Neuromedin B and Gastrin-releasing peptide excite arcuate nucleus neuropeptide y neurons in a novel transgenic mouse expressing strong renilla green fluorescent protein in NPY neurons

Journal of Neuroscience

Volumn 29, Issue 14, 2009, Pages 4622-4639

  Van Den Pol, Anthony N ^a   Yao, Yang ^a,d   Fu, Li Ying ^a   Foo, Kylie ^c   Huang, Hao ^a   Coppari, Roberto ^b,e   Lowell, Bradford B ^b   Broberger, Christian ^c  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b HARVARD UNIVERSITY   (United States)

^c KAROLINSKA INSTITUTE   (Sweden)

^d NANKAI UNIVERSITY   (China)

^e UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 [2 (4 METHOXYPHENYL) 2 [3 (4 METHOXYPHENYL)PROPOXY]ETHYL] 1H IMIDAZOLE; 2 [2 [4 (4 NITROBENZYLOXY)PHENYL]ETHYL]ISOTHIOUREA METHANESULFONATE; BOMBESIN; CANNABINOID; CATION CHANNEL; CHOLINE; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; GASTRIN RELEASING PEPTIDE; GHRELIN; GREEN FLUORESCENT PROTEIN; MELANOCORTIN RECEPTOR AGONIST; NEUROMEDIN B; NEUROPEPTIDE; NEUROPEPTIDE Y; NICKEL; OREXIN; SODIUM; SODIUM CALCIUM EXCHANGE PROTEIN;

ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; CONTROLLED STUDY; DEPOLARIZATION; ELECTRIC POTENTIAL; ENERGY BALANCE; EXCITATION; EXTRACELLULAR CALCIUM; HOMEOSTASIS; HYPOTHALAMUS; IMMUNOCYTOCHEMISTRY; MEMBRANE POTENTIAL; MOUSE; NERVE CELL; NEUROTRANSMISSION; NONHUMAN; PIPETTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RENILLA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TRANSGENIC MOUSE;

ANIMALS; ARCUATE NUCLEUS; ELECTROPHYSIOLOGY; GASTRIN-RELEASING PEPTIDE; GENE EXPRESSION REGULATION; GREEN FLUORESCENT PROTEINS; HUMANS; MICE; MICE, TRANSGENIC; NEUROKININ B; NEURONS; NEUROPEPTIDE Y; RENILLA;

EID: 65549091103     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3249-08.2009     Document Type: Article

References (90)

1. Acuna-Goycolea C, van den Pol AN (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.
2. Acuna-Goycolea C, van den Pol AN (2009) Neuroendocrine proopiomelanocortin neurons are excited by hypocretin/orexin. J Neurosci 29:1503-1515.
3. Acuna-Goycolea C, Tamamaki N, Yanagawa Y, Obata K, van den Pol AN (2005) Mechanisms of neuropeptide Y, peptide YY, and pancreatic polypeptide inhibition of identified green fluorescent protein-expressing GABA neurons in the hypothalamic neuroendocrine arcuate nucleus. J Neurosci 25:7406-7419.
4. Bai FL, Yamano M, Shiotani Y, Emson PC, Smith AD, Powell JF, Tohyama M (1985) An arcuato-paraventricular and -dorsomedial hypothalamic neuropeptide Y-containing system which lacks noradrenaline in the rat. Brain Res 331:172-175.
5. 3-36 physiologically inhibits food intake. Nature 418:650-654.
6. Broberger C, De Lecea L, Sutcliffe JG, Hökfelt T (1998) Hypocretin/orexin-and melanin concentrating hormone-expressing cells form distinct populations in the rodent lateral hypothalamus: Relationship to the neuropeptide Y and agouti gene-related protein systems. J Comp Neurol 402:460-474.
7. Broberger C, Visser TJ, Kuhar MJ, Hökfelt T (1999) Neuropeptide Y inner-vation and neuropeptide-Y-Y1-receptor-expressing neurons in the para-ventricular hypothalamic nucleus of the mouse. Neuroendocrinology 70:295-305.
8. Brown MR, Rivier J, Vale W (1977) Bombesin affects the central nervous system to produce hyperglycemia in rats. Life Sci 21:1729-1734.
9. Chen G, van den Pol AN (1996) Multiple NPY receptors coexist in pre-and postsynaptic sites: Inhibition of GABA release in isolated self-innervating SCN neurons. J Neurosci 16:7711-7724.
10. Chronwall BM (1985) Anatomy and physiology of the neuroendocrine arcuate nucleus. Peptides 6 [Suppl 2]:1-11.
11. Chronwall BM, Pisano JJ, Bishop JF, Moody TW, O'Donohue TL (1985a) Biochemical and histochemical characterization of ranatensin immuno-reactive peptides in rat brain: Lack of coexistence with bombesin/GRP. Brain Res 338:97-113.
12. Chronwall BM, DiMaggio DA, Massari VJ, Pickel VM, Ruggiero DA, O'Donohue TL. (1985b) The anatomy of neuropeptide-Y-containing neurons in rat brain. Neuroscience 15:1159-1181.
13. Coll AP, Farooqi IS, O'Rahilly S (2007) The hormonal control of food intake. Cell 129:251-262.
14. Colmers WF, Wahlestedt C (1993) The biology of neuropeptide Y and related peptides. Totovva, NJ: Humana.
15. Colmers WF, Klapstein GJ, Fournier A, St-Pierre S, Treherne KA (1991) Presynaptic inhibition by neuropeptide Y in rat hippocampal slice in vitro is mediated by a Y2 receptor. Br J Pharmacol 102:41-44.
16. Cone RD (2006) Studies on the physiological functions of the melanocortin system. Endocr Rev 27:736-749.
17. Cota D, Tschop MH, Horvath TL, Levine AS (2006) Cannabinoids, opioids and eating behavior: The molecular face of hedonism? Brain Res Rev 51:85-107.
18. Cowley MA, Smart JL, Rubinstein M, Cerdán MG, Diano S, Horvath TL, Cone RD, Low MJ (2001) Leptin activates anorexigenic POMC neurons through a neural network in the arcuate nucleus. Nature 411:480-484.
19. Cowley MA, Smith RG, Diano S, Tschöp M, Pronchuk N, Grove KL, Stras-burger CJ, Bidlingmaier M, Esterman M, Heiman ML, Garcia-Segura LM, Nillni EA, Mendez P, Low MJ, Sotonyi P, Friedman JM, Liu H, Pinto S, Colmers WF, Cone RD, Horvath TL (2003) The distribution and mechanism of action of ghrelin in the CNS demonstrates a novel hypothalamic circuit regulating energy homeostasis. Neuron 37:649-661.
20. de Quidt ME, Emson PC (1986) Distribution of neuropeptide Y-like immunoreactivity in the rat central nervous system-II. Immunohisto chemical analysis. Neuroscience 18:545-618.
21. Elias CF, Lee C, Kelly J, Aschkenasi C, Ahima RS, Couceyro PR, Kuhar MJ, Saper CB, Elmquist JK (1998) Leptin activates hypothalamic CART neurons projecting to the spinal cord. Neuron 21:1375-1385.
22. Elias CF, Aschkenasi C, Lee C, Kelly J, Ahima RS, Bjorbaek C, Flier JS, Saper CB, Elmquist JK (1999) Leptin differentially regulates NPY and POMC neurons projecting to the lateral hypothalamic area. Neuron 23:775-786.
23. Elmquist JK, Elias CF, Saper CB (1999) From lesions to leptin: Hypothalamic control of food intake and body weight. Neuron 22:221-232.
24. Eriksson KS, Sergeeva O, Brown RE, Haas HL (2001) Orexin/hypocretin excites the histaminergic neurons of the tuberomammillary nucleus. J Neurosci 21:9273-9279.
25. Flynn FW (1993) Fourth ventricular injection of selective bombesin receptor antagonists facilitates feeding in rats. Am J Physiol 264:R218-R221.
26. Flynn FW (1989) Fourth ventricle bombesin injection suppresses ingestive behaviors in rats. Am J Physiol 256:R590-R596.
27. Fu LY, van den Pol AN (2007) GABA excitation in mouse hilar neuropeptide Y neurons. J Physiol 579:445-464.
28. Fu LY, van den Pol AN (2008) Agouti-related peptide and MC3/4 receptor agonists both inhibit excitatory hypothalamic ventromedial nucleus neurons. J Neurosci 28:5433-5449.
29. Fu LY, Acuna-Goycolea C, van den Pol AN (2004) Neuropeptide Y inhibits hypocretin/orexin neurons by multiple presynaptic and postsynaptic mechanisms: Tonic depression of the hypothalamic arousal system. J Neurosci 24:8741-8751.
30. Gao XB, van den Pol AN (2001) Melanin concentrating hormone depresses synaptic activity of glutamate and GABA neurons from rat lateral hypo-thalamus. J Physiol 533:237-252.
31. Gehlert DR, Chronwall BM, Schafer MP, O'Donohue TL (1987) Localization of neuropeptide Y messenger ribonucleic acid in rat and mouse brain by in situ hybridization. Synapse 1:25-31.
32. Gibbs J, Fauser DJ, Rowe EA, Rolls BJ, Rolls ET, Maddison SP (1979) Bombesin suppresses feeding in rats. Nature 282:208-210.
33. Gonzalez N, Moody TW, Igarashi H, Ito T, Jensen RT (2008) Bombesin-related peptides and their receptors: Recent advances in their role in physiology and disease states. Curr Opin Endocrinol Diabetes Obes 15:58-64.
34. Grove KL, Chen P, Koegler FH, Schiffmaker A, Susan Smith M, Cameron JL (2003) Fasting activates neuropeptide Y neurons in the arcuate nucleus and the paraventricular nucleus in the rhesus macaque. Mol Brain Res 113:133-138.
35. Gutzwiller JP, Drewe J, Hildebrand P, Rossi L, Lauper JZ, Beglinger C (1994) Effect of intravenous human gastrin-releasing peptide on food intake in humans. Gastroenterology 106:1168-1173.
36. 2+ activate a transient inward current in chick dorsal root ganglion cells. Biophys J, 50:753-757.
37. Hahn TM, Breininger JF, Baskin DG, Schwartz MW (1998) Coexpression of Agrp and NPY in fasting-activated hypothalamic neurons. Nat Neurosci 1:271-272.
38. Halaszovich CR, Zitt C, Jungling E, Luckhoff A (2000) Inhibition of TRP3 channels by lanthanides. Block from the cytosolic side of the plasma membrane. J Biol Chem 275:37423-37428.
39. Heisler LK, Cowley MA, Tecott LH, Fan W, Low MJ, Smart JL, Rubinstein M, Tatro JB, Marcus JN, Holstege H, Lee CE, Cone RD, Elmquist JK (2002) Activation of central melanocortin pathways by fenfluramine. Science 297:609-611.
40. Heisler LK, Jobst EE, Sutton GM, Zhou L, Borok E, Thornton-Jones Z, Liu HY, Zigman JM, Balthasar N, Kishi T, Lee CE, Aschkenasi CJ, Zhang CY, Yu J, Boss O, Mountjoy KG, Clifton PG, Lowell BB, Friedman JM, Hor-vath T, Butler AA, Elmquist JK, Cowley MA (2006) Serotonin reciprocally regulates melanocortin neurons to modulate food intake. Neuron 51:239-249.
41. Hentges ST, Low MJ, Williams JT (2005) Differential regulation of synaptic inputs by constitutively released endocannabinoids and exogenous cannabinoids. J Neurosci 25:9746-9751.
42. Hogan B, Costantini F, Lacey E (1986) Introduction of new genetic information into the developing mouse embryo. In: Manipulating the mouse embryo, pp. 153-197. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
43. 2+ exchange in cells expressing NCX1. J Biol Chem 271:22391-22397.
44. Jensen RT, Battey JF, Spindel ER, Benya RV (2008) International union of pharmacology. LXVIII Mammalian bombesin receptors: Nomenclature, distribution, pharmacology, signaling, and functions in normal and disease states. Pharmacol Rev 60:1-42.
45. Jobst EE, Enriori PJ, Cowley MA (2004) The electro physiology of feeding circuits. Trends Endocrinol Metab 15:488-499.
46. Kamichi S, Wada E, Aoki S, Sekiguchi M, Kimura I, Wada K (2005) Immunohisto chemical localization of gastrin-releasing peptide receptor in the mouse brain. Brain Res 1032:162-170.
47. Kang L, Routh VH, Kuzhikandathil EV, Gaspers LD, Levin BE (2004) Physiological and molecular characteristics of rat hypothalamic ventromedial nucleus glucosensing neurons. Diabetes 53:549-559.
48. Kim MS, Pak YK, Jang PG, Namkoong C, Choi YS, Won JC, Kim KS, Kim SW, Kim HS, Park JY, Kim YB, Lee KU (2006) Role of hypothalamic Foxo1 in the regulation of food intake and energy homeostasis. Nat Neurosci 9:901-906.
49. Kimura J, Miyamae S, Noma A (1987) Identification of sodium-calcium exchange current in single ventricular cells of guinea-pig. J Physiol 384: 199-222.
50. Kopp J, Xu ZQ, Zhang X, Pedrazzini T, Herzog H, Kresse A, Wong H, Walsh JH, Hökfelt T (2002) Expression of the neuropeptide Y Y1 receptor in the CNS of rat and of wild-type and Y1 receptor knock-out mice. Focus on immunohisto chemical localization. Neuroscience 111:443-532.
51. Kumarnsit E, Johnstone LE, Leng G (2003) Actions of neuropeptide Y and growth hormone secretagogues in the arcuate nucleus and ventromedial hypothalamic nucleus. Eur J Neurosci 17:937-944.
52. Ladenheim EE, Knipp S (2007) Capsaicin treatment differentially affects feeding suppression by bombesin-like peptides. Physiol Behav 91:36-41.
53. Ladenheim EE, Taylor JE, Coy DH, Moran TH (1994) Blockade of feeding inhibition by neuromedin B using a selective receptor antagonist. Eur J Pharmacol 271:R7-R9.
54. Ladenheim EE, Taylor JE, Coy DH, Carrigan TS, Wohn A, Moran TH (1997) Caudal hindbrain neuromedin B-preferring receptors participate in the control of food intake. Am J Physiol 272:R433-R437.
55. Lee EC, Yu D, Martinez de Velasco J, Tessarollo L, Swing DA, Court DL, Jenkins NA, Copeland NG (2001) A highly efficient Escherichia coli-based chromosome engineering system adapted for recombinogenic targeting and subcloning of BAC DNA. Genomics 73:56-65.
56. Lin JY, Pan JT (1994) Stimulatory effects of bombesin-like peptides on hypothalamic arcuate neurons in rat brain slices. Brain Res Bull 35:241-246.
57. Liu RJ, van den Pol AN, Aghajanian GK (2002) Hypocretins (orexins) regulate serotonin neurons in the dorsal raphe nucleus by excitatory direct and inhibitory indirect actions. J Neurosci 22:9453-9464.
58. McDonald JK, Koenig JI (1993) Neuropeptide Y actions on reproductive and endocrine functions. In: The biology of Neuropeptide Y and related peptides (Colmers WF and Wahlestedt C, eds), pp 419-456. Totowa NJ: Humana.
59. Merali Z, Moody TW, Coy D (1993) Blockade of brain bombesin/GRP receptors increases food intake in satiated rats. Am J Physiol 264:R1031-R1034.
60. Merali Z, McIntosh J, Kent P, Michaud D, Anisman H (1998) Aversive and appetitive events evoke the release of corticotropin-releasing hormone and bombesin-like peptides at the central nucleus of the amygdala. J Neurosci 18:4758-4766.
61. Mikkelsen JD, Larsen PJ, O'Hare MM, Wiegand SJ (1991) Gastrin releasing peptide in the rat suprachiasmatic nucleus: An immunohisto chemical, chromatographic and radioimmunological study. Neuroscience 40:55-66.
62. Moody TW, Merali Z (2004) Bombesin-like peptides and associated receptors within the brain: Distribution and behavioral implications. Peptides 25:511-520.
63. Muurahainen NE, Kissileff HR, Pi-Sunyer FX (1993) Intravenous infusion of bombesin reduces food intake in humans. Am J Physiol 264:R350-R354.
64. Myojin T, Kitamura N, Hondo E, Baltazar ET, Pearson GT, Yamada J (2000) Immunohisto chemical localization of neuropeptides in bovine pancreas. Anat Histol Embryol 29:167-172.
65. Ohki-Hamazaki H, Watase K, Yamamoto K, Ogura H, Yamano M, Yamada K, Maeno H, Imaki J, Kikuyama S, Wada E, Wada K (1997) Micelacking bombesin receptor subtype-3 develop metabolic defects and obesity. Nature 390:165-169.
66. Panula P, Yang HY, Costa E (1982) Neuronal location of the bombesin-like immunoreactivity in the central nervous system of the rat. Regul Pept 4:275-283.
67. Paxinos G and Franklin KB (2001) The mouse brain in stereotaxic coordinates. Amsterdam: Elsevier.
68. Pinto S, Roseberry AG, Liu H, Diano S, Shanabrough M, Cai X, Friedman JM, Horvath TL (2004) Rapid rewiring of arcuate nucleus feeding circuits by leptin. Science 304:110-115.
69. Rhim H, Kinney GA, Emmerson PJ, Miller RJ (1997) Regulation of neuro-transmission in the arcute nucleus of the rat by different neuropeptide Y receptors. J Neurosci 17:2980-2989.
70. Roseberry AG, Liu H, Jackson AC, Cai X, Friedman JM (2004) Neuropep-tide Y-mediated inhibition of proopiomelanocortin neurons in the arcuate nucleus shows enhanced desensitization in ob/ob mice. Neuron 41:711-722.
71. Saper CB, Loewy AD, Swanson LW, Cowan WM (1976) Direct hypothalamo-autonomic connections. Brain Res 117:305-312.
72. Saper CB, Chou TC, Elmquist JK (2002) The need to feed: Homeostatic and hedonic control of eating. Neuron 36:199-211.
73. Schwartz MW, Woods SC, Porte D Jr, Seeley RJ, Baskin DG (2000) Central nervous system control of food intake. Nature 404:661-671.
74. Seeley RJ, Woods SC (2003) Monitoring of stored and available fuel by the CNS: Implications for obesity. Nat Rev Neurosci 4:901-909.
75. Sekizawa S, Bonham AC (2006) Group I metabotropic glutamate receptors on second-order baroreceptor neurons are tonically activated and induce a Na+-Ca2+ exchange current. J Neurophysiol 95:882-892.
76. Stanley BG, Leibowitz SF (1985) NPY injected in the paraventricular hypothalamus: A powerful stimulant of feeding behavior. Proc Natl Acad Sci U S A 82:3940-3943.
77. Swanson LW, Kuypers HG (1980) A direct projection from the ventromedial nucleus and retrochiasmatic area of the hypothalamus to the medulla and spinal cord of the rat. Neurosci Lett 17:307-312.
78. Tsushima H, Mori M (2005) Mechanisms underlying anorexia after micro-injection of bombesin into the lateral cerebroventricle. Pharmacol Biochem Behav 80:289-296.
79. Ubink R, Hökfelt T (2000) Expression of neuropeptide Y in olfactory ensheathing cells during prenatal development. J Comp Neurol 423:13-22.
80. Ubink R, Halasz N, Zhang X, Dagerlind A, Hökfelt T (1994) Neuropeptide tyrosine is expressed in ensheathing cells around the olfactory nerves in the rat olfactory bulb. Neuroscience 60:709-726.
81. van den Pol AN, Obrietan K, Chen G, Belousov AB (1996) Neuropeptide Y-mediated long-term depression of excitatory activity in suprachias-matic nucleus neurons. J Neurosci 16:5883-5895.
82. van den Pol AN, Acuna-Goycolea C, Clark KR, Ghosh PK (2004) Physiological properties of hypothalamic MCH neurons identified with selective expression of reporter gene after recombinant virus infection. Neuron 42:635-652.
83. van den Top M, Lee K, Whyment AD, Blanks AM, Spanswick D (2004) Orexigen-sensitive NPY/AgRP pacemaker neurons in the hypothalamic arcuate nucleus. Nat Neurosci 7:493-494.
84. Wada E, Way J, Lebacq-Verheyden AM, Battey JF (1990) Neuromedin B and gastrin-releasing peptide mRNAs are differentially distributed in the rat nervous system. J Neurosci 10:2917-2930.
85. Wada E, Way J, Shapira H, Kusano K, Lebacq-Verheyden AM, Coy D, Jensen R, Battery J (1991) cDNA cloning, characterization and brain region-specific expression of a neuromedin-B-preferring bombesin receptor. Neuron 6:421-430.
86. Wada E, Wray S, Key S, Battey J (1992) Comparison of gene expression for two distinct bombesin receptor subtypes in postnatal rat central nervous system. Mol Cell Neurosci 3:446-460.
87. Wu M, Zaborszky L, Hajszan T, van den Pol AN, Alreja M (2004) Hypocre-tin/orexin innervation and excitation of identified septohippocampal cholinergic neurons. J Neurosci 24:3527-3536.
88. Xiong Z, Lu W, MacDonald JF (1997) Extracellular calcium sensed by a novel cation channel in hippocampal neurons. Proc Natl Acad Sci U S A 94:7012-7017.
89. Zarbin MA, Kuhar MJ, O'Donohue TL, Wolf SS, Moody TW (1985) Auto-radiographic localization of (125I-Tyr4)bombesin binding sites in rat brain. J Neurosci 5:429-437.
90. Zhang C, Bosch MA, Levine JE, Ronnekleiv OK, Kelly MJ (2007) Gonadotropin-releasinghormone neurons express K(ATP) channels that are regulated by estrogen and responsive to glucose and metabolic inhibition. J Neurosci 27:10153-10164.