Two-Faced Immunity? The Evidence for Antibody Enhancement of Malaria Transmission

Bousema, Teun; Sauerwein, Robert W.; Drakeley, Chris

doi:10.1016/j.pt.2018.11.003

Cited by 17 publications

(17 citation statements)

References 97 publications

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“…such as competition between parasites for limited resources or temperature effects on mosquito anti-398 malarial responses may facilitate "transmission enhancement" in mosquitoes exposed to the reduced 399 gametocyte densities. Such transmission enhancement is not without precedent and has also been 400 observed in presence of low levels of anti-gametocytic antibodies (Stone et al, 2018). 401…”

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confidence: 95%

Field relevant variation in ambient temperature modifies the density-dependent establishment of Plasmodium falciparum in mosquitoes: implications for the infectious reservoir and beyond?

Pathak

Shiau

Thomas

et al. 2019

Preprint

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45The relationship between Plasmodium falciparum gametocyte density and infections in mosquitoes is 46 central to understanding the rates of transmission with important implications for control. Here, we 47 determined whether field relevant variation in environmental temperature could also modulate this 48 relationship. Anopheles stephensi were challenged with three densities of P. falciparum gametocytes 49 spanning a ~10-fold gradient, and housed under diurnal/daily temperature range ("DTR") of 9⁰C around 50 means of 20⁰C, 24⁰C and 28⁰C. At the peak stages of infection for each temperature, the proportion of 51 mosquitoes infected with oocysts in the midguts or infectious with sporozoites in the salivary glands were 52 measured (referred to collectively as vector competence hereon), in addition to oocyst intensities from 53 infected midguts. While vector competence was similar at 20 DTR 9⁰C and 24 DTR 9⁰C, the proportion 54 of mosquitoes infected and subsequently infectious were also comparable, with evidence, surprisingly, for 55higher vector competence in mosquitoes challenged with intermediate gametocyte densities. For the same 56 gametocyte densities however, severe reduction in the proportion of infectious mosquitoes was 57 accompanied by a significant decline in vector competence at 28 DTR 9⁰C, although density per se 58 showed a positive and linear effect at this temperature. Unlike vector competence, oocyst intensities 59 decreased with increasing temperatures with a predominantly positive and linear association with 60 gametocyte density, especially at 28 DTR 9⁰C. Oocyst intensities across individual infected midguts 61suggested temperature-specific differences in mosquito susceptibility/resistance : at 20 DTR 9⁰C and 24 62 DTR 9⁰C, dispersion (aggregation) increased in a density-dependent manner but not at 28 DTR 9⁰C where 63 the distributions were consistently random. Limitations notwithstanding, our results have manifold 64 implications in, for instance, how variation in temperature could modify seasonal dynamics of infectious 65 reservoirs and transmission and the contribution of high-/patent-and low-density/sub-patent carriers, to 66 suggestions for design and deployment of transmission-blocking vaccines/drugs, but with a cautionary 67 note suggesting how low efficacy could lead to transmission enhancement in certain environments.

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confidence: 95%

Field relevant variation in ambient temperature modifies the density-dependent establishment of Plasmodium falciparum in mosquitoes: implications for the infectious reservoir and beyond?

Pathak

Shiau

Thomas

et al. 2019

Preprint

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“…Regarding the apparent positive effect of vaccination on indicators of tick development (engorgement, molting, and survival), similar adverse effects of the immune response have been noted in a number of circumstances. Recognized or suspected instances of immune-mediated enhancement have concerned vaccination against viral [ 54 ] agents or pre-existing immunity to bacterial [ 55 ] and parasitic pathogens [ 56 ]. Enhancement has been evidenced as an increased replication of the pathogen, exacerbation of disease manifestation, or even increased susceptibility to infection [ 57 ].…”

Section: Discussionmentioning

confidence: 99%

Failed Disruption of Tick Feeding, Viability, and Molting after Immunization of Mice and Sheep with Recombinant Ixodes ricinus Salivary Proteins IrSPI and IrLip1

et al. 2020

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To identify potential vaccine candidates against Ixodes ricinus and tick-borne pathogen transmission, we have previously sequenced the salivary gland transcriptomes of female ticks infected or not with Bartonella henselae. The hypothesized potential of both IrSPI (I. ricinus serine protease inhibitor) and IrLip1 (I. ricinus lipocalin 1) as protective antigens decreasing tick feeding and/or the transmission of tick-borne pathogens was based on their presumed involvement in dampening the host immune response to tick feeding. Vaccine endpoints included tick larval and nymphal mortality, feeding, and molting in mice and sheep. Whether the antigens were administered individually or in combination, the vaccination of mice or sheep elicited a potent antigen-specific antibody response. However, and contrary to our expectations, vaccination failed to afford protection against the infestation of mice and sheep by I. ricinus nymphs and larvae, respectively. Rather, vaccination with IrSPI and IrLip1 appeared to enhance tick engorgement and molting and decrease tick mortality. To the best of our knowledge, these observations represent the first report of induction of vaccine-mediated enhancement in relation to anti-tick vaccination.

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“…Monoclonal antibodies have been shown to destabilize the influenza HA stem domain, leading to faster kinetics of influenza virus fusion and enhanced respiratory disease (Winarski et al, 2019). Antibody enhancement of malaria transmission and complement activation in conjunction with antibodies in enhancing RBC invasion have been reported too (Biryukov et al, 2016;Stone et al, 2019). The RTS,S vaccine might prime T cells in some hosts and/or produce antibodies that can amplify immune response and enhance clinical symptoms.…”

Section: Partially Protective Vaccines and Effects On Host Populationsmentioning

confidence: 99%

Host-Malaria Parasite Interactions and Impacts on Mutual Evolution

Zhang

Joy

2020

Front. Cell. Infect. Microbiol.

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Malaria is the most deadly parasitic disease, affecting hundreds of millions of people worldwide. Malaria parasites have been associated with their hosts for millions of years. During the long history of host-parasite co-evolution, both parasites and hosts have applied pressure on each other through complex host-parasite molecular interactions. Whereas the hosts activate various immune mechanisms to remove parasites during an infection, the parasites attempt to evade host immunity by diversifying their genome and switching expression of targets of the host immune system. Human intervention to control the disease such as antimalarial drugs and vaccination can greatly alter parasite population dynamics and evolution, particularly the massive applications of antimalarial drugs in recent human history. Vaccination is likely the best method to prevent the disease; however, a partially protective vaccine may have unwanted consequences that require further investigation. Studies of host-parasite interactions and co-evolution will provide important information for designing safe and effective vaccines and for preventing drug resistance. In this essay, we will discuss some interesting molecules involved in host-parasite interactions, including important parasite antigens. We also discuss subjects relevant to drug and vaccine development and some approaches for studying host-parasite interactions.

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Two-Faced Immunity? The Evidence for Antibody Enhancement of Malaria Transmission

Cited by 17 publications

References 97 publications

Field relevant variation in ambient temperature modifies the density-dependent establishment of Plasmodium falciparum in mosquitoes: implications for the infectious reservoir and beyond?

Field relevant variation in ambient temperature modifies the density-dependent establishment of Plasmodium falciparum in mosquitoes: implications for the infectious reservoir and beyond?

Failed Disruption of Tick Feeding, Viability, and Molting after Immunization of Mice and Sheep with Recombinant Ixodes ricinus Salivary Proteins IrSPI and IrLip1

Host-Malaria Parasite Interactions and Impacts on Mutual Evolution

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