Immune evasion strategies of pre-erythrocytic malaria parasites

Mediators of Inflammation

Volumn 2014, Issue , 2014, Pages

  Zheng, Hong ^a   Tan, Zhangping ^a   Xu, Wenyue ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ANOPHELES; HOST RESISTANCE; HUMAN; IMMUNE EVASION; IMMUNE RESPONSE; KUPFFER CELL; LIVER CELL; MALARIA; MOSQUITO BITE; NONHUMAN; PHAGOCYTE; PLASMODIUM; PLASMODIUM (LIFE CYCLE STAGE); PREERYTHROCYTIC STAGE; PROPHYLAXIS; REVIEW; SKIN; SPOROZOITE; SYMPTOM; ANIMAL; AUTOPHAGY; CHEMISTRY; ERYTHROCYTE; FEMALE; IMMUNOLOGY; LIVER; MOSQUITO; PARASITOLOGY; PHYSIOLOGY;

PROTEOGLYCAN;

ANIMALS; ANOPHELES; AUTOPHAGY; CULICIDAE; ERYTHROCYTES; FEMALE; HEPATOCYTES; HUMANS; IMMUNE EVASION; KUPFFER CELLS; LIVER; MALARIA; PHAGOCYTES; PROTEOGLYCANS; SKIN; SPOROZOITES;

EID: 84901811558     PISSN: 09629351     EISSN: 14661861     Source Type: Journal    
DOI: 10.1155/2014/362605     Document Type: Review

References (51)

1. Yamauchi L. M., Coppi A., Snounou G., Sinnis P., Plasmodium sporozoites trickle out of the injection site. Cellular Microbiology 2007 9 5 1215 1222 2-s2.0-34147127535 10.1111/j.1462-5822.2006.00861.x (Pubitemid 46552879)
2. Frevert U., Engelmann S., Zougbédé S., Stange J., Ng B., Matuschewski K., Liebes L., Yee H., Intravital observation of Plasmodium berghei sporozoite infection of the liver. PLoS Biology 2005 3 6 e192 2-s2.0-32244440918
3. Mota M. M., Pradel G., Vanderberg J. P., Hafalla J. C. R., Frevert U., Nussenzweig R. S., Nussenzweig V., Rodriguez A., Migration of Plasmodium sporozoites through cells before infection. Science 2001 291 5501 141 144 2-s2.0-0035808562 10.1126/science.291.5501.141 (Pubitemid 32056684)
4. Sturm A., Amino R., van de Sand C., Regen T., Retzlaff S., Rennenberg A., Krueger A., Pollok J.-M., Menard R., Heussler V. T., Manipulation of host hepatocytes by the malaria parasite for delivery into liver sinusoids. Science 2006 313 5791 1287 1290 2-s2.0-33748314455 10.1126/science.1129720 (Pubitemid 44330952)
5. Amino R., Thiberge S., Martin B., Celli S., Shorte S., Frischknecht F., Ménard R., Quantitative imaging of Plasmodium transmission from mosquito to mammal. Nature Medicine 2006 12 2 220 224 2-s2.0-32244448982 10.1038/nm1350 (Pubitemid 43214749)
6. Torgler R., Bongfen S. E., Romero J. C., Tardivel A., Thome M., Corradin G., Sporozoite-mediated hepatocyte wounding limits Plasmodium parasite development via MyD88-mediated NF- B activation and inducible NO synthase expression. The Journal of Immunology 2008 180 6 3990 3999 2-s2.0-44849129576
7. Liehl P., Zuzarte-Luis V., Chan J., Host-cell sensors for Plasmodium activate innate immunity against liver-stage infection. Nature Medicine 2014 20 1 47 53 10.1038/nm.3424
8. + TCR α β 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 2000 164 3 1463 1469 2-s2.0-0034142340 (Pubitemid 30067262)
9. McKenna K. C., Tsuji M., Sarzotti M., Sacci J. B. Jr., Witney A. A., Azad A. F., γ δ T cells are a component of early immunity against preerythrocytic malaria parasites. Infection and Immunity 2000 68 4 2224 2230 2-s2.0-0033621811 10.1128/IAI.68.4.2224-2230.2000 (Pubitemid 30164858)
10. Roland J., Soulard V., Sellier C., Drapier A.-M., di Santo J. P., Cazenave P.-A., Pied S., NK cell responses to Plasmodium infection and control of intrahepatic parasite development. The Journal of Immunology 2006 177 2 1229 1239 2-s2.0-33745816382 (Pubitemid 44036628)
11. Portugal S., Carret C., Recker M., Armitage A. E., Gonçalves L. A., Epiphanio S., Sullivan D., Roy C., Newbold C. I., Drakesmith H., Mota M. M., Host-mediated regulation of superinfection in malaria. Nature Medicine 2011 17 6 732 737 2-s2.0-79958143306 10.1038/nm.2368
12. Medica D. L., Sinnis P., Quantitative dynamics of Plasmodium yoelii sporozoite transmission by infected anopheline mosquitoes. Infection and Immunity 2005 73 7 4363 4369 2-s2.0-21544439559 10.1128/IAI.73.7.4363-4369.2005 (Pubitemid 40923182)
13. Kebaier C., Voza T., Vanderberg J., Kinetics of mosquito-injected Plasmodium sporozoites in mice: fewer sporozoites are injected into sporozoite-immunized mice. PLoS Pathogens 2009 5 4 e1000399 2-s2.0-66349098083 10.1371/journal.ppat.1000399
14. Siau A., Silvie O., Franetich J.-F., Yalaoui S., Marinach C., Hannoun L., van Gemert G.-J., Luty A. J. F., Bischoff E., David P. H., Snounou G., Vaquero C., Froissard P., Mazier D., Temperature shift and host cell contact up-regulate sporozoite expression of Plasmodium falciparum genes involved in hepatocyte infection. PLoS Pathogens 2008 4 8 2-s2.0-50849111741 10.1371/journal.ppat. 1000121 e1000121
15. Amino R., Giovannini D., Thiberge S., Gueirard P., Boisson B., Dubremetz J.-F., Prévost M.-C., Ishino T., Yuda M., Ménard R., Host cell traversal is important for progression of the malaria parasite through the dermis to the liver. Cell Host & Microbe 2008 3 2 88 96 2-s2.0-38849143095 10.1016/j.chom.2007.12.007 (Pubitemid 351201783)
16. Gueirard P., Tavares J., Thiberge S., Bernex F., Ishino T., Milon G., Franke-Fayard B., Janse C. J., Ménard R., Amino R., 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 2010 107 43 18640 18645 2-s2.0-78649808522 10.1073/pnas.1009346107
17. Voza T., Miller J. L., Kappe S. H., Sinnis P., 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 2012 80 6 2158 2164 10.1128/IAI.00246-12
18. Pradel G., Garapaty S., Frevert U., Proteoglycans mediate malaria sporozoite targeting to the liver. Molecular Microbiology 2002 45 3 637 651 2-s2.0-0036372431 10.1046/j.1365-2958.2002.03057.x (Pubitemid 34989173)
19. Pradel G., Garapaty S., Frevert U., Kupffer and stellate cell proteoglycans mediate malaria sporozoite targeting to the liver. Comparative Hepatology 2004 3 supplement 1, article S47
20. Pradel G., Frevert U., Malaria sporozoites actively enter and pass through rat Kupffer cells prior to hepatocyte invasion. Hepatology 2001 33 5 1154 1165 2-s2.0-0035038271 10.1053/jhep.2001.24237 (Pubitemid 32378215)
21. Kariu T., Ishino T., Yano K., Chinzei Y., Yuda M., CelTOS, a novel malarial protein that mediates transmission to mosquito and vertebrate hosts. Molecular Microbiology 2006 59 5 1369 1379 2-s2.0-33645088696 10.1111/j.1365-2958.2005.05024.x
22. Ishino T., Chinzei Y., Yuda M., Two proteins with 6-cys motifs are required for malarial parasites to commit to infection of the hepatocyte. Molecular Microbiology 2005 58 5 1264 1275 2-s2.0-28244480361 10.1111/j.1365-2958.2005.04801.x (Pubitemid 41705408)
23. Ishino T., Yano K., Chinzei Y., Yuda M., Cell-passage activity is required for the malarial parasite to cross the liver sinusoidal cell layer. PLoS Biology 2004 2 1, article e4 2-s2.0-19344370327 10.1371/journal.pbio. 0020004 (Pubitemid 39234588)
24. Tavares J., Formaglio P., Thiberge S., Mordelet E., van Rooijen N., Medvinsky A., Menard R., Amino R., Role of host cell traversal by the malaria sporozoite during liver infection. The Journal of Experimental Medicine 2013 210 5 905 915 10.1084/jem.20121130
25. Usynin I., Klotz C., Frevert U., Malaria circumsporozoite protein inhibits the respiratory burst in Kupffer cells. Cellular Microbiology 2007 9 11 2610 2628 2-s2.0-34848843529 10.1111/j.1462-5822.2007.00982.x (Pubitemid 47500514)
26. Klotz C., Frevert U., Plasmodium yoelii sporozoites modulate cytokine profile and induce apoptosis in murine Kupffer cells. International Journal for Parasitology 2008 38 14 1639 1650 2-s2.0-51449104230 10.1016/j.ijpara.2008.05. 018
27. Steers N., Schwenk R., Bacon D. J., Berenzon D., Williams J., Krzych U., The immune status of Kupffer cells profoundly influences their responses to infectious Plasmodium berghei sporozoites. European Journal of Immunology 2005 35 8 2335 2346 2-s2.0-23844500084 10.1002/eji.200425680 (Pubitemid 41179754)
28. Chen J., Xu W., Zhou T., Ding Y., Duan J., Huang F., Inhibitory role of toll-like receptors agonists in Plasmodium yoelii liver stage development. Parasite Immunology 2009 31 8 466 473 2-s2.0-68249162070 10.1111/j.1365-3024. 2009.01126.x
29. Meis J. F., Verhave J. P., Jap P. H., Sinden R. E., Meuwissen J. H., Ultrastructural observations on the infection of rat liver by Plasmodium berghei sporozoites in vivo. Journal of Protozoology 1983 30 2 361 366 2-s2.0-0020574112 (Pubitemid 13012713)
30. Singh A. P., Buscaglia C. A., Wang Q., Levay A., Nussenzweig D. R., Walker J. R., Winzeler E. A., Fujii H., Fontoura B. M. A., Nussenzweig V., Plasmodium circumsporozoite protein promotes the development of the liver stages of the parasite. Cell 2007 131 3 492 504 2-s2.0-35548952254 10.1016/j.cell.2007.09.013 (Pubitemid 350007696)
31. Frevert U., Galinski M. R., Hügel F.-U., Allon N., Schreier H., Smulevitch S., Shakibaei M., Clavijo P., Malaria circumsporozoite protein inhibits protein synthesis in mammalian cells. The EMBO Journal 1998 17 14 3816 3826 2-s2.0-0032527804 10.1093/emboj/17.14.3816 (Pubitemid 28333968)
32. Silvie O., Rubinstein E., Franetich J.-F., Prenant M., Belnoue E., Rénia L., Hannoun L., Elings W., Levy S., Boucheix C., Mazier D., Hepatocyte CD81 is required for Plasmodium falciparum and Plasmodium yoelii sporozoite infectivity. Nature Medicine 2003 9 1 93 96 2-s2.0-0037234454 10.1038/nm808 (Pubitemid 36098266)
33. Charrin S., Yalaoui S., Bartosch B., Cocquerel L., Franetich J.-F., Boucheix C., Mazier D., Rubinstein E., Silvie O., The Ig domain protein CD9P-1 down-regulates CD81 ability to support Plasmodium yoelii infection. The Journal of Biological Chemistry 2009 284 46 31572 31578 2-s2.0-70450267376 10.1074/jbc.M109.057927
34. Rodrigues C. D., Hannus M., Prudêncio M., Martin C., Gonçalves L. A., Portugal S., Epiphanio S., Akinc A., Hadwiger P., Jahn-Hofmann K., Röhl I., van Gemert G.-J., Franetich J.-F., Luty A. J. F., Sauerwein R., Mazier D., Koteliansky V., Vornlocher H.-P., Echeverri C. J., Mota M. M., Host scavenger receptor SR-BI plays a dual role in the establishment of malaria parasite liver infection. Cell Host & Microbe 2008 4 3 271 282 2-s2.0-50849115819 10.1016/j.chom.2008.07.012
35. Mota M. M., Hafalla J. C. R., Rodriguez A., Migration through host cells activates Plasmodium sporozoites for infection. Nature Medicine 2002 8 11 1318 1322 2-s2.0-0036851878 10.1038/nm785 (Pubitemid 35373566)
36. Ono T., Cabrita-Santos L., Leitao R., Bettiol E., Purcell L. A., Diaz-Pulido O., Andrews L. B., Tadakuma T., Bhanot P., Mota M. M., Rodriguez A., Adenylyl cyclase α and cAMP signaling mediate Plasmodium sporozoite apical regulated exocytosis and hepatocyte infection. PLoS Pathogens 2008 4 2 e1000008 2-s2.0-40349098210 10.1371/journal.ppat.1000008 (Pubitemid 351340693)
37. Carrolo M., Giordano S., Cabrita-Santos L., Corso S., Vigário A. M., Silva S., Leirião P., Carapau D., Armas-Portela R., Comoglio P. M., Rodriguez A., Mota M. M., Hepatocyte growth factor and its receptor are required for malaria infection. Nature Medicine 2003 9 11 1363 1369 2-s2.0-0345708275 10.1038/nm947 (Pubitemid 37466184)
38. Kappe S. H. I., Buscaglia C. A., Nussenzweig V., Plasmodium sporozoite molecular cell biology. Annual Review of Cell and Developmental Biology 2004 20 29 59 2-s2.0-8444221999 10.1146/annurev.cellbio.20.011603.150935 (Pubitemid 39488632)
39. Coppi A., Pinzon-Ortiz C., Hutter C., Sinnis P., The Plasmodium circumsporozoite protein is proteolytically processed during cell invasion. The Journal of Experimental Medicine 2005 201 1 27 33 2-s2.0-12344299732 10.1084/jem.20040989 (Pubitemid 40130080)
40. Coppi A., Tewari R., Bishop J. R., Bennett B. L., Lawrence R., Esko J. D., Billker O., Sinnis P., Heparan sulfate proteoglycans provide a signal to Plasmodium sporozoites to stop migrating and productively invade host cells. Cell Host & Microbe 2007 2 5 316 327 2-s2.0-35848931896 10.1016/j.chom.2007. 10.002 (Pubitemid 350056399)
41. van de Sand C., Horstmann S., Schmidt A., Sturm A., Bolte S., Krueger A., Lütgehetmann M., Pollok J.-M., Libert C., Heussler V. T., The liver stage of Plasmodium berghei inhibits host cell apoptosis. Molecular Microbiology 2005 58 3 731 742 2-s2.0-27444440200 10.1111/j.1365-2958.2005.04888.x (Pubitemid 41532471)
42. Leirião P., Albuquerque S. S., Corso S., van Gemert G.-J., Sauerwein R. W., Rodriguez A., Giordano S., Mota M. M., HGF/MET signalling protects Plasmodium -infected host cells from apoptosis. Cellular Microbiology 2005 7 4 603 609 2-s2.0-15944378526 10.1111/j.1462-5822.2004.00490.x (Pubitemid 40439458)
43. Kaushansky A., Metzger P. G., Douglass A. N., Mikolajczak S. A., Lakshmanan V., Kain H. S., Kappe S. H., Malaria parasite liver stages render host hepatocytes susceptible to mitochondria-initiated apoptosis. Cell Death & Disease 2013 4 e762 10.1038/cddis.2013.286
44. Kaushansky A., Ye A. S., Austin L. S., Mikolajczak S. A., Vaughan A. M., Camargo N., Metzger P. G., Douglass A. N., Macbeath G., Kappe S. H., Suppression of host p53 is critical for Plasmodium liver-stage infection. Cell Reports 2013 3 3 630 637 10.1016/j.celrep.2013.02.010
45. Kuballa P., Nolte W. M., Castoreno A. B., Xavier R. J., Autophagy and the immune system. Annual Review of Immunology 2012 30 611 646 2-s2.0-84859386792 10.1146/annurev-immunol-020711-074948
46. Coppens I., Metamorphoses of malaria: the role of autophagy in parasite differentiation. Essays in Biochemistry 2011 51 127 136
47. Cowman A. F., Kappe S. H. I., Malaria's stealth shuttle. Science 2006 313 5791 1245 1246 2-s2.0-33748302725 10.1126/science.1132940 (Pubitemid 44330937)
48. Graewe S., Rankin K. E., Lehmann C., Deschermeier C., Hecht L., Froehlke U., Stanway R. R., Heussler V., Hostile takeover by Plasmodium: reorganization of parasite and host cell membranes during liver stage egress. PLoS Pathogens 2011 7 9 2-s2.0-80053453918 10.1371/journal.ppat.1002224 e1002224
49. Baer K., Klotz C., Kappe S. H. I., Schnieder T., Frevert U., Release of hepatic Plasmodium yoelii merozoites into the pulmonary microvasculature. PLoS Pathogens 2007 3 11 e171 2-s2.0-38749138941 10.1371/journal.ppat.0030171 (Pubitemid 350291602)
50. Epiphanio S., Mikolajczak S. A., Gonçalves L. A., Pamplona A., Portugal S., Albuquerque S., Goldberg M., Rebelo S., Anderson D. G., Akinc A., Vornlocher H.-P., Kappe S. H. I., Soares M. P., Mota M. M., Heme oxygenase-1 is an anti-inflammatory host factor that promotes murine Plasmodium liver infection. Cell Host & Microbe 2008 3 5 331 338 2-s2.0-43049168497 10.1016/j.chom.2008.04.003 (Pubitemid 351635999)
51. Wen-Yue X., Xing-Xiang W., Jie Q., Jian-Hua D., Fu-Sheng H., Plasmodium yoelii: influence of immune modulators on the development of the liver stage. Experimental Parasitology 2010 126 2 254 258 2-s2.0-77955275842 10.1016/j.exppara.2010.05.005