Membrane trafficking and organelle biogenesis in Giardia lamblia: Use it or lose it

International Journal for Parasitology

Volumn 41, Issue 5, 2011, Pages 471-480

  Faso, Carmen ^a   Hehl, Adrian B ^a  

^a UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Antigenic variation; Biopolymer; Encystation; Golgi; Mitosome; Peripheral vesicle; Reductive evolution

Indexed keywords

IRON SULFUR PROTEIN;

ANTIGEN; CELL ORGANELLE; CYST; ENCYSTMENT; MEMBRANE; METAZOAN; MITOCHONDRION; PARASITE; PROTEIN; PROTOZOAN;

APICOMPLEXAN LIFE CYCLE STAGE; BIOGENESIS; CELL ORGANELLE; CYST FORMATION; ENDOCYTOSIS; ENDOPLASMIC RETICULUM; GENE CONTROL; GIARDIA LAMBLIA; GLYCOSYLATION; GOLGI COMPLEX; HOST; INTESTINE EPITHELIUM; MEMBRANE TRANSPORT; MITOCHONDRION; NONHUMAN; REVIEW; SECRETION; SMALL INTESTINE; TROPHOZOITE;

BIOGENESIS; CELL MEMBRANE; GIARDIA LAMBLIA; ORGANELLES; PROTEIN TRANSPORT; PROTOZOAN PROTEINS;

GIARDIA; GIARDIA INTESTINALIS; METAZOA; PROTOZOA;

EID: 79952709066     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpara.2010.12.014     Document Type: Review

References (118)

1. Abdul-Wahid A., Faubert G.M. Similarity in cyst wall protein (CWP) trafficking between encysting Giardia duodenalis trophozoites and CWP-expressing human embryonic kidney-293 cells. Biochem. Biophys. Res. Commun. 2004, 324:1069-1080.
2. Abodeely M., DuBois K.N., Hehl A., Stefanic S., Sajid M., DeSouza W., Attias M., Engel J.C., Hsieh I., Fetter R.D., McKerrow J.H. A contiguous compartment functions as endoplasmic reticulum and endosome/lysosome in Giardia lamblia. Eukaryotic Cell 2009, 8:1665-1676.
3. Ackers J.P., Dhir V., Field M.C. A bioinformatic analysis of the RAB genes of Trypanosoma brucei. Mol. Biochem. Parasitol. 2005, 141:89-97.
4. Adam R.D., Aggarwal A., Lal A.A., de La Cruz V.F., McCutchan T., Nash T.E. Antigenic variation of a cysteine-rich protein in Giardia lamblia. J. Exp. Med. 1988, 167:109-118.
5. Banerjee S., Vishwanath P., Cui J., Kelleher D.J., Gilmore R., Robbins P.W., Samuelson J. The evolution of N-glycan-dependent endoplasmic reticulum quality control factors for glycoprotein folding and degradation. Proc. Natl. Acad. Sci. USA 2007, 104:11676-11681.
6. Banerjee S., Cui J., Robbins P.W., Samuelson J. Use of Giardia, which appears to have a single nucleotide-sugar transporter for UDP-GlcNAc, to identify the UDP-Glc transporter of Entamoeba. Mol. Biochem. Parasitol. 2008, 159:44-53.
7. Benchimol M. The release of secretory vesicle in encysting Giardia lamblia. FEMS Microbiol. Lett. 2004, 235:81-87.
8. Bernander R., Palm J.E., Svard S.G. Genome ploidy in different stages of the Giardia lamblia life cycle. Cell Microbiol. 2001, 3:55-62.
9. Boehm M., Bonifacino J.S. Adaptins: the final recount. Mol. Biol. Cell 2001, 12:2907-2920.
10. Boucher S.E., Gillin F.D. Excystation of in vitro-derived Giardia lamblia cysts. Infect. Immun. 1990, 58:3516-3522.
11. Bulik D.A., van Ophem P., Manning J.M., Shen Z., Newburg D.S., Jarroll E.L. UDP-N-acetylglucosamine pyrophosphorylase, a key enzyme in encysting Giardia, is allosterically regulated. J. Biol. Chem. 2000, 275:14722-14728.
12. Burri L., Keeling P.J. Protein targeting in parasites with cryptic mitochondria. Int. J. Parasitol. 2007, 37:265-272.
13. Castillo-Romero A., Leon-Avila G., Wang C.C., Perez Rangel A., Camacho Nuez M., Garcia Tovar C., Ayala-Sumuano J.T., Luna-Arias J.P., Hernandez J.M. Rab11 and actin cytoskeleton participate in Giardia lamblia encystation, guiding the specific vesicles to the cyst wall. PLoS Negl. Trop. Dis. 2010, 4:e697.
14. Cavalier-Smith T. A revised six-kingdom system of life. Biol. Rev. Cambridge Philos. Soc. 1998, 73:203-266.
15. Chatterjee A., Carpentieri A., Ratner D.M., Bullitt E., Costello C.E., Robbins P.W., Samuelson J. Giardia cyst wall protein 1 is a lectin that binds to curled fibrils of the GalNAc homopolymer. PLoS Pathogens 2010, 6:e1001059.
16. Chin A.C., Teoh D.A., Scott K.G., Meddings J.B., Macnaughton W.K., Buret A.G. Strain-dependent induction of enterocyte apoptosis by Giardia lamblia disrupts epithelial barrier function in a caspase-3-dependent manner. Infect. Immun. 2002, 70:3673-3680.
17. Chiu P.W., Huang Y.C., Pan Y.J., Wang C.H., Sun C.H. A novel family of cyst proteins with epidermal growth factor repeats in Giardia lamblia. PLoS Negl. Trop. Dis. 2010, 4:e677.
18. Dacks J.B., Doolittle W.F. Novel syntaxin gene sequences from Giardia, Trypanosoma and algae: implications for the ancient evolution of the eukaryotic endomembrane system. J. Cell Sci. 2002, 115:1635-1642.
19. Dacks J.B., Davis L.A., Sjogren A.M., Andersson J.O., Roger A.J., Doolittle W.F. Evidence for Golgi bodies in proposed 'Golgi-lacking' lineages. Proc. Biol. Sci. 2003, 270(Suppl. 2):S168-171.
20. Dacks J.B., Doolittle W.F. Molecular and phylogenetic characterization of syntaxin genes from parasitic protozoa. Mol. Biochem. Parasitol. 2004, 136:123-136.
21. Dacks J.B., Field M.C. Evolution of the eukaryotic membrane-trafficking system: origin, tempo and mode. J. Cell Sci. 2007, 120:2977-2985.
22. Dagley M.J., Dolezal P., Likic V.A., Smid O., Purcell A.W., Buchanan S.K., Tachezy J., Lithgow T. The protein import channel in the outer mitosomal membrane of Giardia intestinalis. Mol. Biol. Evol. 2009, 26:1941-1947.
23. Das S., Gillin F.D. Giardia lamblia: increased UDP-N-acetyl-D-glucosamine and N-acetyl-D-galactosamine transferase activities during encystation. Exp. Parasitol. 1996, 83:19-29.
24. Davids B.J., Mehta K., Fesus L., McCaffery J.M., Gillin F.D. Dependence of Giardia lamblia encystation on novel transglutaminase activity. Mol. Biochem. Parasitol. 2004, 136:173-180.
25. Davids B.J., Palm J.E., Housley M.P., Smith J.R., Andersen Y.S., Martin M.G., Hendrickson B.A., Johansen F.E., Svard S.G., Gillin F.D., Eckmann L. Polymeric immunoglobulin receptor in intestinal immune defense against the lumen-dwelling protozoan parasite Giardia. J. Immunol. 2006, 177:6281-6290.
26. Davids B.J., Reiner D.S., Birkeland S.R., Preheim S.P., Cipriano M.J., McArthur A.G., Gillin F.D. A new family of giardial cysteine-rich non-VSP protein genes and a novel cyst protein. PloS One 2006, 1:e44.
27. de Carvalho T.B., David E.B., Coradi S.T., Guimaraes S. Protease activity in extracellular products secreted in vitro by trophozoites of Giardia duodenalis. Parasitol. Res. 2008, 104:185-190.
28. Dolezal P., Smid O., Rada P., Zubacova Z., Bursac D., Sutak R., Nebesarova J., Lithgow T., Tachezy J. Giardia mitosomes and trichomonad hydrogenosomes share a common mode of protein targeting. Proc. Natl. Acad. Sci. USA 2005, 102:10924-10929.
29. DuBois K.N., Abodeely M., Sakanari J., Craik C.S., Lee M., McKerrow J.H., Sajid M. Identification of the major cysteine protease of Giardia and its role in encystation. J. Biol. Chem. 2008, 283:18024-18031.
30. Eckmann L., Laurent F., Langford T.D., Hetsko M.L., Smith J.R., Kagnoff M.F., Gillin F.D. Nitric oxide production by human intestinal epithelial cells and competition for arginine as potential determinants of host defense against the lumen-dwelling pathogen Giardia lamblia. J. Immunol. 2000, 164:1478-1487.
31. Elias E.V., Quiroga R., Gottig N., Nakanishi H., Nash T.E., Neiman A., Lujan H.D. Characterization of SNAREs determines the absence of a typical Golgi apparatus in the ancient eukaryote Giardia lamblia. J. Biol. Chem. 2008, 283:35996-36010.
32. Feely D.E., Dyer J.K. Localization of acid phosphatase activity in Giardia lamblia and Giardia muris trophozoites. J. Protozol. 1987, 34:80-83.
33. Feely D.E., Holberton D.V., Erlandsen S.L. The Biology of Giardia 1990, 11-49. Elsevier Science Publishers, New York. E.A. Meyer (Ed.).
34. Gaechter V., Schraner E., Wild P., Hehl A.B. The single dynamin family protein in the primitive protozoan giardia lamblia is essential for stage conversion and endocytic transport. Traffic 2008, 9:57-71.
35. Gerwig G.J., van Kuik J.A., Leeflang B.R., Kamerling J.P., Vliegenthart J.F., Karr C.D., Jarroll E.L. The Giardia intestinalis filamentous cyst wall contains a novel beta(1-3)-N-acetyl-D-galactosamine polymer: a structural and conformational study. Glycobiology 2002, 12:499-505.
36. Gillin F.D., Reiner D.S., Gault M.J., Douglas H., Das S., Wunderlich A., Sauch J.F. Encystation and expression of cyst antigens by Giardia lamblia in vitro. Science 1987, 235:1040-1043.
37. Gillin F.D., Reiner D.S., McCaffery M. Organelles of protein transport in Giardia lamblia. Parasitol. Today 1991, 7:113-116.
38. Gottig N., Elias E.V., Quiroga R., Nores M.J., Solari A.J., Touz M.C., Lujan H.D. Active and passive mechanisms drive secretory granule biogenesis during differentiation of the intestinal parasite Giardia lamblia. J. Biol. Chem. 2006, 281:18156-18166.
39. Gupta R.S., Aitken K., Falah M., Singh B. Cloning of Giardia lamblia heat shock protein HSP70 homologs: implications regarding origin of eukaryotic cells and of endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 1994, 91:2895-2899.
40. Hehl A.B., Marti M., Kohler P. Stage-specific expression and targeting of cyst wall protein-green fluorescent protein chimeras in Giardia. Mol. Biol. Cell 2000, 11:1789-1800.
41. Hehl A.B., Marti M. Secretory protein trafficking in Giardia intestinalis. Mol. Microbiol. 2004, 53:19-28.
42. Hehl A.B., Regos A., Schraner E., Schneider A. Bax function in the absence of mitochondria in the primitive protozoan Giardia lamblia. PloS One 2007, 2:e488.
43. Hernandez Y., Castillo C., Roychowdhury S., Hehl A., Aley S.B., Das S. Clathrin-dependent pathways and the cytoskeleton network are involved in ceramide endocytosis by a parasitic protozoan, Giardia lamblia. Int. J. Parasitol. 2007, 37:21-32.
44. Jarroll E.L., Manning P., Lindmark D.G., Coggins J.R., Erlandsen S.L. Giardia cyst wall-specific carbohydrate: evidence for the presence of galactosamine. Mol. Biochem. Parasitol. 1989, 32:121-131.
45. Jimenez J.C., Uzcanga G., Zambrano A., Di Prisco M.C., Lynch N.R. Identification and partial characterization of excretory/secretory products with proteolytic activity in Giardia intestinalis. J. Parasitol. 2000, 86:859-862.
46. Jimenez J.C., Morelle W., Michalsky J.C., Dei-Cas E. Excreted/secreted glycoproteins of G. intestinalis play an essential role in the antibody response. Parasitol. Res. 2007, 100:715-720.
47. Kane A.V., Ward H.D., Keusch G.T., Pereira M.E. In vitro encystation of Giardia lamblia: large-scale production of in vitro cysts and strain and clone differences in encystation efficiency. J. Parasitol. 1991, 77:974-981.
48. Kasper L.H., Bradley M.S., Pfefferkorn E.R. Identification of stage-specific sporozoite antigens of Toxoplasma gondii by monoclonal antibodies. J. Immunol. 1984, 132:443-449.
49. Katelaris P.H., Naeem A., Farthing M.J. Activity of metronidazole, azithromycin and three benzimidazoles on Giardia lamblia growth and attachment to a human intestinal cell line. Aliment Pharm. Therap. 1994, 8:187-192.
50. Keister D.B. Axenic culture of Giardia lamblia in TYI-S-33 medium supplemented with bile. Trans. R. Soc. Trop. Med. Hyg. 1983, 77:487-488.
51. Kloepper T.H., Kienle C.N., Fasshauer D. An elaborate classification of SNARE proteins sheds light on the conservation of the eukaryotic endomembrane system. Mol. Biol. Cell 2007, 18:3463-3471.
52. Knodler L.A., Noiva R., Mehta K., McCaffery J.M., Aley S.B., Svard S.G., Nystul T.G., Reiner D.S., Silberman J.D., Gillin F.D. Novel protein-disulfide isomerases from the early-diverging protist Giardia lamblia. J. Biol. Chem. 1999, 274:29805-29811.
53. Konrad C., Spycher C., Hehl A.B. Selective condensation drives partitioning and sequential secretion of cyst wall proteins in differentiating Giardia lamblia. PLoS Pathogens 2010, 6:e1000835.
54. Koumandou V.L., Dacks J.B., Coulson R.M., Field M.C. Control systems for membrane fusion in the ancestral eukaryote; evolution of tethering complexes and SM proteins. BMC Evol. Biol. 2007, 7:29.
55. Lal K., Field M.C., Carlton J.M., Warwicker J., Hirt R.P. Identification of a very large Rab GTPase family in the parasitic protozoan Trichomonas vaginalis. Mol. Biochem. Parasitol. 2005, 143:226-235.
56. Lanfredi-Rangel A., Attias M., de Carvalho T.M., Kattenbach W.M., De Souza W. The peripheral vesicles of trophozoites of the primitive protozoan Giardia lamblia may correspond to early and late endosomes and to lysosomes. J. Struct. Biol. 1998, 123:225-235.
57. Lanfredi-Rangel A., Kattenbach W.M., Diniz J.A., de Souza W. Trophozoites of Giardia lamblia may have a Golgi-like structure. FEMS Microbiol. Lett. 1999, 181:245-251.
58. Langford T.D., Silberman J.D., Weiland M.E., Svard S.G., McCaffery J.M., Sogin M.L., Gillin F.D. Giardia lamblia: identification and characterization of Rab and GDI proteins in a genome survey of the ER to Golgi endomembrane system. Exp. Parasitol. 2002, 101:13-24.
59. Lee F.J., Moss J., Vaughan M. Human and Giardia ADP-ribosylation factors (ARFs) complement ARF function in Saccharomyces cerevisiae. J. Biol. Chem. 1992, 267:24441-24445.
60. Li E., Zhao A., Shea-Donohue T., Singer S.M. Mast cell-mediated changes in smooth muscle contractility during mouse giardiasis. Infect. Immun. 2007, 75:4514-4518.
61. Lindmark D.G. Giardia lamblia: localization of hydrolase activities in lysosome-like organelles of trophozoites. Exp. Parasitol. 1988, 65:141-147.
62. Lujan H.D., Marotta A., Mowatt M.R., Sciaky N., Lippincott-Schwartz J., Nash T.E. Developmental induction of Golgi structure and function in the primitive eukaryote Giardia lamblia. J. Biol. Chem. 1995, 270:4612-4618.
63. Lujan H.D., Mowatt M.R., Conrad J.T., Bowers B., Nash T.E. 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. 1995, 270:29307-29313.
64. Lujan H.D., Mowatt M.R., Byrd L.G., Nash T.E. Cholesterol starvation induces differentiation of the intestinal parasite Giardia lamblia. Proc. Natl. Acad. Sci. USA 1996, 93:7628-7633.
65. Lujan H.D., Mowatt M.R., Conrad J.T., Nash T.E. Increased expression of the molecular chaperone BiP/GRP78 during the differentiation of a primitive eukaryote. Biol. Cell 1996, 86(1):11-18.
66. Lujan H.D., Touz M.C. Protein trafficking in Giardia lamblia. Cell Microbiol. 2003, 5:427-434.
67. Macechko P.T., Steimle P.A., Lindmark D.G., Erlandsen S.L., Jarroll E.L. Galactosamine-synthesizing enzymes are induced when Giardia encyst. Mol. Biochem. Parasitol. 1992, 56:301-309.
68. Marti M., Li Y., Kohler P., Hehl A.B. Conformationally correct expression of membrane-anchored Toxoplasma gondii SAG1 in the primitive protozoan Giardia duodenalis. Infect. Immun. 2002, 70:1014-1016.
69. Marti M., Li Y., Schraner E.M., Wild P., Kohler P., Hehl A.B. The secretory apparatus of an ancient eukaryote: protein sorting to separate export pathways occurs before formation of transient Golgi-like compartments. Mol. Biol. Cell 2003, 14:1433-1447.
70. Marti M., Regos A., Li Y., Schraner E.M., Wild P., Muller N., Knopf L.G., Hehl A.B. An ancestral secretory apparatus in the protozoan parasite Giardia intestinalis. J. Biol. Chem. 2003, 278:24837-24848.
71. McCaffery J.M., Faubert G.M., Gillin F.D. Giardia lamblia: traffic of a trophozoite variant surface protein and a major cyst wall epitope during growth, encystation, and antigenic switching. Exp. Parasitol. 1994, 79:236-249.
72. McCaffery J.M., Gillin F.D. Giardia lamblia: ultrastructural basis of protein transport during growth and encystation. Exp. Parasitol. 1994, 79:220-235.
73. Meyer E.A. Giardia as an organism. Giardia: From Molecules to Disease 1994, 3-13. CAB International. R.C.A. Thompson (Ed.).
74. Morelle W., Jimenez J.C., Cieniewski-Bernard C., Dei-Cas E., Michalski J.C. Characterization of the N-linked glycans of Giardia intestinalis. Glycobiology 2005, 15:549-559.
75. Morrison H.G., McArthur A.G., Gillin F.D., Aley S.B., Adam R.D., Olsen G.J., Best A.A., Cande W.Z., Chen F., Cipriano M.J., Davids B.J., Dawson S.C., Elmendorf H.G., Hehl A.B., Holder M.E., Huse S.M., Kim U.U., Lasek-Nesselquist E., Manning G., Nigam A., Nixon J.E., Palm D., Passamaneck N.E., Prabhu A., Reich C.I., Reiner D.S., Samuelson J., Svard S.G., Sogin M.L. Genomic minimalism in the early diverging intestinal parasite Giardia lamblia. Science 2007, 317:1921-1926.
76. Mowatt M.R., Lujan H.D., Cotten D.B., Bowers B., Yee J., Nash T.E., Stibbs H.H. Developmentally regulated expression of a Giardia lamblia cyst wall protein gene. Mol. Microbiol. 1995, 15:955-963.
77. Muller J., Sterk M., Hemphill A., Muller N. Characterization of Giardia lamblia WB C6 clones resistant to nitazoxanide and to metronidazole. J. Antimicrob. Chemother. 2007, 60:280-287.
78. Murtagh J.J., Mowatt M.R., Lee C.M., Lee F.J., Mishima K., Nash T.E., Moss J., Vaughan M. Guanine nucleotide-binding proteins in the intestinal parasite Giardia lamblia. Isolation of a gene encoding an approximately 20-kDa ADP-ribosylation factor. J. Biol. Chem. 1992, 267:9654-9662.
79. Palm J.E., Weiland M.E., Griffiths W.J., Ljungstrom I., Svard S.G. Identification of immunoreactive proteins during acute human giardiasis. J. Infect. Dis. 2003, 187:1849-1859.
80. Panaro M.A., Cianciulli A., Mitolo V., Mitolo C.I., Acquafredda A., Brandonisio O., Cavallo P. Caspase-dependent apoptosis of the HCT-8 epithelial cell line induced by the parasite Giardia intestinalis. FEMS Immunol. Med. Microbiol. 2007, 51:302-309.
81. Papanastasiou P., Hiltpold A., Bommeli C., Kohler P. 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 1996, 35:10143-10148.
82. Papanastasiou P., McConville M.J., Ralton J., Kohler P. The variant-specific surface protein of Giardia, VSP4A1, is a glycosylated and palmitoylated protein. Biochem. J. 1997, 322(Pt 1):49-56.
83. Ratner D.M., Cui J., Steffen M., Moore L.L., Robbins P.W., Samuelson J. Changes in the N-glycome, glycoproteins with Asn-linked glycans, of Giardia lamblia with differentiation from trophozoites to cysts. Eukaryotic Cell 2008, 7:1930-1940.
84. Regoes A., Zourmpanou D., Leon-Avila G., van der Giezen M., Tovar J., Hehl A.B. Protein import, replication, and inheritance of a vestigial mitochondrion. J. Biol. Chem. 2005, 280:30557-30563.
85. Reiner D.S., Douglas H., Gillin F.D. Identification and localization of cyst-specific antigens of Giardia lamblia. Infect. Immun. 1989, 57:963-968.
86. Reiner D.S., McCaffery M., Gillin F.D. Sorting of cyst wall proteins to a regulated secretory pathway during differentiation of the primitive eukaryote, Giardia lamblia. Eur. J. Cell Biol. 1990, 53:142-153.
87. Ringqvist E., Palm J.E., Skarin H., Hehl A.B., Weiland M., Davids B.J., Reiner D.S., Griffiths W.J., Eckmann L., Gillin F.D., Svard S.G. Release of metabolic enzymes by Giardia in response to interaction with intestinal epithelial cells. Mol. Biochem. Parasitol. 2008, 159:85-91.
88. Rivero M.R., Vranych C.V., Bisbal M., Maletto B.A., Ropolo A.S., Touz M.C. Adaptor protein 2 regulates receptor-mediated endocytosis and cyst formation in Giardia lamblia. Biochem J. 2010, 428:33-45.
89. Rodriguez-Fuentes G.B., Cedillo-Rivera R., Fonseca-Linan R., Arguello-Garcia R., Munoz O., Ortega-Pierres G., Yepez-Mulia L. Giardia duodenalis: analysis of secreted proteases upon trophozoite-epithelial cell interaction in vitro. Memorias do Instituto Oswaldo Cruz 2006, 101:693-696.
90. Roxstrom-Lindquist K., Ringqvist E., Palm D., Svard S. Giardia lamblia-induced changes in gene expression in differentiated Caco-2 human intestinal epithelial cells. Infect. Immun. 2005, 73:8204-8208.
91. Saito-Nakano Y., Loftus B.J., Hall N., Nozaki T. The diversity of Rab GTPases in Entamoeba histolytica. Exp. Parasitol. 2005, 110:244-252.
92. Samra H.K., Ganguly N.K., Garg U.C., Goyal J., Mahajan R.C. Effect of excretory-secretory products of Giardia lamblia on glucose and phenylalanine transport in the small intestine of Swiss albino mice. Biochem. Int. 1988, 17:801-812.
93. Samuelson J., Banerjee S., Magnelli P., Cui J., Kelleher D.J., Gilmore R., Robbins P.W. The diversity of dolichol-linked precursors to Asn-linked glycans likely results from secondary loss of sets of glycosyltransferases. Proc. Natl. Acad. Sci. USA 2005, 102:1548-1553.
94. Schledzewski K., Brinkmann H., Mendel R.R. Phylogenetic analysis of components of the eukaryotic vesicle transport system reveals a common origin of adaptor protein complexes 1, 2, and 3 and the F subcomplex of the coatomer COPI. J. Mol. Evol. 1999, 48:770-778.
95. Sheffield H.G., Bjorvat B. Ultrastructure of the cyst of Giardia lamblia. Am. J. Trop. Med. Hyg. 1977, 26:23-30.
96. Silverman J.M., Reiner N.E. Exosomes and other microvesicles in infection biology: organelles with unanticipated phenotypes. Cell Microbiol. 2011, 13:1-9.
97. Slavin I., Saura A., Carranza P.G., Touz M.C., Nores M.J., Lujan H.D. Dephosphorylation of cyst wall proteins by a secreted lysosomal acid phosphatase is essential for excystation of Giardia lamblia. Mol. Biochem. Parasitol. 2002, 122:95-98.
98. Smith P.D., Gillin F.D., Spira W.M., Nash T.E. Chronic giardiasis: studies on drug sensitivity, toxin production, and host immune response. Gastroenterology 1982, 83:797-803.
99. Soltys B.J., Falah M., Gupta R.S. Identification of endoplasmic reticulum in the primitive eukaryote Giardia lamblia using cryoelectron microscopy and antibody to Bip. J. Cell Sci. 1996, 109(Pt 7):1909-1917.
100. Stefanic S., Palm D., Svard S.G., Hehl A.B. Organelle proteomics reveals cargo maturation mechanisms associated with Golgi-like encystation vesicles in the early-diverged protozoan Giardia lamblia. J. Biol. Chem. 2006, 281:7595-7604.
101. Stefanic S., Morf L., Kulangara C., Regos A., Sonda S., Schraner E., Spycher C., Wild P., Hehl A.B. Neogenesis and maturation of transient Golgi-like cisternae in a simple eukaryote. J. Cell Sci. 2009, 122:2846-2856.
102. Sun C.H., McCaffery J.M., Reiner D.S., Gillin F.D. Mining the Giardia lamblia genome for new cyst wall proteins. J. Biol. Chem. 2003, 278:21701-21708.
103. Svard S.G., Rafferty C., McCaffery J.M., Smith M.W., Reiner D.S., Gillin F.D. A signal recognition particle receptor gene from the early-diverging eukaryote, Giardia lamblia. Mol. Biochem. Parasitol. 1999, 98:253-264.
104. Tai J.H., Ong S.J., Chang S.C., Su H.M. Giardiavirus enters Giardia lamblia WB trophozoite via endocytosis. Exp. Parasitol. 1993, 76:165-174.
105. Teoh D.A., Kamieniecki D., Pang G., Buret A.G. Giardia lamblia rearranges F-actin and alpha-actinin in human colonic and duodenal monolayers and reduces transepithelial electrical resistance. J. Parasitol. 2000, 86:800-806.
106. Thirion J., Wattiaux R., Jadot M. The acid phosphatase positive organelles of the Giardia lamblia trophozoite contain a membrane bound cathepsin C activity. Biol. Cell 2003, 95(2):99-105.
107. Tomavo S., Dubremetz J.F., Schwarz R.T. A family of glycolipids from Toxoplasma gondii. Identification of candidate glycolipid precursor(s) for Toxoplasma gondii glycosylphosphatidylinositol membrane anchors. J. Biol. Chem. 1992, 267:11721-11728.
108. Touz M.C., Gottig N., Nash T.E., Lujan H.D. Identification and characterization of a novel secretory granule calcium-binding protein from the early branching eukaryote Giardia lamblia. J. Biol. Chem. 2002, 277:50557-50563.
109. Touz M.C., Nores M.J., Slavin I., Carmona C., Conrad J.T., Mowatt M.R., Nash T.E., Coronel C.E., Lujan H.D. The activity of a developmentally regulated cysteine proteinase is required for cyst wall formation in the primitive eukaryote Giardia lamblia. J. Biol. Chem. 2002, 277:8474-8481.
110. Touz M.C., Lujan H.D., Hayes S.F., Nash T.E. Sorting of encystation-specific cysteine protease to lysosome-like peripheral vacuoles in Giardia lamblia requires a conserved tyrosine-based motif. J. Biol. Chem. 2003, 278:6420-6426.
111. Touz M.C., Kulakova L., Nash T.E. 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 2004, 15:3053-3060.
112. Touz M.C., Conrad J.T., Nash T.E. A novel palmitoyl acyl transferase controls surface protein palmitoylation and cytotoxicity in Giardia lamblia. Mol. Microbiol. 2005, 58:999-1011.
113. Touz M.C., Ropolo A.S., Rivero M.R., Vranych C.V., Conrad J.T., Svard S.G., Nash T.E. Arginine deiminase has multiple regulatory roles in the biology of Giardia lamblia. J. Cell Sci. 2008, 121:2930-2938.
114. Tovar J., Fischer A., Clark C.G. The mitosome, a novel organelle related to mitochondria in the amitochondrial parasite Entamoeba histolytica. Mol. Microbiol. 1999, 32:1013-1021.
115. Tovar J., Leon-Avila G., Sanchez L.B., Sutak R., Tachezy J., van der Giezen M., Hernandez M., Muller M., Lucocq J.M. Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature 2003, 426:172-176.
116. Troeger H., Epple H.J., Schneider T., Wahnschaffe U., Ullrich R., Burchard G.D., Jelinek T., Zeitz M., Fromm M., Schulzke J.D. Effect of chronic Giardia lamblia infection on epithelial transport and barrier function in human duodenum. Gut 2007, 56:328-335.
117. Van Keulen H., Steimle P.A., Bulik D.A., Borowiak R.K., Jarroll E.L. Cloning of two putative Giardia lamblia glucosamine 6-phosphate isomerase genes only one of which is transcriptionally activated during encystment. J. Eukaryot. Microbiol. 1998, 45:637-642.
118. Ward W., Alvarado L., Rawlings N.D., Engel J.C., Franklin C., McKerrow J.H. A primitive enzyme for a primitive cell: the protease required for excystation of Giardia. Cell 1997, 89:437-444.