Humoral protection against mosquito bite-transmitted Plasmodium falciparum infection in humanized mice (original) (raw)
References
Seder, R. A., Chang, L. J., Enama, M. E., Zephir, K. L., Sarwar, U. N. & Gordon, I. J. et al. Protection against malaria by intravenous immunization with a nonreplicating sporozoite vaccine. Science341, 1359–1365 (2013). ArticleCASPubMed Google Scholar
Ishizuka, A. S., Lyke, K. E., DeZure, A., Berry, A. A., Richie, T. L. & Mendoza, F. H. et al. Protection against malaria at 1 year and immune correlates following PfSPZ vaccination. Nat. Med.22, 614–623 (2016). ArticleCASPubMed Google Scholar
Kester, K. E., Cummings, J. F., Ofori-Anyinam, O., Ockenhouse, C. F., Krzych, U. & Moris, P. et al. Randomized, double-blind, phase 2a trial of falciparum malaria vaccines RTS,S/AS01B and RTS,S/AS02A in malaria-naive adults: safety, efficacy, and immunologic associates of protection. J. Infect. Dis.200, 337–346 (2009). ArticleCASPubMed Google Scholar
Olotu, A., Fegan, G., Wambua, J., Nyangweso, G., Awuondo, K. O. & Leach, A. et al. Four-year efficacy of RTS,S/AS01E and its interaction with malaria exposure. N. Eng. J. Med.368, 1111–1120 (2013). ArticleCAS Google Scholar
White, M. T., Bejon, P., Olotu, A., Griffin, J. T., Riley, E. M. & Kester, K. E. et al. The relationship between RTS,S vaccine-induced antibodies, CD4(+) T cell responses and protection against Plasmodium falciparum infection. PLoS One8, e61395 (2013). ArticleCASPubMedPubMed Central Google Scholar
Behet, M. C., Foquet, L., van Gemert, G. J., Bijker, E. M., Meuleman, P. & Leroux-Roels, G. et al. Sporozoite immunization of human volunteers under chemoprophylaxis induces functional antibodies against pre-erythrocytic stages of Plasmodium falciparum. Malar. J.13, 136 (2014). ArticlePubMedPubMed Central Google Scholar
Epstein, J. E., Paolino, K. M., Richie, T. L., Sedegah, M., Singer, A. & Ruben, A. J. et al. Protection against Plasmodium falciparum malaria by PfSPZ Vaccine. JCI Insight2, e89154 (2017). ArticlePubMedPubMed Central Google Scholar
Lyke, K. E., Ishizuka, A. S., Berry, A. A., Chakravarty, S., DeZure, A. & Enama, M. E. et al. Attenuated PfSPZ vaccine induces strain-transcending T cells and durable protection against heterologous controlled human malaria infection. Proc. Natl. Acad. Sci. USA114, 2711–2716 (2017). ArticleCASPubMedPubMed Central Google Scholar
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). ArticlePubMed Google Scholar
Kebaier, C., Voza, T. & Vanderberg, J. Kinetics of mosquito-injected Plasmodium sporozoites in mice: fewer sporozoites are injected into sporozoite-immunized mice. PLoS Pathog.5, e1000399 (2009). ArticlePubMedPubMed Central Google Scholar
Sinnis, P. & Zavala, F. The skin stage of malaria infection: biology and relevance to the malaria vaccine effort. Future Microbiol.3, 275–278 (2008). ArticlePubMed Google Scholar
Cha, S. J., Kim, M. S., Pandey, A. & Jacobs-Lorena, M. Identification of GAPDH on the surface of Plasmodium sporozoites as a new candidate for targeting malaria liver invasion. J. Exp. Med.213, 2099–2112 (2016). ArticleCASPubMedPubMed Central Google Scholar
Lindner, S. E., Swearingen, K. E., Harupa, A., Vaughan, A. M., Sinnis, P. & Moritz, R. L. et al. Total and putative surface proteomics of malaria parasite salivary gland sporozoites. Mol. Cell. Proteomics12, 1127–1143 (2013). ArticleCASPubMedPubMed Central Google Scholar
Swearingen, K. E., Lindner, S. E., Shi, L., Shears, M. J., Harupa, A. & Hopp, C. S. et al. Interrogating the Plasmodium sporozoite surface: identification of surface-exposed proteins and demonstration of glycosylation on CSP and TRAP by mass spectrometry-based proteomics. PLoS Pathog.12, e1005606 (2016). ArticlePubMedPubMed Central Google Scholar
Espinosa, D. A., Yadava, A., Angov, E., Maurizio, P. L., Ockenhouse, C. F. & Zavala, F. Development of a chimeric Plasmodium berghei strain expressing the repeat region of the P. vivax circumsporozoite protein for in vivo evaluation of vaccine efficacy. Infect. Immun.81, 2882–2887 (2013). ArticleCASPubMedPubMed Central Google Scholar
Bauza, K., Malinauskas, T., Pfander, C., Anar, B., Jones, E. Y. & Billker, O. et al. Efficacy of a Plasmodium vivax malaria vaccine using ChAd63 and modified vaccinia Ankara expressing thrombospondin-related anonymous protein as assessed with transgenic Plasmodium berghei parasites. Infect. Immun.82, 1277–1286 (2014). ArticlePubMedPubMed Central Google Scholar
Persson, C., Oliveira, G. A., Sultan, A. A., Bhanot, P., Nussenzweig, V. & Nardin, E. Cutting edge: a new tool to evaluate human pre-erythrocytic malaria vaccines: rodent parasites bearing a hybrid Plasmodium falciparum circumsporozoite protein. J. Immunol.169, 6681–6685 (2002). ArticleCASPubMed Google Scholar
Sauerwein, R. W., Roestenberg, M. & Moorthy, V. S. Experimental human challenge infections can accelerate clinical malaria vaccine development. Nat. Rev. Immunol.11, 57–64 (2011). ArticleCASPubMed Google Scholar
Cummings, J. F., Spring, M. D., Schwenk, R. J., Ockenhouse, C. F., Kester, K. E. & Polhemus, M. E. et al. Recombinant Liver Stage Antigen-1 (LSA-1) formulated with AS01 or AS02 is safe, elicits high titer antibody and induces IFN-gamma/IL-2 CD4+ T cells but does not protect against experimental Plasmodium falciparum infection. Vaccine28, 5135–5144 (2010). ArticleCASPubMed Google Scholar
Kester, K. E., Gray Heppner, D. Jr., Moris, P., Ofori-Anyinam, O., Krzych, U. & Tornieporth, N. et al. Sequential Phase 1 and Phase 2 randomized, controlled trials of the safety, immunogenicity and efficacy of combined pre-erythrocytic vaccine antigens RTS,S and TRAP formulated with AS02 Adjuvant System in healthy, malaria naive adults. Vaccine32, 6683–6691 (2014). ArticleCASPubMed Google Scholar
McConkey, S. J., Reece, W. H., Moorthy, V. S., Webster, D., Dunachie, S. & Butcher, G. et al. Enhanced T-cell immunogenicity of plasmid DNA vaccines boosted by recombinant modified vaccinia virus Ankara in humans. Nat. Med.9, 729–735 (2003). ArticleCASPubMed Google Scholar
Ockenhouse, C. F., Sun, P. F., Lanar, D. E., Wellde, B. T., Hall, B. T. & Kester, K. et al. Phase I/IIa safety, immunogenicity, and efficacy trial of NYVAC-Pf7, a pox-vectored, multiantigen, multistage vaccine candidate for Plasmodium falciparum malaria. J. Infect. Dis.177, 1664–1673 (1998). ArticleCASPubMed Google Scholar
Porter, D. W., Thompson, F. M., Berthoud, T. K., Hutchings, C. L., Andrews, L. & Biswas, S. et al. A human Phase I/IIa malaria challenge trial of a polyprotein malaria vaccine. Vaccine29, 7514–7522 (2011). ArticleCASPubMedPubMed Central Google Scholar
Richie, T. L., Charoenvit, Y., Wang, R., Epstein, J. E., Hedstrom, R. C. & Kumar, S. et al. Clinical trial in healthy malaria-naive adults to evaluate the safety, tolerability, immunogenicity and efficacy of MuStDO5, a five-gene, sporozoite/hepatic stage Plasmodium falciparum DNA vaccine combined with escalating dose human GM-CSF DNA. Hum. Vaccin. Immunother.8, 1564–1584 (2012). ArticleCASPubMedPubMed Central Google Scholar
Steel, R. W., Kappe, S. H. & Sack, B. K. An expanding toolkit for preclinical pre-erythrocytic malaria vaccine development: bridging traditional mouse malaria models and human trials. Future Microbiol.11, 1563–1579 (2016). ArticleCASPubMed Google Scholar
Amino, R., Giovannini, D., Thiberge, S., Gueirard, P., Boisson, B. & Dubremetz, J. F. et al. Host cell traversal is important for progression of the malaria parasite through the dermis to the liver. Cell Host Microbe3, 88–96 (2008). ArticleCASPubMed Google Scholar
Tavares, J., Formaglio, P., Thiberge, S., Mordelet, E., Van Rooijen, N. & Medvinsky, A. et al. Role of host cell traversal by the malaria sporozoite during liver infection. J. Exp. Med.210, 905–915 (2013). ArticleCASPubMedPubMed Central Google Scholar
Vaughan, A. M., Mikolajczak, S. A., Wilson, E. M., Grompe, M., Kaushansky, A. & Camargo, N. et al. Complete Plasmodium falciparum liver-stage development in liver-chimeric mice. J. Clin. Invest.122, 3618–3628 (2012). ArticleCASPubMedPubMed Central Google Scholar
Mikolajczak, S. A., Vaughan, A. M., Kangwanrangsan, N., Roobsoong, W., Fishbaugher, M. & Yimamnuaychok, N. et al. Plasmodium vivax liver stage development and hypnozoite persistence in human liver-chimeric mice. Cell Host Microbe17, 526–535 (2015). ArticleCASPubMedPubMed Central Google Scholar
Foquet, L., Hermsen, C. C., van Gemert, G. J., Van Braeckel, E., Weening, K. E. & Sauerwein, R. et al. Vaccine-induced monoclonal antibodies targeting circumsporozoite protein prevent Plasmodium falciparum infection. J. Clin. Invest.124, 140–144 (2014). ArticleCASPubMed Google Scholar
Foquet, L., Meuleman, P., Hermsen, C. C., Sauerwein, R. & Leroux-Roels, G. Assessment of parasite liver-stage burden in human-liver chimeric mice. Methods Mol. Biol.1325, 59–68 (2015). ArticleCASPubMed Google Scholar
Sack, B. K., Miller, J. L., Vaughan, A. M., Douglass, A., Kaushansky, A. & Mikolajczak, S. et al. Model for in vivo assessment of humoral protection against malaria sporozoite challenge by passive transfer of monoclonal antibodies and immune serum. Infect. Immun.82, 808–817 (2014). ArticlePubMedPubMed Central Google Scholar
Kublin, J. G., Mikolajczak, S. A., Sack, B. K., Fishbaugher, M. E., Seilie, A. & Shelton, L., et al. Complete attenuation of genetically engineered Plasmodium falciparum sporozoites in human subjects. Sci. Transl. Med.9, 371 (2017).
Keitany, G. J., Sack, B., Smithers, H., Chen, L., Jang, I. K. & Sebastian, L. et al. Immunization of mice with live-attenuated late liver stage-arresting Plasmodium yoelii parasites generates protective antibody responses to preerythrocytic stages of malaria. Infect. Immun.82, 5143–5153 (2014). ArticlePubMedPubMed Central Google Scholar
Vaughan, A. M., Mikolajczak, S. A., Camargo, N., Lakshmanan, V., Kennedy, M. & Lindner, S. E. et al. A transgenic Plasmodium falciparum NF54 strain that expresses GFP-luciferase throughout the parasite life cycle. Mol. Biochem. Parasitol.186, 143–147 (2012). ArticleCASPubMed Google Scholar
Kipps, T. J., Parham, P., Punt, J. & Herzenberg, L. A. Importance of immunoglobulin isotype in human antibody-dependent, cell-mediated cytotoxicity directed by murine monoclonal antibodies. J. Exp. Med.161, 1–17 (1985). ArticleCASPubMed Google Scholar
Overdijk, M. B., Verploegen, S., Ortiz Buijsse, A., Vink, T., Leusen, J. H. & Bleeker, W. K. et al. Crosstalk between human IgG isotypes and murine effector cells. J. Immunol.189, 3430–3438 (2012). ArticleCASPubMed Google Scholar
Gonzalez-Quintela, A., Alende, R., Gude, F., Campos, J., Rey, J. & Meijide, L. M. et al. Serum levels of immunoglobulins (IgG, IgA, IgM) in a general adult population and their relationship with alcohol consumption, smoking and common metabolic abnormalities. Clin. Exp. Immunol.151, 42–50 (2008). ArticleCASPubMedPubMed Central Google Scholar
Roestenberg, M., McCall, M., Hopman, J., Wiersma, J., Luty, A. J. & van Gemert, G. J. et al. Protection against a malaria challenge by sporozoite inoculation. N. Eng. J. Med.361, 468–477 (2009). ArticleCAS Google Scholar
Roestenberg, M., Teirlinck, A. C., McCall, M. B., Teelen, K., Makamdop, K. N. & Wiersma, J. et al. Long-term protection against malaria after experimental sporozoite inoculation: an open-label follow-up study. Lancet377, 1770–1776 (2011). ArticleCASPubMed Google Scholar
Hodgson, S. H., Douglas, A. D., Edwards, N. J., Kimani, D., Elias, S. C. & Chang, M. et al. Increased sample volume and use of quantitative reverse-transcription PCR can improve prediction of liver-to-blood inoculum size in controlled human malaria infection studies. Malar. J.14, 33 (2015). ArticlePubMedPubMed Central Google Scholar
Murphy, S. C., Prentice, J. L., Williamson, K., Wallis, C. K., Fang, F. C. & Fried, M. et al. Real-time quantitative reverse transcription PCR for monitoring of blood-stage Plasmodium falciparum infections in malaria human challenge trials. Am. J. Trop. Med. Hyg.86, 383–394 (2012). ArticleCASPubMedPubMed Central Google Scholar
Potocnjak, P., Yoshida, N., Nussenzweig, R. S. & Nussenzweig, V. Monovalent fragments (Fab) of monoclonal antibodies to a sporozoite surface antigen (Pb44) protect mice against malarial infection. J. Exp. Med.151, 1504–1513 (1980). ArticleCASPubMed Google Scholar
Charoenvit, Y., Sedegah, M., Yuan, L. F., Gross, M., Cole, C. & Bechara, R. et al. Active and passive immunization against Plasmodium yoelii sporozoites. Bull. World Health Organ.68, Suppl:26–Suppl:32 (1990). Google Scholar
Charoenvit, Y., Mellouk, S., Cole, C., Bechara, R., Leef, M. F. & Sedegah, M. et al. Monoclonal, but not polyclonal, antibodies protect against Plasmodium yoelii sporozoites. J. Immunol.146, 1020–1025 (1991). CASPubMed Google Scholar
Vanderberg, J., Mueller, A. K., Heiss, K., Goetz, K., Matuschewski, K. & Deckert, M. et al. Assessment of antibody protection against malaria sporozoites must be done by mosquito injection of sporozoites. Am. J. Pathol.171, 1405–1406 (2007). author reply 6. ArticlePubMed Google Scholar
Bijker, E. M., Bastiaens, G. J., Teirlinck, A. C., van Gemert, G. J., Graumans, W. & van de Vegte-Bolmer, M. et al. Protection against malaria after immunization by chloroquine prophylaxis and sporozoites is mediated by preerythrocytic immunity. Proc Natl Acad Sci USA110, 7862–7867 (2013). ArticleCASPubMedPubMed Central Google Scholar
Bijker, E. M., Teirlinck, A. C., Schats, R., van Gemert, G. J., van de Vegte-Bolmer, M. & van Lieshout, L. et al. Cytotoxic markers associate with protection against malaria in human volunteers immunized with Plasmodium falciparum sporozoites. J. Infect. Dis.210, 1605–1615 (2014). ArticlePubMedPubMed Central Google Scholar
Epstein, J. E., Tewari, K., Lyke, K. E., Sim, B. K., Billingsley, P. F. & Laurens, M. B. et al. Live attenuated malaria vaccine designed to protect through hepatic CD8(+) T cell immunity. Science334, 475–480 (2011). ArticleCASPubMed Google Scholar
Doll, K. L. & Harty, J. T. Correlates of protective immunity following whole sporozoite vaccination against malaria. Immunol. Res.59, 166–176 (2014). ArticleCASPubMedPubMed Central Google Scholar
Sheehy, S. H., Duncan, C. J., Elias, S. C., Choudhary, P., Biswas, S. & Halstead, F. D. et al. ChAd63-MVA-vectored blood-stage malaria vaccines targeting MSP1 and AMA1: assessment of efficacy against mosquito bite challenge in humans. Mol. Ther.20, 2355–2368 (2012). ArticleCASPubMedPubMed Central Google Scholar
Hill, A. V., Reyes-Sandoval, A., O’Hara, G., Ewer, K., Lawrie, A. & Goodman, A. et al. Prime-boost vectored malaria vaccines: progress and prospects. Hum. Vaccin.6, 78–83 (2010). ArticleCASPubMed Google Scholar
Hodgson, S. H., Ewer, K. J., Bliss, C. M., Edwards, N. J., Rampling, T. & Anagnostou, N. A. et al. 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). ArticleCASPubMed Google Scholar
Bruna-Romero, O., Hafalla, J. C., Gonzalez-Aseguinolaza, G., Sano, G., Tsuji, M. & Zavala, F. Detection of malaria liver-stages in mice infected through the bite of a single Anopheles mosquito using a highly sensitive real-time PCR. Int. J. Parasitol.31, 1499–1502 (2001). ArticleCASPubMed Google Scholar
Ak, M., Bower, J. H., Hoffman, S. L., Sedegah, M., Lees, A. & Carter, M. et al. Monoclonal antibodies of three different immunoglobulin G isotypes produced by immunization with a synthetic peptide or native protein protect mice against challenge with Plasmodium yoelii sporozoites. Infect. Immun.61, 2493–2497 (1993). CASPubMedPubMed Central Google Scholar
Yilmaz, B., Portugal, S., Tran, T. M., Gozzelino, R., Ramos, S. & Gomes, J. et al. Gut microbiota elicits a protective immune response against malaria transmission. Cell.159, 1277–1289 (2014). ArticleCASPubMedPubMed Central Google Scholar
Felgner, P. L., Roestenberg, M., Liang, L., Hung, C., Jain, A. & Pablo, J. et al. Pre-erythrocytic antibody profiles induced by controlled human malaria infections in healthy volunteers under chloroquine prophylaxis. Sci. Rep.3, 3549 (2013). ArticlePubMedPubMed Central Google Scholar
Weiss, W. R., Sedegah, M., Beaudoin, R. L., Miller, L. H. & Good, M. F. CD8+ T cells (cytotoxic/suppressors) are required for protection in mice immunized with malaria sporozoites. Proc. Natl. Acad. Sci. USA85, 573–576 (1988). ArticleCASPubMedPubMed Central Google Scholar
Rodrigues, M., Nussenzweig, R. S. & Zavala, F. The relative contribution of antibodies, CD4+ and CD8+ T cells to sporozoite-induced protection against malaria. Immunology80, 1–5 (1993). CASPubMedPubMed Central Google Scholar
Celada, A., Cruchaud, A. & Perrin, L. H. Opsonic activity of human immune serum on in vitro phagocytosis of Plasmodium falciparum infected red blood cells by monocytes. Clin. Exp. Immunol.47, 635–644 (1982). CASPubMedPubMed Central Google Scholar
Mazurier, F., Fontanellas, A., Salesse, S., Taine, L., Landriau, S. & Moreau-Gaudry, F. et al. A novel immunodeficient mouse model—RAG2 x common cytokine receptor gamma chain double mutants--requiring exogenous cytokine administration for human hematopoietic stem cell engraftment. J. Interferon Cytokine Res.19, 533–541 (1999). ArticleCASPubMed Google Scholar
Miller, J. L., Murray, S., Vaughan, A. M., Harupa, A., Sack, B. & Baldwin, M. et al. Quantitative bioluminescent imaging of pre-erythrocytic malaria parasite infection using luciferase-expressing Plasmodium yoelii. PLoS One8, e60820 (2013). ArticleCASPubMedPubMed Central Google Scholar
Foquet, L., Hermsen, C. C., van Gemert, G. J., Van Braeckel, E., Weening, K. E. & Sauerwein, R., et al. Vaccine-induced monoclonal antibodies targetingcircumsporozoite protein prevent Plasmodium falciparum infection. J. Clin. Invest.124, 140–144 (2013)
Murphy, S. C., Daza, G., Chang, M. & Coombs, R. Laser cutting eliminates nucleic acid cross-contamination in dried-blood-spot processing. J. Clin. Microbiol.50, 4128–4130 (2012). ArticlePubMedPubMed Central Google Scholar
Billman, Z. P., Seilie, A. M. & Murphy, S. C. Purification of Plasmodium sporozoites enhances parasite-specific CD8+ T cell responses. Infect. Immun.84, 2233–2242 (2016). ArticleCASPubMedPubMed Central Google Scholar
Kaushansky, A., Rezakhani, N., Mann, H. & Kappe, S. H. Development of a quantitative flow cytometry-based assay to assess infection by Plasmodium falciparum sporozoites. Mol. Biochem. Parasitol.183, 100–103 (2012). ArticleCASPubMedPubMed Central Google Scholar
Douglass, A. N., Metzger, P. G., Kappe, S. H. & Kaushansky, A. Flow cytometry-based assessment of antibody function against malaria pre-erythrocytic infection. Methods Mol. Biol.1325, 49–58 (2015). ArticleCASPubMed Google Scholar