Investigation of Defense Response and Immune Priming in Biomphalaria Glabrata and Biomphalaria Straminea, Two Species with Different Susceptibility to Schistosoma Mansoni

Overview

Journal Parasitol Res

Specialty Parasitology

Date 2019 Dec 11

PMID 31820168

Citations 5

Authors

Elverson Soares de Melo

Fabio Andre Brayner

Nairomberg Cavalcanti Portela Junior

Iany Raissa Silva Franca

Luiz Carlos Alves

Affiliations

Soon will be listed here.

Abstract

For many years, the immune response of invertebrates was considered to lack any mechanism of memory. However, the study of their response has shown a kind of acquired immunity, which is not so well understood given the lack of knowledge of the invertebrate defense system. This event can be called "innate immune memory." Recent studies using Biomphalaria glabrata snails have reported this phenomenon, relating it to an increase in humoral products, but no focus was given to hemocyte response or to other species of snails. In this study, we focus on hemocyte dynamics and some humoral factors in the species B. glabrata and B. straminea, the most widespread species in Brazil, sensitized and non-sensitized to the Schistosoma mansoni worm. We report a change in the prevalent hemocyte type after sensitization, through an increase in the proportion of granulocytes, as well as a change in the total number of hemocytes caused by a second exposure to the parasite. We also showed that melanization is not a key factor in Biomphalaria snail defense and varies little after the second exposure event. The data reported in this article confirm the effect of immune priming on these snails and suggest that the increase of humoral products shown in the literature is accompanied by variation in hemocytes after sensitization.

Citing Articles

The Invertebrate Immunocyte: A Complex and Versatile Model for Immunological, Developmental, and Environmental Research.

Sacchi S, Malagoli D, Franchi N Cells. 2025; 13(24.

PMID: 39768196 PMC: 11674123. DOI: 10.3390/cells13242106.

Metagenomic Analysis Reveals Variations in Gut Microbiomes of the -Transmitting Snails and .

Li P, Hong J, Wu M, Yuan Z, Li D, Wu Z Microorganisms. 2023; 11(10).

PMID: 37894077 PMC: 10609589. DOI: 10.3390/microorganisms11102419.

Investigation of Immune Responses in Giant African Snail, , against a Two-Round Lipopolysaccharide Challenge.

Wang X, Tang Y, Li Z, Wu Q, Qiao X, Wan F Int J Mol Sci. 2023; 24(15).

PMID: 37569567 PMC: 10418618. DOI: 10.3390/ijms241512191.

Status Quo and Future Perspectives of Molecular and Genomic Studies on the Genus -The Intermediate Snail Host of .

Au M, Williams G, Hui J Int J Mol Sci. 2023; 24(5).

PMID: 36902324 PMC: 10003693. DOI: 10.3390/ijms24054895.

The Enhanced Immune Protection in Small Abalone Against a Secondary Infection With .

Yao T, Lu J, Bai C, Xie Z, Ye L Front Immunol. 2021; 12:685896.

PMID: 34295333 PMC: 8290317. DOI: 10.3389/fimmu.2021.685896.

References

Yang C, Wang L, Zhang H, Wang L, Huang M, Sun Z . A new fibrinogen-related protein from Argopecten irradians (AiFREP-2) with broad recognition spectrum and bacteria agglutination activity. Fish Shellfish Immunol. 2014; 38(1):221-9. DOI: 10.1016/j.fsi.2014.03.025. View

Zhang T, Qiu L, Sun Z, Wang L, Zhou Z, Liu R . The specifically enhanced cellular immune responses in Pacific oyster (Crassostrea gigas) against secondary challenge with Vibrio splendidus. Dev Comp Immunol. 2014; 45(1):141-50. DOI: 10.1016/j.dci.2014.02.015. View

Araque W, Barrios E, Rodriguez P, Delgado V, Finol H . Ultrastructural study of the in vitro interaction between Biomphalaria glabrata hemocytes and Schistosoma mansoni miracidia. Mem Inst Oswaldo Cruz. 2004; 98(7):905-8. DOI: 10.1590/s0074-02762003000700008. View

Sire C, Rognon A, Theron A . Failure of Schistosoma mansoni to reinfect Biomphalaria glabrata snails: acquired humoral resistance or intra-specific larval antagonism?. Parasitology. 1998; 117 ( Pt 2):117-22. DOI: 10.1017/s0031182098002923. View

Portet A, Galinier R, Pinaud S, Portela J, Nowacki F, Gourbal B . BgTEP: An Antiprotease Involved in Innate Immune Sensing in . Front Immunol. 2018; 9:1206. PMC: 5989330. DOI: 10.3389/fimmu.2018.01206. View

Guillou F, Roger E, Mone Y, Rognon A, Grunau C, Theron A . Excretory-secretory proteome of larval Schistosoma mansoni and Echinostoma caproni, two parasites of Biomphalaria glabrata. Mol Biochem Parasitol. 2007; 155(1):45-56. DOI: 10.1016/j.molbiopara.2007.05.009. View

Martins-Souza R, Pereira C, Coelho P, Martins-Filho O, Negrao-Correa D . Flow cytometry analysis of the circulating haemocytes from Biomphalaria glabrata and Biomphalaria tenagophila following Schistosoma mansoni infection. Parasitology. 2009; 136(1):67-76. DOI: 10.1017/S0031182008005155. View

Hanington P, Lun C, Adema C, Loker E . Time series analysis of the transcriptional responses of Biomphalaria glabrata throughout the course of intramolluscan development of Schistosoma mansoni and Echinostoma paraensei. Int J Parasitol. 2010; 40(7):819-31. PMC: 2866805. DOI: 10.1016/j.ijpara.2009.12.005. View

Portet A, Pinaud S, Tetreau G, Galinier R, Cosseau C, Duval D . Integrated multi-omic analyses in Biomphalaria-Schistosoma dialogue reveal the immunobiological significance of FREP-SmPoMuc interaction. Dev Comp Immunol. 2017; 75:16-27. DOI: 10.1016/j.dci.2017.02.025. View

10.

Sun J, Lan J, Shi X, Yang M, Yang H, Zhao X . A fibrinogen-related protein (FREP) is involved in the antibacterial immunity of Marsupenaeus japonicus. Fish Shellfish Immunol. 2014; 39(2):296-304. DOI: 10.1016/j.fsi.2014.05.005. View

11.

Cerenius L, Lee B, Soderhall K . The proPO-system: pros and cons for its role in invertebrate immunity. Trends Immunol. 2008; 29(6):263-71. DOI: 10.1016/j.it.2008.02.009. View

12.

Souza C, Borges C, Santana A, Andrade Z . Comparative histopathology of Biomphalaria glabrata, B. tenagophila and B. straminea with variable degrees of resistance to Schistosoma mansoni miracidia. Mem Inst Oswaldo Cruz. 1997; 92(4):517-22. DOI: 10.1590/s0074-02761997000400014. View

13.

Cavalcanti M, Filho F, Mendonca A, Duarte G, Barbosa C, De Castro C . Morphological characterization of hemocytes from Biomphalaria glabrata and Biomphalaria straminea. Micron. 2011; 43(2-3):285-91. DOI: 10.1016/j.micron.2011.09.002. View

14.

Accorsi A, Bucci L, de Eguileor M, Ottaviani E, Malagoli D . Comparative analysis of circulating hemocytes of the freshwater snail Pomacea canaliculata. Fish Shellfish Immunol. 2013; 34(5):1260-8. DOI: 10.1016/j.fsi.2013.02.008. View

15.

Bahgat M, Doenhoff M, Kirschfink M, Ruppel A . Serine protease and phenoloxidase activities in hemocytes of Biomphalaria glabrata snails with varying susceptibility to infection with the parasite Schistosoma mansoni. Parasitol Res. 2002; 88(6):489-94. DOI: 10.1007/s00436-002-0595-6. View

16.

Oliveira A, Levada P, Zanotti-Magalhaes E, Magalhaes L, Ribeiro-Paes J . Differences in the number of hemocytes in the snail host Biomphalaria tenagophila, resistant and susceptible to Schistosoma mansoni infection. Genet Mol Res. 2010; 9(4):2436-45. DOI: 10.4238/vol9-4gmr1143. View

17.

Leonard P, Adema C, Zhang S, Loker E . Structure of two FREP genes that combine IgSF and fibrinogen domains, with comments on diversity of the FREP gene family in the snail Biomphalaria glabrata. Gene. 2001; 269(1-2):155-65. DOI: 10.1016/s0378-1119(01)00444-9. View

18.

De Seta L, Magalhaes L, de Carvalho J . [Behavior of hemolymph amebocytes from planorbidae in the presence of Schistosoma mansoni larvae parasitism, after inoculation of Indian ink or fracture of the shell]. Rev Saude Publica. 1996; 30(4):332-40. DOI: 10.1590/s0034-89101996000400006. View

19.

Kurtz J . Memory in the innate and adaptive immune systems. Microbes Infect. 2004; 6(15):1410-7. DOI: 10.1016/j.micinf.2004.10.002. View

20.

Vergote D, Bouchut A, Sautiere P, Roger E, Galinier R, Rognon A . Characterisation of proteins differentially present in the plasma of Biomphalaria glabrata susceptible or resistant to Echinostoma caproni. Int J Parasitol. 2005; 35(2):215-24. DOI: 10.1016/j.ijpara.2004.11.006. View