Endogenous opioids upregulate brain-derived neurotrophic factor mRNA through δ- and μ-opioid receptors independent of antidepressant-like effects

European Journal of Neuroscience

Volumn 23, Issue 4, 2006, Pages 984-994

  Zhang, Huina ^a   Torregrossa, Mary M ^a   Jutkiewicz, Emily M ^a   Shi, Yong Gong ^a   Rice, Kenner C ^b   Woods, James H ^a   Watson, Stanley J ^a   Holden Ko, M C ^a,c  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^c NATIONAL CHENGCHI UNIVERSITY   (Taiwan)

Author keywords

Amygdala; Forced swim test; Frontal cortex; Hippocampus; In situ hybridization; Neurotrophins

Indexed keywords

4 [ALPHA (4 ALLYL 2,5 DIMETHYL 1 PIPERAZINYL) 3 HYDROXYBENZYL] N,N DIETHYLBENZAMIDE; BETA ENDORPHIN; BRAIN DERIVED NEUROTROPHIC FACTOR; DELTA OPIATE RECEPTOR; ENDOMORPHIN 1; ENDOMORPHIN 2; KAPPA OPIATE RECEPTOR ANTAGONIST; MESSENGER RNA; METENKEPHALIN; MU OPIATE RECEPTOR; MU OPIATE RECEPTOR ANTAGONIST; NALTREXONE; NALTRINDOLE; NORBINALTORPHIMINE; OPIATE AGONIST; OPIATE ANTAGONIST; OPIATE PEPTIDE;

AMYGDALOID NUCLEUS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR; CONTROLLED STUDY; DEPRESSION; DRUG EFFECT; DRUG MECHANISM; FORCED SWIMMING TEST; FRONTAL CORTEX; HIPPOCAMPUS; IMMOBILIZATION; IN SITU HYBRIDIZATION; LOCOMOTION; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; UPREGULATION;

ANALGESICS, OPIOID; ANALYSIS OF VARIANCE; ANIMALS; AUTORADIOGRAPHY; BEHAVIOR, ANIMAL; BENZAMIDES; BRAIN-DERIVED NEUROTROPHIC FACTOR; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; FREEZING REACTION, CATALEPTIC; IN SITU HYBRIDIZATION; INJECTIONS, INTRAVENTRICULAR; MALE; NALTREXONE; NARCOTICS; OPIOID PEPTIDES; PIPERAZINES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, OPIOID, DELTA; RECEPTORS, OPIOID, MU; RNA, MESSENGER; SWIMMING; UP-REGULATION;

EID: 33644751619     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2006.04621.x     Document Type: Article

References (56)

1. Baamonde A. Dauge V. Ruiz-Gayo M. Fulga IG. Turcaud S. Fournie-Zaluski MC. Ronques BP. 1992 Antidepressant-type effects of endogenous enkephalins protected by systemic RB101 are mediated by opioid delta and dopamine D1 receptor stimulation EurJPharmacol 216 157 166
2. Bengzon J. Kokaia Z. Ernfors P. Kokaia M. Leanza G. Nilsson OG. Persson H. Lindvall O. 1993 Regulation of neurotrophin and trkA, trkB and trkC tyrosine kinase receptor messenger RNA expression in kindling Neuroscience 53 433 446
3. Bhattacharya SK. Saraswati M. Sen AP. 1992 Effect of centrally administered enkephalins on carrageenan-induced paw oedema in rats ResExpMed 192 443 449
4. Binder DK. Scharfman HE. 2004 Brain-derived neurotrophic factor Growth Factors 22 123 131
5. Bishop MJ. McNutt RW. 1995 An efficient synthesis of the benahydrylpiperazine delta opioid agonist (+)-BW373U86 BioorgMedChemLett 5 1311 1314
6. Bodnar RJ. Klein GE. 2004 Endogenous opiates and behavior: 2003 Peptides 25 2205 2256
7. Broom DC. Jutkiewicz EM. Folk JE. Traynor JR. Rice KC. Woods JH. 2002a Nonpeptidic delta-opioid receptor agonists reduce immobility in the forced swim assay in rats Neuropsychopharmacology 26 744 755
8. Broom DC. Jutkiewicz EM. Folk JE. Traynor JR. Rice KC. Woods JH. 2002b Convulsant activity of a non-peptidic delta-opioid receptor agonists is not required for its antidepressant effects in Sprague-Dawley rats Psychopharmacology 164 42 48
9. Cahill CM. McClellan KA. Morinville A. Hoffert C. Hubatsch D. O'Donnell D. Beaudet A. 2001 Immunohistochemical distribution of opioid receptors in the rat central nervous system: evidence for somatodendritic labeling and antigen-specific cellular compartmentalization JCompNeurol 440 65 84
10. Carrigan KA. Nelson CJ. Lysle DT. 2000 Endomorphin-1 induces antinociception without immunomodulatory effects in the rat Psychopharmacology 151 299 305
11. Castren E. 2004 Neurotrophins as mediators of drug effects on mood, addiction, and neuroprotection MolNeurobiol 29 289 302
12. Chang KJ. Rigdon GC. Howard JL. McNutt RW. 1993 A novel, potent and selective nonpeptidic delta opioid receptor agonist BW373U86 JPharmacolExpTher 267 852 857
13. Cryan JF. Markou A. Lucki I. 2002 Assessing antidepressant activity in rodents: recent developments and future needs Trends PharmacolSci 23 238 245
14. D'Sa C. Duman RS. 2002 Antidepressants and neuroplasticity BipolarDisord 4 183 194
15. Darko DF. Risch SC. Gillin JC. Golshan S. 1992 Association of beta-endorphin with specific clinical symptoms of depression AmJPsychiatry 149 1162 1167
16. Eisch AJ. Bolanos CA. de Wit J. Simonak RD. Pudiak CM. Barrot M. Verhaagen J. Nestler EJ. 2003 Brain-derived neurotrophic factor in the ventral midbrain-nucleus accumbens pathway: a role in depression BiolPsychiatry 54 994 1005
17. Elhassan AM. Papadogiannakis N. Adem A. Suliman I. Gad A. Lindgren JU. 2000 Intracerebroventricular met-enkephalin administration modulates adjuvant arthritis Brain Res 879 23 28
18. Ernfors P. Bengzon J. Kokaia Z. Persson H. Lindvall O. 1991 Increased levels of messenger RNAs for neurotrophic factors in the brain during kindling epileptogenesis Neuron 7 165 176
19. Filliol D. Ghozland S. Chluba J. Martin M. Matthes HW. Simonin F. Befort K. Gaveriaux-Ruff C. Dierich A. LeMeur M. Valverde O. Maldonado R. Kieffer BL. 2000 Mice deficient for delta- and mu-opioid receptors exhibit opposing alterations of emotional responses NatGenet 25 195 200
20. Gaveriaux-Ruff C. Kieffer BL. 2002 Opioid receptor genes inactivated in mice: the highlights Neuropeptides 36 62 71
21. Hashimoto K. Shimizu E. Iyo M. 2004 Critical role of brain-derived factor in mood disorders Brain ResRev 45 104 114
22. Hashimoto K. Watanabe K. Nishimura T. Iyo M. Shirayama Y. Minabe Y. 1998 Behavioral changes and expression of heat shock protein hsp-70 mRNA, brain-derived neurotrophic factor mRNA, and cyclooxygenase-2 mRNA in rat brain following seizures induced by systemic administration of kainic acid Brain Res 804 212 223
23. Hayes AG. Skingle M. Tyers MB. 1983 Antinociceptive profile of dynorphin in the rat Life Sci 33 657 660
24. Heese K. Otten U. Mathivet P. Raiteri M. Marescaux C. Bernasconi R. 2000 GABA(B) receptor antagonists elevate both mRNA and protein levels of the neurotrophins nerve growth factor (NGF) and brain-derived neurotrophic factor (BDNF) but not neurotrophin-3 (NT-3) in brain and spinal cord of rats Neuropharmacology 39 449 462
25. Huang EJ. Reichardt LF. 2001 Neurotrophins: roles in neuronal development and function AnnuRevNeurosci 24 677 736
26. Humpel C. Wetmore C. Olson L. 1993 Regulation of brain-derived neurotrophic factor messenger RNA and protein at the cellular level in pentylenetetrazol-induced epileptic seizures Neuroscience 53 909 918
27. Hung KC. Wu HE. Mizoguchi H. Tseng LF. 2002 Acute antinociceptive tolerance and unidirectional cross-tolerance to endomorphin-1 and endomorphin-2 given intraventricularly in the rat EurJPharmacol 448 169 174
28. Isackson PJ. Huntsman MM. Murray KD. Gall CM. 1991 BDNF mRNA expression is increased in adult rat forebrain after limbic seizures: temporal patterns of induction distinct from NGF Neuron 6 937 948
29. Jenab S. Kest B. Franklin SO. Inturrisi CE. 1995 Quantitative distribution of the delta opioid receptor mRNA in the mouse and rat CNS Life Sci 56 2343 2355
30. Jutkiewicz EM. Eller EB. Folk JE. Rice KC. Traynor JR. Woods JH. 2004 Delta-opioid agonists: differential efficacy and potency of SNC80 and its 3-OH (SNC86) and 3-desoxy (SNC162) derivatives in Sprague-Dawley rats JPharmacolExpTher 309 173 181
31. Kastin AJ. Scollan EL. Ehrensing RH. Schally AV. Coy DH. 1978 Enkephalin and other peptides reduce passiveness PharmacolBiochemBehav 9 515 519
32. Kline NS. Li CH. Lehmann HE. Lajtha A. Laski E. Cooper T. 1977 -Endorphin-induced changes in schizophrenic and depressed patients ArchGenPsychiatry 34 1111 1113
33. Ko MCH. Lee H. Harrison C. Clark MJ. Song HF. Naughton NN. Woods JH. Traynor JR. 2003 Studies of -, -, and -opioid receptor density and G protein activation in the cortex and thalamus of monkeys JPharmacolExpTher 306 179 186
34. Konig M. Zimmer AM. Steiner H. Holmes PV. Crawley JN. Brownstein MJ. Zimmer A. 1996 Pain responses, anxiety and aggression in mice deficient in pre-proenkephalin Nature 383 535 538
35. Le Foll B. Diaz J. Sokoloff P. 2005 A single cocaine exposure increases BDNF and D3 receptor expression: implications for drug-conditioning Neuroreport 16 175 178
36. Maher CE. Selley DE. Childers SR. 2000 Relationship of opioid receptor binding to activation of G-proteins in specific rat brain regions BiochemPharmacol 59 1395 1401
37. Malcangio M. Lessmann V. 2003 A common thread for pain and memory synapses? Brain-derived neurotrophic factor and trkB receptors Trends PharmacolSci 24 116 121
38. Mansour A. Khachaturian H. Lewis ME. Akil H. Watson SJ. 1988 Anatomy of CNS opioid receptors Trends Neurosci 11 308 314
39. Nibuya M. Morinobu S. Duman RS. 1995 Regulation of BDNF and trkB mRNA in rat brain by chronic electroconvulsive seizure and antidepressant drug treatments JNeurosci 15 7539 7547
40. Paxinos G. Watson C. 1986 The Rat Brain in Stereotaxic Coordinates, 2nd Edn. Academic Press San Diego
41. Porsolt RD. Pichon M. Jalfre M. 1977 Depression: a new animal model to antidepressant treatment Nature 266 730 732
42. Ragnauth A. Schuller A. Morgan M. Chan J. Ogawa S. Pintar J. Bodnar RJ. Pfaff DW. 2001 Female preproenkephalin-knockout mice display altered emotional response ProcNatlAcadSciUSA 98 1958 1963
43. Roques BP. 2000 Novel approaches to targeting neuropeptides system Trends PharmacolSci 21 475 483
44. Russo-Neustadt AA. Alejandre H. Garcia C. Ivy AS. Chen MJ. 2004 Hippocampal brain-derived neurotrophic factor expression following treatment with reboxetine, citalopram, and physical exercise Neuropsychopharmacology 29 2189 2199
45. Scarone S. Gambini O. Calabrese G. Sacerdote P. Bruni M. Carucci M. Panerai AE. 1990 Asymmetrical distribution of beta-endorphin in cerebral hemispheres of suicides: preliminary data Psychiatry Res 32 159 166
46. Shimizu E. Hashimoto K. Okamura N. Koike K. Komatsu N. Kumakiri C. Nakazato M. Watanabe H. Shinoda N. Okada S. Iyo M. 2003 Alterations of serum levels of brain-derived neurotrophic factor (BDNF) in depressed patients with or without antidepressants BiolPsychiatry 54 70 75
47. Shirayama Y. Chen AC. Nakagawa S. Russell DS. Duman RS. 2002 Brain-derived neurotrophic factor produces antidepressant effects in behavioral model of depression JNeurosci 22 3251 3261
48. Simon EJ. 1991 Opioid receptors and endogenous opioid peptides MedResRev 11 357 374
49. Siuciak JA. Lewis DR. Wiegand SJ. Lindsay RM. 1997 Antidepressant-like effect of brain-derived neurotrophic factor (BDNF) PharmacolBiochemBehav 56 131 137
50. Takemori AE. Ho BY. Naeseth JS. Portoghese PS. 1988 Nor-binaltorphimine, a highly selective kappa-opioid antagonist in analgesic and receptor binding assays JPharmacolExpTher 246 255 258
51. Tejedor-Real P. Mico JA. Maldonado R. Roques BP. Gibert-Rahola J. 1995 Implication of endogenous opioid system in the learned helplessness model of depression PharmacolBiochemBehav 52 145 152
52. Torregrossa MM. Isgor C. Folk JE. Rice KC. Watson SJ. Woods JH. 2004 The -opioid receptor agonist (+)BW373U86 regulates BDNF mRNA expression in rats Neuropsychopharmacology 29 649 659
53. Tseng LF. Wei ET. Loh HH. Li CH. 1980 -Endorphin: central sites of analgesia, catalepsy and body temperature changes in rats JPharmacolExpTher 214 328 332
54. Walker EA. Makhay MM. House ID. Young AM. 1994 In vivo apparent pA2 analysis for naltrexone antagonism of discriminative stimulus and analgesic effects of opiate agonists in rats JPharmacolExpTher 271 959 968
55. Zadina JE. Hackler L. Ge LJ. Kastin AJ. 1997 A potent and selective endogenous agonist for the -opiate receptor Nature 386 499 502
56. Zastawny RL. George SR. Nguyen T. Cheng R. Tsatsos J. Briones-Urbina R. O'Dowd BF. 1994 Cloning, characterization, and distribution of a mu-opioid receptor in rat brain JNeurochem 62 2099 2105