Encystation of Giardia lamblia: a model for other parasites

Current Opinion in Microbiology

Volumn 10, Issue 6, 2007, Pages 554-559

  Lauwaet, Tineke ^a   Davids, Barbara J ^a   Reiner, David S ^a   Gillin, Frances D ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOGENESIS; CELL DIFFERENTIATION; CELL FUNCTION; CELL STRUCTURE; GIARDIA LAMBLIA; INTESTINE PARASITE; MICROBIAL COLONIZATION; MOLECULAR MECHANICS; NONHUMAN; PROTOZOON; REVIEW; SIGNAL TRANSDUCTION; TROPHOZOITE;

ANIMALS; CELL WALL; GENE EXPRESSION REGULATION; GIARDIA LAMBLIA; PROTOZOAN PROTEINS;

GIARDIA; GIARDIA INTESTINALIS;

EID: 36549083072     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mib.2007.09.011     Document Type: Review

References (48)

1. Huang D.B., and White A.C. An updated review on Cryptosporidium and Giardia. Gastroenterol Clin North Am 35 (2006) 291-314. This recent review summarizes the pathogenesis, clinical symptoms, and epidemiology of giardiasis compared with cryptosporidiosis.
2. Adam R.D. Biology of Giardia lamblia. Clin Microbiol Rev 14 (2001) 447-475
3. Lee P., and Faubert G.M. Oral immunization of BALB/c mice by intragastric delivery of Streptococcus gordonii-expressing Giardia cyst wall protein 2 decreases cyst shedding in challenged mice. FEMS Microbiol Lett 265 (2006) 225-236
4. Lee P., and Faubert G.M. Expression of the Giardia lamblia cyst wall protein 2 in Lactococcus lactis. Microbiology 152 (2006) 1981-1990
5. Larocque R., Nakagaki K., Lee P., Abdul-Wahid A., and Faubert G.M. Oral immunization of BALB/c mice with Giardia duodenalis recombinant cyst wall protein inhibits shedding of cysts. Infect Immun 71 (2003) 5662-5669
6. Palm D., Weiland M., McArthur A.G., Winiecka-Krusnell J., Cipriano M.J., Birkeland S.R., Pacocha S.E., Davids B., Gillin F., Linder E., et al. Developmental changes in the adhesive disk during Giardia differentiation. Mol Biochem Parasitol 141 (2005) 199-207. In this paper, the authors describe the structure and protein composition of the attachment disk in the Giardia life cycle. In addition, they characterize the new disk protein SALP-1. This is one of the few papers showing immunofluorescence images of excysting cells.
7. Svard S.G., Hagblom P., and Palm J.E. Giardia lamblia-a model organism for eukaryotic cell differentiation. FEMS Microbiol Lett 218 (2003) 3-7
8. Marti M., and Hehl A.B. Encystation-specific vesicles in Giardia: a primordial Golgi or just another secretory compartment?. Trends Parasitol 19 (2003) 440-446
9. Hehl A.B., and Marti M. Secretory protein trafficking in Giardia intestinalis. Mol Microbiol 53 (2004) 19-28
10. Lujan H.D., and Touz M.C. Protein trafficking in Giardia lamblia. Cell Microbiol 5 (2003) 427-434
11. Chavez-Munguia B., Omana-Molina M., Gonzalez-Lazaro M., Gonzalez-Robles A., Cedillo-Rivera R., Bonilla P., and Martinez-Palomo A. Ultrastructure of cyst differentiation in parasitic protozoa. Parasitol Res 100 (2007) 1169-1175. This review illustrates and compares the ultrastructure of E. invadens, A. castellanii, and G. lamblia ESV and cyst walls.
12. Mowatt M.R., Lujan H.D., Cotten D.B., Bowers B., Yee J., Nash T.E., and Stibbs H.H. Developmentally regulated expression of a Giardia lamblia cyst wall protein gene. Mol Microbiol 15 (1995) 955-963
13. Lujan H.D., Mowatt M.R., Conrad J.T., Bowers B., and 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 270 (1995) 29307-29313
14. Sun C.H., McCaffery J.M., Reiner D.S., and Gillin F.D. Mining the Giardia lamblia genome for new cyst wall proteins. J Biol Chem 278 (2003) 21701-21708
15. Davids B.J., Reiner D.S., Birkeland S.R., Preheim S.P., Cipriano M.J., McArthur A.G., and Gillin F.D. A new family of giardial cysteine-rich non-VSP protein genes and a novel cyst protein. PLoS ONE 1 (2006) e44. This paper describes a protein, HCNCp, with sequence similarity to Giardia variant surface proteins, which surprisingly does not localize to the Giardia trophozoite surface membrane but traffics via the ESV to the cyst wall. It belongs to a group of 61 unusual cysteine-rich proteins.
16. Reiner D.S., McCaffery M., and 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 53 (1990) 142-153
17. Gottig N., Elias E.V., Quiroga R., Nores M.J., Solari A.J., Touz M.C., and Lujan H.D. Active and passive mechanisms drive secretory granule biogenesis during differentiation of the intestinal parasite Giardia lamblia. J Biol Chem 281 (2006) 18156-18166
18. Thiele C., Gerdes H.H., and Huttner W.B. Protein secretion: puzzling receptors. Curr Biol 7 (1997) R496-R500
19. Reiner D.S., McCaffery J.M., and Gillin F.D. Reversible interruption of Giardia lamblia cyst wall protein transport in a novel regulated secretory pathway. Cell Microbiol 3 (2001) 459-472
20. Stefanic S., Palm D., Svard S.G., and 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 281 (2006) 7595-7604. In this paper, the authors report the first limited proteomic analysis of isolated ESV. The ESV were isolated from encysting trophozoites by sucrose density fractionation, and proteins in the ESV-containing fraction were resolved by 2D-PAGE and identified by mass spectrometry.
21. McArthur A.G., Knodler L.A., Silberman J.D., Davids B.J., Gillin F.D., and Sogin M.L. The evolutionary origins of eukaryotic protein disulfide isomerase domains: new evidence from the Amitochondriate protist Giardia lamblia. Mol Biol Evol 18 (2001) 1455-1463
22. 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., and Gillin F.D. Novel protein-disulfide isomerases from the early-diverging protist Giardia lamblia. J Biol Chem 274 (1999) 29805-29811
23. Davids B.J., Mehta K., Fesus L., McCaffery J.M., and Gillin F.D. Dependence of Giardia lamblia encystation on novel transglutaminase activity. Mol Biochem Parasitol 136 (2004) 173-180
24. 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., and Gillin F.D. Novel protein-disulfide isomerases from the early-diverging protist Giardia lamblia. J Biol Chem 275 (2000) 28339
25. Touz M.C., Nores M.J., Slavin I., Carmona C., Conrad J.T., Mowatt M.R., Nash T.E., Coronel C.E., and 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 277 (2002) 8474-8481
26. Slavin I., Saura A., Carranza P.G., Touz M.C., Nores M.J., and Lujan H.D. Dephosphorylation of cyst wall proteins by a secreted lysosomal acid phosphatase is essential for excystation of Giardia lamblia. Mol Biochem Parasitol 122 (2002) 95-98
27. Touz M.C., Gottig N., Nash T.E., and Lujan H.D. Identification and characterization of a novel secretory granule calcium-binding protein from the early branching eukaryote Giardia lamblia. J Biol Chem 277 (2002) 50557-50563
28. Lauwaet T., Davids B.J., Torres-Escobar A., Birkeland S.R., Cipriano M.J., Preheim S.P., Palm D., Svard S.G., McArthur A.G., and Gillin F.D. Protein phosphatase 2A plays a crucial role in Giardia lamblia differentiation. Mol Biochem Parasitol 152 (2007) 80-89. Using antisense mRNA and immunofluorescence analysis, authors demonstrate a role for PP2A-C in Giardia encystation and excystation and show its localization throughout the life cycle.
29. Merzendorfer H. Insect chitin synthases: a review. J Comp Physiol [B] 176 (2006) 1-15
30. Lesage G., and Bussey H. Cell wall assembly in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 70 (2006) 317-343
31. Gerwig G.J., van Kuik J.A., Leeflang B.R., Kamerling J.P., Vliegenthart J.F., Karr C.D., and 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 12 (2002) 499-505
32. Van Dellen K.L., Bulik D.A., Specht C.A., Robbins P.W., and Samuelson J.C. Heterologous expression of an Entamoeba histolytica chitin synthase in Saccharomyces cerevisiae. Eukaryot Cell 5 (2006) 203-206
33. Sun C.H., Palm D., McArthur A.G., Svard S.G., and Gillin F.D. A novel Myb-related protein involved in transcriptional activation of encystation genes in Giardia lamblia. Mol Microbiol 46 (2002) 971-984
34. Yang H., Chung H.J., Yong T., Lee B.H., and Park S. Identification of an encystation-specific transcription factor, Myb protein in Giardia lamblia. Mol Biochem Parasitol 128 (2003) 167-174
35. Sun C.H., Su L.H., and Gillin F.D. Novel plant-GARP-like transcription factors in Giardia lamblia. Mol Biochem Parasitol 146 (2006) 45-57
36. Davis-Hayman S.R., Hayman J.R., and Nash T.E. Encystation-specific regulation of the cyst wall protein 2 gene in Giardia lamblia by multiple cis-acting elements. Int J Parasitol 33 (2003) 1005-1012
37. Knodler L.A., Svard S.G., Silberman J.D., Davids B.J., and Gillin F.D. Developmental gene regulation in Giardia lamblia: first evidence for an encystation-specific promoter and differential 5′ mRNA processing. Mol Microbiol 34 (1999) 327-340
38. Hehl A.B., Marti M., and Kohler P. Stage-specific expression and targeting of cyst wall protein-green fluorescent protein chimeras in Giardia. Mol Biol Cell 11 (2000) 1789-1800
39. Marti M., Li Y., Schraner E.M., Wild P., Kohler P., and 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 14 (2003) 1433-1447
40. Gibson C., Schanen B., Chakrabarti D., and Chakrabarti R. Functional characterisation of the regulatory subunit of cyclic AMP-dependent protein kinase A homologue of Giardia lamblia: differential expression of the regulatory and catalytic subunits during encystation. Int J Parasitol 36 (2006) 791-799. The authors report an increased activity of PKAc and describe the expression and localization patterns of PKAc and PKAr in encystation.
41. Ellis JGt, Davila M., and Chakrabarti R. Potential involvement of extracellular signal-regulated kinase 1 and 2 in encystation of a primitive eukaryote, Giardia lamblia. Stage-specific activation and intracellular localization. J Biol Chem 278 (2003) 1936-1945
42. Bazan-Tejeda M.L., Arguello-Garcia R., Bermudez-Cruz R.M., Robles-Flores M., and Ortega-Pierres G. Protein kinase C isoforms from Giardia duodenalis: identification and functional characterization of a beta-like molecule during encystment. Arch Microbiol 187 (2007) 55-66. In this paper, the presence of PKC-like activity in Giardia is reported for the first time. Inhibition of this activity blocks encystation.
43. Kim K.T., Mok M.T., and Edwards M.R. Protein kinase B from Giardia intestinalis. Biochem Biophys Res Commun 334 (2005) 333-341
44. Abel E.S., Davids B.J., Robles L.D., Loflin C.E., Gillin F.D., and Chakrabarti R. Possible roles of protein kinase A in cell motility and excystation of the early diverging eukaryote Giardia lamblia. J Biol Chem 276 (2001) 10320-10329
45. Lopez A.B., Sener K., Jarroll E.L., and van Keulen H. Transcription regulation is demonstrated for five key enzymes in Giardia intestinalis cyst wall polysaccharide biosynthesis. Mol Biochem Parasitol 128 (2003) 51-57
46. Gallego E., Alvarado M., and Wasserman M. Identification and expression of the protein ubiquitination system in Giardia intestinalis. Parasitol Res 101 (2007) 1-7
47. Marti M., Regos A., Li Y., Schraner E.M., Wild P., Muller N., Knopf L.G., and Hehl A.B. An ancestral secretory apparatus in the protozoan parasite Giardia intestinalis. J Biol Chem 278 (2003) 24837-24848
48. 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., et al. Genomic minimalism in the early diverging intestinal parasite Giardia lamblia. Science 317 (2007) 1921-1926. This is a comprehensive review of the data obtained from the Giardia lamblia genome-sequencing project. It highlights gene classes and the molecular components of unique cellular processes in Giardia.