Evidence for mucin-like glycoproteins that tether sporozoites of Cryptosporidium parvum to the inner surface of the oocyst wall

Eukaryotic Cell

Volumn 9, Issue 1, 2010, Pages 84-96

  Chatterjee, Anirban ^a   Banerjee, Sulagna ^a   Steffen, Martin ^b   O'Connor, Roberta M ^c   Ward, Honorine D ^c   Robbins, Phillips W ^a   Samuelson, John ^a  

^a BOSTON UNIVERSITY   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c TUFTS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLYCOPROTEIN; MUCIN; OOCYST WALL PROTEIN, CRYPTOSPORIDIUM; PROTOZOAL PROTEIN;

ANIMAL; ARTICLE; CATTLE; CELL WALL; CHEMISTRY; CRYPTOSPORIDIUM PARVUM; CYTOLOGY; HUMAN; IMMUNOELECTRON MICROSCOPY; METABOLISM; MOUSE; OOCYST; SPOROZOITE;

ANIMALS; CATTLE; CELL WALL; CRYPTOSPORIDIUM PARVUM; GLYCOPROTEINS; HUMANS; MICE; MICROSCOPY, IMMUNOELECTRON; MUCINS; OOCYSTS; PROTOZOAN PROTEINS; SPOROZOITES;

CRYPTOSPORIDIUM; CRYPTOSPORIDIUM PARVUM; MACLURA POMIFERA;

EID: 75649109239     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00288-09     Document Type: Article

References (49)

1. Abrahamsen, M. S., T. J. Templeton, S. Enomoto, J. E. Abrahante, G. Zhu, C. A. Lancto, et al. 2004. Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science 304:441-445.
2. Adams, E. W., D. M. Ratner, H. R. Bokesch, J. B. McMahon, B. R. O'Keefe, and P. H. Seeberger. 2004. Oligosaccharide and glycoprotein microarrays as tools in HIV glycobiology: glycan-dependent gp120/protein interactions. Chem. Biol. 11:875-881.
3. Banerjee, S., J. Cui, P. W. Robbins, and J. Samuelson. 2008. 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. 159:44-53.
4. Barnes, D. A., A. Bonnin, J. X. Huang, L. Gousset, J. Wu, J. Gut, P. Doyle, J. F. Dubremetz, H. Ward, and C. Petersen. 1998. A novel multi-domain mucin-like glycoprotein of Cryptosporidium parvum mediates invasion. Mol. Biochem. Parasitol. 96:93-110.
5. Bhat, N., A. Joe, M. PereiraPerrin, and H. D. Ward. 2007. Cryptosporidium p30, a galactose/N-acetylgalactosamine-specific lectin, mediates infection in vitro. J. Biol. Chem. 282:34877-34887.
6. Cevallos, A. M., X. Zhang, M. K. Waldor, S. Jaison, X. Zhou, S. Tzipori, M. R. Neutra, and H. D. Ward. 2000. Molecular cloning and expression of a gene encoding Cryptosporidium parvum glycoproteins gp40 and gp15. Infect. Immun. 68:4108-4116.
7. Cevallos, A. M., N. Bhat, R. Verdon, D. H. Hamer, B. Stein, S. Tzipori, M. E. Pereira, G. T. Keusch, and H. D. Ward. 2000. Mediation of Cryptosporidium parvum infection in vitro by mucin-like glycoproteins defined by a neutralizing monoclonal antibody. Infect. Immun. 68:5167-5175.
8. Chen, X. M., S. P. O'Hara, B. Q. Huang, J. B. Nelson, J. J. Lin, G. Zhu, H. D. Ward, and N. F. LaRusso. 2004. Apical organelle discharge by Cryptosporidium parvum is temperature, cytoskeleton, and intracellular calcium dependent and required for host cell invasion. Infect. Immun. 72:6806-6816.
9. de Groot, P. W., A. D. de Boer, J. Cunningham, H. L. Dekker, L. de Jong, K. L. Hellingwerf, C. de Koster, and F. M. Klis. 2004. Proteomic analysis of Candida albicans cell walls reveals covalently bound carbohydrate-active enzymes and adhesins. Eukaryot. Cell 3:955-965.
10. Dubey, J. P., D. S. Lindsay, and C. A. Speer. 1998. Structures of Toxoplasma gondii tachyzoites, bradyzoites, and sporozoites and biology and development of tissue cysts. Clin. Microbiol. Rev. 11:267-299.
11. Entrala, E., Y. Sbihi, M. Sánchez-Moreno, and C. Mascaró. 2001. Antigen incorporation on Cryptosporidium parvum oocyst walls. Mem. Inst. Oswaldo Cruz 96:233-235.
12. Fayer, R. 2004. Cryptosporidium: a water-borne zoonotic parasite. Vet. Parasitol. 126:37-56.
13. Ghosh, S., M. Frisardi, R. Rogers, and J. Samuelson. 2001. How Giardia swim and divide. Infect. Immun. 69:7866-7872.
14. Harris, J. R., and F. Petry. 1999. Cryptosporidium parvum: structural components of the oocyst wall. J. Parasitol. 85:839-849.
15. Hirschberg, C. B., P. W. Robbins, and C. Abeijon. 1998. Transporters of nucleotide sugars, ATP, and nucleotide sulfate in the endoplasmic reticulum and Golgi apparatus. Annu. Rev. Biochem. 67:49-69.
16. Jamet, E., C. Albenne, G. Boudart, M. Irshad, H. Canut, and R. Pont-Lezica. 2008. Recent advances in plant cell wall proteomics. Proteomics 8:893-908.
17. Jenkins, M. C., C. Murphy, J. Trout, and R. Fayer. 2006. An improved electron microscopic technique for the immunolabeling of Cryptosporidium parvum oocysts. J. Parasitol. 92:403-405.
18. Jenkins, M. C., J. Trout, C. Murphy, J. A. Harp, J. Higgins, W. Wergin, and R. Fayer. 1999. Cloning and expression of a DNA sequence encoding a 41-kilodalton Cryptosporidium parvum oocyst wall protein. Clin. Diagn. Lab Immunol. 6:912-920.
19. Krogh, A., B. Larsson, G. von Heijne, and E. L. Sonnhammer. 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 305:567-580.
20. Lally, N. C., G. D. Baird, S. J. McQuay, F. Wright, and J. J. Oliver. 1992. A 2359-base pair DNA fragment from Cryptosporidium parvum encoding a repetitive oocyst protein. Mol. Biochem. Parasitol. 56:69-78.
21. Leav, B. A., M. R. Mackay, A. Anyanwu, R. M. O'Connor, A. M. Cevallos, G. Kindra, N. C. Rollins, M. L. Bennish, R. G. Nelson, and H. D. Ward. 2002. Analysis of sequence diversity at the highly polymorphic Cpgp40/15 locus among Cryptosporidium isolates from human immunodeficiency virus-in-fected children in South Africa. Infect. Immun. 70:3881-3890.
22. Marchler-Bauer, A., J. B. Anderson, M. K. Derbyshire, C. DeWeese-Scott, N. R. Gonzales, et al. 2007. CDD: a conserved domain database for inter-active domain family analysis. Nucleic Acids Res. 35:D237-D240.
23. Nanduri, J., S. Williams, T. Aji, and T. P. Flanigan. 1999. Characterization of an immunogenic glycocalyx on the surfaces of Cryptosporidium parvum oocysts and sporozoites. Infect. Immun. 67:2022-2024.
24. Nielsen, H., S. Brunak, and G. von Heijne. 1999. Machine learning approaches for the prediction of signal peptides and other protein sorting signals. Protein Eng. 12:3-9.
25. O'Connor, R. M., P. B. Burns, T. Ha-Ngoc, K. Scarpato, W. Khan, G. Kang, and H. Ward. 2009. Polymorphic mucin antigens CpMuc4 and CpMuc5 are integral to Cryptosporidium parvum infection in vitro. Eukaryot. Cell 8:461-469.
26. O'Connor, R. M., J. W. Wanyiri, A. M. Cevallos, J. W. Priest, and H. D. Ward. 2007. Cryptosporidium parvum glycoprotein gp40 localizes to the sporozoite surface by association with gp15. Mol. Biochem. Parasitol. 156: 80-83.
27. Petry, F. 2004. Structural analysis of Cryptosporidium parvum. Microsc. Microanal. 10:586-601.
28. Ranucci, L., H. M. Muller, G. La Rosa, I. Reckmann, M. A. Morales, F. Spano, E. Pozio, and A. Crisanti. 1993. Characterization and immunolocalization of a Cryptosporidium protein containing repeated amino acid motifs. Infect. Immun. 61:2347-2356.
29. Samuelson, J., S. Banerjee, P. Magnelli, J. Cui, D. J. Kelleher, R. Gilmore, and P. W. Robbins. 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. U.S.A.102:1548-1553.
30. Sanderson, S. J., D. Xia, H. Prieto, J. Yates, M. Heiges, J. C. Kissinger, E. Bromley, K. Lal, R. E. Sinden, F. Tomley, and J. M. Wastling. 2008. Determining the protein repertoire of Cryptosporidium parvum sporozoites. Proteomics 8:1398-1414.
31. Smith, H. V., R. A. Nichols, and A. M. Grimason. 2005. Cryptosporidium excystation and invasion: getting to the guts of the matter. Trends Parasitol. 21:133-142.
32. Snelling, W. J., Q. Lin, J. E. Moore, B. C. Millar, F. Tosini, E. Pozio, J. S. Dooley, and C. J. Lowery. 2007. Proteomic analysis and protein expression during sporozoite excystation of Cryptosporidium parvum (coccidia, Apicomplexa). Mol. Cell Proteomics 6:346-355.
33. Spano, F., C. Puri, L. Ranucci, L. Putignani, and A. Crisanti. 1997. Cloning of the entire COWP gene of Cryptosporidium parvum and ultrastructural localization of the protein during sexual parasite development. Parasitology 114:427-437.
34. Stein, B., L. Stover, A. Gillem, K. Winters, J. H. Leet, and C. Chauret. 2006. The effect of lectins on Cryptosporidium parvum oocyst in vitro attachment to host cells. J. Parasitol. 92:1-9.
35. Strong, W. B., J. Gut, and R. G. Nelson. 2000. Cloning and sequence analysis of a highly polymorphic Cryptosporidium parvum gene encoding a 60-kilo-dalton glycoprotein and characterization of its 15-and 45-kilodalton zoite surface antigen products. Infect. Immun. 68:4117-4134.
36. Sun, C. H., J. M. McCaffery, D. S. Reiner, and F. D. Gillin. 2003. Mining the Giardia lamblia genome for new cyst wall proteins. J. Biol. Chem. 278:21701-21708.
37. Templeton, T. J., C. A. Lancto, V. Vigdorovich, C. Liu, N. R. London, K. Z. Hadsall, and M. S. Abrahamsen. 2004. The Cryptosporidium oocyst wall protein is a member of a multigene family and has a homolog in Toxoplasma. Infect. Immun. 72:980-987.
38. Tosini, F., A. Agnoli, R. Mele, M. A. Gomez Morales, and E. Pozio. 2004. A new modular protein of Cryptosporidium parvum, with ricin B and LCCL domains, expressed in the sporozoite invasive stage. Mol. Biochem. Parasitol. 134:137-147.
39. Tzipori, S., and H. Ward. 2002. Cryptosporidiosis: biology, pathogenesis and disease. Microbes Infect. 4:1047-1058.
40. Van Dellen, K. L., A. Chatterjee, D. M. Ratner, P. E. Magnelli, J. Cipollo, M. Steffin, P. W. Robbins, and J. Samuelson. 2006. Unique posttranslational modifications of chitin-binding lectins of Entamoeba invadens cyst walls. Eukaryot. Cell 5:836-848.
41. Wang, Y., S.-I. Wu, and W. S. Hancock. 2006. Approaches to the study of N-linked glycoproteins in human plasma using lectin affinity chromatography and nano-HPLC coupled to electrospray linear ion trap-Fourier transform mass spectrometry. Glycobiology 16:514-523.
42. Wanyiri, J. W., R. O'Connor, G. Allison, K. Kim, A. Kane, J. Qiu, A. G. Plaut, and H. D. Ward. 2007. Proteolytic processing of the Cryptosporidium glycoprotein gp40/15 by human furin and by a parasite-derived furin-like protease activity. Infect. Immun. 75:184-192.
43. Ward, H., and A. M. Cevallos. 1998. Cryptosporidium: molecular basis of host-parasite interaction. Adv. Parasitol. 40:151-185.
44. Weir, C., G. Vesey, M. Slade, B. Ferrari, D. A. Veal, and K. Williams. 2000. An immunoglobulin G1 monoclonal antibody highly specific to the wall of Cryptosporidium oocysts. Clin. Diagn. Lab. Immunol. 7:745-750.
45. Winter, G., A. A. Gooley, K. L. Williams, and M. B. Slade. 2000. Characterization of a major sporozoite surface glycoprotein of Cryptosporidum parvum. Funct. Integr. Genomics 1:207-217.
46. Xiao, L., J. Limor, U. M. Morgan, I. M. Sulaiman, R. C. Thompson, and A. A. Lal. 2000. Sequence differences in the diagnostic target region of the oocyst wall protein gene of Cryptosporidium parasites. Appl. Environ. Microbiol. 66:5499-5502.
47. Xu, P., G. Widmer, Y. Wang, L. S. Ozaki, J. M. Alves, M. G. Serrano, D. Puiu, P. Manque, D. Akiyoshi, et al. 2004. The genome of Cryptosporidium hominis. Nature 431:1107-1112.
48. Yates, J. R., III, E. Carmack, L. Hays, A. J. Link, and J. K. Eng. 1999. Automated protein identification using microcolumn liquid chromatography-tandem mass spectrometry. Methods Mol. Biol. 112:553-569.
49. Zhu, G., M. J. Marchewka, and J. S. Keithly. 2000. Cryptosporidium parvum appears to lack a plastid genome. Microbiology 146:315-321.