A role for proinflammatory cytokines and fractalkine in analgesia, tolerance, and subsequent pain facilitation induced by chronic intrathecal morphine

Journal of Neuroscience

Volumn 24, Issue 33, 2004, Pages 7353-7365

  Johnston, Ian N ^a   Milligan, Erin D ^a   Wieseler Frank, Julie ^a   Frank, Matthew G ^a   Zapata, Varlin ^a   Campisi, Jay ^a   Langer, Stephen ^a   Martin, David ^b   Green, Paula ^c   Fleshner, M ^a   Leinwand, Leslie ^a   Maier, Steven F ^a   Watkins, Linda R ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b AMGEN INC   (United States)

^c GLAXOSMITHKLINE   (United Kingdom)

Author keywords

Allodynia; Anti inflammatory cytokines; Hyperalgesia; Interleukin 1; Interleukin 10; Proinflammatory cytokines; Rats

Indexed keywords

ADENOVIRUS VECTOR; CHEMOKINE; CYTOKINE; FRACTALKINE; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 10; INTERLEUKIN 1BETA; MORPHINE; NEUTRALIZING ANTIBODY; CHEMOKINE (C X3 C MOTIF) LIGAND 1; CHEMOKINE (C-X3-C MOTIF) LIGAND 1; CX3C CHEMOKINE; CYTOKINE RECEPTOR; INTERLEUKIN 1; MEMBRANE PROTEIN; MESSENGER RNA; NARCOTIC ANALGESIC AGENT; SIALOGLYCOPROTEIN; V28 RECEPTOR; VIRUS RECEPTOR;

ALLODYNIA; ANALGESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CEREBROSPINAL FLUID; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; DRUG TOLERANCE; GENE THERAPY; HYPERALGESIA; MALE; NOCICEPTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PAIN; PRIORITY JOURNAL; RAT; SPINAL CORD; ANIMAL; BIOSYNTHESIS; DRUG ANTAGONISM; DRUG EFFECT; GENETICS; HEAT; IMMUNOLOGY; INFLAMMATION; INTRASPINAL DRUG ADMINISTRATION; METABOLISM; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANALGESICS, OPIOID; ANIMALS; CHEMOKINES, CX3C; DRUG TOLERANCE; GENE THERAPY; HEAT; HYPERALGESIA; INFLAMMATION; INJECTIONS, SPINAL; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; INTERLEUKIN-1; INTERLEUKIN-10; MALE; MEMBRANE PROTEINS; MORPHINE; PAIN; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, CYTOKINE; RECEPTORS, HIV; RNA, MESSENGER; SIALOGLYCOPROTEINS; SPINAL CORD;

EID: 7244226284     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1850-04.2004     Document Type: Article

References (60)

1. Apte RN, Durum SK, Oppenheim JJ (1990) Opioids modulate interleukin-1 production and secretion by bone-marrow macrophages. Immunol Lett 24:141-148.
2. Azuma Y, Ohura K (2002) Endomorphin-2 modulates productions of TNF-alpha, IL-1beta, IL-10, and IL-12, and alters functions related to innate immune of macrophages. Inflammation 26:223-232.
3. Beitner-Johnson D, Guitart X, Nestler EJ (1993) Glial fibrillary acidic protein and the mesolimbic dopamine system: regulation by chronic morphine and Lewis-Fischer strain differences in the rat ventral tegmental area. J Neurochem 61:1766-1773.
4. Boddeke EW (2001) Involvement of chemokines in pain. Eur J Pharmacol 429:115-119.
5. Brewer KL, Bethea JR, Yezierski RP (1999) Neuroprotective effects of interleukin-10 following excitotoxic spinal cord injury. Exp Neurol 159:484-493.
6. Celerier E, Laulin J, Larcher A, Le Moal M, Simonnet G (1999) Evidence for opiate-activated NMDA processes masking opiate analgesia in rats. Brain Res 847:18-25.
7. Chao CC, Gekker G, Sheng WS, Hu S, Tsang M, Peterson PK (1994) 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 269:198-203.
8. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL (1994) Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 53:55-63.
9. Chapman GA, Moores K, Harrison D, Campbell CA, Stewart BR, Strijbos PJ (2000) Fractalkine cleavage from neuronal membranes represents an acute event in the inflammatory response to excitotoxic brain damage. J Neurosci 20:RC87(1-5).
10. Chomczynski P, Sacchi N (1987) Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal Biochem 162:156-159.
11. Das KP, McMillian MK, Bing G, Hong JS (1995) Modulatory effects of [Met5]-enkephalin on interleukin-1 beta secretion from microglia in mixed brain cell cultures. J Neuroimmunol 62:9-17.
12. Fairbanks CA, Wilcox GL (1997) Acute tolerance to spinally administered morphine compares mechanistically with chronically induced morphine tolerance. J Pharmacol Exp Ther 282:1408-1417.
13. Fairbanks CA, Wilcox GL (2000) Spinal plasticity of acute opioid tolerance. J Biomed Sci 7:200-212.
14. Falchi M, Ferrara F, Gharib C, Dib B (2001) Hyperalgesic effect of intrathecally administered interleukin-1 in rats. Drugs Exp Clin Res 27:97-101.
15. Gomez-Flores R, Rice KC, Zhang X, Weber RJ (2001) Increased tumor necrosis factor-alpha and nitric oxide production by rat macrophages following in vitro stimulation and intravenous administration of the delta-opioid agonist SNC 80. Life Sci 68:2675-2684.
16. Gul H, Yildiz O, Dogrul A, Yesilyurt O, Isimer A (2000) The interaction between IL-1beta and morphine: possible mechanism of the deficiency of morphine-induced analgesia in diabetic mice. Pain 89:39-45.
17. Haddad JJ (2002) Cytokines and related receptor-mediated signaling pathways. Biochem Biophys Res Commun 297:700-713.
18. Hansen MK, Nguyen KT, Fleshner M, Goehler LE, Gaykema RP, Maier SF, Watkins LR (2000a) Effects of vagotomy on serum endotoxin, cytokines, and corticosterone after intraperitoneal lipopolysaccharide. Am J Physiol Regul Integr Comp Physiol 278:R331-R336.
19. Hansen MK, Nguyen KT, Goehler LE, Gaykema RP, Fleshner M, Maier SF, Watkins LR (2000b) Effects of vagotomy on lipopolysaccharide-induced brain interleukin-1beta protein in rats. Auton Neurosci 85:119-126.
20. Harvey LO (1986) Efficient estimation of sensory thresholds. Behav Res Methods Instr Comp 18:623-632.
21. Ji G-C, Ma F, Zhang Y-Q, Wu G-C (2002) Thermal hyperalgesic effects induced by intracerebroventricular injection of interleukin-1beta in rats. Sheng Li Xue Bao 54:325-328.
22. Kanaan SA, Poole S, Saade NE, Jabbur S, Safieh-Garabedian B (1998) Interleukin-10 reduces the endotoxin-induced hyperalgesia in mice. J Neuroimmunol 86:142-150.
23. Kowalski J, Makowiecka K, Belowski D, Herman ZS (2000) Augmenting effect of methionine-enkephalin on interleukin-6 production by cytokine-stimulated murine macrophages. Neuropeptides 34:187-192.
24. Larcher A, Laulin JP, Celerier E, Le Moal M, Simonnet G (1998) Acute tolerance associated with a single opiate administration: involvement of N-methyl-D-aspartate-dependent pain facilitatory systems. Neuroscience 84:583-589.
25. Laughlin TM, Bethea JR, Yezierski RP, Wilcox GL (2000) Cytokine involvement in dynorphin-induced allodynia. Pain 84:159-167.
26. Law PY, Wong YH, Loh HH (2000) Molecular mechanisms and regulation of opioid receptor signaling. Ann Rev Pharmacol Toxicol 40:389-430.
27. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25:402-408.
28. Ma J-Y, Zhao Z-Q (2002) The involvement of glia in long-term plasticity in the spinal dorsal horn of the rat. NeuroReport 13:1781-1784.
29. Maderspach K, Solomonia R (1988) Glial and neuronal opioid receptors: apparent positive cooperativity observed in intact cultured cells. Brain Res 441:41-47.
30. Mantz J, Cordier J, Giaume C (1993) Effects of general anesthetics on intercellular communications mediated by gap junctions between astrocytes in primary culture. Anesthesiology 78:892-901.
31. Mao J (2002) Opioid-induced abnormal pain sensitivity: implications in clinical opioid therapy. Pain 100:213-217.
32. Mao J, Mayer DJ (2001) Spinal cord neuroplasticity following repeated opioid exposure and its relation to pathological pain. Ann NY Acad Sci 933:175-184.
33. Mao J, Sung B, Ji RR, Lim G (2002) Chronic morphine induces downregulation of spinal glutamate transporters: implications in morphine tolerance and abnormal pain sensitivity. J Neurosci 22:8312-8323.
34. McCarthy L, Wetzel M, Sliker JK, Eisenstein TK, Rogers TJ (2001) Opioids, opioid receptors, and the immune response. Drug Alcohol Depend 62:111-123.
35. McNally GP, Westbrook RF (1998) Effects of systemic, intracerebral, or intrathecal administration of an N-methyl-D-aspartate receptor antagonist on associative morphine analgesic tolerance and hyperalgesia in rats. Behav Neurosci 112:966-978.
36. Mellon RD, Bayer BM (1998) Evidence for central opioid receptors in the immunomodulatory effects of morphine: review of potential mechanisim(s) of action. J Neuroimmunol 83:19-28.
37. Milligan ED, Mehmert KK, Hinde JL, Harvey LO, Martin D, Tracey KJ, Maier SF, Watkins LR (2000) Thermal hyperalgesia and mechanical allodynia produced by intrathecal administration of the human immunodeficiency virus-1 (HIV-1) envelope glycoprotein, gp120. Brain Res 861:105-116.
38. Milligan ED, O'Connor KA, Nguyen KT, Armstrong CB, Twining C, Gaykema RP, Holguin A, Martin D, Maier SF, Watkins LR (2001) Intrathecal HIV-1 envelope glycoprotein gp120 induces enhanced pain states mediated by spinal cord proinflammatory cytokines. J Neurosci 21:2808-2819.
39. Milligan ED, Twining C, Chapman GA, O'Connor K, Maier SF, Watkins LR (2002) Spinal cord fractalkine, a chemokine, is involved in exaggerated pain states. Brain Behav Immunity 16:201.
40. Milligan ED, Langer SJ, Sloane EM, Chacur M, Weiseler-Frank J, Frank MG, Flotte TR, Cruz P, Leinwand L, Maier SF, Watkins LR (2003) Inflammatory and chronic constriction injury-induced pain states are controlled by spinal delivery of viral and non-viral vectors encoding the antiinflammatory gene, interleukin-10 (IL10), Soc Neurosci Abstr 29:587.9.
41. O'Connor K, Holguin A, Hansen MK, Maier SF, Watkins LR (2004) A method for measuring multiple cytokines from small samples. Brain Behav Immunity 18:274-280.
42. Oka T, Aou S, Hori T (1993) Intracerebroventricular injection of interleukin-1 beta induces hyperalgesia in rats. Brain Res 624:61-68.
43. Peng X, Mosser DM, Adler MW, Rogers TJ, Meissler Jr JJ, Eisenstein TK (2000) Morphine enhances interleukin-12 and the production of other pro-inflammatory cytokines in mouse peritoneal macrophages. J Leukocyte Biol 68:723-728.
44. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45.
45. Poole S, Cunha FQ, Selkirk S, Lorenzetti BB, Ferreira SH (1995) Cytokine-mediated inflammatory hyperalgesia limited by interleukin-10. Br J Pharmacol 115:684-688.
46. Raghavendra V, Rutkowski MD, DeLeo JA (2002) The role of spinal neuroimmune activation in morphine tolerance/hyperalgesia in neuropathic and sham-operated rats. J Neurosci 22:9980-9989.
47. Reeve AJ, Patel S, Fox A, Walker K, Urban L (2000) Intrathecally administered endotoxin or cytokines produce allodynia, hyperalgesia and changes in spinal cord neuronal responses to nociceptive stimuli in the rat. Eur J Pain 4:247-257.
48. Roy S, Cain KJ, Chapin RB, Charboneau RG, Barke RA (1998) Morphine modulates NF kappa B activation in macrophages. Biochem Biophys Res Commun 245:392-396.
49. Schaack J, Langer S, Guo X (1995) Efficient selection of recombinant adeno-viruses by vectors that express beta-galactosidase. J Virol 69:3920-3923.
50. Song P, Zhao ZQ (2001) The involvement of glial cells in the development of morphine tolerance. Neurosci Res [Suppl] 39:281-286.
51. Szabo I, Chen X-H, Xin L, Adler MW, Howard OMZ, Oppenheim JJ, Rogers TJ (2002) Heterologous desensitization of opioid receptors by chemokines inhibits fchemotaxis and enhances the perception of pain. Proc Natl Acad Sci USA 99:10276-10281.
52. Tadano T, Namioka M, Nakagawasai O, Tan-No K, Matsushima K, Endo Y, Kisara K (1999) Induction of nociceptive responses by intrathecal injection of interleukin-1 in mice. Life Sci 65:255-261.
53. Treutwein B, Strasburger H (1999) Fitting the psychometric function. Percept Psychophys 61:87-106.
54. Vanderah TW, Ossipov MH, Lai J, Malan Jr TP, Porreca F (2001) Mechanisms of opioid-induced pain and antinociceptive tolerance: descending facilitation and spinal dynorphin. Pain 92:5-9.
55. Watkins L, Kinscheck I, Miller J, Coghill R, Frank H, Mayer D (1984) CCK antagonists enhance opiate analgesia and appear to reverse morphine tolerance. Pain 18:S353.
56. Watkins LR, Maier SF (2003) Glia: a novel drug discovery target for clinical pain. Nat Rev 2:973-985.
57. Watkins LR, Milligan ED, Maier SF (2001) Spinal cord glia: new players in pain. Pain 93:201-205.
58. Watkins LR, Milligan ED, Maier SF (2003) Glial proinflammatory cytokines mediate exaggerated pain states: implications for clinical pain. Adv Exp Med Biol 521:1-21.
59. Yaksh TL, Kohl RL, Rudy TA (1977) Induction of tolerance and withdrawal in rats receiving morphine in the spinal subarachnoid space. Eur J Pharmacol 42:275-284.
60. Yaksh TL, Hassenbusch S, Burchiel K, Hildebrand KR, Page LM, Coffey RJ (2002) Inflammatory masses associated with intrathecal drug infusion: a review of preclinical evidence and human data. Pain Med 3:300-312.