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Contribution of Microscopy to a Better Knowledge of the Biology of Giardia lamblia

Published online by Cambridge University Press:  01 October 2004

Wanderley de Souza ,
Adriana Lanfredi-Rangel  and
Loraine Campanati
Wanderley de Souza
Affiliation:
Laboratório de Ultraestrutura Celular, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, CCS-Bloco G, 21949-900, Rio de Janeiro-RJ, Brazil
Adriana Lanfredi-Rangel
Affiliation:
Laboratório de Ultraestrutura Celular, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, CCS-Bloco G, 21949-900, Rio de Janeiro-RJ, Brazil
Loraine Campanati
Affiliation:
Laboratório de Ultraestrutura Celular, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal do Rio de Janeiro, CCS-Bloco G, 21949-900, Rio de Janeiro-RJ, Brazil
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Abstract

Giardia lamblia is a flagellated protozoan of great medical and biological importance. It is the causative agent of giardiasis, one of the most prevalent diarrheal disease both in developed and third-world countries. Morphological studies have shown that G. lamblia does not present structures such as peroxisomes, mitochondria, and a well-elaborated Golgi complex. In this review, special emphasis is given to the contribution made by various microscopic techniques to a better knowledge of the biology of the protozoan. The application of video microscopy, immunofluorescence confocal laser scanning microscopy, and several techniques associated with transmission electron microscopy (thin section, enzyme cytochemistry, freeze-fracture, deep-etching, fracture-flip) to the study of the cell surface, peripheral vesicles, endoplasmic reticulum–Golgi complex system, and of the encystation vesicles found in trophozoites and during the process of trophozoite-cyst transformation are discussed.

Keywords

Giardia lambliavideo microscopyconfocal laser scanning microscopytransmission electron microscopy
Type
Feature Articles
Information
Microscopy and Microanalysis , Volume 10 , Issue 5 , October 2004 , pp. 513 - 527
Copyright
© 2004 Microscopy Society of America

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References

REFERENCES

Adam, R.D. (1991). The biology of Giardia spp. Microbiol Rev 55, 706–732.Google Scholar
Adam, R.D. (2001). Biology of Giardia lamblia. Clin Microbiol Rev 14, 447–475.Google Scholar
Arguello-Garcia, R., Arguello-Lopez, C., Gonzalez-Robles, A., Castillo-Figueroa, A.M., & Ortega-Pierres, M.G. (2002). Sequential exposure and assembly of cyst wall filaments on the surface of encysting Giardia duodenalis. Parasitology 125, 209–219.Google Scholar
Benchimol, M. (2003). A new set of vesicles in Giardia lamblia. Exp Parasitol 102, 30–37.Google Scholar
Bingham, A.K. & Meyer, E.A. (1979). Giardia excystation can be induced in vitro in acidic solution. Nature 227, 301–302.Google Scholar
Boucher, S.-E.M. & Gillin, F.D. (1990). Excystation of in vitro-derived Giardia lamblia cysts. Infect Immun 58, 3516–3522.Google Scholar
Campanati, L., Holloschi, A., Troester, H., Spring, H., de Souza, W., & Monteiro-Leal, L.H. (2002). Video-microscopy observations of fast dynamic processes in the protozoon Giardia lamblia. Cell Mot Cytosk 51, 213–224.Google Scholar
Chavez, B. & Martinez-Palomo, A. (1995). Giardia lamblia: Freeze-fracture ultrastructure of the ventral disk plasma membrane. J Eukaryot Microbiol 42, 136–141.Google Scholar
Dacks, J.B. & Doolittle, F. (2002). Novel syntaxin gene sequences from Giardia, Trypanosoma and algae: Implications for the ancient evolution of the eukaryotic endomembrane system. J Cell Sci 115, 1635–1642.Google Scholar
Dobell, C. (1932). The discovery of the intestinal protozoa of man. Proc Roy Soc Med 13, 1–15.Google Scholar
Elmendorf, H.G., Dawson, S.C., & McCaffery, J.M. (2002). The cytoskeleton of Giardia lamblia. Int J Parasit 33, 3–28.Google Scholar
Embley, T.M. & Hirt, R.P. (1998). Early-branching eukariotes? Curr Opin Genet Dev 8, 624–629.Google Scholar
Erlandsen, S.L., Berrick, W.J., Schupp, D.E., Shields, J.M., Jarrol, E.L., Sauch, J.F., & Pawley, J.B. (1990). High-resolution immunogold localization of Giardia cyst wall antigens using field emission SEM with secondary and backscatter electron imaging. J Histochem Cytochem 38, 625–632.Google Scholar
Erlandsen, S.L. & Feely, D.E. (1984). Giardia and Giardiasis. Trophozoite motility and the mechanism of attachment. In Giardia and Giardiasis Pathogenesis and Epidemiology, Erlandsen S.L. & Meyer E.A. (Eds.), pp. 33–60. New York: Plenum Press.
Erlandsen, S.L., Macechko, P.T., Van Keulen, H., & Jarrol, E.L. (1996). Formation of Giardia cyst wall: Studies on extracellular assembly using immunogold labeling and high resolution field emission SEM. J Eukaryot Microbiol 43, 416–429.Google Scholar
Faubert, G., Reiner, D.S., & Gillin, F.D. (1991). Giardia lamblia: Regulation of secretory vesicle formation and loss of ability to reattach during excystation in vitro. Exp Parasitol 72, 345–354.Google Scholar
Feely, D.E. & Dyer, J.K. (1987). Localization of acid phosphatase activity in Giardia lamblia and Giardia muris trofozoites. J Protozool 34, 80–83.Google Scholar
Friend, D.S. (1966). The fine structure of Giardia muris. J Cell Biol 29, 317–332.Google Scholar
Gerwig, G.J., Van Kuik, J.A., Leeflang, B.R., Kamerling, J.P., Vliegenthart, J.F., Karr, C.D., & Jarroll, E.L. (2002). The Giardia intestinalis filamentous cyst wall contains a novel beta (1-3)-N-acetyl-D-galactosamine polymer: A structural and conformational study. Glycobiology 12, 499–505.Google Scholar
Gillin, F.D., Reiner, D.S., Gault, M.J., Douglas, H., Das, S., Wunderlich, A., & Sauch, J.F. (1987). Encystation and expression of cyst antigens by Giardia lamblia in vitro. Science 235, 1040–1043.Google Scholar
Gosh, S., Frisardi, M., Rogers, R., & Samuelson, J. (2001). How Giardia swim and divide. Infect Immunol 69, 7866–7872.Google Scholar
Holberton, D.V. (1973). Fine structure of the ventral disk apparatus and the mechanism of attachment in the flagellate Giardia muris. J Cell Sci 13, 11–41.Google Scholar
Holberton, D.V. (1974). Attachment of Giardia: Hydrodynamic model based on flagellar activity. J Exp Biol 60, 207–221.Google Scholar
Kane, A.V., Ward, H.D., Keusch, G.T., & Pereira, M. (1991). In vitro encystation of Giardia lamblia: Large-scale production of in vitro cysts and strain and clone differences in encystation efficiency. J Parasitol 77, 974–981.Google Scholar
Kattenbach, W.M., Diniz-Junior, J.A., Benchimol, M., & De Souza, W. (1996). A deep-etch study of the cytoskeleton of Giardia duodenalis. Biol Cell 86, 161–166.Google Scholar
Kattenbach, W.M., Pimenta, P.F.P., De Souza, W., & Pinto da Silva, P. (1991). Giardia duodenalis: A freeze-fracture, fracture-flip and cytochemistry study. Parasitol Res 77, 651–658.Google Scholar
Keister, D.B. (1983). Axenic culture of Giardia lamblia in TyI-S-33 medium supplemented with bile. Trans Roy Soc Trop Med Hyg 77, 487.Google Scholar
Lanfredi-Rangel, A., Attias, M., Carvalho, T.M.U., Kattenbach, W.M., & de Souza, W. (1998). The peripheral vesicles of trophozoites of the primitive protozoan Giardia lamblia may correspond to early and late endosomes and to lysossomes. J Struct Biol 123, 225–235.Google Scholar
Lanfredi-Rangel, A., Attias, M., Reiner, D., Gillin, F.D., & De Souza, W. (2002a). The fine structure of the biogenesis of the encystation secretory vesicles (ESVs) of Giardia lamblia. Rev Inst Med Trop São Paulo 44, 102.Google Scholar
Lanfredi-Rangel, A., Campanati, L., Bittencourt-Silvestre, J., & De Souza, W. (2002b). Morphological characterization of the phases of encystation of Giardia lamblia. In Proceedings of the Meeting of the Brazilian Society for Cell Biology. Brazilian Society for Cell Biology.
Lanfredi-Rangel, A., Diniz, J.A., Jr., & De Souza, W. (1999a). Presence of a protrusion on the ventral disk of adhered trophozoites of Giardia lamblia. Parasitol Res 85, 951–952.Google Scholar
Lanfredi-Rangel, A., Kattenbach, W.M., Diniz, J.A., Jr., & De Souza, W. (1999b). Trophozoites of Giardia lamblia may have a Golgi-like structure. FEMS Microbiol Lett 181, 245–251.Google Scholar
Langford, T.D., Silberman, J.D., Weiland, M.E., Svard, S.G., McCaffery, J.M., Sogin, M.L., & Gillin, F.D. (2002). Exp Parasitol 101, 13–24.
Leipe, D.D., Gunderson, J.H., Nerad, T.A., & Sogin, M.L. (1993). Small subunit ribosomal RNA+ of Hexamita inflata and the quest for the first branch in the eukaryotic tree. Mol Biochem Parasitol 59, 41–48.Google Scholar
Lipsky, N.G. & Pagano, R.E. (1985). A vital stain for the Golgi apparatus. Science 228, 745–747.Google Scholar
Lloyd, D., Harris, J.C., Maroulis, S., Wadley, R., Ralphs, J.R., Hann, A.C., Turner, M.P., & Edwards, M.R. (2002). The “primitive” microaerophile Giardia intestinalis (syn. lamblia, duodenalis) has specialized membranes with electron transport and membrane-potential-generating functions. Microbiology 148, 1349–1354.Google Scholar
Luján, H.D., Marotta, A., Mowatt, M.R., Sciaky, N., Lippincott-Schwartz, J., & Nash, T.E. (1995). Developmental induction of Golgi structure and function in the primitive eukaryote Giardia lamblia. J Biol Chem 270, 4612–4618.Google Scholar
Luján, H.D., Mowatt, M.R., Byrd, L.G., & Nash, T.E. (1996a). Cholesterol starvation induces differentiation of the intestinal parasite Giardia lamblia. Proc Natl Acad Sci USA 93, 7628–7633.Google Scholar
Luján, H.D., Mowatt, M.R., Conrad, J.T., & Nash, T.E. (1996b). Increased expression of the molecular chaperone BiP/GRP78 during the differentiation of a primitive eukaryote. Biol Cell 86, 11–18.Google Scholar
Luján, H.D., Mowatt, M.R., & Nash, T.E. (1997). Mechanisms of Giardia lamblia differentiation into cysts. Microb Mol Biol Rev 61, 294–304.Google Scholar
Manning, P., Erlandsen, S.L., & Jarroll, E.L. (1992). Carbohydrate and amino acid analyses of Giardia muris cysts. J Protozool 39, 290–296.Google Scholar
McCaffery, J.M., Faubert, G.M., & 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.Google Scholar
McCaffery, J.M. & Gillin, F.D. (1994). Giardia lamblia: Ultrastructural basis of protein transport during growth and encystation. Exp Parasitol 79, 220–235.Google Scholar
Mowatt, M.R., Luján, H.D., Cotten, D.B., Bowers, B., Yee, J., Nash, T.E., & Stibbs, H.H. (1995). Developmentally regulated expression of a Giardia lamblia cyst wall protein gene. Mol Microbiol 15, 955–963.Google Scholar
Nohynkova, E., Draber, P., Reischig, J., & Kulda, J. (2000). Localization of gamma-tubulin in interphase and mitotic cells of a unicellular eukaryote, Giardia intestinalis. Eur J Cell Biol 79, 438–445.Google Scholar
Owen, R.L. Nemanic, P.C. Steven, D.P., & Mueller, J.C. (1980). The structural basis of Giardia function. Trans Roy Soc Trop Med Hyg 74, 429–433.Google Scholar
Pimenta, P.F.P., Da Silva, P.P., & Nash, T. (1991). Variant surface antigens of Giardia lamblia are associated with the presence of a thick cell coat: Thin section and label fracture immunocytochemistry survey. Infect Immun 59, 3989–3996.Google Scholar
Reiner, D.S., McCaffery, M., & 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.Google Scholar
Sogin, M.L., Gunderson, J.H., Elwood, H.J., Alonso, R.A., & Peattie, D.A. (1989). Phylogenetic meaning of the kingdon concept: An unusual ribosomal RNA from Giardia lamblia. Science 243, 75–77.Google Scholar
Soltys, B.J., Falah, M., & 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.Google Scholar
Touz, M.C., Gottig, N., Nash, T.E., & Luján, H.D. (2002a). Identification and characterization of a novel secretory granule calcium-binding protein from the early branching eukaryote Giardia lamblia. J Biol Chem 277, 50557–50563.Google Scholar
Touz, M.C., Nores, M.J., Slavin, I., Carmona, C., Corad, J.T., Mowatt, M.R., Nash, T.E., Coronel, C.E., & Luján, H.D. (2002b). 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.Google Scholar