Analgesic antidepressants promote the responsiveness of locus coeruleus neurons to noxious stimulation: Implications for neuropathic pain

Pain

Volumn 153, Issue 7, 2012, Pages 1438-1449

  Alba Delgado, Cristina ^a,b   Mico, Juan Antonio ^a,b   Sánchez Blázquez, Pilar ^b,c   Berrocoso, Esther ^a,b  

^a UNIVERSITY OF CÁDIZ   (Spain)

^b CENTRO DE INVESTIGACIÓN BIOMÉDICA EN RED DE SALUD MENTAL CIBERSAM   (Spain)

^c INSTITUTO CAJAL   (Spain)

Author keywords

Desipramine; Duloxetine; Electrophysiology; Locus coeruleus; Neuropathic pain; Noxious stimulation

Indexed keywords

ALPHA 2 ADRENERGIC RECEPTOR; CAPSAICIN; DESIPRAMINE; DULOXETINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

AFFERENT NERVE GROUP 1; ANALGESIC ACTIVITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BRAIN NERVE CELL; CHRONIC CONSTRICTION INJURY; CONTROLLED STUDY; EVOKED SOMATOSENSORY RESPONSE; LOCUS CERULEUS; MALE; MYELINATED NERVE; NEUROPATHIC PAIN; NOCICEPTION; NOCICEPTIVE STIMULATION; NONHUMAN; NONMYELINATED NERVE; PRIORITY JOURNAL; RAT; SCIATIC NERVE;

ANALGESICS; ANIMALS; ANTIDEPRESSIVE AGENTS; DISEASE MODELS, ANIMAL; LOCUS COERULEUS; MALE; N-METHYLASPARTATE; NEURALGIA; NEURONS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ADRENERGIC, ALPHA-2; SPINAL CORD;

EID: 84862494075     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1016/j.pain.2012.03.034     Document Type: Article

References (55)

1. Aghajanian GK, Cedarbaum JM, Wang RY. Evidence for norepinephrine- mediated collateral inhibition of locus coeruleus neurons. Brain Res 1977;136:570-7. (Pubitemid 8228265)
2. Alba-Delgado C, Borges G, Sanchez-Blazquez P, Ortega JE, Horrillo I, Mico JA, Meana JJ, Neto F, Berrocoso E. The function of alpha-2-adrenoceptors in the rat locus coeruleus is preserved in the chronic constriction injury model of neuropathic pain. Psychopharmacology (Berl) 2011 [Epub ahead of print].
3. Andrade R, Aghajanian GK. Locus coeruleus activity in vitro: intrinsic regulation by a calcium-dependent potassium conductance but not alpha 2-adrenoceptors. J Neurosci 1984;4:161-70. (Pubitemid 14198297)
4. Aston-Jones G, Cohen JD. An integrative theory of locus coeruleusnorepinephrine function: adaptive gain and optimal performance. Annu Rev Neurosci 2005;28:403-50. (Pubitemid 41098911)
5. Bennett GJ, Xie YK. A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 1988;33:87-107.
6. Berrocoso E, De Benito MD, Mico JA. Role of serotonin 5-HT1A and opioid receptors in the antiallodynic effect of tramadol in the chronic constriction injury model of neuropathic pain in rats. Psychopharmacology (Berl) 2007;193:97-105. (Pubitemid 46906628)
7. Berrocoso E, Mico JA. In vivo effect of venlafaxine on locus coeruleus neurons: role of opioid, alpha(2)-adrenergic, and 5-hydroxytryptamine(1A) receptors. J Pharmacol Exp Ther 2007;322:101-7. (Pubitemid 46956369)
8. Berrocoso E, Mico JA, Ugedo L. In vivo effect of tramadol on locus coeruleus neurons is mediated by alpha2-adrenoceptors and modulated by serotonin. Neuropharmacology 2006;51:146-53.
9. Berrocoso E, Mico JA, Vitton O, Ladure P, Newman-Tancredi A, Depoortere R, Bardin L. Evaluation of milnacipran, in comparison with amitriptyline, on cold and mechanical allodynia in a rat model of neuropathic pain. Eur J Pharmacol 2011;655:46-51.
10. Bobula B, Hess G. Antidepressant treatments-induced modifications of glutamatergic transmission in rat frontal cortex. Pharmacol Rep 2008;60:865-71.
11. Brightwell JJ, Taylor BK. Noradrenergic neurons in the locus coeruleus contribute to neuropathic pain. Neuroscience 2009;160:174-85.
12. Cedarbaum JM, Aghajanian GK. Noradrenergic neurons of the locus coeruleus: inhibition by epinephrine and activation by the alpha-antagonist piperoxane. Brain Res 1976;112:413-9.
13. Chiang C, Aston-Jones G. Response of locus coeruleus neurons to footshock stimulation is mediated by neurons in the rostral ventral medulla. Neuroscience 1993;53:705-15. (Pubitemid 23114559)
14. Clark FM, Yeomans DC, Proudfit HK. The noradrenergic innervation of the spinal cord: differences between two substrains of Sprague-Dawley rats determined using retrograde tracers combined with immunocytochemistry. Neurosci Lett 1991;125:155-8.
15. Ennis M, Aston-Jones G. Evidence for self- and neighbor-mediated postactivation inhibition of locus coeruleus neurons. Brain Res 1986;374:299-305. (Pubitemid 16077981)
16. Finnerup NB, Otto M, McQuay HJ, Jensen TS, Sindrup SH. Algorithm for neuropathic pain treatment: an evidence based proposal. Pain 2005;118:289-305. (Pubitemid 41752987)
17. Florin-Lechner SM, Druhan JP, Aston-Jones G, Valentino RJ. Enhanced norepinephrine release in prefrontal cortex with burst stimulation of the locus coeruleus. Brain Res 1996;742:89-97. (Pubitemid 27016011)
18. Garzon J, Rodriguez-Munoz M, Lopez-Fando A, Sanchez-Blazquez P. Activation of mu-opioid receptors transfers control of Galpha subunits to the regulator of G-protein signaling RGS9-2: role in receptor desensitization. J Biol Chem 2005;280:8951-60. (Pubitemid 40409587)
19. Goldstein DJ, Lu Y, Detke MJ, Lee TC, Iyengar S. Duloxetine vs. placebo in patients with painful diabetic neuropathy. Pain 2005;116:109-18. (Pubitemid 40828506)
20. Grace AA, Bunney BS. The control of firing pattern in nigral dopamine neurons: burst firing. J Neurosci 1984;4:2877-90. (Pubitemid 15224432)
21. Grandoso L, Pineda J, Ugedo L. Comparative study of the effects of desipramine and reboxetine on locus coeruleus neurons in rat brain slices. Neuropharmacology 2004;46:815-23. (Pubitemid 38368914)
22. Grant MM, Weiss JM. Effects of chronic antidepressant drug administration and electroconvulsive shock on locus coeruleus electrophysiologic activity. Biol Psychiatry 2001;49:117-29. (Pubitemid 32120159)
23. Hargreaves K, Dubner R, Brown F, Flores C, Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 1988;32:77-88.
24. Hayashida K, Obata H, Nakajima K, Eisenach JC. Gabapentin acts within the locus coeruleus to alleviate neuropathic pain. Anesthesiology 2008;109:1077-84.
25. Hayashida K, Parker RA, Eisenach JC. Activation of glutamate transporters in the locus coeruleus paradoxically activates descending inhibition in rats. Brain Res 2010;1317:80-6.
26. Hirata H, Aston-Jones G. A novel long-latency response of locus coeruleus neurons to noxious stimuli: mediation by peripheral C-fibers. J Neurophysiol 1994;71:1752-61. (Pubitemid 24153040)
27. Hirata H, Aston-Jones G. Long-latency responses of brain noradrenergic neurons to noxious stimuli are preferentially attenuated by intravenous morphine. Brain Res 1996;714:9-18. (Pubitemid 26120790)
28. Jett MF, McGuirk J, Waligora D, Hunter JC. The effects of mexiletine, desipramine and fluoxetine in rat models involving central sensitization. Pain 1997;69:161-9. (Pubitemid 27081422)
29. Lacroix D, Blier P, Curet O, de Montigny C. Effects of long-term desipramine administration on noradrenergic neurotransmission: electrophysiological studies in the rat brain. J Pharmacol Exp Ther 1991;257:1081-90.
30. Liu XJ, Gingrich JR, Vargas-Caballero M, Dong YN, Sengar A, Beggs S, Wang SH, Ding HK, Frankland PW, Salter MW. Treatment of inflammatory and neuropathic pain by uncoupling Src from the NMDA receptor complex. Nat Med 2008;14:1325-32.
31. Ma W, Eisenach JC. Chronic constriction injury of sciatic nerve induces the upregulation of descending inhibitory noradrenergic innervation to the lumbar dorsal horn of mice. Brain Res 2003;970:110-8. (Pubitemid 36423186)
32. Mao J, Mayer DJ, Price DD. Patterns of increased brain activity indicative of pain in a rat model of peripheral mononeuropathy. J Neurosci 1993;13:2689-702. (Pubitemid 23151783)
33. Mateo Y, Fernandez-Pastor B, Meana JJ. Acute and chronic effects of desipramine and clorgyline on alpha(2)-adrenoceptors regulating noradrenergic transmission in the rat brain: a dual-probe microdialysis study. Br J Pharmacol 2001;133:1362-70. (Pubitemid 32783498)
34. Mendell LM. Physiological properties of unmyelinated fiber projection to the spinal cord. Exp Neurol 1966;16:316-32.
35. Mico JA, Ardid D, Berrocoso E, Eschalier A. Antidepressants and pain. Trends Pharmacol Sci 2006;27:348-54. (Pubitemid 43963184)
36. Ortega-Alvaro A, Gibert-Rahola J, Mellado-Fernandez ML, Chover AJ, Mico JA. The effects of different monoaminergic antidepressants on the analgesia induced by spinal cord adrenal medullary transplants in the formalin test in rats. Anesth Analg 1997;84:816-20. (Pubitemid 27147708)
37. Parker RB, Waud DR. Pharmacological estimation of drug-receptor dissociation constants. Statistical evaluation. I. Agonists. J Pharmacol Exp Ther 1971;177:1-12.
38. Paxinos G, Watson C. The rat brain in stereotaxic coordinates. 6th ed. Amsterdam: Elsevier; 2009.
39. Sanchez-Blazquez P, Rodriguez-Munoz M, Garzon J. Mu-opioid receptors transiently activate the Akt-nNOS pathway to produce sustained potentiation of PKC-mediated NMDAR-CaMKII signaling. PLoS One 2010;5:e11278.
40. Sands SA, Reisman SA, Enna SJ. Effect of antidepressants on GABA(B) receptor function and subunit expression in rat hippocampus. Biochem Pharmacol 2004;68:1489-95. (Pubitemid 39286452)
41. Sindrup SH, Gram LF, Skjold T, Grodum E, Brosen K, Beck-Nielsen H. Clomipramine vs desipramine vs placebo in the treatment of diabetic neuropathy symptoms. A double-blind cross-over study. Br J Clin Pharmacol 1990;30:683-91. (Pubitemid 20377596)
42. Singewald N, Schneider C, Philippu A. Effects of neuroactive compounds, noxious and cardiovascular stimuli on the release of amino acids in the rat locus coeruleus. Neurosci Lett 1994;180:55-8. (Pubitemid 24314879)
43. Skolnick P, Popik P, Trullas R. Glutamate-based antidepressants: 20 years on. Trends Pharmacol Sci 2009;30:563-9.
44. Svensson TH, Usdin T. Feedback inhibition of brain noradrenaline neurons by tricyclic antidepressants: alpha-receptor mediation. Science 1978;202:1089-91.
45. Tanabe M, Takasu K, Takeuchi Y, Ono H. Pain relief by gabapentin and pregabalin via supraspinal mechanisms after peripheral nerve injury. J Neurosci Res 2008;86:3258-64.
46. Tokarski K, Bobula B, Wabno J, Hess G. Repeated administration of imipramine attenuates glutamatergic transmission in rat frontal cortex. Neuroscience 2008;153:789-95.
47. Tsuruoka M, Maeda M, Nagasawa I, Inoue T. Spinal pathways mediating coeruleospinal antinociception in the rat. Neurosci Lett 2004;362:236-9. (Pubitemid 38648949)
48. Van Bockstaele EJ, Colago EE. Selective distribution of the NMDA-R1 glutamate receptor in astrocytes and presynaptic axon terminals in the nucleus locus coeruleus of the rat brain: an immunoelectron microscopic study. J Comp Neurol 1996;369:483-96. (Pubitemid 26162599)
49. Viisanen H, Pertovaara A. Influence of peripheral nerve injury on response properties of locus coeruleus neurons and coeruleospinal antinociception in the rat. Neuroscience 2007;146:1785-94. (Pubitemid 46783215)
50. Wattiez AS, Libert F, Privat AM, Loiodice S, Fialip J, Eschalier A, Courteix C. Evidence for a differential opioidergic involvement in the analgesic effect of antidepressants: prediction for efficacy in animal models of neuropathic pain? Br J Pharmacol 2011;163:792-803.
51. Wei H, Pertovaara A. Spinal and pontine alpha2-adrenoceptors have opposite effects on pain-related behavior in the neuropathic rat. Eur J Pharmacol 2006;551:41-9. (Pubitemid 44648060)
52. West CH, Weiss JM. Effects of chronic antidepressant drug administration and electroconvulsive shock on activity of dopaminergic neurons in the ventral tegmentum. Int J Neuropsychopharmacol 2011;14:201-10.
53. Wong DT. Duloxetine (LY 248686): an inhibitor of serotonin and noradrenaline uptake and an antidepressant drug candidate. Expert Opin Investig Drugs 1998;7:1691-9. (Pubitemid 28451663)
54. Yalcin I, Tessier LH, Petit-Demouliere N, Doridot S, Hein L, Freund-Mercier MJ, Barrot M. Beta2-adrenoceptors are essential for desipramine, venlafaxine or reboxetine action in neuropathic pain. Neurobiol Dis 2009;33:386-94.
55. Zamalloa T, Bailey CP, Pineda J. Glutamate-induced post-activation inhibition of locus coeruleus neurons is mediated by AMPA/kainate receptors and sodium-dependent potassium currents. Br J Pharmacol 2009;156:649-61.