Schistosome ABC multidrug transporters: From pharmacology to physiology

International Journal for Parasitology: Drugs and Drug Resistance

Volumn 4, Issue 3, 2014, Pages 301-309

  Greenberg, Robert M ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

ABC transporters; Drug resistance; Excretion; Parasite host interactions; Praziquantel; Reproduction; Schistosoma; Schistosomiasis

Indexed keywords

ABC TRANSPORTER; BREAST CANCER RESISTANCE PROTEIN; DEXVERAPAMIL; IVERMECTIN; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 1; MULTIDRUG RESISTANCE PROTEIN; PRAZIQUANTEL;

ANTHELMINTIC ACTIVITY; APOPTOSIS; BLOOD BRAIN BARRIER; CAENORHABDITIS ELEGANS; CELL DIFFERENTIATION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CYTOPLASM; DRUG SENSITIVITY; EGG PRODUCTION; ENZYME SPECIFICITY; EXCRETION; FASCIOLA HEPATICA; HOST PARASITE INTERACTION; IMMUNE RESPONSE; IMMUNOMODULATION; OOCYTE MATURATION; PARASITE SURVIVAL; PARASITE TRANSMISSION; PARASITE VIRULENCE; PERMEABILITY BARRIER; REVIEW; SCHISTOSOMA; SCHISTOSOMA MANSONI; SCHISTOSOMIASIS; SIGNAL TRANSDUCTION; TUMOR PROMOTION;

EID: 84916880545     PISSN: None     EISSN: 22113207     Source Type: Journal    
DOI: 10.1016/j.ijpddr.2014.09.007     Document Type: Review

References (152)

1. Aksoy E., Zouain C.S., Vanhoutte F., Fontaine J., Pavelka N., Thieblemont N., Willems F., Ricciardi-Castagnoli P., Goldman M., Capron M., Ryffel B., Trottein F. Double-stranded RNAs from the helminth parasite Schistosoma activate TLR3 in dendritic cells. J. Biol. Chem. 2005, 280:277-283.
2. Aller S.G., Yu J., Ward A., Weng Y., Chittaboina S., Zhuo R., Harrell P.M., Trinh Y.T., Zhang Q., Urbatsch I.L., Chang G. Structure of P-glycoprotein reveals a molecular basis for poly-specific drug binding. Science 2009, 323:1718-1722.
3. Ambudkar S.V., Kimchi-Sarfaty C., Sauna Z.E., Gottesman M.M. P-glycoprotein: from genomics to mechanism. Oncogene 2003, 22:7468-7485.
4. Andrews P., Thomas H., Pohlke R., Seubert J. Praziquantel. Med. Res. Rev. 1983, 3:147-200.
5. Angeli V., Faveeuw C., Rove O., Fontaine J., Teissiere E., Capron A., Wolowczuk I., Capron M., Trottein F. Role of the parasite-derived prostaglandin D2 in the inhibition of epidermal Langerhans cell migration during schistosomiasis infection. J. Exp. Med. 2001, 193:1135-1147.
6. Annilo T., Chen Z.Q., Shulenin S., Constantino J., Thomas L., Lou H., Stefanov S., Dean M. Evolution of the vertebrate ABC gene family: analysis of gene birth and death. Genomics 2006, 88:1-11.
7. Aragon A.D., Imani R.A., Blackburn V.R., Cupit P.M., Melman S.D., Goronga T., Webb T., Loker E.S., Cunningham C. Towards an understanding of the mechanism of action of praziquantel. Mol. Biochem. Parasitol. 2009, 164:57-65.
8. Ardelli B.F. Transport proteins of the ABC systems superfamily and their role in drug action and resistance in nematodes. Parasitol. Int. 2013, 62:639-646.
9. Ardelli B.F., Prichard R.K. Inhibition of P-glycoprotein enhances sensitivity of Caenorhabditis elegans to ivermectin. Vet. Parasitol. 2013, 191:264-275.
10. Aye I.L.M.H., Singh A.T., Keelan J.A. Transport of lipids by ABC proteins: interactions and implications for cellular toxicity, viability, and function. Chem. Biol. Interact. 2009, 180:327-339.
11. Borst P., Elferink R.O. Mammalian ABC transporters in health and disease. Annu. Rev. Biochem. 2002, 71:537-592.
12. Borst P., van Blitterswijk W.J., Borst J., Tepper A.D., Schinkel A.H. New physiological functions for drug-transporting P-glycoproteins?. Drug Resist. Updates 1998, 1:337-339.
13. Borst P., Zelcer N., van Helvoort A. ABC transporters in lipid transport. Biochim. Biophys. Acta 2000, 1486:128-144.
14. Bosch I., Dunussi-Joannopoulos K., Wu R.L., Furlong S.T., Croop J. Phosphatidylcholine and phosphatidylethanolamine behave as substrates of the human MDR1 P-glycoprotein. Biochemistry 1997, 36:5685-5694.
15. Boumendjel A., Florin A., Boutonnat J. Reversal agents of multidrug resistance mediated by multidrug resistance-associated proteins (MRPs). ABC Transporters and Multidrug Resistance 2009, 261-288. John Wiley & Sons Inc, Hoboken, NJ. A. Boumendjel, J. Boutonnat, J. Robert (Eds.).
16. Caffrey C.R. Chemotherapy of schistosomiasis: present and future. Curr. Opin. Chem. Biol. 2007, 11:433-439.
17. Chai J.-Y. Praziquantel treatment in trematode and cestode infections: an update. Infection and Chemotherapy 2013, 45:32-43.
18. 2+ entry phenologs predict new anti-schistosomal agents. PLoS Pathog. 2014, 10:e1003942.
19. Chan J.D., Zarowiecki M., Marchant J.S. Ca2+ channels and praziquantel: a view from the free world. Parasitol. Int. 2012, in press.
20. Chen Z.S., Lee K., Kruh G.D. Transport of cyclic nucleotides and estradiol 17-beta-D-glucuronide by multidrug resistance protein 4. Resistance to 6-mercaptopurine and 6-thioguanine. J. Biol. Chem. 2001, 276:33747-33754.
21. Chubb J.M., Bennett J.L., Akera T., Brody T.M. Effects of praziquantel, a new anthelmintic, on electromechanical properties of isolated rat atria. J. Pharmacol. Exp. Therapeutics 1978, 207:284-293.
22. Cioli D., Pica-Mattoccia L. Praziquantel. Parasitol. Res. 2003, 90(Suppl. 1):S3-S9.
23. Cioli D., Pica Mattoccia L., Basso A., Guidi A. Schistosomiasis control: praziquantel forever?. Mol. Biochem. Parasitol. 2014, 21:21-25. in press.
24. Cleland T.A. Inhibitory glutamate receptor channels. Mol. Neurobiol. 1996, 13:97-136.
25. Coley H.M. Overcoming multidrug resistance in cancer: clinical studies of P-glycoprotein inhibitors. Methods Mol. Biol. 2010, 596:341-358.
26. Colley D.G., Bustinduy A.L., Secor W.E., King C.H. Human schistosomiasis. Lancet 2014, 383:2253-2264.
27. Cornwell M.M., Pastan I., Gottesman M.M. Certain calcium channel blockers bind specifically to multidrug-resistant human KB carcinoma membrane vesicles and inhibit drug binding to P-glycoprotein. J. Biol. Chem. 1987, 262:2166-2170.
28. Couto F.F., Coelho P.M., Araujo N., Kusel J.R., Katz N., Mattos A.C. Use of fluorescent probes as a useful tool to identify resistant Schistosoma mansoni isolates to praziquantel. Parasitology 2010, 137:1791-1797.
29. Cui Y., Konig J., Buchholz J.K., Spring H., Leier I., Keppler D. Drug resistance and ATP-dependent conjugate transport mediated by the apical multidrug resistance protein, MRP2, permanently expressed in human and canine cells. Mol. Pharmacol. 1999, 55:929-937.
30. Daleke D.L. Phospholipid flippases. J. Biol. Chem. 2007, 282:821-825.
31. Dassa E., Bouige P. The ABC of ABCs: a phylogenetic and functional classification of ABC systems in living organisms. Res. Microbiol. 2001, 152:211-229.
32. Day T.A., Botros S. Drug resistance in schistosomes. Parasitic Flatworms: Molecular Biology, Biochemistry, Immunology and Physiology 2006, 256-268. CAB International, Oxfordshire, UK. A. Maule, N.J. Marks (Eds.).
33. Dean M., Allikmets R. Complete characterization of the human ABC gene family. J. Bioenerg. Biomembr. 2001, 33:475-479.
34. Dean M., Annilo T. Evolution of the ATP-binding cassette (ABC) transporter superfamily in vertebrates. Annu. Rev. Genomics Hum. Genet. 2005, 6:123-142.
35. Dean M., Rzhetsky A., Allikmets R. The human ATP-binding cassette (ABC) transporter superfamily. Genome Res. 2001, 11:1156-1166.
36. Doenhoff M.J., Pica-Mattoccia L. Praziquantel for the treatment of schistosomiasis: its use for control in areas with endemic disease and prospects for drug resistance. Exp. Rev. Anti-infect. Ther. 2006, 4:199-210.
37. Doenhoff M.J., Cioli D., Utzinger J. Praziquantel: mechanisms of action, resistance and new derivatives for schistosomiasis. Curr. Opin. Infect. Dis. 2008, 21:659-667.
38. Drach J., Gsur A., Hamilton G., Zhao S., Angerler J., Fiegl M., Zojer N., Raderer M., Haberl I., Andreeff M., Huber H. Involvement of P-glycoprotein in the transmembrane transport of interleukin-2 (IL-2), IL-4, and interferon-gamma in normal human T lymphocytes. Blood 1996, 88:1747-1754.
39. Dufour V., Beech R.N., Wever C., Dent J.A., Geary T.G. Molecular cloning and characterization of novel glutamate-gated chloride channel subunits from Schistosoma mansoni. PLoS Pathog. 2013, 9:e1003586.
40. Eisenbraun M.D., Miller R.A. Mdr1a-encoded P-glycoprotein is not required for peripheral T cell proliferation, cytokine release, or cytotoxic effector function in mice. J. Immunol. 1999, 163:2621-2627.
41. Ernest S., Bello-Reuss E. Secretion of platelet-activating factor is mediated by MDR1 P-glycoprotein in cultured human mesangial cells. J. Am. Soc. Nephrol. 1999, 10:2306-2313.
42. Fletcher J.I., Haber M., Henderson M.J., Norris M.D. ABC transporters in cancer: more than just drug efflux pumps. Nat. Rev. Cancer 2010, 10:147-156.
43. Frank M.H., Denton M.D., Alexander S.I., Khoury S.J., Sayegh M.H., Briscoe D.M. Specific MDR1 P-glycoprotein blockade inhibits human alloimmune T cell activation in vitro. J. Immunol. 2001, 166:2451-2459.
44. Garba A., Lamine M.S., Barkire N., Djibo A., Sofo B., Gouvras A.N., Labbo R., Sebangou H., Webster J.P., Fenwick A., Utzinger J. Efficacy and safety of two closely spaced doses of praziquantel against Schistosoma haematobium and S. mansoni and re-infection patterns in school-aged children in Niger. Acta Trop. 2013, 128:334-344.
45. Gardner D.R., Brezden B.L. The sites of action of praziquantel in a smooth muscle of Lymnaea stagnalis. Can. J. Physiol. Pharmacol. 1984, 62:282-287.
46. Geary T.G., Woo K., McCarthy J.S., Mackenzie C.D., Horton J., Prichard R.K., de Silva N.R., Olliaro P.L., Lazdins-Helds J.K., Engels D.A., Bundy D.A. Unresolved issues in anthelmintic pharmacology for helminthiases of humans. Int. J. Parasitol. 2010, 40:1-13.
47. Gimenez-Bonafe P., Guillen Canovas A., Ambrosio S., Tortosa A., Perez-Tomas R. Drugs modulating MDR. Research Signpost 2008, 63-99. Kerala, India. N.A. Colabufo (Ed.).
48. 2+ channels targets of praziquantel action?. Int. J. Parasitol. 2005, 35:1-9.
49. 2+ channels and praziquantel in flatworm neuromusculature. Parasitology 2005, 131(Suppl.):S97-S108.
50. Greenberg R.M. ABC multidrug transporters in schistosomes and other parasitic flatworms. Parasitol. Int. 2013, 62:647-653.
51. Greenberg R.M. New approaches for understanding mechanisms of drug resistance in schistosomes. Parasitology 2013, 140:1534-1546.
52. Greenberg R.M., John B., Hunter C.A., Kasinathan R.S. Schistosome ABC multidrug transporters: roles in parasite physiology, drug susceptibility and immunomodulatory signaling. Am. J. Trop. Med. Hyg. 2013, 89:A953.
53. Guo Y., Kotova E., Chen Z.S., Lee K., Hopper-Borge E., Belinsky M.G., Kruh G.D. MRP8, ATP-binding cassette C11 (ABCC11), is a cyclic nucleotide efflux pump and a resistance factor for fluoropyrimidines 2',3'-dideoxycytidine and 9'-(2'-phosphonylmethoxyethyl)adenine. J. Biol. Chem. 2003, 278:29509-29514.
54. Hayeshi R., Masimirembwa C., Mukanganyama S., Ungell A.L. The potential inhibitory effect of antiparasitic drugs and natural products on P-glycoprotein mediated efflux. Eur. J. Pharm. Sci. 2006, 29:70-81.
55. Higgins C.F., Gottesman M.M. Is the multidrug transporter a flippase?. Trends Biochem. Sci. 1992, 17:18-21.
56. Hines-Kay J., Cupit P.M., Sanchez M.C., Rosenberg G.H., Hanelt B., Cunningham C. Transcriptional analysis of Schistosoma mansoni treated with praziquantel in vitro. Mol. Biochem. Parasitol. 2012, 186:87-94.
57. Hinz A., Tampe R. ABC transporters and immunity: mechanism of self-defense. Biochemistry 2012, 51:4981-4989.
58. Honig S.M., Fu S., Mao X., Yopp A., Gunn M.D., Randolph G.J., Bromberg J.S. FTY720 stimulates multidrug transporter- and cysteinyl leukotriene-dependent T cell chemotaxis to lymph nodes. J. Clin. Invest. 2003, 111:627-637.
59. Hotez P.J., Fenwick A. Schistosomiasis in Africa: an emerging tragedy in our new global health decade. PLoS Negl. Trop. Dis. 2009, 3:e485.
60. Hu Y., Platzer E.G., Bellier A., Aroian R.V. Discovery of a highly synergistic anthelmintic combination that shows mutual hypersusceptibility. Proc. Natl. Acad. Sci. 2010, 107:5955-5960.
61. Hyde S.C., Emsley P., Hartshorn M.J., Mimmack M.M., Gileadi U., Pearce S.R., Gallagher M.P., Gill D.R., Hubbard R.E., Higgins C.F. Structural model of ATP-binding proteins associated with cystic fibrosis, multidrug resistance and bacterial transport. Nature 1990, 346:362-365.
62. James C.E., Hudson A.L., Davey M.W. Drug resistance mechanisms in helminths: is it survival of the fittest?. Trends Parasitol. 2009, 25:328-335.
63. James C.E., Hudson A.L., Davey M.W. An update on P-glycoprotein and drug resistance in Schistosoma mansoni. Trends Parasitol. 2009, 25:538-539.
64. Jin M.S., Oldham M.L., Zhang Q., Chen J. Crystal structure of the multidrug transporter P-glycoprotein from Caenorhabditis elegans. Nature 2012, 490:566-569.
65. Johnstone R.W., Ruefli A.A., Smyth M.J. Multiple physiological functions for multidrug transporter P-glycoprotein?. Trends Biochem. Sci. 2000, 25:1-6.
66. Johnstone R.W., Ruefli A.A., Tainton K.M., Smyth M.J. A role for P-glycoprotein in regulating cell death. Leukemia and Lymphoma 2000, 38:1-11.
67. Kartner N., Riordan J.R., Ling V. Cell surface P-glycoprotein associated with multidrug resistance in mammalian cell lines. Science 1983, 221:1285-1288.
68. Kasinathan R.S., Greenberg R.M. Pharmacology and potential physiological significance of schistosome multidrug resistance transporters. Exp. Parasitol. 2012, 132:2-6.
69. Kasinathan R.S., Goronga T., Messerli S.M., Webb T.R., Greenberg R.M. Modulation of a Schistosoma mansoni multidrug transporter by the antischistosomal drug praziquantel. FASEB J. 2010, 24:128-135.
70. Kasinathan R.S., Morgan W.M., Greenberg R.M. Genetic knockdown and pharmacological inhibition of parasite multidrug resistance transporters disrupts egg production in Schistosoma mansoni. PLoS Negl. Trop. Dis. 2011, 5:e1425.
71. Kerboeuf D., Blackhall W., Kaminsky R., von Samson-Himmelstjerna G. P-glycoprotein in helminths: function and perspectives for anthelmintic treatment and reversal of resistance. Int. J. Antimicrob. Agents 2003, 22:332-346.
72. Kim W.S., Weickert C.S., Garner B. Role of ATP-binding cassette transporters in brain lipid transport and neurological disease. J. Neurochem. 2008, 104:1145-1166.
73. King C.H. Parasites and poverty: the case of schistosomiasis. Acta Trop. 2010, 113:95-104.
74. King C.H., Dangerfield-Cha M. The unacknowledged impact of chronic schistosomiasis. Chronic Illness 2008, 4:65-79.
75. King C.H., Olbrych S.K., Soon M., Singer M.E., Carter J., Colley D.G. Utility of repeated praziquantel dosing in the treatment of schistosomiasis in high-risk communities in Africa: a systematic review. PLoS Negl. Trop. Dis. 2011, 5:e1321.
76. Kooij G., Backer R., Koning J.J., Reijerkerk A., van Horssen J., van der Pol S.M.A., Drexhage J., Schinkel A., Dijkstra C.D., den Haan J.M.M., Geijtenbeek T.B.H., de Vries H.E. P-Glycoprotein Acts as an Immunomodulator during Neuroinflammation. PLoS ONE 2009, 4:e8212.
77. Kooij G., van Horssen J., Bandaru W., Haughey N.J., De Vries H.E. The role of ATP-binding cassette transporters in neuro-inflammation: relevance for bioactive lipids. Front. Pharmacol. 2012, 3:74.
78. Koopmann J.O., Post M., Neefjes J.J., Hammerling G.J., Momburg F. Translocation of long peptides by transporters associated with antigen processing (TAP). Eur. J. Immunol. 1996, 26:1720-1728.
79. Kusel J.R., McVeigh P., Thornhill J.A. The schistosome excretory system: a key to regulation of metabolism, drug excretion and host interaction. Trends Parasitol. 2009, 25:353-358.
80. 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., Ribeiro F. The effects of drugs, ions, and poly-l-lysine on the excretory system of Schistosoma mansoni. Mem. Inst. Oswaldo Cruz 2006, 101:293-298.
81. + T cell help to facilitate parasite development. PLoS Pathog. 2010, 29:e1000892.
82. Leier I., Jedlitschky G., Buccholz U., Cole S.P., Deeley R.G., Keppler D. The MRP gene encodes an ATP-dependent export pump for leukotriene C4 and structurally related conjugates. J. Biol. Chem. 1994, 269:27807-27810.
83. Leprohon P., Legare D., Ouellette M. ABC transporters involved in drug resistance in human parasites. Essays Biochem. 2011, 50:121-144.
84. Lespine A., Alvinerie M., Vercruysse J., Prichard R.K., Geldhof P. ABC transporter modulation: a strategy to enhance the activity of macrocyclic lactone anthelmintics. Trends Parasitol. 2008, 24:293-298.
85. Lespine A., Menez C., Bourguinat C., Prichard R.K. P-glycoproteins and other multidrug resistance transporters in the pharmacology of anthelmintics: prospects for reversing transport-dependent anthelmintic resistance. Int. J. Parasitol.: Drugs Drug Resistance 2012, 2:58-75.
86. Li J., Jaimes K.F., Aller S.G. Refined structures of mouse P-glycoprotein. Protein Sci. 2014, 23:34-46.
87. Liang X.J., Aszalos A. Multidrug transporters as drug targets. Curr. Drug Targets 2006, 7:911-921.
88. Liptrott N.J., Penny M., Bray P.G., Sathish J., Khoo S.H., Back D.J., Owen A. The impact of cytokines on the expression of drug transporters, cytochrome P450 enzymes and chemokine receptors in human PBMC. Br. J. Pharmacol. 2009, 156:497-508.
89. McCluskey J., Rossjohn J., Purcell A.W. TAP genes and immunity. Curr. Opin. Immunol. 2004, 16:651-659.
90. Mealey K.L., Bentjen S.A., Gay J.M., Cantor G.H. Ivermectin sensitivity in collies is associated with a deletion mutation of the mdr1 gene. Pharmacogenetics 2001, 11:727-733.
91. Mizutani T., Masuda M., Nakai E., Furumiya K., Togawa H., Nakamura Y., Kawai Y., Nakahira K., Shinkai S., Takahashi K. Genuine functions of P-glycoprotein (ABCB1). Curr. Drug Metab. 2008, 9:167-174.
92. Moreland J.L., Gramada A., Buzko O.V., Zhang Q., Bourne P.E. The molecular biology toolkit (MBT): a modular platform for developing molecular visualization applications. BMC Bioinformatics 2005, 6:21.
93. Moreno Y., Nabhan J.F., Solomon J., Mackenzie C.D., Geary T.G. Ivermectin disrupts the function of the excretory-secretory apparatus in microfilariae of Brugia malayi. Proc. Natl. Acad. Sci. 2010, 107:20120-20125.
94. Morjani H., Madoulet C. Reversal agents for P-glycoprotein-mediated multidrug resistance. ABC Transporters and Multidrug Resistance 2009, 241-259. John Wiley & Sons Inc, Hoboken, NJ. A. Boumendjel, J. Boutonnat, J. Robert (Eds.).
95. Mutapi F., Rujeni N., Bourke C., Mitchell K., Appleby L., Nausch N., Midzi N., Mduluza T. Schistosoma haematobium treatment in 1-5 year old children: safety and efficacy of the antihelminthic drug praziquantel. PLoS Negl. Trop. Dis. 2011, 5:e1143.
96. Ndeffo Mbah M.L., Poolman E.M., Atkins K.E., Orenstein E.W., Meyers L.A., Townsend J.P., Galvani A.P. Potential cost-effectiveness of schistosomiasis treatment for reducing HIV transmission in Africa - the case of Zimbabwean women. PLoS Negl. Trop. Dis. 2013, 7:e2346.
97. Pawlik A., Baskiewicz-Masiuk M., Machalinski B., Kurzawski M., Gawronska-Szklarz B. Involvement of C3435T and G2677T multidrug resistance gene polymorphisms in release of cytokines from peripheral blood mononuclear cells treated with methotrexate and dexamethasone. Eur. J. Pharmacol. 2005, 528:27-36.
98. Pearce E.J., Macdonald C.A. The immunobiology of schistosomiasis. Nat. Rev. Immunol. 2002, 2:499-511.
99. Pendse S.S., Behjadi S., Schatton T., Izawa A., Sayegh M.H., Frank M.H. P-glycoprotein functions as a differentiation switch in antigen presenting cell maturation. Am. J. Transplant. 2006, 6:2884-2893.
100. Pica-Mattoccia L., Cioli D. Sex- and stage-related sensitivity of Schistosoma mansoni to in vivo and in vitro praziquantel treatment. Int. J. Parasitol. 2004, 34:527-533.
101. 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., Valle C. Schistosoma mansoni: lack of correlation between praziquantel-induced intra-worm calcium influx and parasite death. Exp. Parasitol. 2008, 119:332-335.
102. Piehler A.P., Ozcurumez M., Kaminski W.E. A-subclass ATP-binding cassette proteins in brain lipid homeostasis and neurodegeneration. Front. Psychiatry 2012, 3:17.
103. Pohl A., Lage H., Muller P., Pomorski T., Herrmann A. Transport of phosphatidylserine via MDR1 (multidrug resistance 1) P-glycoprotein in a human gastric carcinoma cell line. Biochem. J. 2002, 365:259-268.
104. Quazi F., Molday R.S. Lipid transport by mammalian ABC proteins. Essays Biochem. 2011, 50:265-290.
105. Raggers R.J., Vogels I., van Meer G. Multidrug-resistance P-glycoprotein (MDR1) secretes platelet-activating factor. Biochem. J. 2001, 357:859-865.
106. Raghu G., Park S.W., Roninson I.B., Mechetner E.B. Monoclonal antibodies against P-glycoprotein, an MDR1 gene product, inhibit interleukin-2 release from PHA-activated lymphocytes. Exp. Hematol. 1996, 24:1258-1264.
107. Randolph G.J., Beaulieu S., Pope M., Sugawara I., Hoffman L., Steinman R.M., Muller W.A. A physiologic function for P-glycoprotein (MDR-1) during the migration of dendritic cells from skin via afferent lymphatic vessels. Proc. Natl. Acad. Sci. 1998, 95:6924-6929.
108. Redman C.A., Robertson A., Fallon P.G., Modha J., Kusel J.R., Doenhoff M.J., Martin R.J. Praziquantel: an urgent and exciting challenge. Parasitol. Today 1996, 12:14-20.
109. Reid G., Wielinga P., Zelcer N., van der Heijden J.W., Kuil A., de Haas M., Wijnholds J., Borst P. The human multidrug resistance protein MRP4 functions as a prostaglandin efflux transporter and is inhibited by nonsteroidal antiinflammatory drugs. Proc. Natl. Acad Sci 2003, 100:9244-9249.
110. Rius M., Hummel-Eisenbeiss J., Keppler D. ATP-dependent transport of leukotrienes B4 and C4 by the multidrug resistance protein ABCC4 (MRP4). J. Phamacol. Exp. Ther. 2008, 324:86094.
111. Robb S.M., Ross E., Sanchez Alvarado A. SmedGD: the Schmidtea mediterranea genome database. Nucleic Acids Res. 2008, 36:599-606.
112. Romsicki Y., Sharom F.J. Phospholipid flippase activity of the reconstituted P-glycoprotein multidrug transporter. Biochemistry 2001, 40:6937-6947.
113. Sabah A.A., Fletcher C., Webbe G., Doenhoff M.J. Schistosoma mansoni: chemotherapy of infections of different ages. Exp. Parasitol. 1986, 61:294-303.
114. Safa A.R. Photoaffinity labeling of the multidrug-resistance-related P-glycoprotein with photoactive analogs of verapamil. Proc. Natl. Acad. Sci. 1988, 85:187-191.
115. Saier M.H., Paulsen I.T. Phylogeny of multidrug transporters. Semin. Cell Dev. Biol. 2001, 12:205-213.
116. Salafsky B., Fusco A.C. Schistosoma mansoni: a comparison of secreted vs nonsecreted eicosanoids in developing schistosomulae and adults. Exp. Parasitol. 1987, 64:361-367.
117. Sarkadi B., Homolya L., Szakacs G., Varadi A. Human multidrug resistance ABCB and ABCG transporters: participation in a chemoimmunity defense system. Physiol. Rev. 2006, 86:1179-1236.
118. Sato H., Kusel J.R., Thornhill J. Functional visualization of the excretory system of adult Schistosoma mansoni by the fluorescent marker resorufin. Parasitology 2002, 125:527-535.
119. Sato H., Kusel J.R., Thornhill J. Excretion of fluorescent substrates of mammalian multidrug resistance-associated protein (MRP) in the Schistosoma mansoni excretory system. Parasitology 2004, 128:43-52.
120. Savage J., Meaney M., Brennan G.P., Hoey E., Trudgett A., Fairweather I. Increased action of triclabendazole (TCBZ) in vitro against a TCBZ-resistant isolate of Fasciola hepatica following its co-incubation with the P-glycoprotein inhibitor, R(+)-verapamil. Exp. Parasitol. 2013, 135:642-653.
121. 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., Borst P. Disruption of the mouse mdr1a P-glycoprotein gene leads to a deficiency in the blood-brain barrier and to increased sensitivity to drugs. Cell 1994, 77:491-502.
122. Sesay S., Paye J., Bah M.S., McCarthy F.M., Conteh A., Sonnie M., Hodges M.H., Zhang Y. Schistosoma mansoni infection after three years of mass drug administration in Sierra Leone. Parasite Vector 2014, 7:14.
123. Seyffir F., Tampe R. ABC transporters in adaptive immunity. Biochim. Biophys. Acta 2014, in press.
124. Sharom F.J. Flipping and flopping-lipids on the move. IUBMB Life 2011, 63:736-746.
125. Sharom F.J. The P-glycoprotein multidrug transporter. Essays Biochem. 2011, 50:161-178.
126. Sheps J.A., Ralph S., Zhao Z.Y., Baillie D.L., Ling V. The ABC transporter gene family of Caenorhabditis elegans has implications for the evolutionary dynamics of multidrug resistance in eukaryotes. Genome Biol. 2004, 5:R15.
127. Shukla S., Wu C.P., Ambudkar S.V. Development of inhibitors of ATP-binding cassette drug transporters: present status and challenges. Exp. Opin. Drug Metabol. Toxicol. 2008, 4:205-223.
128. Sousa-Figueiredo J.C., Betson M., Atuhaire A., Arinaitwe M., Navaratnam A.M., Kabatereine N.B., Bickle Q., Stothard J.R. Performance and safety of praziquantel for treatment of intestinal schistosomiasis in infants and preschool children. PLoS Negl. Trop. Dis. 2012, 6:e1864.
129. Sturrock R.F. Schistosomiasis epidemiology and control: how did we get here and where should we go?. Mem. Inst. Oswaldo Cruz 2001, 96(Supplement):17-27.
130. Sundaram P., Echalier B., Han W., Hull D., Timmons L. ATP-binding cassette transporters are required for efficient RNA interference in Caenorhabditis elegans. Mol. Biol. Cell 2006, 17:3678-3688.
131. Szakacs G., Paterson J.K., Ludwig J.A., Booth-Genthe C., Gottesman M.M. Targeting multidrug resistance in cancer. Nat. Rev. Drug Discovery 2006, 5:219-234.
132. Tanaka H., Tsuji M. From discovery to eradication of schistosomiasis in Japan: 1847-1996. Int. J. Parasitol. 1997, 27:1465-1480.
133. Toure S., Zhang Y., Bosque-Oliva E., Ky C., Ouedraogo A., Koukounari A., Gabrielli A.F., Bertrand S., Webster J.P., Fenwick A. Two-year impact of single praziquantel treatment on infection in the national control programme on schistosomiasis in Burkina Faso. Bull. World Health Organ. 2008, 86:780-787.
134. Tukahebwa E., Vennervald B.J., Nuwaha F., Kabatereine N.B., Magnussen P. Comparative efficacy of one versus two doses of praziquantel on cure rate of Schistosoma mansoni infection and re-infection in Mayuge District, Uganda. Trans. R. Soc. Trop. Med. Hyg. 2013, 107:397-404.
135. van de Ven R., Scheffer G.L., Reurs A.W., Lindenberg J.J., Oerlemans R., Jansen G., Gillet J.P., Glasgow J.N., Pereboev A., Curiel D.T., Scheper R.J., de Gruijl T.D. A role for multidrug resistance protein 4 (MRP4; ABCC4) in human dendritic cell migration. Blood 2008, 112:2353-2359.
136. van de Ven R., Oerlemans R., van der Heijden J.W., Scheffer G.L., de Gruijl T.D., Jansen G., Scheper R.J. ABC drug transporters and immunity: novel therapeutic targets in autoimmunity and cancer. J. Leukoc. Biol. 2009, 86:1075-1087.
137. van de Ven R., Scheffer G.L., Scheper R.J., de Gruijl T.D. The ABC of dendritic cell development and function. Trends Immunol. 2009, 30:421-429.
138. van der Kleij D., Latz E., Brouwers J.F.H.M., Kruize Y.C.M., Schmitz M., Kurt-Jones E.A., Espevik T., de Jong E.C., Kapsenberg M.L., Golenbock D.T., Tielens A.G.M., Yazdanbakhsh M. A novel host-parasite lipid cross-talk. Schistosomal lyso-phosphatidylserine activates toll-like receptor 2 and affects immune polarization. J. Biol. Chem. 2002, 277:48122-48129.
139. Van der Kleij D., Van Remoortere A., Schuitemaker J.H., Kapsenberg M.L., Deeider A.M., Tielens A.G.M., Hokke C.H., Yazdanbakhsh M. Triggering of innate immune responses by schistosome egg glycolipids and their carbohydrate epitope GalNAc beta 1-4(Fuc alpha 1-2Fuc alpha 1-3)GlcNAc. J. Infect. Dis. 2002, 185:531-539.
140. van der Werf M.J., de Vlas S.J., Brooker S., Looman C.W., Nagelkerke N.J., Habbema J.D., Engels D. Quantification of clinical morbidity associated with schistosome infection in sub-Saharan Africa. Acta Trop. 2003, 86:125-139.
141. van Meer G., Halter D., Sprong H., Somerharju P., Egmond M.R. ABC lipid transporters: extruders, flippases, or flopless activators?. FEBS Lett. 2006, 580:1171-1177.
142. van Riet E., Everts B., Retra K., Phylipsen M., van Hellemond J.J., Tielens A.G.M., van der Kleij D., Hartgers F.C., Yazdanbakhsh M. Combined TLR2 and TLR4 ligation in the context of bacterial or helminth extracts in human monocyte derived dendritic cells: molecular correlates for Th1/Th2 polarization. BMC Immunol. 2009, 10:9.
143. 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., Dunne D.W. Regression of hepatosplenomegaly in Kenyan school-aged children after praziquantel treatment and three years of greatly reduced exposure to Schistosoma mansoni. Trans. R. Soc. Trop. Med. Hyg. 2005, 99:150-160.
144. Walter, M., Kuris, A., 2003. Methods for the inhibition of egg production in trematodes. US Patent Number 6,514,963 B2.
145. Wang W., Wang L., Liang Y.S. Susceptibility or resistance of praziquantel in human schistosomiasis: a review. Parasitol. Res. 2012, 111:1871-1877.
146. Wielinga P.R., van der Heijden I., Reid G., Beijnen J.H., Wijnholds J., Borst P. Characterization of the MRP4- and MRP5-mediated transport of cyclic nucleotides from intact cells. J. Biol. Chem. 2003, 278:17664-17671.
147. Wilkinson R., Law C.J., Hoey E.M., Fairweather I., Brennan G.P., Trudgett A. An amino acid substitution in Fasciola hepatica P-glycoprotein from triclabendazole-resistant and triclabendazole-susceptible populations. Mol. Biochem. Parasitol. 2012, 186:69-72.
148. Wilson M.S., Mentink-Kane M.M., Pesce J.T., Ramalingam T.R., Thompson R., Wynn T.A. Immunopathology of schistosomiasis. Immunol. Cell Biol. 2007, 85:148-154.
149. Wolstenholme A. Ion channels and receptor as targets for the control of parasitic nematodes. Int. J. Parasitol.: Drugs Drug Resistance 2011, 1:2-13.
150. Wu Z.H., Lu M.K., Hu L.Y., Li X. Praziquantel synergistically enhances paclitaxel efficacy to inhibit cancer cell growth. PLoS ONE 2012, 7:e51721.
151. Xiao S.H., Catto B.A., Webster L.T. Effects of praziquantel on different developmental stages of Schistosoma mansoni in vitro and in vivo. J. Infect. Dis. 1985, 151:1130-1137.
152. Yang C.P., Mellado W., Horwitz S.B. Azidopine photoaffinity labeling of multidrug resistance-associated glycoproteins. Biochem. Pharmacol. 1988, 37:1417-1421.