Electron microscopy and cytochemistry analysis of the endocytic pathway of pathogenic protozoa

Progress in Histochemistry and Cytochemistry

Volumn 44, Issue 2, 2009, Pages 67-124

  de Souza, Wanderley ^a,b   Sant'Anna, Celso ^a,b   Cunha e Silva, Narcisa L ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b INSTITUTO NACIONAL DE METROLOGIA   (Brazil)

Author keywords

Apicomplexa; Electron microscopy cytochemistry; Endocytosis; Entamoeba; Giardia; Lysosome; Protozoa; Reservosome; Trichomonas; Trypanosomatids

Indexed keywords

ARTICLE; CELL PROLIFERATION; CELL SURVIVAL; CYTOCHEMISTRY; ELECTRON MICROSCOPY; ENDOCYTOSIS; ENTAMOEBA; ENTAMOEBA DISPAR; ENTAMOEBA HISTOLYTICA; EUKARYOTIC CELL; GIARDIA; GIARDIA LAMBLIA; IMMUNITY; LEISHMANIA; LIFE CYCLE; MAMMAL; MORPHOLOGY; NONHUMAN; PLASMODIUM; PROTOZOON; TRICHOMONAS; TRICHOMONAS FOETUS; TRICHOMONAS VAGINALIS; TRYPANOSOMA BRUCEI; TRYPANOSOMA CRUZI; YEAST CELL;

ANIMALS; ENDOCYTOSIS; ENTAMOEBA; GIARDIA; HISTOCYTOCHEMISTRY; LEISHMANIA; MICROSCOPY, ELECTRON; PLASMODIUM; PROTOZOA; TRICHOMONAS; TRYPANOSOMA BRUCEI BRUCEI; TRYPANOSOMA CRUZI;

APICOMPLEXA; ENTAMOEBA; EUKARYOTA; GIARDIA; MAMMALIA; PLASMODIUM (APICOMPLEXA); PROTOZOA; TRICHOMONAS; TRYPANOSOMA BRUCEI; TRYPANOSOMA CRUZI; TRYPANOSOMATIDAE;

EID: 67349135043     PISSN: 00796336     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.proghi.2009.01.001     Document Type: Article

References (195)

1. Adade C.M., de Castro S.L., and Soares M.J. Ultrastructural localization of Trypanosoma cruzi lysosomes by aryl sulphatase cytochemistry. Micron 38 (2007) 252-256
2. Addis M.F., Rappelli P., Delogu G., Carta F., Cappuccinelli P., and Fiori P.L. Cloning and molecular characterization of a cDNA clone coding for Trichomonas vaginalis alpha-actinin and intracellular localization of the protein. Infect Immun 66 (1998) 4924-4931
3. Affonso A.L., Benchimol M., Ribeiro K.C., Lins U., and De Souza W. Further studies on the endocytic activity of Tritrichomonas foetus. Parasitol Res 80 (1994) 403-413
4. Affonso A.L., de Almeida J.C., and Benchimol M. Partial characterization of cytoplasmic compartments involved in the endocytic process of Tritrichomonas foetus. Eur J Cell Biol 72 (1997) 247-256
5. Aikawa M. Parasitological review. Plasmodium: the fine structure of malarial parasites. Exp Parasitol 30 (1971) 284-320
6. Aikawa M., Hepler P.K., Huff C.G., and Sprinz H. The feeding mechanism of avian malarial parasites. J Cell Biol 28 (1966) 355-373
7. Alberio S.O., Dias S.S., Faria F.P., Mortara R.A., Barbieri C.L., and Freymuller Haapalainen E. Ultrastructural and cytochemical identification of megasome in Leishmania (Leishmania) chagasi. Parasitol Res 92 (2004) 246-254
8. Alexander D.L., Schwartz K.J., Balber A.E., and Bangs J.D. Developmentally regulated trafficking of the lysosomal membrane protein p67 in Trypanosoma brucei. J Cell Sci 115 (2002) 3253-3263
9. Alexander J., and Vickerman K. Fusion of host cell secondary lysosomes with the parasitophorous vacuoles of Leishmania mexicana-infected macrophages. J Protozool 22 (1975) 502-508
10. Allen C.L., Goulding D., and Field M.C. Clathrin-mediated endocytosis is essential in Trypanosoma brucei. EMBO J 22 (2003) 4991-5002
11. Alvarez V.E., Kosec G., Sant'Anna C., Turk V., Cazzulo J.J., and Turk B. Autophagy is involved in nutritional stress response and differentiation in Trypanosoma cruzi. J Biol Chem 283 (2008) 3454-3464
12. Alvarez V.E., Kosec G., Sant'Anna C., Turk V., Cazzulo J.J., and Turk B. Blocking autophagy to prevent parasite differentiation: a possible new strategy for fighting parasitic infections?. Autophagy 4 (2008) 361-363
13. Anderson R.G., Falck J.R., Goldstein J.L., and Brown M.S. Visualization of acidic organelles in intact cells by electron microscopy. Proc Natl Acad Sci USA 81 (1984) 4838-4842
14. Andrews N.W. Lysosomes and the plasma membrane: trypanosomes reveal a secret relationship. J Cell Biol 158 (2002) 389-394
15. Angermüller S., and Fahimi H.D. Imidazole-buffered osmium tetroxide: an excellent stain for visualization of lipids in transmission electron microscopy. Histochem J 14 (1982) 823-835
16. Antoine J.C., Jouanne C., Ryter A., and Benichou J.C. Leishmania amazonensis: acidic organelles in amastigotes. Exp Parasitol 67 (1988) 287-300
17. Antoine J.C., Jouanne C., and Ryter A. Megasomes as the targets of leucine methyl ester in Leishmania amazonensis amastigotes. Parasitology 1 (1989) 1-9
18. Antoine J.C., Lang T., Prina E., Courret N., and Hellio R. H-2M molecules, like MHC class II molecules, are targeted to parasitophorous vacuoles of Leishmania-infected macrophages and internalized by amastigotes of L. amazonensis and L. mexicana. J Cell Sci 112 (1999) 2559-2570
19. Araripe J.R., Cunha e Silva N.L., Leal S.T., De Souza W., and Rondinelli E. Trypanosoma cruzi: TcRAB7 protein is localized at the Golgi apparatus in epimastigotes. Biochem Biophys Res Commun 321 (2004) 397-402
20. Araripe J.R., Ramos F.P., Cunha e Silva N.L., Urmenyi T.P., Silva R., Leite Fontes C.F., et al. Characterization of a RAB5 homologue in Trypanosoma cruzi. Biochem Biophys Res Commun 329 (2005) 638-645
21. Bailey G.B., Day D.B., Nokkaew C., and Harper C.C. Stimulation by target cell membrane lipid of actin polymerization and phagocytosis by Entamoeba histolytica. Infect Immun 55 (1987) 1848-1853
22. Balzac F., Avolio M., Degani S., Kaverina I., Torti M., Silengo L., et al. E-cadherin endocytosis regulates the activity of Rap1: a traffic light GTPase at the crossroads between cadherin and integrin function. J Cell Sci 118 (2005) 4765-4783
23. Batista E.J., and De Souza W. Involvement of protein kinases on the process of erythrophagocytis by Entamoeba histolytica. Cell Biol Int 28 (2004) 243-248
24. Batista E.J., de Menezes Feitosa L.F., and de Souza W. The endocytic pathway in Entamoeba histolytica. Parasitol Res 86 (2000) 881-890
25. Benchimol M., Batista C., and De Souza W. Fibronectin- and laminin-mediated endocytic activity in the parasitic protozoa Trichomonas vaginalis and Tritrichomonas foetus. J Submicrosc Cytol Pathol 22 (1990) 39-45
26. Benchimol M., da Cunha e Silva N.L., Elias C.A., and de Souza W. Tritrichomonas foetus: ultrastructure and cytochemistry of endocytosis. Exp Parasitol 62 (1986) 405-415
27. Bloom F.E., and Aghajanian G.K. Fine structural and cytochemical analysis of the staining of synaptic junctions with phosphotungstic acid. J Ultrastruct Res 22 (1968) 361-375
28. Bockman A., and Winborn W.B. Electron microscopic localization of exogenous ferritin within vacuoles of Giardia muris (sp.). J. Protozool. 15 (1968) 26-30
29. Boettner D.R., Huston C.D., Linford A.S., Buss S.N., Houpt E., Sherman N.E., et al. Entamoeba histolytica phagocytosis of human erythrocytes involves PATMK, a member of the transmembrane kinase family. PLoS Pathog 4 (2008) 8
30. Bogitsh B.J., Ribeiro-Rodrigues R., and Carter C.E. In vitro effects of mannan and cytochalasin B on the uptake of horseradish peroxidase and [14C]sucrose by Trypanosoma cruzi epimastigotes. J Parasitol 81 (1995) 144-148
31. Boiso J.F., Docampo R., and Stoppani A.O.M. Investigacion citoquimica por microscopia electronica de la presencia de microperoxisomas en Trypanosoma cruzi. Medicina (Buenos Aires) 37 (1977) 365-370
32. Bonifacino J.S., and Traub L.M. Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu Rev Biochem 72 (2003) 395-447
33. Borges V.M., Vannier-Santos M.A., and de Souza W. Subverted transferrin trafficking in Leishmania-infected macrophages. Parasitol Res 84 (1998) 811-822
34. Bracha R., Kobiler D., and Mirelman D. Attachment and ingestion of bacteria by trophozoites of Entamoeba histolytica. Infect Immun 36 (1982) 396-406
35. Bricheux G., and Brugerolle G. Molecular cloning of actin genes in Trichomonas vaginalis and phylogeny inferred from actin sequences. FEMS Microbiol Lett 153 (1997) 205-213
36. Bricheux G., Coffe G., Bayle D., and Brugerolle G. Characterization, cloning and immunolocalization of a coronin homologue in Trichomonas vaginalis. Eur J Cell Biol 79 (2000) 413-422
37. Bricheux G., Coffe G., Pradel N., and Brugerolle G. Evidence for an uncommon alpha-actinin protein in Trichomonas vaginalis. Mol Biochem Parasitol 95 (1998) 241-249
38. Brickman M.J., Cook J.M., and Balber A.E. Low temperature reversibly inhibits transport from tubular endosomes to a perinuclear, acidic compartment in African trypanosomes. J Cell Sci 108 (1995) 3611-3621
39. Bright N.A., Gratian M.J., and Luzio J.P. Endocytic delivery to lysosomes mediated by concurrent fusion and kissing events in living cells. Curr Biol 15 (2005) 360-365
40. Brugerolle G. Mise en evidence du processus d'endocytose et de structures lysosomiques chez Trichomonas vaginalis. C R Acad Sci (Paris) 272 (1971) 2558-2560
41. Brugerolle G., Bricheux G., and Coffe G. Actin cytoskeleton demonstration in Trichomonas vaginalis and in other trichomonads. Biol Cell 88 (1996) 29-36
42. Carlton J.M., Hirt R.P., Silva J.C., Delcher A.L., Schatz M., Zhao Q., et al. Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science 315 (2007) 207-212
43. Chadda R., Howes M.T., Plowman S.J., Hancock J.F., Parton R.G., and Mayor S. Cholesterol-sensitive Cdc42 activation regulates actin polymerization for endocytosis via the GEEC pathway. Traffic 8 (2007) 702-717
44. Chanez A.L., Hehl A.B., Engstler M., and Schneider A. Ablation of the single dynamin of T. brucei blocks mitochondrial fission and endocytosis and leads to a precise cytokinesis arrest. J Cell Sci 119 (2006) 2968-2974
45. Coombs G.H., Tetley L., Moss V.A., and Vickerman K. Three dimensional structure of the Leishmania amastigote as revealed by computer-aided reconstruction from serial sections. Parasitology 92 (1986) 13-23
46. Coppens I., Opperdoes F.R., Courtoy P.J., and Baudhuin P. Receptor-mediated endocytosis in the bloodstream form of Trypanosoma brucei. J Protozool 34 (1987) 465-473
47. Corrêa J.R., Atella G.C., Batista M.M., and Soares M.J. Transferrin uptake in Trypanosoma cruzi is impaired by interference on cytostome-associated cytoskeleton elements and stability of membrane cholesterol, but not by obstruction of clathrin-dependent endocytosis. Exp Parasitol 119 (2008) 58-66
48. Corrêa J.R., Atella G.C., Menna-Barreto R.S., and Soares M.J. Clathrin in Trypanosoma cruzi: in silico gene identification, isolation, and localization of protein expression sites. J Eukaryot Microbiol 54 (2007) 297-302
49. Cuevas I.C., Rohloff P., Sanchez D.O., and Docampo R. Characterization of farnesylated protein tyrosine phosphatase TcPRL-1 from Trypanosoma cruzi. Eukaryot Cell 4 (2005) 1550-1561
50. Cullen P.J. Endosomal sorting and signalling: an emerging role for sorting nexins. Nat Rev Mol Cell Biol 9 (2008) 574-582
51. Cunha-e-Silva N., Sant'Anna C., Pereira M.G., Porto-Carreiro I., Jeovanio A.L., and de Souza W. Reservosomes: multipurpose organelles?. Parasitol Res 99 (2006) 325-327
52. Cunha-e-Silva N.L., Atella G.C., Porto-Carreiro I.A., Morgado-Diaz J.A., Pereira M.G., and De Souza W. Isolation and characterization of a reservosome fraction from Trypanosoma cruzi. FEMS Microbiol Lett 214 (2002) 7-12
53. De Figueiredo R.C., and Soares M.J. Low temperature blocks fluid-phase pinocytosis and receptor-mediated endocytosis in Trypanosoma cruzi epimastigotes. Parasitol Res 86 (2000) 413-418
54. De Matteis M.A., and Luini A. Exiting the Golgi complex. Nat Rev Mol Cell Biol 9 (2008) 273-284
55. De Melo L.D., Nepomuceno-Silva J.L., Sant'Anna C., Eisele N., Ferraro R.B., Meyer-Fernandes J.R., et al. TcRho1 of Trypanosoma cruzi: role in metacyclogenesis and cellular localization. Biochem Biophys Res Commun 323 (2004) 1009-1016
56. De Melo L.D., Sant'Anna C., Reis S.A., Lourenco D., De Souza W., Lopes U.G., et al. Evolutionary conservation of actin-binding proteins in Trypanosoma cruzi and unusual subcellular localization of the actin homologue. Parasitology 135 (2008) 955-965
57. De Souza Leao S., Lang T., Prina E., Hellio R., and Antoine J.C. Intracellular Leishmania amazonensis amastigotes internalize and degrade MHC class II molecules of their host cells. J Cell Sci 108 (1995) 3219-3231
58. De Souza W. Basic cell biology of Trypanosoma cruzi. Curr Pharm Des 8 (2002) 269-285
59. de Souza W., de Carvalho T.U., Benchimol M., and Chiari E. Trypanosoma cruzi: ultrastructural, cytochemical and freeze-fracture studies of protein uptake. Exp Parasitol 45 (1978) 101-115
60. Denny P.W., Morgan G.W., Field M.C., and Smith D.F. Leishmania major: clathrin and adaptin complexes of an intra-cellular parasite. Exp Parasitol 109 (2005) 33-37
61. Eakin A.E., Mills A.A., Harth G., McKerrow J.H., and Craik C.S. The sequence, organization, and expression of the major cysteine protease (cruzain) from Trypanosoma cruzi. J Biol Chem 267 (1992) 7411-7420
62. Egan T.J., Combrinck J.M., Egan J., Hearne G.R., Marques H.M., Ntenteni S., et al. Fate of haem iron in the malaria parasite Plasmodium falciparum. Biochem J 365 (2002) 343-347
63. Elliott D.A., McIntosh M.T., Hosgood III H.D., Chen S., Zhang G., Baevova P., et al. Four distinct pathways of hemoglobin uptake in the malaria parasite Plasmodium falciparum. Proc Natl Acad Sci USA 105 (2008) 2463-2468
64. El-Sayed N.M., Myler P.J., Bartholomeu D.C., Nilsson D., Aggarwal G., Tran A.N., et al. The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309 (2005) 409-415
65. Engel J.C., Doyle P.S., Palmer J., Hsieh I., Bainton D.F., and McKerrow J.H. Cysteine protease inhibitors alter Golgi complex ultrastructure and function in Trypanosoma cruzi. J Cell Sci 111 (1998) 597-606
66. Engel J.C., Torres C., Hsieh I., Doyle P.S., and McKerrow J.H. Upregulation of the secretory pathway in cysteine protease inhibitor-resistant Trypanosoma cruzi. J Cell Sci 113 (2000) 1345-1354
67. Engstler M., Bangs J.D., and Field M.C. Intracellular transport systems in trypanosomes: function, evolution and virulence. In: Barry J.D., Mottram J., McCulloch R., and Acosta-Serrano A. (Eds). Trypanosomes - after the genome (2007), Horizon Press
68. Engstler M., Thilo L., Weise F., Grunfelder C.G., Schwarz H., Boshart M., et al. Kinetics of endocytosis and recycling of the GPI-anchored variant surface glycoprotein in Trypanosoma brucei. J Cell Sci 117 (2004) 1105-1115
69. Feely D.E., and Dyer J.K. Localization of acid phosphatase activity in Giardia lamblia and Giardia muris trophozoites. J Protozool 34 (1987) 80-83
70. Field H., Farjah M., Pal A., Gull K., and Field M.C. Complexity of trypanosomatid endocytosis pathways revealed by Rab4 and Rab5 isoforms in Trypanosoma brucei. J Biol Chem 273 (1998) 32102-32110
71. Field M.C., and Carrington M. Intracellular membrane transport systems in Trypanosoma brucei. Traffic 5 (2004) 905-913
72. Francioli P., Shio H., Roberts R.B., and Muller M. Phagocytosis and killing of Neisseria gonorrhoeae by Trichomonas vaginalis. J Infect Dis 147 (1983) 87-94
73. Franco-Barraza J., Zamudio-Meza H., Franco E., del Carmen Dominguez-Robles M., Villegas-Sepulveda N., and Meza I. Rho signaling in Entamoeba histolytica modulates actomyosin-dependent activities stimulated during invasive behavior. Cell Motil Cytoskeleton 63 (2006) 117-131
74. Frick M., Bright N.A., Riento K., Bray A., Merrified C., and Nichols B.J. Coassembly of flotillins induces formation of membrane microdomains, membrane curvature, and vesicle budding. Curr Biol 17 (2007) 1151-1156
75. Gaechter V., Schraner E., Wild P., and Hehl A.B. The single dynamin family protein in the primitive protozoan Giardia lamblia is essential for stage conversion and endocytic transport. Traffic 9 (2008) 57-71
76. Garcia E.S., and Azambuja P. Development and interactions of Trypanosoma cruzi within the insect vector. Parasitol Today 7 (1991) 240-244
77. Garcia-Salcedo J.A., Perez-Morga D., Gijon P., Dilbeck V., Pays E., and Nolan D.P. A differential role for actin during the life cycle of Trypanosoma brucei. EMBO J 23 (2004) 780-789
78. Ghedin E., Debrabant A., Engel J.C., and Dwyer D.M. Secretory and endocytic pathways converge in a dynamic endosomal system in a primitive protozoan. Traffic 2 (2001) 175-188
79. Gonzalez-Robles A., Lazaro-Haller A., Espinosa-Cantellano M., Anaya-Velazquez F., and Martinez-Palomo A. Trichomonas vaginalis: ultrastructural bases of the cytopathic effect. J Eukaryot Microbiol 42 (1995) 641-651
80. Goodyer I.D., Pouvelle B., Schneider T.G., Trelka D.P., and Taraschi T.F. Characterization of macromolecular transport pathways in malaria-infected erythrocytes. Mol Biochem Parasitol 87 (1997) 13-28
81. Grab D.J., Shaw M.K., Wells C.W., Verjee Y., Russo D.C., Webster P., et al. The transferrin receptor in African trypanosomes: identification, partial characterization and subcellular localization. Eur J Cell Biol 62 (1993) 114-126
82. Grassart A., Dujeancourt A., Lazarow P.B., Dautry-Varsat A., and Sauvonnet N. Clathrin-independent endocytosis used by the IL-2 receptor is regulated by Rac1, Pak1 and Pak2. EMBO Rep 9 (2008) 356-362
83. Grunfelder C.G., Engstler M., Weise F., Schwarz H., Stierhof Y.D., Morgan G.W., et al. Endocytosis of a glycosylphosphatidylinositol-anchored protein via clathrin-coated vesicles, sorting by default in endosomes, and exocytosis via RAB11-positive carriers. Mol Biol Cell 14 (2003) 2029-2040
84. Hernandez Y., Castillo C., Roychowdhury S., Hehl A., Aley S.B., and Das S. Clathrin-dependent pathways and the cytoskeleton network are involved in ceramide endocytosis by a parasitic protozoan, Giardia lamblia. Int J Parasitol 37 (2007) 21-32
85. Hung C.H., Qiao X., Lee P.T., and Lee M.G. Clathrin-dependent targeting of receptors to the flagellar pocket of procyclic-form Trypanosoma brucei. Eukaryot Cell 3 (2004) 1004-1014
86. Huston C.D., Boettner D.R., Miller-Sims V., and Petri Jr. W.A. Apoptotic killing and phagocytosis of host cells by the parasite Entamoeba histolytica. Infect Immun 71 (2003) 964-972
87. Idrissi F.Z., Grotsch H., Fernandez-Golbano I.M., Presciatto-Baschong C., Riezman H., and Geli M.I. Distinct acto/myosin-I structures associate with endocytic profiles at the plasma membrane. J Cell Biol 180 (2008) 1219-1232
88. Ilgoutz S.C., Mullin K.A., Southwell B.R., and McConville M.J. Glycosylphosphatidylinositol biosynthetic enzymes are localized to a stable tubular subcompartment of the endoplasmic reticulum in Leishmania mexicana. EMBO J 18 (1999) 3643-3654
89. Jain R., Santi-Rocca J., Padhan N., Bhattacharya S., Guillen N., and Bhattacharya A. Calcium-binding protein 1 of Entamoeba histolytica transiently associates with phagocytic cups in a calcium-independent manner. Cell Microbiol 10 (2008) 1373-1389
90. Jeffries T.R., Morgan G.W., and Field M.C. A developmentally regulated rab11 homologue in Trypanosoma brucei is involved in recycling processes. J Cell Sci 114 (2001) 2617-2626
91. Jordens I., Marsman M., Kuijl C., and Neefjes J. Rab proteins, connecting transport and vesicle fusion. Traffic 6 (2005) 1070-1077
92. Juliano C., Cappuccinelli P., and Mattana A. In vitro phagocytic interaction between Trichomonas vaginalis isolates and bacteria. Eur J Clin Microbiol Infect Dis 10 (1991) 497-502
93. Kaksonen M., Toret C.P., and Drubin D.G. A modular design for the clathrin- and actin-mediated endocytosis machinery. Cell 123 (2005) 305-320
94. Kattenbach W.M., Pimenta P.F., de Souza W., and Pinto da Silva P. Giardia duodenalis: a freeze-fracture, fracture-flip and cytochemistry study. Parasitol Res 77 (1991) 651-658
95. Kollien A.H., and Schaub G.A. The development of Trypanosoma cruzi in triatominae. Parasitol Today 16 (2000) 381-387
96. Lafourcade C., Sobo K., Kieffer-Jaquinod S., Garin J., and van der Goot F.G. Regulation of the V-ATPase along the endocytic pathway occurs through reversible subunit association and membrane localization. PLoS ONE 3 (2008) e2758
97. Landfear S.M., and Ignatushchenko M. The flagellum and flagellar pocket of trypanosomatids. Mol Biochem Parasitol 115 (2001) 1-17
98. Lanfredi-Rangel A., Attias M., de Carvalho T.M., Kattenbach W.M., and De Souza W. The peripheral vesicles of trophozoites of the primitive protozoan Giardia lamblia may correspond to early and late endosomes and to lysosomes. J Struct Biol 123 (1998) 225-235
99. Langreth S.G., Jensen J.B., Reese R.T., and Trager W. Fine structure of human malaria in vitro. J Protozool 25 (1978) 443-452
100. Lara F.A., Sant'Anna C., Lemos D., Laranja G.A., Coelho M.G., Reis Salles I., et al. Heme requirement and intracellular trafficking in Trypanosoma cruzi epimastigotes. Biochem Biophys Res Commun 30; 355 (2007) 16-22
101. Lazarus M.D., Schneider T.G., and Taraschi T.F. A new model for hemoglobin ingestion and transport by the human malaria parasite Plasmodium falciparum. J Cell Sci 121 (2008) 1937-1949
102. Leabu M. Membrane fusion in cells: molecular machinery and mechanisms. J Cell Mol Med 10 (2006) 423-427
103. Lindmark D.G. Giardia lamblia: localization of hydrolase activities in lysosome-like organelles of trophozoites. Exp Parasitol 65 (1988) 141-147
104. +-ATPases with different enzymatic properties. J Biol Chem 277 (2002) 44497-44506
105. Luzio J.P., Pryor P.R., and Bright N.A. Lysosomes: fusion and function. Nat Rev Mol Cell Biol 8 (2007) 622-632
106. Marion S., Laurent C., and Guillen N. Signalization and cytoskeleton activity through myosin IB during the early steps of phagocytosis in Entamoeba histolytica: a proteomic approach. Cell Microbiol 7 (2005) 1504-1518
107. Marion S., Wilhelm C., Voigt H., Bacri J.C., and Guillen N. Overexpression of myosin IB in living Entamoeba histolytica enhances cytoplasm viscosity and reduces phagocytosis. J Cell Sci 117 (2004) 3271-3279
108. Marotta D.E., Gerald N., and Dwyer D.M. Rab5b localization to early endosomes in the protozoan human pathogen Leishmania donovani. Mol Cell Biochem 292 (2006) 107-117
109. Martinez-Palomo A., De Souza W., and Gonzalez-Robles A. Topographical differences in the distribution of surface coat components and intramembrane particles. A cytochemical and freeze-fracture study in culture forms of Trypanosoma cruzi. J Cell Biol 69 (1976) 507-513
110. Mauricio de Mendonca S.M., Nepomuceno da Silva J.L., Cunha-e-Silva N., de Souza W., and Gazos Lopes U. Characterization of a Rab11 homologue in Trypanosoma cruzi. Gene 243 (2000) 179-185
111. Mayor S., and Pagano R.E. Pathways of clathrin-independent endocytosis. Nat Rev Mol Cell Biol 8 (2007) 603-612
112. McConville M.J., Mullin K.A., Ilgoutz S.C., and Teasdale R.D. Secretory pathway of trypanosomatid parasites. Microbiol Mol Biol Rev 66 (2002) 122-154 table of contents
113. McGrory T., Meysick K., Lemchuk-Favel L.T., and Garber G.E. The interaction of Lactobacillus acidophilus and Trichomonas vaginalis in vitro. J Parasitol 80 (1994) 50-54
114. Mitra B.N., Kobayashi S., Saito-Nakano Y., and Nozaki T. Entamoeba histolytica: differences in phagosome acidification and degradation between attenuated and virulent strains. Exp Parasitol 114 (2006) 57-61
115. Mitra B.N., Saito-Nakano Y., Nakada-Tsukui K., Sato D., and Nozaki T. Rab11B small GTPase regulates secretion of cysteine proteases in the enteric protozoan parasite Entamoeba histolytica. Cell Microbiol 9 (2007) 2112-2125
116. Morgan G.W., Allen C.L., Jeffries T.R., Hollinshead M., and Field M.C. Developmental and morphological regulation of clathrin-mediated endocytosis in Trypanosoma brucei. J Cell Sci 114 (2001) 2605-2615
117. Morgan G.W., Goulding D., and Field M.C. The single dynamin-like protein of Trypanosoma brucei regulates mitochondrial division and is not required for endocytosis. J Biol Chem 279 (2004) 10692-10701
118. Morgan G.W., Hall B.S., Denny P.W., Carrington M., and Field M.C. The kinetoplastida endocytic apparatus. Part I: a dynamic system for nutrition and evasion of host defences. Trends Parasitol 18 (2002) 491-496
119. Morgan G.W., Hall B.S., Denny P.W., Field M.C., and Carrington M. The endocytic apparatus of the kinetoplastida. Part II: machinery and components of the system. Trends Parasitol 18 (2002) 540-546
120. Mullin K.A., Foth B.J., Ilgoutz S.C., Callaghan J.M., Zawadzki J.L., McFadden G.I., et al. Regulated degradation of an endoplasmic reticulum membrane protein in a tubular lysosome in Leishmania mexicana. Mol Biol Cell 12 (2001) 2364-2377
121. Mussmann R., Engstler M., Gerrits H., Kieft R., Toaldo C.B., Onderwater J., et al. Factors affecting the level and localization of the transferrin receptor in Trypanosoma brucei. J Biol Chem 279 (2004) 40690-40698
122. Nakada-Tsukui K., Saito-Nakano Y., Ali V., and Nozaki T. A retromerlike complex is a novel Rab7 effector that is involved in the transport of the virulence factor cysteine protease in the enteric protozoan parasite Entamoeba histolytica. Mol Biol Cell 16 (2005) 5294-5303
123. Nayak R.C., Sahasrabuddhe A.A., Bajpai V.K., and Gupta C.M. A novel homologue of coronin colocalizes with actin in filament-like structures in Leishmania. Mol Biochem Parasitol 143 (2005) 152-164
124. Nolan D.P., and Garcia-Salcedo J.A. Loss of actin does not affect export of newly synthesized proteins to the surface of Trypanosoma brucei. Mol Biochem Parasitol 157 (2008) 233-235
125. Okada M., Huston C.D., Mann B.J., Petri Jr. W.A., Kita K., and Nozaki T. Proteomic analysis of phagocytosis in the enteric protozoan parasite Entamoeba histolytica. Eukaryot Cell 4 (2005) 827-831
126. Okada M., and Nozaki T. New insights into molecular mechanisms of phagocytosis in Entamoeba histolytica by proteomic analysis. Arch Med Res 37 2 (2006) 244-252
127. Olliaro P., Castelli F., Milano F., Filice G., and Carosi G. Ultrastructure of Plasmodium falciparum "in vitro". I. Base-line for drug effects evaluation. Microbiologica 12 (1989) 7-14
128. Orozco E., Guarneros G., Martinez-Palomo A., and Sanchez T. Entamoeba histolytica. Phagocytosis as a virulence factor. J Exp Med 158 (1983) 1511-1521
129. Orth J.D., Krueger E.W., Weller S.G., and McNiven M.A. A novel endocytic mechanism of epidermal growth factor receptor sequestration and internalization. Cancer Res 66 (2006) 3603-3610
130. Overath P., and Engstler M. Endocytosis, membrane recycling and sorting of GPI-anchored proteins: Trypanosoma brucei as a model system. Mol Microbiol 53 (2004) 735-744
131. Pal A., Hall B.S., Nesbeth D.N., Field H.I., and Field M.C. Differential endocytic functions of Trypanosoma brucei Rab5 isoforms reveal a glycosylphosphatidylinositol-specific endosomal pathway. J Biol Chem 277 (2002) 9529-9539
132. Parton R.G., and Simons K. The multiple faces of caveolae. Nat Rev Mol Cell Biol 8 (2007) 185-194
133. Parussini F., Garcia M., Mucci J., Aguero F., Sanchez D., Hellman U., et al. Characterization of a lysosomal serine carboxypeptidase from Trypanosoma cruzi. Mol Biochem Parasitol 131 (2003) 11-23
134. Peck R.F., Shiflett A.M., Schwartz K.J., McCann A., Hajduk S.L., and Bangs J.D. The LAMP-like protein p67 plays an essential role in the lysosome of African trypanosomes. Mol Microbiol 68 (2008) 933-946
135. Pereira-Neves A., and Benchimol M. Phagocytosis by Trichomonas vaginalis: new insights. Biol Cell 99 (2007) 87-101
136. Peterson K.M., and Alderete J.F. Selective acquisition of plasma proteins by Trichomonas vaginalis and human lipoproteins as a growth requirement for this species. Mol Biochem Parasitol 12 (1984) 37-48
137. Peterson K.M., and Alderete J.F. Iron uptake and increased intracellular enzyme activity follow host lactoferrin binding by Trichomonas vaginalis receptors. J Exp Med 160 (1984) 398-410
138. Pimenta P.F., de Souza W., Souto-Padron T., and Pinto da Silva P. The cell surface of Trypanosoma cruzi: a fracture-flip, replica-staining label-fracture survey. Eur J Cell Biol 50 (1989) 263-271
139. Porto-Carreiro I., Attias M., Miranda K., De Souza W., and Cunha-e-Silva N. Trypanosoma cruzi epimastigote endocytic pathway: cargo enters the cytostome and passes through an early endosomal network before storage in reservosomes. Eur J Cell Biol 79 (2000) 858-869
140. Pupkis M.F., Tetley L., and Coombs G.H. Leishmania mexicana: amastigote hydrolases in unusual lysosomes. Exp Parasitol 62 (1986) 29-39
141. Ravdin J.I. Immunobiology of human infection by Entamoeba histolytica. Pathol Immunopathol Res 8 (1989) 179-205
142. Rendon-Maldonado J.G., Espinosa-Cantellano M., Gonzalez-Robles A., and Martinez-Palomo A. Trichomonas vaginalis: in vitro phagocytosis of lactobacilli, vaginal epithelial cells, leukocytes, and erythrocytes. Exp Parasitol 89 (1998) 241-250
143. Rodriguez M.A., and Orozco E. Characterization of the EhRabB recombinant protein of Entamoeba histolytica. Arch Med Res 31 (2000) S171-S172
144. Rudzinska M.A., Trager W., and Bray R.S. Pinocytotic uptake and the digestion of hemoglobin in malaria parasites. J Protozool 12 (1965) 563-576
145. Sahasrabuddhe A.A., Bajpai V.K., and Gupta C.M. A novel form of actin in Leishmania: molecular characterisation, subcellular localisation and association with subpellicular microtubules. Mol Biochem Parasitol 134 (2004) 105-114
146. Sahoo N., Labruyere E., Bhattacharya S., Sen P., Guillen N., and Bhattacharya A. Calcium binding protein 1 of the protozoan parasite Entamoeba histolytica interacts with actin and is involved in cytoskeleton dynamics. J Cell Sci 117 (2004) 3625-3634
147. Saito-Nakano Y., Loftus B.J., Hall N., and Nozaki T. The diversity of Rab GTPases in Entamoeba histolytica. Exp Parasitol 110 (2005) 244-252
148. Saito-Nakano Y., Mitra B.N., Nakada-Tsukui K., Sato D., and Nozaki T. Two Rab7 isotypes, EhRab7A and EhRab7B, play distinct roles in biogenesis of lysosomes and phagosomes in the enteric protozoan parasite Entamoeba histolytica. Cell Microbiol 9 (2007) 1796-1808
149. Saito-Nakano Y., Yasuda T., Nakada-Tsukui K., Leippe M., and Nozaki T. Rab5-associated vacuoles play a unique role in phagocytosis of the enteric protozoan parasite Entamoeba histolytica. J Biol Chem 279 (2004) 49497-49507
150. Saksena S., Sun J., Chu T., and Emr S.D. ESCRTing proteins in the endocytic pathway. Trends Biochem Sci 32 (2007) 561-573
151. Saliba K.J., and Kirk K. Nutrient acquisition by intracellular apicomplexan parasites: staying in for dinner. Int J Parasitol 31 (2001) 1321-1330
152. Sandvig K., Torgersen M.L., Raa H.A., and van Deurs B. Clathrin-independent endocytosis: from nonexisting to an extreme degree of complexity. Histochem Cell Biol 129 (2008) 267-276
153. Sant'Anna C., De Souza W., and Cunha-e-Silva N. Biogenesis of the reservosomes of Trypanosoma cruzi. Microsc Microanal 10 (2004) 637-646
154. Sant'Anna C., Pereira M.G., Lemgruber L., de Souza W., and Cunha e Silva N.L. New insights into the morphology of Trypanosoma cruzi reservosome. Microsc Res Tech 71 (2008) 599-605
155. Sant'Anna C., Parussini F., Lourenço D., de Souza W., Cazzulo J.J., and Cunha-E-Silva N.L. All Trypanosoma cruzi developmental forms present lysosome-related organelles. Histochem Cell Biol 130 (2008) 1187-1198
156. Sant'Anna C, Nakayasu ES, Pereira MG, Lourenço D, De Souza W, Almeida IC, et al. Subcellular proteomics of Trypanosoma cruzi reservosomes. Proteomics 2009; in press, doi:10.1002/pmic.200800730.
157. Santos C.C., Sant'Anna C., Terres A., Cunha-e-Silva N.L., Scharfstein J., and de A.L.A.P. Chagasin, the endogenous cysteine-protease inhibitor of Trypanosoma cruzi, modulates parasite differentiation and invasion of mammalian cells. J Cell Sci 118 (2005) 901-915
158. Schmunis G.A., and Cruz J.R. Safety of the blood supply in Latin America. Clin Microbiol Rev 18 (2005) 12-29
159. Scholtyseck E., Teras J., Kasakova I., and Sethi K.K. Electron microscope observations on the interaction of Mycoplasma fermentans with Trichomonas vaginalis. Z Parasitenkd 71 (1985) 435-442
160. Schuler H., Mueller A.K., and Matuschewski K. Unusual properties of Plasmodium falciparum actin: new insights into microfilament dynamics of apicomplexan parasites. FEBS Lett 579 (2005) 655-660
161. Singh S.B., Tandon R., Krishnamurthy G., Vikram R., Sharma N., Basu S.K., et al. Rab5-mediated endosome-endosome fusion regulates hemoglobin endocytosis in Leishmania donovani. EMBO J 22 (2003) 5712-5722
162. Slomianny C. Three-dimensional reconstruction of the feeding process of the malaria parasite. Blood Cells 16 (1990) 369-378
163. Smythe W.A., Joiner K.A., and Hoppe H.C. Actin is required for endocytic trafficking in the malaria parasite Plasmodium falciparum. Cell Microbiol 10 (2008) 452-464
164. Soares M.J., and De Souza W. Cytoplasmic organelles of trypanosomatids: a cytochemical and stereological study. J Submicrosc Cytol Pathol 20 (1988) 349-361
165. Soares M.J., and De Souza W. Endocytosis of gold-labeled proteins and LDL by Trypanosoma cruzi. Parasitol Res 77 (1991) 461-468
166. Soares M.J., Souto-Padron T., Bonaldo M.C., Goldenberg S., and de Souza W. A stereological study of the differentiation process in Trypanosoma cruzi. Parasitol Res 75 (1989) 522-527
167. Soares M.J., Souto-Padron T., and De Souza W. Identification of a large pre-lysosomal compartment in the pathogenic protozoon Trypanosoma cruzi. J Cell Sci 102 (1992) 157-167
168. Souto-Padron T., Campetella O.E., Cazzulo J.J., and de Souza W. Cysteine proteinase in Trypanosoma cruzi: immunocytochemical localization and involvement in parasite-host cell interaction. J Cell Sci 96 (1990) 485-490
169. Steverding D., Stierhof Y.D., Chaudhri M., Ligtenberg M., Schell D., Beck-Sickinger A.G., et al. ESAG 6 and 7 products of Trypanosoma brucei form a transferrin binding protein complex. Eur J Cell Biol 64 (1994) 78-87
170. Street D.A., Wells C., Taylor-Robinson D., and Ackers J.P. Interaction between Trichomonas vaginalis and other pathogenic micro-organisms of the human genital tract. Br J Vener Dis 60 (1984) 31-38
171. Tai J.H., Ong S.J., Chang S.C., and Su H.M. Giardiavirus enters Giardia lamblia WB trophozoite via endocytosis. Exp Parasitol 76 (1993) 165-174
172. Taraschi T.F., Trelka D., Schneider T., and Matthews I. Plasmodium falciparum: characterization of organelle migration during merozoite morphogenesis in asexual malaria infections. Exp Parasitol 88 (1998) 184-193
173. Temesvari L.A., Harris E.N., Stanley Jr. S.L., and Cardelli J.A. Early and late endosomal compartments of Entamoeba histolytica are enriched in cysteine proteases, acid phosphatase and several Ras-related Rab GTPases. Mol Biochem Parasitol 103 (1999) 225-241
174. Torres C., Perez-Victoria F.J., Parodi-Talice A., Castanys S., and Gamarro F. Characterization of an ABCA-like transporter involved in vesicular trafficking in the protozoan parasite Trypanosoma cruzi. Mol Microbiol 54 (2004) 632-646
175. Touz M.C., Kulakova L., and Nash T.E. Adaptor protein complex 1 mediates the transport of lysosomal proteins from a Golgi-like organelle to peripheral vacuoles in the primitive eukaryote Giardia lamblia. Mol Biol Cell 15 (2004) 3053-3060
176. Touz M.C., Lujan H.D., Hayes S.F., and Nash T.E. Sorting of encystation-specific cysteine protease to lysosome-like peripheral vacuoles in Giardia lamblia requires a conserved tyrosine-based motif. J Biol Chem 278 (2003) 6420-6426
177. Trager W. Living together. The biology of animal parasitism (1986), Plenum Press, New York
178. Traub-Cseko Y.M., Duboise M., Boukai L.K., and McMahon-Pratt D. Identification of two distinct cysteine proteinase genes of Leishmania pifanoi axenic amastigotes using the polymerase chain reaction. Mol Biochem Parasitol 57 (1993) 101-115
179. Tsutsumi V., Ramirez-Rosales A., Lanz-Mendoza H., Shibayama M., Chavez B., Rangel-Lopez E., et al. Entamoeba histolytica: erythrophagocytosis, collagenolysis, and liver abscess production as virulence markers. Trans R Soc Trop Med Hyg 86 (1992) 170-172
180. Ueda-Nakamura T., Attias M., and de Souza W. Megasome biogenesis in Leishmania amazonensis: a morphometric and cytochemical study. Parasitol Res 87 (2001) 89-97
181. Ueda-Nakamura T., Attias M., and de Souza W. Comparative analysis of megasomes in members of Leishmania mexicana complex. Res Microbiol 158 (2007) 456-462
182. Ueda-Nakamura T., da Conceicao Rocha Sampaio M., Cunha-e-Silva N.L., Traub-Cseko Y.M., and de Souza W. Expression and processing of megasome cysteine proteinases during Leishmania amazonensis differentiation. Parasitol Res 88 (2002) 332-337
183. Van Meel E., and Klumperman J. Imaging and imagination: understanding the endo-lysosomal system. Histochem Cell Biol 129 (2008) 253-266
184. Vargas M., Voigt H., Sansonetti P., and Guillen N. Molecular characterization of myosin IB from the lower eukaryote Entamoeba histolytica, a human parasite. Mol Biochem Parasitol 86 (1997) 61-73
185. Vatarunakamura C., Ueda-Nakamura T., and de Souza W. Visualization of the cytostome in Trypanosoma cruzi by high resolution field emission scanning electron microscopy using secondary and backscattered electron imaging. FEMS Microbiol Lett 242 (2005) 227-230
186. Vieira M., Rohloff P., Luo S., Cunha-e-Silva N.L., de Souza W., and Docampo R. Role for a P-type H+-ATPase in the acidification of the endocytic pathway of Trypanosoma cruzi. Biochem J 392 (2005) 467-474
187. Voigt H., Olivo J.C., Sansonetti P., and Guillen N. Myosin IB from Entamoeba histolytica is involved in phagocytosis of human erythrocytes. J Cell Sci 112 Pt 8 (1999) 1191-1201
188. Voyiatzaki C.S., and Soteriadou K.P. Identification and isolation of the Leishmania transferrin receptor. J Biol Chem 267 (1992) 9112-9117
189. Waller R.F., and McConville M.J. Developmental changes in lysosome morphology and function Leishmania parasites. Int J Parasitol 32 (2002) 1435-1445
190. Webster P. Endocytosis by African trypanosomes. I. Three-dimensional structure of the endocytic organelles in Trypanosoma brucei and T. congolense. Eur J Cell Biol 49 (1989) 295-302
191. Webster P., and Fish W.R. Endocytosis by African trypanosomes. II. Occurrence in different life-cycle stages and intracellular sorting. Eur J Cell Biol 49 (1989) 303-310
192. Weise F., Stierhof Y.D., Kuhn C., Wiese M., and Overath P. Distribution of GPI-anchored proteins in the protozoan parasite Leishmania, based on an improved ultrastructural description using high-pressure frozen cells. J Cell Sci 113 (2000) 4587-4603
193. Welsh C.F., and Assoian R.K. A growing role for Rho family GTPases as intermediaries in growth factor- and adhesion-dependent cell cycle progression. Biochim Biophys Acta 1471 (2000) M21-M29
194. Welter B.H., Powell R.R., Laughlin R.C., McGugan G.C., Bonner M., King A., et al. Entamoeba histolytica: comparison of the role of receptors and filamentous actin among various endocytic processes. Exp Parasitol 113 (2006) 91-99
195. WHO. Control of Chagas disease. WHO Tech Series vol. 811, Geneva, 1991. p. 1-95.