Development of whole sporozoite malaria vaccines

Expert Review of Vaccines

Volumn 16, Issue 1, 2017, Pages 45-54

  Hollingdale, Michael R ^a   Sedegah, Martha ^a  

^a NAVAL MEDICAL RESEARCH CENTER   (United States)

Author keywords

antibodies; CD8+ T cells; Malaria; protection; sporozoites; vaccine

Indexed keywords

CHLOROQUINE; MALARIA VACCINE; SPOROZOITE VACCINE; LIVE VACCINE;

CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CRYOPRESERVATION; DRUG EFFICACY; HUMAN; MALARIA FALCIPARUM; MOSQUITO; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; REVIEW; SPOROZOITE; VACCINATION; CLINICAL TRIAL (TOPIC); IMMUNOLOGY; MALARIA, FALCIPARUM; TREATMENT OUTCOME;

CLINICAL TRIALS AS TOPIC; HUMANS; MALARIA VACCINES; MALARIA, FALCIPARUM; PLASMODIUM FALCIPARUM; SPOROZOITES; TREATMENT OUTCOME; VACCINES, ATTENUATED;

EID: 85003671350     PISSN: 14760584     EISSN: 17448395     Source Type: Journal    
DOI: 10.1080/14760584.2016.1203784     Document Type: Review

References (99)

1. Choumet V, Attout T, Chartier L, et al. Visualizing non infectious and infectious Anopheles gambiae blood feedings in naive and saliva-immunized mice. PLoS One. 2012;7:e50464.• Visualization of sporozoites deposited by mosquito bite within the skin and influence of mosquito saliva.
2. Vanderberg JP., Imaging mosquito transmission of Plasmodium sporozoites into the mammalian host:immunological implications. Parasitol Int. 2014;63:150–164.•• Visualization of sporozoites deposited by mosquito bite within the skin.
3. Radtke AJ, Tse SW, Zavala F. From the draining lymph node to the liver:the induction and effector mechanisms of malaria-specific CD8+ T cells. Semin Immunopathol. 2015;37:211–220.
4. Radtke AJ, Kastenmuller W, Espinosa DA, et al. Lymph-node resident CD8alpha+ dendritic cells capture antigens from migratory malaria sporozoites and induce CD8+ T cell responses. PLoS Pathog. 2015;11:e1004637.
5. WHO. World Malaria Report 2015. 2015. http://www.who.int/malaria/publications/world-malaria-report-2015/report/en/.
6. PMI. Nineth Annual Report to Congress. 2015. http://www.fightingmalaria.gov/resources/reports/pmi_annual_report11.pdf.
7. Ariey F, Witkowski B, Amaratunga C, et al. A molecular marker of artemisinin-resistant Plasmodium falciparum malaria. Nature. 2014;505:50–55.
8. Takala-Harrison S, Jacob CG, Arze C, et al. Independent emergence of artemisinin resistance mutations among Plasmodium falciparum in Southeast Asia. J Infect Dis. 2015;211:670–679.
9. St Laurent B, Miller B, Burton TA, et al. Artemisinin-resistant Plasmodium falciparum clinical isolates can infect diverse mosquito vectors of Southeast Asia and Africa. Nat Commun. 2015;6:8614.
10. Moorthy VS, Newman RD, Okwo-Bele JM. Malaria vaccine technology roadmap. Lancet. 2013;382:1700–1701.• Definition of malaria vaccine efficacy targets and plans for their achievement.
11. Teneza-Mora N, Lumsden J, Villasante E. A malaria vaccine for travelers and military personnel:requirements and top candidates. Vaccine. 2015;33:7551–7558.
12. Nussenzweig RS, Vanderberg J, Most H, et al. Protective immunity produced by the injection of x-irradiated sporozoites of plasmodium berghei. Nature. 1967;216:160–162.•• Foundation of using irradiation-attenuated sporozoites to elicit complete protection.
13. Gwadz RW, Cochrane AH, Nussenzweig V, et al. Preliminary studies on vaccination of rhesus monkeys with irradiated sporozoites of Plasmodium knowlesi and characterization of surface antigens of these parasites. Bull World Health Organ. 1979;57(Suppl 1):165–173.
14. Sigler CI, Leland P, Hollingdale MR. In vitro infectivity of irradiated Plasmodium berghei sporozoites to cultured hepatoma cells. Am J Trop Med Hyg. 1984;33:544–547.
15. Nussenzweig V, Nussenzweig RS. Circumsporozoite proteins of malaria parasites. Cell. 1985;42:401–403.
16. Orjih AU, Nussenzweig RS. Immunization against rodent malaria with cryopreserved irradiated sporozoites of Plasmodium berghei. Am J Trop Med Hyg. 1980;29:343–347.
17. Beaudoin RL, Strome CP, Mitchell F, et al. Plasmodium berghei:immunization of mice against the ANKA strain using the unaltered sporozoite as an antigen. Exp Parasitol. 1977;42:1–5.
18. Clyde DF, McCarthy VC, Miller RM, et al. Specificity of protection of man immunized against sporozoite-induced falciparum malaria. Am J Med Sci. 1973;266:398–403.•• First human clinical trial of using irradiation-attenuated sporozoites.
19. Clyde DF, Most H, McCarthy VC, et al. Immunization of man against sporozite-induced falciparum malaria. Am J Med Sci. 1973;266:169–177.
20. Clyde DF. Immunization of man against falciparum and vivax malaria by use of attenuated sporozoites. Am J Trop Med Hyg. 1975;24:397–401.
21. Rieckmann KH, Beaudoin RL, Cassells JS, et al. Use of attenuated sporozoites in the immunization of human volunteers against falciparum malaria. Bull World Health Organ. 1979;57(Suppl 1):261–265.
22. Hoffman SL, Goh LM, Luke TC, et al. Protection of humans against malaria by immunization with radiation-attenuated Plasmodium falciparum sporozoites. J Infect Dis. 2002;185:1155–1164.•• Important review of P. falciparum RAS clinical trials between 1989 and 1999.
23. Richie TL, Billingsley PF, Sim BK, et al. Progress with Plasmodium falciparum sporozoite (PfSPZ)-based malaria vaccines. Vaccine. 2015;33:7452–7461.• Comprehensive review of whole sporozoite vaccine evaluation in domestic and field trials.
24. Nussenzweig RS, Montuori W, Spitalny GL, et al. Antibodies against sporozoites of human and simian malaria produced in rats. J Immunol. 1973;110:600–601.
25. Potocnjak P, Yoshida N, Nussenzweig RS, et al. Monovalent fragments (Fab) of monoclonal antibodies to a sporozoite surface antigen (Pb44) protect mice against malarial infection. J Exp Med. 1980;151:1504–1513.
26. Fernandez-Arias C, Mashoof S, Huang J, et al. Circumsporozoite protein as a potential target for antimalarials. Expert Rev Anti Infect Ther. 2015;13:923–926.
27. Zavala F, Tam JP, Hollingdale MR, et al. Rationale for development of a synthetic vaccine against Plasmodium falciparum malaria. Science. 1985;228:1436–1440.
28. Ballou WR, Hoffman SL, Sherwood JA, et al. Safety and efficacy of a recombinant DNA Plasmodium falciparum sporozoite vaccine. Lancet. 1987;1:1277–1281.
29. Herrington DA, Clyde DF, Losonsky G, et al. Safety and immunogenicity in man of a synthetic peptide malaria vaccine against Plasmodium falciparum sporozoites. Nature. 1987;328:257–259.
30. Cohen J, Nussenzweig V, Nussenzweig R, et al. From the circumsporozoite protein to the RTS, S/AS candidate vaccine. Hum Vaccin. 2010;6:90–96.• Identification of CSP and vaccine development.
31. Casares S, Brumeanu TD, Richie TL. The RTS,S malaria vaccine. Vaccine. 2010;28:4880–4894.
32. Stoute JA, Slaoui M, Heppner DG, et al. A preliminary evaluation of a recombinant circumsporozoite protein vaccine against Plasmodium falciparum malaria. RTS,S malaria vaccine evaluation group. N Engl J Med. 1997;336:86–91.
33. Agnandji ST, Fernandes JF, Bache EB, et al. Clinical development of RTS,S/AS malaria vaccine:a systematic review of clinical Phase I-III trials. Future Microbiol. 2015;10:1553–1578.
34. Rts SCTP. Efficacy and safety of RTS,S/AS01 malaria vaccine with or without a booster dose in infants and children in Africa:final results of a phase 3, individually randomised, controlled trial. Lancet. 2015;386:31–45.
35. White MT, Bejon P, Olotu A, et al. A combined analysis of immunogenicity, antibody kinetics and vaccine efficacy from phase 2 trials of the RTS,S malaria vaccine. BMC Med. 2014;12:117.
36. White MT, Verity R, Churcher TS, et al. Vaccine approaches to malaria control and elimination:insights from mathematical models. Vaccine. 2015;33:7544–7550.
37. White MT, Verity R, Griffin JT, et al. Immunogenicity of the RTS,S/AS01 malaria vaccine and implications for duration of vaccine efficacy:secondary analysis of data from a phase 3 randomised controlled trial. Lancet Infect Dis. 2015;15:1450–1458.
38. Secretariat WPACa. Malaria Policy Advisory Committee to the WHO:conclusions and recommendations of seventh biannual meeting (March 2015). Malar J. 2015;14:295–301.
39. Dups JN, Pepper M, Cockburn IA. Antibody and B cell responses to Plasmodium sporozoites. Front Microbiol. 2014;5:625.
40. Weiss WR, Jiang CG. Protective CD8+ T lymphocytes in primates immunized with malaria sporozoites. PLoS One. 2012;7:e31247.
41. Tsuji M. A retrospective evaluation of the role of T cells in the development of malaria vaccine. Exp Parasitol. 2010;126:421–425.
42. Krzych U, Dalai S, Zarling S, et al. Memory CD8 T cells specific for plasmodia liver-stage antigens maintain protracted protection against malaria. Front Immunol. 2012;3:370.
43. Frevert U, Krzych U. Plasmodium cellular effector mechanisms and the hepatic microenvironment. Front Microbiol. 2015;6:482.• Discussion of protective immunity to liver stages and liver architecture and function.
44. Zarling S, Berenzon D, Dalai S, et al. 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.
45. Nganou-Makamdop K, Van Gemert GJ, Arens T, et al. Long term protection after immunization with P. berghei sporozoites correlates with sustained IFNgamma responses of hepatic CD8+ memory T cells. PLoS One. 2012;7:e36508.
46. Teirlinck AC, McCall MB, Roestenberg M, et al. Longevity and composition of cellular immune responses following experimental Plasmodium falciparum malaria infection in humans. PLoS Pathog. 2011;7:e1002389.
47. Morrot A, Rodrigues MM. Tissue signatures influence the activation of intrahepatic CD8(+) T cells against malaria sporozoites. Front Microbiol. 2014;5:440.
48. Zarling S, Krzych U. Characterization of liver CD8 T cell subsets that are associated with protection against pre-erythrocytic Plasmodium parasites. Methods Mol Biol. 2015;1325:39–48.
49. Tse SW, Cockburn IA, Zhang H, et al. Unique transcriptional profile of liver-resident memory CD8+ T cells induced by immunization with malaria sporozoites. Genes Immun. 2013;14:302–309.
50. Cockburn IA, Chen YC, Overstreet MG, et al. Prolonged antigen presentation is required for optimal CD8+ T cell responses against malaria liver stage parasites. PLoS Pathog. 2010;6:e1000877.
51. Bertolino P, Bowen DG. Malaria and the liver:immunological hide-and-seek or subversion of immunity from within? Front Microbiol. 2015;6:41.
52. Crompton PD, Moebius J, Portugal S, et al. Malaria immunity in man and mosquito:insights into unsolved mysteries of a deadly infectious disease. Annu Rev Immunol. 2014;32:157–187.• Comprehensive review of immunity to malaria.
53. Cockburn IA, Zavala F. Dendritic cell function and antigen presentation in malaria. Curr Opin Immunol. 2016;40:1–6.
54. Jobe O, Donofrio G, Sun G, et al. 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.
55. Huang J, Tsao T, Zhang M, et al. 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.
56. Cockburn IA, Amino R, Kelemen RK, et al. In vivo imaging of CD8+ T cell-mediated elimination of malaria liver stages. Proc Natl Acad Sci USA. 2013;110:9090–9095.
57. Nahrendorf W, Scholzen A, Sauerwein RW, et al. Cross-stage immunity for malaria vaccine development. Vaccine. 2015;33:7513–7517.
58. Chuang I, Sedegah M, Cicatelli S, et al. DNA prime/Adenovirus boost malaria vaccine encoding P. falciparum CSP and AMA1 induces sterile protection associated with cell-mediated immunity. PLoS One. 2013;8:e55571.
59. Cockburn IA, Tse SW, Zavala F. CD8+ T cells eliminate liver-stage Plasmodium berghei parasites without detectable bystander effect. Infect Immun. 2014;82:1460–1464.
60. Cabrera M, Pewe LL, Harty JT, et al. In vivo CD8+ T cell dynamics in the liver of Plasmodium yoelii immunized and infected mice. PLoS One. 2013;8:e70842.
61. Aguiar JC, Bolton J, Wanga J, et al. Discovery of novel Plasmodium falciparum pre-erythrocytic antigens for vaccine development. PLoS One. 2015;10:e0136109.
62. Epstein JE, Tewari K, Lyke KE, et al. Live attenuated malaria vaccine designed to protect through hepatic CD8+ T cell immunity. Science. 2011;334:475–480.
63. Seder RA, Chang LJ, Enama ME, et al. Protection against malaria by intravenous immunization with a nonreplicating sporozoite vaccine. Science. 2013;341:1359–1365.•• First demonstration of 100% efficacy induced by the PfSPZ vaccine.
64. Bastiaens GJ, Van Meer MP, Scholzen A, et al. Safety, immunogenicity, and protective efficacy of intradermal immunization with aseptic, purified, cryopreserved Plasmodium falciparum sporozoites in volunteers under chloroquine prophylaxis:a randomized controlled trial. Am J Trop Med Hyg. 2016;94:663–673.
65. Roestenberg M, Bijker EM, Sim BK, et al. Controlled human malaria infections by intradermal injection of cryopreserved Plasmodium falciparum sporozoites. Am J Trop Med Hyg. 2013;88:5–13.
66. Sheehy SH, Spencer AJ, Douglas AD, et al. Optimising controlled human malaria infection studies using cryopreserved parasites administered by needle and syringe. PLoS One. 2013;8:e65960.
67. Shekalaghe S, Rutaihwa M, Billingsley PF, et al. Controlled human malaria infection of Tanzanians by intradermal injection of aseptic, purified, cryopreserved Plasmodium falciparum sporozoites. Am J Trop Med Hyg. 2014;91:471–480.
68. Lyke KE, Laurens MB, Strauss K, et al. Optimizing intradermal administration of cryopreserved plasmodium falciparum sporozoites in controlled human malaria infection. Am J Trop Med Hyg. 2015;93:1274–1284.
69. Mordmuller B, Supan C, Sim KL, et al. Direct venous inoculation of Plasmodium falciparum sporozoites for controlled human malaria infection:a dose-finding trial in two centres. Malar J. 2015;14:117.
70. Gomez-Perez GP, Legarda A, Munoz J, et al. Controlled human malaria infection by intramuscular and direct venous inoculation of cryopreserved Plasmodium falciparum sporozoites in malaria-naive volunteers:effect of injection volume and dose on infectivity rates. Malar J. 2015;14:306.
71. Hodgson SH, Juma E, Salim A, et al. Evaluating controlled human malaria infection in Kenyan adults with varying degrees of prior exposure to Plasmodium falciparum using sporozoites administered by intramuscular injection. Front Microbiol. 2014;5:686.
72. Roestenberg M, McCall M, Hopman J, et al. Protection against a malaria challenge by sporozoite inoculation. N Engl J Med. 2009;361:468–477.• First demonstration of the CPS vaccine in humans.
73. Schats R, Bijker EM, van Gemert GJ, et al. Heterologous protection against malaria after immunization with Plasmodium falciparum Sporozoites. PLoS One. 2015;10:e0124243.
74. Roestenberg M, Teirlinck AC, McCall MB, et al. Long-term protection against malaria after experimental sporozoite inoculation:an open-label follow-up study. Lancet. 2011;377:1770–1776.
75. Bijker EM, Teirlinck AC, Schats R, et al. Cytotoxic markers associate with protection against malaria in human volunteers immunized with Plasmodium falciparum sporozoites. J Infect Dis. 2014;210:1605–1615.
76. Bijker EM, Bastiaens GJ, Teirlinck AC, et al. Protection against malaria after immunization by chloroquine prophylaxis and sporozoites is mediated by preerythrocytic immunity. Proc Natl Acad Sci USA. 2013;110:7862–7867.
77. Spring M, Murphy J, Nielsen R, et al. First-in-human evaluation of genetically attenuated Plasmodium falciparum sporozoites administered by bite of Anopheles mosquitoes to adult volunteers. Vaccine. 2013;31:4975–4983.• First clinical trial of the genetically attenuated GAP vaccine.
78. Butler NS, Vaughan AM, Harty JT, et al. Whole parasite vaccination approaches for prevention of malaria infection. Trends Immunol. 2012;33:247–254.
79. Epstein JE, Richie TL. The whole parasite, pre-erythrocytic stage approach to malaria vaccine development:a review. Curr Opin Infect Dis. 2013;26:420–428.
80. Spring M, Polhemus M, Ockenhouse C. Controlled human malaria infection. J Infect Dis. 2014;209(Suppl 2):S40–S45.
81. March S, Ng S, Velmurugan S, et al. A microscale human liver platform that supports the hepatic stages of Plasmodium falciparum and vivax. Cell Host Microbe. 2013;14:104–115.
82. Hoffman SL, Billingsley PF, James E, et al. Development of a metabolically active, non-replicating sporozoite vaccine to prevent Plasmodium falciparum malaria. Hum Vaccin. 2010;6:97–106.• Foundation of the manufacture of the PfSPZ vaccine.
83. Mo AX, Pesce J, Hall BF. Exploring immunological mechanisms of the whole sporozoite vaccination against P. falciparum malaria. Vaccine. 2015;33:2851–2857.
84. Bijker EM, Borrmann S, Kappe SH, et al. Novel approaches to whole sporozoite vaccination against malaria. Vaccine. 2015;33:7462–7468.
85. Murphy SC, Kas A, Stone BC, et al. A T-cell response to a liver-stage Plasmodium antigen is not boosted by repeated sporozoite immunizations. Proc Natl Acad Sci USA. 2013;110:6055–6060.
86. Bijker EM, Schats R, Obiero JM, et al. Sporozoite immunization of human volunteers under mefloquine prophylaxis is safe, immunogenic and protective:a double-blind randomized controlled clinical trial. PLoS One. 2014;9:e112910.
87. Friesen J, Silvie O, Putrianti ED, et al. Natural immunization against malaria:causal prophylaxis with antibiotics. Sci Transl Med. 2010;2:40ra49.
88. Pfeil J, Sepp KJ, Heiss K, et al. Protection against malaria by immunization with non-attenuated sporozoites under single-dose piperaquine-tetraphosphate chemoprophylaxis. Vaccine. 2014;32:6005–6011.
89. Doua JY, Matangila J, Lutumba P, et al. Intermittent preventive treatment:efficacy and safety of sulfadoxine-pyrimethamine and sulfadoxine-pyrimethamine plus piperaquine regimens in schoolchildren of the Democratic Republic of Congo:a study protocol for a randomized controlled trial. Trials. 2013;14:311.
90. Mueller AK, Camargo N, Kaiser K, et al. Plasmodium liver stage developmental arrest by depletion of a protein at the parasite-host interface. Proc Natl Acad Sci USA. 2005;102:3022–3027.• Foundation of genetically attenuated parasites in malaria vaccine development.
91. VanBuskirk KM, O’Neill MT, De La Vega P, et al. Preerythrocytic, live-attenuated Plasmodium falciparum vaccine candidates by design. Proc Natl Acad Sci USA. 2009;106:13004–13009.
92. Vaughan AM, Wang R, Kappe SH. Genetically engineered, attenuated whole-cell vaccine approaches for malaria. Hum Vaccin. 2010;6:107–113.• Importance of genetically attenuated parasites in malaria vaccine development.
93. Butler NS, Schmidt NW, Vaughan AM, et al. Superior antimalarial immunity after vaccination with late liver stage-arresting genetically attenuated parasites. Cell Host Microbe. 2011;9:451–462.
94. Douradinha B, van Dijk M, Van Gemert GJ, et al. Immunization with genetically attenuated P52-deficient Plasmodium berghei sporozoites induces a long-lasting effector memory CD8+ T cell response in the liver. J Immune Based Ther Vaccines. 2011;9:6.
95. Cooney LA, Gupta M, Thomas S, et al. Short-lived effector CD8 T cells induced by genetically attenuated malaria parasite vaccination express CD11c. Infect Immun. 2013;81:4171–4181.
96. Finney OC, Keitany GJ, Smithers H, et al. Immunization with genetically attenuated P. falciparum parasites induces long-lived antibodies that efficiently block hepatocyte invasion by sporozoites. Vaccine. 2014;32:2135–2138.
97. Mikolajczak SA, Lakshmanan V, Fishbaugher M, et al. A next-generation genetically attenuated Plasmodium falciparum parasite created by triple gene deletion. Mol Ther. 2014;22:1707–1715.
98. van Schaijk BC, Ploemen IH, Annoura T, et al. A genetically attenuated malaria vaccine candidate based on P. falciparum b9/slarp gene-deficient sporozoites. Elife. 2014;3. [Epub ahead of print].
99. Sack BK, Keitany GJ, Vaughan AM, et al. Mechanisms of stage-transcending protection following immunization of mice with late liver stage-arresting genetically attenuated malaria parasites. PLoS Pathog. 2015;11:e1004855.• Further development of the GAP vaccine.