Molecular characterisation of the recovery process in the entomopathogenic nematode Heterorhabditis bacteriophora

International Journal for Parasitology

Volumn 43, Issue 10, 2013, Pages 843-852

  Moshayov, Anat ^a   Koltai, Hinanit ^a   Glazer, Itamar ^a  

^a VOLCANI CENTER   (Israel)

Author keywords

Caenorhabditis elegans; Genetic pathways; Infective juveniles; Insect parasitic nematodes; Recovery

Indexed keywords

DOUBLE STRANDED RNA; SOMATOMEDIN C;

BIOASSAY; ENTOMOPATHOGENIC ORGANISM; GENE EXPRESSION; GROWTH RESPONSE; HOST-PARASITE INTERACTION; JUVENILE; MOLECULAR ANALYSIS; NEMATODE; PARASITISM;

ARTICLE; BIOASSAY; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; ENTOMOPATHOGENIC NEMATODE; GENE EXPRESSION; GENE IDENTIFICATION; GENE SILENCING; GENETIC TRANSCRIPTION; HETERORHABDITIS BACTERIOPHORA; HOST PARASITE INTERACTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PARASITISM; QUANTITATIVE ASSAY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

CAENORHABDITIS ELEGANS; HETERORHABDITIS BACTERIOPHORA; HEXAPODA; NEMATODA;

EID: 84881548061     PISSN: 00207519     EISSN: 18790135     Source Type: Journal    
DOI: 10.1016/j.ijpara.2013.05.009     Document Type: Article

References (57)

1. AbuHatab M., Selvan S., Gaugler R. Role of proteases in penetration of insect gut by the entomopathogenic nematode Steinernema glaseri (Nematoda: Steinernematidae). J. Invertebr. Pathol. 1995, 66:125-130.
2. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J. Mol. Biol. 1990, 215:403-410.
3. Apweiler R., Bairoch A., Wu C.H., Barker W.C., Boeckmann B., Ferro S., Gasteiger E., Huang H., Lopez R., Magrane M., Martin M.J., Natale D.A., O'Donovan C., Redaschi N., Yeh L.S. UniProt: the universal protein knowledge base. Nucleic Acids Res. 2004, 32:D115-D119.
4. Beall M.J., Pearce E.J. Transforming growth factor-beta and insulin-like signalling pathways in parasitic helminthes. Int. J. Parasitol. 2002, 32:399-404.
5. Birnby D.A., Link E.M., Vowels J.J., Tian H., Colacurcio P.L., Thomas J.H. A transmembrane guanylyl cyclase (DAF-11) and Hsp90 (DAF-21) regulate a common set of chemosensory behaviors in Caenorhabditis elegans. Genetics 2000, 155:85-104.
6. Blaxter M.L., De Ley P., Garey J.R., Liu L.X., Scheldeman P., Vierstraete A., Vanfleteren J.R., Mackey L.Y., Dorris M., Frisse L.M., Vida J.T., Thomas W.K. A molecular evolutionary framework for the phylum Nematoda. Nature 1998, 392:71-75.
7. Burnell A.M., Houthoofd K., O'Hanlon K., Vanfleteren J.R. Alternate metabolism during the dauer stage of the nematode Caenorhabditis elegans. Exp. Gerontol. 2005, 40:850-856.
8. Caenorhabditis elegans Sequencing Consortium Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 1998, 282:2012-2018.
9. Ciche T.A., Ensign J.C. For the insect pathogen Photorhabdus luminescens, which end of a nematode is out?. Appl. Environ. Microbiol. 2003, 69:1890-1897.
10. Ciche T.A., Sternberg P.W. Postembryonic RNAi in Heterorhabditis bacteriophora: a nematode insect parasite and host for insect pathogenic symbionts. BMC Dev. Biol. 2007, 7:101-111.
11. Ehlers R.U. Current and future use of nematodes in biocontrol: practice and commercial aspects in regard to regulatory policies. Biocontrol Sci. Technol. 1996, 6:303-316.
12. Ehlers R.U. Mass production of entomopathogenic nematodes for plant protection. Appl. Microbiol. Biotechnol. 2001, 56:623-633.
13. Ehlers R.U., Lunau S., Krasomil-Osterfeld K., Osterfeld K.H. Liquid culture of the entomopathogenic nematode-bacterium complex Heterorhabditis megidis/Photorhabdus luminescens. Biocontrol 1998, 43:77-86.
14. Encalada E.S., Willis J., Lyczak R., Bowerman B. A spindle checkpoint functions during mitosis in the early Caenorhabditis elegans embryo. Mol. Biol. Cell 2005, 16:1056-1070.
15. Ghedin E., Wang S., Spiro D., Caler E., Zhao Q., Crabtree J., Allen J.E., Delcher A.L., Guiliano D.B., Miranda-Saavedra D., Angiuoli S.V., Creasy T., Amedeo P., Haas B., El-Sayed N.M., Wortman J.R., Feldblyum T., Tallon L., Schatz M., Shumway M., Koo H., Salzberg S.L., Schobel S., Pertea M., Pop M., White O., Barton G.J., Carlow C.K., Crawford M.J., Daub J., Dimmic M.W., Estes C.F., Foster J.M., Ganatra M., Gregory W.F., Johnson N.M., Jin J., Komuniecki R., Korf I., Kumar S., Laney S., Li B.W., Li W., Lindblom T.H., Lustigman S., Ma D., Maina C.V., Martin D.M., McCarter J.P., McReynolds L., Mitreva M., Nutman T.B., Parkinson J., Peregrín-Alvarez J.M., Poole C., Ren Q., Saunders L., Sluder A.E., Smith K., Stanke M., Unnasch T.R., Ware J., Wei A.D., Weil G., Williams D.J., Zhang Y., Williams S.A., Fraser-Liggett C., Slatko B., Blaxter M.L., Scott A.L. Draft genome of the filarial nematode parasite Brugia malayi. Science 2007, 317:756-760.
16. Glazer I. Survival biology. Entomopathogenic Nematology 2002, 169-187. CABI Publishing, Wallingford, UK. R. Gaugler (Ed.).
17. Golden J.W., Riddle D.L. A pheromone influences larval development in the nematode Caenorhabditis elegans. Science 1982, 218:578-580.
18. Gomes A.V., Potter J.D., Szczesna-Cordary D. The role of troponins in muscle contraction. IUBMB Life 2002, 54:323-333.
19. Greenwald, I., 2005. LIN-12/Notch signaling in C. elegans. In: The C. elegans Research Community (Ed.), WormBook. doi/10.1895/wormbook.1.10.1, http://www.wormbook.org.
20. Han R., Ehlers R.U. Pathogenicity, development, and reproduction of Heterorhabditis bacteriophora and Steinernema carpocapsae under axenic in vivo conditions. J. Invertebr. Pathol. 2000, 75:55-58.
21. Henkle-Duhrsen K., Kampkotter A. Antioxidant enzyme families in parasitic nematodes. Mol. Biochem. Parasitol. 2001, 114:129-142.
22. Hirao A., Ehlers R.U. Influence of cell density and phase variants of bacterial symbionts (Xenorhabdus spp.) on dauer juvenile recovery and development of biocontrol nematodes Steinernema carpocapsae and S. feltiae (Nematoda: Rhabditida). Appl. Microbiol. Biotechnol. 2009, 84:77-85.
23. Hirao A., Ehlers R.U. Influence of inoculum density on population dynamics and dauer juvenile yields in liquid culture of biocontrol nematodes Steinernema carpocapsae and S. feltiae (Nematoda: Rhabditida). Appl. Microbiol. Biotechnol. 2010, 85:507-515.
24. Holway A.H., Hung C., Michael W.M. Systematic, RNA-interference mediated identification of mus-101 modifier genes in Caenorhabditis elegans. Genetics 2005, 169:1451-1460.
25. Holway A.H., Kim S.H., La Volpe A., Michael W.M. Checkpoint silencing during the DNA damage response in Caenorhabditis elegans embryos. J. Cell Biol. 2006, 172:999-1008.
26. Hoogewijs D., De Henau S., Dewilde S., Moens L., Couvreur M., Borgonie G., Vinogradov S.N., Roy S.W., Vanfleteren J.R. The Caenorhabditis globin gene family reveals extensive nematode-specific radiation and diversification. BMC Evol. Biol. 2008, 8:279-291.
27. Hu, P.J., 2007. Dauer. In: The C. elegans Research Community (Ed.), WormBook. doi/10.1895/wormbook.1.144.1, http://www.wormbook.org.
28. Jacob J., Vanholme B., Haegeman A., Gheysen G. Four transthyretin-like genes of the migratory plant-parasitic nematode Radopholus similis: members of an extensive nematode-specific family. Gene 2007, 402:9-19.
29. Johnigk S.A., Ecke F., Poehling M., Ehlers R.U. Liquid culture mass production of biocontrol nematodes, Heterorhabditis bacteriophora (Nematoda: Rhabditida): improved timing of dauer juvenile inoculation. Appl. Microbiol. Biotechnol. 2004, 64:651-658.
30. Jones S.J., Riddle D.L., Pouzyrev A.T., Velculescu V.E., Hillier L., Eddy S.R., Stricklin S.L., Baillie D.L., Waterston R., Marra M.A. Changes in gene expression associated with developmental arrest and longevity in Caenorhabditis elegans. Genome Res. 2001, 11:1346-1352.
31. Kanehisa M., Goto S. KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 2000, 28:27-30.
32. Kaya H.K., Stock S.P. Techniques in insect nematology. Manual of Techniques in Insect Pathology 1997, 281-324. Academic Press, San Diego. L.A. Lacey (Ed.).
33. Kelleher D.J., Gilmore R. An evolving view of the eukaryotic oligosaccharyltransferase. Glycobiology 2006, 16:47R-62R.
34. Kennedy M.W., Britton C., Price N.C., Kelly S.M., Cooper A. The DvA-1 polyprotein of the parasitic nematode Dictyocaulus viviparus. A small helix-rich lipid-binding protein. J. Biol. Chem. 1995, 270:19277-19281.
35. Kim S.H., Michael W.M. Regulated proteolysis of DNA polymerase eta during the DNA-damage response in C. elegans. Mol. Cell 2008, 32:757-766.
36. Kloor D., Osswald H. S-adenosylhomocysteine hydrolase as a target for intracellular adenosine action. Trends Pharmacol. Sci. 2004, 25:294-297.
37. Lin C.L., Leu S., Lu M.C., Ouyang P. Over-expression of SR-cyclophilin, an interaction partner of nuclear pinin, releases SR family splicing factors from nuclear speckles. Biochem. Biophys. Res. Commun. 2004, 321:638-647.
38. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25:402-408.
39. Loukas A., Maizels R.M. Helminth C-type lectins and host-parasite interactions. Parasitol. Today 2000, 16:333-339.
40. Martin J., Abubucker S., Heizer E., Taylor C.M., Mitreva M. Nematode.net update 2011: addition of data sets and tools featuring next-generation sequencing data. Nucleic Acids Res. 2011, 40:1-9.
41. McDermott L., Moore J., Brass A., Price N.C., Kelly S.M., Cooper A., Kennedy M.W. Mutagenic and chemical modification of the ABA-1 allergen of the nematode Ascaris: consequences for structure and lipid binding properties. Biochemistry 2001, 40:9918-9926.
42. McElwee J.J. Addressing the age-old question of old age. Genome Biol. 2004, 5:337.
43. Mende V.N., Bird D.M., Albert P.S., Riddle D.L. Dpy-13: a nematode collagen gene that affects body shape. Cell 1988, 55:567-576.
44. Morley J.F., Morimoto R.I. Regulation of longevity in Caenorhabditis elegans by heat shock factor and molecular chaperones. Mol. Biol. Cell 2004, 15:657-664.
45. Ouellet J., Li S., Roy R. Notch signalling is required for both dauer maintenance and recovery in C. elegans. Development 2008, 135:2583-2592.
46. Paradis S., Ruvkun G. Caenorhabditis elegans Akt/PKB transduces insulin receptor-like signals from AGE-1 PI3 kinase to the DAF-16 transcription factor. Gene Dev. 1998, 12:2488-2498.
47. Parkinson J., Mitreva M., Whitton C., Thomson M., Daub J., Martin J., Schmid R., Hall N., Barrell B., Waterston R.H., McCarter J.P., Blaxter M.L. A transcriptomic analysis of the phylum Nematoda. Nat. Genet. 2004, 36:1259-1267.
48. Rea L.S., Ventura N., Johnson T.E. Relationship between mitochondrial electron transport chain dysfunction, development, and life extension in Caenorhabditis elegans. PLoS Biol. 2007, 5:e259.
49. Riddle D.L., Albert P.S. C. elegans II 1997, Cold Spring Harbor Laboratory Press, Plainview, NY.
50. Saverwyns H., Visser A., Van Durme J., Power D., Morgado I., Kennedy M.W., Knox D.P., Schymkowitz J., Rousseau F., Gevaert K., Vercruysse J., Claerebout E., Geldhof P. Analysis of the transthyretin-like (TTL) gene family in Ostertagia ostertagi-comparison with other strongylid nematodes and Caenorhabditis elegans. Int. J. Parasitol. 2008, 38:1545-1556.
51. Seeler J.S., Dejean A. Nuclear and unclear functions of SUMO. Nat. Rev. Mol. Cell Biol. 2003, 4:690-699.
52. Sommerville R.I., Davey K.G. Diapause in parasitic nematodes: a review. Can. J. Zool. 2002, 80:1817-1840.
53. Strauch O., Ehlers R.U. Food signal production of Photorhabdus luminescens inducing the recovery of entomopathogenic nematodes Heterorhabditis spp. in liquid culture. Appl. Microbiol. Biotechnol. 1998, 50:369-374.
54. Tsang Y.W., Lemire B.D. The role of mitochondria in the life of the nematode, Caenorhabditis elegans. Biochim. Biophys. Acta 2003, 1638:91-105.
55. Tsang Y.W., Leanne S., Sayles C., Grad I.L., Pilgrim B.D., Lemire D.B. Mitochondrial respiratory chain deficiency in Caenorhabditis elegans results in developmental arrest and increased life span. J. Biol. Chem. 2001, 276:32240-32246.
56. Vinogradov S.N., Moens L. Diversity of globin function: enzymatic, transport, storage, and sensing. J. Biol. Chem. 2008, 283:8773-8777.
57. Wang J., Kim S.K. Global analysis of dauer gene expression in Caenorhabditis elegans. Development 2003, 130:1621-1634.