Nuclear factor κb signaling in opioid functions and receptor gene expression

Journal of Neuroimmune Pharmacology

Volumn 1, Issue 3, 2006, Pages 270-279

  Chen, Yulong L ^a   Law, Ping Yee ^a   Loh, Horace H ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

Akt; Gene expression; NF B; Opioid receptor; PI3K

Indexed keywords

IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; NARCOTIC ANALGESIC AGENT; OPIATE RECEPTOR;

ANIMAL; DRUG EFFECT; GENE EXPRESSION; HUMAN; METABOLISM; PHYSIOLOGY; REVIEW; SIGNAL TRANSDUCTION;

ANALGESICS, OPIOID; ANIMALS; GENE EXPRESSION; HUMANS; NF-KAPPA B; RECEPTORS, OPIOID; SIGNAL TRANSDUCTION;

EID: 33747356511     PISSN: 15571890     EISSN: 15571904     Source Type: Journal    
DOI: 10.1007/s11481-006-9028-0     Document Type: Conference Paper

References (119)

1. Ai W, Gong J, Yu L (1999) MAP kinase activation by mu opioid receptor involves phosphatidylinositol 3-kinase but not the cAMP/PKA pathway. FEBS Lett 456:196-200
2. Augustin LB, Felsheim RF, Min BH, Fuchs SM, Fuchs JA, Loh HH (1995) Genomic structure of the mouse delta opioid receptor gene. Biochem Biophys Res Commun 207:111-119
3. Azuma Y, Ohura K (2002) Endomorphins 1 and 2 inhibit IL-10 and IL-12 production and innate immune functions, and potentiate NF-kappaB DNA binding in THP-1 differentiated to macrophage-like cells. Scand J Immunol 56:260-269
4. Baeuerle PA, Baltimore D (1996) NF-kappa B: ten years after. Cell 87:13-20
5. 2+ accumulation. Proc Natl Acad Sci USA 92:9328-9332
6. Bohn LM, Gainetdinov RR, Lin FT, Lefkowitz RJ, Caron MG (2000) Mu-opioid receptor desensitization by beta-arrestin-2 determines morphine tolerance but not dependence. Nature 408:720-723
7. Borlongan CV, Wang Y, Su TP (2004) Delta opioid peptide (D-Ala 2, D-Leu 5) enkephalin: linking hibernation and neuroprotection. Front Biosci 9:3392-3398
8. Brunet A, Datta SR, Greenberg ME (2001) Transcription-dependent and -independent control of neuronal survival by the PI3K-Akt signaling pathway. Curr Opin Neurobiol 11:297-305
9. Capasso A (2001) Involvement of nuclear factor-κB in the expression of opiate withdrawal. Prog Neuro-psychopharmacol Biol Psychiatry 25:1259-1268
10. Carr DJ, Carpenter GW, Garza HH Jr, France CP, Prakash OM (1995) Chronic and infrequent opioid exposure suppresses IL-2R expression on rhesus monkey peripheral blood mononuclear cells following stimulation with pokeweed mitogen. Int J Neurosci 81:137-148
11. Carter BD, Kaltschmidt C, Kaltschmidt B, Offenhauser N, Bohm-Matthaei R, Baeuerle PA, Barde YA (1996) Selective activation of NF-kappa B by nerve growth factor through the neurotrophin receptor p75. Science 272:542-545
12. Chen LF, Greene WC (2004) Shaping the nuclear action of NF-kappaB. Nat Rev Mol Cell Biol 5:392-401
13. Chen Y, Mestek A, Liu J, Yu L (1993) Molecular cloning of a rat kappa opioid receptor reveals sequence similarities to the mu and delta opioid receptors. Biochem J 295(Pt 3):625-628
14. Chen YL, Law PY, Loh HH (2006) Sustained activation of phosphatidylinositol 3-kinase/akt/nuclear factor {kappa}B signaling mediates G protein-coupled {delta}-opioid receptor gene expression. J Biol Chem 281:3067-3074
15. Chuang LF, Killam KF Jr, Chuang RY (1997) Induction and activation of mitogen-activated protein kinases of human lymphocytes as one of the signaling pathways of the immunomodulatory effects of morphine sulfate. J Biol Chem 272:26815-26817
16. Colasanti M, Persichini T (2000) Nitric oxide: an inhibitor of NFkappaB/Rel system in glial cells. Brain Res Bull 52:155-161
17. Collier HO, Francis DL (1975) Morphine abstinence is associated with increased brain cyclic AMP. Nature 255:159-162
18. Conant K, Ma M, Nath A, Major EO (1996) Extracellular human immunodeficiency virus type 1 Tat protein is associated with an increase in both NF-kappa B binding and protein kinase C activity in primary human astrocytes. J Virol 70:1384-1389
19. Czlonkowski A, Stein C, Herz A (1993) Peripheral mechanisms of opioid antinociception in inflammation: involvement of cytokines. Eur J Pharmacol 242:229-235
20. DelaTorre A, Schroeder RA, Kuo PC (1997) Alteration of NF-kappa B p50 DNA binding kinetics by S-nitrosylation. Biochem Biophys Res Commun 238:703-706
21. Dixit V, Mak TW (2002) NF-kappaB signaling. Many roads lead to madrid. Cell 111:615-619
22. Evans CJ, Keith DE Jr, Morrison H, Magendzo K, Edwards RH (1992) Cloning of a delta opioid receptor by functional expression. Science 258:1952-1955
23. Fischer EG (1988) Opioid peptides modulate immune functions. A review. Immunopharmacol Immunotoxicol 10:265-326
24. Fukuda K, Kato S, Mori K, Nishi M, Takeshima H (1993) Primary structures and expression from cDNAs of rat opioid receptor delta- and mu-subtypes. FEBS Lett 327:311-314
25. Fukuda K, Kato S, Morikawa H, Shoda T, Mori K (1996) Functional coupling of the delta-, mu-, and kappa-opioid receptors to mitogen-activated protein kinase and arachidonate release in Chinese hamster ovary cells. J Neurochem 67:1309-1316
26. Gao H, Sun Y, Wu Y, Luan B, Wang Y, Qu B, Pei G (2004) Identification of beta-arrestin2 as a G protein-coupled receptor-stimulated regulator of NF-kappaB pathways. Mol Cell 14:303-317
27. Gaveriaux C, Peluso J, Simonin F, Laforet J, Kieffer B (1995) Identification of kappa- and delta-opioid receptor transcripts in immune cells. FEBS Lett 369:272-276
28. Gaveriaux-Ruff C, Matthes HW, Peluso J, Kieffer BL (1998) Abolition of morphine-immunosuppression in mice lacking the mu-opioid receptor gene. Proc Natl Acad Sci USA 95:6326-6330
29. Georges F, Normand E, Bloch B, Le Moine C (1998) Opioid receptor gene expression in the rat brain during ontogeny, with special reference to the mesostriatal system: an in situ hybridization study. Brain Res Dev Brain Res 109:187-199
30. Ghosh S, Karin M (2002) Missing pieces in the NF-kappaB puzzle. Cell 109(Suppl):S81-S96
31. Guerrini L, Blasi F, Denis-Donini S (1995) Synaptic activation of NF-kappa B by glutamate in cerebellar granule neurons in vitro. Proc Natl Acad Sci USA 92:9077-9081
32. Henry DJ, Grandy DK, Lester HA, Davidson N, Chavkin C (1995) Kappa-opioid receptors couple to inwardly rectifying potassium channels when coexpressed by Xenopus oocytes. Mol Pharmacol 47:551-557
33. Hirano F, Tanaka H, Hirano Y, Hiramoto M, Handa H, Makino I, Scheidereit C (1998) Functional interference of Sp1 and NF-kappaB through the same DNA binding site. Mol Cell Biol 18:1266-1274
34. Hou YN, Vlaskovska M, Cebers G, Kasakov L, Liljequist S, Terenius L (1996) A mu-receptor opioid agonist induces AP-1 and NFkappa B transcription factor activity in primary cultures of rat cortical neurons. Neurosci Lett 212:159-162
35. Kieffer BL, Gaveriaux-Ruff C (2002) Exploring the opioid system by gene knockout. Prog Neurobiol 66:285-306
36. Kieffer BL, Befort K, Gaveriaux-Ruff C, Hirth CG (1992) The delta-opioid receptor: isolation of a cDNA by expression cloning and pharmacological characterization. Proc Natl Acad Sci USA 89:12048-12052
37. Kraus J, Borner C, Giannini E, Hollt V (2003) The role of nuclear factor kappaB in tumor necrosis factor-regulated transcription of the human mu-opioid receptor gene. Mol Pharmacol 64:876-884
38. Law PY, Wong YH, Loh HH (2000) Molecular mechanisms and regulation of opioid receptor signaling. Annu Rev Pharmacol Toxicol 40:389-430
39. Law PY, Loh HH, Wei LN (2004) Insights into the receptor transcription and signaling: implications in opioid tolerance and dependence. Neuropharmacology 47(Suppl 1):300-311
40. Lawrence DM, el-Hamouly W, Archer S, Leary JF, Bidlack JM (1995) Identification of kappa opioid receptors in the immune system by indirect immunofluorescence. Proc Natl Acad Sci USA 92:1062-1066
41. Lezoualc'h F, Sagara Y, Holsboer F, Behl C (1998) High constitutive NF-kappaB activity mediates resistance to oxidative stress in neuronal cells. J Neurosci 18:3224-3232
42. Li LY, Chang KJ (1996) The stimulatory effect of opioids on mitogen-activated protein kinase in Chinese hamster ovary cells transfected to express mu-opioid receptors. Mol Pharmacol 50:599-602
43. Li Q, Verma IM (2002) NF-kappaB regulation in the immune system. Nat Rev Immunol 2:725-734
44. Li S, Zhu J, Chen C, Chen YW, Deriel JK, Ashby B, Liu-Chen LY (1993) Molecular cloning and expression of a rat kappa opioid receptor. Biochem J 295(Pt 3):629-633
45. Li MD, McAllen K, Sharp BM (1999) Regulation of delta opioid receptor expression by anti-CD3-epsilon, PMA, and ionomycin in murine splenocytes and T cells. J Leukoc Biol 65:707-714
46. Li Y, Zhang T, Douglas SD, Lai JP, Xiao WD, Pleasure DE, Ho WZ (2003) Morphine enhances hepatitis C virus (HCV) replicon expression. Am J Pathol 163:1167-1175
47. Lieb K, Fiebich BL, Berger M, Bauer J, Schulze-Osthoff K (1997) The neuropeptide substance P activates transcription factor NF-kappa B and kappa B-dependent gene expression in human astrocytoma cells. J Immunol 159:4952-4958
48. Magazine HI, Liu Y, Bilfinger TV, Fricchione GL, Stefano GB (1996) Morphine-induced conformational changes in human monocytes, granulocytes, and endothelial cells and in invertebrate immunocytes and microglia are mediated by nitric oxide. J Immunol 156:4845-4850
49. Maggirwar SB, Sarmiere PD, Dewhurst S, Freeman RS (1998) Nerve growth factor-dependent activation of NF-kappaB contributes to survival of sympathetic neurons. J Neurosci 18:10356-10365
50. Marshall HE, Hess DT, Stamler JS (2004) S-Nitrosylation: physiological regulation of NF-kappaB. Proc Natl Acad Sci USA 101:8841-8842
51. Matthews JR, Botting CH, Panico M, Morris HR, Hay RT (1996) Inhibition of NF-kappaB DNA binding by nitric oxide. Nucleic Acids Res 24:2236-2242
52. Mattson MP (2003) Insulating axons via NF-kappaB. Nat Neurosci 6:105-106
53. McCarthy L, Wetzel M, Sliker JK, Eisenstein TK, Rogers TJ (2001) Opioids, opioid receptors, and the immune response. Drug Alcohol Depend 62:111-123
54. Meffert MK, Baltimore D (2005) Physiological functions for brain NF-kappaB. Trends Neurosci 28:37-43
55. Meffert MK, Chang JM, Wiltgen BJ, Fanselow MS, Baltimore D (2003) NF-kappa B functions in synaptic signaling and behavior. Nat Neurosci 6:1072-1078
56. Meng F, Xie GX, Thompson RC, Mansour A, Goldstein A, Watson SJ, Akil H (1993) Cloning and pharmacological characterization of a rat kappa opioid receptor. Proc Natl Acad Sci USA 90:9954-9958
57. Middleton G, Wyatt S, Ninkina N, Davies AM (2001) Reciprocal developmental changes in the roles of Bcl-w and Bcl-x(L) in regulating sensory neuron survival. Development 128:447-457
58. Miyamae T, Fukushima N, Misu Y, Ueda H (1993) Delta opioid receptor mediates phospholipase C activation via Gi in Xenopus oocytes. FEBS Lett 333:311-314
59. Murphy TJ (2003) Simple nuclear factor kappaB-mediated mu-opioid receptor induction in immune cells. Mol Pharmacol 64:796-797
60. Natarajan K, Singh S, Burke TR Jr, Grunberger D, Aggarwal BB (1996) Caffeic acid phenethyl ester is a potent and specific inhibitor of activation of nuclear transcription factor NF-kappa B. Proc Natl Acad Sci USA 93:9090-9095
61. Nestler EJ (1992) Molecular mechanisms of drug addiction. J Neurosci 12:2439-2450
62. Nestler EJ (1997) Molecular mechanisms of opiate and cocaine addiction. Curr Opin Neurobiol 7:713-719
63. Nestler EJ (2004) Historical review: molecular and cellular mechanisms of opiate and cocaine addiction. Trends Pharmacol Sci 25:210-218
64. Nickols JC, Valentine W, Kanwal S, Carter BD (2003) Activation of the transcription factor NF-kappaB in Schwann cells is required for peripheral myelin formation. Nat Neurosci 6:161-167
65. O'Neill LA, Kaltschmidt C (1997) NF-kappa B: a crucial transcription factor for glial and neuronal cell function. Trends Neurosci 20:252-258
66. Ozawa T, Nakagawa T, Minami M, Satoh M (1999) Supersensitization of the adenylyl cyclase system in Chinese hamster ovary cells coexpressing cloned opioid receptors and Gz, a PTX-insensitive G protein. Neurosci Lett 267:117-120
67. Park SW, Wei LN (2003) Regulation of c-myc gene by nitric oxide via inactivating NF-kappa B complex in P19 mouse embryonal carcinoma cells. J Biol Chem 278:29776-29782
68. Park SW, Li J, Loh HH, Wei LN (2002) A novel signaling pathway of nitric oxide on transcriptional regulation of mouse kappa opioid receptor gene. J Neurosci 22:7941-7947
69. Park SW, Huq MD, Hu X, Wei LN (2005) Tyrosine nitration on p65: a novel mechanism to rapidly inactivate nuclear factor-kappaB. Mol Cell Proteomics 4:300-309
70. Parry GC, Mackman N (1997) Role of cyclic AMP response element-binding protein in cyclic AMP inhibition of NF-kappaB-mediated transcription. J Immunol 159:5450-5456
71. Philippe D, Chakass D, Thuru X, Zerbib P, Tsicopoulos A, Geboes K, Bulois P, Breisse M, Vorng H, Gay J, Colombel JF, Desreumaux P, Chamaillard M (2006) Mu opioid receptor expression is increased in inflammatory bowel diseases: implications for homeostatic intestinal inflammation. Gut 55:815-823
72. 2+ channel and adenylyl cyclase modulation by cloned mu-opioid receptors in GH3 cells. Mol Pharmacol 47:1041-1049
73. Pol O, Alameda F, Puig MM (2001) Inflammation enhances mu-opioid receptor transcription and expression in mice intestine. Mol Pharmacol 60:894-899
74. Polakiewicz RD, Schieferl SM, Dorner LF, Kansra V, Comb MJ (1998a) A mitogen-activated protein kinase pathway is required for mu-opioid receptor desensitization. J Biol Chem 273:12402-12406
75. Polakiewicz RD, Schieferl SM, Gingras AC, Sonenberg N, Comb MJ (1998b) mu-Opioid receptor activates signaling pathways implicated in cell survival and translational control. J Biol Chem 273:23534-23541
76. Pomerantz JL, Baltimore D (2002) Two pathways to NF-kappaB. Mol Cell 10:693-695
77. Prather PL, Loh HH, Law PY (1994) Interaction of delta-opioid receptors with multiple G proteins: a non-relationship between agonist potency to inhibit adenylyl cyclase and to activate G proteins. Mol Pharmacol 45:997-1003
78. Rogers TJ, Peterson PK (2003) Opioid G protein-coupled receptors: signals at the crossroads of inflammation. Trends Immunol 24:116-121
79. Rojo AI, Salinas M, Martin D, Perona R, Cuadrado A (2004) Regulation of Cu/Zn-superoxide dismutase expression via the phosphatidylinositol 3 kinase/Akt pathway and nuclear factor-kappaB. J Neurosci 24:7324-7334
80. Roy S, Barke RA, Loh HH (1998a) Mu-opioid receptor-knockout mice: role of mu-opioid receptor in morphine mediated immune functions. Brain Res Mol Brain Res 61:190-194
81. Roy S, Cain KJ, Chapin RB, Charboneau RG, Barke RA (1998b) Morphine modulates NF kappa B activation in macrophages. Biochem Biophys Res Commun 245:392-396
82. Rozenfeld-Granot G, Toren A, Amariglio N, Nagler A, Rosenthal E, Biniaminov M, Brok-Simoni F, Rechavi G (2002) MAP kinase activation by mu opioid receptor in cord blood CD34(+)CD38(-) cells. Exp Hematol 30:473-480
83. Salzet M, Vieau D, Day R (2000) Crosstalk between nervous and immune systems through the animal kingdom: focus on opioids. Trends Neurosci 23:550-555
84. Schmitz R (1985) Friedrich Wilhelm Serturner and the discovery of morphine. Pharm Hist 27:61-74
85. Shahabi NA, McAllen K, Matta SG, Sharp BM (2000) Expression of delta opioid receptors by splenocytes from SEB-treated mice and effects on phosphorylation of MAP kinase. Cell Immunol 205:84-93
86. Sharma SK, Klee WA, Nirenberg M (1975) Dual regulation of adenylate cyclase accounts for narcotic dependence and tolerance. Proc Natl Acad Sci USA 72:3092-3096
87. Sharp BM (2003) Opioid receptor expression and intracellular signaling by cells involved in host defense and immunity. Adv Exp Med Biol 521:98-105
88. Sheng WS, Hu S, Lokensgard JR, Peterson PK (2003) U50,488 inhibits HIV-1 Tat-induced monocyte chemoattractant protein-1 (CCL2) production by human astrocytes. Biochem Pharmacol 65:9-14
89. Sibinga NE, Goldstein A (1988) Opioid peptides and opioid receptors in cells of the immune system. Annu Rev Immunol 6:219-249
90. i and adenylyl cyclase. Br J Pharmacol 120:1165-1171
91. Sofroniew MV, Howe CL, Mobley WC (2001) Nerve growth factor signaling, neuroprotection, and neural repair. Annu Rev Neurosci 24:1217-1281
92. Standifer KM, Pasternak GW (1997) G proteins and opioid receptor-mediated signalling. Cell Signal 9:237-248
93. Stefano GB, Hartman A, Bilfinger TV, Magazine HI, Liu Y, Casares F, Goligorsky MS (1995) Presence of the mu3 opiate receptor in endothelial cells. Coupling to nitric oxide production and vasodilation. J Biol Chem 270:30290-30293
94. Stein C, Hassan AH, Przewlocki R, Gramsch C, Peter K, Herz A (1990) Opioids from immunocytes interact with receptors on sensory nerves to inhibit nociception in inflammation. Proc Natl Acad Sci USA 87:5935-5939
95. Sun P, Loh HH (2002) Transcriptional regulation of mouse delta-opioid receptor gene. Role of Ikaros in the stimulated transcription of mouse delta-opioid receptor gene in activated T cells. J Biol Chem 277:12854-12860
96. Suzuki S, Chuang TK, Chuang LF, Doi RH, Chuang RY (2001) Morphine upregulates kappa-opioid receptors of human lymphocytes. Adv Exp Med Biol 493:81-87
97. Tallent M, Dichter MA, Bell GI, Reisine T (1994) The cloned kappa opioid receptor couples to an N-type calcium current in undifferentiated PC-12 cells. Neuroscience 63:1033-1040
98. Taylor DA, Fleming WW (2001) Unifying perspectives of the mechanisms underlying the development of tolerance and physical dependence to opioids. J Pharmacol Exp Ther 297:11-18
99. Viatour P, Merville MP, Bours V, Chariot A (2005) Phosphorylation of NF-kappaB and IkappaB proteins: implications in cancer and inflammation. Trends Biochem Sci 30:43-52
100. Walker JS (2003) Anti-inflammatory effects of opioids. Adv Exp Med Biol 521:148-160
101. Wang J, Barke RA, Charboneau R, Loh HH, Roy S (2003) Morphine negatively regulates interferon-gamma promoter activity in activated murine T cells through two distinct cyclic AMP-dependent pathways. J Biol Chem 278:37622-37631
102. Wang X, Douglas SD, Commons KG, Pleasure DE, Lai J, Ho C, Bannerman P, Williams M, Ho W (2004) A non-peptide substance P antagonist (CP-96,345) inhibits morphine-induced NF-kappa B promoter activation in human NT2-N neurons. J Neurosci Res 75:544-553
103. + channel and NFkappaB activity in corneal epithelial cells. Exp Cell Res 311:39-48
104. Welters ID, Fimiani C, Bilfinger TV, Stefano GB (2000a) NF-kappaB, nitric oxide and opiate signaling. Med Hypotheses 54:263-268
105. Welters ID, Menzebach A, Goumon Y, Cadet P, Menges T, Hughes TK, Hempelmann G, StefanoGB (2000b)Morphine inhibits NF-kappaB nuclear binding in human neutrophils and monocytes by a nitric oxide-dependent mechanism. Anesthesiology 92:1677-1684
106. Williams JT, Christie MJ, Manzoni O (2001) Cellular and synaptic adaptations mediating opioid dependence. Physiol Rev 81:299-343
107. Wong YH, Federman A, Pace AM, Zachary I, Evans T, Pouyssegur J, Bourne HR (1991) Mutant alpha subunits of Gi2 inhibit cyclic AMP accumulation. Nature 351:63-65
108. Wooten MW, Vandenplas ML, Seibenhener ML, Geetha T, Diaz-Meco MT (2001) Nerve growth factor stimulates multisite tyrosine phosphorylation and activation of the atypical protein kinase C's via a src kinase pathway. Mol Cell Biol 21:8414-8427
109. Yang J, Lin Y, Guo Z, Cheng J, Huang J, Deng L, Liao W, Chen Z, Liu Z, Su B (2001) The essential role of MEKK3 in TNF-induced NF-kappaB activation. Nat Immunol 2:620-624
110. Yasuda K, Raynor K, Kong H, Breder CD, Takeda J, Reisine T, Bell GI (1993) Cloning and functional comparison of kappa and delta opioid receptors from mouse brain. Proc Natl Acad Sci USA 90:6736-6740
111. Ye RD (2001) Regulation of nuclear factor kappaB activation by G-protein-coupled receptors. J Leukoc Biol 70:839-848
112. Yeh SH, Lin CH, Lee CF, Gean PW (2002) A requirement of nuclear factor-kappaB activation in fear-potentiated startle. J Biol Chem 277:46720-46729
113. Yeiser EC, Rutkoski NJ, Naito A, Inoue J, Carter BD (2004) Neurotrophin signaling through the p75 receptor is deficient in traf6-/- mice. J Neurosci 24:10521-10529
114. Yuan J, Yankner BA (2000) Apoptosis in the nervous system. Nature 407:802-809
115. Zadina JE, Hackler L, Ge LJ, Kastin AJ (1997) A potent and selective endogenous agonist for themu-opiate receptor. Nature 386:499-502
116. Zhang N, Oppenheim JJ (2005) Crosstalk between chemokines and neuronal receptors bridges immune and nervous systems. J Leukoc Biol 78:1210-1214
117. Zhang T, Li Y, Lai JP, Douglas SD, Metzger DS, O'Brien CP, Ho WZ (2003) Alcohol potentiates hepatitis C virus replicon expression. Hepatology 38:57-65
118. Zhong H, May MJ, Jimi E, Ghosh S (2002) The phosphorylation status of nuclear NF-kappa B determines its association with CBP/p300 or HDAC-1. Mol Cell 9:625-636
119. Zhu Y, Hsu MS, Pintar JE (1998) Developmental expression of the mu, kappa, and delta opioid receptor mRNAs in mouse. J Neurosci 18:2538-2549