Secretory protein trafficking in Giardia intestinalis

Molecular Microbiology

Volumn 53, Issue 1, 2004, Pages 19-28

  Hehl, Adrian B ^a   Marti, Matthias ^b  

^a UNIVERSITY OF ZURICH   (Switzerland)

^b WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

PROTOZOAL PROTEIN; SECRETORY PROTEIN;

CELL MEMBRANE; CELL NUCLEUS; CELL ORGANELLE; CELL STRUCTURE; CELL SURFACE; CYTOARCHITECTURE; GIARDIA LAMBLIA; INTRACELLULAR SPACE; INTRACELLULAR TRANSPORT; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN TARGETING; PROTEIN TRANSPORT; PROTOZOON; REGULATORY MECHANISM; SHORT SURVEY; SIGNAL TRANSDUCTION; TROPHOZOITE;

ANIMALS; CELL COMPARTMENTATION; GIARDIA LAMBLIA; HUMANS; PROTEIN TRANSPORT; PROTOZOAN PROTEINS; SECRETORY VESICLES;

EUKARYOTA; GIARDIA; GIARDIA INTESTINALIS; PROTOZOA;

EID: 3142518032     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2004.04115.x     Document Type: Short Survey

References (67)

1. Adam, R.D. (2001) Biology of Giardia lamblia. Clin Microbiol Rev 14: 447-475.
2. Adam, R.D., Aggarwal, A., Lal, A.A., de La Cruz, V.F., McCutchan, T., and Nash, T.E. (1988) Antigenic variation of a cysteine-rich protein in Giardia lamblia. J Exp Med 167: 109-118.
3. Bauer, B., Engelbrecht, S., Bakker-Grunwald, T., and Scholze, H. (1999) Functional identification of alpha 1-giardin as an annexin of Giardia lamblia. FEMS Microbiol Lett 173: 147-153.
4. Benchimol, M. (2002) A new set of vesicles in Giardia lamblia. Exp Parasitol 102: 30-37.
5. Boll, W., Ohno, H., Songyang, Z., Rapoport, I., Cantley, L.C., Bonifacino, J.S., and Kirchhausen, T. (1996) Sequence requirements for the recognition of tyrosine-based endocytic signals by clathrin AP-2 complexes. EMBO J 15: 5789-5795.
6. Bonifacino, J.S., and Dell'Angelica, E.C. (1999) Molecular bases for the recognition of tyrosine-based sorting signals. J Cell Biol 145: 923-926.
7. Bonifacino, J.S., and Traub, L.M. (2003) Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu Rev Biochem 72: 395-447.
8. Brugerolle, G. (1974) Contribution a l'étude cytologique et phylétique des diplozaires (zoomastigophorea, diplozoa, Dangeard 1910). III. Etude ultrastructurale du genre Hexamita (Dujardin 1836). Protistologica 10: 83-90.
9. Canfield, W.M., Johnson, K.F., Ye, R.D., Gregory, W., and Kornfeld, S. (1991) Localization of the signal for rapid internalization of the bovine cation-independent mannose 6-phosphate/insulin-like growth factor-II receptor to amino acids 24-29 of the cytoplasmic tail. J Biol Chem 266: 5682-5688.
10. Cavalier-Smith, T. (1989) Molecular phylogeny. Archaebacteria and Archezoa. Nature 339: 100-101.
11. Cavalier-Smith, T., and Chao, E.E. (1996) Molecular phylogeny of the free-living archezoan Trepomonas agilis and the nature of the first eukaryote. J Mol Evol 43: 551-562.
12. Dacks, J.B., Davis, L.A., Sjogren, A.M., Andersson, J.O., Roger, A.J., and Doolittle, W.F. (2003) Evidence for Golgi bodies in proposed 'Golgi-lacking' lineages. Proc R Soc London B Biol Sci 270 (Suppl. 2): S168-S171.
13. Das, S., Traynor-Kaplan, A., Reiner, D.S., Meng, T.C., and Gillin, F.D. (1991) A surface antigen of Giardia lamblia with a glycosylphosphatidylinositol anchor. J Biol Chem 266: 21318-21325.
14. Das, S., Traynor-Kaplan, A., Kachintorn, U., Aley, S.B., and Gillin, F.D. (1994) GP49, an invariant GPI-anchored antigen of Giardia lamblia. Braz J Med Biol Res 27: 463-469.
15. Eichinger, D. (2001) Encystation in parasitic protozoa. Curr Opin Microbiol 4: 421-426.
16. Einfeld, D.A., and Stibbs, H.H. (1984) Identification and characterization of a major surface antigen of Giardia lamblia. Infect Immun 46: 377-383.
17. Elmendorf, H.G., Singer, S.M., and Nash, T.E. (2000) Targeting of proteins to the nuclei of Giardia lamblia. Mol Biochem Parasitol 106: 315-319.
18. Embley, T.M., and Hirt, R.P. (1998) Early branching eukaryotes? Curr Opin Genet Dev 8: 624-629.
19. Erlandsen, S.L., Macechko, P.T., van Keulen, H., and Jarroll, E.L. (1996) Formation of the Giardia cyst wall: studies on extracellular assembly using immunogold labeling and high resolution field emission SEM. J Eukaryot Microbiol 43: 416-429.
20. Feely, D.E., and Dyer, J.K. (1987) Localization of acid phosphatase activity in Giardia lamblia and Giardia muris trophozoites. J Protozool 34: 80-83.
21. Gillin, F.D., Hagblom, P., Harwood, J., Aley, S.B., Reiner, D.S., McCaffery, M., et al. (1990) Isolation and expression of the gene for a major surface protein of Giardia lamblia. Proc Natl Acad Sci USA 87: 4463-4467.
22. Gu, F., Crump, C.M., and Thomas, G. (2001) Trans-Golgi network sorting. Cell Mol Life Sci 58: 1067-1084.
23. Hedges, S.B. (2002) The origin and evolution of model organisms. Nature Rev Genet 3: 838-849.
24. Hedges, S.B., Chen, H., Kumar, S., Wang, D.Y., Thompson, A.S., and Watanabe, H. (2001) A genomic timescale for the origin of eukaryotes. BMC Evol Biol 1: 4.
25. Hehl, A.B., Marti, M., and Kohler, P. (2000) Stage-specific expression and targeting of cyst wall protein-green fluorescent protein chimeras in Giardia. Mol Biol Cell 11: 1789-1800.
26. Knodler, L.A., Noiva, R., Mehta, K., McCaffery, J.M., Aley, S.B., Svard, S.G., et al. (1999) Novel protein-disulfide isomerases from the early-diverging protist Giardia lamblia. J Biol Chem 274: 29805-29811.
27. Lane, S., and Lloyd, D. (2002) Current trends in research into the waterborne parasite Giardia. Crit Rev Microbiol 28: 123-147.
28. Lanfredi-Rangel, A., Attias, M., de Carvalho, T.M., Kattenbach, W.M., and De Souza, W. (1998) The peripheral vesicles of trophozoites of the primitive protozoan Giardia lamblia may correspond to early and late endosomes and to lysosomes. J Struct Biol 123: 225-235.
29. Lanfredi-Rangel, A., Attias, M., Reiner, D.S., Gillin, F.D., and De Souza, W. (2003) Fine structure of the biogenesis of Giardia lamblia encystation secretory vesicles. J Struct Biol 143: 153-163.
30. Langford, T.D., Silberman, J.D., Weiland, M.E., Svard, S.G., McCaffery, J.M., Sogin, M.L., and Gillin, F.D. (2002) Giardia lamblia: identification and characterization of Rab and GDI proteins in a genome survey of the ER to Golgi endomembrane system. Exp Parasitol 101: 13-24.
31. Lev, B., Ward, H., Keusch, G.T., and Pereira, M.E. (1986) Lectin activation in Giardia lamblia by host protease: a novel host-parasite interaction. Science 232: 71-73.
32. Lloyd, D., and Harris, J.C. (2002) Giardia: highly evolved parasite or early branching eukaryote? Trends Microbiol 10: 122-127.
33. Lujan, H.D., Marotta, A., Mowatt, M.R., Sciaky, N., Lippincott-Schwartz, J., and Nash, T.E. (1995a) Developmental induction of Golgi structure and function in the primitive eukaryote Giardia lamblia. J Biol Chem 270: 4612-4618.
34. Lujan, H.D., Mowatt, M.R., Conrad, J.T., Bowers, B., and Nash, T.E. (1995b) Identification of a novel Giardia lamblia cyst wall protein with leucine-rich repeats. Implications for secretory granule formation and protein assembly into the cyst wall. J Biol Chem 270: 29307-29313.
35. Lujan, H.D., Mowatt, M.R., Conrad, J.T., and Nash, T.E. (1996) Increased expression of the molecular chaperone BiP/GRP78 during the differentiation of a primitive eukaryote. Biol Cell 86: 11-18.
36. Lujan, H.D., Mowatt, M.R., and Nash, T.E. (1997) Mechanisms of Giardia lamblia differentiation into cysts. Microbiol Mol Biol Rev 61: 294-304.
37. McArthur, A.G., Morrison, H.G., Nixon, J.E., Passamaneck, N.Q., Kim, U., Hinkle, G., et al. (2000) The Giardia genome project database. FEMS Microbiol Lett 189: 271-273.
38. McArthur, A.G., Knodler, L.A., Silberman, J.D., Davids, B.J., Gillin, F.D., and Sogin, M.L. (2001) The evolutionary origins of eukaryotic protein disulfide isomerase domains: new evidence from the amitochondriate protist Giardia lamblia. Mol Biol Evol 18: 1455-1463.
39. McCaffery, J.M., and Gillin, F.D. (1994) Giardia lamblia: ultrastructural basis of protein transport during growth and encystation. Exp Parasitol 79: 220-235.
40. McCaffery, J.M., Faubert, G.M., and Gillin, F.D. (1994) Giardia lamblia: traffic of a trophozoite variant surface protein and a major cyst wall epitope during growth, encystation, and antigenic switching. Exp Parasitol 79: 236-249.
41. Marti, M., and Hehl, A.B. (2003) Encystation-specific vesicles in Giardia: a primordial Golgi or just another secretory compartment? Trends Parasitol 19: 440-446.
42. Marti, M., Li, Y., Kohler, P., and Hehl, A.B. (2002) Conformationally correct expression of membrane-anchored Toxoplasma gondii SAG1 in the primitive protozoan Giardia duodenalis. Infect Immun 70: 1014-1016.
43. Marti, M., Li, Y., Schraner, E.M., Wild, P., Kohler, P., and Hehl, A.B. (2003a) The secretory apparatus of an ancient eukaryote: protein sorting to separate export pathways occurs before formation of transient Golgi-like compartments. Mol Biol Cell 14: 1433-1447.
44. Marti, M., Regos, A., Li, Y., Schraner, E.M., Wild, P., Muller, N., et al. (2003b) An ancestral secretory apparatus in the protozoan parasite Giardia intestinalis. J Biol Chem 278: 24837-24848.
45. Mowatt, M.R., Lujan, H.D., Gotten, D.B., Bowers, B., Yee, J., Nash, T.E., and Stibbs, H.H. (1995) Developmentally regulated expression of a Giardia lamblia cyst wall protein gene. Mol Microbiol 15: 955-963.
46. Nash, T.E., and Mowatt, M.R. (1992) Characterization of a Giardia lamblia variant-specific surface protein (VSP) gene from isolate GS/M and estimation of the VSP gene repertoire size. Mol Biochem Parasitol 51: 219-227.
47. Nash, T.E., Gillin, F.D., and Smith, P.D. (1983) Excretory-secretory products of Giardia lamblia. J Immunol 131: 2004-2010.
48. Nash, T.E., Aggarwal, A., Adam, R.D., Conrad, J.T., and Merritt, J.W., Jr (1988) Antigenic variation in Giardia lamblia. J Immunol 141: 636-641.
49. Owen, D.J., and Evans, P.R. (1998) A structural explanation for the recognition of tyrosine-based endocytotic signals. Science 262: 1327-1332.
50. Papanastasiou, P., Hiltpold, A., Bommeli, C., and Kohler, P. (1996) The release of the variant surface protein of Giardia to its soluble isoform is mediated by the selective cleavage of the conserved carboxy-terminal domain. Biochemistry 35: 10143-10148.
51. 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.
52. Reiner, D.S., McCaffery, M., and Gillin, F.D. (1990) Sorting of cyst wall proteins to a regulated secretory pathway during differentiation of the primitive eukaryote, Giardia lamblia. Eur J Cell Biol 53: 142-153.
53. Reiner, D.S., McCaffery, J.M., and Gillin, F.D. (2001) Reversible interruption of Giardia lamblia cyst wall protein transport in a novel regulated secretory pathway. Cell Microbiol 3: 459-472.
54. Roger, A.J., Svard, S.G., Tovar, J., Clark, C.G., Smith, M.W., Gillin, F.D., and Sogin, M.L. (1998) A mitochondrial-like chaperonin 60 gene in Giardia lamblia: evidence that diplomonads once harbored an endosymbiont related to the progenitor of mitochondria. Proc Natl Acad Sci USA 95: 229-234.
55. Rohrer, J., Schweizer, A., Russell, D., and Kornfeld, S. (1996) The targeting of Lamp1 to lysosomes is dependent on the spacing of its cytoplasmic tail tyrosine sorting motif relative to the membrane. J Cell Biol 132: 565-576.
56. Sogin, M.L., Gunderson, J.H., Elwood, H.J., Alonso, R.A., and Peattie, D.A. (1989) Phylogenetic meaning of the kingdom concept: an unusual ribosomal RNA from Giardia lamblia. Science 243: 75-77.
57. Soltys, B.J., Falah, M., and Gupta, R.S. (1996) Identification of endoplasmic reticulum in the primitive eukaryote Giardia lamblia using cryoelectron microscopy and antibody to Bip. J Cell Sci 109: 1909-1917.
58. Subramanian, A.B., Navarro, S., Carrasco, R.A., Marti, M., and Das, S. (2000) Role of exogenous inositol and phosphatidylinositol in glycosylphosphatidylinositol anchor synthesis of GP49 by Giardia lamblia. Biochim Biophys Acta 1483: 69-80.
59. Sun, C.H., McCaffery, J.M., Reiner, D.S., and Gillin, F.D. (2003) Mining the Giardia lamblia genome for new cyst wall proteins. J Biol Chem 278: 21701-21708.
60. Svard, S.G., Rafferty, C., McCaffery, J.M., Smith, M.W., Reiner, D.S., and Gillin, F.D. (1999) A signal recognition particle receptor gene from the early-diverging eukaryote, Giardia lamblia. Mol Biochem Parasitol 98: 253-264.
61. Svard, S.G., Hagblom, P., and Palm, J.E. (2003) Giardia lamblia - a model organism for eukaryotic cell differentiation. FEMS Microbiol Lett 218: 3-7.
62. Touz, M.C., Mores, M.J., Slavin, I., Carmona, C., Conrad, J.T., Mowatt, M.R., et al. (2002a) The activity of a developmentally regulated cysteine proteinase is required for cyst wall formation in the primitive eukaryote Giardia lamblia. J Biol Chem 277: 8474-8481.
63. Touz, M.C., Gottig, N., Nash, T.E., and Lujan, H.D. (2002b) Identification and characterization of a novel secretory granule calcium-binding protein from the early branching eukaryote Giardia lamblia. J Biol Chem 277: 50557-50563.
64. Touz, M.C., Lujan, H.D., Hayes, S.F., and Nash, T.E. (2003) Sorting of encystation-specific cysteine protease to lysosome-like peripheral vacuoles in Giardia lamblia requires a conserved tyrosine-based motif. J Biol Chem 278: 6420-6426.
65. Tovar, J., Leon-Avila, G., Sanchez, L.B., Sutak, R., Tachezy, J., Van DerGiezen, M., et al. (2003) Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature 426: 172-176.
66. Ward, H.D., Keusch, G.T., and Pereira, M.E. (1990) Induction of a phosphomannosyl binding lectin activity in Giardia. Bioessays 12: 211-215.
67. Weiland, M.E., Palm, J.E., Griffiths, W.J., McCaffery, J.M., and Svard, S.G. (2003) Characterisation of alpha-1 giardin: an immunodominant Giardia lamblia annexin with glycosaminoglycan-binding activity. Int J Parasitol 33: 1341-1351.