A proteomic approach to investigate the distribution and abundance of surface and internal fasciola hepatica proteins during the chronic stage of natural liver fluke infection in cattle

Journal of Proteome Research

Volumn 11, Issue 7, 2012, Pages 3592-3604

  Haçariz, Orçun ^a   Sayers, Gearóid ^b   Baykal, Ahmet Tarik ^a  

^a MATERIALS INSTITUTE   (Turkey)

^b UNIVERSITY COLLEGE DUBLIN   (Ireland)

Author keywords

AKT interacting protein; Fasciola hepatica; integrin beta 7; label free proteomics; sterol O acyltransferase 2; surface protein fraction

Indexed keywords

BETA7 INTEGRIN; CELL SURFACE PROTEIN; PROTEIN KINASE B; STEROL O ACYLTRANSFERASE 2; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CATTLE; CELL MEMBRANE; CONTROLLED STUDY; DRUG TARGETING; ELECTROSPRAY; FASCIOLA HEPATICA; FASCIOLIASIS; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; INTEGUMENT; INTERNAL PROTEIN FRACTION; MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEOMICS; SEQUENCE HOMOLOGY; SURFACE PROTEIN FRACTION; ULTRA PERFORMANCE LIQUID CHROMATOGRAPHY; XENOPUS TROPICALIS;

ANIMALS; CATTLE; CATTLE DISEASES; CHRONIC DISEASE; FASCIOLA HEPATICA; FASCIOLIASIS; GIANT CELLS; HELMINTH PROTEINS; PROTEOME; PROTEOMICS;

BOS; FASCIOLA HEPATICA; HOMO SAPIENS; MUS MUSCULUS; TREMATODA; VERMES; XENOPUS TROPICALIS;

EID: 84863623138     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr300015p     Document Type: Article

References (71)

1. Mas-Coma, S. Epidemiology of fascioliasis in human endemic areas J. Helminthol. 2005, 79 (3) 207-216 (Pubitemid 41192534)
2. Piedrafita, D.; Spithill, T. W.; Smith, R. E.; Raadsma, H. W. Improving animal and human health through understanding liver fluke immunology Parasite Immunol. 2010, 32 (8) 572-581
3. Moll, L.; Gaasenbeek, C. P.; Vellema, P.; Borgsteede, F. H. Resistance of Fasciola hepatica against triclabendazole in cattle and sheep in The netherlands Vet. Parasitol. 2000, 91 (1-2) 153-158 (Pubitemid 30411964)
4. Alvarez-Sánchez, M. A.; Mainar-Jaime, R. C.; Pérez- García, J.; Rojo-Vázquez, F. A. Resistance of Fasciola hepatica to triclabendazole and albendazole in sheep in Spain Vet. Rec. 2006, 159 (13) 424-425 (Pubitemid 44489768)
5. McGonigle, L.; Mousley, A.; Marks, N. J.; Brennan, G. P.; Dalton, J. P.; Spithill, T. W.; Day, T. A.; Maule, A. G. The silencing of cysteine proteases in Fasciola hepatica newly excysted juveniles using RNA interference reduces gut penetration Int. J. Parasitol. 2008, 38 (2) 149-155 (Pubitemid 350266652)
6. Robinson, M. W.; Menon, R.; Donnelly, S. M.; Dalton, J. P.; Ranganathan, S. An integrated transcriptomics and proteomics analysis of the secretome of the helminth pathogen Fasciola hepatica: Proteins associated with invasion and infection of the mammalian host Mol. Cell. Proteomics 2009, 8 (8) 1891-1907
7. Hernández-González, A.; Valero, M. L.; del Pino, M. S.; Oleaga, A.; Siles-Lucas, M. Proteomic analysis of in vitro newly excysted juveniles from Fasciola hepatica Mol. Biochem. Parasitol. 2010, 172 (2) 121-128
8. Young, N. D.; Hall, R. S.; Jex, A. R.; Cantacessi, C.; Gasser, R. B. Elucidating the transcriptome of Fasciola hepatica -a key to fundamental and biotechnological discoveries for a neglected parasite Biotechnol. Adv. 2010, 28 (2) 222-231
9. Moxon, J. V.; LaCourse, E. J.; Wright, H. A.; Perally, S.; Prescott, M. C.; Gillard, J. L.; Barrett, J.; Hamilton, J. V.; Brophy, P. M. Proteomic analysis of embryonic Fasciola hepatica: Characterization and antigenic potential of a developmentally regulated heat shock protein Vet. Parasitol. 2010, 169 (1-2) 62-75
10. Cancela, M.; Ruétalo, N.; Dell'Oca, N.; da Silva, E.; Smircich, P.; Rinaldi, G.; Roche, L.; Carmona, C.; Alvarez-Valín, F.; Zaha, A.; Tort, J. F. Survey of transcripts expressed by the invasive juvenile stage of the liver fluke Fasciola hepatica BMC Genomics 2010, 11, 227
11. Wilson, R. A.; Wright, J. M.; de Castro-Borges, W.; Parker-Manuel, S. J.; Dowle, A. A.; Ashton, P. D.; Young, N. D.; Gasser, R. B.; Spithill, T. W. Exploring the Fasciola hepatica tegument proteome Int. J. Parasitol. 2011, 41 (13-14) 1347-1359
12. Chemale, G.; Perally, S.; LaCourse, E. J.; Prescott, M. C.; Jones, L. M.; Ward, D.; Meaney, M.; Hoey, E.; Brennan, G. P.; Fairweather, I.; Trudgett, A.; Brophy, P. M. Comparative proteomic analysis of triclabendazole response in the liver fluke Fasciola hepatica J. Proteome Res. 2010, 9 (10) 4940-4951
13. Korf, I.; Yandell, M.; Bedell, J. A. BLAST Protocols. In BLAST-An Essential Guide to the Basic Local Alignment Search tool, 1 st ed.; O'Reilly and Associates, Inc: Sebastopol, CA, 2003; pp 152-155.
14. Young, N. D.; Jex, A. R.; Cantacessi, C.; Hall, R. S.; Campbell, B. E.; Spithill, T. W.; Tangkawattana, S.; Tangkawattana, P.; Laha, T.; Gasser, R. B. A portrait of the transcriptome of the neglected trematode, Fasciola gigantica -biological and biotechnological implications PLoS Neglected Trop. Dis. 2011, 5 (2) e1004
15. Jefferies, J. R.; Campbell, A. M.; van Rossum, A. J.; Barrett, J.; Brophy, P. M. Proteomic analysis of Fasciola hepatica excretory-secretory products Proteomics 2001, 1 (9) 1128-1132 (Pubitemid 33696478)
16. Morphew, R. M.; Wright, H. A.; LaCourse, E. J.; Woods, D. J.; Brophy, P. M. Comparative proteomics of excretory-secretory proteins released by the liver fluke Fasciola hepatica in sheep host bile and during in vitro culture ex host Mol. Cell. Proteomics 2007, 6 (6) 963-972 (Pubitemid 47019398)
17. Robinson, M. W.; Tort, J. F.; Lowther, J.; Donnelly, S. M.; Wong, E.; Xu, W.; Stack, C. M.; Padula, M.; Herbert, B.; Dalton, J. P. Proteomics and phylogenetic analysis of the cathepsin L protease family of the helminth pathogen Fasciola hepatica: Expansion of a repertoire of virulence-associated factors Mol. Cell. Proteomics 2008, 7 (6) 1111-1123 (Pubitemid 351943958)
18. Gourbal, B. E.; Guillou, F.; Mitta, G.; Sibille, P.; Thèron, A.; Pointier, J. P.; Coustau, C. Excretory-secretory products of larval Fasciola hepatica investigated using a two-dimensional proteomic approach Mol. Biochem. Parasitol. 2008, 161 (1) 63-66
19. Spithill, T. W.; Dalton, J. P. Progress in development of liver fluke vaccines Parasitol. Today 1998, 14 (6) 224-228 (Pubitemid 28240078)
20. Dalton, J. P.; Mulcahy, G. Parasite vaccines-a reality? Vet. Parasitol. 2001, 98 (1-3) 149-167
21. Robinson, M. W.; McFerran, N.; Trudgett, A.; Hoey, L.; Fairweather, I. A possible model of benzimidazole binding to beta-tubulin disclosed by invoking an inter-domain movement J. Mol. Graph. Model. 2004, 23 (3) 275-284 (Pubitemid 39463106)
22. Chambers, E.; Ryan, L. A.; Hoey, E. M.; Trudgett, A.; McFerran, N. V.; Fairweather, I.; Timson, D. J. Liver fluke β-tubulin isotype 2 binds albendazole and is thus a probable target of this drug Parasitol. Res. 2010, 107 (5) 1257-1264
23. Robinson, M. W.; Trudgett, A.; Hoey, E. M.; Fairweather, I. Triclabendazole-resistant Fasciola hepatica: Beta-tubulin and response to in vitro treatment with triclabendazole Parasitology 2002, 124 (Pt 3) 325-338 (Pubitemid 34250745)
24. Threadgold, L. T. The tegument and associated structures of Fasciola hepatic a Q. J. Microsc. Sci. 1963, 104 (Pt 4) 505-512
25. Hillyer, G. V. Isolation of Fasciola hepatica tegument antigens J. Clin. Microbiol. 1980, 12 (5) 695-699 (Pubitemid 10025061)
26. Brown, W. C.; Davis, W. C.; Dobbelaere, D. A.; Rice-Ficht, A. C. CD4+ T-cell clones obtained from cattle chronically infected with Fasciola hepatica and specific for adult worm antigen express both unrestricted and Th2 cytokine profiles Infect. Immun. 1994, 62 (3) 818-827 (Pubitemid 24065560)
27. Flynn, R. J.; Mannion, C.; Golden, O.; Hacariz, O.; Mulcahy, G. Experimental Fasciola hepatica infection alters responses to tests used for diagnosis of bovine tuberculosis Infect. Immun. 2007, 75 (3) 1373-1381 (Pubitemid 46385831)
28. Haçariz, O.; Sayers, G.; Flynn, R. J.; Lejeune, A.; Mulcahy, G. IL-10 and TGF-beta1 are associated with variations in fluke burdens following experimental fasciolosis in sheep Parasite Immunol. 2009, 31 (10) 613-622
29. Haçariz, O.; Sayers, G.; McCullough, M.; Garrett, M.; O'Donovan, J.; Mulcahy, G. The effect of Quil A adjuvant on the course of experimental Fasciola hepatica infection in sheep Vaccine 2009, 27 (1) 45-50
30. Jenkins, M. B.; Eaglesham, B. S.; Anthony, L. C.; Kachlany, S. C.; Bowman, D. D.; Ghiorse, W. C. Significance of wall structure, macromolecular composition, and surface polymers to the survival and transport of Cryptosporidium parvum oocysts Appl. Environ. Microbiol. 2010, 76 (6) 1926-1934
31. Haçariz, O.; Sayers, G.; Mulcahy, G. A preliminary study to understand the effect of Fasciola hepatica tegument on naïve macrophages and humoral responses in an ovine model Vet. Immunol. Immunopathol. 2011, 139 (2-4) 245-249
32. Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of proteindye binding Anal. Biochem. 1976, 72, 248-254
33. Marchler-Bauer, A.; Lu, S.; Anderson, J. B.; Chitsaz, F.; Derbyshire, M. K.; DeWeese-Scott, C.; Fong, J. H.; Geer, L. Y.; Geer, R. C.; Gonzales, N. R.; Gwadz, M.; Hurwitz, D. I.; Jackson, J. D.; Ke, Z.; Lanczycki, C. J.; Lu, F.; Marchler, G. H.; Mullokandov, M.; Omelchenko, M. V.; Robertson, C. L.; Song, J. S.; Thanki, N.; Yamashita, R. A.; Zhang, D.; Zhang, N.; Zheng, C.; Bryant, S. H. CDD: a Conserved Domain Database for the functional annotation of proteins Nucleic Acids Res. 2011, 39 (Database issue) D225-229
34. Altschul, S. F.; Madden, T. L.; Schäffer, A. A.; Zhang, J.; Zhang, Z.; Miller, W.; Lipman, D. J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs Nucleic Acids Res. 1997, 25 (17) 3389-3402 (Pubitemid 27359211)
35. Logan-Klumpler, F. J.; De Silva, N.; Boehme, U.; Rogers, M. B.; Velarde, G.; McQuillan, J. A.; Carver, T.; Aslett, M.; Olsen, C.; Subramanian, S.; Phan, I.; Farris, C.; Mitra, S.; Ramasamy, G.; Wang, H.; Tivey, A.; Jackson, A.; Houston, R.; Parkhill, J.; Holden, M.; Harb, O. S.; Brunk, B. P.; Myler, P. J.; Roos, D.; Carrington, M.; Smith, D. F.; Hertz-Fowler, C.; Berriman, M. GeneDB - an annotation database for pathogens Nucleic Acids Res. 2012, 40 (Database issue) D98-108
36. Brownridge, P.; Beynon, R. J. The importance of the digest: proteolysis and absolute quantification in proteomics Methods 2011, 54 (4) 351-360
37. Aarnisalo, A. A.; Green, K. M.; O'Malley, J.; Makary, C.; Adams, J.; Merchant, S. N.; Evans, J. E. A method for MS(E) differential proteomic analysis of archival formalin-fixed celloidin-embedded human inner ear tissue Hear. Res. 2010, 270 (1-2) 15-20
38. Hwang, H. H.; Moon, P. G.; Lee, J. E.; Kim, J. G.; Lee, W.; Ryu, S. H.; Baek, M. C. Identification of the target proteins of rosiglitazone in 3T3-L1 adipocytes through proteomic analysis of cytosolic and secreted proteins Mol. Cells 2011, 31 (3) 239-246
39. D'Aguanno, S.; D'Alessandro, A.; Pieroni, L.; Roveri, A.; Zaccarin, M.; Marzano, V.; De Canio, M.; Bernardini, S.; Federici, G.; Urbani, A. New insights into neuroblastoma cisplatin resistance: a comparative proteomic and meta-mining investigation J. Proteome Res. 2011, 10 (2) 416-428
40. Vissers, J. P.; Langridge, J. I.; Aerts, J. M. Analysis and quantification of diagnostic serum markers and protein signatures for Gaucher disease Mol. Cell. Proteomics 2007, 6 (5) 755-766 (Pubitemid 46831929)
41. Cheng, F. Y.; Blackburn, K.; Lin, Y. M.; Goshe, M. B.; Williamson, J. D. Absolute protein quantification by LC/MS(E) for global analysis of salicylic acid-induced plant protein secretion responses J. Proteome Res. 2009, 8 (1) 82-93
42. Silva, J. C.; Gorenstein, M. V.; Li, G. Z.; Vissers, J. P.; Geromanos, S. J. Absolute quantification of proteins by LCMSE: A virtue of parallel MS acquisition Mol. Cell. Proteomics 2006, 5 (1) 144-156 (Pubitemid 43169347)
43. Bostanci, N.; Heywood, W.; Mills, K.; Parkar, M.; Nibali, L.; Donos, N. Application of label-free absolute quantitative proteomics in human gingival crevicular fluid by LC/MS E (gingival exudatome) J. Proteome Res. 2010, 9 (5) 2191-2199
44. Stitt, A. W.; Fairweather, I.; Trudgett, A. G.; Johnston, C. F. Fasciola hepatica: Localization and partial characterization of tubulin Parasitol. Res. 1992, 78 (2) 103-107
45. Ryan, L. A.; Hoey, E.; Trudgett, A.; Fairweather, I.; Fuchs, M.; Robinson, M. W.; Chambers, E.; Timson, D. J.; Ryan, E.; Feltwell, T.; Ivens, A.; Bentley, G.; Johnston, D. Fasciola hepatica expresses multiple alpha- and beta-tubulin isotypes Mol. Biochem. Parasitol. 2008, 159 (1) 73-78 (Pubitemid 351469922)
46. Cancela, M.; Carmona, C.; Rossi, S.; Frangione, B.; Goñi, F.; Berasain, P. Purification, characterization, and immunolocalization of paramyosin from the adult stage of Fasciola hepatica Parasitol. Res. 2004, 92 (6) 441-448 (Pubitemid 38658336)
47. Lee, S. H.; Song, C. Y.; Lee, K. B.; Lee, H. S. Study on the chromosomal proteins of Fasciola hepatica Kisaengchunghak Chapchi. 1978, 16 (1) 26-40 (Pubitemid 9105801)
48. Galindo, M.; Varela, N.; Espinoza, I.; Toro, G. C.; Hellman, U.; Wernstedt, C.; Galanti, N. Chromatin from two classes of platyhelminthes display both protist H1 and higher eukaryote core histones FEBS Lett. 2004, 567 (2-3) 225-229 (Pubitemid 38748396)
49. Vichasri-Grams, S.; Subpipattana, P.; Sobhon, P.; Viyanant, V.; Grams, R. An analysis of the calcium-binding protein 1 of Fasciola gigantica with a comparison to its homologs in the phylum Platyhelminthes Mol. Biochem. Parasitol. 2006, 146 (1) 10-23 (Pubitemid 43132798)
50. Bennaars-Eiden, A.; Higgins, L.; Hertzel, A. V.; Kapphahn, R. J.; Ferrington, D. A.; Bernlohr, D. A. Covalent modification of epithelial fatty acid-binding protein by 4-hydroxynonenal in vitro and in vivo. Evidence for a role in antioxidant biology J. Biol. Chem. 2002, 277 (52) 50693-50702 (Pubitemid 36042231)
51. Muro, A.; Casanueva, P.; López-Abán, J.; Ramajo, V.; Martínez-Fernández, A. R.; Hillyer, G. V. Identification of Fasciola hepatica recombinant 15-kDa fatty acid-binding protein T-cell epitopes that protect against experimental fascioliasis in rabbits and mice J. Parasitol. 2007, 93 (4) 817-823 (Pubitemid 47502193)
52. López-Abán, J.; Casanueva, P.; Nogal, J.; Arias, M.; Morrondo, P.; Diez-Baños, P.; Hillyer, G. V.; Martínez- Fernández, A. R.; Muro, A. Progress in the development of Fasciola hepatica vaccine using recombinant fatty acid binding protein with the adjuvant adaptation system ADAD Vet. Parasitol. 2007, 145 (3-4) 287-296 (Pubitemid 46442774)
53. López-Abán, J.; Nogal-Ruiz, J. J.; Vicente, B.; Morrondo, P.; Diez-Baños, P.; Hillyer, G. V.; Martínez-Fernández, A. R.; Feliciano, A. S.; Muro, A. The addition of a new immunomodulator with the adjuvant adaptation ADAD system using fatty acid binding proteins increases the protection against Fasciola hepatica Vet. Parasitol. 2008, 153 (1-2) 176-181 (Pubitemid 351447308)
54. Mendes, R. E.; Zafra, R.; Pérez-Ecija, R. A.; Buffoni, L.; Martínez-Moreno, A.; Tendler, M.; Pérez, J. Evaluation of local immune response to Fasciola hepatica experimental infection in the liver and hepatic lymph nodes of goats immunized with Sm14 vaccine antigen Mem. Inst. Oswaldo Cruz 2010, 105 (5) 698-705
55. Tendler, M.; Brito, C. A.; Vilar, M. M.; Serra-Freire, N.; Diogo, C. M.; Almeida, M. S.; Delbem, A. C.; Da Silva, J. F.; Savino, W.; Garratt, R. C.; Katz, N.; Simpson, A. S. Schistosoma mansoni fatty acid-binding protein, Sm14, is the potential basis of a dual-purpose anti-helminth vaccine. Proc. Natl. Acad. Sci. USA 1996, 93 (1) 269-273 (Pubitemid 26038141)
56. Oelkers, P.; Behari, A.; Cromley, D.; Billheimer, J. T.; Sturley, S. L. Characterization of two human genes encoding acyl coenzyme A:cholesterol acyltransferase-related enzymes J. Biol. Chem. 1998, 273 (41) 26765-26771 (Pubitemid 28471693)
57. Chang, C. C.; Sakashita, N.; Ornvold, K.; Lee, O.; Chang, E. T.; Dong, R.; Lin, S.; Lee, C. Y.; Strom, S. C.; Kashyap, R.; Fung, J. J.; Farese, R. V., Jr.; Patoiseau, J. F.; Delhon, A.; Chang, T. Y. Immunological quantitation and localization of ACAT-1 and ACAT-2 in human liver and small intestine J. Biol. Chem. 2000, 275 (36) 28083-28092
58. Lundahl, J.; Sehmi, R.; Hayes, L.; Howie, K.; Denburg, J. A. Selective upregulation of a functional beta7 integrin on differentiating eosinophils Allergy 2000, 55 (9) 865-872 (Pubitemid 30643912)
59. Pankov, R.; Yamada, K. M. Fibronectin at a glance J. Cell Sci. 2002, 115 (Pt 20) 3861-3863 (Pubitemid 35256486)
60. To, W. S.; Midwood, K. S. Plasma and cellular fibronectin:distinct and independent functions during tissue repair Fibrogenesis Tissue Repair 2011, 4, 21
61. Marcos, L. A.; Terashima, A.; Yi, P.; Andrade, R.; Cubero, F. J.; Albanis, E.; Gotuzzo, E.; Espinoza, J. R.; Friedman, S. L. Mechanisms of liver fibrosis associated with experimental Fasciola hepatica infection: roles of Fas2 proteinase and hepatic stellate cell activation J. Parasitol. 2011, 97 (1) 82-87
62. Xu, L.; Sowa, M. E.; Chen, J.; Li, X.; Gygi, S. P.; Harper, J. W. An FTS/Hook/p107(FHIP) complex interacts with and promotes endosomal clustering by the homotypic vacuolar protein sorting complex Mol. Cell. Biol. 2008, 19 (12) 5059-5071
63. Remy, I.; Michnick, S. W. Regulation of apoptosis by the Ft1 protein, a new modulator of protein kinase B/Akt Mol. Cell. Biol. 2004, 24 (4) 1493-1504 (Pubitemid 38167073)
64. Andrade, L. F.; Nahum, L. A.; Avelar, L. G.; Silva, L. L.; Zerlotini, A.; Ruiz, J. C.; Oliveira, G. Eukaryotic protein kinases (ePKs) of the helminth parasite Schistosoma mansoni BMC Genomics 2011, 12, 215
65. Stitt, A. W.; Fairweather, I.; Trudgett, A. G.; Johnston, C. F.; Anderson, S. M. Localisation of actin in the liver fluke Fasciola hepatica Parasitol. Res. 1992, 78 (2) 96-102
66. Wright, C.; Edelmann, M.; diGleria, K.; Kollnberger, S.; Kramer, H.; McGowan, S.; McHugh, K.; Taylor, S.; Kessler, B.; Bowness, P. Ankylosing spondylitis monocytes show upregulation of proteins involved in inflammation and the ubiquitin proteasome pathway Ann. Rheum. Dis. 2009, 68 (10) 1626-1632
67. Rosenegger, D.; Wright, C.; Lukowiak, K. A quantitative proteomic analysis of long-term memory Mol. Brain 2010, 3, 9
68. Mannová, P.; Fang, R.; Wang, H.; Deng, B.; McIntosh, M. W.; Hanash, S. M; Beretta, L. Modification of host lipid raft proteome upon hepatitis C virus replication Mol. Cell. Proteomics 2006, 5 (12) 2319-2325 (Pubitemid 46040636)
69. Cockman, M. E.; Webb, J. D.; Kramer, H. B.; Kessler, B. M.; Ratcliffe, P. J. Proteomics-based identification of novel factor inhibiting hypoxia-inducible factor (FIH) substrates indicates widespread asparaginyl hydroxylation of ankyrin repeat domain-containing proteins Mol. Cell. Proteomics 2009, 8 (3) 535-546
70. Stitt, A. W.; Fairweather, I. Fasciola hepatica: The effect of the microfilament inhibitor cytochalasin B on the ultrastructure of the adult fluke Parasitol. Res. 1991, 77 (8) 675-685
71. Braschi, S.; Curwen, R. S.; Ashton, P. D.; Verjovski-Almeida, S.; Wilson, A. The tegument surface membranes of the human blood parasite Schistosoma mansoni: a proteomic analysis after differential extraction Proteomics 2006, 6 (5) 1471-1482