Prime and target immunization protects against liver-stage malaria in mice

Science Translational Medicine

Volumn 10, Issue 460, 2018, Pages

  Gola, Anita ^a,b   Silman, Daniel ^a   Walters, Adam A ^a   Sridhar, Saranya ^a   Uderhardt, Stefan ^b   Salman, Ahmed M ^a,c   Halbroth, Benedict R ^a   Bellamy, Duncan ^a   Bowyer, Georgina ^a   Powlson, Jonathan ^a   Baker, Megan ^a   Venkatraman, Navin ^a   Poulton, Ian ^a   Berrie, Eleanor ^a   Roberts, Rachel ^a   Lawrie, Alison M ^a   Angus, Brian ^d   Khan, Shahid M ^c   Janse, Chris J ^c   Ewer, Katie J ^a   Germain, Ronald N ^b   Spencer, Alexandra J ^a   Hill, Adrian V S ^a   more..

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER; NANOPARTICLE; OVALBUMIN;

ADMINISTRATION AND DOSAGE; ANIMAL; C57BL MOUSE; CD8+ T LYMPHOCYTE; CHEMISTRY; CLINICAL TRIAL; GENE VECTOR; GROWTH, DEVELOPMENT AND AGING; HUMAN; IMMUNIZATION; IMMUNOLOGY; INTRAVENOUS DRUG ADMINISTRATION; LIFE CYCLE STAGE; LIVER; LIVER CELL; MALARIA FALCIPARUM; METABOLISM; PARASITOLOGY; PATHOLOGY; PHASE 1 CLINICAL TRIAL; PHYSIOLOGY; PLASMODIUM BERGHEI; PLASMODIUM FALCIPARUM; SPOROZOITE;

ANIMALS; BIOMARKERS; CD8-POSITIVE T-LYMPHOCYTES; GENETIC VECTORS; HEPATOCYTES; HUMANS; IMMUNIZATION; INJECTIONS, INTRAVENOUS; LIFE CYCLE STAGES; LIVER; MALARIA, FALCIPARUM; MICE, INBRED C57BL; NANOPARTICLES; OVALBUMIN; PLASMODIUM BERGHEI; PLASMODIUM FALCIPARUM; POLYLACTIC ACID-POLYGLYCOLIC ACID COPOLYMER; SPOROZOITES;

EID: 85054083554     PISSN: 19466234     EISSN: 19466242     Source Type: Journal    
DOI: 10.1126/scitranslmed.aap9128     Document Type: Article

References (59)

1. S. Bhatt, D. J. Weiss, E. Cameron, D. Bisanzio, B. Mappin, U. Dalrymple, K. E. Battle, C. L. Moyes, A. Henry, P. A. Eckhoff, E. A. Wenger, O. Briët, M. A. Penny, T. A. Smith, A. Bennett, J. Yukich, T. P. Eisele, J. T. Griffin, C. A. Fergus, M. Lynch, F. Lindgren, J. M. Cohen, C. L. Murray, D. L. Smith, S. I. Hay, R. E. Cibulskis, P. W. Gething, The effect of malaria control on Plasmodium falciparum in Africa between 2000 and 2015. Nature 526, 207-211 (2015).
2. Global. WHO declares emergency against AIDS, TB, malaria. AIDS Policy Law 21, 5 (2006).
3. TRS, S Clinical Trials Partnership, S. T. Agnandji, B. Lell, S. S. Soulanoudjingar, J. F. Fernandes, J. F. Fernandes, B. P. Abossolo, C. Conzelmann, B. G. Methogo, Y. Doucka, A. Flamen, B. Mordmüller, S. Issifou, P. G. Kremsner, J. Sacarlal, P. Aide, M. Lanaspa, J. J. Aponte, A. Nhamuave, D. Quelhas, Q. Bassat, S. Mandjate, E. Macete, P. Alonso, S. Abdulla, N. Salim, O. Juma, M. Shomari, K. Shubis, F. Machera, A. S. Hamad, R. Minja, A. Mtoro, A. Sykes, S. Ahmed, A. M. Urassa, A. M. Ali, G. Mwangoka, M. Tanner, H. Tinto, U. D'Alessandro, H. Sorgho, I. Valea, M. C. Tahita, W. Kaboré, S. Ouédraogo, Y. Sandrine, R. T. Guiguemdé, J. B. Ouédraogo, M. J. Hamel, S. Kariuki, C. Odero, M. Oneko, K. Otieno, N. Awino, J. Omoto, J. Williamson, V. Muturi-Kioi, K. F. Laserson, L. Slutsker, W. Otieno, L. Otieno, O. Nekoye, S. Gondi, A. Otieno, B. Ogutu, R. Wasuna, V. Owira, D. Jones, A. A. Onyango, P. Njuguna, R. Chilengi, P. Akoo, C. Kerubo, J. Gitaka, C. Maingi, T. Lang, A. Olotu, B. Tsofa, P. Bejon, N. Peshu, K. Marsh, S. Owusu-Agyei, K. P. Asante, K. Osei-Kwakye, O. Boahen, S. Ayamba, K. Kayan, R. Owusu-Ofori, D. Dosoo, I. Asante, G. Adjei, G. Adjei, D. Chandramohan, B. Greenwood, J. Lusingu, S. Gesase, A. Malabeja, O. Abdul, H. Kilavo, C. Mahende, E. Liheluka, M. Lemnge, T. Theander, C. Drakeley, D. Ansong, T. Agbenyega, S. Adjei, H. O. Boateng, T. Rettig, J. Bawa, J. Sylverken, D. Sambian, A. Agyekum, L. Owusu, F. Martinson, I. Hoffman, T. Mvalo, P. Kamthunzi, R. Nkomo, A. Msika, A. Jumbe, N. Chome, D. Nyakuipa, J. Chintedza, W. R. Ballou, M. Bruls, J. Cohen, Y. Guerra, E. Jongert, D. Lapierre, A. Leach, M. Lievens, O. Ofori-Anyinam, J. Vekemans, T. Carter, D. Leboulleux, C. Loucq, A. Radford, B. Savarese, D. Schellenberg, M. Sillman, P. Vansadia, First results of phase 3 trial of RTS, S/AS01 malaria vaccine in African children. N. Engl. J. Med. 365, 1863-1875 (2011).
4. + T cells and antibodies required for immunity to malaria sporozoites. Nature 330, 664-666 (1987).
5. W. R. Weiss, M. Sedegah, R. L. Beaudoin, L. H. Miller, M. F. Good, 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 (1988).
6. A. V. Hill, A. Reyes-Sandoval, G. O'Hara, K. Ewer, A. Lawrie, A. Goodman, A. Nicosia, A. Folgori, S. Colloca, R. Cortese, S. C. Gilbert, S. J. Draper, Prime-boost vectored malaria vaccines: Progress and prospects. Hum. Vaccin. 6, 78-83 (2010).
7. S. Li, M. Rodrigues, D. Rodriguez, J. R. Rodriguez, M. Esteban, P. Palese, R. S. Nussenzweig, F. Zavala, 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 (1993).
8. + T-cell immunity to human malaria induced by chimpanzee adenovirus-MVA immunisation. Nat. Commun. 4, 2836 (2013).
9. + T-cell responses. Infect. Immun. 78, 145-153 (2010).
10. S. Capone, A. Reyes-Sandoval, M. Naddeo, L. Siani, V. Ammendola, C. S. Rollier, A. Nicosia, S. Colloca, R. Cortese, A. Folgori, A. V. Hill, Immune responses against a liver-stage malaria antigen induced by simian adenoviral vector AdCh63 and MVA prime-boost immunisation in non-human primates. Vaccine 29, 256-265 (2010).
11. C. Ogwang, D. Kimani, N. J. Edwards, R. Roberts, J. Mwacharo, G. Bowyer, C. Bliss, S. H. Hodgson, P. Njuguna, N. K. Viebig, A. Nicosia, E. Gitau, S. Douglas, J. Illingworth, K. Marsh, A. Lawrie, E. B. Imoukhuede, K. Ewer, B. C. Urban, A. V. S. Hill, P. Bejon; MVVC Group, Prime-boost vaccination with chimpanzee adenovirus and modified vaccinia Ankara encoding TRAP provides partial protection against Plasmodium falciparum infection in Kenyan adults. Sci. Transl. Med. 7, 286re285 (2015).
12. S. Dunachie, A. V. S. Hill, H. A. Fletcher, Profiling the host response to malaria vaccination and malaria challenge. Vaccine 33, 5316-5320 (2015).
13. I. A. Cockburn, Y.-C. Chen, M. G. Overstreet, J. R. Lees, N. van Rooijen, D. L. Farber, F. Zavala, Prolonged antigen presentation is required for optimal CD8+ T cell responses against malaria liver stage parasites. PLOS Pathog. 6, e1000877 (2010).
14. I. N. Crispe, M. Giannandrea, I. Klein, B. John, B. Sampson, S. Wuensch, Cellular and molecular mechanisms of liver tolerance. Immunol. Rev. 213, 101-118 (2006).
15. U. Protzer, M. K. Maini, P. A. Knolle, Living in the liver: Hepatic infections. Nat. Rev. Immunol. 12, 201-213 (2012).
16. S. S. Tay, Y. C. Wong, D. M. McDonald, N. A. W. Wood, B. Roediger, F. Sierro, C. McGuffog, I. E. Alexander, G. A. Bishop, J. R. Gamble, W. Weninger, G. W. McCaughan, P. Bertolino, D. G. Bowen, Antigen expression level threshold tunes the fate of CD8 T cells during primary hepatic immune responses. Proc. Natl. Acad. Sci. U.S.A. 111, E2540-E2549 (2014).
17. T. Gebhardt, L. M. Wakim, L. Eidsmo, P. C. Reading, W. R. Heath, F. R. Carbone, Memory T cells in nonlymphoid tissue that provide enhanced local immunity during infection with herpes simplex virus. Nat. Immunol. 10, 524-530 (2009).
18. D. Masopust, D. Choo, V. Vezys, E. J. Wherry, J. Duraiswamy, R. Akondy, J. Wang, K. A. Casey, D. L. Barber, K. S. Kawamura, K. A. Fraser, R. J. Webby, V. Brinkmann, E. C. Butcher, K. A. Newell, R. Ahmed, Dynamic T cell migration program provides resident memory within intestinal epithelium. J. Exp. Med. 207, 553-564 (2010).
19. D. Masopust, V. Vezys, E. J. Wherry, D. L. Barber, R. Ahmed, Cutting edge: Gut microenvironment promotes differentiation of a unique memory CD8 T cell population. J. Immunol. 176, 2079-2083 (2006).
20. E. M. Steinert, J. M. Schenkel, K. A. Fraser, L. K. Beura, L. S. Manlove, B. Z. Igyártó, P. J. Southern, D. Masopust, Quantifying memory CD8 T cells reveals regionalization of immunosurveillance. Cell 161, 737-749 (2015).
21. + T cells during infection with influenza virus due to selective expression of IFITM3. Nat. Immunol. 14, 238-245 (2013).
22. + T cells. Nature 477, 216-219 (2011).
23. J. M. Schenkel, K. A. Fraser, L. K. Beura, K. E. Pauken, V. Vezys, D. Masopust, Resident memory CD8 T cells trigger protective innate and adaptive immune responses. Science 346, 98-101 (2014).
24. + T cells induced by immunization with malaria sporozoites. Genes Immun. 14, 302-309 (2013).
25. S.-W. Tse, A. J. Radtke, D. A. Espinosa, I. A. Cockburn, F. Zavala, The chemokine receptor CXCR6 is required for the maintenance of liver memory CD8+ T cells specific for infectious pathogens. J. Infect. Dis. 210, 1508-1516 (2014).
26. + T cell immunity. Science 334, 475-480 (2011).
27. L. M. Wakim, J. Smith, I. Caminschi, M. H. Lahoud, J. A. Villadangos, Antibody-targeted vaccination to lung dendritic cells generates tissue-resident memory CD8 T cells that are highly protective against influenza virus infection. Mucosal Immunol. 8, 1060-1071 (2015).
28. H. Shin, A. Iwasaki, A vaccine strategy that protects against genital herpes by establishing local memory T cells. Nature 491, 463-467 (2012).
29. + T cell response to respiratory virus infections. Immunity 29, 101-113 (2008).
30. RM) cells in the absence of persisting local antigen presentation. Proc. Natl. Acad. Sci. U.S.A. 109, 7037-7042 (2012).
31. G. Stary, A. Olive, A. F. Radovic-Moreno, D. Gondek, D. Alvarez, P. A. Basto, M. Perro, V. D. Vrbanac, A. M. Tager, J. Shi, J. A. Yethon, O. C. Farokhzad, R. Langer, M. N. Starnbach, U. H. von Andrian, A mucosal vaccine against Chlamydia trachomatis generates two waves of protective memory T cells. Science 348, aaa8205 (2015).
32. + T cells form a front-line defense against malaria liver-stage infection. Immunity 45, 889-902 (2016).
33. A. K. Mohammad, J. J. Reineke, Quantitative detection of PLGA nanoparticle degradation in tissues following intravenous administration. Mol. Pharm. 10, 2183-2189 (2013).
34. S. Stoll, J. Delon, T. M. Brotz, R. N. Germain, Dynamic imaging of T cell-dendritic cell interactions in lymph nodes. Science 296, 1873-1876 (2002).
35. J.-W. Lin, T. N. Shaw, T. Annoura, A. Fougère, P. Bouchier, S. Chevalley-Maurel, H. Kroeze, B. Franke-Fayard, C. J. Janse, K. N. Couper, S. M. Khan, The subcellular location of ovalbumin in Plasmodium berghei blood stages influences the magnitude of T-cell responses. Infect. Immun. 82, 4654-4665 (2014).
36. S. Mandala, R. Hajdu, J. Bergstrom, E. Quackenbush, J. Xie, J. Milligan, R. Thornton, G.-J. Shei, D. Card, C. Keohane, M. Rosenbach, J. Hale, C. L. Lynch, K. Rupprecht, W. Parsons, H. Rosen, Alteration of lymphocyte trafficking by sphingosine-1-phosphate receptor agonists. Science 296, 346-349 (2002).
37. S. P. Kasturi, I. Skountzou, R. A. Albrecht, D. Koutsonanos, T. Hua, H. I. Nakaya, R. Ravindran, S. Stewart, M. Alam, M. Kwissa, F. Villinger, N. Murthy, J. Steel, J. Jacob, R. J. Hogan, A. Garcia-Sastre, R. Compans, B. Pulendran, Programming the magnitude and persistence of antibody responses with innate immunity. Nature 470, 543-547 (2011).
38. S. Bruno, Z. Darzynkiewicz, Cell cycle dependent expression and stability of the nuclear protein detected by Ki-67 antibody in HL-60 cells. Cell Prolif. 25, 31-40 (1992).
39. + T cell-mediated elimination of malaria liver stages. Proc. Natl. Acad. Sci. U.S.A. 110, 9090-9095 (2013).
40. + 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 (2013).
41. S. L. Hoffman, D. Isenbarger, G. W. Long, M. Sedegah, A. Szarfman, L. Waters, M. R. Hollingdale, P. H. van der Meide, D. S. Finbloom, W. R. Ballou, Sporozoite vaccine induces genetically restricted T cell elimination of malaria from hepatocytes. Science 244, 1078-1081 (1989).
42. N. Iijima, A. Iwasaki, T cell memory. A local macrophage chemokine network sustains protective tissue-resident memory CD4 T cells. Science 346, 93-98 (2014).
43. M. Y. Gerner, W. Kastenmuller, I. Ifrim, J. Kabat, R. N. Germain, Histo-cytometry: A method for highly multiplex quantitative tissue imaging analysis applied to dendritic cell subset microanatomy in lymph nodes. Immunity 37, 364-376 (2012).
44. H. A. McNamara, Y. Cai, M. V. Wagle, Y. Sontani, C. M. Roots, L. A. Miosge, J. H. O'Connor, H. J. Sutton, V. V. Ganusov, W. R. Heath, P. Bertolino, C. G. Goodnow, I. A. Parish, A. Enders, I. A. Cockburn, Up-regulation of LFA-1 allows liver-resident memory T cells to patrol and remain in the hepatic sinusoids. Sci. Immunol. 2, eaaj1996 (2017).
45. M. Cabrera, L. L. Pewe, J. T. Harty, U. Frevert, In vivo CD8+ T cell dynamics in the liver of Plasmodium yoelii immunized and infected mice. PLOS ONE 8, e70842 (2013).
46. T. I. Arnon, J. G. Cyster, Blood, sphingosine-1-phosphate and lymphocyte migration dynamics in the spleen. Curr. Top. Microbiol. Immunol. 378, 107-128 (2014).
47. K. J. Ewer, T. Lambe, C. S. Rollier, A. J. Spencer, A. V. Hill, L. Dorrell, Viral vectors as vaccine platforms: From immunogenicity to impact. Curr. Opin. Immunol. 41, 47-54 (2016).
48. P. Romero, J. L. Maryanski, G. Corradin, R. S. Nussenzweig, V. Nussenzweig, F. Zavala, Cloned cytotoxic T cells recognize an epitope in the circumsporozoite protein and protect against malaria. Nature 341, 323-326 (1989).
49. R. J. Longley, A. M. Salman, M. G. Cottingham, K. Ewer, C. J. Janse, S. M. Khan, A. J. Spencer, A. V. S. Hill, Comparative assessment of vaccine vectors encoding ten malaria antigens identifies two protective liver-stage candidates. Sci. Rep. 5, 11820 (2015).
50. A. M. Salman, C. M. Mogollon, J.-W. Lin, F. J. A. van Pul, C. J. Janse, S. M. Khan, Generation of transgenic rodent malaria parasites expressing human malaria parasite proteins. Methods Mol. Biol. 1325, 257-286 (2015).
51. J. Nemunaitis, C. Cunningham, A. Buchanan, A. Blackburn, G. Edelman, P. Maples, G. Netto, A. Tong, B. Randlev, S. Olson, D. Kirn, Intravenous infusion of a replicationselective adenovirus (ONYX-015) in cancer patients: Safety, feasibility and biological activity. Gene Ther. 8, 746-759 (2001).
52. T. Reid, E. Galanis, J. Abbruzzese, D. Sze, L. M. Wein, J. Andrews, B. Randlev, C. Heise, M. Uprichard, M. Hatfield, L. Rome, J. Rubin, D. Kirn, Hepatic arterial infusion of a replication-selective oncolytic adenovirus (dl1520): Phase II viral, immunologic, and clinical endpoints. Cancer Res. 62, 6070-6079 (2002).
53. E. J. Small, M. A. Carducci, J. M. Burke, R. Rodriguez, L. Fong, L. van Ummersen, D. C. Yu, J. Aimi, D. Ando, P. Working, D. Kirn, G. Wilding, A phase I trial of intravenous CG7870, a replication-selective, prostate-specific antigen-targeted oncolytic adenovirus, for the treatment of hormone-refractory, metastatic prostate cancer. Mol. Ther. 14, 107-117 (2006).
54. S. H. Hodgson, K. J. Ewer, C. M. Bliss, N. J. Edwards, T. Rampling, N. A. Anagnostou, E. de Barra, T. Havelock, G. Bowyer, I. D. Poulton, S. de Cassan, R. Longley, J. J. Illingworth, A. D. Douglas, P. B. Mange, K. A. Collins, R. Roberts, S. Gerry, E. Berrie, S. Moyle, S. Colloca, R. Cortese, R. E. Sinden, S. C. Gilbert, P. Bejon, A. M. Lawrie, A. Nicosia, S. N. Faust, A. V. S. Hill, Evaluation of the efficacy of ChAd63-MVA vectored vaccines expressing circumsporozoite protein and ME-TRAP against controlled human malaria infection in malaria-naive individuals. J. Infect. Dis. 211, 1076-1086 (2015).
55. S. Franz, P. Rennert, M. Woznik, J. Grützke, A. Lüdde, E. M. Arriero Pais, T. Finsterbusch, H. Geyer, A. Mankertz, N. Friedrich, Mumps virus SH protein inhibits NF-κB activation by interacting with tumor necrosis factor receptor 1, interleukin-1 receptor 1, and toll-like receptor 3 complexes. J. Virol. 91, e01037-17 (2017).
56. N. W. Schmidt, N. S. Butler, V. P. Badovinac, J. T. Harty, Extreme CD8 T cell requirements for anti-malarial liver-stage immunity following immunization with radiation attenuated sporozoites. PLOS Pathog. 6, e1000998 (2010).
57. K. A. Hogquist, S. C. Jameson, W. R. Heath, J. L. Howard, M. J. Bevan, F. R. Carbone, T cell receptor antagonist peptides induce positive selection. Cell 76, 17-27 (1994).
58. + T cell responses to malaria antigen ME-TRAP by fusion to MHC class II invariant chain. PLOS ONE 9, e100538 (2014).
59. D. Bates, M. Mächler, B. Bolker, S. Walker, Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1-48 (2015).