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Hybrid Schistosomes in Africa
Causal agents of schistosomiasis are dioecious, digenean schistosomes affecting mankind in 76 countries. Natural and anthropogenic changes impact on breaking species isolation barriers favoring introgressive hybridization, i.e., allelic exchange among gene pools of sympatric, interbreeding species leading to instant large genetic diversity. Phylogenetic distance matters, thus the less species differ phylogenetically the more likely they hybridize.
1. Schistosomiasis and Parasite Hybridization
Schistosomiasis affects mankind in 76 countries causing an estimated annual mortality rate of 280,000, 779 million people at risk of infection, 250 million people with active infections, and 440 million people with residual morbidity . The disease burden is largest throughout sub-Saharan Africa accounting for >90% caused by the clinically most relevant human-pathogenic species Schistosoma mansoni (Sm) and S. haematobium (Sh) . Though schistosomiasis is likely underrecognized among the veterinary sector, inclusive of livestock and wildlife animals, it is assumed that in particular ruminants, rodents and non-human primates are carriers of zoonotic species .
The causal agents of this neglected tropical disease are dioecious digenean schistosomes within the Platyhelminthes; species by clade of the Schistosoma genus including their geographical distribution, and intermediate and definitive hosts are illustrated in Figure 1 .
2. Schistosome Hybrids across Africa
2.1. S. haematobium/S. guineensis Hybrids
Interactions between Sh and Sg are reported from South-West Cameroon; of note is the re-description of S. intercalatum (Si) from Lower Guinea, e.g., Cameroon, Gabon, Equatorial Guinea and São Tomé, as Sg . Ecological changes such as forest clearance and agricultural development evolving in the 1960s besides population movement favored the presence of snail hosts, e.g., Bulinus wrighti, B. forskalii and B. truncatus, and species sympatry and interplay; this materialized the complete replacement of Sg by Sh within 25–30 years through introgressive hybridization and competitive extinction abetted by behavioral, reproductive and genetic advantages . Experiments confirmed greater competitiveness and pairing abilities of ShxSg crosses over parental species, and Sh being dominant over Sg, which supports observations made in Cameroon and elsewhere, e.g., Kinshasa, Democratic Republic of Congo, and Dogon Country, Mali . Retrospective experiments among schistosomes of laboratory maintained urinary ova of Cameroonian children detected hybridization between Sh and Sg among 100%, 33% and 5% isolates from Kumba, Loum (1990), and Loum (1999 and 2000), respectively; the remainder had pure Sh, but no Sg despite established B. forskalii hosts . Findings were confirmed by four-banded single-stranded conformational polymorphism (SSCP) profiles of second nuclear ribosomal internal transcribed spacer (ITS2) fragments. Sequencing isolates from Loum revealed unequivocal intermediate SNPs at the positions 25, 80 and 130 within ITS2 fragments compared to parental strains, i.e., guanine-cytosine-guanine for Sh, and adenine-thymine-adenine for Sg, clearly demonstrating ShxSg recombinants with dominance, thus inheritance, of Sh over Sg .
2.2. S. haematobium/S. bovis Hybrids
2.3. S. haematobium/S. mansoni Hybrids
2.4. S. mansoni/S. rodhaini Hybrids
3. Schistosomal Hybridization—Interference on Leading Vaccine Candidates
Extensive small-scale gene amplifications and alterations are contributing to a steady schistosomal genomic evolution . SNPs emerging through transversional/transitional or synonymous/non-synonymous nucleotide substitutions leading to e.g., alternative splicing or silent mutations are of high importance in particular among sequences serving as drug or vaccine targets; they may lead to structural and functional protein alterations impacting charge changes and residue conservation affecting drug binding sites or antibody recognition of antigenic epitopes . Hosts react in the following general manners against schistosomal infections, i.e., development of age-dependent partial protective immunity to reinfection from repeated adult worm death, and initiation of immunopathogenic and/or immunoregulatory mechanisms against parasitic antigens released from eggs trapped in tissues .
Preliminary findings of the phase 2a trial confirmed rSm14+GLA-SE’s safety and strong, long-lasting immunogenicity, and reported 92% seroconversion following the second dose with cellular responses, memory cells and T-cell activation makers . However, Sm14 isoforms demonstrate the potential of structural instability resulting in its aggregation and precipitation and, in turn, to uncertain immunoprotection and functional alterations .
rSh28GST+Alhydrogel/Bilhvax® vaccine candidate was tested in a phase 3 safety, efficacy, disease recurrence and immunogenicity trial among Sh infected schoolchildren from the ShxSb and ShxSm hybrid endemic SRB receiving two-dose PZQ pre-treatment, three-dose immunization, and a single-dose PZQ treatment prior to a final vaccine booster dose . rSh28GST+Alhydrogel proved its safety, strong, long-lasting immunogenicity, and anti-worm fecundity with inhibited egg viability despite the fact that the primary endpoint of significant delay in schistosomiasis recurrence was not reached in the trial .
Of interest related to the ShxSm hybrid type could be the potential of the Smp80-GLA-SE/SchistoShield® vaccine candidate to confer robust, balanced Th1/Th2 cross-species prophylactic and therapeutic protection against Sh in addition to Sj as demonstrated in rodents and baboons . This observation could be due to 95% and 84% amino acid homology among calpain of Sh and Sj with Sm, respectively. Likewise, an ongoing phase 1 dose-escalation, safety and immunogenicity Sm-TSP-2/Sm-TSP-2Al® trial coupled with a subsequent 2b Sm-TSP-2/Sm-TSP-2Al® trial among Sm and Sh exposed healthy male and female Ugandan adults receiving three-dose immunization could reveal promising cross-species protective effects depending on the level of inter- and/or intra-species polymorphism of the TSP-2 EC2 domain .
4. ConclusionsA vaccine as the current candidate in advanced to pre-clinical and clinical phases with cross-species protective potential is needed to complement preventive measures, and protect long-term against transmission, infection, and disease recurrence and sequelae. Despite the strong evidence of naturally occurring schistosomal hybrids of large functional and structural diversity, its potential impact on current vaccine candidates is yet unclear and requires further research. Vaccine targets exposed at the schistosome tegumental surface should not evolve rapidly leading to sequence heterogenicity in natural parasite populations, and rendering its use as a vaccine candidate ineffective, but rather highly conserved. Additionally, natural history studies seem of particular importance in areas with known endemicity for hybrid schistosomes that are targeted for clinical trials.
The entry is from 10.3390/microorganisms9071465
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