Needle-free, spirulina-produced Plasmodium falciparum circumsporozoite vaccination provides sterile protection against pre-erythrocytic malaria in mice.
Journal
NPJ vaccines
ISSN: 2059-0105
Titre abrégé: NPJ Vaccines
Pays: England
ID NLM: 101699863
Informations de publication
Date de publication:
04 Oct 2022
04 Oct 2022
Historique:
received:
25
02
2022
accepted:
05
09
2022
entrez:
4
10
2022
pubmed:
5
10
2022
medline:
5
10
2022
Statut:
epublish
Résumé
Antibodies against the Plasmodium falciparum circumsporozoite protein (PfCSP) can block hepatocyte infection by sporozoites and protect against malaria. Needle-free vaccination strategies are desirable, yet most PfCSP-targeted vaccines like RTS,S require needle-based administration. Here, we evaluated the edible algae, Arthrospira platensis (commonly called 'spirulina') as a malaria vaccine platform. Spirulina were genetically engineered to express virus-like particles (VLPs) consisting of the woodchuck hepatitis B core capsid protein (WHcAg) displaying a (NANP)
Identifiants
pubmed: 36195607
doi: 10.1038/s41541-022-00534-5
pii: 10.1038/s41541-022-00534-5
pmc: PMC9532447
doi:
Types de publication
Journal Article
Langues
eng
Pagination
113Subventions
Organisme : NIAID NIH HHS
ID : R41 AI138623
Pays : United States
Organisme : NIAID NIH HHS
ID : R42 AI138623
Pays : United States
Informations de copyright
© 2022. The Author(s).
Références
World Health Organization. 2021. World Malaria Report. (World Health Organization, Geneva, 2021).
Rogerson, S. J. et al. Identifying and combating the impacts of COVID-19 on malaria. BMC Med. 18, 239 (2020).
pubmed: 32727467
pmcid: 7391033
doi: 10.1186/s12916-020-01710-x
Weiss, D. J. et al. Indirect effects of the COVID-19 pandemic on malaria intervention coverage, morbidity, and mortality in Africa: a geospatial modelling analysis. Lancet Infect. Dis. 21, 59–69 (2021).
pubmed: 32971006
pmcid: 7505634
doi: 10.1016/S1473-3099(20)30700-3
Sherrard-Smith, E. et al. The potential public health consequences of COVID-19 on malaria in Africa. Nat. Med. 26, 1411–1416 (2020).
pubmed: 32770167
pmcid: 7613562
doi: 10.1038/s41591-020-1025-y
Keitany, G. J. 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).
pubmed: 25267837
pmcid: 4249261
doi: 10.1128/IAI.02320-14
RTS, S Clinical Trials Partnership. 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 386, 31–45 (2015).
doi: 10.1016/S0140-6736(15)60721-8
Datoo, M. S. et al. Efficacy of a low-dose candidate malaria vaccine, R21 in adjuvant Matrix-M, with seasonal administration to children in Burkina Faso: a randomised controlled trial. Lancet 397, 1809–1818 (2021).
pubmed: 33964223
pmcid: 8121760
doi: 10.1016/S0140-6736(21)00943-0
Ainai, A., Suzuki, T., Tamura, S. I. & Hasegawa, H. Intranasal administration of whole inactivated influenza virus vaccine as a promising influenza vaccine candidate. Viral Immunol. 30, 451–462 (2017).
pubmed: 28650274
doi: 10.1089/vim.2017.0022
Hassan, A. O. et al. A single-dose intranasal ChAd vaccine protects upper and lower respiratory tracts against SARS-CoV-2. Cell 183, 169-184.e13 (2020).
pubmed: 32931734
pmcid: 7437481
doi: 10.1016/j.cell.2020.08.026
Marasini, N. & Kaminskas, L. M. Subunit-based mucosal vaccine delivery systems for pulmonary delivery - Are they feasible? Drug Dev. Ind. Pharm. 45, 882–894 (2019).
pubmed: 30767591
doi: 10.1080/03639045.2019.1583758
Ciferri, O. Spirulina, the edible microorganism. Microbiol. Rev. 47, 551–578 (1983).
pubmed: 6420655
pmcid: 283708
doi: 10.1128/mr.47.4.551-578.1983
Food and Drug Administration, H. Vol. 78 FR 68713 (ed Food and Drug Administration) 68713-68714 (Food and Drug Administration, Washington, DC, 2013).
Masuda, K. & Chitundu, M. Multiple micronutrient supplementation using Spirulina platensis during the first 1000 days is positively associated with development in children under five years: a follow up of a randomized trial in Zambia. Nutrients 11, 730 (2019).
Masuda, K. & Chitundu, M. Multiple micronutrient supplementation using Spirulina platensis and infant growth, morbidity, and motor development: Evidence from a randomized trial in Zambia. PLoS ONE 14, e0211693 (2019).
pubmed: 30759117
pmcid: 6373937
doi: 10.1371/journal.pone.0211693
Jensen, G. S., Drapeau, C., Lenninger, M. & Benson, K. F. Clinical safety of a high dose of phycocyanin-enriched aqueous extract from Arthrospira (Spirulina) platensis: results from a randomized, double-blind, placebo-controlled study with a focus on anticoagulant activity and platelet activation. J. Med. Food 19, 645–653 (2016).
pubmed: 27362442
pmcid: 4948198
doi: 10.1089/jmf.2015.0143
Jester, B. et al. Development of spirulina for the manufacture and oral delivery of protein therapeutics. Nat. Biotechnol. 40, 956–964 (2022).
pubmed: 35314813
pmcid: 9200632
doi: 10.1038/s41587-022-01249-7
Whitacre, D. C. et al. P. falciparum and P. vivax epitope-focused VLPs elicit sterile immunity to blood stage infections. PLoS ONE 10, e0124856 (2015).
pubmed: 25933001
pmcid: 4416889
doi: 10.1371/journal.pone.0124856
Milich, D. R. et al. The hepatitis nucleocapsid as a vaccine carrier moiety. Ann. N. Y. Acad. Sci. 754, 187–201 (1995).
pubmed: 7542855
doi: 10.1111/j.1749-6632.1995.tb44451.x
Pumpens, P., Borisova, G. P., Crowther, R. A. & Grens, E. Hepatitis B virus core particles as epitope carriers. Intervirology 38, 63–74 (1995).
pubmed: 8666525
doi: 10.1159/000150415
McGonigle, R. et al. An N-terminal extension to the hepatitis B virus core protein forms a poorly ordered trimeric spike in assembled virus-like particles. J. Struct. Biol. 189, 73–80 (2015).
pubmed: 25557498
pmcid: 4318616
doi: 10.1016/j.jsb.2014.12.006
Cockburn, I. A. & Seder, R. A. Malaria prevention: from immunological concepts to effective vaccines and protective antibodies. Nat. Immunol. 19, 1199–1211 (2018).
pubmed: 30333613
doi: 10.1038/s41590-018-0228-6
Oyen, D. et al. Cryo-EM structure of P. falciparum circumsporozoite protein with a vaccine-elicited antibody is stabilized by somatically mutated inter-Fab contacts. Sci. Adv. 4, eaau8529 (2018).
pubmed: 30324137
pmcid: 6179375
doi: 10.1126/sciadv.aau8529
Billaud, J. N. et al. Combinatorial approach to hepadnavirus-like particle vaccine design. J. Virol. 79, 13656–13666 (2005).
pubmed: 16227285
pmcid: 1262598
doi: 10.1128/JVI.79.21.13656-13666.2005
Peyret, H. et al. Tandem fusion of hepatitis B core antigen allows assembly of virus-like particles in bacteria and plants with enhanced capacity to accommodate foreign proteins. PLoS ONE 10, e0120751 (2015).
pubmed: 25830365
pmcid: 4382129
doi: 10.1371/journal.pone.0120751
Walker, A., Skamel, C. & Nassal, M. SplitCore: an exceptionally versatile viral nanoparticle for native whole protein display regardless of 3D structure. Sci. Rep. 1, 5 (2011).
pubmed: 22355524
pmcid: 3216493
doi: 10.1038/srep00005
Venkatakrishnan, B. & Zlotnick, A. The structural biology of hepatitis B virus: form and function. Annu. Rev. Virol. 3, 429–451 (2016).
pubmed: 27482896
pmcid: 5646271
doi: 10.1146/annurev-virology-110615-042238
Shen, J. R. & Kamiya, N. Crystallization and the crystal properties of the oxygen-evolving photosystem II from Synechococcus vulcanus. Biochem 39, 14739–14744 (2000).
doi: 10.1021/bi001402m
Fromme, P., Jordan, P. & Krauss, N. Structure of photosystem I. Biochim Biophys. Acta 1507, 5–31 (2001).
pubmed: 11687205
doi: 10.1016/S0005-2728(01)00195-5
Zhou, S., Yang, S. Q. & Standring, D. N. Characterization of hepatitis B virus capsid particle assembly in Xenopus oocytes. J. Virol. 66, 3086–3092 (1992).
pubmed: 1560538
pmcid: 241070
doi: 10.1128/jvi.66.5.3086-3092.1992
Schödel, F. et al. Structure of hepatitis B virus core and e-antigen. A single precore amino acid prevents nucleocapsid assembly. J. Biol. Chem. 268, 1332–1337 (1993).
pubmed: 8419335
doi: 10.1016/S0021-9258(18)54079-5
Ball, J. M. et al. Recombinant Norwalk virus-like particles given orally to volunteers: phase I study. Gastroenterol 117, 40–48 (1999).
doi: 10.1016/S0016-5085(99)70548-2
Kapusta, J. et al. A plant-derived edible vaccine against hepatitis B virus. FASEB J. 13, 1796–1799 (1999).
pubmed: 10506582
doi: 10.1096/fasebj.13.13.1796
Kapusta, J. et al. Oral immunization of human with transgenic lettuce expressing hepatitis B surface antigen. Adv. Exp. Med. Biol. 495, 299–303 (2001).
pubmed: 11774582
doi: 10.1007/978-1-4615-0685-0_41
Laere, E. et al. Plant-based vaccines: production and challenges. J. Bot. 2016, 4928637 (2016).
Yoshida, S., Araki, H. & Yokomine, T. Baculovirus-based nasal drop vaccine confers complete protection against malaria by natural boosting of vaccine-induced antibodies in mice. Infect. Immun. 78, 595–602 (2010).
pubmed: 19901059
doi: 10.1128/IAI.00877-09
Arakawa, T. et al. Nasal immunization with a malaria transmission-blocking vaccine candidate, Pfs25, induces complete protective immunity in mice against field isolates of Plasmodium falciparum. Infect. Immun. 73, 7375–7380 (2005).
pubmed: 16239536
pmcid: 1273902
doi: 10.1128/IAI.73.11.7375-7380.2005
Carcaboso, A. M. et al. Potent, long lasting systemic antibody levels and mixed Th1/Th2 immune response after nasal immunization with malaria antigen loaded PLGA microparticles. Vaccine 22, 1423–1432 (2004).
pubmed: 15063565
doi: 10.1016/j.vaccine.2003.10.020
Moorthy, S. A., Yasawardena, S. G. & Ramasamy, R. Age-dependent systemic antibody responses and immunisation-associated changes in mice orally and nasally immunised with Lactococcus lactis expressing a malaria parasite protein. Vaccine 27, 4947–4952 (2009).
pubmed: 19545652
doi: 10.1016/j.vaccine.2009.06.011
Moorthy, G. & Ramasamy, R. Mucosal immunisation of mice with malaria protein on lactic acid bacterial cell walls. Vaccine 25, 3636–3645 (2007).
pubmed: 17280749
doi: 10.1016/j.vaccine.2007.01.070
Nacer, A. et al. Imaging murine NALT following intranasal immunization with flagellin-modified circumsporozoite protein malaria vaccines. Mucosal Immunol. 7, 304–314 (2014).
pubmed: 23820750
doi: 10.1038/mi.2013.48
Pasetti, M. F., Simon, J. K., Sztein, M. B. & Levine, M. M. Immunology of gut mucosal vaccines. Immunol. Rev. 239, 125–148 (2011).
pubmed: 21198669
pmcid: 3298192
doi: 10.1111/j.1600-065X.2010.00970.x
Wang, L. & Coppel, R. L. Oral vaccine delivery: can it protect against non-mucosal pathogens. Expert Rev. Vaccines 7, 729–738 (2008).
pubmed: 18665772
doi: 10.1586/14760584.7.6.729
Kwon, M. H. et al. Plasmodium vivax: comparison of the immune responses between oral and parenteral immunization of rPv54 in BALB/c mice. Exp. Parasitol. 126, 217–223 (2010).
pubmed: 20460123
doi: 10.1016/j.exppara.2010.05.001
Challacombe, S. J., Rahman, D., Jeffery, H., Davis, S. S. & O’Hagan, D. T. Enhanced secretory IgA and systemic IgG antibody responses after oral immunization with biodegradable microparticles containing antigen. Immunology 76, 164–168 (1992).
pubmed: 1628895
pmcid: 1421730
Carcaboso, A. M. et al. Immune response after oral administration of the encapsulated malaria synthetic peptide SPf66. Int. J. Pharm. 260, 273–282 (2003).
pubmed: 12842346
doi: 10.1016/S0378-5173(03)00266-7
Wang, L., Goschnick, M. W. & Coppel, R. L. Oral immunization with a combination of Plasmodium yoelii merozoite surface proteins 1 and 4/5 enhances protection against lethal malaria challenge. Infect. Immun. 72, 6172–6175 (2004).
pubmed: 15385527
pmcid: 517577
doi: 10.1128/IAI.72.10.6172-6175.2004
Tacket, C. O. et al. Safety of live oral Salmonella typhi vaccine strains with deletions in htrA and aroC aroD and immune response in humans. Infect. Immun. 65, 452–456 (1997).
pubmed: 9009296
pmcid: 174616
doi: 10.1128/iai.65.2.452-456.1997
Tacket, C. O. et al. Phase 2 clinical trial of attenuated Salmonella enterica serovar typhi oral live vector vaccine CVD 908-htrA in U.S. volunteers. Infect. Immun. 68, 1196–1201 (2000).
pubmed: 10678926
pmcid: 97267
doi: 10.1128/IAI.68.3.1196-1201.2000
Aggarwal, A. et al. Oral Salmonella: malaria circumsporozoite recombinants induce specific CD8
pubmed: 1698908
doi: 10.1084/jem.172.4.1083
Ruiz-Perez, F. et al. Expression of the Plasmodium falciparum immunodominant epitope (NANP)(4) on the surface of Salmonella enterica using the autotransporter MisL. Infect. Immun. 70, 3611–3620 (2002).
pubmed: 12065502
pmcid: 128084
doi: 10.1128/IAI.70.7.3611-3620.2002
Schorr, J., Knapp, B., Hundt, E., Kupper, H. A. & Amann, E. Surface expression of malarial antigens in Salmonella typhimurium: induction of serum antibody response upon oral vaccination of mice. Vaccine 9, 675–681 (1991).
pubmed: 1950099
doi: 10.1016/0264-410X(91)90194-B
Gonzalez, C. et al. Salmonella typhi vaccine strain CVD 908 expressing the circumsporozoite protein of Plasmodium falciparum: strain construction and safety and immunogenicity in humans. J. Infect. Dis. 169, 927–931 (1994).
pubmed: 8133113
doi: 10.1093/infdis/169.4.927
Ramasamy, R. et al. Immunogenicity of a malaria parasite antigen displayed by Lactococcus lactis in oral immunisations. Vaccine 24, 3900–3908 (2006).
pubmed: 16545511
pmcid: 7115539
doi: 10.1016/j.vaccine.2006.02.040
Zhang, Z. H., Jiang, P. H., Li, N. J., Shi, M. & Huang, W. Oral vaccination of mice against rodent malaria with recombinant Lactococcus lactis expressing MSP-1(19). World J. Gastroenterol. 11, 6975–6980 (2005).
pubmed: 16437602
pmcid: 4717040
doi: 10.3748/wjg.v11.i44.6975
Gregory, J. A. et al. Algae-produced Pfs25 elicits antibodies that inhibit malaria transmission. PLoS ONE 7, e37179 (2012).
pubmed: 22615931
pmcid: 3353897
doi: 10.1371/journal.pone.0037179
Dauvillee, D. et al. Engineering the chloroplast targeted malarial vaccine antigens in Chlamydomonas starch granules. PLoS ONE 5, e15424 (2010).
pubmed: 21179538
pmcid: 3002285
doi: 10.1371/journal.pone.0015424
Gregory, J. A., Topol, A. B., Doerner, D. Z. & Mayfield, S. Alga-produced cholera toxin-Pfs25 fusion proteins as oral vaccines. Appl Environ. Microbiol. 79, 3917–3925 (2013).
pubmed: 23603678
pmcid: 3697563
doi: 10.1128/AEM.00714-13
Noe, A. R. et al. Bridging computational vaccinology and vaccine development through systematic identification, characterization, and downselection of conserved and variable circumsporozoite protein CD4 T cell epitopes from diverse Plasmodium falciparum strains. Front. Immunol. 12, 689920 (2021).
pubmed: 34168657
pmcid: 8217813
doi: 10.3389/fimmu.2021.689920
Frank, I. et al. Acute resolving woodchuck hepatitis virus (WHV) infection is associated with a strong cytotoxic T-lymphocyte response to a single WHV core peptide. J. Virol. 81, 7156–7163 (2007).
pubmed: 17459928
pmcid: 1933276
doi: 10.1128/JVI.02711-06
Menne, S., Maschke, J., Lu, M., Grosse-Wilde, H. & Roggendorf, M. T-Cell response to woodchuck hepatitis virus (WHV) antigens during acute self-limited WHV infection and convalescence and after viral challenge. J. Virol. 72, 6083–6091 (1998).
pubmed: 9621072
pmcid: 110414
doi: 10.1128/JVI.72.7.6083-6091.1998
Menne, S. et al. Deficiencies in the acute-phase cell-mediated immune response to viral antigens are associated with development of chronic woodchuck hepatitis virus infection following neonatal inoculation. J. Virol. 76, 1769–1780 (2002).
pubmed: 11799172
pmcid: 135887
doi: 10.1128/JVI.76.4.1769-1780.2002
Klein, S. L. & Flanagan, K. L. Sex differences in immune responses. Nat. Rev. Immunol. 16, 626–638 (2016).
pubmed: 27546235
doi: 10.1038/nri.2016.90
Klein, S. L., Marriott, I. & Fish, E. N. Sex-based differences in immune function and responses to vaccination. Trans. R. Soc. Trop. Med. Hyg. 109, 9–15 (2015).
pubmed: 25573105
pmcid: 4447843
doi: 10.1093/trstmh/tru167
Vom Steeg, L. G., Flores-Garcia, Y., Zavala, F. & Klein, S. L. Irradiated sporozoite vaccination induces sex-specific immune responses and protection against malaria in mice. Vaccine 37, 4468–4476 (2019).
pubmed: 31262583
pmcid: 7862922
doi: 10.1016/j.vaccine.2019.06.075
Flanagan, K. L., Fink, A. L., Plebanski, M. & Klein, S. L. Sex and gender differences in the outcomes of vaccination over the life course. Annu. Rev. Cell Dev. Biol. 33, 577–599 (2017).
pubmed: 28992436
doi: 10.1146/annurev-cellbio-100616-060718
Casadei, E. & Salinas, I. Comparative models for human nasal infections and immunity. Dev. Comp. Immunol. 92, 212–222 (2019).
pubmed: 30513304
doi: 10.1016/j.dci.2018.11.022
Pabst, R. Mucosal vaccination by the intranasal route. Nose-associated lymphoid tissue (NALT)-Structure, function and species differences. Vaccine 33, 4406–4413 (2015).
pubmed: 26196324
doi: 10.1016/j.vaccine.2015.07.022
Chatterjee, D. et al. Avid binding by B cells to the Plasmodium circumsporozoite protein repeat suppresses responses to protective subdominant epitopes. Cell Rep. 35, 108996 (2021).
pubmed: 33852850
pmcid: 8052187
doi: 10.1016/j.celrep.2021.108996
World Health Organization. Programmatic Options for Implementation of Malaria RTS,S Vaccination Schedule for Young Children. (2015).
Kennedy, M. et al. A rapid and scalable density gradient purification method for Plasmodium sporozoites. Malar. J. 11, 421 (2012).
pubmed: 23244590
pmcid: 3543293
doi: 10.1186/1475-2875-11-421
Ogawa, T. & Terui, G. Studies on the growth of Spirulina platensis. on the pure culture of Spirulina platensis. J. Fermentation Technol. 48, 361–367 (1970).
Frey, A., Di Canzio, J. & Zurakowski, D. A statistically defined endpoint titer determination method for immunoassays. J. Immunol. Methods 221, 35–41 (1998).
pubmed: 9894896
doi: 10.1016/S0022-1759(98)00170-7
Zhao, Z. et al. Structural differences between the woodchuck hepatitis virus core protein in the dimer and capsid states are consistent with entropic and conformational regulation of assembly. J. Virol. 93, e00141–19 (2019).
pubmed: 31043524
pmcid: 6600186
doi: 10.1128/JVI.00141-19