Effects of a single exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on macro- and microstructures of feeding and drinking in two differently TCDD-sensitive rat strains

Pharmacology Biochemistry and Behavior

Volumn 99, Issue 3, 2011, Pages 487-499

  Lensu, Sanna ^a,b   Tiittanen, Pekka ^a   Lindén, Jere ^c   Tuomisto, Jouko ^a   Pohjanvirta, Raimo ^c  

^a NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

^b UNIVERSITY OF EASTERN FINLAND   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

2,3,7,8 Tetrachlorodibenzo p dioxin, TCDD; Automated monitoring; Drinking; Feeding; Rat strain differences; Wasting syndrome

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; AROMATIC HYDROCARBON RECEPTOR;

ANIMAL EXPERIMENT; CIRCADIAN RHYTHM; COMPARATIVE STUDY; CONFERENCE PAPER; DARKNESS; DRINKING; DRINKING BEHAVIOR; FEEDING; FEEDING BEHAVIOR; FOOD INTAKE; HAN WISTAR RAT; HYPOPHAGIA; LIGHT DARK CYCLE; LONG EVANS RAT; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; RAT STRAIN; TIME;

ANIMALS; CIRCADIAN RHYTHM; DRINKING BEHAVIOR; DRUG RESISTANCE; FEEDING BEHAVIOR; MALE; RATS; RATS, INBRED STRAINS; SPECIES SPECIFICITY; TETRACHLORODIBENZODIOXIN;

RATTUS;

EID: 79959847230     PISSN: 00913057     EISSN: 18735177     Source Type: Journal    
DOI: 10.1016/j.pbb.2011.04.022     Document Type: Conference Paper

References (73)

1. Birnbaum LS, Tuomisto J. Non-carcinogenic effects of TCDD in animals. Food Addit Contam 2000;17:275-88. (Pubitemid 30410586)
2. Bock KW, Köhle C. Ah receptor: dioxin-mediated toxic responses as hints to deregulated physiologic functions. Biochem Pharmacol 2006;72:393-404. (Pubitemid 44061741)
3. Brobeck JR. Neural regulation of food intake. Ann NY Acad Sci 1955;63:44-55.
4. Christian BJ, Inhorn SL, Peterson RE. Relationship of the wasting syndrome to lethality in rats treated with 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol Appl Pharmacol 1986;82:239-55.
5. Cottone P, Sabino V, Steardo L, Zorrilla EP. FG 7142 specifically reducesmeal size and the rate and regularity of sustained feeding in female rats: evidence that benzodiazepine inverse agonists reduce food palatability. Neuropsychopharmacology 2007;32:1069-81. (Pubitemid 46631985)
6. Donhoffer S. Body size and metabolic rate: exponent and coefficient of the allometric equation. The role of units. J Theor Biol 1986;119:125-37.
7. Elander L, Engstrom L, Hallbeck M, Blomqvist A. IL-1 beta and LPS induce anorexia by distinct mechanisms differentially dependent on microsomal prostaglandin E synthase-1. Am J Physiol Regul Integr Comp Physiol 2007;292:R258-67.
8. Fantino M, Cabanac M. Body-weight regulation with a proportional hoarding response in the rat. Physiol Behav 1980;24:939-42. (Pubitemid 10052652)
9. Fekete EM, Inoue K, Zhao Y, Rivier JE, Vale WW, Szucs A, et al. Delayed satiety-like actions and altered feeding microstructure by a selective type 2 corticotropin-releasing factor agonist in rats: intra-hypothalamic urocortin 3 administration reduces food intake by prolonging the post-meal interval. Neuropsychopharmacology 2007;32:1052-68. (Pubitemid 46631977)
10. Feldman HA, McMahon TA. The mass exponent for energy metabolism is not a statistical artifact. Respir Physiol 1983;52:149-63. (Pubitemid 13055195)
11. Fitzsimons TJ, Le Magnen J. Eating as a regulatory control of drinking in the rat. J Comp Physiol Psychol 1969;67:273-83.
12. Furness SGB, Whelan F. The pleiotropy of dioxin toxicity-xenobiotic misappropriation of the aryl hydrocarbon receptor's alternative physiological roles. Pharmacol Ther 2009;124:336-53.
13. Gasiewicz TA, Neal RA. 2,3,7,8-Tetrachlorodibenzo-p-dioxin tissue distribution, excretion, and effects on clinical chemical parameters in guinea pigs. Toxicol Appl Pharmacol 1979;51:329-39.
14. Gasiewicz TA, Holscher MA, Neal RA. The effect of total parenteral nutrition on the toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin in the rat. Toxicol Appl Pharmacol 1980;54:469-88.
15. Geary N, Asarian L, Sheahan J, Langhans W. Estradiol-mediated increases in the anorexia induced by intraperitoneal injection of bacterial lipopolysaccharide in female rats. Physiol Behav 2004;82:251-61. (Pubitemid 38981610)
16. Giannakopoulos G, Galanopoulou P, Daifotis Z, Couvaris C. Effects of mesulergine treatment on diet selection, brain serotonin (5-HT) and dopamine (DA) turnover in free feeding rats. Prog Neuropsychopharmacol Biol Psychiatry 1998;22:803-13. (Pubitemid 28396345)
17. Glendinning JI, Smith JC. Consistency of meal patterns in laboratory rats. Physiol Behav 1994;56:7-16. (Pubitemid 24223336)
18. Hakk H, Diliberto JJ, Birnbaum LS. The effect of dose on 2,3,7,8-TCDD tissue distribution, metabolism and elimination in CYP1A2 (-/-) knockout and C57BL/6 N parental strains of mice. Toxicol Appl Pharmacol 2009;241:119-26.
19. Hillebrand JJG, Kas MJH, Adan RAH. To eat or not to eat; regulation by the melanocortin system. Physiol Behav 2006;89:97-102. (Pubitemid 44148659)
20. Hulsey MG, Lu H, Wang T, Martin RJ, Baile CA. Intracerebroventricular (i.c.v.) administration of mouse leptin in rats: behavioral specificity and effects on meal patterns. Physiol Behav 1998;65:445-55. (Pubitemid 29015760)
21. Johnson AW, Sherwood A, Smith DR, Wosiski-Kuhn M, Gallagher M, Holland PC. An analysis of licking microstructure in three strains of mice. Appetite 2010;54:320-30.
22. Keen-Rhinehart E, Dailey MJ, Bartness T. Physiological mechanisms for food-hoarding motivation in animals. Philos Trans R Soc B 2010;365:961-75.
23. Kelling CK, Christian BJ, Inhorn SL, Peterson RE. Hypophagia-induced weight loss in mice, rats, and guinea pigs treated with 2,3,7,8- tetrachlorodibenzo-p-dioxin. Fundam Appl Toxicol 1985;5:700-12.
24. KorkalainenM, Lindén J, Tuomisto J, Pohjanvirta R. Effect of TCDD on mRNA expression of genes encoding bHLH/PAS proteins in rat hypothalamus. Toxicology 2005;208:1-11. (Pubitemid 40143323)
25. Laviano A, Meguid MM, Cascino A, Molfino A, Fanelli FR. Tryptophan in wasting diseases: at the crossing between immune function and behavior. Curr Opin Clin Nutr Metab Care 2009;12:392-7.
26. Lensu S, Tiittanen P, Pohjanvirta R. Circadian differences between two rat strains in their feeding and drinking micro- and macrostructures. Biol Rhythm Res 2011a: 1-21, doi:10.1080/09291016.2010.525381 iFirst article.
27. Lensu S, Tuomisto JT, Tuomisto J, Pohjanvirta R. Characterization of the 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD)-provoked strong and rapid aversion to unfamiliar foodstuffs in rats. Toxicol 2011b;283:140-50.
28. Lensu S, Tuomisto JT, Tuomisto J, Viluksela M, Niittynen M, Pohjanvirta R. Immediate and highly sensitive aversion response to a novel food item linked to AH receptor stimulation. Toxicol Lett 2011c;203:252-7.
29. Lindén J, Korkalainen M, Lensu S, Tuomisto J, Pohjanvirta R. Effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) and leptin on hypothalamic mRNA expression of factors participating in food intake regulation in a TCDD-sensitive and a TCDD-resistant rat strain. J Biochem Mol Toxicol 2005;19:139-48.
30. Lindén J, Lensu S, Tuomisto J, Pohjanvirta R. Dioxins, the aryl hydrocarbon receptor and the central regulation of energy balance. Front Neuroendocrinol 2010;31:452-78.
31. Mandal PK. Dioxin: a review of its environmental effects and its aryl hydrocarbon receptor biology. J Comp Physiol B 2005;175:221-30. (Pubitemid 40764087)
32. Meguid MM, Fetissov SO, Varma M, Sato T, Zhang L, Laviano A, et al. Hypothalamic dopamine and serotonin in the regulation of food intake. Nutrition 2000a;16: 843-57.
33. Meguid MM, Sato T, Torelli GF, Laviano A, Fanelli FR. An analysis of temporal changes in meal number and meal size at onset of anorexia in male tumor-bearing rats. Nutrition 2000b;16:305-6. (Pubitemid 30176060)
34. Mukai M, Tischkau SA. Effects of tryptophan photoproducts in the circadian timing system: searching for a physiological role for aryl hydrocarbon receptor. Toxicol Sci 2007;95:172-81. (Pubitemid 44942787)
35. Mukai M, Lin T-M, Peterson RE, Cooke PS, Tischkau SA. Behavioral rhythmicity of mice lacking AhR and attenuation of light-induced phase shift by 2,3,7,8-tetrachlorodibenzo-p-dioxin. J Biol Rhythms 2008;23:200-10. (Pubitemid 351652366)
36. Pohjanvirta R. Transgenic mouse lines expressing rat AH receptor variants-a new animal model for research on AH receptor function and dioxin toxicity mechanisms. Toxicol Appl Pharmacol 2009;236:166-82.
37. Pohjanvirta R, Tuomisto J. Han/Wistar rats are exceptionally resistant to TCDD. II. Arch Toxicol Suppl 1987;11:344-7. (Pubitemid 17091603)
38. Pohjanvirta R, Tuomisto J. 2,3,7,8-Tetrachlorodibenzo-p-dioxin enhances responsiveness to post-ingestive satiety signals. Toxicology 1990a;63:285-99.
39. Pohjanvirta R, Tuomisto J. Remarkable residual alterations in responses to feeding regulatory challenges in Han/Wistar rats after recovery from the acute toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD). Food Chem Toxicol 1990b;28:677-86.
40. Pohjanvirta R, Tuomisto J. Short-term toxicity of 2,3,7,8- tetrachlorodibenzo-p-dioxin in laboratory animals: effects, mechanisms, and animal models. Pharmacol Rev 1994;46:483-549.
41. Pohjanvirta R, Tuomisto J, Vartiainen T, Rozman K. Han/Wistar rats are exceptionally resistant to TCDD. I. Pharmacol Toxicol 1987;60:145-50.
42. Pohjanvirta R, Tuomisto J, Vikkula K. Screening of pharmacological agents given peripherally with respect to TCDD-induced wasting syndrome in Long-Evans rats. Pharmacol Toxicol 1988;63:240-7.
43. Pohjanvirta R, Unkila M, Tuomisto J. The loss of glucoprivic feeding is an early-stage alteration in TCDD-treated Han/Wistar rats. Pharmacol Toxicol 1990a;67:441-3.
44. Pohjanvirta R, Vartiainen T, Uusi-Rauva A, Monkkonen J, Tuomisto J. Tissue distribution, metabolism, and excretion of 14 C-TCDD in a TCDD-susceptible and a TCDD-resistant rat strain. Pharmacol Toxicol 1990b;66:93-100. (Pubitemid 20105605)
45. Pohjanvirta R, Unkila M, Tuomisto J. Characterization of the enhanced responsiveness to postingestive satiety signals in 2,3,7,8-tetrachlorodibenzo-p- dioxin (TCDD)-treated Han/Wistar rats. Pharmacol Toxicol 1991;69:433-41.
46. Pohjanvirta R, Unkila M, Tuomisto J. Comparative acute lethality of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD), 1,2,3,7,8-pentachlorodibenzo-p- dioxin and 1,2,3,4,7,8-hexachlorodibenzo-p-dioxin in the most TCDD-susceptible and the most TCDD-resistant rat strain. Pharmacol Toxicol 1993;73:52-6.
47. Pohjanvirta R, Unkila M, Tuomisto J. TCDD-induced hypophagia is not explained by nausea. Pharmacol Biochem Behav 1994;47:273-82. (Pubitemid 24034962)
48. Pohjanvirta R, Wong JM, Li W, Harper PA, Tuomisto J, Okey AB. Point mutation in intron sequence causes altered carboxyl-terminal structure in the aryl hydrocarbon receptor of the most 2,3,7,8-tetrachlorodibenzo-p-dioxin- resistant rat strain. Mol Pharmacol 1998;54:86-93.
49. Potter CL, Menahan LA, Peterson RE. Relationship of alterations in energy metabolism to hypophagia in rats treated with 2,3,7,8-tetrachlorodibenzo-p- dioxin. Fundam Appl Toxicol 1986;6:89-97.
50. Qu XY, Metz RP, Porter WW, Neuendorff N, Earnest BJ, Earnest DJ. The clock genes period 1 and period 2 mediate diurnal rhythms in dioxin-induced Cyp1A1 expression in the mouse mammary gland and liver. Toxicol Lett 2010;196:28-32.
51. Rannug A, Fritsche E. The aryl hydrocarbon receptor and light. Biol Chem 2006;387:1149-57. (Pubitemid 44402061)
52. Reidelberger RD, Haver AC, Arnelo U, Smith DD, Schaffert CS, Permert J. Amylin receptor blockade stimulates food intake in rats. Am J Physiol Regul Integr Comp Physiol 2004;287:R568-74.
53. Richardson VM, Santostefano MJ, Birnbaum LS. Daily cycle of bHLH-PAS proteins, Ah receptor and Arnt, in multiple tissues of female Sprague-Dawley rats. Biochem Biophys Res Commun 1998;252:225-31. (Pubitemid 28534655)
54. Rosenwasser AM. Functional neuroanatomy of sleep and circadian rhythms. Brain Res Rev 2009;61:281-306.
55. Seefeld MD, Peterson RE. Digestible energy and efficiency of feed utilization in rats treated with 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol Appl Pharmacol 1984;74:214-22.
56. Seefeld MD, Corbett SW, Keesey RE, Peterson RE. Characterization of the wasting syndrome in rats treated with 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol Appl Pharmacol 1984a;73:311-22.
57. Seefeld MD, Keesey RE, Peterson RE. Body weight regulation in rats treated with 2,3,7,8-tetrachlorodibenzo-p-dioxin. Toxicol Appl Pharmacol 1984b;76:526-36.
58. Shimba S, Watabe Y. Crosstalk between the AHR signaling pathway and circadian rhythm. Biochem Pharmacol 2009;77:560-5.
59. Simanainen U, Tuomisto JT, Tuomisto J, Viluksela M. Structure-activity relationships and dose responses of polychlorinated dibenzo-p-dioxins for short-term effects in 2,3,7,8-tetrachlorodibenzo-p-dioxin-resistant and -sensitive rat strains. Toxicol Appl Pharmacol 2002;181:38-47.
60. Sirkka U, Pohjanvirta R, Nieminen SA, Tuomisto J, Ylitalo P. Acute neurobehavioural effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in Han/Wistar rats. Pharmacol Toxicol 1992;71:284-8.
61. Tuomisto JT, Pohjanvirta R, Unkila M, Tuomisto J. TCDD-induced anorexia and wasting syndrome in rats: effects of diet-induced obesity and nutrition. Pharmacol Biochem Behav 1999a;62:735-42. (Pubitemid 29127179)
62. Tuomisto JT, Viluksela M, Pohjanvirta R, Tuomisto J. The AH receptor and a novel gene determine acute toxic responses to TCDD: segregation of the resistant alleles to different rat lines. Toxicol Appl Pharmacol 1999b;155:71-81. (Pubitemid 29102763)
63. Tuomisto JT, Viluksela M, Pohjanvirta R, Tuomisto J. Changes in food intake and food selection in rats after 2,3,7, 8-tetrachlorodibenzo-p-dioxin (TCDD) exposure. Pharmacol Biochem Behav 2000;65:381-7.
64. Unkila M, Pohjanvirta R, MacDonald E, Tuomisto JT, Tuomisto J. Dose response and time course of alterations in tryptophan metabolism by 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in the most TCDD-susceptible and the most TCDD-resistant rat strain: relationship with TCDD lethality. Toxicol Appl Pharmacol 1994;128:280-92.
65. Unkila M, Pohjanvirta R, Tuomisto J. Biochemical effects of 2,3,7,8-tetrachlorodibenzop-dioxin (TCDD) and related compounds on the central nervous system. Int J Biochem Cell Biol 1995;27:443-55.
66. van Dijk G, Thiele TE. Glucagon-like peptide-1 (7-36) amide: a central regulator of satiety and interoceptive stress. Neuropeptides 1999;33:406-14.
67. Vartiainen T, Lampi P, Tuomisto JT, Tuomisto J. Polychlorodibenzo-p- dioxin and polychlorodibenzofuran concentrations in human fat samples in a village after pollution of drinking water with chlorophenols. Chemosphere 1995;30:1429-38.
68. Viluksela M, Stahl BU, Birnbaum LS, Schramm KW, Kettrup A, Rozman KK. Subchronic/chronic toxicity of a mixture of four chlorinated dibenzo-p-dioxins in rats. I. Design, general observations, hematology, and liver concentrations. Toxicol Appl Pharmacol 1998;151:57-69.
69. Weber LW, Lebofsky M, Stahl BU, Gorski JR, Muzi G, Rozman K. Reduced activities of key enzymes of gluconeogenesis as possible cause of acute toxicity of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) in rats. Toxicology 1991;66:133-44.
70. West AR, Galloway MP. Regulation of serotonin-facilitated dopamine release in vivo: the role of protein kinase A activating transduction mechanisms. Synapse 1996;23:20-7. (Pubitemid 26138644)
71. Xu CX, Krager SL, Liao DF, Tischkau SA. Disruption of CLOCK-BMAL1 transcriptional activity is responsible for aryl hydrocarbon receptor-mediated regulation of period 1 gene. Toxicol Sci 2010;115:98-108.
72. Zeger SL, Liang KY. Longitudinal data-analysis for discrete and continuous outcomes. Biometrics 1986;42:121-30.
73. Zorrilla EP, Inoue K, Fekete EM, Tabarin A, Valdez GR, Koob GF. Measuring meals: structure of prandial food and water intake of rats. Am J Physiol Regul Integr Comp Physiol 2005;288:R1450-67.