Modulation of a Schistosoma mansoni multidrug transporter by the antischistosomal drug praziquantel

FASEB Journal

Volumn 24, Issue 1, 2010, Pages 128-135

  Kasinathan, Ravi S ^a   Goronga, Tinopiwa ^b   Messerli, Shanta M ^c   Webb, Thomas R ^b   Greenberg, Robert M ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^c MARINE BIOLOGICAL LABORATORY   (United States)

Author keywords

Drug resistance; Efflux transporter; Verapamil

Indexed keywords

CARRIER PROTEIN; GLYCOPROTEIN P; NIFEDIPINE; PRAZIQUANTEL; PROTEIN SMDR2; UNCLASSIFIED DRUG; VERAPAMIL;

ANIMAL CELL; ARTICLE; CHO CELL; DRUG MECHANISM; DRUG METABOLISM; DRUG PROTEIN BINDING; DRUG TRANSPORT; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SCHISTOSOMA; SCHISTOSOMA MANSONI;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; ANIMALS; BASE SEQUENCE; CHO CELLS; CRICETINAE; CRICETULUS; DNA PRIMERS; DNA, HELMINTH; DRUG RESISTANCE, MULTIPLE; GENES, HELMINTH; HELMINTH PROTEINS; P-GLYCOPROTEINS; PRAZIQUANTEL; RECOMBINANT PROTEINS; RHODAMINES; SCHISTOSOMA MANSONI; SCHISTOSOMICIDES; TRANSFECTION; VANADATES;

CRICETULUS GRISEUS; MAMMALIA; PLATYHELMINTHES; SCHISTOSOMA MANSONI;

EID: 75149198677     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.09-137091     Document Type: Article

References (44)

1. Engels, D., Chitsulo, L., Montresor, A., and Savioli, L. (2002) The global epidemiological situation of schistosomiasis and new approaches to control and research. Acta Tropica 82, 139 -146
2. Chitsulo, L., Loverde, P., and Engels, D. (2004) Schistosomiasis. Nat. Rev. Microbiol. 2, 12-13
3. Gryseels, B., Polman, K., Clerinx, J., and Kestens, L. (2006) Human schistosomiasis. Lancet 368, 1106-1118
4. Kusel, J. R., McVeigh, P., and Thornhill, J. A. (2009) The schistosome excretory system: a key to regulation of metabolism, drug excretion and host interaction. Trends Parasitol. 25, 353-358
5. Andrews, P. (1985) Praziquantel: mechanisms of anti-schistosomal activity. Pharmacol. Ther. 29, 129-156
6. 2+ channels targets of praziquantel action? Int. J. Parasitol. 35, 1-9
7. 2+ channels and praziquantel in flatworm neuromusculature. Parasitology 131(Suppl.), S97-S108
8. Doenhoff, M. J., Cioli, D., and Utzinger, J. (2008) Praziquantel: mechanisms of action, resistance and new derivatives for schistosomiasis. Curr. Opin. Infect. Dis. 21, 659-667
9. Day, T. A., Bennett, J. L., and Pax, R. A. (1992) Praziquantel: the enigmatic antiparasitic. Parasitol. Today 8, 342-344
10. Redman, C. A., Robertson, A., Fallon, P. G., Modha, J., Kusel, J. R., Doenhoff, M. J., and Martin, R. J. Praziquantel. (1996) An urgent and exciting challenge. Parasitol. Today 12, 14 -20
11. Jeziorski, M. C., and Greenberg, R. M. (2006) Voltage-gated calcium channel subunits from platyhelminths: potential role in praziquantel action. Int. J. Parasitol. 36, 625-632
12. 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. Mol. Biochem. Parasitol. 164, 57-65
13. Angelucci, F., Basso, A., Bellelli, A., Brunori, M., Pica Mattoccia, L., and Valle, C. (2007) The anti-schistosomal drug praziquantel is an adenosine antagonist. Parasitology 134, 1215-1221
14. Gnanasekar, M., Salunkhe, A. M., Mallia, A. K., He, Y. X., and Kalyanasundaram, R. (2009) Praziquantel affects the regulatory myosin light chain of Schistosoma mansoni. Antimicrob. Agents Chemother. 53, 1054-1060
15. Tallima, H., and El Ridi, R. (2007) Praziquantel binds Schistosoma mansoni adult worm actin. Int. J. Antimicrob. Agents 29, 570-575
16. 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. Exp. Parasitol. 119, 332-335
17. Day, T. A., and Botros, S. (2006) Drug resistance in schistosomes. In Parasitic Flatworms: Molecular Biology, Biochemistry, Immunology and Physiology (Maule, A., and Marks, N. J., eds) pp. 256-268, CAB International, Wallington, Oxfordshire, UK
18. Leonard, G. D., Fojo, T., and Bates, S. E. (2003) The role of ABC transporters in clinical practice. Oncologist 8, 411-424
19. Ambudkar, S. V., Kimchi-Sarfaty, C., Sauna, Z. E., and Gottesman, M. M. (2003) P-glycoprotein: from genomics to mechanism. Oncogene 22, 7468-7485
20. Seeger, M. A., and van Veen, H. W. (2009) Molecular basis of multidrug transport by ABC transporters. Biochim. Biophys. Acta 1794, 725-737
21. 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
22. Paulsen, I. T. (2003) Multidrug efflux pumps and resistance: regulation and evolution. Curr. Opin. Microbiol. 6, 446-451
23. Zhou, S. F., Wang, L. L., Di, Y. M., Xue, C. C., Duan, W., Li, C. G., and Li, Y. (2008) Substrates and inhibitors of human multidrug resistance associated proteins and the implications in drug development. Curr. Med. Chem. 15, 1981-2039
24. Valderramos, S. G., and Fidock, D. A. (2006) Transporters involved in resistance to antimalarial drugs. Trends Pharmacol. Sci. 27, 594-601
25. Lespine, A., Alvinerie, M., Vercruysse, J., Prichard, R. K., and Geldhof, P. (2008) ABC transporter modulation: a strategy to enhance the activity of macrocyclic lactone anthelmintics. Trends Parasitol. 24, 293-298
26. 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. Mol. Biochem. Parasitol. 91, 327-335
27. Sangster, N. C., Bannan, S. C., Weiss, A. S., Nulf, S. C., Klein, R. D., and Geary, T. G. (1999) Haemonchus contortus: sequence heterogeneity of internucleotide binding domains from Pglycoproteins. Exp. Parasitol. 91, 250-257
28. Blackhall, W. J., Prichard, R. K., and Beech, R. N. (2008) P-glycoprotein selection in strains of Haemonchus contortus resistant to benzimidazoles. Vet. Parasitol. 152, 101-107
29. Bourguinat, C., Ardelli, B. F., Pion, S. D., Kamgno, J., Gardon, J., Duke, B. O., Boussinesq, M., and Prichard, R. K. (2008) P-glycoprotein-like protein, a possible genetic marker for ivermectin resistance selection in Onchocerca volvulus. Mol. Biochem. Parasitol. 158, 101-111
30. 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. Int. J. Antimicrob. Agents 22, 332-346
31. Jones, P. M., and George, A. M. (2005) Multidrug resistance in parasites: ABC transporters, P-glycoproteins and molecular modelling. Int. J. Parasitol. 35, 555-566
32. Messerli, S. M., Kasinathan, R. S., Morgan, W., Spranger, S., and Greenberg, R. M. (2009) Schistosoma mansoni Pglycoprotein levels increase in response to praziquantel exposure and correlate with reduced praziquantel susceptibility. Mol. Biochem. Parasitol. 167, 54 -59
33. 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. Mol. Biochem. Parasitol. 65, 351-356
34. 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
35. 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
36. 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
37. 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. Mem. Inst. Oswaldo Cruz 101, Suppl. 1, 293-298
38. 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. Eur. J. Pharm. Sci. 29, 70-81
39. Walter, M., and Kuris, A. (2003) Methods for the inhibition of egg production in trematodes. U.S. Patent 6,514,963 B2
40. Kohler, S., and Stein, W. D. (2003) Optimizing chemotherapy by measuring reversal of P-glycoprotein activity in plasma membrane vesicles. Biotechnol. Bioeng. 81, 507-517
41. Senior, A. E., al-Shawi, M. K., and Urbatsch, I. L. (1995) The catalytic cycle of P-glycoprotein. FEBS Lett. 377, 285-289
42. Shapiro, A. B., and Ling, V. (1998) The mechanism of ATP-dependent multidrug transport by P-glycoprotein. Acta Physiol. Scand. Suppl. 643, 227-234
43. Bonn, D. (2004) Schistosomiasis: a new target for calcium channel blockers. Lancet Infect. Dis. 4, 190
44. 2+ channels. J. Exp. Biol. 203, 841-856