Evidence that opioids may have toll-like receptor 4 and MD-2 effects

Brain, Behavior, and Immunity

Volumn 24, Issue 1, 2010, Pages 83-95

  Hutchinson, Mark R ^a,b   Zhang, Yingning ^a   Shridhar, Mitesh ^a   Evans, John H ^a   Buchanan, Madison M ^a   Zhao, Tina X ^a   Slivka, Peter F ^a   Coats, Benjamen D ^a   Rezvani, Niloofar ^a   Wieseler, Julie ^a   Hughes, Travis S ^a   Landgraf, Kyle E ^a   Chan, Stefanie ^b   Fong, Stephanie ^b   Phipps, Simon ^c   Falke, Joseph J ^a   Leinwand, Leslie A ^c   Maier, Steven F ^a   Yin, Hang ^a   Rice, Kenner C ^d   Watkins, Linda R ^a   more..

^a UNIVERSITY OF COLORADO   (United States)

^b UNIVERSITY OF ADELAIDE   (Australia)

^c UNIVERSITY OF NEWCASTLE   (Australia)

^d NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

Author keywords

Analgesia; Dependence; Glia; Knockout; Microglia; Opioid; Toll like receptor 4

Indexed keywords

BUPRENORPHINE; DEXTRORPHAN; FENTANYL; LEVORPHANOL; METHADONE; MORPHINE; MORPHINE 3 GLUCURONIDE; NALMEFENE; NALOXONE; NARCOTIC ANALGESIC AGENT; OPIATE RECEPTOR; OXYCODONE; PETHIDINE; PROTEIN MD 2; TOLL LIKE RECEPTOR 4;

ADULT ANIMAL; ANALGESIA; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CELL LINE; CELL STRAIN HEK293; COMPUTER MODEL; CONTROLLED STUDY; DRUG MECHANISM; DRUG TOLERANCE; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; HYPERALGESIA; IN VITRO STUDY; IN VIVO STUDY; MACROPHAGE; MALE; NONHUMAN; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; SIGNAL TRANSDUCTION; SIMULATION;

ANALGESIA; ANALGESICS, OPIOID; ANIMALS; CELL LINE; COMPUTER SIMULATION; HOT TEMPERATURE; HYPERALGESIA; INFUSION PUMPS; INJECTIONS, SPINAL; LYMPHOCYTE ANTIGEN 96; MACROPHAGES; MALE; MICE; NALOXONE; NARCOTIC ANTAGONISTS; PAIN MEASUREMENT; RATS; RATS, SPRAGUE-DAWLEY; REACTION TIME; RECEPTORS, OPIOID, MU; SIGNAL TRANSDUCTION; SUBSTANCE WITHDRAWAL SYNDROME; TOLL-LIKE RECEPTOR 4; TRANSFECTION;

EID: 71749111875     PISSN: 08891591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbi.2009.08.004     Document Type: Article

References (54)

1. Chao C.C., Gekker G., Sheng W.S., Hu S., Tsang M., and Peterson P.K. Priming effect of morphine on the production of tumor necrosis factor-alpha by microglia: implications in respiratory burst activity and human immunodeficiency virus-1 expression. J. Pharmacol. Exp. Ther. 269 (1994) 198-203
2. Chen Z.R., Irvine R.J., Bochner A.A., and Somogyi F. Mu receptor binding of some commonly used opioids and their metabolites. Life Sci. 48 (1991) 2165-2171
3. Cui Y., Chen Y., Zhi J.L., Guo R.X., Feng J.Q., and Chen P.X. Activation of p38 mitogen-activated protein kinase in spinal microglia mediates morphine antinociceptive tolerance. Brain Res. 1069 (2006) 235-243
4. Cui Y., Liao X.X., Liu W., Guo R.X., Wu Z.Z., Zhao C.M., Chen P.X., and Feng J.Q. A novel role of minocycline: attenuating morphine antinociceptive tolerance by inhibition of p38 MAPK in the activated spinal microglia. Brain Behav. Immun. 22 (2008) 114-123
5. Cuschieri J., Bulger E., Billgrin J., Garcia I., and Maier R.V. Acid sphingomyelinase is required for lipid Raft TLR4 complex formation. Surg. Infect. 8 (2007) 91-106
6. Dauphinee S.M., and Karsan A. Lipopolysaccharide signaling in endothelial cells. Lab. Invest. 86 (2006) 9-22
7. Dobrenis K., Makman M.H., and Stefano G.B. Occurrence of the opiate alkaloid-selective mu3 receptor in mammalian microglia, astrocytes and Kupffer cells. Brain Res. 686 (1995) 239-248
8. Dziarski R., Wang Q., Miyake K., Kirschning C.J., and Gupta D. MD-2 enables Toll-like receptor 2 (TLR2)-mediated responses to lipopolysaccharide and enhances TLR2-mediated responses to Gram-positive and Gram-negative bacteria and their cell wall components. J. Immunol. 166 (2001) 1938-1944
9. El-Hage N., Gurwell J.A., Singh I.N., Knapp P.E., Nath A., and Hauser K.F. Synergistic increases in intracellular Ca2+, and the release of MCP-1, RANTES, and IL-6 by astrocytes treated with opiates and HIV-1 Tat. Glia 50 (2005) 91-106
10. Evans J.H., and Falke J.J. Ca2+ influx is an essential component of the positive-feedback loop that maintains leading-edge structure and activity in macrophages. Proc. Natl. Acad. Sci. USA 104 (2007) 16176-16181
11. Gaveriaux-Ruff C., Filliol D., Simonin F., Matthes H.W., and Kieffer B.L. Immunosuppression by delta-opioid antagonist naltrindole: delta- and triple mu/delta/kappa-opioid receptor knockout mice reveal a nonopioid activity. J. Pharmacol. Exp. Ther. 298 (2001) 1193-1198
12. Gaveriaux-Ruff C., Matthes H.W., Peluso J., and Kieffer B.L. Abolition of morphine-immunosuppression in mice lacking the mu-opioid receptor gene. Proc. Natl. Acad. Sci. USA 95 (1998) 6326-6330
13. Greeneltch K.M., Haudenschild C.C., Keegan A.D., and Shi Y. The opioid antagonist naltrexone blocks acute endotoxic shock by inhibiting tumor necrosis factor-alpha production. Brain Behav. Immun. 18 (2004) 476-484
14. Gupta K., Kshirsagar S., Chang L., Schwartz R., Law P.Y., Yee D., and Hebbel R.P. Morphine stimulates angiogenesis by activating proangiogenic and survival-promoting signaling and promotes breast tumor growth. Cancer Res. 62 (2002) 4491-4498
15. Hargreaves K., Dubner R., Brown F., Flores C., and Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32 (1988) 77-88
16. Horvath R.J., and DeLeo J.A. Morphine enhances microglial migration through modulation of P2X4 receptor signaling. J. Neurosci. 29 (2009) 998-1005
17. Hoshino K., Takeuchi O., Kawai T., Sanjo H., Ogawa T., Takeda Y., Takeda K., and Akira S. Cutting edge: toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J. Immunol. 162 (1999) 3749-3752
18. Hutchinson M.R., Bland S.T., Johnson K.W., Rice K.C., Maier S.F., and Watkins L.R. Opioid-induced glial activation: mechanisms of activation and implications for opioid analgesia, dependence and reward. TheScientificWorldJournal 7 (2007) 98-111
19. Hutchinson M.R., Coats B.D., Lewis S.S., Zhang Y., Sprunger D.B., Rezvani N., Baker E.M., Jekich B.M., Wieseler J.L., Somogyi A.A., Martin D., Poole S., Judd C.M., Maier S.F., and Watkins L.R. Proinflammatory cytokines oppose opioid-induced acute and chronic analgesia. Brain Behav. Immun. 22 (2008) 1178-1189
20. Hutchinson M.R., Lewis S.S., Coats B.D., Skyba D.A., Crysdale N.Y., Berkelhammer D.L., Brzeski A., Northcutt A., Vietz C.M., Judd C.M., Maier S.F., Watkins L.R., and Johnson K.W. Reduction of opioid withdrawal and potentiation of acute opioid analgesia by systemic AV411 (ibudilast). Brain Behav. Immun. 23 (2009) 240-250
21. Hutchinson M.R., Northcutt A.L., Chao L.W., Kearney J.J., Zhang Y., Berkelhammer D.L., Loram L.C., Rozeske R.R., Bland S.T., Maier S.F., Gleeson T.T., and Watkins L.R. Minocycline suppresses morphine-induced respiratory depression, suppresses morphine-induced reward, and enhances systemic morphine-induced analgesia. Brain Behav. Immun. 22 (2008) 1248-1256
22. Hutchinson M.R., Zhang Y., Brown K., Coats B.D., Shridhar M., Sholar P.W., Patel S.J., Crysdale N.Y., Harrison J.A., Maier S.F., Rice K.C., and Watkins L.R. Non-stereoselective reversal of neuropathic pain by naloxone and naltrexone: involvement of toll-like receptor 4 (TLR4). Eur. J. Neurosci. 28 (2008) 20-29
23. Hwang C.K., Kim C.S., Choi H.S., McKercher S.R., and Loh H.H. Transcriptional regulation of mouse mu opioid receptor gene by PU.1. J. Biol. Chem. 279 (2004) 19764-19774
24. Johnston I.N., Milligan E.D., Wieseler-Frank J., Frank M.G., Zapata V., Campisi J., Langer S., Martin D., Green P., Fleshner M., Leinwand L., Maier S.F., and Watkins L.R. A role for proinflammatory cytokines and fractalkine in analgesia, tolerance, and subsequent pain facilitation induced by chronic intrathecal morphine. J. Neurosci. 24 (2004) 7353-7365
25. Juni A., Klein G., Pintar J.E., and Kest B. Nociception increases during opioid infusion in opioid receptor triple knock-out mice. Neuroscience 147 (2007) 439-444
26. Laird, M.H., Rhee, S.H., Perkins, D.J., Medvedev, A.E., Piao, W., Fenton, M.J., Vogel, S.N., 2009. TLR4/MyD88/PI3K interactions regulate TLR4 signaling. J. Leukoc. Biol.
27. Li Y., Sun X., Zhang Y., Huang J., Hanley G., Ferslew K.E., Peng Y., and Yin D. Morphine promotes apoptosis via TLR2, and this is negatively regulated by beta-arrestin 2. Biochem. Biophys. Res. Commun. 378 (2009) 857-861
28. Liang D.Y., Guo T., Liao G., Kingery W.S., Peltz G., and Clark J.D. Chronic pain and genetic background interact and influence opioid analgesia, tolerance, and physical dependence. Pain 121 (2006) 232-240
29. Lipovsky M.M., Gekker G., Hu S., Peterson A.I., and Hoepelman P.K. Morphine enhances complement receptor-mediated phagocytosis of Cryptococcus neoformans by human microglia. Clin. Immunol. Immunopathol. 87 (1998) 163-167
30. Liu B., Du L., and Hong J.S. Naloxone protects rat dopaminergic neurons against inflammatory damage through inhibition of microglia activation and superoxide generation. J. Pharmacol. Exp. Ther. 293 (2000) 607-617
31. Liu S.L., Li Y.H., Shi G.Y., Chen Y.H., Huang C.W., Hong J.S., and Wu H.L. A novel inhibitory effect of naloxone on macrophage activation and atherosclerosis formation in mice. J. Am. Coll. Cardiol. 48 (2006) 1871-1879
32. Narita M., Imai S., Kasukawa A., Yajima Y., and Suzuki T. Increased level of neuronal phosphoinositide 3-kinase gamma by the activation of mu-opioid receptor in the mouse periaqueductal gray matter: further evidence for the implication in morphine-induced antinociception. Neuroscience 124 (2004) 515-521
33. Narita M., Miyatake M., Narita M., Shibasaski M., Shindo K., Nakamura A., Kuzumaki N., Nagumo Y., and Suzuki T. Direct evidence of astrocytic modulation in the development of rewarding effects induced by drugs of abuse. Neuropsychopharmacology 31 (2006) 2476-2488
34. Ojaniemi M., Glumoff V., Harju K., Liljeroos M., Vuori K., and Hallman M. Phosphatidylinositol 3-kinase is involved in Toll-like receptor 4-mediated cytokine expression in mouse macrophages. Eur. J. Immunol. 33 (2003) 597-605
35. Okun E., Griffioen K., Lathia J., Tang S., Mattson M., and Arumugam T. Toll-like receptors in neurodegeneration. Brain Res. Rev. 59 (2008) 278-292
36. Ossipov M.H., Lai J., King T., Vanderah T.W., and Porreca F. Underlying mechanisms of pronociceptive consequences of prolonged morphine exposure. Biopolymers 80 (2005) 319-324
37. Park B.S., Song D.H., Kim H.M., Choi B.S., Lee H., and Lee J.O. The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex. Nature 458 (2009) 1191-1195
38. Peterson P.K., Molitor T.W., and Chao C.C. The opioid-cytokine connection. J. Neuroimmunol. 83 (1998) 63-69
39. Polakiewicz R.D., Schieferl S.M., Gingras A.C., Comb N., and Sonenberg M.J. mu-Opioid receptor activates signaling pathways implicated in cell survival and translational control. J. Biol. Chem. 273 (1998) 23534-23541
40. Rady J.J., and Fujimoto J.M. Confluence of antianalgesic action of diverse agents through brain interleukin(1beta) in mice. J. Pharmacol. Exp. Ther. 299 (2001) 659-665
41. Raghavendra V., Rutkowski M.D., and DeLeo J.A. The role of spinal neuroimmune activation in morphine tolerance/hyperalgesia in neuropathic and sham-operated rats. J. Neurosci. 22 (2002) 9980-9989
42. Raghavendra V., Tanga F.Y., and DeLeo J.A. Attenuation of morphine tolerance, withdrawal-induced hyperalgesia, and associated spinal inflammatory immune responses by propentofylline in rats. Neuropsychopharmacology 29 (2004) 327-334
43. Ruzicka B.B., and Akil H. The interleukin-1beta-mediated regulation of proenkephalin and opioid receptor messenger RNA in primary astrocyte-enriched cultures. Neuroscience 79 (1997) 517-524
44. Schilling D., Thomas K., Nixdorff K., Vogel S.N., and Fenton M.J. Toll-like receptor 4 and Toll-IL-1 receptor domain-containing adapter protein (TIRAP)/myeloid differentiation protein 88 adapter-like (Mal) contribute to maximal IL-6 expression in macrophages. J. Immunol. 169 (2002) 5874-5880
45. Shavit Y., Wolf G., Goshen I., Livshits D., and Yirmiya R. Interleukin-1 antagonizes morphine analgesia and underlies morphine tolerance. Pain 115 (2005) 50-59
46. Song P., and Zhao Z.Q. The involvement of glial cells in the development of morphine tolerance. Neurosci. Res. 39 (2001) 281-286
47. Stefano G.B. Autoimmunovascular regulation: morphine and anandamide and ancodamide stimulated nitric oxide release. J. Neuroimmunol. 83 (1998) 70-76
48. Takayama N., and Ueda H. Morphine-induced chemotaxis and brain-derived neurotrophic factor expression in microglia. J. Neurosci. 25 (2005) 430-435
49. Wang J., Barke R.A., Charboneau R., Schwendener R., and Roy S. Morphine induces defects in early response of alveolar macrophages to Streptococcus pneumoniae by modulating TLR9-NF-kappa B signaling. J. Immunol. 180 (2008) 3594-3600
50. Watkins L.R., Hutchinson M.R., Johnston I.N., and Maier S.F. Glia: novel counter-regulators of opioid analgesia. Trends Neurosci. 28 (2005) 661-669
51. Wu H.E., Hong J.S., and Tseng L.F. Stereoselective action of (+)-morphine over (-)-morphine in attenuating the (-)-morphine-produced antinociception via the naloxone-sensitive sigma receptor in the mouse. Eur. J. Pharmacol. 571 (2007) 145-151
52. Wu H.E., Sun H.S., Cheng C.W., Terashvili M., and Tseng L.F. Dextro-Naloxone or levo-naloxone reverses the attenuation of morphine antinociception induced by lipopolysaccharide in the mouse spinal cord via a non-opioid mechanism. Eur. J. Neurosci. 24 (2006) 2575-2580
53. Wu H.E., Sun H.S., Terashivili M., Schwasinger E., Sora I., Hall F.S., Uhl G.R., and Tseng L.F. Dextro- and levo-morphine atten0uate opioid delta and kappa receptor agonist produced analgesia in mu-opioid receptor knockout mice. Eur. J. Pharmacol. 531 (2006) 103-107
54. Wu H.E., Thompson J., Sun H.S., Terashvili M., and Tseng L.F. Antianalgesia: stereoselective action of dextro-morphine over levo-morphine on glia in the mouse spinal cord. J. Pharmacol. Exp. Ther. 314 (2005) 1101-1108