Opioid-Induced central immune signaling: Implications for opioid analgesia

Headache

Volumn 55, Issue 4, 2015, Pages 475-489

  Grace, Peter M ^a   Maier, Steven F ^a   Watkins, Linda R ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

allodynia; hyperalgesia; opioid receptor; P2X4 receptor; P2X7 receptor; TLR4

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; CANNABINOID 2 RECEPTOR AGONIST; CERAMIDE; CHEMOKINE; COMPLEMENT COMPONENT C5A; DEXTRO SERINE; FRACTALKINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 6; MITOGEN ACTIVATED PROTEIN KINASE; MU OPIATE RECEPTOR; OPIATE; PROTEIN KINASE C GAMMA; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR; NARCOTIC ANALGESIC AGENT; TLR4 PROTEIN, HUMAN;

ANALGESIA; ASTROCYTE; BLOOD BRAIN BARRIER; CELL COUNT; CELL ISOLATION; CENTRAL NERVOUS SYSTEM; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DRUG TOLERANCE; ENDOTHELIUM CELL; EXTRACELLULAR MATRIX; EXTRACELLULAR SPACE; FEMALE; HUMAN; HYDROLYSIS; HYPERALGESIA; IMMUNOCOMPETENT CELL; INNATE IMMUNITY; INTRACELLULAR SIGNALING; MALE; MORPHINE TOLERANCE; NEUROTRANSMISSION; NOCICEPTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SEX DIFFERENCE; SYNAPTIC TRANSMISSION; ADVERSE EFFECTS; ANIMAL; CHEMICALLY INDUCED; DRUG EFFECTS; IMMUNOLOGY; SIGNAL TRANSDUCTION;

ANALGESIA; ANALGESICS, OPIOID; ANIMALS; CENTRAL NERVOUS SYSTEM; DRUG TOLERANCE; HUMANS; HYPERALGESIA; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4;

EID: 84927911504     PISSN: 00178748     EISSN: 15264610     Source Type: Journal    
DOI: 10.1111/head.12552     Document Type: Review

References (138)

1. Chapman CR, Lipschitz DL, Angst MS, et al. Opioid pharmacotherapy for chronic non-cancer pain in the United States: A research guideline for developing an evidence-base. J Pain. 2010; 11: 807-829.
2. Levin M,. Opioids in headache. Headache. 2014; 54: 12-21.
3. Buse DC, Pearlman SH, Reed ML, Serrano D, Ng-Mak DS, Lipton RB,. Opioid use and dependence among persons with migraine: Results of the AMPP study. Headache. 2012; 52: 18-36.
4. Mazer-Amirshahi M, Dewey K, Mullins PM, et al. Trends in opioid analgesic use for headaches in US emergency departments. Am J Emerg Med. 2014; 32: 1068-1073.
5. Christie MJ,. Cellular neuroadaptations to chronic opioids: Tolerance, withdrawal and addiction. Br J Pharmacol. 2008; 154: 384-396.
6. Chu LF, Angst MS, Clark D,. Opioid-induced hyperalgesia in humans: Molecular mechanisms and clinical considerations. Clin J Pain. 2008; 24: 479-496.
7. Grace PM, Hutchinson MR, Maier SF, Watkins LR,. Pathological pain and the neuroimmune interface. Nat Rev Immunol. 2014; 14: 217-231.
8. Hutchinson MR, Shavit Y, Grace PM, Rice KC, Maier SF, Watkins LR,. Exploring the neuroimmunopharmacology of opioids: An integrative review of mechanisms of central immune signaling and their implications for opioid analgesia. Pharmacol Rev. 2011; 63: 772-810.
9. Beitner-Johnson D, Guitart X, Nestler EJ,. Glial fibrillary acidic protein and the mesolimbic dopamine system: Regulation by chronic morphine and Lewis-Fisher strain differences in the rat ventral tegmental area. J Neurochem. 1993; 61: 1766-1773.
10. Song P, Zhao ZQ,. The involvement of glial cells in the development of morphine tolerance. Neurosci Res. 2001; 39: 281-286.
11. Eidson LN, Murphy AZ,. Blockade of Toll-like receptor 4 attenuates morphine tolerance and facilitates the pain relieving properties of morphine. J Neurosci. 2013; 33: 15952-15963.
12. Harada S, Nakamoto K, Tokuyama S,. The involvement of midbrain astrocyte in the development of morphine tolerance. Life Sci. 2013; 93: 573-578.
13. Holdridge SV, Armstrong SA, Taylor AM, Cahill CM,. Behavioural and morphological evidence for the involvement of glial cell activation in delta opioid receptor function: Implications for the development of opioid tolerance. Mol Pain. 2007; 3: 7.
14. Cui Y, Liao XX, Liu W, et al. A novel role of minocycline: Attenuating morphine antinociceptive tolerance by inhibition of p38 MAPK in the activated spinal microglia. Brain Behav Immun. 2008; 22: 114-123.
15. Mika J, Wawrzczak-Bargiela A, Osikowicz M, Makuch W, Przewlocka B,. Attenuation of morphine tolerance by minocycline and pentoxifylline in naive and neuropathic mice. Brain Behav Immun. 2009; 23: 75-84.
16. Raghavendra V, Tanga FY, DeLeo JA,. Attenuation of morphine tolerance, withdrawal-induced hyperalgesia, and associated spinal inflammatory immune responses by propentofylline in rats. Neuropsychopharmacology. 2004; 29: 327-334.
17. Raghavendra V, Rutkowski MD, DeLeo JA,. The role of spinal neuroimmune activation in morphine tolerance/hyperalgesia in neuropathic and sham-operated rats. J Neurosci. 2002; 22: 9980-9989.
18. Hutchinson MR, Lewis SS, Coats BD, et al. Reduction of opioid withdrawal and potentiation of acute opioid analgesia by systemic AV411 (ibudilast). Brain Behav Immun. 2009; 23: 240-250.
19. Thomas J, Hutchinson MR,. Exploring neuroinflammation as a potential avenue to improve the clinical efficacy of opioids. Expert Rev Neurother. 2012; 12: 1311-1324.
20. Hutchinson MR, Watkins LR,. Why is neuroimmunopharmacology crucial for the future of addiction research? Neuropharmacology. 2014; 76 (Pt B): 218-227.
21. Jacobsen JH, Watkins LR, Hutchinson MR,. Discovery of a novel site of opioid action at the innate immune pattern-recognition receptor TLR4 and its role in addiction. Int Rev Neurobiol. 2014; 118: 129-163.
22. Araque A, Navarrete M,. Glial cells in neuronal network function. Philos Trans R Soc Lond B Biol Sci. 2010; 365: 2375-2381.
23. Hanisch UK,. Functional diversity of microglia-how heterogeneous are they to begin with? Front Cell Neurosci. 2013; 7: 65.
24. Nimmerjahn A, Kirchhoff F, Helmchen F,. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science. 2005; 308: 1314-1318.
25. Kettenmann H, Hanisch UK, Noda M, Verkhratsky A,. Physiology of microglia. Physiol Rev. 2011; 91: 461-553.
26. Sofroniew MV,. Molecular dissection of reactive astrogliosis and glial scar formation. Trends Neurosci. 2009; 32: 638-647.
27. Ulmann L, Hatcher JP, Hughes JP, et al. Up-regulation of P2X4 receptors in spinal microglia after peripheral nerve injury mediates BDNF release and neuropathic pain. J Neurosci. 2008; 28: 11263-11268.
28. Grace PM, Rolan PE, Hutchinson MR,. Peripheral immune contributions to the maintenance of central glial activation underlying neuropathic pain. Brain Behav Immun. 2011; 25: 1322-1332.
29. Grace PM, Ramos KM, Rodgers KM, et al. Activation of adult rat CNS endothelial cells by opioid-induced toll-like receptor 4 (TLR4) signaling induces proinflammatory, biochemical, morphological, and behavioral sequelae. Neuroscience. 2014; 280C: 299-317.
30. Wang X, Loram LC, Ramos K, et al. Morphine activates neuroinflammation in a manner parallel to endotoxin. Proc Natl Acad Sci U S A. 2012; 109: 6325-6330.
31. Olin M, Oh S, Roy S, Peterson P, Molitor T,. Morphine induces splenocyte trafficking into the CNS. J Neuroimmune Pharmacol. 2012; 7: 436-443.
32. Brack A, Rittner HL, Stein C,. Immunosuppressive effects of opioids-clinical relevance. J Neuroimmune Pharmacol. 2011; 6: 490-502.
33. Tian L, Rauvala H, Gahmberg CG,. Neuronal regulation of immune responses in the central nervous system. Trends Immunol. 2009; 30: 91-99.
34. Hoarau JJ, Krejbich-Trotot P, Jaffar-Bandjee MC, et al. Activation and control of CNS innate immune responses in health and diseases: A balancing act finely tuned by neuroimmune regulators (NIReg). CNS Neurol Disord Drug Targets. 2011; 10: 25-43.
35. Narita M, Suzuki M, Narita M, et al. Neuronal protein kinase C gamma-dependent proliferation and hypertrophy of spinal cord astrocytes following repeated in vivo administration of morphine. Eur J Neurosci. 2004; 19: 479-484.
36. Wang Z, Ma W, Chabot JG, Quirion R,. Calcitonin gene-related peptide as a regulator of neuronal CaMKII-CREB, microglial p38-NFkappaB and astroglial ERK-Stat1/3 cascades mediating the development of tolerance to morphine-induced analgesia. Pain. 2010; 151: 194-205.
37. Zhao CM, Guo RX, Hu F, et al. Spinal MCP-1 contributes to the development of morphine antinociceptive tolerance in rats. Am J Med Sci. 2012; 344: 473-479.
38. Johnston IN, Milligan ED, Wieseler-Frank J, et al. A role for proinflammatory cytokines and fractalkine in analgesia, tolerance, and subsequent pain facilitation induced by chronic intrathecal morphine. J Neurosci. 2004; 24: 7353-7365.
39. Peterson PK, Molitor TW, Chao CC,. The opioid-cytokine connection. J Neuroimmunol. 1998; 83: 63-69.
40. Calvo CF, Cesselin F, Gelman M, Glowinski J,. Identification of an opioid peptide secreted by rat embryonic mixed brain cells as a promoter of macrophage migration. Eur J Neurosci. 2000; 12: 2676-2684.
41. Turchan-Cholewo J, Dimayuga FO, Ding Q, et al. Cell-specific actions of HIV-Tat and morphine on opioid receptor expression in glia. J Neurosci Res. 2008; 86: 2100-2110.
42. Horvath RJ, Romero-Sandoval EA, De Leo JA,. Inhibition of microglial P2X4 receptors attenuates morphine tolerance, Iba1, GFAP and mu opioid receptor protein expression while enhancing perivascular microglial ED2. Pain. 2010; 150: 401-413.
43. Horvath RJ, DeLeo J,. Morphine enhances microglial migration through modulation of P2X4 receptor signaling. J Neurosci. 2009; 29: 998-1005.
44. Kao SC, Zhao X, Lee CY, et al. Absence of mu opioid receptor mRNA expression in astrocytes and microglia of rat spinal cord. Neuroreport. 2012; 23: 378-384.
45. Merighi S, Gessi S, Varani K, Fazzi D, Stefanelli A, Borea PA,. Morphine mediates a proinflammatory phenotype via mu-opioid receptor-PKCvarepsilon-Akt-ERK1/2 signaling pathway in activated microglial cells. Biochem Pharmacol. 2013; 86: 487-496.
46. Hutchinson MR, Zhang Y, Brown K, et al. Non-stereoselective reversal of neuropathic pain by naloxone and naltrexone: Involvement of toll-like receptor 4 (TLR4). Eur J Neurosci. 2008; 28: 20-29.
47. Hutchinson MR, Zhang Y, Shridhar M, et al. Evidence that opioids may have toll-like receptor 4 and MD-2 effects. Brain Behav Immun. 2010; 24: 83-95.
48. Hutchinson MR, Northcutt AL, Hiranita T, et al. Opioid activation of toll-like receptor 4 contributes to drug reinforcement. J Neurosci. 2012; 32: 11187-11200.
49. Lewis SS, Loram LC, Hutchinson MR, et al. (+)-naloxone, an opioid-inactive toll-like receptor 4 signaling inhibitor, reverses multiple models of chronic neuropathic pain in rats. J Pain. 2012; 13: 498-506.
50. Juni A, Klein G, Pintar JE, Kest B,. Nociception increases during opioid infusion in opioid receptor triple knock-out mice. Neuroscience. 2007; 147: 439-444.
51. Gaveriaux-Ruff C, Filliol D, Simonin F, Matthes HW, Kieffer BL,. Immunosuppression by delta-opioid antagonist naltrindole: Delta- and triple mu/delta/kappa-opioid receptor knockout mice reveal a nonopioid activity. J Pharmacol Exp Ther. 2001; 298: 1193-1198.
52. Waxman AR, Arout C, Caldwell M, Dahan A, Kest B,. Acute and chronic fentanyl administration causes hyperalgesia independently of opioid receptor activity in mice. Neurosci Lett. 2009; 462: 68-72.
53. Wu HE, Sun HS, Cheng CW, Terashvili M, Tseng LF,. 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. 2006; 24: 2575-2580.
54. Hutchinson MR, Bland ST, Johnson KW, Rice KC, Maier SF, Watkins LR,. Opioid-induced glial activation: Mechanisms of activation and implications for opioid analgesia, dependence, and reward. Scientificworldjournal. 2007; 7: 98-111.
55. Nicotra L, Loram LC, Watkins LR, Hutchinson MR,. Toll-like receptors in chronic pain. Exp Neurol. 2012; 234: 316-329.
56. Johnson JL, Rolan PE, Johnson ME, et al. Codeine-induced hyperalgesia and allodynia: Investigating the role of glial activation. Transl Psychiatry. 2014; 4: e482.
57. Lewis SS, Hutchinson MR, Rezvani N, et al. Evidence that intrathecal morphine-3-glucuronide may cause pain enhancement via toll-like receptor 4/MD-2 and interleukin-1beta. Neuroscience. 2010; 165: 569-583.
58. Watkins LR, Hutchinson MR, Rice KC, Maier SF,. The "toll" of opioid-induced glial activation: Improving the clinical efficacy of opioids by targeting glia. Trends Pharmacol Sci. 2009; 30: 581-591.
59. Zhang Y, Li H, Li Y, et al. Essential role of toll-like receptor 2 in morphine-induced microglia activation in mice. Neurosci Lett. 2011; 489: 43-47.
60. Berta T, Liu T, Liu YC, Xu ZZ, Ji RR,. Acute morphine activates satellite glial cells and up-regulates IL-1beta in dorsal root ganglia in mice via matrix metalloprotease-9. Mol Pain. 2012; 8: 18.
61. Hutchinson MR, Coats BD, Lewis SS, et al. Proinflammatory cytokines oppose opioid-induced acute and chronic analgesia. Brain Behav Immun. 2008; 22: 1178-1189.
62. Hutchinson MR, Northcutt AL, Chao LW, et al. Minocycline suppresses morphine-induced respiratory depression, suppresses morphine-induced reward, and enhances systemic morphine-induced analgesia. Brain Behav Immun. 2008; 22: 1248-1256.
63. Bao YH, Zhou QH, Chen R, et al. Gabapentin attenuates morphine tolerance through interleukin-10. Neuroreport. 2014; 25: 71-76.
64. Shavit Y, Wolf G, Goshen I, Livshits D, Yirmiya R,. Interleukin-1 antagonizes morphine analgesia and underlies morphine tolerance. Pain. 2005; 115: 50-59.
65. Berta T, Liu YC, Xu ZZ, Ji RR,. Tissue plasminogen activator contributes to morphine tolerance and induces mechanical allodynia via astrocytic IL-1beta and ERK signaling in the spinal cord of mice. Neuroscience. 2013; 247: 376-385.
66. Li YH, Jin H, Xu JS, Guo GQ, Chen DL, Bo Y,. Complement factor C5a and C5a receptor contribute to morphine tolerance and withdrawal-induced hyperalgesia in rats. Exp Ther Med. 2012; 4: 723-727.
67. Shen CH, Tsai RY, Shih MS, et al. Etanercept restores the antinociceptive effect of morphine and suppresses spinal neuroinflammation in morphine-tolerant rats. Anesth Analg. 2011; 112: 454-459.
68. Cui Y, Chen Y, Zhi JL, Guo RX, Feng JQ, Chen PX,. Activation of p38 mitogen-activated protein kinase in spinal microglia mediates morphine antinociceptive tolerance. Brain Res. 2006; 1069: 235-243.
69. Wang Z, Ma W, Chabot JG, Quirion R,. Cell-type specific activation of p38 and ERK mediates calcitonin gene-related peptide involvement in tolerance to morphine-induced analgesia. FASEB J. 2009; 23: 2576-2586.
70. Tai YH, Tsai RY, Lin SL, et al. Amitriptyline suppresses neuroinflammation-dependent interleukin-10-p38 mitogen-activated protein kinase-heme oxygenase-1 signaling pathway in chronic morphine-infused rats. Anesthesiology. 2009; 110: 1379-1389.
71. Tumati S, Largent-Milnes TM, Keresztes A, et al. Repeated morphine treatment-mediated hyperalgesia, allodynia and spinal glial activation are blocked by co-administration of a selective cannabinoid receptor type-2 agonist. J Neuroimmunol. 2012; 244: 23-31.
72. Niu Z, Ma J, Chu H, Zhao Y, Feng W, Cheng Y,. Melanocortin 4 receptor antagonists attenuates morphine antinociceptive tolerance, astroglial activation and cytokines expression in the spinal cord of rat. Neurosci Lett. 2012; 529: 112-117.
73. Jiang C, Xu L, Chen L, et al. Selective suppression of microglial activation by paeoniflorin attenuates morphine tolerance. Eur J Pain. 2014: In press.
74. Johnston IN, Westbrook RF,. Inhibition of morphine analgesia by LPS: Role of opioid and NMDA receptors and spinal glia. Behav Brain Res. 2005; 156: 75-83.
75. Stevens CW, Aravind S, Das S, Davis RL,. Pharmacological characterization of LPS and opioid interactions at the toll-like receptor 4. Br J Pharmacol. 2013; 168: 1421-1429.
76. Watkins LR, Wang X, Mustafa S, Hutchinson MR,. In vivo veritas: (+)-Naltrexone's actions define translational importance: A letter in response to Skolnick et al. "Translational potential of naloxone and naltrexone as TLR4 antagonists." Trends Pharmacol Sci. 2014; 35: 432-433.
77. Ferrini F, Trang T, Mattioli TA, et al. Morphine hyperalgesia gated through microglia-mediated disruption of neuronal Cl(-) homeostasis. Nat Neurosci. 2013; 16: 183-192.
78. Fukagawa H, Koyama T, Kakuyama M, Fukuda K,. Microglial activation involved in morphine tolerance is not mediated by toll-like receptor 4. J Anesth. 2013; 27: 93-97.
79. Mattioli TA, Leduc-Pessah H, Skelhorne-Gross G, et al. Toll-like receptor 4 mutant and null mice retain morphine-induced tolerance, hyperalgesia, and physical dependence. PLoS One. 2014; 9: e97361.
80. Goodridge HS, McGuiness S, Houston KM, et al. Phosphorylcholine mimics the effects of ES-62 on macrophages and dendritic cells. Parasite Immunol. 2007; 29: 127-137.
81. Ndengele MM, Cuzzocrea S, Masini E, et al. Spinal ceramide modulates the development of morphine antinociceptive tolerance via peroxynitrite-mediated nitroxidative stress and neuroimmune activation. J Pharmacol Exp Ther. 2009; 329: 64-75.
82. Muscoli C, Doyle T, Dagostino C, et al. Counter-regulation of opioid analgesia by glial-derived bioactive sphingolipids. J Neurosci. 2010; 30: 15400-15408.
83. Muscoli C, Cuzzocrea S, Ndengele MM, et al. Therapeutic manipulation of peroxynitrite attenuates the development of opiate-induced antinociceptive tolerance in mice. J Clin Invest. 2007; 117: 3530-3539.
84. Little JW, Cuzzocrea S, Bryant L, et al. Spinal mitochondrial-derived peroxynitrite enhances neuroimmune activation during morphine hyperalgesia and antinociceptive tolerance. Pain. 2013; 154: 978-986.
85. Doyle T, Esposito E, Bryant L, Cuzzocrea S, Salvemini D,. NADPH-oxidase 2 activation promotes opioid-induced antinociceptive tolerance in mice. Neuroscience. 2013; 241: 1-9.
86. Doyle T, Bryant L, Muscoli C, et al. Spinal NADPH oxidase is a source of superoxide in the development of morphine-induced hyperalgesia and antinociceptive tolerance. Neurosci Lett. 2010; 483: 85-89.
87. Liu W, Wang CH, Cui Y, et al. Inhibition of neuronal nitric oxide synthase antagonizes morphine antinociceptive tolerance by decreasing activation of p38 MAPK in the spinal microglia. Neurosci Lett. 2006; 410: 174-177.
88. Zhou D, Chen ML, Zhang YQ, Zhao ZQ,. Involvement of spinal microglial P2X7 receptor in generation of tolerance to morphine analgesia in rats. J Neurosci. 2010; 30: 8042-8047.
89. Chen ML, Cao H, Chu YX, et al. Role of P2X7 receptor-mediated IL-18/IL-18R signaling in morphine tolerance: Multiple glial-neuronal dialogues in the rat spinal cord. J Pain. 2012; 13: 945-958.
90. Reaux-Le Goazigo A, Rivat C, Kitabgi P, Pohl M, Melik Parsadaniantz S,. Cellular and subcellular localization of CXCL12 and CXCR4 in rat nociceptive structures: Physiological relevance. Eur J Neurosci. 2012; 36: 2619-2631.
91. Reaux-Le Goazigo A, Van Steenwinckel J, Rostene W, Melik Parsadaniantz S,. Current status of chemokines in the adult CNS. Prog Neurobiol. 2013; 104: 67-92.
92. Heinisch S, Palma J, Kirby LG,. Interactions between chemokine and mu-opioid receptors: Anatomical findings and electrophysiological studies in the rat periaqueductal grey. Brain Behav Immun. 2011; 25: 360-372.
93. Parsadaniantz SM, Rivat C, Rostene W, Goazigo AR,. Opioid and chemokine receptor crosstalk: A promising target for pain therapy? Nat Rev Neurosci. 2015; 16: 69-78.
94. Szabo I, Chen XH, Xin L, et al. Heterologous desensitization of opioid receptors by chemokines inhibits chemotaxis and enhances the perception of pain. Proc Natl Acad Sci U S A. 2002; 99: 10276-10281.
95. Chen X, Geller EB, Rogers TJ, Adler MW,. Rapid heterologous desensitization of antinociceptive activity between mu or delta opioid receptors and chemokine receptors in rats. Drug Alcohol Depend. 2007; 88: 36-41.
96. Rivat C, Sebaihi S, Van Steenwinckel J, et al. Src family kinases involved in CXCL12-induced loss of acute morphine analgesia. Brain Behav Immun. 2014; 38: 38-52.
97. Vanderah TW, Suenaga NM, Ossipov MH, Malan TP Jr, Lai J, Porreca F,. Tonic descending facilitation from the rostral ventromedial medulla mediates opioid-induced abnormal pain and antinociceptive tolerance. J Neurosci. 2001; 21: 279-286.
98. Ossipov MH, Lai J, King T, Vanderah TW, Porreca F,. Underlying mechanisms of pronociceptive consequences of prolonged morphine exposure. Biopolymers. 2005; 80: 319-324.
99. Hay JL, Kaboutari J, White JM, Salem A, Irvine R,. Model of methadone-induced hyperalgesia in rats and effect of memantine. Eur J Pharmacol. 2010; 626: 229-233.
100. Doverty M, White JM, Somogyi AA, Bochner F, Ali R, Ling W,. Hyperalgesic responses in methadone maintenance patients. Pain. 2001; 90: 91-96.
101. Hay JL, White JM, Bochner F, Somogyi AA, Semple TJ, Rounsefell B,. Hyperalgesia in opioid-managed chronic pain and opioid-dependent patients. J Pain. 2009; 10: 316-322.
102. Angst MS, Clark JD,. Opioid-induced hyperalgesia: A qualitative systematic review. Anesthesiology. 2006; 104: 570-587.
103. Pud D, Yarnitsky D, Eisenberg E, Andersen OK, Arendt-Nielsen L,. Effects of cold stimulation on secondary hyperalgesia (HA) induced by capsaicin in healthy volunteers. Exp Brain Res. 2006; 170: 22-29.
104. Johnson JL, Hutchinson MR, Williams DB, Rolan P,. Medication-overuse headache and opioid-induced hyperalgesia: A review of mechanisms, a neuroimmune hypothesis and a novel approach to treatment. Cephalalgia. 2013; 33: 52-64.
105. Scher AI, Lipton RB, Stewart WF, Bigal M,. Patterns of medication use by chronic and episodic headache sufferers in the general population: Results from the frequent headache epidemiology study. Cephalalgia. 2010; 30: 321-328.
106. Capuano A, De Corato A, Lisi L, Tringali G, Navarra P, Dello Russo C,. Proinflammatory-activated trigeminal satellite cells promote neuronal sensitization: Relevance for migraine pathology. Mol Pain. 2009; 5: 43.
107. Zhang XC, Kainz V, Burstein R, Levy D,. Tumor necrosis factor-alpha induces sensitization of meningeal nociceptors mediated via local COX and p38 MAP kinase actions. Pain. 2011; 152: 140-149.
108. Zhang X, Burstein R, Levy D,. Local action of the proinflammatory cytokines IL-1beta and IL-6 on intracranial meningeal nociceptors. Cephalalgia. 2012; 32: 66-72.
109. Due MR, Piekarz AD, Wilson N, et al. Neuroexcitatory effects of morphine-3-glucuronide are dependent on Toll-like receptor 4 signaling. J Neuroinflammation. 2012; 9: 200.
110. Wilson NM, Jung H, Ripsch MS, Miller RJ, White FA,. CXCR4 signaling mediates morphine-induced tactile hyperalgesia. Brain Behav Immun. 2011; 25: 565-573.
111. Loyd DR, Murphy AZ,. The neuroanatomy of sexual dimorphism in opioid analgesia. Exp Neurol. 2014; 259: 57-63.
112. Clayton JA, Collins FS,. Policy: NIH to balance sex in cell and animal studies. Nature. 2014; 509: 282-283.
113. Loram LC, Sholar PW, Taylor FR, et al. Sex and estradiol influence glial pro-inflammatory responses to lipopolysaccharide in rats. Psychoneuroendocrinology. 2012; 37: 1688-1699.
114. Lewis SS, Hutchinson MR, Frick MM, et al. Select steroid hormone glucuronide metabolites can cause toll-like receptor 4 activation and enhanced pain. Brain Behav Immun. 2015; 44: 128-136.
115. Sorge RE, LaCroix-Fralish ML, Tuttle AH, et al. Spinal cord Toll-like receptor 4 mediates inflammatory and neuropathic hypersensitivity in male but not female mice. J Neurosci. 2011; 31: 15450-15454.
116. Smitherman TA, Burch R, Sheikh H, Loder E,. The prevalence, impact, and treatment of migraine and severe headaches in the United States: A review of statistics from national surveillance studies. Headache. 2013; 53: 427-436.
117. Colas R, Munoz P, Temprano R, Gomez C, Pascual J,. Chronic daily headache with analgesic overuse: Epidemiology and impact on quality of life. Neurology. 2004; 62: 1338-1342.
118. Celerier E, Gonzalez JR, Maldonado R, Cabanero D, Puig MM,. Opioid-induced hyperalgesia in a murine model of postoperative pain: Role of nitric oxide generated from the inducible nitric oxide synthase. Anesthesiology. 2006; 104: 546-555.
119. Loram LC, Grace PM, Strand KA, et al. Prior exposure to repeated morphine potentiates mechanical allodynia induced by peripheral inflammation and neuropathy. Brain Behav Immun. 2012; 26: 1256-1264.
120. Horvath RJ, Landry RP, Romero-Sandoval EA, DeLeo JA,. Morphine tolerance attenuates the resolution of postoperative pain and enhances spinal microglial p38 and extracellular receptor kinase phosphorylation. Neuroscience. 2010; 169: 843-854.
121. Hook MA, Liu GT, Washburn SN, et al. The impact of morphine after a spinal cord injury. Behav Brain Res. 2007; 179: 281-293.
122. Chou R, Deyo R, Devine B, et al. The Effectiveness and Risks of Long-Term Opioid Treatment of Chronic Pain, 2014. http://www.ncbi.nlm.nih.gov/books/NBK258809/.
123. van Gulik L, Ahlers SJ, van de Garde EM, et al. Remifentanil during cardiac surgery is associated with chronic thoracic pain 1 yr after sternotomy. Br J Anaesth. 2012; 109: 616-622.
124. Salengros JC, Huybrechts I, Ducart A, et al. Different anesthetic techniques associated with different incidences of chronic post-thoracotomy pain: Low-dose remifentanil plus presurgical epidural analgesia is preferable to high-dose remifentanil with postsurgical epidural analgesia. J Cardiothorac Vasc Anesth. 2010; 24: 608-616.
125. Smith AM, Dragunow M,. The human side of microglia. Trends Neurosci. 2014; 37: 125-135.
126. Ji RR, Berta T, Nedergaard M,. Glia and pain: Is chronic pain a gliopathy? Pain. 2013; 154: S10-28.
127. Landry RP, Jacobs VL, Romero-Sandoval EA, DeLeo JA,. Propentofylline, a CNS glial modulator does not decrease pain in post-herpetic neuralgia patients: In vitro evidence for differential responses in human and rodent microglia and macrophages. Exp Neurol. 2012; 234: 340-350.
128. Watkins LR, Hutchinson MR, Johnson KW, et al. Propentofylline, a CNS glial modulator, does not decrease pain in post-herpetic neuralgia patients: In vitro evidence for differential responses in human and rodent microglia and macrophages. Exp Neurol. 2012; 234: 351-353.
129. Watkins LR, Hutchinson MR,. A concern on comparing "apples" and "oranges" when differences between microglia used in human and rodent studies go far, far beyond simply species: Comment on Smith and Dragunow. Trends Neurosci. 2014; 37: 189-190.
130. Byrd D, Murray J, Safdieh G, Morgello S,. Impact of opiate addiction on neuroinflammation in HIV. J Neurovirol. 2012; 18: 364-373.
131. Kwok YH, Hutchinson MR, Gentgall MG, Rolan PE,. Increased responsiveness of peripheral blood mononuclear cells to in vitro TLR 2, 4 and 7 ligand stimulation in chronic pain patients. PLoS One. 2012; 7: e44232.
132. Gagnon M, Bergeron MJ, Lavertu G, et al. Chloride extrusion enhancers as novel therapeutics for neurological diseases. Nat Med. 2013; 19: 1524-1528.
133. Ji RR, Xu ZZ, Gao YJ,. Emerging targets in neuroinflammation-driven chronic pain. Nat Rev Drug Discov. 2014; 13: 533-548.
134. Jin H, Li YH, Xu JS, Guo GQ, Chen DL, Bo Y,. Lipoxin A4 analog attenuates morphine antinociceptive tolerance, withdrawal-induced hyperalgesia, and glial reaction and cytokine expression in the spinal cord of rat. Neuroscience. 2012; 208: 1-10.
135. Kwilasz AJ, Grace PM, Serbedzija P, Maier SF, Watkins LR,. The therapeutic potential of interleukin-10 in neuroimmune diseases. Neuropharmacology. 2014: In press.
136. Wang X, Grace PM, Pham MN, et al. Rifampin inhibits Toll-like receptor 4 signaling by targeting myeloid differentiation protein 2 and attenuates neuropathic pain. FASEB J. 2013; 27: 2713-2722.
137. Lu CH, Chao PC, Borel CO, et al. Preincisional intravenous pentoxifylline attenuating perioperative cytokine response, reducing morphine consumption, and improving recovery of bowel function in patients undergoing colorectal cancer surgery. Anesth Analg. 2004; 99: 1465-1471, table of contents.
138. Wordliczek J, Szczepanik AM, Banach M, et al. The effect of pentoxifiline on post-injury hyperalgesia in rats and postoperative pain in patients. Life Sci. 2000; 66: 1155-1164.