Differential patterns of neuronal activation in the brainstem and hypothalamus following peripheral injection of GLP-1, oxyntomodulin and lithium chloride in mice detected by manganese-enhanced magnetic resonance imaging (MEMRI)

NeuroImage - Tập 44 - Trang 1022-1031 - 2009
James R.C. Parkinson1, Owais B. Chaudhri1, Yu-Ting Kuo2,3, Benjamin C.T. Field1, Amy H. Herlihy4, Waljit S. Dhillo1, Mohammad A. Ghatei1, Stephen R. Bloom1, Jimmy D. Bell5
1Department of Investigative Medicine, Hammersmith Hospital, Imperial College London, UK
2Department of Medical Imaging, Kaohsiung Medical University Hospital, Kaohsiung Medical University, Kaohsiung, Taiwan
3Department of Radiology, Faculty of Medicine, College of Medicine, Kaohsiung Medical University, Kaohsiung, Taiwan
4Biological Imaging Centre, Imaging Sciences Department, MRC Clinical Sciences Centre, Hammersmith Hospital, Imperial College London, UK
5Molecular Imaging Group, MRC Clinical Sciences Centre, Hammersmith Hospital, Imperial College London, Du Cane Road, London, W12 0NN UK

Tài liệu tham khảo

Abbott, 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, 10.1016/j.brainres.2005.03.011 Amori, 2007, Efficacy and safety of incretin therapy in type 2 diabetes: systematic review and meta-analysis, JAMA, 298, 194, 10.1001/jama.298.2.194 Baggio, 2004, Oxyntomodulin and glucagon-like peptide-1 differentially regulate murine food intake and energy expenditure, Gastroenterology, 127, 546, 10.1053/j.gastro.2004.04.063 Batterham, 2007, PYY modulation of cortical and hypothalamic brain areas predicts feeding behaviour in humans, Nature, 450, 106, 10.1038/nature06212 Chaudhri, 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, 10.1016/j.bbrc.2006.09.033 Cohen, 2003, Oxyntomodulin suppresses appetite and reduces food intake in humans, J. Clin. Endocrinol. Metab., 88, 4696, 10.1210/jc.2003-030421 Curran, 1995, Fos: an immediate-early transcription factor in neurons, J. Neurobiol., 26, 403, 10.1002/neu.480260312 Dakin, 2001, Oxyntomodulin inhibits food intake in the rat, Endocrinology, 142, 4244, 10.1210/endo.142.10.8430 Dakin, 2002, Repeated ICV administration of oxyntomodulin causes a greater reduction in body weight gain than in pair-fed rats, Am. J. Physiol. Endocrinol. Metab., 283, E1173, 10.1152/ajpendo.00233.2002 Dakin, 2004, Peripheral oxyntomodulin reduces food intake and body weight gain in rats, Endocrinology, 145, 2687, 10.1210/en.2003-1338 Date, 2002, The role of the gastric afferent vagal nerve in ghrelin-induced feeding and growth hormone secretion in rats, Gastroenterology, 123, 1120, 10.1053/gast.2002.35954 Fehmann, 1994, Stable expression of the rat GLP-I receptor in CHO cells: activation and binding characteristics utilizing GLP-I(7-36)-amide, oxyntomodulin, exendin-4, and exendin(9–39), Peptides, 15, 453, 10.1016/0196-9781(94)90204-6 Fineman, 2004, Effectiveness of progressive dose-escalation of exenatide (exendin-4) in reducing dose-limiting side effects in subjects with type 2 diabetes, Diabetes/ Metab. Res. Rev., 20, 411, 10.1002/dmrr.499 Franklin, 1997 Fraser, 1995, Oral-pharyngeal-esophageal and gastric cues contribute to meal-induced c-fos expression, Am. J. Physiol., 268, R223 Gautron, 2005, Influence of feeding status on neuronal activity in the hypothalamus during lipopolysaccharide-induced anorexia in rats, Neuroscience, 134, 933, 10.1016/j.neuroscience.2005.03.063 Ghatei, 1983, Molecular forms of human enteroglucagon in tissue and plasma: plasma responses to nutrient stimuli in health and in disorders of the upper gastrointestinal tract, J. Clin. Endocrinol. Metab., 57, 488, 10.1210/jcem-57-3-488 Glatzle, 2001, Postprandial neuronal activation in the nucleus of the solitary tract is partly mediated by CCK-A receptors, Am. J. Physiol., Regul. Integr. Comp. Physiol., 281, R222, 10.1152/ajpregu.2001.281.1.R222 Gutzwiller, 1999, Glucagon-like peptide-1: a potent regulator of food intake in humans, Gut, 44, 81, 10.1136/gut.44.1.81 Harris, 1998, Using c-fos as a neural marker of pain, Brain Res. Bull., 45, 1, 10.1016/S0361-9230(97)00277-3 Herrera, 1996, Activation of c-fos in the brain, Prog. Neurobiol., 50, 83, 10.1016/S0301-0082(96)00021-4 Hewson, 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, 10.1046/j.1365-2826.2000.00584.x Hoffman, 2002, Anatomical markers of activity in neuroendocrine systems: are we all 'fos-ed out'?, J. Neuroendocrinol., 14, 259, 10.1046/j.1365-2826.2002.00775.x Holst, 1997, Enteroglucagon, Annu. Rev. Physiol., 59, 257, 10.1146/annurev.physiol.59.1.257 Holzer, 2003, Afferent signalling of gastric acid challenge, J. Physiol. Pharmacol., 54, 43 Karniol, 1978, Acute and chronic effects of lithium chloride on physiological and psychological measures in normals, Psychopharmacology (Berl), 57, 289, 10.1007/BF00426753 Kervran, 1987, Distribution of oxyntomodulin and glucagon in the gastrointestinal tract and the plasma of the rat, Endocrinology, 121, 704, 10.1210/endo-121-2-704 King, 2006, The rise, fall, and resurrection of the ventromedial hypothalamus in the regulation of feeding behavior and body weight, Physiol. Behav., 87, 221, 10.1016/j.physbeh.2005.10.007 Kinzig, 2002, The diverse roles of specific GLP-1 receptors in the control of food intake and the response to visceral illness, J. Neurosci., 22, 10470, 10.1523/JNEUROSCI.22-23-10470.2002 Kreymann, 1987, Glucagon-like peptide-1 7–36: a physiological incretin in man, Lancet, 2, 1300, 10.1016/S0140-6736(87)91194-9 Kuo, 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, 10.1002/jmri.20285 Kuo, 2006, Manganese-enhanced magnetic resonance imaging (MEMRI) without compromise of the blood-brain barrier detects hypothalamic neuronal activity in vivo, NMR Biomed., 19, 1028, 10.1002/nbm.1070 Kuo, 2007, The temporal sequence of gut peptide CNS interactions tracked in vivo by magnetic resonance imaging, J. Neurosci., 27, 12341, 10.1523/JNEUROSCI.2391-07.2007 Lachey, 2005, The role of central glucagon-like peptide-1 in mediating the effects of visceral illness: differential effects in rats and mice, Endocrinology, 146, 458, 10.1210/en.2004-0419 Le, 1992, Oxyntomodulin-like immunoreactivity: diurnal profile of a new potential enterogastrone, J. Clin. Endocrinol. Metab., 74, 1405 Lin, 1997, Manganese ion enhances T1-weighted MRI during brain activation: an approach to direct imaging of brain function, Magn. Reson. Med., 38, 378, 10.1002/mrm.1910380305 Liu, 2000, The temporal response of the brain after eating revealed by functional MRI, Nature, 405, 1058, 10.1038/35016590 Lorenz, 1982, Vagal mediation of the cholecystokinin satiety effect in rats, Physiol. Behav., 29, 599, 10.1016/0031-9384(82)90226-8 Luckman, 1994, Induction of c-fos expression in hypothalamic magnocellular neurons requires synaptic activation and not simply increased spike activity, J. Neurosci., 14, 4825, 10.1523/JNEUROSCI.14-08-04825.1994 McCann, 1989, LiCl and CCK inhibit gastric emptying and feeding and stimulate OT secretion in rats, Am. J. Physiol., 256, R463 Meeran, 1999, Repeated intracerebroventricular administration of glucagon-like peptide-1-(7-36) amide or exendin-(9-39) alters body weight in the rat, Endocrinology, 140, 244, 10.1210/endo.140.1.6421 Miller, 2004, Anorexigenic C75 alters c-Fos in mouse hypothalamic and hindbrain subnuclei, NeuroReport, 15, 925, 10.1097/00001756-200404090-00038 Naslund, 1999, Energy intake and appetite are suppressed by glucagon-like peptide-1 (GLP-1) in obese men, Int. J. Obes. Relat. Metab. Disord., 23, 304, 10.1038/sj.ijo.0800818 Neary, 2005, Peptide YY3–36 and glucagon-like peptide-17-36 inhibit food intake additively, Endocrinology, 146, 5120, 10.1210/en.2005-0237 Olszewski, 2000, Opioids affect acquisition of LiCl-induced conditioned taste aversion: involvement of OT and VP systems, Am. J. Physiol., Regul. Integr. Comp. Physiol., 279, R1504, 10.1152/ajpregu.2000.279.4.R1504 Orskov, 1994, Tissue and plasma concentrations of amidated and glycine-extended glucagon-like peptide I in humans, Diabetes, 43, 535, 10.2337/diab.43.4.535 Parkinson, 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 Poon, 2005, Exenatide improves glycemic control and reduces body weight in subjects with type 2 diabetes: a dose-ranging study, Diabetes Technol. Ther., 7, 467, 10.1089/dia.2005.7.467 Price, 2008, The area Postrema: a brain monitor and integrator of systemic autonomic state, J. Neuroendocrinol., 20, 245, 10.1111/j.1365-2826.2007.01641.x Riediger, 2004, Peptide YY directly inhibits ghrelin-activated neurons of the arcuate nucleus and reverses fasting-induced c-Fos expression, Neuroendocrinology, 79, 317, 10.1159/000079842 Rinaman, 1999, A functional role for central glucagon-like peptide-1 receptors in lithium chloride-induced anorexia, Am. J. Physiol., 277, R1537 Rinaman, 2007, Experimental dissociation of neural circuits underlying conditioned avoidance and hypophagic responses to lithium chloride, Am. J. Physiol., Regul. Integr. Comp. Physiol., 293, R1495, 10.1152/ajpregu.00393.2007 Roca, 2004, Comparative analysis of transcriptional profiles between two apoptotic pathways of light-induced retinal degeneration, Neuroscience, 129, 779, 10.1016/j.neuroscience.2004.08.021 Sakai, 1999, Possible routes of visceral information in the rat brain in formation of conditioned taste aversion, Neurosci. Res., 35, 53, 10.1016/S0168-0102(99)00067-X Schwartz, 2000, Central nervous system control of food intake, Nature, 404, 661, 10.1038/35007534 Seeley, 2000, The role of CNS glucagon-like peptide-1 (7–36) amide receptors in mediating the visceral illness effects of lithium chloride, J. Neurosci., 20, 1616, 10.1523/JNEUROSCI.20-04-01616.2000 Shughrue, 1996, Glucagon-like peptide-1 receptor (GLP1-R) mRNA in the rat hypothalamus, Endocrinology, 137, 5159, 10.1210/endo.137.11.8895391 Silva, 2004, Manganese-enhanced magnetic resonance imaging (MEMRI): methodological and practical considerations, NMR Biomed., 17, 532, 10.1002/nbm.945 Stanley, 2005, Hormonal regulation of food intake, Physiol. Rev., 85, 1131, 10.1152/physrev.00015.2004 Stark, 2008, 5-HT(2C) antagonism blocks blood oxygen level-dependent pharmacological-challenge magnetic resonance imaging signal in rat brain areas related to feeding, Eur. J. Neurosci., 27, 457, 10.1111/j.1460-9568.2007.06002.x Tang-Christensen, 2001, Glucagon-like peptide containing pathways in the regulation of feeding behaviour, Int. J. Obes. Relat. Metab. Disord., 25, S42, 10.1038/sj.ijo.0801912 Tataranni, 2003, Functional neuroimaging: a new generation of human brain studies in obesity research, Obes. Rev., 4, 229, 10.1046/j.1467-789X.2003.00111.x Thiele, 1997, Central infusion of GLP-1, but not leptin, produces conditioned taste aversions in rats, Am. J. Physiol., 272, R726 Thiele, 1998, Central infusion of glucagon-like peptide-1-(7–36) amide (GLP-1) receptor antagonist attenuates lithium chloride-induced c-Fos induction in rat brainstem, Brain Res., 801, 164, 10.1016/S0006-8993(98)00584-8 Timofeeva, 2001, Activation of the central nervous system in obese Zucker rats during food deprivation, J. Comp. Neurol., 441, 71, 10.1002/cne.1398 Timofeeva, 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, 10.1046/j.1460-9568.2002.01942.x Tolessa, 1998, Inhibitory effect of glucagon-like peptide-1 on small bowel motility. Fasting but not fed motility inhibited via nitric oxide independently of insulin and somatostatin, J. Clin. Invest., 102, 764, 10.1172/JCI942 Turton, 1996, A role for glucagon-like peptide-1 in the central regulation of feeding, Nature, 379, 69, 10.1038/379069a0 Wei, 1995, Tissue-specific expression of the human receptor for glucagon-like peptide-I: brain, heart and pancreatic forms have the same deduced amino acid sequences, FEBS Lett., 358, 219, 10.1016/0014-5793(94)01430-9 Wettergren, 1997, The inhibitory effect of glucagon-like peptide-1 (GLP-1) 7–36 amide on gastric acid secretion in humans depends on an intact vagal innervation, Gut, 40, 597, 10.1136/gut.40.5.597 Wolgin, 1990, Effect of lithium chloride-induced aversion on appetitive and consummatory behavior, Behav. Neurosci., 104, 438, 10.1037/0735-7044.104.3.438 Wynne, 2005, Subcutaneous oxyntomodulin reduces body weight in overweight and obese subjects: a double-blind, randomized, controlled trial, Diabetes, 54, 2390, 10.2337/diabetes.54.8.2390 Yamamori, 1991, CDF/LIF selectively increases c-fos and jun-B transcripts in sympathetic neurons, NeuroReport, 2, 173, 10.1097/00001756-199104000-00003 Yu, 1994, Signalling the molecular stress response to nephrotoxic and mutagenic cysteine conjugates: differential roles for protein synthesis and calcium in the induction of c-fos and c-myc mRNA in LLC-PK1 cells, J. Cell. Physiol., 161, 303, 10.1002/jcp.1041610215 Zhang, 2003, Convergence of gastric vagal and cerebellar fastigial nuclear inputs on glycemia-sensitive neurons of lateral hypothalamic area in the rat, Neurosci. Res., 45, 9, 10.1016/S0168-0102(02)00192-X