Are rhoptries in Apicomplexan parasites secretory granules or secretory lysosomal granules?

Molecular Microbiology

Volumn 52, Issue 6, 2004, Pages 1531-1541

  Ngô, Huân M ^a,b   Yang, Mei ^a   Joiner, Keith A ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Sheridan Commun Technol Middle S   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APICOMPLEXA; BIOGENESIS; BIOSYNTHESIS; CELL ACTIVITY; CELL FUNCTION; CELL ORGANELLE; CELL STRUCTURE; CELL VACUOLE; CELLULAR DISTRIBUTION; ENDOCYTOSIS; EUKARYOTE; INTRACELLULAR SPACE; LYSOSOME; MOLECULAR MODEL; MORPHOLOGY; NONHUMAN; PARASITE; PARASITISM; PLASMODIUM; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROCESSING; RHOPTRY; SECRETORY GRANULE; SHORT SURVEY; TOXOPLASMA; TOXOPLASMA GONDII;

ANIMALS; APICOMPLEXA; LYSOSOMES; PLASMODIUM; SECRETORY VESICLES; TOXOPLASMA;

APICOMPLEXA; EUKARYOTA; INVERTEBRATA; MAMMALIA; PLASMODIUM FALCIPARUM; PROTOZOA; TOXOPLASMA; TOXOPLASMA GONDII;

EID: 3042557931     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2004.04056.x     Document Type: Short Survey

References (56)

1. Baldi, D.L., Andrews, K.T., Waller, R.F., Roos, D.S., Howard, R.F., Crabb, B.S., and Cowman, A.F. (2000) RAP1 controls rhoptry targeting of RAP2 in the malaria parasite Plasmodium falciparum. EMBO J 19: 2435-2443.
2. Bannister, L.H., Hopkins, J.M., Fowler, R.E., Krishna, S., and Mitchell, G.H. (2000) Ultrastructure of rhoptry development in Plasmodium falciparum erythrocytic schizonts. Parasitology 121: 273-287.
3. Beckers, C.J.M., Dubremetz, J.F., Mercereau-Puijalon, O., and Joiner, K.A. (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.
4. Blackman, M.J., Fujioka, H., Stafford, W.H., Sajid, M., Clough, B., Fleck, S.L., et al. (1998) A subtilisin-like protein in secretory organelles of Plasmodium falciparum merozoites. J Biol Chem 273: 23398-23409.
5. Blott, E.J., and Griffiths, G.M. (2002) Secretory lysosomes. Nature Rev Mol Cell Biol 2002 (3): 122-131.
6. Boehm, M., and Bonifacino, J.S. (2001) Adaptins. The final recount. Mol Biol Cell 12: 2907-2920.
7. Bouchot, A., Jaillet, J.D., Bonhomme, A., Alessandro, N.P., Laquerriere, P., Kilian, L., et al. (2001) Detection and localization of a Ca2+-ATPase activity in Toxoplasma gondii. Cell Struct Funct 26: 49-60.
8. Bradley, P.J., and Boothroyd, J.C. (1999) Identification of the pro-mature processing site of Toxoplasma ROP1 by mass spectrometry. Mol Biochem Parasitol 100: 103-109.
9. Bradley, P.J., and Boothroyd, J.C. (2001) The pro region of Toxoplasma ROP1 is a rhoptry-targeting signal. Int J Parasitol 31: 1177-1186.
10. Braun-Breton, C., Rosenberry, T.L., and da Silva, L.P. (1988) Induction of the proteolytic activity of a membrane protein in Plasmodium falciparum by phosphatidyl inositol-specific phospholipase C. Nature 332: 457-459.
11. Burgoyne, R.D., and Morgan, A. (2003) Secretory granule exocytosis. Physiol Rev 83: 581-632.
12. Conseil, V., Soete, M., and Dubremetz, J.F. (1999) Serine protease inhibitors block invasion of host cells by Toxoplasma gondii. Antimicrob Agents Chemother 43: 1358-1361.
13. Coppens, I., and Joiner, K.A. (2003) Host but not parasite cholesterol controls Toxoplasma entry by modulating organelle discharge. Mol Biol Cell 14: 3804-3820.
14. Denzer, K., Kleijmeer, M.J., Heijnen, H.F., Stoorvogel, W., and Geuze, H.J. (2000) Exosome: from internal vesicle of the multivesicular body to intercellular signaling device. J Cell Sci 113: 3365-3374.
15. Etzion, Z., Murray, M., and Perkins, M. (1991) Isolation and characterization of rhoptries of Plasmodium falciparum. Mol Biochem Parasitol 47: 51-62.
16. Foussard, F., Leriche, M.A., and Dubremetz, J.F. (1991) Characterization of the lipid content of Toxoplasma gondii rhoptries. Parasitalogy 102: 367-370.
17. Glombik, M.M., and Gerdes, H.H. (2000) Signal-mediated sorting of neuropeptides and prohormones: secretory granule biogenesis revisited. Biochimie 82: 315-326.
18. Hackett, F., Sajid, M., Withers-Martinez, C., Grainger, M., and Blackman, M.J. (1999) PfSUB-2: a second subtilisin-like protein in Plasmodium falciparum merozoites. Mol Biochem Parasitol 103: 183-195.
19. Hakansson, S., Charron, A.J., and Sibley, L.D. (2001) Toxoplasma evacuoles: a two-step process of secretion and fusion forms the parasitophorous vacuole. EMBO J 20: 3132-3144.
20. Hausmann, K. (1978) Extrusive organelles in protists. Int Rev Cytol 25: 197-276.
21. He, C.Y., Shaw, M.K., Pletcher, C.H., Striepen, B., Tilney, L.G., and Roos, D.S. (2001) A plastid segregation defect in the protozoan parasite Toxoplasma gondii. EMBO J 20: 330-339.
22. Hiller, N.L., Akompong, T., Morrow, J.S., Holder, A.A., and Haldar, K. (2003) Identification of a stomatin orthologue in vacuoles induced in human erythrocytes by malaria parasites: a role for microbial raft-protein in apicomplexan vacuole biogenesis. J Biol Chem 278: 48413-48421.
23. Hoppe, H.C., Ngo, H.M., Yang, M., and Joiner, K.A. (2000) Targeting to rhoptry organelles of Toxoplasma gondii involves evolutionary conserved mechanisms. Nature Cell Biol 2: 449-456.
24. Howard, R.F., and Schmidt, C.M. (1995) The secretary pathway of Plasmodium falciparum regulates transport of p82/RAP1 to the rhoptries. Mol Biochem Parasitol 74: 43-54.
25. Huete-Perez, J.A., Engel, J.C., Brinen, L.S., Mottram, J.C., and McKerrow, J.H. (1999) Protease trafficking in two primitive eukaryotes is mediated by a prodomain protein motif. J Biol Chem 274: 16249-16256.
26. Joiner, K.A., and Roos, D.S. (2002) Secretory traffic in the eukaryotic parasite Toxoplasma gondii: less is more. J Cell Biol 157: 557-563.
27. Laslop, A., Weiss, C., Savaria, D., Eiter, C., Tooze, S.A., Seidah, N.G., and Winkler, H. (1998) Proteolytic processing of chromogranin B and secretogranin II by prohormone convertases. J Neurochem 70: 374-383.
28. Luzio, J.P., Poupon, V., Lindsay, M.R., Mullock, B.M., Piper, R.C., and Pryor, P.R. (2003) Membrane dynamics and the biogenesis of lysosomes. Mol Membr Biol 20: 141-154.
29. McIntyre, G.F., and Erickson, A.M. (1993) The lysosomal proenzyme receptor that binds procathepsin L to microsomal membranes at pH 5 is a 43-kDa integral membrane protein. Proc Natl Acad Sci USA 90: 10588-10592.
30. Miller, S.A., Binder, E.M., Blackman, M.J., Carruthers, V.B., and Kim, K. (2001) A conserved subtilisin-like protein TgSUB1 in microneme organelles of Toxoplasma gondii. J Biol Chem 276: 45341-45348.
31. Miller, S.A., Thathy, V., Ajoika, J.W., Blackman, M.J., and Kim, K. (2003) TgSUB2 is a Toxoplasma gondii rhoptry organelle processing proteinase. Mol Microbiol 49: 883-894.
32. Nakaar, V., Ngô, H.M., Aronson, E.P., Coppens, I., Stedman, T.T., and Joiner, K.A. (2002) Pleiotropic effect due to targeted depletion of secretory rhoptry protein ROP2 in Toxoplasma gondii. J Cell Sci 116: 2311-2320.
33. Ngô, H., Hoppe, H.C., and Joiner, K.A. (2000) Differential sorting and post-secretory targeting of proteins in parasitic invasion. Trends Cell Biol 10: 67-72.
34. Ngô, H.M., Yang, M., Pypaert, M., Hoppe, H.C., and Joiner, K.A. (2003) Biogenesis of secretory organelles in an apicomplexan parasite is dependent on the AP-1 adaptin. J Biol Chem 278: 5343-5352.
35. Palade, G. (1975) Intracellular aspects of the process of protein synthesis. Science 189: 347-358.
36. Pelletier, L., Stern, C.A., Pypaert, M., Sheff, D., Ngo, H.M., Roper, N., et al. (2002) Golgi biogenesis in Toxoplasma gondii. Nature 418: 548-552.
37. Plattner, H., and Kissmehl, R. (2003) Molecular aspects of membrane trafficking in paramecium. Int Rev Cytol 232: 185-216.
38. Preiser, P., Kaviratne, M., Khan, S., Bannister, L., and Jarra, W. (2000) The apical organelles of malaria merozoites: host cell selection, invasion, host immunity and immune evasion. Microbes Infect 2: 1461-1477.
39. Que, X., Ngo, H., Lawton, J., Gray, M., Liu, Q., Engel, J., et al. (2002) The cathepsin B of Toxoplasma gondii, toxopain-1, is critical for parasite invasion and rhoptry protein processing. J Biol Chem 277: 25791-25797.
40. Reichmann, G., Dlugonska, H., and Fischer, H.G. (2002) Characterization of TgROP9 (p36), a novel rhoptry protein of Toxoplasma gondii tachyzoites identified by T cell clone. Mol Biochem Parasitol 119: 43-54.
41. Robibaro, B., Hoppe, H.C., Yang, M., Coppens, I., Ngo, H.M., Stedman, T.T., et al. (2001) Endocytosis in different lifestyles of protozoan parasitism: role in nutrient uptake with special reference to Toxoplasma gondii. Int J Parasitol 31: 1343-1353.
42. Robibaro, B., Stedman, T.T., Coppens, I., Ngo, H.M., Pypaert, M., Bivona, T., et al. (2002) Toxoplasma gondii Rab5 enhances cholesterol acquisition from host cells. Cell Microbiol 4: 139-152.
43. Rosenthal, P.J. (1999) Proteases of protozoan parasites. Adv Parasitol 43: 105-159.
44. Saffer, L.D., Mercereau-Puijalon, O., Dubremetz, J.F., and Schwartzman, J. (1992) Localization of a Toxoplasma gondii rhoptry protein by immunoelectron microscopy during and after host cell penetration. J Protozool 39: 526-530.
45. Sam-Yellowe, T.Y. (1996) Rhoptry organelles of the apicomplexa: their role in host cell invasion and intracellular survival. Parasitol Today 12: 308-316.
46. Shaw, M.K., Roos, D.S., and Tilney, L.G. (1998) Acidic compartments and rhoptry formation in Toxoplasma gondii. Parasitol 117: 435-443.
47. Shaw, M.K., Roos, D.S., and Tilney, L.G. (2002) Cysteine and serine protease inhibitors block intracellular development and disrupt the secretory pathway of Toxoplasma gondii. Microbes Infect 4: 119-132.
48. Sinai, A.P., and Joiner, K.A. (2001) The Toxoplasma gondii protein ROP2 mediates host organelle association with the parasitophorous vacuole membrane. J Cell Biol 154: 95-108.
49. Soldati, D. (1998) Processing of Toxoplasma ROP1 protein in nascent rhoptries. Mol Biochem Parasitol 96: 37-48.
50. Soldati, D., Kim, K., Kampmeier, J., Dubremetz, J.F., and Boothroyd, J.C. (1995) Complementation of a Toxoplasma gondii ROP1 knock-out mutant using phleomycin selection. Mol Biochem Parasitol 74: 87-97.
51. Storrie, B. (1988) Assembly of lysosomes: perspectives from comparative molecular cell biology. Int Rev Cytol 111: 53-105.
52. Striepen, B., Soldati, D., Garcia-Reguet, N., Dubremetz, J.F., and Roos, D.S. (2001) Targeting of soluble proteins to the rhoptries and micronemes in Toxoplasma gondii. Mol Biochem Parasitol 113: 45-63.
53. Suss-Toby, E., Zimmerberg, J., and Ward, G.E. (1996) Toxoplasma invasion: the parasitophorous vacuole is formed from host cell plasma membrane and pinches off via a fission pore. Proc Natl Acad Sci USA 93: 8413-8418.
54. Topolska, A.E., Lidgett, A., Truman, D., Fujioka, H., and Coppel, R.L. (2003) Characterisation of a membrane-associated rhoptry protein of Plasmodium falciparum. J Biol Chem 279: 4648-4656.
55. Wubbolts, R., Leckie, R.S., Veenhuizen, P.T., Schwarzmann, G., Mobius, W., Hoernschemeyer, J., et al. (2003) Proteomic and biochemical analyses of human B cell-derived exosomes. Potential implications for their function and multivesicular body formation. J Biol Chem 278: 10963-10972.
56. Yang, M., Coppens, I., Wormsley, S., Baevova, P., Hoppe, H.C., and Joiner, K.A. (2004) The Plasmodium falciparum Vps4 homolog mediates multivesicular body formation. J Cell Sci (in press).