Murine alloantigen acquisition by schistosomula of Schistosoma mansoni: Further evidence for the presence of K, D, and I region gene products on the tegumental surface

Abstract

Previous studies have demonstrated that shistosomula, recovered from the lungs of Schistosoma mansoni-infected mice, acquire H-2Kk and both Ik and Is gene products. We confirmed and extended those observations by identifying several individual antigenic specificities mapping not only to H-2Kk and I-Ak (Sher, Hall & Vadas 1978), but to H-2Dk, I-Ek, H-2Kb, H-2Db and I-Ab as well. Private H-2 specificities 23 (H-2Kk) and 32 (H-2Dk) were identified on the tegumental surface of schistosomula isolated from C3H/Crgl mice (H-2k). Larvae isolated from C57Bl/10Sn (B10) mice (H-2b) were shown to acquire private specificities 33 and 2, which map to H-2Kb and H-2Db respectively. I region associated (Ia) antigens coded for by genes mapping in the I-A subregion (Ia.2 and 3) and I-E subregion (Ia.7) were also acquired from C3H/Crgl mice. Schistosomula from B10 donors were shown to acquire Ia specificities 3 and 8, which are under I-A subregion control. Evidence that monoclonal antibodies recognize H-2 antigens on the larval surface is also demonstrated.

Dichotomy in the tissue origin of schistosome acquired class I and class II major histocompatibility complex antigens.

“…The results of our experiments indicate that in murine chimeras schistosomes acquire class I (K region) MHC antigens exclusively from a nonhemapoietic tissue source, whereas the class II (I region) antigens expressed by the parasites are of bone marrow origin. Previous studies have suggested that MHC molecule acquisition by schistosomes occurs principally in the lungs since these antigens are most readily detected on parasites recovered from this site (3)(4)(5)(6). For this reason and for the purpose of eliminating MHC antigen acquisition from other tissue sites, the parasites studied in the present experiments were derived from in vitro prepared (mechanical) schistosomula injected by the intravenous route into the lungs rather than by natural percutaneous infection.…”

“…By masking antigenic determinants on the tegument of the organism, these host molecules may allow the parasite to evade vertebrate immune responses (1,2). An important set of molecules acquired by schistosomes during murine infection are class I and class II products of the major histocompatibility complex (MHC) (3)(4)(5). These glycoproteins can be detected on schistosomula and adult worms Schistosoma mansoni during their development in mice (3)(4)(5)(6) and have serologic properties and electrophoretic mobilities indistinguishable from the class I and class II MHC molecules expressed on host cells (7).…”

“…An important set of molecules acquired by schistosomes during murine infection are class I and class II products of the major histocompatibility complex (MHC) (3)(4)(5). These glycoproteins can be detected on schistosomula and adult worms Schistosoma mansoni during their development in mice (3)(4)(5)(6) and have serologic properties and electrophoretic mobilities indistinguishable from the class I and class II MHC molecules expressed on host cells (7). Furthermore, schistosome acquired class I antigens exist in a form recognizable by allogeneic T lymphocytes and able to restrict the recognition of other determinants (haptens, minor histocompatibility antigens) on the parasite surface (8,9).…”

Heterogeneity of class I and class II MHC sequences in Schistosoma mansoni

“…Although MHC genes have been regarded as being specific to vertebrates, MHC antigens have been found on the surfaces of adult worms of Schistosoma mansoni and schistosomula (Sher et al 1978;Gitter and Damian 1982), and the existence of host antigens on schistosomes has been hypothesized to contribute to the ability of these parasites to evade host immune responses. Several hypotheses, including horizontal acquisition and induction as a result of natural selection, have been proposed to explain the mechanisms underlying schistosome-host antigen sharing (Sher et al 1978;Capron et al 1976;Smithers and Terry 1976;Damian 1979Damian , 1987Simpson et al 1983;Howell 1985;Salzet et al 2000), although the induction mechanism has not been clarified.…”

Human erythrocytes adhering to schistosomula of Schistosoma mansoni lyse and fail to transfer membrane components to the parasite.

“…One of the mechanisms of immune evasion may be the acquisition of host antigens so that the parasite becomes a wolf in sheep's clothing (27). Supporting this theory, various host molecules have been found on the parasite, namely, Forssman antigens (7), ABH blood group glycolipids (6,12), murine histocompatibility antigens (9,10,(23)(24)(25), complement and IgG receptors (16,27), and various serum proteins (14,28). Although the presence of these antigens has not been demonstrated to protect against immune recognition, the hypothesis is an attractive one and the methods by which these antigens are acquired merit further study.…”