Oxidative stress-responsive intracellular regulation specific for the angiostatic form of human tryptophanyl-tRNA synthetase

Biochemistry

Volumn 44, Issue 1, 2005, Pages 225-232

  Wakasugi, Keisuke ^a,b   Nakano, Tomomi ^b   Morishima, Isao ^a  

^a KYOTO UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CELLS; ENZYMES; MONOMERS; MUTAGENESIS; OXIDATION; SYNTHESIS (CHEMICAL);

AMINOACYLATION POTENTIAL; FULL-LENGTH PROTEINS; HUMAN CELLS; INTRACELLULAR REGULATION;

RNA;

AMMONIA; ANGIOSTATIC PROTEIN; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; TRYPTOPHAN TRANSFER RNA LIGASE;

AMINOACYLATION; ARTICLE; HUMAN; INTRACELLULAR MEMBRANE; MUTAGENESIS; OXIDATION; OXIDATIVE STRESS; PRIORITY JOURNAL;

ALTERNATIVE SPLICING; BINDING SITES; ERYTHROCYTES; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASES; HUMANS; MODELS, MOLECULAR; OXIDATIVE STRESS; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; SEQUENCE DELETION; TRYPTOPHAN-TRNA LIGASE;

EID: 11844305571     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi048313k     Document Type: Article

References (62)

1. Garret, M., Pajot, B., Trézéguet, V., Labouesse, J., Merle, M., Gandar, J.-C., Benedetto, J.-P., Sallafranque, M.-L., Alterio, J., Gueguen, M., Sarger, C., Labouesse, B., and Bonnet, J. (1991) A mammalian tryptophanyl-tRNA synthetase shows little homology to prokaryotic synthetases but near identity with mammalian peptide chain release factor. Biochemistry 30, 7809-7817.
2. Frolova, L. Y., Grigorieva, A. Y., Sudomoina, M. A., and Kisselev, L. L. (1993) The human gene encoding tryptophanyl-tRNA synthetase: Interferon-response elements and exon-intron organization, Gene 128, 237-245.
3. Shiba, K. (2002) Intron positions delineate the evolutionary path of a pervasively appended peptide in five human aminoacyl-tRNA synthetases, J. Mol. Evol. 55, 727-733.
4. Raben, N., Nichols, R., Dohlman, J., McPhie, P., Sridhar, V., Hyde, C., Leff, R., and Plotz, P. (1994) A motif in human histidyl-tRNA synthetase which is shared among several aminoacyl-tRNA synthetases is a coiled-coil that is essential for enzymatic activity and contains the major autoantigenic epitope, J. Biol. Chem. 269, 24277-24283.
5. Cahuzac, B., Berthonneau, E., Birlirakis, N., Guittet, E., and Mirande, M. (2000) A recurrent RNA-binding domain is appended to eukaryotic aminoacyl-tRNA synthetases. EMBO J. 19, 445-452.
6. Jeong, E.-J., Hwang, G.-S., Kim, K. H., Kim, M. J., Kim, S., and Kim, K.-S. (2000) Structural analysis of multifunctional peptide motifs in human bifunctional tRNA synthetase: Identification of RNA-binding residues and functional implications for tandem repeats. Biochemistry 39, 15775-15782.
7. Kaminska, M., Shalak, V., and Mirande, M. (2001) The appended C-domain of human methionyl-tRNA synthetase has a tRNA-sequestering function, Biochemistry 40, 14309-14316.
8. Yang, X.-L., Otero, F. J., Skene, R. J., McRee, D. E., Schimmel, P., and Ribas de Pouplana, L. (2003) Crystal structures that suggest late development of genetic code components for differentiating aromatic side chains. Proc. Natl. Acad. Sci. U.S.A. 100, 15376-15380.
9. Kise, Y., Lee. S. W., Park, S. G., Fukai, S., Sengoku, T., Ishii, R., Yokoyama, S., Kim, S., and Nureki, O. (2004) A short peptide insertion crucial for angiostatic activity of human tryptophanyl-tRNA synthetase, Nat. Struct. Mol. Biol. 11, 149-156.
10. Yu, Y., Liu, Y., Shen. N., Xu, X., Xu, F., Jia, J., Jin, Y., Arnold, E., and Ding, J. (2004) Crystal structure of human tryptophanyl-tRNA synthetase catalytic fragment: Insights into substrate recognition, tRNA binding, and angiogenesis activity, J. Biol. Chem. 279, 8378-8388.
11. Yang, X.-L., Schimmel, P., and Ewalt, K. L. (2004) Relationship of two human tRNA synthetases used in cell signaling, Trends Biochem. Sci. 29, 250-256.
12. Tolstrup, A. B., Bejder, A., Fleckner, J., and Justesen, J. (1995) Transcriptional regulation of the interferon-γ-inducible tryptophanyl-tRNA synthetase includes alternative splicing, J. Biol. Chem. 270, 397-403.
13. Turpaev, K. T., Zakhariev, V. M., Sokolova, I. V., Narovlyansky, A. N., Amchenkova, A. M., Justesen, J., and Frolova, L. Y. (1996) Alternative processing of the tryptophanyl-tRNA synthetase mRNA from interferon-treated human cells, Eur. J. Biochem. 240, 732-737.
14. Shaw, A. C., Larsen, M. R., Roepstorff, P., Justesen, J., Christiansen, G., and Birkelund, S. (1999) Mapping and identification of interferon γ-regulated HeLa cell proteins separated by immobilized pH gradient two-dimensional gel electrophoresis, Electrophoresis 20, 984-993.
15. Kisselev, L., Frolova, L., and Haenni, A.-L. (1993) Interferon inducibility of mammalian tryptophanyl-tRNA synthetase: New perspectives. Trends Biochem. Sci. 18, 263-267.
16. Fleckner, J., Martensen, P. M., Tolstrup, A. B., Kjeldgaard, N. O., and Justesen, J. (1995) Differential regulation of the human, interferon inducible tryptophanyl-tRNA synthetase by various cytokines in cell lines, Cytokine 7, 70-77.
17. Wakasugi, K., Slike, B. M., Hood, J., Otani, A., Ewalt, K. L., Friedlander, M., Cheresh, D. A., and Schimmel, P. (2002) A human aminoacyl-tRNA synthetase as a regulator of angiogenesis. Proc. Natl. Acad. Sci. U.S.A. 99, 173-177.
18. Filonenko, V. V., Beresten, S. F., Rubikaite, B. I., and Kisselev, L. L. (1989) Bovine tryptophanyl-tRNA synthetase and glyceraldehyde-3-phosphate dehydrogenase from a complex, Biochem. Biophys. Res. Commun. 161, 481-488.
19. Eaton, P., Byers, H. L., Leeds, N., Ward, M. A., and Shattock, M. J. (2002) Detection, quantitation, purification, and identification of cardiac proteins S-thiolated during ischemia and reperfusion, J. Biol. Chem. 277, 9806-9811.
20. Little, C., and O'Brien, P. J. (1969) Mechanism of peroxide-inactivation of the sulphydryl enzyme glyceraldehyde-3-phosphate dehydrogenase, Eur. J. Biochem. 10, 533-538.
21. Schmalhausen, E. V., Nagradova, N. K., Boschi-Muller, S., Branlant, G., and Muronetz, V. I. (1999) Mildly oxidized GAPDH: The coupling of the dehydrogenase and acyl phosphatase activities, FEBS Lett. 452, 219-222.
22. Molina y Vedia, L., McDonald, B., Reep, B., Brüne, B., Di Silvio, M., Billiar, T. R., and Lapetina, E. G. (1992) Nitric oxide-induced S-nitrosylation of glyceraldehyde-3-phosphate dehydrogenase inhibits enzymatic activity and increases endogenous ADP-ribosylation, J. Biol. Chem. 267, 24929-24932.
23. Mohr, S., Hallak, H., de Boitte, A., Lapetina, E. G., and Brüne, B. (1999) Nitric oxide-induced S-glutathionylation and inactivation of glyceraldehyde-3-phosphate dehydrogenase, J. Biol. Chem. 274, 9427-9430.
24. Ravichandran, V., Seres, T., Moriguchi, T., Thomas, J. A., and Johnston. R. B., Jr. (1994) S-Thiolation of glyceraldehyde-3-phosphate dehydrogenase induced by the phagocytosis-associated respiratory burst in blood monocytes, J. Biol. Chem. 269, 25010-25015.
25. Singh, R., and Green, M. R. (1993) Sequence-specific binding of transfer RNA by glyceraldehyde-3-phosphate dehydrogenase, Science 259, 365-368.
26. Arutyunova, E. I., Danshina, P. V., Domnina, L. V., Pleten, A. P., and Muronetz, V. I. (2003) Oxidation of glyceraldehyde-3-phosphate dehydrogenase enhances its binding to nucleic acids, Biochem. Biophys. Res. Commun. 307, 547-552.
27. Varadarajan, R., Lambright, D. G., and Boxer, S. G. (1989) Electrostatic interactions in wild-type and mutant recombinant human myoglobins, Biochemistry 28, 3771-3781.
28. Kisselev, L. L., Favorova, O. O., Nurbekov, M. K., Dmitriyenko, S. G., and Engelhardt, W. A. (1981) Bovine tryptophanyl-tRNA synthetase. A zinc metalloenzyme, Eur. J. Biochem. 120, 511-517.
29. Johnson, J. D., Spellmann, J. M., White, K. H., Barr, K. K., and John, T. R. (2002) Human tryptophanyl-tRNA synthetase can efficiently complement the Saccharomyces cerevisiae homologue, Wrs1P, FEMS Microbiol. Lett. 216, 111-115.
30. Go, M. (1981) Correlation of DNA exonic regions with protein structural units in haemoglobin, Nature 291, 90-92.
31. Go, M. (1983) Modular structural units, exons, and function in chicken lysozyme, Proc. Natl. Acad. Sci. U.S.A. 80, 1964-1968.
32. Ercolani, L., Florence, B., Denaro, M., and Alexander, M. (1988) Isolation and complete sequence of a functional human glyceraldehyde-3-phosphate dehydrogenase gene. J. Biol. Chem. 263, 15335-15341.
33. Kersanach, R., Brinkmann, H., Liaud, M.-F., Zhang, D.-X., Martin, W., and Cerff, R. (1994) Five identical intron positions in ancient duplicated genes of eubacterial origin. Nature 367, 387-389.
34. Long, M., De Souza, S. J., Rosenberg, C., and Gilbert, W. (1996) Exon shuffling and the origin of the mitochondrial targeting function in plant cytochrome c1 precursor. Proc. Natl. Acad. Sci. U.S.A. 93, 7727-7731.
35. Gilbert, W. (1978) Why genes in pieces? Nature 271, 501.
36. Blake. C. C. (1979) Exons encode protein functional units, Nature 277, 598.
37. Wakasugi, K., Ishimori, K., Imai, K., Wada, Y., and Morishima, I. (1994) "Module" substitution in hemoglobin subunits: Preparation and characterization of a "chimera βα-subunit". J. Biol. Chem. 269, 18750-18756.
38. Wakasugi, K., Quinn. C. L., Tao, N., and Schimmel, P. (1998) Genetic code in evolution: Switching species-specific aminoacylation with a peptide transplant, EMBO J. 17, 297-305.
39. +-binding region (Rossmann fold), J. Biol. Chem. 270, 2755-2763.
40. Mercer, W. D., Winn, S. I., and Watson, H. C. (1976) Twinning in crystals of human skeletal muscle D-glyceraldehyde-3-phosphate dehydrogenase, J. Mol. Biol. 104, 277-283.
41. Biro, J., Fabry, S., Dietmaier, W., Bogedain, C., and Hensel, R. (1990) Engineering thermostability in archaebacterial glyceraldehyde-3-phosphate dehydrogenase. Hints for the important role of interdomain contacts in stabilizing protein conformation, FEBS Lett. 275, 130-134.
42. Wakasugi, K., Ishimori, K., and Morishima, I. (1997) "Module"- substituted globins: Artificial exon shuffling among myoglobin, hemoglobin α- and β-subunits, Biophys. Chem. 68, 265-273.
43. Wakasugi, K., Nakano, T., and Morishima, I. (2003) Oxidized human neuroglobin as a heterotrimeric Gα protein guanine nucleotide dissociation inhibitor, J. Biol. Chem. 278, 36505-36512.
44. Wakasugi, K., Nakano, T., Kitatsuji, C., and Morishima, I. (2004) Human neuroglobin interacts with flotillin-1, a lipid raft microdomain-associated protein. Biochem. Biophys. Res. Commun. 318, 453-460.
45. Wakasugi, K., Nakano, T., and Morishima, I. (2004) Association of human neuroglobin with cystatin C, a cysteine proteinase inhibitor, Biochemistry 43, 5119-5125.
46. Ovádi, J., Telegdi, M., Batke, J., and Keleti, T. (1971) Functional non-identity of subunits and isolation of active dimers of D-glyceraldehyde-3-phosphate dehydrogenase. Eur. J. Biochem. 22, 430-438.
47. +-binding fold of glyceraldehyde-3-phosphate dehydrogenase as a novel RNA-binding domain, Biochem. Biophys. Res. Commun. 275, 253-260.
48. Kim, J. H., Lee, S., Park, J. B., Lee, S. D., Kim, J. H., Ha, S. H., Hasumi, K., Endo, A., Suh, P.-G., and Ryu, S. H. (2003) Hydrogen peroxide induces association between glyceraldehyde 3-phosphate dehydrogenase and phospholipase D2 to facilitate phospholipase D2 in PC12 cells, J. Neurochem. 85, 1228-1236.
49. Chihade, J. W., and Schimmel, P. (1999) Assembly of a catalytic unit for RNA microhelix aminoacylation using nonspecific RNA binding domains, Proc. Natl. Acad. Sci. U.S.A. 96, 12316-12321.
50. Kaminska, M., Deniziak, M., Kerjan, P., Barciszewski, J., and Mirande, M. (2000) A recurrent general RNA binding domain appended to plant methionyl-tRNA synthetase acts as a cis-acting cofactor for aminoacylation, EMBO J. 19, 6908-6917.
51. Wang, C.-C., and Schimmel. P. (1999) Species barrier to RNA recognition overcome with nonspecific RNA binding domains, J. Biol. Chem. 274. 16508-16512.
52. Simos, G., Sauer, A., Fasiolo, F., and Hurt, E. C. (1998) A conserved domain with Arclp delivers tRNA to aminoacyl-tRNA synthetases, Mol. Cell 1, 235-242.
53. Park, S. G., Jung, K. H., Lee. J. S., Jo, Y. J., Motegi, H., Kim, S., and Shiba, K. (1999) Precursor of pro-apoptotic cytokine modulates aminoacylation activity of tRNA synthetase. J. Biol. Chem. 274, 16673-16676.
54. Deinert, K., Fasiolo, F., Hurt, E. C., and Simos, G. (2001) Arc1p organizes the yeast aminoacyl-tRNA synthetase complex and stabilizes its interaction with the cognate tRNAs, J. Biol. Chem. 276, 6000-6008.
55. Zuniga, R., Salazar, J., Canales, M., and Orellana, O. (2002) A dispensable peptide from Acidithiobacillus ferrooxidans tryptophanyl-tRNA synthetase affects tRNA binding, FEBS Lett. 532, 387-390.
56. Krause, S. W., Rehli, M., Kreutz, M., Schwarzfischer, L., Paulauskis, J. D., and Andreesen, R. (1996) Differential screening identifies genetic markers of monocyte to macrophage maturation, J. Leukocyte Biol. 60, 540-545.
57. Matsunaga, T., Ishida, T., Takekawa, M., Nishimura, S., Adachi, M., and Imai, K. (2002) Analysis of gene expression during maturation of immature dendritic cells derived from peripheral blood monocytes, Scand. J. Immunol. 56, 593-601.
58. Xue, H., and Wong, J. T.-F. (1995) Interferon induction of human tryptophanyl-tRNA synthetase safeguards the synthesis of tryptophan-rich immune-system proteins: A hypothesis, Gene 165, 335-339.
59. Boehm. U., Klamp, T., Groot, M., and Howard, J. C. (1997) Cellular responses to interferon-γ, Annu. Rev. Immunol. 15, 749-795.
60. Schroder, K., Hertzog, P. J., Ravasi, T., and Hume, D. A. (2004) Interferon-γ: An overview of signals, mechanisms and functions. J. Leukocyte Biol. 75, 163-189.
61. Paley, E. L., Baranov, V. N., Alexandrova, N. M., and Kisselev, L. L. (1991) Tryptophanyl-tRNA synthetase in cell lines resistant to tryptophan analogs. Exp. Cell Res. 195, 66-78.
62. Kantengwa, S., Jornot, L., Devenoges, C., and Nicod, L. P. (2003) Superoxide anions induce the maturation of human dendritic cells, Am. J. Crit. Care Med. 167, 431-437.