Effects of albumin-conjugated PYY on food intake: The respective roles of the circumventricular organs and vagus nerve

European Journal of Neuroscience

Volumn 32, Issue 5, 2010, Pages 826-839

  Baraboi, Elena Dana ^a   Michel, Chantal ^a   Smith, Pauline ^b   Thibaudeau, Karen ^c   Ferguson, Alastair V ^b   Richard, Denis ^a  

^a LAVAL UNIVERSITY   (Canada)

^b QUEEN S UNIVERSITY   (Canada)

^c INSTITUTE FOR RESEARCH IN IMMUNOLOGY AND CANCER   (Canada)

Author keywords

area postrema; c fos; peptide tyrosine tyrosine; rat; subdiaphragmatic vagotomy; subfornical organ

Indexed keywords

ALBUMIN; GLUCOSE; INSULIN; PEPTIDE YY [3-36];

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANOREXIA; AREA POSTREMA; ARTICLE; BLOOD BRAIN BARRIER; BODY WEIGHT; CONTROLLED STUDY; FOOD INTAKE; GLUCOSE BLOOD LEVEL; INSULIN BLOOD LEVEL; MALE; NONHUMAN; PARABRACHIAL NUCLEUS; PRIORITY JOURNAL; RAT; STRIA TERMINALIS; SUBFORNICAL ORGAN; VAGOTOMY; VAGUS NERVE; WEIGHT GAIN;

ANIMALS; APPETITE DEPRESSANTS; APPETITE REGULATION; AREA POSTREMA; BLOOD GLUCOSE; BODY WEIGHT; BRAIN; DRINKING; EATING; HUMANS; INSULIN; MALE; NEURONS; PEPTIDE YY; RATS; RATS, WISTAR; SERUM ALBUMIN; SUBFORNICAL ORGAN; VAGOTOMY; VAGUS NERVE;

EID: 77956399053     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2010.07318.x     Document Type: Article

References (75)

1. Abbott, C.R., Monteiro, M., Small, C.J., Sajedi, A., Smith, K.L., Parkinson, J.R., Ghatei, M.A. Bloom, S.R. (2005) The inhibitory effects of peripheral administration of peptide YY(3-36) and glucagon-like peptide-1 on food intake are attenuated by ablation of the vagal-brainstem-hypothalamic pathway. Brain Res., 1044, 127 131.
2. Acuna-Goycolea, C. van den Pol, A.N. (2005) Peptide YY(3-36) inhibits both anorexigenic proopiomelanocortin and orexigenic neuropeptide Y neurons: implications for hypothalamic regulation of energy homeostasis. J. Neurosci., 25, 10510 10519.
3. Adrian, T.E., Ferri, G.L., Bacarese-Hamilton, A.J., Fuessl, H.S., Polak, J.M. Bloom, S.R. (1985) Human distribution and release of a putative new gut hormone, peptide YY. Gastroenterology, 89, 1070 1077.
4. Banks, W.A. (2008) The blood-brain barrier: connecting the gut and the brain. Regul. Pept., 149, 11 14.
5. Batterham, R.L., Cowley, M.A., Small, C.J., Herzog, H., Cohen, M.A., Dakin, C.L., Wren, A.M., Brynes, A.E., Low, M.J., Ghatei, M.A., Cone, R.D. Bloom, S.R. (2002) Gut hormone PYY(3-36) physiologically inhibits food intake. Nature, 418, 650 654.
6. Batterham, R.L., Cohen, M.A., Ellis, S.M., Le Roux, C.W., Withers, D.J., Frost, G.S., Ghatei, M.A. Bloom, S.R. (2003) Inhibition of food intake in obese subjects by peptide YY3-36. N. Engl. J. Med., 349, 941 948.
7. Batterham, R.L., ffytche, D.H., Rosenthal, J.M., Zelaya, F.O., Barker, G.J., Withers, D.J. Williams, S.C. (2007) PYY modulation of cortical and hypothalamic brain areas predicts feeding behaviour in humans. Nature, 450, 106 109.
8. Berthoud, H.R. (2002) Multiple neural systems controlling food intake and body weight. Neurosci. Biobehav. Rev., 26, 393 428.
9. Blevins, J.E., Chelikani, P.K., Haver, A.C. Reidelberger, R.D. (2008) PYY(3-36) induces Fos in the arcuate nucleus and in both catecholaminergic and non-catecholaminergic neurons in the nucleus tractus solitarius of rats. Peptides, 29, 112 119.
10. Boey, D., Heilbronn, L., Sainsbury, A., Laybutt, R., Kriketos, A., Herzog, H. Campbell, L.V. (2006a) Low serum PYY is linked to insulin resistance in first-degree relatives of subjects with type 2 diabetes. Neuropeptides, 40, 317 324.
11. Boey, D., Lin, S., Karl, T., Baldock, P., Lee, N., Enriquez, R., Couzens, M., Slack, K., Dallmann, R., Sainsbury, A. Herzog, H. (2006b) Peptide YY ablation in mice leads to the development of hyperinsulinaemia and obesity. Diabetologia, 49, 1360 1370.
12. Bonaz, B., Taylor, I. Tache, Y. (1993) Peripheral peptide YY induces c-fos-like immunoreactivity in the rat brain. Neurosci. Lett., 163, 77 80.
13. Bottcher, G., Alumets, J., Hakanson, R. Sundler, F. (1986) Co-existence of glicentin and peptide YY in colorectal L-cells in cat and man. An electron microscopic study. Regul. Pept. 13, 283 291.
14. Bottcher, G., Ahren, B., Lundquist, I. Sundler, F. (1989) Peptide YY: intrapancreatic localization and effects on insulin and glucagon secretion in the mouse. Pancreas, 4, 282 288.
15. Challis, B.G., Pinnock, S.B., Coll, A.P., Carter, R.N., Dickson, S.L. 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.
16. Challis, B.G., Coll, A.P., Yeo, G.S., Pinnock, S.B., Dickson, S.L., Thresher, R.R., Dixon, J., Zahn, D., Rochford, J.J., White, A., Oliver, R.L., Millington, G., Aparicio, S.A., Colledge, W.H., Russ, A.P., Carlton, M.B. O'Rahilly, S. (2004) Mice lacking pro-opiomelanocortin are sensitive to high-fat feeding but respond normally to the acute anorectic effects of peptide-YY(3-36). Proc. Natl. Acad. Sci. USA, 101, 4695 4700.
17. Chelikani, P.K., Haver, A.C. Reidelberger, R.D. (2006) Dose-dependent effects of peptide YY(3-36) on conditioned taste aversion in rats. Peptides, 27, 3193 3201.
18. Chelikani, P.K., Haver, A.C. Reidelberger, R.D. (2007) Intermittent intraperitoneal infusion of peptide YY(3-36) reduces daily food intake and adiposity in obese rats. Am. J. Physiol. Regul. Integr. Comp. Physiol., 293, R39 R46.
19. Chronwall, B.M. (1985) Anatomy and physiology of the neuroendocrine arcuate nucleus. Peptides, 6 (Suppl 2 1 11.
20. Chuang, V.T., Kragh-Hansen, U. Otagiri, M. (2002) Pharmaceutical strategies utilizing recombinant human serum albumin. Pharm. Res., 19, 569 577.
21. Cox, J.E. Powley, T.L. (1981) Prior vagotomy blocks VMH obesity in pair-fed rats. Am. J. Physiol., 240, E573 E583.
22. Cox, J.E. Randich, A. (2004) Enhancement of feeding suppression by PYY(3-36) in rats with area postrema ablations. Peptides, 25, 985 989.
23. Degen, L., Oesch, S., Casanova, M., Graf, S., Ketterer, S., Drewe, J. Beglinger, C. (2005) Effect of peptide YY3-36 on food intake in humans. Gastroenterology, 129, 1430 1436.
24. Deng, X., Guarita, D.R., Pedroso, M.R., Kreiss, C., Wood, P.G., Sved, A.F. Whitcomb, D.C. (2001a) PYY inhibits CCK-stimulated pancreatic secretion through the area postrema in unanesthetized rats. Am. J. Physiol. Regul. Integr. Comp. Physiol., 281, R645 R653.
25. Deng, X., Guarita, D.R., Pedroso, M.R., Wood, P.G., Kreiss, C., Sved, A.F. Whitcomb, D.C. (2001b) Area postrema lesion alters the effects of peptide YY on 2-DG-stimulated pancreatic exocrine secretion. Dig. Dis. Sci., 46, 2460 2469.
26. Dong, H.W., Petrovich, G.D. Swanson, L.W. (2001) Topography of projections from amygdala to bed nuclei of the stria terminalis. Brain Res. Brain Res. Rev., 38, 192 246.
27. Dumont, Y., Fournier, A., St-Pierre, S Quirion, R. (1996) Autoradiographic distribution of [125I]Leu31,Pro34]PYY and [125I]PYY3-36 binding sites in the rat brain evaluated with two newly developed Y1 and Y2 receptor radioligands. Synapse, 22, 139 158.
28. Eberlein, G.A., Eysselein, V.E., Schaeffer, M., Layer, P., Grandt, D., Goebell, H., Niebel, W., Davis, M., Lee, T.D. Shively, J.E. (1989) A new molecular form of PYY: structural characterization of human PYY(3-36) and PYY(1-36). Peptides, 10, 797 803.
29. Fry, M., Hoyda, T.D. Ferguson, A.V. (2007) Making sense of it: roles of the sensory circumventricular organs in feeding and regulation of energy homeostasis. Exp. Biol. Med. (Maywood), 232, 14 26.
30. Grandt, D., Schimiczek, M., Beglinger, C., Layer, P., Goebell, H., Eysselein, V.E. Reeve, J.R., Jr. (1994) Two molecular forms of peptide YY (PYY) are abundant in human blood: characterization of a radioimmunoassay recognizing PYY 1-36 and PYY 3-36. Regul. Pept., 51, 151 159.
31. Greeley, G.H., Jr., Jeng, Y.J., Gomez, G., Hashimoto, T., Hill, F.L., Kern, K., Kurosky, T., Chuo, H.F. Thompson, J.C. (1989) Evidence for regulation of peptide-YY release by the proximal gut. Endocrinology, 124, 1438 1443.
32. Gustafson, E.L., Smith, K.E., Durkin, M.M., Walker, M.W., Gerald, C., Weinshank, R. Branchek, T.A. (1997) Distribution of the neuropeptide Y Y2 receptor mRNA in rat central nervous system. Brain Res. Mol. Brain Res., 46, 223 235.
33. Halatchev, I.G. Cone, R.D. (2005) Peripheral administration of PYY(3-36) produces conditioned taste aversion in mice. Cell Metab., 1, 159 168.
34. Halatchev, I.G., Ellacott, K.L., Fan, W. Cone, R.D. (2004) Peptide YY3-36 inhibits food intake in mice through a melanocortin-4 receptor-independent mechanism. Endocrinology, 145, 2585 2590.
35. Higuchi, H., Niki, T. Shiiya, T. (2008) Feeding behavior and gene expression of appetite-related neuropeptides in mice lacking for neuropeptide Y Y5 receptor subclass. World J. Gastroenterol., 14, 6312 6317.
36. Hindmarch, C., Fry, M., Yao, S.T., Smith, P.M., Murphy, D. Ferguson, A.V. (2008) Microarray analysis of the transcriptome of the subfornical organ in the rat: regulation by fluid and food deprivation. Am. J. Physiol. Regul. Integr. Comp. Physiol., 295, R1914 R1920.
37. van den Hoek, A.M., Heijboer, A.C., Corssmit, E.P., Voshol, P.J., Romijn, J.A., Havekes, L.M. Pijl, H. (2004) PYY3-36 reinforces insulin action on glucose disposal in mice fed a high-fat diet. Diabetes, 53, 1949 1952.
38. van den Hoek, A.M., Heijboer, A.C., Voshol, P.J., Havekes, L.M., Romijn, J.A., Corssmit, E.P. Pijl, H. (2007) Chronic PYY3-36 treatment promotes fat oxidation and ameliorates insulin resistance in C57BL6 mice. Am. J. Physiol. Endocrinol. Metab., 292, E238 E245.
39. Hoffman, G.E., Smith, M.S. Verbalis, J.G. (1993) c-Fos and related immediate early gene products as markers of activity in neuroendocrine systems. Front. Neuroendocrinol., 14, 173 213.
40. Jette, L., Leger, R., Thibaudeau, K., Benquet, C., Robitaille, M., Pellerin, I., Paradis, V., van Wyk, P., Pham, K. Bridon, D.P. (2005) Human growth hormone-releasing factor (hGRF)1-29-albumin bioconjugates activate the GRF receptor on the anterior pituitary in rats: identification of CJC-1295 as a long-lasting GRF analog. Endocrinology, 146, 3052 3058.
41. Koda, S., Date, Y., Murakami, N., Shimbara, T., Hanada, T., Toshinai, K., Niijima, A., Furuya, M., Inomata, N., Osuye, K. Nakazato, M. (2005) The role of the vagal nerve in peripheral PYY3-36-induced feeding reduction in rats. Endocrinology, 146, 2369 2375.
42. Koegler, F.H., Enriori, P.J., Billes, S.K., Takahashi, D.L., Martin, M.S., Clark, R.L., Evans, A.E., Grove, K.L., Cameron, J.L. Cowley, M.A. (2005) Peptide YY(3-36) inhibits morning, but not evening, food intake and decreases body weight in rhesus macaques. Diabetes, 54, 3198 3204.
43. van der Kooy, D. Koda, L.Y. (1983) Organization of the projections of a circumventricular organ: the area postrema in the rat. J. Comp. Neurol., 219, 328 338.
44. Leger, R. Thibaudeau, K. Paradis, V., Liscourt, P., Robitaille, M., Huang, X., Quraishi, O., Bousquet-Gagnon, N., Carette, J., Bridon, D.P. Castaigne, J.P. (2005) DAC PYY3-36 Albumin Bioconjugate CJC-1682: A Peripherally Long Lasting PYY Analog Reduces Food Intake in Normal Rats. The Endocrine Society 87th Annual Meeting, San Diego, California.
45. Martin, J.R., Rogers, R.C. Novin, D. (1977) Excessive gastric retention by vagotomized rats and rabbits given a solid diet. Bull. Psychon. Soc., 10, 291 294.
46. Miselis, R.R. (1981) The efferent projections of the subfornical organ of the rat: a circumventricular organ within a neural network subserving water balance. Brain Res., 230, 1 23.
47. Moran, T.H., Smedh, U., Kinzig, K.P., Scott, K.A., Knipp, S. 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.
48. Nieuwenhuizen, A.G., Karlsson, S., Fridolf, T. Ahren, B. (1994) Mechanisms underlying the insulinostatic effect of peptide YY in mouse pancreatic islets. Diabetologia, 37, 871 878.
49. Norgren, R. Smith, G.P. (1988) Central distribution of subdiaphragmatic vagal branches in the rat. J. Comp. Neurol., 273, 207 223.
50. Parker, R.M. Herzog, H. (1999) Regional distribution of Y-receptor subtype mRNAs in rat brain. Eur. J. Neurosci., 11, 1431 1448.
51. Parkinson, J.R., Dhillo, W.S., Small, C.J., Chaudhri, O.B., Bewick, G.A., Pritchard, I., Moore, S., Ghatei, M.A. 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.
52. Pittner, R.A., Moore, C.X., Bhavsar, S.P., Gedulin, B.R., Smith, P.A., Jodka, C.M., Parkes, D.G., Paterniti, J.R., Srivastava, V.P. Young, A.A. (2004) Effects of PYY[3-36] in rodent models of diabetes and obesity. Int. J. Obes. Relat. Metab. Disord., 28, 963 971.
53. Reidelberger, R.D., Haver, A.C., Chelikani, P.K. Buescher, J.L. (2008) Effects of different intermittent peptide YY (3-36) dosing strategies on food intake, body weight, and adiposity in diet-induced obese rats. Am. J. Physiol. Regul. Integr. Comp. Physiol., 295, R449 R458.
54. Reilly, S. (1999) The parabrachial nucleus and conditioned taste aversion. Brain Res. Bull., 48, 239 254.
55. Ricardo, J.A. Koh, E.T. (1978) Anatomical evidence of direct projections from the nucleus of the solitary tract to the hypothalamus, amygdala, and other forebrain structures in the rat. Brain Res., 153, 1 26.
56. 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. Bloom, S.R. (2006) Attenuated peptide YY release in obese subjects is associated with reduced satiety. Endocrinology, 147, 3 8.
57. Sagar, S.M., Sharp, F.R. Curran, T. (1988) Expression of c-fos protein in brain: metabolic mapping at the cellular level. Science, 240, 1328 1331.
58. Saper, C.B. Loewy, A.D. (1980) Efferent connections of the parabrachial nucleus in the rat. Brain Res., 197, 291 317.
59. Sawchenko, P.E. (1983) Central connections of the sensory and motor nuclei of the vagus nerve. J. Auton. Nerv. Syst., 9, 13 26.
60. Sileno, A.P., Brandt, G.C., Spann, B.M. Quay, S.C. (2006) Lower mean weight after 14 days intravenous administration peptide YY3-36 (PYY3-36) in rabbits. Int. J. Obes. (Lond)., 30, 68 72.
61. Simmons, D.M., Arriza, J.L. Swanson, L.W. (1989) A complete protocol for in situ hybridization of messenger RNAs in brain and other tissues with radiolabeled single-stranded RNA probes. J. Histotechnol., 12, 169 181.
62. St Andre, J., Albanos, K. Reilly, S. (2007) C-fos expression in the rat brain following lithium chloride-induced illness. Brain Res., 1135, 122 128.
63. Stanic, D., Brumovsky, P., Fetissov, S., Shuster, S., Herzog, H. Hokfelt, T. (2006) Characterization of neuropeptide Y2 receptor protein expression in the mouse brain. I. Distribution in cell bodies and nerve terminals. J. Comp. Neurol., 499, 357 390.
64. Sunn, N., McKinley, M.J. Oldfield, B.J. (2003) Circulating angiotensin II activates neurones in circumventricular organs of the lamina terminalis that project to the bed nucleus of the stria terminalis. J. Neuroendocrinol., 15, 725 731.
65. Swanson, L.W. Lind, R.W. (1986) Neural projections subserving the initiation of a specific motivated behavior in the rat: new projections from the subfornical organ. Brain Res., 379, 399 403.
66. Szecowka, J., Tatemoto, K., Rajamaki, G. Efendic, S. (1983) Effects of PYY and PP on endocrine pancreas. Acta. Physiol. Scand., 119, 123 126.
67. Talsania, T., Anini, Y., Siu, S., Drucker, D.J. Brubaker, P.L. (2005) Peripheral exendin-4 and peptide YY(3-36) synergistically reduce food intake through different mechanisms in mice. Endocrinology, 146, 3748 3756.
68. Thiele, T.E., Naveilhan, P. Ernfors, P. (2004) Assessment of ethanol consumption and water drinking by NPY Y(2) receptor knockout mice. Peptides, 25, 975 983.
69. Timofeeva, E., Picard, F., Duclos, M., Deshaies, Y. Richard, D. (2002) Neuronal activation and corticotropin-releasing hormone expression in the brain of obese (fa/fa) and lean (fa/?) Zucker rats in response to refeeding. Eur. J. Neurosci., 15, 1013 1029.
70. Timofeeva, E., Baraboi, E.D. Richard, D. (2005) Contribution of the vagus nerve and lamina terminalis to brain activation induced by refeeding. Eur. J. Neurosci., 22, 1489 1501.
71. Vrang, N., Madsen, A.N., Tang-Christensen, M., Hansen, G. Larsen, P.J. (2006) PYY(3-36) reduces food intake and body weight and improves insulin sensitivity in rodent models of diet-induced obesity. Am. J. Physiol. Regul. Integr. Comp. Physiol., 291, R367 R375.
72. Wultsch, T., Painsipp, E., Donner, S., Sperk, G., Herzog, H., Peskar, B.A. Holzer, P. (2006) Selective increase of dark phase water intake in neuropeptide-Y Y2 and Y4 receptor knockout mice. Behav. Brain Res., 168, 255 260.
73. Yoshinaga, K., Mochizuki, T., Yanaihara, N., Oshima, K., Izukura, M., Kogire, M., Sumi, S., Gomez, G., Uchida, T. Thompson, J.C. (1992) Structural requirements of peptide YY for biological activity at enteric sites. Am. J. Physiol., 263, G695 G701.
74. Zardetto-Smith, A.M. Gray, T.S. (1987) A direct neural projection from the nucleus of the solitary tract to the subfornical organ in the rat. Neurosci. Lett., 80, 163 166.
75. Zhang, X., Shi, T., Holmberg, K., Landry, M., Huang, W., Xiao, H., Ju, G. Hokfelt, T. (1997) Expression and regulation of the neuropeptide Y Y2 receptor in sensory and autonomic ganglia. Proc. Natl. Acad. Sci. USA, 94, 729 734.