Original Article

Comparative Functional Study of Thioester-containing Related Proteins in the Recently Sequenced Genome of Biomphalaria glabrata


Background: There is paucity of information on functional relationship and characterization of Biomphalaria glabrata thioester-containing proteins (BgTEP) to other well-annotated homologues. We performed functional characterization studies of BgTEP to homologues in Anopheles gambiae and in disparate invertebrates.

Methods: Genomic sequences of TEPs were retrieved after annotation of the B. glabrata genome. In addition, TEP sequences deposited in NCBI protein database were also retrieved and utilized for sequence analysis. BgTEP relatedness to its other homologues as well as functional domain and protein-protein interaction analysis was performed.

Results: Our analysis resulted in the identification of TEPs in a number of organisms including, B. glabrata, A. gambiae, and Chlamys farreri. In addition, we identified 19 TEP sequences spread across 10 animal species. The B. glabrata genome contains 14190 unannotated proteins after filtration with about 85% of its proteome annotated. The phylogenetics, functional domain and protein-protein interaction analyses suggest an immunological role for BgTEP in B. glabrata.

Conclusion: The predicted role of thioester-containing proteins to be involved in immunological role in B. glabrata may have a strong effect on resistance to infection.

Prentice MA. Schistosomiasis and its in-termediate hosts in the Lesser Antillean Is-lands of the Caribbean. Pan Am J Public Health. 1980; 14(3):258-68.

Lockyer AE, Spinks JN, Walker AJ et al. Biomphalaria glabrata transcriptome: identifi-cation of cell-signalling, transcriptional control and immune-related genes from open reading frame expressed sequence tags (ORESTES). Dev Comp Immunol. 2007; 31(8):763-82.

Mutuku MW, Dweni CK, Mwangi M et al. Field-derived Schistosoma mansoni and Bi-omphalaria pfeifferi in Kenya: a compatible association characterized by lack of strong local adaptation, and presence of some snails able to persistently produce cercariae for over a year. Parasit Vectors. 2014; 7(1):533.

Zoni AC, Catalá L, Ault SK. Schistosomia-sis Prevalence and Intensity of Infection in Latin America and the Caribbean Coun-tries, 1942-2014: A Systematic Review in the Context of a Regional Elimination Goal. PLoS Negl Trop Dis. 2016; 10(3):e0004493.

Colley DG, Bustinduy AL, Secor WE, King CH. Human schistosomiasis. Lancet. 2014; 383(9936):2253-64.

Lai YS, Biedermann P, Ekpo UF et al. Spatial distribution of schistosomiasis and treatment needs in sub-Saharan Africa: a systematic review and geostatistical analy-sis. Lancet Infect Dis. 2015; 15(8):927-40.

Michaud CM, Gordon WS, Reich MR. The global burden of disease due to schis-tosomiasis. Disease Control Priorities Pro-ject Working Paper. 2003; 19.

Bocanegra C, Gallego S, Mendioroz J et al. Epidemiology of schistosomiasis and Usefulness of Indirect Diagnostic Tests in School-Age Children in Cubal, Central Angola. PLoS Negl Trop Dis. 2015; 9(10):e0004055.

Fenwick A, Webster JP, Bosque-Oliva E et al. The schistosomiasis Control Initiative (SCI): rationale, development and imple-mentation from 2002–2008. Parasitol. 2009; 136(13):1719-30.

French MD, Churcher TS, Webster JP et al. Estimation of changes in the force of infection for intestinal and urogenital schistosomiasis in countries with schisto-somiasis control initiative-assisted pro-grammes. Parasit Vectors. 2015; 8(1):1.

de Moraes J. Antischistosomal natural compounds: present challenges for new drug screens. Cur Top in Trop Med. 2012; 333-58

Coeli R, Baba EH, Araujo N, Coelho PM, Oliveira G. Praziquantel treatment decreas-es Schistosoma mansoni genetic diversity in experimental infections. PLoS Negl Trop Dis. 2013; 7(12):e2596.

Fukushige M, Mitchell KM, Bourke CD, Woolhouse ME, Mutapi F. A meta-analysis of experimental studies of attenu-ated Schistosoma mansoni vaccines in the mouse model. Front Immunol. 2015; 6:85.

Lardans V, Dissous C. Snail control strat-egies for reduction of schistosomiasis transmission. Parasit Today. 1998; 14(10):413-7.

King CH, Bertsch D. Historical perspec-tive: snail control to prevent schistosomia-sis. PLoS Negl Trop Dis. 2015; 9(4):e0003657.

Southgate VR. Schistosomiasis in the Sen-egal River Basin: before and after the con-struction of the dams at Diama, Senegal and Manantali, Mali and future prospects. J Helminthol. 1997; 71(02):125-32.

Adenowo AF, Oyinloye BE, Ogunyinka BI, Kappo AP. Impact of human schisto-somiasis in sub-Saharan Africa. Braz J In-fect Dis. 2015; 19(2):196-205.

Kenny NJ, Truchado-García M, Grande C. Deep, multi-stage transcriptome of the schistosomiasis vector Biomphalaria glabrata provides platform for understanding mol-luscan disease-related pathways. BMC In-fect Dis. 2016; 16(1):618.

Coustau C, Gourbal B, Duval D, Yoshino TP, Adema CM, Mitta G. Advances in gastropod immunity from the study of the interaction between the snail Biomphalaria glabrata and its parasites: a review of re-search progress over the last decade. Fish Shellfish Immu. 2015; 46(1):5-16.

Zhang SM, Loker ES, Sullivan JT. Patho-gen-associated molecular patterns activate expression of genes involved in cell prolif-eration, immunity and detoxification in the amebocyte-producing organ of the snail Biomphalaria glabrata. Dev Comp Immunol. 2016; 56:25-36.

Coustau C. Immunity in parasite-vector snails. Med Sci (Paris). 2009; 25(4):399-403.

Hanington PC, Forys MA, Loker ES. A somatically diversified defense factor, FREP3, is a determinant of snail resistance to schistosome infection. PLoS Negl Trop Dis. 2012; 6(3):e1591.

Gorbushin AM, Panchin YV, Iakovleva NV. In search of the origin of FREPs: characterization of Aplysia californica fi-brinogen-related proteins. Dev Comp Immunol. 2010; 34(4):465-73.

Dheilly NM, Duval D, Mouahid G et al. A family of variable immunoglobulin and lec-tin domain containing molecules in the snail Biomphalaria glabrata. Dev Comp Im-munol. 2015; 48(1):234-43.

Hanington PC, Zhang SM. The primary role of fibrinogen-related proteins in in-vertebrates is defense, not coagulation. J Innate Immun. 2010; 3(1):17-27.

Adema CM. Fibrinogen-related proteins (FREPs) in mollusks. In: Pathogen-Host Interactions: Antigenic Variation v. Somat-ic Adaptations 2015 (pp. 111-129). Spring-er International Publishing.

Pinaud S, Portela J, Duval D et al. A shift from cellular to humoral responses con-tributes to innate immune memory in the vector snail Biomphalaria glabrata. PLoS Pathog. 2016; 12(1):e1005361.

Coustau C, Kurtz J, Moret Y. A Novel Mechanism of Immune Memory Unveiled at the Invertebrate–Parasite Interface. Trends Parasitol. 2016; 32(5):353-5.

Humphries J, Harter B. Identification of nuclear factor kappaB (NF-κB) binding motifs in Biomphalaria glabrata. Dev Comp Immunol. 2015; 53(2):366-70.

Galinier R, Portela J, Moné Y. Biompha-lysin, a new β pore-forming toxin involved in Biomphalaria glabrata immune defense against Schistosoma mansoni. PLoS Pathog. 2013; 9(3):e1003216.

Giraldo-Calderón GI, Emrich SJ, Mac-Callum RM. VectorBase: an updated bioin-formatics resource for invertebrate vectors and other organisms related with human diseases. Nucleic Acids Res. 2014:gku1117.

Moné Y, Gourbal B, Duval D, Du Pas-quier L, Kieffer-Jaquinod S, Mitta G. A large repertoire of parasite epitopes matched by a large repertoire of host im-mune receptors in an invertebrate host/parasite model. PLoS Negl Trop Dis. 2010; 4(9):e813.

Deleury E, Dubreuil G, Elangovan N. Specific versus non-specific immune re-sponses in an invertebrate species evi-denced by a comparative de novo se-quencing study. PLoS One. 2012; 7(3):e32512.

Mitta G, Adema CM, Gourbal B, Loker ES, Theron A. Compatibility polymor-phism in snail/schistosome interactions: From field to theory to molecular mecha-nisms. Dev Comp Immunol. 2012; 37(1):1-8.

Levashina EA, Moita LF, Blandin S, Vriend G, Lagueux M, Kafatos FC. Con-served role of a complement-like protein in phagocytosis revealed by dsRNA knockout in cultured cells of the mosquito, Anopheles gambiae. Cell. 2001; 104(5):709-18.

Dinguirard N and Yoshino TP. A Biompha-laria glabrata thioester-containing protein. 2008. (GenBank Accession No: ACL00841.1) Unpublished.

Wu XJ, Humphries JE, Dinguirard N, Chung CY, Yoshino TP. Differentially ex-pressed gene transcripts from LTP (larval transformation protein) treated Biomphalaria glabrata embryonic cell line identified by subtractive hybridization. 2013. (GenBank Accession No: AHH81765.1) Un-published.

Megy K, Emrich SJ, Lawson D. Vector Base: improvements to a bioinformatics resource for invertebrate vector genomics. Nucleic Acids Res. 2012; 40(D1):D729-34.

Kearse M, Moir R, Wilson A. Geneious Basic: an integrated and extendable desk-top software platform for the organization and analysis of sequence data. Bioinfor-matics. 2012; 28(12):1647-9.

Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics re-search. Bioinformatics. 2005; 21(18):3674-6.

Conesa A, Götz S. Blast2GO: A compre-hensive suite for functional analysis in plant genomics. Int J Plant Genomics. 2008; 619832. doi:10.1155/2008/619832.

Götz S, García-Gómez JM, Terol J et al. High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res. 2008; 36(10):3420-35.

Ittner LM, Götz J. Amyloid-β and tau—a toxic pas de deux in Alzheimer's disease. Nat Rev Neurosci. 2011; 12(2):67-72.

Gasteiger E, Hoogland C, Gattiker A, Duvaud SE, Wilkins MR, Appel RD, Bai-roch A. Protein identification and analysis tools on the ExPASy server. Humana Press; 2005.

Petersen SE, Posner MI. The attention system of the human brain: 20 years after. Annu Rev Neurosci. 2012; 35:73.

Emanuelsson O, Nielsen H, Brunak S, Von Heijne G. Predicting subcellular locali-zation of proteins based on their N-terminal amino acid sequence. J Mol Biol. 2000; 300(4):1005-16.

Khachatryan V, Sirunyan AM, Tumasyan A et al. Precise determination of the mass of the Higgs boson and tests of compati-bility of its couplings with the standard model predictions using proton collisions at 7 and 8, text {TeV}. Eur Phys J E. 2015; 75(5):1-50.

Bjellqvist B, Hughes GJ, Pasquali C et al. The focusing positions of polypeptides in immobilized pH gradients can be predict-ed from their amino acid sequences. Elec-trophoresis. 1993; 14(1):1023-31.

Bjellqvist B, Basse B, Olsen E, Celis JE. Reference points for comparisons of two‐dimensional maps of proteins from different human cell types defined in a pH scale where isoelectric points correlate with polypeptide compositions. Electrophore-sis. 1994; 15(1):529-39.

Chazan A. Peptide property calculator. Ev-anston, IL: Northwestern University: http://www. basic. nwu. edu/biotool/ProteinCalc. html. 2002.

IssueVol 13 No 1 (2018) QRcode
SectionOriginal Article(s)
Biomphalaria glabrata Thioester-containing proteins Schistosomiasis

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How to Cite
O. FALADE M, OTARIGHO B. Comparative Functional Study of Thioester-containing Related Proteins in the Recently Sequenced Genome of Biomphalaria glabrata. Iran J Parasitol. 1;13(1):79-88.