Cell 2008, 134:624-633.
7. Bolger T.A., Wente S.R. Gle1 is a multifunctional DEAD-box protein regulator that modulates Ded1 in translation initiation. JBiol Chem 2011, 286:39750-39759.
8. Braud C., Zheng W., Xiao W. LONO1 encoding a nucleoporin is required for embryogenesis and seed viability in Arabidopsis. Plant Physiol 2012, 160:823-836.
9. Collins R., Karlberg T., Lehtio L., Schutz P., van den Berg S., Dahlgren L.G., et al. The DEXD/H-box RNA helicase DDX19 is regulated by an {alpha}-helical switch. JBiol Chem 2009, 284:10296-10300.
10. Cooper T.A., Wan L., Dreyfuss G. RNA and disease. Cell 2009, 136:777-793.
11. Folkmann A.W., Collier S.A., Zhan X., Aditi, Ohi M.D., Wente S.R. Gle1 functions during mRNA export in an oligomeric complex that is altered in human disease. Cell 2013, 155:582-593.
12. 6 and Nup159: a working model for mRNP export. Nucleus 2011, 2:540-548.
13. Glaser F., Pupko T., Paz I., Bell R.E., Bechor-Shental D., Martz E., et al. ConSurf: identification of functional regions in proteins by surface-mapping of phylogenetic information. Bioinforma 2003, 19:163-164.
14. Hall J.G. Genetic aspects of arthrogryposis. Clin Orthop Relat Res 1985, 44-53.
15. Herva R., Leisti J., Kirkinen P., Seppanen U. Alethal autosomal recessive syndrome of multiple congenital contractures. Am J Med Genet 1985, 20:431-439.
16. Hodge C.A., Tran E.J., Noble K.N., Alcazar-Roman A.R., Ben-Yishay R., Scarcelli J.J., 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.
17. Holm L., Park J. DaliLite workbench for protein structure comparison. Bioinforma 2000, 16:566-567.
18. Hurt J.A., Silver P.A. mRNA nuclear export and human disease. Dis Model Mech 2008, 1:103-108.
19. Jankowsky E. RNA helicases at work: binding and rearranging. Trends Biochem Sci 2011, 36:19-29.
20. Jankowsky E., Bowers H. Remodeling of ribonucleoprotein complexes with DExH/D RNA helicases. Nucleic Acids Res 2006, 34:4181-4188.
21. Jankowsky E., Fairman M.E. RNA helicases-one fold for many functions. Curr Opin Struct Biol 2007, 17:316-324.
22. Jao L.E., Appel B., Wente S.R. Azebrafish model of lethal congenital contracture syndrome 1 reveals Gle1 function in spinal neural precursor survival and motor axon arborization. Development 2012, 139:1316-1326.
23. Kelley L.A., Sternberg M.J. Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 2009, 4:363-371.
24. Kendirgi F., Barry D.M., Griffis E.R., Powers M.A., Wente S.R. An essential role for hGle1 nucleocytoplasmic shuttling in mRNA export. JCell Biol 2003, 160:1029-1040.
25. Kendirgi F., Rexer D.J., Alcazar-Roman A.R., Onishko H.M., Wente S.R. 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.
26. Korneeva N.L., First E.A., Benoit C.A., Rhoads R.E. Interaction between the NH2-terminal domain of eIF4A and the central domain of eIF4G modulates RNA-stimulated ATPase activity. JBiol Chem 2005, 280:1872-1881.
27. Landau M., Mayrose I., Rosenberg Y., Glaser F., Martz E., Pupko T., et al. ConSurf 2005: the projection of evolutionary conservation scores of residues on protein structures. Nucleic Acids Res 2005, 33:W299-W302.
28. Mallam A.L., Del Campo M., Gilman B., Sidote D.J., Lambowitz A.M. Structural basis for RNA-duplex recognition and unwinding by the DEAD-box helicase Mss116p. Nature 2012, 490:121-125.
29. Marcotrigiano J., Lomakin I.B., Sonenberg N., Pestova T.V., Hellen C.U., Burley S.K. Aconserved HEAT domain within eIF4G directs assembly of the translation initiation machinery. Mol Cell 2001, 7:193-203.
30. McKee A.E., Silver P.A. Systems perspectives on mRNA processing. Cell Res 2007, 17:581-590.
31. Miller A.L., Suntharalingam M., Johnson S.L., Audhya A., Emr S.D., Wente S.R. Cytoplasmic inositol hexakisphosphate production is sufficient for mediating the Gle1-mRNA export pathway. JBiol Chem 2004, 279:51022-51032.
32. von Moeller H., Basquin C., Conti E. The mRNA export protein DBP5 binds RNA and the cytoplasmic nucleoporin NUP214 in a mutually exclusive manner. Nat Struct Mol Biol 2009, 16:247-254.
33. Montpetit B., Thomsen N.D., Helmke K.J., Seeliger M.A., Berger J.M., Weis K. Aconserved mechanism of DEAD-box ATPase activation by nucleoporins and InsP6 in mRNA export. Nature 2011, 472:238-242.
34. Moon D., Bae J., Cho H., Yoon J. The fission yeast homologue of Glel is essential for growth and involved in mRNA expor. JMicrobiol 1998, 46:422-428.
35. Muller-McNicoll M., Neugebauer K.M. How cells get the message: dynamic assembly and function of mRNA-protein complexes. Nat Rev Genet 2013, 14:275-287.
36. Murphy R., Wente S.R. An RNA-export mediator with an essential nuclear export signal. Nature 1996, 383:357-360.
37. Nielsen K.H., Chamieh H., Andersen C.B., Fredslund F., Hamborg K., Le Hir H., et al. Mechanism of ATP turnover inhibition in the EJC. RNA 2009, 15:67-75.
38. 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 2011, 25:1065-1077.
39. Nousiainen H.O., Kestila M., Pakkasjarvi N., Honkala H., Kuure S., Tallila J., et al. Mutations in mRNA export mediator GLE1 result in a fetal motoneuron disease. Nat Genet 2008, 40:155-157.
40. Raboy V. Seeds for a better future: 'low phytate' grains help to overcome malnutrition and reduce pollution. Trends Plant Sci 2001, 6:458-462.
41. Rayala H.J., Kendirgi F., Barry D.M., Majerus P.W., Wente S.R. The mRNA export factor human Gle1 interacts with the nuclear pore complex protein Nup155. Mol Cell Proteomics 2004, 3:145-155.
42. Renoux A.J., Todd P.K. Neurodegeneration the RNA way. Prog Neurobiol 2012, 97:173-189.
43. Rocak S., Linder P. DEAD-box proteins: the driving forces behind RNA metabolism. Nat Rev Mol Cell Biol 2004, 5:232-241.
44. Rogers G.W., Richter N.J., Lima W.F., Merrick W.C. Modulation of the helicase activity of eIF4A by eIF4B, eIF4H, and eIF4F. JBiol Chem 2001, 276:30914-30922.
45. Schmitt C., von Kobbe C., Bachi A., Pante N., Rodrigues J.P., Boscheron 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.
46. Schutz P., Bumann M., Oberholzer A.E., Bieniossek C., Trachsel H., Altmann M., et al. Crystal structure of the yeast eIF4A-eIF4G complex: an RNA-helicase controlled by protein-protein interactions. Proc Natl Acad Sci USA 2008, 105:9564-9569.
47. Stewart M. Ratcheting mRNA out of the nucleus. Mol Cell 2007, 25:327-330.
48. Strahm Y., Fahrenkrog B., Zenklusen D., Rychner E., Kantor J., Rosbach M., et al. The RNA export factor Gle1p is located on the cytoplasmic fibrils of the NPC and physically interacts with the FG-nucleoporin Rip1p, the DEAD-box protein Rat8p/Dbp5p and a new protein Ymr 255p. EMBO J 1999, 18:5761-5777.
49. Stutz F., Kantor J., Zhang D., McCarthy T., Neville M., Rosbash M. The yeast nucleoporin rip1p contributes to multiple export pathways with no essential role for its FG-repeat region. Genes Dev 1997, 11:2857-2868.
50. Tran E.J., Zhou Y., Corbett A.H., Wente S.R. The DEAD-box protein Dbp5 controls mRNA export by triggering specific RNA:protein remodeling events. Mol Cell 2007, 28:850-859.
51. Valkov E., Dean J.C., Jani D., Kuhlmann S.I., Stewart M. Structural basis for the assembly and disassembly of mRNA nuclear export complexes. Biochim Biophys Acta 2012, 1819:578-592.
52. Vuopala K., Ignatius J., Herva R. Lethal arthrogryposis with anterior horn cell disease. Hum Pathol 1995, 26:12-19.
53. Watkins J.L., Murphy R., Emtage J.L., Wente S.R. The human homologue of Saccharomyces cerevisiae Gle1p is required for poly(A)+ RNA export. Proc Natl Acad Sci USA 1998, 95:6779-6784.
54. Weirich C.S., Erzberger J.P., Berger J.M., Weis K. The N-terminal domain of Nup159 forms a beta-propeller that functions in mRNA export by tethering the helicase Dbp5 to the nuclear pore. Mol Cell 2004, 16:749-760.
55. Weirich C.S., Erzberger J.P., Flick J.S., Berger J.M., Thorner J., Weis K. 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.
56. Wolf A., Krause-Gruszczynska M., Birkenmeier O., Ostareck-Lederer A., Huttelmaier S., Hatzfeld M. Plakophilin 1 stimulates translation by promoting eIF4A1 activity. JCell Biol 2010, 188:463-471.
57. Yang H.S., Jansen A.P., Komar A.A., Zheng X., Merrick W.C., Costes S., et al. The transformation suppressor Pdcd4 is a novel eukaryotic translation initiation factor 4A binding protein that inhibits translation. Mol Cell Biol 2003, 23:26-37.