Building arks for tRNA: Structure and function of the Arc1p family of non-catalytic tRNA-binding proteins

FEBS Letters

Volumn 584, Issue 18, 2010, Pages 3842-3849

  Karanasios, Eleftherios ^a,c   Simos, George ^a,b  

^a UNIVERSITY OF THESSALY   (Greece)

^b INSTITUTE OF HUMAN PERFORMANCE AND REHABILITATION   (Greece)

^c ADDENBROOKE S HOSPITAL   (United Kingdom)

Author keywords

Arc1p; P18; P38; P43; Trbp111; TRNA

Indexed keywords

AMINO ACID TRANSFER RNA LIGASE; FUNGAL PROTEIN; PROTEIN ARC1P; PROTEIN P18; PROTEIN P43; PROTEIN TRBP111; RNA BINDING PROTEIN; SYNAPTOPHYSIN; TRANSFER RNA; UNCLASSIFIED DRUG; ARC1 PROTEIN, S CEREVISIAE; BACTERIAL PROTEIN; CYTOKINE; SACCHAROMYCES CEREVISIAE PROTEIN; SMALL INDUCIBLE CYTOKINE SUBFAMILY E, MEMBER 1; TRANS-ACTIVATION RESPONSIVE RNA-BINDING PROTEIN; TRBP111 PROTEIN, AQUIFEX AEOLICUS; TUMOR PROTEIN;

AMINOACYLATION; CELL STRUCTURE; CELLULAR DISTRIBUTION; EUKARYOTE; HUMAN; MOLECULAR BIOLOGY; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROKARYOTE; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; PROTEIN STRUCTURE; REVIEW; RNA TRANSPORT; SEQUENCE HOMOLOGY; CHEMISTRY; METABOLISM; PROTEIN CONFORMATION;

BACTERIAL PROTEINS; CYTOKINES; HUMANS; NEOPLASM PROTEINS; PROTEIN CONFORMATION; RNA, TRANSFER; RNA-BINDING PROTEINS; SACCHAROMYCES CEREVISIAE PROTEINS; TRANSFER RNA AMINOACYLATION;

EUKARYOTA; PROKARYOTA;

EID: 77956916364     PISSN: 00145793     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.febslet.2010.08.023     Document Type: Review

References (58)

1. Crick F. Central dogma of molecular biology. Nature 1970, 227:561-563.
2. Wolin S.L., Matera A.G. The trials and travels of tRNA. Genes Dev. 1999, 13:1-10.
3. Hopper A.K., Pai D.A., Engelke D.R. Cellular dynamics of tRNAs and their genes. FEBS Lett. 2010, 584:310-317.
4. Hausmann C.D., Ibba M. Aminoacyl-tRNA synthetase complexes: molecular multitasking revealed. FEMS Microbiol. Rev. 2008, 32:705-721.
5. Guo M., Schimmel P., Yang X.L. Functional expansion of human tRNA synthetases achieved by structural inventions. FEBS Lett. 2010, 584:434-442.
6. Mirande M. Processivity of translation in the eukaryote cell: role of aminoacyl-tRNA synthetases. FEBS Lett. 2010, 584:443-447.
7. Simos G., Segref A., Fasiolo F., Hellmuth K., Shevchenko A., Mann M., Hurt E.C. The yeast protein Arc1p binds to tRNA and functions as a cofactor for the methionyl- and glutamyl-tRNA synthetases. EMBO J. 1996, 15:5437-5448.
8. Simos G., Tekotte H., Grosjean H., Segref A., Sharma K., Tollervey D., Hurt E.C. Nuclear pore proteins are involved in the biogenesis of functional tRNA. EMBO J. 1996, 15:2270-2284.
9. Hellmuth K., Lau D.M., Bischoff F.R., Kunzler M., Hurt E., Simos G. Yeast Los1p has properties of an exportin-like nucleocytoplasmic transport factor for tRNA. Mol. Cell. Biol. 1998, 18:6374-6386.
10. Mirande M., Cirakoglu B., Waller J.P. Macromolecular complexes from sheep and rabbit containing seven aminoacyl-tRNA synthetases. III. Assignment of aminoacyl-tRNA synthetase activities to the polypeptide components of the complexes. J. Biol. Chem. 1982, 257:11056-11063.
11. Deinert K., Fasiolo F., Hurt E.C., Simos G. Arc1p organizes the yeast aminoacyl-tRNA synthetase complex and stabilizes its interaction with the cognate tRNAs. J. Biol. Chem. 2001, 276:6000-6008.
12. Galani K., Grosshans H., Deinert K., Hurt E.C., Simos G. The intracellular location of two aminoacyl-tRNA synthetases depends on complex formation with Arc1p. EMBO J. 2001, 20:6889-6898.
13. Quevillon S., Mirande M. The p18 component of the multisynthetase complex shares a protein motif with the beta and gamma subunits of eukaryotic elongation factor 1. FEBS Lett. 1996, 395:63-67.
14. Simos G., Sauer A., Fasiolo F., Hurt E.C. A conserved domain within Arc1p delivers tRNA to aminoacyl-tRNA synthetases. Mol. Cell 1998, 1:235-242.
15. Simader H., Hothorn M., Kohler C., Basquin J., Simos G., Suck D. Structural basis of yeast aminoacyl-tRNA synthetase complex formation revealed by crystal structures of two binary sub-complexes. Nucleic Acids Res. 2006, 34:3968-3979.
16. Kao J., et al. Characterization of a novel tumor-derived cytokine. Endothelial-monocyte activating polypeptide II. J. Biol. Chem. 1994, 269:25106-25119.
17. Quevillon S., Agou F., Robinson J.C., Mirande M. The p43 component of the mammalian multi-synthetase complex is likely to be the precursor of the endothelial monocyte-activating polypeptide II cytokine. J. Biol. Chem. 1997, 272:32573-32579.
18. Kaminska M., Deniziak M., Kerjan P., Barciszewski J., Mirande M. A recurrent general RNA binding domain appended to plant methionyl-tRNA synthetase acts as a cis-acting cofactor for aminoacylation. EMBO J. 2000, 19:6908-6917.
19. Morales A.J., Swairjo M.A., Schimmel P. Structure-specific tRNA-binding protein from the extreme thermophile Aquifex aeolicus. EMBO J. 1999, 18:3475-3483.
20. Frantz J.D., Gilbert W. A novel yeast gene product, G4p1, with a specific affinity for quadruplex nucleic acids. J. Biol. Chem. 1995, 270:20692-20697.
21. Swairjo M.A., Morales A.J., Wang C.C., Ortiz A.R., Schimmel P. Crystal structure of trbp111: a structure-specific tRNA-binding protein. EMBO J. 2000, 19:6287-6298.
22. Nomanbhoy T., Morales A.J., Abraham A.T., Vortler C.S., Giege R., Schimmel P. Simultaneous binding of two proteins to opposite sides of a single transfer RNA. Nat. Struct. Biol. 2001, 8:344-348.
23. Shalak V., Kaminska M., Mitnacht-Kraus R., Vandenabeele P., Clauss M., Mirande M. The EMAPII cytokine is released from the mammalian multisynthetase complex after cleavage of its p43/proEMAPII component. J. Biol. Chem. 2001, 276:23769-23776.
24. Shalak V., Guigou L., Kaminska M., Wautier M.P., Wautier J.L., Mirande M. Characterization of p43(ARF), a derivative of the p43 component of multiaminoacyl-tRNA synthetase complex released during apoptosis. J. Biol. Chem. 2007, 282:10935-10943.
25. Kim Y., Shin J., Li R., Cheong C., Kim K., Kim S. A novel anti-tumor cytokine contains an RNA binding motif present in aminoacyl-tRNA synthetases. J. Biol. Chem. 2000, 275:27062-27068.
26. Renault L., et al. Structure of the EMAPII domain of human aminoacyl-tRNA synthetase complex reveals evolutionary dimer mimicry. EMBO J. 2001, 20:570-578.
27. Kawaguchi S., Muller J., Linde D., Kuramitsu S., Shibata T., Inoue Y., Vassylyev D.G., Yokoyama S. The crystal structure of the ttCsaA protein: an export-related chaperone from Thermus thermophilus. EMBO J. 2001, 20:562-569.
28. Walter P., Weygand-Durasevic I., Sanni A., Ebel J.P., Fasiolo F. Deletion analysis in the amino-terminal extension of methionyl-tRNA synthetase from Saccharomyces cerevisiae shows that a small region is important for the activity and stability of the enzyme. J. Biol. Chem. 1989, 264:17126-17130.
29. Karanasios E., Simader H., Panayotou G., Suck D., Simos G. Molecular determinants of the yeast Arc1p-aminoacyl-tRNA synthetase complex assembly. J. Mol. Biol. 2007, 374:1077-1090.
30. Simader H., Suck D. Expression, purification, crystallization and preliminary phasing of the heteromerization domain of the tRNA-export and aminoacylation cofactor Arc1p from yeast. Acta Crystallogr., Sect. F: Struct. Biol. Cryst. Commun. 2006, 62:346-349.
31. Simader H., Hothorn M., Suck D. Structures of the interacting domains from yeast glutamyl-tRNA synthetase and tRNA-aminoacylation and nuclear-export cofactor Arc1p reveal a novel function for an old fold. Acta Crystallogr., Sect. F: Struct. Biol. Cryst. Commun. 2006, 62:1510-1519.
32. Park S.G., Ewalt K.L., Kim S. Functional expansion of aminoacyl-tRNA synthetases and their interacting factors: new perspectives on housekeepers. Trends Biochem. Sci. 2005, 30:569-574.
33. Kim K.J., et al. Determination of three-dimensional structure and residues of the novel tumor suppressor AIMP3/p18 required for the interaction with ATM. J. Biol. Chem. 2008, 283:14032-14040.
34. Quevillon S., Robinson J.C., Berthonneau E., Siatecka M., Mirande M. Macromolecular assemblage of aminoacyl-tRNA synthetases: identification of protein-protein interactions and characterization of a core protein. J. Mol. Biol. 1999, 285:183-195.
35. Kaminska M., Havrylenko S., Decottignies P., Gillet S., Le Marechal P., Negrutskii B., Mirande M. Dissection of the structural organization of the aminoacyl-tRNA synthetase complex. J. Biol. Chem. 2009, 284:6053-6060.
36. Kaminska M., Shalak V., Mirande M. The appended C-domain of human methionyl-tRNA synthetase has a tRNA-sequestering function. Biochemistry 2001, 40:14309-14316.
37. Cahuzac B., Berthonneau E., Birlirakis N., Guittet E., Mirande M. A recurrent RNA-binding domain is appended to eukaryotic aminoacyl-tRNA synthetases. EMBO J. 2000, 19:445-452.
38. Robinson J.C., Kerjan P., Mirande M. Macromolecular assemblage of aminoacyl-tRNA synthetases: quantitative analysis of protein-protein interactions and mechanism of complex assembly. J. Mol. Biol. 2000, 304:983-994.
39. Ahn H.C., Kim S., Lee B.J. Solution structure and p43 binding of the p38 leucine zipper motif: coiled-coil interactions mediate the association between p38 and p43. FEBS Lett. 2003, 542:119-124.
40. Kim J.Y., Kang Y.S., Lee J.W., Kim H.J., Ahn Y.H., Park H., Ko Y.G., Kim S. P38 is essential for the assembly and stability of macromolecular tRNA synthetase complex: implications for its physiological significance. Proc. Natl Acad. Sci. USA 2002, 99:7912-7916.
41. Francin M., Kaminska M., Kerjan P., Mirande M. The N-terminal domain of mammalian Lysyl-tRNA synthetase is a functional tRNA-binding domain. J. Biol. Chem. 2002, 277:1762-1769.
42. Frugier M., Moulinier L., Giege R. A domain in the N-terminal extension of class IIb eukaryotic aminoacyl-tRNA synthetases is important for tRNA binding. EMBO J. 2000, 19:2371-2380.
43. Park S.G., Jung K.H., Lee J.S., Jo Y.J., Motegi H., Kim S., Shiba K. Precursor of pro-apoptotic cytokine modulates aminoacylation activity of tRNA synthetase. J. Biol. Chem. 1999, 274:16673-16676.
44. Graindorge J.S., Senger B., Tritch D., Simos G., Fasiolo F. Role of Arc1p in the modulation of yeast glutamyl-tRNA synthetase activity. Biochemistry 2005, 44:1344-1352.
45. Kushiro T., Schimmel P. Trbp111 selectively binds a noncovalently assembled tRNA-like structure. Proc. Natl Acad. Sci. USA 2002, 99:16631-16635.
46. Karanasios E., Boleti H., Simos G. Incorporation of the Arc1p tRNA-binding domain to the catalytic core of MetRS can functionally replace the yeast Arc1p-MetRS complex. J. Mol. Biol. 2008, 381:763-771.
47. Guigou L., Shalak V., Mirande M. The tRNA-interacting factor p43 associates with mammalian arginyl-tRNA synthetase but does not modify its tRNA aminoacylation properties. Biochemistry 2004, 43:4592-4600.
48. Golinelli-Cohen M.P., Zakrzewska A., Mirande M. Complementation of yeast Arc1p by the p43 component of the human multisynthetase complex does not require its association with yeast MetRS and GluRS. J. Mol. Biol. 2004, 340:15-27.
49. Grosshans H., Hurt E., Simos G. An aminoacylation-dependent nuclear tRNA export pathway in yeast. Genes Dev. 2000, 14:830-840.
50. Murthi A., Shaheen H.H., Huang H.Y., Preston M.A., Lai T.P., Phizicky E.M., Hopper A.K. Regulation of tRNA bidirectional nuclear-cytoplasmic trafficking in Saccharomyces cerevisiae. Mol. Biol. Cell 2010, 21:639-649.
51. Hopper A.K., Shaheen H.H. A decade of surprises for tRNA nuclear-cytoplasmic dynamics. Trends Cell Biol. 2008, 18:98-104.
52. Simos G., Grosshans H., Hurt E. Nuclear export of tRNA. Results Probl. Cell Differ. 2002, 35:115-131.
53. Steiner-Mosonyi M., Mangroo D. The nuclear tRNA aminoacylation-dependent pathway may be the principal route used to export tRNA from the nucleus in Saccharomyces cerevisiae. Biochem. J. 2004, 378:809-816.
54. Galani K., Hurt E., Simos G. The tRNA aminoacylation co-factor Arc1p is excluded from the nucleus by an Xpo1p-dependent mechanism. FEBS Lett. 2005, 579:969-975.
55. Kaminska M., Havrylenko S., Decottignies P., Le Marechal P., Negrutskii B., Mirande M. Dynamic organization of aminoacyl-tRNA synthetase complexes in the cytoplasm of human cells. J. Biol. Chem. 2009, 284:13746-13754.
56. Frechin M., Senger B., Braye M., Kern D., Martin R.P., Becker H.D. Yeast mitochondrial Gln-tRNA(Gln) is generated by a GatFAB-mediated transamidation pathway involving Arc1p-controlled subcellular sorting of cytosolic GluRS. Genes Dev. 2009, 23:1119-1130.
57. Rinehart J., Krett B., Rubio M.A., Alfonzo J.D., Soll D. Saccharomyces cerevisiae imports the cytosolic pathway for Gln-tRNA synthesis into the mitochondrion. Genes Dev. 2005, 19:583-592.
58. Frechin M., Kern D., Martin R.P., Becker H.D., Senger B. Arc1p: anchoring, routing, coordinating. FEBS Lett. 2010, 584:427-433.