A contiguous compartment functions as endoplasmic reticulum and endosome/lysosome in Giardia lamblia

Eukaryotic Cell

Volumn 8, Issue 11, 2009, Pages 1665-1676

  Abodeely, Maria ^a,b   Dubois, Kelly N ^a,b   Hehl, Adrian ^c   Stefanie, Sasa ^a,c   Sajid, Mohammed ^a   Desouza, Wanderley ^d   Attias, Mareia ^d   Engel, Juan C ^a   Hsieh, Ivy ^a   Fetter, Richard D ^a   McKerrow, James H ^a  

^a Sandler Center for Basic Research in Parasitic Diseases   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

PROTOZOAL PROTEIN;

ARTICLE; ENDOPLASMIC RETICULUM; ENDOSOME; GENETICS; GIARDIA LAMBLIA; LYSOSOME; METABOLISM; ULTRASTRUCTURE;

ENDOPLASMIC RETICULUM; ENDOSOMES; GIARDIA LAMBLIA; LYSOSOMES; PROTOZOAN PROTEINS;

EUKARYOTA; GIARDIA; GIARDIA INTESTINALIS; MAMMALIA; PROTOZOA;

EID: 72449160258     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00123-09     Document Type: Article

References (47)

1. Adam, R. D. 2001. Biology of Giardia lamblia. Clin. Microbiol. Rev. 14:447-475.
2. Alberts, B. 2002. Molecular biology of the cell. Garland Science, New York, NY.
3. Baldauf, S. L. 2003. The deep roots of eukaryotes. Science 300:1703-1706.
4. Benchimol, M. 2004. Giardia lamblia: behavior of the nuclear envelope. Parasitol. Res. 94:254-264.
5. Benchimol, M., B. Piva, L. Campanati, and W. de Souza. 2004. Visualization of the funis of Giardia lamblia by high-resolution field emission scanning electron microscopy-new insights. J. Struct. Biol. 147:102-115.
6. Dacks, J. B., and M. C. Field. 2007. Evolution of the eukaryotic membranetrafficking system: origin, tempo and mode. J. Cell Sci. 120:2977-2985.
7. Day, P. M., J. W. Yewdell, A. Poigador, R. N. Germain, and J. R. Bennink. 1997. Direct delivery of exogenous MHC class I molecule-binding oligopeptides to the endoplasmic reticulum of viable cells. Proc. Natl. Acad. Sci. USA 94:8064-8069.
8. de Meester, F., E. Shaw, H. Scholze, T. Stolarsky, and D. Mirelman. 1990. Specific labeling of cysteine proteinases in pathogenic and nonpathogenic Entamoeba histolytica. Infect. Immun. 58:1396-1401.
9. DuBois, K. N., M. Abodeely, J. Sakanari, C. S. Craik, M. Lee, J. H. McKerrow, and M. Sajid. 2008. Identification of the major cysteine protease of Giardia and its role in encystation. J. Biol. Chem. 283:18024-18031.
10. Federovitch, C. M., D. Ron, and R. Y. Hampton. 2005. The dynamic ER: experimental approaches and current questions. Curr. Opin. Cell Biol. 17: 409-414.
11. 11. Gagnon, E., S. Duelos, C. Rondeau, E. Chevet, P. H. Cameron, O. SteeleMortimer, J. Paiement, J. J. Bergeron, and M. Desjardins. 2002. Endoplasmic reticulum-mediated phagocytosis is a mechanism of entry into macrophages. Cell 110:119-131. (Pubitemid 34874611)
12. Gething, M. J., and J. Sambrook. 1992. Protein folding in the cell. Nature 355:33-45.
13. Gillin, F. D., S. E. Boucher, S. S. Rossi, and D. S. Reiner. 1989. Giardia lamblia: the roles of bile, lactic acid, and pH in the completion of the life cycle in vitro. Exp. Parasitol. 69:164-174.
14. Gillin, F. D., D. S. Reiner, M. J. Gault, H. Douglas, S. Das, A. Wunderlich, and J. F. Sauch. 1987. Encystation and expression of cyst antigens by Giardia lamblia in vitro. Science 235:1040-1043.
15. Gupta, R. S., K. Aitken, M. Falah, and B. Singh. 1994. Cloning of Giardia lamblia heat shock protein HSP70 homologs: implications regarding origin of eukaryotic cells and of endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 91:2895-2899.
16. 16. Hashimoto, T., Y. Nakamura, F. Nakamura, T. Shirakura, J. Adachi, N. Goto, K. Okamoto, and M. Hasegawa. 1994. Protein phylogeny gives a robust estimation for early divergences of eukaryotes: phylogenetic place of a mitochondria-lacking protozoan, Giardia lamblia. Mol. Biol. Evol. 11:65-71. (Pubitemid 24034124)
17. Hedges, S. B. 2002. The origin and evolution of model organisms. Nat. Rev. Genet. 3:838-849.
18. 18. Hernandez, Y., C. Castillo, S. Roychowdhury, A. Hehl, S. B. Aley, and S. Das. 2007. Clathrin-dependent pathways and the cytoskeleton network are involved in ceramide endocytosis by a parasitic protozoan, Giardia lamblia. Int. J. Parasitol. 37:21-32. (Pubitemid 44958559)
19. 19. Kartenbeck, J., H. Stukenbrok, and A. Helenius. 1989. Endocytosis of simian virus 40 into the endoplasmic reticulum. J. Cell Biol. 109:2721-2729. (Pubitemid 20011899)
20. 20. Knodler, L. A., R. Noiva, K. Mehta, J. M. McCaffery, S. B. Aley, S. G. Svard, T. G. Nystul, D. S. Reiner, J. D. Silberman, and F. D. Gillin. 1999. Novel protein-disulfide isomerases from the early-diverging protist Giardia lamblia. J. Biol. Chem. 274:29805-29811. (Pubitemid 29483355)
21. Kulda, J., and E. Nohynkova. 1996. Giardia in humans and animals, p. 225-422. In J. Kreier (ed.), Parasitic protozoa, 2nd ed. Academic Press, San Diego, CA.
22. Lanfredi-Rangel, A., M. Attias, T. M. de Carvalho, W. M. Kattenbach, and W. De Souza. 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.
23. Lanfredi-Rangel, A., M. Attias, D. S. Reiner, F. D. Gillin, and W. De Souza. 2003. Fine structure of the biogenesis of Giardia lamblia encystation secretory vesicles. J. Struct. Biol. 143:153-163.
24. Lewis, P. R., and D. P. Knight. 1996. Staining methods for section matrial. Elsevier Biomedical Press, Amsterdam, The Netherlands.
25. 25. Lord, J. M., and L. M. Roberts. 1998. Toxin entry: retrograde transport through the secretory pathway. J. Cell Biol. 140:733-736. (Pubitemid 28141213)
26. Marti, M., A. Regos, Y. Li, E. M. Schraner, P. Wild, N. Müller, L. G. Knopf, and A. B. Hehl. 2003. An ancestral secretory apparatus in the protozoan parasite Giardia intestinalis. J. Biol. Chem. 278:24837-24848.
27. McCaffery, J. M., and F. D. Gillin. 1994. Giardia lamblia: ultrastructural basis of protein transport during growth and encystation. Exp. Parasitol. 79:220-235.
28. Morgan, G. W., B. S. Hall, P. W. Denny, M. Carrington, and M. C. Field. 2002. The kinetoplastida endocytic apparatus. Fart I. A dynamic system for nutrition and evasion of host defences. Trends Parasitol. 18:491-496.
29. Mottram, J., M. J. North, and M. Sajid. 2004. Trichomonad and Giardia cysteine endopeptidases, p. 1170-1173. In N. D. Rawlings, A. J. Barrett, and J. F. Woessner (ed.), Handbook of proteolytic enzymes. Academic Press, London, United Kingdom.
30. 30. Nishikawa, S., J. L. Brodsky, and K. Nakatsukasa. 2005. Roles of molecular chaperones in endoplasmic reticulum (ER) quality control and ER-associated degradation (ERAD). J. Biochem. 137:551-555. (Pubitemid 40874532)
31. Paulsson, K., and P. Wang. 2003. Chaperones and folding of MHC class I molecules in the endoplasmic reticulum. Biochim. Biophys. Acta 1641:1-12.
32. Perret, E., A. Lakkaraju, S. Deborde, R. Schreiner, and E. Rodriguez-Boulan. 2005. Evolving endosomes: how many varieties and why? Curr. Opin. Cell Biol. 17:423-434.
33. Porter, K. R. 1953. Observations on a submicroscopic basophilic component of cytoplasm. J. Exp. Med. 97:727-750.
34. Reiner, D. S., H. Douglas, and F. D. Gillin. 1989. Identification and localization of cyst-specific antigens of Giardia lamblia. Infect. Immun. 57:963-968.
35. Roger, A. J., H. G. Morrison, and M. L. Sogin. 1999. Primary structure and phylogenetic relationships of a malate dehydrogenase gene from Giardia lamblia. J. Mol. Evol. 48:750-755.
36. 36. Sandvig, K., and B. van Deurs. 2002. Transport of protein toxins into cells: pathways used by ricin, cholera toxin and Shiga toxin. FEBS Lett. 529:49-53. (Pubitemid 35283911)
37. Singer, S. M., J. Yee, and T. E. Nash. 1998. Episomal and integrated maintenance of foreign DNA in Giardia lamblia. Mol. Biochem. Parasitol. 92:59-69.
38. Sogin, M. L., J. H. Gunderson, H. J. Elwood, R. A. Alonso, and D. A. Peattie. 1989. Phylogenetic meaning of the kingdom concept: an unusual ribosomal RNA from Giardia lamblia. Science 243:75-77.
39. Soltys, B. J., M. Falah, and R. S. Gupta. 1996. Identification of endoplasmic reticulum in the primitive eukaryote Giardia lamblia using cryoelectron microscopy and antibody to Bip. J. Cell Sci. 109:1909-1917.
40. 40. Stefanic, S., D. Palm, S. G. Svard, and A. B. Hehl. 2006. Organelle proteomics reveals cargo maturation mechanisms associated with Golgi-like encystation vesicles in the early-diverged protozoan Giardia lamblia. J. Biol. Chem. 281:7595-7604. (Pubitemid 43847530)
41. Tai, J. H., S. J. Ong, S. C. Chang, and H. M. Su. 1993. Giardiavirus enters Giardia lamblia WB trophozoite via endocytosis. Exp. Parasitol. 76:165-174.
42. Touret, N., P. Paroutis, M. Terebiznik, R. E. Harrison, S. Trombetta, M. Pypaert, A. Chow, A. Jiang, J. Shaw, C. Yip, H. P. Moore, N. van der Wel, D. Houben, P. J. Peters, C. de Chastellier, I. Mellman, and S. Grinstein. 2005. Quantitative and dynamic assessment of the contribution of the ER to phagosome formation. Cell 123:157-170.
43. Touz, M. C., L. Kulakova, and T. E. Nash. 2004. Adaptor protein complex 1 mediates the transport of lysosomal proteins from a Golgi-like organelle to peripheral vacuoles in the primitive eukaryote Giardia lamblia. Mol. Biol. Cell 15:3053-3060.
44. Towler, M. C., P. A. Gleeson, S. Hoshino, P. Rahkila, V. Manalo, N. Ohkoshi, C. Ordahl, R. G. Parton, and F. M. Brodsky. 2004. Clathrin isoform CHC22, a component of neuromuscular and myotendinous junctions, binds sorting nexin 5 and has increased expression during myogenesis and muscle regeneration. Mol. Biol. Cell 15:3181-3195.
45. Turk, V., B. Turk, and D. Turk. 2001. Lysosomal cysteine proteases: facts and opportunities. EMBO J. 20:4629-4633.
46. Ward, W., L. Alvarado, N. D. Rawlings, J. C. Engel, C. Franklin, and J. H. McKerrow. 1997. A primitive enzyme for a primitive cell: the protease required for excystation of Giardia. Cell 89:437-444.
47. Zheng, Q. S., M. B. Braunfeld, J. W. Sedat, and D. A. Agard. 2004. An improved strategy for automated electron microscopic tomography. J. Struct. Biol. 147:91-101.