CD8+ T cells eliminate liver-stage Plasmodium berghei parasites without detectable bystander effect

Infection and Immunity

Volumn 82, Issue 4, 2014, Pages 1460-1464

  Cockburn, Ian A ^a,b   Tse, Sze Wah ^a,c   Zavala, Fidel ^a  

^a JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^b Biology and Environment   (Australia)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD8 ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BYSTANDER EFFECT; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; HEPATITIS; IN VIVO STUDY; LIVER CELL; MIXED INFECTION; MOUSE; NONHUMAN; PARASITE CLEARANCE; PARASITOSIS; PLASMODIUM BERGHEI; PLASMODIUM BERGHEI INFECTION; PRIORITY JOURNAL; TRANSFER CELL;

ANIMALS; ANTIGENS, PROTOZOAN; BYSTANDER EFFECT; CD8-POSITIVE T-LYMPHOCYTES; HEPATOCYTES; LIVER; MALARIA; MICE; MICE, INBRED C57BL; PARASITE LOAD; PLASMODIUM BERGHEI;

EID: 84896467579     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01500-13     Document Type: Article

References (34)

1. Weiss WR, Sedegah M, Beaudoin RL, Miller LH, Good MF. 1988. CD8+ T cells (cytotoxic/suppressors) are required for protection in mice immunized with malaria sporozoites. Proc. Natl. Acad. Sci. U. S. A. 85: 573-576. http://dx.doi.org/10.1073/pnas.85.2.573.
2. Schofield L, Villaquiran J, Ferreira A, Schellekens H, Nussenzweig R, Nussenzweig V. 1987. Gamma interferon, CD8+ T cells and antibodies required for immunity to malaria sporozoites. Nature 330:664-666. http://dx.doi.org/10.1038/330664a0.
3. Nussenzweig RS, Vanderberg J, Most H, Orton C. 1967. Protective immunity produced by the injection of X-irradiated sporozoites of Plasmodium berghei. Nature 216:160-162. http://dx.doi.org/10.1038/216160a0.
4. Nussler A, Pied S, Goma J, Renia L, Miltgen F, Grau GE, Mazier D. 1991. TNF inhibits malaria hepatic stages in vitro via synthesis of IL-6. Int. Immunol. 3:317-321. http://dx.doi.org/10.1093/intimm/3.4.317.
5. Tsuji M, Miyahira Y, Nussenzweig RS, Aguet M, Reichel M, Zavala F. 1995. Development of antimalaria immunity in mice lacking IFN-gamma receptor. J. Immunol. 154:5338-5344.
6. Butler NS, Schmidt NW, Harty JT. 2010. Differential effector pathways regulate memory CD8 T cell immunity against Plasmodium berghei versus P. yoelii sporozoites. J. Immunol. 184:2528-2538. http://dx.doi.org/10.4049/jimmunol.0903529.
7. Renggli J, Hahne M, Matile H, Betschart B, Tschopp J, 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. http://dx.doi.org/10.1046/j.1365-3024.1997.d01-190.x.
8. Frevert U, Nacer A. 2013. Immunobiology of Plasmodium in liver and brain. Parasite Immunol. 35:267-282. http://dx.doi.org/10.1111/pim.12039.
9. Hafalla JC, Cockburn IA, Zavala F. 2006. Protective and pathogenic roles of CD8+ T cells during malaria infection. Parasite Immunol. 28:15-24. http://dx.doi.org/10.1111/j.1365-3024.2006.00777.x.
10. Cockburn IA, Amino R, Kelemen RK, Kuo SC, Tse SW, Radtke A, Mac-Daniel L, Ganusov VV, Zavala F, Menard R. 2013. In vivo imaging of CD8+ T cell-mediated elimination of malaria liver stages. Proc. Natl. Acad. Sci. U. S. A. 110:9090-9095. http://dx.doi.org/10.1073/pnas.1303858110.
11. + 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. http://dx.doi.org/10.1128/IAI.00570-13.
12. Bongfen SE, Balam S, Torgler R, Romero JF, Corradin G. 2008. Processing of the circumsporozoite protein in infected hepatocytes is not dependent on aspartic proteases. Parasite Immunol. 30:375-378. http://dx.doi.org/10.1111/j.1365-3024.2008.01032.x.
13. Bongfen SE, Torgler R, Romero JF, Renia L, Corradin G. 2007. Plasmodium berghei-infected primary hepatocytes process and present the circumsporozoite protein to specific CD8+ T cells in vitro. J. Immunol. 178:7054-7063.
14. Chakravarty S, Cockburn IA, Kuk S, Overstreet MG, Sacci JB, Zavala F. 2007. CD8+ T lymphocytes protective against malaria liver stages are primed in skin-draining lymph nodes. Nat. Med. 13:1035-1041. http://dx.doi.org/10.1038/nm1628.
15. Cockburn IA, Tse SW, Radtke AJ, Srinivasan P, Chen YC, Sinnis P, Zavala F. 2011. Dendritic cells and hepatocytes use distinct pathways to process protective antigen from plasmodium in vivo. PLoS Pathog. 7:e1001318. http://dx.doi.org/10.1371/journal.ppat.1001318.
16. Hogquist KA, Jameson SC, Heath WR, Howard JL, Bevan MJ, Carbone FR. 1994. T cell receptor antagonist peptides induce positive selection. Cell 76:17-27. http://dx.doi.org/10.1016/0092-8674(94)90169-4.
17. Amino R, Giovannini D, Thiberge S, Gueirard P, Boisson B, Dubremetz JF, Prevost MC, Ishino T, Yuda M, Menard R. 2008. Host cell traversal is important for progression of the malaria parasite through the dermis to the liver. Cell Host Microbe 3:88-96. http://dx.doi.org/10.1016/j.chom.2007.12.007.
18. Graewe S, Retzlaff S, Struck N, Janse CJ, Heussler VT. 2009. Going live: a comparative analysis of the suitability of the RFP derivatives RedStar, mCherry and tdTomato for intravital and in vitro live imaging of Plasmodium parasites. Biotechnol. J. 4:895-902. http://dx.doi.org/10.1002/biot.200900035.
19. Thiberge S, Blazquez S, Baldacci P, Renaud O, Shorte S, Menard R, Amino R. 2007. In vivo imaging of malaria parasites in the murine liver. Nat. Protoc. 2:1811-1818. http://dx.doi.org/10.1038/nprot.2007.257.
20. Bruna-Romero O, Hafalla JC, Gonzalez-Aseguinolaza G, Sano G, Tsuji M, Zavala F. 2001. Detection of malaria liver-stages in mice infected through the bite of a single Anopheles mosquito using a highly sensitive real-time PCR. Int. J. Parasitol. 31:1499-1502. http://dx.doi.org/10.1016/S0020-7519(01)00265-X.
21. Engelmann S, Sinnis P, Matuschewski K. 2006. Transgenic Plasmodium berghei sporozoites expressing beta-galactosidase for quantification of sporozoite transmission. Mol. Biochem. Parasitol. 146:30-37. http://dx.doi.org/10.1016/j.molbiopara.2005.10.015.
22. Jin Y, Kebaier C, Vanderberg J. 2007. Direct microscopic quantification of dynamics of Plasmodium berghei sporozoite transmission from mosquitoes to mice. Infect. Immun. 75:5532-5539. http://dx.doi.org/10.1128/IAI.00600-07.
23. Medica DL, Sinnis P. 2005. Quantitative dynamics of Plasmodium yoelii sporozoite transmission by infected anopheline mosquitoes. Infect. Immun. 73:4363-4369. http://dx.doi.org/10.1128/IAI.73.7.4363-4369.2005.
24. Precopio ML, Betts MR, Parrino J, Price DA, Gostick E, Ambrozak DR, Asher TE, Douek DC, Harari A, Pantaleo G, Bailer R, Graham BS, Roederer M, Koup RA. 2007. Immunization with vaccinia virus induces polyfunctional and phenotypically distinctive CD8(+) T cell responses. J. Exp. Med. 204:1405-1416. http://dx.doi.org/10.1084/jem.20062363.
25. Huse M, Lillemeier BF, Kuhns MS, Chen DS, Davis MM. 2006. T cells use two directionally distinct pathways for cytokine secretion. Nat. Immunol. 7:247-255. http://dx.doi.org/10.1038/ni1304.
26. Kupfer A, Mosmann TR, 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. http://dx.doi.org/10.1073/pnas.88.3.775.
27. Sanderson NS, Puntel M, Kroeger KM, Bondale NS, Swerdlow M, Iranmanesh N, Yagita H, Ibrahim A, Castro MG, Lowenstein PR. 2012. Cytotoxic immunological synapses do not restrict the action of interferongamma to antigenic target cells. Proc. Natl. Acad. Sci. U. S. A. 109:7835-7840. http://dx.doi.org/10.1073/pnas.1116058109.
28. Muller AJ, Filipe-Santos O, Eberl G, Aebischer T, Spath GF, Bousso P. 2012. CD4+ T cells rely on a cytokine gradient to control intracellular pathogens beyond sites of antigen presentation. Immunity 37:147-157. http://dx.doi.org/10.1016/j.immuni.2012.05.015.
29. Trimnell A, Takagi A, Gupta M, Richie TL, Kappe SH, Wang R. 2009. Genetically attenuated parasite vaccines induce contact-dependent CD8+ T cell killing of Plasmodium yoelii liver stage-infected hepatocytes. J. Immunol. 183:5870-5878. http://dx.doi.org/10.4049/jimmunol.0900302.
30. Morrot A, Zavala F. 2004. Effector and memory CD8+ T cells as seen in immunity to malaria. Immunol. Rev. 201:291-303. http://dx.doi.org/10.1111/j.0105-2896.2004.00175.x.
31. Schmidt NW, Butler NS, Badovinac VP, Harty JT. 2010. Extreme CD8 T cell requirements for anti-malarial liver-stage immunity following immunization with radiation attenuated sporozoites. PLoS Pathog. 6:e1000998. http://dx.doi.org/10.1371/journal.ppat.1000998.
32. Schmidt NW, Podyminogin RL, Butler NS, Badovinac VP, Tucker BJ, Bahjat KS, Lauer P, Reyes-Sandoval A, Hutchings CL, Moore AC, Gilbert SC, Hill AV, Bartholomay LC, Harty JT. 2008. Memory CD8 T cell responses exceeding a large but definable threshold provide long-term immunity to malaria. Proc. Natl. Acad. Sci. U. S. A. 105:14017-14022. http://dx.doi.org/10.1073/pnas.0805452105.
33. Cockburn IA, Chakravarty S, Overstreet MG, Garcia-Sastre A, Zavala F. 2008. Memory CD8+ T cell responses expand when antigen presentation overcomes T cell self-regulation. J. Immunol. 180:64-71.
34. Li S, Rodrigues M, Rodriguez D, Rodriguez JR, Esteban M, Palese P, Nussenzweig RS, Zavala F. 1993. Priming with recombinant influenza virus followed by administration of recombinant vaccinia virus induces CD8+ T-cell-mediated protective immunity against malaria. Proc. Natl. Acad. Sci. U. S. A. 90:5214-5218. http://dx.doi.org/10.1073/pnas.90.11.5214.