Comparative analysis of excretory-secretory antigens of Trichinella spiralis and Trichinella britovi muscle larvae by two-dimensional difference gel electrophoresis and immunoblotting

Proteome Science

Volumn 10, Issue 1, 2012, Pages

  Bien, Justyna ^a   Näreaho, Anu ^b   Varmanen, Pekka ^b   Gozdzik, Katarzyna ^a   Moskwa, Bozena ^a   Cabaj, Wladyslaw ^a   Nyman, Tuula A ^c   Savijoki, Kirsi ^b,c  

^a W STEFA SKI INSTITUTE OF PARASITOLOGY   (Poland)

^b UNIVERSITY OF HELSINKI   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

2 D DIGE; E S; Immunoblotting; Trichinella britovi; Trichinella spiralis

Indexed keywords

5' NUCLEOTIDASE; ANTISERUM; EXCRETORY SECRETORY PROTEIN; GLYCOPROTEIN P43; HELMINTH PROTEIN; P49 PROTEIN; PROTEIN P43; SERINE PROTEINASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; EXPERIMENTAL PIG; FEMALE; IMMUNOBLOTTING; IMMUNOREACTIVITY; LARVA; LIQUID CHROMATOGRAPHY; MOUSE; MUSCLE LARVA; NONHUMAN; PROTEIN ANALYSIS; PROTEIN PROCESSING; PROTEIN PURIFICATION; TANDEM MASS SPECTROMETRY; TRICHINELLA BRITOVI; TRICHINELLA SPIRALIS; TWO DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS;

SUIDAE; TRICHINELLA; TRICHINELLA BRITOVI; TRICHINELLA SPIRALIS;

EID: 84856778357     PISSN: None     EISSN: 14775956     Source Type: Journal    
DOI: 10.1186/1477-5956-10-10     Document Type: Article

References (66)

1. Murrell KD, Lichtenfels RJ, Zarlenga DS, Pozio E. The systematics of Trichinella with a key to species. Vet Parasitol 2000, 93:293-307. 10.1016/S0304-4017(00)00347-2, 11099843.
2. Pozio E, Zarlenga DS. Recent advances on the taxonomy, systematics and epidemiology of Trichinella. Int J Parasitol 2005, 35:1191-1204. 10.1016/j.ijpara.2005.07.012, 16153648.
3. Krivokapich SJ, Prous CL, Gatti GM, Confalonieri V, Molina V, Matarasso H, Guarnera E. Molecular evidence for a novel encapsulated genotype of Trichinella from Patagonia, Argentina. Vet Parasitol 2008, 156:234-240. 10.1016/j.vetpar.2008.06.003, 18650017.
4. Nowosad P, Pozio E. First report of Trichinella britovi in wildlife from Poland. Acta Parasitologica 1998, 43:236-237.
5. Cabaj W, Pozio E, Moskwa B, Malczewski A. Trichinella britovi and T. spiralis in red foxes (Vulpes vulpes) in Poland. Acta Parasitologica 2000, 45:340-344.
6. Pozio E. Trichinellosis in the European Union: epidemiology, ecology and economic impact. Parasitol Today 1998, 14:35-38. 10.1016/S0169-4758(97)01165-4, 17040688.
7. Dupouy-Camet J. Trichinellosis: a worldwide zoonosis. Vet Parasitol 2000, 93:191-200. 10.1016/S0304-4017(00)00341-1, 11099837.
8. Carnieri I, Ancelle T, Dupouy-Camet J, Pozio E. Different aetiological agents cause the European outbreaks of horsemeat induced human trichinellosis. Trichinellosis 1998, 387-391. Madrid: Consejo Superior de Investigaciones Cientificas, Spain Publishing, Tanner CE, Martinez-Fernandez AR, Bolas-Fernandez F.
9. Ainsworth R, Andrew JRL, Abernethy D. Trichinella pseudospiralis the first human case. Trichinellosis 1994, 461-465. Rome: Istituto Superiore di Saitá, Italia Publishing, Cambell W, Pozio E, Bruschi F.
10. Gomez-Garcia V, Hernandez-Quero J, Rodrguez-Osorio M. Short report: Human infection with Trichinella britovi in Granada, Spain. Am J Trop Med Hyg 2003, 68:463-464.
11. Gari-Toussaint M, Tieulié N, Baldin JL, Dupouy-Camet J, Delaunay P, Fuzibet JG, Le Fichoux Y, Pozio E, Marty P. Human trichinellosis due to Trichinella britovi in southern France after consumption of frozen wild boar meat. Eurosurveillance 2005, 10:550.
12. Boireau P, Vallee I, Roman T, Perret C, Mingyuan L, Gamble HR, Gajadhar A. Trichinella in horses: a low frequency infection with high human risk. Vet Parasitol 2000, 93:309-320. 10.1016/S0304-4017(00)00348-4, 11099844.
13. Pozio E, Serrano FJ, La Rosa G, Reina D, Perez-Martin E, Navarrete I. Evidence of potential gene flow in Trichinella spiralis and in Trichinella britovi in nature. J Parasitol 1997, 83:163-166.
14. Kapel CM, Oivanen L, La Rosa G, Mikkonen T, Pozio E. Evaluation of two PCR-based techniques for molecular epidemiology in Finland, a high-endemic area with four sympatric Trichinella species. Parasite 2001, 8:39-43.
15. Cabaj W, Moskwa B, Pastusiak K, Bień J. Distribution of Trichinella species in Poland. Kosm Probl Nauk Biologicznych 2005, 54:95-103.
16. Rodríguez E, Olmedo J, Ubeira FM, Blanco C, Gárate T. Mixed infection, Trichinella spiralis and Trichinella britovi, in a wild boar hunted in the Province of Cáceres (Spain). Exp Parasitol 2008, 119:430-432. 10.1016/j.exppara.2008.03.017, 18466901.
17. Liciardi M, Marucci G, Addis G, Ludovisi A, Gomez Morales MA, Deiana B, Cabaj W, Pozio E. Trichinella britovi and Trichinella spiralis mixed infection in a horse from Poland. Vet Parasitol 2009, 161:345-348. 10.1016/j.vetpar.2009.01.013, 19217211.
18. Cabaj W, Moskwa B, Pastusiak K, Malczewski A. Trichinellosis in wild animals and domestic pigs in Poland. Med Weter 2004, 60:80-83.
19. Despommier DD. Biology. Trichinella and trichinosis 1983, 75-151. New York: Plenum Press, Campbell WC.
20. Mitreva M, Jasmer DP. Biology and genome of Trichinella spiralis. WormBook 2006, 23:1-21.
21. Bruschi F, Murrell KD. New aspects of human trichinellosis: the impact of new Trichinella species. Postgrad Med J 2002, 78:15-22. 10.1136/pmj.78.915.15, 1742236, 11796866.
22. Pozio E, Varese P, Morales MA, Croppo GP, Pelliccia D, Bruschi F. Comparison of human trichinellosis caused by Trichinella spiralis and by Trichinella britovi. Am J Trop Med Hyg 1993, 48:568-575.
23. Dupouy-Camet J, Paugam A, De Pinieux G, Lavarde V, Vieillefond A. Trichinella murrelli: pathological features in human muscles at different delays after infection. Parasite 2001, 8:S176-S179.
24. Jongwutiwes S, Chantachum N, Kraivichian P, Siriyasatien P, Putaporntip C, Tamburrini A, La Rosa G, Sreesunpasirikul C, Yingyourd P, Pozio E. First outbreak of human trichinellosis caused by Trichinella pseudospiralis. Clin Infect Dis 1998, 26:111-115. 10.1086/516278, 9455518.
25. Ranque S, Faugère B, Pozio E, La Rosa G, Tamburrini A, Pellissier JF, Brouqui P. Trichinella pseudospiralis outbreak in France. Emerg Infect Dis 2000, 6:543-547. 10.3201/eid0605.000517, 2627956, 10998388.
26. Gamble HR, Anderson WR, Graham CE, Murrel KD. Diagnosis of swine trichinosis by enzyme-linked immunosorbent assay (ELISA) using an excretory-secretory antigen. Vet Parasitol 1983, 13:349-361. 10.1016/0304-4017(83)90051-1, 6686388.
27. Su X, Prestwood AK, McGraw RA. Cloning and expression of complementary DNA encoding an antigen of Trichinella spiralis. Mol Biochem Parasitol 1991, 77:76-82.
28. Sofronic-Milosavljevic L, Pozio E, Patrascu IV, Skerovic N, Gomez Morales MA, Gamble HR. Immunodiagnosis of Trichinella infection in the horse. Parasite 2001, 8:260-262.
29. Yera H, Andiva S, Perret C, Limonne D, Boireau P, Dupouy-Camet J. Development and evaluation of a Western blot kit for diagnosis of human trichinellosis. Clin Diagn Lab Immunol 2003, 10:793-796. 193884, 12965906.
30. Gamble HR, Pozio E, Bruschi F, Nöckler K, Kapel CM, Gajadhar AA. International Commission on Trichinellosis: recommendations on the use of serological tests for the detection of Trichinella infection in animals and man. Parasite 2004, 11:3-13.
31. Mitreva M, Jasmer DP, Zarlenga DS, Wang Z, Abubucker S, Martin J, Taylor CM, Yin Y, Fulton L, Minx P, et al. The draft genome of the parasitic nematode Trichinella spiralis. Nat Genet 2011, 43:228-235. 10.1038/ng.769, 3057868, 21336279.
32. Lilley KS, Razzaq A, Dupree P. Two-dimensional gel electrophoresis: recent advances in sample preparation, detection and quantitation. Curr Opin Chem Biol 2002, 6:46-50. 10.1016/S1367-5931(01)00275-7, 11827822.
33. Westermeier R, Marouga R. Protein detection methods in proteomics research. Biosci Rep 2005, 25:19-32. 10.1007/s10540-005-2845-1, 16222417.
34. Viswanathan S, Unlü M, Minden JS. Two-dimensional difference gel electrophoresis. Nat Protoc 2006, 1:1351-1358. 10.1038/nprot.2006.234, 17406422.
35. Dea-Ayuela MA, Bolas-Fernandez F. Two-dimensional electrophoresis and mass spectrometry for the identification of species-specific Trichinella antigens. Vet Parasitol 2005, 132:43-49. 10.1016/j.vetpar.2005.05.018, 15994008.
36. Robinson MW, Connolly B. Proteomic analysis of the excretory-secretory proteins of the Trichinella spiralis L1 larva, a nematode parasite of skeletal muscle. Proteomics 2005, 5:4525-4532. 10.1002/pmic.200402057, 16220533.
37. Robinson MW, Gare DC, Connolly B. Profiling excretory-secretory proteins of Trichinella spiralis muscle larvae by two dimensional gel electrophoresis and mass spectrometry. Vet Parasitol 2005, 132:37-41. 10.1016/j.vetpar.2005.05.019, 15992999.
38. Näreaho A, Ravanko K, Hölttä E, Sukura A. Comparative analysis of Trichinella spiralis and Trichinella nativa proteins by two-dimensional gel electrophoresis. Parasitol Res 2006, 98:349-354. 10.1007/s00436-005-0086-7, 16380837.
39. Robinson MW, Greig R, Beattie KA, Lamont DJ, Connolly B. Comparative analysis of the excretory-secretory proteome of the muscle larva of Trichinella pseudospiralis and Trichinella spiralis. Int J Parasitol 2007, 37:139-148. 10.1016/j.ijpara.2006.08.007, 17007860.
40. Cabaj W, Przyjałkowski Z. Biological characteristics of Trichinella spiralis and T. pseudospiralis infections in mice. Acta Parasitologica Polonica 1987, 32:195-204.
41. Gamble HR, Bessonov AS, Cuperlovic K, Gajadhar AA, van Knapen F, Nöeckler K, Schenone H, Zhu X. International Commission on Trichinellosis: recommendations on methods for the control of Trichinella in domestic and wild animals intended for human consumption. Vet Parasitol 2000, 93:393-408. 10.1016/S0304-4017(00)00354-X, 11099850.
42. O'Connell KL, Stultus JT. Identification of mouse liver proteins on two-dimensional electrophoresis gels by matrix-assisted laser desorption/ionization mass spectrometry of in situ enzymatic digests. Electrophoresis 1997, 18:349-359. 10.1002/elps.1150180309, 9150913.
43. Shevchenko A, Wilm M, Vorm O, Mann M. Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Analitical Chem 1996, 68:850-858.
44. Koskenniemi K, Koponen J, Kankainen M, Savijoki K, Tynkkynen S, de Vos WM, Kalkkinen N, Varmanen P. Proteome analysis of Lactobacillus rhamnosus GG using 2-D DIGE and mass spectrometry shows differential protein production in laboratory and industrial-type growth media. J Proteome Res 2009, 8:4993-5007. 10.1021/pr9003823, 19780546.
45. Gounaris K, Selkirk ME, Sadeghi SJ. A nucleotidase with unique catalytic properties is secreted by Trichinella spiralis. Mol Biochem Parasitol 2004, 136:257-264. 10.1016/j.molbiopara.2004.04.008, 15478804.
46. Wisnewski N, McNeil M, Grieve RB, Wassom DL. Characterization of novel fucosyl- and tyvelosyl-containing glycoconjugates from Trichinella spiralis muscle stage larvae. Mol Biochem Parasitol 1993, 61:25-35. 10.1016/0166-6851(93)90155-Q, 8259130.
47. Yan Y, Tong GZ, Lu JL. Cloning of two structural genes encoding specific proteins in ES antigen from Trichinella spiralis muscle larvae and their high level expression in E. coli and yeast. Chin J of Vet Sci 1997, 17:581-588.
48. Denkers EY, Wassom DL, Hayes CE. Characterization of Trichinella spiralis antigens sharing an immunodominant, carbohydrate-associated determinant distinct from phosphorylcholine. Mol Biochem Parasitol 1990, 41:241-249. 10.1016/0166-6851(90)90187-Q, 1697936.
49. Baek WO, Vijayalakshmi MA. Effect of chemical glycosylation of RNase A on the protein stability and surface histidines accessibility in immobilized metal ion affinity electrophoresis (IMAGE) system. Biochim Biophys Acta 1997, 1336:394-402. 10.1016/S0304-4165(97)00050-0, 9367166.
50. Romaris F, North SJ, Gagliardo LF, Butcher BA, Ghosh K, Beiting DP, Panico M, Arasu P, Dell A, Morris HR, Appleton JA. A putative serine protease among excretory-secretory glycoproteins of L1 Trichinella spiralis. Mol Biochem Parasitol 2002, 122:149-160. 10.1016/S0166-6851(02)00094-4, 12106869.
51. Robinson MW, Massie DH, Connolly B. Secretion and processing of a novel multi-domain cystatin-like protein by intracellular stages of Trichinella spiralis. Mol Biochem Parasitol 2007, 151:9-17. 10.1016/j.molbiopara.2006.09.008, 17081632.
52. Dubin G. Proteinaceous cystein protease inhibitors. Cell Mol Life Sci 2005, 62:653-669. 10.1007/s00018-004-4445-9, 15770418.
53. Wu Z, Nagano I, Takahashi Y. A panel of antigens of muscle larvae of Trichinella spiralis and T. pseudospiralis as revealed by two-dimensional Western blot and immunoelectron microscopy. Parasitology 1999, 118:615-622. 10.1017/S0031182099004187, 10406040.
54. Dea-Ayuela MA, Bolase-Fernandez F. Dynamics of the IgG3 responses following immunisation of BALB/c mice with somatic and excretory/secretory antigens from various Trichinella species. Folia Parasitol (Praha) 2000, 47:172-180.
55. Mcvay CS, Tsung A, Appleton J. Participation of parasite surface glycoproteins in antibody-mediated protection of epithelial cells against Trichinella spiralis. Infect Immun 1998, 66:1941-1945. 108147, 9573073.
56. Vassilatis DK, Polvere RI, Despommier DD, Goold AM, Van der Ploeg LH. Developmental expression of a 43-kDa secreted glycoprotein from Trichinella spiralis. Mol Biochem Parasitol 1996, 78:13-23. 10.1016/S0166-6851(96)02595-9, 8813673.
57. Appleton JA, Schain LR, McGregor DD. Rapid expulsion of Trichinella spiralis in suckling rats: mediation by monoclonal antibodies. Immunology 1988, 65:487-492. 1385491, 3209237.
58. Yao C, Jasmer DP. Nuclear antigens in Trichinella spiralis infected muscle cells: nuclear extraction, compartmentalization, and complex formation. Mol Biochem Parasitol 1998, 92:207-218. 10.1016/S0166-6851(97)00199-0, 9657326.
59. McVay CS, Bracken P, Gagliardo LF, Appleton J. Antibodies to tyvelose exhibit multiple modes of interference with the epithelial niche of Trichinella spiralis. Infect Immun 2000, 68:1912-1918. 10.1128/IAI.68.4.1912-1918.2000, 97366, 10722582.
60. Appleton JA, Bell RGM, Homan W, van Knapen F. Consensus on Trichinella spiralis antigens and antibody. Parasitol Today 1991, 7:190-192.
61. Pompa-Mera EN, Yepez-Mulia L, Ocana-Mondragon A, Garcia-Zepeda EA, Ortega-Pierres G, Gonzalez-Bonilla CR. Trichinella spiralis: Intranasal immunization with attenuated Salmonella enterica a gp43 antigen-derived 30mer epitope elicits protection in BALB/c mice. Exp Parasitol 2011, 129:393-401. 10.1016/j.exppara.2011.08.013, 21907709.
62. Gounaris K. Nucleotidase cascades are catalyzed by secreted proteins of the parasitic nematode Trichinella spiralis. Infect Immun 2002, 70:4917-4924. 10.1128/IAI.70.9.4917-4924.2002, 128271, 12183537.
63. Liu MY, Wang XL, Fu BQ, Li CY, Wu XP, Rhun D, Chen XJ, Boireau P. Identification of stage-specifically expressed genes of Trichinella spiralis by suppression subtractive hybridization. Parasitology 2007, 135:77-83.
64. Todorova VK, Stoyanov DI. Partial characterization of serine proteinases secreted by adult Trichinella spiralis. Parasitol Res 2000, 86:684-687. 10.1007/PL00008552, 10952270.
65. Bioreau P, Vayssier M, Fabien JF, Perret C, Calamel M, Soulé C. Characterization of eleven antigenic groups in Trichinella genus and identification of stage and species markers. Parasitology 1997, 115:641-651. 10.1017/S0031182097001716, 9488876.
66. Ortega-Pierres MG, Yepez-Mulia L, Homan W, Gamble HR, Lim PL, Takahashi Y, Wassom DI, Appleton JA. Workshop on a detailed characterization of Trichinella spiralis antigens: a platform for future studies on antigens and antibodies to this parasite. Parasite Immunol 1996, 18:273-284. 10.1046/j.1365-3024.1996.d01-103.x, 9229380.