IMRAS-Immunization with radiation-attenuated Plasmodium falciparum sporozoites by mosquito bite: Cellular immunity to sporozoites, CSP, AMA1, TRAP and CelTOS

PLoS One. 2021 Aug 20;16(8):e0256396. doi: 10.1371/journal.pone.0256396. eCollection 2021.

Abstract

Background: Immunization with radiation-attenuated sporozoites (RAS) by mosquito bites provides >90% sterile protection against Plasmodium falciparum malaria in humans. We conducted a clinical trial based on data from previous RAS clinical trials that suggested that 800-1200 infected bites should induce ~50% protective vaccine efficacy (VE) against controlled human malaria infection (CHMI) administered three weeks after the final immunization. Two cohorts were immunized separately. VE was 55% in Cohort 1 but 90% in Cohort 2, the cohort that received a higher first dose and a reduced (fractional) fifth dose. Immune responses were better boosted by the fractional fifth dose in Cohort 2 and suggested the importance of the fractional fifth dose for increased protection in Cohort 2 responses. Three protected subjects were later boosted and were protected suggesting that protection could be extended to at least 67 weeks.

Methods: The ex vivo FluoroSpot assay was used to measure peripheral IFN-γ, IL2, and IFN-γ+IL2 responses to PfNF54 sporozoites and malaria antigens CSP, AMA1, TRAP, and CelTOS using pools of synthetic overlapping 15mer peptides spanning each antigen.

Results: There was no correlation between IFN-γ, IL2, and IFN-γ+IL2 responses to sporozoites and protection, but fold-increases between post-4th and post-5th responses greater than 1.0 occurred mostly in protected subjects. IFN-γ and IL2 responses to TRAP, CelTOS and CSP occurred only in protected subjects. Peripheral IFN-γ, IL2, and IFN-γ+IL2 responses were short-lived and low by 27 weeks post-CHMI but were restored by boosting.

Conclusions: These studies highlight the importance of vaccine dose and schedule for vaccine efficacy, and suggest that CSP, TRAP, AMA1 and CelTOS may be targets of protective immunity. The correlation between fold-increases in responses and protection should be explored in other vaccine trials.

Trial registration: ClinicalTrials.gov NCT01994525.

MeSH terms

  • Adolescent
  • Adult
  • Animals
  • Antigens, Protozoan / immunology
  • Culicidae / immunology
  • Culicidae / parasitology
  • Female
  • Humans
  • Immunity, Cellular
  • Immunization / methods
  • Insect Bites and Stings / immunology
  • Interferon-gamma / immunology
  • Interferon-gamma / metabolism
  • Interleukin-2 / immunology
  • Malaria Vaccines* / immunology
  • Malaria, Falciparum* / immunology
  • Malaria, Falciparum* / parasitology
  • Malaria, Falciparum* / prevention & control
  • Male
  • Middle Aged
  • Plasmodium falciparum* / immunology
  • Plasmodium falciparum* / radiation effects
  • Protozoan Proteins* / immunology
  • Sporozoites* / immunology
  • Sporozoites* / radiation effects
  • Vaccines, Attenuated / immunology
  • Young Adult

Substances

  • Malaria Vaccines
  • Protozoan Proteins
  • Antigens, Protozoan
  • Interferon-gamma
  • Vaccines, Attenuated
  • Interleukin-2

Associated data

  • ClinicalTrials.gov/NCT01994525

Grants and funding

This study was funded in part by the Bill & Melinda Gates Foundation in the form of a Global Health grant (OPP1034596) awarded to the Naval Medical Research Center through cooperative research and development agreements for TLR (NMRC-12-3941) and JEE (NCRADA NMRC-15-0579). This study was also funded in part by the Military Infectious Diseases Research Program in the form of funds to MS (F0447_15_NM; work unit A1215). The Bill & Melinda Gates Foundation provided support in the form of salaries for JL, SR, and JCB. The funder reviewed and approved the study design but had no role in data collection and analysis, decision to publish, or preparation of the manuscript. TLR transitioned from the Navy to the private sector in January 2014 prior to the initiation of the clinical trial, and thereafter received salary support from Sanaria Inc. (https://sanaria.com). The funder had no role in study design, data collection, and analysis, decision to publish, or preparation of the manuscript. The specific roles of these authors are articulated in the ‘author contributions’ section.