Chitinase secretion by encysting Entamoeba invadens and transfected Entamoeba histolytica trophozoites: Localization of secretory vesicles, endoplasmic reticulum, and Golgi apparatus

Infection and Immunity

Volumn 67, Issue 6, 1999, Pages 3073-3081

  Ghosh, Sudip K ^a   Field, Jessica ^a   Frisardi, Marta ^a   Rosenthal, Benjamin ^a   Mai, Zhiming ^a   Rogers, Rick ^a   Samuelson, John ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHITINASE;

ARTICLE; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; ENDOPLASMIC RETICULUM; ENTAMOEBA HISTOLYTICA; ENTAMOEBA INVADENS; ENZYME RELEASE; GENE EXPRESSION; GENETIC CONSERVATION; GOLGI COMPLEX; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TARGETING; TROPHOZOITE;

EID: 0033023401     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/iai.67.6.3073-3081.1999     Document Type: Article

References (74)

1. Agrawal, A., V. C. Pandey, S. Kumar, and P. Sagar. 1989. Secretion of acid phosphatase by axenic Entamoeba histolytica NIH-200 and properties of the extracellular enzyme. J. Protozool. 36:90-92.
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. Amor, J. C., D. H. Harrison, R. A. Kahn, and D. Ringe. 1994. Structure of the human ADP-ribosylation factor 1 complexed with GDP. Nature 372:704-708.
4. Aoe, T., E. Cukierman, A. Lee, D. Cassel, P. J. Peters, and V. W. Hsu. 1997. The KDEL receptor, ERD2, regulates intracellular traffic by recruiting a GTPase-activating protein for ARF1. EMBO J. 16:7305-7316.
5. Arroyo-Begovich, A., and A. Carbez-Trejo. 1982. Location of chitin in the cyst wall of Entamoeba invadens with the colloidal gold tracers. J. Parasitol. 68:253-258.
6. Avron, B., R. M. Deutsch, and D. Mirelman. 1982. Chitin synthesis inhibitors prevent cyst formation by trophozoites. Biochem. Biophys. Res. Commun. 108:815-821.
7. Bakker-Grunwald, T., and C. Wostmann. 1993. Entamoeba histolytica as a model for the primitive eukaryotic cell. Parasitol. Today 9:27-31.
8. Bruchhaus, I., T. Jacobs, M. Leippe, and E. Tannich. 1996. Entamoeba histolytica and Entamoeba dispar. Differences in numbers and expression of cysteine proteinase genes. Mol. Microbiol. 22:255-263.
9. Bui, E. T. N., P. J. Bradley, and P. J. Johnson. 1996. A common evolutionary origin for mitochondria and hydrogenosomes. Proc. Natl. Acad. Sci. USA 93:9651-9656.
10. Bukau, B., and A. L. Horwich. 1998. The Hsp70 and Hsp60 chaperone machines. Cell 92:351-366.
11. Clark, C. G., and A. J. Roger. 1995. Direct evidence for secondary loss of mitochondria in Entamoeba histolytica. Proc. Natl. Acad. Sci. USA 92:6518-6521.
12. Cosson, P., and F. Letourneur. 1997. Coatomer (COPI)-coated vesicles: role in intracellular transport and protein sorting. Curr. Opin. Cell Biol. 9:484-487.
13. Das, S., and F. D. Gillin. 1991. Chitin synthase in encysting Entamoeba invadens. Biochem. J. 280:641-647.
14. de la Vega, H., C. A. Specht, C. E. Semino, P. W. Robbins, D. Eichinger, D. Caplivskl, S. Ghosh, and J. Samuelson. 1997. Cloning and expression of chitinases of Entamoebae. Mol. Biochem. Parasitol. 85:139-147.
15. Eichinger, D. 1997. Encystation of entamoeba parasites. Bioessays 19:633-639.
16. Evan, G. I., G. K. Lewis, G. Ramsay, and J. M. Bishop. 1985. Isolation of monoclonal antibodies specific for human c-myc proto-oncogene product. Mol. Cell. Biol. 5:3610-3616.
17. 16a. Field, J., and J. Samuelson. Unpublished observations.
18. Ghosh, S. K., A. Lohia, A. Kumar, and J. Samuelson. 1996. Overexpression of P-glycoprotein gene 1 by transfected Entamoeba histolytica confers emetine-resistance. Mol. Biochem. Parasitol. 82:257-260.
19. racA in cultured Entamoeba histolytica. Infect. Immun. 65:4243-4249.
20. Gillin, F. D., D. S. Reiner, and J. M. McCaffery. 1996. Cell biology of the primitive eukaryote Giardia lamblia. Annu. Rev. Microbiol. 50:679-705.
21. Gray, M. W. 1989. The evolutionary origins of organelles. Trends Genet. 5:294-299.
22. Greasley, S. E., H. Jhoti, C. Teahan, R. Solari, A. Fensome, G. M. Thomas, S. Cockcroft, and B. Bax. 1995. The structure of rat ADP-ribosylation factor-1 (ARF-1) completed to GDP determined from two different crystal forms. Nat. Struct. Biol. 2:797-806.
23. Gupta, R. S., K. Aitken, M. Fala, and B. Singh. 1994. Cloning of Giardia lamblia heat shock protein HSP70 homologs: implications regarding the origin of eukaryotic cells and of endoplasmic reticulum. Proc. Natl. Acad. Sci. USA 91:2895-2899.
24. Hall, A. 1994. Small GTP-binding proteins and the regulation of the actin cytoskeleton. Annu. Rev. Cell Biol. 10:31-54.
25. Harlow, E., and D. Lane. 1988. Antibodies: a laboratory manual. Cold Spring Harbor Press, Cold Spring Harbor, N.Y.
26. Horn, M., and G. Banting. 1994. Okadoic acid treatment leads to fragmentation of the trans-Golgi network and an increase in expression of TGN38 at the cell surface. Biochem. J. 301:69-73.
27. Jacobs, T., I. Bruchhaus, T. Dandekar, E. Tannich, and M. Leippe. 1998. Isolation and molecular characterization of a surface-bound proteinase of Entamoeba histolytica. Mol. Microbiol. 27:269-276.
28. Kimura, A., Y. Hara, T. Kimoto, Y. Okuno, and T. Nakabayashi. 1997. Cloning and expression of E. histolytica gene which includes a PDI active site. Arch. Med. Res. 288:76-77.
29. Kjeldgaard, M., J. Nyborg, and B. F. Clark. 1996. The GTP binding motif: variations on a theme. FASEB J. 10:1347-1368.
30. Klausner, R. D., J. G. Donaldson, and J. Lippincott-Schwartz. 1992. Brefeldin A: insights into control of membrane traffic and organelle structure. J. Cell Biol. 116:1071-1080.
31. Kornfeld, R., and S. Kornfeld. 1985. Assembly of asparagine-linked oligosaccharides. Annu. Rev. Biochem. 54:631-664.
32. +-dependent alcohol dehydrogenase gene of Entamoeba histolytica. Proc. Natl. Acad. Sci. USA 89:10188-10192.
33. Lee, C. C., X. Wu, R. A. Gibbs, R. G. Cook, D. M. Muzny, and C. T. Caskey. 1988. Generation of cDNA probes directed by amino acid sequence: cloning of urate oxidase. Science 239:1288-1291.
34. + of Hexamita inflata and the quest for the first branch in the eukaryotic tree. Mol. Biochem. Parasitol. 59:41-48.
35. Leippe, M. 1997. Amoebapores. Parasitol. Today 13:178-183.
36. Leippe, M., H. J. Sievertsen, E. Tannich, and R. D. Horstmann. 1995. Spontaneous release of cysteine proteinases but not of pore-forming peptides by viable Entamoeba histolytica. Parasitology 111:569-574.
37. rac homologues. Gene 173:205-208.
38. Lujan, H. D., A. Marotta, M. R. Mowatt, N. Sciaky, J. Lippincott-Schwartz, and T. E. Nash. 1995. Developmental induction of Golgi structure and function in the primitive eukaryote Giardia lamblia. J. Biol. Chem. 270:4612-4618.
39. Lujan, H. D., M. R. Mowatt, J. T. Conrad, and T. E. Nash. 1996. Increased expression of the molecular chaperone BiP/GRP78 during differentiation of a primitive eukaryote. Biol. Cell 86:11-18.
40. Lujan, H. D., M. R. Mowatt, and T. E. Nash. 1997. Mechanisms of Giardia lamblia differentiation into cysts. Microbiol. Mol. Biol. Rev. 61:294-304.
41. Mai, Z., and J. Samuelson. 1998. A new gene family (ariel) encodes asparagine-rich Entamoeba histolytica antigens, which resemble the vaccine candidate serine-rich E. histolytica protein. Infect. Immun. 66:353-355.
42. Mai, Z., S. Ghosh, M. Frisardi, B. Rosenthal, R. Rogers, and J. Samuelson. 1999. Hsp60 is targeted to a cryptic mitochondrion-derived organelle ("crypton") in the microaerophilic protozoan parasite Entamoeba histolytica. Mol. Cell. Biol. 19:2198-2205.
43. 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. Nat. Acad. Sci. USA 88:3248-3252.
44. Martinez-Palomo, A. 1982. Cell biology, p. 5-59. In K. N. Brown (ed.), The biology of Entamoeba histolytica. John Wiley/Research Studies Press, New York, N.Y.
45. Mazzuco, A., M. Benchimol, and W. De Souza. 1997. Endoplasmic reticulum and Golgi-like elements in entamoeba. Micron 28:241-247.
46. McCoy, J. J., B. J. Mann, T. S. Vedvick, and W. A Petri, Jr. 1993. Sequence analysis of genes encoding the light subunit of the Entamoeba histolytica galactose-specific adhesin. Mol. Biochem. Parasitol. 61:325-328.
47. Mirelman, D. 1987. Ameba-bacterium relationship in amebiasis. Microb. Rev. 51:272-284.
48. Mowatt, M. R., H. D. Lujan, D. B. Cotten, B. Bowers, J. Yee, T. E. Nash, and H. H. Stibbs. 1995. Developmentally regulated expression of a Giardia lam-blia cyst wall protein gene. Mol. Microbiol. 15:955-963.
49. Muller, M. 1988. Energy metabolism of protozoa without mitochondria. Annu. Rev. Microbiol. 42:465-488.
50. Nambiar, M. P., T. Oda, C. Chen, Y. Kuwazuru, and H. C. Wu. 1993. Involvement of the Golgi region in the intracellular trafficking of cholera toxin. J. Cell. Physiol. 154:222-228.
51. Nielsen, H., J. Engelbrecht, S. Brunak, and G. von Heijne. 1997. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng. 10:1-6.
52. Petri, W. A., Jr., M. D. Chapman, T. Snodgrass, B. J. Mann, J. Broman, and J. I. Ravdin. 1989. Subunit structure of the galactose and N-acetyl-galactosamine-inhibitable lectin of Entamoeba histolytica. J. Biol. Chem. 264: 3007-3012.
53. Petri, W. A., Jr., and J. I. Ravdin. 1991. Protection of gerbils from amebic liver abscess by immunization with the galactose-specific adherence lectin of Entamoeba histolytica. Infect. Immun. 59:97-101.
54. Plaimauer, B., S. Ortner, G. Wiedermann, O. Scheiner, and M. Duchene. 1993. Molecular characterization of the cDNA coding for translation elongation factor-2 of pathogenic Entamoeba histolytica. DNA Cell Biol. 12:89-96.
55. Prasher, D. C. 1995. Using GFP to see the light. Trends Genet. 11:320-323.
56. Ramos, M. A., G. C. Mercado, L. M. Salgado, R. Sanchez-Lopez, R. P. Stock, P. M. Lizardi, and A. Alagon. 1997. Entamoeba histolytica contains a gene encoding a homologue to the 54-kD subunit of the signal recognition particle. Mol. Biochem. Parasitol. 88:225-235.
57. Ravdin, J. I. 1995. Amebiasis. State-of-the-art clinical article. Clin. Infect. Dis. 20:1453-1464.
58. Reeves, R. E. 1984. Metabolism of Entamoeba histolytica Schaudinn, 1903. Adv. Parasitol. 23:105-142.
59. Rodriguez, M. A., and E. Orozco. 1986. Isolation and characterization of phagocytosis- and virulence-deficient mutants of Entamoeba histolytica. J. Infect. Dis. 154:27-32.
60. Roger, A. J., S. G. Svard, J. Tovar, C. G. Clark, M. W. Smith, F. D. Gillen, and M. L. Sogin. 1998. A mitochondrial-like chaperonin 60 gene in Giardia lamblia: evidence that diplomonads once harbored an endosymbiont related to the progenitor of mitochondria. Proc. Natl. Acad. Sci. USA 95:229-234.
61. Rosenthal, B., Z. Mai, D. Caplivski, S. Ghosh, H. de la Vega, T. Graf, and J. Samuelson. 1997. Evidence for the bacterial origin of genes encoding fermentation enzymes of the amitochondriate protozoan parasite Entamoeba histolytica. J. Bacteriol. 179:3736-3745.
62. Rothman, J. E., and F. T. Wieland. 1996. Protein sorting by transport vesicles. Science 272:227-234.
63. Sanchez-Lopez, R., S. Gama-Castro, M. A. Ramos, E. Merino, P. M. Lizardi, and A. Alagon. 1998. Cloning and expression of the Entamoeba histolytica ERD2 gene. Mol. Biochem. Parasitol. 92:355-359.
64. Schlesinger, P. 1988. Lysosomes and Entamoeba histolytica, p. 297-313. In J. I. Ravdin (ed.), Amebiasis: human infection by Entamoeba histolytica. Churchill Livingstone, New York, N.Y.
65. Scholze, H., and E. Tannich. 1994. Cysteine endopeptidases of Entamoeba histolytica. Methods Enzymol. 244:512-523.
66. Smith, D. B., and K. S. Johnson. 1988. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene 67:31-40.
67. Smith, R. F., and T. F. Smith. 1992. Pattern-induced multi-sequence alignment (PIMA) algorithm employing secondary structure-dependent gap penalties for use in comparative protein modeling. Protein Eng. 5:35-41.
68. Stanley, S. L., Jr., K. Tian, J. P. Koester, and E. Li. 1995. The serine-rich Entamoeba histolytica protein is a phosphorylated membrane protein containing O-linked terminal N-acetylglucosamine residues. J. Biol. Chem. 270: 4121-4126.
69. Talamas-Rohana, P., and I. Meza. 1988. Interaction between pathogenic amebae and fibronectin: substrate degradation and changes in cytoskeleton organization. J. Cell Biol. 120:577-585.
70. Traub, L. M., and S. Kornfeld. 1997. The trans-Golgi network: a late secretory sorting station. Curr. Opin. Cell Biol. 9:527-533.
71. Valdivia, R. H., A. E. Hromockyj, D. Monack, L. Ramakrishnan, and S. Falkow. 1996. Applications for green fluorescent protein (GFP) in the study of host-pathogen interactions. Gene 173:47-52.
72. Van de Peer, Y., and R. De Wachter. 1994. TREECON for Windows: a software package for the construction and drawing of evolutionary trees for the Microsoft Windows environment. CABIOS 10:569-570.
73. Villagomez-Castro, J. C., C. Calvo-Mendez, and E. Lopez-Romero. 1992. Chitinase activity in encysting Entamoeba invadens and its inhibition by allosamidin. Mol. Biochem. Parasitol. 52:53-62.
74. Zhang, T., P. R. Cieslak, and S. L. Stanley, Jr. 1994. Protection of gerbils from amebic liver abscess by immunization with recombinant Entamoeba histolytica antigen. Infect. Immun. 62:1166-1170.