Dendritic cell function and antigen presentation in malaria

Current Opinion in Immunology

Volumn 40, Issue , 2016, Pages 1-6

  Cockburn, Ian A ^a   Zavala, Fidel ^b  

^a Australian National University   (Australia)

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

Author keywords

[No Author keywords available]

Indexed keywords

CD8ALPHA ANTIGEN; GLYCOPROTEIN P 15095; TRANSPORTER ASSOCIATED WITH ANTIGEN PROCESSING 1; CD8 ANTIGEN; MALARIA VACCINE; PARASITE ANTIGEN;

ANTIGEN PRESENTATION; BRAIN MALARIA; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CROSS PRESENTATION; DENDRITIC CELL; IMMUNE RESPONSE; LIVER CELL; LYMPH NODE; LYMPHOCYTE FUNCTION; MALARIA; NONHUMAN; PARASITE CLEARANCE; PATHOGENESIS; PLASMODIUM BERGHEI; PLASMODIUM CHABAUDI; PLASMODIUM FALCIPARUM; PLASMODIUM VIVAX; PLASMODIUM YOELII; PROTEIN MOTIF; REVIEW; SPOROZOITE; T LYMPHOCYTE ACTIVATION; ANIMAL; BRAIN; ENDOTHELIUM CELL; HUMAN; IMMUNOLOGY; LIFE CYCLE STAGE; LYMPHOCYTE ACTIVATION; METABOLISM; PARASITOLOGY; PATHOLOGY; PHYSIOLOGY; PLASMODIUM;

ANIMALS; ANTIGENS, CD8; ANTIGENS, PROTOZOAN; BRAIN; CD8-POSITIVE T-LYMPHOCYTES; CROSS-PRIMING; DENDRITIC CELLS; ENDOTHELIAL CELLS; HUMANS; LIFE CYCLE STAGES; LYMPHOCYTE ACTIVATION; MALARIA; MALARIA VACCINES; PLASMODIUM;

EID: 84956604985     PISSN: 09527915     EISSN: 18790372     Source Type: Journal    
DOI: 10.1016/j.coi.2016.01.010     Document Type: Review

References (56)

1. Rodrigues M.M., Cordey A.S., Arreaza G., Corradin G., Romero P., Maryanski J.L., Nussenzweig R.S., Zavala F. CD8+ cytolytic T cell clones derived against the Plasmodium yoelii circumsporozoite protein protect against malaria. Int Immunol 1991, 3:579-585.
2. Romero P., Maryanski J.L., Corradin G., Nussenzweig R.S., Nussenzweig V., Zavala F. Cloned cytotoxic T cells recognize an epitope in the circumsporozoite protein and protect against malaria. Nature 1989, 341:323-326.
3. Carvalho L.H., Sano G., Hafalla J.C., Morrot A., Curotto de Lafaille M.A. IL-4-secreting CD4+ T cells are crucial to the development of CD8+ T-cell responses against malaria liver stages. Nat Med 2002, 8:166-170.
4. Oliveira G.A., Kumar K.A., Calvo-Calle J.M., Othoro C., Altszuler D., Nussenzweig V., Nardin E.H. Class II-restricted protective immunity induced by malaria sporozoites. Infect Immun 2008, 76:1200-1206.
5. Perez-Mazliah D., Langhorne J. CD4 T-cell subsets in malaria: TH1/TH2 revisited. Front Immunol 2014, 5:671.
6. Howland S.W., Claser C., Poh C.M., Gun S.Y., Renia L. Pathogenic CD8+ T cells in experimental cerebral malaria. Semin Immunopathol 2015, 37:221-231.
7. Bertolino P., Bowen D.G., McCaughan G.W., Fazekas de St Groth B. Antigen-specific primary activation of CD8+ T cells within the liver. J Immunol 2001, 166:5430-5438.
8. Tay S.S., Wong Y.C., McDonald D.M., Wood N.A., Roediger B., Sierro F., McGuffog C., Alexander I.E., Bishop G.A., Gamble J.R., et al. Antigen expression level threshold tunes the fate of CD8 T cells during primary hepatic immune responses. Proc Natl Acad Sci U S A 2014, 111:E2540-E2549.
9. Wuensch S.A., Pierce R.H., Crispe I.N. Local intrahepatic CD8+ T cell activation by a non-self-antigen results in full functional differentiation. J Immunol 2006, 177:1689-1697.
10. Chakravarty S., Cockburn I.A., Kuk S., Overstreet M.G., Sacci J.B., Zavala F. CD8+ T lymphocytes protective against malaria liver stages are primed in skin-draining lymph nodes. Nat Med 2007, 13:1035-1041.
11. Cockburn I.A., Chen Y.C., Overstreet M.G., Lees J.R., van Rooijen N., Farber D.L., Zavala F. Prolonged antigen presentation is required for optimal CD8+ T cell responses against malaria liver stage parasites. PLoS Pathog 2010, 6:e1000877.
12. Jung S., Unutmaz D., Wong P., Sano G., De los Santos K., Sparwasser T., Wu S., Vuthoori S., Ko K., Zavala F., et al. In vivo depletion of CD11c+ dendritic cells abrogates priming of CD8+ T cells by exogenous cell-associated antigens. Immunity 2002, 17:211-220.
13. Lau L.S., Fernandez-Ruiz D., Mollard V., Sturm A., Neller M.A., Cozijnsen A., Gregory J.L., Davey G.M., Jones C.M., Lin Y.H., et al. 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 2014, 10:e1004135.
14. Sano G., Hafalla J.C., Morrot A., Abe R., Lafaille J.J., Zavala F. Swift development of protective effector functions in naive CD8(+) T cells against malaria liver stages. J Exp Med 2001, 194:173-180.
15. Cockburn I.A., Tse S.W., Radtke A.J., Srinivasan P., Chen Y.C., Sinnis P., Zavala F. Dendritic cells and hepatocytes use distinct pathways to process protective antigen from plasmodium in vivo. PLoS Pathog 2011, 7:e1001318.
16. Amino R., Giovannini D., Thiberge S., Gueirard P., Boisson B., Dubremetz J.F., Prevost M.C., Ishino T., Yuda M., Menard R. Host cell traversal is important for progression of the malaria parasite through the dermis to the liver. Cell Host Microbe 2008, 3:88-96.
17. Mac-Daniel L., Buckwalter M.R., Berthet M., Virk Y., Yui K., Albert M.L., Gueirard P., Menard R. Local immune response to injection of Plasmodium sporozoites into the skin. J Immunol 2014, 193:1246-1257.
18. Hopp C.S., Chiou K., Ragheb D.R., Salman A., Khan S.M., Liu A.J., Sinnis P. Longitudinal analysis of Plasmodium sporozoite motility in the dermis reveals component of blood vessel recognition. Elife 2015, 4.
19. Radtke A.J., Kastenmuller W., Espinosa D.A., Gerner M.Y., Tse S.W., Sinnis P., Germain R.N., Zavala F.P., Cockburn I.A. Lymph-node resident CD8alpha+ dendritic cells capture antigens from migratory malaria sporozoites and induce CD8+ T cell responses. PLoS Pathog 2015, 11:e1004637.
20. Montagna G.N., Biswas A., Hildner K., Matuschewski K., Dunay I.R. Batf3 deficiency proves the pivotal role of CD8alpha dendritic cells in protection induced by vaccination with attenuated Plasmodium sporozoites. Parasite Immunol 2015, 10.1111/pim.12222.
21. Cockburn I.A., Amino R., Kelemen R.K., Kuo S.C., Tse S.W., Radtke A., Mac-Daniel L., Ganusov V.V., Zavala F., Menard R. In vivo imaging of CD8+ T cell-mediated elimination of malaria liver stages. Proc Natl Acad Sci U S A 2013, 110:9090-9095.
22. Kimura K., Kimura D., Matsushima Y., Miyakoda M., Honma K., Yuda M., Yui K. CD8+ T cells specific for a malaria cytoplasmic antigen form clusters around infected hepatocytes and are protective at the liver stage of infection. Infect Immun 2013, 81:3825-3834.
23. Cockburn I.A., Tse S.W., Zavala F. CD8+ T cells eliminate liver-stage Plasmodium berghei parasites without detectable bystander effect. Infect Immun 2014, 82:1460-1464.
24. Huang J., Tsao T., Zhang M., Rai U., Tsuji M., Li X. A sufficient role of MHC class I molecules on hepatocytes in anti-plasmodial activity of CD8 (+) T cells in vivo. Front Microbiol 2015, 6:69.
25. Guidotti L.G., Inverso D., Sironi L., Di Lucia P., Fioravanti J., Ganzer L., Fiocchi A., Vacca M., Aiolfi R., Sammicheli S., et al. Immunosurveillance of the liver by intravascular effector CD8(+) T cells. Cell 2015, 161:486-500.
26. Bongfen S.E., Balam S., Torgler R., Romero J.F., Corradin G. Processing of the circumsporozoite protein in infected hepatocytes is not dependent on aspartic proteases. Parasite Immunol 2008, 30:375-378.
27. Bongfen S.E., Torgler R., Romero J.F., Renia L., Corradin G. Plasmodium berghei-infected primary hepatocytes process and present the circumsporozoite protein to specific CD8+ T cells in vitro. J Immunol 2007, 178:7054-7063.
28. de Koning-Ward T.F., Gilson P.R., Boddey J.A., Rug M., Smith B.J., Papenfuss A.T., Sanders P.R., Lundie R.J., Maier A.G., Cowman A.F., et al. A newly discovered protein export machine in malaria parasites. Nature 2009, 459:945-949.
29. Elsworth B., Matthews K., Nie C.Q., Kalanon M., Charnaud S.C., Sanders P.R., Chisholm S.A., Counihan N.A., Shaw P.J., Pino P., et al. PTEX is an essential nexus for protein export in malaria parasites. Nature 2014, 511:587-591.
30. Montagna G.N., Beigier-Bompadre M., Becker M., Kroczek R.A., Kaufmann S.H., Matuschewski K. Antigen export during liver infection of the malaria parasite augments protective immunity. MBio 2014, 5. e01321-e01314.
31. Hafalla J.C., Bauza K., Friesen J., Gonzalez-Aseguinolaza G., Hill A.V., Matuschewski K. Identification of targets of CD8(+) T cell responses to malaria liver stages by genome-wide epitope profiling. PLoS Pathog 2013, 9:e1003303.
32. Longley R.J., Bauza K., Ewer K.J., Hill A.V., Spencer A.J. Development of an in vitro assay and demonstration of Plasmodium berghei liver-stage inhibition by TRAP-specific CD8+ T cells. PLoS One 2015, 10:e0119880.
33. Cebrian I., Visentin G., Blanchard N., Jouve M., Bobard A., Moita C., Enninga J., Moita L.F., Amigorena S., Savina A. Sec22b regulates phagosomal maturation and antigen crosspresentation by dendritic cells. Cell 2011, 147:1355-1368.
34. Goldszmid R.S., Coppens I., Lev A., Caspar P., Mellman I., Sher A. Host ER-parasitophorous vacuole interaction provides a route of entry for antigen cross-presentation in Toxoplasma gondii-infected dendritic cells. J Exp Med 2009, 206:399-410.
35. Lopez J., Bittame A., Massera C., Vasseur V., Effantin G., Valat A., Buaillon C., Allart S., Fox B.A., Rommereim L.M., et al. Intravacuolar membranes regulate CD8 T cell recognition of membrane-bound Toxoplasma gondii protective antigen. Cell Rep 2015, 13:2272-2286.
36. Urban B.C., Ferguson D.J., Pain A., Willcox N., Plebanski M., Austyn J.M., Roberts D.J. Plasmodium falciparum-infected erythrocytes modulate the maturation of dendritic cells. Nature 1999, 400:73-77.
37. Wykes M.N., Good M.F. What really happens to dendritic cells during malaria?. Nat Rev Microbiol 2008, 6:864-870.
38. Wykes M.N., Liu X.Q., Beattie L., Stanisic D.I., Stacey K.J., Smyth M.J., Thomas R., Good M.F. Plasmodium strain determines dendritic cell function essential for survival from malaria. PLoS Pathog 2007, 3:e96.
39. Pinzon-Charry A., Woodberry T., Kienzle V., McPhun V., Minigo G., Lampah D.A., Kenangalem E., Engwerda C., Lopez J.A., Anstey N.M., et al. Apoptosis and dysfunction of blood dendritic cells in patients with falciparum and vivax malaria. J Exp Med 2013, 210:1635-1646.
40. Woodberry T., Minigo G., Piera K.A., Amante F.H., Pinzon-Charry A., Good M.F., Lopez J.A., Engwerda C.R., McCarthy J.S., Anstey N.M. Low-level Plasmodium falciparum blood-stage infection causes dendritic cell apoptosis and dysfunction in healthy volunteers. J Infect Dis 2012, 206:333-340.
41. Kho S., Marfurt J., Noviyanti R., Kusuma A., Piera K.A., Burdam F.H., Kenangalem E., Lampah D.A., Engwerda C.R., Poespoprodjo J.R., et al. Preserved dendritic cell HLA-DR expression and reduced regulatory T cell activation in asymptomatic Plasmodium falciparum and P. vivax infection. Infect Immun 2015, 83:3224-3232.
42. Lundie R.J., de Koning-Ward T.F., Davey G.M., Nie C.Q., Hansen D.S., Lau L.S., Mintern J.D., Belz G.T., Schofield L., Carbone F.R., et al. 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 2008, 105:14509-14514.
43. Sponaas A.M., Cadman E.T., Voisine C., Harrison V., Boonstra A., O'Garra A., Langhorne J. Malaria infection changes the ability of splenic dendritic cell populations to stimulate antigen-specific T cells. J Exp Med 2006, 203:1427-1433.
44. Borges da Silva H., Fonseca R., Cassado Ados A., Machado de Salles E., de Menezes M.N., Langhorne J., Perez K.R., Cuccovia I.M., Ryffel B, Barreto V.M., et al. In vivo approaches reveal a key role for DCs in CD4+ T cell activation and parasite clearance during the acute phase of experimental blood-stage malaria. PLoS Pathog 2015, 11:e1004598.
45. Horne-Debets J.M., Faleiro R., Karunarathne D.S., Liu X.Q., Lineburg K.E., Poh C.M., Grotenbreg G.M., Hill G.R., MacDonald K.P., Good M.F., et al. PD-1 dependent exhaustion of CD8+ T cells drives chronic malaria. Cell Rep 2013, 5:1204-1213.
46. Imai T., Shen J., Chou B., Duan X., Tu L., Tetsutani K., Moriya C., Ishida H., Hamano S., Shimokawa C., et al. Involvement of CD8+ T cells in protective immunity against murine blood-stage infection with Plasmodium yoelii 17XL strain. Eur J Immunol 2010, 40:1053-1061.
47. Piva L., Tetlak P., Claser C., Karjalainen K., Renia L., Ruedl C. Cutting edge: Clec9A+ dendritic cells mediate the development of experimental cerebral malaria. J Immunol 2012, 189:1128-1132.
48. Nacer A., Movila A., Baer K., Mikolajczak S.A., Kappe S.H., Frevert U. Neuroimmunological blood-brain barrier opening in experimental cerebral malaria. PLoS Pathog 2012, 8:e1002982.
49. Pai S., Qin J., Cavanagh L., Mitchell A., El-Assaad F., Jain R., Combes V., Hunt N.H., Grau G.E., Weninger W. Real-time imaging reveals the dynamics of leukocyte behaviour during experimental cerebral malaria pathogenesis. PLoS Pathog 2014, 10:e1004236.
50. Shaw T.N., Stewart-Hutchinson P.J., Strangward P., Dandamudi D.B., Coles J.A., Villegas-Mendez A., Gallego-Delgado J., van Rooijen N., Zindy E., Rodriguez A., et al. Perivascular arrest of CD8+ T cells is a signature of experimental cerebral malaria. PLoS Pathog 2015, 11:e1005210.
51. Howland S.W., Poh C.M., Gun S.Y., Claser C., Malleret B., Shastri N., Ginhoux F., Grotenbreg G.M., Renia L. Brain microvessel cross-presentation is a hallmark of experimental cerebral malaria. EMBO Mol Med 2013, 5:916-931.
52. Howland S.W., Poh C.M., Renia L. Activated brain endothelial cells cross-present malaria antigen. PLoS Pathog 2015, 11:e1004963.
53. Jambou R., Combes V., Jambou M.J., Weksler B.B., Couraud P.O., Grau G.E. Plasmodium falciparum adhesion on human brain microvascular endothelial cells involves transmigration-like cup formation and induces opening of intercellular junctions. PLoS Pathog 2010, 6:e1001021.
54. El-Assaad F., Wheway J., Hunt N.H., Grau G.E., Combes V. Production, fate and pathogenicity of plasma microparticles in murine cerebral malaria. PLoS Pathog 2014, 10:e1003839.
55. Wheway J., Latham S.L., Combes V., Grau G.E. Endothelial microparticles interact with and support the proliferation of T cells. J Immunol 2014, 193:3378-3387.
56. Howland S.W., Ng G.X., Chia S.K., Renia L. Investigating proteasome inhibitors as potential adjunct therapies for experimental cerebral malaria. Parasite Immunol 2015, 37:599-604.