The temporal sequence of gut peptide-CNS interactions tracked in vivo by magnetic resonance imaging

Journal of Neuroscience

Volumn 27, Issue 45, 2007, Pages 12341-12348

  Kuo, Yu Ting ^a,b   Parkinson, James R C ^a   Chaudhri, Owais B ^a   Herlihy, Amy H ^a   So, Po Wah ^a   Dhillo, Waljit S ^a   Small, Caroline J ^a   Bloom, Stephen R ^a   Bell, Jimmy D ^a  

^a HAMMERSMITH HOSPITAL   (United Kingdom)

^b KAOHSIUNG MEDICAL UNIVERSITY   (Taiwan)

Author keywords

Appetite; Ghrelin; Hypothalamus; Manganese; MRI; PYY3 36

Indexed keywords

GHRELIN; MANGANESE; PEPTIDE YY;

ADOLESCENT; ANIMAL EXPERIMENT; ANTERIOR HYPOTHALAMUS; APPETITE; ARCUATE NUCLEUS; ARTICLE; BEHAVIOR; CENTRAL NERVOUS SYSTEM; ENVIRONMENTAL FACTOR; FOOD INTAKE; GENE EXPRESSION; HYPOTHALAMUS; IMMEDIATE EARLY GENE; IN VIVO STUDY; MALE; METABOLISM; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; ONCOGENE C FOS; PRIORITY JOURNAL; REGULATORY MECHANISM; SATIETY; THALAMUS VENTRAL NUCLEUS;

ANIMALS; BRAIN; CENTRAL NERVOUS SYSTEM; EATING; GASTROINTESTINAL HORMONES; GHRELIN; MAGNETIC RESONANCE IMAGING; MALE; MICE; MICE, INBRED C57BL; NEUROPEPTIDE Y; TIME FACTORS;

EID: 36048939625     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2391-07.2007     Document Type: Article

References (54)

1. Abbott CR, Rossi M, Wren AM, Murphy KG, Kennedy AR, Stanley SA, Zollner AN, Morgan DG, Morgan I, Ghatei MA, Small CJ, Bloom SR (2001) Evidence of an orexigenic role for cocaine- and amphetamine-regulated transcript after administration into discrete hypothalamic nuclei. Endocrinology 142:3457-3463.
2. Aoki I, Tanaka C, Takegami T, Ebisu T, Umeda M, Fukunaga M, Fukuda K, Silva AC, Koretsky AP, Naruse S (2002) Dynamic activity-induced manganese-dependent contrast magnetic resonance imaging (DAIM MRI). Magn Reson Med 48:927-933.
3. Banks WA, Tschop M, Robinson SM, Heiman ML (2002) Extent and direction of ghrelin transport across the blood-brain barrier is determined by its unique primary structure. J Pharmacol Exp Ther 302:822-827.
4. Batterham RL, Cowley MA, Small CJ, Herzog H, Cohen MA, Dakin CL, Wren AM, Brynes AE, Low MJ, Ghatei MA, Cone RD, Bloom SR (2002) Gut hormone PYY(3-36) physiologically inhibits food intake. Nature 418:650-654.
5. Batterham RL, Cohen MA, Ellis SM, Le Roux CW, Withers DJ, Frost GS, Ghatei MA, Bloom SR (2003) Inhibition of food intake in obese subjects by peptide YY3-36. N Engl J Med 349:941-948.
6. 2: a potential alternative to IV injection for tissue contrast enhancement in magnetic resonance imaging. Magn Reson Imaging 2:307-314.
7. Chaudhri OB, Parkinson JR, Kuo YT, Druce MR, Herlihy AH, Bell JD, Dhillo WS, Stanley SA, Ghatei MA, Bloom SR (2006) Differential hypothalamic neuronal activation following peripheral injection of GLP-1 and oxyntomodulin in mice detected by manganese-enhanced magnetic resonance imaging. Biochem Biophys Res Commun 350:298-306.
8. Chen X, Ge YL, Jiang ZY, Liu CQ, Depoortere I, Peeters TL (2005) Effects of ghrelin on hypothalamic glucose responding neurons in rats. Brain Res 1055:131-136.
9. Dakin CL, Small CJ, Batterham RL, Neary NM, Cohen MA, Patterson M, Ghatei MA, Bloom SR (2004) Peripheral oxyntomodulin reduces food intake and body weight gain in rats. Endocrinology 145:2687-2695.
10. Drapeau P, Nachshen DA (1984) Manganese fluxes and manganese-dependent neurotransmitter release in presynaptic nerve endings isolated from rat brain. J Physiol (Lond) 348:493-510.
11. Elmquist JK, Coppari R, Balthasar N, Ichinose M, Lowell BB (2005) Identifying hypothalamic pathways controlling food intake, body weight, and glucose homeostasis. J Comp Neurol 493:63-71.
12. Fray PJ, Sahakian BJ, Robbins TW, Koob GF, Iversen SD (1980) An observational method for quantifying the behavioural effects of dopamine agonists: contrasting effects of d-amphetamine and apomorphine. Psychopharmacology (Berl) 69:253-259.
13. Han L, Rowland NE (1996) Dissociation of Fos-like immunoreactivity in lamina terminalis and magnocellular hypothalamic nuclei induced by hypernatremia. Brain Res 708:45-49.
14. Harris JA (1998) Using c-fos as a neural marker of pain. Brain Res Bull 45:1-8.
15. Hewson AK, Dickson SL (2000) Systemic administration of ghrelin induces Fos and Egr-1 proteins in the hypothalamic arcuate nucleus of fasted and fed rats. J Neuroendocrinol 12:1047-1049.
16. Hoffman GE, Lyo D (2002) Anatomical markers of activity in neuroendocrine systems: are we all 'fos-ed out'? J Neuroendocrinol 14:259-268.
17. Hu TC, Pautler RG, MacGowan GA, Koretsky AP (2001) Manganese-enhanced MRI of mouse heart during changes in inotropy. Magn Reson Med 46:884-890.
18. Hunter DR, Haworth RA, Berkoff HA (1981) Cellular manganese uptake by the isolated perfused rat heart: a probe for the sarcolemma calcium channel. J Mol Cell Cardiol 13:823-832.
19. Kawasaki M, Yamaguchi K, Saito J, Ozaki Y, Mera T, Hashimoto H, Fujihara H, Okimoto N, Ohnishi H, Nakamura T, Ueta Y (2005) Expression of immediate early genes and vasopressin heteronuclear RNA in the paraventricular and supraoptic nuclei of rats after acute osmotic stimulus. J Neuroendocrinol 17:227-237.
20. Kringelbach ML, de Araujo I, Rolls ET (2004) Taste-related activity in the human dorsolateral prefrontal cortex. NeuroImage 21:781-788.
21. Kuo YT, Herlihy AH, So PW, Bhakoo KK, Bell JD (2005) In vivo measurements of T1 relaxation times in mouse brain associated with different modes of systemic administration of manganese chloride. J Magn Reson Imaging 21:334-339.
22. Kuo YT, Herlihy AH, So PW, Bell JD (2006) Manganese-enhanced magnetic resonance imaging (MEMRI) without compromise of the blood-brain barrier detects hypothalamic neuronal activity in vivo. NMR Biomed 19:1028-1034.
23. 2: dose-dependent and temporal evolution of T1 contrast. Magn Reson Med 53:640-648.
24. Lin YJ, Koretsky AP (1997) Manganese ion enhances T1-weighted MRI during brain activation: an approach to direct imaging of brain function. Magn Reson Med 38:378-388.
25. Liu Y, Gao JH, Liu HL, Fox PT (2000) The temporal response of the brain after eating revealed by functional MRI. Nature 405:1058-1062.
26. London RE, Toney G, Gabel SA, Funk A (1989) Magnetic resonance imaging studies of the brains of anesthetized rats treated with manganese chloride. Brain Res Bull 23:229-235.
27. 2+ contrasted T1-weighted MRI. Auton Neurosci 113:43-54.
28. Murphy VA, Rosenberg JM, Smith QR, Rapoport SI (1991) Elevation of brain manganese in calcium-deficient rats. Neurotoxicology 12:255-263.
29. Nakazato M, Murakami N, Date Y, Kojima M, Matsuo H, Kangawa K, Matsukura S (2001) A role for ghrelin in the central regulation of feeding. Nature 409:194-198.
30. Narita K, Kawasaki F, Kita H (1990) Mn and Mg influxes through Ca channels of motor nerve terminals are prevented by verapamil in frogs. Brain Res 510:289-295.
31. Neary NM, Small CJ, Druce MR, Park AJ, Ellis SM, Semjonous NM, Dakin CL, Filipsson K, Wang F, Kent AS, Frost GS, Ghatei MA, Bloom SR (2005) Peptide YY3-36 and glucagon-like peptide-17-36 inhibit food intake additively. Endocrinology 146:5120-5127.
32. Newland MC, Ceckler TL, Kordower JH, Weiss B (1989) Visualizing manganese in the primate basal ganglia with magnetic resonance imaging. Exp Neurol 106:251-258.
33. Nonaka N, Shioda S, Niehoff ML, Banks WA (2003) Characterization of blood-brain barrier permeability to PYY3-36 in the mouse. J Pharmacol Exp Ther 306:948-953.
34. Ojemann JG, Akbudak E, Snyder AZ, McKinstry RC, Raichle ME, Conturo TE (1997) Anatomic localization and quantitative analysis of gradient refocused echo-planar fMRI susceptibility artifacts. NeuroImage 6:156-167.
35. Olszewski PK, Grace MK, Billington CJ, Levine AS (2003) Hypothalamic paraventricular injections of ghrelin: effect on feeding and c-Fos immunoreactivity. Peptides 24:919-923.
36. Pautler RG (2004) In vivo, trans-synaptic tract-tracing utilizing manganese-enhanced magnetic resonance imaging (MEMRI). NMR Biomed 17:595-601.
37. Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates. London: Academic.
38. Rabin O, Hegedus L, Bourre JM, Smith QR (1993) Rapid brain uptake of manganese(II) across the blood-brain barrier. J Neurochem 61:509-517.
39. Riediger T, Bothe C, Becskei C, Lutz TA (2004) Peptide YY directly inhibits ghrelin-activated neurons of the arcuate nucleus and reverses fasting-induced c-Fos expression. Neuroendocrinology 79:317-326.
40. Saleem KS, Pauls JM, Augath M, Trinath T, Prause BA, Hashikawa T, Logothetis NK (2002) Magnetic resonance imaging of neuronal connections in the macaque monkey. Neuron 34:685-700.
41. Silva AC, Lee JH, Aoki I, Koretsky AP (2004) Manganese-enhanced magnetic resonance imaging (MEMRI): methodological and practical considerations. NMR Biomed 17:532-543.
42. Smeets PA, de Graaf C, Stafleu A, van Osch MJ, van der Grond J (2005) Functional MRI of human hypothalamic responses following glucose ingestion. NeuroImage 24:363-368.
43. Smith KL, Patterson M, Dhillo WS, Patel SR, Semjonous NM, Gardiner JV, Ghatei MA, Bloom SR (2006) Neuropeptide S stimulates the hypothalamo-pituitary- adrenal axis and inhibits food intake. Endocrinology 147:3510-3518.
44. Stanley S, Wynne K, McGowan B, Bloom S (2005) Hormonal regulation of food intake. Physiol Rev 85:1131-1158.
45. Stark JA, Davies KE, Williams SR, Luckman SM (2006) Functional magnetic resonance imaging and c-Fos mapping in rats following an anorectic dose of m-chlorophenylpiperazine. NeuroImage 31:1228-1237.
46. Tataranni PA, Delparigi A (2003) Functional neuroimaging: a new generation of human brain studies in obesity research. Obes Rev 4:229-238.
47. Tschop M, Smiley DL, Heiman ML (2000) Ghrelin induces adiposity in rodents. Nature 407:908-913.
48. Van der Linden A, Van Meir V, Tindemans I, Verhoye M, Balthazart J (2004) Applications of manganese-enhanced magnetic resonance imaging (MEMRI) to image brain plasticity in song birds. NMR Biomed 17:602-612.
49. Watanabe T, Frahm J, Michaelis T (2004) Functional mapping of neural pathways in rodent brain in vivo using manganese-enhanced three-dimensional magnetic resonance imaging. NMR Biomed 17:554-568.
50. Wren AM, Small CJ, Abbott CR, Dhillo WS, Seal LJ, Cohen MA, Batterham RL, Taheri S, Stanley SA, Ghatei MA, Bloom SR (2001a) Ghrelin causes hyperphagia and obesity in rats. Diabetes 50:2540-2547.
51. Wren AM, Seal LJ, Cohen MA, Brynes AE, Frost GS, Murphy KG, Dhillo WS, Ghatei MA, Bloom SR (2001b) Ghrelin enhances appetite and increases food intake in humans. J Clin Endocrinol Metab 86:5992.
52. Wren AM, Small CJ, Abbott CR, Jethwa PH, Kennedy AR, Murphy KG, Stanley SA, Zollner AN, Ghatei MA, Bloom SR (2002a) Hypothalamic actions of neuromedin U. Endocrinology 143:4227-4234.
53. Wren AM, Small CJ, Fribbens CV, Neary NM, Ward HL, Seal LJ, Ghatei MA, Bloom SR (2002b) The hypothalamic mechanisms of the hypophysiotropic action of ghrelin. Neuroendocrinology 76:316-324.
54. Xiong JJ, Hatton GI (1996) Differential responses of oxytocin and vasopressin neurons to the osmotic and stressful components of hypertonic saline injections: a Fos protein double labeling study. Brain Res 719:143-153.