Dictyocaulus viviparus genome, variome and transcriptome elucidate lungworm biology and support future intervention

Scientific Reports

Volumn 6, Issue , 2016, Pages

  McNulty, Samantha N ^a   Strübe, Christina ^b   Rosa, Bruce A ^a   Martin, John C ^a   Tyagi, Rahul ^a   Choi, Young Jun ^a   Wang, Qi ^a   Pepin, Kymberlie Hallsworth ^a   Zhang, Xu ^a   Ozersky, Philip ^a   Wilson, Richard K ^a   Sternberg, Paul W ^c   Gasser, Robin B ^d   Mitreva, Makedonka ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^c CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^d UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL MARKER;

ANIMAL; BIOLOGY; BOVINE; CATTLE DISEASE; DICTYOCAULOSIS; DICTYOCAULUS; DNA SEQUENCE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC VARIATION; GENETICS; GENOME; GENOMICS; GROWTH, DEVELOPMENT AND AGING; HOST PARASITE INTERACTION; LUNG; METABOLISM; PARASITOLOGY; PHYLOGENY; PROCEDURES;

ANIMALS; BIOMARKERS; CATTLE; CATTLE DISEASES; COMPUTATIONAL BIOLOGY; DICTYOCAULUS; DICTYOCAULUS INFECTIONS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENETIC VARIATION; GENOME; GENOMICS; HOST-PARASITE INTERACTIONS; LUNG; PHYLOGENY; SEQUENCE ANALYSIS, DNA;

EID: 84957818783     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep20316     Document Type: Article

References (68)

1. Coles, G. C. The future of veterinary parasitology. Veterinary parasitology 98, 31-39 (2001).
2. Jackson, F. Nutrition and immunity of nematodes of livestock. Parasite Immunol. 30, 61-62, doi: 10.1111/j.1365-3024.2007.01007.x (2008).
3. Panuska, C. Lungworms of ruminants. The Veterinary clinics of North America. Food animal practice 22, 583-593, doi: 10.1016/j. cvfa.2006.06.002 (2006).
4. Holzhauer, M., van Schaik, G., Saatkamp, H. W. & Ploeger, H. W. Lungworm outbreaks in adult dairy cows: estimating economic losses and lessons to be learned. The Veterinary record 169, 494, doi: 10.1136/vr.d4736 (2011).
5. Jorgensen, R. J., Ronne, H., Helsted, C. & Iskander, A. R. Spread of infective Dictyocaulus viviparus larvae in pasture and to grazing cattle: experimental evidence of the role of Pilobolus fungi. Veterinary parasitology 10, 331-339 (1982).
6. von Samson-Himmelstjerna, G. & Schnieder, T. Morphology of inhibited larvae of the bovine lungworm Dictyocaulus viviparus. Journal of helminthology 73, 79-83 (1999).
7. Anderson, R. C. Nematode parasites of vertebrates: their development and transmission. 2nd Edition edn, (CABI Publishing, 2000).
8. Gibbs, H. C. Mechanisms of survival of nematode parasites with emphasis on hypobiosis. Veterinary parasitology 11, 25-48 (1982).
9. Michel, J. F. & Mackenzie, A. Duration of the Acquired Resistance of Calves to Infection with Dictyocaulus viviparus. Res. Vet. Sci. 6, 344-395 (1965).
10. Matthews, J. B., Davidson, A. J., Freeman, K. L. & French, N. P. Immunisation of cattle with recombinant acetylcholinesterase from Dictyocaulus viviparus and with adult worm ES products. International journal for parasitology 31, 307-317 (2001).
11. McKeand, J. B. Vaccine development and diagnostics of Dictyocaulus viviparus. Parasitology 120 Suppl, S17-23 (2000).
12. Molento, M. B., Depner, R. A. & Mello, M. H. Suppressive treatment of abamectin against Dictyocaulus viviparus and the occurrence of resistance in first-grazing-season calves. Veterinary parasitology 141, 373-376, doi: 10.1016/j.vetpar.2006.01.061 (2006).
13. Fiel, C., Guzman, M., Steffan, P., Prieto, O. & Bhushan, C. Comparative efficacy of trichlorphon and trichlorphon/ivermectin combination treatment against anthelmintic-resistant cattle nematodes in Argentina. Parasitology research 109 Suppl 1, S105-112, doi: 10.1007/s00436-011-2407-3 (2011).
14. Strube, C. et al. Vaccination with recombinant paramyosin against the bovine lungworm Dictyocaulus viviparus considerably reduces worm burden and larvae shedding. Parasites & vectors 8, 119, doi: 10.1186/s13071-015-0733-5 (2015).
15. Cantacessi, C. et al. Deep insights into Dictyocaulus viviparus transcriptomes provides unique prospects for new drug targets and disease intervention. Biotechnology advances 29, 261-271, doi: 10.1016/j.biotechadv.2010.11.005 (2011).
16. Laabs, E. M., Schnieder, T. & Strube, C. Transcriptional differences between hypobiotic and non-hypobiotic preadult larvae of the bovine lungworm Dictyocaulus viviparus. Parasitology research 110, 151-159, doi: 10.1007/s00436-011-2464-7 (2012).
17. Strube, C., Buschbaum, S. & Schnieder, T. Genes of the bovine lungworm Dictyocaulus viviparus associated with transition from pasture to parasitism. Infection, genetics and evolution: journal of molecular epidemiology and evolutionary genetics in infectious diseases 12, 1178-1188, doi: 10.1016/j.meegid.2012.04.004 (2012).
18. von Holtum, C., Strube, C., Schnieder, T. & von Samson-Himmelstjerna, G. Development and evaluation of a recombinant antigenbased ELISA for serodiagnosis of cattle lungworm. Veterinary parasitology 151, 218-226, doi: 10.1016/j.vetpar.2007.11.006 (2008).
19. Schunn, A. M., Forbes, A., Schnieder, T. & Strube, C. Validation of a Dictyocaulus viviparus MSP-ELISA and cut-off adjustment in a one-year longitudinal field study in dairy cattle herds. Veterinary parasitology 189, 291-298, doi: 10.1016/j.vetpar.2012.04.012 (2012).
20. Laing, R. et al. The genome and transcriptome of Haemonchus contortus, a key model parasite for drug and vaccine discovery. Genome biology 14, R88, doi: 10.1186/gb-2013-14-8-r88 (2013).
21. Schwarz, E. M. et al. The genome and developmental transcriptome of the strongylid nematode Haemonchus contortus. Genome biology 14, R89, doi: 10.1186/gb-2013-14-8-r89 (2013).
22. Tang, Y. T. et al. Genome of the human hookworm Necator americanus. Nature genetics, doi: 10.1038/ng.2875 (2014).
23. Mitreva, M. et al. The draft genome of the parasitic nematode Trichinella spiralis. Nature genetics 43, 228-235, doi: 10.1038/ng.769 (2011).
24. Koutsovoulos, G., Makepeace, B., Tanya, V. N. & Blaxter, M. Palaeosymbiosis revealed by genomic fossils of Wolbachia in a strongyloidean nematode. PLoS genetics 10, e1004397, doi: 10.1371/journal.pgen.1004397 (2014).
25. McNulty, S. N. et al. Transcriptomic and proteomic analyses of a Wolbachia-free filarial parasite provide evidence of trans-kingdom horizontal gene transfer. PloS one 7, e45777, doi: 10.1371/journal.pone.0045777 (2012).
26. Wang, Z., Zarlenga, D., Martin, J., Abubucker, S. & Mitreva, M. Exploring metazoan evolution through dynamic and holistic changes in protein families and domains. BMC evolutionary biology 12, 138, doi: 10.1186/1471-2148-12-138 (2012).
27. Cantacessi, C. & Gasser, R. B. SCP/TAPS proteins in helminths-where to from now? Mol. Cell. Probes 26, 54-59, doi: 10.1016/j. mcp.2011.10.001 (2012).
28. Hasnain, S. Z., McGuckin, M. A., Grencis, R. K. & Thornton, D. J. Serine protease(s) secreted by the nematode Trichuris muris degrade the mucus barrier. PLoS neglected tropical diseases 6, 11 (2012).
29. Chu, D. et al. Molecular characterization of Ancylostoma ceylanicum Kunitz-type serine protease inhibitor: evidence for a role in hookworm-associated growth delay. Infect. Immun. 72, 2214-2221 (2004).
30. Overington, J. P., Al-Lazikani, B. & Hopkins, A. L. How many drug targets are there? Nat. Rev. Drug Discov. 5, 993-996, doi: 10.1038/nrd2199 (2006).
31. Hoglund, J., Engstrom, A., Morrison, D. A. & Mattsson, J. G. Genetic diversity assessed by amplified fragment length polymorphism analysis of the parasitic nematode Dictyocaulus viviparus the lungworm of cattle. International journal for parasitology 34, 475-484 (2004).
32. Hoglund, J., Morrison, D. A., Mattsson, J. G. & Engstrom, A. Population genetics of the bovine/cattle lungworm (Dictyocaulus viviparus) based on mtDNA and AFLP marker techniques. Parasitology 133, 89-99 (2006).
33. Hu, M., Hoglund, J., Chilton, N. B., Zhu, X. & Gasser, R. B. Mutation scanning analysis of mitochondrial cytochrome c oxidase subunit 1 reveals limited gene flow among bovine lungworm subpopulations in Sweden. Electrophoresis 23, 3357-3363, doi: 10.1002/1522-2683(200210)23:19<3357::AID-ELPS3357>3.0.CO;2-B (2002).
34. Laabs, E. M., Schnieder, T. & Strube, C. In vitro studies on the sexual maturation of the bovine lungworm Dictyocaulus viviparus during the development of preadult larvae to adult worms. Parasitology research 110, 1249-1259, doi: 10.1007/s00436-011-2622-y (2012).
35. Rosa, B. A., Jasmer, D. P. & Mitreva, M. Genome-Wide Tissue-Specific Gene Expression, Co-expression and Regulation of Coexpressed Genes in Adult Nematode Ascaris suum. PLoS Negl Trop Dis 8, e2678, doi: 10.1371/journal.pntd.0002678 (2014).
36. Hasnain, S. Z. et al. Muc5ac: a critical component mediating the rejection of enteric nematodes. J. Exp. Med. 208, 893-900, doi: 10.1084/jem.20102057 (2011).
37. Hunter, S. et al. InterPro in 2011: new developments in the family and domain prediction database. Nucleic acids research 40, D306-312, doi: 10.1093/nar/gkr948 (2012).
38. Asojo, O. A. et al. X-ray structure of Na-ASP-2, a pathogenesis-related-1 protein from the nematode parasite, Necator americanus, and a vaccine antigen for human hookworm infection. Journal of molecular biology 346, 801-814, doi: 10.1016/j.jmb.2004.12.023 (2005).
39. Hobert, O. The neuronal genome of Caenorhabditis elegans. WormBook: the online review of C. elegans biology, 1-106, doi: 10.1895/wormbook.1.161.1 (2013).
40. Dent, J. A., Smith, M. M., Vassilatis, D. K. & Avery, L. The genetics of ivermectin resistance in Caenorhabditis elegans. Proceedings of the National Academy of Sciences of the United States of America 97, 2674-2679 (2000).
41. Cohen, P. Protein kinases-the major drug targets of the twenty-first century? Nat. Rev. Drug Discov. 1, 309-315, doi: 10.1038/nrd773 (2002).
42. Taylor, C. M. et al. Using existing drugs as leads for broad spectrum anthelmintics targeting protein kinases. PLoS pathogens 9, e1003149, doi: 10.1371/journal.ppat.1003149 (2013).
43. Taylor, C. M. et al. Discovery of anthelmintic drug targets and drugs using chokepoints in nematode metabolic pathways. PLoS pathogens 9, e1003505, doi: 10.1371/journal.ppat.1003505 (2013).
44. Ross, M. K. & Crow, J. A. Human carboxylesterases and their role in xenobiotic and endobiotic metabolism. J. Biochem. Mol. Toxicol. 21, 187-196 (2007).
45. Pezzementi, L., Krejci, E., Chatonnet, A., Selkirk, M. E. & Matthews, J. B. A tetrameric acetylcholinesterase from the parasitic nematode Dictyocaulus viviparus associates with the vertebrate tail proteins PRiMA and ColQ. Mol. Biochem. Parasitol. 181, 40-48, doi: 10.1016/j.molbiopara.2011.10.005 (2012).
46. Huby, F., Mallet, S. & Hoste, H. Role of acetylcholinesterase (AChE) secreted by parasitic nematodes on the growth of the cell line from epithelial origin HT29-D4. Parasitology 118 (Pt 5), 489-498 (1999).
47. Dalzell, J. J. et al. RNAi effector diversity in nematodes. PLoS neglected tropical diseases 5, e1176, doi: 10.1371/journal.pntd.0001176 (2011).
48. Vergara, I. A. et al. Genome-wide variations in a natural isolate of the nematode Caenorhabditis elegans. BMC genomics 15, 255, doi: 10.1186/1471-2164-15-255 (2014).
49. Barrett, T. et al. NCBI GEO: archive for functional genomics data sets-update. Nucleic acids research 41, D991-995, doi: 10.1093/nar/gks1193 (2013).
50. Edgar, R., Domrachev, M. & Lash, A. E. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic acids research 30, 207-210 (2002).
51. Margulies, M. et al. Genome sequencing in microfabricated high-density picolitre reactors. Nature 437, 376-380, doi: 10.1038/nature03959 (2005).
52. Parra, G., Bradnam, K., Ning, Z., Keane, T. & Korf, I. Assessing the gene space in draft genomes. Nucleic acids research 37, 289-297, doi: 10.1093/nar/gkn916 (2009).
53. Cantarel, B. L. et al. MAKER: an easy-to-use annotation pipeline designed for emerging model organism genomes. Genome research 18, 188-196, doi: 10.1101/gr.6743907 (2008).
54. Kanehisa, M., Goto, S., Sato, Y., Furumichi, M. & Tanabe, M. KEGG for integration and interpretation of large-scale molecular data sets. Nucleic acids research 40, D109-114, doi: 10.1093/nar/gkr988 (2012).
55. O'Brien, K. P., Remm, M. & Sonnhammer, E. L. Inparanoid: a comprehensive database of eukaryotic orthologs. Nucleic acids research 33, D476-480, doi: 10.1093/nar/gki107 (2005).
56. Li, L., Stoeckert, C. J., Jr. & Roos, D. S. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome research 13, 2178-2189, doi: 10.1101/gr.1224503 (2003).
57. Guiliano, D. B. & Blaxter, M. L. Operon conservation and the evolution of trans-splicing in the phylum Nematoda. PLoS genetics 2, e198, doi: 10.1371/journal.pgen.0020198 (2006).
58. Blumenthal, T. et al. A global analysis of Caenorhabditis elegans operons. Nature 417, 851-854, doi: 10.1038/nature00831 (2002).
59. Li, H. & Durbin, R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25, 1754-1760, doi: 10.1093/bioinformatics/btp324 (2009).
60. McKenna, A. et al. The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome research 20, 1297-1303, doi: 10.1101/gr.107524.110 (2010).
61. Cingolani, P. et al. A program for annotating and predicting the effects of single nucleotide polymorphisms, SnpEff: SNPs in the genome of Drosophila melanogaster strain w1118; iso-2; iso-3. Fly 6, 80-92, doi: 10.4161/fly.19695 (2012).
62. Danecek, P. et al. The variant call format and VCFtools. Bioinformatics 27, 2156-2158, doi: 10.1093/bioinformatics/btr330 (2011).
63. Wang, D., Zhang, Y., Zhang, Z., Zhu, J. & Yu, J. KaKs-Calculator 2.0: a toolkit incorporating gamma-series methods and sliding window strategies. Genomics Proteomics Bioinformatics 8, 77-80, doi: 10.1016/S1672-0229(10)60008-3 (2010).
64. Tajima, F. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585-595 (1989).
65. Kim, D. et al. TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome biology 14, R36, doi: 10.1186/gb-2013-14-4-r36 (2013).
66. Anders, S., Pyl, T. P. & Huber, W. HTSeq - A Python framework to work with high-throughput sequencing data. bioRxiv, doi: 10.1101/002824. (2014).
67. Anders, S. & Huber, W. Differential expression analysis for sequence count data. Genome biology 11, R106, doi: 10.1186/gb-2010-11-10-r106 (2010).
68. Anders, S. et al. Count-based differential expression analysis of RNA sequencing data using R and Bioconductor. Nature protocols 8, 1765-1786, doi: 10.1038/nprot.2013.099 (2013).