Giardia cyst wall protein 1 is a lectin that binds to curled fibrils of the GaINAc homopolymer

PLoS Pathogens

Volumn 6, Issue 8, 2010, Pages 61-62

  Chatterjee, Aparajita ^a   Carpentieri, Andrea ^a   Ratner, Daniel M ^a   Bullitt, Esther ^b   Costello, Catherine E ^b   Robbins, Phillips W ^a   Samuelson, John ^a  

^a BOSTON UNIVERSITY   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHYMOTRYPSIN; GLYCOSIDASE; LECTIN; LECTIN CWP1; LECTIN CWP2; MALTOSE BINDING PROTEIN; N ACETYLGALACTOSAMINE; UNCLASSIFIED DRUG; CWP1 PROTEIN, GIARDIA LAMBLIA; PROTOZOAL PROTEIN;

ARTICLE; CELL MEMBRANE PERMEABILITY; CELL VACUOLE; CELL WALL; CONTROLLED STUDY; CYST (RESTING STAGE); ENZYME DEGRADATION; EXCYSTATION; FIBER; FLOW CYTOMETRY; GIARDIA LAMBLIA; LIFE CYCLE; NONHUMAN; PROTEIN BINDING; PROTEIN STRUCTURE; TROPHOZOITE; ULTRASOUND; CELL SEPARATION; CHEMISTRY; METABOLISM; TRANSMISSION ELECTRON MICROSCOPY;

GIARDIA; GIARDIA INTESTINALIS;

ACETYLGALACTOSAMINE; CELL SEPARATION; CELL WALL; FLOW CYTOMETRY; GIARDIA LAMBLIA; LECTINS; MICROSCOPY, ELECTRON, TRANSMISSION; PROTOZOAN PROTEINS;

EID: 77958121047     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001059     Document Type: Article

References (53)

1. Adam RD (2001) Biology of Giardia lamblia. Clin Microbiol Rev 14: 447-475.
2. Morrison HG, McArthur AG, Gillin FD, Aley SB, Adam RD, et al. (2007) Genomic minimalism in the early diverging intestinal parasite Giardia lamblia. Science 317: 1921-1926.
3. Franzen O, Jerlstrom-Hultqvist J, Castro E, Sherwood E, Ankarklev J, et al. (2009) Draft genome sequencing of Giardia intestinalis assemblage B isolate GS: is human giardiasis caused by two different species? PLoS Pathog 5: e1000560.
4. Steiner TS, Thielman NM, Guerrant RL (1997) Protozoal agents: what are the dangers for the public water supply? Annu Rev Med 48: 329-340.
5. Lauwaet T, Davids BJ, Reiner DS, Gillin FD (2007) Encystation of Giardia lamblia: a model for other parasites. Curr Opin Microbiol 210: 554-559.
6. Lujan HD, Mowatt MR, Conrad JT, Bowers B, Nash TE (1995) 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: 29307-29313.
7. Mowatt MR, Lujan HD, Cotten DB, Bowers B, Yee J, et al. (1995) Developmentally regulated expression of a Giardia lamblia cyst wall protein gene. Mol Microbiol 15: 955-963.
8. Hehl AB, Marti M, Kohler P (2000) Stage-specific expression and targeting of cyst wall protein-green fluorescent protein chimeras in Giardia. Mol Biol Cell 11: 1789-1800.
9. Sun CH, McCaffery JM, Reiner DS, Gillin FD (2003) Mining the Giardia lamblia genome for new cyst wall proteins. J Biol Chem 278: 21701-21708.
10. Meng TC, Hetsko ML, Gillin FD (1996) Inhibition of Giardia lamblia excystation by antibodies against cyst walls and by wheat germ agglutinin. Infect Immun 64: 2151-2157.
11. Boone JH, Wilkins TD, Nash TE, Brandon JE, Macias EA, et al. (1999) TechLab and alexon Giardia enzyme-linked immunosorbent assay kits detect cyst wall protein 1. J Clin Microbiol 37: 611-614.
12. Lee P, Abdul-Wahid A, Faubert GM (2009) Comparison of the local immune response against Giardia lamblia cyst wall protein 2 induced by recombinant Lactococcus lactis and Streptococcus gordonii. Microbes Infect 11: 20-28.
13. Ortega-Barria E, Ward HD, Evans JE, Pereira ME (1990) N-acetyl-Dglucosamine is present in cysts and trophozoites of Giardia lamblia and serves as receptor for wheatgerm agglutinin. Mol Biochem Parasitol 43: 151-165.
14. Samuelson J, Banerjee S, Magnelli P, Cui J, Kelleher DJ, et al. (2005) The diversity of protist and fungal dolichol-linked precursors to Asn-linked glycans likely results from secondary loss of sets of glycosyltransferases. Proc Natl Acad Sci USA 102: 1548-1553.
15. Ratner DM, Cui J, Steffen M, Moore LL, Robbins PW, et al. (2008) Changes in the N-glycome, glycoproteins with Asn linked glycans, of Giardia lamblia with differentiation from trophozoites to cysts. Eukaryot Cell 7: 1930-1940.
16. Davids BJ, Reiner DS, Birkeland SR, Preheim SP, Cipriano MJ, et al. (2006) A new family of giardial cysteine-rich non-VSP protein genes and a novel cyst protein. PLoS ONE 1: e44.
17. Chiu PW, Huang YC, Pan YJ, Wang CH, Sun CH (2010) A novel family of cyst proteins with epidermal growth factor repeats in Giardia lamblia. PLoS Negl Trop Dis 45: e677.
18. Stefanic S, Morf L, Kulangara C, Regos A, Sonda S, et al. (2009) Neogenesis and maturation of transient Golgi-like cisternae in a simple eukaryote. J Cell Sci 122: 2846-2856.
19. Gottig N, Elias EV, Quiroga R, Nores MJ, Solari AJ, et al. (2006) Active and passive mechanisms drive secretory granule biogenesis during differentiation of the intestinal parasite Giardia lamblia. J Biol Chem 281: 18156-18166.
20. Konrad C, Spycher C, Hehl AB (2010) Selective condensation drives partitioning and sequential secretion of cyst wall proteins in differentiating Giardia lamblia. PLoS Pathog 6: e1000835.
21. Touz MC, Nores MJ, Slavin I, Carmona C, Conrad JT, et al. (2002) 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.
22. Ward W, Alvarado L, Rawlings ND, Engel JC, Franklin C, et al. (1997) A primitive enzyme for a primitive cell: the protease required for excystation of Giardia. Cell 89: 437-444.
23. Boucher SE, Gillin FD (1990) Excystation of in vitro-derived Giardia lamblia cysts. Infect Immun 58: 3516-3522.
24. Reiner DS, McCaffery JM, Gillin FD (2001) Reversible interruption of Giardia lamblia cyst wall protein transport in a novel regulated secretory pathway. Cell Microbiol 3: 459-472.
25. Davids BJ, Mehta K, Fesus L, McCaffery JM, Gillin FD (2004) Dependence of Giardia lamblia encystation on novel transglutaminase activity. Mol Biochem Parasitol 136: 173-180.
26. Slavin I, Saura A, Carranza PG, Touz MC, Nores MJ, et al. (2002) Dephosphorylation of cyst wall proteins by a secreted lysosomal acid phosphatase is essential for excystation of Giardia lamblia. Mol Biochem Parasitol 122: 95-98.
27. Lauwaet T, Davids BJ, Torres-Escobar A, Birkeland SR, Cipriano MJ, et al. (2007) Protein phosphatase 2A plays a crucial role in Giardia lamblia differentiation. Mol Biochem Parasitol 152: 80-89.
28. Gerwig GJ, van Kuik JA, Leeflang BR, Kamerling JP, Vliegenthart JF, et al. (2002) The Giardia intestinalis filamentous cyst wall contains a novel beta(1-3)-Nacetyl- D-galactosamine polymer: a structural and conformational study. Glycobiology 12: 499-505.
29. Erlandsen SL, Macechko PT, van Keulen H, Jarroll EL (1996) Formation of the Giardia cyst wall: studies on extracellular assembly using immunogold labeling and high resolution field emission SEM. J Eukaryot Microbiol 43: 416-429.
30. Chavez-Munguia B, Cedillo-Rivera R, Martinez-Palomo A (2004) The ultrastructure of the cyst wall of Giardia lamblia. J Eukaryot Microbiol 51: 220-226.
31. Karr CD, Jarroll EL (2004) Cyst wall synthase: N-acetylgalactosaminyltransferase activity is induced to form the novel N-acetylgalactosamine polysaccharide in the Giardia cyst wall. Microbiology 150: 1237-1243.
32. West CM (2003) Comparative analysis of spore coat formation, structure, and function in Dictyostelium. Int Rev Cytol 222: 237-293.
33. Lesage G, Bussey H (2006) Cell wall assembly in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 70: 317-343.
34. Jamet E, Albenne C, Boudart G, Irshad M, Canut H, et al. (2008) Recent advances in plant cell wall proteomics. Proteomics 8: 893-908.
35. Frisardi M, Ghosh SK, Field J, Van Dellen K, Rogers R, et al. (2000) The most abundant glycoprotein of amebic cyst walls (Jacob) is a lectin with five Cys-rich, chitin-binding domains. Infect Immun 68: 4217-4224.
36. Van Dellen K, Ghosh SK, Robbins PW, Loftus B, Samuelson J (2002) Entamoeba histolytica lectins contain unique 6-Cys or 8-Cys chitin-binding domains. Infect Immun 70: 3259-3263.
37. de la Vega H, Specht CA, Semino CE, Robbins PW, Eichinger D, et al. (1997) Cloning and expression of chitinases of Entamoebae. Mol Biochem Parasitol 85: 139-147.
38. Van Dellen KL, Chatterjee A, Ratner DM, Magnelli PE, Cipollo JF, et al. (2006) Unique posttranslational modifications of chitin-binding lectins of Entamoeba invadens cyst walls. Eukaryot Cell 5: 836-848.
39. Chatterjee A, Ghosh SK, Jang K, Bullitt E, Moore L, et al. (2009) Evidence for a "wattle and daub" model of the cyst wall of entamoeba. PLoS Pathog 5: e1000498.
40. Manners DJ, Meyer MT (1977) The molecular structures of some glucans from the cell walls of Schizosaccharomyces pombe. Carbohydr Res 57: 189-203.
41. Nallamsetty S, Waugh DS (2007) A generic protocol for the expression and purification of recombinant proteins in Escherichia coli using a combinatorial His6- maltose binding protein fusion tag. Nat Protoc 2: 383-391.
42. Cabib E, Roh DH, Schmidt M, Crotti LB, Varma A (2001) The yeast cell wall and septum as paradigms of cell growth and morphogenesis. J Biol Chem 276: 19679-19682.
43. Nanduri J, Williams S, Aji T, Flanigan TP (1999) Characterization of an immunogenic glycocalyx on the surfaces of Cryptosporidium parvum oocysts and sporozoites. Infect Immun 67: 2022-2024.
44. Oliver RM (1973) Negative stain electron microscopy of protein macromolecules. Methods Enzymol 27: 616-762.
45. Chatterjee A, Banerjee S, Steffen M, O'Connor RM, Ward HD, et al. (2010) Evidence for mucin-like glycoproteins that tether sporozoites of Cryptosporidium parvum to the inner surface of the oocyst wall. Eukaryot Cell 9: 84-96.
46. Ghosh S, Frisardi M, Rogers R, Samuelson J (2001) How Giardia swim and divide. Infect Immun 69: 7866-7872.
47. Ding SY, Himmel ME (2006) The maize primary cell wall microfibril: a new model derived from direct visualization. J Agric Food Chem 54: 597-606.
48. Lenardon MD, Whitton RK, Munro CA, Marshall D, Gow NA (2007) Individual chitin synthase enzymes synthesize microfibrils of differing structure at specific locations in the Candida albicans cell wall. Mol Microbiol 66: 1164-1173.
49. Wright HT, Sandrasegaram G, Wright CS (1991) Evolution of a family of Nacetylglucosamine binding proteins containing the disulfide-rich domain of wheat germ agglutinin. J Mol Evol 33: 283-294.
50. Jin MS, Lee JO (2008) Structures of the toll-like receptor family and its ligand complexes. Immunity 29: 182-191.
51. Shaw MH, Reimer T, Kim YG, Nuñez G (2008) NOD-like receptors (NLRs): bona fide intracellular microbial sensors. Curr Opin Immunol 20: 377-382.
52. Cabib E, Shematuck EM (1981) Structural polysaccharides of plants and fungi: comparative and morphogenetic aspects. In: Ginsburg V, Robbins P, eds. Biology of Carbohydrates. New York: John Wiley & Sons vol 1: 51-90.
53. Carrington WA, Lynch RM, Moore ED, Isenberg G, Fogarty KE, et al. (1995) Superresolution three-dimensional images of fluorescence in cells with minimal light exposure. Science 268: 1483-1487.