Type A Trichothecene Diacetoxyscirpenol-Induced Emesis Corresponds to Secretion of Peptide YY and Serotonin in Mink
Language English Country Switzerland Media electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
Grant support
Excellence project
UHK - International
CEP Register
2016YFD0501207, 2016YFD0501009
National Key R & D Program - International
31972741, 31572576
NSFC - International
2016T90477
China Postdoctoral Science Foundation - International
PubMed
32630472
PubMed Central
PMC7354585
DOI
10.3390/toxins12060419
PII: toxins12060419
Knihovny.cz E-resources
- Keywords
- diacetoxyscirpenol, emesis, mycotoxin, peptide YY, serotonin, trichothecene,
- MeSH
- Serotonin 5-HT3 Receptor Antagonists pharmacology MeSH
- Antiemetics pharmacology MeSH
- Granisetron pharmacology MeSH
- Disease Models, Animal MeSH
- Mink MeSH
- Peptide YY blood MeSH
- Receptors, Gastrointestinal Hormone metabolism MeSH
- Receptors, Serotonin, 5-HT3 metabolism MeSH
- Secretory Pathway MeSH
- Serotonin blood MeSH
- Trichothecenes * MeSH
- Up-Regulation MeSH
- Animals MeSH
- Vomiting blood chemically induced prevention & control MeSH
- Check Tag
- Female MeSH
- Animals MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Serotonin 5-HT3 Receptor Antagonists MeSH
- Antiemetics MeSH
- diacetoxyscirpenol MeSH Browser
- Granisetron MeSH
- Peptide YY MeSH
- peptide YY receptor MeSH Browser
- Receptors, Gastrointestinal Hormone MeSH
- Receptors, Serotonin, 5-HT3 MeSH
- Serotonin MeSH
- Trichothecenes * MeSH
The trichothecene mycotoxins contaminate cereal grains and have been related to alimentary toxicosis resulted in emetic response. This family of mycotoxins comprises type A to D groups of toxic sesquiterpene chemicals. Diacetoxyscirpenol (DAS), one of the most toxic type A trichothecenes, is considered to be a potential risk for human and animal health by the European Food Safety Authority. Other type A trichothecenes, T-2 toxin and HT-2 toxin, as well as type B trichothecene deoxynivalenol (DON), have been previously demonstrated to induce emetic response in the mink, and this response has been associated with the plasma elevation of neurotransmitters peptide YY (PYY) and serotonin (5-hydroxytryptamine, 5-HT). However, it is found that not all the type A and type B trichothecenes have the capacity to induce PYY and 5-HT. It is necessary to identify the roles of these two emetogenic mediators on DAS-induced emesis. The goal of this study was to determine the emetic effect of DAS and relate this effect to PYY and 5-HT, using a mink bioassay. Briefly, minks were fasted one day before experiment and given DAS by intraperitoneally and orally dosing on the experiment day. Then, emetic episodes were calculated and blood collection was employed for PYY and 5-HT test. DAS elicited robust emetic responses that corresponded to upraised PYY and 5-HT. Blocking the neuropeptide Y2 receptor (NPY2R) diminished emesis induction by PYY and DAS. The serotonin 3 receptor (5-HT3R) inhibitor granisetron totally restrained the induction of emesis by serotonin and DAS. In conclusion, our findings demonstrate that PYY and 5-HT have critical roles in DAS-induced emetic response.
See more in PubMed
Pestka J.J. Toxicological mechanisms and potential health effects of deoxynivalenol and nivalenol. World Mycotoxin J. 2010;3:323–347. doi: 10.3920/WMJ2010.1247. DOI
Pestka J.J. Deoxynivalenol: Mechanisms of action, human exposure, and toxicological relevance. Arch. Toxicol. 2010;84:663–679. doi: 10.1007/s00204-010-0579-8. PubMed DOI
Zhang J., Zhang H., Liu S., Wu W., Zhang H. Comparison of anorectic potencies of type A Trichothecenes T-2 toxin, HT-2 toxin, Diacetoxyscirpenol, and Neosolaniol. Toxins. 2018;10:179. doi: 10.3390/toxins10050179. PubMed DOI PMC
JECFA . Deoxynivalenol. WHO Press; Geneva, Switzerland: 2011. Evaluation of certain contaminants in food: 72nd report of the joint FAO/WHO expert committee on food additives; pp. 37–48. (WHO Technical Report Series, No. 959).
Vesonder R.F., Ciegler A., Jensen A.H. Isolation of the emetic principle from fusarium-infected corn. Appl. Microbiol. 1973;26:1008–1010. doi: 10.1128/AEM.26.6.1008-1010.1973. PubMed DOI PMC
Lysøe E., Frandsen R.J.N., Divon H.H., Terzi V., Orrù L., Lamontanara A., Kolseth A.-K., Nielsen K.F., Thrane U. Draft genome sequence and chemical profiling of Fusarium langsethiae, an emerging producer of type A trichothecenes. Int. J. Food Microbiol. 2016;221:29–36. doi: 10.1016/j.ijfoodmicro.2016.01.008. PubMed DOI
Knutsen H.K., Alexander J., Barregård L., Bignami M., Brüschweiler B., Ceccatelli S., Cottrill B., DiNovi M., Grasl-Kraupp B., Hogstrand C., et al. Risk to human and animal health related to the presence of 4,15-diacetoxyscirpenol in food and feed. EFSA J. 2018;16 doi: 10.2903/j.efsa.2018.5367. PubMed DOI PMC
Andrews P.L.R., Davis C.J., Bingham S., Davidson H.I.M., Hawthorn J., Maskell L. The abdominal visceral innervation and the emetic reflex: Pathways, pharmacology, and plasticity. Can. J. Physiol. Pharmacol. 1990;68:325–345. doi: 10.1139/y90-047. PubMed DOI
Bauer J., Bollwahn W., Gareis M., Gedek B., Heinritzi K. Kinetic profiles of diacetoxyscirpenol and two of its metabolites in blood serum of pigs. Appl. Environ. Microbiol. 1985;49:842–845. doi: 10.1128/AEM.49.4.842-845.1985. PubMed DOI PMC
Bauer J., Gareis M., Gedek B. Metabolism of the trichothecenes T-2 toxin, diacetoxyscirpenol, and deoxynivalenol by farm animals. In: Chelkowski J., editor. Topics in Secondary Metabolism-Volume 2, Fusarium: Mycotoxins, Taxonomy and Pathogenicity. Elsevier; Amsterdam, The Netherlands: 1989. pp. 139–165.
Ueno Y. General toxicology. In: Ueno Y., editor. Trichothecenes: Chemical, Biological, and Toxicological Aspects. Elsevier; New York, NY, USA: 1983. pp. 135–146.
Coppock R.W., Gelberg H.B., Hoffmann W.E., Buck W.B. The acute toxicopathy of intravenous diacetoxyscirpenol (anguidine) administration in swine. Fundam. Appl. Toxicol. 1985;5:1034–1049. doi: 10.1016/0272-0590(85)90140-X. PubMed DOI
Coppock R.W., Hoffmann W.E., Gelberg H.B., Bass D., Buck W.B. Hematologic changes induced by intravenous administration of diacetoxyscirpenol in pigs, dogs, and calves. Am. J. Veter-Res. 1989;50:411–415. PubMed
Hornby P.J. Central neurocircuitry associated with emesis. Am. J. Med. 2001;111:106S–112S. doi: 10.1016/S0002-9343(01)00849-X. PubMed DOI
Johnston K.D., Lu Z., Rudd J.A. Looking beyond 5-HT3 receptors: A review of the wider role of serotonin in the pharmacology of nausea and vomiting. Eur. J. Pharmacol. 2014;722:13–25. doi: 10.1016/j.ejphar.2013.10.014. PubMed DOI
Naylor R., Rudd J.A. Mechanisms of chemotherapy/radiotherapy-induced emesis in animal models. Oncology. 1996;53:8–17. doi: 10.1159/000227634. PubMed DOI
Navari R.M., Aapro M. Antiemetic prophylaxis for chemotherapy-induced nausea and vomiting. N. Engl. J. Med. 2016;374:1356–1367. doi: 10.1056/NEJMra1515442. PubMed DOI
Koga T., Fukuda H. Descending pathway from the central pattern generator of vomiting. NeuroReport. 1997;8:2587–2590. doi: 10.1097/00001756-199707280-00033. PubMed DOI
Le Roux C.W., Borg C.-M., Murphy K.G., Vincent R.P., Ghatei M.A., Bloom S.R. Supraphysiological doses of intravenous PYY3-36 cause nausea, but no additional reduction in food intake. Ann. Clin. Biochem. Int. J. Lab. Med. 2008;45:93–95. doi: 10.1258/acb.2007.007068. PubMed DOI
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 trichothecene deoxynivalenol (vomitoxin) Toxicol. Sci. 2013;133:186–195. doi: 10.1093/toxsci/kft033. PubMed DOI PMC
Rojas C., Raje M., Tsukamoto T., Slusher B.S. Molecular mechanisms of 5-HT3 and NK1 receptor antagonists in prevention of emesis. Eur. J. Pharmacol. 2014;722:26–37. doi: 10.1016/j.ejphar.2013.08.049. PubMed DOI
Hesketh P.J. Chemotherapy-induced nausea and vomiting. N. Engl. J. Med. 2008;358:2482–2494. doi: 10.1056/NEJMra0706547. PubMed DOI
Kovac A.L. Comparative pharmacology and guide to the use of the serotonin 5-HT3 receptor antagonists for postoperative nausea and vomiting. Drugs. 2016;76:1719–1735. doi: 10.1007/s40265-016-0663-3. PubMed DOI
Du Bois A., Vach W., Kiechle M., Cramer-Giraud U., Meerpohl H.G. Pathophysiology, Severity, Pattern, and Risk Factors for Carboplatin-induced Emesis. Oncology. 1996;53:46–50. doi: 10.1159/000227640. PubMed DOI
Perry M.R., Rhee J., Smith W.L. Plasma levels of peptide YY correlate with Cisplatin-induced emesis in dogs. J. Pharm. Pharmacol. 1994;46:553–557. doi: 10.1111/j.2042-7158.1994.tb03855.x. PubMed DOI
Wu W., Bates M.A., Bursian S.J., Link J.E., Flannery B.M., Sugita-Konishi Y., Watanabe M., Zhang H., Pestka J.J. Comparison of emetic potencies of the 8-ketotrichothecenes deoxynivalenol, 15-acetyldeoxynivalenol, 3-acetyldeoxynivalenol, fusarenon X, and nivalenol. Toxicol. Sci. 2012;131:279–291. doi: 10.1093/toxsci/kfs286. PubMed DOI PMC
Wu W., Zhou H.-R., Bursian S.J., Link J.E., Pestka J.J. Emetic responses to T-2 toxin, HT-2 toxin and emetine correspond to plasma elevations of peptide YY3–36 and 5-hydroxytryptamine. Arch. Toxicol. 2015;90:997–1007. doi: 10.1007/s00204-015-1508-7. PubMed DOI PMC
Wu W., Zhou H.-R., Bursian S.J., Pan X., Link J.E., Berthiller F., Adam G., Krantis A., Durst T., Pestka J.J., 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. Toxicol. Sci. 2014;142:167–181. doi: 10.1093/toxsci/kfu166. PubMed DOI PMC
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. doi: 10.1093/toxsci/kft335. PubMed DOI PMC
Horn C.C. Why is the neurobiology of nausea and vomiting so important? Appetite. 2007;50:430–434. doi: 10.1016/j.appet.2007.09.015. PubMed DOI PMC
Du Sert N.P., Holmes A.M., Wallis R., Andrews P.L. Predicting the emetic liability of novel chemical entities: A comparative study. Br. J. Pharmacol. 2012;165:1848–1867. doi: 10.1111/j.1476-5381.2011.01669.x. PubMed DOI PMC
Du Sert N.P., Rudd J.A., Apfel C.C., Andrews P.L.R. Cisplatin-induced emesis: Systematic review and meta-analysis of the ferret model and the effects of 5-HT3 receptor antagonists. Cancer Chemother. Pharmacol. 2010;67:667–686. doi: 10.1007/s00280-010-1339-4. PubMed DOI PMC
Kottschade L., Novotny P., Lyss A., Mazurczak M., Loprinzi C., Barton D.L. Chemotherapy-induced nausea and vomiting: Incidence and characteristics of persistent symptoms and future directions NCCTG N08C3 (Alliance) Support. Care Cancer. 2016;24:2661–2667. doi: 10.1007/s00520-016-3080-y. PubMed DOI PMC
Kris M.G., Gralla R.J., Clark R.A., Tyson L.B., O’Connell J.P., Wertheim M.S., Kelsen D.P. Incidence, course, and severity of delayed nausea and vomiting following the administration of high-dose cisplatin. J. Clin. Oncol. 1985;3:1379–1384. doi: 10.1200/JCO.1985.3.10.1379. PubMed DOI
Tohmola N., Johansson A., Sane T., Renkonen R., Hämäläinen E., Itkonen O. Transient elevation of serum 5-HIAA by dietary serotonin and distribution of 5-HIAA in serum protein fractions. Ann. Clin. Biochem. Int. J. Lab. Med. 2014;52:428–433. doi: 10.1177/0004563214554842. PubMed DOI
Bearcroft C.P., Farthing M.J.G., Perrett D. Determination of 5-hydroxytryptamine, 5-hydroxyindoleacetic acid and tryptophan in plasma and urine by HPLC with fluorimetric detection. Biomed. Chromatogr. 1995;9:23–27. doi: 10.1002/bmc.1130090105. PubMed DOI
Kojima S.-I., Tohei A., Anzai N. A role for endogenous peptide YY in tachykinin NK2 receptor-triggered 5-HT release from guinea pig isolated colonic mucosa. Br. J. Pharmacol. 2012;167:1362–1368. doi: 10.1111/j.1476-5381.2012.02094.x. PubMed DOI PMC
Prelusky D.B., Trenholm H.L. The efficacy of various classes of anti-emetics in preventing deoxynivalenol-induced vomiting in swine. Nat. Toxins. 1993;1:296–302. doi: 10.1002/nt.2620010508. PubMed DOI
Fioramonti J., Dupuy C., Dupuy J., Bueno L. The mycotoxin, deoxynivalenol, delays gastric emptying through serotonin-3 receptors in rodents. J. Pharmacol. Exp. Ther. 1993;266:1255–1260. PubMed
Halatchev I.G., Cone R.D. Peripheral administration of PYY3–36 produces conditioned taste aversion in mice. Cell Metab. 2005;1:159–168. doi: 10.1016/j.cmet.2005.02.003. PubMed DOI
Zhang J., Jia H., Wang Q., Wu W., Zhang H. Role of peptide YY3-36 and glucose-dependent insulinotropic polypeptide in anorexia induction by trichothecences t-2 toxin, ht-2 toxin, diacetoxyscirpenol, and neosolaniol. Toxicol. Sci. 2017;159:203–210. doi: 10.1093/toxsci/kfx128. PubMed DOI
Zhang J., Sheng K., Wu W., Zhang H. Anorectic responses to T-2 toxin, HT-2 toxin, diacetoxyscirpenol and neosolaniol correspond to plasma elevations of neurotransmitters 5-hydroxytryptamine and substance P. Ecotoxicol. Environ. Saf. 2018;161:451–458. doi: 10.1016/j.ecoenv.2018.06.005. PubMed DOI
Sheng K., Zhang H., Yue J., Gu W., Gu C., Zhang H., Wu W. Anorectic response to the trichothecene T-2 toxin correspond to plasma elevations of the satiety hormone glucose-dependent insulinotropic polypeptide and peptide YY 3-36. Toxicology. 2018:28–36. doi: 10.1016/j.tox.2018.04.007. PubMed DOI