Selective impairment of spinal mu-opioid receptor mechanism by plasticity of serotonergic facilitation mediated by 5-HT2A and 5-HT2B receptors

Pain

Volumn 153, Issue 7, 2012, Pages 1418-1425

  Aira, Zigor ^a   Buesa, Itsaso ^a   García Del Caño, Gontzal ^a   Salgueiro, Monika ^a   Mendiable, Nahia ^a   Mingo, Janire ^a   Aguilera, Luciano ^a   Bilbao, Juan ^a   Azkue, Jon Jatsu ^a  

^a UNIVERSITY OF THE BASQUE COUNTRY UPV EHU   (Spain)

Author keywords

Electrophysiology; Immunocytochemistry; Opioid receptors; Protein kinase C; Rat; Serotonin receptors; Spinal cord; Spinal field potentials

Indexed keywords

1 (1 METHYL 5 INDOLYL) 3 (3 METHYL 5 ISOTHIAZOLYL)UREA; 4F 4PP; DELTA OPIATE RECEPTOR; DELTA OPIATE RECEPTOR AGONIST; DELTORPHIN; ENKEPHALIN[2 DEXTRO ALANINE 4 METHYLPHENYLALANINE 5 GLYCINE]; MU OPIATE RECEPTOR; OPIATE; SEROTONIN 2 ANTAGONIST; SEROTONIN 2A ANTAGONIST; SEROTONIN 2A RECEPTOR; SEROTONIN 2B RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN HOMOGENATE; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; EVOKED SPINAL CORD RESPONSE; IC 50; IMMUNOFLUORESCENCE; MALE; NERVE CELL PLASTICITY; NERVE CONDUCTION; NERVE LIGATION; NOCICEPTIVE STIMULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RAT; SEROTONINERGIC NERVE CELL; SPINAL CORD DORSAL HORN; SPINAL NERVE; UPREGULATION; WESTERN BLOTTING;

ANALGESICS, OPIOID; ANIMALS; ENKEPHALIN, ALA(2)-MEPHE(4)-GLY(5)-; MALE; NEURONAL PLASTICITY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, SEROTONIN, 5-HT2A; RECEPTOR, SEROTONIN, 5-HT2B; RECEPTORS, OPIOID, MU; SEROTONIN 5-HT2 RECEPTOR ANTAGONISTS; SPINAL CORD; SYNAPTIC TRANSMISSION;

EID: 84862506576     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1016/j.pain.2012.03.017     Document Type: Article

References (66)

1. Aira Z, Buesa I, Salgueiro M, Bilbao J, Aguilera L, Zimmermann M, Azkue JJ. Subtype-specific changes in 5-HT receptor-mediated modulation of C fibre-evoked spinal field potentials are triggered by peripheral nerve injury. Neuroscience 2010;168:831-41.
2. Ambriz-Tututi M, Cruz SL, Urquiza-Marín H, Granados-Soto V. Formalin-induced long-term secondary allodynia and hyperalgesia are maintained by descending facilitation. Pharmacol Biochem Behav 2011;98:417-24.
3. Angst MS, Clark JD. Opioid-induced hyperalgesia: a qualitative systematic review. Anesthesiology 2006;104:570-87.
4. Arguis MJ, Perez J, Martínez G, Ubre M, Gomar C. Contralateral neuropathic pain following a surgical model of unilateral nerve injury in rats. Reg Anesth Pain Med 2008;33:211-6. (Pubitemid 351539078)
5. Arvanov VL, Liang X, Magro P, Roberts R, Wang RY. A pre- and postsynaptic modulatory action of 5-HT and the 5-HT2A, 2C receptor agonist DOB on NMDA-evoked responses in the rat medial prefrontal cortex. Eur J Neurosci 1999;11:2917-34. (Pubitemid 29364208)
6. Bailey CP, Smith FL, Kelly E, Dewey WL, Henderson G. How important is protein kinase C in mu-opioid receptor desensitization and morphine tolerance? Trends Pharmacol Sci 2006;27:558-65. (Pubitemid 44572396)
7. Ballantyne JC, Shin NS. Efficacy of opioids for chronic pain: a review of the evidence. Clin J Pain 2008;24:469-78.
8. Beck H, Schröck H, Sandkühler J. Controlled superfusion of the rat spinal cord for studying non-synaptic transmission: an autoradiographic analysis. J Neurosci Methods 1995;58:193-202.
9. Blank T, Zwart R, Nijholt I, Spiess J. Serotonin 5-HT2 receptor activation potentiates N-methyl-D-aspartate receptor-mediated ion currents by a protein kinase C-dependent mechanism. J Neurosci Res 1996;45:153-60. (Pubitemid 26257316)
10. Brenner GJ, Ji RR, Shaffer S, Woolf CJ. Peripheral noxious stimulation induces phosphorylation of the NMDA receptor NR1 subunit at the PKC-dependent site, serine-896, in spinal cord dorsal horn neurons. Eur J Neurosci 2004;20:375-84. (Pubitemid 38969623)
11. Buesa I, Ortiz V, Aguilera L, Torre F, Zimmermann M, Azkue JJ. Disinhibition of spinal responses to primary afferent input by antagonism at GABA receptors in urethane-anaesthetised rats is dependent on NMDA and metabotropic glutamate receptors. Neuropharmacology 2006;50:585-94.
12. Buesa I, Urrutia A, Aira Z, Salgueiro M, Bilbao J, Mozas M, Aguilera L, Zimmermann M, Azkue JJ. Depression of C fibre-evoked spinal field potentials by the spinal delta opioid receptor is enhanced in the spinal nerve ligation model of neuropathic pain: involvement of the mu-subtype. Neuropharmacology 2008;55:1376-82.
13. Burgess SE, Gardell LR, Ossipov MH, Malan Jr TP, Vanderah TW, Lai J, Porreca F. Time-dependent descending facilitation from the rostral ventromedial medulla maintains, but does not initiate, neuropathic pain. J Neurosci 2002;22:5129-36. (Pubitemid 37465626)
14. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 1994;53:55-63. (Pubitemid 24238751)
15. Chen HS, Chen J. Secondary heat, but not mechanical, hyperalgesia induced by subcutaneous injection of beevenom in the conscious rat: effect of systemic MK-801, a non-competitive NMDA receptor antagonist. Eur J Pain 2000;4:389-401. (Pubitemid 32104314)
16. Doly S, Madeira A, Fischer J, Brisorgueil MJ, Daval G, Bernard R, Vergé D, Conrath M. The 5-HT2A receptor is widely distributed in the rat spinal cord and mainly localized at the plasma membrane of postsynaptic neurons. J Comp Neurol 2004;472:496-511. (Pubitemid 38508832)
17. Esmaeili-Mahani S, Shimokawa N, Javan M, Maghsoudi N, Motamedi F, Koibuchi N, Ahmadiani A. Low-dose morphine induces hyperalgesia through activation of G alphas, protein kinase C, and L-type Ca 2+ channels in rats. J Neurosci Res 2008;86:471-9. (Pubitemid 351196753)
18. Galeotti N, Stefano GB, Guarna M, Bianchi E, Ghelardini C. Signaling pathway of morphine induced acute thermal hyperalgesia in mice. Pain 2006;123:294-305.
19. Guan Y, Terayama R, Dubner R, Ren K. Plasticity in excitatory amino acid receptor-mediated descending pain modulation after inflammation. J Pharmacol Exp Ther 2002;300:513-20.
20. Guo W, Robbins MT, Wei F, Zou S, Dubner R, Ren K. Supraspinal brain-derived neurotrophic factor signaling: a novel mechanism for descending pain facilitation. J Neurosci 2006;26:126-37. (Pubitemid 43089525)
21. Hong Y, Wang D, Chabot JG, Ma W, Chen P, Quirion R. A role for protein kinase C-dependent upregulation of adrenomedullin in the development of morphine tolerance in male rats. J Neurosci 2010;30:12508-16.
22. Hori Y, Endo K, Takahashi T. Long-lasting synaptic facilitation induced by serotonin in superficial dorsal horn neurons of the rat spinal cord. J Physiol 1996;492:867-76. (Pubitemid 26154370)
23. Hoyer D, Hannon JP, Martin GR. Molecular, pharmacological and functional diversity of 5-HT receptors. Pharmacol Biochem Behav 2002;71:533-54. (Pubitemid 34219205)
24. Kim SH, Chung JM. An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 1992;50:355-63.
25. Kjørsvik A, Størkson R, Tjølsen A, Hole K. Differential effects of activation of lumbar and thoracic 5-HT2A/2C receptors on nociception in rats. Pharmacol Biochem Behav 1997;56:523-7. (Pubitemid 27145835)
26. Kjørsvik Bertelsen A, Warsame Afrah A, Gustafsson H, Tjølsen A, Hole K, Stiller CO. Stimulation of spinal 5-HT(2A/2C) receptors potentiates the capsaicin-induced in vivo release of substance P-like immunoreactivity in the rat dorsal horn. Brain Res 2003;987:10-6. (Pubitemid 37267881)
27. Kramer HK, Simon EJ. Role of protein kinase C (PKC) in agonist-induced muopioid receptor down-regulation: I. PKC translocation to the membrane of SH-SY5Y neuroblastoma cells is induced by mu-opioid agonists. J Neurochem 1999;72:585-93. (Pubitemid 29055220)
28. Kwiat GC, Basbaum AI. The origin of brainstem noradrenergic and serotonergic projections to the spinal cord dorsal horn in the rat. Somatosens Mot Res 1992;9:157-73.
29. Lee JJ, Hahm ET, Min BI, Cho YW. Activation of protein kinase C antagonizes the opioid inhibition of calcium current in rat spinal dorsal horn neurons. Brain Res 2004;1017:108-19.
30. Li P, Kerchner GA, Sala C, Wei F, Huettner JE, Sheng M, Zhuo M. MPA receptor-PDZ interactions in facilitation of spinal sensory synapses. Nat Neurosci 1999;2:972-7. (Pubitemid 30599559)
31. Li Y, Roerig SC. Alteration of spinal protein kinase C expression and kinetics in morphine, but not clonidine, tolerance. Biochem Pharmacol 1999;58:493-501. (Pubitemid 29281551)
32. Lim G, Wang S, Zeng Q, Sung B, Yang L, Mao J. Expression of spinal NMDA receptor and PKCgamma after chronic morphine is regulated by spinal glucocorticoid receptor. J Neurosci 2005;25:11145-54. (Pubitemid 43089559)
33. Lopez-Garcia JA. Serotonergic modulation of spinal sensory circuits. Curr Top Med Chem 2006;6:1987-96. (Pubitemid 44524472)
34. Maeshima T, Ito R, Hamada S, Senzaki K, Hamaguchi-Hamada K, Shutoh F, Okado N. The cellular localization of 5-HT2A receptors in the spinal cord and spinal ganglia of the adult rat. Brain Res 1998;797:118-24. (Pubitemid 28331496)
35. Mao J, Price DD, Phillips LL, Lu J, Mayer DJ. Increases in protein kinase C gamma immunoreactivity in the spinal cord of rats associated with tolerance to the analgesic effects of morphine. Brain Res 1995;677:257-67.
36. Mase H, Sakai A, Sakamoto A, Suzuki H. A subset of l-opioid receptor-expressing cells in the rostral ventromedial medulla contribute to thermal hyperalgesia in experimental neuropathic pain. Neurosci Res 2011;70:35-43.
37. Mayer DJ, Mao J, Price DD. The development of morphine tolerance and dependence is associated with translocation of protein kinase C. Pain 1995;61:365-74.
38. Miki K, Zhou QQ, Guo W, Guan Y, Terayama R, Dubner R, Ren K. Changes in gene expression and neuronal phenotype in brain stem pain modulatory circuitry after inflammation. J Neurophysiol 2002;87:750-60. (Pubitemid 34670842)
39. Mizoguchi H, Wu HE, Narita M, Hall FS, Sora I, Uhl GR, Nagase H, Tseng LF. Antagonistic property of buprenorphine for putative epsilon-opioid receptor-mediated G-protein activation by beta-endorphin in pons/medulla of the muopioid receptor knockout mouse. Neuroscience 2002;115:715-21. (Pubitemid 35336014)
40. Narita M, Narita M, Mizoguchi H, Tseng LF. Inhibition of protein kinase C, but not of protein kinase A, blocks the development of acute antinociceptive tolerance to an intrathecally administered mu-opioid receptor agonist in the mouse. Eur J Pharmacol 1995;280:R1-3.
41. Narita M, Mizoguchi H, Suzuki T, Narita M, Dun NJ, Imai S, Yajima Y, Nagase H, Suzuki T, Tseng LF. Enhanced mu-opioid responses in the spinal cord of mice lacking protein kinase Cgamma isoform. J Biol Chem 2001;276:15409-14.
42. Nishiyama T. Effects of a 5-HT2A receptor antagonist, sarpogrelate on thermal or inflammatory pain. Eur J Pharmacol 2005;516:18-22. (Pubitemid 40780113)
43. Obata H, Saito S, Sasaki M, Ishizaki K, Goto F. Antiallodynic effect of intrathecally administered 5-HT(2) agonists in rats with nerve ligation. Pain 2001;90:173-9. (Pubitemid 32146571)
44. Ossipov MH, Hong Sun T, Malan Jr P, Lai J, Porreca F. Mediation of spinal nerve injury induced tactile allodynia by descending facilitatory pathways in the dorsolateral funiculus in rats. Neurosci Lett 2000;290:129-32. (Pubitemid 30628358)
45. Overland AC, Kitto KF, Chabot-Doré AJ, Rothwell PE, Fairbanks CA, Stone LS, Wilcox GL. Protein kinase C mediates the synergistic interaction between agonists acting at alpha2-adrenergic and delta-opioid receptors in spinal cord. J Neurosci 2009;29:13264-73.
46. Petraschka M, Li S, Gilbert TL, Westenbroek RE, Bruchas MR, Schreiber S, Lowe J, Low MJ, Pintar JE, Chavkin C. The absence of endogenous beta-endorphin selectively blocks phosphorylation and desensitization of mu opioid receptors following partial sciatic nerve ligation. Neuroscience 2007;146:1795-807. (Pubitemid 46783223)
47. Portenoy RK. Management of common opioid side effects during long-term therapy of cancer pain. Ann Acad Med Singapore 1994;23:160-70. (Pubitemid 24160125)
48. Ren K, Dubner R. Pain facilitation and activity-dependent plasticity in pain modulatory circuitry: role of BDNF-TrkB signaling and NMDA receptors. Mol Neurobiol 2007;35:224-35. (Pubitemid 350129684)
49. Rubovitch V, Gafni M, Sarne Y. The mu opioid agonist DAMGO stimulates cAMP production in SK-N-SH cells through a PLC-PKC-Ca++ pathway. Brain Res Mol Brain Res 2003;110:261-6. (Pubitemid 36184698)
50. Shenker NG, Haigh RC, Mapp PI, Harris N, Blake DR. Contralateral hyperalgesia and allodynia following intradermal capsaicin injection in man. Rheumatology (Oxford) 2008;47:1417-21.
51. Skagerberg G, Björklund A. Topographic principles in the spinal projections of serotonergic and non-serotonergic brainstem neurons in the rat. Neuroscience 1985;15:445-80. (Pubitemid 15002128)
52. Terayama R, Guan Y, Dubner R, Ren K. Activity-induced plasticity in brain stem pain modulatory circuitry after inflammation. Neuroreport 2000;11:1915-9. (Pubitemid 30429135)
53. Terayama R, Dubner R, Ren K. The roles of NMDA receptor activation and nucleus reticularis gigantocellularis in the time-dependent changes in descending inhibition after inflammation. Pain 2002;97:171-81. (Pubitemid 34603320)
54. Thibault K, Van Steenwinckel J, Brisorgueil MJ, Fischer J, Hamon M, Calvino B, Conrath M. Serotonin 5-HT2A receptor involvement and Fos expression at the spinal level in vincristine-induced neuropathy in the rat. Pain 2008;140:305-22.
55. Tillu DV, Gebhart GF, Sluka KA. Descending facilitatory pathways from the RVM initiate and maintain bilateral hyperalgesia after muscle insult. Pain 2008;136:331-9.
56. Tsai RY, Tai YH, Tzeng JI, Cherng CH, Yeh CC, Wong CS. Ultra-low dose naloxone restores the antinociceptive effect of morphine in pertussis toxin-treated rats by reversing the coupling of mu-opioid receptors from Gs-protein to coupling to Gi-protein. Neuroscience 2009;164:435-43.
57. Ueda H, Ueda M. Mechanisms underlying morphine analgesic tolerance and dependence. Front Biosci 2009;14:5260-72.
58. Vanderah TW, Suenaga NM, Ossipov MH, Malan Jr TP, Lai J, Porreca F. Tonic descending facilitation from the rostral ventromedial medulla mediates opioid-induced abnormal pain and antinociceptive tolerance. J Neurosci 2001;21:279-86. (Pubitemid 32098751)
59. Vanderah TW, Ossipov MH, Lai J, Malan Jr TP, Porreca F. Mechanisms of opioid-induced pain and antinociceptive tolerance. Descending facilitation and spinal dynorphin. Pain 2001;92:5-9. (Pubitemid 32367931)
60. Van Steenwinckel J, Brisorgueil MJ, Fischer J, Vergé D, Gingrich JA, Bourgoin S, Hamon M, Bernard R, Conrath M. Role of spinal serotonin 5-HT2A receptor in 2′,3′-dideoxycytidine-induced neuropathic pain in the rat and the mouse. Pain 2008;137:66-80. (Pubitemid 351802242)
61. Wang YY, Wei YY, Huang J, Wang W, Tamamaki N, Li YQ, Wu SX. Expression patterns of 5-HT receptor subtypes 1A and 2A on GABAergic neurons within the spinal dorsal horn of GAD67-GFP knock-in mice. J Chem Neuroanat 2009;38:75-81.
62. Wei F, Dubner R, Zou S, Ren K, Bai G, Wei D, Guo W. Molecular depletion of descending serotonin unmasks its novel facilitatory role in the development of persistent pain. J Neurosci 2010;30:8624-36.
63. Willis WD. Role of neurotransmitters in sensitization of pain responses. Ann NY Acad Sci 2001;933:142-56.
64. Zhang LJ, Wang XJ, Han JS. Phorbol ester suppression of opioid analgesia in rats. Life Sci 1990;47:1775-82. (Pubitemid 20374732)
65. Zhuo M. Silent glutamatergic synapses and long-term facilitation in spinal dorsal horn neurons. Prog Brain Res 2000;129:101-13. (Pubitemid 35461188)
66. Zimmermann M. Pathobiology of neuropathic pain. Eur J Pharmacol 2001;429:23-37. (Pubitemid 33043979)