PAIN
Volume 108, Issue 1 , Pages 67-75 , March 2004

Endogenous peripheral antinociception in early inflammation is not limited by the number of opioid-containing leukocytes but by opioid receptor expression

Received 25 August 2003 ,Revised 21 November 2003 ,Accepted 1 December 2003.

References 

  1. Antonijevic I, Mousa SA, Schäfer M, Stein C. Perineurial defect and peripheral opioid analgesia in inflammation. J Neurosci. 1995;15:165–172
  2. Blackwell TS, Lancaster LH, Blackwell TR, Venkatakrishnan A, Christman JW. Chemotactic gradients predict neutrophilic alveolitis in endotoxin-treated rats. Am J Respir Crit Care Med. 1999;159:1644–1652
  3. Bourgoin S, Le Bars D, Clot AM, Hamon M, Cesselin F. Subcutaneous formalin induces a segmental relase of Met-enkephalin-like material from the spinal cord. Pain. 1990;41:323–329
  4. Buzas B, Cox BM. Quantitative analysis of mu and delta opioid receptor gene expression in rat brain and peripheral ganglia using competitive polyme rase chain reaction. Neuroscience. 1997;76:479–489
  5. Cabot PJ, Carter L, Gaiddon C, Zhang Q, Schäfer M, Loeffler JP, et al. Immune cell-derived β-endorphin-production, release and control of inflammatory pain in rats. J Clin Invest. 1997;100:142–148
  6. Crisp T, Stafinsky JL, Hoskins DL, Perni VC, Uram M, Gordon TL. Age related changes in the spinal antinociceptive effects of DAGO, DPDPE and beta-endorphin in the rat. Brain Res. 1994;643:282–286
  7. Cunha FQ, Lorenzetti BB, Poole S, Ferreira SH. Interleukin-8 as a mediator of sympathetic pain. Br J Pharmacol. 1991;104:765–767
  8. Cunha FQ, Poole S, Lorenzetti BB, Ferreira SH. The pivotal role of tumour necrosis factor alpha in the development of inflammatory hyperalgesia. Br J Pharmacol. 1992;107:660–664
  9. Frevert CW, Farone A, Danaee H, Paulauskis JD, Kobzik L. Functional characterization of rat chemokine macrophage inflammatory protein-2. Inflammation. 1995;19:133–142
  10. Hassan AH, Ableitner A, Stein C, Herz A. Inflammation of the rat paw enhances axonal transport of opioid receptors in the sciatic nerve and increases their density in the inflamed tissue. Neuroscience. 1993;55:185–195
  11. Julius D, Basbaum AI. Molecular mechanisms of nociception. Nature. 2001;413:203–210
  12. Lorenzetti BB, Veiga FH, Canetti CA, Poole S, Cunha FQ, Ferreira SH. CINC-1 mediates the sympathetic component of inflammatory mechanical hypersensitivitiy in rats. Eur Cytokine Netw. 2002;13:456–461
  13. Machelska H, Cabot PJ, Mousa SA, Zhang Q, Stein C. Pain control in inflammation governed by selectins. Nat Med. 1998;4:1425–1428
  14. Machelska H, Mousa SA, Brack A, Schopohl JK, Rittner HL, Schäfer M, et al. Opioid control of inflammatory pain regulated by intercellular adhesion molecule-1. J Neurosci. 2002;22:5588–5596
  15. McColl SR, Clark-Lewis I. Inhibition of murine neutrophil recruitment in vivo by CXC chemokine receptor antagonists. J Immunol. 1999;163:2829–2835
  16. Mercer-Jones MA, Shrotri MS, Heinzelmann M, Peyton JC, Cheadle WG. Regulation of early peritoneal neutrophil migration by macrophage inflammatory protein-2 and mast cells in experimental peritonitis. J Leukoc Biol. 1999;65:249–255
  17. Mousa SA, Zhang Q, Sitte N, Ji R, Stein C. Beta-endorphin-containing memory-cells and mu-opioid receptors undergo transport to peripheral inflamed tissue. J Neuroimmunol. 2001;115:71–78
  18. Mousa SA, Machelska H, Schäfer M, Stein C. Immunohistochemical localization of endomorphin-1 and endomorphin-2 in immune cells and spinal cord in a model of inflammatory pain. J Neuroimmunol. 2002;126:5–15
  19. Oh SB, Tran PB, Gillard SE, Hurley RW, Hammond DL, Miller RJ. Chemokines and glycoprotein120 produce pain hypersensitivity by directly exciting primary nociceptive neurons. J Neurosci. 2001;21:5027–5035
  20. Pol O, Alameda F, Puig MM. Inflammation enhances mu-opioid receptor transcription and expression in mice intestine. Mol Pharmacol. 2001;60:894–899
  21. Pol O, Valle L, Puig MM. Antisense oligodeoxynucleotides to mu- and delta-opioid receptor mRNA block the enhanced effects of opioids during intestinal inflammation. Eur J Pharmacol. 2001;428:127–136
  22. Przewlocki R, Hassan AH, Lason W, Epplen C, Herz A, Stein C. Gene expression and localization of opioid peptides in immune cells of inflamed tissue: functional role in antinociception. Neuroscience. 1992;48:491–500
  23. Puig MM, Pol O. Peripheral effects of opioids in a model of chronic intestinal inflammation in mice. J Pharmacol Exp Ther. 1998;287:1068–1075
  24. Rittner HL, Brack A, Machelska H, Mousa SA, Bauer M, Schäfer M, et al. Opioid peptide expressing leukocytes—identification, recruitment and simultaneously increasing inhibiton of inflammatory pain. Anesthesiology. 2001;95:500–508
  25. Rittner HL, Brack A, Stein C. Pro- versus analgesic actions of immune cells. Curr Opin Anaesthesiol. 2003;16:527–533
  26. Schäfer M, Carter L, Stein C. Interleukin 1 beta and corticotropin-releasing factor inhibit pain by releasing opioids from immune cells in inflamed tissue. Proc Natl Acad Sci USA. 1994;91:4219–4223
  27. Schäfer M, Imai Y, Uhl GR, Stein C. Inflammation enhances peripheral mu-opioid receptor-mediated analgesia, but not mu-opioid receptor transcription in dorsal root ganglia. Eur J Pharmacol. 1995;279:165–169
  28. Schäfer M, Mousa SA, Zhang Q, Carter L, Stein C. Expression of corticotropin-releasing factor in inflamed tissue is required for intrinsic peripheral opioid analgesia. Proc Natl Acad Sci USA. 1996;93:6096–6100
  29. Schmal H, Shanley TP, Jones ML, Friedl HP, Ward PA. Role for macrophage inflammatory protein-2 in lipopolysaccharide-induced lung injury in rats. J Immunol. 1996;156:1963–1972
  30. Scholz J, Woolf CJ. Can we conquer pain?. Nat Neurosci. 2002;5:1062–1067
  31. Shaqura MA, Zöllner C, Mousa SA, Stein C, Schäfer M. Characterization of μ opioid receptor binding and G-protein coupling in rat hypothalamus, spinal cord and primary afferent neurons during inflammatory pain. J Pharmacol Exp Ther. 2003;Oct 30: Epub ahead of print
  32. Shibata F, Konishi K, Kato H, Komorita N, al-Mokdad M, Fujioka M, et al. Recombinant production and biological properties of rat cytokine-induced neutrophil chemoattractants, GRO/CINC-2 alpha, CINC-2 beta and CINC-3. Eur J Biochem. 1995;231:306–311
  33. Stein C, Gramsch C, Herz A. Intrinsic mechanisms of antinociception in inflammation: local opioid receptors and beta-endorphin. J Neurosci. 1990;10:1292–1298
  34. Stein C, Hassan AH, Przewlocki R, Gramsch C, Peter K, Herz A. Opioids from immunocytes interact with receptors on sensory nerves to inhibit nociception in inflammation. Proc Natl Acad Sci USA. 1990;87:5935–5939
  35. Stein C, Hassan AH, Lehrberger K, Giefing J, Yassouridis A. Local analgesic effect of endogenous opioid peptides. Lancet. 1993;342:321–324
  36. Stein C, Schäfer M, Machelska H. Attacking pain at its source: new perspectives on opioids. Nat Med. 2003;9:1003–1008
  37. Takemori AE, Portoghese PS. Enkephalin antinociception in mice is mediated by delta 1- and delta 2-opioid receptors in the brain and spinal cord, respectively. Eur J Pharmacol. 1993;242:145–150
  38. Watkins LR, Maier SF. Beyond neurons: evidence that immune and glial cells contribute to pathological pain states. Physiol Rev. 2002;82:981–1011
  39. Wiekowski MT, Chen SC, Zalamea P, Wilburn BP, Kinsley DJ, Sharif WW, et al. Disruption of neutrophil migration in a conditional transgenic model: evidence for CXCR2 desensitization in vivo. J Immunol. 2001;167:7102–7110
  40. Xu Y, Gu Y, Wu P, Li GW, Huang LY. Efficiencies of transgene expression in nociceptive neurons through different routes of delivery of adeno-associated viral vectors. Hum Gene Ther. 2003;14:897–906
  41. Xu Y, Gu Y, Xu GY, Wu P, Li GW, Huang LY. Adeno-associated viral transfer of opioid receptor gene to primary sensory neurons: a strategy to increase opioid antinociception. Proc Natl Acad Sci USA. 2003;100:6204–6209
  42. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain. 1983;16:109–110
  43. Zöllner C, Shaqura MA, Bopaiah CP, Mousa S, Stein C, Schäfer M. Painful inflammation-induced increase in μ-opioid receptor binding and G-protein coupling in primary afferent neurons. Mol Pharmacol. 2003;64:202–210

PII: S0304-3959(03)00485-8

doi: 10.1016/j.pain.2003.12.008

PAIN
Volume 108, Issue 1 , Pages 67-75 , March 2004

Article Tools

* Image Usage & Resolution