Time series analysis of the transcriptional responses of Biomphalaria glabrata throughout the course of intramolluscan development of Schistosoma mansoni and Echinostoma paraensei

International Journal for Parasitology

Volumn 40, Issue 7, 2010, Pages 819-831

  Hanington, Patrick C ^a   Lun, Cheng Man ^a   Adema, Coen M ^a   Loker, Eric S ^a  

^a UNIVERSITY OF NEW MEXICO   (United States)

Author keywords

Biomphalaria glabrata; Echinostoma paraensei; Host parasite interactions; Immunity; Immunosuppression; Microarray; Schistosoma mansoni; Transcript expression

Indexed keywords

FIBRINOGEN RELATED PROTEIN 4; GENE PRODUCT; LECTIN; UNCLASSIFIED DRUG;

ANTIPARASITE DEFENSE; BIOMONITORING; GENE EXPRESSION; GENETIC ANALYSIS; GENOTYPE; HOST-PARASITE INTERACTION; IMMUNITY; INVASIVE SPECIES; LARVAL DEVELOPMENT; SNAIL; TIME SERIES ANALYSIS;

ARTICLE; BIOMPHALARIA GLABRATA; CERCARIA (TREMATODE LARVA); CONTROLLED STUDY; DISEASE COURSE; DOWN REGULATION; ECHINOSTOMA; ECHINOSTOMA PARAENSEI; HOST PARASITE INTERACTION; HOST RESISTANCE; LARVAL DEVELOPMENT; NONHUMAN; NUCLEOTIDE SEQUENCE; PHAGOCYTE; SCHISTOSOMA MANSONI; SPOROCYST; TIME SERIES ANALYSIS; TRANSCRIPTION REGULATION; TREMATODIASIS; UPREGULATION;

ANIMALS; BIOMPHALARIA; DOWN-REGULATION; ECHINOSTOMA; GENE EXPRESSION PROFILING; IMMUNE EVASION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SCHISTOSOMA MANSONI; STRESS, PHYSIOLOGICAL; TIME FACTORS; UP-REGULATION;

BASOMMATOPHORA; BIOMPHALARIA GLABRATA; ECHINOSTOMA PARAENSEI; GASTROPODA; SCHISTOSOMA MANSONI; TREMATODA; VERTEBRATA;

EID: 77952546384     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpara.2009.12.005     Document Type: Article

References (114)

1. Abrous M., Rondelaud D., Dreyfuss G., Cabaret J. Unusual transmission of the liver fluke, Fasciola hepatica, by Lymnaea glabra or Planorbis leucostoma in France. J Parasitol 1998, 84:1257-1259.
2. Adema C.M., Arguello D.F., Stricker S.A., Loker E.S. A time-lapse study of interactions between Echinostoma paraensei intramolluscan larval stages and adherent hemocytes from Biomphalaria glabrata and Helix aspersa. J Parasitol 1994, 80:719-727.
3. Appleton C.C. Studies on Austrobilharzia terrigalensis (Trematoda: Schistosomatidae) in the Swan Estuary, Western Australia: infection in the definitive host, Larus novaehollandiae. Int J Parasitol 1983, 13:249-259.
4. Aragon A.D., Quinones G.A., Thomas E.V., Roy S., Werner-Washburne M. Release of extraction-resistant mRNA in stationary phase Saccharomyces cerevisiae produces a massive increase in transcript abundance in response to stress. Genome Biol 2006, 7:R9.
5. Ataev G.L., Dobrovolskij A.A., Fournier A., Jourdane J. Migration and development of mother sporocysts of Echinostoma caproni (Digenea: Echinostomatidae). J Parasitol 1997, 83:444-453.
6. Barat-Houari M., Hilliou F., Jousset F.X., Sofer L., Deleury E., Rocher J., Ravallec M., Galibert L., Delobel P., Feyereisen R., Fournier P., Volkoff A.N. Gene expression profiling of Spodoptera frugiperda hemocytes and fat body using cDNA microarray reveals polydnavirus-associated variations in lepidopteran host genes transcript levels. BMC Genomics 2006, 7:160.
7. Bayne C.J. Successful parasitism of vector snail Biomphalaria glabrata by the human blood fluke (trematode) Schistosoma mansoni: a 2009 assessment. Mol Biochem Parasitol 2009, 165:8-18.
8. Bhaskar L., Krishnan V.S., Thampan R.V. Cytoskeletal elements and intracellular transport. J Cell Biochem 2007, 101:1097-1108.
9. Bischoff V., Vignal C., Duvic B., Boneca I.G., Hoffmann J.A., Royet J. Downregulation of the Drosophila immune response by peptidoglycan-recognition proteins SC1 and SC2. PLoS Pathog 2006, 2:e14.
10. Boete C., Paul R.E., Koella J.C. Direct and indirect immunosuppression by a malaria parasite in its mosquito vector. Proc Biol Sci 2004, 271:1611-1615.
11. Boswell C.A., Bayne C.J. Lectin-dependent cell-mediated cytotoxicity in an invertebrate model: Con A does not act as a bridge. Immunology 1986, 57:261-264.
12. Bouchut A., Roger E., Coustau C., Gourbal B., Mitta G. Compatibility in the Biomphalaria glabrata/Echinostoma caproni model: potential involvement of adhesion genes. Int J Parasitol 2006, 36:175-184.
13. Bouchut A., Sautiere P.E., Coustau C., Mitta G. Compatibility in the Biomphalaria glabrata/Echinostoma caproni model: Potential involvement of proteins from hemocytes revealed by a proteomic approach. Acta Trop 2006, 98:234-246.
14. Bouchut A., Coustau C., Gourbal B., Mitta G. Compatibility in the Biomphalaria glabrata/Echinostoma caproni model: new candidate genes evidenced by a suppressive subtractive hybridization approach. Parasitology 2007, 134:575-588.
15. Buresova V., Hajdusek O., Franta Z., Sojka D., Kopacek P. IrAM-An alpha2-macroglobulin from the hard tick Ixodes ricinus: characterization and function in phagocytosis of a potential pathogen Chryseobacterium indologenes. Dev Comp Immunol 2009, 33:489-498.
16. Cervi L., Rubinstein H., Masih D.T. Involvement of excretion-secretion products from Fasciola hepatica inducing suppression of the cellular immune responses. Vet Parasitol 1996, 61:97-111.
17. Chen X., Dings R.P., Nesmelova I., Debbert S., Haseman J.R., Maxwell J., Hoye T.R., Mayo K.H. Topomimetics of amphipathic beta-sheet and helix-forming bactericidal peptides neutralize lipopolysaccharide endotoxins. J Med Chem 2006, 49:7754-7765.
18. Clarke D.J. Photorhabdus: a model for the analysis of pathogenicity and mutualism. Cellular Microbiology 2008, 10:2159-2167.
19. Crews A.E., Yoshino T.P. Schistosoma mansoni: effect of infection on reproduction and gonadal growth in Biomphalaria glabrata. Exp Parasitol 1989, 68:326-334.
20. Curtis L.A. Tenure of individual larval trematode infections in an estuarine gastropod. Journal of the Marine Biological Association of the United Kingdom 2003, 83:1047-1051.
21. Davies D.H., Vinson S.B. Interference with function of plasmatocytes of Heliothis virescens in vivo by calyx fluid of the parasitoid Campoletis sonorensis. Cell Tissue Res 1988, 251:467-475.
22. De Jong-Brink M. How schistosomes profit from the stress responses they elicit in their hosts. Adv Parasitol 1995, 35:177-256.
23. Duvaux-Miret O., Stefano G.B., Smith E.M., Dissous C., Capron A. Immunosuppression in the definitive and intermediate hosts of the human parasite Schistosoma mansoni by release of immunoactive neuropeptides. Proc Natl Acad Sci U S A 1992, 89:778-781.
24. Fytrou A., Schofield P.G., Kraaijeveld A.R., Hubbard S.F. Wolbachia infection suppresses both host defence and parasitoid counter-defence. Proceedings of the Royal Society B-Biological Sciences 2006, 273:791-796.
25. Gonzalez M., Gueguen Y., Destoumieux-Garzon D., Romestand B., Fievet J., Pugniere M., Roquet F., Escoubas J.M., Vandenbulcke F., Levy O., Saune L., Bulet P., Bachere E. Evidence of a bactericidal permeability increasing protein in an invertebrate, the Crassostrea gigas Cg-BPI. Proc Natl Acad Sci U S A 2007, 104:17759-17764.
26. Goodall C.P., Bender R.C., Broderick E.J., Bayne C.J. Constitutive differences in Cu/Zn superoxide dismutase mRNA levels and activity in hemocytes of Biomphalaria glabrata (Mollusca) that are either susceptible or resistant to Schistosoma mansoni (Trematoda). Mol Biochem Parasitol 2004, 137:321-328.
27. Goodall C.P., Bender R.C., Brooks J.K., Bayne C.J. Biomphalaria glabrata cytosolic copper/zinc superoxide dismutase (SOD1) gene: association of SOD1 alleles with resistance/susceptibility to Schistosoma mansoni. Mol Biochem Parasitol 2006, 147:207-210.
28. Gruden-Movsesijan A., Milosavljevic Lj S. The involvement of the macrophage mannose receptor in the innate immune response to infection with parasite Trichinella spiralis. Vet Immunol Immunopathol 2006, 109:57-67.
29. Guillou F., Mitta G., Galinier R., Coustau C. Identification and expression of gene transcripts generated during an anti-parasitic response in Biomphalaria glabrata. Dev Comp Immunol 2007, 31:657-671.
30. Guillou F., Roger E., Mone Y., Rognon A., Grunau C., Theron A., Mitta G., Coustau C., Gourbal B.E. Excretory-secretory proteome of larval Schistosoma mansoni and Echinostoma caproni, two parasites of Biomphalaria glabrata. Mol Biochem Parasitol 2007, 155:45-56.
31. Guimaraes A.C., Kawarabayashi M., Nunes E.V., Ferraz S.N., Chiosini C.B., Tolezano J.E., Gama-Rodrigues J.J., Okumura M. Experimental toxoplasmosis, and immunosuppression (parasite evaluation and histological alterations). Rev Hosp Clin Fac Med Sao Paulo 1997, 52:316-320.
32. Guo D., Zhang Y., Zeng D., Wang H., Li X., Li Y., Fan X. Functional properties of hemocyanin from Oncomelania hupensis, the intermediate host of Schistosoma japonicum. Exp Parasitol 2009, 123:277-281.
33. Ha E.M., Lee K.A., Seo Y.Y., Kim S.H., Lim J.H., Oh B.H., Kim J., Lee W.J. Coordination of multiple dual oxidase-regulatory pathways in responses to commensal and infectious microbes in drosophila gut. Nat Immunol. 2009.
34. Hanelt B., Lun C.M., Adema C.M. Comparative ORESTES-sampling of transcriptomes of immune-challenged Biomphalaria glabrata snails. J Invertebr Pathol 2008, 99:192-203.
35. Hertel L.A., Adema C.M., Loker E.S. Differential expression of FREP genes in two strains of Biomphalaria glabrata following exposure to the digenetic trematodes Schistosoma mansoni and Echinostoma paraensei. Dev Comp Immunol 2005, 29:295-303.
36. Humbert E., Coustau C. Refractoriness of host haemocytes to parasite immunosuppressive factors as a putative resistance mechanism in the Biomphalaria glabrata-Echinostoma caproni system. Parasitology 2001, 122:651-660.
37. Iakovleva N.V., Shaposhnikova T.G., Gorbushin A.M. Rediae of echinostomatid and heterophyid trematodes suppress phagocytosis of haemocytes in Littorina littorea (Gastropoda: Prosobranchia). Exp Parasitol 2006, 113:24-29.
38. Ittiprasert, W., Miller, A., Myers, J., Nene, V., El-Sayed, N.M., Knight, M., Identification of immediate response genes dominantly expressed in juvenile resistant and susceptible Biomphalaria glabrata snails upon exposure to Schistosoma mansoni. Mol Biochem Parasitol 169, 27-39.
39. Janssen K.P., Schleicher M. Dictyostelium discoideum: a genetic model system for the study of professional phagocytes. Profilin, phosphoinositides and the lmp gene family in Dictyostelium. Biochim Biophys Acta 2001, 1525:228-233.
40. Jung Y., Nowak T.S., Zhang S.M., Hertel L.A., Loker E.S., Adema C.M. Manganese superoxide dismutase from Biomphalaria glabrata. J Invertebr Pathol 2005, 90:59-63.
41. Knight M., Raghavan N., Goodall C., Cousin C., Ittiprasert W., Sayed A., Miller A., Williams D.L., Bayne C.J. Biomphalaria glabrata peroxiredoxin: Effect of Schistosoma mansoni infection on differential gene regulation. Mol Biochem Parasitol. 2009.
42. Krarup A., Sorensen U.B., Matsushita M., Jensenius J.C., Thiel S. Effect of capsulation of opportunistic pathogenic bacteria on binding of the pattern recognition molecules mannan-binding lectin, L-ficolin, and H-ficolin. Infect Immun 2005, 73:1052-1060.
43. Labropoulou V., Douris V., Stefanou D., Magrioti C., Swevers L., Iatrou K. Endoparasitoid wasp bracovirus-mediated inhibition of hemolin function and lepidopteran host immunosuppression. Cell Microbiol 2008, 10:2118-2128.
44. Li C., Song L., Zhao J., Zhu L., Zou H., Zhang H., Wang H., Cai Z. Preliminary study on a potential antibacterial peptide derived from histone H2A in hemocytes of scallop Chlamys farreri. Fish Shellfish Immunol 2007, 22:663-672.
45. Li C.Y., Guo Z., Wang Z. TGFbeta receptor saxophone non-autonomously regulates germline proliferation in a Smox/dSmad2-dependent manner in Drosophila testis. Dev Biol 2007, 309:70-77.
46. Lie K.J. Larval Trematode Antagonism - Principles and Possible Application as a Control Method. Experimental Parasitology 1973, 33:343-349.
47. Lie K.J., Heyneman D., Jeong K.H. Studies on resistance in snails. 7. Evidence of interference with the defense reaction in Biomphalaria glabrata by trematode larvae. J Parasitol 1976, 62:608-615.
48. Lie K.J., Heyneman D. Schistosoma mansoni, Echinostoma lindoense, and Paryphostomum segregatum: interference by trematode larvae with acquired resistance in snails, Biomphalaria glabrata. Exp Parasitol 1977, 42:343-347.
49. Lie K.J., Heyneman D., Richards C.S. Schistosoma mansoni: temporary reduction of natural resistance in Biomphalaria glabrata induced by irradiated miracidia of Echinostoma paraensei. Exp Parasitol 1977, 43:54-62.
50. Lie K.J., Heyneman D. Capacity of irradiated echinostome sporocysts to protect Schistosoma mansoni in resistant Biomphalaria glabrata. Int J Parasitol 1979, 9:539-543.
51. Lie K.J., Jeong K.H., Heyneman D. Selective interference with granulocyte function induced by Echinostoma paraensei (Trematoda) larvae in Biomphalaria glabrata (Mollusca). J Parasitol 1981, 67:790-796.
52. Lie K.J., Jeong K.H., Heyneman D. Further characterization of acquired resistance in Biomphalaria glabrata. J Parasitol 1982, 68:529-531.
53. Lieb B., Dimitrova K., Kang H.S., Braun S., Gebauer W., Martin A., Hanelt B., Saenz S.A., Adema C.M., Markl J. Red blood with blue-blood ancestry: intriguing structure of a snail hemoglobin. Proc Natl Acad Sci U S A 2006, 103:12011-12016.
54. Lockyer A.E., Spinks J., Noble L.R., Rollinson D., Jones C.S. Identification of genes involved in interactions between Biomphalaria glabrata and Schistosoma mansoni by suppression subtractive hybridization. Mol Biochem Parasitol 2007, 151:18-27.
55. Lockyer A.E., Spinks J.N., Walker A.J., Kane R.A., Noble L.R., Rollinson D., Dias-Neto E., Jones C.S. Biomphalaria glabrata transcriptome: identification of cell-signalling, transcriptional control and immune-related genes from open reading frame expressed sequence tags (ORESTES). Dev Comp Immunol 2007, 31:763-782.
56. Lockyer A.E., Spinks J., Kane R.A., Hoffmann K.F., Fitzpatrick J.M., Rollinson D., Noble L.R., Jones C.S. Biomphalaria glabrata transcriptome: cDNA microarray profiling identifies resistant- and susceptible-specific gene expression in haemocytes from snail strains exposed to Schistosoma mansoni. BMC Genomics 2008, 9:634.
57. Loker E.S., Bayne C.J., Yui M.A. Echinostoma paraensei: hemocytes of Biomphalaria glabrata as targets of echinostome mediated interference with host snail resistance to Schistosoma mansoni. Exp Parasitol 1986, 62:149-154.
58. Loker E.S., Hertel L.A. Alterations in Biomphalaria glabrata plasma induced by infection with the digenetic trematode Echinostoma paraensei. J Parasitol 1987, 73:503-513.
59. Loker E.S., Boston M.E., Bayne C.J. Differential adherence of M line Biomphalaria glabrata hemocytes to Schistosoma mansoni and Echinostoma paraensei larvae, and experimental manipulation of hemocyte binding. J Invertebr Pathol 1989, 54:260-268.
60. Loker E.S., Cimino D.F., Hertel L.A. Excretory-secretory products of Echinostoma paraensei sporocysts mediate interference with Biomphalaria glabrata hemocyte functions. J Parasitol 1992, 78:104-115.
61. Loker E.S., Adema C.M. Schistosomes, Echinostomes and Snails - Comparative Immunobiology. Parasitology Today 1995, 11:120-124.
62. Marikovsky M., Ziv V., Nevo N., Harris-Cerruti C., Mahler O. Cu/Zn superoxide dismutase plays important role in immune response. J Immunol 2003, 170:2993-3001.
63. Mitta G., Galinier R., Tisseyre P., Allienne J.F., Girerd-Chambaz Y., Guillou F., Bouchut A., Coustau C. Gene discovery and expression analysis of immune-relevant genes from Biomphalaria glabrata hemocytes. Dev Comp Immunol 2005, 29:393-407.
64. Niemann G.M., Lewis F.A. Schistosoma mansoni: influence of Biomphalaria glabrata size on susceptibility to infection and resultant cercarial production. Exp Parasitol 1990, 70:286-292.
65. Nishihira J., Ishibashi T., Fukushima T., Sun B., Sato Y., Todo S. Macrophage migration inhibitory factor (MIF): Its potential role in tumor growth and tumor-associated angiogenesis. Ann N Y Acad Sci 2003, 995:171-182.
66. Noda S., Loker E.S. Phagocytic activity of hemocytes of M-line Biomphalaria glabrata snails: effect of exposure to the trematode Echinostoma paraensei. J Parasitol 1989, 75:261-269.
67. Okamoto O., Fujiwara S. Dermatopontin, a novel player in the biology of the extracellular matrix. Connect Tissue Res 2006, 47:177-189.
68. Oladiran A., Belosevic M. Trypanosoma carassii hsp70 increases expression of inflammatory cytokines and chemokines in macrophages of the goldfish (Carassius auratus L.). Dev Comp Immunol 2009, 33:1128-1136.
69. Onodera S., Suzuki K., Matsuno T., Kaneda K., Takagi M., Nishihira J. Macrophage migration inhibitory factor induces phagocytosis of foreign particles by macrophages in autocrine and paracrine fashion. Immunology 1997, 92:131-137.
70. Ouaissi A., Ouaissi M., Sereno D. Glutathione S-transferases and related proteins from pathogenic human parasites behave as immunomodulatory factors. Immunol Lett 2002, 81:159-164.
71. Pan C.T. Studies on the host-parasite relationship between Schistosoma mansoni and the snail Australorbis glabratus. Am J Trop Med Hyg 1965, 14:931-976.
72. Pan S.C. Schistosoma mansoni: the ultrastructure of larval morphogenesis in Biomphalaria glabrata and of associated host-parasite interactions. Jpn J Med Sci Biol 1996, 49:129-149.
73. Pearson A.M., Baksa K., Ramet M., Protas M., McKee M., Brown D., Ezekowitz R.A. Identification of cytoskeletal regulatory proteins required for efficient phagocytosis in Drosophila. Microbes Infect 2003, 5:815-824.
74. Petalidis L., Bhattacharyya S., Morris G.A., Collins V.P., Freeman T.C., Lyons P.A. Global amplification of mRNA by template-switching PCR: linearity and application to microarray analysis. Nucleic Acids Res 2003, 31:e142.
75. Pfluger W. Experimental epidemiology of schistosomiasis. II. Prepatency of Schistosoma mansoni in Biomphalaria glabrata at diurnally fluctuating temperatures. Z Parasitenkd 1981, 66:221-229.
76. Richards C.S., Knight M., Lewis F.A. Genetics of Biomphalaria glabrata and its effect on the outcome of Schistosoma mansoni infection. Parasitol Today 1992, 8:171-174.
77. Rigaud T., Moret Y. Differential phenoloxidase activity between native and invasive gammarids infected by local acanthocephalans: differential immunosuppression? Parasitology 2003, 127:571-577.
78. Sakamoto K., Chao W.S., Katsube K., Yamaguchi A. Distinct roles of EGF repeats for the Notch signaling system. Exp Cell Res 2005, 302:281-291.
79. Sanad M.M., Salem S.A., el-Dessouky K.I., Azab M.E. Experimental trichinosis: effect of immunosuppression on the host-parasite system. J Egypt Soc Parasitol 1991, 21:423-438.
80. Sandland G.J., Foster A.V., Zavodna M., Minchella D.J. Interplay between host genetic variation and parasite transmission in the Biomphalaria glabrata-Schistosoma mansoni system. Parasitol Res 2007, 101:1083-1089.
81. Schneider M.R., Wolf E. The epidermal growth factor receptor ligands at a glance. J Cell Physiol 2009, 218:460-466.
82. Sharma C., Vomastek T., Tarcsafalvi A., Catling A.D., Schaeffer H.J., Eblen S.T., Weber M.J. MEK partner 1 (MP1): regulation of oligomerization in MAP kinase signaling. J Cell Biochem 2005, 94:708-719.
83. Shelby K.S., Webb B.A. Polydnavirus-mediated suppression of insect immunity. Journal of Insect Physiology 1999, 45:507-514.
84. Sheps J.A., Ralph S., Zhao Z., Baillie D.L., Ling V. The ABC transporter gene family of Caenorhabditis elegans has implications for the evolutionary dynamics of multidrug resistance in eukaryotes. Genome Biol 2004, 5:R15.
85. Sorensen R.E., Minchella D.J. Snail-trematode life history interactions: past trends and future directions. Parasitology 2001, 123(Suppl):S3-18.
86. Sousa W.P. Size-Dependent Predation on the Salt-Marsh Snail Cerithidea-Californica Haldeman. Journal of Experimental Marine Biology and Ecology 1993, 166:19-37.
87. Southgate V.R., Brown D.S., Warlow A., Knowles R.J., Jones A. The influence of Calicophoron microbothrium on the susceptibility of Bulinus tropicus to Schistosoma bovis. Parasitol Res 1989, 75:381-391.
88. Stroschein-Stevenson S.L., Foley E., O'Farrell P.H., Johnson A.D. Identification of Drosophila gene products required for phagocytosis of Candida albicans. PLoS Biol 2006, 4:e4.
89. Suderman R.J., Pruijssers A.J., Strand M.R. Protein tyrosine phosphatase-H2 from a polydnavirus induces apoptosis of insect cells. J Gen Virol 2008, 89:1411-1420.
90. Takamatsu N., Shiba T., Muramoto K., Kamiya H. Molecular cloning of the defense factor in the albumen gland of the sea hare Aplysia kurodai. FEBS Lett 1995, 377:373-376.
91. Vasta G.R., Quesenberry M., Ahmed H., O'Leary N. C-type lectins and galectins mediate innate and adaptive immune functions: their roles in the complement activation pathway. Dev Comp Immunol 1999, 23:401-420.
92. Vergote D., Bouchut A., Sautiere P.E., Roger E., Galinier R., Rognon A., Coustau C., Salzet M., Mitta G. Characterisation of proteins differentially present in the plasma of Biomphalaria glabrata susceptible or resistant to Echinostoma caproni. Int J Parasitol 2005, 35:215-224.
93. Vermeire J.J., Yoshino T.P. Antioxidant gene expression and function in in vitro-developing Schistosoma mansoni mother sporocysts: possible role in self-protection. Parasitology 2007, 134:1369-1378.
94. Wang Z., Wu Z., Jian J., Lu Y. Cloning and expression of heat shock protein 70 gene in the haemocytes of pearl oyster (Pinctada fucata, Gould 1850) responding to bacterial challenge. Fish Shellfish Immunol 2009, 26:639-645.
95. Wertheim B., Kraaijeveld A.R., Schuster E., Blanc E., Hopkins M., Pletcher S.D., Strand M.R., Partridge L., Godfray H.C.J. Genome-wide gene expression in response to parasitoid attack in Drosophila. Genome Biology 2005, 6:R94.
96. Wu X.J., Sabat G., Brown J.F., Zhang M., Taft A., Peterson N., Harms A., Yoshino T.P. Proteomic analysis of Schistosoma mansoni proteins released during in vitro miracidium-to-sporocyst transformation. Mol Biochem Parasitol 2009, 164:32-44.
97. Yang X.L., Cox-Foster D.L. Impact of an ectoparasite on the immunity and pathology of an invertebrate: Evidence for host immunosuppression and viral amplification. Proceedings of the National Academy of Sciences of the United States of America 2005, 102:7470-7475.
98. Yoshino T.P., Bayne C.J. Mimicry of snail host antigens by miracidia and primary sporocysts of Schistosoma mansoni. Parasite Immunol 1983, 5:317-328.
99. Yoshino T.P., Dinguirard N., Kunert J., Hokke C.H. 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 2008, 411:46-58.
100. Zavalova L.L., Yudina T.G., Artamonova, Baskova I.P. Antibacterial non-glycosidase activity of invertebrate destabilase-lysozyme and of its helical amphipathic peptides. Chemotherapy 2006, 52:158-160.
101. Zelck U.E., Von Janowsky B. Antioxidant enzymes in intramolluscan Schistosoma mansoni and ROS-induced changes in expression. Parasitology 2004, 128:493-501.
102. Zhang H., Wang H., Wang L., Song L., Song X., Zhao J., Li L., Qiu L. Cflec-4, a multidomain C-type lectin involved in immune defense of Zhikong scallop Chlamys farreri. Dev Comp Immunol 2009, 33:780-788.
103. Zhang S.M., Loker E.S. The FREP gene family in the snail Biomphalaria glabrata: additional members, and evidence consistent with alternative splicing and FREP retrosequences. Fibrinogen-related proteins. Dev Comp Immunol 2003, 27:175-187.
104. Zhang S.M., Loker E.S. Representation of an immune responsive gene family encoding fibrinogen-related proteins in the freshwater mollusc Biomphalaria glabrata, an intermediate host for Schistosoma mansoni. Gene 2004, 341:255-266.
105. Zhang S.M., Loker E.S. Representation of an immune responsive gene family encoding fibrinogen-related proteins in the freshwater mollusc Biomphalaria glabrata, an intermediate host for Schistosoma mansoni. Gene 2004, 341:255-266.
106. Zhang S.M., Zeng Y., 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 2007, 59:883-898.
107. Zhang S.M., Nian H., Zeng Y., 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 2008, 32:1119-1130.
108. Zhang S.M., Nian H., Zeng Y., 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. Developmental and Comparative Immunology 2008, 32:1119-1130.
109. Zhang S.M., Zeng Y., Loker E.S. Expression profiling and binding properties of fibrinogen-related proteins (FREPs), plasma proteins from the schistosome snail host Biomphalaria glabrata. Innate Immun 2008, 14:175-189.
110. Zhang Y., Yan F., Hu Z., Zhao X., Min S., Du Z., Zhao S., Ye X., Li Y. Hemocyanin from shrimp Litopenaeus vannamei shows hemolytic activity. Fish Shellfish Immunol 2009, 27:330-335.
111. Zhuang Z.H., Zhou Y., Yu M.C., Silverman N., Ge B.X. Regulation of Drosophila p38 activation by specific MAP2 kinase and MAP3 kinase in response to different stimuli. Cell Signal 2006, 18:441-448.
112. Zou Z., Jiang H. Manduca sexta serpin-6 regulates immune serine proteinases PAP-3 and HP8. cDNA cloning, protein expression, inhibition kinetics, and function elucidation. J Biol Chem 2005, 280:14341-14348.
113. Zou Z., Picheng Z., Weng H., Mita K., Jiang H. A comparative analysis of serpin genes in the silkworm genome. Genomics 2009, 93:367-375.
114. Zuniga E., Motran C., Montes C.L., Diaz F.L., Bocco J.L., Gruppi A. Trypanosoma cruzi-induced immunosuppression: B cells undergo spontaneous apoptosis and lipopolysaccharide (LPS) arrests their proliferation during acute infection. Clin Exp Immunol 2000, 119:507-515.