Fentanyl decreases discharges of C and A nociceptors to suprathreshold mechanical stimulation in chronic inflammation

Journal of Neurophysiology

Volumn 108, Issue 10, 2012, Pages 2827-2836

  Moshourab, Rabih ^a   Stein, Christoph ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Inflammation; Nociceptor; Opioids; Peripheral

Indexed keywords

FENTANYL CITRATE; NALOXONE;

A FIBER NOCICEPTOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; C FIBER NOCICEPTOR; CHRONIC PAIN; CONTROLLED STUDY; HYPERALGESIA; IN VITRO STUDY; MALE; NERVE CELL EXCITABILITY; NOCICEPTION; NOCICEPTIVE STIMULATION; NONHUMAN; PAIN RECEPTOR; PAIN THRESHOLD; PRIORITY JOURNAL; RAT;

ACTION POTENTIALS; ANALGESICS, OPIOID; ANIMALS; FENTANYL; FREUND'S ADJUVANT; HINDLIMB; INFLAMMATION; MALE; MECHANORECEPTORS; NERVE FIBERS; NOCICEPTORS; RATS; RATS, WISTAR; SENSORY THRESHOLDS; SKIN; TOUCH;

EID: 84869167187     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00082.2012     Document Type: Article

References (75)

1. Andreev N, Urban L, Dray A. Opioids suppress spontaneous activity of polymodal nociceptors in rat paw skin induced by ultraviolet irradiation. Neuroscience 58: 793-798, 1994.
2. Andrew D, Greenspan JD. Mechanical and heat sensitization of cutaneous nociceptors after peripheral inflammation in the rat. J Neurophysiol 82: 2649-2656, 1999.
3. Antonijevic I, Mousa SA, Schäfer M, Stein C. Perineurial defect and peripheral opioid analgesia in inflammation. J Neurosci 15: 165-172, 1995.
4. Banik RK, Brennan TJ. Sensitization of primary afferents to mechanical and heat stimuli after incision in a novel in vitro mouse glabrous skin-nerve preparation. Pain 138: 380-391, 2008.
5. Baumann TK, Simone DA, Shain CN, LaMotte RH. Neurogenic hyperalgesia: the search for the primary cutaneous afferent fibers that contribute to capsaicininduced pain and hyperalgesia. J Neurophysiol 66: 212-227, 1991.
6. Brack A, Rittner HL, Machelska H, Shaqura M, Mousa SA, Labuz D, Zöllner C, Schäfer M, Stein C. Endogenous peripheral antinociception in early inflammation is not limited by the number of opioid-containing leukocytes but by opioid receptor expression. Pain 108: 67-75, 2004.
7. Brennan TJ, Vandermeulen EP, Gebhart GF. Characterization of a rat model of incisional pain. Pain 64: 493-501, 1996.
8. Busch-Dienstfertig M, Stein C. Opioid receptors and opioid peptide-producing leukocytes in inflammatory pain-basic and therapeutic aspects. Brain Behav Immun 24: 683-694, 2010.
9. Búzás B, Cox BM. Quantitative analysis of mu and delta opioid receptor gene expression in rat brain and peripheral ganglia using competitive polymerase chain reaction. Neuroscience 76: 479-489, 1997.
10. Coggeshall RE, Zhou S, Carlton SM. Opioid receptors on peripheral sensory axons. Brain Res 764: 126-132, 1997.
11. Djouhri L, Koutsikou S, Fang X, McMullan S, Lawson SN. Spontaneous pain, both neuropathic and inflammatory, is related to frequency of spontaneous firing in intact C-fiber nociceptors. J Neurosci 26: 1281-1292, 2006.
12. Djouhri L, Lawson SN. Abeta-fiber nociceptive primary afferent neurons: a review of incidence and properties in relation to other afferent A-fiber neurons in mammals. Brain Res Brain Res Rev 46: 131-145, 2004.
13. Du J, Zhou S, Coggeshall R, Carlton S. N-methyl-D-aspartate-induced excitation and sensitization of normal and inflamed nociceptors. Neuroscience 118: 547-562, 2003.
14. Fraser GL, Gaudreau G, Clarke PBS, Ménard DP, Perkins MN. Antihyperalgesic effects of δ opioid agonists in a rat model of chronic inflammation. Br J Pharmacol 129: 1668-1672, 2000.
15. Garell PC, McGillis SL, Greenspan JD. Mechanical response properties of nociceptors innervating feline hairy skin. J Neurophysiol 75: 1177-1189, 1996.
16. Gebhart GF, Su X, Joshi S, Ozaki N, Sengupta JN. Peripheral opioid modulation of visceral pain. Ann N Y Acad Sci 909: 41-50, 2000.
17. Gold MS, Gebhart GF. Nociceptor sensitization in pain pathogenesis. Nat Med 16: 1248-1257, 2010.
18. Grant GJ, Vermeulen K, Zakowski MI, Langerman L. Perineural antinociceptive effect of opioids in a rat model. Acta Anaesthesiol Scand 45: 906-910, 2001.
19. Hämäläinen MM, Gebhart GF, Brennan TJ. Acute effect of an incision on mechanosensitive afferents in the plantar rat hindpaw. J Neurophysiol 87: 712-720, 2002.
20. Handwerker HO, Anton F, Kocher L, Reeh PW. Nociceptor functions in intact skin and in neurogenic or non-neurogenic inflammation. Acta Physiol Hung 69: 333-342, 1987.
21. Handwerker HO, Kilo S, Reeh PW. Unresponsive afferent nerve fibres in the sural nerve of the rat. J Physiol 435: 229-242, 1991.
22. Hassan AHS, 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 55: 185-195, 1993.
23. Iadarola MJ, Brady LS, Draisci G, Dubner R. Enhancement of dynorphin gene expression in spinal cord following experimental inflammation: stimulus specificity, behavioral parameters and opioid receptor binding. Pain 35: 313-326, 1988.
24. Jaffe RA, Rowe MA. A comparison of the local anesthetic effects of meperidine, fentanyl, and sufentanil on dorsal root axons. Anesth Analg 83: 776-781, 1996.
25. Kocher L, Anton F, Reeh PW, Handwerker HO. The effect of carrageenaninduced inflammation on the sensitivity of unmyelinated skin nociceptors in the rat. Pain 29: 363-373, 1987.
26. Kress M, Koltzenburg M, Reeh PW, Handwerker HO. Responsiveness and functional attributes of electrically localized terminals of cutaneous C-fibers in vivo and in vitro. J Neurophysiol 68: 581-595, 1992.
27. Lechner SG, Lewin GR. Peripheral sensitisation of nociceptors via Gproteindependent potentiation of mechanotransduction currents. J Physiol 587: 3493-3503, 2009.
28. Leem JW, Willis WD, Chung JM. Cutaneous sensory receptors in the rat foot. J Neurophysiol 69: 1684-1699, 1993.
29. Lewin GR, Moshourab R. Mechanosensation and pain. J Neurobiol 61: 30-44, 2004.
30. Li JL, Ding YQ, Li YQ, Li JS, Nomura S, Kaneko T, Mizuno N. Immunocytochemical localization of mu-opioid receptor in primary afferent neurons containing substance P or calcitonin gene-related peptide. A light and electron microscope study in the rat. Brain Res 794: 347-352, 1998.
31. Lynn B, Carpenter SE. Primary afferent units from the hairy skin of the rat hind limb. Brain Res 238: 29-43, 1982.
32. Maekawa K, Minami M, Yabuuchi K, Toya T, Katao Y, Hosoi Y, Onogi T, Satoh M. In situ hybridization study of mu-and kappa-opioid receptor mRNAs in the rat spinal cord and dorsal root ganglia. Neurosci Lett 168: 97-100, 1994.
33. Mantyh PW. Cancer pain and its impact on diagnosis, survival and quality of life. Nat Rev Neurosci 7: 797-809, 2006.
34. Meyer RA, Davis KD, Cohen RH, Treede RD, Campbell JN. Mechanically insensitive afferents (MIAs) in cutaneous nerves of monkey. Brain Res 561: 252-261, 1991.
35. Milenkovic N, Wetzel C, Moshourab R, Lewin GR. Speed and temperature dependences of mechanotransduction in afferent fibers recorded from the mouse saphenous nerve. J Neurophysiol 100: 2771-2783, 2008.
36. Mousa SA, Cheppudira BP, Shaqura M, Fischer O, Hofmann J, Hellweg R, Schäfer M. Nerve growth factor governs the enhanced ability of opioids to suppress inflammatory pain. Brain 130: 502-513, 2007.
37. 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 126: 5-15, 2002.
38. Newbould BB. Chemotherapy of arthritis induced in rats by mycobacterial adjuvant. Br J Pharmacol Chemother 21: 127-136, 1963.
39. Olausson H, Wessberg J, Morrison I, McGlone F, Vallbo A. The neurophysiology of unmyelinated tactile afferents. Neurosci Biobehav Rev 34: 185-191, 2010.
40. Picard PR, Tramèr MR, McQuay HJ, Moore RA. Analgesic efficacy of peripheral opioids (all except intra-articular): a qualitative systematic review of randomised controlled trials. Pain 72: 309-318, 1997.
41. Pogatzki EM, Gebhart GF, Brennan TJ. Characterization of Aδ-and C-fibers innervating the plantar rat hindpaw one day after an incision. J Neurophysiol 87: 721-731, 2002.
42. Puehler W, Rittner HL, Mousa SA, Brack A, Krause H, Stein C, Schäfer M. Interleukin-1 beta contributes to the upregulation of kappa opioid receptor mrna in dorsal root ganglia in response to peripheral inflammation. Neuroscience 141: 989-998, 2006.
43. Puehler W, Zöllner C, Brack A, Shaqura MA, Krause H, Schäfer M, Stein C. Rapid upregulation of δ opioid receptor mrna in dorsal root ganglia in response to peripheral inflammation depends on neuronal conduction. Neuroscience 129: 473-479, 2004.
44. Reeh PW. Sensory receptors in mammalian skin in an in vitro preparation. Neurosci Lett 66: 141-146, 1986.
45. Reeh PW, Bayer J, Kocher L, Handwerker HO. Sensitization of nociceptive cutaneous nerve fibers from the rat's tail by noxious mechanical stimulation. Exp Brain Res 65: 505-512, 1987.
46. Rittner HL, Brack A, Machelska H, Mousa SA, Bauer M, Schäfer M, Stein C. Opioid peptide-expressing leukocytes: identification, recruitment, and simultaneously increasing inhibition of inflammatory pain. Anesthesiology 95: 500-508, 2001.
47. Rittner HL, Hackel D, Yamdeu RS, Mousa SA, Stein C, Schäfer M, Brack A. Antinociception by neutrophil-derived opioid peptides in noninflamed tissue-role of hypertonicity and the perineurium. Brain Behav Immun 23: 548-557, 2009.
48. Rukwied R, Dusch M, Schley M, Forsch E, Schmelz M. Nociceptor sensitization to mechanical and thermal stimuli in pig skin in vivo. Eur J Pain 12: 242-250, 2008.
49. 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 91: 4219-4223, 1994.
50. Schaible HG, Richter F, Ebersberger A, Boettger MK, Vanegas H, Natura G, Vazquez E, Segond von Banchet G. Joint pain. Exp Brain Res 196: 153-162, 2009.
51. Scherrer G, Imamachi N, Cao YQ, Contet C, Mennicken F, O'Donnell D, Kieffer BL, Basbaum AI. Dissociation of the opioid receptor mechanisms that control mechanical and heat pain. Cell 137: 1148-1159, 2009.
52. Schmelz M, Schmid R, Handwerker HO, Torebjörk HE. Encoding of burning pain from capsaicin-treated human skin in two categories of unmyelinated nerve fibres. Brain 123: 560-571, 2000.
53. Schmelz M, Schmidt R, Ringkamp M, Handwerker HO, Torebjörk HE. Sensitization of insensitive branches of C nociceptors in human skin. J Physiol 480: 389-394, 1994.
54. Schmidt R, Schmelz M, Forster C, Ringkamp M, Torebjork E, Handwerker H. Novel classes of responsive and unresponsive C nociceptors in human skin. J Neurosci 15: 333-341, 1995.
55. Schmidt R, Schmelz M, Torebjörk HE, Handwerker HO. Mechanoinsensitive nociceptors encode pain evoked by tonic pressure to human skin. Neuroscience 98: 793-800, 2000.
56. Senami M, Aoki M, Kitahata LM, Collins JG, Kumeta Y, Murata K. Lack of opiate effects on cat C polymodal nociceptive fibers. Pain 27: 81-90, 1986.
57. Silbert SC, Beacham DW, McCleskey EW. Quantitative single-cell differences in δ-opioid receptor mRNA distinguish myelinated and unmyelinated nociceptors. J Neurosci 23: 34-42, 2003.
58. Slugg RM, Meyer RA, Campbell JN. Response of cutaneous A-and C-fiber nociceptors in the monkey to controlled-force stimuli. J Neurophysiol 83: 2179-2191, 2000.
59. Steen K, Reeh P, Anton F, Handwerker H. Protons selectively induce lasting excitation and sensitization to mechanical stimulation of nociceptors in rat skin, in vitro. J Neurosci 12: 86-95, 1992.
60. Steen KH, Steen AE, Kreysel HW, Reeh PW. Inflammatory mediators potentiate pain induced by experimental tissue acidosis. Pain 66: 163-170, 1996.
61. Stein C. The control of pain in peripheral tissue by opioids. N Engl J Med 332: 1685-1690, 1995.
62. Stein C, Gramsch C, Herz A. Intrinsic mechanisms of antinociception in inflammation: local opioid receptors and beta-endorphin. J Neurosci 10: 1292-1298, 1990a.
63. Stein C, Hassan AH, Przewłocki 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 87: 5935-5939, 1990b.
64. Stein C, Millan MJ, Herz A. Unilateral inflammation of the hindpaw in rats as a model of prolonged noxious stimulation: alterations in behavior and nociceptive thresholds. Pharmacol Biochem Behav 31: 445-451, 1988a.
65. Stein C, Millan MJ, Shippenberg TS, Herz A. Peripheral effect of fentanyl upon nociception in inflamed tissue of the rat. Neurosci Lett 84: 225-228, 1988b.
66. Stein C, Schäfer M, Machelska H. Attacking pain at its source: new perspectives on opioids. Nat Med 9: 1003-1008, 2003.
67. Treede RD, Meyer RA, Campbell JN. Myelinated mechanically insensitive afferents from monkey hairy skin: heat-response properties. J Neurophysiol 80: 1082-1093, 1998.
68. Wang H, Wessendorf MW. Equal proportions of small and large DRG neurons express opioid receptor mRNAs. J Comp Neurol 429: 590-600, 2001.
69. Wang HB, Zhao B, Zhong YQ, Li KC, Li ZY, Wang Q, Lu YJ, Zhang ZN, He SQ, Zheng HC, Wu SX, Hökfelt TGM, Bao L, Zhang X. Coexpression of δ-and μ-opioid receptors in nociceptive sensory neurons. Proc Natl Acad Sci USA 107: 13117-13122, 2010.
70. Wenk HN, Brederson JD, Honda CN. Morphine directly inhibits nociceptors in inflamed skin. J Neurophysiol 95: 2083-2097, 2006.
71. Wilder-Smith OH, Schreyer T, Scheffer GJ, Arendt-Nielsen L. Patients with chronic pain after abdominal surgery show less preoperative endogenous pain inhibition and more postoperative hyperalgesia: a pilot study. J Pain Palliat Care Pharmacother 24: 119-128, 2010.
72. Woolf CJ, Salter MW. Neuronal plasticity: increasing the gain in pain. Science 288: 1765-1769, 2000.
73. Xiao WH, Bennett GJ. Persistent low-frequency spontaneous discharge in A-fiber and C-fiber primary afferent neurons during an inflammatory pain condition. Anesthesiology 107: 813-821, 2007.
74. Yuge O, Matsumoto M, Kitahata LM, Collins JG, Senami M. Direct opioid application to peripheral nerves does not alter compound action potentials. Anesth Analg 64: 667-671, 1985.
75. Zimmermann K, Hein A, Hager U, Kaczmarek JS, Turnquist BP, Clapham DE, Reeh PW. Phenotyping sensory nerve endings in vitro in the mouse. Nat Protoc 4: 174-196, 2009.