Anorexia induction by the trichothecene deoxynivalenol (vomitoxin) is mediated by the release of the gut satiety hormone peptide YY

Toxicological Sciences

Volumn 130, Issue 2, 2012, Pages 289-297

  Flannery, Brenna M ^a,b   Clark, Erica S ^a,b   Pestka, James J ^a,b,c  

^a Michigan State University   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

^c NONE   (United States)

Author keywords

Anorexia; Cholecystokinin; Deoxynivalenol; Mouse; Peptide YY

Indexed keywords

AMYLIN; CHOLECYSTOKININ; DEVAZEPIDE; GASTRIC INHIBITORY POLYPEPTIDE; GHRELIN; GLUCAGON LIKE PEPTIDE 1; LEPTIN; N [2 [1,2 DIHYDRO 3,5(4H) DIOXO 1,2 DIPHENYL 1,2,4 TRIAZOL 4 YL]ETHYL] N2 [[1 [2 [4 [5,11 DIHYDRO 6(6H) OXODIBENZ[B,E]AZEPIN 11 YL] 1 PIPERAZINYL] 2 OXOETHYL]CYCLOPENTYL]ACETYL]ARGININAMIDE; PANCREAS POLYPEPTIDE; PEPTIDE YY; VOMITOXIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ANOREXIA; ARTICLE; CONTROLLED STUDY; FEMALE; FOOD INTAKE; GROWTH INHIBITION; HORMONE RELEASE; INTESTINE; MOUSE; NONHUMAN; PROTEIN BLOOD LEVEL; SATIETY;

ADMINISTRATION, ORAL; ANIMALS; ANOREXIA; APPETITE DEPRESSANTS; APPETITE REGULATION; ARGININE; BEHAVIOR, ANIMAL; BENZAZEPINES; CHOLECYSTOKININ; DEVAZEPIDE; DOSE-RESPONSE RELATIONSHIP, DRUG; EATING; FEMALE; FOOD CONTAMINATION; INJECTIONS, INTRAPERITONEAL; MICE; MYCOTOXINS; PEPTIDE YY; RECEPTORS, CHOLECYSTOKININ; RECEPTORS, NEUROPEPTIDE Y; SATIATION; TIME FACTORS; TRICHOTHECENES;

ANIMALIA;

EID: 84869401179     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfs255     Document Type: Article

References (50)

1. Adrian, T. E., Ferri, G. L., Bacarese-Hamilton, A. J., Fuessl, H. S., Polak, J. M., and Bloom, S. R. (1985). Human distribution and release of a putative new gut hormone, peptide YY. Gastroenterology 89, 1070-1077.
2. Amuzie, C. J., and Pestka, J. J. (2010). Suppression of insulin-like growth factor acid-labile subunit expression-a novel mechanism for deoxynivalenol-induced growth retardation. Toxicol. Sci. 113, 412-421.
3. Arnold, D. L., McGuire, P. F., Nera, E. A., Karpinski, K. F., Bickis, M. G., Zawidzka, Z. Z., Fernie, S., and Vesonder, R. F. (1986). The toxicity of orally administered deoxynivalenol (vomitoxin) in rats and mice. Food Chem. Toxicol. 24, 935-941.
4. Azcona-Olivera, J. I., Ouyang, Y., Murtha, J., Chu, F. S., and Pestka, J. J. (1995). Induction of cytokine mRNAs in mice after oral exposure to the trichothecene vomitoxin (deoxynivalenol): Relationship to toxin distribution and protein synthesis inhibition. Toxicol. Appl. Pharmacol. 133, 109-120.
5. Brothers, S. P., Saldanha, S. A., Spicer, T. P., Cameron, M., Mercer, B. A., Chase, P., McDonald, P., Wahlestedt, C., and Hodder, P. S. (2010). Selective and brain penetrant neuropeptide y y2 receptor antagonists discovered by whole-cell high-throughput screening. Mol. Pharmacol. 77, 46-57.
6. Brown, T. A., Washington, M. C., Metcalf, S. A., and Sayegh, A. I. (2011). The feeding responses evoked by cholecystokinin are mediated by vagus and splanchnic nerves. Peptides 32, 1581-1586.
7. Canady, R. A., Coker, R. D., Rgan, S. K., Krska, R., Kuiper-Goodman, T., Olsen, M., Pestka, J. J., Resnik, S., and Schlatter, J. (2001). Deoxynivalenol. In Safety Evaluation of Certain Mycotoxins in Food. Fifty-Sixth Report of The Joint Fao /Who Expert Committee on Food Additives, International Programme on Chemical Safety, pp. 420-555. World Health Organization, Geneva.
8. Challis, B. G., Pinnock, S. B., Coll, A. P., Carter, R. N., Dickson, S. L., and O'Rahilly, S. (2003). Acute effects of PYY3-36 on food intake and hypothalamic neuropeptide expression in the mouse. Biochem. Biophys. Res. Commun. 311, 915-919.
9. Chua, A. S., Keeling, P. W., and Dinan, T. G. (2006). Role of cholecystokinin and central serotonergic receptors in functional dyspepsia. World J. Gastroenterol. 12, 1329-1335.
10. de Lartigue, G., Dimaline, R., Varro, A., and Dockray, G. J. (2007). Cocaineand amphetamine-regulated transcript: Stimulation of expression in rat vagal afferent neurons by cholecystokinin and suppression by ghrelin. J. Neurosci. 27, 2876-2882.
11. Degen, L., Oesch, S., Casanova, M., Graf, S., Ketterer, S., Drewe, J., and Beglinger, C. (2005). Effect of peptide YY3-36 on food intake in humans. Gastroenterology 129, 1430-1436.
12. Fioramonti, J., Dupuy, C., Dupuy, J., and Bueno, L. (1993). The mycotoxin, deoxynivalenol, delays gastric emptying through serotonin-3 receptors in rodents. J. Pharmacol. Exp. Ther. 266, 1255-1260.
13. Flannery, B. M., Wu, W., and Pestka, J. J. (2011). Characterization of deoxynivalenol-induced anorexia using mouse bioassay. Food Chem. Toxicol. 49, 1863-1869.
14. Forsyth, D. M., Yoshizawa, T., Morooka, N., and Tuite, J. (1977). Emetic and refusal activity of deoxynivalenol to swine. Appl. Environ. Microbiol. 34, 547-552.
15. Gantz, I., Erondu, N., Mallick, M., Musser, B., Krishna, R., Tanaka, W. K., Snyder, K., Stevens, C., Stroh, M. A., Zhu, H., et al. (2007). Efficacy and safety of intranasal peptide YY3-36 for weight reduction in obese adults. J. Clin. Endocrinol. Metab. 92, 1754-1757.
16. Germain, N., Galusca, B., Le Roux, C. W., Bossu, C., Ghatei, M. A., Lang, F., Bloom, S. R., and Estour, B. (2007). Constitutional thinness and lean anorexia nervosa display opposite concentrations of peptide YY, glucagon-like peptide 1, ghrelin, and leptin. Am. J. Clin. Nutr. 85, 967-971.
17. Gibbs, J., Falasco, J. D., and McHugh, P. R. (1976). Cholecystokinin-decreased food intake in rhesus monkeys. Am. J. Physiol. 230, 15-18.
18. Girardet, C., Bonnet, M. S., Jdir, R., Sadoud, M., Thirion, S., Tardivel, C., Roux, J., Lebrun, B., Mounien, L., Trouslard, J., et al. (2011a). Central inflammation and sickness-like behavior induced by the food contaminant deoxynivalenol: A PGE2-independent mechanism. Toxicol. Sci. 124, 179-191.
19. Girardet, C., Bonnet, M. S., Jdir, R., Sadoud, M., Thirion, S., Tardivel, C., Roux, J., Lebrun, B., Wanaverbecq, N., Mounien, L., et al. (2011b). The food-contaminant deoxynivalenol modifies eating by targeting anorexigenic neurocircuitry. PLOS ONE 6, e26134.
20. Glendinning, J. I. (2007). How do predators cope with chemically defended foods? Biol. Bull. 213, 252-266.
21. Goyarts, T., Dänicke, S., Rothkötter, H. J., Spilke, J., Tiemann, U., and Schollenberger, M. (2005). On the effects of a chronic deoxynivalenol intoxication on performance, haematological and serum parameters of pigs when diets are offered either for ad libitum consumption or fed restrictively. J. Vet. Med. A. Physiol. Pathol. Clin. Med. 52, 305-314.
22. Harding, R. K., and McDonald, T. J. (1989). Identification and characterization of the emetic effects of peptide YY. Peptides 10, 21-24.
23. Hughes, D. M., Gahl, M. J., Graham, C. H., and Grieb, S. L. (1999). Overt signs of toxicity to dogs and cats of dietary deoxynivalenol. J. Anim. Sci. 77, 693-700.
24. Jia, Q., and Pestka, J. J. (2005). Role of cyclooxygenase-2 in deoxynivalenol-induced immunoglobulin a nephropathy. Food Chem. Toxicol. 43, 721-728.
25. Kelley, K. W., Blutheacute; R. M., Dantzer, R., Zhou, J. H., Shen, W. H., Johnson, R. W., and Broussard, S. R. (2003). Cytokine-induced sickness behavior. Brain Behav. Immun. 17(Suppl. 1), S112-S118.
26. Khoo, J., Rayner, C. K., Feinle-Bisset, C., Jones, K. L., and Horowitz, M. (2010). Gastrointestinal hormonal dysfunction in gastroparesis and functional dyspepsia. Neurogastroenterol. Motil. 22, 1270-1278.
27. Krantis, A., and Durst, T. (2001). Methods and compositions for regulating gut motility. World Intellectual Property Organization. PCT/CA00/00790 Available at: http://www.wipo.int/patentscope/search/en/WO2001001968.
28. Lawson, E. A., Eddy, K. T., Donoho, D., Misra, M., Miller, K. K., Meenaghan, E., Lydecker, J., Herzog, D., and Klibanski, A. (2011). Appetite-regulating hormones cortisol and peptide YY are associated with disordered eating psychopathology, independent of body mass index. Eur. J. Endocrinol. 164, 253-261.
29. le Roux, C. W., Batterham, R. L., Aylwin, S. J., Patterson, M., Borg, C. M., Wynne, K. J., Kent, A., Vincent, R. P., Gardiner, J., Ghatei, M. A., et al. (2006). Attenuated peptide YY release in obese subjects is associated with reduced satiety. Endocrinology 147, 3-8.
30. Liddle, R. A., Green, G. M., Conrad, C. K., and Williams, J. A. (1986). Proteins but not amino acids, carbohydrates, or fats stimulate cholecystokinin secretion in the rat. Am. J. Physiol. 251(2 Pt 1), G243-G248.
31. Moran, T. H., Baldessarini, A. R., Salorio, C. F., Lowery, T., and Schwartz, G. J. (1997). Vagal afferent and efferent contributions to the inhibition of food intake by cholecystokinin. Am. J. Physiol. 272(4 Pt 2), R1245-R1251.
32. Moran, T. H., Smedh, U., Kinzig, K. P., Scott, K. A., Knipp, S., and Ladenheim, E. E. (2005). Peptide YY(3-36) inhibits gastric emptying and produces acute reductions in food intake in rhesus monkeys. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288, R384-R388.
33. Moschovi, M., Trimis, G., Vounatsou, M., Katsibardi, K., Margeli, A., Dimitriadi, F., Papassotiriou, I., Chrousos, G., and Tzortzatou-Stathopoulou, F. (2008). Serial plasma concentrations of PYY and ghrelin during chemotherapy in children with acute lymphoblastic leukemia. J. Pediatr. Hematol. Oncol. 30, 733-737.
34. Parker, S. L., and Balasubramaniam, A. (2008). Neuropeptide Y Y2 receptor in health and disease. Br. J. Pharmacol. 153, 420-431.
35. Parkinson, J. R., Dhillo, W. S., Small, C. J., Chaudhri, O. B., Bewick, G. A., Pritchard, I., Moore, S., Ghatei, M. A., and Bloom, S. R. (2008). PYY3-36 injection in mice produces an acute anorexigenic effect followed by a delayed orexigenic effect not observed with other anorexigenic gut hormones. Am. J. Physiol. Endocrinol. Metab. 294, E698-E708.
36. Perry, M. R., Rhee, J., and Smith, W. L. (1994). Plasma levels of peptide YY correlate with cisplatin-induced emesis in dogs. J. Pharm. Pharmacol. 46, 553-557.
37. Pestka, J. J. (2010). Deoxynivalenol: Mechanisms of action, human exposure, and toxicological relevance. Arch. Toxicol. 84, 663-679.
38. Pestka, J. J., and Amuzie, C. J. (2008). Tissue distribution and proinflammatory cytokine gene expression following acute oral exposure to deoxynivalenol: Comparison of weanling and adult mice. Food Chem. Toxicol. 46, 2826-2831.
39. Pestka, J. J., and Zhou, H. R. (2000). Interleukin-6-deficient mice refractory to IgA dysregulation but not anorexia induction by vomitoxin (deoxynivalenol) ingestion. Food Chem. Toxicol. 38, 565-575.
40. Pestka, J. J., and Zhou, H. R. (2002). Effects of tumor necrosis factor type 1 and 2 receptor deficiencies on anorexia, growth and IgA dysregulation in mice exposed to the trichothecene vomitoxin. Food Chem. Toxicol. 40, 1623-1631.
41. Pestka, J. J., Lin, W. S., and Miller, E. R. (1987). Emetic activity of the trichothecene 15-acetyldeoxynivalenol in swine. Food Chem. Toxicol. 25, 855-858.
42. Prelusky, D. B. (1994). The effect of deoxynivalenol on serotoninergic neurotransmitter levels in pig blood. J. Environ. Sci. Health B. 29, 1203-1218.
43. Prelusky, D. B., Hartin, K. E., Trenholm, H. L., and Miller, J. D. (1988). Pharmacokinetic fate of 14C-labeled deoxynivalenol in swine. Fundam. Appl. Toxicol. 10, 276-286.
44. Schwartz, M. W. (2006). Central nervous system regulation of food intake. Obesity (Silver Spring) 14(Suppl. 1), 1S-8S.
45. Schwartz, M. W., Woods, S. C., Porte, D., Jr, Seeley, R. J., and Baskin, D. G. (2000). Central nervous system control of food intake. Nature 404, 661-671.
46. Silver, A. J., Flood, J. F., and Morley, J. E. (1988). Effect of gastrointestinal peptides on ingestion in old and young mice. Peptides 9, 221-225.
47. Van Der Veek, P. P., Biemond, I., and Masclee, A. A. (2006). Proximal and distal gut hormone secretion in irritable bowel syndrome. Scand. J. Gastroenterol. 41, 170-177.
48. Weatherford, S. C., Chiruzzo, F. Y., and Laughton, W. B. (1992). Satiety induced by endogenous and exogenous cholecystokinin is mediated by CCK-A receptors in mice. Am. J. Physiol. 262(4 Pt 2), R574-R578.
49. Zhou, H. R., Harkema, J. R., Hotchkiss, J. A., Yan, D., Roth, R. A., and Pestka, J. J. (2000). Lipopolysaccharide and the trichothecene vomitoxin (deoxynivalenol) synergistically induce apoptosis in murine lymphoid organs. Toxicol. Sci. 53, 253-263.
50. Zhou, H. R., Yan, D., and Pestka, J. J. (1997). Differential cytokine mRNA expression in mice after oral exposure to the trichothecene vomitoxin (deoxynivalenol): Dose response and time course. Toxicol. Appl. Pharmacol. 144, 294-305.