Gender-enriched transcripts in Haemonchus contortus - predicted functions and genetic interactions based on comparative analyses with Caenorhabditis elegans

International Journal for Parasitology

Volumn 38, Issue 1, 2008, Pages 65-83

  Campbell, Bronwyn E ^a   Nagaraj, Shivashankar H ^b   Hu, Min ^a   Zhong, Weiwei ^c   Sternberg, Paul W ^c   Ong, Eng K ^d   Loukas, Alex ^e   Ranganathan, Shoba ^b   Beveridge, Ian ^a   McInnes, Russell L ^f   Hutchinson, Gareth W ^g   Gasser, Robin B ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b MACQUARIE UNIVERSITY   (Australia)

^c CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^d MUSEUM VICTORIA   (Australia)

^e QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^f AGILENT TECHNOLOGIES   (Australia)

^g NSW DEPARTMENT OF PRIMARY INDUSTRIES   (Australia)

Author keywords

Development; Differential transcription; Gender; Haemonchus contortus; Nematode; Oligonucleotide microarray analysis; Prediction of function and genetic interactions; Reproduction

Indexed keywords

COMPARATIVE STUDY; DATABASE; DEVELOPMENTAL STAGE; GENETICS; HOMOLOGY; NEMATODE; RNA; RUMINANT;

ADOLESCENT; AMINO ACID TRANSPORT; ARTICLE; BOVIDS; CAENORHABDITIS ELEGANS; CARBOHYDRATE TRANSPORT; ENERGY YIELD; EXPRESSED SEQUENCE TAG; FEMALE; GENDER; GENE INTERACTION; HAEMONCHUS CONTORTUS; LIPID METABOLISM; LIPID TRANSPORT; MALE; MEIOSIS; MICROARRAY ANALYSIS; MITOSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; OOCYTE DEVELOPMENT; SPERMATOGENESIS;

ANIMALS; BASE SEQUENCE; CAENORHABDITIS ELEGANS; EXPRESSED SEQUENCE TAGS; FEMALE; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORKS; GENES, HELMINTH; HAEMONCHUS; HELMINTH PROTEINS; LARVA; MALE; MOLECULAR SEQUENCE DATA; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; TRANSCRIPTION, GENETIC;

CAENORHABDITIS ELEGANS; HAEMONCHUS CONTORTUS; NEMATODA;

EID: 37049037965     PISSN: 00207519     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijpara.2007.07.001     Document Type: Article

References (89)

1. Aboobaker A.A., and Blaxter M.L. Functional genomics for parasitic nematodes and platyhelminths. Trends Parasitol. 20 (2004) 178-184
2. Adrian G.S., McCammon M.T., Montgomery D.L., and Douglas M.G. Sequences required for delivery and localization of the ADP/ATP translocator to the mitochondrial inner membrane. Mol. Cell. Biol. 6 (1986) 626-634
3. Artal-Sanz M., and Tavernarakis N. Proteolytic mechanisms in necrotic cell death and neurodegeneration. FEBS Lett. 579 (2005) 3287-3296
4. Bendtsen J.D., Nielsen H., von Heijne G., and Brunak S. Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 340 (2004) 783-790
5. Besier B. New anthelmintics for livestock: the time is right. Trends Parasitol. 23 (2007) 21-24
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., and Thomas W.K. A molecular evolutionary framework for the phylum Nematoda. Nature 392 (1998) 71-75
7. Boag P.R., Newton S.E., and 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., and Gasser R.B. Molecular characterisation of a serine/threonine phosphatase of Oesophagostomum dentatum, and functional analysis of homologues in Caenorhabditis elegans. Int. J. Parasitol. 33 (2003) 313-325
9. Boxem M., Srinivasan D.G., and van den Heuvel S. The Caenorhabditis elegans gene ncc-1 encodes a cdc2-related kinase required for M phase in meiotic and mitotic cell divisions, but not for S phase. Development 126 (1999) 2227-2239
10. Brandt B.W., Zwaan B.J., Beekman M., Westendorp R.G., and Slagboom P.E. Shuttling between species for pathways of lifespan regulation: a central role for the vitellogenin gene family?. Bioessays 27 (2005) 339-346
11. Britton C., and Murray L. A cathepsin L protease essential for Caenorhabditis elegans embryogenesis is functionally conserved in parasitic nematodes. Mol. Biochem. Parasitol. 122 (2002) 21-33
12. Brown A., Girod N., Billett E.E., and Pritchard D.I. Necator americanus (human hookworm) aspartyl proteinases and digestion of skin macromolecules during skin penetration. Am. J. Trop. Med. Hyg. 60 (1999) 840-847
13. Coles G.C. The future of veterinary parasitology. Vet. Parasitol. 98 (2001) 31-39
14. Cottee P.A., Nisbet A.J., Boag P.R., Larsen M., and Gasser R.B. Major sperm protein of Oesophagostomum dentatum. Parasitology 129 (2004) 479-490
15. Cottee P.A., Nisbet A.J., Abs EL-Osta Y.G., Webster T.L., and Gasser R.B. Construction of gender-enriched cDNA archives for adult Oesophagostomum dentatum by suppressive subtractive hybridization and a microarray analysis of expressed sequence tags. Parasitology 132 (2006) 691-708
16. Coyne M.J., and Smith G. The mortality and fecundity of Haemonchus contortus in parasite-naive and parasite-exposed sheep following single experimental infections. Int. J. Parasitol. 22 (1992) 315-325
17. Dahout-Gonzalez C., Nury H., Trézéguet V., Lauquin G.J.-M., Pebay-Peyroula E., and Brandolin G. Molecular, functional, and pathological aspects of the mitochondrial ADP/ATP carrier. Physiology 21 (2006) 242-249
18. de la Cruz J., Sanz-Martinez E., and Remacha M. The essential WD-repeat protein Rsa4p is required for rRNA processing and intra-nuclear transport of 60S ribosomal subunits. Nucleic Acids Res. 33 (2005) 5728-5739
19. Fire A., Xu S., Montgomery M.K., Kostas S.A., Driver S.E., and Mello C.C. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391 (1998) 806-811
20. Geldhof P., Murray L., Couthier A., Gilleard J.S., McLauchlan G., Knox D.P., and Britton C. Testing the efficacy of RNA interference in Haemonchus contortus. Int. J. Parasitol. 36 (2006) 801-810
21. Geldhof P., Visser A., Clark D., Saunders G., Britton C., Gilleard J., Berriman M., and Knox D.P. RNA interference in parasitic helminths: current situation, potential pitfalls and future prospects. Parasitology 134 (2007) 609-619
22. Gilleard J.S. The use of Caenorhabditis elegans in parasitic nematode research. Parasitology 128 (2004) S49-S70
23. Gilleard J.S., Woods D.J., and Dow J.A. Model-organism genomics in veterinary parasite drug-discovery. Trends Parasitol. 21 (2005) 302-305
24. Gilleard J.S. Understanding anthelmintic resistance: the need for genomics and genetics. Int. J. Parasitol. 36 (2006) 1227-1239
25. Gobert G.N., Moertel L.P., and McManus D.P. Microarrays: new tools to unravel parasite transcriptomes. Parasitology 131 (2005) 439-448
26. Gönczy P., Echeverri C., Oegema K., Coulson A., Jones S.J.M., Copley R.R., Duperon J., Oegema J., Brehm M., Cassin E., Hannak E., Kirkham M., Pichler S., Flohrs K., Goessen A., Leidel S., Alleaume A.M., Martin C., Özlü B.P., and Hyman A.A. Functional genomic analysis of cell division in C. elegans using RNAi of genes on chromosome III. Nature 408 (2000) 331-336
27. Grant B., and Hirsh D. Receptor-mediated endocytosis in the Caenorhabditis elegans oocyte. Mol. Biol. Cell. 10 (1999) 4311-4326
28. Halestrap A., and Brenner C. The adenine nucleotide translocase: a central component of the mitochondrial permeability transition pore and key player in cell death. Curr. Med. Chem. 10 (2003) 1507-1525
29. Hanazawa M., Mochii M., Ueno N., Kohara Y., and 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
30. Harris J.E., Govindan J.A., Yamamoto I., Schwartz J., Kaverina I., and Greenstein D. Major sperm protein signalling promotes oocyte microtubule reorganization prior to fertilization in Caenorhabditis elegans. Dev. Biol. 299 (2006) 105-121
31. Hu M., Abs EL-Osta Y.G., Campbell B.E., Boag P.R., Nisbet A.J., Beveridge I., and Gasser R.B. Trichostrongylus vitrinus (Nematoda: Strongylida): Molecular characterization and transcriptional analaysis of Tv-stp-1, a serine/threonine phosphatase gene. Exp. Parasitol. 117 (2007) 22-34
32. Hu M., Campbell B.E., Pellegrino M., Loukas A., Beveridge I., Ranganathan S., and Gasser R.B. Genomic characterization of Tv-ant-1, a Caenorhabditis elegans tag-61 homologue from the parasitic nematode Trichostrongylus vitrinus. Gene. 397 (2007) 12-25
33. Issa Z., Grant W.N., Stasiuk S., and Shoemarker C.B. Development of methods for RNA interference in the sheep gastrointestinal parasite, Trichostrongylus colubriformis. Int. J. Parasitol. 35 (2005) 935-940
34. Jiang M., Ryu J., Kiraly M., Duke K., Reinke V., and Kim S.K. Genome-wide analysis of developmental and sex-regulated gene expression profiles in Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 98 (2001) 218-223
35. 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., Ziperlen P., and Ahringer J. Systemic functional analysis of the Caenorhabditis elegans genome using RNAi. Nature 421 (2003) 231-237
36. Knox D.P., Geldhof P., Visser A., and Britton C. RNA interference in parasitic nematodes of animals: a reality check?. Trends Parasitol. 23 (2007) 105-107
37. Kotze A.C., and Bagnall N.H. RNA interference in Haemonchus contortus: suppression of beta-tubulin gene expression in L3, L4 and adult worms in vitro. Mol. Biochem. Parasitol. 145 (2006) 101-110
38. Krogh A., Larsson B., von Heijne G., and Sonnhammer E.L.L. Predicting transmembrane protein topology with a hidden Markov model: Application to complete genomes. J. Mol. Biol. 305 (2001) 567-580
39. Li B.-W., Rush A.C., Crosby S.D., Warren W.C., Williams S.A., Mitreva M., and Weil G.J. Profiling of gender-regulated gene transcripts in the filarial nematode Brugia malayi by cDNA oligonucleotide array analysis. Mol. Biochem. Parasitol. 143 (2005) 49-57
40. -ΔΔCT method. Methods 25 (2001) 402-408
41. Liu J., and Kipreos E.T. Evolution of cyclin-dependent kinases (CDKs) and CDK-activating kinases (CAKs): differential conservation of CAKs in yeast and metazoa. Mol. Biol. Evol. 17 (2000) 1061-1074
42. 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
43. Loukas A., Bethony J.M., Williamson A.L., Goud G.N., Mendez S., Zhan B., Hawdon J.M., Elena Bottazzi M., Brindley P.J., and Hotez P.J. Vaccination of dogs with a recombinant cysteine protease from the intestine of canine hookworms diminishes the fecundity and growth of worms. J. Infect. Dis. 189 (2004) 1952-1961
44. Maeda I., Kohara Y., Yamamoto M., and Sugimoto A. Large-scale analysis of gene function in Caenorhabditis elegans by high-throughput RNAi. Curr. Biol. 6 11 (2001) 171-176
45. MAFF, 1977. Manual of Veterinary Parasitological Laboratory Techniques. Technical Bulletin 18. Her Majesty's Stationary Office, London, UK.
46. McCarrey J.R., and Thomas K. Human testis-specific PGK gene lacks introns and possesses characteristics of a processed gene. Nature 326 (1987) 501-505
47. McLeod R.S. Costs of major parasites to the Australian livestock industries. Int. J. Parasitol. 25 (1995) 1363-1367
48. Mello C.C., and Conte Jr. D. Revealing the world of RNA interference. Nature 431 (2004) 338-342
49. Miller M.A., Nguyen V.Q., Lee M.-H., Kosinski M., Schedl T., Caprioli R.M., and Greenstein D. A sperm cytoskeletal protein that signals oocyte meiotic maturation and ovulation. Science 291 (2001) 2144-2147 (Errata in vol. 292, 53 and 639)
50. Miller M.A., Ruest P.J., Kosinski M., Hanks S.K., and Greenstein D. An Eph receptor sperm-sensing control mechanism for oocyte meiotic maturation in Caenorhabditis elegans. Genes Dev. 17 (2003) 187-200
51. Moller S., Croning M.D.R., and Apweiler R. Evaluation of methods for the prediction of membrane spanning regions. Bioinformatics 17 (2001) 646-653
52. Mori H., Palmer R.E., and Sternberg P.W. The identification of a Caenorhabditis elegans homolog of p34cdc2 kinase. Mol. Gen. Genet. 245 (1994) 781-786
53. th stage larvae (L4) during self-cure from the intestine. Exp. Parasitol. 104 (2003) 113-121
54. Muhlrad P.J., and Ward S. Spermiogenesis initiation in Caenorhabditis elegans involves a casein kinase 1 encoded by the spe-6 gene. Genetics 161 (2002) 143-155
55. Nakamura N., Komiyama M., Fujioka M., and Mori C. Sorting specificity of spermatogenic cell specific region of mouse hexokinase-s (mHk1-s). Mol. Reprod. Dev. 64 (2003) 113-119
56. Nagaraj, S.H., Deshpande, N., Gasser, R.B., Ranganathan, S., 2007. ESTExplorer: an expressed sequence tag (EST) assembly and annotation platform. Nucleic Acids Res. 35(WebServer Issue), W143-W147.
57. Newton S.E., Boag P.R., and Gasser R.B. Opportunities and prospects for investigating developmentally regulated and sex-specific genes and their expression in intestinal nematodes of humans. In: Holland C.V., and Kennedy M.W. (Eds). World Class Parasites: Volume 2. The Geohelminths: Ascaris, Trichuris and Hookworm (2002), Kluwer Academic Publishers., Boston/Dordrecht/London 235-268
58. Nielsen H., Engelbrecht J., Brunak S., and von Heijne G. Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Prot. Eng. 10 (1997) 1-6
59. Nikolaou S., Hartman D., Presidente P.J.A., Newton S.E., and Gasser R.B. HcSTK, a Caenorhabditis elegans PAR-1 homologue from the parasitic nematode, Haemonchus contortus. Int. J. Parasitol. 32 (2002) 749-758
60. Nikolaou S., and Gasser R.B. Prospects for exploring molecular developmental processes in Haemonchus contortus. Int. J. Parasitol. 36 (2006) 859-868
61. Nikolaou S., Hu M., Chilton N.B., Hartman D., Nisbet A.J., Presidente P.J., and Gasser R.B. Isolation and characterization of class II myosin genes from Haemonchus contortus. Parasitol. Res. 99 (2006) 200-203 (Erratum in: Parasitol Res. 99, 204).
62. Nisbet A.J., and Gasser R.B. Profiling of gender-specific gene expression for Trichostrongylus vitrinus (Nematoda: Strongylida) by microarray analysis of expressed sequence tag libraries constructed by suppressive-subtractive hybridisation. Int. J. Parasitol. 34 (2004) 633-643
63. Nisbet A.J., Cottee P., and Gasser R.B. Molecular biology of reproduction and development in parasitic nematodes - progress and opportunities. Int. J. Parasitol. 34 (2004) 125-138
64. Parkinson J., Mitreva M., Whitton C., Thomson M., Daub J., Martin J., Schmid R., Hall N., Barrell B., Waterston R.H., McCarter J.P., and Blaxter M.L. A transcriptomic analysis of the phylum Nematoda. Nat. Genet. 36 (2004) 1259-1267
65. 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., and Kim S.K. A global profile of germline gene expression in C. elegans. Mol. Cell 6 (2000) 605-616
66. Roberts T.M., and Stewart M. Nematode sperm locomotion. Curr. Opin. Cell Biol. 7 (1995) 13-17
67. Roberts T.M., and 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
68. Roberts T.M., Pavalko F.M., and Ward S. Membrane and cytoplasmic proteins are transported in the same organelle complex during nematode spermatogenesis. J. Cell Biol. 102 (1986) 1787-1796
69. Roos M.H., and Tielens A.G. Differential expression of two succinate dehydrogenase subunit-B genes and a transition in energy metabolism during the development of the parasitic nematode Haemonchus contortus. Mol. Biochem. Parasitol. 66 (1994) 273-281
70. Rossanigo C.E., and Gruner L. The length of strongylid nematode infective larvae as a reflection of developmental conditions in faeces and consequences on their viability. Parasitol. Res. 82 (1996) 304-311
71. Smith G. The economics of parasite control: obstacles to creating reliable models. Vet. Parasitol. 72 (1997) 437-444
72. Schmitt-Wrede H.P., Waldraff A., Krucken J., Harder A., and Wunderlich F. Characterization of a hexokinase encoding cDNA of the parasitic nematode Haemonchus contortus. Biochim. Biophys. Acta 1444 (1999) 439-444
73. Sonnichsen B., Koski L.B., Walsh A., Marschall P., Neumann B., Brehm M., Alleaume A.M., Artele J., Bettencourt P., Cassin E., Hewitson M., Holz C., Khan M., Lazik S., Martin C., Nitzsche B., Ruer M., Stamford J., Winzi M., Heinkel R., Roder M., Finell J., Hantsch H., Jones S.J., Jones M., Piano F., Gunsalus K.C., Oegema K., Gonczy P., Coulson A., Hyman A.A., and Echeverri C.J. Full-genome RNAi profiling of early embryogenesis in Caenorhabditis elegans. Nature 434 (2005) 462-469
74. Spieth J., and Blumenthal T. The Caenorhabditis elegans vitellogenin gene family includes a gene encoding a distantly related protein. Mol. Cell. Biol. 5 (1985) 2495-2501
75. Stoll N.R. Studies with the strongyloid nematode, Haemonchus contortus. Am. J. Hyg. 10 (1929) 384-418
76. Sugimoto A. High-throughput RNAi in Caenorhabditis elegans: genome-wide screens and functional genomics. Differentiation 72 (2004) 81-91
77. Syntichaki P., Xu K., Driscoll M., and Tavernarakis N. Specific aspartyl and calpain proteases are required for neurodegeneration in Celegans. Nature 419 (2002) 939-944
78. Thompson F.J., Barker G.L.A., Hughes L., Wilkers C.P., Coghill J., and Viney M.E. A microarray analysis of gene expression in the free-living stages of the parasitic nematode of Strongyloides ratti. BMC Genomics 7 (2006) 157-178
79. Voutev R., Killian D.J., Ahn J.H., and Hubbard E.J. Alterations in ribosome biogenesis cause specific defects in C. elegans hermaphrodite gonadogenesis. Dev. Biol. 298 (2006) 45-58
80. Walker J.E., and Runswick M.J. The mitochondrial transport protein superfamily. J. Bioenerg. Biomembr. 25 (1993) 435-446
81. Ward S., and Klass M. The location of the major protein in Caenorhabditis elegans sperm and spermatocytes. Dev. Biol. 92 (1982) 203-208
82. Welch P.J., and Wang J.Y. Coordinated synthesis and degradation of cdc2 in the mammalian cell cycle. Proc. Natl. Acad. Sci. USA 89 (1992) 3093-3097
83. Williamson A.L., Brindley P.J., Knox D.P., Hotez P.J., and Loukas A. Digestive proteases of blood-feeding nematodes. Trends Parasitol. 19 (2003) 417-423
84. Williamson A.L., Lecchi P., Turk B.E., Choe Y., Hotez P.J., McKerrow J.H., Cantley L.C., Sajid M., Craik C.S., and Loukas A. A multi-enzyme cascade of hemoglobin proteolysis in the intestine of blood-feeding hookworms. J. Biol. Chem. 279 (2004) 35950-35957
85. Wolstenholme A.J., Fairweather I., Prichard R., von Samson-Himmelstjerna G., and Sangster N.C. Drug resistance in veterinary helminths. Trends Parasitol. 20 (2004) 469-476
86. Yang Y.H., Dudoit S., Luu P., Lin D.M., Peng V., Ngai J., and Speed T.P. Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Res. 30 (2002) e15
87. Yatsuda A.P., Bakker N., Krijgsveld J., Knox D.P., Heck A.J., and de Vries E. Identification of secreted cysteine proteases from the parasitic nematode Haemonchus contortus detected by biotinylated inhibitors. Infect. Immun. 74 (2006) 1989-1993
88. Zawadzki J.L., Presidente P.J., Meeusen E.N., and de Veer M.J. RNAi in Haemonchus contortus: a potential method for target validation. Trends Parasitol. 22 (2006) 495-499
89. Zhong W., and Sternberg P.W. Genome-wide prediction of C. elegans genetic interactions. Science 311 (2006) 1481-1484