Hypothalamic injection of non-opioid peptides increases gene expression of the opioid enkephalin in hypothalamic and mesolimbic nuclei: Possible mechanism underlying their behavioral effects

Peptides

Volumn 30, Issue 12, 2009, Pages 2423-2431

  Karatayev, Olga ^a   Barson, Jessica R ^a   Chang, Guo Qing ^a   Leibowitz, Sarah F ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

Enkephalin; Galanin; mRNA; Orexin; Rat

Indexed keywords

ALCOHOL; DIGOXIGENIN; ENKEPHALIN; FAT; GALANIN; GALANIN RECEPTOR; MESSENGER RNA; OREXIN; OREXIN 1 RECEPTOR; OREXIN 2 RECEPTOR; SODIUM CHLORIDE;

ALCOHOL CONSUMPTION; AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; FAT INTAKE; FEEDING BEHAVIOR; GENE EXPRESSION; HYPOTHALAMUS; HYPOTHALAMUS PERIVENTRICULAR NUCLEUS; IN SITU HYBRIDIZATION; ISOTOPE LABELING; LIMBIC CORTEX; MALE; NERVE CELL; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; RECEPTOR DENSITY; THALAMUS MIDLINE NUCLEUS; VENTRAL TEGMENTUM;

ANIMALS; CELL NUCLEUS; ENKEPHALINS; GALANIN; GENE EXPRESSION; HYPOTHALAMUS; IN SITU HYBRIDIZATION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; NEUROPEPTIDES; NEUROTRANSMITTER AGENTS; NUCLEUS ACCUMBENS; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; VENTRAL TEGMENTAL AREA;

RATTUS;

EID: 70449670323     PISSN: 01969781     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.peptides.2009.09.025     Document Type: Article

References (97)

1. Ahima R.S., Garcia M.M., and Harlan R.E. Glucocorticoid regulation of preproenkephalin gene expression in the rat forebrain. Brain Res Mol Brain Res 16 (1992) 119-127
2. Ambati S., Duan J., Choi Y.H., Hartzell D.L., Della-Fera M.A., and Baile C.A. ICV vs. VMH injection of leptin: comparative effects on hypothalamic gene expression. Behav Brain Res 196 (2009) 279-285
3. Backberg M., Hervieu G., Wilson S., and Meister B. Orexin receptor-1 (OX-R1) immunoreactivity in chemically identified neurons of the hypothalamus: focus on orexin targets involved in control of food and water intake. Eur J Neurosci 15 (2002) 315-328
4. Bals-Kubik R., Ableitner A., Herz A., and Shippenberg T.S. Neuroanatomical sites mediating the motivational effects of opioids as mapped by the conditioned place preference paradigm in rats. J Pharmacol Exp Ther 264 (1993) 489-495
5. Barson JR, Carr A, Soun JE, Sobhani NC, Rada P, Leibowitz SF, et al. Opioids in the hypothalamic paraventricular nucleus stimulate ethanol intake. Unpublished results 2009.
6. Cassell M.D., Gray T.S., and Kiss J.Z. Neuronal architecture in the rat central nucleus of the amygdala: a cytological, hodological, and immunocytochemical study. J Comp Neurol 246 (1986) 478-499
7. Chang G.-Q., Gaysinskaya V., Karatayev O., and Leibowitz S.F. Maternal high-fat diet and fetal programming: increased proliferation of hypothalamic peptide-producing neurons that increase risk for overeating and obesity. J Neurosci 28 (2008) 12107-12119
8. Chang G.-Q., Karatayev O., Ahsan R., Avena N.M., Lee C., Lewis M.J., et al. Effect of ethanol on hypothalamic opioid peptides, enkephalin, and dynorphin: relationship with circulating triglycerides. Alcohol Clin Exp Res 31 (2007) 249-259
9. Chang GQ, Barson JR, Karatayev O, Chang SY, Chan YW, Leibowitz SF. Effect of chronic ethanol on enkephalin in the hypothalamus and extra-hypothalamic areas. Unpublished results 2009.
10. Chang G.Q., Karatayev O., Ahsan R., Gaysinskaya V., Marwil Z., and Leibowitz S.F. Dietary fat stimulates endogenous enkephalin and dynorphin in the paraventricular nucleus: role of circulating triglycerides. Am J Physiol Endocrinol Metab 292 (2007) E561-E570
11. Chang G.Q., Karatayev O., Davydova Z., and Leibowitz S.F. Circulating triglycerides impact on orexigenic peptides and neuronal activity in hypothalamus. Endocrinology 145 (2004) 3904-3912
12. Clegg D.J., Air E.L., Woods S.C., and Seeley R.J. Eating elicited by orexin-A, but not melanin-concentrating hormone, is opioid mediated. Endocrinology 143 (2002) 2995-3000
13. Corwin R.L., Robinson J.K., and Crawley J.N. Galanin antagonists block galanin-induced feeding in the hypothalamus and amygdala of the rat. Eur J Neurosci 5 (1993) 1528-1533
14. Cowen M.S., and Lawrence A.J. Alterations in central preproenkephalin mRNA expression after chronic free-choice ethanol consumption by fawn-hooded rats. Alcohol Clin Exp Res 25 (2001) 1126-1133
15. Curran E.J., and Watson Jr. S.J. Dopamine receptor mRNA expression patterns by opioid peptide cells in the nucleus accumbens of the rat: a double in situ hybridization study. J Comp Neurol 361 (1995) 57-76
16. Date Y., Ueta Y., Yamashita H., Yamaguchi H., Matsukura S., Kangawa K., et al. Orexins, orexigenic hypothalamic peptides, interact with autonomic, neuroendocrine and neuroregulatory systems. Proc Natl Acad Sci USA 96 (1999) 748-753
17. de Gortari P., Mendez M., Rodriguez-Keller I., Perez-Martinez L., and Joseph-Bravob P. Acute ethanol administration induces changes in TRH and proenkephalin expression in hypothalamic and limbic regions of rat brain. Neurochem Int 37 (2000) 483-496
18. de Lecea L., Kilduff T.S., Peyron C., Gao X., Foye P.E., Danielson P.E., et al. The hypocretins: hypothalamus-specific peptides with neuroexcitatory activity. Proc Natl Acad Sci USA 95 (1998) 322-327
19. Di Chiara G. Nucleus accumbens shell and core dopamine: differential role in behavior and addiction. Behav Brain Res 137 (2002) 75-114
20. Dube M.G., Horvath T.L., Leranth C., Kalra P.S., and Kalra S.P. Naloxone reduces the feeding evoked by intracerebroventricular galanin injection. Physiol Behav 56 (1994) 811-813
21. Dube M.G., Kalra S.P., and Kalra P.S. Food intake elicited by central administration of orexins/hypocretins: identification of hypothalamic sites of action. Brain Res 842 (1999) 473-477
22. Ericson E., and Ahlenius S. Suggestive evidence for inhibitory effects of galanin on mesolimbic dopaminergic neurotransmission. Brain Res 822 (1999) 200-209
23. Foster K.L., McKay P.F., Seyoum R., Milbourne D., Yin W., Sarma P.V., et al. GABA(A) and opioid receptors of the central nucleus of the amygdala selectively regulate ethanol-maintained behaviors. Neuropsychopharmacology 29 (2004) 269-284
24. Furudono Y., Ando C., Yamamoto C., Kobashi M., and Yamamoto T. Involvement of specific orexigenic neuropeptides in sweetener-induced overconsumption in rats. Behav Brain Res 175 (2006) 241-248
25. Garzon M., and Pickel V.M. Ultrastructural localization of enkephalin and mu-opioid receptors in the rat ventral tegmental area. Neuroscience 114 (2002) 461-474
26. Georges F., Stinus L., Bloch B., and Le Moine C. Chronic morphine exposure and spontaneous withdrawal are associated with modifications of dopamine receptor and neuropeptide gene expression in the rat striatum. Eur J Neurosci 11 (1999) 481-490
27. Giraudo S.Q., Billington C.J., and Levine A.S. Effects of the opioid antagonist naltrexone on feeding induced by DAMGO in the central nucleus of the amygdala and in the paraventricular nucleus in the rat. Brain Res 782 (1998) 18-23
28. Gosnell B.A. Involvement of mu opioid receptors in the amygdala in the control of feeding. Neuropharmacology 27 (1988) 319-326
29. Gundlach A.L., Burazin T.C., and Larm J.A. Distribution, regulation and role of hypothalamic galanin systems: renewed interest in a pleiotropic peptide family. Clin Exp Pharmacol Physiol 28 (2001) 100-105
30. Gundlach A.L., Wisden W., Morris B.J., and Hunt S.P. Localization of preprogalanin mRNA in rat brain: in situ hybridization study with a synthetic oligonucleotide probe. Neurosci Lett 114 (1990) 241-247
31. Harris G.C., and Aston-Jones G. Arousal and reward: a dichotomy in orexin function. Trends Neurosci 29 (2006) 571-577
32. Hasue R.H., and Shammah-Lagnado S.J. Origin of the dopaminergic innervation of the central extended amygdala and accumbens shell: a combined retrograde tracing and immunohistochemical study in the rat. J Comp Neurol 454 (2002) 15-33
33. Hawes J.J., and Picciotto M.R. Characterization of GalR1, GalR2, and GalR3 immunoreactivity in catecholaminergic nuclei of the mouse brain. J Comp Neurol 479 (2004) 410-423
34. Hebb A.L., Zacharko R.M., Gauthier M., Trudel F., Laforest S., and Drolet G. Brief exposure to predator odor and resultant anxiety enhances mesocorticolimbic activity and enkephalin expression in CD-1 mice. Eur J Neurosci 20 (2004) 2415-2429
35. Heyser C.J., Roberts A.J., Schulteis G., and Koob G.F. Central administration of an opiate antagonist decreases oral ethanol self-administration in rats. Alcohol Clin Exp Res 23 (1999) 1468-1476
36. Honkaniemi J. Colocalization of peptide- and tyrosine hydroxylase-like immunoreactivities with Fos-immunoreactive neurons in rat central amygdaloid nucleus after immobilization stress. Brain Res 598 (1992) 107-113
37. June H.L., Cummings R., Eiler II W.J., Foster K.L., McKay P.F., Seyoum R., et al. Central opioid receptors differentially regulate the nalmefene-induced suppression of ethanol- and saccharin-reinforced behaviors in alcohol-preferring (P) rats. Neuropsychopharmacology 29 (2004) 285-299
38. Kane J.K., Parker S.L., Matta S.G., Fu Y., Sharp B.M., and Li M.D. Nicotine up-regulates expression of orexin and its receptors in rat brain. Endocrinology 141 (2000) 3623-3629
39. Kelley A.E., Baldo B.A., Pratt W.E., and Will M.J. Corticostriatal-hypothalamic circuitry and food motivation: integration of energy, action and reward. Physiol Behav 86 (2005) 773-795
40. Kelley A.E., Will M.J., Steininger T.L., Zhang M., and Haber S.N. Restricted daily consumption of a highly palatable food (chocolate Ensure(R)) alters striatal enkephalin gene expression. Eur J Neurosci 18 (2003) 2592-2598
41. Kim E.M., Quinn J.G., Levine A.S., and O'Hare E. A bi-directional mu-opioid-opioid connection between the nucleus of the accumbens shell and the central nucleus of the amygdala in the rat. Brain Res 1029 (2004) 135-139
42. Koob G.F. Dynamics of neuronal circuits in addiction: reward, antireward, and emotional memory. Pharmacopsychiatry 42 Suppl. (1) (2009) S32-41
43. Koob G.F., and Le Moal M. Review. Neurobiological mechanisms for opponent motivational processes in addiction. Philos Trans R Soc Lond B: Biol Sci 363 (2008) 3113-3123
44. Kyrkouli S.E., Stanley B.G., Seirafi R.D., and Leibowitz S.F. Stimulation of feeding by galanin: anatomical localization and behavioral specificity of this peptide's effects in the brain. Peptides 11 (1990) 995-1001
45. Leibowitz S.F., Akabayashi A., Wang J., Alexander J.T., Dourmashkin J.T., and Chang G.Q. Increased caloric intake on a fat-rich diet: role of ovarian steroids and galanin in the medial preoptic and paraventricular nuclei and anterior pituitary of female rats. J Neuroendocrinol 19 (2007) 753-766
46. Levine A.S., Olszewski P.K., Mullett M.A., Pomonis J.D., Grace M.K., Kotz C.M., et al. Intra-amygdalar injection of DAMGO: effects on c-Fos levels in brain sites associated with feeding behavior. Brain Res 1015 (2004) 9-14
47. Loughlin S.E., Islas M.I., Cheng M.Y., Lee A.G., Villegier A.S., and Leslie F.M. Nicotine modulation of stress-related peptide neurons. J Comp Neurol 497 (2006) 575-588
48. Lu X.Y., Bagnol D., Burke S., Akil H., and Watson S.J. Differential distribution and regulation of OX1 and OX2 orexin/hypocretin receptor messenger RNA in the brain upon fasting. Horm Behav 37 (2000) 335-344
49. Lucas L.R., Pompei P., Ono J., and McEwen B.S. Effects of adrenal steroids on basal ganglia neuropeptide mRNA and tyrosine hydroxylase radioimmunoreactive levels in the adrenalectomized rat. J Neurochem 71 (1998) 833-843
50. MacDonald A.F., Billington C.J., and Levine A.S. Alterations in food intake by opioid and dopamine signaling pathways between the ventral tegmental area and the shell of the nucleus accumbens. Brain Res 1018 (2004) 78-85
51. Martin G., Fabre V., Siggins G.R., and de Lecea L. Interaction of the hypocretins with neurotransmitters in the nucleus accumbens. Regul Pept 104 (2002) 111-117
52. McLean S., and Hoebel B.G. Feeding induced by opiates injected into the paraventricular hypothalamus. Peptides 4 (1983) 287-292
53. Mitchell V., Bouret S., Howard A.D., and Beauvillain J.C. Expression of the galanin receptor subtype Gal-R2 mRNA in the rat hypothalamus. J Chem Neuroanat 16 (1999) 265-277
54. Mitchell V., Habert-Ortoli E., Epelbaum J., Aubert J.P., and Beauvillain J.C. Semiquantitative distribution of galanin-receptor (GAL-R1) mRNA-containing cells in the male rat hypothalamus. Neuroendocrinology 66 (1997) 160-172
55. Mucha R.F., and Iversen S.D. Increased food intake after opioid microinjections into nucleus accumbens and ventral tegmental area of rat. Brain Res 397 (1986) 214-224
56. Naleid A.M., Grace M.K., Chimukangara M., Billington C.J., and Levine A.S. Paraventricular opioids alter intake of high-fat but not high-sucrose diet depending on diet preference in a binge model of feeding. Am J Physiol: Regul Integr Comp Physiol 293 (2007) R99-R105
57. Narita M., Nagumo Y., Hashimoto S., Narita M., Khotib J., Miyatake M., et al. Direct involvement of orexinergic systems in the activation of the mesolimbic dopamine pathway and related behaviors induced by morphine. J Neurosci 26 (2006) 398-405
58. Noel M.B., and Wise R.A. Ventral tegmental injections of a selective mu or delta opioid enhance feeding in food-deprived rats. Brain Res 673 (1995) 304-312
59. O'Donnell D., Ahmad S., Wahlestedt C., and Walker P. Expression of the novel galanin receptor subtype GALR2 in the adult rat CNS: distinct distribution from GALR1. J Comp Neurol 409 (1999) 469-481
60. Oades R.D., and Halliday G.M. Ventral tegmental (A10) system: neurobiology. 1. Anatomy and connectivity. Brain Res 434 (1987) 117-165
61. Oliva J.M., and Manzanares J. Gene transcription alterations associated with decrease of ethanol intake induced by naltrexone in the brain of Wistar rats. Neuropsychopharmacology 32 (2007) 1358-1369
62. Palmiter R.D. Is dopamine a physiologically relevant mediator of feeding behavior?. Trends Neurosci 30 (2007) 375-381
63. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates (1998), Academic Press, New York
64. Phillips A.G., and LePiane F.G. Reward produced by microinjection of (d-Ala2), Met5-enkephalinamide into the ventral tegmental area. Behav Brain Res 5 (1982) 225-229
65. Quinn J.G., O'Hare E., Levine A.S., and Kim E.M. Evidence for a mu-opioid-opioid connection between the paraventricular nucleus and ventral tegmental area in the rat. Brain Res 991 (2003) 206-211
66. Rada P., Avena N.M., Leibowitz S.F., and Hoebel B.G. Ethanol intake is increased by PVN galanin injection and reduced by a GAL antagonist. Alcohol 33 (2004) 91-97
67. Rada P, Barson JR, Leibowitz SF, Hoebel BG. Opioids in the hypothalamus control dopamine and acetylcholine levels in the nucleus accumbens. Unpublished results 2009.
68. Rada P., Mark G.P., and Hoebel B.G. Galanin in the hypothalamus raises dopamine and lowers acetylcholine release in the nucleus accumbens: a possible mechanism for hypothalamic initiation of feeding behavior. Brain Res 798 (1998) 1-6
69. Ragnauth A., Ruegg H., and Bodnar R.J. Evaluation of opioid receptor subtype antagonist effects in the ventral tegmental area upon food intake under deprivation, glucoprivic and palatable conditions. Brain Res 767 (1997) 8-16
70. Reagan L.P., Rosell D.R., Wood G.E., Spedding M., Munoz C., Rothstein J., et al. Chronic restraint stress up-regulates GLT-1 mRNA and protein expression in the rat hippocampus: reversal by tianeptine. Proc Natl Acad Sci USA 101 (2004) 2179-2184
71. Rodaros D., Caruana D.A., Amir S., and Stewart J. Corticotropin-releasing factor projections from limbic forebrain and paraventricular nucleus of the hypothalamus to the region of the ventral tegmental area. Neuroscience 150 (2007) 8-13
72. Sakanaka M., Magari S., Shibasaki T., and Inoue N. Co-localization of corticotropin-releasing factor- and enkephalin-like immunoreactivities in nerve cells of the rat hypothalamus and adjacent areas. Brain Res 487 (1989) 357-362
73. Sakurai T., Amemiya A., Ishii M., Matsuzaki I., Chemelli R.M., Tanaka H., et al. Orexins and orexin receptors: a family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell 92 (1998) 573-585
74. Sawchenko P.E., and Pfeiffer S.W. Ultrastructural localization of neuropeptide Y and galanin immunoreactivity in the paraventricular nucleus of the hypothalamus in the rat. Brain Res 474 (1988) 231-245
75. Schneider E.R., Rada P., Darby R.D., Leibowitz S.F., and Hoebel B.G. Orexigenic peptides and alcohol intake: differential effects of orexin, galanin, and ghrelin. Alcohol: Clin Exp Res 31 (2007) 1858-1865
76. See R.E. Neural substrates of cocaine-cue associations that trigger relapse. Eur J Pharmacol 526 (2005) 140-146
77. Shandra A.A., Mazarati A.M., and Servetskii K.L. Influence of the neuropeptide galanin on active avoidance in rats. Neurosci Behav Physiol 24 (1994) 429-432
78. Shirayama Y., and Chaki S. Neurochemistry of the nucleus accumbens and its relevance to depression and antidepressant action in rodents. Curr Neuropharmacol 4 (2006) 277-291
79. Shor-Posner G., Azar A.P., Filart R., Tempel D., and Leibowitz S.F. Morphine-stimulated feeding: analysis of macronutrient selection and paraventricular nucleus lesions. Pharmacol Biochem Behav 24 (1986) 931-939
80. Smith B.K., York D.A., and Bray G.A. Effects of dietary preference and galanin administration in the paraventricular or amygdaloid nucleus on diet self-selection. Brain Res Bull 39 (1996) 149-154
81. Spangler R., Wittkowski K.M., Goddard N.L., Avena N.M., Hoebel B.G., and Leibowitz S.F. Opiate-like effects of sugar on gene expression in reward areas of the rat brain. Brain Res Mol Brain Res 124 (2004) 134-142
82. Swanson L.W. The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res Bull 9 (1982) 321-353
83. Sweet D.C., Levine A.S., and Kotz C.M. Functional opioid pathways are necessary for hypocretin-1 (orexin-A)-induced feeding. Peptides 25 (2004) 307-314
84. Tachibana T., Mori M., Khan M.S., Ueda H., Sugahara K., and Hiramatsu K. Central administration of galanin stimulates feeding behavior in chicks. Comp Biochem Physiol A: Mol Integr Physiol (2008)
85. Tempel D.L., Leibowitz K.J., and Leibowitz S.F. Effects of PVN galanin on macronutrient selection. Peptides 9 (1988) 309-314
86. Uhl G.R., Ryan J.P., and Schwartz J.P. Morphine alters preproenkephalin gene expression. Brain Res 459 (1988) 391-397
87. Valassi E., Scacchi M., and Cavagnini F. Neuroendocrine control of food intake. Nutr Metab Cardiovasc Dis 18 (2008) 158-168
88. Wallace D.M., Magnuson D.J., and Gray T.S. The amygdalo-brainstem pathway: selective innervation of dopaminergic, noradrenergic and adrenergic cells in the rat. Neurosci Lett 97 (1989) 252-258
89. Wallace D.M., Magnuson D.J., and Gray T.S. Organization of amygdaloid projections to brainstem dopaminergic, noradrenergic, and adrenergic cell groups in the rat. Brain Res Bull 28 (1992) 447-454
90. Wang S., and Gustafson E.L. Galanin receptor subtypes. Drug News Perspect 11 (1998) 458-468
91. Woods J.S., and Leibowitz S.F. Hypothalamic sites sensitive to morphine and naloxone: effects on feeding behavior. Pharmacol Biochem Behav 23 (1985) 431-438
92. Zachariou V., Brunzell D.H., Hawes J., Stedman D.R., Bartfai T., Steiner R.A., et al. The neuropeptide galanin modulates behavioral and neurochemical signs of opiate withdrawal. Proc Natl Acad Sci USA 100 (2003) 9028-9033
93. Zachariou V., Parikh K., and Picciotto M.R. Centrally administered galanin blocks morphine place preference in the mouse. Brain Res 831 (1999) 33-42
94. Zhang M., Gosnell B.A., and Kelley A.E. Intake of high-fat food is selectively enhanced by mu opioid receptor stimulation within the nucleus accumbens. J Pharmacol Exp Ther 285 (1998) 908-914
95. Zhang M., and Kelley A.E. Intake of saccharin, salt, and ethanol solutions is increased by infusion of a mu opioid agonist into the nucleus accumbens. Psychopharmacology (Berl) 159 (2002) 415-423
96. Zhang S., Blache D., Vercoe P.E., Adam C.L., Blackberry M.A., Findlay P.A., et al. Expression of orexin receptors in the brain and peripheral tissues of the male sheep. Regul Pept 124 (2005) 81-87
97. Zheng H., Patterson L.M., and Berthoud H.R. Orexin signaling in the ventral tegmental area is required for high-fat appetite induced by opioid stimulation of the nucleus accumbens. J Neurosci 27 (2007) 11075-11082