International Journal of Infectious Diseases
Volume 12, Issue 6 , Pages e49-e59 , November 2008

Asparaginyl endopeptidase from the carcinogenic liver fluke, Opisthorchis viverrini, and its potential for serodiagnosis

  • Thewarach Laha

      Affiliations

    • Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, Thailand
    • Corresponding Author InformationCorresponding author. Tel.: +66 43 348 387; fax: +66 43 202475.
    • ,
  • Jittiyawadee Sripa

      Affiliations

    • Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, Thailand
    • ,
  • Banchob Sripa

      Affiliations

    • Department of Pathology, Faculty of Medicine, Khon Kaen University, Khon Kaen, Thailand
    • ,
  • Mark Pearson

      Affiliations

    • Division of Infectious Diseases, Queensland Institute of Medical Research, Brisbane, Queensland, Australia
    • ,
  • Leon Tribolet

      Affiliations

    • Division of Infectious Diseases, Queensland Institute of Medical Research, Brisbane, Queensland, Australia
    • ,
  • Sasithorn Kaewkes

      Affiliations

    • Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, Thailand
    • ,
  • Paiboon Sithithaworn

      Affiliations

    • Department of Parasitology, Faculty of Medicine, Khon Kaen University, Khon Kaen 40002, Thailand
    • ,
  • Paul J. Brindley

      Affiliations

    • Department of Microbiology, Immunology and Tropical Medicine, George Washington University Medical Center, Washington, DC, USA
    • ,
  • Alex Loukas

      Affiliations

    • Division of Infectious Diseases, Queensland Institute of Medical Research, Brisbane, Queensland, Australia

Received 24 January 2008 ,Revised 5 March 2008 ,Accepted 18 March 2008.

References 

  1. Sripa B, Kaewkes S, Sithithaworn P, Mairiang E, Laha T, Smout M, et al. Liver fluke induces cholangiocarcinoma. PLoS Med. 2007;4:e201
  2. Harinasuta T, Riganti M, Bunnag D. Opisthorchis viverrini infection: pathogenesis and clinical features. Arzneimittelforschung. 1984;34:1167–1169
  3. Thamavit W, Bhamarapravati N, Sahaphong S, Vajrasthira S, Angsubhakorn S. Effects of dimethylnitrosamine on induction of cholangiocarcinoma in Opisthorchis viverrini-infected Syrian golden hamsters. Cancer Res. 1978;38:4634–4639
  4. International Agency for Research on Cancer/World Health Organization. IARC monographs on the evaluation of carcinogenic risks to humans. Schistosomes, liver flukes and Helicobacter pylori. Vol. 61. Lyon: IARC; 1994.
  5. Vatanasapt V, Sripa B, Sithithaworn P, Mairiang P. Liver flukes and liver cancer. Cancer Surv. 1999;33:313–343
  6. Haswell-Elkins MR, Sithithaworn P, Elkins D. Opisthorchis viverrini and cholangiocarcinoma in Northeast Thailand. Parasitol Today. 1992;8:86–89
  7. Ohshima H, Bartsch H. Chronic infections and inflammatory processes as cancer risk factors: Possible role of nitric oxide in carcinogenesis. Mutat Res. 1994;305:253–264
  8. Sripa B, Kaewkes S. Gall bladder and extrahepatic bile duct changes in Opisthorchis viverrini-infected hamsters. Acta Trop. 2002;83:29–36
  9. Sripa B, Kaewkes S. Localisation of parasite antigens and inflammatory responses in experimental opisthorchiasis. Int J Parasitol. 2000;30:735–740
  10. Wongratanacheewin S, Bunnag D, Vaeusorn N, Sirisinha S. Characterization of humoral immune response in the serum and bile of patients with opisthorchiasis and its application in immunodiagnosis. Am J Trop Med Hyg. 1988;38:356–362
  11. McKerrow JH, Caffrey C, Kelly B, Loke P, Sajid M. Proteases in parasitic diseases. Annu Rev Pathol. 2006;1:497–536
  12. Dalton JP, Hola-Jamriska L, Brindley PJ. Asparaginyl endopeptidase activity in adult Schistosoma mansoni. Parasitology. 1995;111:575–580
  13. Caffrey CR, Mathieu MA, Gaffney AM, Salter JP, Sajid M, Lucas KD, et al. Identification of a cDNA encoding an active asparaginyl endopeptidase of Schistosoma mansoni and its expression in Pichia pastoris. FEBS Lett. 2000;466:244–248
  14. Tkalcevic J, Ashman K, Meeusen E. Fasciola hepatica: rapid identification of newly excysted juvenile proteins. Biochem Biophys Res Commun. 1995;213:169–174
  15. Adisakwattana P, Viyanant V, Chaicumpa W, Vichasri-Grams S, Hofmann A, Korge G, et al. Comparative molecular analysis of two asparaginyl endopeptidases and encoding genes from Fasciola gigantica. Mol Biochem Parasitol. 2007;156:102–116
  16. Oliver EM, Skuce PJ, McNair CM, Knox DP. Identification and characterization of an asparaginyl proteinase (legumain) from the parasitic nematode, Haemonchus contortus. Parasitology. 2006;133:237–244
  17. Sajid M, McKerrow JH, Hansell E, Mathieu MA, Lucas KD, Hsieh I, et al. Functional expression and characterization of Schistosoma mansoni cathepsin B and its trans-activation by an endogenous asparaginyl endopeptidase. Mol Biochem Parasitol. 2003;131:65–75
  18. Skelly PJ, Krautz-Peterson G. Schistosome asparaginyl endopeptidase (legumain) is not essential for cathepsin B1 activation in vivo. Mol Biochem Parasitol. 2008;159:54–58
  19. Klinkert MQ, Felleisen R, Link G, Ruppel A, Beck E. Primary structures of Sm31/32 diagnostic proteins of Schistosoma mansoni and their identification as proteases. Mol Biochem Parasitol. 1989;33:113–122
  20. Laha T, Pinlaor P, Mulvenna J, Sripa B, Sripa M, Smout MJ, et al. Gene discovery for the carcinogenic human liver fluke, Opisthorchis viverrini. BMC Genomics. 2007;8:e189
  21. Honjo S, Srivatanakul P, Sriplung H, Kikukawa H, Hanai S, Uchida K, et al. Genetic and environmental determinants of risk for cholangiocarcinoma via Opisthorchis viverrini in a densely infested area in Nakhon Phanom, northeast Thailand. Int J Cancer. 2005;117:854–860Erratum: Int J Cancer 2005;117:1066
  22. Hall TA. BioEdit: a user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucleic Acids Symp Ser. 1999;41:1167–1169
  23. Thompson JD, Higgins DG, Gibson TJ. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994;22:4673–4680
  24. Sripa B, Kaewkes S. Relationship between parasite-specific antibody responses and intensity of Opisthorchis viverrini infection in hamsters. Parasite Immunol. 2000;22:139–145
  25. Hara-Nishimura I. Plant legumain, asparaginyl endopeptidase. In:  Barrett AJ,  Rawlings ND,  Woessner JF editor. Handbook of proteolytic enzymes. London: Elsevier; 2004;p. 1310–1313
  26. Brindley PJ, Dalton JP. Schistosome legumain. In:  Barrett AJ,  Rawlings ND,  Woessner JF editor. Handbook of proteolytic enzymes. London: Elsevier; 2004;p. 1305–1310
  27. Chen JM, Rawlings ND, Stevens RA, Barrett AJ. Identification of the active site of legumain links it to caspases, clostripain and gingipains in a new clan of cysteine endopeptidases. FEBS Letters. 1998;441:361–365
  28. Chen JM, Dando PM, Barrett AJ. Mammalian legumain. In:  Barrett AJ,  Rawlings ND,  Woessner JF editor. Handbook of proteolytic enzymes. London: Elsevier; 2004;p. 1302–1305
  29. Götz B, Klinkert MQ. Expression and partial characterization of a cathepsin B-like enzyme (Sm31) and a proposed ‘haemoglobinase’ (Sm32) from Schistosoma mansoni. Biochem J. 1993;290:801–806
  30. Dalton JP, Brindley PJ. Schistosome asparaginyl endopeptidase SM32 in hemoglobin digestion. Parasitol Today. 1996;12:125
  31. Delcroix M, Sajid M, Caffrey CR, Lim KC, Dvorák J, Hsieh I, et al. A multienzyme network functions in intestinal protein digestion by a platyhelminth parasite. J Biol Chem. 2006;281:39316–39329
  32. Sajid M, McKerrow JH. Cysteine proteases of parasitic organisms. Mol Biochem Parasitol. 2002;120:1–21Erratum: Mol Biochem Parasitol 2002;121:159
  33. Choi JH, Lee JH, Yu HS, Jeong HJ, Kim J, Hong YC, et al. Molecular and biochemical characterization of hemoglobinase, a cysteine proteinase, in Paragonimus westermani. Korean J Parasitol. 2006;44:187–196
  34. Skuce PJ, Redmond DL, Liddell S, Stewart EM, Newlands GF, Smith WD, et al. Molecular cloning and characterization of gut-derived cysteine proteinases associated with a host protective extract from Haemonchus contortus. Parasitology. 1999;119:405–412
  35. Sirisinha S, Chawengkirttikul R, Haswell-Elkins MR, Elkins DB, Kaewkes S, Sithithaworn P. Evaluation of a monoclonal antibody-based enzyme linked immunosorbent assay for the diagnosis of Opisthorchis viverrini infection in an endemic area. Am J Trop Med Hyg. 1995;52:521–524
  36. Ruangsittichai J, Viyanant V, Vichasri-Grams S, Sobhon P, Tesana S, Upatham ES, et al. Opisthorchis viverrini: identification of a glycine–tyrosine rich eggshell protein and its potential as a diagnostic tool for human opisthorchiasis. Int J Parasitol. 2006;36:1329–1339
  37. Sakolvaree Y, Ybanez L, Chaicumpa W. Parasites elicited cross-reacting antibodies to Opisthorchis viverrini. Asian Pac J Allergy Immunol. 1997;15:115–122
  38. Akai PS, Pungpak S, Chaicumpa W, Viroj K, Bunnag D, Befus AD. Serum antibody response to Opisthorchis viverrini antigen as a marker for opisthorchiasis-associated cholangiocarcinoma. Trans R Soc Trop Med Hyg. 1994;88:471–474
  39. Verity CK, McManus DP, Brindley PJ. Vaccine efficacy of recombinant cathepsin D aspartic protease from Schistosoma japonicum. Parasite Immunol. 2001;23:153–162
  40. Loukas A, Bethony J, Brooker S, Hotez P. Hookworm vaccines: past, present, and future. Lancet Infect Dis. 2006;6:733–741
  41. Dalton JP, Neill SO, Stack C, Collins P, Walshe A, Sekiya M, et al. Fasciola hepatica cathepsin L-like proteases: biology, function, and potential in the development of first generation liver fluke vaccines. Int J Parasitol. 2003;33:1173–1181
  42. Abdulla MH, Lim KC, Sajid M, McKerrow JH, Caffrey CR. Schistosomiasis mansoni: novel chemotherapy using a cysteine protease inhibitor. PLoS Med. 2007;4:e14
  43. Kaewpitoon N, Laha T, Kaewkes S, Yongvanit P, Brindley PJ, Loukas A, et al. Characterization of cysteine proteases from the carcinogenic liver fluke, Opisthorchis viverrini. Parasitol Res. 2008;102:757–764

PII: S1201-9712(08)01360-X

doi: 10.1016/j.ijid.2008.03.033

International Journal of Infectious Diseases
Volume 12, Issue 6 , Pages e49-e59 , November 2008

Article Tools

* Image Usage & Resolution