Mechanisms of Stage-Transcending Protection Following Immunization of Mice with Late Liver Stage-Arresting Genetically Attenuated Malaria Parasites

PLoS Pathogens

Volumn 11, Issue 5, 2015, Pages

  Sack, Brandon K ^a   Keitany, Gladys J ^b   Vaughan, Ashley M ^a   Miller, Jessica L ^a   Wang, Ruobing ^a   Kappe, Stefan H I ^a,c  

^a SEATTLE BIOMEDICAL RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF WASHINGTON SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MALARIA VACCINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; FEMALE; IMMUNE RESPONSE; IMMUNOFLUORESCENCE; INFECTION PREVENTION; MALARIA; MOUSE; NONHUMAN; SPOROZOITE; T CELL DEPLETION; VACCINATION; ANIMAL; B LYMPHOCYTE; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNIZATION; IMMUNOLOGY; LIVER; PARASITOLOGY; PLASMODIUM YOELII; PROCEDURES; T LYMPHOCYTE;

MAMMALIA; MUS; PLASMODIUM PARASITES; PLASMODIUM YOELII;

ANIMALS; B-LYMPHOCYTES; FEMALE; IMMUNIZATION; LIVER; MALARIA; MALARIA VACCINES; MICE; PLASMODIUM YOELII; SPOROZOITES; T-LYMPHOCYTES; VACCINATION;

EID: 84930329022     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1004855     Document Type: Article

References (82)

1. Vaughan A. M., Kappe S. H., Malaria vaccine development: persistent challenges. Current opinion in immunology 24, 324–331 (2012). doi: 10.1016/j.coi.2012.03.009 22521906
2. Duffy P. E., Sahu T., Akue A., Milman N., Anderson C., Pre-erythrocytic malaria vaccines: identifying the targets. Expert review of vaccines 11, 1261–1280 (2012). doi: 10.1586/erv.12.92 23176657
3. Stewart M. J., Nawrot R. J., Schulman S., Vanderberg J. P., Plasmodium berghei sporozoite invasion is blocked in vitro by sporozoite-immobilizing antibodies. Infection and immunity 51, 859–864 (1986). 3512436
4. Vanderberg J. P., Frevert U., Intravital microscopy demonstrating antibody-mediated immobilisation of Plasmodium berghei sporozoites injected into skin by mosquitoes. Int J Parasitol 34, 991–996 (2004). 15313126
5. Kebaier C., Voza T., Vanderberg J., Kinetics of mosquito-injected Plasmodium sporozoites in mice: fewer sporozoites are injected into sporozoite-immunized mice. PLoS pathogens 5, e1000399 (2009).
6. Hollingdale M. R., Zavala F., Nussenzweig R. S., Nussenzweig V., Antibodies to the protective antigen of Plasmodium berghei sporozoites prevent entry into cultured cells. J Immunol 128, 1929–1930 (1982).
7. Sack B. K., et al. Model for In Vivo Assessment of Humoral Protection against Malaria Sporozoite Challenge by Passive Transfer of Monoclonal Antibodies and Immune Serum. Infection and immunity 82, 808–817 (2014). doi: 10.1128/IAI.01249-13 24478094
8. Van Braeckel-Budimir N., Harty J. T., CD8 T-cell-mediated protection against liver-stage malaria: lessons from a mouse model. Frontiers in microbiology 5, 272 (2014). doi: 10.3389/fmicb.2014.00272 24936199
9. Agnandji S. T., et al. First results of phase 3 trial of RTS,S/AS01 malaria vaccine in African children. The New England journal of medicine 365, 1863–1875 (2011). doi: 10.1056/NEJMoa1102287 22007715
10. Agnandji S. T., et al. A phase 3 trial of RTS,S/AS01 malaria vaccine in African infants. The New England journal of medicine 367, 2284–2295 (2012). doi: 10.1056/NEJMoa1208394 23136909
11. Roestenberg M., et al. Protection against a malaria challenge by sporozoite inoculation. The New England journal of medicine 361, 468–477 (2009). doi: 10.1056/NEJMoa0805832 19641203
12. Roestenberg M., et al. Long-term protection against malaria after experimental sporozoite inoculation: an open-label follow-up study. Lancet 377, 1770–1776 (2011). doi: 10.1016/S0140-6736(11)60360-7 21514658
13. Bijker, E. M. et al. Cytotoxic Markers Associate With Protection Against Malaria in Human Volunteers Immunized With Plasmodium falciparum Sporozoites. The Journal of infectious diseases (2014).
14. Mueller A. K., et al. Plasmodium liver stage developmental arrest by depletion of a protein at the parasite-host interface. Proceedings of the National Academy of Sciences of the United States of America 102, 3022–3027 (2005). 15699336
15. Mueller A. K., Labaied M., Kappe S. H., Matuschewski K., Genetically modified Plasmodium parasites as a protective experimental malaria vaccine. Nature 433, 164–167 (2005). 15580261
16. Khan S. M., Janse C. J., Kappe S. H., Mikolajczak S. A., Genetic engineering of attenuated malaria parasites for vaccination. Current opinion in biotechnology 23, 908–916 (2012). doi: 10.1016/j.copbio.2012.04.003 22560204
17. Jobe O., 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. The Journal of infectious diseases 196, 599–607 (2007). 17624847
18. Peng X., et al. Artesunate versus chloroquine infection-treatment-vaccination defines stage-specific immune responses associated with prolonged sterile protection against both pre-erythrocytic and erythrocytic Plasmodium yoelii infection. J Immunol 193, 1268–1277 (2014). doi: 10.4049/jimmunol.1400296 24958899
19. Doll K. L., Harty J. T., Correlates of protective immunity following whole sporozoite vaccination against malaria. Immunologic research 59, 166–176 (2014). doi: 10.1007/s12026-014-8525-0 24825778
20. Epstein J. E., et al. Live attenuated malaria vaccine designed to protect through hepatic CD8(+) T cell immunity. Science 334, 475–480 (2011). doi: 10.1126/science.1211548 21903775
21. Tarun A. S., 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. The Journal of infectious diseases 196, 608–616 (2007). 17624848
22. Trimnell A., et al. Genetically attenuated parasite vaccines induce contact-dependent CD8+ T cell killing of Plasmodium yoelii liver stage-infected hepatocytes. J Immunol 183, 5870–5878 (2009). doi: 10.4049/jimmunol.0900302 19812194
23. Schmidt N. W., Butler N. S., Badovinac V. P., Harty J. T., Extreme CD8 T cell requirements for anti-malarial liver-stage immunity following immunization with radiation attenuated sporozoites. PLoS pathogens 6, e1000998 (2010).
24. Keitany G. J., et al. Immunization of mice with live-attenuated late liver stage-arresting P. yoelii parasites generates protective antibody responses to pre-erythrocytic stages of malaria. Infection and immunity (2014).
25. Doll K. L., Butler N. S., Harty J. T., CD8 T cell independent immunity after single dose infection-treatment-vaccination (ITV) against Plasmodium yoelii. Vaccine 32, 483–491 (2014). doi: 10.1016/j.vaccine.2013.11.058 24321740
26. Birkett A. J., Moorthy V. S., Loucq C., Chitnis C. E., Kaslow D. C., Malaria vaccine R&D in the Decade of Vaccines: breakthroughs, challenges and opportunities. Vaccine 31 Suppl 2, B233–243 (2013). doi: 10.1016/j.vaccine.2013.02.040 23598488
27. Ogutu B. R., et al. Blood stage malaria vaccine eliciting high antigen-specific antibody concentrations confers no protection to young children in Western Kenya. PloS one 4, e4708 (2009). doi: 10.1371/journal.pone.0004708 19262754
28. Butler N. S., et al. Superior antimalarial immunity after vaccination with late liver stage-arresting genetically attenuated parasites. Cell host & microbe 9, 451–462 (2011).
29. Vaughan A. M., et al. Type II fatty acid synthesis is essential only for malaria parasite late liver stage development. Cellular microbiology 11, 506–520 (2009). doi: 10.1111/j.1462-5822.2008.01270.x 19068099
30. Kumazaki K., et al. AID-/-mus-/- mice are agammaglobulinemic and fail to maintain B220-CD138+ plasma cells. J Immunol 178, 2192–2203 (2007). 17277124
31. Wojciechowski W., et al. Cytokine-producing effector B cells regulate type 2 immunity to H. polygyrus. Immunity 30, 421–433 (2009).
32. Doll K. L., Butler N. S., Harty J. T., Tracking the total CD8 T cell response following whole Plasmodium vaccination. Methods Mol Biol 923, 493–504 (2013). 22990800
33. Szalai A. J., Briles D. E., Volanakis J. E., Role of complement in C-reactive-protein-mediated protection of mice from Streptococcus pneumoniae. Infection and immunity 64, 4850–4853 (1996). 8890251
34. Nussenzweig R. S., Vanderberg J., Most H., Orton C., Protective immunity produced by the injection of x-irradiated sporozoites of plasmodium berghei. Nature 216, 160–162 (1967). 6057225
35. Aly A. S., et al. Targeted deletion of SAP1 abolishes the expression of infectivity factors necessary for successful malaria parasite liver infection. Molecular microbiology 69, 152–163 (2008). doi: 10.1111/j.1365-2958.2008.06271.x 18466298
36. Pinzon-Charry A., et al. Low doses of killed parasite in CpG elicit vigorous CD4+ T cell responses against blood-stage malaria in mice. The Journal of clinical investigation 120, 2967–2978 (2010). doi: 10.1172/JCI39222 20628205
37. Beeson J. G., Osier F. H., Engwerda C. R., Recent insights into humoral and cellular immune responses against malaria. Trends in parasitology 24, 578–584 (2008). doi: 10.1016/j.pt.2008.08.008 18848497
38. Imai T., et al. Involvement of CD8+ T cells in protective immunity against murine blood-stage infection with Plasmodium yoelii 17XL strain. European journal of immunology 40, 1053–1061 (2010).
39. Mogil R. J., Patton C. L., Green D. R., Cellular subsets involved in cell-mediated immunity to murine Plasmodium yoelii 17X malaria. J Immunol 138, 1933–1939 (1987).
40. Podoba J. E., Stevenson M. M., CD4+ and CD8+ T lymphocytes both contribute to acquired immunity to blood-stage Plasmodium chabaudi AS. Infection and immunity 59, 51–58 (1991). 1898902
41. Horne-Debets J. M., et al. PD-1 dependent exhaustion of CD8+ T cells drives chronic malaria. Cell reports 5, 1204–1213 (2013). doi: 10.1016/j.celrep.2013.11.002 24316071
42. Sabchareon A., et al. Parasitologic and clinical human response to immunoglobulin administration in falciparum malaria. The American journal of tropical medicine and hygiene 45, 297–308 (1991). 1928564
43. Cohen S., Mc G. I., Carrington S., Gamma-globulin and acquired immunity to human malaria. Nature 192, 733–737 (1961). 13880318
44. Marsh K., Otoo L., Hayes R. J., Carson D. C., Greenwood B. M., Antibodies to blood stage antigens of Plasmodium falciparum in rural Gambians and their relation to protection against infection. Transactions of the Royal Society of Tropical Medicine and Hygiene 83, 293–303 (1989). 2694458
45. Rotman H. L., Daly T. M., Clynes R., Long C. A., Fc receptors are not required for antibody-mediated protection against lethal malaria challenge in a mouse model. J Immunol 161, 1908–1912 (1998).
46. White W. I., Evans C. B., Taylor D. W., Antimalarial antibodies of the immunoglobulin G2a isotype modulate parasitemias in mice infected with Plasmodium yoelii. Infection and immunity 59, 3547–3554 (1991). 1894361
47. Pleass R. J., et al. Novel antimalarial antibodies highlight the importance of the antibody Fc region in mediating protection. Blood 102, 4424–4430 (2003). 12855589
48. Oeuvray C., et al. Cytophilic immunoglobulin responses to Plasmodium falciparum glutamate-rich protein are correlated with protection against clinical malaria in Dielmo, Senegal. Infection and immunity 68, 2617–2620 (2000). 10768952
49. Dodoo D., et al. Naturally acquired antibodies to the glutamate-rich protein are associated with protection against Plasmodium falciparum malaria. The Journal of infectious diseases 181, 1202–1205 (2000). 10720556
50. Courtin D., et al. The quantity and quality of African children's IgG responses to merozoite surface antigens reflect protection against Plasmodium falciparum malaria. PloS one 4, e7590 (2009). doi: 10.1371/journal.pone.0007590 19859562
51. Hirunpetcharat C., et al. CpG oligodeoxynucleotide enhances immunity against blood-stage malaria infection in mice parenterally immunized with a yeast-expressed 19 kDa carboxyl-terminal fragment of Plasmodium yoelii merozoite surface protein-1 (MSP1(19)) formulated in oil-based Montanides. Vaccine 21, 2923–2932 (2003).
52. Yoneto T., et al. A critical role of Fc receptor-mediated antibody-dependent phagocytosis in the host resistance to blood-stage Plasmodium berghei XAT infection. J Immunol 166, 6236–6241 (2001). 11342646
53. Taylor R. R., Allen S. J., Greenwood B. M., Riley E. M., IgG3 antibodies to Plasmodium falciparum merozoite surface protein 2 (MSP2): increasing prevalence with age and association with clinical immunity to malaria. The American journal of tropical medicine and hygiene 58, 406–413 (1998). 9574783
54. Taylor R. R., Smith D. B., Robinson V. J., McBride J. S., Riley E. M., Human antibody response to Plasmodium falciparum merozoite surface protein 2 is serogroup specific and predominantly of the immunoglobulin G3 subclass. Infection and immunity 63, 4382–4388 (1995). 7591074
55. Salmon D., Vilde J. L., Andrieu B., Simonovic R., Lebras J., Role of immune serum and complement in stimulation of the metabolic burst of human neutrophils by Plasmodium falciparum. Infection and immunity 51, 801–806 (1986). 3512435
56. Kumaratilake L. M., Ferrante A., Jaeger T., Morris-Jones S. D., The role of complement, antibody, and tumor necrosis factor alpha in the killing of Plasmodium falciparum by the monocytic cell line THP-1. Infection and immunity 65, 5342–5345 (1997). 9393837
57. Pang X. L., Horii T., Complement-mediated killing of Plasmodium falciparum erythrocytic schizont with antibodies to the recombinant serine repeat antigen (SERA). Vaccine 16, 1299–1305 (1998). 9682394
58. Atkinson J. P., Glew R. H., Neva F. A., Frank M. M., Serum complement and immunity in experimental simian malaria. II. Preferential activation of early components and failure of depletion of late components to inhibit protective immunity. The Journal of infectious diseases 131, 26–33 (1975).
59. Biryukov S., Stoute J. A., Complement activation in malaria: friend or foe? Trends in molecular medicine 20, 293–301 (2014). doi: 10.1016/j.molmed.2014.01.001 24508275
60. Osier F. H., et al. Opsonic phagocytosis of Plasmodium falciparum merozoites: mechanism in human immunity and a correlate of protection against malaria. BMC medicine 12, 108, doi: 10.1186/1741-7015-12-108 (2014). 24980799
61. Crispe I. N., Liver antigen-presenting cells. Journal of hepatology 54, 357–365 (2011). doi: 10.1016/j.jhep.2010.10.005 21084131
62. Ebrahimkhani M. R., Mohar I., Crispe I. N., Cross-presentation of antigen by diverse subsets of murine liver cells. Hepatology 54, 1379–1387 (2011). doi: 10.1002/hep.24508 21721032
63. Balam S., Romero J. F., Bongfen S. E., Guillaume P., Corradin G., CSP—a model for in vivo presentation of Plasmodium berghei sporozoite antigens by hepatocytes. PloS one 7, e51875 (2012). doi: 10.1371/journal.pone.0051875 23272182
64. van Dijk M. R., et al. Genetically attenuated, P36p-deficient malarial sporozoites induce protective immunity and apoptosis of infected liver cells. Proceedings of the National Academy of Sciences of the United States of America 102, 12194–12199 (2005). 16103357
65. Kaushansky A., et al. Malaria parasite liver stages render host hepatocytes susceptible to mitochondria-initiated apoptosis. Cell death & disease 4, e762 (2013).
66. Leiriao P., Mota M. M., Rodriguez A., Apoptotic Plasmodium-infected hepatocytes provide antigens to liver dendritic cells. The Journal of infectious diseases 191, 1576–1581 (2005). 15838783
67. Lau L. S., 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 pathogens 10, e1004135 (2014).
68. Jobe O., et al. Immunization with radiation-attenuated Plasmodium berghei sporozoites induces liver cCD8alpha+DC that activate CD8+T cells against liver-stage malaria. PloS one 4, e5075 (2009). doi: 10.1371/journal.pone.0005075 19347042
69. Plebanski M., et al. Direct processing and presentation of antigen from malaria sporozoites by professional antigen-presenting cells in the induction of CD8 T-cell responses. Immunology and cell biology 83, 307–312 (2005). 15877610
70. Lyon J. A., et al. Protection induced by Plasmodium falciparum MSP1(42) is strain-specific, antigen and adjuvant dependent, and correlates with antibody responses. PloS one 3, e2830 (2008). doi: 10.1371/journal.pone.0002830 18665258
71. Ling I. T., Ogun S. A., Holder A. A., Immunization against malaria with a recombinant protein. Parasite immunology 16, 63–67 (1994). 8015856
72. Blackman M. J., Scott-Finnigan T. J., Shai S., Holder A. A., Antibodies inhibit the protease-mediated processing of a malaria merozoite surface protein. The Journal of experimental medicine 180, 389–393 (1994). 7516416
73. Burns J. M., Jr.Majarian W. R., Young J. F., Daly T. M., Long C. A., A protective monoclonal antibody recognizes an epitope in the carboxyl-terminal cysteine-rich domain in the precursor of the major merozoite surface antigen of the rodent malarial parasite, Plasmodium yoelii. J Immunol 143, 2670–2676 (1989). 2477452
74. Ahlborg N., Ling I. T., Howard W., Holder A. A., Riley E. M., Protective immune responses to the 42-kilodalton (kDa) region of Plasmodium yoelii merozoite surface protein 1 are induced by the C-terminal 19-kDa region but not by the adjacent 33-kDa region. Infection and immunity 70, 820–825 (2002). 11796616
75. Yuen D., et al. Antigenicity and immunogenicity of the N-terminal 33-kDa processing fragment of the Plasmodium falciparum merozoite surface protein 1, MSP1: implications for vaccine development. Vaccine 25, 490–499 (2007).
76. Belnoue E., et al. Vaccination with live Plasmodium yoelii blood stage parasites under chloroquine cover induces cross-stage immunity against malaria liver stage. J Immunol 181, 8552–8558 (2008). 19050274
77. Pombo D. J., et al. Immunity to malaria after administration of ultra-low doses of red cells infected with Plasmodium falciparum. The Lancet 360, 610–617 (2002). 12241933
78. Belnoue E., et al. Protective T cell immunity against malaria liver stage after vaccination with live sporozoites under chloroquine treatment. J Immunol 172, 2487–2495 (2004). 14764721
79. Seder, R. A. et al. Protection Against Malaria by Intravenous Immunization with a Nonreplicating Sporozoite Vaccine. Science (2013).
80. van Schaijk B. C., et al. Type II fatty acid biosynthesis is essential for Plasmodium falciparum sporozoite development in the midgut of Anopheles mosquitoes. Eukaryotic cell 13, 550–559 (2014). doi: 10.1128/EC.00264-13 24297444
81. Lindner S. E., et al. Enzymes involved in plastid-targeted phosphatidic acid synthesis are essential for Plasmodium yoelii liver-stage development. Molecular microbiology 91, 679–693 (2014). doi: 10.1111/mmi.12485 24330260
82. Tonkin C. J., et al. Localization of organellar proteins in Plasmodium falciparum using a novel set of transfection vectors and a new immunofluorescence fixation method. Molecular and biochemical parasitology 137, 13–21 (2004). 15279947