Identification of protein components of egg masses indicates parental investment in immunoprotection of offspring by Biomphalaria glabrata (Gastropoda, Mollusca)

Developmental and Comparative Immunology

Volumn 34, Issue 4, 2010, Pages 425-435

  Hathaway, Jennifer J M ^a   Adema, Coen M ^a   Stout, Barbara A ^a   Mobarak, Charlotte D ^b   Loker, Eric S ^a  

^a UNIVERSITY OF NEW MEXICO   (United States)

^b UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

Author keywords

Bioinformatics; C type lectins; Cu Zn SOD; Freshwater mollusc; Lipopolysaccharide binding protein bactericidal permeability increasing protein; Pheromone; Proteomics

Indexed keywords

APLYSIANIN E; BINDING PROTEIN; COPPER ZINC SUPEROXIDE DISMUTASE; DODECYL SULFATE SODIUM; GRAM NEGATIVE BACTERIA BINDING PROTEIN; HEMOCYANIN; LECTIN; LIPOPOLYSACCHARIDE BINDING PROTEIN; MONOPHENOL MONOOXYGENASE; PHEROMONE; PROTEINASE INHIBITOR; UNCLASSIFIED DRUG; VON WILLEBRAND FACTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; APLYSIA; ARTICLE; BIOMPHALARIA GLABRATA; BLOOD CELL; CONTROLLED STUDY; ENZYME ACTIVITY; EVOLUTIONARY HOMOLOGY; HOST PARASITE INTERACTION; INNATE IMMUNITY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROGENY; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SCHISTOSOMIASIS MANSONI; SEQUENCE ANALYSIS; TANDEM MASS SPECTROMETRY; UNINDEXED SEQUENCE; WORM EGG;

APLYSIA; BIOMPHALARIA GLABRATA; GASTROPODA; MOLLUSCA; NEGIBACTERIA; SCHISTOSOMA; SCHISTOSOMA MANSONI;

EID: 74449085862     PISSN: 0145305X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dci.2009.12.001     Document Type: Article

References (74)

1. Gryseels B., Polman K., Clerinx J., and Kestens L. Human schistosomiasis. Lancet 368 (2006) 1106-1118
2. Poiani A. Complexity of seminal fluid: a review. Behav Ecol Sociobiol 60 (2006) 289-310
3. Current W.L. Cryptobia sp. in the snail Triadopsis multilineata (Say): fine structure of attached flagellates and their mode of attachment to the spermatheca. J Protozool 27 (1980) 278-287
4. Morand S., and Faliex E. Study on the life cycle of a sexually transmitted nematode parasite of a terrestrial snail. J Parasitol 80 (1994) 1049-1052
5. Fries C.R., and Grant D.M. Rickettsiae in gill epithelial cells of the hard clam, Mercenaria mercenaria. J Invertebr Pathol 57 (1991) 166-171
6. Anderson R.C. On the development and transmission of Cosmocercoides dukae of terrestrial mollusks in Ontario. Can J Zool 38 (1960) 801-825
7. Benkendorff K., Davis A.R., and Bremner J.B. Chemical defense in the egg masses of benthic invertebrates: an assessment of antibacterial activity in 39 mollusks and 4 polychaetes. J Invertebr Pathol 78 (2001) 109-118
8. Benkendorff K., Pillai R., and Bremner J.B. 2,4,5-Tribromo-1H-imidazole in the egg masses of three muricid molluscs. Nat Prod Res 18 (2004) 427-431
9. Ramasamy M.S., and Murugan A. Fouling deterrent chemical defence in three muricid gastropod egg masses from the Southeast coast of India. Biofouling 27 (2007) 259-265
10. Takamatsu N., Shiba T., Muramoto K., and Kamiya H. Molecular cloning of the defense factor in the albumen gland of the sea hare Aplysia kurodai. FEBS Lett 377 (1995) 373-376
11. Ko{combining double acute accent}hler W., Prokop O., and Ku{combining double acute accent}hnemund O. Routine identification of group-C streptococci by means of an agglutinin (protectin) from the albumen gland of the edible snail, Helix pomatia. J Med. Microbiol 6 (1973) 127-130
12. Patchett R.A., Kelly A.F., and Kroll R.G. The adsorption of bacteria to immobilized lectins. J Appl Bacteriol 71 (1991) 277-284
13. Sanchez J.F., Lescar J., Chazalet V., Audfray A., Gagnon J., Alvarez R., et al. Biochemical and structural analysis of Helix pomatia agglutinin. A hexameric lectin with a novel fold. J Biol Chem 281 (2006) 20171-20180
14. Slifkin M., and Cumbie R. Rapid detection of herpes simplex virus with fluorescein-labeled Helix pomatia lectin. J Clin Microbiol 27 (1989) 1036-1039
15. Nagle G.T., de Jong-Brink M., Painter S.D., and Li K.W. Structure, localization and potential role of a novel molluscan trypsin inhibitor in Lymnaea. Eur J Biochem 268 (2001) 1213-1221
16. Paraense W.L. Self- and cross-fertilization in Australorbis glabratus. Mem Inst Oswaldo Cruz 63 (1955) 285-291
17. Sturrock R.F. The intermediate hosts and host-parasite relationships. In: Jordan P., Webbe G., and Sturrock R.F. (Eds). Human schistosomiasis (1993), CAB International, Wallingford 33-85
18. Geraerts P.M., and Joosse J. Freshwater snails (Basommatophora). In: Tompa A.S., Verdonk N.H., and van den Biggelaar J.A.M. (Eds). The mollusca 7: reproduction (1984), Academic Press, New York 141-207
19. Morishita F., Mukai S.T., and Saleuddin A.S. Release of proteins and polysaccharides from the albumen gland of the freshwater snail Helisoma duryi: effect of cAMP and brain extracts. J Comp Physiol A 182 (1998) 817-825
20. Plesch B., de Jong-Brink m, and Boer H.H. Histological and histochemical observations on the reproductive tract of the hermaphroditic pond snail Lymaea stagnalis (L). Neth J Zool 21 (1971) 180-201
21. Goudsmit E.M. Galactogen catabolism by embryos of the freshwater snails, Bulimnaea megasoma and Lymnaea stagnalis. Comp Biochem Physiol B 53 (1976) 439-442
22. Michelson E.H., and Dubois L. Agglutinins and lysins in the molluscan family Planorbidae: a survey of hemolymph, egg-masses, and albumen-gland extracts. Biol Bull 153 (1977) 219-227
23. Stein P.C., and Basch P.F. Purification and binding properties of hemagglutinin from Biomphalaria glabrata. J Invertebr Pathol 33 (1979) 10-18
24. Jeong K.H., Sussman S., Rosen S.D., Lie K.J., and Heyneman D. Distribution and variation of hemagglutinating activity in the hemolymph of Biomphalaria glabrata. J Invert Pathol 38 (1981) 256-263
25. Boswell C.A., and Bayne C.J. Isolation, characterization and functional assessment of a hemagglutinin from the plasma of Biomphalaria glabrata, intermediate host of Schistosoma mansoni. Dev Comp Immunol 8 (1984) 559-568
26. Bai G., Li J., Christensen B.M., and Yoshino T.P. Phenoloxidase activity in the reproductive system and egg masses of the pulmonate gastropod, Biomphalaria glabrata. Comp Biochem Physiol B: Biochem Mol Biol 114 (1996) 353-359
27. Bai G., Brown J.F., Watson C., and Yoshino T.P. Isolation and characterization of phenoloxidase from egg masses of the gastropod mollusc, Biomphalaria glabrata. Comp Biochem Physiol B: Biochem Mol Biol 118 (1997) 463-469
28. Bai G., Johnston L.A., Watson C.O., and Yoshino T.P. Phenoloxidase activity in the reproductive system of Biomphalaria glabrata: role in egg production and effect of schistosome infection. J Parasitol 83 (1997) 852-858
29. Miller A.N., Ofori K., Lewis F., and Knight M. Schistosoma mansoni: use of a subtractive cloning strategy to search for RFLPs in parasite-resistant Biomphalaria glabrata. Exp Parasitol 84 (1996) 420-428
30. Mukai S.T., Hoque T., Morishita F., and Saleuddin A.S.M. Cloning and characterization of a candidate nutritive glycoprotein from the albumen gland of the freshwater snail Helisoma duryi (Mollusca, Pulmonata). Invert Biol 123 (2004) 82-91
31. Bouchut A., Coustau C., Gourbal B., and Mitta G. Compatibility in the Biomphalaria glabrata/Echinostoma caproni model: new candidate genes evidenced by a suppressive subtractive hybridization approach. Parasitology 134 (2007) 575-588
32. Vergote D., Bouchut A., Sautière P.E., Roger E., Galinier R., Rognon A., et al. Characterisation of proteins differentially present in the plasma of Biomphalaria glabrata susceptible or resistant to Echinostoma caproni. Int J Parasitol 35 (2005) 215-224
33. Guillou F., Mitta G., Galinier R., and Coustau C. Identification and expression of gene transcripts generated during an anti-parasitic response in Biomphalaria glabrata. Dev Comp Immunol 31 (2007) 657-671
34. Adema C.M., Luo M.Z., Hanelt B., Hertel L.A., Marshall J.J., Zhang S.M., et al. A bacterial artificial chromosome library for Biomphalaria glabrata, intermediate snail host of Schistosoma mansoni. Mem Inst Oswaldo Cruz 101 Suppl. 1 (2006) 167-177
35. Loker E.S., and Hertel L.A. Alterations in Biomphalaria glabrata plasma induced by infection with the digenetic trematode Echinostoma paraensei. J Parasitol 73 (1987) 503-513
36. Shevchenko A., Wilm M., Vorm O., and Mann M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68 (1996) 850-858
37. Jannotti-Passos L.K., Andrade H.M., Caldeira R.L., Romanha A.J., Murta S.M., Chapeaurouge D.A., et al. Proteome analysis of the cardiac and pericardial tissue of Biomphalaria tenagophila populations susceptible and resistant to Schistosoma mansoni infection. Acta Trop 105 (2008) 229-234
38. Guillou F., Mitta G., Dissous C., Pierce R., and Coustau C. Use of individual polymorphism to validate potential functional markers: case of a candidate lectin (BgSel) differentially expressed in susceptible and resistant strains of Biomphalaria glabrata. Comp Biochem Physiol B: Biochem Mol Biol 138 (2004) 175-181
39. Léonard P.M., Adema C.M., Zhang S.-M., and Loker E.S. Structure of two FREP genes that encode IgSF and fibrinogen domains, with comments on diversity of the FREP gene family in the snail Biomphalaria glabrata. Gene 269 (2001) 155-165
40. Zhang S.-M., Léonard P.M., Adema C.M., and Loker E.S. Parasite responsive IgSF members in the snail Biomphalaria glabrata: characterization of novel genes with tandemly arranged IgSF domains and a fibrinogen domain. Immunogenetics 53 (2001) 684-694
41. Raghavan N., and Knight M. The snail (Biomphalaria glabrata) genome project. Trends Parasitol 22 (2006) 148-151
42. Bender R.C., and Bayne C.J. Purification and characterization of a tetrameric alpha-macroglobulin proteinase inhibitor from the gastropod mollusc Biomphalaria glabrata. Biochem J 316 (1996) 893-900
43. Armstrong P.B., and Quigley J.P. Alpha2-macroglobulin: an evolutionarily conserved arm of the innate immune system. Dev Comp Immunol 23 (1999) 375-390
44. Padhi A., Buchheim M.A., and Verghese B. Dynamic evolutionary pattern of alpha2-macroglobulin in a model organism, the zebrafish (Danio rerio). Mol Immunol 45 (2008) 3312-3318
45. Fryer S.E., Bender R.C., and Bayne C.J. Inhibition of cysteine proteinase from Schistosoma mansoni larvae by alpha-macroglobulin from the plasma of Biomphalaria glabrata. J Parasitol 82 (1996) 343-347
46. Silverman G.A., Whisstock J.C., Askew D.J., Pak S.C., Luke C.J., Cataltepe S., et al. Human clade B serpins (ov-serpins) belong to a cohort of evolutionarily dispersed intracellular proteinase inhibitor clades that protect cells from promiscuous proteolysis. Cell Mol Life Sci 61 (2004) 301-325
47. Armstrong P.B. Proteases and protease inhibitors: a balance of activities in host-pathogen interaction. Immunobiology 211 (2006) 263-281
48. Kanost M.R., Jiang H., and Yu X.Q. Innate immune responses of a lepidopteran insect, Manduca sexta. Immunol Rev 198 (2004) 97-105
49. Lieb B., Dimitrova K., Kang H.S., Braun S., Gebauer W., Martin A., et al. Red blood with blue-blood ancestry: intriguing structure of a snail hemoglobin. Proc Natl Acad Sci USA 103 (2006) 12011-12016
50. Decker H., and Jaenicke E. Recent findings on phenoloxidase activity and antimicrobial activity of hemocyanins. Dev Comp Immunol 28 (2004) 673-687
51. Decker H., Schweikardt T., Nillius D., Salzbrunn U., Jaenicke E., and Tuczek F. Similar enzyme activation and catalysis in hemocyanins and tyrosinases. Gene 398 (2007) 183-191
52. Nagai T., Osaki T., and Kawabata S. Functional conversion of hemocyanin to phenoloxidase by horseshoe crab antimicrobial peptides. J Biol Chem 276 (2001) 27166-27170
53. Destoumieux-Garzón D., Saulnier D., Garnier J., Jouffrey C., Bulet P., and Bachère E. Crustacean immunity. Antifungal peptides are generated from the C terminus of shrimp hemocyanin in response to microbial challenge. J Biol Chem 276 (2001) 47070-47077
54. Lee S.Y., Lee B.L., and Söderhäll K. Processing of crayfish hemocyanin subunits into phenoloxidase. Biochem Biophys Res Commun 322 (2004) 490-496
55. Lei K., Li F., Zhang M., Yang H., Luo T., and Xu X. Difference between hemocyanin subunits from shrimp Penaeus japonicus in anti-WSSV defense. Dev Comp Immunol 32 (2008) 808-813
56. Jaenicke E., Fraune S., May S., Irmak P., Augustin R., Meesters C., et al. Is activated hemocyanin instead of phenoloxidase involved in immune response in woodlice?. Dev Comp Immunol 33 (2009) 1055-1063
57. Mitta G., Galinier R., Tisseyre P., Allienne J.F., Girerd-Chambaz Y., Guillou F., et al. Gene discovery and expression analysis of immune-relevant genes from Biomphalaria glabrata hemocytes. Dev Comp Immunol 29 (2005) 393-407
58. Tirapé A., Bacque C., Brizard R., Vandenbulcke F., and Boulo V. Expression of immune-related genes in the oyster Crassostrea gigas during ontogenesis. Dev Comp Immunol 31 (2007) 859-873
59. Levy O. Antimicrobial proteins and peptides of blood: templates for novel antimicrobial agents. Blood 96 (2000) 2664-2672
60. 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
61. Lemaitre B., and Hoffmann J. The host defense of Drosophila melanogaster. Annu Rev Immunol 25 (2007) 697-743
62. Wang X., Fuchs J.F., Infanger L.C., Rocheleau T.A., Hillyer J.F., Chen C.C., et al. Mosquito innate immunity: involvement of beta 1,3-glucan recognition protein in melanotic encapsulation immune responses in Armigeres subalbatus. Mol Biochem Parasitol 139 (2005) 65-73
63. Horak P., and van der Knaap W.P.W. Lectins in snail-trematode immune interactions: a review. Folia Parasitol 44 (1997) 161-172
64. Bianchet M.A., Ahmed H., Vasta G.R., and Amzel L.M. Structural aspects of lectin-ligand interactions. In: Vasta G.R., and Ahmed H. (Eds). Animal lectins: a functional view (2009), CRC Press/Taylor & Francis, Boca Raton, FL 475-491
65. Jung Y., Nowak S., Hertel L.A., Zhang S.-M., Loker E.S., and Adema C.M. Manganese superoxide dismutase from Biomphalaria glabrata. J Invertebr Pathol 90 (2005) 59-63
66. Bayne C.J. Successful parasitism of vector snail Biomphalaria glabrata by the human blood fluke (trematode) Schistosoma mansoni: a 2009 assessment. Mol Biochem Parasitol 165 (2009) 8-18
67. Obara K., Otsuka-Fuchino H., Sattayasai N., Nonomura Y., Tsuchiya T., and Tamiya T. Molecular cloning of the antibacterial protein of the giant African snail, Achatina fulica Férussac. Eur J Biochem 209 (1992) 1-6
68. Jimbo M.F., Nakanishi R., Sakai K., Muramoto, and Kamiya H. Characterization of l-amino acid oxidase and antimicrobial activity of aplysianin A, a sea hare-derived antitumor-antimicrobial protein. Fish Sci 69 (2003) 1240-1246
69. Bouchut A., Roger E., Coustau C., Gourbal B., and Mitta G. Compatibility in the Biomphalaria glabrata/Echinostoma caproni model: potential involvement of adhesion genes. Int J Parasitol 36 (2006) 175-184
70. Cummins S.F., Nichols A.E., Schein C.H., and Nagle G.T. Newly identified water-borne protein pheromones interact with attractin to stimulate mate attraction in Aplysia. Peptides 27 (2006) 597-606
71. Vianey-Liaud M., and Dussart G. Aspects of pairing and reproduction in the hermaphrodite freshwater snail Biomphalaria glabrata (Gastropoda: Pulmonata). J Moll Stud 68 (2002) 245-250
72. Boyle J.P., and Yoshino T.P. Monoamines in the albumen gland, plasma, and central nervous system of the snail Biomphalaria glabrata during egg-laying. Comp Biochem Physiol A: Mol Integr Physiol 132 (2002) 411-422
73. Little T.J., O'Connor B., Colegrave N., Watt K., and Read A.F. Maternal transfer of strain-specific immunity in an invertebrate. Curr Biol 13 (2003) 489-492
74. Gorman M.J., Kankanala P., and Kanost M.R. Bacterial challenge stimulates innate immune responses in extra-embryonic tissues of tobacco hornworm eggs. Insect Mol Biol 13 (2004) 19-24