Review of mechanisms of deoxynivalenol‐induced anorexia: The role of gut microbiota

Deoxynivalenol (DON) is one of the most important mycotoxins in cereal‐based foods or other food productions, produced by Fusarium species. Because of the high occurrence of DON in food combined with vast consumption of cereals and grain worldwide, the DON‐contaminated food is a very harmful factor for human and animal health. DON has been reported to induce anorexia at lower or chronic doses in animal models. However, further researches for DON‐induced anorexia are limited. Previous publications demonstrated a close link between Bacteroidetes and Firmicutes, two kinds of gut microbiota, with weight loss and the effect of low administration of DON on neurotransmitters in the frontal cortex, cerebellum, hypothalamus, hippocampus and pons/medulla. These data are similar to other studies, which show selective 5HTα receptor agonists apparently causing hyperphagia whereas 5HT1β agonists appear to induce anorexia. Thus, the neurochemical effects of lower DON exposure can be as a result of peripheral toxicological events such as emesis, which overwhelmed its more subtle feed refusal activity. Besides, changes in the microbiota have an impact on stress‐related behaviors like anxiety and depression, which can lead to weight loss through decreased feed intake. Gut dysbiosis is also associated with brain dysfunction and with behavioral changes. These conclusions illustrate as well a potential explanation for DON‐induced anorexia.In this review, we summarize information about DON‐induced anorexia from previous studies and provide our opinion for future investigations that could establish a link between gut microbiota, neurotransmitters, anorexia and weight loss under the DON exposure. Copyright © 2017 John Wiley & Sons, Ltd.

[1]  Christina Wayman Microbes and the gut–brain axis , 2016 .

[2]  V. Moutardier,et al.  Hydrolytic Fate of 3/15-Acetyldeoxynivalenol in Humans: Specific Deacetylation by the Small Intestine and Liver Revealed Using in Vitro and ex Vivo Approaches , 2016, Toxins.

[3]  G. Schatzmayr,et al.  Deoxynivalenol and its masked forms in food and feed , 2015 .

[4]  J. Pestka,et al.  High Sensitivity of Aged Mice to Deoxynivalenol (Vomitoxin)-Induced Anorexia Corresponds to Elevated Proinflammatory Cytokine and Satiety Hormone Responses , 2015, Toxins.

[5]  I. Oswald,et al.  Deoxynivalenol inhibits the expression by goblet cells of intestinal mucins through a PKR and MAP kinase dependent repression of the resistin-like molecule β. , 2015, Molecular nutrition & food research.

[6]  T. Reinehr,et al.  The gut sensor as regulator of body weight , 2015, Endocrine.

[7]  J. Foster,et al.  Gut brain axis: diet microbiota interactions and implications for modulation of anxiety and depression. , 2015, Current opinion in biotechnology.

[8]  R. Barbouche,et al.  The food born mycotoxin deoxynivalenol induces low-grade inflammation in mice in the absence of observed-adverse effects. , 2015, Toxicology letters.

[9]  J. Pestka,et al.  Comparison of anorectic potencies of the trichothecenes T-2 toxin, HT-2 toxin and satratoxin G to the ipecac alkaloid emetine , 2015, Toxicology reports.

[10]  S. Bursian,et al.  Comparison of anorectic and emetic potencies of deoxynivalenol (vomitoxin) to the plant metabolite deoxynivalenol-3-glucoside and synthetic deoxynivalenol derivatives EN139528 and EN139544. , 2014, Toxicological sciences : an official journal of the Society of Toxicology.

[11]  Carlo C Maley,et al.  Is eating behavior manipulated by the gastrointestinal microbiota? Evolutionary pressures and potential mechanisms , 2014, BioEssays : news and reviews in molecular, cellular and developmental biology.

[12]  M. Laurentie,et al.  Evaluation of an Oral Subchronic Exposure of Deoxynivalenol on the Composition of Human Gut Microbiota in a Model of Human Microbiota-Associated Rats , 2013, PloS one.

[13]  M. Maresca From the Gut to the Brain: Journey and Pathophysiological Effects of the Food-Associated Trichothecene Mycotoxin Deoxynivalenol , 2013, Toxins.

[14]  J. Pestka,et al.  Anorexia induction by the trichothecene deoxynivalenol (vomitoxin) is mediated by the release of the gut satiety hormone peptide YY. , 2012, Toxicological sciences : an official journal of the Society of Toxicology.

[15]  K. Naehrer,et al.  A Three-Year Survey on the Worldwide Occurrence of Mycotoxins in Feedstuffs and Feed , 2012, Toxins.

[16]  S. Collins,et al.  Microbes and the gut‐brain axis , 2012, Neurogastroenterology and motility : the official journal of the European Gastrointestinal Motility Society.

[17]  Marcus J Claesson,et al.  An irritable bowel syndrome subtype defined by species-specific alterations in faecal microbiota , 2011, Gut.

[18]  John F. Cryan,et al.  Brain–Gut–Microbe Communication in Health and Disease , 2011, Front. Physio..

[19]  A. Jean,et al.  The Food-Contaminant Deoxynivalenol Modifies Eating by Targeting Anorexigenic Neurocircuitry , 2011, PloS one.

[20]  H. Dupont,et al.  The intestinal microbiota and chronic disorders of the gut , 2011, Nature Reviews Gastroenterology &Hepatology.

[21]  Nathalie M. Delzenne,et al.  Targeting gut microbiota in obesity: effects of prebiotics and probiotics , 2011, Nature Reviews Endocrinology.

[22]  J. Pestka,et al.  Characterization of deoxynivalenol-induced anorexia using mouse bioassay. , 2011, Food and chemical toxicology : an international journal published for the British Industrial Biological Research Association.

[23]  T. Dinan,et al.  Altered peripheral toll‐like receptor responses in the irritable bowel syndrome , 2011, Alimentary pharmacology & therapeutics.

[24]  Patrice D Cani,et al.  The gut microbiome as therapeutic target. , 2011, Pharmacology & therapeutics.

[25]  Wei-Wei Zhang,et al.  Gut bacteria alteration in obese people and its relationship with gene polymorphism. , 2011, World journal of gastroenterology.

[26]  H. Forssberg,et al.  Normal gut microbiota modulates brain development and behavior , 2011, Proceedings of the National Academy of Sciences.

[27]  F. Shanahan The colonic microflora and probiotic therapy in health and disease , 2011, Current opinion in gastroenterology.

[28]  S. Melgar,et al.  Inflammatory bowel disease—From mechanisms to treatment strategies , 2010, Autoimmunity.

[29]  S. Fukudo,et al.  Altered profiles of intestinal microbiota and organic acids may be the origin of symptoms in irritable bowel syndrome , 2009, Neurogastroenterology and motility : the official journal of the European Gastrointestinal Motility Society.

[30]  D. Naslain,et al.  Gut microbiota fermentation of prebiotics increases satietogenic and incretin gut peptide production with consequences for appetite sensation and glucose response after a meal. , 2009, The American journal of clinical nutrition.

[31]  A. Martí,et al.  Interplay Between Weight Loss and Gut Microbiota Composition in Overweight Adolescents , 2009, Obesity.

[32]  V. Mai,et al.  Recent advances and remaining gaps in our knowledge of associations between gut microbiota and human health. , 2009, World journal of gastroenterology.

[33]  S. Bougeard,et al.  Impact of Deoxynivalenol on the Intestinal Microflora of Pigs , 2008, International journal of molecular sciences.

[34]  Kevin W. Williams,et al.  5-HT2CRs Expressed by Pro-Opiomelanocortin Neurons Regulate Energy Homeostasis , 2008, Neuron.

[35]  S. Salminen,et al.  Distinct composition of gut microbiota during pregnancy in overweight and normal-weight women. , 2008, The American journal of clinical nutrition.

[36]  D. F. Orr,et al.  Antimicrobial activity of neuropeptides against a range of micro-organisms from skin, oral, respiratory and gastrointestinal tract sites , 2008, Journal of Neuroimmunology.

[37]  P. Turnbaugh,et al.  Microbial ecology: Human gut microbes associated with obesity , 2006, Nature.

[38]  T. Moran,et al.  Peptide YY(3-36) inhibits gastric emptying and produces acute reductions in food intake in rhesus monkeys. , 2005, American journal of physiology. Regulatory, integrative and comparative physiology.

[39]  R. Schothorst,et al.  Report from SCOOP task 3.2.10 "collection of occurrence data of Fusarium toxins in food and assessment of dietary intake by the population of EU member states". Subtask: trichothecenes. , 2004, Toxicology letters.

[40]  J. Doré,et al.  Direct Analysis of Genes Encoding 16S rRNA from Complex Communities Reveals Many Novel Molecular Species within the Human Gut , 1999, Applied and Environmental Microbiology.

[41]  D. Prelusky Effect of intraperitoneal infusion of deoxynivalenol on feed consumption and weight gain in the pig. , 1998, Natural toxins.

[42]  E. Zoetendal,et al.  Temperature Gradient Gel Electrophoresis Analysis of 16S rRNA from Human Fecal Samples Reveals Stable and Host-Specific Communities of Active Bacteria , 1998, Applied and Environmental Microbiology.

[43]  Gerwin C. Raangs,et al.  Variations of Bacterial Populations in Human Feces Measured by Fluorescent In Situ Hybridization with Group-Specific 16S rRNA-Targeted Oligonucleotide Probes , 1998, Applied and Environmental Microbiology.

[44]  D. Prelusky A study on the effect of deoxynivalenol on serotonin receptor binding in pig brain membranes. , 1996, Journal of environmental science and health. Part. B, Pesticides, food contaminants, and agricultural wastes.

[45]  K. Wilson,et al.  Human colonic biota studied by ribosomal DNA sequence analysis , 1996, Applied and environmental microbiology.

[46]  J. Pestka,et al.  Toxicology of deoxynivalenol (vomitoxin). , 1996, Journal of toxicology and environmental health.

[47]  G R Gibson,et al.  Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. , 1995, The Journal of nutrition.

[48]  D. Prelusky The effect of deoxynivalenol on serotoninergic neurotransmitter levels in pig blood. , 1994, Journal of environmental science and health. Part. B, Pesticides, food contaminants, and agricultural wastes.

[49]  H. Trenholm,et al.  Effects of low-level dietary deoxynivalenol on haematological and clinical parameters of the pig. , 1994, Natural toxins.

[50]  L. Buéno,et al.  The mycotoxin, deoxynivalenol, delays gastric emptying through serotonin-3 receptors in rodents. , 1993, The Journal of pharmacology and experimental therapeutics.

[51]  G. Macfarlane,et al.  Short chain fatty acids in human large intestine, portal, hepatic and venous blood. , 1987, Gut.

[52]  G. Kennett,et al.  5-HT1B agonists induce anorexia at a postsynaptic site. , 1987, European journal of pharmacology.

[53]  S. Swanson,et al.  Sex-related reduced weight gains in growing swine fed diets containing deoxynivalenol. , 1985, Journal of animal science.

[54]  R. Ismagilov,et al.  Indigenous Bacteria from the Gut Microbiota Regulate Host Serotonin Biosynthesis , 2015 .

[55]  E. Szigethy,et al.  Inflammatory bowel disease. , 2011, Pediatric clinics of North America.

[56]  L. Paulin,et al.  Multilayered epithelium in a rat model and human Barrett's esophagus: Similar expression patterns of transcription factors and differentiation markers , 2008, BMC gastroenterology.

[57]  J. H. Jansen,et al.  The effects of naturally deoxynivalenol-contaminated oats on the clinical condition, blood parameters, performance and carcass composition of growing pigs , 2005, Veterinary Research Communications.

[58]  H. Flint,et al.  Assessment of microbial diversity in human colonic samples by 16S rDNA sequence analysis. , 2002, FEMS microbiology ecology.

[59]  H. Trenholm,et al.  Effect of deoxynivalenol on neurotransmitters in discrete regions of swine brain , 1992, Archives of environmental contamination and toxicology.

[60]  B. A. Koch,et al.  Deoxynivalenol-contaminated wheat in swine diets. , 1985, Journal of animal science.

[61]  P. McHugh,et al.  Cholecystokinin-decreased food intake in rhesus monkeys. , 1976, The American journal of physiology.