In vivo imaging of malaria parasites - Recent advances and future directions

Current Opinion in Microbiology

Volumn 8, Issue 4, 2005, Pages 407-414

  Amino, Rogerio ^a,b   Ménard, Robert ^a   Frischknecht, Freddy ^a,c  

^a INSTITUT PASTEUR   (France)

^b FEDERAL UNIVERSITY OF SÃO PAULO   (Brazil)

^c UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DISEASE CARRIER; ENVIRONMENT; EPITHELIUM; ERYTHROCYTE; HOST; HOST PARASITE INTERACTION; IMAGING SYSTEM; INTESTINE; MALARIA; MAMMAL; MOSQUITO; NONHUMAN; PLASMODIUM; QUANTITATIVE ANALYSIS; REVIEW; SPECIES INVASION; SPOROZOITE;

ANIMALS; CULICIDAE; ERYTHROCYTES; HOST-PARASITE RELATIONS; HUMANS; INSECT VECTORS; MALARIA; MICROSCOPY, CONFOCAL; PLASMODIUM;

INSECTA; MAMMALIA;

EID: 22544455356     PISSN: 13695274     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mib.2005.06.019     Document Type: Review

References (79)

1. M. Aikawa Parasitological review. Plasmodium: the fine structure of malarial parasites Exp Parasitol 30 1971 284 320
2. P. Monaghan, H. Cook, P. Hawes, J. Simpson, and F. Tomley High-pressure freezing in the study of animal pathogens J Microsc 212 2003 62 70
3. L.H. Bannister, J.M. Hopkins, G. Margos, A.R. Dluzewski, and G.H. Mitchell Three-dimensional ultrastructure of the ring stage of Plasmodium falciparum: evidence for export pathways Microsc Microanal 10 2004 551 562
4. R. McIntosh, D. Nicastro, and D. Mastronarde New views of cells in 3D: an introduction to electron tomography Trends Cell Biol 15 2005 43 51
5. Frischknecht F, Leonard K, Menard R, Cyrklaff M: Cryo-electron tomography of Plasmodium sporozoites. Abstract 5A, 15th Molecular Parasitology Meeting, Woods Hole 2004.
6. T.A. Freyvogel Shape, movement in situ and locomotion of plasmodial ookinetes Acta Trop 23 1966 201 222
7. J.P. Vanderberg Studies on the motility of Plasmodium sporozoites J Protozool 21 1974 527 537
8. M. Yoeli Movement of the sporozoite of Plasmodium berghei Nature 201 1964 1344 1345
9. I.W. Sherman, S. Eda, and E. Winograd Cytoadherence and sequestration in Plasmodium falciparum: defining the ties that bind Microbes Infect 5 2003 897 909
10. M.E. Wickham, M. Rug, S.A. Ralph, N. Klonis, G.I. McFadden, L. Tilley, and A.F. Cowman Trafficking and assembly of the cytoadherence complex in Plasmodium falciparum-infected human erythrocytes EMBO J 20 2001 5636 5649
11. B.J. Foth, S.A. Ralph, C.J. Tonkin, N.S. Struck, M. Fraunholz, D.S. Roos, A.F. Cowman, and G.I. McFadden Dissecting apicoplast targeting in the malaria parasite Plasmodium falciparum Science 299 2003 705 708
12. R.F. Waller, M.B. Reed, A.F. Cowman, and G.I. McFadden Protein trafficking to the plastid of Plasmodium falciparum is via the secretory pathway EMBO J 19 2000 1794 1802
13. M. Klemba, W. Beatty, I. Gluzman, and D.E. Goldberg Trafficking of plasmepsin II to the food vacuole of the malaria parasite Plasmodium falciparum J Cell Biol 164 2004 47 56
14. A. Adisa, M. Rug, N. Klonis, M. Foley, A.F. Cowman, and L. Tilley The signal sequence of exported protein-1 directs the green fluorescent protein to the parasitophorous vacuole of transfected malaria parasites J Biol Chem 278 2003 6532 6542
15. C. Lopez-Estrano, S. Bhattacharjee, T. Harrison, and K. Haldar Cooperative domains define a unique host cell-targeting signal in Plasmodium falciparum-infected erythrocytes Proc Natl Acad Sci USA 100 2003 12402 12407
16. N.L. Hiller, S. Bhattacharjee, C. van Ooij, K. Liolios, T. Harrison, C. Lopez-Estrano, and K. Haldar A host-targeting signal in virulence proteins reveals a secretome in malarial infection Science 306 2004 1934 1937
17. M. Marti, R.T. Good, M. Rug, E. Knuepfer, and A.F. Cowman Targeting malaria virulence and remodeling proteins to the host erythrocyte Science 306 2004 1930 1933
18. F. Wissing, C.P. Sanchez, P. Rohrbach, S. Ricken, and M. Lanzer Illumination of the malaria parasite Plasmodium falciparum alters intracellular pH. Implications for live cell imaging J Biol Chem 277 2002 37747 37755
19. A. Atherton, and G.V. Born Quantitative investigations of the adhesiveness of circulating polymorphonuclear leucocytes to blood vessel walls J Physiol 222 1972 447 474
20. C. Raventos-Suarez, D.K. Kaul, F. Macaluso, and R.L. Nagel Membrane knobs are required for the microcirculatory obstruction induced by Plasmodium falciparum-infected erythrocytes Proc Natl Acad Sci USA 82 1985 3829 3833
21. D.K. Kaul, M.E. Fabry, F. Costantini, E.M. Rubin, and R.L. Nagel In vivo demonstration of red cell-endothelial interaction, sickling and altered microvascular response to oxygen in the sickle transgenic mouse J Clin Invest 96 1995 2845 2853
22. D.K. Kaul, X.D. Liu, R.L. Nagel, and H.L. Shear Microvascular hemodynamics and in vivo evidence for the role of intercellular adhesion molecule-1 in the sequestration of infected red blood cells in a mouse model of lethal malaria Am J Trop Med Hyg 58 1998 240 247
23. M. Ho, M.J. Hickey, A.G. Murray, G. Andonegui, and P. Kubes Visualization of Plasmodium falciparum-endothelium interactions in human microvasculature: mimicry of leukocyte recruitment J Exp Med 192 2000 1205 1211
24. M. Aikawa Human cerebral malaria Am J Trop Med Hyg 39 1988 3 10
25. O. Billker, V. Lindo, M. Panico, A.E. Etienne, T. Paxton, A. Dell, M. Rogers, R.E. Sinden, and H.R. Morris Identification of xanthurenic acid as the putative inducer of malaria development in the mosquito Nature 392 1998 289 292
26. 2+ reporters at the single-cell level Proc Natl Acad Sci USA 97 2000 7260 7265
27. O. Billker, S. Dechamps, R. Tewari, G. Wenig, B. Franke-Fayard, and V. Brinkmann Calcium and a calcium-dependent protein kinase regulate gamete formation and mosquito transmission in a malaria parasite Cell 117 2004 503 514 GFP-aequorin parasites were used to investigate the calcium response during gametocyte differentiation into gametes. This in vitro assay allowed the identification of a signaling pathway leading from xanthurenic acid via a plant-like calcium dependent kinase to differentiation. These parasites will also provide a useful tool to study calcium signaling during other stages of Plasmodium infection.
28. L.A. Baton, and L.C. Ranford-Cartwright How do malaria ookinetes cross the mosquito midgut wall? Trends Parasitol 21 2005 22 28 A recent review that describes in detail the interaction of ookinetes with the midgut epithelium.
29. A. Danielli, C. Barillas-Mury, S. Kumar, F.C. Kafatos, and T.G. Loukeris Overexpression and altered nucleocytoplasmic distribution of Anopheles ovalbumin-like SRPN10 serpins in Plasmodium-infected midgut cells Cell Microbiol 7 2005 181 190
30. D. Vlachou, T. Zimmermann, R. Cantera, C.J. Janse, A.P. Waters, and F.C. Kafatos Real-time, in vivo analysis of malaria ookinete locomotion and mosquito midgut invasion Cell Microbiol 6 2004 671 685 The authors used in vivo and ex vivo imaging to investigate the complex motile phenotypes of ookinetes in mosquito midguts. A detailed analysis of their extensive datasets confirmed previous in vitro observations [ 6,33 ] and adds valuable quantitative data.
31. Y.S. Han, J. Thompson, F.C. Kafatos, and C. Barillas-Mury Molecular interactions between Anopheles stephensi midgut cells and Plasmodium berghei: the time bomb theory of ookinete invasion of mosquitoes EMBO J 19 2000 6030 6040
32. L. Gupta, S. Kumar, Y.S. Han, P.F. Pimenta, and C. Barillas-Mury Midgut epithelial responses of different mosquito-Plasmodium combinations: the actin cone zipper repair mechanism in Aedes aegypti Proc Natl Acad Sci USA 102 2005 4010 4015
33. H. Zieler, and J.A. Dvorak Invasion in vitro of mosquito midgut cells by the malaria parasite proceeds by a conserved mechanism and results in death of the invaded midgut cells Proc Natl Acad Sci USA 97 2000 11516 11521
34. R. Natarajan, V. Thathy, M.M. Mota, J.C. Hafalla, R. Menard, and K.D. Vernick Fluorescent Plasmodium berghei sporozoites and pre-erythrocytic stages: a new tool to study mosquito and mammalian host interactions with malaria parasites Cell Microbiol 3 2001 371 379
35. F. Frischknecht, P. Baldacci, B. Martin, C. Zimmer, S. Thiberge, J.C. Olivo-Marin, S.L. Shorte, and R. Menard Imaging movement of malaria parasites during transmission by Anopheles mosquitoes Cell Microbiol 6 2004 687 694 In vivo and ex vivo imaging was used to reveal the motile behavior of sporozoites within the salivary system of mosquitoes. The authors suggest that the regulation of motility within glands might influence transmission to the vertebrate host.
36. R. Rosenberg, R.A. Wirtz, I. Schneider, and R. Burge An estimation of the number of malaria sporozoites ejected by a feeding mosquito Trans R Soc Trop Med Hyg 84 1990 209 212
37. J.C. Beier Malaria sporozoites: survival, transmission and disease control Parasitol Today 9 1993 210 215
38. P.F. Pimenta, M. Touray, and L.H. Miller The journey of malaria sporozoites in the mosquito salivary gland J Eukaryot Microbiol 41 1994 608 624
39. C.R. Sterling, M. Aikawa, and J.P. Vanderberg The passage of Plasmodium berghei sporozoites through the salivary glands of Anopheles stephensi: an electron microscope study J Parasitol 59 1973 593 605
40. L.S. Rickman, T.R. Jones, G.W. Long, S. Paparello, I. Schneider, C.F. Paul, R.L. Beaudoin, and S.L. Hoffman Plasmodium falciparum-infected Anopheles stephensi inconsistently transmit malaria to humans Am J Trop Med Hyg 43 1990 441 445
41. M.F. Boyd, and S.F. Kitchen The demonstration of sporozoites in human tissue Am J Trop Med Hyg 19 1939 27 31
42. H. Matsuoka, S. Yoshida, M. Hirai, and A. Ishii A rodent malaria, Plasmodium berghei, is experimentally transmitted to mice by merely probing of infective mosquito, Anopheles stephensi Parasitol Int 51 2002 17 23
43. T. Ponnudurai, A.H. Lensen, G.J. van Gemert, M.G. Bolmer, and J.H. Meuwissen Feeding behaviour and sporozoite ejection by infected Anopheles stephensi Trans R Soc Trop Med Hyg 85 1991 175 180
44. S. Sidjanski, and J.P. Vanderberg Delayed migration of Plasmodium sporozoites from the mosquito bite site to the blood Am J Trop Med Hyg 57 1997 426 429
45. A.U. Krettli, and L.A. Dantas Which routes do Plasmodium sporozoites use for successful infections of vertebrates? Infect Immun 68 2000 3064 3065
46. J.P. Vanderberg, and U. Frevert Intravital microscopy demonstrating antibody-mediated immobilisation of Plasmodium berghei sporozoites injected into skin by mosquitoes Int J Parasitol 34 2004 991 996
47. J.E. Cohen Mathematics is biology's next microscope, only better; biology is mathematics' next physics, only better PLoS Biol 2 2004 e439 A timely review that emphasizes the importance of quantitative analysis over simple phenomenological reporting. It provides interesting historic examples of how biology has progressed through the application of mathematical tools as well as giving an intriguing outlook for the future of quantitative analysis methods and their influence on biology, and vice versa.
48. C.E. Demeure, K. Brahimi, F. Hacini, F. Marchand, R. Peronet, M. Huerre, P. St-Mezard, J.F. Nicolas, P. Brey, and G. Delespesse Anopheles mosquito bites activate cutaneous mast cells leading to a local inflammatory response and lymph node hyperplasia J Immunol 174 2005 3932 3940 Mast cells are found to play an important role in mediation of the effects of mosquito saliva on skin and lymph nodes. This could lead to new studies that investigate possible modulation of these effects by Plasmodium sporozoites.
49. M.D. Cahalan, I. Parker, S.H. Wei, and M.J. Miller Real-time imaging of lymphocytes in vivo Curr Opin Immunol 15 2003 372 377
50. C. Sumen, T.R. Mempel, I.B. Mazo, and U.H. von Andrian Intravital microscopy: visualizing immunity in context Immunity 21 2004 315 329
51. P. Bousso, and E.A. Robey Dynamic behavior of T cells and thymocytes in lymphoid organs as revealed by two-photon microscopy Immunity 21 2004 349 355
52. P. Baldacci, and R. Menard The elusive malaria sporozoite in the mammalian host Mol Microbiol 54 2004 298 306
53. U. Frevert Sneaking in through the back entrance: the biology of malaria liver stages Trends Parasitol 20 2004 417 424
54. M.M. Mota, and A. Rodriguez Migration through host cells: the first steps of Plasmodium sporozoites in the mammalian host Cell Microbiol 6 2004 1113 1118
55. M. Carrolo, S. Giordano, L. Cabrita-Santos, S. Corso, A.M. Vigario, S. Silva, P. Leiriao, D. Carapau, R. Armas-Portela, and P.M. Comoglio Hepatocyte growth factor and its receptor are required for malaria infection Nat Med 9 2003 1363 1369
56. M.M. Mota, J.C. Hafalla, and A. Rodriguez Migration through host cells activates Plasmodium sporozoites for infection Nat Med 8 2002 1318 1322
57. P. Bhanot, K. Schauer, I. Coppens, and V. Nussenzweig A surface phospholipase is involved in the migration of Plasmodium sporozoites through cells J Biol Chem 280 2005 6752 6760
58. T. Ishino, Y. Chinzei, and M. Yuda A Plasmodium sporozoite protein with a membrane attack complex domain is required for breaching the liver sinusoidal cell layer prior to hepatocyte infection Cell Microbiol 7 2005 199 208
59. M. Yuda, and T. Ishino Liver invasion by malarial parasites - how do malarial parasites break through the host barrier? Cell Microbiol 6 2004 1119 1125
60. ••] are from a series of papers that describe several proteins that play a role in host cell transmigration by sporozoites and ookinetes. This suggests that transmigration of cells by both parasite stages is essential for successful progression through the life cycle.
61. •].
62. A.K. Müller, M. Labaied, S.H. Kappe, and K. Matuschewski Genetically modified Plasmodium parasites as a protective experimental malaria vaccine Nature 433 2005 164 167 The authors knocked out a gene that is involved in liver stage maturation of the rodent malaria parasite Plasmodium berghei. They showed that immunization of mice with these recombinant parasites protects against subsequent sporozoite challenges.
63. B. Franke-Fayard, H. Trueman, J. Ramesar, J. Mendoza, M. van der Keur, R. van der Linden, R.E. Sinden, A.P. Waters, and C.J. Janse A Plasmodium berghei reference line that constitutively expresses GFP at a high level throughout the complete life cycle Mol Biochem Parasitol 137 2004 23 33
64. T.G. Carvalho, S. Thiberge, H. Sakamoto, and R. Menard Conditional mutagenesis using site-specific recombination in Plasmodium berghei Proc Natl Acad Sci USA 101 2004 14931 14936 This study uses the FLP recombination system from yeast to describe the proof of principle for the stage-specific modification of genes in Plasmodium berghei.
65. N. Faust, F. Varas, L.M. Kelly, S. Heck, and T. Graf Insertion of enhanced green fluorescent protein into the lysozyme gene creates mice with green fluorescent granulocytes and macrophages Blood 96 2000 719 726
66. R.L. Lindquist, G. Shakhar, D. Dudziak, H. Wardemann, T. Eisenreich, M.L. Dustin, and M.C. Nussenzweig Visualizing dendritic cell networks in vivo Nat Immunol 5 2004 1243 1250
67. O.P. Perera, I.R. Harrell, and A.M. Handler Germ-line transformation of the South American malaria vector, Anopheles albimanus, with a piggyBac/EGFP transposon vector is routine and highly efficient Insect Mol Biol 11 2002 291 297
68. G.L. Grossman, C.S. Rafferty, J.R. Clayton, T.K. Stevens, O. Mukabayire, and M.Q. Benedict Germline transformation of the malaria vector, Anopheles gambiae, with a piggyBac transposable element Insect Mol Biol 10 2001 597 604
69. F. Catteruccia, T. Nolan, T.G. Loukeris, C. Blass, C. Savakis, F.C. Kafatos, and A. Crisanti Stable germline transformation of the malaria mosquito Anopheles stephensi Nature 405 2000 900 901
70. A.A. Sultan, V. Thathy, V. Nussenzweig, and R. Menard Green fluorescent protein as a marker in Plasmodium berghei transformation Infect Immun 67 1999 2602 2606
71. C.R. Engwerda, L. Beattie, and F.H. Amante The importance of the spleen in malaria Trends Parasitol 21 2005 75 80
72. M. Yoeli, and B.J. Hargreaves Brain capillary blockage produced by a virulent strain of rodent malaria Science 184 1974 572 573
73. T. Lang, S. Goyard, M. Lebastard, and G. Milon Bioluminescent Leishmania expressing luciferase for rapid and high throughput screening of drugs acting on amastigote-harbouring macrophages and for quantitative real-time monitoring of parasitism features in living mice Cell Microbiol 7 2005 383 392
74. J.P. Saeij, J.P. Boyle, M.E. Griss, G. Arrizabalaga, and J.C. Boothroyd Bioluminescence imaging of Toxoplasma gondii infection in living mice reveals dramatic differences between strains Infect Immun 73 2005 695 702
75. N. Hitziger, I. Dellacasa, B. Albiger, and A. Barragan Dissemination of Toxoplasma gondii to immunoprivileged organs and role of Toll/interleukin-1 receptor signalling for host resistance assessed by in vivo bioluminescence imaging Cell Microbiol 7 2005 837 848
76. M. Sugiyama, E. Ikeda, S. Kawai, T. Higuchi, H. Zhang, N. Khan, K. Tomiyoshi, T. Inoue, H. Yamaguchi, and K. Katakura Cerebral metabolic reduction in severe malaria: fluorodeoxyglucose-positron emission tomography imaging in a primate model of severe human malaria with cerebral involvement Am J Trop Med Hyg 71 2004 542 545
77. E.G. Solon, S.K. Balani, and F.W. Lee Whole-body autoradiography in drug discovery Curr Drug Metab 3 2002 451 462
78. D. Piwnica-Worms, D.P. Schuster, and J.R. Garbow Molecular imaging of host-pathogen interactions in intact small animals Cell Microbiol 6 2004 319 331
79. A.H. Hielscher Optical tomographic imaging of small animals Curr Opin Biotechnol 16 2005 79 88