Recent Progress in Transcriptomics of Key Gastrointestinal Nematodes of Animals - Fundamental Research Toward New Intervention Strategies

Parasitic Helminths: Targets, Screens, Drugs and Vaccines

Volumn , Issue , 2012, Pages 61-72

  Cantacessi, Cinzia ^a   Campbell, Bronwyn E ^a   Jex, Aaron R ^a   Hall, Ross S ^a   Young, Neil D ^a   Nolan, Matthew J ^a   Gasser, Robin B ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Bioinformatics; Drug; Gastrointestinal nematode; Next generation sequencing; Parasite; Transcriptomics; Vaccine

Indexed keywords

EID: 84886216819     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9783527652969.ch4     Document Type: Chapter

References (91)

1. de Silva, N.R., Brooker, S., Hotez, P.J., Montresor, A., Engels, D., and Savioli, L. (2003) Soil-transmitted helminth infections: updating the global picture. Trends Parasitol., 19, 547-551.
2. Bethony, J., Brooker, S., Albonico, M., Geiger, S.M., Loukas, A., Diemert, D., and Hotez, P.J. (2006) Soil-transmitted helminth infections: ascariasis, trichuriasis, and hookworm. Lancet, 367, 1521-1532.
3. Nikolaou, S. and Gasser, R.B. (2006) Prospects for exploring molecular developmental processes in Haemonchus contortus. Int. J. Parasitol., 36, 859-868.
4. Harhay, M.O., Horton, J., and Olliaro, P.L. (2010) Epidemiology and control of human gastrointestinal parasites in children. Expert Rev. Anti Infect. Ther., 8, 219-234.
5. Hotez, P.J., Fenwick, A., Savioli, L., and Molyneux, D.H. (2009) Rescuing the bottom billion through control of neglected tropical diseases. Lancet, 373, 1570-1575.
6. Sutherland, I. and Scott, I. (2010) Gastrointestinal Nematodes of Sheep and Cattle: Biology and Control, Wiley-Blackwell, Chichester.
7. Wolstenholme, A.J., Fairweather, I., Prichard, R., von Samson-Himmelstjerna, G., and Sangster, N.C. (2004) Drug resistance in veterinary helminths. Trends Parasitol., 20, 469-476.
8. Skrjabin, K.I., Sobolev, A.A., and Ivashkin, V.M. (1967) Principles of Nematology. Izdatel.sto Akademii Nauk SSSR/Israel Program for Scientific Translations, Washington, DC.
9. Blaxter, M.L., De Ley, P., Garey, J.R., Liu, L.X., Scheldeman, P., Vierstraete, A., Vanfleteren, J.R. et al. (1998) A molecular evolutionary framework for the phylum Nematoda. Nature, 392, 71-75.
10. Knox, D.P. (2000) Development of vaccines against gastrointestinal nematodes. Parasitology, 120, S43-S61.
11. Crompton, D.W. (2001) Ascaris and ascariasis. Adv. Parasitol., 48, 285-375.
12. Maizels, R.M. and Yazdanbakhsh, M. (2003) Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat. Rev. Immunol., 3, 733-744.
13. Hotez, P.J., Brooker, S., Bethony, J., Bottazzi, M.E., Loukas, A., and Xiao, S. (2004) Hookworm infection. N. Engl. J. Med., 351, 799-807.
14. Loukas, A., Bethony, J., Brooker, S., and Hotez, P. (2006) Hookworm vaccines: past, present, and future. Lancet Infect. Dis., 6, 733-741.
15. Holden-Dye, L. and Walker, R.J. (2007) Anthelmintic drugs, in WormBook (ed. The C. elegans Research Community), doi: 10.1895/wormbook.1.143.1.
16. Pearson, M.S., Ranjit, N., and Loukas, A. (2010) Blunting the knife: development of vaccines targeting digestive proteases of blood-feeding helminth parasites. Biol. Chem., 391, 901-911.
17. Keiser, J. and Utzinger, J. (2010) The drugs we have and the drugs we need against major helminth infections. Adv. Parasitol., 73, 197-230.
18. Margulies, M., Egholm, M., Altman,W.E., Attlya, S., Bader, J.S., Bemben, L.A., Berka, J. et al. (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature, 437, 376-380.
19. Bentley, D.R., Balasubramanian, S., Swerdlow, H.P., Smith, H.P., Smith, G.P., Milton, J., Brown, C.G. et al. (2008) Accurate whole human genome sequencing using reversible terminator chemistry. Nature, 456, 53-59.
20. Harris, T.D., Buzby, P.R., Babcock, H., Beer, E., Bowers, J., Braslavsky, I., Causey, M. et al. (2008) Single-molecule DNA sequencing of a viral genome. Science, 320, 106-109.
21. Pandey, V., Nutter, R.C., and Prediger, E. (2008) Applied Biosystems SOLiD_ system: ligation-based sequencing, in Next Generation Genome Sequencing: Towards Personalized Medicine (ed. J.M. Milton), Wiley-VCH Verlag GmbH, Weinheim, pp. 29-41.
22. Adams, M.D., Kelley, J.M., Gocayne, J.D., Dubnick, M., Polymeropoulos, M.H., Xiao, H., Merril, C.R. et al. (1991) Complementary DNA sequencing: expressed sequence tags and human genome project. Science, 252, 1651-1656.
23. Nagaraj, S.H., Gasser, R.B., and Ranganathan, S. (2007) A hitchhiker.s guide to expressed sequence tag (EST) analysis. Brief. Bioinfomatics, 8, 6-21.
24. Parkinson, J. and Blaxter, M. (2009) Expressed sequence tags: an overview. Methods Mol. Biol., 533, 1-12.
25. Huang, X. and Madan, A. (1999) CAP3: a DNA sequence assembly program. Genome Res., 9, 868-877.
26. Conesa, A., Gotz, S., Garcia-Gomez, J.M., Terol, J., Talon, M., Talón, M., and Robles, M. (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics, 21, 3674-3676.
27. Nagaraj, S.H., Deshpande, N., Gasser, R.B., and Ranganathan, S. (2007) ESTExplorer: an expressed sequence tag (EST) assembly and annotation platform. Nucleic Acids Res., 35, W135-W147.
28. Soderlund, C., Johnson, E., Bomhoff, M., and Descour, A. (2009) PAVE: program for assembling and viewing ESTs. BMC Genomics, 10, 400.
29. Falgueras, J., Lara, A.J., Fernandez-Poso, N., Canton, F.R., Perez-Trabado, G., and Claros, M. (2010) SeqTrim: a high throughput pipeline for pre-processing any type of sequence read. BMC Bioinformatics, 11, 38.
30. Myers, E.W. (1995) Toward simplifying and accurately formulating fragment assembly. J. Comput. Biol., 2, 275-290.
31. Zerbino, D.R. and Birney, E. (2008) Velvet: algorithms for de novo short read assembly using de Bruijn graphs. Genome Res., 18, 821-829.
32. Scheibye-Alsing, K., Hoffmann, S., Frankel, A., Jensen, P., Stadler, P.F., Mang, Y., Tommerup, N. et al. (2009) Sequence assembly. Comput. Biol. Chem., 33, 121-136.
33. Miller, J.R., Koren, S., and Sutton, G. (2010) Assembly algorithms for nextgeneration sequencing data.Genomics, 95, 315-327.
34. Li, R., Li, Y., Kristiansen, K., and Wang, J. (2008) SOAP: short oligonucleotide alignment program. Bioinformatics, 24, 713-714.
35. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990) Basic local alignment search tool. J. Mol. Biol., 215, 403-410.
36. Iseli, C., Jongeneel, C.V., and Bucher, P. (1999) ESTScan: a program for detecting, evaluating, and reconstructing potential coding regions in EST sequences. Proc. Int. Conf. Intell. Syst. Mol. Biol., 1, 138-148.
37. Min, X.J., Butler, G., Storms, R., and Tsang, A. (2005) OrfPredictor: predicting protein-coding regions in EST-derived sequences. Nucleic Acids Res., 33, W677-W680.
38. Ashburner, M., Ball, C.A., Blake, J.A., Botstein, D., Butler, H. et al. (2000) Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat. Genet., 25, 25-29.
39. Bateman, A., Birney, E., Durbin, R., Eddy, S.R., Howe, K.L., and Sonnhammer, E.L. (2000) The Pfam protein families database. Nucleic Acids Res., 28, 263-266.
40. Hunter, S., Apweiler, R., Attwood, T.K., Bairoch, A., Bateman, A., Binns, D., Bork, P. et al. (2009) InterPro: the integrative protein signature database. Nucleic Acids Res., 37, D211-D215.
41. Wheeler, D.L., Church, D.M., Lash, A.E., Leipe, D.D., and Madden, T.L. (2001) Database resources of the National Center for Biotechnology Information. Nucleic Acids Res., 29, 11-16.
42. Shumway, M., Cochrane, G., and Sugawara, H. (2010) Archiving next generation sequencing data. Nucleic Acids Res., 38, D870-D871.
43. Cherry, J.M., Ball, C., Weng, S., Juvic, G., Schmidt, R., Adler, C., Dunn, B. et al. (1997) Genetic and physical maps of Saccharomyces cerevisiae. Nature, 387, 67-73.
44. Tweedie, S., Ashburner, M., Falls, K., Leyland, P., McQuilton, P., Marygold, S., Millburn, G. et al. (2009) FlyBase: enhancing Drosophila Gene Ontology annotations. Nucleic Acids Res., 37, D555-D559.
45. Bult, C.J., Epping, J.T., Kadin, J.A., Richardson, J.E., Blake, J.A., and Eppig, J.T. and Mouse Genome Database Group. (2008) The mouse genome database (MGD): mouse biology and model systems. Nucleic Acids Res., 36, D724-D728.
46. Harris, T.W., Antoshechkin, I., Bieri, T., Blasiar, D., Chan, J., Chen, W.J., De La Cruz, N. et al. (2010) WormBase: a comprehensive resource for nematode research. Nucleic Acids Res., 38, D463-D467.
47. Nagaraj, S.H., Gasser, R.B., Nisbet, A.J., and Ranganathan, S. (2008) In silico analysis of expressed sequence tags from Trichostrongylus vitrinus (Nematoda): comparison of the automated ESTExplorer workflow platform with conventional database searches. BMC Bioinformatics, 9, S10.
48. Cantacessi, C., Jex, A.R., Hall, R.S., Young, N.D., Campbell, B.E., Joachim, A., Nolan, M.J. et al. (2010) A practical, bioinformatic workflow system for large data sets generated by next-generation sequencing. Nucleic Acids Res., 38, e171.
49. Cantacessi, C., Mitreva, M., Campbell, B.E., Hall, R.S., Young, N.D., Jex, A.R., Ranganathan, S., and Gasser, R.B. (2010) First transcriptomic analysis of the economically important parasitic nematode, Trichostrongylus colubriformis, using a next-generation sequencing approach. Infect. Genet. Evol., 10, 1199-1207.
50. Cantacessi, C., Campbell, B.E., Young, N.D., Jex, A.R., Hall, R.S., Presidente, P.J.,Zawadzki, J.L. et al. (2010) Differences in transcription between free-livingCO2-activated third-stage larvae of Haemonchus contortus. BMC Genomics, 11, 266.
51. Cantacessi, C., Mitreva, M., Jex, A.R., Young, N.D., Campbell, B.E., Hall, R.S., Doyle, M.A. et al. (2010)Massively parallel sequencing and analysis of the Necator americanus transcriptome. PLoS Negl. Trop. Dis., 4, e684.
52. Björnberg, F., Lantz, M., and Gullberg, U. (1995) Metalloproteases and serineproteases are involved in the cleavage of the two tumour necrosis factor (TNF) receptors to soluble forms in the myeloid cell lines U-937 and THP-1. Scand. J. Immunol., 42, 418-424.
53. Shaw, R.J., McNeill, M.M., Maass, D.R., Hein, W.R., Barber, T.K., Wheeler, M., Morris, C.A., and Shoemaker, C.B. (2003) Identification and characterisation of an aspartyl protease inhibitor homologue as a major allergen of Trichostrongylus colubriformis. Int. J. Parasitol., 33, 1233-1243.
54. Williamson, A.L., Brindley, P.J., Knox, D.P., Hotez, P.J., and Loukas, A. (2003) Digestive proteases of bloodfeeding nematodes. Trends Parasitol., 19, 417-423.
55. Fetterer, R.H. (1996)Growth and cuticular synthesis in Ascaris suum larvae during development from third to fourth stage in vitro. Vet. Parasitol., 65, 275-282.
56. Pratt, D., Cox, G.N., Milhausen, M.J., and Boisvenue, R.J. (1990) A developmentally regulated cysteine protease gene family in Haemonchus contortus. Mol. Biochem. Parasitol., 43, 181-191.
57. Williamson, A.L., Lecchi, P., Turk, B.E., Choe, Y., Hotez, P.J., McKerrow, J.H., Cantley, L.C. et al. (2004) A multi-enzyme cascade of hemoglobin proteolysis in the intestine of blood-feeding hookworms. J. Biol. Chem., 279, 35950-35957.
58. Ranjit, N., Zhan, B., Hamilton, B., Stenzel, D., Lowther, J., Pearson, M., Gorman, J., Hotez, P., and Loukas, A. (2009) Proteolytic degradation of hemoglobin in the intestine of the human hookworm Necator americanus. J. Infect. Dis., 199, 904-912.
59. Datu, B.J., Gasser, R.B., Nagaraj, S.H., Ong, E.K., O'Donoghue, P., McInnes, R., Ranganathan, S., and Loukas, A. (2008) Transcriptional changes in the hookworm, Ancylostoma caninum, during the transition from a free-living to a parasitic larva. PLoS Negl. Trop. Dis., 2, e130.
60. Cantacessi, C., Loukas, A., Campbell, B.E., Mulvenna, J., Ong, E.K., Zhong, W., Sternberg, P.W. et al. (2009) Exploring transcriptional conservation between Ancylostoma caninum and Haemonchus contortus by oligonucleotide microarray and bioinformatic analyses. Mol. Cell. Probes, 23, 1-9.
61. Moser, J.M., Freitas, T., Arasu, P., and Gibson, G. (2005) Gene expression profiles associated with the transition to parasitism in Ancylostoma caninum larvae. Mol. Biochem. Parasitol., 143, 39-48.
62. Mitreva, M., McCarter, J.P., Arasu, P., Hawdon, J.,Martin, J., Dante, M., Wylie, T. et al. (2005) Investigating hookworm genomes by comparative analysis of two Ancylostoma species. BMC Genomics, 26, 58.
63. Abubucker, S., Martin, J., Yin, Y., Fulton, L., Yang, S.P., Hallsworth-Pepin, K., Johnston, J.S. et al. (2008) The canine hookworm genome: analysis and classification of Ancylostoma caninum survey sequences. Mol. Biochem. Parasitol., 157, 187-192.
64. Furmidge, B.A., Horn, L.A., and Pritchard, D.I. (1996) The antihaemostatic strategies of the human hookworm Necator americanus. Parasitology, 112, 81-87.
65. Milstone, A.M., Harrison, L.M., Bungiro, R.D., Kuzmic, P., and Cappello, M. (2000) A broad spectrum Kunitz type serine protease inhibitor secreted by the hookworm Ancylostoma ceylanicum. J. Biol. Chem., 275, 29391-29399.
66. Grad, L.I., Sayles, L.C., and Lemire, B.D. (2007) Isolation and functional analysis of mitochondria from the nematode Caenorhabditis elegans. Methods Mol. Biol., 372, 51-66.
67. Hu, M., Zhong, W., Campbell, B.E., Sternberg, P.W., Pellegrino, M.W., and Gasser, R.B. (2010) Elucidating ANTs in worms using genomic and bioinformatic tools - biotechnological prospects? Biotechnol. Adv., 28, 49-60.
68. Campbell, B.E., Boag, P.R., Hofmann, A., Cantacessi, C., Wang, C.K., Taylor, P., Hu, M., Sindhu, Z., Loukas, A., Sternberg, P.W., and Gasser, R.B. (2011) Atypical (RIO) protein kinases from Haemonchus contortus - promise as new targets for nematocidal drugs. Biotechnol. Adv., 29, 338-350.
69. Campbell, B.E., Hofmann, A., McCluskey, A., and Gasser, R.B. (2011) Serine/threonine phosphatases in socioeconomically important parasitic nematodes - prospects as novel drug targets? Biotechnol. Adv., 29, 28-39.
70. McCluskey, A., Keane, M.A., Walkom, C.C., Bowyer, M.C., Sim, A.T.R., Young, D.J., and Sakoff, J.A. (2002) The first two cantharidin analogues displaying PP1 selectivity. Bioorg. Med. Chem. Lett., 12, 391-393.
71. Hill, T.A., Stewart, S.G., Sauer, B., Gilbert, J., Ackland, S.P., Sakoff, J.A., and McCluskey, A. (2007) Heterocyclic substituted cantharidin and norcantharidin analogues - synthesis, protein phosphatase (1 and 2A) inhibition, and anti-cancer activity. Bioorg. Med. Chem. Lett., 17, 3392-3397.
72. Cantacessi, C., Campbell, B.E., Visser, A., Geldhof, P., Nolan, M.J., Nisbet, A.J., Matthews, J.B. et al. (2009)Aportrait of the.SCP/TAPS. proteins of eukaryotes - developing a framework for fundamental research and biotechnological outcomes. Biotechnol. Adv., 27, 376-388.
73. Hawdon, J.M., Jones, B.F., Hoffman, D.R., and Hotez, P.J. (1996) Cloning and characterization of Ancylostoma-secreted protein. A novel protein associated with the transition to parasitism by infective hookworm larvae. J. Biol. Chem., 271, 6672-6678.
74. Zhan, B., Liu, Y., Badamchian, M., Williamson, A., Feng, J., Loukas, A., Hawdon, J.M., and Hotez, P.J. (2003) Molecular characterisation of the Ancylostoma-secreted protein family from the adult stage of Ancylostoma caninum. Int. J. Parasitol., 33, 897-907.
75. Mulvenna, J., Hamilton, B., Nagaraj, S., Smyth, D., Loukas, A., and Gorman, J. (2009) Proteomic analysis of the excretory/ secretory component of the blood-feeding stage of the hookworm, Ancylostoma caninum. Mol. Cell. Proteomics, 8, 109-121.
76. Mendez, S., D'Samuel, A., Antoine, A.D., Ahn, S., and Hotez, P. (2008) Use of the air pouch model to investigate immune responses to a hookworm vaccine containing the Na-ASP-2 protein in rats. Parasite Immunol., 30, 53-56.
77. Xiao, S., Zhan, B., Xue, J., Goud, G.N., Loukas, A., Liu, Y., Williamson, A. et al. (2008) The evaluation of recombinant hookworm antigens as vaccines in hamsters (Mesocricetus auratus) challenged with human hookworm, Necator americanus. Exp. Parasitol., 118, 32-40.
78. Coassin, S., Brandstatter, A., and Kronenberg, F. (2010) Lost in the space of bioinformatic tools: a constantly updated survival guide for genetic epidemiology. The GenEpi Toolbox. Atherosclerosis, 209, 321-335.
79. Karp, P.D. (1998) What we do not know about sequence analysis and sequence databases. Bioinformatics, 14, 753-754.
80. Geldhof, P., Visser, A., Clark, D., Saunders, G., Britton, C., Gilleard, J., Berriman, M., and Knox, D. (2007) RNA interference in parasitic helminths: current situation, potential pitfalls and future prospects. Parasitology, 134, 609-619.
81. Samarasinghe, B., Knox, D.P., and Britton, C. (2011) Factors affecting susceptibility to RNA interference in Haemonchus contortus and in vivo silencing of an H11 aminopeptidase gene. Int. J. Parasitol., 41, 51-59.
82. Viney, M.E. and Thompson, F.J. (2008) Two hypotheses to explain why RNA interference does not work in animal parasitic nematodes. Int. J. Parasitol., 38, 43-47.
83. Hu, M., Lok, J.B., Ranjit, N.,Massey, H.C. Jr, Sternberg, P.W., and Gasser, R.B. (2010) Structural and functional characterisation of the fork head transcription factor-encoding gene, Hc-daf-16, from the parasitic nematode Haemonchus contortus (Strongylida). Int. J. Parasitol., 40, 405-415.
84. Stepek, G., McCormack, G., and Page, A.P. (2010) Collagen processing and cuticle formation is catalysed by the astacin metalloprotease DPY-31 in free-living and parasitic nematodes. Int. J. Parasitol., 40, 533-542.
85. Doyle, M.A.,Gasser, R.B.,Woodcroft, B.J., Hall, R.S., and Ralph, S.A. (2010) Drug target prediction and prioritization: using orthology to predict essentiality in parasite genomes. BMC Genomics, 11, 222.
86. Krasky, A., Rohwer, A., Schroeder, J., and Selzer, P.M. (2007) A combined bioinformatics and chemoinformatics approach for the development of new antiparasitic drugs. Genomics, 89, 36-43.
87. Caffrey, C.R., Rohwer, A., Oellien, F., Marhofer, R.J., Braschi, S., Oliveira, G., McKerrow, J.H., and Selzer, P.M. (2009) A comparative chemogenomics strategy to predict potential drug targets in the metazoan pathogen, Schistosoma mansoni. PLoS One, 4, e4413.
88. McCarter, J.P. (2004) Genomic filtering: an approach to discovering novel antiparasitics. Trends Parasitol., 20, 462-468.
89. Seib, K.L., Dougan, G., and Rappuoli, R. (2009) The key role of genomics in modern vaccine and drug design for emerging infectious diseases. PLoS Genet., 5, e1000612.
90. Hopkins, A.L. and Groom, C.R. (2002) The druggable genome. Nature, 1, 727-730.
91. Chang, A., Scheer, M., Grote, A., Schomburg, I., and Schomburg, D. (2009) BRENDA, AMENDA and FRENDA the enzyme information system: new content and tools in 2009. Nucleic Acids Res., 37, D588-D592.