Schistosomin from the snail Biomphalaria glabrata: Expression studies suggest no involvement in trematode-mediated castration

Molecular and Biochemical Parasitology

Volumn 165, Issue 1, 2009, Pages 79-86

  Zhang, Si Ming ^a   Nian, Hong ^a   Wang, Bo ^a   Loker, Eric S ^a   Adema, Coen M ^a  

^a UNIVERSITY OF NEW MEXICO   (United States)

Author keywords

Biomphalaria glabrata; Echinostoma paraensei; Mollusc; Parasitic castration; Schistosoma mansoni; Schistosomin

Indexed keywords

COMPLEMENTARY DNA; MESSENGER RNA; NEUROPEPTIDE; PEPTIDE; PROTEIN; SCHISTOSOMIN; SIGNAL PEPTIDE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BIOMPHALARIA GLABRATA; CONTROLLED STUDY; ECHINOSTOMA; INFECTION; LYMNAEA; MATURITY; NONHUMAN; NUCLEOTIDE SEQUENCE; ONTOGENY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SCHISTOSOMA MANSONI;

AMINO ACID SEQUENCE; ANIMALS; BASE SEQUENCE; BIOMPHALARIA; BLOTTING, WESTERN; ESCHERICHIA COLI; GENE EXPRESSION REGULATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; MOLECULAR SEQUENCE DATA; ORCHIECTOMY; PEPTIDES; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT; TREMATODA;

BIOMPHALARIA GLABRATA; ECHINOSTOMA PARAENSEI; GASTROPODA; LYMNAEA STAGNALIS; MOLLUSCA; SCHISTOSOMA; SCHISTOSOMA MANSONI; TREMATODA; TRICHOBILHARZIA OCELLATA;

EID: 60649119015     PISSN: 01666851     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molbiopara.2009.01.006     Document Type: Article

References (50)

1. De Jong-Brink M., Bergamin-Sassen M., and Soto M.S. Multiple strategies of schistosomes to meet their requirements in the intermediate snail host. Parasitology 123 (2001) S129-S141
2. Schallig D.H.F.H., Hordijk P.L., Oosthoek P.W., et al. Schistosomin, a peptide present in the hemolymph of Lymnaea stagnalis infected with Trichobilharzia ocellata, is produced only in the snail central nervous system. Parasitol Res 77 (1991) 152-156
3. Hoek R.M., vanKesteren R.E., Smit A.B., et al. Altered gene expression in the host brain caused by a trematode parasite: neuropeptide genes are preferentially affected during parasitosis. Proc Natl Acad Sci USA 94 (1997) 14072-14076
4. Hordijk P.L., De Jong-Brink M., and Termaat A. The neuropeptide schistosomin and hemolymph from parasitized snails induce similar changes in excitability in neuroendocrine cells controlling reproduction and growth in a freshwater snail. Neurosci Lett 36 (1992) 193-197
5. Hordijk P.L., Vanloenhout H., Ebberink R.H.M., et al. Neuropeptide schistosomin inhibits hormonally induced ovulation in the freshwater snail Lymnaea stagnalis. J Exp Zool 259 (1991) 268-271
6. Hordijk P.L., Ebberink R.H.M., De Jong-Brink M., et al. Isolation of schistosomin, a neuropeptide which antagonizes gonadotropic-hormones in a freshwater snail. Eur J Biochem 195 (1991) 131-136
7. De Jong-Brink M., Hoek R.M., Smith A.B., et al. Schistosoma parasites evoke stress responses in their snail host by a cytokine-like factor interfering with neuroendocrine mechanisms. Netherlands J Zool 45 (1995) 113-116
8. De Jong-Brink M., Hordijk P.L., Vergeest D.P., et al. The anti-gonadotropic neuropeptide schistosomin interferes with peripheral and central neuroendocrine mechanisms involved in the regulation of reproduction and growth in the schistosome-infected snail Lymnaea stagnalis. Prog Brain Res 92 (1992) 385-396
9. Steinmann P., Keiser J., Bos R., et al. Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infect Dis 6 (2006) 411-425
10. Cooper L.A., Larson S.E., and Lewis F.A. Male reproductive success of Schistosoma mansoni-infected Biomphalaria glabrata snails. J Parasitol 82 (1996) 428-431
11. Ademo S.A. Modulating the modulators: parasites, neuromodulators and host behavioral change. Brain Behav Evol 60 (2002) 370-377
12. Blair L., and Webster J.P. Dose-dependent schistosome-induce mortality and morbidity risk elevates host reproductive effort. J Evol Biol 20 (2007) 54-61
13. De Jong-Brink M., Saadany M.E.L., and Soto M.S. The occurrence of schistosomin, an antagonist of female gonadotropic-hormones, is a general phenomenon in hemolymph of schistosome-infected freshwater snails. Parasitology 103 (1990) 371-378
14. Raghavan N., Miller A.N., and Gardner M. Comparative gene analysis of Biomphalaria glabrata hemocytes pre- and post-exposure to miracidia of Schistosoma mansoni. Mol Biochem Parasitol 126 (2003) 181-191
15. Vergote D., Bouchut A., Sautiere P.E., et al. Characterisation of proteins differentially present in the plasma of Biomphalaria glabrata susceptible or resistant to Echinostoma caproni. Intl J Parasitol 35 (2005) 215-224
16. Guillou F., Mitta G., and Galinier R. Identification and expression of gene transcripts generated during an anti-parasitic response in Biomphalaria glabrata. Dev Comp Immunol 31 (2007) 657-671
17. Lockyer A.E., Spinks J.N., Walker A.J., et al. Biomphalaria glabrata transcriptome identification of cell-signalling, transcriptional control and immune-related genes from open reading frame expressed sequence tags (ORESTES). Dev Comp Immunol 31 (2007) 763-782
18. Hanelt B., Lun C.M., and Adema C.M. Comparative ORESTES-sampling of transcriptomes of immune-challenged Biomphalaria glabrata snails. J Invertebr Pathol 99 (2008) 192-203
19. Goodall C.P., Bender R.C., and Brooks J.K. Biomphalaria glabrata cytosolic copper/zinc superoxide dismutase (SOD1) gene: association of SOD1 alleles with resistance/susceptibility to Schistosoma mansoni. Mol Biochem Parasitol 147 (2006) 207-210
20. Humphries J.E., and Yoshino T.P. Schistosoma mansoni excretory-secretory products stimulate a p38 signalling pathway in Biomphalaria glabrata embryonic cells. Intl J Parasitol 36 (2006) 37-46
21. Bender R.C., Goodall C.P., Blouin M.S., et al. Variation in expression of Biomphalaria glabrata SOD1: a potential controlling factor in susceptibility/resistance to Schistosomin mansoni. Dev Comp Immunol 31 (2007) 874-878
22. Yoshino T.P., Dinguirard N., Kunert J., et al. Molecular and functional characterization of a tandem-repeat galectin from the freshwater snail Biomphalaria glabrata, intermediate host of the human blood fluke Schistosoma mansoni. Gene 411 (2008) 46-58
23. Zhang S.-M., Adema C.M., Kepler T.B., and Loker E.S. Diversification of Ig genes in an invertebrate. Science 395 (2004) 251-254
24. Zhang S.-M., Zeng Y., and Loker E.S. Characterization of immune genes from the schistosome host snail Biomphalaria glabrata that encode peptidoglycan recognition proteins and gram-negative bacteria binding protein. Immunogenetics 59 (2007) 883-898
25. Zhang S.-M., Nian H., Zeng Y., and DeJong R.J. Fibrinogen-bearing protein genes in the snail Biomphalaria glabrata: characterization of two novel genes and expression studies during ontogenesis and trematode infection. Dev Comp Immunol 32 (2008) 1119-1130
26. Zahoor Z., Davies A.J., Kirk R.S., Rollonson D., and Walker A.J. Disruption of ERK signaling in Biomphalaria glabrata defence cells by Schistosoma mansoni: implications for parasite survival in the snail host. Dev Comp Immunol 32 (2008) 1561-1571
27. Stibbs H.H., Owczarzak A., Bayne C.J., et al. Schistosome sporocyst-killing amebas isolated from Biomphalaria glabrata. J Invertebr Pathol 33 (1979) 59-170
28. Loker E.S., and Hertel L.A. Alterations in Biomphalaria glabrata plasma induced by infection with the digenetic trematode Echinostoma paraensei. J Parasitol 75 (1987) 505-513
29. Winnepenninckx B., Backeljau T., and Dewachter R. Extraction of high-molecular-weight DNA from mollusks. Trend Genet 9 (1993) 407-1407
30. Jiang Y., Loker S.M., and Zhang S.-M. In vivo and in vitro knockdown of FREP2 gene expression in the snail Biomphalaria glabrata using RNA interference. Dev Comp Immunol 30 (2006) 855-866
31. Zhang S.-M., Zeng Y., and Loker E.S. Expression profiling and binding properties of fibrinogen-related proteins (FREPs), plasma proteins from the schistosome snail host Biomphalaria glabrata. Innate Immun. 14 (2008) 175-189
32. Adema C.M., Hertel L.A., Miller R.D., and Loker E.S. A family of fibrinogen-related proteins that precipitates parasite-derived molecules is produced by an invertebrate after infection. Proc Natl Acad Sci USA 94 (1997) 8691-8996
33. Schultz J., Milpetz F., Bork P., et al. SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci USA 95 (1998) 5857-5864
34. Kumar S., Tamura K., and Nei M. MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Briefing Bioinform 5 (2004) 150-163
35. Zhang S.-M., and Loker E.S. Representation of an immune responsive gene family encoding fibrinogen-related proteins (FREPs) in the freshwater mollusc Biomphalaria glabrata, an intermediate host for Schistosoma mansoni. Gene 341 (2004) 255-266
36. -ΔΔCT method. Methods 25 (2001) 402-408
37. Adema C.M., Luo M.Z., Hanelt B., et al. A bacterial artificial chromosome library for Biomphalaria glabrata, intermediate snail host of Schistosoma mansoni. Mem Inst Oswaldo Cruz Suppl. 1 (2006) 167-177
38. Wu Z., and Zhu B. Characterization and function of CREB homologue from Crassostrea ariakensis stimulated by rickettsia-like organism. Dev Comp Immunol 32 (2008) 1572-1581
39. Knudsen B., Kohn A.B., Nahir B., et al. Complete DNA sequence of the mitochondrial genome of the sea slug, Aplysia californica: conservation of the gene order in Euthyneura. Mol Phylogenet Evol 38 (2006) 459-469
40. Blair D., Davis G.M., and Wu B. Evolutionary relationships between trematodes and snails emphasizing schistosomes and paragonimids. Parasitology 123 (2001) S229-243
41. Goodson M.S., Kojadinovic M., Troll J.V., et al. Identifying components of the NF-kappa B pathway in the beneficial Euprymna scolopes Vibrio fischeri light organ symbiosis. Appl Environ Microbiol 71 (2005) 6934-6946
42. Song L., Xu W., Li C.H., et al. Development of expressed sequence tags from the bay scallop, Argopecten irradians irradians. Mar Biotechol 8 (2006) 61-169
43. Tanguy A., Guo X.M., and Ford S.E. Discovery of genes expressed in response to Perkinsus marinus challenge in Eastern (Crassostrea virginica) and Pacific (C. gigas) oysters. Gene 338 (2004) 121-131
44. Tanguy A., Bierne N., Saavedra C., et al. Increasing genomic information in bivalves through new EST collections in four species: development of new genetic markers for environmental studies and genome evolution. Gene 408 (2008) 27-36
45. Ebberink R.H.M., Van Loenhout H., Geraerts W.P.M., and Joosse J. Purification and amino-acid sequence of the ovulation neurohormone of Lymnaea stagnalis. Proc Natl Acad Sci USA 82 (1985) 7767-7771
46. Dictus W.J.A.G., De Jong-Brink M., and Boer H.H. A neuropeptide (calfluxin) is involved in the influx of calcium into mitochondria of the albumin gland of the fresh-water snail Lymnaea stagnalis. General Comp Endocrinol 65 (1987) 439-450
47. Crew A.E., and Yoshino T.P. Schistosoma mansoni: effect of infection on the reproduction and gonal growth in Biomphalaria glabrata. Exp Parasitol 68 (1989) 326-334
48. Crew A.E., and Yoshin0 T.P. Influence of larval schistosomes on polysaccharide synthesis in albumin glands of Biomphalaria glabrata. Parasitology 101 (1990) 351-359
49. Thompson S.N. Redirection of host metabolism and effects on parasite nutrition. In: Beckage N.E., Thompson S.N., and Federici B.A. (Eds). Parasites and pathogen of insects (1993), Academic Press, New York 125-144
50. Bai F.X., Johnston L.A., Watson C.O., et al. Phenoloxidase activity in the reproductive system of Biomphalaria glabrata: role in egg production and effect of schistosome infection. J Parasitol 83 (1997) 852-858