Application of proteomics and metabolomics for investigation of food toxins

Food Research International

Volumn 54, Issue 1, 2013, Pages 1042-1051

  Giacometti, Jasminka ^a   Tomljanović, Alena Buretić ^b   Josić, Djuro ^a,c  

^a University of Rijeka   (Croatia)

^b UNIVERSITY OF RIJEKA   (Croatia)

^c BROWN UNIVERSITY   (United States)

Author keywords

Food safety; Marine toxins; Metabolomics; Mycotoxins; Proteomics

Indexed keywords

EXTRACELLULAR ENVIRONMENTS; IDENTIFICATION OF PROTEINS; MARINE TOXINS; METABOLIC PATHWAYS; METABOLOMICS; MYCOTOXINS; PROTEOMICS; SECRETION SYSTEMS;

BIOHAZARDS; FOOD PROCESSING; FOOD SAFETY; METABOLITES; MOLECULAR BIOLOGY; PROTEINS;

FOOD MICROBIOLOGY;

ANIMALIA; BACTERIA (MICROORGANISMS); FUNGI;

EID: 84886233933     PISSN: 09639969     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.foodres.2012.10.019     Document Type: Article

References (91)

1. Adav S.S., Li A.A., Manavalan A., Punt P., Sze S.K. Quantitative iTRAQ secretome analysis of Aspergillus niger reveals novel hydrolytic enzymes research articles. Journal of Proteome Research 2010, 9:3932-3940.
2. Anklam E., Stroka J., Boenke A. Acceptance of analytical methods for implementation of EU legislation with a focus on mycotoxins. Food Control 2002, 13(3):173-183. 10.1016/S0956-7135(01)00098-6.
3. Anonymous Marine biotoxins food and nutrition paper, FAO food and nutrition paper 80. North 2004, 1-229. Food and Agriculture Organization of the United Nations (FAO). North. Rome.
4. Aranishi F., Okimoto T., Izumi S. Identification of gadoid species (Pisces, Gadidae) by PCR-RFLP analysis. Journal of Applied Genetics 2005, 46(1):69-73.
5. Arlt V.M., Stiborová M., Brocke J., Simões M.L., Lord G.M., Nortier J.L., et al. Aristolochic acid mutagenesis: Molecular clues to the aetiology of Balkan endemic nephropathy-associated urothelial cancer. Carcinogenesis 2007, 28(11):2253-2261. 10.1093/carcin/bgm082.
6. Bhadauria V., Banniza S., Wang L.-X., Wei Y.-D., Peng Y.-L. Proteomic studies of phytopathogenic fungi, oomycetes and their interactions with hosts. European Journal of Plant Pathology 2009, 126(1):81-95. 10.1007/s10658-009-9521-4.
7. Bhatnagar D., Rajasekaran K., Payne G.A., Brown R.L., Yu J., Cleveland T.E. The "omics" tools: genomics, proteomics, metabolomics and their potential for solving the aflatoxin contamination problem. World Mycotoxin Journal 2008, 1(1):3-12. 10.3920/WMJ2008.x001.
8. Bowman S.M., Free S.J. The structure and synthesis of the fungal cell wall. BioEssays News and Reviews in Molecular Cellular and Developmental Biology 2006, 28(8):799-808. (CRC Press). 10.1002/bies.20441.
9. Braaksma M., Martens-Uzunova E.S., Punt P.J., Schaap P.J. An inventory of the Aspergillus niger secretome by combining in silico predictions with shotgun proteomics data. BMC Genomics 2010, 11(1):584. (BioMed Central Ltd). 10.1186/1471-2164-11-584.
10. Caprioli R.M., Farmer T.B., Gile J. Molecular imaging of biological samples: Localization of peptides and proteins using MALDI-TOF MS. Analytical Chemistry 1997, 69(23):4751-4760.
11. Capriotti A.L., Caruso G., Cavaliere C., Foglia P., Samperi R., Lagana A., et al. Multiclass mycotoxins analysis in food, environmental and biological matrices with chromatography/mass spectrometry. Mass Spectrometry Reviews 2011, 10.1002/mas.
12. Carberry S., Neville C.M., Kavanagh K.a, Doyle S. Analysis of major intracellular proteins of Aspergillus fumigatus by MALDI mass spectrometry: identification and characterisation of an elongation factor 1B protein with glutathione transferase activity. Biochemical and Biophysical Research Communications 2006, 341(4):1096-1104. 10.1016/j.bbrc.2006.01.078.
13. Chan L.L., Hodgkiss I.J., Lam P.K.-S., Wan J.M.-F., Chou H.-N., Lum J.H.-K., et al. Use of two-dimensional gel electrophoresis to differentiate morphospecies of Alexandrium minutum, a paralytic shellfish poisoning toxin-producing dinoflagellate of harmful algal blooms. Proteomics 2005, 5(6):1580-1593. 10.1002/pmic.200401020.
14. Chan L.L., Sit W.-H., Lam P.K.-S., Hsieh D.P.H., Hodgkiss I.J., Wan J.M.-F., et al. Identification and characterization of a "biomarker of toxicity" from the proteome of the paralytic shellfish toxin-producing dinoflagellate Alexandrium tamarense (Dinophyceae). Proteomics 2006, 6(2):654-666.
15. Choi J., Park J., Kim D., Jung K., Kang S., Lee Y.-H. Fungal secretome database: Integrated platform for annotation of fungal secretomes. BMC Genomics 2010, 11:105. 10.1186/1471-2164-11-105.
16. Crespo-Sempere A., Gil J.V., Martínez-Culebras P.V. Proteome analysis of the fungus Aspergillus carbonarius under ochratoxin A producing conditions. International Journal of Food Microbiology 2011, 147(3):162-169. (Elsevier B.V.). 10.1016/j.ijfoodmicro.2011.03.021.
17. D'Alessandro A., Zolla L. We are what we eat: food safety and proteomics. Journal of Proteome Research 2012, 11(1):26-36. 10.1021/pr2008829.
18. Dodds P.N., Rafiqi M., Gan P.H.P., Hardham A.R., Jones D.A., Ellis J.G. Effectors of biotrophic fungi and oomycetes: Pathogenicity factors and triggers of host resistance. New Phytologist 2009, 183(4):993-1000.
19. Draisci R., Lucentini L., Giannetti L., Boria P., Stacchini A. Detection of diarrhoetic shellfish toxins in mussels from Italy by ionspray liquid chromatography-mass spectrometry. Toxicon Official Journal of the International Society on Toxinology 1995, 33(12):1591-1603.
20. Dubois M., Demoulin L., Charlier C., Singh G., Godefroy S.B., Campbell K., et al. Development of ELISAs for detecting domoic acid, okadaic acid, and saxitoxin and their applicability for the detection of marine toxins in samples collected in Belgium. Food Additives & Contaminants. Part A, Chemistry, Analysis, Control, Exposure & Risk Assessment 2010, 27(6):859-868.
21. Ferranti P., Nasi A., Bruno M., Basile A., Serpe L., Gallo P. A peptidomic approach for monitoring and characterising peptide cyanotoxins produced in Italian lakes by matrix-assisted laser desorption/ionisation and quadrupole time-of-flight mass spectrometry. Rapid Communications in Mass Spectrometry RCM 2011, 25(9):1173-1183. 10.1002/rcm.4973.
22. Ferreira De Oliveira J.M.P., Van Passel M.W.J., Schaap P.J., De Graaff L.H. Proteomic analysis of the secretory response of Aspergillus niger to d-maltose and d-xylose. PLoS One 2011, 6(6):9. 10.1371/journal.pone.0020865.
23. Forné I., Abián J., Cerdà J. Fish proteome analysis: Model organisms and non-sequenced species. Proteomics 2010, 10(4):858-872. 10.1002/pmic.200900609.
24. Garet E., González-Fernández A., Lago J., Vieites J.M., Cabado A.G. Comparative evaluation of enzyme-linked immunoassay and reference methods for the detection of shellfish hydrophilic toxins in several presentations of seafood. Journal of Agricultural and Food Chemistry 2010, 58(3):1410-1415.
25. Gašo-Sokač D., Kovač S., Josić D. Application of proteomics in food technology and food biotechnology: Process development, quality control and product safety. Food Technology and Biotechnology 2010, 48(3):284-295.
26. Gašo-Sokač D., Kovač S., Josić D. Use of roteomic methodology in optimization of processing and quality control of food of animal origin. Food Technology and Biotechnology 2011, 49(4):397-412.
27. Getie M., Schmelzer C.E.H., Neubert R.H.H. Characterization of peptides resulting from digestion of human skin elastin with elastase. Proteins 2005, 61(3):649-657.
28. Gill S., Murphy M., Clausen J., Richard D., Quilliam M., MacKinnon S., et al. Neural injury biomarkers of novel shellfish toxins, spirolides: a pilot study using immunochemical and transcriptional analysis. NeuroToxicology 2003, 24(4-5):593-604.
29. Grollman A.P., Jelaković B. Role of environmental toxins in endemic (Balkan) nephropathy. Journal of the American Society of Nephrology 2007, 18(11):2817-2823. 10.1681/ASN.2007050537.
30. Groseclose M.R., Massion P.P., Chaurand P., Caprioli R.M. High-throughput proteomic analysis of formalin-fixed paraffin-embedded tissue microarrays using MALDI imaging mass spectrometry. Proteomics 2008, 8(18):3715-3724. 10.1002/pmic.200800495.
31. Han M.-J., Kim N.-J., Lee S.Y., Chang H.N. Extracellular proteome of Aspergillus terreus grown on different carbon sources. Current Genetics 2010, 56(4):369-382.
32. Hess P., Gallacher S., Bates L.A., Brown N., Quilliam M.A. Determination and confirmation of the amnesic shellfish poisoning toxin, domoic acid, in shellfish from Scotland by liquid chromatography and mass spectrometry. Journal of AOAC International 2001, 84(5):1657-1667.
33. Houterman P.M., Cornelissen B.J.C., Rep M. Suppression of plant resistance gene-based immunity by a fungal effector. PLoS Pathogens 2008, 4(5):e1000061. 10.1371/journal.ppat.1000061.
34. Hsieh Y., Chen J., Korfmacher W.a Mapping pharmaceuticals in tissues using MALDI imaging mass spectrometry. Journal of Pharmacological and Toxicological Methods 2007, 55(2):193-200. 10.1016/j.vascn.2006.06.004.
35. http://www.ncbi.nlm.nih.gov/genome.
36. Huang F., Clifton J., Yang X., Rosenquist T., Hixson D., Kovač S., et al. SELDI-TOF as a method for biomarker discovery in the urine of aristolochic-acid-treated mice. Electrophoresis 2009, 30:1168-1174. 10.1002/elps.200800548.
37. Hunt D.F., Henderson R.A., Shabanowitz J., Sakaguchi K., Michel H., Sevilir N., et al. Pillars article: Characterization of peptides bound to the class I MHC molecule HLA-A2.1 by mass spectrometry. The Journal of Immunology 2007, 179(5):2669-2671. (Science 1992. 255: 1261-1263). 10.1126/science.1546328.
38. Jakubowski J.A., Sweedler J.V. Sequencing and mass profiling highly modified conotoxins using global reduction/alkylation followed by mass spectrometry. Analytical Chemistry 2004, 76(22):6541-6547.
39. Josić D., Kovač S. Molecular imaging mass spectrometry. Kemija u industriji 2009, 58(5):207-213.
40. Käferstein F., Abdussalam M. Food safety in the 21st century. Bulletin of the World Health Organization 1999, 77(4):347-351.
41. Kim Y., Nandakumar M.P., Marten M.R. The state of proteome profiling in the fungal genus Aspergillus. Briefings in Functional Genomics & Proteomics 2008, 7(2):87-94. 10.1093/bfgp/elm031.
42. Kniemeyer O. Proteomics of eukaryotic microorganisms: The medically and biotechnologically important fungal genus Aspergillus. Proteomics 2011, 11(15):3232-3243. 10.1002/pmic.201100087.
43. Lu X., Sun J., Nimtz M., Wissing J., Zeng A.-P., Rinas U. The intra- and extracellular proteome of Aspergillus niger growing on defined medium with xylose or maltose as carbon substrate. Microbial Cell Factories 2010, 9:23. 10.1186/1475-2859-9-23.
44. MacCabe A.P., Orejas M., Tamayo E.N., Villanueva A., Ramón D. Improving extracellular production of food-use enzymes from Aspergillus nidulans. Journal of Biotechnology 2002, 96(1):43-54.
45. Mallick P., Kuster B. Proteomics: a pragmatic perspective. Nature Biotechnology 2010, 28(7):695-709. 10.1038/nbt.1658.
46. Marques A., Nunes M.L., Moore S.K., Strom M.S. Climate change and seafood safety: Human health implications. Food Research International 2010, 43(7):1766-1779. (Elsevier Ltd.). 10.1016/j.foodres.2010.02.010.
47. Martinez I., Jakobsen Friis T. Application of proteome analysis to seafood authentication. Proteomics 2004, 4(2):347-354. 10.1002/pmic.200300569.
48. Martinez I., James F., Loréal H. Application of modern analytical techniques to ensure seafood safety and authenticity. FAO Fisheries Technical Paper 2005, 455:73. Fisheries (Bethesda), Rome.
49. Martins J.C., Leão P.N., Vasconcelos V. Differential protein expression in Corbicula fluminea upon exposure to a Microcystis aeruginosa toxic strain. Toxicon Official Journal of the International Society on Toxinology 2009, 53(4):409-416.
50. Medina M.L., Francisco W.A. Isolation and enrichment of secreted proteins from filamentous fungi. Methods In Molecular Biology Clifton Nj 2008, 425(2):275-285. 10.1007/978-1-60327-210-0_22.
51. Møller M.T.N., Samari H.R., Fengsrud M., Strømhaug P.E., Ostvold A.C., Seglen P.O. Okadaic acid-induced, naringin-sensitive phosphorylation of glycine N-methyltransferase in isolated rat hepatocytes. The Biochemical Journal 2003, 373(Pt 2):505-513. 10.1042/BJ20030502.
52. Monsinjon T., Knigge T. Proteomic applications in ecotoxicology. Proteomics 2007, 7(16):2997-3009. 10.1002/pmic.200700101.
53. Newey L.J., Caten C.E., Green J.R. Rapid adhesion of Stagonospora nodorum spores to a hydrophobic surface requires pre-formed cell surface glycoproteins. Mycological Research 2007, 111(Pt 11):1255-1267.
54. Nzoughet J.K., Hamilton J.T.G., Botting C.H., Douglas A., Devine L., Nelson J., et al. Proteomics identification of azaspiracid toxin biomarkers in blue mussels, Mytilus edulis. Molecular & Cellular Proteomics 2009, 8(8):1811-1822. 10.1074/mcp.M800561-MCP200.
55. Nzoughet K.J., Hamilton J.T.G., Floyd S.D., Douglas A., Nelson J., Devine L., et al. Azaspiracid: first evidence of protein binding in shellfish. Toxicon Official Journal of the International Society on Toxinology 2008, 51(7):1255-1263.
56. Paper J.M., Scott-Craig J.S., Adhikari N.D., Cuomo C., Walton J.D. Comparative proteomics of extracellular proteins in vitro and in planta from the pathogenic fungus Fusarium graminearum. Proteomics 2007, 7(17):3171-3183. 10.1002/pmic.200700184.
57. Pešić I., Stefanović V., Müller G.A., Müller C.A., Cukuranović R., Jahn O., et al. Identification and validation of six proteins as marker for endemic nephropathy. Journal of Proteomics 2011, 74(10):1994-2007. 10.1016/j.jprot.2011.05.020.
58. Picariello G., Mamone G., Addeo F., Ferranti P. Novel mass spectrometry-based applications of the 'omic' sciences in food technology and biotechnology. Food Technology and Biotechnology 2012, 50(3):286-305.
59. Piñeiro C., Barros-Velázquez J., Vázquez J., Figueras a, Gallardo J.M. Proteomics as a tool for the investigation of seafood and other marine products. Journal of Proteome Research 2003, 2(2):127-135.
60. Piñeiro C., Cañas B., Carrera M. The role of proteomics in the study of the influence of climate change on seafood products. Food Research International 2010, 43(7):1791-1802. 10.1016/j.foodres.2009.11.012.
61. Plakas S.M., Dickey R.W. Advances in monitoring and toxicity assessment of brevetoxins in molluscan shellfish. Toxicon Official Journal of the International Society on Toxinology 2010, 56(2):137-149.
62. Qin G., Tian S., Chan Z., Li B. Crucial role of antioxidant proteins and hydrolytic enzymes in pathogenicity of Penicillium expansum: Analysis based on proteomics approach. Molecular Cellular Proteomics MCP 2007, 6(3):425-438. 10.1074/mcp.M600179-MCP200.
63. Quod J.P., Turquet J. Ciguatera in Réunion Island (SW Indian Ocean): Epidemiology and clinical patterns. Toxicon official journal of the International Society on Toxinology 1996, 34(7):779-785.
64. Richard J.L. Some major mycotoxins and their mycotoxicoses - An overview. International Journal of Food Microbiology 2007, 119(1-2):3-10.
65. Rizwan M., Miller I., Tasneem F., Böhm J., Gemeiner M., Razzazi-Fazeli E. Proteome analysis of Aspergillus ochraceus. Mycotoxin Research 2010, 26(3):171-180. 10.1007/s12550-010-0051-x.
66. Ronzitti G., Milandri A., Scortichini G., Poletti R., Rossini G.P. Protein markers of algal toxin contamination in shellfish. Toxicon official journal of the International Society on Toxinology 2008, 52(6):705-713.
67. Rossignoli A.E., Blanco J. Cellular distribution of okadaic acid in the digestive gland of Mytilus galloprovincialis (Lamarck, 1819). Toxicon Official Journal of the International Society on Toxinology 2008, 52(8):957-959.
68. Rossignoli A.E., Blanco J. Subcellular distribution of okadaic acid in the digestive gland of Mytilus galloprovincialis: First evidences of lipoprotein binding to okadaic acid. Toxicon Official Journal of the International Society on Toxinology 2009, 55(2-3):221-226.
69. Sala G.L., Ronzitti G., Sasaki M., Fuwa H., Yasumoto T., Bigiani A., et al. Proteomic analysis reveals multiple patterns of response in cells exposed to a toxin mixture. Chemical Research in Toxicology 2009, 22(6):1077-1085. 10.1021/tx900044p.
70. Samyn B., Sergeant K., Memmi S., Debyser G., Devreese B., Van Beeumen J. MALDI-TOF/TOF de novo sequence analysis of 2-D PAGE-separated proteins from Halorhodospira halophila, a bacterium with unsequenced genome. Electrophoresis 2006, 27(13):2702-2711.
71. Seng P., Drancourt M., Gouriet F., La Scola B., Fournier P.-E., Rolain J.M., et al. Ongoing revolution in bacteriology: routine identification of bacteria by matrix-assisted laser desorption ionization time-of-flight mass spectrometry. Clinical Infectious Diseases 2009, 49(4):543-551.
72. Sharma M., Soni R., Nazir A., Oberoi H.S., Chadha B.S. Evaluation of glycosyl hydrolases in the secretome of Aspergillus fumigatus and saccharification of alkali-treated rice straw. Applied Biochemistry and Biotechnology 2011, 163(5):577-591. 10.1007/s12010-010-9064-3.
73. Song J., Win J., Tian M., Schornack S., Kaschani F., Ilyas M., et al. Apoplastic effectors secreted by two unrelated eukaryotic plant pathogens target the tomato defense protease Rcr3. Proceedings of the National Academy of Sciences of the United States of America 2009, 106(5):1654-1659.
74. Sørensen L.M., Lametsch R., Andersen M.R., Nielsen P.V., Frisvad J.C. Proteome analysis of Aspergillus niger: lactate added in starch-containing medium can increase production of the mycotoxin fumonisin B2 by modifying acetyl-CoA metabolism. BMC Microbiology 2009, 9:255. 10.1186/1471-2180-9-255.
75. Suzuki T., Igarashi T., Ichimi K., Watai M., Suzuki M., Ogiso E., et al. Kinetics of diarrhetic shellfish poisoning toxins, okadaic acid, dinophysistoxin-1, pectenotoxin-6 and yessotoxin in scallops Patinopectin yessoensis. Fisheries Science 2005, 71:948-955. 10.1111/j.1444-2906.2005.01049.x.
76. Tannu N.S., Hemby S.E. De novo protein sequence analysis of Macaca mulatta. BMC Genomics 2007, 8(1):270. (BioMed Central.). 10.1186/1471-2164-8-270.
77. Taylor C.F., Paton N.W., Lilley K.S., Binz P.-A., Julian R.K., Jones A.R., et al. The minimum information about a proteomics experiment (MIAPE). Nature Biotechnology 2007, 25(8):887-893. 10.1038/1329.
78. Taylor R.D., Saparno A., Blackwell B., Anoop V., Gleddie S., Tinker N.A., et al. Proteomic analyses of Fusarium graminearum grown under mycotoxin-inducing conditions. Proteomics 2008, 8(11):2256-2265.
79. Vale P., Sampayo M.A. Comparison between HPLC and a commercial immunoassay kit for detection of okadaic acid and esters in Portuguese bivalves. Toxicon Official Journal of the International Society on Toxinology 1999, 37(11):1565-1577.
80. van Egmond H.P., Schothorst R.C., Jonker M.A. Regulations relating to mycotoxins in food: Perspectives in a global and European context. Analytical and Bioanalytical Chemistry 2007, 389(1):147-157. 10.1007/s00216-007-1317-9.
81. Van Esse H.P., Van't Klooster J.W., Bolton M.D., Yadeta K.A., Van Baarlen P., Boeren S., et al. The Cladosporium fulvum virulence protein Avr2 inhibits host proteases required for basal defense. The Plant Cell 2008, 20(7):1948-1963.
82. Vandergaag B., Spath S., Dietrich H., Stigter E., Boonzaaijer G., Vanosenbruggen T., et al. Biosensors and multiple mycotoxin analysis. Food Control 2003, 14(4):251-254. 10.1016/S0956-7135(03)00008-2.
83. Wang D.-Z., Li C., Xie Z.-X., Dong H.-P., Lin L., Hong H.-S. Homology-driven proteomics of dinoflagellates with unsequenced genomes using MALDI-TOF/TOF and automated de novo sequencing. Evidence-Based Complementary and Alternative Medicine 2011, 2011:1-16. 10.1155/2011/471020.
84. Ward O.P. Production of recombinant proteins by filamentous fungi. Biotechnology Advances 2011, 253-257. (Elsevier B.V.). 10.1016/j.biotechadv.2011.09.012.
85. Wartenberg D., Lapp K., Jacobsen I.D., Dahse H.-M., Kniemeyer O., Heinekamp T., et al. Secretome analysis of Aspergillus fumigatus reveals Asp-hemolysin as a major secreted protein. International Journal of Medical Microbiology: IJMM 2011, 301(7):602-611. 10.1016/j.ijmm.2011.04.016.
86. Watson D.S., Feng X., Askew D.S., Jambunathan K., Kodukula K., Galande A.K. Substrate specifity profiling of the Aspergillus fumigatus proteolytic secretome reveals consensus motifs with predominance of Ile/Leu and Phe/Tyr. PLoS One 2011, 6(6):e21001. 10.1371/journal.pone.0021001.
87. Wong C.K., Hung P., Lee K.L.H., Kam K.M. Solid-phase extraction clean-up of ciguatoxin-contaminated coral fish extracts for use in the mouse bioassay. Food Additives and Contaminants: Part A, Chemistry, Analysis, Control, Exposure and Risk Assessment 2009, 26(2):236-247. 10.1080/02652030802342505.
88. Woods A.S., Jackson S.N. Brain tissue lipidomics: direct probing using matrix-assisted laser desorption/ionization mass spectrometry. The AAPS Journal 2006, 8(2):E391-E395.
89. Yang F.E.N., Jensen J.D., Svensson B., Jørgensen H.J.L., Collinge D.B., Finnie C. Secretomics identifies Fusarium graminearum proteins involved in the interaction with barley and wheat. Molecular Plant Pathology 2011, 1-9. 10.1111/J.1364-3703.2011.00759.X.
90. Yergey A.L., Coorssen J.R., Backlund P.S., Blank P.S., Humphrey G.A., Zimmerberg J., et al. De novo sequencing of peptides. Methods 2002, 13(7):784-791. 10.1016/S1044-0305(02)00393-8.
91. Zinedine A., Soriano J.M., Moltó J.C., Mañes J. Review on the toxicity, occurrence, metabolism, detoxification, regulations and intake of zearalenone: an oestrogenic mycotoxin. Food and Chemical Toxicology an International Journal Published for the British Industrial Biological Research Association 2007, 45(1):1-18. 10.1016/j.fct.2006.07.030.