Mutations Linked to Leukoencephalopathy with Vanishing White Matter Impair the Function of the Eukaryotic Initiation Factor 2B Complex in Diverse Ways

Molecular and Cellular Biology

Volumn 24, Issue 8, 2004, Pages 3295-3306

  Li, Wei ^a   Wang, Xuemin ^a   Van Der Knaap, Marjo S ^b   Proud, Christopher G ^a  

^a UNIVERSITY OF DUNDEE   (United Kingdom)

^b VU UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

GUANINE NUCLEOTIDE EXCHANGE FACTOR; MESSENGER RNA; PROTEIN SUBUNIT;

ARTICLE; BINDING AFFINITY; CATALYSIS; COMPLEX FORMATION; DEGENERATIVE DISEASE; DISEASE COURSE; DISEASE SEVERITY; FRAMESHIFT MUTATION; GENE MUTATION; HUMAN; HUMAN CELL; LEUKOENCEPHALOPATHY; LEUKOENCEPHALOPATHY WITH VANISHING WHITE MATTER; NUCLEOTIDE SEQUENCE; PHENOTYPE; POINT MUTATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; RNA TRANSLATION; TRANSLATION REGULATION; WHITE MATTER;

ANIMALS; BRAIN; BRAIN DISEASES; CELL LINE; EUKARYOTIC INITIATION FACTOR-2B; HUMANS; MACROMOLECULAR SUBSTANCES; MUTATION; NEURODEGENERATIVE DISEASES; PHENOTYPE; PROTEIN BINDING; PROTEIN SUBUNITS; RECOMBINANT FUSION PROTEINS;

EUKARYOTA;

EID: 1842453031     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.24.8.3295-3306.2004     Document Type: Article

References (40)

1. Asano, K., T. Krishnamoorthy, L. Phan, G. D. Pavitt, and A. G. Hinnebusch. 1999. Conserved bipartite motifs in yeast eIF5 and eIF2Bε GTPase-activating and GDP-GTP exchange factors in translation initiation, mediate binding to their common substrate eIF2. EMBO J. 18:1673-1688.
2. Bushman, J. L, A. I. Asuru, R. L. Matts, and A. G. Hinnebusch. 1993. Evidence that GCD6 and GCD7, translational regulators of GCN4, are subunits of the guanine nucleotide exchange factor for eIF-2 in Saccharomyces cerevisiae. Mol. Cell. Biol. 13:1920-1932.
3. Clemens, M. J. 2001. Initiation factor eIF2α phosphorylation in stress responses and apoptosis. Prog. Mol. Subcell. Biol. 27:57-89.
4. Colthurst, D. R., D. G. Campbell, and C. G. Proud. 1987. Structure and regulation of eukaryotic initiation factor eIF-2. Sequence of the site in the alpha subunit phosphorylated by the haem-controlled repressor and by the double-stranded RNA-activated inhibitor. Eur. J. Biochem. 166:357-363.
5. Craddock, B. L., and C. G. Proud. 1996. The α-subunit of mammalian initiation factor eIF-2B is essential for catalytic activity. Biochem. Biophys. Res. Commun. 220:843-847.
6. Fabian, J. R., S. R. Kimball, N. K. Heinzinger, and L. S. Jefferson. 1997. Subunit assembly and guanine nucleotide exchange factor activity of eukaryotic initiation factor eIF2B subunits expressed in Sf9 cells. J. Biol. Chem. 272:12359-12365.
7. Fogli, A., D. Rodriguez E. Eymard-Pierre, F. Boubour, P. Labauge, B. F. Meaney, S. Zeesman, C. R. Kaneski, B. Schiffmann, and O. Boespflug-Tanguy. 2003. Ovarian failure related to eukaryotic initiation factor 2B mutations. Am. J. Hum. Genet. 72:1544-1550.
8. Fogli, A., K. Wong, E. Eymard-Pierre, J. Wenger, J. P. Bouffard, E. Goldin, D. N. Black, O. Boespflug-Tanguy, and R. Schiffmann. 2002. Cree leukoencephalopathy and CACH/VWM disease are allelic at the EIF2B5 locus. Ann Neurol. 52:506-510.
9. Gomez, E., S. S. Mohammad, and G. D. Pavitt. 2002. Characterization of the minimal catalytic domain within eIF2B: the guanine-nucleotide exchange factor for translation initiation. EMBO J. 21:5292-5301.
10. Gomez, E., and G. D. Pavitt. 2000. Identification of domains and residues within the ε subunit of eukaryotic translation initiation factor 2B (eIF2Bε) required for guanine nucleotide exchange reveals a novel activation function promoted by eIF2B complex formation. Mol. Cell. Biol. 20:3965-3976.
11. Hall-Jackson. C. A., D. A. Cross, N. Morrice, and C. Smythe. 1999. ATR is a caffeine-sensitive, DNA-activated protein kinase with a substrate specificity distinct from DNA-PK. Oncogene 18:6707-6713.
12. Hanefeld, F., U. Holzbach, B. Kruse, E. Wilichowski, H. J. Christen, and J. Frahm. 1993. Diffuse white matter disease in three children: an encephalopathy with unique features on magnetic resonance imaging and proton magnetic resonance spectroscopy. Neuropediatrics 24:244-248.
13. Harding, H. P., I. Novoa, Y. Zhang, H. Zeng, R. Wek, M. Schapira, and D. Ron. 2000. Regulated translation initiation controls stress-induced gene expression in mammalian cells. Mol. Cell 6:1099-1108.
14. Harding, H. P., Y. Zhang, and D. Ron. 1999. Protein translation and folding are coupled by an endoplasmic-reticulum resident kinase. Nature 397:271-274.
15. Harding, H. P., Y. Zhang, H. Zeng, I. Novoa, P. D. Lu, M. Calfon, N. Sadri, C. Yun, B. Popko, R. Paules, D. F. Stojdl, J. C. Bell, T. Hettmann, J. M. Leiden, and D. Ron. 2003. An integrated stress response regulates amino acid metabolism and resistance to oxidative stress. Mol. Cell 11:619-633.
16. Hinnehusch, A. G. 2000. Mechanism and regulation of methionyl-tRNA binding to ribosomes, p. 185-243. In N. Sonenberg, J. W. B. Hershey, and M. B. Mathews (ed.), Translational control of gene expression. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
17. Jiang, H. Y., S. A. Wek, B. C. McGrath, D. Scheuner, R. J. Kaufman, D. R. Cavener, and R. C. Wek. 2003. Phosphoarylation of the α subunit of eukaryotic initiation factor 2 is required for activation of NF-κB in response to diverse cellular stresses. Mol. Cell. Biol. 23:5651-5663.
18. Kimball, S. R., N. K. Heinzinger, R. L. Horetsky, and L. S. Jefferson. 1998. Identification of interprotein interactions between the subunits of eukaryotic initiation factors eIF2 and eIF2B. J. Biol. Chem. 273:3039-3044.
19. Koonin, E. V. 1995. Multidomain organization of eukaryotic guanine nucleotide exchange factor eIF-2B revealed by analysis of conserved sequence motifs. Protein Sci. 4:1608-1617.
20. Krishnamoorthy, T., G. D. Pavitt, F. Zhang, T. E. Dever, and A. G. Hinnebusch. 2001. Tight binding of the phosphorylated α subunit of initiation factor 2 (eIF2α) to the regulatory subunits of guanine nucleotide exchange factor eIF2B is required for inhibition of translation initiation. Mol. Cell. Biol. 21:5018-5030.
21. Leegwater, P. A. J., A. A. Konst, B. Kuyt, L. A. Sandkuijl, S. Naidu, C. B. Oudejans, R. B. Schutgens, J. C. Pronk, and M. S. Van der Knaap. 1999, The gene for leukoencephalopathy with vanishing white matter is located on chromosome 3q27. Am. J. Hum. Genet. 65:728-734.
22. Leegwater, P. A. J., G. Vermeulen, A. A. M. Koenst, S. Naidu, J. Mulders, A. Visser, P. Kersbergen, D. Mobach, D. Fonds, C. G. M. van Berkel R. J. L. F. Lemmers, R. Frants, C. B. M. Oudejans, R. B. H. Schutgens, J. C. Pronk, and M. van der Knaap. 2001. Subunits of the translation initiation factor eIF2B are mutated in leukoencephaly with vanishing white matter. Nat. Genet. 29:383-388.
23. Li, W., G. J. Belsham, and C. G. Proud. 2001. Eukaryotic initiation factors 4A (eIF4A) and 4G (eIF4G) mutually interact in a 1:1 ratio in vivo. J. Biol. Chem. 276:29111-29115.
24. Pavitt, G., W. Yang, and A. G. Hinnebusch. 1997. Homologous segments in three subunits of the guanine nucleotide exchange factor eIF2B mediate translational regulation by phosphorylation of eIF2. Mol. Cell. Biol. 17:1298-1313.
25. Pavitt, G. D., K. V. A. Ramaiah, S. R. Kimball, and A. G. Hinnebusch. 1998. eIF2 independently binds two distinct eIF2B subcomplexes that catalyse and regulate guanine-nucleotide exchange. Genes Dev. 12:514-526.
26. Petrov, T., B. D. Underwood, B. Braun, S. S. Alousi, and J. A. Rafols. 2001. Upregulation of iNOS expression and phosphorylation of eIF-2α are paralleled by suppression of protein synthesis in rat hypothalamus in a closed head trauma model. J. Neurotrauma 18:799-812.
27. Price, N. T., S. F. Nakielny, S. J. Clark, and C. G. Proud. 1989. The two forms of the beta-subunit of initiation factor-2 from reticulocyte lysates arise from proteolytic degradation. Biochim. Biophys. Acta 1008:177-182.
28. Proud, C. G. 2001. Regulation of eukaryotic initiation factor eIF2B. Prog. Mol. Subcell. Biol. 26:95-114.
29. Richardson, J., S. S. Mohammad, and G. D. Pavitt. 2004. Mutations causing childhood ataxia with central nervous system hypomyelination reduce eukaryotic initiation factor 2B complex formation and activity. Mol. Cell. Biol. 24:2352-2363.
30. Rowlands, A. G., R. Panniers, and E. C. Henshaw. 1988. The catalytic mechanism of guanine nucleotide exchange factor action and competitive inhibition by phosphorylated eukaryotic initiation factor 2. J. Biol. Chem. 263:5526-5533.
31. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed., p. 7.39. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
32. Scheper, G. C., R. van Wijk, and A. A. M. Thomas. 2001. Regulation of the activity of eukaryotic initiation factors in stressed cells. Prog. Mol. Subcell. Biol. 27:39-56.
33. Scheuner, D., B. Song, E. McEwen C. Liu, R. Laybutt, P. Gillespie, T. Saunders, S. Bonners-Weir, and R. J. Kaufman. 2001. Translational control is required for the unfolded protein response and in vivo glucose homeostasis. Mol. Cell 7:1165-1176.
34. Schiffmann, R., J. R. Moller, B. D. Trapp, H. H. Shih, R. G. Farrer, D. A. Katz, J. R. Alger, C. C. Parker, P. E. Hauer, C. R. Kaneski, et al. 1994. Childhood ataxia with diffuse central nervous system hypomyelination. Ann. Neurol. 35:331-340.
35. Van der Knaap, M. S., P. G. Barth, F. J. Gabreels, E. Franzoni, J. H. Begeer, H. Stroink, J. J. Rotteveel, and J. Valk. 1997. A new leukoencephalopathy with vanishing white matter. Neurology 48:845-855.
36. Van der Knaap, M. S., W. Kamphorst, P. G. Barth, C. L. Kraaijeveld, E., Gut, and J. Valk. 1998. Phenotypic variation in leukoencephalopathy with vanishing white matter. Neurology 51:540-547.
37. Van der Knaap, M. S., P. A. J. Leegwater, A. A. M. Könst, A. Visser, S. Naidu, C. B. M. Oudejans, R. B. J. Schutgens, and J. C. Pronk 2002. Mutations of each of the five subunits of translation initiation factor eIF2B can cause leukoencephalopathy with vanishing white matter. Ann. Neurol. 51:264-270.
38. Wang, X., M. Janmaat, A. Beugnet, F. E. M. Paulin, and C. G. Proud. 2002. Evidence that the dephosphorylation of Ser535 in the ε-subunit of eukaryotic initiation factor 2B is insufficient for the activation of eIF2B by insulin. Biochem. J. 367:475-481.
39. Wang, X., F. E. M. Paulin, L. E. Campbell, E. Gomez, K. O'Brien, N. Morrice, and C. G. Proud. 2001. Eukaryotic initiation factor 2B: identification of multiple phosphorylation sites in the epsilon subunit and their roles in vivo. EMBO J. 20:4349-4359.
40. Yang, W., and A. G. Hinnebusch. 1996. Identification of a regulatory subcomplex in the guanine nucleotide exchange factor eIF2B that mediates inhibition by phosphorylated eIF2. Mol. Cell. Biol. 16:6603-6616.