T-2 toxin induced Salmonella Typhimurium intoxication results in decreased Salmonella numbers in the cecum contents of pigs, despite marked effects on Salmonella-host
详细信息 查看全文
- 作者：Elin Verbrugghe (1)
Virginie Vandenbroucke (2)
Maarten Dhaenens (3)
Neil Shearer (4)
Joline Goossens (2)
Sarah De Saeger (5)
Mia Eeckhout (6)
Katharina D’Herde (7)
Arthur Thompson (4)
Dieter Deforce (3)
Filip Boyen (1)
Bregje Leyman (1)
Alexander Van Parys (1)
Patrick De Backer (2)
Freddy Haesebrouck (1)
Siska Croubels (2)
Frank Pasmans (1) - 刊名：Veterinary Research
- 出版年：2012
- 出版时间：December 2012
- 年：2012
- 卷：43
- 期：1
- 全文大小：538KB
- 参考文献：1. Moss MO: Mycotoxin review-2. Fusarium . / Mycologist 2002, 16:157-61. CrossRef
2. Placinta C, D'Mello J, Macdonald A: A review of worldwide contamination of cereal grains and animal feed with Fusarium mycotoxins. / Anim Feed Sci Tech 1999, 78:21-7. CrossRef
3. Gutleb AC, Morrison E, Murk AJ: Cytotoxicity assays for mycotoxins produced by Fusarium strains: a review. / Environ Toxicol Pharmacol 2002, 11:309-20. CrossRef
4. Hussein HS, Brasel JM: Toxicity, metabolism, and impact of mycotoxins on humans and animals. / Toxicology 2001, 167:101-34. CrossRef
5. Wu Q, Dohnal V, Huang L, Kuca K, Yuan Z: Metabolic pathways of trichothecenes. / Drug Metab Rev 2010, 42:250-67. CrossRef
6. Wang ZG, Feng JN, Tong Z: Human toxicosis caused by moldy rice contaminated with Fusarium and T-2 toxin. / Biomed Environ Sci 1993, 6:65-0.
7. Scientific committee on Food: Opinion of the Scientific Committee on Food on Fusarium Toxins. Part 5: T-2 toxin and HT-2 toxin. [http://ec.europa.eu/food/fs/sc/scf/out88_en.pdf] 2001.
8. European Food Safety Authority: Scientific opinion on the risk for animal and public health related to the presence of T-2 and HT-2 toxin in food and feed. / EFSA J 2011, 9:2481.
9. Schollenberger M, Müller HM, Rüfle M, Suchy S, Plank S, Drochner W: Natural occurrence of 16 Fusarium toxins in grains and feedstuffs of plant origin from Germany. / Mycopathologia 2006, 161:43-2. CrossRef
10. European Food Safety Authority: European summary report on trends and sources of zoonoses and zoonotic agents and food-agents and food-borne outbreaks 2009. / EFSA J 2009, 9:378.
11. Wood RL, Pospischil A, Rose R: Distribution of persistent Salmonella Typhimurium infection in internal organs of swine. / Am J Vet Res 1989, 50:1015-021.
12. Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O'Brien SJ, Jones TF, Fazil A, Hoekstra RM: The global burden of nontyphoidal Salmonella gastroenteritis. / Clin Infect Dis 2010, 50:882-89. CrossRef
13. Cavret S, Lecoeur S: Fusariotoxin transfer in animal. / Food Chem Toxicol 2006, 44:444-53. CrossRef
14. Rafai P, Tuboly S, Bata A, Tilly P, Ványi A, Papp Z, Jakab L, Túry E: Effect of various levels of T-2 toxin in the immune system of growing pigs. / Vet Rec 1995, 136:511-14. CrossRef
15. Kankkunen P, Rintahaka J, Aalto A, Leino M, Majuri ML, Alenius H, Wolff H, Matikainen S: Trichothecene mycotoxins activate inflammatory response in human macrophages. / J Immunol 2009, 182:6418-425. CrossRef
16. Tenk I, Fodor E, Szathmáry C: The effect of pure Fusarium toxins (T-2, F-2, DAS) on the microflora of the gut and on plasma glucocorticoid levels in rat and swine. / Zentralbl Bakteriol Mikrobiol Hyg A 1982, 252:384-93.
17. Tai JH, Pestka JJ: Impaired murine resistance to Salmonella Typhimurium following oral exposure to the trichothecene T-2 toxin. / Food Chem Toxicol 1988, 26:691-98. CrossRef
18. Oswald IP, Desautels C, Laffitte J, Fournout S, Peres SY, Odin M, Le Bars P, Le Bars J, Fairbrother JM: Mycotoxin fumonisin B1 increases intestinal colonization by pathogenic Escherichia coli in pigs. / Appl Environ Microbiol 2003, 69:5870-874. CrossRef
19. Tanguy M, Burel C, Pinton P, Guerre P, Grosjean F, Queguiner M, Cariolet R, Tardieu D, Rault JC, Oswald IP, Fravalo P: Effets des fumonisines sur la santé du porc: sensibilité aux salmonelles et statut immunitaire. / Journées de la Recherche Porcine 2006, 38:393-98. (in French)
20. Boyen F, Pasmans F, Van Immerseel F, Morgan E, Botteldoorn N, Heyndrickx M, Volf J, Favoreel H, Hernalsteens JP, Ducatelle R, Haesebrouck F: A limited role for SsrA/B in persistent Salmonella Typhimurium infections in pigs. / Vet Microbiol 2008, 128:364-73. CrossRef
21. Boyen F, Pasmans F, Donné E, Van Immerseel F, Adriaensen C, Hernalsteen J-P, Ducatelle R, Haesebrouck F: Role of SPI-1 in the interactions of Salmonella Typhimurium with porcine macrophages. / Vet Microbiol 2006, 113:35-4. CrossRef
22. Lundberg U, Vinatzer U, Berdnik D, von Gabain A, Baccarini M: Growth phase-regulated induction of Salmonell a-induced macrophage apoptosis correlates with transient expression of SPI-1 genes. / J Bacteriol 1999, 181:3433-437.
23. Monbaliu S, Van Poucke C, Detavernier C, Dumoulin F, Van De Velde M, Schoeters E, Van Dyck S, Averkieva O, Van Peteghem C, De Saeger S: Occurrence of mycotoxins in feed as analyzed by a multi-mycotoxin LC-MS/MS method. / J Agric Food Chem 2010, 58:66-1. CrossRef
24. Vandenbroucke V, Croubels S, Martel A, Verbrugghe E, Goossens J, Van Deun K, Boyen F, Thompson A, Shearer N, De Backer P, Haesebrouck F, Pasmans F: The mycotoxin deoxynivalenol potentiates intestinal inflammation by Salmonella Typhimurium in porcine ileal loops. / PLoS One 2011, 6:e23871. CrossRef
25. Bouaziz C, Abid-Essefi S, Bouslimi A, El Golli E, Bacha H: Cytotoxicity and related effects of T-2 toxin on cultured Vero cells. / Toxicon 2006, 48:343-52. CrossRef
26. Verbrugghe E, Boyen F, Van Parys A, Van Deun K, Croubels S, Thompson A, Shearer N, Leyman B, Haesebrouck F, Pasmans F: Stress induced Salmonella Typhimurium recrudescence in pigs coincides with cortisol induced increased intracellular proliferation in macrophages. / Vet Res 2011, 42:118. CrossRef
27. Ross PL, Huang YN, Marchese JN, Williamson B, Parker K, Hattan S, Khainovski N, Pillai S, Dey S, Daniels S, Purkayastha S, Juhasz P, Martin S, Bartlet-Jones M, He F, Jacobson A, Pappin DJ: Multiplexed protein quantitation in Saccharomyces cerevisiae using amine-reactive isobaric tagging reagents. / Mol Cell Proteomics 2004, 3:1154-169. CrossRef
28. Bijttebier J, Tilleman K, Deforce D, Dhaenens M, Van Soom A, Maes D: Proteomic study to identify factors in follicular fluid and/or serum involved in in vitro cumulus expansion of porcine oocytes. / Soc Reprod Fertil Suppl 2009, 66:205-06.
29. Colaert N, Van Huele C, Degroeve S, Staes A, Vandekerckhove J, Gevaert K, Martens L: Combining quantitative proteomics data processing workflows for greater sensitivity. / Nat Methods 2011, 8:481-83. CrossRef
30. Nagy G, Danino V, Dobrindt U, Pallen M, Chaudhuri R, Em?dy L, Hinton JC, Hacker J: Downregulation of key virulence factors makes the Salmonella enterica serovar Typhimurium rfaH mutant a promising live-attenuated vaccine candidate. / Infect Immun 2006, 74:5914-925. CrossRef
31. Edgar R, Domrachev M, Lash AE: Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. / Nucleic Acids Res 2002, 30:207-10. CrossRef
32. Gene Expression Omnibus [http://www.ncbi.nlm.nih.gov/geo/query/acc.cgi?acc=GSE30925]
33. UniProtKB/Swiss-Prot protein sequence database [http://expasy.org/sprot/]
34. Ginisty H, Sicard H, Roger B, Bouvet P: Structure and functions of nucleolin. / J Cell Sci 1999, 112:761-72.
35. Hayano T, Takahashi N, Kato S, Maki N, Suzuki M: Two distinct forms of peptidylprolyl-cis-trans-isomerase are expressed separately in periplasmic and cytoplasmic compartments of Escherichia coli cells. / Biochemistry 1991, 30:3041-048. CrossRef
36. Carr-Schmid A, Valente L, Loik VI, Williams T, Starita LM, Kinzy TG: Mutations in elongation factor 1beta, a guanine nucleotide exchange factor, enhance translational fidelity. / Mol Cell Biol 1999, 19:5257-266.
37. Wang T, Arifoglu P, Ronai Z, Tew KD: Glutathione S-transferase P1- (GSTP1-) inhibits c-Jun N-terminal kinase (JNK1) signaling through interaction with the C terminus. / J Biol Chem 2001, 276:20999-1003. CrossRef
38. Li B, Dedman JR, Kaetzel MA: Intron disruption of the annexin IV gene reveals novel transcripts. / J Biol Chem 2003, 278:43276-3283. CrossRef
39. Iwahashi Y, Kitagawa E, Iwahashi H: Analysis of mechanisms of T-2 toxin toxicity using yeast DNA microarrays. / Int J Mol Sci 2008, 9:2585-600. CrossRef
40. Van Raaij MJ, Abrahams JP, Leslie AG, Walker JE: The structure of bovine F-1ATPase complexed with the antibiotic inhibitor aurovertin B. / Proc Natl Acad Sci USA 1996, 93:6913-917. CrossRef
41. Thameem F, Yang X, Permana PA, Wolford JK, Bogardus C, Prochazka M: Evaluation of the microsomal glutathione S-transferase 3 (MGST3) locus on 1q23 as a Type 2 diabetes susceptibility gene in Pima Indians. / Hum Genet 2003, 113:353-58. CrossRef
42. Heizmann CW, Fritz G, Sch?fer BW: S100 proteins: structure, functions and pathology. / Front Biosci 2002, 7:d1356-d1368. CrossRef
43. Sturchler E, Cox JA, Durussel I, Weibel M, Heizmann CW: S100A16, a novel calcium-binding protein of the EF-hand superfamily. / J Biol Chem 2006, 281:38905-8917. CrossRef
44. Harvey RB, Kubena LF, Huff WE, Corrier DE, Rottinghaus GE, Phillips TD: Effects of treatment of growing swine with aflatoxin and T-2 toxin. / Am J Vet Res 1990, 51:1688-693.
45. Harvey RB, Kubena LF, Elissalde MH, Rottinghaus GE, Corrier DE: Administration of ochratoxin A and T-2 toxin to growing swine. / Am J Vet Res 1994, 55:1757-761.
46. Rafai P, Bata A, Ványi A, Papp Z, Brydl E, Jakab L, Tuboly S, Túry E: Effect of various levels of T-2 toxin on the clinical status, performance and metabolism of growing pigs. / Vet Rec 1995, 136:485-89. CrossRef
47. Shifrin VI, Anderson P: Trichothecene mycotoxins trigger a ribotoxic stress response that activates c-Jun N-terminal kinase and p38 mitogen-activated protein kinase and induces apoptosis. / J Biol Chem 1999, 274:13985-3992. CrossRef
48. Yang H, Chung DH, Kim YB, Choi YH, Moon Y: Ribotoxic mycotoxin deoxynivalenol induces G2/M cell cycle arrest via p21Cip/WAF1 mRNA stabilization in human epithelial cells. / Toxicology 2008, 243:145-54. CrossRef
49. Hermeking H, Lengauer C, Polyak K, He TC, Zhang L, Thiagalingam S, Kinzler KW, Vogelstein B: 14--3 sigma is a p53-regulated inhibitor of G2/M progression. / Mol Cell 1997, 1:3-1. CrossRef
50. DiPaola RS: To arrest or not to G(2)-M Cell-cycle arrest. / Clin Cancer Res 2002, 8:3311-314.
51. Ziprin RL, McMurray DN: Differential effect of T-2 toxin on murine host resistance to three facultative intracellular bacterial pathogens: Listeria monocytogenes, Salmonella Typhimurium, and Mycobacterium bovis . / Am J Vet Res 1988, 49:1188-192.
52. Kubena LF, Bailey RH, Byrd JA, Young CR, Corrier DE, Stanker LH, Rottinghaust GE: Cecal volatile fatty acids and broiler chick susceptibility to Salmonella Typhimurium colonization as affected by aflatoxins and T-2 toxin. / Poult Sci 2001, 80:411-17.
53. Waché YJ, Valat C, Postollec G, Bougeard S, Burel C, Oswald IP, Fravalo P: Impact of deoxynivalenol on the intestinal microflora of pigs. / Int J Mol Sci 2009, 10:1-7. CrossRef
54. Almond G: Research applications using pigs. / Vet Clin North Am Food Anim Pract 1996, 12:707-16.
55. Skjolaas KA, Burkey TE, Dritz SS, Minton JE: Effects of Salmonella enterica serovars Typhimurium (ST) and Choleraesuis (SC) on chemokine and cytokine expression in swine ileum and jejunal epithelial cells. / Vet Immunol Immunopathol 2006, 111:199-09. CrossRef
56. Zhou HR, Yan D, Pestka JJ: Induction of cytokine gene expression in mice after repeated and subchronic oral exposure to vomitoxin (Deoxynivalenol): differential toxin-induced hyporesponsiveness and recovery. / Toxicol Appl Pharmacol 1998, 51:347-58. CrossRef
57. Kruber P, Trump S, Behrens J, Lehmann I: T-2 toxin is a cytochrome P450 1A1 inducer and leads to MAPK/p38- but not aryl hydrocarbon receptor-dependent interleukin-8 secretion in the human intestinal epithelial cell line Caco-2. / Toxicology 2011, 284:34-1. CrossRef
58. Maresca M, Yahi N, Younès-Sakr L, Boyron M, Caporiccio B, Fantini J: Both direct and indirect effects account for the pro-inflammatory activity of enteropahogenic mycotoxins on the human intestinal epithelium: Stimulation of interleukin-8 secretion, potentiation of interleukin-1β effect and increase in the transepithelial passage of commensal bacteria. / Toxicol Appl Pharmacol 2008, 228:84-2. CrossRef
59. Vandenbroucke V, Croubels S, Verbrugghe E, Boyen F, De Backer P, Ducatelle R, Rychlik I, Haesebrouck F, Pasmans F: The mycotoxin deoxynivalenol promotes uptake of Salmonella Typhimurium in porcine macrophages, associated with ERK1/2 induced cytoskeleton reorganization. / Vet Res 2009, 40:64. CrossRef
60. Maresca M, Fantini J: Some food-associated mycotoxins as potential risk factors in humans predisposed to chronic intestinal inflammatory diseases. / Toxicon 2010, 56:282-94. CrossRef
61. Singh S, Gupta PD: Tampering with cytokeratin expression results in cell dysfunction. / Epithelial Cell Biol 1994, 3:79-3.
62. Hartwig JH, Thelen M, Rosen A, Janmey PA, Nairn AC, Aderem A: MARCKS is an actin filament crosslinking protein regulated by protein kinase C and calcium-calmodulin. / Nature 1992, 356:618-22. CrossRef
63. Sribenja S, Li M, Wongkham S, Wongkham C, Yao Q, Chen C: Advances in thymosin beta10 research: differential expression, molecular mechanisms, and clinical implications in cancer and other conditions. / Cancer Invest 2009, 27:1016-022. CrossRef
64. Tran TC, Singleton C, Fraley TS, Greenwood JA: Cysteine-rich protein 1 (CRP1) regulates actin filament bundling. / BMC Cell Biol 2005, 6:45. CrossRef
65. Gutsche-Perelroizen I, Lepault J, Ott A, Carlier MF: Filament assembly from profilinactin. / J Biol Chem 1999, 274:6234-243. CrossRef
66. Van Kol SW, Hendriksen PJ, van Loveren H, Peijnenburg A: The effects of deoxynivalenol on gene expression in the murine thymus. / Toxicol Appl Pharmacol 2011, 250:299-11. CrossRef
67. Shah DH, Zhou X, Addwebi T, Davis MA, Orfe L, Call DR, Guard J, Besser TE: Cell invasion of poultry-associated Salmonella enterica serovar Enteritidis isolates is associated with pathogenicity, motility and proteins secreted by the type III secretion system. / Microbiology 2011, 157:1428-445. CrossRef
68. Boyen F, Pasmans F, Van Immerseel F, Morgan E, Adriaensen C, Hernalsteens JP, Decostere A, Ducatelle R, Haesebrouck F: Salmonella Typhimurium SPI-1 genes promote intestinal but not tonsillar colonization in pigs. / Microbes Infect 2006, 8:2899-907. CrossRef - 作者单位：Elin Verbrugghe (1)
Virginie Vandenbroucke (2)
Maarten Dhaenens (3)
Neil Shearer (4)
Joline Goossens (2)
Sarah De Saeger (5)
Mia Eeckhout (6)
Katharina D’Herde (7)
Arthur Thompson (4)
Dieter Deforce (3)
Filip Boyen (1)
Bregje Leyman (1)
Alexander Van Parys (1)
Patrick De Backer (2)
Freddy Haesebrouck (1)
Siska Croubels (2)
Frank Pasmans (1)
1. Department of Pathology, Bacteriology and Avian Diseases, Faculty of Veterinary Medicine, Ghent University, 9820, Merelbeke, Belgium
2. Department of Pharmacology, Toxicology and Biochemistry, Faculty of Veterinary Medicine, Ghent University, 9820, Merelbeke, Belgium
3. Department of Pharmaceutics, Faculty of Pharmaceutical Sciences, Ghent University, 9000, Ghent, Belgium
4. Department of Foodborne Bacterial Pathogens, Institute of Food Research, Norwich Research Park, NR4 7UA, Norwich, UK
5. Department of Bioanalysis, Faculty of Pharmaceutical Sciences, Ghent University, 9000, Ghent, Belgium
6. Department of Food Science and Technology, Faculty of Applied bioengineering, University College Ghent, 9000, Ghent, Belgium
7. Department of Basic Medical Sciences, Faculty of Medicine and Health Sciences, Ghent University, 9000, Ghent, Belgium
文摘
The mycotoxin T-2 toxin and Salmonella Typhimurium infections pose a significant threat to human and animal health. Interactions between both agents may result in a different outcome of the infection. Therefore, the aim of the presented study was to investigate the effects of low and relevant concentrations of T-2 toxin on the course of a Salmonella Typhimurium infection in pigs. We showed that the presence of 15 and 83 μg T-2 toxin per kg feed significantly decreased the amount of Salmonella Typhimurium bacteria present in the cecum contents, and a tendency to a reduced colonization of the jejunum, ileum, cecum, colon and colon contents was noticed. In vitro, proteomic analysis of porcine enterocytes revealed that a very low concentration of T-2 toxin (5 ng/mL) affects the protein expression of mitochondrial, endoplasmatic reticulum and cytoskeleton associated proteins, proteins involved in protein synthesis and folding, RNA synthesis, mitogen-activated protein kinase signaling and regulatory processes. Similarly low concentrations (1-100 ng/mL) promoted the susceptibility of porcine macrophages and intestinal epithelial cells to Salmonella Typhimurium invasion, in a SPI-1 independent manner. Furthermore, T-2 toxin (1-5 ng/mL) promoted the translocation of Salmonella Typhimurium over an intestinal porcine epithelial cell monolayer. Although these findings may seem in favour of Salmonella Typhimurium, microarray analysis showed that T-2 toxin (5 ng/mL) causes an intoxication of Salmonella Typhimurium, represented by a reduced motility and a downregulation of metabolic and Salmonella Pathogenicity Island 1 genes. This study demonstrates marked interactions of T-2 toxin with Salmonella Typhimurium pathogenesis, resulting in bacterial intoxication.