Current and prospective chemotherapy options for schistosomiasis

Expert Opinion on Orphan Drugs

Volumn 3, Issue 2, 2015, Pages 195-205

  You, Hong ^a   McManus, Donald P ^a   Gobert, Geoffrey N ^a  

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

Drug targets; Parasitic helminth; Praziquantel; Schistosoma; Schistosome; Schistosomiasis

Indexed keywords

ARTEMETHER; ARTEMISININ; ARTESUNATE; CALCIUM; DIHYDROARTEMISININ; GLUTATHIONE REDUCTASE; MEFLOQUINE; PRAZIQUANTEL; SEPTIN; THIOREDOXIN;

APOPTOSIS; DRUG MECHANISM; DRUG TARGETING; HUMAN; MICROCALORIMETRY; NONHUMAN; PRIORITY JOURNAL; REVIEW; SCHISTOSOMA; SCHISTOSOMIASIS; SIGNAL TRANSDUCTION;

EID: 84922120729     PISSN: None     EISSN: 21678707     Source Type: Journal    
DOI: 10.1517/21678707.2015.998998     Document Type: Review

References (99)

1. King CH, Dickman K, Tisch DJ. Reassessment of the cost of chronic helminthic infection: a meta-analysis of disability-related outcomes in endemic schistosomiasis. Lancet 2005;365:1561-9
2. Gryseels B, Polman K, Clerinx J, Kestens L. Human schistosomiasis. Lancet 2006;368:1106-18
3. Chuah C, Jones MK, Burke ML, et al. Cellular and chemokine-mediated regulation in schistosome-induced hepatic pathology. Trends Parasitol 2014;30:141-50
4. Murray CJ, Vos T, Lozano R, et al. Disability-adjusted life years (DALYs) for 291 diseases and injuries in 21 regions, 1990-2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 2013;380:2197-223
5. King CH. Parasites and poverty: the case of schistosomiasis. Acta Trop 2010;113:95-104
6. Beaumier CM, Gillespie PM, Hotez PJ, Bottazzi ME. New vaccines for neglected parasitic diseases and dengue. Transl Res 2013;162:144-55
7. Liu R, Dong HF, Guo Y, et al. Efficacy of praziquantel and artemisinin derivatives for the treatment and prevention of human schistosomiasis: a systematic review and meta-analysis. Parasit Vectors 2011;4:201
8. Harder A. Chemotherapeutic approaches to schistosomes: current knowledge and outlook. Parasitol Res 2002;88:395-7
9. Manneck T, Keiser J, Muller J. Mefloquine interferes with glycolysis in schistosomula of Schistosoma mansoni via inhibition of enolase. Parasitology 2012;139:497-505
10. Coles GC, Bruce JI. In vitro selection of drug resistant Schistosoma mansoni. Int J Parasitol 1987;17:767-71
11. Organization WH. The control of Schistosomiasis. WHO; Geneva: 1985. p. 728
12. Danso-Appiah A, Garner P, Olliaro PL, Utzinger J. Treatment of urinary schistosomiasis: methodological issues and research needs identified through a Cochrane systematic review. Parasitology 2009;136:1837-49
13. Silva IM, Thiengo R, Conceicao MJ, et al. Therapeutic failure of praziquantel in the treatment of Schistosoma haematobium infection in Brazilians returning from Africa. Mem Inst Oswaldo Cruz 2005;100:445-9
14. Roquis D, Lepesant JM, Villafan E, et al. Exposure to hycanthone alters chromatin structure around specific gene functions and specific repeats in Schistosoma mansoni. Front Genet 2014;5:207
15. Chai JY. Praziquantel treatment in trematode and cestode infections: an update. Infect Chemother 2013;45:32-43
16. Gustafsson LL, Beermann B, Abdi YA. Handbook of drugs for tropical parasitic infections. Taylor and Francis; London: 1987
17. WHO. Schistosomiasis: population requiring preventive chemotherapy and number of people treated in 2010. Wkly Epidemiol Rec 2012;87:37-44
18. Sayed AA, Simeonov A, Thomas CJ, et al. Identification of oxadiazoles as new drug leads for the control of schistosomiasis. Nat Med 2008;14:407-12
19. Xiao SH, Keiser J, Chen MG, et al. Research and development of antischistosomal drugs in the People's Republic of China a 60-year review. Adv Parasitol 2010;73:231-95
20. Doenhoff MJ, Cioli D, Utzinger J. Praziquantel: mechanisms of action, resistance and new derivatives for schistosomiasis. Curr Opin Infect Dis 2008;21:659-67
21. Cioli D, Pica-Mattoccia L. Praziquantel. Parasitol Res 2003;90(Supp 1):S3-9
22. Greenberg RM. Ca2+ signalling, voltagegated Ca2+ channels and praziquantel in flatworm neuromusculature. Parasitology 2005;131(Suppl):S97-S108
23. Pica-Mattoccia L, Orsini T, Basso A, et al. Schistosoma mansoni: lack of correlation between praziquantel-induced intra-worm calcium influx and parasite death. Exp Parasitol 2008;119:332-5
24. Pica-Mattoccia L, Doenhoff MJ, Valle C, et al. Genetic analysis of decreased praziquantel sensitivity in a laboratory strain of Schistosoma mansoni. Acta Trop 2009;111:82-5
25. Gray DJ, Ross AG, Li YS, McManus DP. Diagnosis and management of schistosomiasis. BMJ 2011;342:d2651
26. Cioli D, Botros SS, Wheatcroft-Francklow K, et al. Determination of ED50 values for praziquantel in praziquantel-resistant and-susceptible Schistosoma mansoni isolates. Int J Parasitol 2004;34:979-87
27. Gryseels B, Mbaye A, De Vlas SJ, et al. Are poor responses to praziquantel for the treatment of Schistosoma mansoni infections in Senegal due to resistance? An overview of the evidence. Trop Med Int Health 2001;6:864-73
28. Danso-Appiah A, De Vlas SJ. Interpreting low praziquantel cure rates of Schistosoma mansoni infections in Senegal. Trends Parasitol 2002;18:125-9
29. Huyse T, Van den Broeck F, Jombart T, et al. Regular treatments of praziquantel do not impact on the genetic make-up of Schistosoma mansoni in Northern Senegal. Infect Genet Evol 2013;18:100-5
30. Ismail M, Botros S, Metwally A, et al. Resistance to praziquantel: direct evidence from Schistosoma mansoni isolated from Egyptian villagers. Am J Trop Med Hyg 1999;60:932-5
31. Gobert GN, Jones MK. Discovering new schistosome drug targets: the role of transcriptomics. Curr Drug Targets 2008;9:922-30
32. Sato H, Kusel JR, Thornhill J. Excretion of fluorescent substrates of mammalian multidrug resistance-associated protein (MRP) in the Schistosoma mansoni excretory system. Parasitology 2004;128:43-52
33. Kasinathan RS, Morgan WM, Greenberg RM. Schistosoma mansoni express higher levels of multidrug resistance-associated protein 1 (SmMRP1) in juvenile worms and in response to praziquantel. Mol Biochem Parasitol 2010;173:25-31
34. Kasinathan RS, Sharma LK, Cunningham C, et al. Inhibition or knockdown of ABC transporters enhances susceptibility of adult and juvenile schistosomes to Praziquantel. PLoS Negl Trop Dis 2014;8:e3265
35. James CE, Hudson AL, Davey MW. Drug resistance mechanisms in helminths: is it survival of the fittest? Trends Parasitol 2009;25:328-35
36. Kopp SR, Coleman GT, Traub RJ, et al. Acetylcholine receptor subunit genes from Ancylostoma caninum: altered transcription patterns associated with pyrantel resistance. Int J Parasitol 2009;39:435-41
37. You H, McManus DP, Hu W, et al. Transcriptional responses of in vivo praziquantel exposure in schistosomes identifies a functional role for calcium signalling pathway member CamKII. PLoS Pathog 2013;9:e1003254 .
38. Smout MJ, Kotze AC, McCarthy JS, Loukas A. A novel high throughput assay for anthelmintic drug screening and resistance diagnosis by real-time monitoring of parasite motility. PLoS Negl Trop Dis 2010;4:e885
39. Runge FE, Heger R. Use of microcalorimetry in monitoring stability studies. Example: vitamin A esters. J Agric Food Chem 2000;48:47-55
40. Braissant O, Wirz D, Gopfert B, Daniels AU. Biomedical use of isothermal microcalorimeters. Sensors (Basel) 2010;10:9369-83
41. Keiser J, Manneck T, Kirchhofer C, Braissant O. Isothermal microcalorimetry to study the activity of triclabendazole and its metabolites on juvenile and adult Fasciola hepatica. Exp Parasitol 2013;133:265-8
42. Manneck T, Braissant O, Haggenmuller Y, Keiser J. Isothermal microcalorimetry to study drugs against Schistosoma mansoni. J Clin Microbiol 2011;49:1217-25
43. Gregory CA, Gunn WG, Peister A, Prockop DJ. An Alizarin red-based assay of mineralization by adherent cells in culture: comparison with cetylpyridinium chloride extraction. Anal Biochem 2004;329:77-84
44. Perez del Villar L, Burguillo FJ, Lopez-Aban J, Muro A. Systematic review and meta-analysis of artemisinin based therapies for the treatment and prevention of schistosomiasis. PLoS One 2012;7:e45867
45. Ho WE, Peh HY, Chan TK, Wong WS. Artemisinins: pharmacological actions beyond anti-malarial. Pharmacol Ther 2014;142:126-39
46. Li HJ, Wang W, Li YZ, et al. Effects of artemether, artesunate and dihydroartemisinin administered orally at multiple doses or combination in treatment of mice infected with Schistosoma japonicum. Parasitol Res 2011;109:515-19
47. Xiao SH. Development of antischistosomal drugs in China, with particular consideration to praziquantel and the artemisinins. Acta Trop 2005;96:153-67
48. Xiao S, Utzinger J, Chollet J, et al. Effect of artemether against Schistosoma haematobium in experimentally infected hamsters. Int J Parasitol 2000;30:1001-6
49. Zhai ZL, Zhang Y, Liu HX, et al. [Effect of artemether on enzymes involved in carbohydrate metabolism of Schistosoma japonicum]. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi 2000;18:162-4
50. Lepore R, Simeoni S, Raimondo D, et al. Identification of the Schistosoma mansoni molecular target for the antimalarial drug artemether. J Chem Inf Model 2011;51:3005-16
51. Xiao SH, You JQ, Mei JY, et al. Effect of artemether on glucose uptake and glycogen content in Schistosoma japonicum. Zhongguo Yao Li Xue Bao 1997;18:363-7
52. Eckstein-Ludwig U, Webb RJ, Van Goethem ID, et al. Artemisinins target the SERCA of Plasmodium falciparum. Nature 2003;424:957-61
53. Krishna S, Woodrow CJ, Staines HM, et al. Re-evaluation of how artemisinins work in light of emerging evidence of in vitro resistance. Trends Mol Med 2006;12:200-5
54. Xiao SH, You JQ, Gao HF, et al. Schistosoma japonicum: effect of artemether on glutathione S-transferase and superoxide dismutase. Exp Parasitol 2002;102:38-45
55. El-Lakkany NM, Seif El-Din SH. Haemin enhances the in vivo efficacy of artemether against juvenile and adult Schistosoma mansoni in mice. Parasitol Res 2013;112:2005-15
56. Abdin AA, Ashour DS, Shoheib ZS. Artesunate effect on schistosome thioredoxin glutathione reductase and cytochrome c peroxidase as new molecular targets in schistosoma mansoni-infected mice. Biomed Environ Sci 2013;26:953-61
57. Campos EG SJ, Prichard RK. Cytochrome c peroxidase in Schistosoma mansoni enzyme kinetics and cellular location. Comp Biochem Physiol 1995;111:371-7
58. Li HJ, Xu FL, Wang YH, et al. Dihydroartemisinin: a new story of an old drug against Schistosoma mansoni infection. Parasitol Res 2014;113:239-41
59. Li HJ, Wang W, Li YZ, et al. In vivo activity of dihydroartemisinin against Schistosoma mansoni schistosomula in mice. Southeast Asian J Trop Med Public Health 2013;44:379-87
60. Wang W, Li HJ, Qu GL, et al. Is there a reduced sensitivity of dihydroartemisinin against praziquantelresistant Schistosoma japonicum? Parasitol Res 2014;113:223-8
61. El-Beshbishi SN, Taman A, El-Malky M, et al. First insight into the effect of single oral dose therapy with artemisininnaphthoquine phosphate combination in a mouse model of Schistosoma mansoni infection. Int J Parasitol 2013;43:521-30
62. Xiao SH. Mefloquine, a new type of compound against schistosomes and other helminthes in experimental studies. Parasitol Res 2013;112:3723-40
63. Zhang CW, Xiao SH. Histopathological changes of juvenile Schistosoma japonicum harbored in mice treated orally with mefloquine at a smaller single dose. Parasitol Res 2012;110:2281-8
64. Xiao SH, Zhang CW. [Preliminary observation on the effect of mefloquine against egg granuloma formation in the liver of mice infected with Schistosoma japonicum]. Zhongguo Ji Sheng Chong Xue Yu Ji Sheng Chong Bing Za Zhi 2013;31:81-6
65. Keiser J, Manneck T, Vargas M. Interactions of mefloquine with praziquantel in the Schistosoma mansoni mouse model and in vitro. J Antimicrob Chemother 2011;66:1791-7
66. Keiser J, Silue KD, Adiossan LK, et al. Praziquantel, mefloquine-praziquantel, and mefloquine-artesunate-praziquantel against Schistosoma haematobium: a randomized, exploratory, open-label trial. PLoS Negl Trop Dis 2014;8:e2975
67. Basra A, Mombo-Ngoma G, Melser MC, et al. Efficacy of mefloquine intermittent preventive treatment in pregnancy against Schistosoma haematobium infection in Gabon: a nested randomized controlled assessor-blinded clinical trial. Clin Infect Dis 2013;56:e68-75
68. Young ND, Jex AR, Li B, et al. Whole-genome sequence of Schistosoma haematobium. Nat Genet 2012;44:221-5
69. Schistosoma japonicum Genome Sequencing and Functional Analysis Consortium. The Schistosoma japonicum genome reveals features of host-parasite interplay. Nature 2009;460:345-51
70. Berriman M, Haas BJ, LoVerde PT, et al. The genome of the blood fluke Schistosoma mansoni. Nature 2009;460:352-8
71. Cabal-Hierro L, Lazo PS. Signal transduction by tumor necrosis factor receptors. Cell Signal 2012;24:1297-305
72. Souers AJ, Leverson JD, Boghaert ER, et al. ABT-199, a potent and selective BCL-2 inhibitor, achieves antitumor activity while sparing platelets. Nat Med 2013;19:202-8
73. Lee EF, Young ND, Lim NT, et al. Apoptosis in schistosomes: toward novel targets for the treatment of schistosomiasis. Trends Parasitol 2014;30:75-84
74. Peng J, Gobert GN, Hong Y, et al. Apoptosis governs the elimination of Schistosoma japonicum from the nonpermissive host Microtus fortis. PLoS One 2011;6:e21109
75. Riedl SJ, Shi Y. Molecular mechanisms of caspase regulation during apoptosis. Nat Rev Mol Cell Biol 2004;5:897-907
76. Han H, Peng J, Gobert GN, et al. Apoptosis phenomenon in the schistosomulum and adult worm life cycle stages of Schistosoma japonicum. Parasitol Int 2013;62:100-8
77. Lee EF, Clarke OB, Evangelista M, et al. Discovery and molecular characterization of a Bcl-2-regulated cell death pathway in schistosomes. Proc Natl Acad Sci USA 2011;108:6999-7003
78. Kumar S, Biswal DK, Tandon V. In-silico analysis of caspase-3 and-7 proteases from blood-parasitic Schistosoma species (Trematoda) and their human host. Bioinformation 2013;9:456-63
79. Silke J, Meier P. Inhibitor of apoptosis (IAP) proteins-modulators of cell death and inflammation. Cold Spring Harb Perspect Biol 2013;5:a008730
80. Dao J, Zhu L, Luo R, et al. Molecular characterization of SjBIRP, another apoptosis inhibitor, from Schistosoma japonicum. Parasitol Res 2014;113:4065-71
81. Pinton P, Giorgi C, Siviero R, et al. Calcium and apoptosis: ER-mitochondria Ca2+ transfer in the control of apoptosis. Oncogene 2008;27:6407-18
82. Xiao SH, Mei JY, Jiao PY. The in vitro effect of mefloquine and praziquantel against juvenile and adult Schistosoma japonicum. Parasitol Res 2009;106:237-46
83. Hines-Kay J, Cupit PM, Sanchez MC, et al. Transcriptional analysis of Schistosoma mansoni treated with praziquantel in vitro. Mol Biochem Parasitol 2012;186:87-94
84. Vanderstraete M, Gouignard N, Cailliau K, et al. Dual targeting of insulin and venus kinase Receptors of Schistosoma mansoni for novel anti-schistosome therapy. PLoS Negl Trop Dis 2013;7:e2226
85. Beckmann S, Grevelding CG. Imatinib has a fatal impact on morphology, pairing stability and survival of adult Schistosoma mansoni in vitro. Int J Parasitol 2010;40:521-6
86. Beckmann S, Leutner S, Gouignard N, et al. Protein kinases as potential targets for novel anti-schistosomal strategies. Curr Pharm Des 2012;18:3579-94
87. Knobloch J, Beckmann S, Burmeister C, et al. Tyrosine kinase and cooperative TGFbeta signaling in the reproductive organs of Schistosoma mansoni. Exp Parasitol 2007;117:318-36
88. You H, Zhang W, Jones MK, et al. Cloning and characterisation of Schistosoma japonicum insulin receptors. PLoS One 2010;5:e9868
89. Vanderstraete M, Gouignard N, Cailliau K, et al. Venus kinase receptors control reproduction in the platyhelminth parasite Schistosoma mansoni. PLoS Pathog 2014;10:e1004138
90. Buro C, Oliveira KC, Lu Z, et al. Transcriptome analyses of inhibitortreated schistosome females provide evidence for cooperating Src-kinase and TGFbeta receptor pathways controlling mitosis and eggshell formation. PLoS Pathog 2013;9:e1003448
91. Long T, Cailliau K, Beckmann S, et al. Schistosoma mansoni Polo-like kinase 1: a mitotic kinase with key functions in parasite reproduction. Int J Parasitol 2010;40:1075-86
92. Swierczewski BE, Davies SJ. A schistosome cAMP-dependent protein kinase catalytic subunit is essential for parasite viability. PLoS Negl Trop Dis 2009;3:e505
93. Swierczewski BE, Davies SJ. Developmental regulation of protein kinase A expression and activity in Schistosoma mansoni. Int J Parasitol 2010;40:929-35
94. Kuntz AN, Davioud-Charvet E, Sayed AA, et al. Thioredoxin glutathione reductase from Schistosoma mansoni: an essential parasite enzyme and a key drug target. PLoS Med 2007;4:e206
95. Weirich CS, Erzberger JP, Barral Y. The septin family of GTPases: architecture and dynamics. Nat Rev Mol Cell Biol 2008;9:478-89
96. Zeraik AE, Rinaldi G, Mann VH, et al. Septins of Platyhelminths: identification, phylogeny, expression and localization among developmental stages of Schistosoma mansoni. PLoS Negl Trop Dis 2013;7:e2602
97. Zeraik AE, Galkin VE, Rinaldi G, et al. Reversible paralysis of Schistosoma mansoni by forchlorfenuron, a phenylurea cytokinin that affects septins. Int J Parasitol 2014;44:523-31
98. Zhang Y, Koukounari A, Kabatereine N, et al. Parasitological impact of 2-year preventive chemotherapy on schistosomiasis and soil-transmitted helminthiasis in Uganda. BMC Med 2007;5:27
99. Parker M, Allen T. Does mass drug administration for the integrated treatment of neglected tropical diseases really work? Assessing evidence for the control of schistosomiasis and soiltransmitted helminths in Uganda. Health Res Policy Syst 2011;9:3