Serum albumin and α-1 acid glycoprotein impede the killing of Schistosoma mansoni by the tyrosine kinase inhibitor Imatinib

International Journal for Parasitology: Drugs and Drug Resistance

Volumn 4, Issue 3, 2014, Pages 287-295

  Beckmann, Svenja ^a   Long, Thavy ^b   Scheld, Christina ^a   Geyer, Rudolf ^a   Caffrey, Conor R ^b   Grevelding, Christoph G ^a  

^a JUSTUS LIEBIG UNIVERSITY   (Germany)

^b University of California at San Francisco   (United States)

Author keywords

Abl tyrosine kinase (Abl); Erythromycin; Imatinib (Gleevec, Glivec, STI 571); In vitro culture; Protein tyrosine kinase (PTK); Schistosoma mansoni; Serum albumin (SA); 1 acidic glycoprotein (AGP)

Indexed keywords

ERYTHROMYCIN; IMATINIB; OROSOMUCOID; SERUM ALBUMIN;

ARTICLE; BLOOD COMPONENT; CONTROLLED STUDY; DRUG BIOAVAILABILITY; EGG PRODUCTION; ENERGY RESOURCE; HELMINTHIASIS; IN SITU HYBRIDIZATION; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; NONHUMAN; OOCYTE; PHYSIOLOGICAL PROCESS; SCHISTOSOMA; SCHISTOSOMA MANSONI; SCHISTOSOMULUM;

EID: 85027957220     PISSN: None     EISSN: 22113207     Source Type: Journal    
DOI: 10.1016/j.ijpddr.2014.07.005     Document Type: Article

References (86)

1. Abdulla M.H., Ruelas D.S., Wolff B., Snedecor J., Lim K.C., Xu F., Renslo A.R., Williams J., McKerrow J.H., Caffrey C.R. Drug discovery for schistosomiasis: hit and lead compounds identified in a library of known drugs by medium-throughput phenotypic screening. PLoS Negl. Trop. Dis. 2009, 3(7):e478. 10.1371/journal.pntd.0000478.
2. Andrade L.F., Mourão M., Geraldo J.A., Coelho F.S., Silva L.L., Neves R.H., Machado-Silva J.R., Araujo N., Nacif-Pimenta R., Caffrey C.R., Oliveira G. Regulation of Schistosoma mansoni development and reproduction by the mitogen activated protein kinase signaling pathway. PLoS Negl. Trop. Dis. 2014, 8(6):e2949. 10.1371/journal.pntd.0002949.
3. Awidi A., Ayed A.O., Bsoul N., Magablah A., Mefleh R., Dweiri M., Ramahi M., Arafat E., Bishtawi M., Marie L. Relationship of serum imatinib trough level and response in CML patients: long term follow-up. Leuk. Res. 2010, 34(12):1573-1575.
4. Azuma M., Nishioka Y., Aono Y., Inayama M., Makino H., Kishi J., Shono M., Kinoshita K., Uehara H., Ogushi F., Izumi K., Sone S. Role of alpha1-acid glycoprotein in therapeutic antifibrotic effects of imatinib with macrolides in mice. Am. J. Respir. Crit. Care Med. 2007, 176(12):1243-1250.
5. Basch P.F. Cultivation of Schistosoma mansoni in vitro. I. Establishment of cultures from cercariae and development until pairing. J. Parasitol. 1981, 67:179-185.
6. Beckmann S., Grevelding C.G. Imatinib has a fatal impact on morphology, pairing stability and survival of adult Schistosoma mansoni in vitro. Int. J. Parasitol. 2010, 40(5):521-526.
7. Beckmann S., Hahnel S., Cailliau K., Vanderstraete M., Browaeys E., Dissous C., Grevelding C.G. Characterization of the Src/Abl Hybrid Kinase SmTK6 of Schistosoma mansoni. J. Biol. Chem. 2011, 286:42325-42336.
8. Beckmann S., Leutner S., Gouignard N., Dissous C., Grevelding C.G. Protein kinases as potential targets for novel anti-schistosomal strategies. Curr. Pharm. Des. 2012, 18(24):3579-3594.
9. Bennett M.W., Caulfield J.P. Schistosoma mansoni: ingestion of dextrans, serum albumin, and IgG by schistosomula. Exp. Parasitol. 1991, 73(1):52-61.
10. Berriman M., Haas B.J., LoVerde P.T., Wilson R.A., Dillon G.P., Cerqueira G.C., Mashiyama S.T., Al-Lazikani B., Andrade L.F., Ashton P.D., Aslett M.A., Bartholomeu D.C., Blandin G., Caffrey C.R., Coghlan A., Coulson R., Day T.A., Delcher A., DeMarco R., Djikeng A., Eyre T., Gamble J.A., Ghedin E., Gu Y., Hertz-Fowler C., Hirai H., Hirai Y., Houston R., Ivens A., Johnston D.A., Lacerda D., Macedo C.D., McVeigh P., Ning Z., Oliveira G., Overington J.P., Parkhill J., Pertea M., Pierce R.J., Protasio A.V., Quail M.A., Rajandream M.A., Rogers J., Sajid M., Salzberg S.L., Stanke M., Tivey A.R., White O., Williams D.L., Wortman J., Wu W., Zamanian M., Zerlotini A., Fraser-Liggett C.M., Barrell B.G., El-Sayed N.M. The genome of the blood fluke Schistosoma mansoni. Nature 2009, 460(7253):352-358.
11. Black C.L., Steinauer M.L., Mwinzi P.N., Secor E.W., Karanja D.M., Colley D.G. Impact of intense, longitudinal retreatment with praziquantel on cure rates of schistosomiasis mansoni in a cohort of occupationally exposed adults in western Kenya. Trop. Med. Int. Health 2009, 14:450-457.
12. Buro C., Oliveira K.C., Lu Z., Leutner S., Beckmann S., Dissous C., Cailliau K., Verjovski-Almeida S., Grevelding C.G. Transcriptome analyses of inhibitor-treated schistosome females provide evidence for cooperating Src-kinase and TGFβ receptor pathways controlling mitosis and eggshell formation. PLoS Pathog. 2013, 9(6):e1003448. 10.1371/journal.ppat.1003448.
13. Buro C., Beckmann S., Oliveira K., Dissous C., Cailliau K., Verjovski-Almeida S., Grevelding C.G. Imatinib treatment causes substantial transcriptional changes in adult Schistosoma mansoni in vitro exhibiting pleiotropic effects. PLoS Negl. Trop. Dis. 2014, 8(6):e2923. 10.1371/journal.pntd.0002923.
14. Caffrey C.R. Chemotherapy of schistosomiasis: present and future. Curr. Opin. Chem. Biol. 2007, 11(4):433-439.
15. Caffrey C.R., Williams D.L., Todd M.H., Nelson D.L., Keiser J., Utzinger J. Antibacterial Drug Discovery: From Molecular Targets to Drug Candidates 2009, 301-321. Wiley-VCH Verlag GmbH & Co. KGaA, Weinheim. M. Selzer (Ed.).
16. Caffrey, C.R., Selzer, P.M., 2012. In: Caffrey, C.R., Selzer, P.M. (Eds.), Parasitic Helminths: Targets, Screens, Drugs and Vaccines, Wiley-Blackwell.
17. Cheever A.W., Powers K.G. Schistosoma mansoni infection in rhesus monkeys:changes in egg production and egg distribution in prolonged infections in intact and splenectomized monkeys. Ann. Trop. Med. Parasitol. 1969, 63:83-93.
18. Chen Assessment of morbidity due to Schistosoma japonicum infection in China. Infect. Dis. Poverty 2014, 3(1):6. 10.1186/2049-9957-3-6.
19. Da'dara A.A., Faghiri Z., Krautz-Peterson G., Bhardwaj R., Skelly P.J. Schistosome Na, K-ATPase as a therapeutic target. Trans. R. Soc. Trop. Med. Hyg. 2013, 107(2):74-82.
20. Danso-Appiah A., Olliaro P.L., Donegan S., Sinclair D., Utzinger J. Drugs for treating Schistosoma mansoni infection. Cochrane Database Syst. Rev. 2013, 2013. 10.1002/14651858.CD000528.pub2.
21. De Bont J., Vercruysse J. Schistosomiasis in cattle. Adv. Parasitol. 1998, 41:285-364.
22. Delcroix M., Sajid M., Caffrey C.R., Lim K.C., Dvorák J., Hsieh I., Bahgat M., Dissous C., McKerrow J.H. A multienzyme network functions in intestinal protein digestion by a platyhelminth parasite. J. Biol. Chem. 2006, 281(51):39316-39329.
23. de Saram P.S., Ressurreição M., Davies A.J., Rollinson D., Emery A.M., Walker A.J. Functional mapping of protein kinase A reveals its importance in adult Schistosoma mansoni motor activity. PLoS Negl. Trop. Dis. 2013, 7(1):e1988. 10.1371/journal.pntd.0001988.
24. Dissous C., Grevelding C.G. Piggy-backing the concept of cancer drugs for schistosomiasis treatment: a tangible perspective?. Trends Parasitol. 2011, 27(2):59-66.
25. Dissous, C., Vanderstraete, M., Beckmann, S., Gouignard, N., Leutner, S., Buro, C., Grevelding, C.G., 2013. Receptor tyrosine kinase signalling and drug targeting in schistosomes. In: Doerig, C., Spaeth, G., Wiese, M., Selzer, P.M. (Eds.), Protein Phosphorylation in Parasites: Novel Targets for Antiparasitic Intervention, Wiley-Blackwell, Part IV, pp. 337-356.
26. 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.
27. Druker B.J., Talpaz M., Resta D.J., Peng B., Buchdunger E., Ford J.M., Lydon N.B., Kantarjian H., Capdeville R., Ohno-Jones S., Sawyers C.L. Efficacy and safety of a specific inhibitor of the BCR-ABL tyrosine kinase in chronic myeloid leukemia. N. Engl. J. Med. 2001, 344(14):1031-1037.
28. Fabbro D., Ruetz S., Buchdunger E., Cowan-Jacob S.W., Fendrich G., Liebetanz J., Mestan J., O'Reilly T., Traxler P., Chaudhuri B., Fretz H., Zimmermann J., Meyer T., Caravatti G., Furet P., Manley P.W. Protein kinases as targets for anticancer agents: from inhibitors to useful drugs. Pharmacol. Ther. 2002, 93(2-3):79-98.
29. Fenwick A., Rollinson D., Southgate V. Implementation of human schistosomiasis control: Challenges and prospects. Adv. Parasitol. 2006, 61:567-622.
30. Fitos I., Visy J., Zsila F., Mády G., Simonyi M. Selective binding of imatinib to the genetic variants of human alpha1-acid glycoprotein. Biochim. Biophys. Acta 2006, 1760(11):1704-1712.
31. Fitos I., Simon Á., Zsila F., Mády G., Bencsura Á., Varga Z., Orfi L., Kéri G., Visy J. Characterization of binding mode of imatinib to human α1-acid glycoprotein. Int. J. Biol. Macromol. 2012, 50(3):788-795.
32. Gambacorti-Passerini C., Barni R., le Coutre P., Zucchetti M., Cabrita G., Cleris L., Rossi F., Gianazza E., Brueggen J., Cozens R., Pioltelli P., Pogliani E., Corneo G., Formelli F., D'Incalci M. Role of alpha1 acid glycoprotein in the in vivo resistance of human BCR-ABL(+) leukemic cells to the abl inhibitor STI571 (Imatinib). J. Natl Cancer Inst. 2000, 92:1641-1650.
33. Gambacorti-Passerini C.B., Rossi F., Verga M., Ruchatz H., Gunby R., Frapolli R., Zucchetti M., Scapozza L., Bungaro S., Tornaghi L., Rossi F., Pioltelli P., Pogliani E., D'Incalci M., Corneo G. Differences between in vivo and in vitro sensitivity to imatinib of Bcr/Abl+ cells obtained from leukemic patients. Blood Cells Mol. Dis. 2002, 28(3):361-372.
34. Gambacorti-Passerini C., Zucchetti M., Russo D., Frapolli R., Verga M., Bungaro S., Tornaghi L., Rossi F., Pioltelli P., Pogliani E., Alberti D., Corneo G., D'Incalci M. Alpha1 acid glycoprotein binds to imatinib (STI571) and substantially alters its pharmacokinetics in chronic myeloid leukemia patients. Clin. Cancer Res. 2003, 9(2):625-632.
35. Geary T.G. Are new anthelmintics needed to eliminate human helminthiases?. Curr. Opin. Infect. Dis. 2012, 25(6):709-717.
36. Greenberg R.M. ABC multidrug transporters in schistosomes and other parasitic flatworms. Parasitol. Int. 2013, 62(6):647-653.
37. Grevelding C.G. The female-specific W1 sequence of the Puerto Rican strain of Schistosoma mansoni occurs in both genders of a Liberian strain. Mol. Biochem. Parasitol. 1995, 71:269-272.
38. Harder A. Chemotherapeutic approaches to schistosomes: current knowledge and outlook. Parasitol. Res. 2002, 88:395-397.
39. Heegaard P.M., Miller I., Sorensen N.S., Soerensen K.E., Skovgaard K. Pig α1-acid glycoprotein: characterization and first description in any species as a negative acute phase protein. PLoS One 2013, 8(7):e68110. 10.1371/journal.pone.0068110.
40. Hegde A.H., Punith R., Seetharamappa J. Optical, structural and thermodynamic studies of the association of an anti-leucamic drug imatinib mesylate with transport protein. J. Fluoresc. 2012, 22(1):521-528.
41. Hochepied T., Berger F.G., Baumann H., Libert C. Alpha(1)-acid glycoprotein: an acute phase protein with inflammatory and immunomodulating properties. Cytokine Growth Factor Rev. 2003, 14(1):25-34.
42. Holtfreter M.C., Loebermann M., Frei E., Riebold D., Wolff D., Hartung G., Kinzelbach R., Reisinger E.C. Schistosomula, pre-adults and adults of Schistosoma mansoni ingest fluorescence-labelled albumin in vitro and in vivo: implication for a drug-targeting model. Parasitology 2010, 137(11):1645-1652.
43. Huang H.H., Rigouin C., Williams D.L. The redox biology of schistosome parasites and applications for drug development. Curr. Pharm. Des. 2012, 18(24):3595-3611.
44. Huang Y.X., Manderson L. The social and economic context and determinants of schistosomiasis japonica. Acta Trop. 2005, 96:223-231.
45. Ishikawa Y., Kiyoi H., Watanabe K., Miyamura K., Nakano Y., Kitamura K., Kohno A., Sugiura I., Yokozawa T., Hanamura A., Yamamoto K., Iida H., Emi N., Suzuki R., Ohnishi K., Naoe T. Trough plasma concentration of imatinib reflects BCR-ABL kinase inhibitory activity and clinical response in chronic-phase chronic myeloid leukemia: a report from the BINGO study. Cancer Sci. 2010, 101(10):2186-2192.
46. Ismail M., Botros S., Metwally A., William S., Farghally A., Tao L.F., Day T.A., Bennett J.L. Resistance to praziquantel: direct evidence from Schistosoma mansoni isolated from Egyptian villagers. Am. J. Trop. Med. Hyg. 1999, 60:932-935.
47. 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.
48. Kasinathan R.S., Greenberg R.M. Pharmacology and potential physiological significance of schistosome multidrug resistance transporters. Exp. Parasitol. 2012, 132(1):2-6.
49. Katz N., Couto F.F., Araújo N. Imatinib activity on Schistosoma mansoni. Mem. Inst. Oswaldo Cruz 2013, 108(7):850-853.
50. Keiser J. In vitro and in vivo trematode models for chemotherapeutic studies. Parasitology 2010, 137(3):589-603.
51. King C.H. Parasites and poverty: the case of schistosomiasis. Acta Trop. 2010, 113:95-104.
52. Kremer J.M., Wilting J., Janssen L.H. Drug binding to human alpha-1-acid glycoprotein in health and disease. Pharmacol. Rev. 1988, 40:1-47.
53. Kretz O., Weiss H.M., Schumacher M.M., Gross G. In vitro blood distribution and plasma protein binding of the tyrosine kinase inhibitor imatinib and its active metabolite, CGP74588, in rat, mouse, dog, monkey, healthy humans and patients with acute lymphatic leukaemia. Br. J. Clin. Pharmacol. 2004, 58(2):212-216.
54. Larson R.A., Druker B.J., Guilhot F., O'Brien S.G., Riviere G.J., Krahnke T., Gathmann I., Wang Y. Imatinib pharmacokinetics and its correlation with response and safety in chronic-phase chronic myeloid leukemia: a subanalysis of the IRIS study. Blood 2008, 111:4022-4028.
55. Löscher, W., Ungemach, F.R., Kroker, R., 2006. Umrechnung von Humandosierung für Tiere, Dosierungsangaben, -berechnungen und Maßeinheiten. In: Pharmakotherapie bei Haus- und Nutztieren. Löscher, W., Ungemach, F.R., Kroker, R. (Eds.), Parey, 7th Edition, pp. 525-528.
56. Magnussen P. Treatment and re-treatment strategies for schistosomiasis control in different epidemiological settings: a review of 10 years' experiences. Acta Trop. 2003, 86:243-254.
57. Manley P.W., Cowan-Jacob S.W., Buchdunger E., Fabbro D., Fendrich G., Furet P., Meyer T., Zimmermann J. Imatinib: a selective tyrosine kinase inhibitor. Eur. J. Cancer 2002, 38(Suppl. 5):S19-S27.
58. McMullen D.B., Ritchie L.S., Oliver-González J., Knight W.B. Schistosoma mansoni in Macaca mulatta. Long-term studies on the course of primary and challenge infections. Am. J. Trop. Med. Hyg. 1967, 16(5):620-627.
59. 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., Loker E.S. Reduced susceptibility to Praziquantel among naturally occurring Kenyan isolates of Schistosoma mansoni. PLoS Negl. Trop. Dis. 2009, 3(8):e504. 10.1371/journal.pntd.0000504.
60. Mathers C.D., Ezzati M., Lopez A.D. Measuring the burden of neglected tropical diseases the global burden of disease framework. PLoS Negl. Trop. Dis. 2007, 1(2):e114. 10.1371/journal.pntd.0000114.
61. McManus D.P., Gray D.J., Li Y., McManus D.P., Gray D.J., Li Y., Feng Z., Williams G.M., Stewart D., Rey-Ladino J., Ross A.G. Schistosomiasis in the People's Republic of China: the era of the Three Gorges Dam. Clin. Microbiol. Rev. 2010, 23:442-466.
62. Montresor A., Gabrielli A.F., Chitsulo L., Ichimori K., Mariotti S., Engels D., Savioli L. Preventive chemotherapy and the fight against neglected tropical diseases. Expert Rev. Anti Infect. Ther. 2012, 10(2):237-242.
63. Murthy, P.K., Joseph, S.K., Murthy, P.S., 2011. Plant products in the treatment and control of filariasis and other helminth infections and assay systems for antifilarial/anthelmintic activity. Planta Med. 77(6), 647-661.
64. Nagar B., Bornmann W.G., Pellicena P., Schindler T., Veach D.R., Miller W.T., Clarkson B., Kuriyan J. Crystal structures of the kinase domain of c-Abl in complex with the small molecule inhibitor PDI173955 and Imatinib (STI-571). Cancer Res. 2002, 62:4236-4243.
65. Piafsky K.M. Disease-induced changes in the plasma binding of basic drugs. Clin. Pharmacokinet. 1980, 5(3):246-262.
66. Pica-Mattoccia L., Doenhoff M.J., Valle C., Basso A., Troiani A.R., Liberti P., Festucci A., Guidi A., Cioli D. Genetic analysis of decreased praziquantel sensitivity in a laboratory strain of Schistosoma mansoni. Acta Trop. 2009, 111:82-85.
67. Prichard R.K., Basáñez M.G., Boatin B.A., McCarthy J.S., García H.H., Yang G.J., Sripa B., Lustigman S. A research agenda for helminth diseases of humans: intervention for control and elimination. PLoS Negl. Trop. Dis. 2012, 6(4):e1549. 10.1371/journal.pntd.0001602.
68. 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., Berriman M. A systematically improved high quality genome and transcriptome of the human blood fluke Schistosoma mansoni. PLoS Negl. Trop. Dis. 2012, 6(1):e1455. 10.1371/journal.pntd.0001455.
69. Rodriguez C.A., Agudelo M., Zuluaga A.F., Vesga O. In vitro and in vivo comparison of the anti-staphylococcal efficacy of generic products and the innovator of oxacillin. BMC Infect. Dis. 2010, 10:153. 10.1186/1471-2334-10-153.
70. Rojo-Arreola L., Long T., Asarnow D., Suzuki B.M., Singh R., Caffrey C.R. Chemical and genetic validation of the statin drug target to treat the helminth disease, schistosomiasis. PLoS One 2014, 9(1):e87594. 10.1371/journal.pone.0087594.
71. Ross A.G., Bartley P.B., Sleigh A.C., Olds G.R., Li Y., Williams G.M., McManus D.P. Schistosomiasis. N. Engl. J. Med. 2002, 346:1212-1220.
72. Sabra A.N., Botros S.S. Response of Schistosoma mansoni isolates having different drug sensitivity to praziquantel over several life cycle passages with and without therapeutic pressure. J. Parasitol. 2008, 94:537-541.
73. Schistosoma japonicum Genome Sequencing and Functional Analysis Consortium The Schistosoma japonicum genome reveals features of host-parasite interplay. Nature 2009, 460(7253):345-351.
74. Schultz D.R., Arnold P.I. Properties of four acute phase proteins: C-reactive protein, serum amyloid A protein, alpha 1-acid glycoprotein, and fibrinogen. Semin. Arthritis Rheum. 1990, 20(3):129-147.
75. Soeiro M.N., Werbovetz K., Boykin D.W., Wilson W.D., Wang M.Z., Hemphill A. Novel amidines and analogues as promising agents against intracellular parasites: a systematic review. Parasitology 2013, 140(8):929-951.
76. Steinmann P., Keiser J., Bos R., Tanner M., Utzinger J. Schistosomiasis and water resources development: systematic review, meta-analysis, and estimates of people at risk. Lancet Infect. Dis. 2006, 6:411-425.
77. Stothard J.R., Chitsulo L., Kristensen T.K., Utzinger J. Control of schistosomiasis in sub-Saharan Africa: progress made, new opportunities and remaining challenges. Parasitology 2009, 136:1665-1675.
78. Svensson C.K., Woodruff M.N., Baxter J.G., Lalka D. Free drug concentration monitoring in clinical practice. Rationale and current status. Clin. Pharmacokinet. 1986, 11(6):450-469.
79. Swierczewski B.E., Davies S.J. Developmental regulation of protein kinase A expression and activity in Schistosoma mansoni. Int. J. Parasitol. 2010, 40(8):929-935.
80. Tesseromatis C., Alevizou A. The role of the protein-binding on the mode of drug action as well the interactions with other drugs. Eur. J. Drug Metab. Pharmacokinet. 2008, 33(4):225-230.
81. Teoh M., Narayanan P., Moo K.S., Radhakrisman S., Pillappan R., Bukhari N.I., Segarra I. HPLC determination of imatinib in plasma and tissues after multiple oral dose administration to mice. Pak. J. Pharm. Sci. 2010, 23(1):35-41.
82. Waller C.F. Imatinib mesylate. Recent Results Cancer Res. 2010, 184:3-20.
83. Wang T., Zhang S., Wu W., Zhang G., Lu D., Ornbjerg N., Johansen M.V. Treatment and reinfection of water buffaloes and cattle infected with Schistosoma japonicum in Yangtze River Valley, Anhui province. China. J. Parasitol. 2006, 92:1088-1091.
84. World Health Organization, 2013. Schistosomiasis. Fact sheet N°115. Available from: http://www.who.int/mediacentre/factsheets/fs115/en/.
85. Wu H.W., Qin Y.F., Chu K., Meng R., Liu Y., McGarvey S.T., Olveda R., Acosta L., Ji M.J., Fernandez T., Friedman J.F., Kurtis J.D. High prevalence of Schistosoma japonicum infection in water buffaloes in the Philippines assessed by real-time polymerase chain reaction. Am. J. Trop. Med. Hyg. 2010, 82:646-652.
86. Young N.D., Jex A.R., Li B., Liu S., Yang L., Xiong Z., Li Y., Cantacessi C., Hall R.S., Xu X., Chen F., Wu X., Zerlotini A., Oliveira G., Hofmann A., Zhang G., Fang X., Kang Y., Campbell B.E., Loukas A., Ranganathan S., Rollinson D., Rinaldi G., Brindley P.J., Yang H., Wang J., Wang J., Gasser R.B. Whole-genome sequence of Schistosoma haematobium. Nat. Genet. 2012, 44:221-225.