CD8 T Cells from a Novel T Cell Receptor Transgenic Mouse Induce Liver-Stage Immunity That Can Be Boosted by Blood-Stage Infection in Rodent Malaria

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Malaria is a disease caused by Plasmodium species, which have a highly complex life cycle involving both liver and blood stages of mammalian infection. To prevent disease, one strategy has been to induce CD8+ T cells against liver-stage parasites, usually by immunization with stage-specific antigens. Here we describe a T cell receptor specificity that recognizes an antigen expressed in both the liver and blood stages of several rodent Plasmodium species. We generated a T cell receptor transgenic mouse with this specificity and showed that T cells from this line could protect against liver-stage infection. We used this novel tool to identify the site and cell-type involved in priming to a recently developed intravenous attenuated sporozoite vaccine shown to have efficacy in humans. We showed that CD8+ T cells with this specificity could protect against liver-stage infection while causing pathology to the blood stage. Finally, we provided evidence that T cells with cross-stage specificity can be primed and boosted on alternative stages, raising the possibility that antigens expressed in multiple stages might be ideal vaccine candidates for generating strong immunity to liver-stage parasites.

Vyšlo v časopise: CD8 T Cells from a Novel T Cell Receptor Transgenic Mouse Induce Liver-Stage Immunity That Can Be Boosted by Blood-Stage Infection in Rodent Malaria. PLoS Pathog 10(5): e32767. doi:10.1371/journal.ppat.1004135
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1004135

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Zdroje

1. StephensR, CulletonRL, LambTJ (2012) The contribution of Plasmodium chabaudi to our understanding of malaria. Trends Parasitol 28: 73–82.

2. CulletonR, KanekoO (2010) Erythrocyte binding ligands in malaria parasites: intracellular trafficking and parasite virulence. Acta Trop 114: 131–137.

3. Lou J, Lucas R, Grau GE (2001) Pathogenesis of cerebral malaria: recent experimental data and possible applications for humans. Clin Microbiol Rev 14: : 810–820, table of contents.

4. HuntNH, GrauGE, EngwerdaC, BarnumSR, van der HeydeH, et al. (2010) Murine cerebral malaria: the whole story. Trends Parasitol 26: 272–274.

5. SchofieldL, GrauGE (2005) Immunological processes in malaria pathogenesis. Nat Rev Immunol 5: 722–735.

6. AmanteFH, HaqueA, StanleyAC, Rivera FdeL, RandallLM, et al. (2010) Immune-mediated mechanisms of parasite tissue sequestration during experimental cerebral malaria. J Immunol 185: 3632–3642.

7. BaptistaFG, PamplonaA, PenaAC, MotaMM, PiedS, et al. (2010) Accumulation of Plasmodium berghei-infected red blood cells in the brain is crucial for the development of cerebral malaria in mice. Infect Immun 78: 4033–4039.

8. HaqueA, BestSE, UnossonK, AmanteFH, de LabastidaF, et al. (2011) Granzyme B Expression by CD8+ T Cells Is Required for the Development of Experimental Cerebral Malaria. J Immunol 186: 6148–6156.

9. YanezDM, ManningDD, CooleyAJ, WeidanzWP, van der HeydeHC (1996) Participation of lymphocyte subpopulations in the pathogenesis of experimental murine cerebral malaria. J Immunol 157: 1620–1624.

10. ChangWL, JonesSP, LeferDJ, WelbourneT, SunG, et al. (2001) CD8(+)-T-cell depletion ameliorates circulatory shock in Plasmodium berghei-infected mice. Infect Immun 69: 7341–7348.

11. BelnoueE, KayibandaM, VigarioAM, DescheminJC, van RooijenN, et al. (2002) On the pathogenic role of brain-sequestered alphabeta CD8+ T cells in experimental cerebral malaria. J Immunol 169: 6369–6375.

12. MillerLH, BaruchDI, MarshK, DoumboOK (2002) The pathogenic basis of malaria. Nature 415: 673–679.

13. ChakravartyS, CockburnIA, KukS, OverstreetMG, SacciJB, et al. (2007) CD8+ T lymphocytes protective against malaria liver stages are primed in skin-draining lymph nodes. Nat Med 13: 1035–1041.

14. SpencePJ, LanghorneJ (2012) T cell control of malaria pathogenesis. Curr Opin Immunol 24: 444–448.

15. NussenzweigRS, VanderbergJ, MostH, OrtonC (1967) Protective immunity produced by the injection of x-irradiated sporozoites of plasmodium berghei. Nature 216: 160–162.

16. GwadzRW, CochraneAH, NussenzweigV, NussenzweigRS (1979) Preliminary studies on vaccination of rhesus monkeys with irradiated sporozoites of Plasmodium knowlesi and characterization of surface antigens of these parasites. Bull WHO 57 Suppl 1165–173.

17. ClydeDF, MostH, McCarthyVC, VanderbergJP (1973) Immunization of man against sporozite-induced falciparum malaria. Am J Med Sci 266: 169–177.

18. RieckmannKH, CarsonPE, BeaudoinRL, CassellsJS, SellKW (1974) Letter: Sporozoite induced immunity in man against an Ethiopian strain of Plasmodium falciparum. Trans R Soc Trop Med Hyg 68: 258–259.

19. EpsteinJE, TewariK, LykeKE, SimBKL, BillingsleyPF, et al. (2011) Live Attenuated Malaria Vaccine Designed to Protect Through Hepatic CD8+ T Cell Immunity. Science 334: 475–480.

20. ButlerNS, VaughanAM, HartyJT, KappeSH (2012) Whole parasite vaccination approaches for prevention of malaria infection. Trends Immunol 33: 247–254.

21. SederRA, ChangL-J, EnamaME, ZephirKL, SarwarUN, et al. (2013) Protection Against Malaria by Intravenous Immunization with a Nonreplicating Sporozoite Vaccine. Science 341: 1359–1365.

22. RoestenbergM, TeirlinckAC, McCallMBB, TeelenK, MakamdopKN, et al. (2011) Long-term protection against malaria after experimental sporozoite inoculation: an open-label follow-up study. Lancet 377: 1770–1776.

23. HallN (2005) A Comprehensive Survey of the Plasmodium Life Cycle by Genomic, Transcriptomic, and Proteomic Analyses. Science 307: 82–86.

24. Ocana-MorgnerC, MotaMM, RodriguezA (2003) Malaria blood stage suppression of liver stage immunity by dendritic cells. J Exp Med 197: 143–151.

25. BelnoueE, VozaT, CostaFTM, GrünerAC, MauduitM, 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.

26. ClarkeSMR, BarndenM, KurtsC, CarboneFR, MillerJFAP, et al. (2000) Characterisation of the OVA-specific TCR transgenic line OT-I: MHC elements for positive and negative selection. Immunol Cell Biol 78: 110–117.

27. BarbierL, TaySS, McGuffogC, TriccasJA, McCaughanGW, et al. (2012) Two lymph nodes draining the mouse liver are the preferential site of DC migration and T cell activation. J Hepatol 57: 352–358.

28. LundieRJ, de Koning-WardTF, DaveyGM, NieCQ, HansenDS, et al. (2008) Blood-stage Plasmodium infection induces CD8+ T lymphocytes to parasite-expressed antigens, largely regulated by CD8alpha+ dendritic cells. Proc Natl Acad Sci U S A 105: 14509–14514.

29. PivaL, TetlakP, ClaserC, KarjalainenK, ReniaL, et al. (2012) Cutting Edge: Clec9A+ Dendritic Cells Mediate the Development of Experimental Cerebral Malaria. J Immunol 189: 1128–1132.

30. UrbanBC, CorderyD, ShafiMJ, BullPC, NewboldCI, et al. (2006) The frequency of BDCA3-positive dendritic cells is increased in the peripheral circulation of Kenyan children with severe malaria. Infect Immun 74: 6700–6706.

31. GuermonprezP, HelftJ, ClaserC, DeroubaixS, KaranjeH, et al. (2013) Inflammatory Flt3l is essential to mobilize dendritic cells and for T cell responses during Plasmodium infection. Nat Med 19: 730–738.

32. HafallaJC, RaiU, Bernal-RubioD, RodriguezA, ZavalaF (2007) Efficient development of plasmodium liver stage-specific memory CD8+ T cells during the course of blood-stage malarial infection. J Infect Dis 196: 1827–1835.

33. CockburnIA, ChenY-C, OverstreetMG, LeesJR, van RooijenN, et al. (2010) Prolonged Antigen Presentation Is Required for Optimal CD8+ T Cell Responses against Malaria Liver Stage Parasites. PLoS Path 6: e1000877.

34. Ekeruche-MakindeJ, MilesJJ, van den BergHA, SkoweraA, ColeDK, et al. (2013) Peptide length determines the outcome of TCR/peptide-MHCI engagement. Blood 121: 1112–1123.

35. ImaiT, ShenJ, ChouB, DuanX, TuL, et al. (2010) Involvement of CD8+ T cells in protective immunity against murine blood-stage infection with Plasmodium yoelii 17XL strain. Eur J Immunol 40: 1053–1061.

36. TsujiM, ZavalaF (2003) T cells as mediators of protective immunity against liver stages of Plasmodium. Trends Parasitol 19: 88–93.

37. JobeO, DonofrioG, SunG, LiepinshD, SchwenkR, et al. (2009) Immunization with radiation-attenuated Plasmodium berghei sporozoites induces liver cCD8alpha+DC that activate CD8+T cells against liver-stage malaria. PLoS One 4: e5075.

38. SchnorrerP, BehrensGMN, WilsonNS, PooleyJL, SmithCM, et al. (2006) The dominant role of CD8+ dendritic cells in cross-presentation is not dictated by antigen capture. Proc Natl Acad Sci U S A 103: 10729–10734.

39. MuellerSN, HeathW, McLainJD, CarboneFR, JonesCM (2002) Characterization of two TCR transgenic mouse lines specific for herpes simplex virus. Immunol Cell Biol 80: 156–163.

40. Benedict MQ (1997) Care and maintenance of anopheline mosquito colonies. In: Crampton JM BC, Louis C, editor. The Molecular Biology of Insect Disease Vectors. New York: Chapman & Hall. pp. 2–12.

41. RamakrishnanC, DelvesMJ, LalK, BlagboroughAM, ButcherG, et al. (2013) Laboratory maintenance of rodent malaria parasites. Methods Mol Biol 923: 51–72.

42. LauLS, Fernandez RuizD, DaveyGM, de Koning-WardTF, PapenfussAT, et al. (2011) Blood-stage Plasmodium berghei infection generates a potent, specific CD8+ T-cell response despite residence largely in cells lacking MHC I processing machinery. J Infect Dis 204: 1989–1996.

43. MuellerSN, JonesCM, SmithCM, HeathWR, CarboneFR (2002) Rapid cytotoxic T lymphocyte activation occurs in the draining lymph nodes after cutaneous herpes simplex virus infection as a result of early antigen presentation and not the presence of virus. J Exp Med 195: 651–656.

44. KayeJ, VasquezNJ, HedrickSM (1992) Involvement of the same region of the T cell antigen receptor in thymic selection and foreign peptide recognition. J Immunol 148: 3342–3353.

45. BarndenMJ, AllisonJ, HeathWR, CarboneFR (1998) Defective TCR expression in transgenic mice constructed using cDNA-based alpha- and beta-chain genes under the control of heterologous regulatory elements. Immunol Cell Biol 76: 34–40.

46. SmithCM, BelzGT, WilsonNS, VilladangosJA, ShortmanK, et al. (2003) Cutting Edge: Conventional CD8alpha(+) Dendritic Cells Are Preferentially Involved in CTL Priming After Footpad Infection with Herpes Simplex Virus-1. J Immunol 170: 4437–4440.