Structural basis for chirality and directional motility of Plasmodium sporozoites

Cellular Microbiology

Volumn 14, Issue 11, 2012, Pages 1757-1768

  Kudryashev, Mikhail ^a,b   Münter, Sylvia ^a,e   Lemgruber, Leandro ^a   Montagna, Georgina ^c   Stahlberg, Henning ^b   Matuschewski, Kai ^c   Meissner, Markus ^d   Cyrklaff, Marek ^a   Frischknecht, Friedrich ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF BASEL   (Switzerland)

^c MAX PLANCK INSTITUTE FOR INFECTION BIOLOGY   (Germany)

^d UNIVERSITY OF GLASGOW   (United Kingdom)

^e CARL ZEISS SMT AG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; BLEACHING; CHIRALITY; ELECTRON TOMOGRAPHY; GLIDING MOTILITY; HOST PARASITE INTERACTION; LIFE CYCLE; LOCOMOTION; MICROTUBULE; NONHUMAN; PARASITE DEVELOPMENT; PLASMODIUM; POLARIZATION; PRIORITY JOURNAL; SPOROZOITE; STRUCTURE ANALYSIS; TOXOPLASMA GONDII;

CRYOELECTRON MICROSCOPY; ELECTRON MICROSCOPE TOMOGRAPHY; LOCOMOTION; PLASMODIUM; SPOROZOITES; TOXOPLASMA;

TOXOPLASMA GONDII;

EID: 84867650082     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2012.01836.x     Document Type: Article

References (44)

1. Akaki, M., and Dvorak, J.A. (2005) A chemotactic response facilitates mosquito salivary gland infection by malaria sporozoites. J Exp Biol 208: 3211-3218.
2. Amino, R., Menard, R., and Frischknecht, F. (2005) In vivo imaging of malaria parasites - recent advances and future directions. Curr Opin Microbiol 8: 407-414.
3. Amino, R., Thiberge, S., Martin, B., Celli, S., Shorte, S., Frischknecht, F., and Menard, R. (2006) Quantitative imaging of Plasmodium transmission from mosquito to mammal. Nat Med 12: 220-224.
4. Amino, R., Giovannini, D., Thiberge, S., Gueirard, P., Boisson, B., Dubremetz, J.F., etal. (2008) Host cell traversal is important for progression of the malaria parasite through the dermis to the liver. Cell Host Microbe 3: 88-96.
5. Barragan, A., and Sibley, L.D. (2003) Migration of Toxoplasma gondii across biological barriers. Trends Microbiol 11: 426-430.
6. Baum, J., Papenfuss, A.T., Baum, B., Speed, T.P., and Cowman, A.F. (2006) Regulation of apicomplexan actin-based motility. Nat Rev Microbiol 4: 621-628.
7. Baum, J., Gilberger, T.W., Frischknecht, F., and Meissner, M. (2008) Host-cell invasion by malaria parasites: insights from Plasmodium and Toxoplasma Trends Parasitol 24: 557-563.
8. Cooper, J.A. (1987) Effects of cytochalasin and phalloidin on actin. J Cell Biol 105: 1473-1478.
9. Cyrklaff, M., Kudryashev, M., Leis, A., Leonard, K., Baumeister, W., Menard, R., etal. (2007) Cryoelectron tomography reveals periodic material at the inner side of subpellicular microtubules in apicomplexan parasites. J Exp Med 204: 1281-1287.
10. Ejigiri, I., and Sinnis, P. (2009) Plasmodium sporozoite-host interactions from the dermis to the hepatocyte. Curr Opin Microbiol 12: 401-407.
11. Frangakis, A.S., and Hegerl, R. (2001) Noise reduction in electron tomographic reconstructions using nonlinear anisotropic diffusion. J Struct Biol 135: 239-250.
12. Frischknecht, F. (2007) The skin as interface in the transmission of arthropod-borne pathogens. Cell Microbiol 9: 1630-1640.
13. Frischknecht, F., Baldacci, P., Martin, B., Zimmer, C., Thiberge, S., Olivo-Marin, J.C., etal. (2004) Imaging movement of malaria parasites during transmission by Anopheles mosquitoes. Cell Microbiol 6: 687-694.
14. Frixione, E., Mondragon, R., and Meza, I. (1996) Kinematic analysis of Toxoplasma gondii motility. Cell Motil Cytoskeleton 34: 152-163.
15. Hakansson, S., Morisaki, H., Heuser, J., and Sibley, L.D. (1999) Time-lapse video microscopy of gliding motility in Toxoplasma gondii reveals a novel, biphasic mechanism of cell locomotion. Mol Biol Cell 10: 3539-3547.
16. Hegge, S., Kudryashev, M., Smith, A., and Frischknecht, F. (2009) Automated classification of Plasmodium sporozoite movement patterns reveals a shift towards productive motility during salivary gland infection. Biotechnol J 4: 903-913.
17. Hegge, S., Munter, S., Steinbuchel, M., Heiss, K., Engel, U., Matuschewski, K., and Frischknecht, F. (2010) Multistep adhesion of Plasmodium sporozoites. FASEB J 24: 2222-2234.
18. Heintzelman, M.B. (2006) Cellular and molecular mechanics of gliding locomotion in eukaryotes. Int Rev Cytol 251: 79-129.
19. Hellmann, J.K., Munter, S., Kudryashev, M., Schulz, S., Heiss, K., Muller, A.K., etal. (2011) Environmental constraints guide migration of malaria parasites during transmission. PLoS Pathog 7: e1002080.
20. Huynh, M.H., and Carruthers, V.B. (2006) Toxoplasma MIC2 is a major determinant of invasion and virulence. PLoS Pathog 2: e84.
21. Ishino, T., Yano, K., Chinzei, Y., and Yuda, M. (2004) Cell-passage activity is required for the malarial parasite to cross the liver sinusoidal cell layer. PLoS Biol 2: E4.
22. Kappe, S.H., Buscaglia, C.A., and Nussenzweig, V. (2004) Plasmodium sporozoite molecular cell biology. Annu Rev Cell Dev Biol 20: 29-59.
23. Khater, E.I., Sinden, R.E., and Dessens, J.T. (2004) A malaria membrane skeletal protein is essential for normal morphogenesis, motility, and infectivity of sporozoites. J Cell Biol 167: 425-432.
24. Kimsey, R.B., and Spielman, A. (1990) Motility of Lyme disease spirochetes in fluids as viscous as the extracellular matrix. J Infect Dis 162: 1205-1208.
25. Kudryashev, M., Cyrklaff, M., Baumeister, W., Simon, M.M., Wallich, R., and Frischknecht, F. (2009) Comparative cryo-electron tomography of pathogenic Lyme disease spirochetes. Mol Microbiol 71: 1415-1434.
26. Kudryashev, M., Lepper, S., Baumeister, W., Cyrklaff, M., and Frischknecht, F. (2010a) Geometric constrains for detecting short actin filaments by cryogenic electron tomography. PMC Biophys 3: 6.
27. Kudryashev, M., Lepper, S., Stanway, R., Bohn, S., Baumeister, W., Cyrklaff, M., and Frischknecht, F. (2010b) Positioning of large organelles by a membrane- associated cytoskeleton in Plasmodium sporozoites. Cell Microbiol 12: 362-371.
28. Lemgruber, L., Kloetzel, J.A., Souza, W., and Vommaro, R.C. (2009) Toxoplasma gondii: further studies on the subpellicular network. Mem Inst Oswaldo Cruz 104: 706-709.
29. Lucic, V., Forster, F., and Baumeister, W. (2005) Structural studies by electron tomography: from cells to molecules. Annu Rev Biochem 74: 833-865.
30. McIntosh, R., Nicastro, D., and Mastronarde, D. (2005) New views of cells in 3D: an introduction to electron tomography. Trends Cell Biol 15: 43-51.
31. Mann, T., and Beckers, C. (2001) Characterization of the subpellicular network, a filamentous membrane skeletal component in the parasite Toxoplasma gondii Mol Biochem Parasitol 115: 257-268.
32. Matuschewski, K., Nunes, A.C., Nussenzweig, V., and Menard, R. (2002) Plasmodium sporozoite invasion into insect and mammalian cells is directed by the same dual binding system. EMBO J 21: 1597-1606.
33. Mondragon, R., and Frixione, E. (1996) Ca(2+)-dependence of conoid extrusion in Toxoplasma gondii tachyzoites. J Eukaryot Microbiol 43: 120-127.
34. Montagna, G.N., Buscaglia, C.A., Munter, S., Goosmann, C., Frischknecht, F., Brinkmann, V., and Matuschewski, K. (2012) Critical role for heat shock protein 20 (Hsp20) in migration of malarial sporozoites. J Biol Chem 287: 2410-2422.
35. Monteiro, V.G., de Melo, E.J., Attias, M., and de Souza, W. (2001) Morphological changes during conoid extrusion in Toxoplasma gondii tachyzoites treated with calcium ionophore. J Struct Biol 136: 181-189.
36. Morrissette, N.S., and Sibley, L.D. (2002) Cytoskeleton of apicomplexan parasites. Microbiol Mol Biol Rev 66: 21-38.
37. Munter, S., Sabass, B., Selhuber-Unkel, C., Kudryashev, M., Hegge, S., Engel, U., etal. (2009) Plasmodium sporozoite motility is modulated by the turnover of discrete adhesion sites. Cell Host Microbe 6: 551-562.
38. Nickell, S., Forster, F., Linaroudis, A., Net, W.D., Beck, F., Hegerl, R., etal. (2005) TOM software toolbox: acquisition and analysis for electron tomography. J Struct Biol 149: 227-234.
39. Schrevel, J., Asfaux-Foucher, G., Hopkins, J.M., Robert, V., Bourgouin, C., Prensier, G., and Bannister, L.H. (2007) Vesicle trafficking during sporozoite development in Plasmodium berghei: ultrastructural evidence for a novel trafficking mechanism. Parasitology 135: 1-12.
40. Sultan, A.A., Thathy, V., Frevert, U., Robson, K.J., Crisanti, A., Nussenzweig, V., etal. (1997) TRAP is necessary for gliding motility and infectivity of Plasmodium sporozoites. Cell 90: 511-522.
41. Tremp, A.Z., and Dessens, J.T. (2011) Malaria IMC1 membrane skeleton proteins operate autonomously and participate in motility independently of cell shape. J Biol Chem 286: 5383-5391.
42. Tremp, A.Z., Khater, E.I., and Dessens, J.T. (2008) IMC1b is a putative membrane skeleton protein involved in cell shape, mechanical strength, motility, and infectivity of malaria ookinetes. J Biol Chem 283: 27604-27611.
43. Vanderberg, J., Rhodin, J., and Yoeli, M. (1967) Electron microscopic and histochemical studies of sporozoite formation in Plasmodium berghei J Protozool 14: 82-103.
44. Vanderberg, J.P. (1974) Studies on the motility of Plasmodium sporozoites. J Protozool 21: 527-537.