Involvement of p21(racA), phosphoinositide 3-kinase, and vacuolar ATPase in phagocytosis of bacteria and erythrocytes by Entamoeba histolytica: Suggestive evidence for coincidental evolution of amebic invasiveness

Infection and Immunity

Volumn 65, Issue 10, 1997, Pages 4243-4249

  Ghosh, Sudip K ^a   Samuelson, John ^a  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; DEXTRAN; GUANOSINE TRIPHOSPHATASE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN P21; UNCLASSIFIED DRUG; AMMONIUM CHLORIDE; ANDROSTANE DERIVATIVE; ANTIINFECTIVE AGENT; CYSTEINE PROTEINASE INHIBITOR; DRUG DERIVATIVE; GUANINE NUCLEOTIDE BINDING PROTEIN; LEUCINE; MACROLIDE; MONENSIN; N [N (3 CARBOXYOXIRANE 2 CARBONYL)LEUCYL]AGMATINE; RAC PROTEIN; WORTMANNIN;

ARTICLE; BACTERIUM TRANSFORMATION; CELL INVASION; CYTOKINESIS; ENTAMOEBA HISTOLYTICA; ENZYME ANALYSIS; GENE DISRUPTION; HUMAN; HUMAN CELL; HUMAN TISSUE; MICROPHOTOGRAPHY; MOLECULAR EVOLUTION; PHAGOCYTOSIS; PINOCYTOSIS; PRIORITY JOURNAL; ANIMAL; BACTERIUM; BIOLOGICAL MODEL; CAPPING PHENOMENON; CELL VACUOLE; CYTOLOGY; ERYTHROCYTE; EVOLUTION; GENETIC TRANSFORMATION; GENETICS; MACROPHAGE; METABOLISM; MUTATION; PATHOGENICITY; PH; PHYSIOLOGY;

1-PHOSPHATIDYLINOSITOL 3-KINASE; AMMONIUM CHLORIDE; ANDROSTADIENES; ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIA; CYSTEINE PROTEINASE INHIBITORS; ENTAMOEBA HISTOLYTICA; ERYTHROCYTES; EVOLUTION; GTP-BINDING PROTEINS; HYDROGEN-ION CONCENTRATION; IMMUNOLOGIC CAPPING; LEUCINE; MACROLIDES; MACROPHAGES; MODELS, BIOLOGICAL; MONENSIN; MUTATION; PHAGOCYTOSIS; PINOCYTOSIS; RAC GTP-BINDING PROTEINS; TRANSFORMATION, GENETIC; VACUOLES;

EID: 0030610666     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/iai.65.10.4243-4249.1997     Document Type: Article

References (55)

1. Adams, A. E. M., D. I. Johnson, R. M. Longnecker, B. F. Sloat, and J. R. Pringle. 1991. CDC42 and CDC43, two additional genes involved in budding and establishment of cell polarity in the yeast Saccharomyces cerevisiae. J. Cell Biol. 111:131-142.
2. Ahrets, 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.
3. Andersson, M., H. Gunne, B. Agerberth, A. Boman, T. Bergman, R. Sillard, H. Jornvall, V. Mutt, B. Olsson, H. Wigzell, A. Dagerlind, H. G. Boman, and G. H. Gudmundsson. 1995. NK-lysin, a novel effector peptide of cytotoxic T and NK-cells. Structure and cDNA cloning of the porcine form, induction by interleukin 2, antibacterial and antitumour activity. EMBO J. 14:1615-1625.
4. Araki, N., M. T. Johnson, and J. A. Swanson. 1996. A role for phosphoinositide 3-kinase in the completion of macropinocytosis and phagocytosis by macrophages. J. Cell Biol. 135:1249-1260.
5. Bailey, G. B., D. B. Day, and G. W. Gasque. 1985. Rapid polymerization of Entamoeba histolytica actin induced by interaction with target cells. J. Exp. Med. 162:546-558.
6. Biagi, F., and J. Portilla. 1957. Comparison of methods of examining stools for parasites. Am. J. Trop. Med. Hyg. 6:906-911.
7. Bowman, E. J., A. Siebers, and K. Altendorf. 1988. Bafilomycins: a class of inhibitors of membrane ATPases from microorganisms, animal cells, and plant cells. Proc. Natl. Acad. Sci. USA 85:7972-7976.
8. Brandt, H., and R. Perez Tamayo. 1970. Pathology of human amebiasis. Hum. Pathol. 1:351-385.
9. 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.
10. Bush, J., K. Franek, and J. Cardelli. 1993. Cloning and characterization of seven novel Dictyostelium discoideum rac-related genes belonging to the rho family of GTPases. Gene 136:61-68.
11. Chen, W., H. H. Lim, and I. Lim. 1993. A new member of the ras superfamily, the rac1 homologue from Caenorhabditis elegans. J. Biol. Chem. 268:320-324.
12. phox and regulation of phagocytotic NADPH oxidase activity. Science 265:531-537.
13. de la Garza, M., B. Gallegos, and I. Meza. 1989. Characterization of a cytochalasin D-resistant mutant of Entamoeba histolytica. J. Protozool. 36: 556-560.
14. Descoteaux, S., Y. Yi, and J. Samuelson. 1994. Cloning of Entamoeba genes encoding proteolipids of putative vacuolar proton-translocating ATPases (V-ATPases). Infect. Immun. 62:3572-3575.
15. Diamond, L. S., and C. G. Clark. 1993. A redescription of Entamoeba histolytica Schaudinn, 1903 (emended Walker, 1911) separating it from Entamoeba dispar Brumpt, 1925. J. Eukaryot. Microbiol. 40:340-344.
16. Espinosa-Cantellano, M., and A. Martinez-Palomo. 1994. Entamoeba histolytica: mechanism of surface receptor capping. Exp. Parasitol. 79:424-435.
17. 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.
18. Grinstein, S., A. Nanda, G. Lukacs, and O. Rotstein. 1992. V-ATPases in phagocytic cells. J. Exp. Biol. 172:179-192.
19. Groisman, E. A., and H. Ochman. 1994. How to become a pathogen. Trends Microbiol. 2:289-294.
20. Guillen, N. 1996. Role of signaling and cytoskeletal rearrangements in the pathogenesis of Entamoeba histolytica. Trends Microbiol. 4:191-197.
21. Guillen, N. and P. Sansonetti. 1997. Rac G, a small GTPase, regulates capping of surface receptors in Entamoeba histolytica. Arch. Med. Res. 28:S129-S131.
22. Hall, A. 1994. Small GTP-binding proteins and the regulation of the actin cytoskeleton. Annu. Rev. Cell Biol. 10:31-54.
23. Jacobs, T., and M. Leippe. 1995. Purification and molecular cloning of a major antibacterial protein of the protozoan parasite Entamoeba histolytica with lysozyme-like properties. Eur. J. Biochem. 231:831-838.
24. Keene, W. H., M. E. Hidalgo, E. Orozco, and J. H. McKerrow. 1990. Entamoeba histolytica: correlation of the cytopathic effects of virulent trophozoite with secretion of a cysteine proteinase. Exp. Parasitol. 71:199-206.
25. Kobzik, L. 1995. Lung macrophage uptake of unopsonized environmental particulates. J. Immunol. 155:367-376.
26. Lee, D. H., and A. L. Goldberg. 1996. Selective inhibitors of the proteasome-dependcnt and vacuolar pathways of protein degradation in Saccharomyces cerevisiae. J. Biol. Chem. 271:27280-27284.
27. Leippe, M. 1994. Cytolytic and anti-bacterial activity of synthetic peptides derived from amoebapore, the pore-forming peptide of Entamoeba histolytica. Proc. Natl. Acad. Sci. USA 91:2602-2606.
28. Leippe, M. 1997. Amoebapores. Parasitol. Today 13:178-183.
29. Levin, B. R., and C. Svanborg Eden. 1990. Selection and evolution of virulence in bacteria: an ecumenical excursion and modest suggestion. Parasitology 100:S103-S115.
30. Lohden-Bendinger, U., and T. Bakker-Grunwald. 1990. Evidence for a vacuolar-type proton ATPase in Entamoeba histolytica. Z. Naturforsch, 45c:229-232.
31. rac homologues. Gene 173:205-208.
32. Mann, B. J., B. E. Torina, T. S. Vedvick, and W. R. Petri, Jr. 1991. Sequence of a cysteine-rich galactose-specific lectin of Entamoeba histolytica. Proc. Natl. Acad. Sci. USA 88:3248-3252.
33. Marsh, K., M. English, J. Crawley, and N. Peshu. 1996. The pathogenesis of cerebral malaria in African children. Ann. Trop. Med. Parasitol. 90:395-402.
34. Martinez-Palomo, A., and M. Martinez-Baez. 1983. Selective primary health care: strategies for control of disease in the developing world. X. Amebiasis. Rev. Infect. Dis. 5:1093-1102.
35. May, R. M., and R. M. Anderson. 1990. Parasite-host coevolution. Parasitology 100:S89-S101.
36. Mirelman, D. 1987. Ameba-bacterium relationship in amebiasis. Microbiol. Rev. 51:272-284.
37. Ninomiya, N., K. Hazeki, Y. Fukui, T. Seya, T. Okada, O. Hazeki, and M. Ui. 1994. Involvement of phosphotidylinositol 3-kinase in Fcg receptor signaling. J. Biol. Chem. 269:22732-22737.
38. Nobes, C. D., and A. Hall. 1995. Rho, Rac, and Cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81:53-62.
39. Que, X., and S. L. Reed. 1997. Role of extracellular cysteine proteinases in pathogenesis of Entamoeba histolytica invasion. Parasitol. Today 13:190-194.
40. Ravdin, J. I. 1995. Amebiasis. State-of-the-art clinical article. Clin. Infect. Dis. 20:1453-1464.
41. Ravdin, J. I., P. H. Schlesinger, C. F. Murphy, I. Y. Gluzman, and D. J. Krogstad. 1986. Acid intracellular vesicles and cytolysis of mammalian target cells by Entamoeba histolytica trophozoites. J. Protozool. 33:478-486.
42. 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.
43. Read, A. F. 1994. The evolution of virulence. Trends Microbiol. 2:73-76.
44. Reeves, R. E. 1984. Metabolism of Entamoeba histolytica Schaudinn, 1903. Adv. Parasitol. 23:105-142.
45. Ridley, A. J., H. F. Paterson, C. L. Johnston, D. Diekmann, and A. Hall. 1992. The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell 70:401-410.
46. 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.
47. Samuelson, J., N. Azikiwe, and P.-S. Shen. 1995. Proton- and calcium ion-transporting ATPases of Entamoeba histolytica. Parasitol. Today 11:417-420.
48. 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.
49. p (G25K): identification of the GTP-binding protein as the human homologue of the yeast cell-division-cycle protein CDC42. Proc. Natl. Acad. Sci. USA 87:9853-9857.
50. Skolnik, E. Y., B. Margolis, M. Mohammadi, E. Lowenstein, R. Fischer, A. Drepps, A. Ullrich, and J. Schlessinger. 1991. Cloning of the PI 3 kinase-associated p85 utilizing a novel method for expression/cloning of target proteins for receptor tyrosine kinases. Cell 65:83-90.
51. Stanley, S. L., Jr., T. Zhang, D. Rubin, and E. Li. 1995. Role of the Entamoeba histolytica cysteine proteinase in amebic liver abscess formation in severe combined immunodeficiency mice. Infect. Immun. 63:1587-1590.
52. 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.
53. Wilson, I. A., H. L. Niman, R. A. Houghten, A. R. Cherenson, M. L. Connoly, and R. A. Lerner. 1984. The structure of an antigenic determinant in a protein. Cell 37:767-778.
54. Wymann, M. P., G. Bulgarelli-Leva, M. J. Zvelebil, L. Pirola, B. Vanhaesebroek, M. D. Waterfleld, and G. Panayoutou. 1996. Wortmannin inactivates phosphoinositide 3-kinase by covalent modification of Lys-802, a residue involved in the phosphate transfer reaction. Mol. Cell. Biol. 16:1722-1733.
55. Yi, Y., and J. Samuelson. 1994. Primary structure of the Entamoeba histolytica gene (Ehvma1) encoding the catalytic peptide of a putative vacuolar membrane proton-transporting ATPase (V-ATPase). Mol. Biochem. Parasitol. 66:16-169.