Cestode genomics - progress and prospects for advancing basic and applied aspects of flatworm biology

Parasite Immunology

Volumn 34, Issue 2-3, 2012, Pages 130-150

  Olson, P D ^a   Zarowiecki, M ^a,b   Kiss, F ^c   Brehm, K ^c  

^a DEPARTMENT OF LIFE SCIENCES   (United Kingdom)

^b WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^c UNIVERSITY OF WÜRZBURG   (Germany)

Author keywords

Antigen B; Cestode; Echinococcus; EG95; Genome; Hymenolepis; S3Pvac

Indexed keywords

ALBENDAZOLE; BLOOD GROUP B ANTIGEN; HOX PROTEIN; MEBENDAZOLE; PARASITE ANTIGEN; PRAZIQUANTEL; WNT PROTEIN;

CESTODE; CESTODIASIS; CHEMOTHERAPY; DRUG ACTIVITY; DRUG EFFICACY; ECHINOCOCCUS GRANULOSUS; ECHINOCOCCUS MULTILOCULARIS; GENE EXPRESSION; GENETIC POLYMORPHISM; GENOMICS; HOST PARASITE INTERACTION; HUMAN; HYMENOLEPIS; HYMENOLEPIS MICROSTOMA; IMMUNOMODULATION; MOLECULAR EVOLUTION; MOLECULAR PHYLOGENY; MORPHOGENESIS; MULTIGENE FAMILY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SIGNAL TRANSDUCTION; TAENIA SOLIUM; TAENIASIS;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, HELMINTH; CESTODA; CESTODE INFECTIONS; GENOME, HELMINTH; GENOMICS; HELMINTH PROTEINS; HOST-PATHOGEN INTERACTIONS; MOLECULAR SEQUENCE DATA; SEQUENCE ANALYSIS, DNA;

CESTODA; ECHINOCOCCUS; ECHINOCOCCUS GRANULOSUS; ECHINOCOCCUS MULTILOCULARIS; HYMENOLEPIS (CESTODA); PLATYHELMINTHES; RODENTOLEPIS MICROSTOMA; TAENIA SOLIUM;

EID: 80054715434     PISSN: 01419838     EISSN: 13653024     Source Type: Journal    
DOI: 10.1111/j.1365-3024.2011.01319.x     Document Type: Review

References (165)

1. Brehm K. Echinococcus multilocularis as an experimental model in stem cell research and molecular host-parasite interaction. Parasitology 2010; 137: 537-555.
2. Koziol U, Dominguez MF, Marin M, Kun A & Castillo E. Stem cell proliferation during in vitro development of the model cestode Mesocestoides corti from larva to adult worm. Front Zool 2010; 7: 1-12.
3. Peter R, Gschwentner R & Schurmann W. The significance of stem cells in free-living flatworms: one common source for all cells in the adult. J Appl Biomed 2004; 2: 21-35.
4. Wagner DE, Wang IE & Reddien PW. Clonogenic neoblasts are pluripotent adult stem cells that underlie planarian regeneration. Science 2011; 332: 811-816.
5. Reuter M & Kreshchenko N. Flatworm asexual multiplication implicates stem cells and regeneration. Can J Zool 2004; 82: 334-356.
6. Read CP. Longevity of the tapeworm, Hymenolepis diminuta. J Parasitol 1967; 53: 1055.
7. Olson PD, Yoder K, Fajardo L-G LF, et al. Lethal invasive cestodiasis in immunosuppressed patients. J Infect Dis 2003; 187: 1962-1966.
8. Adoutte A, Balavoine G, Lartillot N, Lespinet O, Prud'homme B & de Rosa R. The new animal phylogeny: reliability and implications. Proc Natl Acad Sci USA 2000; 97: 4453-4456.
9. Halanych KM. The new view of animal phylogeny. Annu Rev Ecol Evol Syst 2004; 35: 229-256.
10. Hejnol A, Obst M, Stamatakis A, et al. Assessing the root of bilaterian animals with scalable phylogenoimc methods. Proc R Soc B Biol Sci 2009; 276: 4261-4270.
11. Littlewood DTJ. The evolution of parasitism in flatworms. In Maule AG & Marks N (eds): Parasitic Flatworms: Molecular Biology, Biochemistry, Immunology and Physiology. Wallingford, CAB International, 2006: 1-36.
12. Littlewood DTJ & Olson PD. Small subunit rDNA and the Platyhelminthes: signal, noise, conflict and compromise. In Littlewood DTJ & Bray RA (eds): Interrelationships of the Platyhelminthes. London, Taylor & Francis, 2001: 262-278.
13. Olson PD, Caira JN, Jensen K, Overstreet RM, Palm HW & Beveridge I. Evolution of the trypanorhynch tapeworms: parasite phylogeny supports independent lineages of sharks and rays. Int J Parasitol 2010; 40: 223-242.
14. Olson PD & Tkach VV. Advances and trends in the molecular systematics of the parasitic Platyhelminthes. Adv Parasitol 2005; 60: 165-243.
15. Lockyer AE, Olson PD & Littlewood DTJ. Utility of complete large and small subunit rRNA genes in resolving the phylogeny of the Platyhelminthes: implications and a review of the cercomer theory. Biol J Linn Soc 2003; 78: 155-171.
16. Caira JN, Scholz T & Georgiev BB. Cestode systematics and phylogeny move forward. Syst Parasitol 2006; 65: 171-174.
17. Healy CJ, Caira JN, Jensen K, Webster B & Littlewood DTJ. Proposal for a new tapeworm order, Rhinebothriidea. Int J Parasitol 2009; 39: 497-511.
18. Kuchta R, Scholz T, Brabec J & Bray RA. Suppression of the tapeworm order Pseudophyllidea (Platyhelminthes: Eucestoda) and the proposal of two new orders, Bothriocephalidea and Diphyllobothriidea. Int J Parasitol 2008; 38: 49-55.
19. Olson PD & Caira JN. Evolution of the major lineages of tapeworms (Platyhelminthes: Cestoidea) inferred from 18S ribosomal DNA and elongation factor-1a. J Parasitol 1999; 85: 1134-1159.
20. Olson PD, Littlewood DTJ, Bray RA & Mariaux J. Interrelationships and evolution of the tapeworms (Platyhelminthes: Cestoda). Mol Phylogenet Evol 2001; 19: 443-467.
21. Olson PD, Poddubnaya LG, Littlewood DTJ & Scholz T. On the position of Archigetes and its bearing on the early evolution of the tapeworms. J Parasitol 2008; 94: 898-904.
22. Olson PD, Littlewood DTJ, Griffiths D, Kennedy CR & Arme C. Evidence for the co-existence of separate strains or species of Ligula in Lough Neagh, Northern Ireland. J Helminthol 2002; 76: 171-174.
23. McKay DM & Webb RA. Cestode infections: Immunological considerations from host and tapeworm perspectives. In Maule AG & Marks NJ (eds): Parasitic Flatworms: Molecular Biology, Biochemistry, Immunology and Physiology. Wallingford, CAB International, 2006: 193-209.
24. Hoberg EP. Phylogeny of Taenia: species definitions and origins of human parasites. Parasitol Int 2006; 55: S23-S30.
25. Hrčkova G, O'Connor A, Šnabel V, Mitterpáková M & Olson PD. Molecular and morphological circumscription of Mesocestoides tapeworms from red foxes (Vulpes vulpes) in central Europe. Parasitology 2011; 138: 638-647.
26. Hoberg EP, Alkire NL, de Queiroz A & Jones A. Out of Africa: origins of the Taenia tapeworms in humans. Proc R Soc B Biol Sci 2001; 268: 781-787.
27. Berriman M, Haas BJ, Loverde PT, et al. The genome of the blood fluke Schistosoma mansoni. Nature 2009; 460: 352-358.
28. Consortium TSjGSaFA. The Schistosoma japonicum genome reveals features of host-parasite interplay. Nature 2009; 460: 345-351.
29. Sánchez Alvarado A, Newmark PA, Robb SM & Juste R. The Schmidtea mediterranea database as a molecular resource for studying platyhelminthes, stem cells and regeneration. Development 2002; 129: 5659-5665.
30. Mouton S, Willems M, Braeckman BP, et al. The free-living flatworm Macrostomum lignano: a new model organism for ageing research. Exp Gerontol 2009; 44: 243-249.
31. Dieterich C & Sommer RJ. How to become a parasite - lessons from the genomes of nematodes. Trends Genet 2009; 25: 203-209.
32. Copeland CS, Brindley PJ, Heyers O, et al. Boudicca, a retrovirus-like long terminal repeat retrotransposon from the genome of the human blood fluke Schistosoma mansoni. J Virol 2003; 77: 6153-6166.
33. Copeland CS, Mann VH, Morales ME, Kalinna BH & Brindley PJ. The Sinbad retrotransposon from the genome of the human blood fluke, Schistosoma mansoni, and the distribution of related Pao-like elements. BMC Evol Biol 2005; 5: 20.
34. Spiliotis M & Brehm K. Axenic in vitro cultivation of Echinococcus multilocularis metacestode vesicles and the generation of primary cell cultures. Methods Mol Biol 2009; 470: 245-262.
35. Spiliotis M, Tappe D, Sesterhenn L & Brehm K. Long-term in vitro cultivation of Echinococcus multilocularis metacestodes under axenic conditions. Parasitol Res 2004; 92: 430-432.
36. Spiliotis M, Lechner S, Tappe D, Scheller C, Krohne G & Brehm K. Transient transfection of Echinococcus multilocularis primary cells and complete in vitro regeneration of metacestode vesicles. Int J Parasitol 2008; 38: 1025-1039.
37. Tappe D, Brehm K, Frosch M, et al. Echinococcus multilocularis infection of several Old World monkey species in a breeding enclosure. Am J Trop Med Hyg 2007; 77: 504-506.
38. Han ZG, Brindley PJ, Wang SY & Chen Z. Schistosoma genomics: new perspectives on schistosome biology and host-parasite interaction. Annu Rev Genomics Hum Genet 2009; 10: 211-240.
39. Scott AL & Ghedin E. The genome of Brugia malayi- all worms are not created equal. Parasitol Int 2009; 58: 6-11.
40. Brehm K, Kronthaler K, Jura H & Frosch M. Cloning and characterization of beta-tubulin genes from Echinococcus multilocularis. Mol Biochem Parasitol 2000; 107: 297-302.
41. Fernandez C, Gregory WF, Loke P & Maizels RM. Full-length-enriched cDNA libraries from Echinococcus granulosus contain separate populations of oligo-capped and trans-spliced transcripts and a high level of predicted signal peptide sequences. Mol Biochem Parasitol 2002; 122: 171-180.
42. Koziol U, Iriarte A, Castillo E, et al. Characterization of a putative hsp70 pseudogene transcribed in protoscoleces and adult worms of Echinococcus granulosus. Gene 2009; 443: 1-11.
43. Aguilar-Díaz H, Bobes RJ, Carrero JC, et al. The genome project of Taenia solium. Parasitol Int 2006; 55: S127-S130.
44. Arai HP. Biology of the Tapeworm Hymenolepis diminuta. New York, Academic Press, 1980.
45. Haukisalmi V, Hardman LM, Foronda P, et al. Systematic relationships of hymenolepidid cestodes of rodents and shrews inferred from squences of 28S ribosomal RNA. Zoo Scripta 2010; 39: 631-641.
46. Cunningham LJ & Olson PD. Description of Hymenolepis microstoma (Nottingham strain): a classical tapeworm model for research in the genomic era. Parasit Vectors 2010; 3: 123.
47. Stewart GL, Lumsden RD & Fisher FM. The contributions of Clark P. Read on ecology of the vertebrate gut and its parasites. Bios 1975; 46: 3-21.
48. Tsai IJ, Otto TD & Berriman M. Improving draft assemblies by iterative mapping and assembly of short reads to eliminate gaps. Genome Biol 2010; 11: R41.
49. Otto TD, Sanders M, Berriman M & Newbold C. Iterative Correction of Reference Nucleotides (iCORN) using second generation sequencing technology. Bioinformatics 2010; 26: 1704-1707.
50. Carver T, Bohme U, Otto TD, Parkhill J & Berriman M. BamView: viewing mapped read alignment data in the context of the reference sequence. Bioinformatics 2010; 26: 676-677.
51. Rutherford K, Parkhill J, Crook J, et al. Artemis: sequence visualization and annotation. Bioinformatics 2000; 16: 944-945.
52. Carver T, Berriman M, Tivey A, et al. Artemis and ACT: viewing, annotating and comparing sequences stored in a relational database. Bioinformatics 2008; 24: 2672-2676.
53. Hertz-Fowler C, Peacock CS, Wood V, et al. GeneDB: a resource for prokaryotic and eukaryotic organisms. Nucleic Acids Res 2004; 32: D339-D343.
54. Trapnell C, Pachter L & Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics 2009; 25: 1105-1111.
55. Simpson JT, Wong K, Jackman SD, Schein JE, Jones SJM & Birol I. ABySS: a parallel assembler for short read sequence data. Genome Res 2009; 19: 1117-1123.
56. Smit AFA & Hubley R. RepeatModeler Open-1.0. Available at: 2008-2010.
57. Smit AFA, Hubley R & Green P. RepeatMasker Open-3.0. Available at: 1996-2010.
58. Margulies M, Egholm M, Altman WE, et al. Genome sequencing in microfabricated high-density picolitre reactors. Nature 2005; 437: 376-380.
59. Sommer D, Delcher A, Salzberg S & Pop M. Minimus: a fast, lightweight genome assembler. BMC Bioinformatics 2007; 8: 64.
60. Parra G, Bradnam K & Korf I. CEGMA: a pipeline to accurately annotate core genes in eukaryotic genomes. Bioinformatics 2007; 23: 1061-1067.
61. Eckert J & Deplazes P. Biological, epidemiological, and clinical aspects of echinococcosis, a zoonosis of increasing concern. Clin Microbiol Rev 2004; 17: 107-135.
62. 2+ channels targets of praziquantel action? Int J Parasitol 2005; 35: 1-9.
63. 2+ channel beta subunit are key to its role in sensitivity to the anti-schistosomal drug praziquantel. Parasitology 2003; 127: 349-356.
64. Jeziorski MC & Greenberg RM. Voltage-gated calcium channel subunits from platyhelminths: potential role in praziquantel action. Int J Parasitol 2006; 36: 625-632.
65. Hegglin D & Deplazes P. Control strategy for Echinococcus multilocularis. Emerg Infect Dis 2008; 14: 1626-1628.
66. Zhang W, Zhang Z, Yimit T, et al. A pilot study for control of hyperendemic cystic hydatid disease in China. PLoS Negl Trop Dis 2009; 3: e534.
67. Bygott JM & Chiodini PL. Praziquantel: neglected drug? Ineffective treatment? Or therapeutic choice in cystic hydatid disease? Acta Trop 2009; 111: 95-101.
68. Hemphill A, Spicher M, Stadelmann B, et al. Innovative chemotherapeutical treatment options for alveolar and cystic echinococcosis. Parasitology 2007; 134: 1657-1670.
69. Pawlowski ZS. Role of chemotherapy of taeniasis in prevention of neurocysticercosis. Parasitol Int 2006; 55(Suppl.): S105-S109.
70. Von Samson-Himmelstjerna G, Blackhall WJ, McCarthy JS & Skuce PJ. Single nucleotide polymorphism (SNP) markers for benzimidazole resistance in veterinary nematodes. Parasitology 2007; 134: 1077-1086.
71. Reuter S, Merkle M, Brehm K, Kern P & Manfras B. Effect of amphotericin B on larval growth of Echinococcus multilocularis. Antimicrob Agents Chemother 2003; 47: 620-625.
72. Brehm K. The role of evolutionarily conserved signalling systems in Echinococcus multilocularis development and host-parasite interaction. Med Microbiol Immunol 2010; 199: 247-259.
73. Noble ME, Endicott JA & Johnson LN. Protein kinase inhibitors: insights into drug design from structure. Science 2004; 303: 1800-1805.
74. Dissous C, Ahier A & Khayath N. Protein tyrosine kinases as new potential targets against human schistosomiasis. Bioessays 2007; 29: 1281-1288.
75. Gelmedin V, Caballero-Gamiz R & Brehm K. Characterization and inhibition of a p38-like mitogen-activated protein kinase (MAPK) from Echinococcus multilocularis: antiparasitic activities of p38 MAPK inhibitors. Biochem Pharmacol 2008; 76: 1068-1081.
76. Spiliotis M, Konrad C, Gelmedin V, et al. Characterisation of EmMPK1, an ERK-like MAP kinase from Echinococcus multilocularis which is activated in response to human epidermal growth factor. Int J Parasitol 2006; 36: 1097-1112.
77. Gelmedin V, Spiliotis M & Brehm K. Molecular characterisation of MEK1/2- and MKK3/6-like mitogen-activated protein kinase kinases (MAPKK) from the fox tapeworm Echinococcus multilocularis. Int J Parasitol 2010; 40: 555-567.
78. Spiliotis M, Tappe D, Bruckner S, Mosch HU & Brehm K. Molecular cloning and characterization of Ras- and Raf-homologues from the fox-tapeworm Echinococcus multilocularis. Mol Biochem Parasitol 2005; 139: 225-237.
79. Konrad C, Kroner A, Spiliotis M, Zavala-Gongora R & Brehm K. Identification and molecular characterisation of a gene encoding a member of the insulin receptor family in Echinococcus multilocularis. Int J Parasitol 2003; 33: 301-312.
80. Spiliotis M, Kroner A & Brehm K. Identification, molecular characterization and expression of the gene encoding the epidermal growth factor receptor orthologue from the fox-tapeworm Echinococcus multilocularis. Gene 2003; 323: 57-65.
81. Zavala-Gongora R, Kroner A, Bernthaler P, Knaus P & Brehm K. A member of the transforming growth factor-b receptor family from Echinococcus multilocularis is activated by human bone morphogenetic protein 2. Mol Biochem Parasitol 2006; 146: 265-271.
82. Russ AP & Lampel S. The druggable genome: an update. Drug Discov Today 2005; 10: 1607-1610.
83. Harris CJ & Stevens AP. Chemogenomics: structuring the drug discovery process to gene families. Drug Discov Today 2006; 11: 880-888.
84. Förster S, Gunthel D, Kiss F & Brehm K. Molecular characterisation of a serum-responsive, DAF-12-like nuclear hormone receptor of the fox-tapeworm Echinococcus multilocularis. J Cell Biochem 2011; 112: 1630-1642.
85. Taft AS, Norante FA & Yoshino TP. The identification of inhibitors of Schistosoma mansoni miracidial transformation by incorporating a medium-throughput small-molecule screen. Exp Parasitol 2010; 125: 84-94.
86. Crowther GJ, Shanmugam D, Carmona SJ, et al. Identification of attractive drug targets in neglected-disease pathogens using an in silico approach. PLoS Negl Trop Dis 2010; 4: e804.
87. Brehm K & Spiliotis M. The influence of host hormones and cytokines on Echinococcus multilocularis signalling and development. Parasite 2008; 15: 286-290.
88. Spiliotis M, Mizukami C, Oku Y, Kiss F, Brehm K & Gottstein B. Echinococcus multilocularis primary cells: improved isolation, small-scale cultivation and RNA interference. Mol Biochem Parasitol 2010; 174: 83-87.
89. Mizukami C, Spiliotis M, Gottstein B, Yagi K, Katakura K & Oku Y. Gene silencing in Echinococcus multilocularis protoscoleces using RNA interference. Parasitol Int 2010; 59: 647-652.
90. Sciutto E, Chavarria A, Fragoso G, Fleury A & Larralde C. The immune response in Taenia solium cysticercosis: protection and injury. Parasite Immunol 2007; 29: 621-636.
91. Vuitton DA & Gottstein B. Echinococcus multilocularis and its intermediate host: a model of parasite-host interplay. J Biomed Biotechnol 2010; 2010: 923193.
92. Reyes JL, Terrazas CA, Alonso-Trujillo J, van Rooijen N, Satoskar AR & Terrazas LI. Early removal of alternatively activated macrophages leads to Taenia crassiceps cysticercosis clearance in vivo. Int J Parasitol 2010; 40: 731-742.
93. Gottstein B & Hemphill A. Echinococcus multilocularis: the parasite-host interplay. Exp Parasitol 2008; 119: 447-452.
94. Siracusano A, Margutti P, Delunardo F, et al. Molecular cross-talk in host-parasite relationships: the intriguing immunomodulatory role of Echinococcus antigen B in cystic echinococcosis. Int J Parasitol 2008; 38: 1371-1376.
95. Chemale G, Ferreira HB, Barrett J, Brophy PM & Zaha A. Echinococcus granulosus antigen B hydrophobic ligand binding properties. Biochim Biophys Acta 2005; 1747: 189-194.
96. Mamuti W, Sako Y, Nakao M, et al. Recent advances in characterization of Echinococcus antigen B. Parasitol Int 2006; 55: S57-S62.
97. Frosch P, Hartmann M, Muhlschlegel F & Frosch M. Sequence heterogeneity of the echinococcal antigen B. Mol Biochem Parasitol 1994; 64: 171-175.
98. Fernandez V, Ferreira HB, Fernandez C, Zaha A & Nieto A. Molecular characterisation of a novel 8-kDa subunit of Echinococcus granulosus antigen B. Mol Biochem Parasitol 1996; 77: 247-250.
99. Chemale G, Haag KL, Ferreira HB & Zaha A. Echinococcus granulosus antigen B is encoded by a gene family. Mol Biochem Parasitol 2001; 116: 233-237.
100. Arend AC, Zaha A, Ayala FJ & Haag KL. The Echinococcus granulosus antigen B shows a high degree of genetic variability. Exp Parasitol 2004; 108: 76-80.
101. Mamuti W, Sako Y, Bart JM, et al. Molecular characterization of a novel gene encoding an 8-kDa-subunit of antigen B from Echinococcus granulosus genotypes 1 and 6. Parasitol Int 2007; 56: 313-316.
102. Haag KL, Alves-Junior L, Zaha A & Ayala FJ. Contingent, non-neutral evolution in a multicellular parasite: natural selection and gene conversion in the Echinococcus granulosus antigen B gene family. Gene 2004; 333: 157-167.
103. Haag KL, Gottstein B, Muller N, Schnorr A & Ayala FJ. Redundancy and recombination in the Echinococcus AgB multigene family: is there any similarity with protozoan contingency genes? Parasitology 2006; 133: 411-419.
104. Zhang W, Li J, Jones MK, et al. The Echinococcus granulosus antigen B gene family comprises at least 10 unique genes in five subclasses which are differentially expressed. PLoS Negl Trop Dis 2010; 4: e784.
105. Fujita N, Jaye DL, Kajita M, Geigerman C, Moreno CS & Wade PA. MTA3, a Mi-2/NuRD complex subunit, regulates an invasive growth pathway in breast cancer. Cell 2003; 113: 207-219.
106. Lightowlers MW. Cestode vaccines: origins, current status and future prospects. Parasitology 2006; 133(Suppl.): S27-S42.
107. Chow C, Gauci CG, Cowman AF & Lightowlers MW. A gene family expressing a host-protective antigen of Echinococcus granulosus. Mol Biochem Parasitol 2001; 118: 83-88.
108. Lightowlers MW, Flisser A, Gauci CG, Heath DD, Jensen O & Rolfe R. Vaccination against cysticercosis and hydatid disease. Parasitol Today 2000; 16: 191-196.
109. Jabbar A, Crawford S, Gauci CG, Walduck AK, Anderson GA & Lightowlers MW. Oncospheral penetration glands and secretory blebs are the sources of Taenia ovis vaccine antigens. Infect Immun 2010; 78: 4363-4373.
110. Jabbar A, Jenkins DJ, Crawford S, Walduck AK, Gauci CG & Lightowlers MW. Oncospheral penetration glands are the source of the EG95 vaccine antigen against cystic hydatid disease. Parasitology 2010; 138: 89-99.
111. Jabbar A, Verastegui M, Lackenby JA, et al. Variation in the cellular localization of host-protective oncospheral antigens in Taenia saginata and Taenia solium. Parasite Immunol 2010; 32: 684-695.
112. Gauci C, Merli M, Muller V, et al. Molecular cloning of a vaccine antigen against infection with the larval stage of Echinococcus multilocularis. Infect Immun 2002; 70: 3969-3972.
113. Kouguchi H, Matsumoto J, Katoh Y, Oku Y, Suzuki T & Yagi K. The vaccination potential of EMY162 antigen against Echinococcus multilocularis infection. Biochem Biophys Res Commun 2007; 363: 915-920.
114. Lightowlers MW. Fact or hypothesis: Taenia crassiceps as a model for Taenia solium, and the S3Pvac vaccine. Parasite Immunol 2010; 32: 701-709.
115. Sciutto E, Rosas G, Hernandez M, et al. Improvement of the synthetic tri-peptide vaccine (S3Pvac) against porcine Taenia solium cysticercosis in search of a more effective, inexpensive and manageable vaccine. Vaccine 2007; 25: 1368-1378.
116. Rassy D, Bobes RJ, Rosas G, et al. Characterization of S3Pvac anti-cysticercosis vaccine components: implications for the development of an anti-cestodiasis vaccine. PLoS ONE 2010; 5: e11287.
117. Wahl SM, Wen J & Moutsopoulos N. TGF-b: a mobile purveyor of immune privilege. Immunol Rev 2006; 213: 213-227.
118. Schramm G, Falcone FH, Gronow A, et al. Molecular characterization of an interleukin-4-inducing factor from Schistosoma mansoni eggs. J Biol Chem 2003; 278: 18384-18392.
119. Everts B, Perona-Wright G, Smits HH, et al. Omega-1, a glycoprotein secreted by Schistosoma mansoni eggs, drives Th2 responses. J Exp Med 2009; 206: 1673-1680.
120. Aumuller E, Schramm G, Gronow A, et al. Echinococcus multilocularis metacestode extract triggers human basophils to release interleukin-4. Parasite Immunol 2004; 26: 387-395.
121. Hartmann S & Lucius R. Modulation of host immune responses by nematode cystatins. Int J Parasitol 2003; 33: 1291-1302.
122. Klotz C, Ziegler T, Figueiredo AS, et al. A helminth immunomodulator exploits host signaling events to regulate cytokine production in macrophages. PLoS Pathog 2011; 7: e1001248.
123. Mejri N & Gottstein B. Intraperitoneal Echinococcus multilocularis infection in C57BL/6 mice affects CD40 and B7 costimulator expression on peritoneal macrophages and impairs peritoneal T cell activation. Parasite Immunol 2006; 28: 373-385.
124. Pires-daSilva A & Sommer RJ. The evoution of signaling pathways in animal development. Nat Rev Genet 2002; 4: 39-49.
125. Saló E. The power of regeneration and the stem-cell kingdom: freshwater planarians (Platyhelminthes). Bioessays 2006; 28: 546-559.
126. Newmark PA & Sánchez Alvarado A. Not your father's planarian: a classic model enters the era of functional genomics. Nat Rev Genet 2002; 32: 210-220.
127. Forsthoefel DJ & Newmark PA. Emerging patterns in planarian regeneration. Curr Opin Genet Dev 2009; 19: 412-420.
128. Olson PD. Hox genes and the parasitic flatworms: new opportunities, challenges and lessons from the free-living. Parasitol Int 2008; 57: 8-17.
129. Blair SS. Segmentation in animals. Curr Biol 2008; 18: R991-R995.
130. Seaver EC. Segmentation: mono- or polyphyletic? Int J Dev Biol 2003; 47: 583-595.
131. Riddiford N & Olson PD. Wnt gene loss in flatworms. Dev Genes Evol 2011; 221: 187-197.
132. Lee PN, Pang K, Matus DQ & Martindale MQ. A WNT of things to come: evolution of Wnt signaling and polarity in cnidarians. Semin Cell Dev Biol 2006; 17: 157-167.
133. Ryan JF & Baxevanis AD. Hox, Wnt, and the evolution of the primary body axis: insights from the early-divergent phyla. Biol Direct 2007; 2: 37.
134. Garcia-Fernandez J. Hox, ParaHox, ProtoHox: facts and guesses. Heredity 2005; 94: 145-152.
135. Brooke NM, Garcia-Fernàndez J & Holland PWH. The ParaHox gene cluster is an evolutionary sister of the Hox gene cluster. Nature 1998; 392: 920-922.
136. Kmita M & Duboule D. Organizing axes in time and space; 25years of colinear tinkering. Science 2004; 301: 331-333.
137. de Rosa R, Grenier JK, Andreeva T, et al. Hox genes in brachiopods and priapulids and protostome evolution. Nature 1999; 399: 772-776.
138. Holland PWH & Hogan BLM. Phylogenetic distribution of Antennapedia-like homoeo boxes. Nature 1986; 321: 251-253.
139. Pierce RJ, Wu W, Hirai H, et al. Evidence for a dispersed Hox gene cluster in the platyhelminth parasite Schistosoma mansoni. Mol Biol Evol 2005; 22: 2491-2503.
140. Badets M & Verneau O. Hox genes from the Polystomatidae (Platyhelminthes, Monogenea). Int J Parasitol 2009; 39: 1517-1523.
141. Koziol U, Lalanne AI & Castillo E. Hox genes in the parasitic platyhelminthes Mesocestoides corti, Echinococcus multilocularis, and Schistosoma mansoni: evidence for a reduced Hox complement. Biochem Genet 2009; 47: 100-116.
142. Nogi T & Watanabe K. Position-specific and non-colinear expression of the planarian posterior (Abdominal-B-like) gene. Dev Growth Differ 2001; 43: 177-184.
143. Badets M, Mitta G, Galinier R & Verneau O. Expression patterns of Abd-A/Lox4 in a monogenean parasite with alternative developmnental paths. Mol Biochem Parasitol 2010; 173: 154-157.
144. Salò E & Baguñà J. Regeneration in planarians and other worms: new findings, new tools, and perspectives. J Exp Zool 2002; 292: 528-539.
145. Seo H-C, Edvardsen RB, Maeland AD, et al. Hox cluster disintegration with persistent anteroposterior order of expression in Oikopleura dioica. Nature 2004; 431: 67-71.
146. Cadigan K & Nusse R. Wnt signaling: a common theme in animal development. Genes Dev 1997; 11: 3286-3305.
147. King N, Westbrook M, Young S, et al. The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans. Nature 2008; 451: 783-788.
148. Richards GS & Degnan BM. The dawn of developmental signaling in the Metazoa. Cold Spring Harb Symp Quant Biol 2009; 74: 81-90.
149. De Robertis EM. Wnt signaling in axial patterning and regeneration: lessons from planaria. Sci Signal 2010; 3: pe21.
150. Li H-F, Wang X-B, Jin Y-P, et al. Wnt4, the first member of the Wnt family identified in Schistosoma japonicum, regulates worm development by the canonical pathway. Parasitol Res 2010; 107: 795-805.
151. Salò E, Tauler J, Jimenez E, et al. Hox and paraHox genes in flatworms: characterization and expression. Am Zool 2001; 41: 652-663.
152. Martin BL & Kimelman D. Wnt signaling and the evolution of embryonic posterior development. Curr Biol 2009; 19: R215-R219.
153. Bizarro C, Bengtson M, Ricachenevsky F, Zaha A, Sogayar M & Ferreira H. Differentially expressed sequences from a cestode parasite reveals conserved developmental genes in platyhelminthes. Mol Biochem Parasitol 2005; 144: 114-118.
154. Pierson L, Mousley A, Devine L, Marks N, Day T & Maule AG. RNA interference in a cestode reveals specific silencing of selected highly expressed gene transcripts. Int J Parasitol 2010; 40: 605-615.
155. Gonzalez-Estevez C, Momose T, Gehring WJ & Salo E. Transgenic planarian lines obtained by electroporation using transposon-derived vectors and an eye-specific GFP marker. Proc Natl Acad Sci U S A 2003; 100: 14046-14051.
156. Kines KJ, Mann VH, Morales ME, et al. Transduction of Schistosoma mansoni by vesicular stomatitis virus glycoprotein-pseudotyped Moloney murine leukemia retrovirus. Exp Parasitol 2006; 112: 209-220.
157. Lukashenko NP, Brzheskij VV & Smirnova ZM. A study of chromosomes of Alveococcus multilocularis (Echinococcus multilocularis) Leukart, 1863. Preliminary report. Med Parazitol (Mosk) 1965; 34: 351-352.
158. Mutafova T & Svilenov D. Comparative karyological studies of Echinococcus granulosus and Echinococcus multilocularis. Khelmintologiya 1985; 20: 60-65 (In Bulgarian).
159. Rausch VR & Rausch RL. The karyotype of Echinococcus multilocularis (Cestoda: Taeniidae). Can J Genet Cytol 1981; 23: 151-154.
160. Sakamoto T, Yamashito J & Obayashi M. Studies on echinococcus. 18. Jap J Vet Res 1967; 15: 75-84.
161. Smyth JD. The chromosome number of Echinococcus multilocularis. J Parasitol 1962; 48: 544.
162. Spakulova M, Orosová M, Mackiewicz JS, Rollinson D & Hay SI. Cytogenetics and chromosomes of tapeworms (Platyhelminthes, Cestoda). Adv Parasitol 2011; 74: 177-230.
163. Hossain MM & Jones AW. The chromosomes of Hymenolepis microstoma (Dujardin 1845). J Parasitol 1963; 49: 305-307.
164. Proffitt MR & Jones AW. Chromosome analysis of Hymenolepis microstoma. Exp Parasitol 1969; 25: 72-84.
165. Hoberg EP, Jones A & Bray RA. Phylogenetic analysis among the families of the Cyclophyllidea (Eucestoda) based on comparative morphology, with new hypotheses for co-evolution in vertebrates. Syst Parasitol 1999; 42: 51-73.