Orexigenic response to tail pinch: Role of brain NPY1 and corticotropin releasing factor receptors

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 306, Issue 3, 2014, Pages

  Goebel Stengel, Miriam ^a,b   Stengel, Andreas ^a,c   Wang, Lixin ^a   Taché, Yvette ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MARTIN LUTHER KRANKENHAUS   (Germany)

^c CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

Corticotropin releasing factor; Fecal pellet output; Food intake; Fos; Ghrelin; Neuropeptide Y; Somatostatin receptor 2 antagonist; Stress induced eating; Tail pinch

Indexed keywords

ASTRESSIN; CORTICOTROPIN; CORTICOTROPIN RELEASING FACTOR ANTAGONIST; CORTICOTROPIN RELEASING FACTOR RECEPTOR; GHRELIN; NALPHA (DIPHENYLACETYL) N (4 HYDROXYBENZYL) DEXTRO ARGININAMIDE; NEUROPEPTIDE Y1 RECEPTOR; S 406028; UNCLASSIFIED DRUG;

ADULT; ANIMAL EXPERIMENT; APPETITE; ARTICLE; BODY COMPOSITION; BRAIN FUNCTION; CONTROLLED STUDY; DEFECATION; FOOD INTAKE; GLUCOSE BLOOD LEVEL; HAFFNER TAIL PINCH TEST; LEAN BODY WEIGHT; MALE; MECHANICAL STIMULUS TEST; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; RAT; RHOMBENCEPHALON; SIGNAL TRANSDUCTION; SPRAGUE DAWLEY RAT; TAIL PINCH; WEIGHT GAIN; WEIGHT REDUCTION;

BODY WEIGHT; CORTICOTROPIN RELEASING FACTOR; FECAL PELLET OUTPUT; FOOD INTAKE; FOS; GHRELIN; NEUROPEPTIDE Y; SOMATOSTATIN RECEPTOR 2 ANTAGONIST; STRESS-INDUCED EATING; TAIL PINCH;

ANIMALS; ARGININE; BODY WEIGHT; BRAIN; CORTICOTROPIN-RELEASING HORMONE; EATING; GHRELIN; MALE; NEURONS; NEUROPEPTIDE Y; PEPTIDE FRAGMENTS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, CORTICOTROPIN-RELEASING HORMONE; SOMATOSTATIN;

EID: 84893342893     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00335.2013     Document Type: Article

References (72)

1. Abbott SB, Kanbar R, Bochorishvili G, Coates MB, Stornetta RL, Guyenet PG. C1 neurons excite locus coeruleus and A5 noradrenergic neurons along with sympathetic outflow in rats. J Physiol 590: 2897-2915, 2012.
2. Amer A, Breu J, McDermott J, Wurtman RJ, Maher TJ. 5-Hydroxy-L-tryptophan suppresses food intake in food-deprived and stressed rats. Pharmacol Biochem Behav 77: 137-143, 2004.
3. Antelman SM, Rowland N. Endogenous opiates and stress-induced eating. Science 214: 1149-1151, 1981.
4. Antelman SM, Szechtman H. Tail pinch induces eating in sated rats which appears to depend on nigrostriatal dopamine. Science 189: 731-733, 1975.
5. Antelman SM, Szechtman H, Chin P, Fisher AE. Tail pinch-induced eating, gnawing and licking behavior in rats: dependence on the nigrostriatal dopamine system. Brain Res 99: 319-337, 1975.
6. Asakawa A, Inui A, Kaga T, Yuzuriha H, Nagata T, Fujimiya M, Katsuura G, Makino S, Fujino MA, Kasuga M. A role of ghrelin in neuroendocrine and behavioral responses to stress in mice. Neuroendocrinology 74: 143-147, 2001.
7. Basa NR, Wang L, Arteaga JR, Heber D, Livingston EH, Taché Y. Bacterial lipopolysaccharide shifts fasted plasma ghrelin to postprandial levels in rats. Neurosci Lett 343: 25-28, 2003.
8. Calvez J, Fromentin G, Nadkarni N, Darcel N, Even P, Tome D, Ballet N, Chaumontet C. Inhibition of food intake induced by acute stress in rats is due to satiation effects. Physiol Behav 104: 675-683, 2011.
9. Cescato R, Erchegyi J, Waser B, Piccand V, Maecke HR, Rivier JE, Reubi JC. Design and in vitro characterization of highly sst2-selective somatostatin antagonists suitable for radiotargeting. J Med Chem 51: 4030-4037, 2008.
10. Chotiwat C, Harris RB. Antagonism of specific corticotropin-releasing factor receptor subtypes selectively modifies weight loss in restrained rats. Am J Physiol Regul Integr Comp Physiol 295: R1762-R1773, 2008.
11. Cole RL, Sawchenko PE. Neurotransmitter regulation of cellular activation and neuropeptide gene expression in the paraventricular nucleus of the hypothalamus. J Neurosci 22: 959-969, 2002.
12. Dallman MF. Stress-induced obesity and the emotional nervous system. Trends Endocrinol Metab 21: 159-165, 2010.
13. Elias CF, Aschkenasi C, Lee C, Kelly J, Ahima RS, Bjorbaek C, Flier JS, Saper CB, Elmquist JK. Leptin differentially regulates NPY and POMC neurons projecting to the lateral hypothalamic area. Neuron 23: 775-786, 1999.
14. Erchegyi J, Grace CR, Samant M, Cescato R, Piccand V, Riek R, Reubi JC, Rivier JE. Ring size of somatostatin analogues (ODT-8) modulates receptor selectivity and binding affinity. J Med Chem 51: 2668-2675, 2008.
15. Finger BC, Dinan TG, Cryan JF. The temporal impact of chronic intermittent psychosocial stress on high-fat diet-induced alterations in body weight. Psychoneuroendocrinology 37: 729-741, 2012.
16. Frank S, Kullmann S, Veit R. Food related processes in the insular cortex. Front Hum Neurosci 7: 499, 2013.
17. Glass MJ, Grace M, Cleary JP, Billington CJ, Levine AS. Potency of naloxone's anorectic effect in rats is dependent on diet preference. Am J Physiol Regul Integr Comp Physiol 271: R217-R221, 1996.
18. Goebel M, Stengel A, Wang L, Coskun T, Alsina-Fernandez J, Rivier J, Taché Y. Pattern of Fos expression in the brain induced by selective activation of somatostatin receptor 2 in rats. Brain Res 1351: 150-164, 2010.
19. Goebel M, Stengel A, Wang L, Reeve J Jr, Taché Y. Lipopolysaccharide increases plasma levels of corticotropin-releasing hormone in rats. Neuroendocrinology 93: 165-173, 2011.
20. Hawkins MF, Cubic B, Baumeister AA, Barton C. Microinjection of opioid antagonists into the substantia nigra reduces stress-induced eating in rats. Brain Res 584: 261-265, 1992.
21. Heinrichs SC, Cole BJ, Pich EM, Menzaghi F, Koob GF, Hauger RL. Endogenous corticotropin-releasing factor modulates feeding induced by neuropeptide Y or a tail-pinch stressor. Peptides 13: 879-884, 1992.
22. Heinrichs SC, Menzaghi F, Pich EM, Hauger RL, Koob GF. Corticotropin-releasing factor in the paraventricular nucleus modulates feeding induced by neuropeptide Y. Brain Res 611: 18-24, 1993.
23. Kalra SP, Kalra PS. Neuropeptide Y: a physiological orexigen modulated by the feedback action of ghrelin and leptin. Endocr J 22: 49-56, 2003.
24. Kalra SP, Kalra PS. NPY-an endearing journey in search of a neurochemical on/off switch for appetite, sex and reproduction. Peptides 25: 465-471, 2004.
25. Kampe J, Tschöp MH, Hollis JH, Oldfield BJ. An anatomic basis for the communication of hypothalamic, cortical and mesolimbic circuitry in the regulation of energy balance. Eur J Neurosci 30: 415-430, 2009.
26. Kirkham TC, Blundell JE. Effects of naloxone and naltrexone on meal patterns of freely-feeding rats. Pharmacol Biochem Behav 26: 515-520, 1987.
27. Koch JE, Bodnar RJ. Involvement of mu1 and mu2 opioid receptor subtypes in tail-pinch feeding in rats. Physiol Behav 53: 603-605, 1993.
28. Kovacs KJ. Measurement of immediate-early gene activation-c-fos and beyond. J Neuroendocrinol 20: 665-672, 2008.
29. Krahn DD, Gosnell BA, Grace M, Levine AS. CRF antagonist partially reverses CRF-and stress-induced effects on feeding. Brain Res Bull 17: 285-289, 1986.
30. Krügel U, Fischer J, Radicke S, Sack U, Himmerich H. Antidepressant effect of TNF-blockade in an animal model of depression. J Psychiatr Res 47: 611-616, 2013.
31. Levine AS, Billington Opioids CJ. Are they regulators of feeding? Ann NY Acad Sci 575: 209-219; discussion 219-220, 1989.
32. Levine AS, Morley JE. Stress-induced eating in rats. Am J Physiol Regul Integr Comp Physiol 241: R72-R76, 1981.
33. Leyton M, Stewart J. Acute and repeated activation of male sexual behavior by tail pinch: opioid and dopaminergic mechanisms. Physiol Behav 60: 77-85, 1996.
34. Lowy MT, Maickel RP, Yim GK. Naloxone reduction of stress-related feeding. Life Sci 26: 2113-2118, 1980.
35. Lutter M, Sakata I, Osborne-Lawrence S, Rovinsky SA, Anderson JG, Jung S, Birnbaum S, Yanagisawa M, Elmquist JK, Nestler EJ, Zigman JM. The orexigenic hormone ghrelin defends against depressive symptoms of chronic stress. Nat Neurosci 11: 752-753, 2008.
36. Martinez V, Rivier J, Wang L, Taché Y. Central injection of a new corticotropin-releasing factor (CRF) antagonist, astressin, blocks CRFand stress-related alterations of gastric and colonic motor function. J Pharmacol Exp Ther 280: 754-760, 1997.
37. Morley JE, Levine AS. Stress-induced eating is mediated through endogenous opiates. Science 209: 1259-1261, 1980.
38. O'Shea D, Morgan DG, Meeran K, Edwards CM, Turton MD, Choi SJ, Heath MM, Gunn I, Taylor GM, Howard JK, Bloom CI, Small CJ, Haddo O, Ma JJ, Callinan W, Smith DM, Ghatei MA, Bloom SR. Neuropeptide Y induced feeding in the rat is mediated by a novel receptor. Endocrinology 138: 196-202, 1997.
39. Patterson ZR, Ducharme R, Anisman H, Abizaid A. Altered metabolic and neurochemical responses to chronic unpredictable stressors in ghrelin receptor-deficient mice. Eur J Neurosci 32: 632-639, 2010.
40. Patterson ZR, Khazall R, Mackay H, Anisman H, Abizaid A. Central ghrelin signaling mediates the metabolic response of C57BL/6 male mice to chronic social defeat stress. Endocrinology 154: 1080-1091, 2013.
41. Paxinos G, Watson C. The Rat Brain in Stereotaxic Coordinates. San Diego, CA: Academic, 2007.
42. Rivier JE, Kirby DA, Lahrichi SL, Corrigan A, Vale WW, Rivier CL. Constrained corticotropin releasing factor antagonists (astressin analogues) with long duration of action in the rat. J Med Chem 42: 3175-3182, 1999.
43. Rowland NE. Animal models of overeating. Methods Mol Biol 829: 367-375, 2012.
44. Rowland NE, Antelman SM. Stress-induced hyperphagia and obesity in rats: a possible model for understanding human obesity. Science 191: 310-312, 1976.
45. Rybkin II, Zhou Y, Volaufova J, Smagin GN, Ryan DH, Harris RB. Effect of restraint stress on food intake and body weight is determined by time of day. Am J Physiol Regul Integr Comp Physiol 273: R1612-R1622, 1997.
46. Samarghandian S, Ohata H, Yamauchi N, Shibasaki T. Corticotropinreleasing factor as well as opioid and dopamine are involved in tail-pinchinduced food intake of rats. Neuroscience 116: 519-524, 2003.
47. Schwartz MW, Woods SC, Porte D Jr, Seeley RJ, Baskin DG. Central nervous system control of food intake. Nature 404: 661-671, 2000.
48. Sekino A, Ohata H, Mano-Otagiri A, Arai K, Shibasaki T. Both corticotropin-releasing factor receptor type 1 and type 2 are involved in stress-induced inhibition of food intake in rats. Psychopharmacology (Berl) 176: 30-38, 2004.
49. Skibicka KP, Shirazi RH, Hansson C, Dickson SL. Ghrelin interacts with neuropeptide Y Y1 and opioid receptors to increase food reward. Endocrinology 153: 1194-1205, 2012.
50. Smagin GN, Howell LA, Redmann S Jr, Ryan DH, Harris RB. Prevention of stress-induced weight loss by third ventricle CRF receptor antagonist. Am J Physiol Regul Integr Comp Physiol 276: R1461-R1468, 1999.
51. Smith WJ, Stewart J, Pfaus JG. Tail pinch induces fos immunoreactivity within several regions of the male rat brain: effects of age. Physiol Behav 61: 717-723, 1997.
52. Stanley BG, Magdalin W, Seirafi A, Thomas WJ, Leibowitz SF. The perifornical area: the major focus of (a) patchily distributed hypothalamic neuropeptide Y-sensitive feeding system(s). Brain Res 604: 304-317, 1993.
53. Stengel A, Coskun T, Goebel-Stengel M, Craft LS, Alsina-Fernandez J, Wang L, Rivier J, Taché Y. Chronic injection of pansomatostatin agonist ODT8-SST differentially modulates food intake and decreases body weight gain in lean and diet-induced obese rats. Regul Pept 167: 201-208, 2011.
54. Stengel A, Coskun T, Goebel M, Wang L, Craft L, Alsina-Fernandez J, Rivier J, Taché Y. Central injection of the stable somatostatin analog ODT8-SST induces a somatostatin2 receptor-mediated orexigenic effect: role of neuropeptide Y and opioid signaling pathways in rats. Endocrinology 151: 4224-4235, 2010.
55. Stengel A, Goebel-Stengel M, Wang L, Luckey A, Hu E, Rivier J, Taché Y. Central administration of pan-somatostatin agonist ODT8-SST prevents abdominal surgery-induced inhibition of circulating ghrelin, food intake and gastric emptying in rats. Neurogastroenterol Motil 23: e294-e308, 2011.
56. Stengel A, Goebel M, Wang L, Taché Y. Ghrelin, des-acyl ghrelin and nesfatin-1 in gastric X/A-like cells: role as regulators of food intake and body weight. Peptides 31: 357-369, 2010.
57. Stengel A, Goebel M, Wang L, Rivier J, Kobelt P, Mönnikes H, Taché Y. Selective central activation of somatostatin2 receptor increases food intake, grooming behavior and rectal temperature in rats. J Physiol Pharmacol 61: 399-407, 2010.
58. Stengel A, Keire D, Goebel M, Evilevitch L, Wiggins B, Taché Y, Reeve JR Jr. The RAPID method for blood processing yields new insight in plasma concentrations and molecular forms of circulating gut peptides. Endocrinology 150: 5113-5118, 2009.
59. Stengel A, Taché Y. Corticotropin-releasing factor signaling and visceral response to stress. Exp Biol Med (Maywood) 235: 1168-1178, 2010.
60. Stengel A, Wang L, Taché Y. Stress-related alterations of acyl and desacyl ghrelin circulating levels: mechanisms and functional implications. Peptides 32: 2208-2217, 2011.
61. Taché Y, Bonaz B. Corticotropin-releasing factor receptors and stressrelated alterations of gut motor function. J Clin Invest 117: 33-40, 2007.
62. Tamashiro KL, Nguyen MM, Ostrander MM, Gardner SR, Ma LY, Woods SC, Sakai RR. Social stress and recovery: implications for body weight and body composition. Am J Physiol Regul Integr Comp Physiol 293: R1864-R1874, 2007.
63. Turnbull AV, Rivier CL. Sprague-Dawley rats obtained from different vendors exhibit distinct adrenocorticotropin responses to inflammatory stimuli. Neuroendocrinology 70: 186-195, 1999.
64. Verberne AJ, Sartor DM. Rostroventrolateral medullary neurons modulate glucose homeostasis in the rat. Am J Physiol Endocrinol Metab 299: E802-E807, 2010.
65. Wang L, Goebel-Stengel M, Stengel A, Wu SV, Ohning G, Taché Y. Comparison of CRF-immunoreactive neurons distribution in mouse and rat brains and selective induction of Fos in rat hypothalamic CRF neurons by abdominal surgery. Brain Res 1415: 34-46, 2011.
66. Wang L, Saint-Pierre DH, Taché Y. Peripheral ghrelin selectively increases Fos expression in neuropeptide Y-synthesizing neurons in mouse hypothalamic arcuate nucleus. Neurosci Lett 325: 47-51, 2002.
67. Wang L, Stengel A, Goebel M, Martinez V, Gourcerol G, Rivier J, Taché Y. Peripheral activation of corticotropin-releasing factor receptor 2 inhibits food intake and alters meal structures in mice. Peptides 32: 51-59, 2011.
68. Willesen MG, Kristensen P, Romer J. Co-localization of growth hormone secretagogue receptor and NPY mRNA in the arcuate nucleus of the rat. Neuroendocrinology 70: 306-316, 1999.
69. Zeeni N, Daher C, Fromentin G, Tome D, Darcel N, Chaumontet C. A cafeteria diet modifies the response to chronic variable stress in rats. Stress 16: 211-219, 2013.
70. Zhao DQ, Lu CL, Ai HB. The role of catecholaminergic neurons in the hypothalamus and medullary visceral zone in response to restraint waterimmersion stress in rats. J Physiol Sci 61: 37-45, 2011.
71. Zorrilla EP, Reinhardt LE, Valdez GR, Inoue K, Rivier JE, Vale WW, Koob GF. Human urocortin 2, a corticotropin-releasing factor (CRF)2 agonist, and ovine CRF, a CRF1 agonist, differentially alter feeding and motor activity. J Pharmacol Exp Ther 310: 1027-1034, 2004.
72. Zorrilla EP, Taché Y, Koob GF. Nibbling at CRF receptor control of feeding and gastrocolonic motility. Trends Pharmacol Sci 24: 421-427, 2003.