Inhibition or Knockdown of ABC Transporters Enhances Susceptibility of Adult and Juvenile Schistosomes to Praziquantel

PLoS Neglected Tropical Diseases

Volumn 8, Issue 10, 2014, Pages

  Kasinathan, Ravi S ^a   Sharma, Lalit Kumar ^b   Cunningham, Charles ^c   Webb, Thomas R ^d   Greenberg, Robert M ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

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

^c UNIVERSITY OF NEW MEXICO   (United States)

^d SRI INTERNATIONAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ABC TRANSPORTER; ABC TRANSPORTER INHIBITOR; BREAST CANCER RESISTANCE PROTEIN INHIBITOR; DEXVERAPAMIL; ELACRIDAR; MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 1; MULTIDRUG RESISTANCE PROTEIN; MULTIDRUG RESISTANCE PROTEIN 1 INHIBITOR; PRAZIQUANTEL; PROTEIN INHIBITOR; TARIQUIDAR; UNCLASSIFIED DRUG; XENOBIOTIC AGENT; ZOSUQUIDAR; QUINOLINE DERIVATIVE; TOXIN;

ANALYTIC METHOD; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ENZYME INHIBITION; FEMALE; MOUSE; NONHUMAN; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; SCHISTOSOMA; SCHISTOSOMIASIS; WORM MOTILITY ANALYSIS; ANIMAL; ANTAGONISTS AND INHIBITORS; DISEASE PREDISPOSITION; DRUG EFFECTS; DRUG SENSITIVITY; GENETICS; MULTIDRUG RESISTANCE; PARASITOLOGY;

ANIMALS; DISEASE SUSCEPTIBILITY; DRUG RESISTANCE, MULTIPLE; P-GLYCOPROTEIN; PARASITIC SENSITIVITY TESTS; PRAZIQUANTEL; QUINOLINES; RNA INTERFERENCE; SCHISTOSOMA; SCHISTOSOMIASIS; TOXINS, BIOLOGICAL; XENOBIOTICS;

EID: 84920545860     PISSN: 19352727     EISSN: 19352735     Source Type: Journal    
DOI: 10.1371/journal.pntd.0003265     Document Type: Article

References (83)

1. Hotez PJ, Fenwick A, (2009) Schistosomiasis in Africa: an emerging tragedy in our new global health decade. PLoS Neglected Tropical Diseases 3: e485.
2. King CH, Dangerfield-Cha M, (2008) The unacknowledged impact of chronic schistosomiasis. Chronic Illness 4: 65–79.
3. van der Werf MJ, de Vlas SJ, Brooker S, Looman CW, Nagelkerke NJ, et al. (2003) Quantification of clinical morbidity associated with schistosome infection in sub-Saharan Africa. Acta Tropica 86: 125–139.
4. Doenhoff MJ, 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.
5. Hagan P, Appleton CC, Coles GC, Kusel JR, Tchuem-Tchuente LA, (2004) Schistosomiasis control: keep taking the tablets. Trends in Parasitology 20: 92–97.
6. Caffrey CR, (2007) Chemotherapy of schistosomiasis: present and future. Current Opinion in Chemical Biology 11: 433–439.
7. Toure S, Zhang Y, Bosque-Oliva E, Ky C, Ouedraogo A, et al. (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.
8. Vennervald BJ, Booth M, Butterworth AE, Kariuki HC, Kadzo H, et al. (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.
9. Fenwick A, Savioli L, Engels D, Robert Bergquist N, Todd MH, (2003) Drugs for the control of parasitic diseases: current status and development in schistosomiasis. Trends in Parasitology 19: 509–515.
10. Redman CA, Robertson A, Fallon PG, Modha J, Kusel JR, et al. (1996) Praziquantel: an urgent and exciting challenge. Parasitology Today 12: 14–20.
11. Greenberg RM, (2005) Are Ca2+ channels targets of praziquantel action? International Journal for Parasitology 35: 1–9.
12. Doenhoff MJ, Cioli D, Utzinger J, (2008) Praziquantel: mechanisms of action, resistance and new derivatives for schistosomiasis. Current Opinion in Infectious Diseases 21: 659–667.
13. Mutapi F, Rujeni N, Bourke C, Mitchell K, Appleby L, et al. (2011) Schistosoma haematobium treatment in 1–5 year old children: safety and efficacy of the antihelminthic drug praziquantel. PLoS Neglected Tropical Diseases 5: e1143.
14. Behbehani M, Savioli L (1998) Report of the WHO informal consultation on monitoring of drug efficacy in the control of schistosomiasis and intestinal nematodes. Geneva: World Health Organization. WHO/CDS/CPC/SIP/99.1.
15. Tukahebwa E, Vennervald BJ, Nuwaha F, Kabatereine NB, Magnussen P, (2013) Comparative efficacy of one versus two doses of praziquantel on cure rate of Schistosoma mansoni infection and re-infection in Mayuge District, Uganda. Transactions of the Royal Society of Tropical Medicine and Hygiene 107: 397–404.
16. Melman SD, Steinauer ML, Cunningham C, Kubatko LS, Mwangi IN, et al. (2009) Reduced susceptibility to praziquantel among naturally occurring Kenyan isolates of Schistosoma mansoni. PLoS Neglected Tropical Diseases 3: e504.
17. Couto FF, Coelho PM, Araujo N, Kusel JR, Katz N, et al. (2011) Schistosoma mansoni: a method for inducing resistance to praziquantel using infected Biomphalaria glabrata snails. Memorias do Instituto Oswaldo Cruz 106: 153–157.
18. Fallon PG, Doenhoff MJ, (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.
19. Greenberg RM, (2013) New approaches for understanding mechanisms of drug resistance in schistosomes. Parasitology 140: 1534–1546.
20. Day TA, Botros S (2006) Drug resistance in schistosomes. In: Maule A, Marks NJ, editors. Parasitic Flatworms: Molecular Biology, Biochemistry, Immunology and Physiology. Oxfordshire, UK: CAB International. pp. 256–268.
21. Aragon AD, Imani RA, Blackburn VR, Cupit PM, Melman SD, et al. (2009) Towards an understanding of the mechanism of action of praziquantel. Molecular and Biochemical Parasitology 164: 57–65.
22. Xiao SH, Catto BA, Webster LT, Jr (1985) Effects of praziquantel on different developmental stages of Schistosoma mansoni in vitro and in vivo. Journal of Infectious Diseases 151: 1130–1137.
23. Sabah AA, Fletcher C, Webbe G, Doenhoff MJ, (1986) Schistosoma mansoni: chemotherapy of infections of different ages. Experimental Parasitology 61: 294–303.
24. Pica-Mattoccia L, 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.
25. Lespine A, Alvinerie M, Vercruysse J, Prichard RK, Geldhof P, (2008) ABC transporter modulation: a strategy to enhance the activity of macrocyclic lactone anthelmintics. Trends in Parasitology 24: 293–298.
26. Liang XJ, Aszalos A, (2006) Multidrug transporters as drug targets. Current Drug Targets 7: 911–921.
27. Pohl A, Lage H, Muller P, Pomorski T, Herrmann A, (2002) Transport of phosphatidylserine via MDR1 (multidrug resistance 1) P-glycoprotein in a human gastric carcinoma cell line. Biochemical Journal 365: 259–268.
28. Aye ILMH, Singh AT, Keelan JA, (2009) Transport of lipids by ABC proteins: interactions and implications for cellular toxicity, viability, and function. Chemico-Biological Interactions 180: 327–339.
29. Sundaram P, Echalier B, Han W, Hull D, Timmons L, (2006) ATP-binding cassette transporters are required for efficient RNA interference in Caenorhabditis elegans. Molecular Biology of the Cell 17: 3678–3688.
30. Leier I, Jedlitschky G, Buccholz U, Cole SP, Deeley RG, et al. (1994) The MRP gene encodes an ATP-dependent export pump for leukotriene C4 and structurally related conjugates. Journal of Biological Chemistry 269: 27807–27810.
31. Johnstone RW, Ruefli AA, Smyth MJ, (2000) Multiple physiological functions for multidrug transporter P-glycoprotein? Trends in Biochemical Sciences 25: 1–6.
32. Mizutani T, Masuda M, Nakai E, Furumiya K, Togawa H, et al. (2008) Genuine functions of P-glycoprotein (ABCB1). Current Drug Metabolism 9: 167–174.
33. Yabe T, Suzuki N, Furukawa T, Ishihara T, Katsura I, (2005) Multidrug resistance-associated protein MRP-1 regulates dauer diapause by its export activity in Caenorhabditis elegans. Development 132: 3197–3207.
34. Johnstone RW, Ruefli AA, Tainton KM, Smyth MJ, (2000) A role for P-glycoprotein in regulating cell death. Leukemia and Lymphoma 38: 1–11.
35. Baguley BC, (2010) Multidrug resistance in cancer. Methods in Molecular Biology 596: 1–14.
36. van de Ven R, Oerlemans R, van der Heijden JW, Scheffer GL, de Gruijl TD, et al. (2009) ABC drug transporters and immunity: novel therapeutic targets in autoimmunity and cancer. Journal of Leukocyte Biology 86: 1075–1087.
37. Gottesman MM, Ling V, (2006) The molecular basis of multidrug resistance in cancer: the early years of P-glycoprotein research. FEBS Letters 580: 998–1009.
38. James CE, Hudson AL, Davey MW, (2009) Drug resistance mechanisms in helminths: is it survival of the fittest? Trends in Parasitology 25: 328–335.
39. Lespine A, Menez C, Bourguinat C, Prichard RK, (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.
40. Ardelli BF, (2013) Transport proteins of the ABC systems superfamily and their role in drug action and resistance in nematodes. Parasitology International 62: 639–646.
41. Greenberg RM, (2013) ABC multidrug transporters in schistosomes and other parasitic flatworms. Parasitology International 62: 647–653.
42. Kasinathan RS, Greenberg RM, (2012) Pharmacology and potential physiological significance of schistosome multidrug resistance transporters. Experimental Parasitology 132: 2–6.
43. Messerli SM, Kasinathan RS, Morgan W, Spranger S, Greenberg RM, (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.
44. Kasinathan RS, Morgan WM, Greenberg RM, (2010) 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.
45. Hines-Kay J, Cupit PM, Sanchez MC, Rosenberg GH, Hanelt B, et al. (2012) Transcriptional analysis of Schistosoma mansoni treated with praziquantel in vitro. Molecular and Biochemical Parasitology 186: 87–94.
46. Kasinathan RS, Goronga T, Messerli SM, Webb TR, Greenberg RM, (2010) Modulation of a Schistosoma mansoni multidrug transporter by the antischistosomal drug praziquantel. FASEB Journal 24: 128–135.
47. Kasinathan RS, Morgan WM, Greenberg RM, (2011) Genetic knockdown and pharmacological inhibition of parasite multidrug resistance transporters disrupts egg production in Schistosoma mansoni. PLoS Neglected Tropical Diseases 5: e1425.
48. Sato H, Kusel JR, Thornhill J, (2004) Excretion of fluorescent substrates of mammalian multidrug resistance-associated protein (MRP) in the Schistosoma mansoni excretory system. Parasitology 128: 43–52.
49. Sato H, Kusel JR, Thornhill J, (2002) Functional visualization of the excretory system of adult Schistosoma mansoni by the fluorescent marker resorufin. Parasitology 125: 527–535.
50. Roe M, Folkes A, Ashworth P, Brumwell J, Chima L, et al. (1999) Reversal of P-glycoprotein mediated multidrug resistance by novel anthranilamide derivatives. Bioorganic and Medicinal Chemistry Letters 9: 595–600.
51. Mistry P, Stewart AJ, Dangerfield W, Okiji S, Liddle C, et al. (2001) In vitro and in vivo reversal of P-glycoprotein-mediated multidrug resistance by a novel potent modulator, XR9576. Cancer Research 61: 749–758.
52. Fox E, Bates SE, (2007) Tariquidar (XR9576): a P-glycoprotein drug efflux pump inhibitor. Expert Review of Anti-Cancer Therapy 7: 447–459.
53. Martin C, Berridge G, Mistry P, Higgins C, Charlton P, et al. (1999) The molecular interaction of the high affinity reversal agent XR9576 with P-glycoprotein. British Journal of Pharmacology 128: 403–411.
54. Mehlhorn H, Becker B, Andrews P, Thomas H, Frenkel JK, (1981) In vivo and in vitro experiments on the effects of praziquantel on Schistosoma mansoni: a light and electron microscopic study. Arzneimittel-Forschung 31: 544–554.
55. Xiao SH, Catto BA, (1989) Comparative in vitro and in vivo activity of racemic praziquantel and its levorotated isomer on Schistosoma mansoni. Journal of Infectious Diseases 159: 589–592.
56. Andrews P, Thomas H, Pohlke R, Seubert J, (1983) Praziquantel. Medicinal Research Reviews 3: 147–200.
57. Tanaka M, Ohmae H, Utsunomiya H, Nara T, Irie Y, et al. (1989) A comparison of the antischistosomal effect of levo- and dextro-praziquantel on Schistosoma japonicum and S. mansoni in mice. American Journal of Tropical Medicine and Hygiene 41: 198–203.
58. Woelfle M, Seerden JP, de Gooijer J, Pouwer K, Olliaro P, et al. (2011) Resolution of praziquantel. PLoS Neglected Tropical Diseases 5: e1260.
59. Kongs A, Marks G, Verle P, 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.
60. Lin DD, Liu JX, Liu YM, Hu F, Zhang YY, et al. (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.
61. Lodh N, Mwansa JCL, Mutengo MM, Shiff CJ, (2013) Diagnosis of Schistosoma mansoni without the stool: detecting DNA from filtered urine comparison of three diagnostic tests to detect Schistosoma mansoni infection from filtered urine in Zambia. American Journal of Tropical Medicine and Hygiene 89: 46–50.
62. Higgins CF, Gottesman MM, (1992) Is the multidrug transporter a flippase? Trends in Biochemical Sciences 17: 18–21.
63. Sharom FJ, (2011) The P-glycoprotein multidrug transporter. Essays in Biochemistry 50: 161–178.
64. Kannan P, Telu S, Shukla S, Ambudkar SV, Pike VW, et al. (2011) The “specific” P-glycoprotein inhibitor tariquidar is also a substrate and an inhibitor for Breast Cancer Resistance Protein (BCRP/ABCG2). ACS Chemical Neuroscience 2: 82–89.
65. Hyafil F, Vergely C, Du Vignaud P, Grand-Perret T, (1993) In vitro and in vivo reversal of multidrug resistance by GF120918, an acridonecarboxamide derivative. Cancer Research 53: 4595–4602.
66. de Bruin M, Miyake K, Litman T, Robey R, Bates SE, (1999) Reversal of resistance by GF120918 in cell lines expressing the ABC half-transporter, MXR. Cancer Letters 146: 117–126.
67. Savage J, Meaney M, Brennan GP, Hoey E, Trudgett A, et al. (2013) Effect of the P-glycoprotein inhibitor, R(+)-verapamil on the drug susceptibility of a triclabendazole-resistant isolate of Fasciola hepatica. Veterinary Parasitology 195: 72–86.
68. Walter M, Kuris A (2003) Methods for the inhibition of egg production in trematodes. US Patent Number 6,514,963 B2.
69. Hayeshi R, Masimirembwa C, Mukanganyama S, Ungell AL, (2006) The potential inhibitory effect of antiparasitic drugs and natural products on P-glycoprotein mediated efflux. European Journal of Pharmaceutical Sciences 29: 70–81.
70. Gray DJ, McManus DP, Li Y, Williams GM, Bergquist R, et al. (2010) Schistosomiasis elimination: lessons from the past guide the future. Lancet Infectious Diseases 10: 733–736.
71. Lewis FA (1998) Schistosomiasis. In: Coligan JE, Kruisbeek AM, Margulies DH, Shevach EM, Strober W et al., editors. Current Protocols in Immunology. pp. 19.11.11–19.11.28.
72. Dantzig AH, Shepard RL, Cao J, Law KL, Ehlhardt WJ, et al. (1996) Reversal of P-glycoprotein-mediated multidrug resistance by a potent cyclopropyldibenzosuberane modulator, LY335979. Cancer Research 56: 4171–4179.
73. Allen JD, van Loevezijn A, Lakhai JM, van der Valk M, van Tellingen O, et al. (2002) Potent and specific inhibition of the breast cancer resistance protein multidrug transporter in vitro and in mouse intestine by a novel analogue of fumitremorgin C. Molecular Cancer Therapeutics 1: 417–425.
74. Burkhart CA, Watt F, Murray J, Pajic M, Prokvolit A, et al. (2009) Small molecule MRP1 inhibitor Reversan increases the therapeutic index of chemotherapy in mouse model of neuroblastoma. Cancer Research 69: 6573–6580.
75. Gruber A, Peterson C, Reizenstein P, (1988) D-verapamil and L-verapamil are equally effective in increasing vincristine accumulation in leukemic cells in vitro. International Journal of Cancer 41: 224–226.
76. Pirker R, Keilhauer G, Raschack M, Lechner C, Ludwig H, (1990) Reversal of multi-drug resistance in human KB cell lines by structural analogs of verapamil. International Journal of Cancer 45: 916–919.
77. Varma MV, Ashokraj Y, Dey CS, Panchagnula R, (2003) P-glycoprotein inhibitors and their screening: a perspective from bioavailability enhancement. Pharmacological Research 48: 347–359.
78. Sharma LK, Cupit PM, Goronga T, Webb TR, Cunningham C, (2014) Design and synthesis of molecular probes for the determination of the target of the anthelmintic drug praziquantel. Bioorganic and Medicinal Chemistry Letters 24: 2469–2472.
79. Schneider CA, Rasband WS, Elicieri KW, (2012) NIH Image to ImageJ: 25 years of image analysis. Nature Methods 9: 671–675.
80. Gavet O, Pines J, (2010) Progressive activation of CyclinB1-Cdk1 coordinates entry to mitosis. Developmental Cell 18: 533–543.
81. Krautz-Peterson G, Radwanska M, Ndegwa D, Shoemaker CB, Skelly PJ, (2007) Optimizing gene suppression in schistosomes using RNA interference. Molecular and Biochemical Parasitology 153: 194–202.
82. Sacan A, Ferhatosmanoglu H, Coskun H, (2008) CellTrack: an open-source software for cell tracking and motility analysis. Bioinformatics 24: 1647–1649.
83. Schmittgen TD, Livak KJ, (2008) Analyzing real-time PCR data by the comparative CT method. Nature Protocols 3: 1101–1108.