Profiling of gender-specific gene expression for Trichostrongylus vitrinus (Nematoda: Strongylida) by microarray analysis of expressed sequence tag libraries constructed by suppressive-subtractive hybridisation

International Journal for Parasitology

Volumn 34, Issue 5, 2004, Pages 633-643

  Nisbet, Alasdair J ^a   Gasser, Robin B ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Embryogenesis; Nematode reproduction; Oogenesis; Sex specific genes; Spermatogenesis

Indexed keywords

CHAPERONIN; COMPLEMENTARY DNA; HEAT SHOCK PROTEIN; ISOPROTEIN; PHOSPHOPROTEIN PHOSPHATASE; PROTEASOME; PROTEIN KINASE; VITELLOGENIN;

GENE EXPRESSION; HYBRIDIZATION; NEMATODE;

ANALYTIC METHOD; ANIMAL TISSUE; ARTICLE; CAENORHABDITIS ELEGANS; CARBOHYDRATE METABOLISM; CHROMATIN CONDENSATION; CONTROLLED STUDY; DNA MICROARRAY; EMBRYO DEVELOPMENT; EXPRESSED SEQUENCE TAG; FEMALE; GAMETOGENESIS; GENDER; GENE EXPRESSION PROFILING; GENE FUNCTION; GENE SEQUENCE; GENETIC TRANSCRIPTION; MALE; MICROBIAL GENETICS; NEMATODE; NONHUMAN; PROTEIN PROTEIN INTERACTION; REPRODUCTION; SEQUENCE HOMOLOGY; SEX DIFFERENCE; SIGNAL TRANSDUCTION; SUPPRESSION SUBTRACTIVE HYBRIDIZATION; TRICHOSTRONGYLUS VITRINUS; UBIQUITINATION;

ANIMALS; BASE SEQUENCE; CAENORHABDITIS ELEGANS; DNA, CIRCULAR; DNA, HELMINTH; FEMALE; GENE EXPRESSION PROFILING; MALE; MOLECULAR SEQUENCE DATA; NUCLEIC ACID HYBRIDIZATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY, NUCLEIC ACID; SEX FACTORS; SHEEP; TRICHOSTRONGYLUS;

CAENORHABDITIS; CAENORHABDITIS ELEGANS; NEMATODA; STRONGYLIDA; TRICHOSTRONGYLUS; TRICHOSTRONGYLUS VITRINUS;

EID: 1842506391     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpara.2003.12.007     Document Type: Article

References (61)

1. Aboobaker A.A., Blaxter M.L. Use of RNA interference to investigate gene function in the human filarial nematode parasite Brugia malayi. Mol. Biochem. Parasitol. 129:2003;41-51.
2. Bei Y., Hogan J., Berkowitz L.A., Soto M., Rocheleau C.E., Pang K.M., Collins J., Mello C.C. SRC-1 and Wnt signaling act together to specify endoderm and to control cleavage orientation in early C. elegans embryos. Dev. Cell. 3:2002;113-125.
3. 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. 155:2000;85-104.
4. Blaxter M.L. Caenorhabditis elegans is a nematode. Science. 282:1998;2041-2046.
5. Blaxter M.L., De Ley P., Garey J., Liu L.X., Scheldeman P., Vierstraete A., Vanfleteren J., Mackey L.Y., Dorris M., Frisse L.M., Vida J.T., Thomas W.K. A molecular evolutionary framework for the phylum Nematoda. Nature. 392:1998;71-75.
6. Boag P.R., Newton S.E., Hansen N.P., Christensen C.M., Nansen P., Gasser R.B. Isolation and characterisation of sex-specific transcripts from Oesophagostomum dentatum by RNA arbitrarily-primed PCR. Mol. Biochem. Parasitol. 108:2000;217-224.
7. Boag P.R., Newton S.E., Gasser R.B. Molecular aspects of sexual development and reproduction in nematodes and schistosomes. Adv. Parasitol. 50:2001;153-198.
8. Boag P.R., Ren P., Newton S.E., Gasser R.B. Molecular characterisation of a male-specific serine/threonine phosphatase from Oesophagostomum dentatum (Nematoda: Strongylida), and functional analysis of homologues in Caenorhabditis elegans. Int. J. Parasitol. 33:2003;313-325.
9. Brooks D.R., Isaac R.E. Functional genomics of parasitic worms: the dawn of a new era. Parasitol. Int. 51:2002;319-325.
10. Clark S.G., Stern M.J., Horvitz H.R. C. elegans cell-signalling gene sem-5 encodes a protein with SH2 and SH3 domains. Nature. 356:1992;340-344.
11. Cox D.N., Chao A., Baker J., Chang L., Qiao D., Lin H. A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewal. Genes Dev. 12:1998;3715-3727.
12. Doenecke D., Drabent B., Bode C., Bramlage B., Franke K., Gavenis K., Kosciessa U., Witt O. Histone gene expression and chromatin structure during spermatogenesis. Adv. Exp. Med. Biol. 424:1997;37-48.
13. Gasser R.B., Newton S.E. Genomic and genetic research on bursate nematodes: significance, implications and prospects. Int. J. Parasitol. 30:2000;509-534.
14. Geary T.G., Sangster N.C., Thompson D.P. Frontiers in anthelmintic pharmacology. Vet. Parasitol. 84:1999;275-295.
15. Grant B., Hirsh D. Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Mol. Biol. Cell. 10:1999;4311-4326.
16. Hanazawa M., Mochii M., Ueno N., Kohara Y., Iino Y. Use of cDNA subtraction and RNA interference screens in combination reveals genes required for germ-line development in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA. 98:2001;8686-8691.
17. Harris B.Z., Lim W.A. Mechanism and role of PDZ domains in signaling complex assembly. J. Cell Sci. 114:2001;3219-3231.
18. Hashmi S., Tawe W., Lustigman S. Caenorhabditis elegans and the study of gene function in parasites. Trends Parasitol. 17:2001;387-393.
19. Hershko A., Ciechanover A. The ubiquitin system. Annu. Rev. Biochem. 67:1998;425-479.
20. Hoekstra R., Visser A., Otsen M., Tibben J., Lenstra J.A., Roos M.H. EST sequencing of the parasitic nematode Haemonchus contortus suggests a shift in gene expression during transition to the parasitic stages. Mol. Biochem. Parasitol. 110:2000;53-68.
21. Hu M., Chilton N.B., Gasser R.B. The mitochondrial genome of Strongyloides stercoralis (Nematoda) - idiosyncratic gene order and evolutionary implications. Int. J. Parasitol. 33:2003;1393-1408.
22. Hussein A.S., Kichenin K., Selkirk M.E. Suppression of secreted acetylcholinesterase expression in Nippostrongylus brasiliensis by RNA interference. Mol. Biochem. Parasitol. 122:2002;91-94.
23. Jedrusik M.A., Schulze E. A single histone H1 isoform (H1.1) is essential for chromatin silencing and germline development in Caenorhabditis elegans. Development. 128:2001;1069-1080.
24. Jiang M., Ryu J., Kiraly M., Duke K., Reinke V., Kim S. Genome-wide analysis of developmental and sex-regulated gene expression profiles in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA. 98:2001;218-223.
25. Josefsberg L.B., Dekel N. Translational and post-translational modifications in meiosis of the mammalian oocyte. Mol. Cell. Endocrinol. 187:2002;161-171.
26. Kamath R.S., Fraser A.G., Dong Y., Poulin G., Durbin R., Gotta M., Kanapin A., Le Bot N., Moreno S., Sohrmann M., Welchman D.P., Zipperlen P., Ahringer J. Systematic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature. 42:2003;231-237.
27. Kerr M.K., Churchill G.A. Bootstrapping cluster analysis: Assessing the reliability of conclusions from microarray experiments. Proc. Natl. Acad. Sci. USA. 98:2001;8961-8965.
28. Le Jambre L.F., Gill J.H., Lenane I.J., Baker P. Inheritance of avermectin resistance in Haemonchus contortus. Int. J. Parasitol. 30:2000;105-111.
29. Linder B., Jin Z., Freedman J.H., Rubin C.S. Molecular characterization of a novel, developmentally regulated small embryonic chaperone from Caenorhabditis elegans. J. Biol. Chem. 271:1996;30158-30166.
30. Ma J., Katz E., Belote J.M. Expression of proteasome subunit isoforms during spermatogenesis in Drosophila melanogaster. Insect Mol. Biol. 11:2002;627-639.
31. Maeda I., Kohara Y., Yamamoto M., Sugimoto A. Large-scale analysis of gene function in Caenorhabditis elegans by high-throughput RNAi. Curr. Biol. 11:2001;171-176.
32. MAFF. Manual of Veterinary Parasitological Laboratory Techniques. Technical Bulletin 18. 1977;Her Majesty's Stationary Office, London, UK.
33. Mak C.H., Sun K.W., Ko R.C. Identification of some heat-induced genes of Trichinella spiralis. Parasitology. 123:2001;293-300.
34. McCarrey J.R., Thomas K. Human testis-specific PGK gene lacks introns and possesses characteristics of a processed gene. Nature. 326:1987;501-505.
35. Miller M.A., Nguyen V.Q., Lee M., Kosinski M., Schedl T., Caprioli R.M., Greenstein D. A sperm cytoskeletal protein that signals oocyte meiotic maturation and ovulation. Nature. 291:2001;2144-2147.
36. Miller M.A., Ruest P.J., Kosinski M., Hanks S.T., Greenstein D. An Eph receptor sperm-sensing control mechanism for oocyte meiotic maturation in Caenorhabditis elegans. Genes Dev. 17:2003;187-200.
37. Moghal N., Sternberg P.W. The epidermal growth factor system in Caenorhabditis elegans. Exp. Cell Res. 284:2003;150-159.
38. Mori C., Welch J.E., Fulcher K.D., O'Brien D.A., Eddy E.M. Unique hexokinase messenger ribonucleic acids lacking the porin-binding domain are developmentally expressed in mouse spermatogenic cells. Biol. Reprod. 49:1993;191-203.
39. Nakamura N., Komiyama M., Fujioka M., Mori C. Sorting specificity of spermatogenic cell specific region of mouse hexokinase-s (mHk1-s). Mol. Reprod. Dev. 64:2003;113-119.
40. Newton S.E., Munn E.A. The development of vaccines against gastrointestinal nematode parasites, particularly Haemonchus contortus. Parasitol. Today. 15:1999;116-122.
41. Newton S.E., Boag P.R., Gasser R.B. Opportunities and prospects for investigating developmentally regulated and sex-specific genes and their expression in intestinal nematodes of humans. Holland C.V., Kennedy M.W. World Class Parasites: Volume 2. The Geohelminths: Ascaris, Trichuris and Hookworm. 2002;235-268 Kluwer, Boston.
42. Piano F., Schetter A.J., Morton D.G., Gunsalus K.C., Reinke V., Kim S.K., Kemphues K.J. Gene clustering based on RNAi phenotypes of ovary-enriched genes in C. elegans. Curr. Biol. 12:2002;1959-1964.
43. Powell-Coffman J.A., Knight J., Wood W.B. Onset of C. elegans gastrulation is blocked by inhibition of embryonic transcription with an RNA polymerase antisense RNA. Dev. Biol. 178:1996;472-483.
44. Quackenbush J. Microarray data normalization and transformation. Nat. Genet. 32:2002;496-501.
45. Reinke V., Smith H.E., Nance J., Wang J., Van Doren C., Begley R., Jones S.J.M., Davis E.B., Scherer S., Ward S., Kim S.K. A global profile of germline gene expression in C. elegans. Mol. Cell. 6:2000;605-616.
46. Riddle D.L., Blumenthal T., Meyer B.J., Priess J.R. C. elegans II. 1997;Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
47. Roberts T.M., Stewart M. Acting like actin: the dynamics of the nematode major sperm protein (MSP) cytoskeleton indicate a push-pull mechanism for amoeboid cell motility. J. Cell Biol. 149:2000;7-12.
48. Rogalski T.M., Bullerjahn A.M., Riddle D.L. Lethal and amanitin-resistance mutations in the Caenorhabditis elegans ama-1 and ama-2 genes. Genetics. 120:1988;409-422.
49. Schmitt-Wrede H.P., Waldraff A., Krücken J., Harder A., Wunderlich F. Characterization of a hexokinase encoding cDNA of the parasitic nematode Haemonchus contortus. Biochim. Biophys. Acta. 1444:1999;439-444.
50. Shim E.Y., Walker A.K., Shi Y., Blackwell T.K. CDK-9/cyclin T (P-TEFb) is required in two postinitiation pathways for transcription in the C. elegans embryo. Genes Dev. 16:2002;2135-2146.
51. Smith P., Leung-Chiu W.M., Montgomery R., Orsborn A., Kuznicki K., Gressman-Coberly E., Mutapcic L., Bennett K. The GLH proteins, Caenorhabditis elegans P granule components, associate with CSN-5 and KGB-1, proteins necessary for fertility, and with ZYX-1, a predicted cytoskeletal protein. Dev. Biol. 251:2002;333-347.
52. Smyth G.K., Yang Y.H., Speed T. Statistical issues in cDNA microarray analysis. Methods Mol. Biol. 224:2003;111-136.
53. Steger K., Klonisch T., Gavenis K., Drabent B., Doenecke D., Bergmann M. Expression of mRNA and protein of nucleoproteins during human spermiogenesis. Mol. Hum. Reprod. 4:1998;939-945.
54. Sutovsky P. Ubiquitin-dependent proteolysis in mammalian spermatogenesis, fertilization, and sperm quality control: killing three birds with one stone. Microsc. Res. Tech. 61:2003;88-102.
55. Takai Y., Sasaki T., Matozaki T. Small GTP-binding proteins. Physiol. Rev. 81:2001;153-208.
56. Thamsborg S.M., Roepstorff A., Larsen M. Integrated and biological control of parasites in organic and conventional production systems. Vet. Parasitol. 84:1999;169-186.
57. The C. elegans Sequencing Consortium. Genome sequence of the nematode C. elegans: a platform for investigating biology. Science. 282:1998;2012-2018.
58. Urwin P.E., Lilley C.J., Atkinson H.J. Ingestion of double-stranded RNA by preparasitic juvenile cyst nematodes leads to RNA interference. Mol. Plant Microbe Interact. 15:2002;747-752.
59. Walhout A.J., Reboul J., Shtanko O., Bertin N., Vaglio P., Ge H., Lee H., Doucette-Stamm L., Gunsalus K.C., Schetter A.J., Morton D.G., Kemphues K.J., Reinke V., Kim S.K., Piano F., Vidal M. Integrating interactome, phenome, and transcriptome mapping data for the C. elegans germline. Curr. Biol. 12:2002;1952-1958.
60. Welch J.E., Schatte E.C., O'Brien D.A., Eddy E.M. Expression of a glyceraldehyde 3-phosphate dehydrogenase gene specific to mouse spermatogenic cells. Biol. Reprod. 46:1992;869-878.
61. Yang G.P., Ross D.T., Kuang W.W., Brown P.O., Weigel R.J. Combining SSH and cDNA microarrays for rapid identification of differentially expressed genes. Nucleic Acids Res. 27:1999;1517-1523.