Phosphothioate oligodeoxynucleotides inhibit Plasmodium sporozoite gliding motility

Cellular Microbiology

Volumn 12, Issue 4, 2010, Pages 506-515

  Liehl, Peter ^a   França, Ana Rita ^b   Prudêncio, Miguel ^a   Latz, Eicke ^c   Zaidman Rémy, Anna ^a   Mota, Maria M ^a,b  

^a INSTITUTO DE MEDICINA MOLECULAR   (Portugal)

^b INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

^c UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CPG OLIGODEOXYNUCLEOTIDE; OLIGODEOXYNUCLEOTIDE; PHOSPHOTHIOATE OLIGODEOXYNUCLEOTIDE; TOLL LIKE RECEPTOR 9; UNCLASSIFIED DRUG;

ARTICLE; BINDING AFFINITY; CELL ACTIVATION; CELL MOTILITY; CONTROLLED STUDY; GROWTH INHIBITION; HEPATOMA CELL; HOST PARASITE INTERACTION; HUMAN; HUMAN CELL; IN VITRO STUDY; LIVER CELL; NUCLEOTIDE METABOLISM; PARASITE MIGRATION; PARASITE TRANSMISSION; PLASMODIUM; PLASMODIUM BERGHEI INFECTION; PRIORITY JOURNAL; SPOROZOITE;

ANIMALS; ANTIMALARIALS; CELL LINE; HEPATOCYTES; HUMANS; LOCOMOTION; OLIGODEOXYRIBONUCLEOTIDES; PLASMODIUM BERGHEI; SPOROZOITES;

MAMMALIA; PLASMODIUM BERGHEI;

EID: 77954276394     PISSN: 14625814     EISSN: 14625822     Source Type: Journal    
DOI: 10.1111/j.1462-5822.2009.01411.x     Document Type: Article

References (35)

1. Amino, R., Giovannini, D., Thiberge, S., Gueirard, P., Boisson, B., Dubremetz, J.F., et al. (2008) Host cell traversal is important for progression of the malaria parasite through the dermis to the liver. Cell Host Microbe 3: 88-96.
2. Barrier, M., Lacroix-Lamande, S., Mancassola, R., Auray, G., Bernardet, N., Chausse, A.M., et al. (2006) Oral and intraperitoneal administration of phosphorothioate oligodeoxynucleotides leads to control of Cryptosporidium parvum infection in neonatal mice. J Infect Dis 193: 1400-1407.
3. Chen, J., Xu, W., Zhou, T., Ding, Y., Duan, J., and Huang, F. (2009) Inhibitory role of toll-like receptors agonists in Plasmodium yoelii liver stage development. Parasite Immunol 31: 466-473.
4. Franke-Fayard, B., Trueman, H., Ramesar, J., Mendoza, J., van der Keur, M., van der Linden, R., et al. (2004) A Plasmodium berghei reference line that constitutively expresses GFP at a high level throughout the complete life cycle. Mol Biochem Parasitol 137: 23-33.
5. Frevert, U., Sinnis, P., Cerami, C., Shreffler, W., Takacs, B., and Nussenzweig, V. (1993) Malaria circumsporozoite protein binds to heparan sulfate proteoglycans associated with the surface membrane of hepatocytes. J Exp Med 177: 1287-1298.
6. Frevert, U., Usynin, I., Baer, K., and Klotz, C. (2006) Nomadic or sessile: can Kupffer cells function as portals for malaria sporozoites to the liver? Cell Microbiol 8: 1537-1546.
7. Gantt, S., Persson, C., Rose, K., Birkett, A.J., Abagyan, R., and Nussenzweig, V. (2000) Antibodies against thrombospondin-related anonymous protein do not inhibit Plasmodium sporozoite infectivity in vivo. Infect Immun 68: 3667-3673.
8. Gramzinski, R.A., Doolan, D.L., Sedegah, M., Davis, H.L., Krieg, A.M., and Hoffman, S.L. (2001) Interleukin-12- and gamma interferon-dependent protection against malaria conferred by CpG oligodeoxynucleotide in mice. Infect Immun 69: 1643-1649.
9. Hacker, H., Mischak, H., Miethke, T., Liptay, S., Schmid, R., Sparwasser, T., et al. (1998) CpG-DNA-specific activation of antigen-presenting cells requires stress kinase activity and is preceded by non-specific endocytosis and endosomal maturation. EMBO J 17: 6230-6240.
10. Haldar, K., Murphy, S.C., Milner, D.A., and Taylor, T.E. (2007) Malaria: mechanisms of erythrocytic infection and pathological correlates of severe disease. Annu Rev Pathol 2: 217-249.
11. Jakob, T., Walker, P.S., Krieg, A.M., Udey, M.C., and Vogel, J.C. (1998) Activation of cutaneous dendritic cells by CpGcontaining oligodeoxynucleotides: a role for dendritic cells in the augmentation of Th1 responses by immunostimulatory DNA. J Immunol 161: 3042-3049.
12. Klinman, D.M. (2004) Immunotherapeutic uses of CpG oligodeoxynucleotides. Nat Rev Immunol 4: 249-258.
13. Krieg, A.M. (2002) CpG motifs in bacterial DNA and their immune effects. Annu Rev Immunol 20: 709-760.
14. Kumagai, Y., Takeuchi, O., and Akira, S. (2008) TLR9 as a key receptor for the recognition of DNA. Adv Drug Deliv Rev 60: 795-804.
15. Latz, E., Schoenemeyer, A., Visintin, A., Fitzgerald, K.A., Monks, B.G., Knetter, C.F., et al. (2004) TLR9 signals after translocating from the ER to CpG DNA in the lysosome. Nat Immunol 5: 190-198.
16. Latz, E., Verma, A., Visintin, A., Gong, M., Sirois, C.M., Klein, D.C., et al. (2007) Ligand-induced conformational changes allosterically activate Toll-like receptor 9. Nat Immunol 8: 772-779.
17. Liu, S., Gallo, D.J., Green, A.M., Williams, D.L., Gong, X., Shapiro, R.A., et al. (2002) Role of toll-like receptors in changes in gene expression and NF-kappa B activation in mouse hepatocytes stimulated with lipopolysaccharide. Infect Immun 70: 3433-3442.
18. Luganini, A., Caposio, P., Landolfo, S., and Gribaudo, G. (2008) Phosphorothioate-modified oligodeoxynucleotides inhibit human cytomegalovirus replication by blocking virus entry. Antimicrob Agents Chemother 52: 1111-1120.
19. McCormick, C.J., Tuckwell, D.S., Crisanti, A., Humphries, M.J., and Hollingdale, M.R. (1999) Identification of heparin as a ligand for the A-domain of Plasmodium falciparum thrombospondin-related adhesion protein. Mol Biochem Parasitol 100: 111-124.
20. 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.
21. Medzhitov, R., and Janeway, C.A., Jr (1997) Innate immunity: the virtues of a nonclonal system of recognition. Cell 91: 295-298.
22. Mota, M.M., Pradel, G., Vanderberg, J.P., Hafalla, J.C., Frevert, U., Nussenzweig, R.S., et al. (2001) Migration of Plasmodium sporozoites through cells before infection. Science 291: 141-144.
23. Mota, M.M., Hafalla, J.C., and Rodriguez, A. (2002) Migration through host cells activates Plasmodium sporozoites for infection. Nat Med 8: 1318-1322.
24. Pancake, S.J., Holt, G.D., Mellouk, S., and Hoffman, S.L. (1992) Malaria sporozoites and circumsporozoite proteins bind specifically to sulfated glycoconjugates. J Cell Biol 117: 1351-1357.
25. Pinzon-Ortiz, C., Friedman, J., Esko, J., and Sinnis, P. (2001) The binding of the circumsporozoite protein to cell surface heparan sulfate proteoglycans is required for Plasmodium sporozoite attachment to target cells. J Biol Chem 276: 26784-26791.
26. Prudencio, M., Rodrigues, C.D., Ataide, R., and Mota, M.M. (2008) Dissecting in vitro host cell infection by Plasmodium sporozoites using flow cytometry. Cell Microbiol 10: 218-224.
27. Renia, L., Miltgen, F., Charoenvit, Y., Ponnudurai, T., Verhave, J.P., Collins, W.E., and Mazier, D. (1988) Malaria sporozoite penetration. A new approach by double staining. J Immunol Methods 112: 201-205.
28. Roberts, T.L., Dunn, J.A., Terry, T.D., Jennings, M.P., Hume, D.A., Sweet, M.J., and Stacey, K.J. (2005) Differences in macrophage activation by bacterial DNA and CpGcontaining oligonucleotides. J Immunol 175: 3569-3576.
29. Sanchez-Campillo, M., Chicano, A., Torio, A., Martin-Orozco, E., Gamiz, P., Hernandez-Caselles, T., and Garcia-Penarrubia, P. (2004) Implication of CpG-ODN and reactive oxygen species in the inhibition of intracellular growth of Salmonella typhimurium in hepatocytes. Microbes Infect 6: 813-820.
30. Schlaepfer, E., Audige, A., von Beust, B., Manolova, V., Weber, M., Joller, H., et al. (2004) CpG oligodeoxynucleotides block human immunodeficiency virus type 1 replication in human lymphoid tissue infected ex vivo. J Virol 78: 12344-12354.
31. Sinnis, P. (1998) An immunoradiometric assay for the quantification of Plasmodium sporozoite invasion of HepG2 cells. J Immunol Methods 221: 17-23.
32. Stewart, M.J., and Vanderberg, J.P. (1988) Malaria sporozoites leave behind trails of circumsporozoite protein during gliding motility. J Protozool 35: 389-393.
33. Stewart, M.J., and Vanderberg, J.P. (1991) Malaria sporozoites release circumsporozoite protein from their apical end and translocate it along their surface. J Protozool 38: 411-421.
34. Sturm, A., Amino, R., van de Sand, C., Regen, T., Retzlaff, S., Rennenberg, A., et al. (2006) Manipulation of host hepatocytes by the malaria parasite for delivery into liver sinusoids. Science 313: 1287-1290.
35. Vanderberg, J.P. (1974) Studies on the motility of Plasmodium sporozoites. J Protozool 21: 527-537.