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 Pathogens

Volumn 10, Issue 5, 2014, Pages

  Lau, Lei Shong ^a   Fernandez Ruiz, Daniel ^a   Mollard, Vanessa ^a   Sturm, Angelika ^a   Neller, Michelle A ^b   Cozijnsen, Anton ^a   Gregory, Julia L ^a   Davey, Gayle M ^a   Jones, Claerwen M ^a   Lin, Yi Hsuan ^a   Haque, Ashraful ^b   Engwerda, Christian R ^b   Nie, Catherine Q ^c,d   Hansen, Diana S ^c   Murphy, Kenneth M ^e   Papenfuss, Anthony T ^c   Miles, John J ^b,f,g   Burrows, Scott R ^b   de Koning Ward, Tania ^h   McFadden, Geoffrey I ^a   Carbone, Francis R ^a   Crabb, Brendan S ^a,d,i   Heath, William R ^a   more..

^a UNIVERSITY OF MELBOURNE   (Australia)

^b QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^c WALTER AND ELIZA HALL INSTITUTE OF MEDICAL RESEARCH   (Australia)

^d MACFARLANE BURNET INSTITUTE FOR MEDICAL RESEARCH AND PUBLIC HEALTH   (Australia)

^e WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f UNIVERSITY OF QUEENSLAND   (Australia)

^g CARDIFF UNIVERSITY SCHOOL OF MEDICINE   (United Kingdom)

^h DEAKIN UNIVERSITY   (Australia)

ⁱ MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

LYMPHOCYTE ANTIGEN RECEPTOR;

ADOPTIVE TRANSFER; ANIMAL; ANOPHELES; BLOOD; C57BL MOUSE; CD8+ T LYMPHOCYTE; CELL CULTURE; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNIZATION; IMMUNOLOGY; LIFE CYCLE STAGE; LIVER; MALARIA; MALE; METABOLISM; MOUSE; PARASITOLOGY; PATHOLOGY; PLASMODIUM BERGHEI; PLASMODIUM CHABAUDI; PLASMODIUM YOELII; PROCEDURES; SPOROZOITE; TRANSGENIC MOUSE;

ADOPTIVE TRANSFER; ANIMALS; ANOPHELES; BLOOD; CD8-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; IMMUNIZATION, SECONDARY; LIFE CYCLE STAGES; LIVER; MALARIA; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; PLASMODIUM BERGHEI; PLASMODIUM CHABAUDI; PLASMODIUM YOELII; RECEPTORS, ANTIGEN, T-CELL; SPOROZOITES;

EID: 84901685861     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004135     Document Type: Article

References (46)

1. Stephens R, Culleton RL, Lamb TJ, (2012) The contribution of Plasmodium chabaudi to our understanding of malaria. Trends Parasitol 28: 73-82.
2. Culleton R, Kaneko O, (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. Hunt NH, Grau GE, Engwerda C, Barnum SR, van der Heyde H, et al. (2010) Murine cerebral malaria: the whole story. Trends Parasitol 26: 272-274.
5. Schofield L, Grau GE, (2005) Immunological processes in malaria pathogenesis. Nat Rev Immunol 5: 722-735.
6. Amante FH, Haque A, Stanley AC, Rivera Fde L, Randall LM, et al. (2010) Immune-mediated mechanisms of parasite tissue sequestration during experimental cerebral malaria. J Immunol 185: 3632-3642.
7. Baptista FG, Pamplona A, Pena AC, Mota MM, Pied S, 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. Haque A, Best SE, Unosson K, Amante FH, de Labastida F, 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. Yanez DM, Manning DD, Cooley AJ, Weidanz WP, van der Heyde HC, (1996) Participation of lymphocyte subpopulations in the pathogenesis of experimental murine cerebral malaria. J Immunol 157: 1620-1624.
10. Chang WL, Jones SP, Lefer DJ, Welbourne T, Sun G, et al. (2001) CD8(+)-T-cell depletion ameliorates circulatory shock in Plasmodium berghei-infected mice. Infect Immun 69: 7341-7348.
11. Belnoue E, Kayibanda M, Vigario AM, Deschemin JC, van Rooijen N, et al. (2002) On the pathogenic role of brain-sequestered alphabeta CD8+ T cells in experimental cerebral malaria. J Immunol 169: 6369-6375.
12. Miller LH, Baruch DI, Marsh K, Doumbo OK, (2002) The pathogenic basis of malaria. Nature 415: 673-679.
13. Chakravarty S, Cockburn IA, Kuk S, Overstreet MG, Sacci JB, et al. (2007) CD8+ T lymphocytes protective against malaria liver stages are primed in skin-draining lymph nodes. Nat Med 13: 1035-1041.
14. Spence PJ, Langhorne J, (2012) T cell control of malaria pathogenesis. Curr Opin Immunol 24: 444-448.
15. 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.
16. Gwadz RW, Cochrane AH, Nussenzweig V, Nussenzweig RS, (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 1): 165-173.
17. Clyde DF, Most H, McCarthy VC, Vanderberg JP, (1973) Immunization of man against sporozite-induced falciparum malaria. Am J Med Sci 266: 169-177.
18. Rieckmann KH, Carson PE, Beaudoin RL, Cassells JS, Sell KW, (1974) Letter: Sporozoite induced immunity in man against an Ethiopian strain of Plasmodium falciparum. Trans R Soc Trop Med Hyg 68: 258-259.
19. Epstein JE, Tewari K, Lyke KE, Sim BKL, Billingsley PF, et al. (2011) Live Attenuated Malaria Vaccine Designed to Protect Through Hepatic CD8+ T Cell Immunity. Science 334: 475-480.
20. Butler NS, Vaughan AM, Harty JT, Kappe SH, (2012) Whole parasite vaccination approaches for prevention of malaria infection. Trends Immunol 33: 247-254.
21. Seder RA, Chang L-J, Enama ME, Zephir KL, Sarwar UN, et al. (2013) Protection Against Malaria by Intravenous Immunization with a Nonreplicating Sporozoite Vaccine. Science 341: 1359-1365.
22. Roestenberg M, Teirlinck AC, McCall MBB, Teelen K, Makamdop KN, et al. (2011) Long-term protection against malaria after experimental sporozoite inoculation: an open-label follow-up study. Lancet 377: 1770-1776.
23. Hall N, (2005) A Comprehensive Survey of the Plasmodium Life Cycle by Genomic, Transcriptomic, and Proteomic Analyses. Science 307: 82-86.
24. Ocana-Morgner C, Mota MM, Rodriguez A, (2003) Malaria blood stage suppression of liver stage immunity by dendritic cells. J Exp Med 197: 143-151.
25. Belnoue E, Voza T, Costa FTM, Grüner AC, Mauduit M, 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. Clarke SMR, Barnden M, Kurts C, Carbone FR, Miller JFAP, 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. Barbier L, Tay SS, McGuffog C, Triccas JA, McCaughan GW, 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. Lundie RJ, de Koning-Ward TF, Davey GM, Nie CQ, Hansen DS, 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. Piva L, Tetlak P, Claser C, Karjalainen K, Renia L, et al. (2012) Cutting Edge: Clec9A+ Dendritic Cells Mediate the Development of Experimental Cerebral Malaria. J Immunol 189: 1128-1132.
30. Urban BC, Cordery D, Shafi MJ, Bull PC, Newbold CI, 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. Guermonprez P, Helft J, Claser C, Deroubaix S, Karanje H, 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. Hafalla JC, Rai U, Bernal-Rubio D, Rodriguez A, Zavala F, (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. Cockburn IA, Chen Y-C, Overstreet MG, Lees JR, van Rooijen N, 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-Makinde J, Miles JJ, van den Berg HA, Skowera A, Cole DK, et al. (2013) Peptide length determines the outcome of TCR/peptide-MHCI engagement. Blood 121: 1112-1123.
35. Imai T, Shen J, Chou B, Duan X, Tu L, 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. Tsuji M, Zavala F, (2003) T cells as mediators of protective immunity against liver stages of Plasmodium. Trends Parasitol 19: 88-93.
37. Jobe O, Donofrio G, Sun G, Liepinsh D, Schwenk R, 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. Schnorrer P, Behrens GMN, Wilson NS, Pooley JL, Smith CM, 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. Mueller SN, Heath W, McLain JD, Carbone FR, Jones CM, (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. Ramakrishnan C, Delves MJ, Lal K, Blagborough AM, Butcher G, et al. (2013) Laboratory maintenance of rodent malaria parasites. Methods Mol Biol 923: 51-72.
42. Lau LS, Fernandez Ruiz D, Davey GM, de Koning-Ward TF, Papenfuss AT, 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. Mueller SN, Jones CM, Smith CM, Heath WR, Carbone FR, (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. Kaye J, Vasquez NJ, Hedrick SM, (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. Barnden MJ, Allison J, Heath WR, Carbone FR, (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. Smith CM, Belz GT, Wilson NS, Villadangos JA, Shortman K, 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.