- About this Journal ·
- Abstracting and Indexing ·
- Advance Access ·
- Aims and Scope ·
- Article Processing Charges ·
- Articles in Press ·
- Author Guidelines ·
- Bibliographic Information ·
- Citations to this Journal ·
- Contact Information ·
- Editorial Board ·
- Editorial Workflow ·
- Free eTOC Alerts ·
- Publication Ethics ·
- Reviewers Acknowledgment ·
- Submit a Manuscript ·
- Subscription Information ·
- Table of Contents
Journal of Parasitology Research
Volume 2012 (2012), Article ID 743920, 6 pages
Interaction of Schistosoma mansoni Sporocysts and Hemocytes of Biomphalaria
1Departamento de Parasitologia, ICB-UFMG, Avenida Antônio Carlos 6627, 312170-901 Belo Horizonte, MG, Brazil
2Laboratório de Esquistossomose, Centro de Pesquisa René Rachou/FIOCRUZ, Avenida Augusto de Lima 1715, 30190-002 Belo Horizonte, MG, Brazil
3Laboratório de Parasitologia Básica, ICB-UNIFAL, Rua Gabriel Monteiro da Silva 700, 37130-000 Alfenas, MG, Brazil
Received 16 March 2012; Accepted 18 May 2012
Academic Editor: John Kusel
Copyright © 2012 D. Negrão-Corrêa et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Human infection by Schistosoma mansoni affects more than 100 million people worldwide, most often in populations of developing countries of Africa, Asia, and Latin America. The transmission of S. mansoni in human populations depends on the presence of some species of Biomphalaria that act as an intermediate host. The compatibility between S. mansoni and its intermediate host is influenced by behavioral, physiological, and genetical factors of the mollusc and the parasite. The susceptibility level of the mollusc has been attributed to the capacity of internal defense system (IDS)—hemocytes and soluble components of the hemolymph—to recognize and destroy the parasite, and this will be the center of interest of this paper. The schistosome-resistant Biomphalaria can be an alternative strategy for the control of schistosomiasis.
Schistosomiasis is an important health problem that affects over 200 million people worldwide. Among the schistosome species that infect humans, Schistosoma mansoni is the most prevalent species causing intestinal and hepatic schistosomiasis in more than 100 million people living mainly in sub-Saharan Africa, the Caribbean, and South America, including Brazil [1, 2]. Although campaigns for schistosomiasis control based on chemotherapy have reduced the morbidity and prevalence of this disease, transmission continues in almost all the areas in which interventions has been attempted. The transmission of S. mansoni in human populations has been associated with environmental and socioeconomic conditions, but the presence of susceptible intermediate hosts, consisting of some species of Biomphalaria, is obligatory. In Brazil, out of the eleven species Biomphalaria , only three were found naturally infected by S. mansoni: B. glabrata, B. tenagophila, and B. straminea .
The development of S. mansoni inside the intermediate host starts immediately after the active penetration of the snail by the miracidium, a swimming ciliated larva, through the exposed snail tegument. After penetration, the parasite undergoes morphological and physiological changes, being transformed into primary sporocyst (or mother sporocyst) that remains in the fibromuscular tissue of the host’s cephalopodal region, near the penetration site. After 2-3 weeks, primary sporocysts generate secondary ones (or daughter sporocysts), which migrate from the cephalopodal musculature to the digestive glands or hepatopancreas of the mollusc, where their germinative cells can generate the cercariae [5–7]. The susceptibility level of different Biomphalaria species or strains to infection with the same lineage of S. mansoni can be very diverse, and it is a determinant of vectorial competence.
The compatibility between S. mansoni and its intermediate host is influenced by behavioral and physiological factors of the mollusc. However, the susceptibility level of Biomphalaria to S. mansoni is also determined by the genetic differences of the molluscs, as well as by the genetic constitution of Schistosoma [8, 9]. Newton [10, 11] demonstrated that the susceptibility of B. glabrata snail to S. mansoni depends largely upon genetic factors. Later, these results were corroborated by Richards , who demonstrated that the resistance character, acquired at the maturity phase, is determined by a single dominant gene with mendelian inheritance. The genetic dominance of the resistance character was also confirmed in crossbreeding with the susceptible and resistant strain of B. tenagophila [13, 14]. One of the factors that influence susceptibility, and that may be genetically determined, is the activity of the snail internal defense system (IDS).
The Biomphalaria IDS is composed of soluble components of hemolymph and circulating cells, termed hemocytes, which work in association during the snail responses against infectious agents . In snails, circulating hemocytes, especially the phagocytic cell population, are the principal line of cellular defense involved in destruction of S. mansoni larvae inside the intermediate host [16–23]. However, there is experimental evidence that soluble elements of the hemolymph participate in the protective mechanism against pathogens in many invertebrates [24–27]. Soluble components of the hemolymph can interact directly with pathogenic agents producing toxic substances or lytic peptides, or indirectly through mediator molecules for recognition of the pathogen or hemocyte activators [22, 28–32]. In Biomphalaria, hemocytes circulating in hemolymph or fixed in tissues are mainly produced by a well-defined region located between the pericardium and the posterior epithelium of the mantle cavity, called the amebocyte producing organ (APO) . However, there is some evidence [34–37] that B. glabrata hemocytes may have multicentric origin and sites with proliferation of hemocytes were detected also at the saccular portion of the renal tubules and in the ventricular cavity of the heart.
The existence of a cellular defense mechanism deployed by molluscs against trematode infection was initially suggested by the finding of histological reactions around parasite sporocysts . Histopathological analysis of S. mansoni-infected Biomphalaria showed that hemocyte infiltration around parasite larvae was faster and stronger in snail strains that are more resistant to parasite infection [23, 38]. The confirmation of hemocyte participation in S. mansoni-sporocyst control was provided by experiments that transferred the APO from resistant to susceptible snail strains. In these experiments the APO recipient snails were able to control S. mansoni infection better than the respective controls [39, 40].
The effector mechanisms by which hemocytes are able to kill trematode larvae are partially dependent on the capability of these cells to recognize sporocyst tegument molecules, leading to parasite encapsulation and cellular activation, that result in production of highly toxic metabolites of oxygen and nitrogen associated with parasite killing [41–45]. In this context, a better knowledge of the interactions between the parasite tegument and snail hemocytes is essential for understanding the snail susceptibility to S. mansoni infection. This is needed in order to propose new strategies for parasite transmission control. During the last few years, our research group has used the experimental model of S. mansoni infection in B. tenagophila of Taim strain to explore this interaction and the results are discussed below.
2. Schistosoma mansoni Infection in Biomphalaria tenagophila of Taim Strain
Biomphalaria tenagophila is the second major intermediate host of S. mansoni in Brazil. Snails of this species are well distributed through the southeast and south states of Brazil, from Bahia to Rio Grande do Sul, being responsible for disease transmission in the state of São Paulo and for several disease foci in the states of Santa Catarina, Minas Gerais, Rio de Janeiro, and Rio Grande do Sul [4, 46, 47]. Besides Brazil, B. tenagophila also occurs in Argentina, Peru, Bolivia, Paraguay, and Uruguay . The susceptibility levels of B. tenagophila collected from different geographic areas to infection with the same lineage of S. mansoni are diverse. As far as B. tenagophila is concerned, the geographic lineage isolated at the biological reservoir in Taim (Rio Grande do Sul, Brazil), designated as Taim strain, is absolutely resistant to S. mansoni [13, 48, 49], and the resistance of this B. tenagophila lineage has been explored in our laboratory, where we study the possible mechanisms of the parasite’s destruction. Experimental infections in B. tenagophila Taim have shown that S. mansoni miracidia are able to penetrate this snail strain; however the parasites induce an intense cellular infiltration in the infection site leading to parasite destruction within a few hours of infection , suggesting an important participation of the IDS on determination of resistance to S. mansoni in B. tenagophila Taim. The importance of hemocytes in the parasite control was confirmed by experiments that transferred the hematopoietic organ (APO) from snail of Taim strain to B. tenagophila susceptible to S. mansoni infection. The transference resulted in an absolute resistance against the challenge with S. mansoni in receptor snail whose APO transplant was successful .
The process of destruction of S. mansoni larvae by hemocytes starts with the recognition and encapsulation of the newly penetrated sporocyst. The tegument of S. mansoni transforming miracidium is an important interface for molecular communication between the parasite and Biomphalaria . In this context, the first step in the activation of this defense mechanism is the recognition of the parasite presence by hemocytes. The tegument of S. mansoni sporocyst is composed of highly glycosylated [50–52] molecules that bind to soluble proteins of B. glabrata hemolymph in a carbohydrate-dependent manner . Furthermore, it was demonstrated that excretory-secretory glycoproteins from S. mansoni sporocysts also bind to hemocytes via carbohydrate binding receptors . Therefore, lectin-carbohydrate binding could mediate the association of hemocytes with the trematode tegument [15, 44, 53], and consequently it could be a determinant factor of Biomphalaria susceptibility to S. mansoni infection.
To better understand the interaction of hemocytes with parasite larvae, we used the in vitro assay first developed by Bayne et al. . Using this procedure we tested the effect of purified circulating hemocytes plus soluble hemolymph from different Biomphalaria species or strain on the axenically transformed primary or secondary sporocysts of S. mansoni.
The data clearly showed that addition of purified hemocytes from resistant snail strains, such as B. tenagophila Taim, into culture with primary sporocysts resulted in higher levels of parasite mortality compared to sporocysts cultured with hemocytes from susceptible snail strains, such as B. tenagophila Cabo Frio . Moreover, in primary sporocyst cultures containing hemocytes from B. tenagophila Cabo Frio, the addition of cell-free hemolymph from B. tenagophila Taim resulted in increase of hemocyte binding to parasite tegument and higher mortality rates . Therefore, we demonstrated that high levels of sporocyst mortality were associated with higher number of hemocytes bound to parasite tegument leading to parasite encapsulation [32, 54], experimentally confirming that the ability of hemocytes to recognize the primary sporocyst is related to the resistance of B. tenagophila Taim.
Finally, we investigated if lectin-carbohydrate binding could mediate the association of hemocytes from B. tenagophila Taim with S. mansoni primary sporocysts. Previous work  with S. mansoni infection in B. tenagophila Taim showed that most of the circulating hemocytes recovered from B. tenagophila Taim, but not from B. glabrata BH or B. tenagophila Cabo Frio that are susceptible to S. mansoni infection, were intensively labeled by FITC-conjugated PNA and WGA lectins, and these labeled cells almost disappeared from the circulation during the first few hours after S. mansoni infection. Based on these data we tested, in vitro, the participation of N-acetyl-D-glucosamine carbohydrate moieties on the adhesion and destruction of S. mansoni sporocysts by hemocytes of B. tenagophila Taim. Similarly to the previous data, cultures containing hemocytes plus hemolymph from B. tenagophila Taim encapsulated and destroyed over 30% of the S. mansoni sporocysts in culture. Interestingly, the addition of N-acetyl-D-glucosamine to culture medium, but not mannose, resulted in significant inhibition of cellular adhesion to the parasite tegument and reduction of parasite mortality to 5% . In conclusion, the data indicate that N-acetyl-D-glucosamine moieties influence the recognition of schistosome primary sporocysts by hemocytes of B. tenagophila Taim and implies the mechanism is a determinant of snail resistance against S. mansoni infection.
According to Lodes and Yoshino ; the general pattern of synthesis and release of protein by primary and secondary sporocysts in culture is quite different, showing that the two sporocyst stages are metabolically different. The study of gene expression profiles of S. mansoni daughter sporocysts identified different stage-specific genes, several of which are related to adaptation and development of the parasite in the host [56, 57]. The in vitro interaction of axenically transformed S. mansoni primary sporocysts or secondary sporocysts obtained from infected snails with IDS components of B. glabrata (susceptible) and B. tenagophila Taim (resistant) revealed that the secondary sporocysts are less affected by the IDS, mainly of the resistant snail. Secondary sporocysts had fewer cells adhered to the surface, lower mortality, and less surface damage. These results suggest higher resistance of secondary sporocysts to the effector mechanisms of Biomphalaria when compared to the primary sporocyst. However, the secondary sporocysts were unable to grow when inoculated into B. tenagophila Taim but were able to develop into B. glabrata .
Many authors have found that sporocysts can interfere with snail host reproductive physiology and alter other aspects of the parasite-host interaction, secreting molecules (excretory/secretory products (ESP)), adsorbing Biomphalaria antigens when cultivated in the presence of snail molecules, and synthesizing molecules similar to host molecules even in the absence of Biomphalaria components [55, 59–65]. Recently, experiments with molecular and biochemistry approaches using ESP or sporocysts and hemocytes from schistosome-susceptible and schistosome-resistant B. glabrata demonstrated that the parasite is able to interfere with extracellular signal-regulated kinase (ERK) pathway in susceptible B. glabrata [66–68]. Moreover, resistant B. glabrata presented differential expression of genes potentially associated with the snail IDS after infection with S. mansoni when compared with susceptible strain .
The hemocytes from resistant Biomphalaria species can recognize, encapsulate, and destroy the sporocysts soon after S. mansoni invasion. On the other hand, the ability of the parasite to avoid or disrupt the immune response of the host is fundamental to the establishment of parasite-host compatibility . Similar molecules have been found in S. mansoni and Biomphalaria, suggesting an evolutionary convergence of molecular expression between parasite and snail host [8, 59, 70–72]. This similarity is important for the escape process of the parasite: molecular mimicry [72–74]. According to Salzet et al. , this mechanism can prevent the recognition of the parasite by the host IDS.
These data help us to understand why the snails defense in particular its destruction of primary sporocysts, occurs in the first hours after miracidia penetration. Furthermore, van Die and Cummings  and Lehr et al.  have suggested that glycans play a role in the parasite molecular mimicry process. Although the evolutionary advantages of this adaptive process for the parasite are well understood, it is not known how this process interferes with schistosomiasis  or whether this mechanism could interfere with the snail’s resistance mechanisms. Thus, more experiments using daughter sporocysts must be performed to clarify aspects involved with molecular mimicry in the S. mansoni/Biomphalaria (susceptible and resistant) interaction.
This work was supported by PRONEX (Project no. 12055, Edit. 020/06, Process no. 516/07), FAPEMIG and CNPq, Brazil. The authors would like to thank José Carlos Reis and Selma Fernandes de Souza of the Schistosomiasis Research Group, Institute of Biological Sciences, Federal University of Minas Gerais, for technical support in the experiments.
- B. Gryseels, K. Polman, J. Clerinx, and L. Kestens, “Human schistosomiasis,” The Lancet, vol. 368, no. 9541, pp. 1106–1118, 2006.
- P. J. Hotez, J. M. Bethony, S. C. Oliveira, P. J. Brindley, and A. Loukas, “Multivalent anthelminthic vaccine to prevent hookworm and schistosomiasis,” Expert Review of Vaccines, vol. 7, no. 6, pp. 745–752, 2008.
- T. M. Teodoro, L. K. Janotti-Passos, O. D. S. Carvalho, and R. L. Caldeira, “Occurrence of Biomphalaria cousini (Mollusca: Gastropoda) in Brazil and its susceptibility to Schistosoma mansoni (Platyhelminths: Trematoda),” Molecular Phylogenetics and Evolution, vol. 57, no. 1, pp. 144–151, 2010.
- W. L. Paraense, “The schistosome vectors in the Americas,” Memorias do Instituto Oswaldo Cruz, vol. 96, pp. 7–16, 2001.
- J. F. Maldonado and J. Acosta-Matienzo, “The development of Schistosoma mansoni in the snail intermediate host, Australorbis glabratus,” The Puerto Rico Journal of Public Health Tropical Medicine, vol. 22, pp. 331–373, 1947.
- C. T. Pan, “Studies on the host-parasite relationship between Schistosoma mansoni and the snail Australorbis glabratus,” American Journal of Tropical Medicine and Hygiene, vol. 14, no. 6, pp. 931–976, 1965.
- L. H. Pereira, T. E. Valadares, M. L. da Cunha, and M. C. R. Correa, “Recovery of young daughter sporocysts from snails infected with Schistosoma mansoni,” Transactions of the Royal Society of Tropical Medicine and Hygiene, vol. 78, no. 4, p. 563, 1984.
- P. F. Basch, “Intermediate host specificity in Schistosoma mansoni,” Experimental Parasitology, vol. 39, no. 1, pp. 150–169, 1976.
- C. M. Adema, L. A. Hertel, R. D. Miller, and E. S. Loker, “A family of fibrinogen-related proteins that precipitates parasite-derived molecules is produced by an invertebrate after infection,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 16, pp. 8691–8696, 1997.
- W. L. Newton, “The comparative tissue reaction of two strains of Australorbis glabratus to infection with Schistosoma mansoni,” The Journal of Parasitology, vol. 38, no. 4, pp. 362–366, 1952.
- W. L. Newton, “The inheritance of susceptibility to infection with Schistosoma mansoni in Australorbis glabratus,” Experimental Parasitology, vol. 2, no. 3, pp. 242–257, 1953.
- C. S. Richards, “Genetics of a molluscan vector of schistosomiasis,” Nature, vol. 227, no. 5260, pp. 806–810, 1970.
- M. B. L. Dos Santos, J. R. Freitas, M. C. R. Correia, and P. M. Z. Coelho, “Susceptibility of Biomphalaria tenagophila hybrids to Schistosoma mansoni: crossing between strains from Taim (RS), Cabo Frio (RJ), and Belo Horizonte (MG), Brasil,” Revista do Instituto de Medicina Tropical de Sao Paulo, vol. 21, no. 6, pp. 281–286, 1979.
- F. M. Rosa, A. L. B. Godard, V. Azevedo, and P. M. Z. Coelho, “Biomphalaria tenagophila: dominant character of the resistance to Schistosoma mansoni in descendants of crossbreedings between resistant (Taim, RS) and susceptible (Joinville, SC) strains,” Memorias do Instituto Oswaldo Cruz, vol. 100, no. 1, pp. 19–23, 2005.
- W. P. W. Van der Knaap and E. S. Loker, “Immune mechanisms in trematode-snail interactions,” Parasitology Today, vol. 6, no. 6, pp. 175–182, 1990.
- C. J. Bayne, P. M. Buckley, and P. C. DeWan, “Macrophagelike hemocytes of resistant Biomphalaria glabrata are cytotoxic for sporocysts of Schistosoma mansoni in vitro,” Journal of Parasitology, vol. 66, no. 3, pp. 413–419, 1980.
- C. J. Bayne, P. M. Buckley, and P. C. DeWan, “Schistosoma mansoni: cytotoxicity of hemocytes from susceptible snail hosts for sporocysts in plasma from resistant Biomphalaria glabrata,” Experimental Parasitology, vol. 50, no. 3, pp. 409–416, 1980.
- S. Noda and E. S. Loker, “Phagocytic activity of hemocytes of M-line Biomphalaria glabrata snails: effect of exposure to the trematode Echinostoma paraensei,” Journal of Parasitology, vol. 75, no. 2, pp. 261–269, 1989.
- U. Zelck and W. Becker, “Lectin binding to cells of Schistosoma mansoni sporocysts and surrounding Biomphalaria glabrata tissue,” Journal of Invertebrate Pathology, vol. 55, no. 1, pp. 93–99, 1990.
- E. Ottaviani, “Immunorecognition in the gastropod molluscs with particular reference to the freshwater snail Planorbius corneus (L.) (Gastropoda, Pulmonata),” Bolletino di zoologia, vol. 59, pp. 129–139, 1992.
- C. M. Adema, E. C. van Deutekom-Mulder, K. P. W. van der, and T. Sminia, “Schistosomicidal activities of Lymnaea stagnalis haemocytes: the role of oxygen radicals,” Parasitology, vol. 109, no. 4, pp. 479–485, 1994.
- K. K. Sapp and E. S. Loker, “A comparative study of mechanisms underlying digenean-snail specificity: in vitro interactions between hemocytes and digenean larvae,” Journal of Parasitology, vol. 86, no. 5, pp. 1020–1029, 2000.
- D. Negrão-Corrêa, C. A. J. Pereira, F. M. Rosa, R. L. Martins-Souza, Z. A. Andrade, and P. M. Z. Coelho, “Molluscan response to parasite, Biomphalaria and Schistosoma mansoni interaction,” Invertebrate Survival Journal, vol. 4, pp. 101–111, 2007.
- K. M. Lee, K. Y. Lee, H. W. Choi et al., “Activated phenoloxidase from Tenebrio molitor larvae enhances the synthesis of melanin by using a vitellogenin-like protein in the presence of dopamine,” European Journal of Biochemistry, vol. 267, no. 12, pp. 3695–3703, 2000.
- S. Blandin, S. H. Shiao, L. F. Moita et al., “Complement-like protein TEP1 is a determinant of vectorial capacity in the malaria vector Anopheles gambiae,” Cell, vol. 116, no. 5, pp. 661–670, 2004.
- B. Lemaitre, E. Nicolas, L. Michaut, J. M. Reichhart, and J. A. Hoffmann, “The dorsoventral regulatory gene cassette spatzle/Toll/Cactus controls the potent antifungal response in Drosophila adults,” Cell, vol. 86, no. 6, pp. 973–983, 1996.
- C. A. J. Pereira, R. L. Martins-Souza, P. M. Z. Coelho, W. S. Lima, and D. Negrão-Corrêa, “Effect of Angiostrongylus vasorum infection on Biomphalaria tenagophila susceptibility to Schistosoma mansoni,” Acta Tropica, vol. 98, no. 3, pp. 224–233, 2006.
- A. W. Bernheimer and B. Rudy, “Interactions between membranes and cytolytic peptides,” Biochimica et Biophysica Acta, vol. 864, no. 1, pp. 123–141, 1986.
- F. S. M. Noronha, F. J. Ramalho-Pinto, and M. F. Horta, “Cytolytic activity in the genus Leishmania: involvement of a putative pore-forming protein,” Infection and Immunity, vol. 64, no. 10, pp. 3975–3982, 1996.
- N. Jiang, N. S. Tan, B. Ho, and J. L. Ding, “Respiratory protein-generated reactive oxygen species as an antimicrobial strategy,” Nature Immunology, vol. 8, no. 10, pp. 1114–1122, 2007.
- R. L. Martins-Souza, C. A. J. Pereira, O. A. Martins Filho, P. M. Z. Coelho, A. Corrêa, and D. Negrão-Corrêa, “Differential lectin labelling of circulating hemocytes from Biomphalaria glabrata and Biomphalaria tenagophila resistant or susceptible to Schistosoma mansoni infection,” Memorias do Instituto Oswaldo Cruz, vol. 101, no. 1, pp. 185–192, 2006.
- R. L. Martins-Souza, C. A. Pereira, L. Rodrigues et al., “Participation of N-acetyl-D-glucosamine carbohydrate moieties in the recognition of Schistosoma mansoni sporocysts by haemocytes of Biomphalaria tenagophila,” Memórias do Instituto Oswaldo Cruz, vol. 106, pp. 884–891, 2011.
- J. K. Lie, D. Heyneman, and K. H. Jeong, “Studies on resistance in snails. 4. Induction of ventricular capsules and changes in the amebocyte-producing organ during sensitization of Biomphalaria glabrata snails,” Journal of Parasitology, vol. 62, no. 2, pp. 286–291, 1976.
- M. Matricon-Gondran, “The site of ultrafiltration in the kidney sac of the pulmonate gastropod Biomphalaria glabrata,” Tissue and Cell, vol. 22, no. 6, pp. 911–923, 1990.
- J. T. Sullivan, S. S. Pikios, and A. O. Alonzo, “Mitotic responses to extracts of miracidia and cercariae of Schistosoma mansoni in the amebocyte-producing organ of the snail intermediate host Biomphalaria glabrata,” Journal of Parasitology, vol. 90, no. 1, pp. 92–96, 2004.
- J. T. Sullivan and L. Castro, “Mitotic arrest and toxicity in Biomphalaria glabrata (Mollusca: Pulmonata) exposed to colchicine,” Journal of Invertebrate Pathology, vol. 90, no. 1, pp. 32–38, 2005.
- S. Souza and Z. A. Andrade, “On the origin of the Biomphalaria glabrata hemocytes,” Memorias do Instituto Oswaldo Cruz, vol. 101, no. 1, pp. 213–218, 2006.
- C. P. Souza, C. C. Borges, A. G. Santana, and Z. A. Andrade, “Comparative Histopathology of Biomphalaria glabrata, B. tenagophila and B. straminea with vriable degrees of resistance to Schistosoma mansoni Miracidia,” Memorias do Instituto Oswaldo Cruz, vol. 92, no. 4, pp. 517–522, 1997.
- J. T. Sullivan and J. V. Spence, “Transfer of resistance to Schistosoma mansoni in Biomphalaria glabrata by allografts of amoebocyte-producing organ,” Journal of Parasitology, vol. 80, no. 3, pp. 449–453, 1994.
- L. Barbosa, R. L. Caldeira, O. S. Carvalho, T. H. D. A. Vidigal, L. K. Jannotti-Passos, and P. M. Z. Coelho, “Resistance to Schistosoma mansoni by transplantation of APO Biomphalaria tenagophila,” Parasite Immunology, vol. 28, no. 5, pp. 209–212, 2006.
- U. K. Hahn, R. C. Bender, and C. J. Bayne, “Production of reactive oxygen species by hemocytes of Biomphalaria glabrata: carbohydrate-specific stimulation,” Developmental and Comparative Immunology, vol. 24, no. 6-7, pp. 531–541, 2000.
- U. K. Hahn, R. C. Bender, and C. J. Bayne, “Involvement of nitric oxide in killing of Schistosoma mansoni sporocysts by hemocytes from resistant Biomphalaria glabrata,” Journal of Parasitology, vol. 87, no. 4, pp. 778–785, 2001.
- R. C. Bender, E. J. Broderick, C. P. Goodall, and C. J. Bayne, “Respiratory burst of Biomphalaria glabrata hemocytes: Schistosoma mansoni-resistant snails produce more extracellular H2O2 than susceptible snails,” Journal of Parasitology, vol. 91, no. 2, pp. 275–279, 2005.
- C. J. Bayne, “Successful parasitism of vector snail Biomphalaria glabrata by the human blood fluke (trematode) Schistosoma mansoni: a 2009 assessment,” Molecular and Biochemical Parasitology, vol. 165, no. 1, pp. 8–18, 2009.
- Y. Moné, A. C. Ribou, C. Cosseau et al., “An example of molecular co-evolution: reactive oxygen species (ROS) and ROS scavenger levels in Schistosoma mansoni/Biomphalaria glabrata interactions,” International Journal for Parasitology, vol. 41, no. 7, pp. 721–730, 2011.
- W. L. Paraense, “Distribuição dos caramujos no Brasil,” in Modernos Conhecimentos Sobre a Esquistossomose Mansônica, Biblioteca da Academia Mineira de Medicina, pp. 117–128, 1986.
- O. S. Carvalho, L. K. Janotti-Passos, and R. L. Caldeira, “Importância epidemiológica e biologia molecular aplicada ao estudo dos moluscos do gênero Biomphalaria,” in Schistosoma mansoni: Esquistossomose uma Visão Multidisciplinar, O. S. Carvalho, P. M. Z. Coelho, and H. F. Lenzi, Eds., pp. 149–160, Fiocruz, 2008.
- M. C. R. Correa, P. M. Z. Coelho, and J. R. Freitas, “Susceptibilidae de linhagens de Biomphalaria tenagophila e Biomphalaria glabrata a duas cepas de Schistosoma mansoni—(LE—Belo Horizonte—MG e SJ—São José dos Campos—SP),” Revista do Instituto de Medicina Tropical de Sao Paulo, vol. 21, no. 2, pp. 72–76, 1979.
- P. M. Z. Coelho, F. M. Rosa, E. Maciel et al., “Transmission control of schistosomiasis mansoni by introduction of a resistant strain of Biomphalaria tenagophila in areas where transmission is maintained by this species,” Acta Tropica, vol. 108, no. 2-3, pp. 245–248, 2008.
- L. A. Johnston and T. P. Yoshino, “Analysis of lectin- and snail plasma-binding glycopeptides associated with the tegumental surface of the primary sporocysts of Schistosoma mansoni,” Parasitology, vol. 112, no. 5, pp. 469–479, 1996.
- T. P. Yoshino, T. C. Cheng, and L. R. Renwrantz, “Lectin and human blood group determinants of Schistosoma mansoni: alteration following in vitro transformation of miracidium to mother sporocyst,” Journal of Parasitology, vol. 63, no. 5, pp. 818–824, 1977.
- R. Uchikawa and E. S. Loker, “Lectin-binding properties of the surfaces of in vitro-transformed Schistosoma mansoni and Echinostoma paraensei sporocysts,” Journal of Parasitology, vol. 77, no. 5, pp. 742–748, 1991.
- L. A. Johnston and T. P. Yoshino, “Larval Schistosoma mansoni excretory-secretory glycoproteins (ESPs) bind to hemocytes of Biomphalaria glabrata (gastropoda) via surface carbohydrate binding receptors,” Journal of Parasitology, vol. 87, no. 4, pp. 786–793, 2001.
- C. A. J. Pereira, R. L. Martins-Souza, A. Corrêa Jr., P. M. Z. Coelho, and D. Negrão-Corrêa, “Participation of cell-free haemolymph of Biomphalaria tenagophila in the defence mechanism against Schistosoma mansoni sporocysts,” Parasite Immunology, vol. 30, no. 11-12, pp. 610–619, 2008.
- M. J. Lodes and T. P. Yoshino, “The effect of schistosome excretory-secretory products on Biomphalaria glabrata hemocyte motility,” Journal of Invertebrate Pathology, vol. 56, no. 1, pp. 75–85, 1990.
- E. R. Jolly, C. S. Chin, S. Miller et al., “Gene expression patterns during adaptation of a helminth parasite to different environmental niches,” Genome Biology, vol. 8, no. 4, article R65, 2007.
- A. S. Taft, J. J. Vermeire, J. Bernier et al., “Transcriptome analysis of Schistosoma mansoni larval development using serial analysis of gene expression (SAGE),” Parasitology, vol. 136, no. 5, pp. 469–485, 2009.
- A. C. A. Mattos, R. L. Martins-Souza, J. R. Kusel, and P. M. Z. Coelho, “Interaction between primary and secondary sporocysts of Schistosoma mansoni and the internal defence system of Biomphalaria resistant and susceptible to the parasite,” Memorias do Instituto Oswaldo Cruz, vol. 106, no. 4, pp. 424–432, 2011.
- T. P. Yoshino and C. J. Bayne, “Mimicry of snail host antigens by miracidia and primary sporocysts of Schistosoma mansoni,” Parasite Immunology, vol. 5, no. 3, pp. 317–328, 1983.
- T. P. Yoshino and M. J. Lodes, “Secretory protein biosynthesis in snail hemocytes: in vitro modulation by larval schistosome excretory-secretory products,” Journal of Parasitology, vol. 74, no. 4, pp. 538–547, 1988.
- A. E. Crews and T. P. Yoshino, “Schistosoma mansoni: effect of infection on reproduction and gonadal growth in Biomphalaria glabrata,” Experimental Parasitology, vol. 68, no. 3, pp. 326–334, 1989.
- A. E. Crews and T. P. Yoshino, “Influence of larval schistosomes on polysaccharide synthesis in albumin glands of Biomphalaria glabrata,” Parasitology, vol. 101, no. 3, pp. 351–359, 1990.
- A. E. Crews-Oyen and T. P. Yoshino, “Schistosoma mansoni: characterization of excretory-secretory polypeptides synthesized in vitro by daughter sporocysts,” Experimental Parasitology, vol. 80, no. 1, pp. 27–35, 1995.
- V. A. Connors and T. P. Yoshino, “In vitro effect of larval Schistosoma mansoni excretory-secretory products on phagocytosis-stimulated superoxide production in hemocytes from Biomphalaria glabrata,” Journal of Parasitology, vol. 76, no. 6, pp. 895–902, 1990.
- S. E. Fryer and C. J. Bayne, “Schistosoma mansoni modulation of phagocytosis im Biomphalaria glabrata,” Journal of Parasitology, vol. 76, no. 1, pp. 45–52, 1990.
- Z. Zahoor, A. J. Davies, R. S. Kirk, D. Rollinson, and A. J. Walker, “Disruption of ERK signalling in Biomphalaria glabrata defence cells by Schistosoma mansoni: implications for parasite survival in the snail host,” Developmental and Comparative Immunology, vol. 32, no. 12, pp. 1561–1571, 2008.
- Z. Zahoor, A. J. Davies, R. S. Kirk, D. Rollinson, and A. J. Walker, “Nitric oxide production by Biomphalaria glabrata haemocytes: effects of Schistosoma mansoni ESPs and regulation through the extracellular signal-regulated kinase pathway,” Parasites and Vectors, vol. 2, no. 1, article 18, 2009.
- Z. Zahoor, A. J. Davies, R. S. Kirk, D. Rollinson, and A. J. Walker, “Larval excretory-secretory products from the parasite Schistosoma mansoni modulate HSP70 protein expression in defence cells of its snail host, Biomphalaria glabrata,” Cell Stress and Chaperones, vol. 15, no. 5, pp. 639–650, 2010.
- A. E. Lockyer, J. Spinks, R. A. Kane et al., “Biomphalaria glabrata transcriptome: cDNA microarray profiling identifies resistant- and susceptible-specific gene expression in haemocytes from snail strains exposed to Schistosoma mansoni,” BMC Genomics, vol. 9, article 634, 2008.
- N. A. Peterson, C. H. Hokke, A. M. Deelder, and T. P. Yoshino, “Glycotope analysis in miracidia and primary sporocysts of Schistosoma mansoni: differential expression during the miracidium-to-sporocyst transformation,” International Journal for Parasitology, vol. 39, no. 12, pp. 1331–1344, 2009.
- I. van Die and R. D. Cummings, “Glycan gimmickry by parasitic helminths: a strategy for modulating the host immune response?” Glycobiology, vol. 20, no. 1, pp. 2–12, 2010.
- T. Lehr, S. Frank, S. Natsuka et al., “N-Glycosylation patterns of hemolymph glycoproteins from Biomphalaria glabrata strains expressing different susceptibility to Schistosoma mansoni infection,” Experimental Parasitology, vol. 126, no. 4, pp. 592–602, 2010.
- R. T. Damian, “Molecular mimicry revisited,” Parasitology Today, vol. 3, no. 9, pp. 263–266, 1987.
- T. Lehr, K. Beuerlein, M. J. Doenhoff, C. G. Grevelding, and R. Geyer, “Localization of carbohydrate determinants common to Biomphalaria glabrata as well as to sporocysts and miracidia of Schistosoma mansoni,” Parasitology, vol. 135, no. 8, pp. 931–942, 2008.
- M. Salzet, A. Capron, and G. B. Stefano, “Molecular crosstalk in host-parasite relationships: schistosome- and leech-host interactions,” Parasitology Today, vol. 16, no. 12, pp. 536–540, 2000.