Novel structural components of the ventral disc and lateral crest in giardia intestinalis

PLoS Neglected Tropical Diseases

Volumn 5, Issue 12, 2011, Pages

  Hagen, Kari D ^a   Hirakawa, Matthew P ^a   House, Susan A ^a   Schwartz, Cindi L ^b   Pham, Jonathan K ^a   Cipriano, Michael J ^a   de la Torre, Moises J ^a   Sek, Albert C ^a   Du, Gary ^a   Forsythe, Brystal M ^a   Dawson, Scott C ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF COLORADO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DISC ASSOCIATED PROTEIN; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; PROTOZOAL PROTEIN; UNCLASSIFIED DRUG; PROTEOME;

ARTICLE; AXONEME; CHEMICAL LABELING; CONTROLLED STUDY; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GIARDIA LAMBLIA; MICROTUBULE; MOLECULAR CLONING; MOLECULAR IMAGING; NONHUMAN; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; PROTEOMICS; SEQUENCE ANALYSIS; STRUCTURE ANALYSIS; CELL ADHESION; CHEMISTRY; GENETICS; METABOLISM; METHODOLOGY; MICROSCOPY; PHYSIOLOGY; STAINING; ULTRASTRUCTURE;

CELL ADHESION; GIARDIA LAMBLIA; GREEN FLUORESCENT PROTEINS; MICROSCOPY; PROTEOME; PROTOZOAN PROTEINS; RECOMBINANT FUSION PROTEINS; STAINING AND LABELING;

EID: 84855266088     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0001442     Document Type: Article

References (76)

1. Hotez PJ, (2008) Neglected infections of poverty in the United States of America. PLoS Negl Trop Dis 2: e256.
2. Savioli L, Smith H, Thompson A, (2006) Giardia and Cryptosporidium join the 'Neglected Diseases Initiative'. Trends Parasitol 22: 203-208.
3. Land KM, Johnson PJ, (1999) Molecular basis of metronidazole resistance in pathogenic bacteria and protozoa. Drug Resist Updat 2: 289-294.
4. Barat LM, Bloland PB, (1997) Drug resistance among malaria and other parasites. Infect Dis Clin North Am 11: 969-987.
5. Upcroft J, Samarawickrema N, Brown D, Upcroft P, (1996) Mechanisms of metronidazole resistance in Giardia and Entamoeba. Abstracts of the Interscience Conference on Antimicrobial Agents and Chemotherapy 36: 47.
6. Adam RD, (2001) Biology of Giardia lamblia. Clin Microbiol Rev 14: 447-475.
7. Elmendorf HG, Dawson SC, McCaffery JM, (2003) The cytoskeleton of Giardia lamblia. Int J Parasitol 33: 3-28.
8. Gillin FD, Reiner DS, McCaffery JM, (1996) Cell biology of the primitive eukaryote Giardia lamblia. Annu Rev Microbiol 50: 679-705.
9. Leclerc H, Schwartzbrod L, Dei-Cas E, (2002) Microbial agents associated with waterborne diseases. Crit Rev Microbiol 28: 371-409.
10. Friend DS, (1966) The fine structure of Giardia muris. J Cell Biol 29: 317-332.
11. Dawson SC, House SA, (2010) Life with eight flagella: flagellar assembly and division in Giardia. Curr Opin Microbiol 13: 480-490.
12. House SA, Richter D, Pham JK, Dawson SC, (2011) Giardia flagellar motility is not directly required to maintain attachment to surfaces. PLoS Pathog 7: e1002167.
13. Holberton DV, (1974) Attachment of Giardia-a hydrodynamic model based on flagellar activity. J Exp Biol 60: 207-221.
14. Hansen WR, Fletcher DA, (2008) Tonic shock induces detachment of Giardia lamblia. PLoS Negl Trop Dis 2: e169.
15. Hansen WR, Tulyathan O, Dawson SC, Cande WZ, Fletcher DA, (2006) Giardia lamblia attachment force is insensitive to surface treatments. Eukaryot Cell 5: 781-783.
16. Feely DE, Erlandsen SL, (1981) Isolation and purification of Giardia trophozoites from rat intestine. J Parasitol 67: 59-64.
17. Feely DE, Erlandsen SL, (1982) Effect of cytochalasin-B, low Ca++ concentration, iodoacetic acid, and quinacrine-HCl on the attachment of Giardia trophozoites in vitro. J Parasitol 68: 869-873.
18. Inge PM, Edson CM, Farthing MJ, (1988) Attachment of Giardia lamblia to rat intestinal epithelial cells. Gut 29: 795-801.
19. Mariante RM, Vancini RG, Melo AL, Benchimol M, (2005) Giardia lamblia: evaluation of the in vitro effects of nocodazole and colchicine on trophozoites. Exp Parasitol 110: 62-72.
20. Sousa M, Concalves CA, Bairos VA, Poiares-Da-Silva J, (2001) Adherence of Giardia lamblia trophozoites to Int-407 human intestinal cells. Clin Diagn Lab Immunol 8: 258-265.
21. Feely DE, Schollmeyer JV, Erlandsen SL, (1982) Giardia spp.: distribution of contractile proteins in the attachment organelle. Exp Parasitol 53: 145-154.
22. Crossley R, Holberton DV, (1985) Assembly of 2.5 nm filaments from giardin, a protein associated with cytoskeletal microtubules in Giardia. J Cell Sci 78: 205-231.
23. Crossley R, Holberton DV, (1983) Characterization of proteins from the cytoskeleton of Giardia lamblia. J Cell Sci 59: 81-103.
24. Holberton DV, (1973) Fine structure of the ventral disk apparatus and the mechanism of attachment in the flagellate Giardia muris. J Cell Sci 13: 11-41.
25. Holberton DV, (1981) Arrangement of subunits in microribbons from Giardia. J Cell Sci 47: 167-185.
26. Feely DE, Hoberton DV, Erlandsen SL, (1990) The Biology of Giardia. In: Meyer EA, editors. Giardiasis Amsterdam Elsevier pp. 11-50.
27. Dawson SC, (2010) An insider's guide to the microtubule cytoskeleton of Giardia. Cell Microbiol 12: 588-598.
28. Weiland ME, McArthur AG, Morrison HG, Sogin ML, Svard SG, (2005) Annexin-like alpha giardins: a new cytoskeletal gene family in Giardia lamblia. Int J Parasitol 35: 617-626.
29. Weiland ME, Palm JE, Griffiths WJ, McCaffery JM, Svard SG, (2003) Characterisation of alpha-1 giardin: an immunodominant Giardia lamblia annexin with glycosaminoglycan-binding activity. Int J Parasitol 33: 1341-1351.
30. Bauer B, Engelbrecht S, Bakker-Grunwald T, Scholze H, (1999) Functional identification of alpha-1 giardin as an annexin of Giardia lamblia. FEMS Microbiol Lett 173: 147-153.
31. Peattie DA, (1990) The giardins of Giardia lamblia: genes and proteins with promise. Parasitol Today 6: 52-56.
32. Palm JE, Weiland ME, Griffiths WJ, Ljungstrom I, Svard SG, (2003) Identification of immunoreactive proteins during acute human giardiasis. J Infect Dis 187: 1849-1859.
33. Nohria A, Alonso RA, Peattie DA, (1992) Identification and characterization of gamma giardin and the gamma giardin gene from Giardia lamblia. Mol Biochem Parasitol 56: 27-37.
34. Ellis JG, Davila M, Chakrabarti R, (2003) 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: 1936-1945.
35. Davids BJ, Williams S, Lauwaet T, Palanca T, Gillin FD, (2008) Giardia lamblia aurora kinase: a regulator of mitosis in a binucleate parasite. Int J Parasitol 38: 353-369.
36. Lauwaet T, Smith AJ, Reiner DS, Romijn EP, Wong CC, et al. (2011) Mining the Giardia genome and proteome for conserved and unique basal body proteins. Int J Parasitol 41: 1079-1092.
37. Link AJ, Eng J, Schieltz DM, Carmack E, Mize GJ, et al. (1999) Direct analysis of protein complexes using mass spectrometry. Nat Biotechnol 17: 676-682.
38. 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.
39. Dawson SC, House SA, (2010) Imaging and analysis of the microtubule cytoskeleton in Giardia. Methods Cell Biol 97: 307-339.
40. Jenkins MC, O'Brien CN, Murphy C, Schwarz R, Miska K, et al. (2009) Antibodies to the ventral disc protein delta-giardin prevent in vitro binding of Giardia lamblia trophozoites. J Parasitol 95: 895-899.
41. Keister DB, (1983) Axenic culture of Giardia lamblia in TYI-S-33 medium supplemented with bile. Trans R Soc Trop Med Hyg 77: 487-488.
42. Holberton DV, Ward AP, (1981) Isolation of the cytoskeleton from Giardia. Tubulin and a low-molecular-weight protein associated with microribbon structures. J Cell Sci 47: 139-166.
43. Keller A, Nesvizhskii AI, Kolker E, Aebersold R, (2002) Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 74: 5383-5392.
44. Nesvizhskii AI, Keller A, Kolker E, Aebersold R, (2003) A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 75: 4646-4658.
45. Sagolla MS, Dawson SC, Mancuso JJ, Cande WZ, (2006) Three-dimensional analysis of mitosis and cytokinesis in the binucleate parasite Giardia intestinalis. J Cell Sci 119: 4889-4900.
46. Davis-Hayman SR, Nash TE, (2002) Genetic manipulation of Giardia lamblia. Mol Biochem Parasitol 122: 1-7.
47. Sullivan KF, Kay SA, (1999) Green fluorescent proteins San Diego, London Academic Press.
48. Zeng X, Kahana JA, Silver PA, Morphew MK, McIntosh JR, et al. (1999) Slk19p is a centromere protein that functions to stabilize mitotic spindles. J Cell Biol 146: 415-425.
49. 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.
50. 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.
51. Jerlstrom-Hultqvist J, Franzen O, Ankarklev J, Xu F, Nohynkova E, et al. (2010) Genome analysis and comparative genomics of a Giardia intestinalis assemblage E isolate. BMC Genomics 11: 543.
52. Boudeau J, Miranda-Saavedra D, Barton GJ, Alessi DR, (2006) Emerging roles of pseudokinases. Trends Cell Biol 16: 443-452.
53. Weisbrich A, Honnappa S, Jaussi R, Okhrimenko O, Frey D, et al. (2007) Structure-function relationship of CAP-Gly domains. Nat Struct Mol Biol 14: 959-967.
54. Pfannenschmid F, Wimmer VC, Rios RM, Geimer S, Krockel U, et al. (2003) Chlamydomonas DIP13 and human NA14: a new class of proteins associated with microtubule structures is involved in cell division. J Cell Sci 116: 1449-1462.
55. Marshall J, Holberton DV, (1993) Sequence and structure of a new coiled coil protein from a microtubule bundle in Giardia. J Mol Biol 231: 521-530.
56. Holberton DV, (1973) Mechanism of attachment of Giardia to the wall of the small intestine. Trans R Soc Trop Med Hyg 67: 29-30.
57. Erlandsen SL, Russo AP, Turner JN, (2004) Evidence for adhesive activity of the ventrolateral flange in Giardia lamblia. J Eukaryot Microbiol 51: 73-80.
58. Mueller J, Jones AL, Brandborg LL, (1974) Scanning electron microscope observation in human giardiasis. In: Johari O, editors. Scanning electron microscopy Chicago IIT Research Institute pp. 557-564.
59. Fritz-Laylin LK, Prochnik SE, Ginger ML, Dacks JB, Carpenter ML, et al. (2010) The genome of Naegleria gruberi illuminates early eukaryotic versatility. Cell 140: 631-642.
60. Weber K, Geisler N, Plessmann U, Bremerich A, Lechtreck KF, et al. (1993) SF-assemblin, the structural protein of the 2-nm filaments from striated microtubule associated fibers of algal flagellar roots, forms a segmented coiled coil. J Cell Biol 121: 837-845.
61. Quarmby LM, Mahjoub MR, (2005) Caught Nek-ing: cilia and centrioles. J Cell Sci 118: 5161-5169.
62. Parker JD, Bradley BA, Mooers AO, Quarmby LM, (2007) Phylogenetic analysis of the Neks reveals early diversification of ciliary-cell cycle kinases. PLoS One 2: e1076.
63. Kannan N, Taylor SS, (2008) Rethinking pseudokinases. Cell 133: 204-205.
64. Tumova P, Kulda J, Nohynkova E, (2007) Cell division of Giardia intestinalis: assembly and disassembly of the adhesive disc, and the cytokinesis. Cell Motil Cytoskeleton 64: 288-298.
65. Sedgwick SG, Smerdon SJ, (1999) The ankyrin repeat: a diversity of interactions on a common structural framework. Trends Biochem Sci 24: 311-316.
66. Elmendorf HG, Rohrer SC, Khoury RS, Bouttenot RE, Nash TE, (2005) Examination of a novel head-stalk protein family in Giardia lamblia characterised by the pairing of ankyrin repeats and coiled-coil domains. Int J Parasitol 35: 1001-1011.
67. Davis LH, Otto E, Bennett V, (1991) Specific 33-residue repeat(s) of erythrocyte ankyrin associate with the anion exchanger. J Biol Chem 266: 11163-11169.
68. Piva B, Benchimol M, (2004) The median body of Giardia lamblia: an ultrastructural study. Biol Cell 96: 735-746.
69. Paredez AR, Assaf ZJ, Sept D, Timofejeva L, Dawson SC, et al. (2011) An actin cytoskeleton with evolutionarily conserved functions in the absence of canonical actin-binding proteins. Proc Natl Acad Sci U S A 108: 6151-6156.
70. Nabeshima K, Saitoh S, Yanagida M, (1997) Use of green fluorescent protein for intracellular protein localization in living fission yeast cells. Methods Enzymol 283: 459-471.
71. Bloom KS, Beach DL, Maddox P, Shaw SL, Yeh E, Salmon ED, (1999) Using green fluorescent protein fusion proteins to quantitate microtubule and spindle dynamics in budding yeast. In: Rieder CL, editors. Methods in Cell Biology San Diego Academic Press pp. 369-383.
72. Dawson SC, Sagolla MS, Mancuso JJ, Woessner DJ, House SA, et al. (2007) Kinesin-13 regulates flagellar, interphase, and mitotic microtubule dynamics in Giardia intestinalis. Eukaryot Cell 6: 2354-2364.
73. Touz MC, Conrad JT, Nash TE, (2005) A novel palmitoyl acyl transferase controls surface protein palmitoylation and cytotoxicity in Giardia lamblia. Mol Microbiol 58: 999-1011.
74. Carpenter ML, Cande WZ, (2009) Using morpholinos for gene knockdown in Giardia intestinalis. Eukaryot Cell 8: 916-919.
75. Edgar RC, (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
76. Clamp M, Cuff J, Searle SM, Barton GJ, (2004) The Jalview Java alignment editor. Bioinformatics 20: 426-427.