Correction: Toll-like receptor 4 mutant and null mice retain morphine-induced tolerance, hyperalgesia, and physical dependence (PLoS ONE (2014) 9, 5 (e97361) DOI: 10.1371/journal.pone.0097361);Toll-like receptor 4 mutant and null mice retain morphine-induced tolerance, hyperalgesia, and physical dependence

PLoS ONE

Volumn 9, Issue 5, 2014, Pages

  Mattioli, Theresa Alexandra ^a   Leduc Pessah, Heather ^b   Skelhorne Gross, Graham ^a,c   Nicol, Chris J B ^a,c   Milne, Brian ^a   Trang, Tuan ^b   Cahill, Catherine M ^a,d  

^a QUEEN S UNIVERSITY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c QUEEN S UNIVERSITY   (Canada)

^d UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MORPHINE SULFATE; NALOXONE; PROTEIN C FOS; TOLL LIKE RECEPTOR 4; MORPHINE; NARCOTIC ANTAGONIST; PRIMER DNA;

ADULT; ANALGESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINOCICEPTION; ARTICLE; BEHAVIORAL SCIENCE; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; ENANTIOMER; GENOTYPE; GLIOSIS; HYPERALGESIA; KNOCKOUT MOUSE; MALE; MORPHINE ADDICTION; MORPHINE TOLERANCE; MOUSE; MOUSE MUTANT; NONHUMAN; PAIN; POINT MUTATION; TLR4 GENE; WILD TYPE; WITHDRAWAL REFLEX; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMICALLY INDUCED; DRUG TOLERANCE; GENETICS; IMMUNOHISTOCHEMISTRY; INBRED MOUSE STRAIN; MORPHINE DEPENDENCE; PATHOPHYSIOLOGY; PHYSIOLOGY; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; DNA PRIMERS; DRUG TOLERANCE; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED STRAINS; MORPHINE; MORPHINE DEPENDENCE; NALOXONE; NARCOTIC ANTAGONISTS; POINT MUTATION; REAL-TIME POLYMERASE CHAIN REACTION; TOLL-LIKE RECEPTOR 4;

EID: 84901287696     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0101621     Document Type: Erratum

References (55)

1. Koski G, Klee WA (1981) Opiates inhibit adenylate cyclase by stimulating GTP hydrolysis. Proc Natl Acad Sci USA 78(7): 4185-4189. (Pubitemid 11010303)
2. Matthes HW, Maldonado R, Simonin F, Valverde O, Slowe S, et al. (1996) Loss of morphine-induced analgesia, reward effect and withdrawal symptoms in mice lacking the mu-opioid-receptor gene. Nature 383: 819-823. doi:10.1038/383819a0.
3. Cheng PY, Liu-Chen LY, Pickel VM (1997) Dual ultrastructural immunocytochemical labeling of mu and delta opioid receptors in the superficial layers of the rat cervical spinal cord. Brain Res 778: 367-380. (Pubitemid 28037417)
4. Dobrenis K, Makman MH, Stefano GB (1995) Occurrence of the opiate alkaloid-selective mu3 receptor in mammalian microglia, astrocytes and Kupffer cells. Brain Res 686: 239-248.
5. Eriksson PS, Hansson E, Rönnbäck L (1990) Delta and kappa opiate receptors in primary astroglial cultures from rat cerebral cortex. Neurochem Res 15: 1123-1126.
6. Eriksson PS, Hansson E, Rönnbäck L (1991) Mu and delta opiate receptors in neuronal and astroglial primary cultures from various regions of the brain-coupling with adenylate cyclase, localisation on the same neurones and association with dopamine (D1) receptor adenylate cyclase. Neuropharmacology 30: 1233-1239.
7. Ruzicka BB, Fox CA, Thompson RC, Meng F, Watson SJ, et al. (1995) Primary astroglial cultures derived from several rat brain regions differentially express mu, delta and kappa opioid receptor mRNA. Brain Res Mol Brain Res 34: 209-220.
8. Stiene-Martin A, Zhou R, Hauser KF (1998) Regional, developmental, and cell cycle-dependent differences in mu, delta, and kappa-opioid receptor expression among cultured mouse astrocytes. Glia 22: 249-259. (Pubitemid 28159016)
9. Merighi S, Gessi S, Varani K, Fazzi D, Stefanelli A, et al. (2013) Morphine mediates a proinflammatory phenotype via m-opioid receptor- PKCproinflammatory phenotype via a PAorea PA in mu, delta, and kaBiochem Pharmacol 86(4): 487-496.
10. Horvath RJ, Romero-Sandoval EA, De Leo JA (2010) Inhibition of microglial P2x4 receptors attenuates morphine tolerance, Iba1, GFAP and mu opioid receptor protein expression while enhancing perivascular microglial ED2. Pain 150(3): 401-413.
11. Horvath RJ, DeLeo JA (2009) Morphine enhances microglial migration through modulation of P2x4 receptor signaling. J Neurosci 29(4): 998-1005.
12. Rivat C, Sebaihi S, Van Steenwincel J, Fouquet S, Kitabgi P, et al. (2013) Src family kinases involved in CXCL12-induced loss of acute morphine analgesia. Brain Behav Immun. In press. doi:10.1016/j.bbi.2013.11.010. [Epub ahead of print].
13. Ferrini F, Trang T, Mattioli TAM, Laffray S, Del'Guidice T, et al. (2013) Morphine hyperalgesia gated through microglia-mediated disruption of neuronal Cl(-) homeostasis. Nat Neurosci 16: 183-192.
14. Raghavendra V, Tanga F, Rutkowski MD (2003) Anti-hyperalgesic and morphine-sparing actions of propentofylline following peripheral nerve injury in rats: mechanistic implications of spinal glia and proinflammatory cytokines. Pain 104: 655-664. (Pubitemid 37289065)
15. Raghavendra V, Tanga FY, DeLeo JA (2004) Attenuation of morphine tolerance, withdrawal-induced hyperalgesia, and associated spinal inflammatory immune responses by propentofylline in rats. Neuropsychopharmacology 29: 327-334. doi:10.1038/sj.npp.1300315. (Pubitemid 38175151)
16. Song P, Zhao ZQ (2001) The involvement of glial cells in the development of morphine tolerance. Neurosci Res 39: 281-286. (Pubitemid 32186379)
17. Hutchinson MR, Bland ST, Johnson KW, Rice KC, Maier SF, et al. (2007) Opioid-induced glial activation: mechanisms of activation and implications for opioid analgesia, dependence, and reward. TheScientificWorldJournal 7: 98-111. doi:10.1100/tsw.2007.230. (Pubitemid 350292608)
18. Liu B, Du L, Hong JS (2000) Naloxone protects rat dopaminergic neurons against inflammatory damage through inhibition of microglia activation and superoxide generation. J Pharmacol Exp Ther 293: 607-617. (Pubitemid 30244114)
19. Lehnardt S, Lachance C, Patrizi S, Lefebvre S, Follett PL, et al. (2002) The Toll-Like Receptor TLR4 Is Necessary for Lipopolysaccharide-Induced Oligodendrocyte Injury in the CNS. J Neurosci 22: 2478-2486. (Pubitemid 37465796)
20. Lehnardt S, Massillon L, Follett P, Jensen FE, Ratan R, et al. (2003) Activation of innate immunity in the CNS triggers neurodegeneration through a Toll-like receptor 4-dependent pathway. Proc Natl Acad Sci USA 100: 8514-8519. doi:10.1073/pnas.1432609100. (Pubitemid 36842576)
21. Bowman CC, Rasley A, Tranguch SL, Marriott I (2003) Cultured astrocytes express toll-like receptors for bacterial products. Glia 43: 281-291. doi:10.1002/glia.10256. (Pubitemid 37047684)
22. Forshammar J, Block L, Lundborg C, Biber B, Hansson E (2011) Naloxone and ouabain in ultra-low concentrations restore Na+/K+-ATPase and cytoskeleton in lipopolysaccharide-treated astrocytes. J Biol Chem 286: 31586-31597. doi:10.1074/jbc.M111.247767.
23. Jack CS, Arbour N, Manusow J, Montgrain V, Blain M, et al. (2005) TLR signaling tailors innate immune responses in human microglia and astrocytes. Journal of immunology 175: 4320-4330. (Pubitemid 41361966)
24. Kigerl K, Lai W, Rivest S, Hart RP, Satoskar AR, et al. (2007) Toll-like receptor (TLR)-2 and TLR-4 regulate inflammation, gliosis, and myelin sparing after spinal cord injury. J Neurochem 102: 37-50. doi:10.1111/j.1471-4159.2007. 04524.x. (Pubitemid 46906264)
25. Tanga FY, Nutile-McMenemy N, DeLeo J (2005) The CNS role of Toll-like receptor 4 in innate neuroimmunity and painful neuropathy. Proc Natl Acad Sci USA 102: 5856-5861. (Pubitemid 40559649)
26. Wu H, Hong JS, Tseng LF (2007) Stereoselective action of (+)-morphine over (-)-morphine in attenuating the (2)-morphine-produced antinociception via the naloxone-sensitive sigma receptor in the mouse. Eur J Pharmacol 571: 145-151. doi:10.1016/j.ejphar.2007.06.012. (Pubitemid 47379690)
27. Abd-el-Basset E, Fedoroff S (1995) Effect of bacterial wall lipopolysaccharide (LPS) on morphology, motility, and cytoskeletal organization of microglia in cultures. J Neurosci Res 41: 222-237. doi:10.1002/jnr.490410210.
28. Liu L, Coller JK, Watkins LR, Somogyi AA, Hutchinson MR (2011) Naloxone-precipitated morphine withdrawal behavior and brain IL-1β expression: comparison of different mouse strains. Brain Behav Immun 25(6): 1223-1232. doi:10.1016/j.bbi.2011.03.016.
29. Hameed H, Hameed M, Christo PJ (2010) The effect of morphine on glial cells as a potential therapeutic target for pharmacological development of analgesic drugs. Curr Pain Headache Rep 14(2): 96-104. doi:10.1007/s11916-010- 0093-y.
30. Bettoni I, Comelli F, Rossini C, Granucci F, Giagnoni G, et al. (2008) Glial TLR4 receptor as new target to treat neuropathic pain: efficacy of a new receptor antagonist in a model of peripheral nerve injury in mice. Glia 56: 1312-1319. doi:10.1002/glia.20699.
31. Hutchinson MR, Northcutt AL, Hiranita T, Wang X, Lewis SS, et al. (2012) Opioid activation of toll-like receptor 4 contributes to drug reinforcement. J Neurosci 32: 11187-11200. doi:10.1523/JNEUROSCI.0684-12.2012.
32. Mattioli TAM, Milne B, Cahill CM (2010) Ultra-low dose naltrexone attenuates chronic morphine-induced gliosis in rats. Mol Pain 6: 22. doi:10.1186/1744-8069-6-22.
33. Hoshino K, Takeuchi O, Kawai T, Sanjo H, Ogawa T, et al. (1999) Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J Immunol 162(7): 3749-2752.
34. Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C, et al. (1998) Defective LPS Signaling in C3H/HeJ and C57BL/10ScCr Mice: Mutations in Tlr4 Gene. Science 282: 2085-2088. doi:10.1126/science.282.5396.2085. (Pubitemid 29001265)
35. Sorge RE, LaCroix-Fralish ML, Tuttle AH, Sotocinal SG, Austin JS, et al. (2011) Spinal cord Toll-like receptor 4 mediates inflammatory and neuropathic hypersensitivity in male but not female mice. J Neurosci 31: 15450-15454. doi:10.1523/JNEUROSCI.3859-11.2011.
36. Cook CD, Barrett AC, Roach EL, Bowman JR, Picker M (2000) Sex-related differences in the antinociceptive effects of opioids: importance of rat genotype, nociceptive stimulus intensity, and efficacy at the mu opioid receptor. Psychopharmacology 150: 430-442. (Pubitemid 30470222)
37. Trang T, Ma W, Chabot JG, Quirion R, Jhamandas K (2006) Spinal modulation of calcitonin gene-related peptide by endocannabinoids in the development of opioid physical dependence. Pain 126(1-3): 256-271. (Pubitemid 44751972)
38. Hutchinson MR, Zhang Y, Shridhar M, Evans JH, Buchanan MM, et al. (2010) Evidence that opioids may have toll-like receptor 4 and MD-2 effects. Brain Behav Immun 24: 83-95. doi:10.1016/j.bbi.2009.08.004.
39. Fukagawa H, Koyama T, Kakuyama M, Fukuda K (2013) Microglial activation involved in morphine tolerance is not mediated by toll-like receptor 4. J Anesth 27(1): 93-97.
40. Kest B, Wilson SG, Mogil JS (1999) Sex differences in supraspinal morphine analgesia are dependent on genotype. J Pharmacol Exp Ther 289: 1370-1375. (Pubitemid 29246666)
41. Crain SM, Shen K (2000) Enhanced analgesic potency and reduced tolerance of morphine in 129/SvEv mice: evidence for a deficiency in GM1 ganglioside-regulated excitatory opioid receptor functions. Brain Res 856: 227-235. (Pubitemid 30085530)
42. Hamann SR, Malik H, Sloan JW, Wala EP (2004) Interactions of "ultra-low" doses of naltrexone and morphine in mature and young male and female rats. Receptors Channels 10: 73-81. doi:10.1080/10606820490464334. (Pubitemid 39023204)
43. Semenova S, Kuzmin A, Zvartau E (1995) Strain differences in the analgesic and reinforcing action of morphine in mice. Pharmacol Biochem Behav 50: 17-21.
44. Terner JM, Barrett AC, Lomas LM, Negus SS, Picker MJ (2006) Influence of low doses of naltrexone on morphine antinociception and morphine tolerance in male and female rats of four strains. Pain 122: 90-101. doi:10.1016/j.pain.2006. 01.019.
45. Wang X, Loram LC, Ramos K, de Jesus AJ, Thomas J, et al. (2012) Morphine activates neuroinflammation in a manner parallel to endotoxin. Proc Natl Acad Sci USA 109: 6325-6330. doi:10.1016/j.neuroscience.2012.06.024.
46. Le Bars D, Gozariu M, Cadden SW (2001) Animal models of nociception. Pharmacol Rev 53: 597-652. (Pubitemid 33136239)
47. Cicero TJ, Nock B, Meyer ER (1996) Gender-related differences in the antinociceptive properties of morphine. J Pharmacol Exp Ther 279: 767-773. (Pubitemid 27166850)
48. Elmer GI, Pieper JO, Negus SS, Woods JH (1998) Genetic variance in nociception and its relationship to the potency of morphine-induced analgesia in thermal and chemical tests. Pain 75: 129-140. (Pubitemid 28254864)
49. Mogil JS, Kest B, Sadowski B, Belknap JK (1996) Differential genetic mediation of sensitivity to morphine in genetic models of opiate antinociception: influence of nociceptive assay. J Pharmacol Exp Ther 276: 532-544.
50. Peckham EM, Barkley LM, Divin MF, Cicero TJ, Traynor JR (2005) Comparison of the antinociceptive effect of acute morphine in female and male Sprague-Dawley rats using the long-lasting mu-antagonist methocinnamox. Brain Res 1058: 137-147. (Pubitemid 41416808)
51. Zhang Y, Li H, Li Y, Sun X, Zhu M, et al. (2011) Essential role of toll-like receptor 2 in morphine-induced microglia activation in mice. Neurosci Lett. 489: 43-7.
52. He L, Li H, Chen L, Miao J, Jiang Y, et al. (2011) Toll-like receptor 9 is required for opioid-induced microglia apoptosis. PLoS One. 6: e18190.
53. Stevens CW, Aravind S, Das S, Davis RL (2013) Pharmacological characterization of LPS and opioid interactions at the toll-like receptor 4. Br J Pharmacol. 168: 1421-9.
54. Yoon SY, Patel D, Dougherty PM (2012) Minocycline blocks lipopolysaccharide induced hyperalgesia by suppression of microglia but not astrocytes. Neuroscience 221: 214-224.
55. Raghavendra V, Rutkowski MD, DeLeo J (2002) The role of spinal neuroimmune activation in morphine tolerance/hyperalgesia in neuropathic and sham-operated rats. J Neurosci 22: 9980-9989. (Pubitemid 35332883)