Receptor for retrograde transport in the apicomplexan parasite Toxoplasma gondii

Eukaryotic Cell

Volumn 4, Issue 2, 2005, Pages 432-442

  Pfluger, Stacy L ^a   Goodson, Holly V ^a   Moran, Jennifer M ^a   Ruggiero, Christine J ^a   Ye, Xin ^a   Emmons, Krista M ^a   Hager, Kristin M ^a  

^a UNIVERSITY OF NOTRE DAME   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HDEL RECEPTOR; HYBRID PROTEIN; MEMBRANE PROTEIN; PROTOZOAL PROTEIN; RECEPTOR; SACCHAROMYCES CEREVISIAE PROTEIN;

AMINO ACID SEQUENCE; ANIMAL; ARTICLE; CELL LINE; CLASSIFICATION; COATED VESICLE; CYTOLOGY; GENETIC COMPLEMENTATION; GENETICS; GOLGI COMPLEX; HUMAN; METABOLISM; MOLECULAR GENETICS; PHYLOGENY; PHYSIOLOGY; SEQUENCE ALIGNMENT; TOXOPLASMA; TRANSPORT AT THE CELLULAR LEVEL;

AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL TRANSPORT; CELL LINE; COP-COATED VESICLES; GENETIC COMPLEMENTATION TEST; GOLGI APPARATUS; HUMANS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTOZOAN PROTEINS; RECEPTORS, PEPTIDE; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE ALIGNMENT; TOXOPLASMA;

FUNGI; METAZOA; PLASMODIUM FALCIPARUM; SACCHAROMYCES CEREVISIAE; TOXOPLASMA GONDII;

EID: 13844308306     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.4.2.432-442.2005     Document Type: Article

References (76)

1. Ajioka, J. W. 1998. Toxoplasma gondii: ESTs and gene discovery. Int. J. Parasitol. 28:1025-1031.
2. Ajioka, J. W., J. C. Boothroyd, B. P. Brunk, A. Hehl, L. Hillier, I. D. Manger, M. Marra, G. C. Overton, D. S. Roos, K. L. Wan, et al. 1998. Gene discovery by EST sequencing in Toxoplasma gondii reveals sequences restricted to the Apicomplexa. Genome Res. 8:18-28.
3. Aoe, T., E. Cukierman, A. Lee, D. Cassel, P. J. Peters, and V. W. Hsu. 1997. The KDEL receptor, ERD2, regulates intracellular traffic by recruiting a GTPase-activating protein for ARF1. EMBO J. 16:7305-7316.
4. Aoe, T., I. Huber, C. Vasudevan, S. C. Watkins, G. Romero, D. Cassel, and V. W. Hsu. 1999. The KDEL receptor regulates a GTPase-activating protein for ADP-ribosylation factor 1 by interacting with its non-catalytic domain. J. Biol. Chem. 274:20545-20549.
5. Baldauf, S. L., A. J. Roger, I. Wenk-Siefert, and W. F. Doolittle. 2000. A kingdom-level phylogeny of eukaryotes based on combined protein data. Science 290:972-977.
6. Blobel, G., and B. Dobberstein. 1975. Transfer of proteins across membranes. I. Presence of proteolytically processed and unprocessed nascent immunoglobulin light chains on membrane-bound ribosomes of murine myeloma. J. Cell Biol. 67:835-851.
7. Blobel, G., and B. Dobberstein. 1975. Transfer to proteins across membranes. II. Reconstitution of functional rough microsomes from heterologous components. J. Cell Biol. 67:852-862.
8. Bremser, M., W. Nickel, M. Schweikert, M. Ravazzola, M. Amherdt, C. A. Hughes, T. H. Sollner, J. E. Rothman, and F. T. Wieland. 1999. Coupling of coat assembly and vesicle budding to packaging of putative cargo receptors. Cell 96:495-506.
9. Camps, M., G. Arrizabalaga, and J. Boothroyd. 2002. An rRNA mutation identifies the apicoplast as the target for clindamycin in Toxoplasma gondii. Mol. Microbiol. 43:1309-1318.
10. Cesbron, M. F., L. Lecordier, and C. Mercier. 1996. Role of secretory dense granule organelles in the pathogenesis of toxoplasmosis. Curr. Top. Microbiol. Immunol. 219:59-72.
11. Chaturvedi, S., H. Qi, D. Coleman, A. Rodriguez, P. I. Hanson, B. Striepen, D. S. Roos, and K. A. Joiner. 1999. Constitutive calcium-independent release of Toxoplasma gondii dense granules occurs through the NSF/SNAP/ SNARE/Rab machinery. J. Biol. Chem. 274:2424-2431.
12. Cole, N. B., J. Ellenberg, J. Song, D. DiEuliis, and J. Lippincott-Schwartz. 1998. Retrograde transport of Golgi-localized proteins to the ER. J. Cell Biol. 140:1-15.
13. Delwiche, C. F. 1999. Tracing the thread of plastid diversity through the tapestry of life. Am. Nat. 154:S164-S177.
14. DeRocher, A., C. B. Hagen, J. E. Froehlich, J. E. Feagin, and M. Parsons. 2000. Analysis of targeting sequences demonstrates that trafficking to the Toxoplasma gondii plastid branches off the secretory system. J. Cell Sci. 113:3969-3977.
15. Dubremetz, J. F., N. Garcia-Reguet, V. Conseil, and M. N. Fourmaux. 1998. Apical organelles and host-cell invasion by Apicomplexa. Int. J. Parasitol. 28:1007-1013.
16. Elmendorf, H. G., and K. Haldar. 1993. Identification and localization of ERD2 in the malaria parasite Plasmodium falciparum: separation from sites of sphingomyelin synthesis and implications for organization of the Golgi. EMBO J. 12:4763-4773.
17. Fast, N. M., J. C. Kissinger, D. S. Roos, and P. J. Keeling. 2001. Nuclear-encoded, plastid-targeted genes suggest a single common origin for apicomplexan and dinoflagellate plastids. Mol. Biol. Evol. 18:418-426.
18. Fichera, M. E., and D. S. Roos. 1997. A plastid organelle as a drug target in apicomplexan parasites. Nature 390:407-409.
19. Fullekrug, J., B. Sonnichsen, U. Schafer, P. Nguyen Van, H. D. Soling, and G. Mieskes. 1997. Characterization of brefeldin A induced vesicular structures containing cycling proteins of the intermediate compartment/cis-Golgi network. FEBS Lett. 404:75-81.
20. Hager, K. M., B. Striepen, L. G. Tilney, and D. S. Roos. 1999. The nuclear envelope serves as an intermediary between the ER and Golgi complex in the intracellular parasite Toxoplasma gondii. J. Cell Sci. 112:2631-2638.
21. Hardwick, K. G., J. C. Boothroyd, A. D. Rudner, and H. R. Pelham. 1992. Genes that allow yeast cells to grow in the absence of the HDEL receptor. EMBO J. 11:4187-4195.
22. He, C. Y., M. K. Shaw, C. H. Pletcher, B. Striepen, L. G. Tilney, and D. S. Roos. 2001. A plastid segregation defect in the protozoan parasite Toxoplasma gondii. EMBO J. 20:330-339.
23. He, C. Y., B. Striepen, C. H. Pletcher, J. M. Murray, and D. S. Roos. 2001. Targeting and processing of nuclear-encoded apicoplast proteins in plastid segregation mutants of Toxoplasma gondii. J. Biol. Chem. 276:28436-28442.
24. Higgins, D. G., J. D. Thompson, and T. J. Gibson. 1996. Using CLUSTAL for multiple sequence alignments. Methods Enzymol. 266:383-402.
25. Hoppe, H. C., and K. A. Joiner. 2000. Cytoplasmic tail motifs mediate endoplasmic reticulum localization and export of transmembrane reporters in the protozoan parasite Toxoplasma gondii. Cell. Microbiol. 2:569-578.
26. Hoppe, H. C., H. M. Ngo, M. Yang, and K. A. Joiner. 2000. Targeting to rhoptry organelles of Toxoplasma gondii involves evolutionarily conserved mechanisms. Nat. Cell Biol. 2:449-456.
27. Hsu, V. W., N. Shah, and R. D. Klausner. 1992. A brefeldin A-like phenotype is induced by the overexpression of a human ERD-2-like protein, ELP-1. Cell 69:625-635.
28. Hu, K., T. Mann, B. Striepen, C. J. Beckers, D. S. Roos, and J. M. Murray. 2002. Daughter cell assembly in the protozoan parasite Toxoplasma gondii. Mol. Biol. Cell 13:593-606.
29. Ito, H., Y. Fukuda, K. Murata, and A. Kimura. 1983. Transformation of intact yeast cells treated with alkali cations. J. Bacteriol. 153:163-168.
30. Jackson, M. E., J. C. Simpson, A. Girod, R. Pepperkok, L. M. Roberts, and J. M. Lord. 1999. The KDEL retrieval system is exploited by Pseudomonas exotoxin A, but not by Shiga-like toxin-1, during retrograde transport from the Golgi complex to the endoplasmic reticulum. J. Cell Sci. 112:467-475.
31. Joiner, K. A., and D. S. Roos. 2002. Secretory traffic in the eukaryotic parasite Toxoplasma gondii: less is more. J. Cell Biol. 157:557-563.
32. Karsten, V., H. Qi, C. J. Beckers, A. Reddy, J. F. Dubremetz, P. Webster, and K. A. Joiner. 1998. The protozoan parasite Toxoplasma gondii targets proteins to dense granules and the vacuolar space using both conserved and unusual mechanisms. J. Cell Biol. 141:1323-1333.
33. Klumperman, J., A. Schweizer, H. Clausen, B. L. Tang, W. Hong, V. Oorschot, and H. P. Hauri. 1998. The recycling pathway of protein ERGIC-53 and dynamics of the ER-Golgi intermediate compartment. J. Cell Sci. 111:3411-3425.
34. Kohler, S., C. F. Delwiche, P. W. Denny, L. G. Tilney, P. Webster, R. J. Wilson, J. D. Palmer, and D. S. Roos. 1997. A plastid of probable green algal origin in Apicomplexan parasites. Science 275:1485-1489.
35. Kyte, J., and R. F. Doolittle. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157:105-132.
36. Levine, N. D. 1988. Progress in taxonomy of the Apicomplexan protozoa. J. Protozool. 35:518-520.
37. Lewis, M. J., and H. R. Pelham. 1990. A human homologue of the yeast HDEL receptor. Nature 348:162-163.
38. Lewis, M. J., and H. R. Pelham. 1992. Ligand-induced redistribution of a human KDEL receptor from the Golgi complex to the endoplasmic reticulum. Cell 68:353-364.
39. Lewis, M. J., and H. R. Pelham. 1992. Sequence of a second human KDEL receptor. J. Mol. Biol. 226:913-916.
40. Lewis, M. J., D. J. Sweet, and H. R. Pelham. 1990. The ERD2 gene determines the specificity of the luminal ER protein retention system. Cell 61:1359-1363.
41. Lingelbach, K., and K. A. Joiner. 1998. The parasitophorous vacuole membrane surrounding Plasmodium and Toxoplasma: an unusual compartment in infected cells. J. Cell Sci. 111:1467-1475.
42. Lippincott-Schwartz, J., J. G. Donaldson, A. Schweizer, E. G. Berger, H. P. Hauri, L. C. Yuan, and R. D. Klausner. 1990. Microtubule-dependent retrograde transport of proteins into the ER in the presence of brefeldin A suggests an ER recycling pathway. Cell 60:821-836.
43. Majoul, I., K. Sohn, F. T. Wieland, R. Pepperkok, M. Pizza, J. Hillemann, and H. D. Soling. 1998. KDEL receptor (Erd2p)-mediated retrograde transport of the cholera toxin A subunit from the Golgi involves COPI, p23, and the COOH terminus of Erd2p. J. Cell Biol. 143:601-612.
44. Majoul, I., M. Straub, S. W. Hell, R. Duden, and H. D. Soling. 2001. KDEL-cargo regulates interactions between proteins involved in COPI vesicle traffic: measurements in living cells using FRET. Dev. Cell 1:139-153.
45. Mann, T., and C. Beckers. 2001. Characterization of the subpellicular network, a filamentous membrane skeletal component in the parasite Toxoplasma gondii. Mol. Biochem. Parasitol. 115:257-268.
46. Marks, M. S., H. Ohno, T. Kirchhausen, and J. S. Bonifacino. 1997. Protein sorting by tyrosine-based signals: adapting to the Ys and wherefores. Trends Cell Biol. 7:124-128.
47. McLeod, R., and J. S. Remington. 1987. Toxoplasmosis, p. 791. In E. Braunwald, K. J. Isselbacher, R. G. Petersdorf, J. D. Wilson, J. B. Martin, and A. S. Fauci (ed.), Harrison's principles of internal medicine. McGraw-Hill, New York, N.Y.
48. Morrissette, N. S., V. Bedian, P. Webster, and D. S. Roos. 1994. Characterization of extreme apical antigens from Toxoplasma gondii. Exp. Parasitol. 79:445-459.
49. Nagel, S. D., and J. C. Boothroyd. 1988. The alpha- and beta-tubulins of Toxoplasma gondii are encoded by single copy genes containing multiple introns. Mol. Biochem. Parasitol. 29:261-273.
50. Palmer, J. D. 2000. A single birth of all plastids? Nature 405:32-33.
51. Palmer, J. D., and C. F. Delwiche. 1996. Second-hand chloroplasts and the case of the disappearing nucleus. Proc. Natl. Acad. Sci. USA 93:7432-7435.
52. Pelham, H. R. 1995. Sorting and retrieval between the endoplasmic reticulum and Golgi apparatus. Curr. Opin. Cell Biol. 7:530-535.
53. Pelham, H. R. 1996. The dynamic organisation of the secretory pathway. Cell Struct. Funct. 21:413-419.
54. Pelletier, L., C. A. Stern, M. Pypaert, D. Sheff, H. M. NgO, N. Roper, C. Y. He, K. Hu, D. Toomre, I. Coppens, et al. 2002. Golgi biogenesis in Toxoplasma gondii. Nature 418:548-552.
55. Roos, D. S. 1993. Primary structure of the dihydrofolate reductase-thymidylate synthase gene from Toxoplasma gondii. J. Biol. Chem. 268:6269-6280.
56. Roos, D. S., M. J. Crawford, R. G. Donald, L. M. Fohl, K. M. Hager, J. C. Kissinger, M. G. Reynolds, B. Striepen, and W. J. Sullivan, Jr. 1999. Transport and trafficking: Toxoplasma as a model for Plasmodium. Novartis Found. Symp. 226:176-195
57. Roos, D. S., M. J. Crawford, R. G. Donald, M. Fraunholz, O. S. Harb, C. Y. He, J. C. Kissinger, M. K. Shaw, and B. Striepen. 2002. Mining the Plasmodium genome database to define organellar function: what does the apicoplast do? Philos. Trans. R. Soc. Lond. B 357:35-46.
58. Roos, D. S., M. J. Crawford, R. G. Donald, J. C. Kissinger, L. J. Klimczak, and B. Striepen. 1999. Origin, targeting, and function of the apicomplexan plastid. Curr. Opin. Microbiol. 2:426-432.
59. Roos, D. S., R. G. Donald, N. S. Morrissette, and A. L. Moulton. 1994. Molecular tools for genetic dissection of the protozoan parasite Toxoplasma gondii. Methods Cell Biol. 45:27-63.
60. Scheel, A. A., and H. R. Pelham. 1998. Identification of amino acids in the binding pocket of the human KDEL receptor. J. Biol. Chem. 273:2467-2472.
61. Seemann, J., E. Jokitalo, M. Pypaert, and G. Warren. 2000. Matrix proteins can generate the higher order architecture of the Golgi apparatus. Nature 407:1022-1026.
62. Semenza, J. C., K. G. Hardwick, N. Dean, and H. R. Pelham. 1990. ERD2, a yeast gene required for the receptor-mediated retrieval of luminal ER proteins from the secretory pathway. Cell 61:1349-1357.
63. Shaw, M. K., H. L. Compton, D. S. Roos, and L. G. Tilney. 2000. Microtubules, but not actin filaments, drive daughter cell budding and cell division in Toxoplasma gondii. J. Cell Sci. 113:1241-1254.
64. Sherman, F. 1991. Getting started with yeast. Methods Enzymol. 194:3-21.
65. Sikorski, R. S., and J. D. Boeke. 1991. In vitro mutagenesis and plasmid shuffling: from cloned gene to mutant yeast. Methods Enzymol. 194:302-318.
66. Stedman, T. T., A. R. Sussmann, and K. A. Joiner. 2003. Toxoplasma gondii Rab6 mediates a retrograde pathway for sorting of constitutively secreted proteins to the Golgi complex. J. Biol. Chem. 278:54:33-5443.
67. Striepen, B., C. Y. He, M. Matrajt, D. Soldati, and D. S. Roos. 1998. Expression, selection, and organellar targeting of the green fluorescent protein in Toxoplasma gondii. Mol. Biochem. Parasitol. 92:325-338.
68. Striepen, B., D. Soldati, N. Garcia-Reguet, J. Dubremetz, and D. S. Roos. 2001. Targeting of soluble proteins to the rhoptries and micronemes in Toxoplasma gondii. Mol. Biochem. Parasitol. 113:45-63.
69. Tang, B. L., S. H. Low, H. P. Hauri, and W. Hong. 1995. Segregation of ERGIC53 and the mammalian KDEL receptor upon exit from the 15°C compartment. Eur. J. Cell Biol. 68:398-410.
70. Tang, B. L., S. H. Wong, X. L. Qi, S. H. Low, and W. Hong. 1993. Molecular cloning, characterization, subcellular localization and dynamics of p23, the mammalian KDEL receptor. J. Cell Biol. 120:325-328.
71. Townsley, F. M., D. W. Wilson, and H. R. Pelham. 1993. Mutational analysis of the human KDEL receptor: distinct structural requirements for Golgi retention, ligand binding and retrograde transport. EMBO J. 12:2821-2829.
72. Waller, R. F., P. J. Keeling, R. G. Donald, B. Striepen, E. Handman, N. Lang-Unnasch, A. F. Cowman, G. S. Besra, D. S. Roos, and G. I. McFadden. 1998. Nuclear-encoded proteins target to the plastid in Toxoplasma gondii and Plasmodium falciparum. Proc. Natl. Acad. Sci. USA 95:12352-12357.
73. Waller, R. F., P. J. Keeling, G. G. van Dooren, and G. I. McFadden. 2003. Comment on "A green algal apicoplast ancestor." Science 301:49.
74. Wan, K. L., J. M. Blackwell, and J. W. Ajioka. 1996. Toxoplasma gondii expressed sequence tags: insight into tachyzoite gene expression. Mol. Biochem. Parasitol. 75:179-186.
75. Wan, K. L., V. B. Carruthers, L. D. Sibley, and J. W. Ajioka. 1997. Molecular characterisation of an expressed sequence tag locus of Toxoplasma gondii encoding the micronemal protein MIC2. Mol. Biochem. Parasitol. 84:203-214.
76. Ward, T. H., R. S. Polishchuk, S. Caplan, K. Hirschberg, and J. Lippincott-Schwartz. 2001. Maintenance of Golgi structure and function depends on the integrity of ER export. J. Cell Biol. 155:557-570.