Increased spinal dynorphin levels and phospho-extracellular signal-regulated kinases 1 and 2 and c-Fos immunoreactivity after surgery under remifentanil anesthesia in mice

Molecular Pharmacology

Volumn 77, Issue 2, 2010, Pages 185-194

  Campillo, Ana ^a   González Cuello, Ana ^b   Cabañero, David ^a   Garcia Nogales, Paula ^a   Romero, Asunción ^a   Milanés, M Victoria ^b   Laorden, M Luisa ^b   Puig, Margarita M ^a  

^a UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

^b UNIVERSITY OF MURCIA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

DYNORPHIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PRODYNORPHIN; PROTEIN C FOS; REMIFENTANIL; SEVOFLURANE;

ALLODYNIA; ANESTHESIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG MECHANISM; ENZYME ACTIVATION; ENZYME IMMUNOASSAY; ENZYME PHOSPHORYLATION; GENETIC TRANSCRIPTION; HEAT; HEATING; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INCISION; LUMBAR SPINAL CORD; MALE; MOUSE; NONHUMAN; PAIN; PAIN THRESHOLD; POSTOPERATIVE PERIOD; PRIORITY JOURNAL; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; SENSITIZATION; SPINAL CORD DORSAL HORN; UPREGULATION;

ANESTHETICS, INTRAVENOUS; ANIMALS; DYNORPHINS; GENES, FOS; MALE; MICE; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; PAIN MEASUREMENT; PAIN, POSTOPERATIVE; PIPERIDINES; SPINAL CORD;

EID: 74549139833     PISSN: 0026895X     EISSN: 15210111     Source Type: Journal    
DOI: 10.1124/mol.109.059790     Document Type: Article

References (46)

1. Angst MS and Clark JD (2006) Opioid-induced hyperalgesia: a qualitative systematic review. Anesthesiology 104:570-587.
2. Angst MS, Koppert W, Pahl I, Clark DJ, and Schmelz M (2003) Short-term infusion of the mu-opioid agonist remifentanil in humans causes hyperalgesia during withdrawal. Pain 106:49-57.
3. Beitz AJ, Newman A, Kahn AR, Ruggles T, and Eikmeier L (2004) A polymeric membrane dressing with antinociceptive properties: analysis with a rodent model of stab wound secondary hyperalgesia. J Pain 5:38-47.
4. Benavides M, Laorden ML, Marín MT, and Milanés MV (2005) Role of PKCalpha, gamma isoforms in regulation of c-Fos and TH expression after naloxoneinduced morphine withdrawal in the hypothalamic PVN and medulla oblongata catecholaminergic cell groups. J Neurochem 95:1249-1258.
5. Brennan TJ, Vandermeulen EP, and Gebhart GF (1996) Characterization of a rat model of incisional pain. Pain 64:493-501.
6. Cabañero D, Campillo A, Célérier E, Romero A, and Puig MM (2009a) Pronociceptive effects of remifentanil in a mouse model of postsurgical pain: effect of a second surgery. Anesthesiology 111:1334-1345.
7. Cabañero D, Célérier E, García-Nogales P, MataM, Roques BP, Maldonado R, and Puig MM (2009b) The pro-nociceptive effects of remifentanil or surgical injury in mice are associated with a decrease in delta-opioid receptor mRNA levels: Prevention of the nociceptive response by on-site delivery of enkephalins. Pain 141:88-96.
8. Célérier E, González JR, Maldonado R, Cabañero D, and Puig MM (2006) Opioidinduced hyperalgesia in a murine model of postoperative pain: role of nitric oxide generated from the inducible nitric oxide synthase. Anesthesiology 104:546-555.
9. Chaplan SR, Bach FW, Pogrel JW, Chung JM, and Yaksh TL (1994) Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 53:55-63.
10. Coggeshall RE (2005) Fos, nociception and the dorsal horn. Prog Neurobiol 77:299-352.
11. Costigan M and Woolf CJ (2002) No DREAM, No pain. Closing the spinal gate. Cell 108:297-300.
12. Crown ED, Ye Z, Johnson KM, Xu GY, McAdoo DJ, and Hulsebosch CE (2006) Increases in the activated forms of ERK 1/2, p38 MAPK, and CREB are correlated with the expression of at-level mechanical allodynia following spinal cord injury. Exp Neurol 199:397-407.
13. Cruz CD, Ferreira D, McMahon SB, and Cruz F (2007) The activation of the ERK pathway contributes to the spinal c-fos expression observed after noxious bladder stimulation. Somatosens Mot Res 24:15-20.
14. Dubner R and Ruda MA (1992) Activity-dependent neuronal plasticity following tissue injury and inflammation. Trends Neurosci 15:96-103.
15. Gao YJ and Ji RR (2009) c-Fos and pERK, which is a better marker for neuronal activation and central sensitization after noxious stimulation and tissue injury? Open Pain J 2:11-17.
16. Gardell LR, King T, Ossipov MH, Rice KC, Lai J, Vanderah TW, and Porreca F (2006) Opioid receptor-mediated hyperalgesia and antinociceptive tolerance induced by sustained opiate delivery. Neurosci Lett 396:44-49.
17. González-Cuello A, Sánchez L, Hernández J, Teresa Castells M, Victoria Milanés M, and Laorden ML (2007) Phosphodiesterase 4 inhibitors, rolipram and diazepam block the adaptive changes observed during morphine withdrawal in the heart. Eur J Pharmacol 570:1-9.
18. Hargreaves K, Dubner R, Brown F, Flores C, and Joris J (1988) A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32: 77-88.
19. Harris JA (1998) Using c-fos as a neural marker of pain. Brain Res Bull 45:1-8.
20. Hunt SP, Pini A, and Evan G (1987) Induction of c-fos-like protein in spinal cord neurons following sensory stimulation. Nature 328:632-634.
21. Hunter JC, Woodburn VL, Durieux C, Pettersson EK, Poat JA, and Hughes J (1995) c-fos antisense oligodeoxynucleotide increases formalin-induced nociception and regulates preprodynorphin expression. Neuroscience 65:485-492.
22. Institute of Laboratory Animal Resources (1996) Guide for the Care and Use of Laboratory Animals 7th ed. Institute of Laboratory Animal Resources, Commission on Life Sciences, National Research Council, Washington DC.
23. Ji RR, Baba H, Brenner GJ, and Woolf CJ (1999) Nociceptive-specific activation of ERK in spinal neurons contributes to pain hypersensitivity. Nat Neurosci 2:1114-1119.
24. Ji RR, Befort K, Brenner GJ, and Woolf CJ (2002) ERK MAP kinase activation in superficial spinal cord neurons induces prodynorphin and NK-1 upregulation and contributes to persistent inflammatory pain hypersensitivity. J Neurosci 22:478-485.
25. Ji RR, Gereau RW 4th, Malcangio M, and Strichartz GR (2009) MAP kinase and pain. Brain Res Rev 60:135-148.
26. Ji RR and Rupp F (1997) Phosphorylation of transcription factor CREB in rat spinal cord after formalin-induced hyperalgesia: relationship to c-fos induction. J Neurosci 17:1776-1785.
27. Joly V, Richebe P, Guignard B, Fletcher D, Maurette P, Sessler DI, and Chauvin M (2005) Remifentanil-induced postoperative hyperalgesia and its prevention with small-dose ketamine. Anesthesiology 103:147-155.
28. Kawasaki Y, Kohno T, Zhuang ZY, Brenner GJ, Wang H, Van Der Meer C, Befort K, Woolf CJ, and Ji RR (2004) Ionotropic and metabotropic receptors, protein kinase A, protein kinase C, and Src contribute to C-fiber-induced ERK activation and cAMP response element-binding protein phosphorylation in dorsal horn neurons, leading to central sensitization. J Neurosci 24:8310-8321.
29. Komatsu T, Sakurada C, Sasaki M, Sanai K, Tsuzuki M, Bagetta G, Sakurada S, and Sakurada T (2007) Extracellular signal-regulated kinase (ERK) and nitric oxide synthase mediate intrathecal morphine-induced nociceptive behavior. Neuropharmacology 52:1237-1243.
30. Kominato Y, Tachibana T, Dai Y, Tsujino H, Maruo S, and Noguchi K (2003) Changes in phosphorylation of ERK and Fos expression in dorsal horn neurons following noxious stimulation in a rat model of neuritis of the nerve root. Brain Res 967:89-97.
31. Lai J, Luo MC, Chen Q, Ma S, Gardell LR, Ossipov MH, and Porreca F (2006) Dynorphin A activates bradykinin receptors to maintain neuropathic pain. Nat Neurosci 9:1534-1540.
32. Lai J, Ossipov MH, Vanderah TW, Malan TP Jr, and Porreca F (2001) Neuropathic pain: the paradox of dynorphin. Mol Interv 1:160-167.
33. Le Guen S, Catheline G, and Besson JM (1998) Development of tolerance to the antinociceptive effect of systemic morphine at the lumbar spinal cord level: a c-Fos study in the rat. Brain Res 813:128-138.
34. Li X, Angst MS, and Clark JD (2001) A murine model of opioid-induced hyperalgesia. Brain Res Mol Brain Res 86:56-62.
35. Lonze BE and Ginty DD (2002) Function and regulation of CREB family transcription factors in the nervous system. Neuron 35:605-623.
36. Ma W and Eisenach JC (2003) Intraplantar injection of a cyclooxygenase inhibitor ketorolac reduces immunoreactivities of substance P, calcitonin gene-related peptide, and dynorphin in the dorsal horn of rats with nerve injury or inflammation. Neuroscience 121:681-690.
37. Pfaffl MW, Horgan GW, and Dempfle L(2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:e36.
38. Rivat C, Vera-Portocarrero LP, Ibrahim MM, Mata HP, Stagg NJ, De Felice M, Porreca F, and Malan TP (2009) Spinal NK-1 receptor-expressing neurons and descending pathways support fentanyl-induced pain hypersensitivity in a rat model of postoperative pain. Eur J Neurosci 29:727-737.
39. Schwei MJ, Honore P, Rogers SD, Salak-Johnson JL, Finke MP, Ramnaraine ML, Clohisy DR, and Mantyh PW (1999) Neurochemical and cellular reorganization of the spinal cord in a murine model of bone cancer pain. J Neurosci 19:10886-10897.
40. Svensson CI, Fitzsimmons B, Azizi S, Powell HC, Hua XY, and Yaksh TL (2005) Spinal p38beta isoform mediates tissue injury-induced hyperalgesia and spinal sensitization. J Neurochem 92:1508-1520.
41. Tan-No K, Esashi A, Nakagawasai O, Niijima F, Tadano T, Sakurada C, Sakurada T, Bakalkin G, Terenius L, and Kisara K (2002) Intrathecally administered big dynorphin, a prodynorphin-derived peptide, produces nociceptive behavior through an N-methyl-D-aspartate receptor mechanism. Brain Res 952:7-14.
42. Vanderah TW, Ossipov MH, Lai J, Malan TP Jr, and Porreca F (2001) Mechanisms of opioid-induced pain and antinociceptive tolerance: descending facilitation and spinal dynorphin. Pain 92:5-9.
43. Vera-Portocarrero LP, Zhang ET, King T, Ossipov MH, Vanderah TW, Lai J, and Porreca F (2007) Spinal NK-1 receptor expressing neurons mediate opioid-induced hyperalgesia and antinociceptive tolerance via activation of descending pathways. Pain 129:35-45.
44. Wang Z, Gardell LR, Ossipov MH, Vanderah TW, Brennan MB, Hochgeschwender U, Hruby VJ, Malan TP Jr, Lai J, and Porreca F (2001) Pronociceptive actions of dynorphin maintain chronic neuropathic pain. J Neurosci 21:1779-1786.
45. Zhang XJ, Li Z, Chung EK, Zhang HQ, Xu HX, Sung JJ, and Bian ZX (2009) Activation of extracellular signal-regulated protein kinase is associated with colorectal distension-induced spinal and supraspinal neuronal response and neonatal maternal separation-induced visceral hyperalgesia in rats. J Mol Neurosci 37:274-287.
46. Zhu X, Vincler MA, Parker R, and Eisenach JC (2006) Spinal cord dynorphin expression increases, but does not drive microglial prostaglandin production or mechanical hypersensitivity after incisional surgery in rats. Pain 125:43-52.