Interaction of Biomphalaria cells in primary cultures with Schistosoma mansoni sporocysts

Biomphalaria snails may display varying levels of susceptibility to Schistosoma mansoni infection. We have been developing an in vitro model to study the interaction between the snail and the parasite, using tissue-derived cell cultures from Biomphalaria.

METHODS:

The digestive gland- and kidney-derived cells from primary cultures of resistant (B. tenagophila Taim) and susceptible (B. tenagophila HM and B. glabrata BH) strains of Biomphalaria were exposed to S. mansoni sporocysts.

RESULTS:

S. mansoni sporocysts were surrounded and encapsulated exclusively by cells derived from the digestive gland (DG) of B. tenagophila Taim. The process was followed by a marked decrease in the number of free sporocysts in the culture medium. The morphological characteristics of DG-derived cells in culture have been described.

CONCLUSIONS:

Cells derived from DG (but not SK) primary cultures of B. tenagophila Taim may participate in S. mansoni sporocyst control.

Keywords:
Biomphalaria tenagophila; Biomphalaria glabrata; Schistosoma mansoni; Digestive gland; Saccular kidney; Primary cell culture

Authorship

Aristeu Silva-Neto

Fundação Oswaldo Cruz, Instituto René Rachou, Belo Horizonte, MG, Brasil.Fundação Oswaldo CruzBrasilBelo Horizonte, MG, BrasilFundação Oswaldo Cruz, Instituto René Rachou, Belo Horizonte, MG, Brasil.

Fundação Ezequiel Dias, Diretoria de Pesquisa e Desenvolvimento, Belo Horizonte, MG, Brasil.Fundação Ezequiel DiasBrasilBelo Horizonte, MG, BrasilFundação Ezequiel Dias, Diretoria de Pesquisa e Desenvolvimento, Belo Horizonte, MG, Brasil.

* A Silva-Neto and CO Fonseca equally contributed to the present study

Cristhiane Oliveira da Fonseca

* A Silva-Neto and CO Fonseca equally contributed to the present study

Luciana Maria Silva

Paulo Marcos Zech Coelho

Consuelo Latorre Fortes-Dias

https://orcid.org/0000-0002-4494-5108

Corresponding author: Dra. Consuelo Latorre Fortes-Dias. e-mail:consuelo.latorre@funed.mg.gov.br

*
A Silva-Neto and CO Fonseca equally contributed to the present study

Authors’ contribution: ASN: study design, data acquisition, data interpretation, literature review and article drafting. COF: data acquisition, data interpretation, literature review and article drafting. LMS: supervision of data acquisition and interpretation, project funding. PMZC: study concept, supervision of data acquisition and interpretation, literature review, project funding. CLFD: study concept, supervision of data acquisition and interpretation, literature review, project funding, article drafting and writing. All authors have read and approved the final version of the manuscript.

Conflicts of Interest: The author(s) declare(s) no conflicts of interest.

SCIMAGO INSTITUTIONS RANKINGS

Figures

Figures (5)

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FIGURE 1:
Dissected regions of B. tenagophila Taim (fresh snail) for explant preparation. A. Digestive gland (DG). B. Saccular portion of kidney (SK).

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FIGURE 2:
Photomicrographs of tissue-derived cells of the digestive gland (DG) and saccular portion of kidney (SK) from B. tenagophila Taim (BtT) and B. tenagophila Herivelton Martins (BtHM) after challenge with S. mansoni sporocysts from LE or SJ strain (indicated on the right side). Time after challenge is indicated on top.

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FIGURE 3:
Timeline of the challenge of tissue-derived (DG: digestive gland; SK: saccular portion of kidney) cell cultures from Biomphalaria with S. mansoni sporocysts from the LE strain. Tissue origin: DGBtT, Digestive gland of B. tenagophila Taim; SKBtT, saccular portion of kidney of B. tenagophila Taim; DGBg, Digestive gland of B. glabrata; SKBg, saccular portion of kidney of B. glabrata. Each point represents a replicate, i.e., sporocyst counting per cell culture well prepared from a pooled sample of the respective tissues excised from 10-20 Biomphalaria specimens. Horizontal bars represent median and interquartile ranges for each group of data.

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FIGURE 4:
DG-derived cells from B. tenagophila Taim in primary culture. A: General view of the culture. A wide diversity of cells with different sizes and morphologies spontaneously detached from the tissue explant and migrated into the culture medium. Most of them are rounded shape, with eccentric nucleus and granulated cytoplasm. Cells resembling type I (marked by single head) and type II (marked by double head) cell populations from previous APO-derived culture were observed at minor amounts. B-E: Detailed view of some isolated cells from the culture. B: Rounded cell with fully granulated cytoplasm. C: Rounded cell with clustered granules adjacent to eccentric nucleus (n). D: Rounded cell with large, eccentric nucleus (n) and granulated cytoplasm resembling granulocytes described in Biomphalaria hemolymph (see text). E: Rounded cell with eccentric nucleus (n) and granulated cytoplasm. F-I: Giemsa-stained cells with different ratios of acidophilic (pink color) and basophilic (purple) granules in the cytoplasm.

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FIGURE 5:
Challenge of DG-derived primary culture of B. tenagophila Taim with S. mansoni sporocysts. A: After 4 h of contact. The sporocyst is floating in the medium with no apparent reaction of the cells in culture. B: After 24 h of contact. Sporocyst(s) encapsulated by a tangled network of cells. A number of cell nuclei can be noted as black rounded spots in the network.

FIGURE 1: Dissected regions of B. tenagophila Taim (fresh snail) for explant preparation. A. Digestive gland (DG). B. Saccular portion of kidney (SK).

FIGURE 2: Photomicrographs of tissue-derived cells of the digestive gland (DG) and saccular portion of kidney (SK) from B. tenagophila Taim (BtT) and B. tenagophila Herivelton Martins (BtHM) after challenge with S. mansoni sporocysts from LE or SJ strain (indicated on the right side). Time after challenge is indicated on top.

FIGURE 3: Timeline of the challenge of tissue-derived (DG: digestive gland; SK: saccular portion of kidney) cell cultures from Biomphalaria with S. mansoni sporocysts from the LE strain. Tissue origin: DGBtT, Digestive gland of B. tenagophila Taim; SKBtT, saccular portion of kidney of B. tenagophila Taim; DGBg, Digestive gland of B. glabrata; SKBg, saccular portion of kidney of B. glabrata. Each point represents a replicate, i.e., sporocyst counting per cell culture well prepared from a pooled sample of the respective tissues excised from 10-20 Biomphalaria specimens. Horizontal bars represent median and interquartile ranges for each group of data.

FIGURE 4: DG-derived cells from B. tenagophila Taim in primary culture. A: General view of the culture. A wide diversity of cells with different sizes and morphologies spontaneously detached from the tissue explant and migrated into the culture medium. Most of them are rounded shape, with eccentric nucleus and granulated cytoplasm. Cells resembling type I (marked by single head) and type II (marked by double head) cell populations from previous APO-derived culture were observed at minor amounts. B-E: Detailed view of some isolated cells from the culture. B: Rounded cell with fully granulated cytoplasm. C: Rounded cell with clustered granules adjacent to eccentric nucleus (n). D: Rounded cell with large, eccentric nucleus (n) and granulated cytoplasm resembling granulocytes described in Biomphalaria hemolymph (see text). E: Rounded cell with eccentric nucleus (n) and granulated cytoplasm. F-I: Giemsa-stained cells with different ratios of acidophilic (pink color) and basophilic (purple) granules in the cytoplasm.

FIGURE 5: Challenge of DG-derived primary culture of B. tenagophila Taim with S. mansoni sporocysts. A: After 4 h of contact. The sporocyst is floating in the medium with no apparent reaction of the cells in culture. B: After 24 h of contact. Sporocyst(s) encapsulated by a tangled network of cells. A number of cell nuclei can be noted as black rounded spots in the network.

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Interaction of Biomphalaria cells in primary cultures with Schistosoma mansoni sporocysts

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[1] Corresponding author: Dra. Consuelo Latorre Fortes-Dias. e-mail:consuelo.latorre@funed.mg.gov.br