Plasmodium cellular effector mechanisms and the hepatic microenvironment

Frontiers in Microbiology

Volumn 6, Issue MAY, 2015, Pages

  Frevert, Ute ^a   Krzych, Urszula ^b  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

Author keywords

Antigen presenting cells; CD8 T cells; Liver; Liver lymphatics; Plasmodium

Indexed keywords

CIRCUMSPOROZOITE PROTEIN; GAMMA INTERFERON; INTERLEUKIN DERIVATIVE; MALARIA VACCINE; MEMBRANE ANTIGEN;

CD8+ T LYMPHOCYTE; CELL PHAGOCYTOSIS; CELL SPECIFICITY; CELLULAR IMMUNITY; DENDRITIC CELL; EFFECTOR CELL; HEPATIC MICROENVIRONMENT; IMMUNIZATION; KUPFFER CELL; LIVER CELL; MICROENVIRONMENT; MICROVASCULATURE; NONHUMAN; PLASMODIUM (LIFE CYCLE STAGE); PLASMODIUM FALCIPARUM; REVIEW; SPOROZOITE;

PLASMODIUM FALCIPARUM;

EID: 84931267030     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2015.00482     Document Type: Review

References (217)

1. Ando, K., Guidotti, L. G., Cerny, A., Ishikawa, T., and Chisari, F. V. (1994a). CTL access to tissue antigen is restricted in vivo. J. Immunol. 153, 482-488.
2. Ando, K., Guidotti, L. G., Wirth, S., Ishikawa, T., Missale, G., Moriyama, T., et al. (1994b). Class I-restricted cytotoxic T lymphocytes are directly cytopathic for their target cells in vivo. J. Immunol. 152, 3245-3253.
3. Baer, K., Klotz, C., Kappe, S. H., Schnieder, T., and Frevert, U. (2007a). Release of hepatic Plasmodium yoelii merozoites into the pulmonary microvasculature. PLoS Pathog. 3:e171. doi: 10.1371/journal.ppat.0030171.
4. Baer, K., Roosevelt, M., Van Rooijen, N., Clarkson, A. B. Jr., Schnieder, T., et al. (2007b). Kupffer cells are obligatory for Plasmodium yoelii sporozoite infection of the liver. Cell. Microbiol. 9, 397-412. doi: 10.1111/j.1462-5822.2006.00798.x.
5. Balam, S., Romero, J. F., Bongfen, S. E., Guillaume, P., and Corradin, G. (2012). CSP-A model for in vivo presentation of Plasmodium berghei sporozoite antigens by hepatocytes. PLoS ONE 7:e51875. doi: 10.1371/journal.pone.0051875.
6. Barbieri, L., Battelli, M. G., and Stirpe, F. (1993). Ribosome-inactivating proteins from plants. Biochim. Biophys. Acta 1154, 237-282. doi: 10.1016/0304-4157(93)90002-6.
7. Bayarsaikhan, G., Akbari, M., Yui, K., and Amino, K. (2015). Antigen-driven focal inflammatory death of malaria liver stages. Front. Microbiol. 6:47. doi: 10.3389/fmicb.2015.00047.
8. Belnoue, E., Costa, F. T., Frankenberg, T., Vigario, A. M., Voza, T., Leroy, N., et al. (2004). Protective T cell immunity against malaria liver stage after vaccination with live sporozoites under chloroquine treatment. J. Immunol. 172, 2487-2495. doi: 10.4049/jimmunol.172.4.2487.
9. Belnoue, E., Voza, T., Costa, F. T., Gruner, A. C., Mauduit, M., Rosa, D. S., et al. (2008). Vaccination with live Plasmodium yoelii blood stage parasites under chloroquine cover induces cross-stage immunity against malaria liver stage. J. Immunol. 181, 8552-8558. doi: 10.4049/jimmunol.181.12.8552.
10. Bending, D., De La Pena, H., Veldhoen, M., Phillips, J. M., Uyttenhove, C., Stockinger, B., et al. (2009). Highly purified Th17 cells from BDC2.5NOD mice convert into Th1-like cells in NOD/SCID recipient mice. J. Clin. Invest. 119, 565-572. doi: 10.1172/JCI37865.
11. + T cell tolerance. Eur. J. Immunol. 36, 2960-2970. doi: 10.1002/eji.200636033.
12. Berke, G. (1995). The CTL's kiss of death. Cell 81, 9-12. doi: 10.1016/0092-8674(95)90365-8.
13. Bertolino, P., and Bowen, D. G. (2015). Malaria and the liver: immunological hide-and-seek or subversion of immunity from within? Front. Microbiol. 6:41. doi: 10.3389/fmicb.2015.00041.
14. Bertolino, P., Mccaughan, G. W., and Bowen, D. G. (2002). Role of primary intrahepatic T-cell activation in the 'liver tolerance effect'. Immunol. Cell Biol. 80, 84-92. doi: 10.1046/j.0818-9641.2001.01048.x.
15. Bogdan, C., Rollinghoff, M., and Diefenbach, A. (2000). The role of nitric oxide in innate immunity. Immunol. Rev. 173, 17-26. doi: 10.1034/j.1600-065X.2000.917307.x.
16. Boissonnas, A., Fetler, L., Zeelenberg, I. S., Hugues, S., and Amigorena, S. (2007). In vivo imaging of cytotoxic T cell infiltration and elimination of a solid tumor. J. Exp. Med. 204, 345-356. doi: 10.1084/jem.20061890.
17. Bongfen, S. E., Balam, S., Torgler, R., Romero, J. F., and Corradin, G. (2008). Processing of the circumsporozoite protein in infected hepatocytes is not dependent on aspartic proteases. Parasite Immunol. 30, 375-378. doi: 10.1111/j.1365-3024.2008.01032.x.
18. + T cells in vitro. J. Immunol. 178, 7054-7063. doi: 10.4049/jimmunol.178.11.7054.
19. Briones, M. R. S., Tsuji, M., and Nussenzweig, V. (1996). The large difference in infectivity for mice of Plasmodium berghei and Plasmodium yoelii sporozoites cannot be correlated with their ability to enter hepatocytes. Mol. Biochem. Parasitol. 77, 7-17. doi: 10.1016/0166-6851(96)02574-1.
20. Burgio, V. L., Ballardini, G., Artini, M., Caratozzolo, M., Bianchi, F. B., and Levrero, M. (1998). Expression of co-stimulatory molecules by Kupffer cells in chronic hepatitis of hepatitis C virus etiology. Hepatology 27, 1600-1606. doi: 10.1002/hep.510270620.
21. Butler, N. S., Schmidt, N. W., and Harty, J. T. (2010). Differential effector pathways regulate memory CD8 T cell immunity against Plasmodium berghei versus P. yoelii sporozoites. J. Immunol. 184, 2528-2538. doi: 10.4049/jimmunol.0903529.
22. Butler, N. S., Schmidt, N. W., Vaughan, A. M., Aly, A. S., Kappe, S. H., and Harty, J. T. (2011). Superior antimalarial immunity after vaccination with late liver stage-arresting genetically attenuated parasites. Cell Host Microbe 9, 451-462. doi: 10.1016/j.chom.2011.05.008.
23. Cabrera, M., and Frevert, U. (2012). Novel in vivo imaging techniques for the liver microvasculature. Intravital 1, 107-114. doi: 10.4161/intv.23423.
24. + T cell dynamics in the liver of Plasmodium yoelii immunized and infected mice. PLoS ONE 8:e70842. doi: 10.1371/journal.pone.0070842.
25. Calvo-Calle, J. M., Oliveira, G. A., Watta, C. O., Soverow, J., Parra-Lopez, C., and Nardin, E. H. (2006). A linear peptide containing minimal T-and B-cell epitopes of Plasmodium falciparum circumsporozoite protein elicits protection against transgenic sporozoite challenge. Infect. Immun. 74, 6929-6939. doi: 10.1128/IAI.01151-06.
26. Catalfamo, M., and Henkart, P. A. (2003). Perforin and the granule exocytosis cytotoxicity pathway. Curr. Opin. Immunol. 15, 522-527. doi: 10.1016/S0952-7915(03)00114-6.
27. + T lymphocytes against liver stages of Plasmodium yoelii do not require gamma interferon for antiparasite activity. Infect. Immun. 76, 3628-3631. doi: 10.1128/IAI.00471-08.
28. + T lymphocytes protective against malaria liver stages are primed in skin-draining lymph nodes. Nat. Med. 13, 1035-1041. doi: 10.1038/nm1628.
29. Chen, T., Zamora, R., Zuckerbraun, B., and Billiar, T. R. (2003). Role of nitric oxide in liver injury. Curr. Mol. Med. 3, 519-526. doi: 10.2174/1566524033479582.
30. + T cell-mediated elimination of malaria liver stages. Proc. Natl. Acad. Sci. U.S.A. 110, 9090-9095. doi: 10.1073/pnas.1303858110.
31. Cockburn, I. A., Tse, S. W., Radtke, A. J., Srinivasan, P., Chen, Y. C., Sinnis, P., et al. (2011). Dendritic cells and hepatocytes use distinct pathways to process protective antigen from Plasmodium in vivo. PLoS Pathog. 7:e1001318. doi: 10.1371/journal.ppat.1001318.
32. Conteh, S., Chattopadhyay, R., Anderson, C., and Hoffman, S. L. (2010). Plasmodium yoelii-Infected A. stephensi inefficiently transmit malaria compared to intravenous route. PLoS ONE 5:e8947. doi: 10.1371/journal.pone.0008947.
33. Crispe, I. N. (2009). The liver as a lymphoid organ. Annu. Rev. Immunol. 27, 147-163. doi: 10.1146/annurev.immunol.021908.132629.
34. Crispe, I. N. (2011). Liver antigen-presenting cells. J. Hepatol. 54, 357-365. doi: 10.1016/j.jhep.2010.10.005.
35. Crispe, I. N. (2014). APC licensing and CD4+T cell help in liver-stage malaria. Front. Microbiol. 5:617. doi: 10.3389/fmicb.2014.00617.
36. Crispe, I. N., Giannandrea, M., Klein, I., John, B., Sampson, B., and Wuensch, S. (2006). Cellular and molecular mechanisms of liver tolerance. Immunol. Rev. 213, 101-118. doi: 10.1111/j.1600-065X.2006.00435.x.
37. Danforth, H. D., Aikawa, M., Cochrane, A. H., and Nussenzweig, R. S. (1980). Sporozoites of mammalian malaria: attachment to, interiorization and fate within macrophages. J. Protozool. 27, 193-202. doi: 10.1111/j.1550-7408.1980.tb04680.x.
38. Depoil, D., Zaru, R., Guiraud, M., Chauveau, A., Harriague, J., Bismuth, G., et al. (2005). Immunological synapses are versatile structures enabling selective T cell polarization. Immunity 22, 185-194. doi: 10.1016/j.immuni.2004.12.010.
39. Deschermeier, C., Hecht, L. S., Bach, F., Rutzel, K., Stanway, R. R., Nagel, A., et al. (2012). Mitochondrial lipoic acid scavenging is essential for Plasmodium berghei liver stage development. Cell. Microbiol. 14, 416-430. doi: 10.1111/j.1462-5822.2011.01729.x.
40. Doolan, D. L., and Hoffman, S. L. (2000). The complexity of protective immunity against liver-stage malaria. J. Immunol. 165, 1453-1462. doi: 10.4049/jimmunol.165.3.1453.
41. Doolan, D. L., and Martinez-Alier, N. (2006). Immune response to pre-erythrocytic stages of malaria parasites. Curr. Mol. Med. 6, 169-185. doi: 10.2174/156652406776055249.
42. Dups, J. N., Pepper, M., and Cockburn, I. A. (2014). Antibody and B cell responses to Plasmodium sporozoites. Front. Microbiol. 5:625. doi: 10.3389/fmicb.2014.00625.
43. Dustin, M. L. (2005). A dynamic view of the immunological synapse. Semin. Immunol. 17, 400-410. doi: 10.1016/j.smim.2005.09.002.
44. Ebrahimkhani, M. R., Mohar, I., and Crispe, I. N. (2011). Cross-presentation of antigen by diverse subsets of murine liver cells. Hepatology 54, 1379-1387. doi: 10.1002/hep.24508.
45. + T cell immunity. Science 334, 475-480. doi: 10.1126/science.1211548.
46. Espinoza Mora Mdel, R., Steeg, C., Tartz, S., Heussler, V., Sparwasser, T., Link, A., et al. (2014). Depletion of regulatory T cells augments a vaccine-induced T effector cell response against the liver-stage of malaria but fails to increase memory. PLoS ONE 9:e104627. doi: 10.1371/journal.pone.0104627.
47. + T-cell immunity to human malaria induced by chimpanzee adenovirus-MVA immunisation. Nat. Commun. 4, 2836. doi: 10.1038/ncomms3836.
48. Faroudi, M., Utzny, C., Salio, M., Cerundolo, V., Guiraud, M., Muller, S., et al. (2003). Lytic versus stimulatory synapse in cytotoxic T lymphocyte/target cell interaction: manifestation of a dual activation threshold. Proc. Natl. Acad. Sci. U.S.A. 100, 14145-14150. doi: 10.1073/pnas.2334336100.
49. Ferreira, A., Schofield, L., Enea, V., Schellekens, H., Van Der Meide, P., Collins, W. E., et al. (1986). Inhibition of development of exoerythrocytic forms of malaria parasites by gamma-interferon. Science 232, 881-884. doi: 10.1126/science.3085218.
50. Frevert, U. (1999). Heparan sulphate and RNA-binding sites in the malaria circumsporozoite protein. Biochem. Soc. Trans. 27, 482-487.
51. Frevert, U. (2004). Sneaking in through the back entrance: the biology of malaria liver stages. Trends Parasitol. 20, 417-424. doi: 10.1016/j.pt.2004.07.007.
52. Frevert, U., Engelmann, S., Zougbédé, S., Stange, J., Ng, B., Matuschewski, K., et al. (2005). Intravital observation of Plasmodium berghei sporozoite infection of the liver. PLoS Biol. 3:e192.
53. Frevert, U., Galinski, M. R., Hügel, F.-U., Allon, N., Schreier, H., Smulevitch, S., et al. (1998). Malaria circumsporozoite protein inhibits protein synthesis in mammalian cells. EMBO J. 17, 3816-3826. doi: 10.1093/emboj/17.14.3816.
54. Frevert, U., Moreno, A., Calvo Calle, J. M., Klotz, C., and Nardin, E. (2008a). Imaging human cytotoxic CD4+ T cells specific for Plasmodium falciparum circumsporozoite protein. Int. J. Parasitol. 39, 119-132. doi: 10.1016/j.ijpara.2008.06.014.
55. Frevert, U., Usynin, I., Baer, K., and Klotz, C. (2008b). Plasmodium sporozoite passage across the sinusoidal cell layer. Subcell. Biochem. 47, 182-197. doi: 10.1007/978-0-387-78267-6_15.
56. Frevert, U., and Nacer, A. (2013). Immunobiology of Plasmodium in liver and brain. Parasite Immunol. 35, 267-282. doi: 10.1111/pim.12039.
57. Frevert, U., Nacer, A., Cabrera, M., Movila, A., and Leberl, M. (2014). Imaging Plasmodium immunobiology in the liver, brain, and lung. Parasitol. Int. 63, 171-186. doi: 10.1016/j.parint.2013.09.013.
58. Frevert, U., and Nardin, E. (2008). Cellular effector mechanisms against Plasmodium liver stages. Cell. Microbiol. 10, 1956-1967. doi: 10.1111/j.1462-5822.2008.01211.x.
59. Frevert, U., Sinnis, P., Esko, J. D., and Nussenzweig, V. (1996). Cell surface glycosaminoglycans are not obligatory for Plasmodium berghei invasion in vitro. Mol. Biochem. Parasitol. 76, 257-266. doi: 10.1016/0166-6851(95)02563-4.
60. 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. doi: 10.1111/j.1462-5822.2006.00777.x.
61. Friedl, P., and Weigelin, B. (2008). Interstitial leukocyte migration and immune function. Nat. Immunol. 9, 960-969. doi: 10.1038/ni.f.212.
62. Giannandrea, M., Pierce, R. H., and Crispe, I. N. (2009). Indirect action of tumor necrosis factor-alpha in liver injury during the CD8+ T cell response to an adeno-associated virus vector in mice. Hepatology 49, 2010-2020. doi: 10.1002/hep.22869.
63. Gonzalez-Aseguinolaza, G., De Oliveira, C., Tomaska, M., Hong, S., Bruna-Romero, O., Nakayama, T., et al. (2000). α-galactosylceramide-activated Vα14 natural killer T cells mediate protection against murine malaria. Proc. Natl. Acad. Sci. U.S.A. 97, 8461-8466. doi: 10.1073/pnas.97.15.8461.
64. Graewe, S., Stanway, R. R., Rennenberg, A., and Heussler, V. T. (2012). Chronicle of a death foretold: Plasmodium liver stage parasites decide on the fate of the host cell. FEMS Microbiol. Rev. 36, 111-130. doi: 10.1111/j.1574-6976.2011.00297.x.
65. Greenway, C. V., and Lautt, W. W. (1970). Effects of hepatic venous pressure on transsinusoidal fluid transfer in the liver of the anesthetized cat. Circ. Res. 26, 697-703. doi: 10.1161/01.RES.26.6.697.
66. Groux, H., Bigler, M., De Vries, J. E., and Roncarolo, M. G. (1996). Interleukin-10 induces a long-term antigen-specific anergic state in human CD4+ T cells. J. Exp. Med. 184, 19-29. doi: 10.1084/jem.184.1.19.
67. Gruner, A. C., Snounou, G., Brahimi, K., Letourneur, F., Renia, L., and Druilhe, P. (2003). Pre-erythrocytic antigens of Plasmodium falciparum: from rags to riches? Trends Parasitol. 19, 74-78. doi: 10.1016/S1471-4922(02)00067-3.
68. Guerin-Marchand, C., Druilhe, P., Galey, B., Londono, A., Patarapotikul, J., Beaudoin, R. L., et al. (1987). A liver-stage-specific antigen of Plasmodium falciparum characterized by gene cloning. Nature 329, 164-167. doi: 10.1038/329164a0.
69. Guidotti, L. G. (2002). The role of cytotoxic T cells and cytokines in the control of hepatitis B virus infection. Vaccine 20(Suppl. 4), A80-A82. doi: 10.1016/S0264-410X(02)00392-4.
70. Guidotti, L. G., and Chisari, F. V. (1996). To kill or to cure: options in host defense against viral infection. Curr. Opin. Immunol. 8, 478-483. doi: 10.1016/S0952-7915(96)80034-3.
71. Guidotti, L. G., and Iannacone, M. (2013). Effector CD8 T cell trafficking within the liver. Mol. Immunol. 55, 94-99. doi: 10.1016/j.molimm.2012.10.032.
72. Guidotti, L. G., Rochford, R., Chung, J., Shapiro, M., Purcell, R., and Chisari, F. V. (1999). Viral clearance without destruction of infected cells during acute HBV infection. Science 284, 825-829. doi: 10.1126/science.284.5415.825.
73. Henriksen, J. H., Horn, T., and Christoffersen, P. (1984). The blood-lymph barrier in the liver. A review based on morphological and functional concepts of normal and cirrhotic liver. Liver 4, 221-232. doi: 10.1111/j.1600-0676.1984.tb00932.x.
74. Herbst, S., Schaible, U. E., and Schneider, B. E. (2011). Interferon gamma activated macrophages kill mycobacteria by nitric oxide induced apoptosis. PLoS ONE 6:e19105. doi: 10.1371/journal.pone.0019105.
75. Hoffman, S. L., Crutcher, J. M., Puri, S. K., Ansari, A. A., Finkelman, F., Gately, M. K., et al. (1997). Sterile protection of monkeys against malaria after administration of interleukin-12. Nat. Med. 3, 80-83. doi: 10.1038/nm0197-80.
76. high phenotype, poor CTL function and cell death. J. Hepatol. 57, 830-836. doi: 10.1016/j.jhep.2012.05.015.
77. Hügel, F.-U., Pradel, G., and Frevert, U. (1996). Release of malaria circumsporozoite protein into the host cell cytoplasm and interaction with ribosomes. Mol. Biochem. Parasitol. 81, 151-170. doi: 10.1016/0166-6851(96)02701-6.
78. Huse, M., Lillemeier, B. F., Kuhns, M. S., Chen, D. S., and Davis, M. M. (2006). T cells use two directionally distinct pathways for cytokine secretion. Nat. Immunol. 7, 247-255. doi: 10.1038/ni1304.
79. Inokuchi, S., Tsukamoto, H., Park, E., Liu, Z. X., Brenner, D. A., and Seki, E. (2011). Toll-like receptor 4 mediates alcohol-induced steatohepatitis through bone marrow-derived and endogenous liver cells in mice. Alcohol. Clin. Exp. Res. 35, 1509-1518. doi: 10.1111/j.1530-0277.2011.01487.x.
80. + T cell effector functions after antigen recognition in the liver. Immunity 23, 53-63. doi: 10.1016/j.immuni.2005.05.005.
81. Itoe, M. A., Sampaio, J. L., Cabal, G. G., Real, E., Zuzarte-Luis, V., March, S., et al. (2014). Host cell phosphatidylcholine is a key mediator of malaria parasite survival during liver stage infection. Cell Host Microbe 16, 778-786. doi: 10.1016/j.chom.2014.11.006.
82. Jenne, C. N., and Kubes, P. (2013). Immune surveillance by the liver. Nat. Immunol. 14, 996-1006. doi: 10.1038/ni.2691.
83. +T cells against liver-stage malaria. PLoS ONE 4:e5075. doi: 10.1371/journal.pone.0005075.
84. Jobe, O., Lumsden, J., Mueller, A. K., Williams, J., Silva-Rivera, H., Kappe, S. H., et al. (2007). Genetically attenuated Plasmodium berghei liver stages induce sterile protracted protection that is mediated by major histocompatibility complex Class I-dependent interferon-γ-producing CD8+ T cells. J. Infect. Dis. 196, 599-607. doi: 10.1086/519743.
85. Kafrouni, M. I., Brown, G. R., and Thiele, D. L. (2001). Virally infected hepatocytes are resistant to perforin-dependent CTL effector mechanisms. J. Immunol. 167, 1566-1574. doi: 10.4049/jimmunol.167.3.1566.
86. Kaushansky, A., Ye, A. S., Austin, L. S., Mikolajczak, S. A., Vaughan, A. M., Camargo, N., et al. (2013). Suppression of host p53 is critical for Plasmodium liver-stage infection. Cell Rep. 3, 630-637. doi: 10.1016/j.celrep.2013.02.010.
87. Keefe, D., Shi, L., Feske, S., Massol, R., Navarro, F., Kirchhausen, T., et al. (2005). Perforin triggers a plasma membrane-repair response that facilitates CTL induction of apoptosis. Immunity 23, 249-262. doi: 10.1016/j.immuni.2005.08.001.
88. Kennedy, D. W., and Abkowitz, J. L. (1997). Kinetics of central nervous system microglial and macrophage engraftment: analysis using a transgenic bone marrow transplantation model. Blood 90, 986-993.
89. Khan, S. M., Janse, C. J., Kappe, S. H., and Mikolajczak, S. A. (2012). Genetic engineering of attenuated malaria parasites for vaccination. Curr. Opin. Biotechnol. 23, 1-9. doi: 10.1016/j.copbio.2012.04.003.
90. Khan, Z. M., and Vanderberg, J. P. (1991a). Eosinophil-rich, granulomatous inflammatory response to Plasmodium berghei hepatic schizonts in non-immunized rats is age-related. Am. J. Trop. Med. Hyg. 45, 190-201.
91. Khan, Z. M., and Vanderberg, J. P. (1991b). Role of host cellular response in differential susceptibility of nonimmunized BALB/C mice to Plasmodium berghei and Plasmodium yoelii sporozoites. Infect. Immun. 59, 2529-2534.
92. + T cells specific for a malaria cytoplasmic antigen form clusters around infected hepatocytes and are protective at the liver stage of infection. Infect Immun. 81, 3825-3834. doi: 10.1128/IAI.00570-13.
93. Klein, I., Cornejo, J. C., Polakos, N. K., John, B., Wuensch, S. A., Topham, D. J., et al. (2007). Kupffer cell heterogeneity: functional properties of bone marrow derived and sessile hepatic macrophages. Blood 110, 4077-4085. doi: 10.1182/blood-2007-02-073841.
94. Klotz, C., and Frevert, U. (2008). Plasmodium yoelii sporozoites modulate cytokine profile and induce apoptosis in murine Kupffer cells. Int. J. Parasitol. 38, 1639-1650. doi: 10.1016/j.ijpara.2008.05.018.
95. Klotz, F. W., Scheller, L. F., Seguin, M. C., Kumar, N., Marletta, M. A., Green, S. J., et al. (1995). Co-localization of inducible-nitric oxide synthase and Plasmodium berghei in hepatocytes from rats immunized with irradiated sporozoites. J. Immunol. 154, 3391-3395.
96. Knolle, P. A., and Gerken, G. (2000). Local control of the immune response in the liver. Immunol. Rev. 174, 21-34. doi: 10.1034/j.1600-0528.2002.017408.x.
97. Knolle, P. A., and Limmer, A. (2001). Neighborhood politics: the immunoregulatory function of organ-resident liver endothelial cells. Trends Immunol. 22, 432-437. doi: 10.1016/S1471-4906(01)01957-3.
98. Knolle, P. A., Schlaak, J., Uhrig, A., Kempf, P., Meyer Zum Büschenfelde, K.-H., and Gerken, G. (1995). Human Kupffer cells secrete IL-10 in response to lipopolysaccharide (LPS) challenge. J. Hepatol. 22, 226-229. doi: 10.1016/0168-8278(95)80433-1.
99. Kupfer, A., Mosmann, T. R., and Kupfer, H. (1991). Polarized expression of cytokines in cell conjugates of helper T cells and splenic B cells. Proc. Natl. Acad. Sci. U.S.A. 88, 775-779. doi: 10.1073/pnas.88.3.775.
100. Labaied, M., Jayabalasingham, B., Bano, N., Cha, S. J., Sandoval, J., Guan, G., et al. (2011). Plasmodium salvages cholesterol internalized by LDL and synthesized de novo in the liver. Cell. Microbiol. 13, 569-586. doi: 10.1111/j.1462-5822.2010.01555.x.
101. Lacadena, J., Alvarez-Garcia, E., Carreras-Sangra, N., Herrero-Galan, E., Alegre-Cebollada, J., Garcia-Ortega, L., et al. (2007). Fungal ribotoxins: molecular dissection of a family of natural killers. FEMS Microbiol. Rev. 31, 212-237. doi: 10.1111/j.1574-6976.2006.00063.x.
102. Laine, G. A., Hall, J. T., Laine, S. H., and Granger, J. (1979). Transsinusoidal fluid dynamics in canine liver during venous hypertension. Circ. Res. 45, 317-323. doi: 10.1161/01.RES.45.3.317.
103. - myeloid dendritic cells mediate regulatory T cell recruitment in response to G-CSF treatment. J. Immunol. 191, 2266-2272. doi: 10.4049/jimmunol.1202307.
104. Leiriao, P., Mota, M. M., and Rodriguez, A. (2005). Apoptotic Plasmodium-infected hepatocytes provide antigens to liver dendritic cells. J. Infect. Dis. 191, 1576-1581. doi: 10.1086/429635.
105. Lieberman, J. (2003). The ABCs of granule-mediated cytotoxicity: new weapons in the arsenal. Nat. Rev. Immunol. 3, 361-370. doi: 10.1038/nri1083.
106. Liehl, P., Zuzarte-Luis, V., Chan, J., Zillinger, T., Baptista, F., Carapau, D., et al. (2014). Host-cell sensors for Plasmodium activate innate immunity against liver-stage infection. Nat. Med. 20, 47-53. doi: 10.1038/nm.3424.
107. Limmer, A., Ohl, J., Kurts, C., Ljunggren, H. G., Reiss, Y., Groettrup, M., et al. (2000). Efficient presentation of exogenous antigen by liver endothelial cells to CD8+ T cells results in antigen-specific T-cell tolerance. Nat. Med. 6, 1348-1354. doi: 10.1038/82161.
108. Limmer, A., Ohl, J., Wingender, G., Berg, M., Jungerkes, F., Schumak, B., et al. (2005). Cross-presentation of oral antigens by liver sinusoidal endothelial cells leads to CD8 T cell tolerance. Eur. J. Immunol. 35, 2970-2981. doi: 10.1002/eji.200526034.
109. Lopez, J. A., Susanto, O., Jenkins, M. R., Lukoyanova, N., Sutton, V. R., Law, R. H., et al. (2013). Perforin forms transient pores on the target cell plasma membrane to facilitate rapid access of granzymes during killer cell attack. Blood 121, 2659-2668. doi: 10.1182/blood-2012-07-446146.
110. Luder, C. G., Stanway, R. R., Chaussepied, M., Langsley, G., and Heussler, V. T. (2009). Intracellular survival of apicomplexan parasites and host cell modification. Int. J. Parasitol. 39, 163-173. doi: 10.1016/j.ijpara.2008.09.013.
111. Mackay, I. R. (2002). Hepatoimmunology: a perspective. Immunol. Cell Biol. 80, 36-44. doi: 10.1046/j.1440-1711.2002.01063.x.
112. Magari, S. (1990). Hepatic lymphatic system: structure and function. J. Gastroenterol. Hepatol. 5, 82-93. doi: 10.1111/j.1440-1746.1990.tb01769.x.
113. + T cell cytotoxic activity. J. Immunol. 182, 5560-5569. doi: 10.4049/jimmunol.0803945.
114. Marchand, C., and Druilhe, P. (1990). How to select Plasmodium falciparum pre-erythrocytic antigens in an expression library without defined probe. Bull. World Health Organ. 68(Suppl.), 158-164.
115. Martin-Orozco, N., Chung, Y., Chang, S. H., Wang, Y. H., and Dong, C. (2009). Th17 cells promote pancreatic inflammation but only induce diabetes efficiently in lymphopenic hosts after conversion into Th1 cells. Eur. J. Immunol. 39, 216-224. doi: 10.1002/eji.200838475.
116. Marzo, A. L., Yagita, H., and Lefrancois, L. (2007). Cutting edge: migration to nonlymphoid tissues results in functional conversion of central to effector memory CD8 T cells. J. Immunol. 179, 36-40. doi: 10.4049/jimmunol.179.1.36.
117. Mauduit, M., See, P., Peng, K., Renia, L., and Ginhoux, F. (2012). Dendritic cells and the malaria pre-erythrocytic stage. Immunol. Res. 53, 115-126. doi: 10.1007/s12026-012-8269-7.
118. McCall, M. B., and Sauerwein, R. W. (2010). Interferon-γ-central mediator of protective immune responses against the pre-erythrocytic and blood stage of malaria. J. Leukoc. Biol. 88, 1131-1143. doi: 10.1189/jlb.0310137.
119. McConkey, S. J., Reece, W. H., Moorthy, V. S., Webster, D., Dunachie, S., Butcher, G., et al. (2003). Enhanced T-cell immunogenicity of plasmid DNA vaccines boosted by recombinant modified vaccinia virus Ankara in humans. Nat. Med. 9, 729-735. doi: 10.1038/nm881.
120. Meis, J. F., and Verhave, J. P. (1988). Exoerythrocytic development of malarial parasites. Adv. Parasitol. 27, 1-61. doi: 10.1016/S0065-308X(08)60352-8.
121. Mellouk, S., Green, S. J., Nacy, C. A., and Hoffman, S. L. (1991). IFN-γ inhibits development of Plasmodium berghei exoerythrocytic stages in hepatocytes by an L-arginine-dependent effector mechanism. J. Immunol. 146, 3971-3976.
122. Mellouk, S., Hoffman, S. L., Liu, Z. Z., De La Vega, P., Billiar, T. R., and Nussler, A. K. (1994). Nitric oxide-mediated antiplasmodial activity in human and murine hepatocytes induced by gamma interferon and the parasite itself: enhancement by exogenous tetrahydrobiopterin. Infect. Immun. 62, 4043-4046.
123. Mellouk, S., Maheshwari, R. K., Rhodes-Feuilette, A., Beaudoin, R. L., Berbibuier, N., Matile, H., et al. (1987). Inhibitory activity of interferons and interleukin 1 on the development of Plasmodium falciparum in human hepatocyte cultures. J. Immunol. 139, 4192-4195.
124. Miller, J. L., Sack, B. K., Baldwin, M., Vaughan, A. M., and Kappe, S. H. (2014). Interferon-mediated innate immune responses against malaria parasite liver stages. Cell Rep. 7, 436-447. doi: 10.1016/j.celrep.2014.03.018.
125. Moormann, A. M., Sumba, P. O., Tisch, D. J., Embury, P., King, C. H., Kazura, J. W., et al. (2009). Stability of interferon-gamma and interleukin-10 responses to Plasmodium falciparum liver stage antigen 1 and thrombospondin-related adhesive protein immunodominant epitopes in a highland population from Western Kenya. Am. J. Trop. Med. Hyg. 81, 489-495.
126. 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. doi: 10.1126/science.291.5501.141.
127. Mueller, A. K., Deckert, M., Heiss, K., Goetz, K., Matuschewski, K., and Schluter, D. (2007). Genetically attenuated Plasmodium berghei liver stages persist and elicit sterile protection primarily via CD8 T cells. Am. J. Pathol. 171, 107-115. doi: 10.2353/ajpath.2007.060792.
128. Nagy, L. E. (2003). Recent insights into the role of the innate immune system in the development of alcoholic liver disease. Exp. Biol. Med. (Maywood) 228, 882-890.
129. Nardin, E. (2010). The past decade in malaria synthetic peptide vaccine clinical trials. Hum. Vaccin. 6, 27-38.
130. Nganou-Makamdop, K., and Sauerwein, R. W. (2013). Liver or blood-stage arrest during malaria sporozoite immunization: the later the better? Trends Parasitol. doi: 10.1016/j.pt.2013.03.008 [Epub ahead of print].
131. Nüssler, A., Pied, S., Goma, J., Rénia, L., Miltgen, F., Grau, G. E., et al. (1991). TNF inhibits malaria hepatic stages in vitro via synthesis of IL-6. Int. Immunol. 3, 317-321. doi: 10.1093/intimm/3.4.317.
132. Nussler, A. K., Renia, L., Pasquetto, V., Miltgen, F., Matile, H., and Mazier, D. (1993). In vivo induction of the nitric oxide pathway in hepatocytes after injection with irradiated malaria sporozoites, malaria blood parasites or adjuvants. Eur. J. Immunol. 23, 882-887. doi: 10.1002/eji.1830230417.
133. Ocana-Morgner, C., Mota, M. M., and Rodriguez, A. (2003). Malaria blood stage suppression of liver stage immunity by dendritic cells. J. Exp. Med. 197, 143-151. doi: 10.1084/jem.20021072.
134. Ohtani, O., and Ohtani, Y. (2008). Lymph circulation in the liver. Anat. Rec. (Hoboken) 291, 643-652. doi: 10.1002/ar.20681.
135. Oliveira, G. A., Kumar, K. A., Calvo-Calle, J. M., Othoro, C., Altszuler, D., Nussenzweig, V., et al. (2008). Class II-restricted protective immunity induced by malaria sporozoites. Infect. Immun. 76, 1200-1206. doi: 10.1128/IAI.00566-07.
136. Othoro, C., Johnston, D., Lee, R., Soverow, J., Bystryn, J.-C., and Nardin, E. (2009). Enhanced immunogenicity of Plasmodium falciparum peptide vaccines using a topical adjuvant containing a potent synthetic Toll-like receptor 7 agonist, imiquimod. Infect. Immun. 77, 739-748. doi: 10.1128/IAI.00974-08.
137. Overstreet, M. G., Cockburn, I. A., Chen, Y. C., and Zavala, F. (2008). Protective CD8 T cells against Plasmodium liver stages: immunobiology of an 'unnatural' immune response. Immunol. Rev. 225, 272-283. doi: 10.1111/j.1600-065X.2008.00671.x.
138. Pfefferkorn, E. R. (1984). Interferon gamma blocks the growth of Toxoplasma gondii in human fibroblasts by inducing the host cells to degrade tryptophan. Proc. Natl. Acad. Sci. U.S.A. 81, 908-912. doi: 10.1073/pnas.81.3.908.
139. Pfefferkorn, E. R. (1986). Interferon gamma and the growth of Toxoplasma gondii in fibroblasts. Ann. Inst. Pasteur. Microbiol. 137A, 348-352. doi: 10.1016/S0769-2609(86)80047-3.
140. Pfefferkorn, E. R., Eckel, M., and Rebhun, S. (1986). Interferon-gamma suppresses the growth of Toxoplasma gondii in human fibroblasts through starvation for tryptophan. Mol. Biochem. Parasitol. 20, 215-224. doi: 10.1016/0166-6851(86)90101-5.
141. Pied, S., Civas, A., Berlot-Picard, F., Rénia, L., Miltgen, F., Gentilini, M., et al. (1992). IL-6 induced by IL-1 inhibits malaria pre-erythrocytic stages but its secretion is down-regulated by the parasite. J. Immunol. 146, 197-201.
142. Pied, S., Rénia, L., Nüssler, A., Miltgen, F., and Mazier, D. (1991). Inhibitory activity of IL-6 on malaria hepatic stages. Parasite Immunol. 13, 211-217. doi: 10.1111/j.1365-3024.1991.tb00276.x.
143. Pipkin, M. E., and Lieberman, J. (2007). Delivering the kiss of death: progress on understanding how perforin works. Curr. Opin. Immunol. 19, 301-308. doi: 10.1016/j.coi.2007.04.011.
144. Pradel, G., and Frevert, U. (2001). Plasmodium sporozoites actively enter and pass through Kupffer cells prior to hepatocyte invasion. Hepatology 33, 1154-1165. doi: 10.1053/jhep.2001.24237.
145. Pradel, G., Garapaty, S., and Frevert, U. (2002). Proteoglycans mediate malaria sporozoite targeting to the liver. Mol. Microbiol. 45, 637-651. doi: 10.1046/j.1365-2958.2002.03057.x.
146. Pradel, G., Garapaty, S., and Frevert, U. (2004). Kupffer and stellate cell proteoglycans mediate malaria sporozoite targeting to the liver. Comp. Hepatol. 3(Suppl. 1), S47. doi: 10.1046/j.1365-2958.2002.03057.x.
147. Purcell, L. A., Wong, K. A., Yanow, S. K., Lee, M., Spithill, T. W., and Rodriguez, A. (2008). Chemically attenuated Plasmodium sporozoites induce specific immune responses, sterile immunity and cross-protection against heterologous challenge. Vaccine 26, 4880-4884. doi: 10.1016/j.vaccine.2008.07.017.
148. Racanelli, V., and Rehermann, B. (2006). The liver as an immunological organ. Hepatology 43, S54-S62. doi: 10.1002/hep.21060.
149. + T cell responses. PLoS Pathog. 11:e1004637. doi: 10.1371/journal.ppat.1004637.
150. Rankin, K. E., Graewe, S., Heussler, V. T., and Stanway, R. R. (2010). Imaging liver-stage malaria parasites. Cell. Microbiol. 12, 569-579. doi: 10.1111/j.1462-5822.2010.01454.x.
151. Reid, L. M., Fiorino, A. S., Sigal, S. H., Brill, S., and Holst, P. A. (1992). Extracellular matrix gradients in the space of Disse: relevance to liver biology. Hepatology 15, 1198-1203. doi: 10.1002/hep.1840150635.
152. Renggli, J., Hahne, M., Matile, H., Betschart, B., Tschopp, J., and Corradin, G. (1997). Elimination of P. berghei liver stages is independent of Fas (CD95/Apo-I) or perforin-mediated cytotoxicity. Parasite Immunol. 19, 145-148. doi: 10.1046/j.1365-3024.1997.d01-190.x.
153. Renia, L., Gruner, A. C., Mauduit, M., and Snounou, G. (2013). Vaccination using normal live sporozoites under drug treatment. Methods Mol. Biol. 923, 567-576. doi: 10.1007/978-1-62703-026-7_39.
154. Rennenberg, A., Lehmann, C., Heitmann, A., Witt, T., Hansen, G., Nagarajan, K., et al. (2010). Exoerythrocytic Plasmodium parasites secrete a cysteine protease inhibitor involved in sporozoite invasion and capable of blocking cell death of host hepatocytes. PLoS Pathog. 6:e1000825. doi: 10.1371/journal.ppat.1000825.
155. + T cell clones correlates with their levels of expression of adhesion molecules. J. Exp. Med. 175, 895-905. doi: 10.1084/jem.175.4.895.
156. + cytolytic T cell clones derived against the Plasmodium yoelii circumsporozoite protein protect against malaria. Int. Immunol. 3, 579-585. doi: 10.1093/intimm/3.6.579.
157. Roland, C. R., Walp, L., Stack, R. M., and Flye, M. W. (1994). Outcome of Kupffer cell antigen presentation to a cloned murine Th1 lymphocyte depends on the inducibility of nitric oxide synthase by IFN-gamma. J. Immunol. 153, 5453-5464.
158. Russell, J. H., and Ley, T. J. (2002). Lymphocyte-mediated cytotoxicity. Annu. Rev. Immunol. 20, 323-370. doi: 10.1146/annurev.immunol.20.100201.131730.
159. Sanderson, N. S., Puntel, M., Kroeger, K. M., Bondale, N. S., Swerdlow, M., Iranmanesh, N., et al. (2012). Cytotoxic immunological synapses do not restrict the action of interferon-gamma to antigenic target cells. Proc. Natl. Acad. Sci. U.S.A. 109, 7835-7840. doi: 10.1073/pnas.1116058109.
160. Sangani, B., Sukumaran, P. K., Mahadik, C., Yagnik, H., Telang, S., Vas, F., et al. (1990). Thalassemia in Bombay: the role of medical genetics in developing countries. Bull. World Health Organ. 68, 75-81.
161. Sato, T., Yamamoto, H., Sasaki, C., and Wake, K. (1998). Maturation of rat dendritic cells during intrahepatic translocation evaluated using monoclonal antibodies and electron microscopy. Cell Tissue Res. 294, 503-514. doi: 10.1007/s004410051201.
162. Scheller, L. F., Wirtz, R. A., and Azad, A. F. (1994). Susceptibility of different strains of mice to hepatic infection with Plasmodium berghei. Infect. Immun. 62, 4844-4847.
163. + T cells. Nat. Immunol. 14, 509-513. doi: 10.1038/ni.2568.
164. Schmidt, N. W., Butler, N. S., Badovinac, V. P., and Harty, J. T. (2010). Extreme CD8 T cell requirements for anti-malarial liver-stage immunity following immunization with radiation attenuated sporozoites. PLoS Pathog. 6:e1000998. doi: 10.1371/journal.ppat.1000998.
165. Schmidt, N. W., Butler, N. S., and Harty, J. T. (2011). Plasmodium-host interactions directly influence the threshold of memory CD8 T cells required for protective immunity. J. Immunol. 186, 5873-5884. doi: 10.4049/jimmunol.1100194.
166. Schofield, L., Ferreira, A., Altszuler, R., Nussenzweig, V., and Nussenzweig, R. S. (1987a). Interferon-gamma inhibits the intrahepatocytic development of malaria parasites in vitro. J. Immunol. 139, 2020-2025.
167. + T cells and antibodies required for immunity to malaria sporozoites. Nature 330, 664-666. doi: 10.1038/330664a0.
168. Sedegah, M., Finkelman, F., and Hoffman, S. L. (1994). Interleukin 12 induction of interferon gamma-dependent protection against malaria. Proc. Natl. Acad. Sci. U.S.A. 91, 10700-10702. doi: 10.1073/pnas.91.22.10700.
169. Seder, R. A., Chang, L. J., Enama, M. E., Zephir, K. L., Sarwar, U. N., Gordon, I. J., et al. (2013). Protection against malaria by intravenous immunization with a nonreplicating sporozoite vaccine. Science 341, 1359-1365. doi: 10.1126/science.1241800.
170. + T cells. J. Exp. Med. 180, 353-358. doi: 10.1084/jem.180.1.353.
171. Seki, E., De Minicis, S., Gwak, G. Y., Kluwe, J., Inokuchi, S., Bursill, C. A., et al. (2009). CCR1 and CCR5 promote hepatic fibrosis in mice. J. Clin. Invest. 119, 1858-1870. doi: 10.1172/JCI37444.
172. Sheth, K., and Bankey, P. (2001). The liver as an immune organ. Curr. Opin. Crit. Care 7, 99-104. doi: 10.1097/00075198-200104000-00008.
173. Shi, C., Velazquez, P., Hohl, T. M., Leiner, I., Dustin, M. L., and Pamer, E. G. (2010). Monocyte trafficking to hepatic sites of bacterial infection is chemokine independent and directed by focal intercellular adhesion molecule-1 expression. J. Immunol. 184, 6266-6274. doi: 10.4049/jimmunol.0904160.
174. Shin, S. C. J., Vanderberg, J. P., and Terzakis, J. A. (1982). Direct infection of hepatocytes by sporozoites of Plasmodium berghei. J. Protozool. 29, 448-454. doi: 10.1111/j.1550-7408.1982.tb05431.x.
175. Silva, J. S., Machado, F. S., and Martins, G. A. (2003). The role of nitric oxide in the pathogenesis of Chagas disease. Front. Biosci. 8, s314-s325. doi: 10.2741/1012.
176. Singh, A. P., Buscaglia, C. A., Wang, Q., Levay, A., Nussenzweig, D. R., Walker, J. R., et al. (2007). Plasmodium circumsporozoite protein promotes the development of the liver stages of the parasite. Cell 131, 492-504. doi: 10.1016/j.cell.2007.09.013.
177. Smith, J. E., and Alexander, J. (1986). Evasion of macrophage microbicidal mechanisms by mature sporozoites of Plasmodium yoelii yoelii. Parasitology 93, 33-38. doi: 10.1017/S0031182000049805.
178. Spaccapelo, R., Naitza, S., Robson, K. J. H., and Crisanti, A. (1997). Thrombospondin-related adhesive protein (TRAP) of Plasmodium berghei and parasite motility. Lancet 350, 335. doi: 10.1016/S0140-6736(97)24031-6.
179. Steers, N., Schwenk, R., Bacon, D. J., Berenzon, D., Williams, J., and Krzych, U. (2005). The immune status of Kupffer cells profoundly influences their responses to infectious Plasmodium berghei sporozoites. Eur. J. Immunol. 35, 2335-2346. doi: 10.1002/eji.200425680.
180. Steinhoff, G. (1990). Major histocompatibility complex antigens in human liver transplants. J. Hepatol. 11, 9-15. doi: 10.1016/0168-8278(90)90264-R.
181. Steinhoff, G., Wonigeit, K., and Pichlmayr, R. (1988). Analysis of seffluential changes in major histocompatibility complex expression in human liver grafts after transplantation. Transplantation 45, 394-401. doi: 10.1097/00007890-198802000-00030.
182. Steiniger, B., Falk, P., and Van Der Meide, P. H. (1988). Interferon-γ in vivo. Induction and loss of class II MHC antigens and immature myelomonocytic cells in rat organs. Eur. J. Immunol. 18, 661-669. doi: 10.1002/eji.1830180502.
183. Stewart, M. J., and Vanderberg, J. P. (1988). Malaria sporozoites leave behind trails of circumsporozoite protein during gliding motility. J. Protozool. 35, 389-393. doi: 10.1111/j.1550-7408.1988.tb04115.x.
184. 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. doi: 10.1111/j.1550-7408.1991.tb01379.x.
185. Stewart, M. J., and Vanderberg, J. P. (1992). Electron microscopic analysis of circumsporozoite protein trail formation by gliding malaria sporozoites. J. Protozool. 39, 663-671. doi: 10.1111/j.1550-7408.1992.tb04446.x.
186. Stirpe, F., Barbieri, L., Battelli, M. G., Soria, M., and Lappi, D. A. (1992). Ribosome-inactivating proteins from plants: present status and future prospects. Biotechnology 10, 405-412. doi: 10.1038/nbt0492-405.
187. 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 (New York, N.Y.) 313, 1287-1290. doi: 10.1126/science.1129720.
188. Sumpter, T. L., Abe, M., Tokita, D., and Thomson, A. W. (2007). Dendritic cells, the liver, and transplantation. Hepatology 46, 2021-2031. doi: 10.1002/hep.21974.
189. Takacs, A. C., Swierzy, I. J., and Luder, C. G. (2012). Interferon-gamma restricts Toxoplasma gondii development in murine skeletal muscle cells via nitric oxide production and immunity-related GTPases. PLoS ONE 7:e45440. doi: 10.1371/journal.pone.0045440.
190. Tavares, J., Formaglio, P., Thiberge, S., Mordelet, E., Van Rooijen, N., Medvinsky, A., et al. (2013). Role of host cell traversal by the malaria sporozoite during liver infection. J. Exp. Med. 210, 905-915. doi: 10.1084/jem.20121130.
191. Teirlinck, A. C., McCall, M. B., Roestenberg, M., Scholzen, A., Woestenenk, R., De Mast, Q., et al. (2011). Longevity and composition of cellular immune responses following experimental Plasmodium falciparum malaria infection in humans. PLoS Pathog. 7:e1002389. doi: 10.1371/journal.ppat.1002389.
192. high T cells with susceptibility in Kenyans. PLoS ONE 3:e2027. doi: 10.1371/journal.pone.0002027.
193. Trambas, C. M., and Griffiths, G. M. (2003). Delivering the kiss of death. Nat. Immunol. 4, 399-403. doi: 10.1038/ni0503-399.
194. + T cell killing of Plasmodium yoelii liver stage-infected hepatocytes. J. Immunol. 183, 5870-5878. doi: 10.4049/jimmunol.0900302.
195. Trutmann, M., and Sasse, D. (1994). The lymphatics of the liver. Anat. Embryol. (Berl.) 190, 201-209. doi: 10.1007/BF00234299.
196. Urban, B. C., Ing, R., and Stevenson, M. M. (2005). Early interactions between blood-stage Plasmodium parasites and the immune system. Curr. Top. Microbiol. Immunol. 297, 25-70. doi: 10.1007/3-540-29967-X_2.
197. Usynin, I., Klotz, C., and Frevert, U. (2007). Malaria circumsporozoite protein inhibits the respiratory burst in Kupffer cells. Cell. Microbiol. 9, 2610-2628. doi: 10.1111/j.1462-5822.2007.00982.x.
198. Van Braeckel-Budimir, N., and Harty, J. T. (2014). CD8 T-cell-mediated protection against liver-stage malaria: lessons from a mouse model. Front. Microbiol. 5:272. doi: 10.3389/fmicb.2014.00272.
199. Vanderberg, J., Mueller, A.-K., Heiss, K., Goetz, K., Matuschewski, K., Deckert, M., et al. (2007). Assessment of antibody protection against malaria sporozoites must be done by mosquito injection of sporozoites. Am. J. Pathol. 171, 1405-1406; author reply 1406. doi: 10.2353/ajpath.2007.070661.
200. Vanderberg, J. P. (2014). Imaging mosquito transmission of Plasmodium sporozoites into the mammalian host: immunological implications. Parasitol. Int. 63, 150-164. doi: 10.1016/j.parint.2013.09.010.
201. Vanderberg, J. P., Chew, S., and Stewart, M. J. (1990). Plasmodium sporozoite interactions with macrophages in vitro: a videomicroscopic analysis. J. Protozool. 37, 528-536. doi: 10.1111/j.1550-7408.1990.tb01260.x.
202. Vanderberg, J. P., and Frevert, U. (2004). Intravital microscopy demonstrating antibody-mediated immobilization of Plasmodium berghei sporozoites injected into skin by mosquitoes. Int. J. Parasitol. 34, 991-996. doi: 10.1016/j.ijpara.2004.05.005.
203. van de Sand, C., Horstmann, S., Schmidt, A., Sturm, A., Bolte, S., Krueger, A., et al. (2005). The liver stage of Plasmodium berghei inhibits host cell apoptosis. Mol. Microbiol. 58, 731-742. doi: 10.1111/j.1365-2958.2005.04888.x.
204. Van Rooijen, N., and Sanders, A. (1996). Kupffer cell depletion by liposome-delivered drugs: comparative activity of intracellular clodronate, propamidine, and ethylenediaminetetraacetic acid. Hepatology 23, 1239-1243. doi: 10.1002/hep.510230544.
205. Vaughan, A. M., O'Neill, M. T., Tarun, A. S., Camargo, N., Phuong, T. M., Aly, A. S., et al. (2009). Type II fatty acid synthesis is essential only for malaria parasite late liver stage development. Cell. Microbiol. 11, 506-520. doi: 10.1111/j.1462-5822.2008.01270.x.
206. Vreden, S. G. S., Broek, M. F., Oettinger, M. C., Verhave, J. P., Meuwissen, J. H. E. T., and Sauerwein, R. W. (1992). Cytokines inhibit the development of liver schizonts of the malaria parasite Plasmodium berghei in vivo. Eur. J. Immunol. 22, 2271-2275. doi: 10.1002/eji.1830220914.
207. Wang, R., Arevalo-Herrera, M., Gardner, M. J., Bonelo, A., Carlton, J. M., Gomez, A., et al. (2005). Immune responses to Plasmodium vivax pre-erythrocytic stage antigens in naturally exposed Duffy-negative humans: a potential model for identification of liver-stage antigens. Eur. J. Immunol. 35, 1859-1868. doi: 10.1002/eji.200425807.
208. Warren, A., Le Couteur, D. G., Fraser, R., Bowen, D. G., Mccaughan, G. W., and Bertolino, P. (2006). T lymphocytes interact with hepatocytes through fenestrations in murine liver sinusoidal endothelial cells. Hepatology 44, 1182-1190. doi: 10.1002/hep.21378.
209. Weiss, W. R., Berzofsky, J. A., Houghten, R. A., Sedegah, M., Hollindale, M., and Hoffman, S. L. (1992). A T cell clone directed at the circumsporozoite protein which protects mice against both Plasmodium yoelii and Plasmodium berghei. J. Immunol. 149, 2103-2109.
210. WHO. (2013). "World malaria report: 2013," in WHO Global Malaria Programme. (Geneva: World Health Organization).
211. Wiedemann, A., Depoil, D., Faroudi, M., and Valitutti, S. (2006). Cytotoxic T lymphocytes kill multiple targets simultaneously via spatiotemporal uncoupling of lytic and stimulatory synapses. Proc. Natl. Acad. Sci. U.S.A. 103, 10985-10990. doi: 10.1073/pnas.0600651103.
212. Wilson, K. L., Xiang, S. D., and Plebanski, M. (2015). Montanide, Poly I:C and nanoparticle based vaccines promote differential suppressor and effector cell expansion: a study of induction of CD8 T cells to a minimal Plasmodium berghei epitope. Front. Microbiol. 6:29. doi: 10.3389/fmicb.2015.00029.
213. Wisse, E., De Zanger, R. B., Jacobs, R., and Mccuskey, R. S. (1983). Scanning electron microscope observations on the structure of portal veins, sinusoids and central veins in rat liver. Scan. Electron Microsc. 3, 1441-1452.
214. + T cell activation by a non-self-antigen results in full functional differentiation. J. Immunol. 177, 1689-1697. doi: 10.4049/jimmunol.177.3.1689.
215. Yoneyama, H., and Ichida, T. (2005). Recruitment of dendritic cells to pathological niches in inflamed liver. Med. Mol. Morphol. 38, 136-141. doi: 10.1007/s00795-005-0289-0.
216. Zarling, S., Berenzon, D., Dalai, S., Liepinsh, D., Steers, N., and Krzych, U. (2013). The survival of memory CD8 T cells that is mediated by IL-15 correlates with sustained protection against malaria. J. Immunol. 190, 5128-5141. doi: 10.4049/jimmunol.1203396.
217. Zhang, Y., Wang, H., Ren, J., Tang, X., Jing, Y., Xing, D., et al. (2012). IL-17A synergizes with IFN-gamma to upregulate iNOS and NO production and inhibit chlamydial growth. PLoS ONE 7:e39214. doi: 10.1371/journal.pone.0039214.