The protozoan parasite Toxoplasma gondii targets proteins to dense granules and the vacuolar space using both conserved and unusual mechanisms

Journal of Cell Biology

Volumn 141, Issue 6, 1998, Pages 1323-1333

  Karsten, Verena ^a   Qi, Huilin ^a   Beckers, Con J M ^a,c   Reddy, Anita ^a   Dubremetz, Jean Francois ^b   Webster, Paul ^a   Joiner, Keith A ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INSERM   (France)

^c UNIVERSITY OF ALABAMA SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE PHOSPHATASE; BACTERIAL ENZYME; BACTERIAL PROTEIN; BETA LACTAMASE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL VACUOLE; CONTROLLED STUDY; ESCHERICHIA COLI; HUMAN; HUMAN CELL; MEMBRANE VESICLE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SECRETION; PROTEIN TARGETING; SECRETORY GRANULE; TOXOPLASMA GONDII; VERO CELL;

ALKALINE PHOSPHATASE; AMINO ACID SEQUENCE; ANIMALS; ANTI-BACTERIAL AGENTS; BETA-LACTAMASES; BINDING SITES; BREFELDIN A; CELL MEMBRANE; CERCOPITHECUS AETHIOPS; CYCLOPENTANES; CYTOPLASM; ESCHERICHIA COLI; FLUORESCENT ANTIBODY TECHNIQUE, INDIRECT; GENE EXPRESSION; GLYCOSYLPHOSPHATIDYLINOSITOLS; GOLGI APPARATUS; MACROLIDES; MEMBRANE GLYCOPROTEINS; MICE; MICROSCOPY, IMMUNOELECTRON; MOLECULAR SEQUENCE DATA; PROTEIN SYNTHESIS INHIBITORS; PROTOZOAN PROTEINS; SUBCELLULAR FRACTIONS; TOXOPLASMA; VACUOLES; VERO CELLS; VIRAL ENVELOPE PROTEINS;

ANIMALIA; BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; EUKARYOTA; PROTOZOA; TOXOPLASMA GONDII; VESICULAR STOMATITIS VIRUS;

EID: 0032526698     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.141.6.1323     Document Type: Article

References (55)

1. Bangs, J.D., D. Hereld, J.L. Krakow, G.W. Hart, and P.T. Englund. 1985. Rapid processing of the carboxyl terminus of a trypanosome variant surface glycoprotein. Proc. Natl. Acad Sci. USA. 82:3207-3211.
2. Becker, B., and M. Melkonian. 1996. The secretory pathway of protists: spatial and functional organisation and evolution. Microbiol. Rev. 60:697-721.
3. Beckers, C.J.M., R.G.K. Donald, D.S. Roos, B.J. Luft, J.C. Schwab, Y. Cao, and K.A. Joiner. 1995. Inhibition of cytoplasmic and organellar protein synthesis in Toxoplasma gondii: implications for the target of macrolide antibiotics. J. Clin. Invest. 95:367-376.
4. Beckers, C.J.M., J.F. Dubremetz, O. Mercereau-Puijalon, and K.A. Joiner. 1994. The Toxoplasma gondii rhoptry protein ROP2 is inserted into the parasitophorous vacuole membrane, surrounding the intracellular parasite, and is exposed to the host cell cytoplasm. J. Cell Biol. 127:947-961.
5. Brown, D.A., B. Crise, and J.K. Rose. 1989. Mechanism of membrane anchoring affects polarized expression of two proteins in MDCK cells. Science. 245: 1499-1501.
6. Burg, J.L., D. Perelman, L.H. Kasper, P.L. Ware, and J.C. Boothroyd. 1988. Molecular analysis of the gene encoding the major surface antigen of Toxoplasma gondii. J. Immunol. 141:3584-3591.
7. Burgess, T.L., and R.B. Kelly. 1987. Constitutive and regulated secretion of proteins. Annu. Rev. Cell Biol. 3:243-293.
8. Cabec, V.L., J.B. Cowland, J. Calafat, and N. Borregaard. 1996. Targeting of proteins to granule subsets is determined by timing and not by sorting: the specific granule protein NGAL is localized to azurophil granules when expressed in HL-60 cells. Proc. Natl. Acad. Sci. USA. 93:6454-6457.
9. Carruthers, V., and D. Sibley. 1997. Sequential protein secretion from three distinct organelles of Toxoplasma gondii accompanies invasion of human fibroblasts. Eur. J. Cell Biol. 73:114-123.
10. Castle, A.M., A.Y. Huang, and D. Castle. 1997. Passive sorting in maturing granules of AtT-20 cells: the entry and exit of salivary amylase and proline rich protein. J. Cell Biol. 138:45-54.
11. Cesbron-Delauw, M.F. 1994. Dense-granule organelles of Toxoplasma gondii: their role in the host-parasite relationship. Parasitol. Today. 10:293-296.
12. Chanat, E., and W. Huttner. 1991. Milieu-induced, selective aggregation of regulated secretory proteins in the trans-Golgi network. J. Cell Biol. 115:1505-1519.
13. Colomer, V., K. Lal, T.C. Hoops, and M.J. Rindler. 1994. Exocrine granules specific packaging signals are present in the polypeptide moiety of the pancreatic granule membrane protein GP2 and in amylase: implications for protein targeting to secretory granules. EMBO (Eur. Mol. Biol. Organ.) J. 13: 3711-3719.
14. Colomer, V., G.A. Kicska, and M.J. Rindler. 1996. Secretory granule content proteins and the luminal domains of granule membrane proteins aggregate in vitro at mildly acidic pH. J. Biol. Chem. 271:48-55.
15. fat mice. Cell. 88:73-83.
16. De Lisle, R.C., and R. Bansal. 1996. Brefeldin A inhibits the constitutive-like secretion of a sulfated protein in pancreatic acinar cells. Eur. J. Cell. Biol. 71: 62-71.
17. Didier, M., J.H. Morrissey, R.D. Fugate, D.F. Bainton, and R.P. McEver. 1992. Cytoplasmic domain of P-selectin (CD62) contains the signal for sorting into the regulated secretory pathway. Mol. Biol. Cell. 3:309-321.
18. Dittie, A.S., L. Thomas, G. Thomas, and S.A. Tooze. 1997. Interaction of furin in immature secretory granules from neuroendocrine cells with the AP-1 adaptor complex is modulated by casein kinase II phosphorylation. EMBO (Eur. Mol. Biol. Organ.) J. 16:4859-4870.
19. Donald, R.G.K., D. Carter, B. Ullman, and D. Roos. 1996. Insertional tagging, cloning, and expression of the Toxoplasma gondii hypoxanthine-xanthineguanine phosphoribosyltransferase gene. J. Biol. Chem. 271:14010-14019.
20. Dubremetz, J.F., A. Achbarou, D. Bermudes, and K.A. Joiner. 1993. Kinetics of apical organelle exocytosis during Toxoplasma gondii host cell interaction. Parasitol. Res. 79:402-408.
21. Fernandez, C.J., M. Haugwitz, B. Eaton, and H.P. Moore. 1997. Distinct molecular events during secretory granule biogenesis revealed by sensitivities to brefeldin A. Mol. Biol. Cell. 8:2171-2185.
22. Griffiths, G., R. Back, and M. Marsh. 1989. A quantitative analysis of the endocytic pathway in baby hamster kidney cells. J. Cell Biol. 109:2703-2720.
23. Halonen, S.K., E. Weidner, and J.F. Siebenaller. 1996. Evidence for heterotrimeric GTP-binding proteins in Toxoplasma gondii. J. Eukaryot. Microbiol. 43: 187-192.
24. Inouye, H., S. Michaelis, A. Wright, and J. Beckwith. 1981. Cloning and restriction mapping of the alkaline phosphatase structural gene (phoA) of Escherichia coli and generation of deletion mutants in vitro. J. Bacteriol. 146:668-675.
25. Joiner, K.A., S.A. Fuhrman, H. Mietinnen, L.L. Kasper, and I. Mellman. 1990. Toxoplasma gondii: fusion competence of parasitophorous vacuoles in Fc receptor transfected fibroblasts. Science. 249:641-646.
26. Karsten, V., H. Qi, C.J.M. Beckers, and K.A. Joiner. 1997. Targeting the secretory pathway of Toxoplasma gondii. Methods (Orlando). 13:103-111.
27. Kuliawat, R., and P. Arvan. 1992. Protein targeting via the "constitutive-like" secretory pathway in isolated pancreatic islets: passive sorting in the immature granule compartment. J. Cell Biol. 118:521-529.
28. Kuliawat, R., and P. Arvan. 1994. Distinct molecular mechanisms for protein sorting within immature secretory granules of pancreatic B-cells. J. Cell Biol. 126:77-86.
29. Laemmli, U.K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 227:680-685.
30. Laminet, A.A., and A. Pluckthun. 1989. The precursor of β-lactamase: purification, properties, and folding kinetics. EMBO (Eur. Mol. Biol. Organ.) J. 8:1469-1477.
31. Mevelec, M.N., T. Chardes, O. Mercereau-Puijalon, I. Bourguin, A. Archbarou, J.F. Dubremetz, and D. Bout. 1992. Molecular cloning of GRA4, a dense Toxoplasma gondii dense granule protein, recognized by mucosal IgA antibodies. Mol. Biochem. Parasitol. 56:227-238.
32. Milgram, S.L., B.A. Eipper, and R.E. Mains. 1994. Differential trafficking of soluble and integral membrane secretory granule-associated proteins. J. Cell Biol. 124:33-41.
33. Milgram, S.L., R.E. Mains, and B. A. Eipper. 1996. Identification of routing determinants in the cytosolic domain of a secretory granule-associated integral membrane protein. J. Biol. Chem. 271:17526-17535.
34. Nagel, S.D., and J.C. Boothroyd. 1989. The major surface antigen, P30, of Toxoplasma gondii is anchored by a glycolipid. J. Biol. Chem. 264:5569-5574.
35. Nakaar, V., D. Bermudes, K.R. Peck, and K.J. Joiner. 1997. Upstream elements are required for expression of nucleoside triphosphate hydrolase genes of Toxoplasma gondii. Mol. Biochem. Parasitol. In press.
36. Nishimura, N., and W.E. Balch. 1997. A di-acidic signal required for selective export from the endoplasmatic reticulum. Science. 277:556-558.
37. Ossorio, P.N., J.F. Dubremetz, and K.A. Joiner. 1994. A soluble secretory protein of the intracellular parasite Toxoplasma gondii associates with the parasitophorous vacuole membrane through Hydrophobic interactions. J. Biol. Chem. 269:15350-15357.
38. Perkins, M. 1992. Rhoptry organelles of apicomplexan parasites. Parasitol. Today. 8:28-32.
39. Rodriguez-Boulan, E., and S.K. Powell. 1992. Polarity of epithelial and neuronal cells. Annu. Rev. Cell Biol. 8:395-427.
40. Roos, D.S., R.G.K. Donald, N.S. Morrissette, and A.L.C. Moulton. 1994. Molecular tools for genetic dissection of the protozoan parasite Toxoplasma gondii. Methods Cell Biol. 45:27-63.
41. Rosa, P., U. Weiss, R. Pepperkok, W. Ansorge, C. Niehrs, E.H. Stelzer, and W.B. Huttner. 1989. An antibody against secretogranin I (chromogranin B) is packaged into secretory granules. J. Cell Biol. 109:17-34.
42. Rosa, P., F.A. Barr, J.C. Stinchcombe, C. Binacchi, and W. Huttner. 1992. Brefeldin A inhibits the formation of constitutive secretory vesicles and immature secretory granules from the trans-Golgi network. Eur. J. Cell Biol. 59:265-274.
43. Rose, J., and J. Bergmann. 1983. Altered cytoplasmic domains affect intracellular transport of the vesicular stomatitis virus glycoprotein. Cell. 34:513-524.
44. Seeber, F., J.F. Dubremetz, and J.C. Boothroyd. 1998. Analysis of Toxoplasma gondii stably transfected with a transmembrane variant of its major surface protein SAG1. J. Cell Sci. 111:23-29.
45. Sibley, L.D., J.L. Krahenbuhl, G.M.W. Adams, and E. Weidner. 1986. Toxoplasma modifies macrophage phagosomes by secretion of a vesicular network rich in surface proteins. J. Cell Biol. 103:867-874.
46. Sibley, L.D., I.R. Niesman, S.F. Parmley, and M.-F. Ceshron-Delauw. 1995. Regulated secretion of multi-lamellar vesicles leads to formation of a tubulo-vesicular network in host-cell vacuoles occupied by Toxoplasma gondii. J. Cell Sci. 108:1669-1677.
47. Silverman, J.A., and K.A. Joiner. 1996. Toxoplasma/host cell interaction. In Host Response to Intracellular Pathogens. S.H.E. Kaufman, editor. R.G. Landers, Austin, TX. 313-338.
48. Simons, K., and E. Eikonen. 1997. Functional rafts in cell membranes. Nature. 387:569-572.
49. Sinai, A., and K.A. Joiner. 1997. Safe haven: the cell biology of non-fusogenic pathogen vacuoles. Annu. Rev. Microbiol. 27:415-462.
50. 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. 92:328-338.
51. Thomas, D.C., C.B. Brewer, and M.B. Roth. 1993. Vesicular stomatitis virus glycoprotein contains a dominant cytoplasmic basolateral sorting signal critically dependent upon tyrosine. J. Biol. Chem. 268:3313-3320.
52. Tomavo, S., R. Schwarz, and J.F. Dubremetz. 1989. Evidence for glycosyl-phosphatidyl inositol anchor of Toxoplasma gondii surface antigens. Mol. Cell. Biol. 9:4576-4580.
53. Towbin, H., T. Staehelin, and J. Gordon. 1979. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA. 76:4350-4354.
54. Urbe, S., S.A. Tooze, and F.A. Barr. 1997. Formation of secretory vesicles in the biosynthetic pathway. Biochim. Biophys. Acta. 1358:6-22.
55. Whitt, M.A., E. Chong, and J.K. Rose. 1989. Glycoprotein cytoplasmic domain sequences required for rescue of a vesicular stomatitis virus glycoprotein mutant. J. Virol. 63:3569-3578.