An historical perspective on how advances in microscopic imaging contributed to understanding the leishmania Spp. and trypanosoma cruzi host-parasite relationship

BioMed Research International

Volumn 2014, Issue , 2014, Pages

  Florentino, P T V ^a   Real, F ^a   Bonfim Melo, A ^a   Orikaza, C M ^a   Ferreira, E R ^a   Pessoa, C C ^a   Lima, B R ^a   Sasso, G R S ^a   Mortara, R A ^a  

^a FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

[No Author keywords available]

Indexed keywords

AMASTIGOTE; ANTIBODY LABELING; CELL MIGRATION; CELL VACUOLE; CHAGAS DISEASE; CYTOPLASM; EXOCYTOSIS; HOST CELL; HOST PARASITE INTERACTION; HUMAN; IMMUNOFLUORESCENCE; IN VITRO STUDY; IN VIVO STUDY; INTERNALIZATION; KINETOPLASTID LIFE CYCLE STAGE; LEISHMANIA; LEISHMANIA DONOVANI; LEISHMANIA MAJOR; LEISHMANIA MEXICANA; LEISHMANIASIS; LEPROSY; LYSOSOME; MACROPHAGE; MICROSCOPY; NEUTROPHIL; NONHUMAN; PARASITE SURVIVAL; PARASITOPHOROUS VACUOLE; PHAGOCYTOSIS; PHAGOLYSOSOME; PHLEBOTOMUS; PROMASTIGOTE; REVIEW; SCANNING ELECTRON MICROSCOPY; SPERMATOZOON PENETRATION; TRANSMISSION ELECTRON MICROSCOPY; TRYPANOSOMA CRUZI; TRYPOMASTIGOTE; ANIMAL; PATHOLOGY; PHYSIOLOGY;

ANIMALS; CHAGAS DISEASE; HOST-PARASITE INTERACTIONS; HUMANS; LEISHMANIA; LEISHMANIASIS; MICROSCOPY; TRYPANOSOMA CRUZI;

EID: 84901283552     PISSN: 23146133     EISSN: 23146141     Source Type: Journal    
DOI: 10.1155/2014/565291     Document Type: Review

References (118)

1. Moreira D., López-García P., Vickerman K., An updated view of kinetoplastid phylogeny using environmental sequences and a closer outgroup: proposal for a new classification of the class Kinetoplastea. International Journal of Systematic and Evolutionary Microbiology 2004 54 5 1861 1875 2-s2.0-3242883348 10.1099/ijs.0.63081-0 (Pubitemid 39360009)
2. Stuart K., Brun R., Croft S., Fairlamb A., Gürtler R. E., McKerrow J., Reed S., Tarleton R., Kinetoplastids: related protozoan pathogens, different diseases. Journal of Clinical Investigation 2008 118 4 1301 1310 2-s2.0-41849094126 10.1172/JCI33945 (Pubitemid 351500422)
3. de Souza W., de Carvalho T. M. U., Barrias E. S., Review on Trypanosoma cruzi: host cell interaction. International Journal of Cell Biology 2010 2010 18 2-s2.0-77956868508 10.1155/2010/295394 295394
4. Rosenberger R., A case study in the applied philosophy of imaging: the synaptic vesicle debate. Science Technology and Human Values 2011 36 1 6 32 2-s2.0-78649701501 10.1177/0162243909337117
5. Boxenbaum H., Time concepts in physics, biology, and pharmacokinetics. Journal of Pharmaceutical Sciences 1986 75 11 1053 1062 2-s2.0-0022975813 (Pubitemid 17216549)
6. Mayr E., Cause and effect in biology-kinds of causes, predictability, and teleology are viewed by a practicing biologist. Science 1961 134 1501
7. Egaña Aranguren M., Wolstencroft K., Sattler U., Drummond N., Horridge M., Rector A., Stevens R., Using OWL to model biological knowledge. International Journal of Human Computer Studies 2007 65 7 583 594 2-s2.0-34249019488 10.1016/j.ijhcs.2007.03.006 (Pubitemid 46803278)
8. Ahn A. C., Tewari M., Poon C.-S., Phillips R. S., The limits of reductionism in medicine: could systems biology offer an alternative? PLoS Medicine 2006 3 6 709 713 2-s2.0-33745588546 10.1371/journal.pmed.0030208 (Pubitemid 43987803)
9. Sattler R., Biophilosophy: Analytic and Holistic Perspectives 1986 Berlin, Germany Springer
10. Milestones in light microscopy. Nature Cell Biology 2009 11 1165 1165
11. Xiao G. Q., Corle T. R., Kino G. S., Real-time confocal scanning optical microscope. Applied Physics Letters 1988 53 8 716 718 2-s2.0-36549092409 10.1063/1.99814
12. Landecker H., Seeing things: from microcinematography to live cell imaging. Nature Methods 2009 6 10 707 709 2-s2.0-70349629400 10.1038/nmeth1009-707
13. Lofgren R., The structure of Leishmania tropica as revealed by phase and electron microscopy. Journal of Bacteriology 1950 60 617 625
14. Mortara R. A., Differential interference contrast and confocal fluorescence photomicrograph showing the distribution of the 35/50 kDa surface glycoconjugate of Trypanosoma cruzi trypomastigotes during invasion of HeLa cells. Memórias do Instituto Oswaldo Cruz 1991 86 supplement 1 1
15. Schenkman S., Ferguson M. A. J., Heise N., Cardoso de Almeida M. L., Mortara R. A., Yoshida N., Mucin-like glycoproteins linked to the membrane by glycosylphosphatidylinositol anchor are the major acceptors of sialic acid in a reaction catalyzed by trans-sialidase in metacyclic forms of Trypanosoma cruzi. Molecular and Biochemical Parasitology 1993 59 2 293 304 2-s2.0-0027192912 10.1016/0166-6851(93)90227-O
16. Fernandes M. C., de Andrade L. R., Andrews N. W., Mortara R. A., Trypanosoma cruzi trypomastigotes induce cytoskeleton modifications during hela cell invasion. Memórias do Instituto Oswaldo Cruz 2011 106 8 1014 1016 2-s2.0-84855506399 10.1590/S0074-02762011000800019
17. Sant'Anna C., Campanati L., Gadelha C., Lourenço D., Labati-Terra L., Bittencourt-Silvestre J., Benchimol M., Cunha-e-Silva N. L., De Souza W., Improvement on the visualization of cytoskeletal structures of protozoan parasites using high-resolution field emission scanning electron microscopy (FESEM). Histochemistry and Cell Biology 2005 124 1 87 95 2-s2.0-24344451709 10.1007/s00418-005-0786-1 (Pubitemid 41253166)
18. Gaudet D. A., Kokko E. G., Application of scanning electron microscopy to paraffin-embedded plant tissues to study invasive process of plant-pathogenic fungi. Phytopathology 1984 74 3
19. Geissinger H. D., Correlated light optical and scanning electron microscopy of Gram smears of bacteria and paraffin sections of cardiac muscle. Journal of Microscopy 1971 93 2 109 117 2-s2.0-0015051687
20. Wergin W. P., Yaklich R. W., Roy S., Joy D. C., Erbe E. F., Murphy C. A., Pooley C. D., Imaging thin and thick sections of biological tissue with the secondary electron detector in a field-emission scanning electron microscope. Scanning 1997 19 6 386 395 2-s2.0-0031228966
21. Russell S. D., Daghlian C. P., Scanning electron microscopic observations on deembedded biological tissue sections: comparison of different fixatives and embedding materials. Journal of Electron Microscopy Technique 1985 2 5 489 495 2-s2.0-0021797318 (Pubitemid 15047998)
22. Lainson R., Shaw J. J., Evolution, Classification and Geographical Distribution 1987 San Diego, Calif, USA Academic Press W. Peters, R. Killick-Kendrick, Eds.
23. Altamirano-Enciso A. J., Marzochi M. C. A., Moreira J. S., Schubach A. O., Marzochi K. B. F., On the origin and spread of cutaneous and mucosal leishmaniasis, based on pre- and post- colombian historical source. História Ciências Saúde, Manguinhos, 2003 10 3 852 882 2-s2.0-1642379665
24. Dedet J.-P., Edmond Sergent's discoveries on the vectorial transmission of agents of human and animal infectious diseases. Bulletin de la Societé de Pathologie Exotique 2007 100 2 147 150 2-s2.0-34547359054
25. Théodoridès J., Historical note on the discovery of the transmission of cutaneous leishmaniasis by phlebotomes. Bulletin de la Societé de Pathologie Exotique 1997 90 3 177 178 2-s2.0-0030630895 (Pubitemid 127368082)
26. Wright J. H., Protozoa in a case of tropical ulcer ("Delhi Sore"). Journal of Medical Research 1903 10 472 482
27. Christophers S. R., On a parasite found in persons suffering from enlargement of the spleen in India. Second Report 1904 Calcutta, India Office of the Superintendent of Government Printing
28. Heyneman D., Immunology of leishmaniasis. Bulletin of the World Health Organization 1971 44 4 499 514 2-s2.0-0015188394
29. Ueno N., Wilson M. E., Receptor-mediated phagocytosis of Leishmania: implications for intracellular survival. Trends in Parasitology 2012 28 335 344
30. Pulvertaft R. J. V., Hoyle G. F., Stages in the life-cycle of Leishmania donovani. Transactions of the Royal Society of Tropical Medicine and Hygiene 1960 54 2 191 196 2-s2.0-0000029582
31. Miller H. C., Twohy D. W., Infection of macrophages in culture by leptomonads of Leishmania donovani. The Journal of Protozoology 1967 14 4 781 789 2-s2.0-0014145603
32. Akiyama H. J., Haight R. D., Interaction of Leishmania donovani and hamster peritoneal macrophages. A phase-contrast microscopical study. American Journal of Tropical Medicine and Hygiene 1971 20 4 539 545 2-s2.0-0015090828
33. Forestier C.-L., MacHu C., Loussert C., Pescher P., Späth G. F., Imaging host cell- Leishmania interaction dynamics implicates parasite motility, lysosome recruitment, and host cell wounding in the infection process. Cell Host and Microbe 2011 9 4 319 330 2-s2.0-79955055147 10.1016/j.chom.2011.03.011
34. Courret N., Fréhel C., Gouhier N., Pouchelet M., Prina E., Roux P., Antoine J.-C., Biogenesis of Leishmania -harbouring parasitophorus vacuoles following phagocytosis of the metacyclic promastigote or amastigote stages of the parasites. Journal of Cell Science 2002 115 11 2303 2316 2-s2.0-0036591962 (Pubitemid 34752974)
35. Aikawa M., Hendricks L. D., Ito Y., Jagusiak M., Interactions between macrophagelike cells and Leishmania braziliensis in vitro. American Journal of Pathology 1982 108 1 50 59 2-s2.0-0019946649 (Pubitemid 12090418)
36. Blackwell J. M., Plant J. E., Expression of the natural resistance gene (Lsh) in wild mice infected experimentally with Leishmania donovani or Salmonella typhimurium. Current topics in Microbiology and Immunology 1986 127 323 330 2-s2.0-0022522536
37. Love D. C., Kane M. M., Mosser D. M., Leishmania amazonensis: the phagocytosis of amastigotes by macrophages. Experimental Parasitology 1998 88 3 161 171 2-s2.0-0032030470 10.1006/expr.1998.4232 (Pubitemid 28375783)
38. Coling D., Kachar B., Theory and application of fluorescence microscopy. Current Protocols in Neuroscience 2001 2 Unit 2.1 2-s2.0-45549106079
39. Lodge R., Descoteaux A., Leishmania donovani promastigotes induce periphagosomal F-actin accumulation through retention of the GTPase Cdc42. Cellular Microbiology 2005 7 11 1647 1658 2-s2.0-27244452734 10.1111/j.1462-5822.2005.00582.x (Pubitemid 41511921)
40. Lodge R., Descoteaux A., Phagocytosis of Leishmania donovani amastigotes is Rac1 dependent and occurs in the absence of NADPH oxidase activation. European Journal of Immunology 2006 36 10 2735 2744 2-s2.0-33750224426 10.1002/eji.200636089 (Pubitemid 44608457)
41. Alexander J., Vickerman K., Fusion of host cell secondary lysosomes with the parasitophorous vacuoles of Leishmania mexicana infected macrophages. The Journal of Protozoology 1975 22 4 502 508 2-s2.0-0016754011
42. Chang K. P., Dwyer D. M., Leishmania donovani. Hamster macrophage interactions in vitro: cell entry, intracellular survival, and multiplication of amastigotes. Journal of Experimental Medicine 1978 147 2 515 530 2-s2.0-0017851048 (Pubitemid 8284122)
43. Antoine J.-C., Prina E., Lang T., Courret N., The biogenesis and properties of the parasitophorous vacuoles that harbour Leishmania in murine macrophages. Trends in Microbiology 1998 6 10 392 401 2-s2.0-0031793544 10.1016/S0966-842X(98)01324-9 (Pubitemid 28515691)
44. Prina E., Antoine Cl. J., Localization and activity of various lysosomal proteases in rat macrophages infected with Leishmania amazonensis. Pathologie Biologie 1990 38 10 1020 1022 2-s2.0-0025610357
45. Antoine J.-C., Prina E., Jouanne C., Bongrand P., Parasitophorous vacuoles of Leishmania amazonensis -infected macrophages maintain an acidic pH. Infection and Immunity 1990 58 3 779 787 2-s2.0-0025098455 (Pubitemid 20072645)
46. Lang T., de Chastellier C., Frehel C., Hellio R., Metezeau P., de Souza Leao S., Antoine J.-C., Distribution of MHC class I and of MHC class II molecules in macrophages infected with Leishmania amazonensis. Journal of Cell Science 1994 107 1 69 82 2-s2.0-0028118905 (Pubitemid 24039035)
47. Handman E., Bullen D. V., Interaction of Leishmania with the host macrophage. Trends in Parasitology 2002 18 332 334
48. Real F., Mortara R. A., The diverse and dynamic nature of Leishmania parasitophorous vacuoles studied by multidimensional imaging. PLoS Neglected Tropical Diseases 2012 6 2 2-s2.0-84857894258 10.1371/journal.pntd.0001518 e1518
49. Lang T., Lecoeur H., Prina E., Imaging Leishmania development in their host cells. Trends in Parasitology 2009 25 10 464 473 2-s2.0-70149112325 10.1016/j.pt.2009.07.006
50. Lippuner C., Paape D., Paterou A., Brand J., Richardson M., Smith A. J., Hoffmann K., Brinkmann V., Blackburn C., Aebischer T., Real-time imaging of Leishmania mexicana -infected early phagosomes: a study using primary macrophages generated from green fluorescent protein-Rab5 transgenic mice. FASEB Journal 2009 23 2 483 491 2-s2.0-59649108312 10.1096/fj.08-108712
51. Ridley D. S., A histological classification of cutaneous leishmaniasis and its geographical expression. Transactions of the Royal Society of Tropical Medicine and Hygiene 1980 74 4 515 521 2-s2.0-0019244306
52. Rittig M. G., Schröppel K., Seack K.-H., Sander U., N'Diaye E.-N., Maridonneau-Parini I., Solbach W., Bogdan C., Coiling phagocytosis of trypanosomatids and fungal cells. Infection and Immunity 1998 66 9 4331 4339 2-s2.0-0031662362 (Pubitemid 28402709)
53. Rittig M. G., Bogdan C., Leishmania -host-cell interaction: complexities and alternative views. Parasitology Today 2000 16 7 292 297 2-s2.0-0034235989 10.1016/S0169-4758(00)01692-6 (Pubitemid 30447394)
54. Peters N. C., Egen J. G., Secundino N., Debrabant A., Kimblin N., Kamhawi S., Lawyer P., Fay M. P., Germain R. N., Sacks D., In vivo imaging reveals an essential role for neutrophils in leishmaniasis transmitted by sand flies. Science 2008 321 5891 970 974 2-s2.0-49649116869 10.1126/science.1159194
55. Ng L. G., Hsu A., Mandell M. A., Roediger B., Hoeller C., Mrass P., Iparraguirre A., Cavanagh L. L., Triccas J. A., Beverley S. M., Scott P., Weninger W., Migratory dermal dendritic cells act as rapid sensors of protozoan parasites. PLoS Pathogens 2008 4 11 e1000222 2-s2.0-58949102426 10.1371/journal.ppat.1000222
56. Gueirard P., Laplante A., Rondeau C., Milon G., Desjardins M., Trafficking of Leishmania donovani promastigotes in non-lytic compartments in neutrophils enables the subsequent transfer of parasites to macrophages. Cellular Microbiology 2008 10 1 100 111 2-s2.0-36949038761 10.1111/j.1462-5822. 2007.01018.x (Pubitemid 350239059)
57. Chagas C., Nova tripanozomiaze humana: estudos sobre a morfolojia e o ciclo evolutivo do Schizotrypanum cruzi n. gen., n. sp., ajente etiolojico de nova entidade morbida do homem. Memórias do Instituto Oswaldo Cruz 1909 1 159 218
58. Vianna G., Contribuição para o estudo da anatomia patolójica da "Moléstia de Carlos Chagas" (Esquizotripanose humana ou tireoidite parasitária). Memórias do Instituto Oswaldo Cruz 1911 3 276 293
59. Dias E., Estudos sobre o Schizotrypanum cruzi. Memórias Do Instituto Oswaldo Cruz 1934 28 1 110
60. Villela E., Torres C. M., Histopathology of the central nervous system in experimental paralysis caused by Schizotrypanum cruzi. Memórias do Instituto Oswaldo Cruz 1926 19 199 221
61. Romaña C., Meyer H., Estudo do ciclo evolutivo do, " Schizotrypanum cruzi " em cultura de tecidos de embrião de galinha. Memórias do Instituto Oswaldo Cruz 1942 37 19 27
62. Kofoid C. A., Wood F. D., McNeil E. C. E., The Cycle of Trypanosoma Cruzi in Tissue Culture of Embryonic Heart Muscle 1935 Berkeley, Calif, USA University of California Press
63. Brener Z., Biology of Trypanosoma cruzi. Annual Review of Microbiology 1973 27 347 382 2-s2.0-0015869325
64. Meyer H., Barasa A., Life cycle of Schizotrypanum cruzi in tissue cultures., http://www.itarget.com.br/newclients/sbpz.org.br/2011/extra/download/ cruzi1.mpg
65. Meyer H., Porter K. R., A study of Trypanosoma cruzi with the electron microscope. Parasitology 1954 44 1-2 16 23 2-s2.0-0347141731
66. de Souza W., Electron microscopy of trypanosomes-a historical view. Memórias do Instituto Oswaldo Cruz 2008 103 4 313 325 2-s2.0-47749142812 (Pubitemid 352026434)
67. Dvorak J. A., Hyde T. P., Trypanosoma cruzi: interaction with vertebrate cells in vitro. I. Individual interactions at the cellular and subcellular levels. Experimental Parasitology 1973 34 2 268 283 2-s2.0-0015812731
68. Ferreira E. R., Bonfim-Melo A., Mortara R. A., Bahia D., Trypanosoma cruzi extracellular amastigotes and host cell signaling: more pieces to the puzzle. Frontiers in Immunology 2012 3 363
69. Ley V., Andrews N. W., Robbins E. S., Nussenzweig V., Amastigotes of Trypanosoma cruzi sustain an infective cycle in mammalian cells. Journal of Experimental Medicine 1988 168 2 649 659 2-s2.0-0023713907
70. Lima F. M., Oliveira P., Mortara R. A., Silveira J. F., Bahia D., The challenge of Chagas' disease: has the human pathogen, Trypanosoma cruzi, learned how to modulate signaling events to subvert host cells? New Biotechnology 2010 27 6 837 843 2-s2.0-78649705427 10.1016/j.nbt.2010.02.003
71. Mortara R. A., Andreoli W. K., Tantwaki N. N., Fernandes A. B., Da Silva C. V., Fernandes M. C. D. C., L'Abbate C., Da Silva S., Mammalian cell invasion and intracellular trafficking by Trypanosoma cruzi infective forms. Anais da Academia Brasileira de Ciencias 2005 77 1 77 94 2-s2.0-13444269327 (Pubitemid 40217358)
72. Tomlinson S., Vandekerckhove F., Frevert U., Nussenzweig V., The induction of Trypanosoma cruzi trypomastigote to amastigote transformation by low pH. Parasitology 1995 110 5 547 554 2-s2.0-0029064551
73. Nogueira N., Cohn Z., Trypanosoma cruzi: mechanism of entry and intracellular fate in mammalian cells. Journal of Experimental Medicine 1976 143 6 1402 1420 2-s2.0-0017075718
74. Behbehani K., Developmental cycles of Trypanosoma (Schizotrypanum) cruzi (Chagas, 1909) in mouse peritoneal macrophages in vitro. Parasitology 1973 66 2 343 353 2-s2.0-0015613243
75. Hudson L., Snary D., Morgan S. J., Trypanosoma cruzi: continuous cultivation with murine cell lines. Parasitology 1984 88 283 294 2-s2.0-18544410313
76. Chia-Tung Pan S., Trypanosoma cruzi: in vitro interactions between cultured amastigotes and human skin-muscle cells. Experimental Parasitology 1978 45 2 274 286 2-s2.0-0018083134 (Pubitemid 9011014)
77. Schenkman S., Andrews N. W., Nussenzweig V., Robbins E. S., Trypanosoma cruzi invade a mammalian epithelial cell in a polarized manner. Cell 1988 55 1 157 165 2-s2.0-0024280880
78. Mortara R. A., Trypanosoma cruzi: amastigotes and trypomastigotes interact with different structures on the surface of HeLa cells. Experimental Parasitology 1991 73 1 1 14 2-s2.0-0026199373 10.1016/0014-4894(91)90002-E
79. Schenkman S., Mortara R. A., HeLa cells extend and internalize pseudopodia during active invasion by Trypanosoma cruzi trypomastigotes. Journal of Cell Science 1992 101 4 895 905 2-s2.0-0026577038
80. Procópio D. O., da Silva S., Cunningham C. C., Mortara R. A., Trypanosoma cruzi: effect of protein kinase inhibitors and cytoskeletal protein organization and expression on host cell invasion by amastigotes and metacyclic trypomastigotes. Experimental Parasitology 1998 90 1 1 13 2-s2.0-0344074602 10.1006/expr.1998.4314 (Pubitemid 28406680)
81. Ferreira D., Cortez M., Atayde V. D., Yoshida N., Actin cytoskeleton-dependent and -independent host cell invasion by Trypanosoma cruzi is mediated by distinct parasite surface molecules. Infection and Immunity 2006 74 10 5522 5528 2-s2.0-33749236269 10.1128/IAI.00518-06 (Pubitemid 44484535)
82. Schenkman S., Robbins E. S., Nussenzweig V., Attachment of Trypanosoma cruzi to mammalian cells requires parasite energy, and invasion can be independent of the target cell cytoskeleton. Infection and Immunity 1991 59 2 645 654 2-s2.0-0025968123
83. Tardieux I., Webster P., Ravesloot J., Boron W., Lunn J. A., Heuser J. E., Andrews N. W., Lysosome recruitment and fusion are early events required for trypanosome invasion of mammalian cells. Cell 1992 71 7 1117 1130 2-s2.0-0027049531 10.1016/S0092-8674(05)80061-3 (Pubitemid 23016547)
84. Fonseca Rosestolato C. T., da Matta Furniel Dutra J., de Souza W., Ulisses de Carvalho T. M., Participation of host cell actin filaments during interaction of trypomastigote forms of Trypanosoma cruzi with host cells. Cell Structure and Function 2002 27 2 91 98 2-s2.0-0036547889 10.1247/csf.27.91 (Pubitemid 34846323)
85. Procópio D. O., Barros H. C., Mortara R. A., Actin-rich structures formed during the invasion of cultured cells by infective forms of Trypanosoma cruzi. European Journal of Cell Biology 1999 78 12 911 924 2-s2.0-0343986396 (Pubitemid 30021272)
86. Fernandes M. C., Flannery A. R., Andrews N., Mortara R. A., Extracellular amastigotes of Trypanosoma cruzi are potent inducers of phagocytosis in mammalian cells. Cellular Microbiology 2013 15 977 991
87. Burleigh B. A., Woolsey A. M., Cell signalling and Trypanosoma cruzi invasion. Cellular Microbiology 2002 4 11 701 711 2-s2.0-0036855862 10.1046/j.1462-5822.2002.00226.x (Pubitemid 35378710)
88. Tam C., Idone V., Devlin C., Fernandes M. C., Flannery A., He X., Schuchman E., Tabas I., Andrews N. W., Exocytosis of acid sphingomyelinase by wounded cells promotes endocytosis and plasma membrane repair. Journal of Cell Biology 2010 189 6 1027 1038 2-s2.0-77953576191 10.1083/jcb.201003053
89. Fernandes M. C., Cortez M., Flannery A. R., Tam C., Mortara R. A., Andrews N. W., Trypanosoma cruzi subverts the sphingomyelinase-mediated plasma membrane repair pathway for cell invasion. Journal of Experimental Medicine 2011 208 5 909 921 2-s2.0-79956075012 10.1084/jem.20102518
90. Woolsey A. M., Sunwoo L., Petersen C. A., Brachmann S. M., Cantley L. C., Burleigh B. A., Novel Pl 3-kinase-dependent mechanisms of trypanosome invasion and vacuole maturation. Journal of Cell Science 2003 116 17 3611 3622 2-s2.0-0042829418 10.1242/jcs.00666 (Pubitemid 37063404)
91. Barrias E. S., Reignault L. C., de Souza W., Carvalho T. M., Trypanosoma cruzi uses macropinocytosis as an additional entry pathway into mammalian host cell. Microbes and Infection 2012 14 1340 1351
92. Andrade L. O., Andrews N. W., Lysosomal fusion is essential for the retention of Trypanosoma cruzi inside host cells. Journal of Experimental Medicine 2004 200 9 1135 1143 2-s2.0-8644238313 10.1084/jem.20041408 (Pubitemid 39507053)
93. Caradonna K. L., Burleigh B. A., Mechanisms of host cell invasion by Trypanosoma cruzi. Advances in Parasitology 2011 76 33 61 2-s2.0-80052154495 10.1016/B978-0-12-385895-5.00002-5
94. Tanowitz H., Wittner M., Kress Y., Bloom B., Studies of in vitro infection by Trypanosoma cruzi. I. Ultrastructural studies on the invasion of macrophages and L cells. American Journal of Tropical Medicine and Hygiene 1975 24 1 25 33 2-s2.0-0016433975
95. Ulisses de Carvalho T. M., de Souza W., Early events related with the behaviour of Trypanosoma cruzi within an endocytic vacuole in mouse peritoneal macrophages. Cell Structure and Function 1989 14 4 383 392 2-s2.0-0024419997 (Pubitemid 19245783)
96. de Araújo-Jorge T. C., The biology of Trypanosoma cruzi -macrophage interaction. Memórias do Instituto Oswaldo Cruz 1989 84 4 441 462 2-s2.0-0024748976
97. Rubin-de-Celis S. S. C., Uemura H., Yoshida N., Schenkman S., Expression of trypomastigote trans-sialidase in metacyclic forms of Trypanosoma cruzi increases parasite escape from its parasitophorous vacuole. Cellular Microbiology 2006 8 12 1888 1898 2-s2.0-33750595935 10.1111/j.1462-5822.2006. 00755.x (Pubitemid 44680871)
98. Andrews N. W., Whitlow M. B., Secretion of Trypanosoma cruzi of a hemolysin active at low pH. Molecular and Biochemical Parasitology 1989 33 3 249 256 2-s2.0-0024583847 10.1016/0166-6851(89)90086-8 (Pubitemid 19060261)
99. Andrews N. W., Abrams C. K., Slatin S. L., Griffiths G., A T. cruzi -secreted protein immunologically related to the complement component C9: evidence for membrane pore-forming activity at low pH. Cell 1990 61 7 1277 1287 2-s2.0-0025277577 10.1016/0092-8674(90)90692-8 (Pubitemid 20208832)
100. Moore-Lai D., Rowland E., Discovery and characterization of an antibody, anti-egressin, that is able to inhibit Trypanosoma cruzi egress in vitro. Journal of Parasitology 2004 90 3 524 530 2-s2.0-3142677753 10.1645/GE-145R (Pubitemid 44204179)
101. Wendelken J. L., Rowland E. C., Agglutination of Trypanosoma cruzi in infected cells treated with serum from chronically infected mice. Journal of Parasitology 2009 95 2 337 344 2-s2.0-67651124961 10.1645/GE-1757.1
102. Costales J., Rowland E. C., Human chagasic serum contains antibodies capable of inhibiting Trypanosoma cruzi egress from tissue culture cells. Journal of Parasitology 2005 91 4 950 953 2-s2.0-24944461034 10.1645/GE-429R.1 (Pubitemid 41324783)
103. Costales J., Rowland E. C., A role for protease activity and host-cell permeability during the process of Trypanosoma cruzi egress from infected cells. Journal of Parasitology 2007 93 6 1350 1359 2-s2.0-38849209244 10.1645/GE-1074.1 (Pubitemid 351196652)
104. Coene W., Janssen G., Op de Beeck M., van Dyck D., Phase retrieval through focus variation for ultra-resolution in field-emission transmission electron microscopy. Physical Review Letters 1992 69 26 3743 3746 2-s2.0-0001641367 10.1103/PhysRevLett.69.3743
105. Rocha G. M., Brandão B. A., Mortara R. A., Attias M., de Souza W., Carvalho T. M. U., The flagellar attachment zone of Trypanosoma cruzi epimastigote forms. Journal of Structural Biology 2006 154 1 89 99 2-s2.0-33644998507 10.1016/j.jsb.2005.11.008
106. Zeledón R., Bolaños R., Espejo Navarro M. R., Rojas M., Morphological evidence by scanning electron microscopy of excretion of metacyclic forms of Trypanosoma cruzi in vector's urine. Memorias do Instituto Oswaldo Cruz 1988 83 3 361 365 2-s2.0-0024038818
107. Boker C. A., Schaub G. A., Scanning electron microscopic studies of Trypanosoma cruzi in the rectum of its vector Triatoma infestans. Zeitschrift fur Parasitenkunde 1984 70 4 459 469 2-s2.0-0021136195 (Pubitemid 14060997)
108. Bonaldo M. C., Souto-Padron T., de Souza W., Goldenberg S., Cell-substrate adhesion during Trypanosoma cruzi differentiation. Journal of Cell Biology 1988 106 4 1349 1358 2-s2.0-0023917891
109. Barrias E. S., Dutra J. M. F., de Souza W., Carvalho T. M. U., Participation of macrophage membrane rafts in Trypanosoma cruzi invasion process. Biochemical and Biophysical Research Communications 2007 363 3 828 834 2-s2.0-34948872560 10.1016/j.bbrc.2007.09.068 (Pubitemid 47516712)
110. Mortara R. A., Minelli L. M. S., Vandekerckhove F., Nussenzweig V., Juarez Ramalho-Pinto F., Phosphatidylinositol-specific phospholipase C (PI-PLC) cleavage of GPI-anchored surface molecules of Trypanosoma cruzi triggers in vitro morphological reorganization of trypomastigotes. Journal of Eukaryotic Microbiology 2001 48 1 27 37 2-s2.0-0035123808 (Pubitemid 32180367)
111. Rocha G. M., Miranda K., Weissmüller G., Bisch P. M., de Souza W., Ultrastructure of Trypanosoma cruzi revisited by atomic force microscopy. Microscopy Research and Technique 2008 71 2 133 139 2-s2.0-39449086715 10.1002/jemt.20535 (Pubitemid 351272518)
112. Magno R. C., Lemgruber L., Vommaro R. C., de Souza W., Attias M., Intravacuolar network may act as a mechanical support for Toxoplasma gondii inside the parasitophorous vacuole. Microscopy Research and Technique 2005 67 1 45 52 2-s2.0-22544434016 10.1002/jemt.20182 (Pubitemid 41023207)
113. Flood P. R., Dry-fracturing techniques for the study of soft internal biological tissues in the scanning electron microscope. Scanning Electron Microscopy 1975 2 287 294
114. Cox F. E. G., History of human parasitology. Clinical Microbiology Reviews 2002 15 4 595 612 2-s2.0-0036783078 10.1128/CMR.15.4.595-612.2002 (Pubitemid 41184080)
115. Perleth M., The discovery of Chagas' disease and the formation of the early Chagas' disease concept. History and philosophy of the life sciences 1997 19 2 211 236 2-s2.0-0031300766
116. Köberle F., Chagas' disease and chagas' syndromes: the pathology of American trypanosomiasis. Advances in Parasitology 1968 6 63 116 2-s2.0-0014391262 10.1016/S0065-308X(08)60472-8
117. de la Llave E., Lecoeur H., Besse A., Milon G., Prina E., Lang T., A combined luciferase imaging and reverse transcription polymerase chain reaction assay for the study of Leishmania amastigote burden and correlated mouse tissue transcript fluctuations. Cellular Microbiology 2011 13 1 81 91 2-s2.0-78650293073 10.1111/j.1462-5822.2010.01521.x
118. Goyard S., Dutra P. L., Deolindo P., Autheman D., D'Archivio S., Minoprio P., In vivo imaging of trypanosomes for a better assessment of host-parasite relationships and drug efficacy. Parasitology International 2013 63 260 268