Novel membrane-bound eIF2α kinase in the flagellar pocket of Trypanosoma brucei

Eukaryotic Cell

Volumn 6, Issue 11, 2007, Pages 1979-1991

  Moraes, Maria Carolina S ^a   Jesus, Teresa C L ^a   Hashimoto, Nilce N ^a   Dey, Madhusudan ^b   Schwartz, Kevin J ^c   Alves, Viviane S ^a   Avila, Caria C ^a   Bangs, James D ^c   Dever, Thomas E ^b   Schenkman, Sergio ^a   Castilho, Beatriz A ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^b EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^c UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INITIATION FACTOR 2; PHOSPHOTHREONINE; PROTEIN KINASE R; PROTOZOAL PROTEIN;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CELL MEMBRANE; CHEMISTRY; CYTOLOGY; ENDOSOME; ENZYMOLOGY; FLAGELLUM; GLYCOSYLATION; GROWTH, DEVELOPMENT AND AGING; HUMAN; INTRACELLULAR MEMBRANE; LIFE CYCLE; MAMMAL; METABOLISM; MOLECULAR GENETICS; PHOSPHORYLATION; PROTEIN TERTIARY STRUCTURE; PROTEIN TRANSPORT; SACCHAROMYCES CEREVISIAE; TRYPANOSOMA BRUCEI;

AMINO ACID SEQUENCE; ANIMALS; CELL MEMBRANE; EIF-2 KINASE; ENDOSOMES; EUKARYOTIC INITIATION FACTOR-2; FLAGELLA; GLYCOSYLATION; HUMANS; INTRACELLULAR MEMBRANES; LIFE CYCLE STAGES; MAMMALS; MOLECULAR SEQUENCE DATA; PHOSPHORYLATION; PHOSPHOTHREONINE; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PROTOZOAN PROTEINS; SACCHAROMYCES CEREVISIAE; TRYPANOSOMA BRUCEI BRUCEI;

EUKARYOTA; HEXAPODA; MAMMALIA; PROTISTA; TRYPANOSOMA BRUCEI; TRYPANOSOMATIDAE;

EID: 36849092889     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00249-07     Document Type: Article

References (53)

1. Alexander, D. L., K. J. Schwartz, A. E. Balber, and J. D. Bangs. 2002. Developmentally regulated trafficking of the lysosomal membrane protein p67 in Trypanosoma brucei. J. Cell Sci. 115:3253-3263.
2. Bangs, J. D., L. Uyetake, M. J. Brickman, A. E. Balber, and J. C. Boothroyd. 1993. Molecular cloning and cellular localization of a BiP homologue in Trypanosoma brucei: divergent ER retention signals in a lower eukaryote. J. Cell Sci. 105:1101-1113.
3. Berriman, M., E. Ghedin, C. Hertz-Fowler, G. Blandin, H. Renauld, D. C. Bartholomeu, N. J. Lennard, E. Caler, N. E. Hamlin, B. Haas, U. Bohme, L. Hannick, M. A. Aslett, J. Shallom, L. Marcello, L. Hou, B. Wickstead, U. C. Alsmark, C. Arrowsmith, R. J. Atkin, A. J. Barron, F. Bringaud, K. Brooks, M. Carrington, I. Cherevach, T. J. Chillingworth, C. Churcher, L. N. Clark, C. H. Corton, A. Cronin, R. M. Davies, J. Doggett, A. Djikeng, T. Feldblyum, M. C. Field, A. Fraser, I. Goodhead, Z. Hance, D. Harper, B. R. Harris, H. Hauser, J. Hostetler, A. Ivens, K. Jagels, D. Johnson, J. Johnson, K. Jones, A. X. Kerhornou, H. Koo, N. Larke, S. Landfear, C. Larkin, V. Leech, A. Line, A. Lord, A. Macleod, P. J. Mooney, S. Moule, D. M. Martin, G. W. Morgan, K. Mungall, H. Norbertczak, D. Ormond, G. Pai, C. S. Peacock, J. Peterson, M. A. Quail, E. Rabbinowitsch, M. A. Rajandream, C. Reitter, S. L. Salzberg, M. Sanders, S. Schobel, S. Sharp, M. Simmonds, A. J. Simpson, L. Tallon, C. M. Turner, A. Tait, A. R. Tivey, S. Van Aken, D. Walker, D. Wanless, S. Wang, B. White, O. White, S. Whitehead, J. Woodward, J. Wortman, M. D. Adams, T. M. Embley, K. Gull, E. Ullu, J. D. Barry, A. H. Fairlamb, F. Opperdoes, B. G. Barrell, J. E. Donelson, N. Hall, C. M. Fraser, et al. 2005. The genome of the African trypanosome Trypanosoma brucei. Science 309:416-422.
4. Bertolotti, A., Y. Zhang, L. M. Hendershot, H. P. Harding, and D. Ron. 2000. Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat. Cell Biol. 2:326-332.
5. Brecht, M., and M. Parsons. 1998. Changes in polysome profiles accompany trypanosome development. Mol. Biochem. Parasitol. 97:189-198.
6. Brickman, M. J., J. M. Cook, and A. E. Balber. 1995. Low temperature reversibly inhibits transport from tubular endosomes to a perinuclear, acidic compartment in African trypanosomes. J. Cell Sci. 108:3611-3621.
7. Chung, W. L., M. Carrington, and M. C. Field. 2004. Cytoplasmic targeting signals in transmembrane invariant surface glycoproteins of trypanosomes. J. Biol. Chem. 279:54887-54895.
8. Clayton, C. E. 2002. Life without transcriptional control? From fly to man and back again. EMBO J. 21:1881-1888.
9. Dar, A. C., T. E. Dever, and F. Sicheri. 2005. Higher-order substrate recognition of eIF2α by the RNA-dependent protein kinase PKR. Cell 122:887-900.
10. Dever, T. E. 2002. Gene-specific regulation by general translation factors. Cell 108:545-556.
11. Dever, T. E., J. J. Chen, G. N. Barber, A. M. Cigan, L. Feng, T. F. Donahue, I. M. London, M. G. Katze, and A. G. Hinnebusch. 1993. Mammalian eukaryotic initiation factor 2 alpha kinases functionally substitute for GCN2 protein kinase in the GCN4 translational control mechanism of yeast. Proc. Natl. Acad. Sci. USA 90:4616-4620.
12. Dever, T. E., R. C. Wek, L. Feng, A. M. Cigan, T. F. Donahue, and A. G. Hinnebusch. 1992. Phosphorylation of initiation factor 2α by protein kinase GCN2 mediates gene-specific translational control of GCN4 in yeast. Cell 68:585-596.
13. Dey, M., C. Cao, A. C. Dar, T. Tamura, K. Ozato, F. Sicheri, and T. E. Dever. 2005. Mechanistic link between PKR dimerization, autophosphorylation, and eIF2α substrate recognition. Cell 122:901-913.
14. Dey, M., B. Trieselmann, E. G. Locke, J. Lu, C. Cao, A. C. Dar, T. Krishnamoorthy, J. Dong, F. Sicheri, and T. E. Dever. 2005. PKR and GCN2 kinases and guanine nucleotide exchange factor eukaryotic translation initiation factor 2B (eIF2B) recognize overlapping surfaces on eIF2α. Mol. Cell. Biol. 25:3063-3075.
15. El-Sayed, N. M., P. J. Myler, D. C. Bartholomeu, D. Nilsson, G. Aggarwal, A. N. Tran, E. Ghedin, E. A. Worthey, A. L. Delcher, G. Blandin, S. J. Westenberger, E. Caler, G. C. Cerqueira, C. Branche, B. Haas, A. Anupama, E. Arner, L. Aslund, P. Attipoe, E. Bontempi, F. Bringaud, P. Burton, E. Cadag, D. A. Campbell, M. Carrington, J. Crabtree, H. Darban, J. F. da Silveira, P. de Jong, K. Edwards, P. T. Englund, G. Fazelina, T. Feldblyum, M. Ferella, A. C. Frasch, K. Gull, D. Horn, L. Hou, Y. Huang, E. Kindlund, M. Klingbeil, S. Kluge, H. Koo, D. Lacerda, M. J. Levin, H. Lorenzi, T. Louie, C. R. Machado, R. McCulloch, A. McKenna, Y. Mizuno, J. C. Mottram, S. Nelson, S. Ochaya, K. Osoegawa, G. Pai, M. Parsons, M. Pentony, U. Pettersson, M. Pop, J. L. Ramirez, J. Rinta, L. Robertson, S. L. Salzberg, D. O. Sanchez, A. Seyler, R. Sharma, J. Shetty, A. J. Simpson, E. Sisk, M. T. Tammi, R. Tarleton, S. Teixeira, S. Van Aken, C. Vogt, P. N. Ward, B. Wickstead, J. Wortman, O. White, C. M. Fraser, K. D. Stuart, and B. Andersson. 2005. The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309:409-415.
16. Engstler, M., and M. Boshart. 2004. Cold shock and regulation of surface protein trafficking convey sensitization to inducers of stage differentiation in Trypanosoma brucei. Genes Dev. 18:2798-2811.
17. Engstler, M., F. Weise, K. Bopp, C. G. Grunfelder, M. Gunzel, N. Heddergott, and P. Overath. 2005. The membrane-bound histidine acid phosphatase TbMBAP1 is essential for endocytosis and membrane recycling in Trypanosoma brucei. J. Cell Sci. 118:2105-2118.
18. Field, M. C., and M. Carrington. 2004. Intracellular membrane transport systems in Trypanosoma brucei. Traffic 5:905-913.
19. Gull, K. 2003. Host-parasite interactions and trypanosome morphogenesis: a flagellar pocketful of goodies. Curr. Opin. Microbiol. 6:365-370.
20. Han, A. P., C. Yu, L. Lu, Y. Fujiwara, C. Browne, G. Chin, M. Fleming, P. Leboulch, S. H. Orkin, and J. J. Chen. 2001. Heme-regulated eIF2α kinase (HRI) is required for translational regulation and survival of erythroid precursors in iron deficiency. EMBO J. 20:6909-6918.
21. Hanks, S. K., and T. Hunter. 1995. Protein kinases 6. The eukaryotic protein kinase superfamily: kinase (catalytic) domain structure and classification. FASEB J. 9:576-596.
22. 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.
23. Hashimoto, N. N., L. S. Carnevalli, and B. A. Castilho. 2002. Translation initiation at non-AUG codons mediated by weakened association of eukaryotic initiation factor (eIF) 2 subunits. Biochem. J. 367:359-368.
24. Hinnebusch, A. G. 1997. Translational regulation of yeast GCN4. A window on factors that control initiator-tRNA binding to the ribosome. J. Biol. Chem. 272:21661-21664.
25. Hinnebush, A. G. 1993. Gene-specific translational control of the yeast GCN4 gene by phosphorylation of eukaryotic initiation factor 2. Mol. Microbiol. 10:215-223.
26. Ivens, A. C., C. S. Peacock, E. A. Worthey, L. Murphy, G. Aggarwal, M. Berriman, E. Sisk, M. A. Rajandream, E. Adlem, R. Aert, A. Anupama, Z. Apostolou, P. Attipoe, N. Bason, C. Bauser, A. Beck, S. M. Beverley, G. Bianchettin, K. Borzym, G. Bothe, C. V. Bruschi, M. Collins, E. Cadag, L. Ciarloni, C. Clayton, R. M. Coulson, A. Cronin, A. K. Cruz, R. M. Davies, J. De Gaudenzi, D. E. Dobson, A. Duesterhoeft, G. Fazelina, N. Fosker, A. C. Frasch, A. Fraser, M. Fuchs, C. Gabel, A. Goble, A. Goffeau, D. Harris, C. Hertz-Fowler, H. Hilbert, D. Horn, Y. Huang, S. Klages, A. Knights, M. Kube, N. Larke, L. Litvin, A. Lord, T. Louie, M. Marra, D. Masuy, K. Matthews, S. Michaeli, J. C. Mottram, S. Muller-Auer, H. Munden, S. Nelson, H. Norbertczak, K. Oliver, S. O'Neil, M. Pentony, T. M. Pohl, C. Price, B. Purnelle, M. A. Quail, E. Rabbinowitsch, R. Reinhardt, M. Rieger, J. Rinta, J. Robben, L. Robertson, J. C. Ruiz, S. Rutter, D. Saunders, M. Schafer, J. Schein, D. C. Schwartz, K. Seeger, A. Seyler, S. Sharp, H. Shin, D. Sivam, R. Squares, S. Squares, V. Tosato, C. Vogt, G. Volckaert, R. Wambutt, T. Warren, H. Wedler, J. Woodward, S. Zhou, W. Zimmermann, D. F. Smith, J. M. Blackwell, K. D. Stuart, B. Barrell, et al. 2005. The genome of the kinetoplastid parasite, Leishmania major. Science 309:436-442.
27. Jiang, H. Y., and R. C. Wek. 2005. GCN2 phosphorylation of eIF2α activates NF-κB in response to UV irradiation. Biochem. J. 385:371-380.
28. Jiang, H. Y., and R. C. Wek. 2005. Phosphorylation of the alpha-subunit of the eukaryotic initiation factor-2 (eIF2α) reduces protein synthesis and enhances apoptosis in response to proteasome inhibition. J. Biol. Chem. 280:14189-14202.
29. Kaufman, R. J. 2000. The double-stranded RNA-activated protein kinase PKR, p. 503-527. 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, NY.
30. Kawagishi-Kobayashi, M., C. Cao, J. Lu, K. Ozato, and T. E. Dever. 2000. Pseudosubstrate inhibition of protein kinase PKR by swine pox virus C8L gene product. Virology 276:424-434.
31. Lu, J., E. B. O'Hara, B. A. Trieselmann, P. R. Romano, and T. E. Dever. 1999. The interferon-induced double-stranded RNA-activated protein kinase PKR will phosphorylate serine, threonine, or tyrosine at residue 51 in eukaryotic initiation factor 2α. J. Biol. Chem. 274:32198-32203.
32. Ma, K., K. M. Vattem, and R. C. Wek. 2002. Dimerization and release of molecular chaperone inhibition facilitate activation of eukaryotic initiation factor-2 kinase in response to endoplasmic reticulum stress. J. Biol. Chem. 277:18728-18735.
33. Matthews, K. R., J. R. Ellis, and A. Paterou. 2004. Molecular regulation of the life cycle of African trypanosomes. Trends Parasitol. 20:40-47.
34. McNicoll, F., M. Muller, S. Cloutier, N. Boilard, A. Rochette, M. Dube, and B. Papadopoulou. 2005. Distinct 3′-untranslated region elements regulate stage-specific mRNA accumulation and translation in Leishmania. J. Biol. Chem. 280:35238-35246.
35. Mitchell, D. A., T. K. Marshall, and R. J. Deschenes. 1993. Vectors for the inducible overexpression of glutathione S-transferase fusion proteins in yeast. Yeast 9:715-723.
36. Narasimhan, J., K. A. Staschke, and R. C. Wek. 2004. Dimerization is required for activation of eIF2 kinase Gcn2 in response to diverse environmental stress conditions. J. Biol. Chem. 279:22820-22832.
37. Natarajan, K., M. R. Meyer, B. M. Jackson, D. Slade, C. Roberts, A. G. Hinnebusch, and M. J. Marton. 2001. Transcriptional profiling shows that Gcn4p is a master regulator of gene expression during amino acid starvation in yeast. Mol. Cell. Biol. 21:4347-4368.
38. Paindavoine, P., S. Rolin, S. Van Assel, M. Geuskens, J. C. Jauniaux, C. Dinsart, G. Huet, and E. Pays. 1992. A gene from the variant surface glycoprotein expression site encodes one of several transmembrane adenylate cyclases located on the flagellum of Trypanosoma brucei. Mol. Cell. Biol. 12:1218-1225.
39. Pereira, C. M., E. Sattlegger, H. Y. Jiang, B. M. Longo, C. B. Jaqueta, A. G. Hinnebusch, R. C. Wek, L. E. Mello, and B. A. Castilho. 2005. IMPACT, a protein preferentially expressed in the mouse brain, binds GCN1 and inhibits GCN2 activation. J. Biol. Chem. 280:28316-28323.
40. Qiu, H., J. Dong, C. Hu, C. S. Francklyn, and A. G. Hinnebusch. 2001. The tRNA-binding moiety in GCN2 contains a dimerization domain that interacts with the kinase domain and is required for tRNA binding and kinase activation. EMBO J. 20:1425-1438.
41. Schwartz, K. J., R. F. Peck, N. N. Tazeh, and J. D. Bangs. 2005. GPI valence and the fate of secretory membrane proteins in African trypanosomes. J. Cell Sci. 118:5499-5511.
42. Sherman, F. 1991. Getting started with yeast. Methods Enzymol. 194:3-21.
43. Sikorsky, R. S., and P. Hieter. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122:10-27.
44. Sood, R., A. C. Porter, K. Ma, L. A. Quilliam, and R. C. Wek. 2000. Pancreatic eukaryotic initiation factor-2α kinase (PEK) homologues in humans, Drosophila melanogaster and Caenorhabditis elegans that mediate translational control in response to endoplasmic reticulum stress. Biochem. J. 346:281-293.
45. Sullivan, W. J., Jr., J. Narasimhan, M. M. Bhatti, and R. C. Wek. 2004. Parasite-specific eIF2 (eukaryotic initiation factor-2) kinase required for stress-induced translation control. Biochem. J. 380:523-531.
46. Thompson, G. M., E. Pacheco, E. O. Melo, and B. A. Castilho. 2000. Conserved sequences in the b subunit of archaeal and eukaryal translation initiation factor 2 (eIF2), absent from eIF5, mediate interaction with eIF2γ. Biochem. J. 347:703-709.
47. Ung, T. L., C. Cao, J. Lu, K. Ozato, and T. E. Dever. 2001. Heterologous dimerization domains functionally substitute for the double-stranded RNA binding domains of the kinase PKR. EMBO J. 20:3728-3737.
48. Vassella, E., J. V. Den Abbeele, P. Butikofer, C. K. Renggli, A. Furger, R. Brun, and I. Roditi. 2000. A major surface glycoprotein of Trypanosoma brucei is expressed transiently during development and can be regulated post-transcriptionally by glycerol or hypoxia. Genes Dev. 14:615-626.
49. Vassella, E., B. Reuner, B. Yutzy, and M. Boshart. 1997. Differentiation of African trypanosomes is controlled by a density sensing mechanism which signals cell cycle arrest via the cAMP pathway. J. Cell Sci. 110:2661-2671.
50. Vattem, K. M., and R. C. Wek. 2004. Reinitiation involving upstream ORFs regulates ATF4 mRNA translation in mammalian cells. Proc. Natl. Acad. Sci. USA 101:11269-11274.
51. Yang, R., S. A. Wek, and R. C. Wek. 2000. Glucose limitation induces GCN4 translation by activation of Gcn2 protein kinase. Mol. Cell. Biol. 20:2706-2717.
52. Zhan, K., K. M. Vattem, B. N. Bauer, T. E. Dever, J. J. Chen, and R. C. Wek. 2002. Phosphorylation of eukaryotic initiation factor 2 by heme-regulated inhibitor kinase-related protein kinases in Schizosaccharomyces pombe is important for resistance to environmental stresses. Mol. Cell. Biol. 22:7134-7146.
53. Zhang, P., B. C. McGrath, J. Reinert, D. S. Olsen, L. Lei, S. Gill, S. A. Wek, K. M. Vattem, R. C. Wek, S. R. Kimball, L. S. Jefferson, and D. R. Cavener. 2002. The GCN2 eIF2α kinase is required for adaptation to amino acid deprivation in mice. Mol. Cell. Biol. 22:6681-6688.