The antiretroviral lectin cyanovirin-N targets well-known and novel targets on the surface of Entamoeba histolytica trophozoites

Eukaryotic Cell

Volumn 9, Issue 11, 2010, Pages 1661-1668

  Carpentieri, Andrea ^a   Ratner, Daniel M ^a,e   Ghosh, Sudip K ^a,f   Banerjee, Sulagna ^a,g   Bushkin, G Guy ^a   Cui, Jike ^a,h   Lubrano, Michael ^a,i   Steffen, Martin ^b   Costello, Catherine E ^c   O'Keefe, Barry ^d   Robbins, Phillips W ^a   Samuelson, John ^a  

^a BOSTON UNIVERSITY   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c BOSTON UNIVERSITY MEDICAL CENTER   (United States)

^d NATIONAL CANCER INSTITUTE   (United States)

^e University of Washington   (United States)

^f INDIAN INSTITUTE OF TECHNOLOGY   (India)

^g UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^h Harvard Medical School Center for Biomedical Informatics   (United States)

ⁱ ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIAMEBIC AGENT; ANTIRETROVIRUS AGENT; BACTERIAL PROTEIN; CARRIER PROTEIN; CYANOVIRIN N; GLYCOPROTEIN; MANNOSE BINDING LECTIN; PROTOZOAL PROTEIN;

AMEBIASIS; AMINO ACID SEQUENCE; ANIMAL; ARTICLE; DRUG EFFECT; ENTAMOEBA HISTOLYTICA; GENETICS; HOST PARASITE INTERACTION; HUMAN; IN VITRO STUDY; LIVER AMEBIASIS; METABOLISM; MOLECULAR GENETICS; PARASITOLOGY; PATHOGENICITY; PHAGOCYTOSIS; TROPHOZOITE; VIRULENCE;

AMEBICIDES; AMINO ACID SEQUENCE; ANIMALS; ANTI-RETROVIRAL AGENTS; BACTERIAL PROTEINS; CARRIER PROTEINS; DYSENTERY, AMEBIC; ENTAMOEBA HISTOLYTICA; GLYCOPROTEINS; HOST-PARASITE INTERACTIONS; HUMANS; LIVER ABSCESS, AMEBIC; MANNOSE-BINDING LECTINS; MOLECULAR SEQUENCE DATA; PHAGOCYTOSIS; PROTOZOAN PROTEINS; TROPHOZOITES; VIRULENCE;

ENTAMOEBA HISTOLYTICA; PROTISTA;

EID: 78149243022     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00166-10     Document Type: Article

References (56)

1. 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.
2. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
3. Arhets, P., P. Gounon, P. Sansonetti, and N. Guillen. 1995. Myosin II is involved in capping and uroid formation in the human pathogen Entamoeba histolytica. Infect. Immun. 63:4358-4367.
4. Aurrecoechea, C., J. Brestelli, B. P. Brunk, S. Fischer, B. Gajria, X. Gao, et al. 2010. EuPathDB: a portal to eukaryotic pathogen databases. Nucleic Acids Res. 38:D415-419.
5. Banerjee, S., P. Vishwanath, J. Cui, D. J. Kelleher, R. Gilmore, P. W. Robbins, and J. Samuelson. 2007. Evolution of quality control of protein- folding in the ER lumen. Proc. Natl. Acad. Sci. U. S. A. 104:11676-11681.
6. Bhattacharya, A., R. Arya, C. G. Clark, and J. P. Ackers. 2000. Absence of lipophosphoglycan-like glycoconjugates in Entamoeba dispar. Parasitology 120:31-35.
7. Bruchhaus, I., B. J. Loftus, N. Hall, and E. Tannich. 2003. The intestinal protozoan parasite Entamoeba histolytica contains 20 cysteine protease genes, of which only a small subset is expressed during in vitro cultivation. Eukaryot. Cell 2:501-509.
8. Buss, S. N., S. Hamano, A. Vidrich, C. Evans, Y. Zhang, O. R. Crasta, B. W. Sobral, C. A. Gilchrist, and W. A. Petri, Jr. 2010. Members of the Entamoeba histolytica transmembrane kinase family play non-redundant roles in growth and phagocytosis. Int. J. Parasitol. 40:833-843.
9. Chaudhry, O. A, and W. A. Petri, Jr. 2005. Vaccine prospects for amebiasis. Expert Rev. Vaccines 4:657-668.
10. Clark, C. G., U. C. Alsmark, M. Tazreiter, Y. Saito-Nakano, V. Ali, S. Marion, C. Weber, C. Mukherjee, et al. 2007. Structure and content of the Entamoeba histolytica genome. Adv. Parasitol. 65:51-190.
11. Cui, J., T. Smith, P. W. Robbins, and J. Samuelson. 2009. Darwinian selec- tion for sites of Asn-linked glycosylation in phylogenetically disparate eu- karyotes and viruses. Proc. Natl. Acad. Sci. U. S. A. 106:13421-13426.
12. Davis, P. H., M. Chen, X. Zhang, C. G. Clark, R. R. Townsend, and S. L. Stanley, Jr. 2009. Proteomic comparison of Entamoeba histolytica and En- tamoeba dispar and the role of E. histolytica alcohol dehydrogenase 3 in virulence. PLoS Negl. Trop. Dis. 3:e415.
13. Duncan, D. T., R. Craig, and A. J. Link. 2005. Parallel tandem: a program for parallel processing of tandem mass spectra using PVM or MPI and X!Tan- dem. J. Proteome Res. 4:1842-1847.
14. Dunlop, D. C. C. Bonomelli, F. Mansab, S. Vasiljevic, K. J. Doores, M. R. Wormald, A. S. Palma, T. Feizi, D. J. Harvey, R. A. Dwek, M. Crispin, and C. N. Scanlan. 2010. Polysaccharide mimicry of the epitope of the broadly neutralizing anti-HIV antibody, 2G12, induces enhanced antibody responses to self oligomannose glycans. Glycobiology 20:812-823.
15. Eisenhaber, F., B. Eisenhaber, W. Kubina, S. Maurer-Stroh, G. Neuberger, G. Schneider, and M. Wildpaner. 2003. Prediction of lipid posttranslational modifications and localization signals from protein sequences: big-Pi, NMT and PTS1. Nucleic Acids Res. 31:3631-3634.
16. Espinosa-Cantellano, M., and A. Martinez-Palomo. 1994. Entamoeba histo- lytica: mechanism of surface receptor capping. Exp. Parasitol. 79:424-435.
17. Ghosh, D., O. Krokhin, M. Antonovici, W. Ens, K. G. Standing, R. C. Beavis, and J. A. Wilkins. 2004. Lectin affinity as an approach to the proteomic analysis of membrane glycoproteins. J. Proteome Res. 3:841-850.
18. racA, phosphoino- sitide 3-kinase, and vacuolar ATPase in phagocytosis of bacteria and eryth- rocytes by Entamoeba histolytica: suggestive evidence for coincidental evo- lution of amebic invasiveness. Infect. Immun. 65:4243-4249.
19. Guillen, N. 1996. Role of signaling and cytoskeletal rearrangements in the pathogenesis of Entamoeba histolytica. Trends Microbiol. 4:191-197.
20. Haque, R., C. D. Huston, M. Hughes, E. Houpt, and W. A. Petri Jr. 2003. Amebiasis. N. Engl. J. Med. 348:1565-1573.
21. Helenius, A., and M. Aebi. 2004. Roles of N-linked glycans in the endoplas- mic reticulum. Annu. Rev. Biochem. 73:1019-1049.
22. Higdon, R., N. Kolker, A. Picone, G. van Belle, and E. Kolker. 2004. LIP index for peptide classification using MS/MS and SEQUEST search via logistic regression. OMICS 8:357-369.
23. Koenig, T., B. H. Menze, M. Kirchner, et al. 2008. Robust prediction of the MASCOT score for an improved quality assessment in mass spectrometric proteomics. J. Proteome Res. 7:3708-3717.
24. Krogh, A., B. Larsson, G. von Heijne, and E. L. Sonnhammer. 2001. Pre- dicting transmembrane protein topology with a hidden Markov model: ap- plication to complete genomes. J. Mol. Biol. 305:567-580.
25. Kwong, P. D., M. L. Doyle, D. J. Casper, C. Cicala, S. A. Leavitt, S. Majeed, T. D. Steenbeke, M. Venturi, et al. 2002. HIV-1 evades antibody-mediated neutralization through conformational masking of receptor-binding sites. Nature 420:678-682.
26. Leitsch, D., I. B. Wilson, K. Paschinger, and M. Duchêne. 2006. Comparison of the proteome profiles of Entamoeba histolytica and its close but non- pathogenic relative Entamoeba dispar. Wien. Klin. Wochenschr. 118:37-41.
27. Linford, A. S., H. Moreno, K. R. Good, H. Zhang, U. Singh, and W. A. Petri, Jr. 2009. Short hairpin RNA-mediated knockdown of protein expression in Entamoeba histolytica. BMC Microbiol. 9:38.
28. Liu, X., L. A. Lagenaur, D. A. Simpson, K. P. Essenmacher, C. L. Frazier-Parker, Y. Liu, D. Tsai, S. S. Rao, D. H. Hamer, T. P. Parks, P. P. Lee, and Q. Xu. 2006. Engineered vaginal lactobacillus strain for mucosal delivery of the human immunodeficiency virus inhibitor cyanovirin-N. Antimicrob. Agents Chemother. 50:3250-3259.
29. Loftus, B., I. Anderson, R. Davies, U. C. Alsmark, J. Samuelson, P. Amedeo, P. Roncaglia, M. Berriman, et al. 2005. The genome of the protist parasite Entamoeba histolytica. Nature 433:865-868.
30. Luallen, R. J., C. Agrawal-Gamse, H. Fu, D. F. Smith, R. W. Doms, and Y. Geng. 2010. Antibodies against Man 1,2-Man 1,2-Man oligosaccharide structures recognize envelope glycoproteins from HIV-1 and SIV strains. Glycobiology 20:280-286.
31. Magnelli, P., J. F. Cipollo, D. M. Ratner, J. Cui, D. Kelleher, R. Gilmore, C. E. Costello, P. W. Robbins, and J. Samuelson. 2008. Unique Asn-linked oligosaccharides of the human pathogen Entamoeba histolytica. J. Biol. Chem. 283:18355-18364.
32. Mann, B. J., B. E. Torian, T. S. Vedvick, and W. A. Petri Jr. 1991. Sequence of a cysteine-rich galactose-specific lectin of Entamoeba histolytica. Proc. Natl. Acad. Sci. U. S. A. 88:3248-3252.
33. Marinets, A., T. Zhang, N. Guillen, P. Gounon, B. Bohle, U. Vollmann, O. Scheiner, G. Wiedermann, S. L. Stanley, and M. Duchêne. 1997. Protection against invasive amebiasis by a single monoclonal antibody directed against a lipophosphoglycan antigen localized on the surface of Entamoeba histo- lytica. J. Exp. Med. 186:1557-1565.
34. Mirelman, D., M. Anbar, and R. Bracha. 2008. Epigenetic transcriptional gene silencing in Entamoeba histolytica. IUBMB Life 60:598-604.
35. Moody-Haupt, S., J. H. Patterson, D. Mirelman, and M. J. McConville. 2000. The major surface antigens of Entamoeba histolytica trophozoites are GPI- anchored proteophosphoglycans. J. Mol. Biol. 297:409-420.
36. Nielsen, H., S. Brunak, and G. von Heijne. 1999. Machine learning ap- proaches for the prediction of signal peptides and other protein sorting signals. Protein Eng. 12:3-9.
37. Okada, M., C. D. Huston, M. Oue, B. J. Mann, W. A. Petri Jr., K. Kita, and T. Nozaki. 2006. Kinetics and strain variation of phagosome proteins of Entamoeba histolytica by proteomic analysis. Mol. Biochem. Parasitol. 145: 171-183.
38. O'Keefe, B. R., F. Vojdani, V. Buffa, R. J. Shattock, D. C. Montefiori, J. Bakke, J. Mirsalis, A. L. d'Andrea, S. D. Hume, B. Bratcher, C. J. Saucedo, J. B. McMahon, G. P. Pogue, and K. E. Palmer. 2009. Scaleable manufacture of HIV-1 entry inhibitor griffithsin and validation of its safety and efficacy as a topical microbicide component. Proc. Natl. Acad. Sci. U. S. A. 106:6099-6104.
39. Petri, W. A., Jr., R. Haque, and B. J. Mann. 2002. The bittersweet interface of parasite and host: lectin-carbohydrate interactions during human invasion by the parasite Entamoeba histolytica. Annu. Rev. Microbiol. 56:39-64.
40. Prasad, R., M. Tola, M. P. Sharma, and A. Bhattacharya. 1992. Recognition of Entamoeba histolytica lipophosphoglycan by a strain-specific monoclonal antibody and human immune sera. Mol. Biochem. Parasitol. 56:279-287.
41. Pusch, O., D. Boden, S. Hannify, F. Lee, L. D. Tucker, M. R. Boyd, J. M. Wells, and B. Ramratnam. 2005. Bioengineering lactic acid bacteria to se- crete the HIV-1 virucide cyanovirin. J. Acquir. Immune Defic. Syndr. 40: 512-520.
42. Ratner, D. M., J. Cui, M. Steffen, L. L. Moore, P. W. Robbins, and J. Samuelson. 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.
43. Ravdin, J. I., J. E. John, L. I. Johnston, D. J. Innes, and R. L. Guerrant. 1985. Adherence of Entamoeba histolytica trophozoites to rat and human colonic mucosa. Infect. Immun. 48:293-297.
44. 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.
45. Scanlan, C. N., R. Pantophlet, M. R. Wormald, E. Ollmann Saphire, R. Stanfield, I. A. Wilson, H. Katinger, R. A. Dwek, P. M. Rudd, and D. R. Burton. 2002. The broadly neutralizing anti-human immunodeficiency virus type 1 antibody 2G12 recognizes a cluster of 132 mannose residues on the outer face of gp120. J. Virol. 76:7306-7321.
46. Stanley, S. L, Jr. 2006. Vaccines for amoebiasis: barriers and opportunities. Parasitology 133:S81-S86.
47. Stanley, S. L., Jr., A. Becker, C. Kunz-Jenkins, L. Foster, and E. Li. 1990. Cloning and expression of a membrane antigen of Entamoeba histolytica possessing multiple tandem repeats. Proc. Natl. Acad. Sci. U. S. A. 87:4976-4980.
48. Stanley, S. L., Jr., H. Huizenga, and E. Li. 1992. Isolation and partial characterization of a surface glycoconjugate of Entamoeba histolytica. Mol. Biochem. Parasitol. 50:127-138.
49. Swanson, M. D., H. C. Winter, I. J. Goldstein, and D. M. Markovitz. 2010. A lectin isolated from bananas is a potent inhibitor of HIV replication. J. Biol. Chem. 285:8646-8655.
50. Tavares, P., P. Sansonetti, and N. Guillén. 2000. Cell polarization and adhesion in a motile pathogenic protozoan: role and fate of the Entamoeba histolytica Gal/GalNAc lectin. Microbes Infect. 2:643-649.
51. Teixeira, J. E., and C. D. Huston. 2008. Participation of the serine-rich Entamoeba histolytica protein in amebic phagocytosis of apoptotic host cells. Infect. Immun. 76:959-966.
52. Tolstrup, J., E. Krause, E. Tannich, and I. Bruchhaus. 2007. Proteomic analysis of Entamoeba histolytica. Parasitology 134:289-298.
53. Trombetta, E. S., and A. J. Parodi. 2003. Quality control and protein folding in the secretory pathway. Annu. Rev. Cell Dev. Biol. 19:649-676.
54. Van Dellen, K. L., A. Chatterjee, D. Ratner, P. E. Magnelli, J. Cipollo, M. Steffen, P. W. Robbins, and J. Samuelson. 2006. Unique posttranslational modifications of chitin-binding lectins of Entamoeba invadens cyst walls. Eukaryot. Cell 5:836-848.
55. 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.
56. Yates, J. R., III, E. Carmack, L. Hays, A. J. Link, and J. K. Eng. 1999. Automated protein identification using microcolumn liquid chromatogra- phy-tandem mass spectrometry. Methods Mol. Biol. 112:553-569.