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Recent progress in vaccine development targeting pre-clinical human toxoplasmosis

Ki-Back Chu1orcid, Fu-Shi Quan1,2,*orcid
Parasites, Hosts and Diseases 2023;61(3):231-239.
Published online: August 21, 2023

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*Correspondence: (fsquan@khu.ac.kr)
• Received: August 15, 2022   • Accepted: May 30, 2023

© 2023 The Korean Society for Parasitology and Tropical Medicine

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (https://creativecommons.org/licenses/by-nc/4.0) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

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  • Toxoplasma gondii is an intracellular parasitic organism affecting all warm-blooded vertebrates. Due to the unavailability of commercialized human T. gondii vaccine, many studies have been reported investigating the protective efficacy of pre-clinical T. gondii vaccines expressing diverse antigens. Careful antigen selection and implementing multifarious immunization strategies could enhance protection against toxoplasmosis in animal models. Although none of the available vaccines could remove the tissue-dwelling parasites from the host organism, findings from these pre-clinical toxoplasmosis vaccine studies highlighted their developmental potential and provided insights into rational vaccine design. We herein explored the progress of T. gondii vaccine development using DNA, protein subunit, and virus-like particle vaccine platforms. Specifically, we summarized the findings from the pre-clinical toxoplasmosis vaccine studies involving T. gondii challenge infection in mice published in the past 5 years.
  • Key words: Toxoplasma gondii, vaccine, virus-like particle, protein subunit, DNA
Parasitic diseases are frequently neglected despite their importance and impact on human life. Toxoplasmosis, caused by the Apicomplexan parasite, Toxoplasma gondii, is a neglected disease of global importance. Global statistics demonstrate that T. gondii affects more than a third of the world’s population [1], although seroprevalence can vary across regions [2]. These intracellular parasites are generally asymptomatic in healthy adults but can have fatal consequences in pregnant women and immunocompromised adults. For instance, transmitting T. gondii from mother to fetus can result in several congenital disabilities or stillbirths [3]. Administering drugs, such as pyrimethamine and sulfadiazine, can limit T. gondii infection in patients. However, these drugs are only effective against tachyzoites and cannot exert their full effect against the tissue-dwelling bradyzoites [4].
Furthermore, drug-resistant T. gondii strains continue to emerge globally, resulting in treatment failures. Although the underlying mechanisms remain largely elusive, mutation in the dihydropteroate synthase (dhps) gene could contribute to drug resistance against sulfonamides in T. gondii clinical isolates [5,6]. The clinical drug-resistant isolates, TgCTBr4 and TgCTBr17, acquired from newborn patients in Brazil, were reported to be less susceptible to pyrimethamine and sulfadiazine treatments [7].
Vaccines are highly desirable prophylaxis strategies that limit the dissemination of parasites. Efforts to develop an efficacious vaccine against toxoplasmosis have been ongoing for decades. To date, only one toxoplasmosis vaccine is commercially available. Toxovax is a live-attenuated T. gondii S48 strain that cannot be used in humans as safety profiles have not been clinically evaluated [8]. The exact reasons for prioritizing veterinary toxoplasmosis vaccine development over their clinical counterpart remains unknown, but congenital toxoplasmosis in ewes exhibited a considerable problem in the agricultural sector. Additionally, attaining regulatory approval is less stringent for veterinary vaccines than clinical ones [9].
Despite massive advances in vaccinology, an effective human vaccine for toxoplasmosis remains unavailable. After establishing toxoplasmosis as a significant foodborne infectious disease in the western hemisphere [10], it was not perceived as a threat to the general public. Clinical toxoplasmosis vaccine development has progressed rather slowly. Therefore, vaccine development remains a top priority. Herein, we briefly summarized some antigen components of T. gondii used in several vaccine platforms and highlighted advances in T. gondii vaccine development. We addressed several advantages and pitfalls of each platform that either promote or impede their development.
Vaccines are immune response-inducing biological products that confer protection against a specific infectious disease by exposing pathogenic agents to the host. The vaccine must express one or more antigens derived from the disease-causing pathogen [11]. The immunity induction mechanism is similar for most vaccines, irrespective of the target pathogen or platform. After entry of vaccine antigen, they are transported to compartmentalized secondary lymphoid organs, such as lymph nodes. The antigens activate B cells with specific receptors that recognize these foreign antigens. Once activated, the B cells present the processed vaccine antigen to the T cells and induce cellular signals that stimulate their proliferation and differentiation. The activated B cells produce short-lived plasma cells that secrete large quantities of antibodies. They induce germinal center responses, ensuring the production of memory B and long-lived plasma cells [12]. Simultaneously, antigen-presenting cells, such as dendritic cells, can cross-present the vaccine antigens to the T cells, signaling their differentiation into effector and memory T cells. Combined, these intricate processes contribute to the well-being of vaccinees by creating an immunological memory that confers rapid and robust protection against the target pathogen.
Molecular properties of DNA vaccines
Using nucleic acids for eliciting immune responses in hosts was first reported in the early 1990s by Tang et al. [13]. Since its discovery, DNA vaccines rapidly emerged into the scientific limelight and were actively researched. Structurally, DNA vaccines are composed of a bacteria-derived plasmid encoding a specific antigen of interest whose expression is controlled by a strong viral promoter for optimal gene expression in vivo, such as the cytomegalovirus (CMV) or the simian virus 40 (SV40). The precise mechanism underlying how these DNA vaccines induce cellular and humoral immune responses despite their low expression levels in hosts remains largely unknown. However, 3 possible mechanisms describe how these vaccines may facilitate antigen presentation [14]. First, upon delivery into hosts by the parenteral route of immunization, the plasmid DNA encoding the antigen is internalized by somatic cells in the vicinity, such as myocytes or keratinocytes. The antigens are transcribed within these cells and eventually presented to CD8+ T cells via the membrane histocompatibility complex (MHC) class I. Second, the antigen-presenting cells (APCs), such as dendritic cells, are recruited to the injection site. These cells become transfected by the plasmid DNA and present the expressed antigen of interest via MHC I and II. Last, the plasmid-infected somatocytes are phagocytosed by APCs to enable cross-priming and antigen presentation to CD4+ and CD8+ T cell subsets.
There are several factors favoring DNA vaccines over traditional vaccines. The production costs for DNA vaccines are relatively lower than traditional vaccines. Also, because infectious pathogens are not being introduced into the host, this vaccination approach is safe for use [15]. While DNA vaccines appear promising, there are safety concerns even if an infectious pathogen is not used for immunization. For instance, the possibility of antigen-encoding plasmid DNA integration into the host chromosome is one such consequence [16], though later studies revealed that the probability of genetic integration is extremely low [17]. Furthermore, DNA vaccines are weakly immunogenic. Specifically, suboptimal vaccine efficacies were reported from DNA vaccine studies conducted in non-human primates, as indicated by the low levels of antibody responses [15]. Based on these profiles, several DNA vaccines against various infectious diseases have undergone clinical evaluations but a clinical DNA vaccine trial for toxoplasmosis remains unreported.
Current progress in T. gondii DNA vaccine development
DNA vaccines are the most prevalent vaccine platforms being investigated throughout the world. The sheer amount of DNA vaccine-based publications skyrocketed in the early 2000s, and its popularity has remained unchanged [18]. This research trend is no exception for T. gondii vaccines, as most studies revolve around DNA vaccines. Despite the extensive research, most DNA vaccine results were suboptimal, while a few studies reported exceptional findings. Different T. gondii antigens conferred differing degrees of protection in mice. For example, DNA vaccines expressing the dense granule (GRA) 39 antigen prolonged the survival of Kunming mice by 20 days, but none could survive the challenge infection with the RH strain. Cyst burden reduction upon challenge infection with 10 cysts of PRU strain was suboptimal, as not even 50% cyst burden reduction was observed [19]. Contrastingly, GRA24-expressing DNA vaccines prolonged the survival of RH-infected BALB/c mice up to 30 days post-infection [20]. This was also the case with T. gondii Myc regulation 1 (MYR1)-expressing vaccine, which significantly prolonged the survival of immunized mice against RH challenge infection [21].
Several strategies improved the protective efficacy but were only marginally effective. Adjuvanting DNA vaccines had a minor effect on the vaccine’s protective efficacy. Although supplementing the T. gondii GRA7 DNA vaccine with the calcium phosphate nanoparticle adjuvant prolonged the survival of immunized mice, it was only 2 days longer than the unadjuvanted control group [22]. Conflicting results were observed from multi-antigenic vaccines. Combined immunization with DNA vaccines expressing the microneme proteins (MIC) 5 and 16 as antigens reduced the brain cyst burden by half in mice challenged with the PRU strain but, as with other vaccines, failed to confer prolonged protection against the RH strain [23]. On the contrary, multi-antigenic DNA vaccines expressing the SAG2, rhoptry protein (ROP) 9, and MIC3 ensured that immunized mice survived the challenge infection with the highly virulent RH strain regardless of the infection doses [24]. Protection induced by these DNA vaccines was tabulated and briefly described (Table 1).
Molecular properties of protein subunit vaccines
Protein subunit vaccines use a small fraction of a pathogenic agent’s antigenic component to elicit immune responses in vaccinees. Like the traditional inactivated whole-organism vaccines, protein subunit vaccines are incapable of replicating in hosts and are safe but possess low immunogenicity. Therefore, protein subunit vaccines often require multiple immunization doses or adjuvant incorporation to achieve long-lasting immunity [25]. With the introduction of recombinant DNA technology and advancements in molecular biology, mass-producing foreign genes of interest in various expression systems has become feasible. Bacterial expression systems are frequently used to produce large quantities of protein of interest at a low cost. However, given the nature of prokaryotic organisms, proteins are misfolded, and post-translational modifications (PTMs) observed in mammals are lacking [26]. The need for downstream purification for endotoxin removal and processing of expressed antigens further hampers this. Like the bacterial expression system, yeast and insect cells can rapidly produce significant amounts of proteins of interest. While PTMs occur in these organisms, glycosylation patterns are not identical to those observed in mammalian cells [27]. Based on PTM, mammalian cells would be ideal for antigenic protein production. However, improvements are needed as mammalian cell-derived antigen yields are relatively lower than antigens produced in the aforementioned expression systems.
Current progress in T. gondii recombinant protein subunit vaccine development
Like DNA vaccines, much progress has been made using recombinant subunit vaccines. Subunit protein vaccines are safe, but their immunogenicity pales in comparison to other vaccine platforms [28]. While some protein-based T. gondii vaccines are protective, others failed to elicit desirable protection. The latter was predominantly observed in studies that utilized ubiquitous eukaryotic proteins as antigens. Vaccines expressing the T. gondii aspartic protease 3 (ASP3) prolonged the survival duration by 11 days against RH challenge infection [29]. T. gondii peroxiredoxin 1 (PRX1) vaccine failed to confer complete protection against the moderately virulent type II PLK strain [30]. However, as with DNA vaccines, conflicting protection results were observed from subunit vaccines (Table 2). Cocktail subunit vaccines conferred protection against types I and II T. gondii lineages. Intramuscular immunization with subunit proteins T. gondii macrophage migration inhibitory factor, calcium-dependent protein kinase 3, and the 14-3-3 protein resulted in complete protection against RH tachyzoite and PRU strains [31]. Given this circumstance, more research on improving these vaccines’ protective efficacy is required.
Molecular properties of VLP vaccines
Although VLPs appear similar to protein subunit vaccines, they are not necessarily the same and should be categorized differently. VLPs are highly immunogenic self-assembled particles that mimic the structural aspects of native virions. However, these particles are inherently safe due to the lack of genetic material. Molecular and structural factors that contribute to the high immunogenicity of VLP-based vaccines have been described in detail [32], and as such, these aspects will be briefly described. In VLPs, antigens of interest are repetitively presented in a dense array which is critical to mounting efficient immune responses against the target antigen [33,34].
Furthermore, because the size of VLPs is less than 200 nm, they are rapidly trafficked into the lymph nodes [35]. The surface charge is another structural property of VLPs that improves immunogenicity compared to protein subunit vaccines. For example, particle-based vaccines possess charged surfaces that enhance their interaction with professional APCs, which may not be accurate for solubilized antigens [36]. Nonetheless, there are limitations to VLP vaccine technology, such as production costs. Like protein subunit vaccines, PTM must be considered during VLP vaccine assembly.
Current progress in T. gondii VLP vaccine development
To date, all VLP-based vaccine studies reported are chimeric, expressing parasitic antigens on the surface of influenza virus matrix protein 1. Surprisingly, VLP immunization elicited considerable protection against virulent type I and moderately virulent type II strains in mice, such as those expressing MIC8 [37] and ROP13 [38] as surface antigens (Table 3). In a comparative study, VLPs expressing ROP18 antigens were more efficacious than those expressing ROP4 [39]. Similar to DNA and subunit vaccines, a multi-antigenic vaccine approach enhanced the protective efficacy of VLP vaccines. While ROP4 and ROP13 VLPs were protective and ensured 100% survival [40], VLPs co-expressing ROP4 and ROP13 antigens led to brain cyst burden reduction compared to VLPs expressing either antigen alone in BALB/c mice [41]. VLPs co-expressing MIC8 and ROP18 reduced the parasite burden following challenge infection with the T. gondii GT1 strain [42]. Further supplementing this vaccine with the inner membrane complex subcompartment protein 3 (IMC) conferred partial protection against the virulent GT1 strain but elicited complete protection against ME49 [43,44].
A research group demonstrated that chimeric hepatitis B virus-based VLPs expressing CD8 and CD4 T cell epitopes prolonged the survival of immunized mice upon challenge infection with T. gondii RH strain [45]. The impact of immunization regimen and adjuvant use was also evaluated. Herein, increasing the number of immunizations and supplementing adjuvants did not decrease brain cyst size but significantly reduced the cyst burden in ME49-infected mice [46,47]. More research on these T. gondii VLP vaccines is required, especially against the highly virulent strains, which are lethal even at small infection doses. However, the outlook for this vaccine platform appears promising. Furthermore, as all VLP-based vaccine studies were conducted in mice, evaluating their protective efficacy in higher-order eukaryotic organisms should be considered.
In summary, additional studies are required to improve the protective efficacy of T. gondii vaccines; however, the general outlook for their development seems promising. Numerous studies have proposed improving vaccine efficacy by optimizing immunization strategies, adjuvant usage, or identifying novel candidate antigens. Recent findings have demonstrated that pre-clinical toxoplasmosis vaccines can elicit cellular and humoral immune responses in immunized mice, irrespective of the vaccine platform. Much of the T. gondii vaccine studies have focused on intermediate hosts, and vaccines targeting definitive hosts, including felines, are understudied. Furthermore, given the parasite’s complex life cycle, antigens spanning multiple stages should be carefully evaluated based on their immunogenicity. Future investigations could attempt to address these shortcomings and employ novel strategies for vaccine development.

Author contributions

Conceptualization: Chu KB, Quan FS

Funding acquisition: Quan FS

Writing – original draft: Chu KB

Writing – review & editing: Chu KB, Quan FS

We declare that this research was conducted without any intention for commercial or financial benefits.

This research was supported by the National Research Foundation of Korea (NRF) (2018 R1A6A1A03025124).
Table 1
Protective efficacy of DNA vaccines expressing various T. gondii antigens
Table 1
Antigen Mouse strain Challenged T. gondii strain Survival rate (duration)a Reference
GRA24 Mouse (BALB/c) Type I: RH 0% (32 days) [20]
MYR1 0% (36 days) [21]
MIC3, ROP9, SAG2 >30% [24]
MIC5, MIC16 Mouse (Kunming) Type I: RH
Type II: PRU		 0% (26 days)
NDb 		[23]
GRA39 0% (20 days)
NDb 		[19]

aFrom challenge infection to all fatal.

bNot determined.

Table 2
Efficacy of T. gondii vaccines based on protein subunit
Table 2
Antigen Mouse strain Challenged T. gondii strain Survival rate (duration)a Reference
ASP3 Mouse (BALB/c) Type I: RH 0% (18 days) [29]
PRX1 Type II: PLK <70% [30]
MIF, CDPK3, 14-3-3 Type I: RH
Type II: PRU		 90%
NDb 		[31]

aFrom challenge infection to all fatal.

bNot determined.

Table 3
Protective efficacy of T. gondii vaccines based on virus-like particle
Table 3
Antigen Mouse strain Challenged T. gondii strain Survival rate (duration)a Reference
MIC8 Mouse (BALB/c) Type I: RH 100% [37]
ROP13 Type II: ME49 [38]
IMC, ROP18, MIC8 [47]
ROP18, MIC8 Type I: GT1
Type II: ME49		 0% (17 days)
NDb 		[42]
IMC, ROP18, MIC8 Type I: GT1 20% [43]
B and T cell epitopes Type I: RH
Type II: ME49		 0% (20 days)
NDb 		[45]

aFrom challenge infection to all fatal.

bNot determined.

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Recent progress in vaccine development targeting pre-clinical human toxoplasmosis
Parasites Hosts Dis. 2023;61(3):231-239.   Published online August 21, 2023
DOI: https://doi.org/10.3347/PHD.22097
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Recent progress in vaccine development targeting pre-clinical human toxoplasmosis
Parasites Hosts Dis. 2023;61(3):231-239.   Published online August 21, 2023
DOI: https://doi.org/10.3347/PHD.22097
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Recent progress in vaccine development targeting pre-clinical human toxoplasmosis
Recent progress in vaccine development targeting pre-clinical human toxoplasmosis
Antigen Mouse strain Challenged T. gondii strain Survival rate (duration)a Reference
GRA24 Mouse (BALB/c) Type I: RH 0% (32 days) [20]
MYR1 0% (36 days) [21]
MIC3, ROP9, SAG2 >30% [24]
MIC5, MIC16 Mouse (Kunming) Type I: RH
Type II: PRU		 0% (26 days)
NDb		 [23]
GRA39 0% (20 days)
NDb		 [19]
Antigen Mouse strain Challenged T. gondii strain Survival rate (duration)a Reference
ASP3 Mouse (BALB/c) Type I: RH 0% (18 days) [29]
PRX1 Type II: PLK <70% [30]
MIF, CDPK3, 14-3-3 Type I: RH
Type II: PRU		 90%
NDb		 [31]
Antigen Mouse strain Challenged T. gondii strain Survival rate (duration)a Reference
MIC8 Mouse (BALB/c) Type I: RH 100% [37]
ROP13 Type II: ME49 [38]
IMC, ROP18, MIC8 [47]
ROP18, MIC8 Type I: GT1
Type II: ME49		 0% (17 days)
NDb		 [42]
IMC, ROP18, MIC8 Type I: GT1 20% [43]
B and T cell epitopes Type I: RH
Type II: ME49		 0% (20 days)
NDb		 [45]
Table 1 Protective efficacy of DNA vaccines expressing various T. gondii antigens

From challenge infection to all fatal.

Not determined.

Table 2 Efficacy of T. gondii vaccines based on protein subunit

From challenge infection to all fatal.

Not determined.

Table 3 Protective efficacy of T. gondii vaccines based on virus-like particle

From challenge infection to all fatal.

Not determined.

Table 1

Table 2

Table 3

PHD : Parasites, Hosts and Diseases

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