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Mediators of Inflammation
Volume 2014 (2014), Article ID 362605, 6 pages
http://dx.doi.org/10.1155/2014/362605
Review Article

Immune Evasion Strategies of Pre-Erythrocytic Malaria Parasites

Department of Pathogenic Biology, Third Military Medical University, Chongqing 400038, China

Received 8 January 2014; Revised 25 March 2014; Accepted 27 March 2014; Published 7 May 2014

Academic Editor: Mauricio M. Rodrigues

Copyright © 2014 Hong Zheng et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. L. M. Yamauchi, A. Coppi, G. Snounou, and P. Sinnis, “Plasmodium sporozoites trickle out of the injection site,” Cellular Microbiology, vol. 9, no. 5, pp. 1215–1222, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. U. Frevert, S. Engelmann, S. Zougbédé et al., “Intravital observation of Plasmodium berghei sporozoite infection of the liver,” PLoS Biology, vol. 3, no. 6, Article ID e192, 2005. View at Google Scholar · View at Scopus
  3. M. M. Mota, G. Pradel, J. P. Vanderberg et al., “Migration of Plasmodium sporozoites through cells before infection,” Science, vol. 291, no. 5501, pp. 141–144, 2001. View at Publisher · View at Google Scholar · View at Scopus
  4. A. Sturm, R. Amino, C. van de Sand et al., “Manipulation of host hepatocytes by the malaria parasite for delivery into liver sinusoids,” Science, vol. 313, no. 5791, pp. 1287–1290, 2006. View at Publisher · View at Google Scholar · View at Scopus
  5. R. Amino, S. Thiberge, B. Martin et al., “Quantitative imaging of Plasmodium transmission from mosquito to mammal,” Nature Medicine, vol. 12, no. 2, pp. 220–224, 2006. View at Publisher · View at Google Scholar · View at Scopus
  6. R. Torgler, S. E. Bongfen, J. C. Romero, A. Tardivel, M. Thome, and G. Corradin, “Sporozoite-mediated hepatocyte wounding limits Plasmodium parasite development via MyD88-mediated NF-κB activation and inducible NO synthase expression,” The Journal of Immunology, vol. 180, no. 6, pp. 3990–3999, 2008. View at Google Scholar · View at Scopus
  7. P. Liehl, V. Zuzarte-Luis, J. Chan et al., “Host-cell sensors for Plasmodium activate innate immunity against liver-stage infection,” Nature Medicine, vol. 20, no. 1, pp. 47–53, 2014. View at Publisher · View at Google Scholar
  8. S. Pied, J. Roland, A. Louise et al., “Liver CD4CD8 NK1.1+ TCRαβ intermediate cells increase during experimental malaria infection and are able to exhibit inhibitory activity against the parasite liver stage in vitro,” The Journal of Immunology, vol. 164, no. 3, pp. 1463–1469, 2000. View at Google Scholar · View at Scopus
  9. K. C. McKenna, M. Tsuji, M. Sarzotti, J. B. Sacci Jr., A. A. Witney, and A. F. Azad, “γδ T cells are a component of early immunity against preerythrocytic malaria parasites,” Infection and Immunity, vol. 68, no. 4, pp. 2224–2230, 2000. View at Publisher · View at Google Scholar · View at Scopus
  10. J. Roland, V. Soulard, C. Sellier et al., “NK cell responses to Plasmodium infection and control of intrahepatic parasite development,” The Journal of Immunology, vol. 177, no. 2, pp. 1229–1239, 2006. View at Google Scholar · View at Scopus
  11. S. Portugal, C. Carret, M. Recker et al., “Host-mediated regulation of superinfection in malaria,” Nature Medicine, vol. 17, no. 6, pp. 732–737, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. D. L. Medica and P. Sinnis, “Quantitative dynamics of Plasmodium yoelii sporozoite transmission by infected anopheline mosquitoes,” Infection and Immunity, vol. 73, no. 7, pp. 4363–4369, 2005. View at Publisher · View at Google Scholar · View at Scopus
  13. C. Kebaier, T. Voza, and J. Vanderberg, “Kinetics of mosquito-injected Plasmodium sporozoites in mice: fewer sporozoites are injected into sporozoite-immunized mice,” PLoS Pathogens, vol. 5, no. 4, Article ID e1000399, 2009. View at Publisher · View at Google Scholar · View at Scopus
  14. A. Siau, O. Silvie, J.-F. Franetich et al., “Temperature shift and host cell contact up-regulate sporozoite expression of Plasmodium falciparum genes involved in hepatocyte infection,” PLoS Pathogens, vol. 4, no. 8, Article ID e1000121, 2008. View at Publisher · View at Google Scholar · View at Scopus
  15. R. Amino, D. Giovannini, S. Thiberge et al., “Host cell traversal is important for progression of the malaria parasite through the dermis to the liver,” Cell Host & Microbe, vol. 3, no. 2, pp. 88–96, 2008. View at Publisher · View at Google Scholar · View at Scopus
  16. P. Gueirard, J. Tavares, S. Thiberge et al., “Development of the malaria parasite in the skin of the mammalian host,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 43, pp. 18640–18645, 2010. View at Publisher · View at Google Scholar · View at Scopus
  17. T. Voza, J. L. Miller, S. H. Kappe, and P. Sinnis, “Extrahepatic exoerythrocytic forms of rodent malaria parasites at the site of inoculation: clearance after immunization, susceptibility to primaquine, and contribution to blood-stage infection,” Infection and Immunity, vol. 80, no. 6, pp. 2158–2164, 2012. View at Publisher · View at Google Scholar
  18. G. Pradel, S. Garapaty, and U. Frevert, “Proteoglycans mediate malaria sporozoite targeting to the liver,” Molecular Microbiology, vol. 45, no. 3, pp. 637–651, 2002. View at Publisher · View at Google Scholar · View at Scopus
  19. G. Pradel, S. Garapaty, and U. Frevert, “Kupffer and stellate cell proteoglycans mediate malaria sporozoite targeting to the liver,” Comparative Hepatology, vol. 3, supplement 1, article S47, 2004. View at Google Scholar
  20. G. Pradel and U. Frevert, “Malaria sporozoites actively enter and pass through rat Kupffer cells prior to hepatocyte invasion,” Hepatology, vol. 33, no. 5, pp. 1154–1165, 2001. View at Publisher · View at Google Scholar · View at Scopus
  21. T. Kariu, T. Ishino, K. Yano, Y. Chinzei, and M. Yuda, “CelTOS, a novel malarial protein that mediates transmission to mosquito and vertebrate hosts,” Molecular Microbiology, vol. 59, no. 5, pp. 1369–1379, 2006. View at Publisher · View at Google Scholar · View at Scopus
  22. T. Ishino, Y. Chinzei, and M. Yuda, “Two proteins with 6-cys motifs are required for malarial parasites to commit to infection of the hepatocyte,” Molecular Microbiology, vol. 58, no. 5, pp. 1264–1275, 2005. View at Publisher · View at Google Scholar · View at Scopus
  23. T. Ishino, K. Yano, Y. Chinzei, and M. Yuda, “Cell-passage activity is required for the malarial parasite to cross the liver sinusoidal cell layer,” PLoS Biology, vol. 2, no. 1, article e4, 2004. View at Publisher · View at Google Scholar · View at Scopus
  24. J. Tavares, P. Formaglio, S. Thiberge et al., “Role of host cell traversal by the malaria sporozoite during liver infection,” The Journal of Experimental Medicine, vol. 210, no. 5, pp. 905–915, 2013. View at Publisher · View at Google Scholar
  25. I. Usynin, C. Klotz, and U. Frevert, “Malaria circumsporozoite protein inhibits the respiratory burst in Kupffer cells,” Cellular Microbiology, vol. 9, no. 11, pp. 2610–2628, 2007. View at Publisher · View at Google Scholar · View at Scopus
  26. C. Klotz and U. Frevert, “Plasmodium yoelii sporozoites modulate cytokine profile and induce apoptosis in murine Kupffer cells,” International Journal for Parasitology, vol. 38, no. 14, pp. 1639–1650, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. N. Steers, R. Schwenk, D. J. Bacon, D. Berenzon, J. Williams, and U. Krzych, “The immune status of Kupffer cells profoundly influences their responses to infectious Plasmodium berghei sporozoites,” European Journal of Immunology, vol. 35, no. 8, pp. 2335–2346, 2005. View at Publisher · View at Google Scholar · View at Scopus
  28. J. Chen, W. Xu, T. Zhou, Y. Ding, J. Duan, and F. Huang, “Inhibitory role of toll-like receptors agonists in Plasmodium yoelii liver stage development,” Parasite Immunology, vol. 31, no. 8, pp. 466–473, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. J. F. Meis, J. P. Verhave, P. H. Jap, R. E. Sinden, and J. H. Meuwissen, “Ultrastructural observations on the infection of rat liver by Plasmodium berghei sporozoites in vivo,” Journal of Protozoology, vol. 30, no. 2, pp. 361–366, 1983. View at Google Scholar · View at Scopus
  30. A. P. Singh, C. A. Buscaglia, Q. Wang et al., “Plasmodium circumsporozoite protein promotes the development of the liver stages of the parasite,” Cell, vol. 131, no. 3, pp. 492–504, 2007. View at Publisher · View at Google Scholar · View at Scopus
  31. U. Frevert, M. R. Galinski, F.-U. Hügel et al., “Malaria circumsporozoite protein inhibits protein synthesis in mammalian cells,” The EMBO Journal, vol. 17, no. 14, pp. 3816–3826, 1998. View at Publisher · View at Google Scholar · View at Scopus
  32. O. Silvie, E. Rubinstein, J.-F. Franetich et al., “Hepatocyte CD81 is required for Plasmodium falciparum and Plasmodium yoelii sporozoite infectivity,” Nature Medicine, vol. 9, no. 1, pp. 93–96, 2003. View at Publisher · View at Google Scholar · View at Scopus
  33. S. Charrin, S. Yalaoui, B. Bartosch et al., “The Ig domain protein CD9P-1 down-regulates CD81 ability to support Plasmodium yoelii infection,” The Journal of Biological Chemistry, vol. 284, no. 46, pp. 31572–31578, 2009. View at Publisher · View at Google Scholar · View at Scopus
  34. C. D. Rodrigues, M. Hannus, M. Prudêncio et al., “Host scavenger receptor SR-BI plays a dual role in the establishment of malaria parasite liver infection,” Cell Host & Microbe, vol. 4, no. 3, pp. 271–282, 2008. View at Publisher · View at Google Scholar · View at Scopus
  35. M. M. Mota, J. C. R. Hafalla, and A. Rodriguez, “Migration through host cells activates Plasmodium sporozoites for infection,” Nature Medicine, vol. 8, no. 11, pp. 1318–1322, 2002. View at Publisher · View at Google Scholar · View at Scopus
  36. T. Ono, L. Cabrita-Santos, R. Leitao et al., “Adenylyl cyclase α and cAMP signaling mediate Plasmodium sporozoite apical regulated exocytosis and hepatocyte infection,” PLoS Pathogens, vol. 4, no. 2, Article ID e1000008, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. M. Carrolo, S. Giordano, L. Cabrita-Santos et al., “Hepatocyte growth factor and its receptor are required for malaria infection,” Nature Medicine, vol. 9, no. 11, pp. 1363–1369, 2003. View at Publisher · View at Google Scholar · View at Scopus
  38. S. H. I. Kappe, C. A. Buscaglia, and V. Nussenzweig, “Plasmodium sporozoite molecular cell biology,” Annual Review of Cell and Developmental Biology, vol. 20, pp. 29–59, 2004. View at Publisher · View at Google Scholar · View at Scopus
  39. A. Coppi, C. Pinzon-Ortiz, C. Hutter, and P. Sinnis, “The Plasmodium circumsporozoite protein is proteolytically processed during cell invasion,” The Journal of Experimental Medicine, vol. 201, no. 1, pp. 27–33, 2005. View at Publisher · View at Google Scholar · View at Scopus
  40. A. Coppi, R. Tewari, J. R. Bishop et al., “Heparan sulfate proteoglycans provide a signal to Plasmodium sporozoites to stop migrating and productively invade host cells,” Cell Host & Microbe, vol. 2, no. 5, pp. 316–327, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. C. van de Sand, S. Horstmann, A. Schmidt et al., “The liver stage of Plasmodium berghei inhibits host cell apoptosis,” Molecular Microbiology, vol. 58, no. 3, pp. 731–742, 2005. View at Publisher · View at Google Scholar · View at Scopus
  42. P. Leirião, S. S. Albuquerque, S. Corso et al., “HGF/MET signalling protects Plasmodium-infected host cells from apoptosis,” Cellular Microbiology, vol. 7, no. 4, pp. 603–609, 2005. View at Publisher · View at Google Scholar · View at Scopus
  43. A. Kaushansky, P. G. Metzger, A. N. Douglass et al., “Malaria parasite liver stages render host hepatocytes susceptible to mitochondria-initiated apoptosis,” Cell Death & Disease, vol. 4, Article ID e762, 2013. View at Publisher · View at Google Scholar
  44. A. Kaushansky, A. S. Ye, L. S. Austin et al., “Suppression of host p53 is critical for Plasmodium liver-stage infection,” Cell Reports, vol. 3, no. 3, pp. 630–637, 2013. View at Publisher · View at Google Scholar
  45. P. Kuballa, W. M. Nolte, A. B. Castoreno, and R. J. Xavier, “Autophagy and the immune system,” Annual Review of Immunology, vol. 30, pp. 611–646, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. I. Coppens, “Metamorphoses of malaria: the role of autophagy in parasite differentiation,” Essays in Biochemistry, vol. 51, pp. 127–136, 2011. View at Google Scholar
  47. A. F. Cowman and S. H. I. Kappe, “Malaria's stealth shuttle,” Science, vol. 313, no. 5791, pp. 1245–1246, 2006. View at Publisher · View at Google Scholar · View at Scopus
  48. S. Graewe, K. E. Rankin, C. Lehmann et al., “Hostile takeover by Plasmodium: reorganization of parasite and host cell membranes during liver stage egress,” PLoS Pathogens, vol. 7, no. 9, Article ID e1002224, 2011. View at Publisher · View at Google Scholar · View at Scopus
  49. K. Baer, C. Klotz, S. H. I. Kappe, T. Schnieder, and U. Frevert, “Release of hepatic Plasmodium yoelii merozoites into the pulmonary microvasculature,” PLoS Pathogens, vol. 3, no. 11, Article ID e171, 2007. View at Publisher · View at Google Scholar · View at Scopus
  50. S. Epiphanio, S. A. Mikolajczak, L. A. Gonçalves et al., “Heme oxygenase-1 is an anti-inflammatory host factor that promotes murine Plasmodium liver infection,” Cell Host & Microbe, vol. 3, no. 5, pp. 331–338, 2008. View at Publisher · View at Google Scholar · View at Scopus
  51. X. Wen-Yue, W. Xing-Xiang, Q. Jie, D. Jian-Hua, and H. Fu-Sheng, “Plasmodium yoelii: influence of immune modulators on the development of the liver stage,” Experimental Parasitology, vol. 126, no. 2, pp. 254–258, 2010. View at Publisher · View at Google Scholar · View at Scopus