Hostname: page-component-5f56664f6-spj7j Total loading time: 0 Render date: 2025-05-08T04:38:16.681Z Has data issue: false hasContentIssue false
  • English
  • Français

New approaches for understanding mechanisms of drug resistance in schistosomes

Published online by Cambridge University Press:  03 April 2013

ROBERT M. GREENBERG
ROBERT M. GREENBERG*
Affiliation:
Department of Pathobiology, School of Veterinary Medicine, University of Pennsylvania, 3800 Spruce Street, Philadelphia, PA 19104, USA
*
Corresponding author: Department of Pathobiology, School of Veterinary Medicine, University of Pennsylvania, 3800 Spruce Street, Philadelphia, PA 19104, USA. Tel: 215-898-5678. Fax: 215-898-5301. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Summary

Schistosomes are parasitic flatworms that cause schistosomiasis, a neglected tropical disease that affects hundreds of millions worldwide. Treatment and control of schistosomiasis relies almost entirely on the single drug praziquantel (PZQ), making the prospect of emerging drug resistance particularly worrisome. This review will survey reports of PZQ (and other drug) resistance in schistosomes and other platyhelminths, and explore mechanisms by which drug resistance might develop. Newer genomic and post-genomic strategies that offer the promise of better understanding of how drug resistance might arise in these organisms will be discussed. These approaches could also lead to insights into the mode of action of these drugs and potentially provide markers for monitoring the emergence of resistance.

Keywords

schistosomiasisdrug resistancemultidrug transporterspraziquantel
Type
Research Article
Information
Parasitology , Volume 140 , Issue 12: Genetic and genomic approaches to understanding drug resistance in parasites , October 2013 , pp. 1534 - 1546
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Article purchase

Temporarily unavailable

References

REFERENCES

Aller, S. G., Yu, J., Ward, A., Weng, Y., Chittaboina, S., Zhuo, R., Harrell, P. M., Trinh, Y. T., Zhang, Q., Urbatsch, I. L. and Chang, G. (2009). Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding. Science 323, 1718–1722. doi: 10.1126/science.1168750.CrossRefGoogle ScholarPubMed
Alonso, D., Munoz, J., Gascon, J., Valls, M. E. and Corachan, M. (2006). Failure of standard treatment with praziquantel in two returned travelers with Schistosoma haematobium infection. American Journal of Tropical Medicine and Hygiene 74, 342–344.CrossRefGoogle ScholarPubMed
Ambudkar, S. V., Kimchi-Sarfaty, C., Sauna, Z. E. and Gottesman, M. M. (2003). P-glycoprotein: from genomics to mechanism. Oncogene 22, 7468–7485.CrossRefGoogle ScholarPubMed
Andrews, P., Thomas, H., Pohlke, R. and Seubert, J. (1983). Praziquantel. Medicinal Research Reviews 3, 147–200.CrossRefGoogle ScholarPubMed
Aragon, A. D., Imani, R. A., Blackburn, V. R., Cupit, P. M., Melman, S. D., Goronga, T., Webb, T., Loker, E. S. and Cunningham, C. (2009). Towards an understanding of the mechanism of action of praziquantel. Molecular and Biochemical Parasitology 164, 57–65. doi: 10.1016/j.molbiopara.2008.11.007.CrossRefGoogle ScholarPubMed
Ardelli, B. F. and Prichard, R. K. (2013). Inhibition of P-glycoprotein enhances sensitivity of Caenorhabditis elegans to ivermectin. Veterinary Parasitology 191, 264–275. doi: 10.1016/j.vetpar.2012.09.021.CrossRefGoogle ScholarPubMed
Bartley, D. J., McAllister, H., Bartley, Y., Dupuy, J., Menez, C., Alvinerie, M., Jackson, F. and Lespine, A. (2009). P-glycoprotein interfering agents potentiate ivermectin susceptibility in ivermectin sensitive and resistant isolates of Teladorsagia circumcincta and Haemonchus contortus. Parasitology 136, 1081–1088. doi: 10.1017/S0031182009990345.CrossRefGoogle ScholarPubMed
Beckmann, S. and Grevelding, C. G. (2012). Paving the way for transgenic schistosomes. Parasitology 139, 651–668. doi: 10.1017/S0031182011001466.CrossRefGoogle ScholarPubMed
Behbehani, M. and Savioli, L. (1998). Report of the WHO informal consultation on monitoring of drug efficacy in the control of schistosomiasis and intestinal nematodes. WHO/CDS/CPC/SIP/99.1. World Health Organization, Geneva.Google Scholar
Bhardwaj, R., Krautz-Peterson, G., Da'dara, A., Tzipori, S. and Skelly, P. J. (2011). Tegumental phosphodiesterase SmNPP-5 is a virulence factor for schistosomes. Infection and Immunity 79, 4276–4284. doi: 10.1128/IAI.05431-11.CrossRefGoogle ScholarPubMed
Blackmore, C. G., McNaughton, P. A. and Van Veen, H. W. (2001). Multidrug transporters in prokaryotic and eukaryotic cells: physiological functions and transport mechanisms. Molecular Membrane Biology 18, 97–103.CrossRefGoogle ScholarPubMed
Blanton, R. E., Blank, W. A., Costa, J. M., Carmo, T. M., Reis, E. A., Silva, L. K., Barbosa, L. M., Test, M. R. and Reis, M. G. (2011). Schistosoma mansoni population structure and persistence after praziquantel treatment in two villages of Bahia, Brazil. International Journal for Parasitology 41, 1093–1099. doi: 10.1016/j.ijpara.2011.06.002.CrossRefGoogle ScholarPubMed
Boray, J. C., Crowfoot, P. D., Strong, M. B., Allison, J. R., Schellembaum, M., von Orelli, M. and Sarasin, G. (1983). Treatment of immature and mature Fasciola hepatica infections in sheep with triclabendazole. Veterinary Record 113, 315–317.CrossRefGoogle ScholarPubMed
Borst, P. and Elferink, R. O. (2002). Mammalian ABC transporters in health and disease. Annual Review of Biochemistry 71, 537–592.CrossRefGoogle ScholarPubMed
Bosch, I. B., Wang, Z. X., Tao, L. F. and Shoemaker, C. B. (1994). Two Schistosoma mansoni cDNAs encoding ATP-binding cassette (ABC) family proteins. Molecular and Biochemical Parasitology 65, 351–356.CrossRefGoogle ScholarPubMed
Botros, S., Sayed, H., Amer, N., El-Ghannam, M., Bennett, J. L. and Day, T. A. (2005). Current status of sensitivity to praziquantel in a focus of potential drug resistance in Egypt. International Journal for Parasitology 35, 787–791.CrossRefGoogle Scholar
Brehm, K. (2010). Echinococcus multilocularis as an experimental model in stem cell research and molecular host-parasite interaction. Parasitology 137, 537–555. doi: 10.1017/S0031182009991727.CrossRefGoogle ScholarPubMed
Brindley, P. J. (1994). Relationships between chemotherapy and immunity in schistosomiasis. Advances in Parasitology 34, 133–161.CrossRefGoogle ScholarPubMed
Brindley, P. J. and Sher, A. (1987). The chemotherapeutic effect of praziquantel against Schistosoma mansoni is dependent on host antibody response. Journal of Immunology 139, 215–220.CrossRefGoogle ScholarPubMed
Britton, C., Samarasinghe, B. and Knox, D. P. (2012). Ups and downs of RNA interference in parasitic nematodes. Experimental Parasitology 132, 56–61. doi: 10.1016/j.exppara.2011.08.002.CrossRefGoogle ScholarPubMed
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. doi: 10.1371/journal.pone.0004413.CrossRefGoogle ScholarPubMed
Cantacessi, C., Campbell, B. E., Jex, A. R., Young, N. D., Hall, R. S., Ranganathan, S. and Gasser, R. B. (2012). Bioinformatics meets parasitology. Parasite Immunology 34, 265–275. doi: 10.1111/j.1365-3024.2011.01304.x.CrossRefGoogle ScholarPubMed
Cheng, G., Fu, Z., Lin, J., Shi, Y., Zhou, Y., Jin, Y. and Cai, Y. (2009). In vitro and in vivo evaluation of small interference RNA-mediated gynaecophoral canal protein silencing in Schistosoma japonicum. Journal of Gene Medicine 11, 412–421. doi: 10.1002/jgm.1314.Google Scholar
Cioli, D. (2000). Praziquantel: is there real resistance and are there alternatives? Current Opinion in Infectious Diseases 13, 659–663.CrossRefGoogle ScholarPubMed
Cioli, D. and Pica-Mattoccia, L. (1984). Genetic analysis of hycanthone resistance in Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 33, 80–88.CrossRefGoogle ScholarPubMed
Cioli, D. and Pica-Mattoccia, L. (2003). Praziquantel. Parasitology Research 90(Supp. 1), S3–S9.CrossRefGoogle ScholarPubMed
Cioli, D. and Pica-Mattoccia, L. (2005). Current and future antischistosomal drugs. In Schistosomiasis (ed. Secor, W. E. and Colley, D. G.), pp. 191–206. Springer, New York, NY.CrossRefGoogle Scholar
Cioli, D., Pica-Mattoccia, L. and Moroni, R. (1992). Schistosoma mansoni: hycanthone/oxamniquine resistance is controlled by a single autosomal recessive gene. Experimental Parasitology 75, 425–432.CrossRefGoogle ScholarPubMed
Cioli, D., Pica-Mattoccia, L. and Archer, S. (1993). Drug resistance in schistosomes. Parasitology Today 9, 162–166.CrossRefGoogle ScholarPubMed
Cioli, D., Pica-Mattoccia, L. and Archer, S. (1995). Antischistosomal drugs: past, present…and future? Pharmacology and Therapeutics 68, 35–85.CrossRefGoogle Scholar
Coles, G. C. and Kinoti, G. K. (1997). Defining resistance in Schistosoma. Parasitology Today 13, 157–158.CrossRefGoogle ScholarPubMed
Collins, J. J., King, R. S., Cogswell, A., Williams, D. L. and Newmark, P. A. (2011). An atlas for Schistosoma mansoni organs and life-cycle stages using cell type-specific markers and confocal microscopy. PLoS Neglected Tropical Diseases 8, e1009. doi: 10.1371/journal.pntd.0001009.CrossRefGoogle Scholar
Collins, J. J., Wang, B., Lambrus, B. G., Tharp, M. E., Iver, H. and Newmark, P. A. (2013). Adult somatic stem cells in the human parasite Schistosoma Mansoni. Nature 494, 476–479. doi: 10.1038/nature 11924.CrossRefGoogle ScholarPubMed
Cooper, L. A., Lewis, F. A. and File-Emperador, S. (1989). Re-establishing a life cycle of Schistosoma mansoni from cryopreserved larvae. Journal of Parasitology 75, 353–356.CrossRefGoogle ScholarPubMed
Couto, F. F., Coelho, P. M., Araujo, N., Kusel, J. R., Katz, N., Jannotti-Passos, L. K. and Mattos, A. C. (2011). Schistosoma mansoni: a method for inducing resistance to praziquantel using infected Biomphalaria glabrata snails. Memorias do Instituto Oswaldo Cruz 106, 153–157.CrossRefGoogle ScholarPubMed
Couto, F. F., Coelho, P. M., Araujo, N., Kusel, J. R., Katz, N. and Mattos, A. C. (2010). Use of fluorescent probes as a useful tool to identify resistant Schistosoma mansoni isolates to praziquantel. Parasitology 137, 1791–1797. doi: 10.1017/S003118201000065X.CrossRefGoogle ScholarPubMed
Criscione, C. D., Valentim, C. L. L., Hirai, H., LoVerde, P. T. and Anderson, T. J. C. (2009). Genomic linkage map of the human blood fluke Schistosoma mansoni. Genome Biology 10, R71. doi: 10.1186/gb-2009-10-6-r71.CrossRefGoogle ScholarPubMed
Crisford, A., Murray, C., O'Connor, V., Edwards, R. J., Kruger, N., Welz, C., von Samson-Himmelstjerna, G., Harder, A., Walker, R. J. and Holden-Dye, L. (2011). Selective toxicity of the anthelmintic emodepside revealed by heterologous expression of human KCNMA1 in Caenorhabditis elegans. Molecular Pharmacology 79, 1031–1043. doi: 10.1124/mol.111.071043.CrossRefGoogle ScholarPubMed
Cvilink, V., Lamka, J. and Skalova, L. (2009). Xenobiotic metabolizing enzymes and metabolism of anthelminthics in helminths. Drug Metabolism Reviews 41, 8–26. doi: 10.1080/03602530802602880.CrossRefGoogle ScholarPubMed
Danso-Appiah, A. and De Vlas, S. J. (2002). Interpreting low praziquantel cure rates of Schistosoma mansoni infections in Senegal. Trends in Parasitology 18, 125–129.CrossRefGoogle ScholarPubMed
Dassa, E. and Bouige, P. (2001). The ABC of ABCs: a phylogenetic and functional classification of ABC systems in living organisms. Research in Microbiology 152, 211–229.CrossRefGoogle ScholarPubMed
Day, T. A. and Botros, S. (2006). Drug resistance in schistosomes. In Parasitic Flatworms: Molecular Biology, Biochemistry, Immunology and Physiology (ed. Maule, A. and Marks, N. J.), pp. 256–268. CAB International, Oxfordshire, UK.CrossRefGoogle Scholar
Dean, M. and Annilo, T. (2005). Evolution of the ATP-binding cassette (ABC) transporter superfamily in vertebrates. Annual Review of Genomics and Human Genetics 6, 123–142.CrossRefGoogle ScholarPubMed
Dean, M., Rzhetsky, A. and Allikmets, R. (2001). The human ATP-binding cassette (ABC) transporter superfamily. Genome Research 11, 1156–1166. doi: 10.1101/gr.184901.CrossRefGoogle ScholarPubMed
Dent, J. A., McHardy, M. S., Vassilatis, D. M. and Avery, L. (2000). The genetics of ivermectin resistance in Caenorhabditis elegans. Proceedings of the National Academy of Sciences, USA 97, 2674–2679.CrossRefGoogle ScholarPubMed
Devaney, E., Winter, A. D. and Britton, C. (2010). microRNAs: a role in drug resistance in parasitic nematodes? Trends in Parasitology 26, 428–433. doi: 10.1016/j.pt.2010.05.003.CrossRefGoogle ScholarPubMed
Doenhoff, M. J., Cioli, D. and Utzinger, J. (2008). Praziquantel: mechanisms of action, resistance and new derivatives for schistosomiasis. Current Opinion in Infectious Diseases 21, 659–667. doi: 10.1097/QCO.0b013e328318978f.CrossRefGoogle ScholarPubMed
Doenhoff, M. J., Coles, G. C., Pica-Mattoccia, L. and Wheatcroft-Francklow, K. (2009 a). Chemotherapy and drug resistance in schistosomiasis, fascioliasis and tapeworm infections. In Antimicrobial Drug Resistance, Vol. 1: Mechanisms of Drug Resistance, Vol. 1 (ed. Mayers, D. L.), pp. 629–646. Humana Press, Totowa, NJ.CrossRefGoogle Scholar
Doenhoff, M. J., Hagan, P., Cioli, D., Southgate, V., Pica-Mattoccia, L., Botros, S., Coles, G., Tchuem Tchuente, L. A., Mbaye, A. and Engels, D. (2009 b). Praziquantel: its use in control of schistosomiasis in sub-Saharan Africa and current research needs. Parasitology 136, 1825–1835. doi: 10.1017/S0031182009000493.CrossRefGoogle ScholarPubMed
Doenhoff, M. J. and Pica-Mattoccia, L. (2006). Praziquantel for the treatment of schistosomiasis: its use for control in areas with endemic disease and prospects for drug resistance. Expert Review of Anti-infective Therapy 4, 199–210.CrossRefGoogle ScholarPubMed
Doenhoff, M. J., Sabah, A. A., Fletcher, C., Webbe, G. and Bain, J. (1987). Evidence for an immune-dependent action of praziquantel on Schistosoma mansoni in mice. Transactions of the Royal Society of Tropical Medicine and Hygiene 81, 947–951.CrossRefGoogle ScholarPubMed
Duvoisin, R., Ayuk, M. A., Rinaldi, G., Suttiprapa, S., Mann, V. H., Lee, C. M., Harris, N. and Brindley, P. J. (2012). Human U6 promoter drives stronger shRNA activity than its schistosome orthologue in Schistosoma mansoni and human fibrosarcoma cells. Transgenic Research 21, 511–521. doi: 10.1007/s11248-011-9548-0.CrossRefGoogle ScholarPubMed
Eisenhoffer, G. T., Kang, H. and Sanchez Alvarado, A. (2008). Molecular analysis of stem cells and their descendants during cell turnover and regeneration in the planarian Schmidtea mediterranea. Cell Stem Cell 3, 327–339. doi: 10.1016/j.stem.2008.07.002.CrossRefGoogle ScholarPubMed
Fairweather, I. (2011). Liver fluke isolates: a question of provenance. Veterinary Parasitology 176, 1–8. doi: 10.1016/j.vetpar.2010.12.011.CrossRefGoogle ScholarPubMed
Fallon, P. G. (1995). Short report: diminished susceptibility to praziquantel in a senegal isolate of Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 53, 61–62.CrossRefGoogle Scholar
Fallon, P. G. (1998). Schistosome resistance to praziquantel. Drug Resistance Updates 1, 236–241.CrossRefGoogle ScholarPubMed
Fallon, P. G. and Doenhoff, M. J. (1994). Drug-resistant schistosomiasis: resistance to praziquantel and oxamniquine induced in Schistosoma mansoni in mice is drug specific. American Journal of Tropical Medicine and Hygiene 51, 83–88.CrossRefGoogle ScholarPubMed
Fallon, P. G., Mubarak, J. S., Fookes, R. E., Niang, M., Butterworth, A. E., Sturrock, R. F. and Doenhoff, M. J. (1997). Schistosoma mansoni: maturation rate and drug susceptibility of different geographic isolates. Experimental Parasitology 86, 29–36.CrossRefGoogle ScholarPubMed
Fallon, P. G., Tao, L. F., Ismail, M. M. and Bennett, J. L. (1996). Schistosome resistance to praziquantel: Fact or artifact? Parasitology Today 12, 316–320.CrossRefGoogle ScholarPubMed
Gimenez-Bonafe, P., Guillen Canovas, A., Ambrosio, S., Tortosa, A. and Perez-Tomas, R. (2008). Drugs modulating MDR. (ed. Colabufo, N. A.), pp. 63–99. Research Signpost, Kerala, India.Google Scholar
Gonnert, R. and Andrews, P. (1977). Praziquantel, a new broad-spectrum antischistosomal agent. Zeitschrift für Parasitenkunde 52, 129–150.CrossRefGoogle Scholar
Greenberg, R. M. (2005). Are Ca2+ channels targets of praziquantel action? International Journal for Parasitology 35, 1–9.CrossRefGoogle ScholarPubMed
Gryseels, B., Mbaye, A., De Vlas, S. J., Stelma, F. F., Guisse, F., Van Lieshout, L., Faye, D., Diop, M., Ly, A., Tchuem-Tchuente, L. A., Engels, D. and Polman, K. (2001). Are poor responses to praziquantel for the treatment of Schistosoma mansoni infections in Senegal due to resistance? An overview of the evidence. Tropical Medicine and International Health 6, 864–873.CrossRefGoogle ScholarPubMed
Gryseels, B., Stelma, F. F., Talla, I., van Dam, G. J., Polman, K., Sow, S., Diaw, M., Sturrock, R. F., Doehring-Schwerdtfeger, E., Kardorff, R., Decam, C., Niang, M. and Deelder, A. M. (1994). Epidemiology, immunology and chemotherapy of Schistosoma mansoni infections in a recently exposed community in Senegal. Tropical and Geographical Medicine 46, 209–219.Google Scholar
Hayeshi, R., Masimirembwa, C., Mukanganyama, S. and Ungell, A. L. (2006). The potential inhibitory effect of antiparasitic drugs and natural products on P-glycoprotein mediated efflux. European Journal of Pharmaceutical Sciences 29, 70–81.CrossRefGoogle ScholarPubMed
Herwaldt, B. L., Tao, L. F., van Pelt, W., Tsang, V. C. and Bruce, J. I. (1995). Persistence of Schistosoma haematobium infection despite multiple courses of therapy with praziquantel. Clinical Infectious Diseases 20, 309–315.CrossRefGoogle ScholarPubMed
Higgins, C. F. (2007). Multiple molecular mechanisms for multidrug resistance transporters. Nature 446, 749–757.CrossRefGoogle ScholarPubMed
Hines-Kay, J., Cupit, P. M., Sanchez, M. C., Rosenberg, G. H., Hanelt, B. and Cunningham, C. (2012). Transcriptional analysis of Schistosoma mansoni treated with praziquantel in vitro. Molecular and Biochemical Parasitology 186, 87–94. doi: 10.1016/j.molbiopara.2012.09.006.CrossRefGoogle ScholarPubMed
Hotez, P. J. and Fenwick, A. (2009). Schistosomiasis in Africa: an emerging tragedy in our new global health decade. PLoS Neglected Tropical Diseases 3, e485. doi: 10.1371/journal.pntd.0000485.CrossRefGoogle ScholarPubMed
Ismail, M., Botros, S., Metwally, A., William, S., Farghally, A., Tao, L. F., Day, T. A. and Bennett, J. L. (1999). Resistance to praziquantel: direct evidence from Schistosoma mansoni isolated from Egyptian villagers. American Journal of Tropical Medicine and Hygiene 60, 932–935.CrossRefGoogle ScholarPubMed
Ismail, M., Metwally, A., Farghaly, A., Bruce, J., Tao, L. F. and Bennett, J. L. (1996). Characterization of isolates of Schistosoma mansoni from Egyptian villagers that tolerate high doses of praziquantel. American Journal of Tropical Medicine and Hygiene 55, 214–218.CrossRefGoogle ScholarPubMed
James, C. E., Hudson, A. L. and Davey, M. W. (2009). Drug resistance mechanisms in helminths: is it survival of the fittest? Trends in Parasitology 25, 328–335. doi: 10.1016/j.pt.2009.04.004.CrossRefGoogle ScholarPubMed
Jin, M. S., Oldham, M. L., Zhang, Q. and Chen, J. (2012). Crystal structure of the multidrug transporter P-glycoprotein from Caenorhabditis elegans. Nature 490, 566–569. doi: 10.1038/nature11448.CrossRefGoogle ScholarPubMed
Jones, P. M. and George, A. M. (2005). Multidrug resistance in parasites: ABC transporters, P-glycoproteins and molecular modelling. International Journal for Parasitology 35, 555–566.CrossRefGoogle ScholarPubMed
Kartner, N., Riordan, J. R. and Ling, V. (1983). Cell surface P-glycoprotein associated with multidrug resistance in mammalian cell lines. Science 221, 1285–1288.CrossRefGoogle ScholarPubMed
Kasinathan, R. S., Goronga, T., Messerli, S. M., Webb, T. R. and Greenberg, R. M. (2010 a). Modulation of a Schistosoma mansoni multidrug transporter by the antischistosomal drug praziquantel. FASEB Journal 24, 128–135. doi: 10.1096/fj.09-137091.CrossRefGoogle ScholarPubMed
Kasinathan, R. S. and Greenberg, R. M. (2012). Pharmacology and potential physiological significance of schistosome multidrug resistance transporters. Experimental Parasitology 132, 2–6. doi: 10.1016/j.exppara.2011.03.004.CrossRefGoogle ScholarPubMed
Kasinathan, R. S., Morgan, W. M. and Greenberg, R. M. (2010 b). Schistosoma mansoni express higher levels of multidrug resistance-associated protein 1 (SmMRP1) in juvenile worms and in response to praziquantel. Molecular and Biochemical Parasitology 173, 25–31. doi: 10.1016/j.molbiopara.2010.05.003.CrossRefGoogle ScholarPubMed
Kasinathan, R. S., Morgan, W. M. and Greenberg, R. M. (2011). Genetic knockdown and pharmacological inhibition of parasite multidrug resistance transporters disrupts egg production in Schistosoma mansoni. PLoS Neglected Tropical Diseases 5, e1425. doi: 10.1371/journal.pntd.0001425.CrossRefGoogle ScholarPubMed
Keiser, J. and Utzinger, J. (2012). Antimalarials in the treatment of schistosomiasis. Current Pharmaceutical Design 18, 3531–3538.Google ScholarPubMed
Kerboeuf, D., Blackhall, W., Kaminsky, R. and von Samson-Himmelstjerna, G. (2003). P-glycoprotein in helminths: function and perspectives for anthelmintic treatment and reversal of resistance. International Journal of Antimicrobial Agents 22, 332–346.CrossRefGoogle ScholarPubMed
King, C. H. (2010). Parasites and poverty: the case of schistosomiasis. Acta Tropica 113, 95–104. doi: 10.1016/j.actatropica.2009.11.012.CrossRefGoogle ScholarPubMed
Kongs, A., Marks, G., Verle, P. and Van der Stuyft, P. (2008). The unreliability of the Kato-Katz technique limits its usefulness for evaluating S. mansoni infections. Tropical Medicine and International Health 6, 163–169. doi: 10.1046/j.1365-3156.2001.00687.x.CrossRefGoogle Scholar
Krautz-Peterson, G., Bhardwaj, R., Faghiri, Z., Tararam, C. A. and Skelly, P. J. (2010). RNA interference in schistosomes: machinery and methodology. Parasitology 137, 485–495. doi: 10.1017/S0031182009991168.CrossRefGoogle ScholarPubMed
Kumkate, S., Chunchob, S. and Janvilisri, T. (2008). Expression of ATP-binding cassette multidrug transporters in the giant liver fluke Fasciola gigantica and their possible involvement in the transport of bile salts and anthelmintics. Molecular and Cellular Biochemistry 317, 77–84. doi: 10.1007/s11010-008-9833-2.CrossRefGoogle ScholarPubMed
Kusel, J. R., Oliveira, F. A., Todd, M., Ronketti, F., Lima, S. F., Mattos, A. C., Reis, K. T., Coelho, P. M., Thornhill, J. A. and Ribeiro, F. (2006). The effects of drugs, ions, and poly-l-lysine on the excretory system of Schistosoma mansoni. Memorias do Instituto Oswaldo Cruz 101, 293–298.CrossRefGoogle ScholarPubMed
Kwa, M. S. G., Veenstra, J. G., Dijk, M. V. and Roos, M. H. (1995). β-tubulin genes from the parasitic nematode Haemonchus contortus modulate drug resistance in Caenorhabditis elegans. Journal of Molecular Biology 246, 500–510.CrossRefGoogle ScholarPubMed
Leprohon, P., Legare, D. and Ouellette, M. (2011). ABC transporters involved in drug resistance in human parasites. Essays in Biochemistry 50, 121–144. doi: 10.1042/bse0500121.Google ScholarPubMed
Lespine, A., Menez, C., Bourguinat, C. and Prichard, R. K. (2012). P-glycoproteins and other multidrug resistance transporters in the pharmacology of anthelmintics: prospects for reversing transport-dependent anthelmintic resistance. International Journal for Parasitology: Drugs and Drug Resistance 2, 58–75. doi: 10.1016/j.ijpddr.2011.10.001.Google ScholarPubMed
Liang, Y. S., Coles, G. C., Dai, J. R., Zhu, Y. C. and Doenhoff, M. J. (2001). Biological characteristics of praziquantel-resistant and -susceptible isolates of Schistosoma mansoni. Annals of Tropical Medicine and Parasitology 95, 715–723.CrossRefGoogle ScholarPubMed
Liang, Y. S., Dai, J. R., Zhu, Y. C., Coles, G. C. and Doenhoff, M. J. (2003). Genetic analysis of praziquantel resistance in Schistosoma mansoni. Southeast Asian Journal of Tropical Medicine and Public Health 34, 274–280.Google ScholarPubMed
Liang, Y. S., Li, H. J., Dai, J. R., Wang, W., Qu, G. L., Tao, Y. H., Xing, Y. T., Li, Y. Z., Qian, K. and Wei, J. Y. (2011). Studies on resistance of Schistosoma to praziquantel XIII: resistance of Schistosoma japonicum to praziquantel is experimentally induced in laboratory. Chinese Journal of Schistosomiasis Control 23, 605–610.Google ScholarPubMed
Lin, D. D., Liu, J. X., Liu, Y. M., Hu, F., Zhang, Y. Y., Xu, J. M., Li, J. Y., Ji, M. J., Bergquist, R., Wu, G. L. and Wu, H. W. (2008). Routine Kato-Katz technique underestimates the prevalence of Schistosoma japonicum: a case study in an endemic area of the People's Republic of China. Parasitology International 57, 281–286. doi: 10.1016/j.parint.2008.04.005.CrossRefGoogle Scholar
Mattos, A. C., Pereira, G. C., Jannotti-Passos, L. K., Kusel, J. R. and Coelho, P. M. (2007). Evaluation of the effect of oxamniquine, praziquantel and a combination of both drugs on the intramolluscan phase of Schistosoma mansoni. Acta Tropica 102, 84–91.CrossRefGoogle Scholar
Mealey, K. L., Bentjen, S. A., Gay, J. M. and Cantor, G. H. (2001). Ivermectin sensitivity in collies is associated with a deletion mutation of the mdr1 gene. Pharmacogenetics 11, 727–733.CrossRefGoogle ScholarPubMed
Melman, S. D., Steinauer, M. L., Cunningham, C., Kubatko, L. S., Mwangi, I. N., Wynn, N. B., Mutuku, M. W., Karanja, D. M., Colley, D. G., Black, C. L., Secor, W. E., Mkoji, G. M. and Loker, E. S. (2009). Reduced susceptibility to praziquantel among naturally occurring Kenyan isolates of Schistosoma mansoni. PLoS Neglected Tropical Diseases 3, e504. doi: 10.1371/journal.pntd.0000504.CrossRefGoogle ScholarPubMed
Messerli, S. M., Kasinathan, R. S., Morgan, W., Spranger, S. and Greenberg, R. M. (2009). Schistosoma mansoni P-glycoprotein levels increase in response to praziquantel exposure and correlate with reduced praziquantel susceptibility. Molecular and Biochemical Parasitology 167, 54–59. doi: 10.1016/j.molbiopara.2009.04.007.CrossRefGoogle ScholarPubMed
Mizutani, T., Masuda, M., Nakai, E., Furumiya, K., Togawa, H., Nakamura, Y., Kawai, Y., Nakahira, K., Shinkai, S. and Takahashi, K. (2008). Genuine functions of P-glycoprotein (ABCB1). Current Drug Metabolism 9, 167–174.CrossRefGoogle ScholarPubMed
Molento, M. B. and Prichard, R. K. (1999). Effects of the multidrug-resistance-reversing agents verapamil and CL 347,099 on the efficacy of ivermectin or moxidectin against unselected and drug-selected strains of Haemonchus contortus in jirds (Meriones unguiculatus). Parasitology Research 85, 1007–1011.CrossRefGoogle ScholarPubMed
Moll, L., Gaasenbeek, C. P., Vellema, P. and Borgsteede, F. H. (2000). Resistance of Fasciola hepatica against triclabendazole in cattle and sheep in The Netherlands. Veterinary Parasitology 91, 153–158.CrossRefGoogle ScholarPubMed
Mourao, M. M., Dinguirard, N., Franco, G. R. and Yoshino, T. P. (2009). Phenotypic screen of early-developing larvae of the blood fluke, Schistosoma mansoni, using RNA interference. PLoS Neglected Tropical Diseases 3, e502. doi: 10.1371/journal.pntd.0000502.CrossRefGoogle ScholarPubMed
Mutapi, F., Rujeni, N., Bourke, C., Mitchell, K., Appleby, L., Nausch, N., Midzi, N. and Mduluza, T. (2011). Schistosoma haematobium treatment in 1–5 year old children: safety and efficacy of the antihelminthic drug praziquantel. PLoS Neglected Tropical Diseases 5, e1143. doi: 10.1371/journal.pntd.0001143.CrossRefGoogle ScholarPubMed
Nogi, T., Zhang, D., Chan, J. D. and Marchant, J. S. (2009). A novel biological activity of praziquantel requiring voltage-operated Ca2+ channel β subunits: subversion of flatworm regenerative polarity. PLoS Neglected Tropical Diseases 3, e464. doi: 10.1371/journal.pntd.0000464.CrossRefGoogle ScholarPubMed
Novozhilova, E., Kimber, M. J., Qian, H., McVeigh, P., Robertson, A. P., Zamanian, M., Maule, A. G. and Day, T. A. (2010). FMRFamide-like peptides (FLPs) enhance voltage-gated calcium currents to elicit muscle contraction in the human parasite Schistosoma mansoni. PLoS Neglected Tropical Diseases 4, e790. doi: 10.1371/journal.pntd.0000790.CrossRefGoogle ScholarPubMed
Oliveira, F. A., Kusel, J. R., Ribeiro, F. and Coelho, P. M. (2006). Responses of the surface membrane and excretory system of Schistosoma mansoni to damage and to treatment with praziquantel and other biomolecules. Parasitology 132, 321–330.CrossRefGoogle ScholarPubMed
Paulsen, I. T. (2003). Multidrug efflux pumps and resistance: regulation and evolution. Current Opinion in Microbiology 6, 446–451.CrossRefGoogle ScholarPubMed
Pereira, C., Fallon, P. G., Cornette, J., Capron, A., Doenhoff, M. J. and Pierce, R. J. (1998). Alterations in cytochrome-c oxidase expression between praziquantel-resistant and susceptible strains of Schistosoma mansoni. Parasitology 117(Pt 1), 63–73.CrossRefGoogle ScholarPubMed
Pereira, T. C., Pascoal, V. D., Marchesini, R. B., Maia, I. G., Magalhaes, L. A., Zanotti-Magalhaes, E. M. and Lopes-Cendes, I. (2008). Schistosoma mansoni: evaluation of an RNAi-based treatment targeting HGPRTase gene. Experimental Parasitology 118, 619–623. doi: 10.1016/j.exppara.2007.11.017.CrossRefGoogle ScholarPubMed
Pica-Mattoccia, L., Archer, S. and Cioli, D. (1992). Hycanthone resistance in schistosomes correlates with the lack of an enzymatic activity which produces the covalent binding of hycanthone to parasite macromolecules. Molecular and Biochemical Parasitology 55, 167–175.CrossRefGoogle ScholarPubMed
Pica-Mattoccia, L. and Cioli, D. (2004). Sex- and stage-related sensitivity of Schistosoma mansoni to in vivo and in vitro praziquantel treatment. International Journal for Parasitology 34, 527–533.CrossRefGoogle ScholarPubMed
Pica-Mattoccia, L., Doenhoff, M. J., Valle, C., Basso, A., Troiani, A. R., Liberti, P., Festucci, A., Guidi, A. and Cioli, D. (2009). Genetic analysis of decreased praziquantel sensitivity in a laboratory strain of Schistosoma mansoni. Acta Tropica 111, 82–85. doi: 10.1016/j.actatropica.2009.01.012.CrossRefGoogle Scholar
Pica-Mattoccia, L., Orsini, T., Basso, A., Festucci, A., Liberti, P., Guidi, A., Marcatto-Maggi, A. L., Nobre-Santana, S., Troiani, A. R., Cioli, D. and Valle, C. (2008). Schistosoma mansoni: lack of correlation between praziquantel-induced intra-worm calcium influx and parasite death. Experimental Parasitology 119, 332–335. doi: 10.1016/j.exppara.2008.03.012.CrossRefGoogle ScholarPubMed
Pica-Mattoccia, L., Novi, A. and Cioli, D. (1997). Enzymatic basis for the lack of oxamniquine activity in Schistosoma haematobium infections. Parasitology Research 83, 687–689.CrossRefGoogle ScholarPubMed
Pica-Mattoccia, L., Valle, C., Basso, A., Troiani, A. R., Vigorosi, F., Liberti, P., Festucci, A. and Cioli, D. (2007). Cytochalasin D abolishes the schistosomicidal activity of praziquantel. Experimental Parasitology 115, 344–351.CrossRefGoogle ScholarPubMed
Pommier, Y., Pourquier, P., Urasaki, Y., Wu, J. and Laco, G. S. (1999). Topoisomerase I inhibitors: selectivity and cellular resistance. Drug Resistance Updates 2, 307–318.CrossRefGoogle ScholarPubMed
Pommier, Y., Sordet, O., Antony, S., Hayward, R. L. and Kohn, K. W. (2004). Apoptosis defects and chemotherapy resistance: molecular interaction maps and networks. Oncogene 23, 2934–2959.CrossRefGoogle ScholarPubMed
Prichard, R. K., Hall, C. A., Kelly, J. D., Martin, I. C. and Donald, A. D. (1980). The problem of anthelmintic resistance in nematodes. Australian Veterinary Journal 56, 239–251.CrossRefGoogle ScholarPubMed
Protasio, A. V., Tsai, I. J., Babbage, A., Nichol, S., Hunt, M., Aslett, M. A., De Silva, N., Velarde, G. S., Anderson, T. J., 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, e1455. doi: 10.1371/journal.pntd.0001455.CrossRefGoogle ScholarPubMed
Quack, T., Wippersteg, V. and Grevelding, C. G. (2010). Cell cultures for schistosomes – chances of success or wishful thinking? International Journal for Parasitology 40, 991–1002. doi: 10.1016/j.ijpara.2010.04.013.CrossRefGoogle ScholarPubMed
Redman, C. A., Robertson, A., Fallon, P. G., Modha, J., Kusel, J. R., Doenhoff, M. J. and Martin, R. J. (1996). Praziquantel: an urgent and exciting challenge. Parasitology Today 12, 14–20.CrossRefGoogle ScholarPubMed
Rinaldi, G., Eckert, S. E., Tsai, I. J., Suttiprapa, S., Kines, K. J., Tort, J. F., Mann, V. H., Turner, D. J., Berriman, M. and Brindley, P. J. (2012 a). Germline transgenesis and insertional mutagenesis in Schistosoma mansoni mediated by murine leukemia virus. PloS Pathogens 8, e1002820. doi: 10.1371/journal.ppat.1002820.CrossRefGoogle ScholarPubMed
Rinaldi, G., Suttiprapa, S., Tort, J. F., Folley, A. E., Skinner, D. E. and Brindley, P. J. (2012 b). An antibiotic selection marker for schistosome transgenesis. International Journal for Parasitology 42, 123–130. doi: 10.1016/j.ijpara.2011.11.005.CrossRefGoogle ScholarPubMed
Sabah, A. A., Fletcher, C., Webbe, G. and Doenhoff, M. J. (1986). Schistosoma mansoni: chemotherapy of infections of different ages. Experimental Parasitology 61, 294–303.CrossRefGoogle ScholarPubMed
Sabra, A. N. and Botros, S. S. (2008). Response of Schistosoma mansoni isolates having different drug sensitivity to praziquantel over several life cycle passages with and without therapeutic pressure. Journal of Parasitology 94, 537–541. doi: 10.1645/GE-1297.1.CrossRefGoogle ScholarPubMed
Saier, M. H. and Paulsen, I. T. (2001). Phylogeny of multidrug transporters. Seminars in Cell and Developmental Biology 12, 205–213.CrossRefGoogle ScholarPubMed
Sato, H., Kusel, J. R. and Thornhill, J. (2002). Functional visualization of the excretory system of adult Schistosoma mansoni by the fluorescent marker resorufin. Parasitology 125, 527–535.CrossRefGoogle ScholarPubMed
Sato, H., Kusel, J. R. and Thornhill, J. (2004). Excretion of fluorescent substrates of mammalian multidrug resistance-associated protein (MRP) in the Schistosoma mansoni excretory system. Parasitology 128, 43–52.CrossRefGoogle ScholarPubMed
Sayed, A. A., Simeonov, A., Thomas, C. J., Inglese, J., Austin, C. P. and Williams, D. L. (2008). Identification of oxadiazoles as new drug leads for the control of schistosomiasis. Nature Medicine 14, 407–412. doi: 10.1038/nm1737.CrossRefGoogle ScholarPubMed
Schinkel, A. H., Smit, J. J., van Tellingen, O., Beijnen, J. H., Wagenaar, E., van Deemter, L., Mol, C. A., van der Valk, M. A., Robanus-Maandag, E. C., te Riele, H. P., Berns, A. J. M. and Borst, P. (1994). Disruption of the mouse mdr1a P-glycoprotein gene leads to a deficiency in the blood-brain barrier and to increased sensitivity to drugs. Cell 77, 491–502.CrossRefGoogle ScholarPubMed
Selkirk, M. E., Huang, S. C., Knox, D. P. and Britton, C. (2012). The development of RNA interference (RNAi) in gastrointestinal nematodes. Parasitology 139, 605–612. doi: 10.1017/S0031182011002332.CrossRefGoogle ScholarPubMed
Seto, E. Y., Wong, B. K., Lu, D. and Zhong, B. (2011). Human schistosomiasis resistance to praziquantel in China: should we be worried? American Journal of Tropical Medicine and Hygiene 85, 74–82. doi: 10.4269/ajtmh.2011.10-0542.CrossRefGoogle Scholar
Silva, I. M., Thiengo, R., Conceição, M. J., Rey, L., Lenzi, H. L., Perreira Filho, E. and Ribeiro, P. C. (2005). Therapeutic failure of praziquantel in the treatment of Schistosoma haematobium infection in Brazilians returning from Africa. Memorias do Instituto Oswaldo Cruz 100, 445–449.CrossRefGoogle ScholarPubMed
Sioud, M. (2011). Promises and challenges in developing RNAi as a research tool and therapy. Methods in Molecular Biology 703, 173–187. doi: 10.1007/978-1-59745-248-9_12.CrossRefGoogle ScholarPubMed
Smout, M. J., Kotze, A. C., McCarthy, J. S. and Loukas, A. (2010). A novel high throughput assay for anthelmintic drug screening and resistance diagnosis by real-time monitoring of parasite motility. PLoS Neglected Tropical Diseases 4, e885. doi: 10.1371/journal.pntd.0000885.CrossRefGoogle ScholarPubMed
Stefanic, S., Dvorak, J., Horn, M., Braschi, S., Sojka, D., Ruelas, D. S., Suzuki, B., Lim, K. C., Hopkins, S. D., McKerrow, J. H. and Caffrey, C. R. (2010). RNA interference in Schistosoma mansoni schistosomula: selectivity, sensitivity and operation for larger-scale screening. PLoS Neglected Tropical Diseases 4, e850. doi: 10.1371/journal.pntd.0000850.CrossRefGoogle ScholarPubMed
Stelma, F. F., Sall, S., Daff, B., Sow, S., Niang, M. and Gryseels, B. (1997). Oxamniquine cures Schistosoma mansoni infection in a focus in which cure rates with praziquantel are unusually low. Journal of Infectious Diseases 176, 304–307.CrossRefGoogle Scholar
Stelma, F. F., Talla, I., Sow, S., Kongs, A., Niang, M., Polman, K., Deelder, A. M. and Gryseels, B. (1995). Efficacy and side effects of praziquantel in an epidemic focus of Schistosoma mansoni. American Journal of Tropical Medicine and Hygiene 53, 167–170.CrossRefGoogle Scholar
Suttiprapa, S., Rinaldi, G. and Brindley, P. J. (2012). Genetic manipulation of schistosomes - Progress with integration competent vectors. Parasitology 139, 641–650. doi: 10.1017/S003118201100134X.CrossRefGoogle ScholarPubMed
Swain, M. T., Larkin, D. M., Caffrey, C. R., Davies, S. J., Loukas, A., Skelly, P. J. and Hoffmann, K. F. (2011). Schistosoma comparative genomics: integrating genome structure, parasite biology and anthelmintic discovery. Trends in Parasitology 27, 555–564. doi: 10.1016/j.pt.2011.09.003.CrossRefGoogle ScholarPubMed
Szakacs, G., Paterson, J. K., Ludwig, J. A., Booth-Genthe, C. and Gottesman, M. M. (2006). Targeting multidrug resistance in cancer. Nature Reviews: Drug Discovery 5, 219–234.Google ScholarPubMed
Tchoubrieva, E. B. and Kalinna, B. (2010). Advances in mRNA silencing and transgene expression: a gateway to functional genomics in schistosomes. Biotechnology and Genetic Engineering Reviews 26, 261–280.CrossRefGoogle ScholarPubMed
Tchoubrieva, E. B., Ong, P. C., Pike, R. N., Brindley, P. J. and Kalinna, B. H. (2010). Vector-based RNA interference of cathepsin B1 in Schistosoma mansoni. Cellular and Molecular Life Sciences 67, 3739–3748. doi: 10.1007/s00018-010-0345-3.CrossRefGoogle ScholarPubMed
Tompkins, J. B., Stitt, L. E., Morrissette, A. M. and Ardelli, B. F. (2011). The role of Brugia malayi ATP-binding cassette (ABC) transporters in potentiating drug sensitivity. Parasitology Research 109, 1311–1322. doi: 10.1007/s00436-011-2378-4.CrossRefGoogle ScholarPubMed
Toure, S., Zhang, Y., Bosque-Oliva, E., Ky, C., Ouedraogo, A., Koukounari, A., Gabrielli, A. F., Bertrand, S., Webster, J. P. and Fenwick, A. (2008). Two-year impact of single praziquantel treatment on infection in the national control programme on schistosomiasis in Burkina Faso. Bulletin of the World Health Organization 86, 780–787.CrossRefGoogle ScholarPubMed
Tsai, M. H., Marx, K. A., Ismail, M. M. and Tao, L. (2000). Randomly amplified polymorphic DNA (RAPD) polymerase chain reaction assay for identification of Schistosoma mansoni strains sensitive or tolerant to anti-schistosomal drugs. Journal of Parasitology 86, 146–149.CrossRefGoogle ScholarPubMed
Valle, C., Troiani, A. R., Festucci, A., Pica-Mattoccia, L., Liberti, P., Wolstenholme, A., Francklow, K., Doenhoff, M. J. and Cioli, D. (2003). Sequence and level of endogenous expression of calcium channel beta subunits in Schistosoma mansoni displaying different susceptibilities to praziquantel. Molecular and Biochemical Parasitology 130, 111–115.CrossRefGoogle ScholarPubMed
van de Ven, R., Oerlemans, R., van der Heijden, J. W., Scheffer, G. L., de Gruijl, T. D., Jansen, G. and Scheper, R. J. (2009). ABC drug transporters and immunity: novel therapeutic targets in autoimmunity and cancer. Journal of Leukocyte Biology 86, 1075–1087. doi: 10.1189/jlb.0309147.CrossRefGoogle ScholarPubMed
van der Werf, M. J., de Vlas, S. J., Brooker, S., Looman, C. W., Nagelkerke, N. J., Habbema, J. D. and Engels, D. (2003). Quantification of clinical morbidity associated with schistosome infection in sub-Saharan Africa. Acta Tropica 86, 125–139.CrossRefGoogle ScholarPubMed
van Veen, H. W. (2010). Structural biology: last of the multidrug transporters. Nature 467, 926–927. doi: 10.1038/467926a.CrossRefGoogle ScholarPubMed
Vennervald, B. J., Booth, M., Butterworth, A. E., Kariuki, H. C., Kadzo, H., Ireri, E., Amaganga, C., Kimani, G., Kenty, L., Mwatha, J., Ouma, J. H. and Dunne, D. W. (2005). Regression of hepatosplenomegaly in Kenyan school-aged children after praziquantel treatment and three years of greatly reduced exposure to Schistosoma mansoni. Transactions of the Royal Society of Tropical Medicine and Hygiene 99, 150–160.CrossRefGoogle ScholarPubMed
Ventner, H., Shahi, S., Balakrishnan, L., Velamakanni, S., Bapna, A., Woebking, B. and van Veen, H. W. (2005). Similarities between ATP-dependent and ion-coupled multidrug transporters. Biochemical Society Transactions 33, 1008–1011.CrossRefGoogle Scholar
Vokřál, I., Jirásko, R., Jedličková, V., Bártíková, H., Skálová, L., Lamka, J., Holčapek, M. and Szotáková, B. (2012). The inability of tapeworm Hymenolepis diminuta and fluke Dicrocoelium dendriticum to metabolize praziquantel. Veterinary Parasitology 185, 168–174. doi: 10.1016/j.vetpar.2011.09.026.CrossRefGoogle ScholarPubMed
Wang, W., Dai, J. R., Li, H. J., Shen, X. H. and Liang, Y. S. (2010). Is there reduced susceptibility to praziquantel in Schistosoma japonicum? Evidence from China. Parasitology 137, 1905–1912. doi: 10.1017/S0031182010001204.CrossRefGoogle ScholarPubMed
Wang, W., Dai, J. R., Li, H. J., Shen, X. H. and Liang, Y. S. (2012 a). The sensitivity of Schistosoma japonicum to praziquantel: a field evaluation in areas with low endemicity of China. American Journal of Tropical Medicine and Hygiene 86, 834–836. doi: 10.4269/ajtmh.2012.11-0701.CrossRefGoogle ScholarPubMed
Wang, W., Wang, L. and Liang, Y. S. (2012 b). Susceptibility or resistance of praziquantel in human schistosomiasis: a review. Parasitology Research 111, 1871–1877. doi: 10.1007/s00436-012-3151-z.CrossRefGoogle ScholarPubMed
Webster, J. P., Gower, C. M. and Norton, A. J. (2008). Evolutionary concepts in predicting and evaluating the impact of mass chemotherapy schistosomiasis control programmes on parasites and their hosts. Evolutionary Applications 1, 66–83. doi: 10.1111/j.1752-4571.2007.00012.x.CrossRefGoogle ScholarPubMed
Welz, C., Kruger, N., Schniederjans, M., Miltsch, S. M., Krucken, J., Guest, M., Holden-Dye, L., Harder, A. and von Samson-Himmelstjerna, G. (2011). SLO-1-channels of parasitic nematodes reconstitute locomotor behaviour and emodepside sensitivity in Caenorhabditis elegans slo-1 loss of function mutants. PloS Pathogens 7, e1001330. doi: 10.1371/journal.ppat.1001330.CrossRefGoogle ScholarPubMed
Wilkinson, R., Law, C. J., Hoey, E. M., Fairweather, I., Brennan, G. P. and Trudgett, A. (2012). An amino acid substitution in Fasciola hepatica P-glycoprotein from triclabendazole-resistant and triclabendazole-susceptible populations. Molecular and Biochemical Parasitology 186, 69–72. doi: 10.1016/j.molbiopara.2012.08.008.CrossRefGoogle ScholarPubMed
William, S. and Botros, S. (2004). Validation of sensitivity to praziquantel using Schistosoma mansoni worm muscle tension and Ca2+-uptake as possible in vitro correlates to in vivo ED50 determination. International Journal for Parasitology 34, 971–977.CrossRefGoogle ScholarPubMed
William, S., Botros, S., Ismail, M., Farghally, A., Day, T. A. and Bennett, J. L. (2001 a). Praziquantel-induced tegumental damage in vitro is diminished in schistosomes derived from praziquantel-resistant infections. Parasitology 122, 63–66.CrossRefGoogle ScholarPubMed
William, S., Sabra, A., Ramzy, F., Mousa, M., Demerdash, Z., Bennett, J. L., Day, T. A. and Botros, S. (2001 b). Stability and reproductive fitness of Schistosoma mansoni isolates with decreased sensitivity to praziquantel. International Journal for Parasitology 31, 1093–1100.CrossRefGoogle ScholarPubMed
Xianyi, C., Liying, W., Jiming, C., Xiaonong, Z., Jiang, Z., Jiagang, G., Xiaohua, W., Engels, D. and Minggang, C. (2005). Schistosomiasis control in China: the impact of a 10-year World Bank Loan Project (1992–2001). Bulletin of the World Health Organization 83, 43–48.Google Scholar
Xiao, S. H., Catto, B. A. and Webster, L. T. Jr. (1985). Effects of praziquantel on different developmental stages of Schistosoma mansoni in vitro and in vivo. Journal of Infectious Diseases 151, 1130–1137.CrossRefGoogle ScholarPubMed
Xu, M., Molento, M., Blackhall, W., Ribeiro, P., Beech, R. and Prichard, R. (1998). Ivermectin resistance in nematodes may be caused by alteration of P-glycoprotein homolog. Molecular and Biochemical Parasitology 91, 327–335.CrossRefGoogle ScholarPubMed
Yang, Y., Jin, Y., Liu, P., Shi, Y., Cao, Y., Liu, J., Shi, Y., Li, H. and Lin, J. (2012). RNAi silencing of type V collagen in Schistosoma japonicum affects parasite morphology, spawning, and hatching. Parasitology Research 111, 1251–1257. doi: 10.1007/s00436-012-2959-x.CrossRefGoogle ScholarPubMed
Yu, D. B., Li, Y., Sleigh, A. C., Yu, X. L., Li, Y. S., Wei, W. Y., Liang, Y. S. and McManus, D. P. (2001). Efficacy of praziquantel against Schistosoma japonicum: field evaluation in an area with repeated chemotherapy compared with a newly identified endemic focus in Hunan, China. Transactions of the Royal Society of Tropical Medicine and Hygiene 95, 537–541.CrossRefGoogle Scholar
Zhang, D., Chan, J. D., Nogi, T. and Marchant, J. S. (2011). Opposing roles of voltage-gated Ca2+ channels in neuronal control of regenerative patterning. Journal of Neuroscience 31, 15983–15995. doi: 10.1523/JNEUROSCI.3029-11.2011.CrossRefGoogle ScholarPubMed