TAP-mediated processing of exoerythrocytic antigens is essential for protection induced with radiation-attenuated Plasmodium sporozoites

European Journal of Immunology

Volumn 46, Issue 4, 2016, Pages 885-896

  Pichugin, Alexander ^a   Steers, Nick ^a   De la vega, Patricia ^a   Zarling, Stasya ^a   Chalom, Isaac ^a   Krzych, Urszula ^a  

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

Author keywords

Antigen presenting cells CD8+ T cells Liver Plasmodium Transporter associated with antigen processing (TAP)

Indexed keywords

ANTIGEN; CD8 ANTIGEN; GAMMA INTERFERON; MEMBRANE PROTEIN; ABC TRANSPORTER; CIRCUMSPOROZOITE PROTEIN, PROTOZOAN; HLA ANTIGEN CLASS 1; PARASITE ANTIGEN; PROTOZOAL PROTEIN; TRANSPORTER ASSOCIATED WITH ANTIGEN PROCESSING (TAP);

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ARTICLE; CD8+ T LYMPHOCYTE; CELL DIFFERENTIATION; CONTROLLED STUDY; CROSS PRESENTATION; CYTOSOL; FEMALE; IMMUNIZATION; MOUSE; NONHUMAN; PHAGOSOME; PLASMODIUM; PLASMODIUM BERGHEI; PRIORITY JOURNAL; PROTEIN PROCESSING; RADIATION; RADIATION PROTECTION; SPOROZOITE; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CYTOLOGY; GENETICS; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; KNOCKOUT MOUSE; LIVER; MALARIA; PARASITOLOGY; RADIATION RESPONSE;

ANIMALS; ANTIGEN PRESENTATION; ANTIGENS, PROTOZOAN; ATP-BINDING CASSETTE TRANSPORTERS; CD8-POSITIVE T-LYMPHOCYTES; CELL DIFFERENTIATION; FEMALE; HISTOCOMPATIBILITY ANTIGENS CLASS I; IMMUNIZATION; IMMUNOLOGIC MEMORY; INTERFERON-GAMMA; LIVER; MALARIA; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PLASMODIUM BERGHEI; PROTOZOAN PROTEINS; SPOROZOITES;

EID: 84958074081     PISSN: 00142980     EISSN: 15214141     Source Type: Journal    
DOI: 10.1002/eji.201545748     Document Type: Article

References (65)

1. Harty, J. T., Tvinnereim, A. R. and White, D. W., CD8+ T cell effector mechanisms in resistance to infection. Annu. Rev. Immunol. 2000. 18: 275-308.
2. Chen, L. and Flies, D. B., Molecular mechanisms of T cell co-stimulation and co-inhibition. Nat. Rev. Immunol. 2013. 13: 227-242.
3. Mescher, M. F., Curtsinger, J. M., Agarwal, P., Casey, K. A., Gerner, M., Hammerbeck, C. D., Popescu, F. et al., Signals required for programming effector and memory development by CD8+ T cells. Immunol. Rev. 2006. 211: 81-92.
4. Serwold, T., Gonzalez, F., Kim, J., Jacob, R. and Shastri, N., ERAAP customizes peptides for MHC class I molecules in the endoplasmic reticulum. Nature 2002. 419: 480-483.
5. Rock, K. L. and Shen, L., Cross-presentation: underlying mechanisms and role in immune surveillance. Immunol. Rev. 2005. 207: 166-183.
6. Houde, M., Bertholet, S., Gagnon, E., Brunet, S., Goyette, G., Laplante, A., Princiotta, M. F. et al., Phagosomes are competent organelles for antigen cross-presentation. Nature 2003. 425: 402-406.
7. Ackerman, A. L., Kyritsis, C., Tampe, R. and Cresswell, P., Early phagosomes in dendritic cells form a cellular compartment sufficient for cross presentation of exogenous antigens. Proc. Natl. Acad. Sci. U.S.A. 2003. 100: 12889-12894.
8. Guermonprez, P., Saveanu, L., Kleijmeer, M., Davoust, J., Van Endert, P. and Amigorena, S., ER-phagosome fusion defines an MHC class I cross-presentation compartment in dendritic cells. Nature 2003. 425: 397-402.
9. Jutras, I. and Desjardins, M., Phagocytosis: at the crossroads of innate and adaptive immunity. Annu. Rev. Cell. Dev. Biol. 2005. 21: 511-527.
10. Shen, L., Sigal, L. J., Boes, M. and Rock, K. L., Important role of cathepsin S in generating peptides for TAP-independent MHC class I crosspresentation in vivo. Immunity 2004. 21: 155-165.
11. Shen, L. and Rock, K. L., Priming of T cells by exogenous antigen cross-presented on MHC class I molecules. Curr. Opin. Immunol. 2006. 18: 85-91.
12. Rock, K. L., Exiting the outside world for cross-presentation. Immunity 2006. 25: 523-525.
13. Clyde, D. F., Most, H., McCarthy, V. C. and Vanderberg, J. P., Immunization of man against sporozite-induced falciparum malaria. Am. J. Med. Sci. 1973. 266: 169-177.
14. Epstein, J. E., Tewari, K., Lyke, K. E., Sim, B. K., Billingsley, P. F., Laurens, M. B., Gunasekera, A. et al., Live attenuated malaria vaccine designed to protect through hepatic CD8(+) T cell immunity. Science 2011. 334: 475-480.
15. Rieckmann, K. H., Beaudoin, R. L., Cassells, J. S. and Sell, K. W., Use of attenuated sporozoites in the immunization of human volunteers against falciparum malaria. Bull. World. Health. Organ. 1979. 57(Suppl 1): 261-265.
16. Nussenzweig, R. S., Vanderberg, J., Most, H. and Orton, C., Protective immunity produced by the injection of x-irradiated sporozoites of Plasmodium berghei. Nature 1967. 216: 160-162.
17. Weiss, W. R., Sedegah, M., Beaudoin, R. L., Miller, L. H. and Good, M. F., CD8+ T cells (cytotoxic/suppressors) are required for protection in mice immunized with malaria sporozoites. Proc. Natl. Acad. Sci. U.S.A. 1988. 85: 573-576.
18. White, K. L., Snyder, H. L. and Krzych, U., MHC class I-dependent presentation of exoerythrocytic antigens to CD8+ T lymphocytes is required for protective immunity against Plasmodium berghei. J. Immunol. 1996. 156: 3374-3381.
19. Jobe, O., Lumsden, J., Mueller, A. K., Williams, J., Silva-Rivera, H., Kappe, S. H., Schwenk, R. J. et al., Genetically attenuated Plasmodium berghei liver stages induce sterile protracted protection that is mediated by major histocompatibility complex Class I-dependent interferon-gamma-producing CD8+ T cells. J. Infect. Dis. 2007. 196: 599-607.
20. Mueller, A. K., Labaied, M., Kappe, S. H. and Matuschewski, K., Genetically modified Plasmodium parasites as a protective experimental malaria vaccine. Nature 2005. 433: 164-167.
21. Tarun, A. S., Dumpit, R. F., Camargo, N., Labaied, M., Liu, P., Takagi, A., Wang, R. et al., Protracted sterile protection with Plasmodium yoelii pre-erythrocytic genetically attenuated parasite malaria vaccines is independent of significant liver-stage persistence and is mediated by CD8+ T cells. J. Infect. Dis. 2007. 196: 608-616.
22. Trimnell, A., Takagi, A., Gupta, M., Richie, T. L., Kappe, S. H. and Wang, R., Genetically attenuated parasite vaccines induce contact-dependent CD8+ T cell killing of Plasmodium yoelii liver stage-infected hepatocytes. J. Immunol. 2009. 183: 5870-5878.
23. Berenzon, D., Schwenk, R. J., Letellier, L., Guebre-Xabier, M., Williams, J. and Krzych, U., Protracted protection to Plasmodium berghei malaria is linked to functionally and phenotypically heterogeneous liver memory CD8+ T cells. J. Immunol. 2003. 171: 2024-2034.
24. Cockburn, I. A., Tse, S. W., Radtke, A. J., Srinivasan, P., Chen, Y. C., Sinnis, P. and Zavala, F., Dendritic cells and hepatocytes use distinct pathways to process protective antigen from plasmodium in vivo. PLoS Pathog. 2011. 7: e1001318.
25. Kimura, K., Kimura, D., Matsushima, Y., Miyakoda, M., Honma, K., Yuda, M. and 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.
26. Frevert, U., Intravital observation of Plasmodium berghei sporozoite infection of the liver. PLoS Biol. 2005. 3: e192.
27. Pradel, G., Garapaty, S. and Frevert, U., Proteoglycans mediate malaria sporozoite targeting to the liver. Mol. Microbiol. 2002. 45: 637-651.
28. Hugel, F. U., Pradel, G. and Frevert, U., Release of malaria circumsporozoite protein into the host cell cytoplasm and interaction with ribosomes. Mol. Biochem. Parasitol. 1996. 81: 151-170.
29. Khan, Z. M., Ng, C. and Vanderberg, J. P., Early hepatic stages of Plasmodium berghei: release of circumsporozoite protein and host cellular inflammatory response. Infect. Immun. 1992. 60: 264-270.
30. Kumar, K. A., Sano, G., Boscardin, S., Nussenzweig, R. S., Nussenzweig, M. C., Zavala, F. and Nussenzweig, V., The circumsporozoite protein is an immunodominant protective antigen in irradiated sporozoites. Nature 2006. 444: 937-940.
31. Gruner, A. C., Mauduit, M., Tewari, R., Romero, J. F., Depinay, N., Kayibanda, M., Lallemand, E. et al., Sterile protection against malaria is independent of immune responses to the circumsporozoite protein. PLoS One 2007. 2: e1371.
32. Hafalla, J. C., Bauza, K., Friesen, J., Gonzalez-Aseguinolaza, G., Hill, A. V. and Matuschewski, K., Identification of targets of CD8(+) T cell responses to malaria liver stages by genome-wide epitope profiling. PLoS Pathog. 2013. 9: e1003303.
33. Limbach, K., Aguiar, J., Gowda, K., Patterson, N., Abot, E., Sedegah, M., Sacci, J. et al., Identification of two new protective pre-erythrocytic malaria vaccine antigen candidates. Malar. J. 2011. 10: 65.
34. Speake, C. and Duffy, P. E., Antigens for pre-erythrocytic malaria vaccines: building on success. Parasite Immunol. 2009. 31: 539-546.
35. Bongfen, S. E., Torgler, R., Romero, J. F., Renia, L. and 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.
36. Tulone, C., Sponaas, A. M., Raiber, E. A., Tabor, A. B., Langhorne, J. and Chain, B. M., Differential requirement for cathepsin D for processing of the full length and C-terminal fragment of the malaria antigen MSP1. PLoS One 2011. 6: e24886.
37. Rock, K. L. and Shen, L., Cross-presentation: underlying mechanisms and role in immune surveillance. Immunol. Rev. 2005. 207: 166-183.
38. Sandberg, J. K., Chambers, B. J., Van Kaer, L., Karre, K. and Ljunggren, H. G., TAP1-deficient mice select a CD8+ T cell repertoire that displays both diversity and peptide specificity. Eur. J. Immunol. 1996. 26: 288-293.
39. Bertholet, S., Goldszmid, R., Morrot, A., Debrabant, A., Afrin, F., Collazo-Custodio, C., Houde, M. et al., Leishmania antigens are presented to CD8+ T cells by a transporter associated with antigen processing-independent pathway in vitro and in vivo. J. Immunol. 2006. 177: 3525-3533.
40. Zarling, S., Berenzon, D., Dalai, S., Liepinsh, D., Steers, N. and Krzych, U., The survival of memory CD8 T cells that is mediated by IL-15 correlates with sustained protection against malaria. J. Immunol. 2013. 190: 5128-5141.
41. Krzych, U., Dalai, S., Ehourler, L., Jobe, O. and Egner, L., Infectious challenge of Plasmodium berghei (gamma)-spz immunized mice rescues effector CD8+ T cells, thus assuring protracted protection. J. Immunol. 2010. 184: 52.9.
42. Cockburn, I. A., Tse, S. W. and Zavala, F., CD8+ T cells eliminate liver stage Plasmodium parasites without detectable bystander effect. Infect. Immun. 2014. 82: 1460-1464.
43. Lumsden, J. M., Cranmer, M. A. and Krzych, U., An early commitment to expression of a particular TCRVbeta chain on CD8(+) T cells responding to attenuated Plasmodium berghei sporozoites is maintained following challenge with infectious sporozoites. Parasite Immunol. 2010. 32: 644-655.
44. Weiss, W. R., Mellouk, S., Houghten, R. A., Sedegah, M., Kumar, S., Good, M. F., Berzofsky, J. A. et al., Cytotoxic T cells recognize a peptide from the circumsporozoite protein on malaria-infected hepatocytes. J. Exp. Med. 1990. 171: 763-773.
45. Scheller, L.F. and Azad, A.F., Maintenance of protective immunity against malaria by persistent hepatic parasites derived from irradiated sporozoites. Proc. Natl. Acad. Sci. U.S.A. 1995. 92: 4066-4068.
46. Leiriao, P., Mota, M. M. and Rodriguez, A., Apoptotic Plasmodium-infected hepatocytes provide antigens to liver dendritic cells. J. Infect. Dis. 2005. 191: 1576-1581.
47. Renia, L., Maranon, C., Hosmalin, A., Gruner, A. C., Silvie, O. and Snounou, G., Do apoptotic Plasmodium-infected hepatocytes initiate protective immune responses? J. Infect. Dis. 2006. 193: 163-164; author reply 164-165.
48. Jobe, O., Donofrio, G., Sun, G., Liepinsh, D., Schwenk, R. and Krzych, U., Immunization with radiation-attenuated Plasmodium berghei sporozoites induces liver cCD8alpha+DC that activate CD8+T cells against liver-stage malaria. PLoS One 2009. 4: e5075.
49. Gromme, M., Uytdehaag, F. G., Janssen, H., Calafat, J., van Binnendijk, R. S., Kenter, M. J., Tulp, A. et al., Recycling MHC class I molecules and endosomal peptide loading. Proc. Natl. Acad. Sci. U.S.A. 1999. 96: 10326-10331.
50. Chakravarty, S., Cockburn, I. A., Kuk, S., Overstreet, M. G., Sacci, J. B. and Zavala, F., CD8+ T lymphocytes protective against malaria liver stages are primed in skin-draining lymph nodes. Nat. Med. 2007. 13: 1035-1041.
51. Bertolino, P., Trescol-Biemont, M. C. and Rabourdin-Combe, C., Hepatocytes induce functional activation of naive CD8+ T lymphocytes but fail to promote survival. Eur. J. Immunol. 1998. 28: 221-236.
52. Savina, A., Jancic, C., Hugues, S., Guermonprez, P., Vargas, P., Moura, I. C., Lennon-Dumenil, A. M. et al., NOX2 controls phagosomal pH to regulate antigen processing during crosspresentation by dendritic cells. Cell 2006. 126: 205-218.
53. Delamarre, L., Pack, M., Chang, H., Mellman, I. and Trombetta, E.S., Differential lysosomal proteolysis in antigen-presenting cells determines antigen fate. Science 2005. 307: 1630-1634.
54. Butler, N. S., Schmidt, N. W., Vaughan, A. M., Aly, A. S., Kappe, S. H. and Harty, J. T., Superior antimalarial immunity after vaccination with late liver stage-arresting genetically attenuated parasites. Cell Host Microbe. 2011. 9: 451-462.
55. Balam, S., Romero, J. F., Bongfen, S. E., Guillaume, P. and Corradin, G., CSP-a model for in vivo presentation of Plasmodium berghei sporozoite antigens by hepatocytes. PLoS One 2012. 7: e51875.
56. Willberg, C. B., Ward, S. M., Clayton, R. F., Naoumov, N. V., McCormick, C., Proto, S., Harris, M. et al., Protection of hepatocytes from cytotoxic T cell mediated killing by interferon-alpha. PLoS One 2007. 2: e791.
57. Cockburn, I. A., Amino, R., Kelemen, R. K., Kuo, S. C., Tse, S. W., Radtke, A., Mac-Daniel, L. et al., In vivo imaging of CD8+ T cell-mediated elimination of malaria liver stages. Proc. Natl. Acad. Sci. U.S.A. 2013. 110: 9090-9095.
58. Gubbels, M.J., Striepen, B., Shastri, N., Turkoz, M. and Robey, E.A., Class I major histocompatibility complex presentation of antigens that escape from the parasitophorous vacuole of Toxoplasma gondii. Infect. Immun. 2005. 73: 703-711.
59. Xu, J., Li, D., Ke, Z., Liu, R., Maubach, G. and Zhuo, L., Cathepsin S is aberrantly overexpressed in human hepatocellular carcinoma. Mol. Med. Rep. 2009. 2: 713-718.
60. Van Kaer, L., Ashton-Rickardt, P. G., Ploegh, H. L. and Tonegawa, S., TAP1 mutant mice are deficient in antigen presentation, surface class I molecules, and CD4-8+ T cells. Cell 1992. 71: 1205-1214.
61. Schmidt, N. W., Podyminogin, R. L., Butler, N. S., Badovinac, V. P., Tucker, B. J., Bahjat, K. S., Lauer, P. et al., Memory CD8 T cell responses exceeding a large but definable threshold provide long-term immunity to malaria. Proc. Natl. Acad. Sci. U.S.A. 2008. 105: 14017-14022.
62. Lanar, D. E., Sequence of the circumsporozoite gene of Plasmodium berghei ANKA clone and NK65 strain. Mol. Biochem. Parasitol. 1990. 39: 151-153.
63. Guebre-Xabier, M., Schwenk, R. and Krzych, U., Memory phenotype CD8(+) T cells persist in livers of mice protected against malaria by immunization with attenuated Plasmodium berghei sporozoites. Eur. J. Immunol. 1999. 29: 3978-3986.
64. Salem, M. L., Kadima, A. N., Cole, D. J. and Gillanders, W. E., Defining the antigen-specific T-cell response to vaccination and poly(I:C)/TLR3 signaling: evidence of enhanced primary and memory CD8 T-cell responses and antitumor immunity. J. Immunother. 2005. 28: 220-228.
65. Nussler, A. K., Di Silvio, M., Billiar, T. R., Hoffman, R. A., Geller, D. A., Selby, R., Madariaga, J. et al., Stimulation of the nitric oxide synthase pathway in human hepatocytes by cytokines and endotoxin. J. Exp. Med. 1992. 176: 261-264.