Skip to main content

Advertisement

SpringerLink
Log in

Recent Developments in Recombinant Proteins for Diagnosis of Human Fascioliasis

  • Review
  • Published:
Acta Parasitologica Aims and scope Submit manuscript

Abstract

Fascioliasis is an important neglected tropical disease that causes severe injury to the bile ducts and liver. Therefore, a rapid and accurate method for detection of Fasciola hepatica infection plays a vital role in early treatment. Currently, the diagnosis of fascioliasis is mainly conducted via serological tests using the excretory/secretory (E/S) products, which might cross-react with antigens from other helminth parasitic diseases. Hence, the development of serodiagnosis test using recombinant antigens may contribute to differentiate fascioliasis from other helminth infections. In the past 20 years, many attempts have been made to exert different F. hepatica recombinant antigens to obtain a well-established standard assay with high accuracy. In this review, we address recent studies that refer to the development of serodiagnosis tests for diagnosis of human fascioliasis based on the candidate recombinant antigens produced by different approaches. Meanwhile, in the present review, some main factors have been highlighted to improve the accuracy of diagnostic tests such as the effect of refolding methods to recover antigens’ tertiary structure as well as applying a mixture of recombinant antigens with the highest sensitivity and specificity to improve the accuracy of diagnostic tests.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Acosta D, Cancela M, Piacenza L, Roche L, Carmona C, Tort JF (2008) Fasciola hepatica leucine aminopeptidase, a promising candidate for vaccination against ruminant fasciolosis. Mol Biochem Parasitol 158(1):52–64. https://doi.org/10.1016/j.molbiopara.2007.11.011

    Article  CAS  PubMed  Google Scholar 

  2. Adela Valero M, Victoria Periago M, Pérez-Crespo I, Rodríguez E, Jesús Perteguer M, Gárate T, Mas-Coma S (2012) Assessing the validity of an ELISA test for the serological diagnosis of human fascioliasis in different epidemiological situations. Trop Med Int Health 17(5):630–636. https://doi.org/10.1111/j.1365-3156.2012.02964.x

    Article  CAS  PubMed  Google Scholar 

  3. Aksoy D, Kerimoglu U, Oto A, Erguven S, Arslan S, Unal S, Bayraktar Y (2005) Infection with Fasciola hepatica. Clin Microbiol Infect 11(11):859–861. https://doi.org/10.1111/j.1469-0691.2005.01254.x

    Article  CAS  PubMed  Google Scholar 

  4. Allam G, Bauomy IR, Hemyeda ZM, Sakran TF (2012) Evaluation of a 14.5 kDa-Fasciola gigantica fatty acid binding protein as a diagnostic antigen for human fascioliasis. Parasitol Res 110(5):1863–1871. https://doi.org/10.1007/s00436-011-2711-y

    Article  PubMed  Google Scholar 

  5. Arjona R, Riancho JA, Aguado JM, Salesa R, Gonzalez-Macias J (1995) Fascioliasis in developed countries: a review of classic and aberrant forms of the disease. Medicine 74(1):13–23. https://doi.org/10.1097/00005792-199501000-00002

    Article  CAS  PubMed  Google Scholar 

  6. Awad W, Ibrahim A, Salib F (2009) Using indirect ELISA to assess different antigens for the serodiagnosis of Fasciola gigantica infection in cattle, sheep and donkeys. Res Vet Sci 86(3):466–471. https://doi.org/10.1016/j.rvsc.2008.08.009

    Article  CAS  PubMed  Google Scholar 

  7. Berkmen M (2012) Production of disulfide-bonded proteins in Escherichia coli. Protein Expr Purif 82(1):240–251. https://doi.org/10.1016/j.pep.2011.10.009

    Article  CAS  PubMed  Google Scholar 

  8. Bessette PH, Åslund F, Beckwith J, Georgiou G (1999) Efficient folding of proteins with multiple disulfide bonds in the Escherichia coli cytoplasm. Proc Natl Acad Sci 96(24):13703–13708. https://doi.org/10.1073/pnas.96.24.13703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Cabán-Hernández K, Gaudier JF, Espino AM (2012) Characterization and differential expression of a ferritin protein from Fasciola hepatica. Mol Biochem Parasitol 182(1–2):54–61. https://doi.org/10.1016/j.molbiopara.2011.12.005

    Article  CAS  PubMed  Google Scholar 

  10. Cabán-Hernández K, Gaudier JF, Ruiz-Jiménez C, Espino AM (2014) Development of two antibody detection enzyme-linked immunosorbent assays for serodiagnosis of human chronic fascioliasis. J Clin Microbiol 52(3):766–772. https://doi.org/10.1128/JCM.02875-13

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Carnevale S, Rodrıguez MI, Santillan G, Labbe JH, Cabrera MG, Bellegarde EJ, Guarnera EA (2001) Immunodiagnosis of human fascioliasis by an enzyme-linked immunosorbent assay (ELISA) and a micro-ELISA. Clin Diagn Lab Immunol 8(1):174–177. https://doi.org/10.1128/CDLI.8.1.174-177.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Chen M, Mott K (1990) Progress in assessment of morbidity due to Fasciola hepatica infection: a review of recent literature. Trop Dis Bull 87(4):1–38

    Google Scholar 

  13. Cordova M, Reategui L, Espinoza J (1999) Immunodiagnosis of human fascioliasis with Fasciola hepatica cysteine proteinases. Trans R Soc Trop Med Hyg 93(1):54–57. https://doi.org/10.1016/s0035-9203(99)90178-5

    Article  CAS  PubMed  Google Scholar 

  14. Cornelissen JB, Gaasenbeek CP, Borgsteede FH, Holland WG, Harmsen MM, Boersma WJ (2001) Early immunodiagnosis of fasciolosis in ruminants using recombinant Fasciola hepatica cathepsin L-like protease. Int J Parasitol 31(7):728–737. https://doi.org/10.1016/s0020-7519(01)00175-8

    Article  CAS  PubMed  Google Scholar 

  15. Cywińska A (2005) Epidemiology of fascioliasis in human endemic areas. J Helminthol 79(3):207–216. https://doi.org/10.1079/joh2005296

    Article  Google Scholar 

  16. Dalton JP, Brindley PJ, Knox DP, Brady CP, Hotez PJ, Donnelly S, Loukas A (2003) Helminth vaccines: from mining genomic information for vaccine targets to systems used for protein expression. Int J Parasitol 33(5–6):621–640. https://doi.org/10.1016/s0020-7519(03)00057-2

    Article  CAS  PubMed  Google Scholar 

  17. Dalton JP, Neill SO, Stack C, Collins P, Walshe A, Sekiya M, Khaznadji E (2003) Fasciola hepatica cathepsin L-like proteases: biology, function, and potential in the development of first generation liver fluke vaccines. Int J Parasitol 33(11):1173–1181. https://doi.org/10.1016/s0020-7519(03)00057-2

    Article  CAS  PubMed  Google Scholar 

  18. Dawes B, Hughes D (1964) Fascioliasis: the invasive stages of Fasciola hepatica in mammalian hosts. Adv Parasitol 2:97–168. https://doi.org/10.1016/S0065-308X(08)60587-4

    Article  CAS  PubMed  Google Scholar 

  19. De Marco A (2009) Strategies for successful recombinant expression of disulfide bond-dependent proteins in Escherichia coli. Microb Cell Fact 8(1):26. https://doi.org/10.1016/S0065-308X(08)60587-4

    Article  PubMed  PubMed Central  Google Scholar 

  20. Demerdash ZA, Diab TM, Aly IR, Mohamed SH, Mahmoud FS, Zoheiry MK, El-Bassiouny AE (2011) Diagnostic efficacy of monoclonal antibody based sandwich enzyme linked immunosorbent assay (ELISA) for detection of Fasciola gigantica excretory/secretory antigens in both serum and stool. Parasites Vectors 4(1):176. https://doi.org/10.1186/1756-3305-4-176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Dorny P, Praet N, Deckers N, Gabriël S (2009) Emerging food-borne parasites. Vet Parasitol 163(3):196–206. https://doi.org/10.1016/j.vetpar.2009.05.026

    Article  CAS  PubMed  Google Scholar 

  22. Espino AM, Díaz A, Pérez A, Finlay CM (1998) Dynamics of antigenemia and coproantigens during a human Fasciola hepatica outbreak. J Clin Microbiol 36(9):2723–2726. https://doi.org/10.1128/JCM.36.9.2723-2726.1998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Espino AM, Finlay C (1994) Sandwich enzyme-linked immunosorbent assay for detection of excretory secretory antigens in humans with fascioliasis. J Clin Microbiol 32(1):190–193. https://doi.org/10.1128/JCM.32.1.190-193.1994

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Espino AM, Hillyer GV (2004) A novel Fasciola hepatica saposinlike recombinant protein with immunoprophylactic potential. J Parasitol 90(4):876–879. https://doi.org/10.1645/GE-215R

    Article  CAS  PubMed  Google Scholar 

  25. Espino AM, Morales A, Delgado B, Rivera FM, Figueroa O, Suárez E (2010) Partial immunity to Fasciola hepatica in mice after vaccination with FhSAP2 delivered as recombinant protein or DNA construct. Ethnicity Dis 20(101):S1

    Google Scholar 

  26. Espino AM, Rivera F (2010) Quantitation of cytokine mRNA by real-time RT-PCR during a vaccination trial in a rabbit model of fascioliasis. Vet Parasitol 169(1–2):82–92. https://doi.org/10.1016/j.vetpar.2009.12.018

    Article  CAS  PubMed  Google Scholar 

  27. Espinoza JR, Maco V, Marcos L, Saez S, Neyra V, Terashima A, Huaman MC (2007) Evaluation of Fas2-ELISA for the serological detection of Fasciola hepatica infection in humans. Am J Trop Med Hyg 76(5):977–982. https://doi.org/10.4269/ajtmh.2007.76.977

    Article  CAS  PubMed  Google Scholar 

  28. Fica A, Dabanch J, Farias C, Castro M, Jercic M, Weitzel T (2012) Acute fascioliasis—clinical and epidemiological features of four patients in Chile. Clin Microbiol Infect 18(1):91–96. https://doi.org/10.1111/j.1469-0691.2011.03575.x

    Article  CAS  PubMed  Google Scholar 

  29. Figueroa-Santiago O, Delgado B, Espino AM (2011) Fasciola hepatica saposin-like protein-2–based ELISA for the serodiagnosis of chronic human fascioliasis. Diagn Microbiol Infect Dis 70(3):355–361. https://doi.org/10.1016/j.diagmicrobio.2011.03.016

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Frank SA (2002) Immunology and evolution of infectious disease. Princeton University Press, Princeton (ISBN: 978-0-691-09595-0)

    Book  Google Scholar 

  31. Gaudier JF, Cabán-Hernández K, Osuna A, Espino AM (2012) Biochemical characterization and differential expression of a 16.5 kDa tegument-associated antigen from the liver fluke Fasciola hepatica. Clin Vaccine Immunol 19(3):325–333. https://doi.org/10.1128/CVI.05501-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Gironènes N, Valero MA, García-Bodelón MA, Chico-Calero I, Punzón C, Presno M, Mas-Coma S (2007) Immune suppression in advanced chronic fascioliasis: an experimental study in a rat model. J Infect Dis 195(10):1504–1512. https://doi.org/10.1086/514822

    Article  CAS  Google Scholar 

  33. Gopal GJ, Kumar A (2013) Strategies for the production of recombinant protein in Escherichia coli. Protein J 32(6):419–425. https://doi.org/10.1007/s10930-013-9502-5

    Article  CAS  PubMed  Google Scholar 

  34. Gottstein B, Schneeberger M, Boubaker G, Merkle B, Huber C, Spiliotis M, Doherr MG (2014) Comparative assessment of ELISAs using recombinant saposin-like protein 2 and recombinant cathepsin L-1 from Fasciola hepatica for the serodiagnosis of human fasciolosis. PLoS Negl Trop Dis 8(6):e2860. https://doi.org/10.1371/journal.pntd.0002860

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Harper S, Speicher DW (2011) Purification of proteins fused to glutathione S-transferase. Protein chromatography. Springer, Berlin, pp 259–280. https://doi.org/10.1007/978-1-60761-913-0_14

    Chapter  Google Scholar 

  36. Hillyer GV (1999) Immunodiagnosis of human and animal fasciolosis. Fasciolosis 13:435–447

    Google Scholar 

  37. Hillyer GV, de Galanes MS, Rodriguez-Perez J, Bjorland J, de Lagrava MS, Guzman SR, Bryan RT (1992) Use of the FalconTM assay screening test-enzyme-linked immunosorbent assay (FAST-ELISA) and the enzyme-linked immunoelectrotransfer blot (EITB) to determine the prevalence of human fascioliasis in the Bolivian altiplano. Am J Trop Med Hyg 46(5):603–609. https://doi.org/10.4269/ajtmh.1992.46.603

    Article  CAS  PubMed  Google Scholar 

  38. Hotez PJ, Brindley PJ, Bethony JM, King CH, Pearce EJ, Jacobson J (2008) Helminth infections: the great neglected tropical diseases. J Clin Investig 118(4):1311–1321. https://doi.org/10.1172/JCI34261

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Ikeda T, Oikawa Y, Nishiyama T (1996) Enzyme-linked immunosorbent assay using cysteine proteinase antigens for immunodiagnosis of human paragonimiasis. Am J Trop Med Hyg 55(4):434–437. https://doi.org/10.4269/ajtmh.1996.55.434

    Article  Google Scholar 

  40. Itoh M, Sato S (1990) Multi-dot enzyme-linked immunosorbent assay for serodiagnosis of trematodiasis. Southeast Asian J Trop Med Public Health 21(3):471–474

    CAS  PubMed  Google Scholar 

  41. Kamel HH, Saad GA, Sarhan RM (2013) Dot-blot immunoassay of Fasciola gigantica infection using 27 kDa and adult worm regurge antigens in Egyptian patients. Korean J Parasitol 51(2):177. https://doi.org/10.3347/kjp.2013.51.2.177

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Kaya M, Beştaş R, Çetin S (2011) Clinical presentation and management of Fasciola hepatica infection: single-center experience. World J Gastroenterol 17(44):4899. https://doi.org/10.3748/wjg.v17.i44.4899

    Article  PubMed  PubMed Central  Google Scholar 

  43. Keiser J, Utzinger J (2009) Food-borne trematodiases. Clin Microbiol Rev 22(3):466–483. https://doi.org/10.1128/CMR.00012-09

    Article  PubMed  PubMed Central  Google Scholar 

  44. Kofta W, Mieszczanek J, Płucienniczak G, Wedrychowicz H (2000) Successful DNA immunisation of rats against fasciolosis. Vaccine 18(26):2985–2990. https://doi.org/10.1016/S0264-410X(00)00095-5

    Article  CAS  PubMed  Google Scholar 

  45. Kuerpick B, Schnieder T, Strube C (2013) Evaluation of a recombinant cathepsin L1 ELISA and comparison with the Pourquier and ES ELISA for the detection of antibodies against Fasciola hepatica. Vet Parasitol 193(1–3):206–213. https://doi.org/10.1016/j.vetpar.2012.11.021

    Article  CAS  PubMed  Google Scholar 

  46. Law RH, Smooker PM, Irving JA, Piedrafita D, Ponting R, Kennedy NJ, Spithill TW (2003) Cloning and expression of the major secreted cathepsin B-like protein from juvenile Fasciola hepatica and analysis of immunogenicity following liver fluke infection. Infect Immun 71(12):6921–6932. https://doi.org/10.1128/IAI.71.12.6921-6932.2003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Lobstein J, Emrich CA, Jeans C, Faulkner M, Riggs P, Berkmen M (2012) SHuffle, a novel Escherichia coli protein expression strain capable of correctly folding disulfide bonded proteins in its cytoplasm. Microb Cell Fact 11(1):753. https://doi.org/10.1186/1475-2859-11-56

    Article  CAS  Google Scholar 

  48. Losada S, Chacon N, Colmenares C, Bermudez H, Lorenzo A, Pointier J, Noya O (2005) Schistosoma: cross-reactivity and antigenic community among different species. Exp Parasitol 111(3):182–190. https://doi.org/10.1016/j.exppara.2005.07.00749

    Article  CAS  PubMed  Google Scholar 

  49. Lustigman S, Prichard RK, Gazzinelli A, Grant WN, Boatin BA, McCarthy JS, Basanez M-G (2012) A research agenda for helminth diseases of humans: the problem of helminthiases. PLoS Negl Trop Dis 6(4):e1582. https://doi.org/10.1371/journal.pntd.0001582

    Article  PubMed  PubMed Central  Google Scholar 

  50. Maleewong W, Intapan P, Wongkham C, Tomanakan K, Daenseekaew W, Sukeepaisarnjaroen W (1996) Comparison of adult somatic and excretory-secretory antigens in enzyme-linked immunosorbent assay for serodiagnosis of human infection with Fasciola gigantica. Southeast Asian J Trop Med Public Health 27(3):566–569

    CAS  PubMed  Google Scholar 

  51. Mamathambika BS, Bardwell JC (2008) Disulfide-linked protein folding pathways. Annu Rev Cell Dev Biol 24:211–235. https://doi.org/10.1146/annurev.cellbio.24.110707.175333

    Article  CAS  PubMed  Google Scholar 

  52. Marcilla A, De la Rubia J, Sotillo J, Bernal D, Carmona C, Villavicencio Z, Esteban J (2008) Leucine aminopeptidase is an immunodominant antigen of Fasciola hepatica excretory and secretory products in human infections. Clin Vaccine Immunol 15(1):95–100. https://doi.org/10.1128/CVI.00338-07

    Article  CAS  PubMed  Google Scholar 

  53. Martínez-Sernández V, Muiño L, Perteguer MJ, Gárate T, Mezo M, González-Warleta M, Ubeira FM (2011) Development and evaluation of a new lateral flow immunoassay for serodiagnosis of human fasciolosis. PLoS Negl Trop Dis 5(11):e1376. https://doi.org/10.1371/journal.pntd.0001376

    Article  PubMed  PubMed Central  Google Scholar 

  54. Mas-Coma M, Esteban J, Bargues M (1999) Epidemiology of human fascioliasis: a review and proposed new classification. Bull World Health Organ 77(4):340

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Mas-Coma S (2005) Epidemiology of fascioliasis in human endemic areas. J Helminthol 79(3):207–216. https://doi.org/10.1079/JOH2005296

    Article  CAS  PubMed  Google Scholar 

  56. Mas-Coma S, Bargues M, Valero M (2014) Diagnosis of human fascioliasis by stool and blood techniques: update for the present global scenario. Parasitology 141(14):1918–1946. https://doi.org/10.1017/S0031182014000869

    Article  CAS  PubMed  Google Scholar 

  57. Mas-Coma S, Bargues MD, Valero M (2005) Fascioliasis and other plant-borne trematode zoonoses. Int J Parasitol 35(11–12):1255–1278. https://doi.org/10.1016/j.ijpara.2005.07.010

    Article  CAS  PubMed  Google Scholar 

  58. Mas-Coma S, Valero MA, Bargues MD (2014) Fascioliasis. Digenetic trematodes. Springer, Berlin, pp 77–114. https://doi.org/10.1007/978-1-4939-0915-5_4

    Chapter  Google Scholar 

  59. Mas-Coma S, Valero MA, Bargues MD (2009) Fasciola, lymnaeids and human fascioliasis, with a global overview on disease transmission, epidemiology, evolutionary genetics, molecular epidemiology and control. Adv Parasitol 69:41–146. https://doi.org/10.1016/S0065-308X(09)69002-3

    Article  PubMed  Google Scholar 

  60. Mas CS, Bargues M (1997) Human liver flukes: a review. Res Rev Parasitol 57:15–218

    Google Scholar 

  61. Messens J, Collet J-F (2006) Pathways of disulfide bond formation in Escherichia coli. Int J Biochem Cell Biol 38(7):1050–1062. https://doi.org/10.1016/j.biocel.2005.12.011

    Article  CAS  PubMed  Google Scholar 

  62. Meunier C, Tirard C, Hurtrez-Boussès S, Durand P, Bargues M, Mas-Coma S, Renaud F (2001) Lack of molluscan host diversity and the transmission of an emerging parasitic disease in Bolivia. Mol Ecol 10(5):1333–1340. https://doi.org/10.1046/j.1365-294X.2001.01284.x

    Article  CAS  PubMed  Google Scholar 

  63. Mezo M, González-Warleta M, Carro C, Ubeira FM (2004) An ultrasensitive capture ELISA for detection of Fasciola hepatica coproantigens in sheep and cattle using a new monoclonal antibody (MM3). J Parasitol 90(4):845–852. https://doi.org/10.1645/GE-192R

    Article  PubMed  Google Scholar 

  64. Mirzadeh A, Saadatnia G, Golkar M, Babaie J, Noordin R (2017) Production of refolded Toxoplasma gondii recombinant SAG1-related sequence 3 (SRS3) and its use for serodiagnosis of human toxoplasmosis. Protein Expr Purif 133:66–74. https://doi.org/10.1016/j.pep.2017.03.001

    Article  CAS  PubMed  Google Scholar 

  65. Mirzadeh A, Valadkhani Z, Yoosefy A, Babaie J, Golkar M, Rastaghi ARE, Ashrafi K (2017) Expression, purification and in vitro refolding of the recombinant truncated Saposin-like protein 2 antigen for development of diagnosis of human fascioliasis. Acta Trop 171:163–171. https://doi.org/10.1016/j.actatropica.2017.03.002

    Article  CAS  PubMed  Google Scholar 

  66. Mirzadeh A, Yoosefy A, Kazemirad E, Barati Z, Golkar M, Babaie J, Valadkhani Z (2018) Evaluation of a set of refolded recombinant antigens for serodiagnosis of human fascioliasis. PLoS ONE 13(10):e0203490. https://doi.org/10.1371/journal.pone.0203490

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Mokhtarian K, Akhlaghi L, Meamar AR, Razmjou E, Naeini KM, Gholami S, Falak R (2016) Serodiagnosis of fasciolosis by fast protein liquid chromatography-fractionated excretory/secretory antigens. Parasitol Res 115(8):2957–2965. https://doi.org/10.1007/s00436-016-5049-7

    Article  PubMed  Google Scholar 

  68. Mokhtarian K, Akhlaghi L, Mohammadi M, Meamar AR, Razmjou E, Khoshmirsafa M, Falak R (2016) Evaluation of anti-Cathepsin L1: a more reliable method for serodiagnosis of human fasciolosis. Trans R Soc Trop Med Hyg 110(9):542–550. https://doi.org/10.1093/trstmh/trw063

    Article  CAS  PubMed  Google Scholar 

  69. Morales A, Espino AM (2012) Evaluation and characterization of Fasciola hepatica tegument extract for serodiagnosis of human fascioliasis. Clin Vaccine Immunol 19:1870–1878. https://doi.org/10.1016/S0304-4017(96)01131-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Muro A, Ramajo V, López J, Simón F, Hillyer GV (1997) Fasciola hepatica: vaccination of rabbits with native and recombinant antigens related to fatty acid binding proteins. Vet Parasitol 69(3–4):219–229. https://doi.org/10.1016/S0304-4017(96)01131-4

    Article  CAS  PubMed  Google Scholar 

  71. Nguyen T, Le T, De N, Doan T, Dao T, Vercruysse J, Dorny P (2010) Assessment of a 27-kDa antigen in enzyme-linked immunosorbent assay for the diagnosis of fasciolosis in vietnamese patients. Trop Med Int Health 15(4):462–467. https://doi.org/10.1111/j.1365-3156.2010.02468.x

    Article  CAS  PubMed  Google Scholar 

  72. Nyindo M, Lukambagire A-H (2015) Fascioliasis: an ongoing zoonotic trematode infection. BioMed Res Int. https://doi.org/10.1155/2015/786195

    Article  PubMed  PubMed Central  Google Scholar 

  73. O’Neill SM, Parkinson M, Dowd AJ, Strauss W, Angles R, Dalton JP (1999) Immunodiagnosis of human fascioliasis using recombinant Fasciola hepatica cathepsin L1 cysteine proteinase. Am J Trop Med Hyg 60(5):749–751. https://doi.org/10.4269/ajtmh.1999.60.749

    Article  CAS  PubMed  Google Scholar 

  74. O’Neill SM, Parkinson M, Strauss W, Angles R, Dalton JP (1998) Immunodiagnosis of Fasciola hepatica infection (fascioliasis) in a human population in the Bolivian Altiplano using purified cathepsin L cysteine proteinase. Am J Trop Med Hyg 58(4):417–423. https://doi.org/10.4269/ajtmh.1998.58.417

    Article  CAS  PubMed  Google Scholar 

  75. World Health Organization (2005) The selection and use of essential medicines: report of the WHO expert committee, 2005 (including the 14th model list of essential medicines). World Health Organization, Geneva (ISBN: 9789241209502)

    Google Scholar 

  76. Patil NA, Tailhades J, Hughes RA, Separovic F, Wade JD, Hossain MA (2015) Cellular disulfide bond formation in bioactive peptides and proteins. Int J Mol Sci 16(1):1791–1805. https://doi.org/10.3390/ijms16011791

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Robinson MW, Dalton JP (2009) Zoonotic helminth infections with particular emphasis on fasciolosis and other trematodiases. Philos Trans R Soc Lond 364(1530):2763–2776. https://doi.org/10.1098/rstb.2009.0089

    Article  Google Scholar 

  78. Rodríguez-Pérez J, Rodrǵuez-Medina J, García-Blanco MA, Hillyer GV (1992) Fasciola hepatica: molecular cloning, nucleotide sequence, and expression of a gene encoding a polypeptide homologous to a Schistosoma mansoni fatty acid-binding protein. Exp Parasitol 74(4):400–407. https://doi.org/10.1016/0014-4894(92)90202-L

    Article  PubMed  Google Scholar 

  79. Rokni MB, Massoud J, O’Neill SM, Parkinson M, Dalton JP (2002) Diagnosis of human fasciolosis in the Gilan province of Northern Iran: application of cathepsin L-ELISA. Diagn Microbiol Infect Dis 44(2):175–179. https://doi.org/10.1016/S0732-8893(02)00431-5

    Article  CAS  PubMed  Google Scholar 

  80. Rosano GL, Ceccarelli EA (2014) Recombinant protein expression in Escherichia coli: advances and challenges. Front Microbiol 5:172. https://doi.org/10.3389/fmicb.2014.00172

    Article  PubMed  PubMed Central  Google Scholar 

  81. Rudolph R, Lilie H (1996) In vitro folding of inclusion body proteins. FASEB J 10(1):49–56. https://doi.org/10.1096/fasebj.10.1.8566547

    Article  CAS  PubMed  Google Scholar 

  82. Saba R, Korkmaz M, Inan D, Mamikoğlu L, Turhan Ö, Günseren F, Kabaalioğlu A (2004) Human fascioliasis. Elsevier, Amsterdam. https://doi.org/10.1111/j.1469-0691.2004.00820.x

    Book  Google Scholar 

  83. Sabry H, Mohamed S (2007) Diagnosis efficacy of anti-cysteine protease for detection of Fasciola antigen in serum and stool samples. New Egypt J Med 36:163–169

    Google Scholar 

  84. Sahdev S, Khattar SK, Saini KS (2008) Production of active eukaryotic proteins through bacterial expression systems: a review of the existing biotechnology strategies. Mol Cell Biochem 307(1–2):249–264. https://doi.org/10.1007/s11010-007-9603-6

    Article  CAS  PubMed  Google Scholar 

  85. Salimi-Bejestani M, McGarry J, Felstead S, Ortiz P, Akca A, Williams DJ (2005) Development of an antibody-detection ELISA for Fasciola hepatica and its evaluation against a commercially available test. Res Vet Sci 78(2):177–181. https://doi.org/10.1016/j.rvsc.2004.08.005

    Article  CAS  PubMed  Google Scholar 

  86. Santana BG, Dalton JP, Camargo FV, Parkinson M, Ndao M (2013) The diagnosis of human fascioliasis by enzyme-linked immunosorbent assay (ELISA) using recombinant cathepsin L protease. PLoS Negl Trop Dis 7(9):e2414. https://doi.org/10.1371/journal.pntd.0002414

    Article  Google Scholar 

  87. Sarkari B, Khabisi SA (2017) Immunodiagnosis of human fascioliasis: an update of concepts and performances of the serological assays. J Clin Diagn Res 11(6):OE05. https://doi.org/10.7860/JCDR/2017/26066.10086

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Scott JC, Kennedy MW, McManus DP (2000) Molecular and immunological characterisation of a polymorphic cytosolic fatty acid binding protein from the human blood fluke of humans, Schistosoma japonicum 1. Biochim Biophys Acta 1517(1):53–62. https://doi.org/10.1016/S0167-4781(00)00254-2

    Article  CAS  PubMed  Google Scholar 

  89. Shaheen HI, Kamal KA, Farid Z, Mansour N, Boctor FN, Woody JN (1989) Dot-enzyme-linked immunosorbent assay (dot-ELISA) for the rapid diagnosis of human fascioliasis. J Parasitol 75:549–552. https://doi.org/10.2307/3282904

    Article  CAS  PubMed  Google Scholar 

  90. Shin SH, Hsu A, Chastain HM, Cruz LA, Elder ES, Sapp SG, Handali S (2016) Development of two FhSAP2 recombinant-based assays for immunodiagnosis of human chronic fascioliasis. Am J Trop Med Hyg 95(4):852–855. https://doi.org/10.4269/ajtmh.16-0253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Singh A, Upadhyay V, Panda AK (2015) Solubilization and refolding of inclusion body proteins. Insoluble proteins. Springer, Berlin, pp 283–291. https://doi.org/10.1007/978-1-4939-2205-5_15

    Chapter  Google Scholar 

  92. Smooker PM, Hickford DE, Vaiano SA, Spithill TW (1997) Isolation, cloning, and expression of fatty-acid binding proteins from Fasciola gigantica. Exp Parasitol 85(1):86–91. https://doi.org/10.1006/expr.1996.4098

    Article  CAS  PubMed  Google Scholar 

  93. Sobhorn P, Anantavara S, Dangprasert T, Viyanant V, Krailas D, Upatham E, Kusamran T (1998) Fasciola gigantica: studies of the tegument as a basis for the developments of immunodiagnosis and vaccine. Southeast Asian J Trop Med Public Health 29:387–400

    Google Scholar 

  94. Spithill TW, Smooker PM, Bruce D (1999) 15 Fasciola gigantica: epidemiology, control, immunology and molecular biology. Fasciolosis 50(2):465–525

    Google Scholar 

  95. Strauss W, O’Neill SM, Parkinson M, Angles R, Dalton JP (1999) Diagnosis of human fascioliasis: detection of anti-cathepsin L antibodies in blood samples collected on filter paper. Am J Trop Med Hyg 60(5):746–748. https://doi.org/10.4269/ajtmh.1999.60.746

    Article  CAS  PubMed  Google Scholar 

  96. Tantrawatpan C, Maleewong W, Wongkham C, Wongkham S, Intapan P, Nakashima K (2007) Evaluation of immunoglobulin G4 subclass antibody in a peptide-based enzyme-linked immunosorbent assay for the serodiagnosis of human fascioliasis. Parasitology 134(14):2021–2026. https://doi.org/10.1017/S0031182007003435

    Article  CAS  PubMed  Google Scholar 

  97. Tantrawatpan C, Maleewong W, Wongkham C, Wongkham S, Intapan PM, Nakashima K (2005) Serodiagnosis of human fascioliasis by a cystatin capture enzyme-linked immunosorbent assay with recombinant Fasciola gigantica cathepsin L antigen. Am J Trop Med Hyg 72(1):82–86. https://doi.org/10.4269/ajtmh.2005.72.82

    Article  CAS  PubMed  Google Scholar 

  98. Teofanova D, Hristov P, Yoveva A, Radoslavov G (2012) Native and recombinant fatty acid binding protein 3 from Fasciola hepatica as a potential antigen. Biotechnol Biotechnol Equip 26(sup1):60–64. https://doi.org/10.5504/50YRTIMB.2011.0011

    Article  Google Scholar 

  99. Tezer H, Yuksek SK, Parlakay AÖ, Gülhan B, Tavil B, Tunç B (2013) Evaluation of cases with Fasciola hepatica infection: experience in 6 children. Asian Pac j Trop Dis 3(3):211. https://doi.org/10.1016/S2222-1808(13)60043-2

    Article  PubMed Central  Google Scholar 

  100. Timanova-Atanasova A, Jordanova R, Radoslavov G, Deevska G, Bankov I, Barrett J (2004) A native 13-kDa fatty acid binding protein from the liver fluke Fasciola hepatica. Biochimica Biophys Acta (BBA) 1674(2):200–204. https://doi.org/10.1016/j.bbagen.2004.06.018

    Article  CAS  Google Scholar 

  101. Torres D, Espino AM (2006) Mapping of B-cell epitopes on a novel 11.5-kilodalton Fasciola hepatica–Schistosoma mansoni cross-reactive antigen belonging to a member of the F. hepatica saposin-like protein family. Infect Immun 74(8):4932–4938. https://doi.org/10.1128/IAI.00442-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Ubeira FM, Muiño L, Valero MA, Periago MV, Pérez-Crespo I, Mezo M, Cortizo S (2009) MM3-ELISA detection of Fasciola hepatica coproantigens in preserved human stool samples. Am J Trop Med Hyg 81(1):156–162. https://doi.org/10.4269/ajtmh.2009.81.156

    Article  PubMed  Google Scholar 

  103. Vallejo LF, Rinas U (2004) Strategies for the recovery of active proteins through refolding of bacterial inclusion body proteins. Microb Cell Fact 3(1):11. https://doi.org/10.1186/1475-2859-3-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Wongkham C, Tantrawatpan C, Intapan PM, Maleewong W, Wongkham S, Nakashima K (2005) Evaluation of immunoglobulin G subclass antibodies against recombinant Fasciola gigantica cathepsin L1 in an enzyme-linked immunosorbent assay for serodiagnosis of human fasciolosis. Clin Diagn Lab Immunol 12(10):1152–1156. https://doi.org/10.1128/CDLI.12.10.1152-1156.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Wu K, Chen X-G, Li H, Yan H, Yang P-L, Lun Z-R, Zhu X-Q (2009) Diagnosis of human toxoplasmosis by using the recombinant truncated surface antigen 1 of Toxoplasma gondii. Diagn Microbiol Infect Dis 64(3):261–266. https://doi.org/10.1016/j.diagmicrobio.2009.02.009

    Article  CAS  PubMed  Google Scholar 

  106. Yamano K, Goto A, Nakamura-Uchiyama F, Nawa Y, Hada N, Takeda T (2009) Galβ1-6Gal, antigenic epitope which accounts for serological cross-reaction in diagnosis of Echinococcus multilocularis infection. Parasite Immunol 31(8):481–487. https://doi.org/10.1111/j.1365-3024.2009.01129.x

    Article  CAS  PubMed  Google Scholar 

  107. Yoosefy A, Mirzadeh A, Babaie J, Golkar M, Valadkhani Z (2018) High-level expression of recombinant saposin-Like protein-2 of Fasciola hepatica and its single step purification. J Chem Pharmaceut Res 10(4):29–34

    CAS  Google Scholar 

Download references

Acknowledgements

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Author information

Authors and Affiliations

  1. Department of Biochemistry and Molecular Biology, The University of Melbourne, Parkville, VIC, 3010, Australia

    Abolfazl Mirzadeh & Mohammad Hossein Tanipour

  2. Department of Chemical Engineering, South Tehran Branch, Islamic Azad University, 1584743311, Tehran, Iran

    Farid Jafarihaghighi & Mehdi Ardjmand

  3. Department of Medical Parasitology and Mycology, School of Public Health, Tehran University of Medical Sciences, Tehran, Iran

    Elham Kazemirad

  4. Department of Medical Genetics, Faculty of Medicine, Mashhad University of Medical Sciences, Mashhad, Iran

    Shokouh Shahrokhi Sabzevar

Authors
  1. Abolfazl Mirzadeh
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Farid Jafarihaghighi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Elham Kazemirad
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Shokouh Shahrokhi Sabzevar
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mohammad Hossein Tanipour
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Mehdi Ardjmand
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Abolfazl Mirzadeh.

Ethics declarations

Conflict of Interest

The authors declare no potential conflicts of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Mirzadeh, A., Jafarihaghighi, F., Kazemirad, E. et al. Recent Developments in Recombinant Proteins for Diagnosis of Human Fascioliasis. Acta Parasit. 66, 13–25 (2021). https://doi.org/10.1007/s11686-020-00280-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11686-020-00280-5

Keywords

Search

Navigation