Transcripts analysis of the entomopathogenic nematode Steinernema carpocapsae induced in vitro with insect haemolymph

Molecular and Biochemical Parasitology

Volumn 169, Issue 2, 2010, Pages 79-86

  Hao, You Jin ^a   Montiel, Rafael ^a   Abubucker, Sahar ^b   Mitreva, Makedonka ^b   Simões, Nelson ^a  

^a UNIVERSITY OF THE AZORES   (Portugal)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Entomopathogenic nematode; EST; Nematode transcripts; Secreted proteins; Steinernema carpocapsae; Virulence factors

Indexed keywords

ACETYLCHOLINESTERASE; ANTIOXIDANT; ARABINOGALACTAN; ASPARTIC PROTEINASE; ASTACIN; CD36 ANTIGEN; COMPLEMENTARY DNA; CYSTEINE PROTEINASE; CYTOCHROME B; CYTOCHROME C OXIDASE; ELASTASE; GALECTIN; GLUTATHIONE TRANSFERASE; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; LECTIN; METALLOPROTEINASE; PREALBUMIN; PROTEINASE; PROTEINASE INHIBITOR; RETINOID BINDING PROTEIN; RIBOSOME PROTEIN; SERINE CARBOXYPEPTIDASE; SERINE PROTEINASE; SERINE PROTEINASE INHIBITOR; SPHINGOLIPID ACTIVATOR PROTEIN; TRYPSIN INHIBITOR; VIRULENCE FACTOR;

ARTICLE; CAENORHABDITIS ELEGANS; CLUSTER ANALYSIS; CONTROLLED STUDY; DNA LIBRARY; ENTOMOPATHOGENIC NEMATODE; EXPRESSED SEQUENCE TAG; GENE IDENTIFICATION; GENETIC TRANSCRIPTION; HEMOLYMPH; HOST PARASITE INTERACTION; IN VITRO STUDY; INNATE IMMUNITY; INSECT; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITE VIRULENCE; PATHOGENICITY; PEST CONTROL; PREDICTION; PRIORITY JOURNAL; PROTEIN DATABASE; PROTEIN FUNCTION; PROTEIN SECRETION; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; STEINERNEMA CARPOCAPSAE; STRESS; UNINDEXED SEQUENCE;

ANIMALS; EXPRESSED SEQUENCE TAGS; GENE EXPRESSION PROFILING; GENE LIBRARY; HELMINTH PROTEINS; HEMOLYMPH; INSECTS; RHABDITIDA; VIRULENCE FACTORS;

CAENORHABDITIS ELEGANS; HEXAPODA; NEMATODA; STEINERNEMA CARPOCAPSAE;

EID: 71949097069     PISSN: 01666851     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.molbiopara.2009.10.002     Document Type: Article

References (76)

1. Smart G.C. Entomopathogenic nematodes for the biological control of insects. J Nematol 27 (1995) 529-534
2. Lacey L.A., and Shapiro D.I. Microbial control of insect pests in temperate orchard systems: potential for incorporation into IPM. Annu Rev Entomol 53 (2008) 121-144
3. Martens E.C., and Goodrich-Blair H. The Steinernema carpocapsae intestinal vesicle contains a subcellular structure with which Xenorhabdus nematophila associates during colonization initiation. Cell Microbiol 7 (2005) 1723-1735
4. Grewal P.S., Lewis E.E., Gaugler R., and Campbell J.F. Host finding behavior as a predictor of foraging strategy in entomopathogenic nematodes. Parasitology 108 (1994) 207-215
5. Akhurst R.J., and Dunphy G.B. Tripartite interactions between symbiotically associated entomopathogenic bacteria, nematodes, and their insect hosts. In: Beckage N., Thompson S., and Frederici B. (Eds). Parasites and pathogens of insects vol. 1 (1993), Academic Press, New York 1-23
6. Klein M.G. Efficacy against soil-inhabiting insect pests. In: Gaugler R., and Kaya H. (Eds). Entomopathogenic nematodes in biological control vol. 10 (1990), CRC Press, Boston 195-214
7. Begley J.W. Efficacy against insects in habitats other than soils. In: Gaugler R., and Kaya H. (Eds). Entomopathogenic nematodes in biological control vol. 11 (1990), CRC Press, Boston 215-231
8. Schmid-Hempel P. Evolutionary ecology of insect immune defenses. Annu Rev Entomol 50 (2005) 529-551
9. Lemaitre B., and Hoffmann J. The host defense of Drosophila melanogaster. Annu Rev Immunol 25 (2007) 697-743
10. Dowds B.A., and Peters A. Virulence mechanisms. In: Gaugler R. (Ed). Entomopathogenic nematology vol. 4 (2000), CABI, New York 79-98
11. Cruz N., Rosa J.S., and Simões N. Encapsulation response of 6th instar of Pseudaletia unipuncta (Lepidoptera: Noctuidae) to Steinernema carpocapsae (Nematoda: Steinernematidae). J Invertebr Pathol 78 (2001) 272-274
12. Simões N., Caldas C., Rosa J.S., Bonifassi E., and Laumond C. Pathogenicity caused by high virulent and low virulent strains of Steinernema carpocapsae to Galleria mellonella. J Invertebr Pathol 75 (2000) 47-54
13. Forst S., Dowds B., Boemare N., and Stackebrandt E. Xenorhabdus and Photorhabdus spp.: bugs that kill bugs. Annu Rev Microbiol 51 (1997) 47-72
14. Sergeant M., Jarrett P., Ousley M., and Morgan J.A. Interactions of insecticidal toxin gene products from Xenorhabdus nematophilus PMFI296. Appl Environ Microbiol 69 (2003) 3344-3349
15. Boemare N., Laumond C., and Luciani J. Mise en évidence d'une toxicogenése provoquée par le nematode axénique entomophague Neoaplectana carpocapsae Weiser chez l'insect axénique Galleria mellonella. Acad Sci Ser D 295 (1982) 543-546
16. Burman M. Neoaplectana carpocapsae: toxin production by axenic insect parasitic nematodes. Nematologica 28 (1982) 62-70
17. Laumond C., Simões N., and Boemare N. Toxins of entomoparasitic nematodes. Pathogenicity of Steinernema carpocapsae-prospectives of genetic engineering. C R Acad Agric France 75 (1989) 135-138
18. Sandhu S.K., Jagdale G.B., Hogenhout S.A., and Grewal P.S. Comparative analysis of the expressed genome of the infective juvenile entomopathogenic nematode, Heterorhabditis bacteriophora. Mol Biochem Parasitol 145 (2006) 239-244
19. Bai X., Grewal P.S., Hogenhout S.A., et al. Expressed sequence tag analysis of gene representation in insect parasitic nematode Heterorhabditis bacteriophora. J Parasitol 93 (2007) 1343-1349
20. Mitreva M., Zarlenga D.S., McCarter J.P., and Jasmer D.P. Parasitic nematodes-from genomes to control. Vet Parasitol 148 (2007) 31-42
21. Bedding R.A. Long scale production, storage and transport of the insect parasitic nematodes Neoaplectana spp. and Heterorhabditis spp. Ann Appl Biol 104 (1984) 117-120
22. Mitreva M., McCarter J.P., Martin J., et al. Comparative genomics of gene expression in the parasitic and free-living nematodes Strongyloides stercoralis and Caenorhabditis elegans. Genome Res 14 (2004) 209-220
23. Altschul S.F., Gish W., Miller W., Myers E.W., and Lipman D.J. Basic local alignment search tool. J Mol Biol 215 (1990) 403-410
24. Conesa A., Gotz S., Garcia-Gomez J.M., Terol J., Talon M., and Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21 (2005) 3674-3676
25. Kanehisa M., and Goto S. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res 28 (2000) 27-30
26. Horton P., Park K.J., Obayashi T., et al. WoLF PSORT: protein localization predictor. Nucleic Acids Res 35 (2007) 585-587
27. Bendtsen J.D., Nielsen H., von Heijne G., and Brunak S. Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340 (2004) 783-795
28. Grenier E., Catzeflis F.M., and Abad P. Genome sizes of the entomopathogenic nematodes Steinernema carpocapsae and Heterorhabditis bacteriophora (Nematoda: Rhabditida). Parasitology 114 (1997) 497-501
29. Nollen E.A., Garcia S.M., van Haaften G., et al. Genome-wide RNA interference screen identifies previously undescribed regulators of polyglutamine aggregation. Proc Natl Acad Sci USA 101 (2004) 6403-6408
30. Rual J.F., Ceron J., Koreth J., et al. Toward improving Caenorhabditis elegans phenome mapping with an ORFeome-based RNAi library. Genome Res 14 (2004) 2162-2168
31. Balklava Z., Pant S., Fares H., and Grant B.D. Genome-wide analysis identifies a general requirement for polarity proteins in endocytic traffic. Nat Cell Biol 9 (2007) 1066-1073
32. Wylie T., Martin J.C., Dante M., et al. Nematode.net: a tool for navigating sequences from parasitic and free-living nematodes. Nucleic Acids Res 32 (2004) 423-426
33. McCarter J.P., Mitreva M.D., Martin J., et al. Analysis and functional classification of transcripts from the nematode Meloidogyne incognita. Genome Biol 4 (2003) R26
34. Posas F., Chambers J.R., Heyman J.A., Hoeffler J.P., Nadal E., and Arino J. The transcriptional response of yeast to saline stress. J Biol Chem 275 (2000) 17249-17255
35. Tyson T., Reardon W., Browne J.A., and Burnell A.M. Gene induction by desiccation stress in the entomopathogenic nematode Steinernema carpocapsae reveals parallels with drought tolerance mechanisms in plants. Int J Parasitol 37 (2007) 763-776
36. Sahi C., Agarwal M., Reddy M.K., Sopory S.K., and Grover A. Isolation and expression analysis of salt stress-associated ESTs from contrasting rice cultivars using a PCR-based subtraction method. Theor Appl Genet 106 (2003) 620-628
37. Gaspar Y.M., Nam J., Schultz C.J., et al. Characterization of the Arabidopsis lysine-rich arabinogalactan-protein AtAGP17 mutant (rat1) that results in a decreased efficiency of agrobacterium transformation. Plant Physiol 135 (2004) 2162-2171
38. Sun W., Xu J., Yang J., Kieliszewski M.J., and Showalter A.M. The lysine-rich arabinogalactan-protein subfamily in Arabidopsis: gene expression, glycoprotein purification and biochemical characterization. Plant Cell Physiol 46 (2005) 975-984
39. Vanholme B., Mitreva M., Van Criekinge W., et al. Detection of putative secreted proteins in the plant-parasitic nematode Heterodera schachtii. Parasitol Res 98 (2006) 414-424
40. Seo M., Kho B.M., Guk S.M., Lee S.H., and Chai J.Y. Radioresistance of Anisakis simplex third-stage larvae and the possible role of superoxide dismutase. J Parasitol 92 (2006) 416-418
41. Yin Y., Martin J., McCarter J.P., Clifton S.W., Wilson R.K., and Mitreva M. Identification and analysis of genes expressed in the adult filarial parasitic nematode Dirofilaria immitis. Int. J Parasitol 36 (2006) 829-839
42. Sonnhammer E.L., and Durbin R. Analysis of protein domain families in Caenorhabditis elegans. Genomics 46 (1997) 200-216
43. Jacob J., Vanholme B., Haegeman A., and Gheysen G. Four transthyretin-like genes of the migratory plant-parasitic nematode Radopholus similis: members of an extensive nematode-specific family. Gene 402 (2007) 9-19
44. Hewitson J.P., Harcus Y.M., Curwen R.S., et al. The secretome of the filarial parasite, Brugia malayi: proteomic profile of adult excretory-secretory products. Mol Biochem Parasitol 160 (2008) 8-21
45. Trap C., and Boireau P. Proteases in helminthic parasites. Vet Res 31 (2000) 461-471
46. Balasubramanian N., Hao Y.J., Toubarro D., Nascimento G., and Simões N. Purification, biochemical and molecular analysis of a chymotrypsin protease with prophenoloxidase suppression activity from the entomopothogenic nematode Steinernema carpocapsae. Int J Parasitol 39 (2009) 975-984
47. Toubarro D., Lucena-Robles M., Nascimento G., Costa G., Montiel R., Coelho A.V., et al. An apoptosis-inducing serine protease secreted by the entomopathogenic nematode Steinernema carpocapsae. Int J Parasitol 39 (2009) 1319-1330
48. Hao Y.J., Montiel R., Nascimento G., Toubarro D., and Simões N. Identification and expression analysis of the Steinernema carpocapsae elastase-like serine protease gene during the parasitic stage. Exp Parasitol 122 (2009) 51-60
49. Yang Z., Kyriakides T.R., and Bornstein P. Matricellular proteins as modulators of cell-matrix interactions: adhesive defect in thrombospondin 2-null fibroblasts is a consequence of increased levels of matrix metalloproteinase-2. Mol Biol Cell 11 (2000) 3353-3364
50. Tudor J.E., Pallaghy P.K., Pennington M.W., and Norton R.S. Solution structure of ShK toxin, a novel potassium channel inhibitor from a sea anemone. Nat Struct Biol 3 (1996) 317-320
51. Longbottom D., Redmond D.L., Russell M., Liddell S., Smith W.D., and Knox D.P. Molecular cloning and characterisation of a putative aspartate proteinase associated with a gut membrane protein complex from adult Haemonchus contortus. Mol Biochem Parasitol 88 (1997) 63-72
52. Gallego S.G., Slade R.W., and Brindley P.J. A cDNA encoding a pepsinogen-like, aspartic protease from the human roundworm parasite Strongyloides stercoralis. Acta Trop 71 (1998) 17-26
53. Williamson A.L., Brindley P.J., and Loukas A. Hookworm cathepsin D aspartic proteases: contributing roles in the host-specific degradation of serum proteins and skin macromolecules. Parasitology 126 (2003) 179-185
54. Sajid M., and McKerrow J.H. Cysteine proteases of parasitic organisms. Mol Biochem Parasitol 120 (2002) 1-21
55. Hao Y.J., Montiel R., Nascimento G., Toubarro D., and Simões N. Identification, characterization of functional candidate genes for host-parasite interactions in entomopathogenetic nematode Steinernema carpocapsae by suppressive subtractive hybridization. Parasitol Res 103 3 (2008) 671-683
56. Peanasky R.J., Bentz Y., Paulson B., Graham D.L., and Babin D.R. The isoinhibitors of chymotrypsin/elastase from Ascaris lumbricoides: isolation by affinity chromatography and association with the enzymes. Arch Biochem Biophys 232 (1984) 127-134
57. Morris S.R., and Sakanari J.A. Characterization of the serine protease and serine protease inhibitor from the tissue-penetrating nematode Anisakis simplex. J Biol Chem 269 (1994) 27650-27656
58. Zang X., and Maizels R.M. Serine proteinase inhibitors from nematodes and the arms race between host and pathogen. Trends Biochem Sci 26 (2001) 191-197
59. Hartmann S., and Lucius R. Modulation of host immune responses by nematode cystatins. Int J Parasitol 33 (2003) 1291-1292
60. Pritchard D.I., Brown A., and Toutant J.P. The molecular forms of acetylcholinesterase from Necator americanus (Nematoda), a hookworm parasite of the human intestine. Eur J Biochem 219 (1994) 317-323
61. Loukas A., and Maizels R.M. Helminth C-type lectins and host-parasite interactions. Parasitol Today 16 (2000) 333-339
62. Rabinovich G.A., Rubinstein N., and Toscano M.A. Role of galectins in inflammatory and immunomodulatory processes. Biochim Biophys Acta 1572 (2002) 274-284
63. Lee D.L. Why do some nematode parasites of the alimentary tract secrete acetylcholinesterase?. Int J Parasitol 26 (1996) 499-508
64. Kennedy M.W., Allen J.E., Wright A.S., McCruden A.B., and Cooper A. The gp15/400 polyprotein antigen of Brugia malayi binds fatty acids and retinoids. Mol Biochem Parasitol 71 (1995) 41-50
65. Prior A., Jones J.T., Blok V.C., et al. A surface-associated retinol- and fatty acid-binding protein (Gp-FAR-1) from the potato cyst nematode Globodera pallida: lipid binding activities, structural analysis and expression pattern. Biochem J 356 (2001) 387-394
66. Basavaraju S., Zhan B., Kennedy M.W., Liu Y., Hawdon J., and Hotez P.J. Ac-FAR-1, a 20 kDa fatty acid- and retinol-binding protein secreted by adult Ancylostoma caninum hookworms: gene transcription pattern, ligand binding properties and structural characterisation. Mol Biochem Parasitol 126 (2003) 63-71
67. Fetterer R.H., and Rhoads M.L. Characterization of haemolytic activity from adult Haemonchus contortus. Int J Parasitol 27 (1997) 1037-1040
68. Don T.A., Oksov Y., Lustigman S., and Loukas A. Saposin-like proteins from the intestine of the blood-feeding hookworm, Ancylostoma caninum. Parasitology 134 (2007) 427-436
69. Banyai L., and Patthy L. Amoebapore homologs of Caenorhabditis elegans. Biochim Biophys Acta 1429 (1998) 259-264
70. Alper S., McBride S.J., Lackford B., Freedman J.H., and Schwartz D.A. Specificity and complexity of the Caenorhabditis elegans innate immune response. Mol Cell Biol 27 (2007) 5544-5553
71. Kaufmann S.H.E. Heat-shock proteins: a missing in the host-parasite relationship?. Med Microbiol Immunol 179 (1990) 61-66
72. Somvanshi V.S., Koltai H., and Glazer I. Expression of different desiccation-tolerance related genes in various species of entomopathogenic nematodes. Mol Biochem Parasitol 158 (2008) 65-71
73. Ghosh I., Eisinger S.W., Raghavan N., and Scott A.L. Thioredoxin peroxidases from Brugia malayi. Mol Biochem Parasitol 91 (1998) 207-220
74. Lu W., Egerton G.L., Bianco A.E., and Williams S.A. Thioredoxin peroxidase from Onchocerca volvulus: a major hydrogen peroxide detoxifying enzyme in filarial parasites. Mol Biochem Parasitol 91 (1998) 221-235
75. Brophy P.M., and Pritchard D.I. Parasitic helminth glutathione S-transferases: an update on their potential as targets for immuno- and chemotherapy. Exp Parasitol 79 (1994) 89-96
76. Rojas J., Rodriguez-Osorio M., and Gomez-Garcia V. Immunological characteristics and localization of the Trichinella spiralis glutathione S-transferase. J Parasitol 83 (1997) 630-635