A novel peptide-binding motifs inference approach to understand deoxynivalenol molecular Toxicity

Toxins

Volumn 7, Issue 6, 2015, Pages 1989-2005

  Hassan, Yousef I ^a   Watts, Christena ^a   Li, Xiu Zhen ^a   Zhou, Ting ^a  

^a AGRICULTURE AND AGRI FOOD CANADA   (Canada)

Author keywords

Computational biology; Deoxynivalenol; Enzyme; Modification; Toxicity

Indexed keywords

MULTIDRUG RESISTANCE ASSOCIATED PROTEIN 2; VOMITOXIN; PEPTIDE; PROTEIN BINDING; TRICHOTHECENE DERIVATIVE;

AMINO ACID SEQUENCE; BINDING AFFINITY; BIOINFORMATICS; CHEMICAL MODIFICATION; DETOXIFICATION; IMMUNE DEFICIENCY; IMMUNE RESPONSE; NONHUMAN; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN STRUCTURE; PROTEIN SYNTHESIS; REVIEW; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; ANIMAL; CHEMISTRY; GENOME; HUMAN; METABOLISM; PROTEIN MOTIF;

ANIMALIA;

AMINO ACID MOTIFS; ANIMALS; GENOME; HUMANS; PEPTIDES; PROTEIN BINDING; TRICHOTHECENES;

EID: 84931275322     PISSN: None     EISSN: 20726651     Source Type: Journal    
DOI: 10.3390/toxins7061989     Document Type: Review

References (72)

1. Li, X.; Zhao, L.; Fan, Y.; Jia, Y.; Sun, L.; Ma, S.; Ji, C.; Ma, Q.; Zhang, J. Occurrence of Mycotoxins in Feed Ingredients and Complete Feeds Obtained from the Beijing Region of China. J. Anim. Sci. Biotechnol. 2014, 5, 37.
2. Rodrigues, I.; Naehrer, K. A Three-Year Survey on the Worldwide Occurrence of Mycotoxins in Feedstuffs and Feed. Toxins 2012, 4, 663-675.
3. Savi, G.D.; Piacentini, K.C.; Tibola, C.S.; Scussel, V.M. Mycoflora and Deoxynivalenol in Whole Wheat Grains (Triticum Aestivum l.) from Southern Brazil. Food Addit. Contam. Part B Surveill. 2014, 7, 232-237.
4. Gratz, S.W.; Richardson, A.J.; Duncan, G.; Holtrop, G. Annual Variation of Dietary Deoxynivalenol Exposure during Years of Different Fusarium Prevalence: A Pilot Biomonitoring Study. Food Addit. Contam. Part A 2014, 31, 1579-1585.
5. Maresca, M. From the Gut to the Brain: Journey and Pathophysiological Effects of the Food-Associated Trichothecene Mycotoxin Deoxynivalenol. Toxins 2013, 5, 784-820.
6. Wu, F.; Groopman, J.D.; Pestka, J.J. Public Health Impacts of Foodborne Mycotoxins. Annu. Rev. Food Sci. Technol. 2014, 5, 351-372.
7. Sirot, V.; Fremy, J.M.; Leblanc, J.C. Dietary Exposure to Mycotoxins and Health Risk Assessment in the Second French Total Diet Study. Food Chem. Toxicol. 2013, 52, 1-11.
8. Raad, F.; Nasreddine, L.; Hilan, C.; Bartosik, M.; Parent-Massin, D. Dietary Exposure to Aflatoxins, Ochratoxin A and Deoxynivalenol from a Total Diet Study in an Adult Urban Lebanese Population. Food Chem. Toxicol. 2014, 73, 35-43.
9. Mishra, S.; Dwivedi, P.D.; Pandey, H.P.; Das, M. Role of Oxidative Stress in Deoxynivalenol Induced Toxicity. Food Chem. Toxicol. 2014, 72C, 20-29.
10. Saint-Cyr, M.J.; Perrin-Guyomard, A.; Houee, P.; Rolland, J.G.; Laurentie, M. Evaluation of an Oral Subchronic Exposure of Deoxynivalenol on the Composition of Human Gut Microbiota in a Model of Human Microbiota-Associated Rats. PLoS ONE 2013, 8, doi:10.1371/journal.pone.0080578.
11. Wache, Y.J.; Valat, C.; Postollec, G.; Bougeard, S.; Burel, C.; Oswald, I.P.; Fravalo, P. Impact of Deoxynivalenol on the Intestinal Microflora of Pigs. Int. J. Mol. Sci. 2009, 10, 1-17.
12. Bonnet, M.S.; Roux, J.; Mounien, L.; Dallaporta, M.; Troadec, J.D. Advances in Deoxynivalenol Toxicity Mechanisms: The Brain as a Target. Toxins 2012, 4, 1120-1138.
13. Wu, W.; Bates, M.A.; Bursian, S.J.; Flannery, B.; Zhou, H.R.; Link, J.E.; Zhang, H.; Pestka, J.J. Peptide yy3-36 and 5-Hydroxytryptamine Mediate Emesis Induction by the Trichothecene Deoxynivalenol (Vomitoxin). Toxicol. Sci. 2013, doi:10.1093/toxsci/kft033.
14. Yang, W.; Yu, M.; Fu, J.; Bao, W.; Wang, D.; Hao, L.; Yao, P.; Nüssler, A.K.; Yan, H.; Liu, L. Deoxynivalenol Induced Oxidative Stress and Genotoxicity in Human Peripheral Blood Lymphocytes. Food Chem. Toxicol. 2014, 64, 383-396.
15. Takakura, N.; Nesslany, F.; Fessard, V.; Le Hegarat, L. Absence of in vitro Genotoxicity Potential of the Mycotoxin Deoxynivalenol in Bacteria and in Human tk6 and Heparg Cell Lines. Food Chem. Toxicol. 2014, 66, 113-121.
16. Videmann, B.; Tep, J.; Cavret, S.; Lecoeur, S. Epithelial Transport of Deoxynivalenol: Involvement of Human P-Glycoprotein (abcb1) and Multidrug Resistance-Associated Protein 2 (abcc2). Food Chem. Toxicol. 2007, 45, 1938-1947.
17. Pestka, J.J. Deoxynivalenol: Toxicity, Mechanisms and Animal Health Risks. Anim. Feed Sci. Technol. 2007, 137, 283-298.
18. Rotter, B.A. Invited Review: Toxicology of Deoxynivalenol (Vomitoxin). J. Toxicol. Environ. Health 1996, 48, 1-34.
19. Shifrin, V.I.; 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, 13985-13992.
20. Pinton, P.; Tsybulskyy, D.; Lucioli, J.; Laffitte, J.; Callu, P.; Lyazhri, F.; Grosjean, F.; Bracarense, A.P.; Kolf-Clauw, M.; Oswald, I.P. Toxicity of Deoxynivalenol and its Acetylated Derivatives on the Intestine: Differential Effects on Morphology, Barrier Function, Tight Junction Proteins, and Mitogen-Activated Protein Kinases. Toxicol. Sci. 2012, 130, 180-190.
21. Middlebrook, J.L.; Leatherman, D.L. Binding of t-2 Toxin to Eukaryotic Cell Ribosomes. Biochem. Pharmacol. 1989, 38, 3103-3110.
22. Schmeits, P.C.; Katika, M.R.; Peijnenburg, A.A.; van Loveren, H.; Hendriksen, P.J. DON Shares a Similar Mode of Action as the Ribotoxic Stress Inducer Anisomycin while TBTO Shares ER Stress Patterns with the ER Stress Inducer Thapsigargin based on Comparative Gene Expression Profiling in Jurkat T Cells. Toxicol. Lett. 2014, 224, 395-406.
23. Bae, H.; Gray, J.S.; Li, M.; Vines, L.; Kim, J.; Pestka, J.J. Hematopoietic Cell Kinase Associates with the 40s Ribosomal Subunit and Mediates the Ribotoxic Stress Response to Deoxynivalenol in Mononuclear Phagocytes. Toxicol. Sci. 2010, 115, 444-452.
24. He, K.; Zhou, H.R.; Pestka, J.J. Targets and Intracellular Signaling Mechanisms for Deoxynivalenol-Induced Ribosomal RNA Cleavage. Toxicol. Sci. 2012, 127, 382-390.
25. Cundliffe, E.; Cannon, M.; Davies, J. Mechanism of Inhibition of Eukaryotic Protein Synthesis by Trichothecene Fungal Toxins. Proc. Natl. Acad. Sci. USA 1974, 71, 30-34.
26. Wei, C.-M.; Campbell, I.; McLaughlin, C.; Vaughan, M. Binding of Trichodermin to Mammalian Ribosomes and its Inhibition by Other 12,13-Epoxytrichothecenes. Mol. and Cell. Biochem. 1974, 3, 215-219.
27. Wu, W.; He, K.; Zhou, H.R.; Berthiller, F.; Adam, G.; Sugita-Konishi, Y.; Watanabe, M.; Krantis, A.; Durst, T.; Zhang, H.; et al. Effects of Oral Exposure to Naturally-Occurring and Synthetic Deoxynivalenol Congeners on Proinflammatory Cytokine and Chemokine MRNA Expression in the Mouse. Toxicol. Appl. Pharmacol. 2014, 278, 107-115.
28. Pestka, J.J. Deoxynivalenol: Mechanisms of Action, Human Exposure, and Toxicological Relevance. Arch. Toxicol. 2010, 84, 663-679.
29. Islam, M.R.; Roh, Y.S.; Kim, J.; Lim, C.W.; Kim, B. Differential Immune Modulation by Deoxynivalenol (Vomitoxin) in Mice. Toxicol. Lett. 2013, 221, 152-163.
30. Pestka, J.J.; Zhou, H.R.; Moon, Y.; Chung, Y.J. Cellular and Molecular Mechanisms for Immune Modulation by Deoxynivalenol and Other Trichothecenes: Unraveling a Paradox. Toxicol. Lett. 2004, 153, 61-73.
31. Hirano, S.; Kataoka, T. Deoxynivalenol Induces Ectodomain Shedding of TNF Receptor 1 and thereby Inhibits the TNF-α-induced NF-κB Signaling Pathway. Eur. J. Pharmacol. 2013, 701, 144-151.
32. Pinton, P.; Nougayrède, J.-P.; Del Rio, J.-C.; Moreno, C.; Marin, D.E.; Ferrier, L.; Bracarense, A.-P.; Kolf-Clauw, M.; Oswald, I.P. The Food Contaminant Deoxynivalenol, Decreases Intestinal Barrier Permeability and Reduces Claudin Expression. Toxicol. Appl. Pharmacol. 2009, 237, 41-48.
33. Wang, Y.; Wu, W.; Wang, X.; He, C.; Yue, H.; Ren, Z.; Zhang, H. Inhibitory Effects of Deoxynivalenol on Gastric Secretion in Rats. J. Food Prot. 2014, 77, 1367-1371.
34. Maresca, M.; Fantini, J. Some Food-Associated Mycotoxins as Potential Risk Factors in Humans Predisposed to Chronic Intestinal Inflammatory Diseases. Toxicon 2010, 56, 282-294.
35. Wu, W.; Zhou, H.R.; He, K.; Pan, X.; Sugita-Konishi, Y.; Watanabe, M.; Zhang, H.; Pestka, J.J. Role of Cholecystokinin in Anorexia Induction Following Oral Exposure to the 8-Ketotrichothecenes Deoxynivalenol, 15-Acetyldeoxynivalenol, 3-Acetyldeoxynivalenol, Fusarenon X, and Nivalenol. Toxicol. Sci. 2014, 138, 278-289.
36. Näslund, E.; Hellström, P.M. Appetite Signaling: From Gut Peptides and Enteric Nerves to Brain. Physiol. Behav. 2007, 92, 256-262.
37. Noetzel, S.; Stengel, A.; Inhoff, T.; Goebel, M.; Wisser, A.S.; Bannert, N.; Wiedenmann, B.; Klapp, B.F.; Tache, Y.; Monnikes, H.; et al. CCK-8S Activates c-Fos in a Dose-Dependent Manner in Nesfatin-1 Immunoreactive Neurons in the Paraventricular Nucleus of the Hypothalamus and in the Nucleus of the Solitary Tract of the Brainstem. Regul. Pept. 2009, 157, 84-91.
38. Flannery, B.M.; Clark, E.S.; Pestka, J.J. Anorexia Induction by the Trichothecene Deoxynivalenol (Vomitoxin) is Mediated by the Release of the Gut Satiety Hormone Peptide YY. Toxicol. Sci. 2012, 130, 289-297.
39. Wu, M.; Xiao, H.; Ren, W.; Yin, J.; Tan, B.; Liu, G.; Li, L.; Nyachoti, C.M.; Xiong, X.; Wu, G. Therapeutic Effects of Glutamic Acid in Piglets Challenged with Deoxynivalenol. PLoS ONE 2014, 9, doi:10.1371/journal.pone.0100591.
40. Lessard, M.; Savard, C.; Deschene, K.; Lauzon, K.; Pinilla, V.A.; Gagnon, C.A.; Lapointe, J.; Guay, F.; Chorfi, Y. Impact of Deoxynivalenol (DON) Contaminated Feed on Intestinal Integrity and Immune Response in Swine. Food Chem. Toxicol. 2015, 80, 7-16.
41. Del Regno, M.; Adesso, S.; Popolo, A.; Quaroni, A.; Autore, G.; Severino, L.; Marzocco, S. Nivalenol Induces Oxidative Stress and Increases Deoxynivalenol Pro-Oxidant Effect in Intestinal Epithelial Cells. Toxicol. Appl. Pharmacol. 2015, 285, 118-127.
42. Bianco, G.; Fontanella, B.; Severino, L.; Quaroni, A.; Autore, G.; Marzocco, S. Nivalenol and Deoxynivalenol Affect Rat Intestinal Epithelial Cells: A Concentration Related Study. PLoS ONE 2012, 7, doi:10.1371/journal.pone.0052051.
43. Zhu, C.C.; Hou, Y.J.; Han, J.; Liu, H.L.; Cui, X.S.; Kim, N.H.; Sun, S.C. Effect of Mycotoxin-Containing Diets on Epigenetic Modifications of Mouse Oocytes by Fluorescence Microscopy Analysis. Microsc. Microanal. 2014, 20,1158-1161.
44. International Agency for Research on Cancer. Some Naturally-Occurring Substances: Some Food Items and Constituents, Heterocyclic Amines and Mycotoxins; Lyon, France, 1993; Volume 56, pp. 397-444.
45. Zhou, T.; He, J.; Gong, J. Microbial transformation of trichothecene mycotoxins. World Mycotoxin J. 2008, 1, 23-30.
46. Young, J.C.; Zhou, T.; Yu, H.; Zhu, H.; Gong, J. Degradation of Trichothecene Mycotoxins by Chicken Intestinal Microbes. Food Chem. Toxicol. 2007, 45, 136-143.
47. Sundstøl Eriksen, G.; Pettersson, H.; Lundh, T. Comparative Cytotoxicity of Deoxynivalenol, Nivalenol, their Acetylated Derivatives and De-Epoxy Metabolites. Food Chem. Toxicol. 2004, 42, 619-624.
48. Dänicke, S.; Hegewald, A.-K.; Kahlert, S.; Kluess, J.; Rothkötter, H.J.; Breves, G.; Döll, S. Studies on the Toxicity of Deoxynivalenol (DON), Sodium Metabisulfite, DON-Sulfonate (DONS) and De-Epoxy-DON for Porcine Peripheral Blood Mononuclear Cells and the Intestinal Porcine Epithelial Cell Lines IPEC-1 and IPEC-J2, and on Effects of DON and DONS on Piglets. Food Chem. Toxicol. 2010, 48, 2154-2162.
49. Shima, J.; Takase, S.; Takahashi, Y.; Iwai, Y.; Fujimoto, H.; Yamazaki, M.; Ochi, K. Novel Detoxification of the Trichothecene Mycotoxin Deoxynivalenol by a Soil Bacterium Isolated by Enrichment Culture. Appl. Environ. Microbiol. 1997, 63, 3825-3830.
50. Ikunaga, Y.; Sato, I.; Grond, S.; Numaziri, N.; Yoshida, S.; Yamaya, H.; Hiradate, S.; Hasegawa, M.; Toshima, H.; Koitabashi, M.; et al. Nocardioides sp. Strain WSN05-2, Isolated from a Wheat Field, Degrades Deoxynivalenol, Producing the Novel Intermediate 3-epi-Deoxynivalenol. Appl. Microbiol. Biotechnol. 2011, 89, 419-427.
51. Zhou, T.; He, J. Bacterial Isolate, Methods of Isolating Bacterial Isolates and Methods for Detoxification of Trichothecene Mycotoxins. U.S. Patent US13,500,239, 6 October 2010.
52. Karlovsky, P. Biological Detoxification of the Mycotoxin Deoxynivalenol and its Use in Genetically Engineered Crops and Feed Additives. Appl. Microbiol. Biotechnol. 2011, 91, 491-504.
53. Nagl, V.; Woechtl, B.; Schwartz-Zimmermann, H.E.; Hennig-Pauka, I.; Moll, W.D.; Adam, G.; Berthiller, F. Metabolism of the Masked Mycotoxin Deoxynivalenol-3-Glucoside in Pigs. Toxicol. Lett. 2014, 229, 190-197.
54. Poppenberger, B.; Berthiller, F.; Lucyshyn, D.; Sieberer, T.; Schuhmacher, R.; Krska, R.; Kuchler, K.; Glossl, J.; Luschnig, C.; Adam, G. Detoxification of the Fusarium Mycotoxin Deoxynivalenol by a UDP-Glucosyltransferase from Arabidopsis Thaliana. J. Biol. Chem. 2003, 278, 47905-47914.
55. Maul, R.; Warth, B.; Schebb, N.H.; Krska, R.; Koch, M.; Sulyok, M. In vitro Glucuronidation Kinetics of Deoxynivalenol by Human and Animal Microsomes and Recombinant Human UGT Enzymes. Arch. Toxicol. 2014, 89, 949-960.
56. Wu, X.; Murphy, P.; Cunnick, J.; Hendrich, S. Synthesis and Characterization of Deoxynivalenol Glucuronide: Its Comparative Immunotoxicity with Deoxynivalenol. Food Chem. Toxicol. 2007, 45, 1846-1855.
57. Fruhmann, P.; Weigl-Pollack, T.; Mikula, H.; Wiesenberger, G.; Adam, G.; Varga, E.; Berthiller, F.; Krska, R.; Hametner, C.; Frohlich, J. Methylthiodeoxynivalenol (MTD): Insight into the Chemistry, Structure and Toxicity of Thia-Michael Adducts of Trichothecenes. Org. Biomol. Chem. 2014, 12, 5144-5150.
58. Kadota, T.; Furusawa, H.; Hirano, S.; Tajima, O.; Kamata, Y.; Sugita-Konishi, Y. Comparative Study of Deoxynivalenol, 3-Acetyldeoxynivalenol, and 15-Acetyldeoxynivalenol on Intestinal Transport and IL-8 Secretion in the Human Cell Line Caco-2. Toxicol. in Vitro 2013, 27, 1888-1895.
59. Danicke, S.; Kersten, S.; Valenta, H.; Breves, G. Inactivation of Deoxynivalenol-Contaminated Cereal Grains with Sodium Metabisulfite: A Review of Procedures and Toxicological Aspects. Mycotoxin Res. 2012, 28, 199-218.
60. Alassane-Kpembi, I.; Puel, O.; Oswald, I.P. Toxicological Interactions between the Mycotoxins Deoxynivalenol, Nivalenol and their Acetylated Derivatives in Intestinal Epithelial Cells. Arch. Toxicol. 2014, doi:10.1007/s00204-014-1309-4.
61. Paulsen, I.T.; Park, J.H.; Choi, P.S.; Saier, M.H. Jr. A Family of Gram-Negative Bacterial Outer Membrane Factors that Function in the Export of Proteins, Carbohydrates, Drugs and Heavy Metals from Gram-Negative Bacteria. FEMS Microbiol. Lett. 1997, 156, 1-8.
62. Garvey, G.S.; McCormick, S.P.; Rayment, I. Structural and Functional Characterization of the TRI101 Trichothecene 3-O-Acetyltransferase from Fusarium Sporotrichioides and Fusarium Graminearum: Kinetic insights to Combating Fusarium Head Blight. J. Biol. Chem. 2008, 283, 1660-1669.
63. Khatibi, P.A.; Newmister, S.A.; Rayment, I.; McCormick, S.P.; Alexander, N.J.; Schmale, D.G., 3rd. Bioprospecting for Trichothecene 3-O-Acetyltransferases in the Fungal Genus Fusarium Yields Functional Enzymes with Different Abilities to Modify the Mycotoxin Deoxynivalenol. Appl. Environ. Microbiol. 2011, 77, 1162-1170.
64. Brown, D.W.; Proctor, R.H.; Dyer, R.B.; Plattner, R.D. Characterization of a Fusarium 2-Gene Cluster Involved in Trichothecene C-8 Modification. J. Agric. Food Chem. 2003, 51, 7936-7944.
65. Kimura, M.; Matsumoto, G.; Shingu, Y.; Yoneyama, K.; Yamaguchi, I. The Mystery of the Trichothecene 3-O-Acetyltransferase Gene. Analysis of the Region around TRI101 and Characterization of its Homologue from Fusarium Sporotrichioides. FEBS Lett. 1998, 435, 163-168.
66. Kimura, M.; Kaneko, I.; Komiyama, M.; Takatsuki, A.; Koshino, H.; Yoneyama, K.; Yamaguchi, I. Trichothecene 3-O-Acetyltransferase Protects Both the Producing Organism and Transformed Yeast from Related Mycotoxins. Cloning and Characterization of TRI101. J. Biol. Chem. 1998, 273, 1654-1661.
67. Ito, M.; Sato, I.; Ishizaka, M.; Yoshida, S.; Koitabashi, M.; Yoshida, S.; Tsushima, S. Bacterial Cytochrome P450 System Catabolizing the Fusarium Toxin Deoxynivalenol. Appl. Environ. Microbiol. 2013, 79, 1619-1628.
68. Schweiger, W.; Boddu, J.; Shin, S.; Poppenberger, B.; Berthiller, F.; Lemmens, M.; Muehlbauer, G.J.; Adam, G. Validation of a Candidate Deoxynivalenol-Inactivating UDP-Glucosyltransferase from Barley by Heterologous Expression in Yeast. Mol. Plant-Microbe Interact. 2010, 23, 977-986.
69. Tu, Z.; Xu, Y.; He, Q.; Fu, J.; Liu, X.; Tao, Y. Isolation and Characterisation of Deoxynivalenol Affinity Binders from a Phage Display Library Based on Single-Domain Camelid Heavy Chain Antibodies (VHHS). Food Agric. Immunol. 2012, 23, 123-131.
70. Xu, D.; Zhang, Y. Ab initio Protein Structure Assembly Using Continuous Structure Fragments and Optimized Knowledge-Based Force Field. Proteins 2012, 80, 1715-1735.
71. Holm, L.; Rosenstrom, P. Dali Server: Conservation Mapping in 3D. Nucleic Acids Res. 2010, 38, W545-W549.
72. Hassan, Y.I.; Lepp, D.; He, J.; Zhou, T. Draft Genome Sequences of Devosia sp. Strain 17-2-E-8 and Devosia Riboflavina Strain IFO13584. Genome Announc. 2014, 2, doi:10.1128/genomeA.00994-14.