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Lipid metabolism in Giardia: a post-genomic perspective

Published online by Cambridge University Press:  30 September 2010

M. YICHOY ,
T. T. DUARTE ,
A. DE CHATTERJEE ,
T. L. MENDEZ ,
K. Y. AGUILERA ,
D. ROY ,
S. ROYCHOWDHURY ,
S. B. ALEY  and
S. DAS
M. YICHOY
Affiliation:
Department of Biological Sciences, University of Texas at El Paso, Texas 79968-0519 Infectious Diseases and Immunology, The Border Biomedical Research Centre, University of Texas at El Paso, Texas 79968-0519, USA
T. T. DUARTE
Affiliation:
Department of Biological Sciences, University of Texas at El Paso, Texas 79968-0519 Infectious Diseases and Immunology, The Border Biomedical Research Centre, University of Texas at El Paso, Texas 79968-0519, USA
A. DE CHATTERJEE
Affiliation:
Department of Biological Sciences, University of Texas at El Paso, Texas 79968-0519 Infectious Diseases and Immunology, The Border Biomedical Research Centre, University of Texas at El Paso, Texas 79968-0519, USA
T. L. MENDEZ
Affiliation:
Department of Biological Sciences, University of Texas at El Paso, Texas 79968-0519 Infectious Diseases and Immunology, The Border Biomedical Research Centre, University of Texas at El Paso, Texas 79968-0519, USA
K. Y. AGUILERA
Affiliation:
Department of Biological Sciences, University of Texas at El Paso, Texas 79968-0519 Infectious Diseases and Immunology, The Border Biomedical Research Centre, University of Texas at El Paso, Texas 79968-0519, USA
D. ROY
Affiliation:
Department of Biological Sciences, University of Texas at El Paso, Texas 79968-0519 Infectious Diseases and Immunology, The Border Biomedical Research Centre, University of Texas at El Paso, Texas 79968-0519, USA
S. ROYCHOWDHURY
Affiliation:
Department of Biological Sciences, University of Texas at El Paso, Texas 79968-0519 Neurosciences and Metabolic Disorder Programs, The Border Biomedical Research Centre, University of Texas at El Paso, Texas 79968-0519, USA
S. B. ALEY
Affiliation:
Department of Biological Sciences, University of Texas at El Paso, Texas 79968-0519 Infectious Diseases and Immunology, The Border Biomedical Research Centre, University of Texas at El Paso, Texas 79968-0519, USA
S. DAS*
Affiliation:
Department of Biological Sciences, University of Texas at El Paso, Texas 79968-0519 Infectious Diseases and Immunology, The Border Biomedical Research Centre, University of Texas at El Paso, Texas 79968-0519, USA
*
*Corresponding author: Department of Biological Sciences and the Border Biomedical Research Centre, University of Texas at El Paso, 500 West University Avenue, El Paso, Texas 79968-0519, USA. Tel: +915 747 6896. Fax: +915 747 5808. E-mail: [email protected]
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Summary

Giardia lamblia, a protozoan parasite, infects a wide variety of vertebrates, including humans. Studies indicate that this anaerobic protist possesses a limited ability to synthesize lipid molecules de novo and depends on supplies from its environment for growth and differentiation. It has been suggested that most lipids and fatty acids are taken up by endocytic and non-endocytic pathways and are used by Giardia for energy production and membrane/organelle biosynthesis. The purpose of this article is to provide an update on recent progress in the field of lipid research of this parasite and the validation of lipid metabolic pathways through recent genomic information. Based on current cellular, biochemical and genomic data, a comprehensive pathway has been proposed to facilitate our understanding of lipid and fatty acid metabolism/syntheses in this waterborne pathogen. We envision that the current review will be helpful in identifying targets from the pathways that could be used to design novel therapies to control giardiasis and related diseases.

Keywords

Giardialipidmetabolic pathwaysgiardiasisgenome databaseparasite
Type
Review Article
Information
Parasitology , Volume 138 , Issue 3 , March 2011 , pp. 267 - 278
Copyright
Copyright © Cambridge University Press 2010

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References

REFERENCES

Adam, R. D. (2001). Biology of Giardia lamblia. Clinical Microbiology Reviews 14, 447–475.CrossRefGoogle ScholarPubMed
Bajer, A. (2008). Cryptosporidium and Giardia spp. infections in humans, animals and the environment in Poland. Parasitology Research 104, 1–17.CrossRefGoogle ScholarPubMed
Blair, R. J. and Weller, P. F. (1987). Uptake and esterification of arachidonic acid by trophozoites of Giardia lamblia. Molecular and Biochemical Parasitology 25, 11–18.CrossRefGoogle ScholarPubMed
Castillo, C., Hernandez, Y., Roychowdhury, S. and Das, S. (2009). Cytoskeleton-based lipid transport in a parasitic protozoan, Giardia lamblia. In Giardia and Cryptosporidium: From Molecules to Disease (ed. Ortega-Pierres, G., Caccio, S., Fayer, R., Mank, T., Smith, H. and Thompson, R. C. A.), pp. 292–307. CABI International, Wallingford, UK.CrossRefGoogle Scholar
Correa, G., Morgado-Diaz, J. A. and Benchimol, M. (2004). Centrin in Giardia lamblia – ultrastructural localization. FEMS Microbiology Letters 233, 91–96.CrossRefGoogle ScholarPubMed
Cox, S. S., Van Der Giezen, M., Tarr, S. J., Crompton, M. R. and Tovar, J. (2006). Evidence from bioinformatics, expression and inhibition studies of phosphoinositide-3 kinase signaling in Giardia intestinalis. BMC Microbiology 6, 45.CrossRefGoogle ScholarPubMed
Crossley, R., Marshall, J., Clark, J. T. and Holberton, D. V. (1986). Immunocytochemical differentiation of microtubules in the cytoskeleton of Giardia lamblia using monoclonal antibodies to alpha-tubulin and polyclonal antibodies to associated low molecular weight proteins. Journal of Cell Science 80, 233–252.CrossRefGoogle ScholarPubMed
Das, S., Castillo, C. and Stevens, T. L. (2001). Phospholipid remodeling/generation in Giardia: the role of the Lands cycle. Trends in Parasitology 17, 316–319.CrossRefGoogle ScholarPubMed
Das, S. and Gillin, F. D. (1996). Giardia lamblia: increased UDP-N-acetyl-D-glucosamine and N-acetyl-D-galactosamine transferase activities during encystation. Experimental Parasitology 83, 19–29.CrossRefGoogle ScholarPubMed
Das, S., Reiner, D. S., Zenian, J., Hogan, D. L., Koss, M. A., Wang, C. S. and Gillin, F. D. (1988). Killing of Giardia lamblia trophozoites by human intestinal fluid in vitro. Journal of Infectious Diseases 157, 1257–1260.CrossRefGoogle ScholarPubMed
Das, S., Schteingart, C. D., Hofmann, A. F., Reiner, D. S., Aley, S. B. and Gillin, F. D. (1997). Giardia lamblia: evidence for carrier-mediated uptake and release of conjugated bile acids. Experimental Parasitology 87, 133–141.Google ScholarPubMed
Das, S., Stevens, T. L., Castillo, C., Villasenor, A., Arredondo, H. and Reddy, K. (2002). Lipid metabolism in mucous-dwelling amitochondriate protozoa. International Journal for Parasitology 32, 655–675.CrossRefGoogle ScholarPubMed
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. Journal of Biological Chemistry 266, 21318–21325.CrossRefGoogle ScholarPubMed
Davids, B. J., Reiner, D. S., Birkeland, S. R., Preheim, S. P., Cipriano, M. J., McArthur, A. G. and Gillin, F. D. (2006). A new family of giardial cysteine-rich non-VSP protein genes and a novel cyst protein. PLoS One 1, e44.CrossRefGoogle Scholar
Davids, B. J., Williams, S., Lauwaet, T., Palanca, T. and Gillin, F. D. (2008). Giardia lamblia aurora kinase: a regulator of mitosis in a binucleate parasite. International Journal of Parasitology 38, 353–369.CrossRefGoogle Scholar
Dowhan, W. (1997). Molecular basis for membrane phospholipid diversity: why are there so many lipids? Annual Review of Biochemistry 66, 199–232.CrossRefGoogle ScholarPubMed
Ellis, J. E., Wyder, M. A., Jarroll, E. L. and Kaneshiro, E. S. (1996). Changes in lipid composition during in vitro encystation and fatty acid desaturase activity of Giardia lamblia. Molecular and Biochemical Parasitology 81, 13–25.CrossRefGoogle ScholarPubMed
Elmendorf, H. G., Dawson, S. C. and Mccaffery, J. M. (2003). The cytoskeleton of Giardia lamblia. International Journal for Parasitology 33, 3–28.CrossRefGoogle ScholarPubMed
Farthing, M. J., Keusch, G. T. and Carey, M. C. (1985). Effects of bile and bile salts on growth and membrane lipid uptake by Giardia lamblia. Possible implications for pathogenesis of intestinal disease. Journal of Clinical Investigation 76, 1727–1732.CrossRefGoogle ScholarPubMed
Faubert, G. (2000). Immune response to Giardia duodenalis. Clinical Microbiology Reviews 13, 35–54.CrossRefGoogle ScholarPubMed
Ghosh, S., Frisardi, M., Rogers, R. and Samuelson, J. (2001). How Giardia swim and divide. Infection and Immunity 69, 7866–7872.CrossRefGoogle ScholarPubMed
Gibson, G. R., Ramirez, D., Maier, J., Castillo, C. and Das, S. (1999). Giardia lamblia: incorporation of free and conjugated fatty acids into glycerol-based phospholipids. Experimental Parasitology 92, 1–11.CrossRefGoogle ScholarPubMed
Gillin, F. D., Gault, M. J., Hofmann, A. F., Gurantz, D. and Sauch, J. F. (1986). Biliary lipids support serum-free growth of Giardia lamblia. Infection and Immunity 53, 641–645.CrossRefGoogle ScholarPubMed
Gillin, F. D., Reiner, D. S. and Boucher, S. E. (1988). Small-intestinal factors promote encystation of Giardia lamblia in vitro. Infection and Immunity 56, 705–707.CrossRefGoogle ScholarPubMed
Gillin, F. D., Reiner, D. S., Gault, M. J., Douglas, H., Das, S., Wunderlich, A. and Sauch, J. F. (1987). Encystation and expression of cyst antigens by Giardia lamblia in vitro. Science 235, 1040–1043.CrossRefGoogle ScholarPubMed
Giangaspero, A., Paoletti, B., Iorio, R. and Traversa, D. (2005). Prevalence and molecular characterization of Giardia duodenalis from sheep in central Italy. Parasitology Research 96, 32–37.CrossRefGoogle ScholarPubMed
Hassan, S. M., Maache, M., De La Guardia, R. D., Cordova, O. M., Garcia, J. R., Galiana, M., Castroviejo, D. A., Martins, M. and Osuna, A. (2005). Binding properties and immunolocalization of a fatty acid-binding protein in Giardia lamblia. Journal of Parasitology 91, 284–292.CrossRefGoogle ScholarPubMed
Hernandez, Y., Castillo, C., Roychowdhury, S., Hehl, A., Aley, S. B. and Das, S. (2007 a). Clathrin-dependent pathways and the cytoskeleton network are involved in ceramide endocytosis by a parasitic protozoan, Giardia lamblia. International Journal for Parasitology 37, 21–32.CrossRefGoogle ScholarPubMed
Hernandez, Y., Shpak, M., Duarte, T. T., Mendez, T. L., Maldonado, R. A., Roychowdhury, S., Rodrigues, M. L. and Das, S. (2008). Novel role of sphingolipid synthesis genes in regulating giardial encystation. Infection and Immunity 76, 2939–2949.CrossRefGoogle ScholarPubMed
Hernandez, P. C. and Wasserman, M. (2006). Do genes from the cholesterol synthesis pathway exist and express in Giardia intestinalis? Parasitology Research 98, 194–199.CrossRefGoogle ScholarPubMed
Hernandez, Y., Zamora, G., Ray, S., Chapoy, J., Chavez, E., Valvarde, R., Williams, E., Aley, S. B. and Das, S. (2007 b). Transcriptional analysis of three major putative phosphatidylinositol kinase genes in a parasitic protozoan, Giardia lamblia. Journal of Eukaryotic Microbiology 54, 29–32. Journal for Parasitology 37, 21–32.CrossRefGoogle Scholar
Holberton, D. V. (1973). Fine structure of the ventral disk apparatus and the mechanism of attachment in the flagellate Giardia muris. Journal of Cell Science 13, 11–41.CrossRefGoogle ScholarPubMed
Hunter, P. R. and Thompson, R. C. (2005). The zoonotic transmission of Giardia and Cryptosporidium. International Journal for Parasitology 35, 1181–1190.CrossRefGoogle ScholarPubMed
Iwabe, N. and Miyata, T. (2002). Kinesin-related genes from diplomonad, sponge, amphioxus, and cyclostomes: divergence pattern of kinesin family and evolution of giardial membrane-bounded organella. Molecular Biology and Evolution 19, 1524–1533.CrossRefGoogle ScholarPubMed
Jarroll, E. L., Muller, P. J., Meyer, E. A. and Morse, S. A. (1981). Lipid and carbohydrate metabolism in Giardia lamblia. Molecular and Biochemical Parasitology 2, 187–196.CrossRefGoogle ScholarPubMed
Kamda, J. D. and Singer, S. M. (2009). Phosphoinositide 3-kinase-dependent inhibition of dendritic cell interleukin-12 production by Giardia lamblia. Infection and Immunity 77, 685–693.CrossRefGoogle ScholarPubMed
Kane, A., Ward, H. D., Keusch, G. T. and Pereira, M. E. A. (1991). In vitro encystation of Giardia lamblia: large-scale production of in vitro cysts and strain and clone differences in encystation efficiency. Journal of Parasitology 77, 974–981.CrossRefGoogle ScholarPubMed
Kaneda, Y. and Goutsu, T. (1988). Lipid analysis of Giardia lamblia and its culture medium. Annals of Tropical Medicine and Parasitology 82, 83–90.CrossRefGoogle ScholarPubMed
Kent, C. (1995). Eukaryotic phospholipid biosynthesis. Annual Review of Biochemistry 64, 315–343.CrossRefGoogle ScholarPubMed
Lujan, H. D., Byrd, L. G., Mowatt, M. R. and Nash, T. E. (1994). Serum Cohn fraction IV-1 supports the growth of Giardia lamblia in vitro. Infection and Immunity 62, 4664–4666.CrossRefGoogle ScholarPubMed
Lujan, H. D., Mowatt, M. R., Byrd, L. G. and Nash, T. E. (1996). Cholesterol starvation induces differentiation of the intestinal parasite Giardia lamblia. Proceedings of the National Academy of Sciences, USA 93, 7628–7633.CrossRefGoogle ScholarPubMed
Lujan, H. D., Mowatt, M. R., Chen, G. Z. and Nash, T. E. (1995). Isoprenylation of proteins in the protozoan Giardia lamblia. Molecular and Biochemical Parasitology 72, 121–127.CrossRefGoogle ScholarPubMed
Lauwaet, T., Davids, B. J., Reiner, D. S. and Gillin, F. D. (2007). Encystation of Giardia lamblia: a model for other parasites. Current Opinion in Microbiology 10, 554–559.CrossRefGoogle Scholar
McArthur, A. G., Morrison, H. G., Nixon, J. E. J., Passamaneck, N. Q. E., Kim, U., Hinkle, G., Crocker, M. K., Holder, M. E., Farr, R., Reich, C. I., Olsen, G. E., Aley, S. B., Adam, R. D., Gillin, F. D. and Sogin, M. L. (2000). The Giardia genome project database. FEMS Microbiology Letters 189, 271–273.CrossRefGoogle ScholarPubMed
Mohareb, E. W., Rogers, E. J., Weiner, E. J. and Bruce, J. I. (1991). Giardia lamblia: phospholipid analysis of human isolates. Annals of Tropical Medicine and Parasitology 85, 591–597.CrossRefGoogle ScholarPubMed
Monis, P. T. and Thompson, R. C. (2003). Cryptosporidium and Giardia-zoonoses: fact or fiction? Infection, genetics and evolution. Journal of Molecular Epidemiology and Evolutionary Genetics in Infectious Diseases 3, 233–244.CrossRefGoogle ScholarPubMed
Morgan, C. P., Insall, R., Haynes, L. and Cockcroft, S. (2004). Identification of phospholipase B from Dictyostelium discoideum reveals a new lipase family present in mammals, flies and nematodes, but not yeast. The Biochemical Journal 382, 441–449.CrossRefGoogle Scholar
Morrison, H. G., McArthur, A. G., Gillin, F., Aley, S. B., Adam, R. D., Olsen, G., Best, A., Cande, W. Z., Chen, F., Mj, C., Davids, B. J., Dawson, S. C., Elmendorf, H. G., Hehl, A., Holder, M. E., Huse, S., Kim, U., Lasek-Nesselquist, E., Manning, G., Niqam, A., Nixon, J., Palm, D., Passamaneck, N. Q. E., Prabhu, A., Reich, C. I., Reiner, D. S., Samuelson, J., Svard, S. G. and Sogin, M. L. (2007). Genomic minimalism in the early diverging intestinal parasite Giardia lamblia. Science 317, 1921–1926.CrossRefGoogle ScholarPubMed
Nayak, N., Ganguly, N. K., Walia, B. N., Wahi, V., Kanwar, S. S. and Mahajan, R. C. (1987). Specific secretory IgA in the milk of Giardia lamblia-infected and uninfected women. Journal of Infectious Diseases 155, 724–727.CrossRefGoogle ScholarPubMed
Nohynkova, E., Draber, P., Reischig, J. and Kulda, J. (2000). Localization of gamma-tubulin in interphase and mitotic cells of a unicellular eukaryote, Giardia intestinalis. European Journal of Cell Biology 79, 438–445.CrossRefGoogle ScholarPubMed
Ratner, D. M., Cui, J., Steffen, M., Moore, L. L., Robbins, P. W. and Samuelson, J. (2008). Changes in the N-glycome, glycoproteins with Asn-linked glycans, of Giardia lamblia with differentiation from trophozoites to cysts. Eukaryotic Cell 7, 1930–1940.CrossRefGoogle ScholarPubMed
Rayan, P., Stenzel, D. and McDonnell, P. A. (2005). The effects of saturated fatty acids on Giardia duodenalis trophozoites in vitro. Parasitology Research 97, 191–200.CrossRefGoogle ScholarPubMed
Reiner, D. S., Wang, C. S. and Gillin, F. D. (1986). Human milk kills Giardia lamblia by generating toxic lipolytic products. Journal of Infectious Diseases 154, 825–832.CrossRefGoogle ScholarPubMed
Richardson, D. N., Simmons, M. P. and Reddy, A. S. (2006). Comprehensive comparative analysis of kinesins in photosynthetic eukaryotes. BMC Genomics 7, 18.CrossRefGoogle ScholarPubMed
Sener, K., Shen, Z., Newburg, D. S. and Jarroll, E. L. (2004). Amino sugar phosphate levels in Giardia change during cyst wall formation. Microbiology 150, 1225–1230.CrossRefGoogle ScholarPubMed
Smith, A., Reacher, M., Smerdon, W., Adak, G. K., Nichols, G. and Chalmers, R. M. (2006). Outbreaks of waterborne infectious intestinal disease in England and Wales, 1992–2003. Epidemiology and Infection 134, 1141–1149.CrossRefGoogle ScholarPubMed
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.CrossRefGoogle ScholarPubMed
Sonda, S., Stefanic, S. and Hehl, A. B. (2008). A sphingolipid inhibitor induces a cytokinesis arrest and blocks stage differentiation in Giardia lamblia. Antimicrobiological Agents and Chemotherapeutics 52, 563–569.CrossRefGoogle ScholarPubMed
Stefanic, S., Spycher, C., Morf, L., Fabrias, G., Casas, J., Schraner, E., Wild, P., Hehl, A. B. and Sonda, S. (2010). Glucosylceramide synthesis inhibition affects cell cycle progression, membrane trafficking and stage differentiation in the minimized protozoan Giardia lamblia. Journal of Lipid Research 51, 2527–2545.CrossRefGoogle Scholar
Stevens, T. L., Gibson, G. R., Adam, R. D., Maier, J., Allison-Ennis, M. and Das, S. (1997). Uptake and cellular localization of exogenous lipids by Giardia lamblia, a primitive eukaryote. Experimental parasitology 86, 133–143.CrossRefGoogle ScholarPubMed
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. Biochimica et Biophysica Acta 1483, 69–80.CrossRefGoogle ScholarPubMed
Thompson, R. C. A. (2009). The impact of Giardia on science and society. In Giardia and Cryptosporidium: From Molecules to Disease. (ed. Ortega-Pierres, G., Caccio, S., Fayer, R., Mank, T., Smith, H. and Thompson, R. C. A.), pp. 1–11. CABI Press, Wallingford, UK.Google Scholar
Touz, M. C., Conrad, J. T. and Nash, T. E. (2005). A novel palmitoyl acyl transferase controls surface protein palmitoylation and cytotoxicity in Giardia lamblia. Molecular Microbiology 58, 999–1011.CrossRefGoogle ScholarPubMed
Vargas-Villarreal, J., Escobedo-Guajardo, B. L., Mata-Cardenas, B. D., Palacios-Corona, R., Cortes-Gutierrez, E., Morales-Vallarta, M., Sampayo-Reyes, A. and Said-Fernandez, S. (2007). Activity of intracellular phospholipase A1 and A2 in Giardia lamblia. Journal of Parasitology 93, 979–984.CrossRefGoogle ScholarPubMed
Worgall, T. S., Davis-Hayman, S. R., Magana, M. M., Oelkers, P. M., Zapata, F., Juliano, R. A., Osborne, T. F., Nash, T. E. and Deckelbaum, R. J. (2004). Sterol and fatty acid regulatory pathways in a Giardia lamblia-derived promoter: evidence for SREBP as an ancient transcription factor. Journal of Lipid Research 45, 981–988.CrossRefGoogle Scholar
Xiao, L. and Fayer, R. (2008). Molecular characterisation of species and genotypes of Cryptosporidium and Giardia and assessment of zoonotic transmission. International Journal for Parasitology 38, 1239–1255.CrossRefGoogle ScholarPubMed
Yichoy, M., Nakayasu, E. S., Shpak, M., Aguilar, C., Aley, S. B., Almeida, I. C. and Das, S. (2009). Lipidomic analysis reveals that phosphatidylglycerol and phosphatidylethanolamine are newly generated phospholipids in an early-divergent protozoan, Giardia lamblia. Molecular and Biochemical Parasitology 165, 67–78.CrossRefGoogle Scholar
Yu, L. Z., Birky, C. W. Jr. and Adam, R. D. (2002). The two nuclei of Giardia each have complete copies of the genome and are partitioned equationally at cytokinesis. Eukaryotic Cell 1, 191–199.CrossRefGoogle ScholarPubMed