What helminth genomes have taught us about parasite evolution

Parasitology

Volumn 142, Issue , 2015, Pages S85-S97

  Zarowiecki, Magdalena ^a   Berriman, Matt ^a  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

Author keywords

Cestoda; comparative transcriptomics; evolution of parasitism; Nematoda; Parasite genomics; phylogeny; Trematoda

Indexed keywords

EXCRETORY PROTEIN; MEMBRANE PROTEIN; PEPTIDES AND PROTEINS; PROTEINASE; UNCLASSIFIED DRUG; TRANSCRIPTOME;

ADAPTATION; ANTIGENIC VARIATION; ASCARIS SUUM; BRUGIA MALAYI; BURSAPHELENCHUS XYLOPHILUS; CAENORHABDITIS; CAENORHABDITIS ELEGANS; CLONORCHIS SINENSIS; DIROFILARIA IMMITIS; ECHINOCOCCUS GRANULOSUS; ECHINOCOCCUS MULTILOCULARIS; EVOLUTION; GENOME; GLOBODERA PALLIDA; HAEMONCHUS CONTORTUS; HELMINTH; HETERORHABDITIS BACTERIOPHORA; HOST; IMMUNE SYSTEM; LOA LOA; MELOIDOGYNE HAPLA; MELOIDOGYNE INCOGNITA; METABOLISM; MULTIGENE FAMILY; NECATOR AMERICANUS; NEMATODE; NONHUMAN; ONCHOCERCA VOLVULUS; OXIDATION REDUCTION REACTION; PANAGRELLUS REDIVIVUS; PARASITOSIS; PLATYHELMINTH; PRIORITY JOURNAL; PROTEIN DEGRADATION; REVIEW; ROMANOMERMIS CULICIVORAX; SCHISTOSOMA HEMATOBIUM; SCHISTOSOMA JAPONICUM; SCHISTOSOMA MANSONI; SCHMIDTEA MEDITERRANEA; STRONGYLOIDES RATTI; TAENIA SOLIUM; TRICHINELLA SPIRALIS; TRICHURIS MURIS; TRICHURIS TRICHIURA; ANIMAL; GENETICS; META ANALYSIS; PARASITE; PHYSIOLOGY;

CESTODA; NEMATODA; PLATYHELMINTHES; TREMATODA; VERMES;

ADAPTATION, PHYSIOLOGICAL; ANIMALS; BIOLOGICAL EVOLUTION; GENOME, HELMINTH; HELMINTHS; IMMUNE SYSTEM; NEMATODA; PARASITES; PLATYHELMINTHS; TRANSCRIPTOME;

EID: 84922635506     PISSN: 00311820     EISSN: 14698161     Source Type: Journal    
DOI: 10.1017/S0031182014001449     Document Type: Review

References (72)

1. Abad, P., Gouzy, J., Aury, J. M., Castagnone-Sereno, P., Danchin, E. G. J., Deleury, E., Perfus-Barbeoch, L., Anthouard, V., Artiguenave, F., Blok, V. C., Caillaud, M. C., Coutinho, P. M., Dasilva, C., De Luca, F., Deau, F., Esquibet, M., Flutre, T., Goldstone, J. V., Hamamouch, N., Hewezi, T., Jaillon, O., Jubin, C., Leonetti, P., Magliano, M., Maier, T. R., Markov, G. V., McVeigh, P., Pesole, G., Poulain, J., Robinson-Rechavi, M., et al. (2008). Genome sequence of the metazoan plant-parasitic nematode Meloidogyne incognita. Nature Biotechnology 26, 909-915.
2. Adrian, A. and Rahnenfuhrer, J. (2010). topGO: enrichment analysis for gene ontology. R package version 2.8.
3. Altschul, S. F., Gish, W., Miller, W., Myers, E.W. and Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology 215, 403-410.
4. Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T., Harris, M. A., Hill, D. P., Issel-Tarver, L., Kasarskis, A., Lewis, S., Matese, J. C., Richardson, J. E., Ringwald, M., Rubin, G. M. and Sherlock, G. (2000). Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nature Genetics 25, 25-29.
5. Bai, X. D., Adams, B. J., Ciche, T. A., Clifton, S., Gaugler, R., Kim, K., Spieth, J., Sternberg, P.W., Wilson, R. K. and Grewal, P. S. (2013). A lover and a fighter: the genome sequence of an entomopathogenic nematode Heterorhabditis bacteriophora. PLoS One 8, ARTN e69618.
6. Barry, J. D., Marcello, L., Morrison, L. J., Read, A. F., Lythgoe, K., Jones, N., Carrington, M., Blandin, G., Bohme, U., Caler, E., Hertz-Fowler, C., Renauld, H., El-Sayed, N. and Berriman, M. (2005). What the genome sequence is revealing about trypanosome antigenic variation. Biochemical Society Transactions 33, 986-989.
7. Berriman, M., Haas, B. J., LoVerde, P. T., Wilson, R. A., Dillon, G. P., Cerqueira, G. C., Mashiyama, S. T., Al-Lazikani, B., Andrade, L. F., Ashton, P. D., Aslett, M. A., Bartholomeu, D. C., Blandin, G., Caffrey, C. R., Coghlan, A., Coulson, R., Day, T. A., Delcher, A., DeMarco, R., Djikeng, A., Eyre, T., Gamble, J. A., Ghedin, E., Gu, Y., Hertz-Fowler, C., Hirai, H., Hirai, Y., Houston, R., Ivens, A., Johnston, D. A., et al. (2009). The genome of the blood fluke Schistosoma mansoni. Nature 460, 352-U365.
8. 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.
9. Bird, D. M., Jones, J. T., Opperman, C. H., Kikuchi, T. and Danchin, E. G. J. (2014). Signatures of adaptation to plant parasitism in nematode genomes. Parasitology. doi: 10.1017/S0031182013002163.
10. Blaxter, M. and Koutsovoulos, G. (2014) The evolution of parasitism in Nematoda. Parasitology. doi: 10.1017/S0031182014000791.
11. 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. (1998). A molecular evolutionary framework for the phylum Nematoda. Nature 392, 71-75.
12. Budke, C. M., White, A. C., Jr. and Garcia, H. H. (2009). Zoonotic larval cestode infections: neglected, neglected tropical diseases? PLoS Neglected Tropical Diseases 3, e319.
13. C. elegans Sequencing Consortium (1998). Genome sequence of the nematode C. elegans: a platform for investigating biology. Science 282, 2012-2018.
14. Cantacessi, C., Campbell, B. E., Visser, A., Geldhof, P., Nolan, M. J., Nisbet, A. J., Matthews, J. B., Loukas, A., Hofmann, A., Otranto, D., Sternberg, P.W. and Gasser, R. B. (2009). A portrait of the "SCP/TAPS" proteins of eukaryotes-developing a framework for fundamental research and biotechnological outcomes. Biotechnology Advances 27, 376-388.
15. Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Molecular Biology and Evolution 17, 540-552.
16. Chalmers, I.W., McArdle, A. J., Coulson, R. M. R., Wagner, M. A., Schmid, R., Hirai, H. and Hoffmann, K. F. (2008). Developmentally regulated expression, alternative splicing and distinct sub-groupings in members of the Schistosoma mansoni venom allergen-like (SmVAL) gene family. BMC Genomics 9, 89.
17. Christin, P. A., Weinreich, D. M. and Besnard, G. (2010). Causes and evolutionary significance of genetic convergence. Trends in Genetics 26, 400-405.
18. Cotton, J. A., Lilley, C. J., Jones, L. M., Kikuchi, T., Reid, A. J., Thorpe, P., Tsai, I. J., Beasley, H., Blok, V., Cock, P. J., Eves-van den Akker, S., Holroyd, N., Hunt, M., Mantelin, S., Naghra, H., Pain, A., Palomares-Rius, J. E., Zarowiecki, M., Berriman, M., Jones, J. T. and Urwin, P. E. (2014). The genome and life-stage specific transcriptomes of Globodera pallida elucidate key aspects of plant parasitism by a cyst nematode. Genome Biology 15, R43.
19. Desjardins, C. A., Cerqueira, G. C., Goldberg, J. M., Dunning Hotopp, J. C., Haas, B. J., Zucker, J., Ribeiro, J. M., Saif, S., Levin, J. Z., Fan, L., Zeng, Q., Russ, C., Wortman, J. R., Fink, D. L., Birren, B.W. and Nutman, T. B. (2013). Genomics of Loa loa, a Wolbachia-free filarial parasite of humans. Nature Genetics, 45, 495-500.
20. Diaz, A., Casaravilla, C., Allen, J. E., Sim, R. B. and Ferreira, A. M. (2011). Understanding the laminated layer of larval Echinococcus II: immunology. Trends in Parasitology 27, 264-273.
21. Dieterich, C. and Sommer, R. J. (2009). How to become a parasite-lessons from the genomes of nematodes. Trends in Genetics 25, 203-209.
22. Dieterich, C., Clifton, S.W., Schuster, L. N., Chinwalla, A., Delehaunty, K., Dinkelacker, I., Fulton, L., Fulton, R., Godfrey, J., Minx, P., Mitreva, M., Roeseler, W., Tian, H., Witte, H., Yang, S. P., Wilson, R. K. and Sommer, R. J. (2008). The Pristionchus pacificus genome provides a unique perspective on nematode lifestyle and parasitism. Nature Genetics 40, 1193-1198.
23. Fonseca, C. T., Braz Figueiredo Carvalho, G., Carvalho Alves, C. and de Melo, T. T. (2012). Schistosoma tegument proteins in vaccine and diagnosis development: an update. Journal of Parasitology Research 2012, 541268.
24. Foth, B., Tsai, I., Reid, A., Bancroft, A., Nichol, S., Tracey, A., Holroyd, N., Cotton, J., Stanley, E., Zarowiecki, M., Liu, J., Huckvale, T., Cooper, P., Grencis, R. and Berriman, M. (2014). The whipworm genome and dual-species transcriptomics of an intimate hostpathogen interaction. Nature Genetics 46, 693-700.
25. Ghedin, E., Wang, S. L., 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. S., Crawford, M. J., Daub, J., et al. (2007). Draft genome of the filarial nematode parasite Brugia malayi. Science 317, 1756-1760.
26. Godel, C., Kumar, S., Koutsovoulos, G., Ludin, P., Nilsson, D., Comandatore, F.,Wrobel, N., Thompson, M., Schmid, C. D., Goto, S., Bringaud, F., Wolstenholme, A., Bandi, C., Epe, C., Kaminsky, R., Blaxter, M. and Maser, P. (2012). The genome of the heartworm, Dirofilaria immitis, reveals drug and vaccine targets. FASEB Journal 26, 4650-4661.
27. Hahn, C., Fromm, B. and Bachmann, L. (2014). Comparative genomics of flatworms (Platyhelminthes) reveals shared genomic features of ecto-and endoparastic Neodermata. Genome Biology and Evolution 6, 1105-1117. Advanced access.
28. Harris, A. R., Russell, R. J. and Charters, A. D. (1984). A review of schistosomiasis in immigrants in Western Australia, demonstrating the unusual longevity of Schistosoma mansoni. Transactions of the Royal Society of Tropical Medicine and Hygiene 78, 385-388.
29. Hewitson, J. P., Grainger, J. R. and Maizels, R. M. (2009). Helminth immunoregulation: the role of parasite secreted proteins in modulating host immunity. Molecular and Biochemical Parasitology 167, 1-11.
30. Huang, Y., Chen, W., Wang, X., Liu, H., Chen, Y., Guo, L., Luo, F., Sun, J., Mao, Q., Liang, P., Xie, Z., Zhou, C., Tian, Y., Lv, X., Huang, L., Zhou, J., Hu, Y., Li, R., Zhang, F., Lei, H., Li, W., Hu, X., Liang, C., Xu, J., Li, X. and Yu, X. (2013). The carcinogenic liver fluke, Clonorchis sinensis: new assembly, reannotation and analysis of the genome and characterization of tissue transcriptomes. PLoS One 8, e54732.
31. Hunter, S., Jones, P., Mitchell, A., Apweiler, R., Attwood, T. K., Bateman, A., Bernard, T., Binns, D., Bork, P., Burge, S., de Castro, E., Coggill, P., Corbett, M., Das, U., Daugherty, L., Duquenne, L., Finn, R. D., Fraser, M., Gough, J., Haft, D., Hulo, N., Kahn, D., Kelly, E., Letunic, I., Lonsdale, D., Lopez, R., Madera, M., Maslen, J., McAnulla, C., McDowall, J., et al. (2012). InterPro in 2011:new developments in the family and domain prediction database. Nucleic acids research, 40, D306-D312.
32. Isnard, A., Shio, M. T. and Olivier, M. (2012). Impact of Leishmania metalloprotease GP63 on macrophage signaling. Frontiers in Cellular and Infection Microbiology 2, 72.
33. Jex, A. R., Liu, S. P., Li, B., Young, N. D., Hall, R. S., Li, Y. R., Yang, L. F., Zeng, N., Xu, X., Xiong, Z. J., Chen, F. Y., Wu, X., Zhang, G. J., Fang, X. D., Kang, Y., Anderson, G. A., Harris, T.W., Campbell, B. E., Vlaminck, J., Wang, T., Cantacessi, C., Schwarz, E. M., Ranganathan, S., Geldhof, P., Nejsum, P., Sternberg, P.W., Yang, H. M., Wang, J., Wang, J. and Gasser, R. B. (2011). Ascaris suum draft genome. Nature 479, 529-U257.
34. Katoh, K. and Standley, D.M. (2014). MAFFT: iterative refinement and additional methods. Methods in Molecular Biology 1079, 131-146.
35. Kikuchi, T., Cotton, J. A., Dalzell, J. J., Hasegawa, K., Kanzaki, N., McVeigh, P., Takanashi, T., Tsai, I. J., Assefa, S. A., Cock, P. J., Otto, T. D., Hunt, M., Reid, A. J., Sanchez-Flores, A., Tsuchihara, K., Yokoi, T., Larsson, M. C., Miwa, J., Maule, A. G., Sahashi, N., Jones, J. T. and Berriman, M. (2011). Genomic insights into the origin of parasitism in the emerging plant pathogen Bursaphelenchus xylophilus. PLoS Pathogens 7, e1002219.
36. Koziol, U., Iriarte, A., Castillo, E., Soto, J., Bello, G., Cajarville, A., Roche, L. and Marin, M. (2009). Characterization of a putative hsp70 pseudogene transcribed in protoscoleces and adult worms of Echinococcus granulosus. Gene 443, 1-11.
37. Kumar, S., Koutsovoulos, G., Kaur, G. and Blaxter,M. (2012). Toward 959 nematode genomes. Worm 1, 42-50.
38. Laing, R., Kikuchi, T., Martinelli, A., Tsai, I. J., Beech, R. N., Redman, E., Holroyd, N., Bartley, D. J., Beasley, H., Britton, C., Curran, D., Devaney, E., Gilabert, A., Hunt, M., Jackson, F., Johnston, S. L., Kryukov, I., Li, K. Y., Morrison, A. A., Reid, A. J., Sargison, N., Saunders, G. I., Wasmuth, J. D., Wolstenholme, A., Berriman, M., Gilleard, J. S. and Cotton, J. A. (2013). The genome and transcriptome of Haemonchus contortus, a key model parasite for drug and vaccine discovery. Genome Biology 14, R88.
39. Lemieux, J. E., Kyes, S. A., Otto, T. D., Feller, A. I., Eastman, R. T., Pinches, R. A., Berriman, M., Su, X. Z. and Newbold, C. I. (2013). Genome-wide profiling of chromosome interactions in Plasmodium falciparum characterizes nuclear architecture and reconfigurations associated with antigenic variation. Molecular Microbiology 90, 519-537.
40. Littlewood, D. T. J., Rohde, K. and Clough, K. A. (1999). The interrelationships of all major groups of Platyhelminthes: phylogenetic evidence from morphology and molecules. Biological Journal of the Linnean Society 66, 75-114.
41. Maizels, R. M. and Yazdanbakhsh, M. (2003). Immune regulation by helminth parasites: cellular and molecular mechanisms. Nature Reviews Immunology 3, 733-744.
42. McGwire, B. S., Chang, K. P. and Engman, D. M. (2003). Migration through the extracellular matrix by the parasitic protozoan Leishmania is enhanced by surface metalloprotease gp63. Infection and Immunity 71, 1008-1010.
43. Mitreva, M., Jasmer, D. P., Zarlenga, D. S., Wang, Z. Y., Abubucker, S., Martin, J., Taylor, C. M., Yin, Y., Fulton, L., Minx, P., Yang, S. P., Warren, W. C., Fulton, R. S., Bhonagiri, V., Zhang, X., Hallsworth-Pepin, K., Clifton, S.W., McCarter, J. P., Appleton, J., Mardis, E. R. and Wilson, R. K. (2011). The draft genome of the parasitic nematode Trichinella spiralis. Nature Genetics 43, 228-U274.
44. Moriya, Y., Itoh, M., Okuda, S., Yoshizawa, A. C. and Kanehisa, M. (2007). KAAS: an automatic genome annotation and pathway reconstruction server. Nucleic Acids Research, 35, W182-185
45. Nicol, J., Turner, S., Coyne, D., den Nijs, L., Hockland, S. and Maafi, Z. (eds.) (2011). Current Nematode Threats to World Agriculture, Springer, The Netherlands.
46. Opperman, C. H., Bird, D. M., Williamson, V. M., Rokhsar, D. S., Burke, M., Cohn, J., Cromer, J., Diener, S., Gajan, J., Graham, S., Houfek, T. D., Liu, Q., Mitros, T., Schaff, J., Schaffer, R., Scholl, E., Sosinski, B. R., Thomas, V. P. and Windham, E. (2008). Sequence and genetic map of Meloidogyne hapla: a compact nematode genome for plant parasitism. Proceedings of the National Academy of Sciences of the United States of America 105, 14802-14807.
47. Orme, C. (2013). The caper package: comparative analysis of phylogenetics and evolution in R.Available: http://cran.r-project.org/web/packages/caper.
48. Poulin, R. (2011). Evolutionary Ecology of Parasites, Princeton University press, New Jersey, USA
49. Price, P.W. (1980). Evolutionary biology of parasites. Monographs in Population Biology 15, 1-237.
50. Protasio, A. V., Tsai, I. J., Babbage, A., Nichol, S., Hunt, M., Aslett, M. A., De Silva, N., Velarde, G. S., Anderson, T. J. C., Clark, R. C., Davidson, C., Dillon, G. P., Holroyd, N. E., LoVerde, P. T., Lloyd, C., McQuillan, J., Oliveira, G., Otto, T. D., Parker-Manuel, S. J., Quail, M. A., Wilson, R. A., Zerlotini, A., Dunne, D.W. and Berriman, M. (2012). A systematically improved high quality genome and transcriptome of the human blood fluke Schistosoma mansoni. PLoS Neglected Tropical Diseases 6, ARTN e1455.
51. Quicke, D. L. J. and Belshaw, R. (1999). Incongruence between morphological data sets: an example from the evolution of endoparasitism among parasitic wasps (Hymenoptera: Braconidae). Systematic Biology 48, 436-454.
52. R Core Team (2013). R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/.
53. Rawlings, N. D., Waller, M., Barrett, A. J. and Bateman, A. (2014). MEROPS: the database of proteolytic enzymes, their substrates and inhibitors. Nucleic Acids Research 42, D503-509.
54. Reid, A. (2014). Large, rapidly evolving gene families are at the forefront of host-parasite interactions in Apicomplexa. Parasitology. doi: 10.1017/S0031182014001528.
55. Robb, S. M. C., Ross, E. and Alvarado, A. S. (2008). SmedGD: the Schmidtea mediterranea genome database. Nucleic Acids Research, 36, D599-D606.
56. Roth, A. C., Gonnet, G. H. and Dessimoz, C. (2008). Algorithm of OMA for large-scale orthology inference. BMC Bioinformatics 9, 518.
57. Schiffer, P. H., Kroiher, M., Kraus, C., Koutsovoulos, G. D., Kumar, S., Camps, J. I., Nsah, N. A., Stappert, D., Morris, K., Heger, P., Altmuller, J., Frommolt, P., Nurnberg, P., Thomas, W. K., Blaxter, M. L. and Schierenberg, E. (2013). The genome of Romanomermis culicivorax: revealing fundamental changes in the core developmental genetic toolkit in Nematoda. BMC Genomics 14, 923.
58. Schirmer, R. H., Schollhammer, T., Eisenbrand, G. and Krauth-Siegel, R. L. (1987). Oxidative stress as a defense mechanism against parasitic infections. Free Radical Research Communications 3, 3-12.
59. Schwarz, E. M., Korhonen, P. K., Campbell, B. E., Young, N. D., Jex, A. R., Jabbar, A., Hall, R. S., Mondal, A., Howe, A. C., Pell, J., Hofmann, A., Boag, P. R., Zhu, X. Q., Gregory, T. R., Loukas, A., Williams, B. A., Antoshechkin, I., Brown, C. T., Sternberg, P.W. and Gasser, R. B. (2013). The genome and developmental transcriptome of the strongylid nematode Haemonchus contortus. Genome Biology 14, R89.
60. Spruance, S. L. (1974). Latent period of 53 years in a case of hydatid cyst disease. Archives of Internal Medicine 134, 741-742.
61. Srinivasan, J., Dillman, A. R., Macchietto, M. G., Heikkinen, L., Lakso, M., Fracchia, K. M., Antoshechkin, I., Mortazavi, A., Wong, G. and Sternberg, P.W. (2013). The draft genome and transcriptome of Panagrellus redivivus are shaped by the harsh demands of a free-living lifestyle. Genetics 193, 1279-1295.
62. Stamatakis, A., Hoover, P. and Rougemont, J. (2008). A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology 57, 758-771.
63. Stein, L. D., Bao, Z., Blasiar, D., Blumenthal, T., Brent, M. R., Chen, N., Chinwalla, A., Clarke, L., Clee, C., Coghlan, A., Coulson, A., D'Eustachio, P., Fitch, D.H., Fulton, L. A., Fulton, R. E., Griffiths-Jones, S., Harris, T.W., Hillier, L.W., Kamath, R., Kuwabara, P. E., Mardis, E. R., Marra, M. A., Miner, T. L., Minx, P., Mullikin, J. C., Plumb, R.W., Rogers, J., Schein, J. E., Sohrmann, M., Spieth, J., et al. (2003). The genome sequence of Caenorhabditis briggsae: a platform for comparative genomics. PLoS Biology 1, E45.
64. Steinmann, P., Keiser, J., Bos, R., Tanner, M. and Utzinger, J. (2006). Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infectious Diseases 6, 411-425.
65. Tang, Y. T., Gao, X., Rosa, B. A., Abubucker, S., Hallsworth-Pepin, K., Martin, J., Tyagi, R., Heizer, E., Zhang, X., Bhonagiri-Palsikar, V., Minx, P., Warren, W. C., Wang, Q., Zhan, B., Hotez, P. J., Sternberg, P.W., Dougall, A., Gaze, S. T., Mulvenna, J., Sotillo, J., Ranganathan, S., Rabelo, E. M., Wilson, R. K., Felgner, P. L., Bethony, J., Hawdon, J. M., Gasser, R. B., Loukas, A. and Mitreva, M. (2014). Genome of the human hookworm Necator americanus. Nature Genetics 46, 261-269.
66. Torgerson, P. R. and Macpherson, C. N. (2011). The socioeconomic burden of parasitic zoonoses: global trends. Veterinary Parasitology 182, 79-95.
67. Tran, M. H., Freitas, T. C., Cooper, L., Gaze, S., Gatton, M. L., Jones, M. K., Lovas, E., Pearce, E. J. and Loukas, A. (2010). Suppression of mRNAs encoding tegument tetraspanins from Schistosoma mansoni results in impaired tegument turnover. PLoS Pathogens 6, e1000840.
68. Tsai, I. J., Zarowiecki, M., Holroyd, N., Garciarrubio, A., Sanchez-Flores, A., Brooks, K. L., Tracey, A., Bobes, R. J., Fragoso, G., Sciutto, E., Aslett, M., Beasley, H., Bennett, H. M., Cai, J. P., Camicia, F., Clark, R., Cucher, M., De Silva, N., Day, T. A., Deplazes, P., Estrada, K., Fernandez, C., Holland, P.W. H., Hou, J. L., Hu, S. N., Huckvale, T., Hung, S. S., Kamenetzky, L., Keane, J. A., Kiss, F., et al. (2013). The genomes of four tapeworm species reveal adaptations to parasitism. Nature 496, 57-63.
69. Wang, X., Chen, W., Huang, Y., Sun, J., Men, J., Liu, H., Luo, F., Guo, L., Lv, X., Deng, C., Zhou, C., Fan, Y., Li, X., Huang, L., Hu, Y., Liang, C., Hu, X., Xu, J. and Yu, X. (2011). The draft genome of the carcinogenic human liver fluke Clonorchis sinensis. Genome Biology 12, R107.
70. Young, N. D., Jex, A. R., Li, B., Liu, S. P., Yang, L. F., Xiong, Z. J., Li, Y. R., Cantacessi, C., Hall, R. S., Xu, X., Chen, F. Y., Wu, X., Zerlotini, A., Oliveira, G., Hofmann, A., Zhang, G. J., Fang, X. D., Kang, Y., Campbell, B. E., Loukas, A., Ranganathan, S., Rollinson, D., Rinaldi, G., Brindley, P. J., Yang, H. M., Wang, J., Wang, J. and Gasser, R. B. (2012). Whole-genome sequence of Schistosoma haematobium. Nature Genetics 44, 221-225.
71. Zheng, H., Zhang, W., Zhang, L., Zhang, Z., Li, J., Lu, G., Zhu, Y., Wang, Y., Huang, Y., Liu, J., Kang, H., Chen, J., Wang, L., Chen, A., Yu, S., Gao, Z., Jin, L., Gu, W., Wang, Z., Zhao, L., Shi, B., Wen, H., Lin, R., Jones, M. K., Brejova, B., Vinar, T., Zhao, G., McManus, D. P., Chen, Z., Zhou, Y., et al. (2013). The genome of the hydatid tapeworm Echinococcus granulosus. Nature Genetics 45, 1168-1175.
72. Zhou, Y., Zheng, H. J., Chen, Y. Y., Zhang, L., Wang, K., Guo, J., Huang, Z., Zhang, B., Huang, W., Jin, K., Dou, T. H., Hasegawa, M., Wang, L., Zhang, Y., Zhou, J., Tao, L., Cao, Z.W., Li, Y. X., Vinar, T., Brejova, B., Brown, D., Li, M., Miller, D. J., Blair, D., Zhong, Y., Chen, Z., Hu, W., Wang, Z. Q., Zhang, Q. H., Song, H., et al. (2009). The Schistosoma japonicum genome reveals features of host-parasite interplay. Nature 460, 345-U356.