Long-term effects of decreased noradrenergic central nervous system innervation on pain behavior and opioid antinociception

Journal of Comparative Neurology

Volumn 460, Issue 1, 2003, Pages 38-55

  Jasmin, Luc ^a,b   Boudah, Abdennacer ^a   Ohara, Peter T ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Neurological Surgery   (United States)

Author keywords

Dopamine beta hydroxylase; Endogenous pain inhibition; Nerve injury; Opioid; Saporin; Substance P

Indexed keywords

2 BENZHYDRYL 3 (2 METHOXYBENZYLAMINO) 1 AZABICYCLO[2.2.2]OCTANE; DOPAMINE BETA MONOOXYGENASE; MORPHINE; NALTREXONE; NORADRENALIN; OPIATE; SAPORIN; SUBSTANCE P;

AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTONOMIC DENERVATION; BRAIN CORTEX; BRAIN STEM; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DOPAMINERGIC SYSTEM; FEMALE; HYPERALGESIA; HYPOTHALAMUS; IMMUNOREACTIVITY; LOCUS CERULEUS; MALE; NERVE FIBER REGENERATION; NEUROPATHIC PAIN; NEUROTRANSMISSION; NOCICEPTION; NONHUMAN; NORADRENERGIC NERVE; NORADRENERGIC SYSTEM; PRIORITY JOURNAL; RAT; SEROTONINERGIC SYSTEM; SPINAL CORD;

ANALGESICS, OPIOID; ANIMALS; ANTIBODIES, MONOCLONAL; BEHAVIOR, ANIMAL; BIPHENYL COMPOUNDS; CENTRAL NERVOUS SYSTEM; DENERVATION; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; FEMALE; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; IMMUNOTOXINS; INJECTIONS, INTRAVENTRICULAR; INJECTIONS, SPINAL; LUMBOSACRAL REGION; MALE; MORPHINE; NOREPINEPHRINE; PAIN; PAIN MEASUREMENT; PAIN THRESHOLD; PERIPHERAL NERVOUS SYSTEM DISEASES; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD; SUBSTANCE P; TIME;

EID: 0037454446     PISSN: 00219967     EISSN: None     Source Type: Journal    
DOI: 10.1002/cne.10633     Document Type: Article

References (91)

1. Altier N, Stewart J. 1996. Opioid receptors in the ventral tegmental area contribute to stress-induced analgesia in the formalin test for tonic pain. Brain Res 718:203-206.
2. Archer T, Jonsson G, Minor BG, Post C. 1986. Noradrenergic-serotonergic interactions and nociception in the rat. Eur J Pharmacol 120:295-307.
3. Ardid D, Guilbaud G. 1992. Antinociceptive effects of acute and 'chronic' injections of tricyclic antidepressant drugs in a new model of mononeuropathy in rats. Pain 49:279-287.
4. Basbaum AI, Fields HL. 1984. Endogenous pain control systems: brainstem spinal pathways and endorphin circuitry. Annu Rev Neurosci 7:309-338.
5. Berge OG, Ogren SO. 1984. Limited involvement of central noradrenergic pathways in morphine-induced antinociception. Neuropharmacology 23:1179-1185.
6. Bergsneider M. 2001. Evolving concepts of cerebrospinal fluid physiology. In: Luciano M, editor. Hydrocephalus. Philadelphia: WB Saunders. p 631-638.
7. Blessing WW, Lappi DA, Wiley RG. 1998. Destruction of locus coeruleus neuronal perikarya after injection of anti-dopamine-B-hydroxylase immunotoxin into the olfactory bulb of the rat. Neurosci Lett 243:85-88.
8. Bohn LM, Xu F, Gainetdinov RR, Caron MG. 2000. Potentiated opioid analgesia in norepinephrine transporter knock-out mice. J Neurosci 20:9040-9045.
9. Burkey AR, Carstens E, Wenniger JJ, Tang J, Jasmin L. 1996. An opioidergic cortical antinociception triggering site in the agranular insular cortex of the rat that contributes to morphine antinociception. J Neurosci 16:6612-6623.
10. Cao YQ, Mantyh PW, Carlson EJ, Gillespie AM, Epstein CJ, Basbaum AI. 1998. Primary afferent tachykinins are required to experience moderate to intense pain. Nature 392:390-394.
11. Clark FM, Proudfit HK. 1991a. The projection oflocus coeruleus neurons to the spinal cord in the rat determined by anterograde tracing combined with immunocytochemistry. Brain Res 538:231-245.
12. Clark FM, Proudfit HK. 1991b. The projection of noradrenergic neurons in the A7 catecholamine cell group to the spinal cord in the rat demonstrated by anterograde tracing combined with immunocytochemistry, Brain Res 547:279-288.
13. Clark FM, Proudfit HK. 1993. The projections of noradrenergic neurons in the A5 catecholamine cell group to the spinal cord in the rat: anatomical evidence that A5 neurons modulate nociception. Brain Res 616:200-210.
14. Coudore-Civiale MA, Courteix C, Eschalier A, Fialip J. 1998. Effect of tachykinin receptor antagonists in experimental neuropathic pain. Eur J Pharmacol 361:175-184.
15. Cryan JF, Dalvi A, Jin SH, Hirsch BR, Lucki I, Thomas SA. 2001. Use of dopamine-beta-hydroxylase-deficient mice to determine the role of norepinephrine in the mechanism of action of antidepressant drugs. J Pharmacol Exp Ther 298:651-657.
16. De Felipe C, Herrero JF, O'Brien JA, Palmer JA, Doyle CA, Smith AJ, Laird JM, Belmonte C, Cervero F, Hunt SP. 1998. Altered nociception, analgesia and aggression in mice lacking the receptor for substance P. Nature 392:394-397.
17. Dubuisson D, Dennis SG. 1977. The formalin test: a quantitative study of the analgesic effects of morphine, meperidine, and brain stem stimulation in rats and cats. Pain 4:161-174.
18. Eisenach JC, Hood DD, Curry R. 1998. Intrathecal, but not intravenous, clonidine reduces experimental thermal or capsaicin-induced pain and hyperalgesia in normal volunteers. Anesth Analg 87:591-596.
19. Fasmer OB, Berge OG, Tveiten L, Hole K. 1986. Changes in nociception after 6-hydroxydopamine lesions of descending catecholaminergic pathways in mice. Pharmacol Biochem Behav 24:1441-1444.
20. Fritschy JM, Grzanna R. 1992. Restoration of ascending noradrenergic projections by residual locus coeruleus neurons: compensatory response to neurotoxin-induced cell death in the adult rat brain. J Comp Neurol 321:421-441.
21. Goff JR, Burkey AR, Goff DJ, Jasmin L. 1998. Reorganization of the spinal dorsal horn in models of chronic pain: correlation with behavior. Neuroscience 82:559-574.
22. Goto F, Fujita N, Fujita T. 1990. Cerebrospinal norepinephrine concentrations and the duration of epidural analgesia. Can J Anaesth 37:839-843.
23. Gray AM, Pache DM, Sewell RD. 1999. Do alpha2-adrenoceptors play an integral role in the antinociceptive mechanism of action of antidepressant compounds? Eur J Pharmacol 378:161-168.
24. Hallman H, Sundstrom E, Jonsson G. 1984. Effects of the noradrenaline neurotoxin DSP 4 on monoamine neurons and their transmitter turnover in rat CNS. J Neural Transm 60:89-102.
25. Hao JX, Yu W, Xu XJ, Wiesenfeld-Hallin Z. 1996. Effects of intrathecal vs. systemic clonidine in treating chronic allodynia-like response in spinally injured rats. Brain Res 736:28-34.
26. Harik SI. 1984. Locus ceruleus lesion by local 6-hydroxydopamine infusion causes marked and specific destruction of noradrenergic neurons, long-term depletion of norepinephrine and the enzymes that synthesize it, and enhanced dopaminergic mechanisms in the ipsilateral cerebral cortex. J Neurosci 4:699-707.
27. Hedo G, Lopez-Garcia JA. 2001. Alpha-1A adrenoceptors modulate potentiation of spinal nociceptive pathways in the rat spinal cord in vitro. Neuropharmacology 41:862-869.
28. Igari T, Takeda M, Obara K, Ono S. 1977. Catecholamine metabolism in the patients with rheumatoid arthritis. Tohoku J Exp Med 122:9-20.
29. Ippoliti R, Lendaro E, D'Agostino I, Fiani ML, Guidarini D, Vestri S, Benedetti PA, Brunori M. 1995. A chimeric saporin-transferrin conjugate compared to ricin toxin: role of the carrier in intracellular transport and toxicity. FASEB J 9:1220-1225.
30. Izenwasser S, Kornetsky C. 1988. Potentiation of morphine analgesia by D-amphetamine is mediated by norepinephrine and not dopamine. Pain 33:363-368.
31. Jasmin L, Ohara PT. 2001. Long-term intrathecal catheterization in the rat. J Neurosci Methods 110:81-89.
32. Jasmin L, Kohan L, Franssen M, Janni G, GoffJR. 1998. The cold plate as a test of nociceptive behaviors: description and application to the study of chronic neuropathic and inflammatory pain models. Pain 75:367-382.
33. Jasmin L, Tien D, Weinshenker D, Palmiter RD, Green PG, Janni G, Ohara PT. 2002. The NK1 receptor mediates both the hyperalgesia and the resistance to morphine in mice lacking noradrenaline. Proc Natl Acad Sci U S A 99:1029-1034.
34. Jett MF, Michelson S. 1996. The formalin test in rat: validation of an automated system. Pain 64:19-25.
35. Jones SL. 1991. Descending noradrenergic influences on pain. Prog Brain Res 88:381-394.
36. Kellstein DE, Malseed RT, Ossipov MH, Goldstein FJ. 1988. Effect of chronic treatment with tricyclic antidepressants upon antinociception induced by intrathecal injection of morphine and monoamines. Neuropharmacology 27:1-14.
37. Kiehn O, Sillar KT, Kjaerulff O, McDearmid JR. 1999. Effects of noradrenaline on locomotor rhythm-generating networks in the isolated neonatal rat spinal cord. J Neurophysiol 82:741-746.
38. Kim SH, Chung JM. 1992. An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 50:355-363.
39. Kolb B, Stewart J, Sutherland RJ. 1997. Recovery of function is associated with increased spine density in cortical pyramidal cells after frontal lesions and/or noradrenaline depletion in neonatal rats. Behav Brain Res 89:61-70.
40. Kwiat GC, Basbaum AI. 1992. The origin of brainstem noradrenergic and serotonergic projections to the spinal cord dorsal horn in the rat. Somatosens Mot Res 9:157-173.
41. Legangneux E, Mora JJ, Spreux-Varoquaux O, Thorin I, Herrou M, Alvado G, Gomeni C. 2001. Cerebrospinal fluid biogenic amine metabolites, plasma-rich platelet serotonin and [3H]imipramine reuptake in the primary fibromyalgia syndrome. Rheumatology (Oxford) 40:290-296.
42. Li X, Conklin D, Ma W, Zhu X, Eisenach JC. 2002. Spinal noradrenergic activation mediates allodynia reduction from an allosteric adenosine modulator in a rat model of neuropathic pain. Pain 97:117-125.
43. Liu RJ, Wang R, Nie H, Zhang RX, Qiao JT, Dafny N. 1997. Effects of intrathecal monoamine antagonists on the nociceptive c-Fos expression in a lesioned rat spinal cord. Int J Neurosci 91:169-180.
44. Loughlin SE, Foote SL, Bloom FE. 1986. Efferent projections of nucleus locus coeruleus: topographic organization of cells of origin demonstrated by three-dimensional reconstruction. Neuroscience 18:291-306.
45. Lynch ME. 2001. Antidepressants as analgesics: a review of randomized controlled trials. J Psychiatr Neurosci 26:30-36.
46. Mantyh PW, Rogers SD, Honore P, Allen BJ, Ghilardi JR, Li J, Daughters RS, Lappi DA, Wiley RG, Simone DA. 1997. Inhibition of hyperalgesia by ablation of lamina I spinal neurons expressing the substance P receptor. Science 278:275-279.
47. Martin WJ, Gupta NK, Loo CM, Rohde DS, Basbaum AI. 1999. Differential effects of neurotoxic destruction ofdescending noradrenergic pathways on acute and persistent nociceptive processing. Pain 80:57-65.
48. Martinez-Caro L, Laird JM. 2000. Allodynia and hyperalgesia evoked by sciatic mononeuropathy in NKI receptor knockout mice. Neuroreport 11:1213-1217.
49. Max MB. 1994. Treatment of post-herpetic neuralgia: antidepressants. Ann Neurol 35:S50-S53.
50. McQuay HJ, Tramer M, Nye BA, Carroll D, Wiffen PJ, Moore RA. 1996. A systematic review of antidepressants in neuropathic pain. Pain 68:217-227.
51. Moller KA, Johansson B, Berge OG. 1998. Assessing mechanical allodynia in the rat paw with a new electronic algometer. J Neurosci Methods 84:41-47.
52. Monasky MS, Zinsmeister AR, Stevens CW, Yaksh TL. 1990. Interaction of intrathecal morphine and ST-91 on antinociception in the rat: dose-response analysis, antagonism and clearance. J Pharmacol Exp Ther 254:383-392.
53. Moore R, Card R. 1984. Noradrenaline-containing neuron systems. In: Björklund A, Hökfelt T, editors. Classical transmitters in the CNS. Part I. New York: Elsevier Science. p 123-156.
54. Moorman SJ, Whalen LR. 1993. A model system to determine the effects of specific neurotransmitters on segmental reflexes in the spinal cord of the rat. J Neurosci Methods 46:73-81.
55. Nagasaka H, Yaksh TL. 1990. Pharmacology of intrathecal adrenergic agonists: cardiovascular and nociceptive reflexes in halothane-anesthetized rats. Anesthesiology 73:1198-1207.
56. Oluyomi AO, Hart SL. 1990. Alpha-adrenoceptor involvement in swim stress-induced antinociception in the mouse. J Pharm Pharmacol 42:778-784.
57. Omote K, Kawamata T, Kawamata M, Namiki A. 1998. Formalin-induced nociception activates a monoaminergic descending inhibitory system. Brain Res 814:194-198.
58. Onghena P, Van Houdenhove B. 1992. Antidepressant-induced analgesia in chronic non-malignant pain: a meta-analysis of 39 placebo-controlled studies. Pain 49:205-219.
59. Onttonen T, Pertovaara A. 2000. The mechanical antihyperalgesic effect of intrathecally administered MPV-2426, a novel alpha2-adrenoceptor agonist, in a rat model of postoperative pain. Anesthesiology 92:1740-1745.
60. Ossipov MH, Suarez LJ, Spaulding TC. 1989. Antinociceptive interactions between alpha 2-adrenergic and opiate agonists at the spinal level in rodents. Anesth Analg 68:194-200.
61. Pan HL, Chen SR, Eisenach JC. 1999. Intrathecal clonidine alleviates allodynia in neuropathic rats: interaction with spinal muscarinic and nicotinic receptors. Anesthesiology 90:509-514.
62. Paxinos G, Watson C. 1998. The rat brain in stereotaxic coordinates. New York: Academic Press.
63. Post C, Minor BG, Davies M, Archer T. 1986. Analgesia induced by 5-hydroxytryptamine receptor agonists is blocked or reversed by noradrenaline-depletion in rats. Brain Res 363:18-27.
64. Reader TA, Briere R. 1983. Long-term unilateral noradrenergic denervation: monoamine content and 3H-prazosin binding sites in rat neocortex. Brain Res Bull 11:687-692.
65. Room P, Postema F, Korf J. 1981. Divergent axon collaterals of rat locus coeruleus neurons: demonstration by a fluorescent double labeling technique. Brain Res 221:219-230.
66. Rosa C, Ghione S, Mezzasalma L, Pellegrini M, Basile Fasolo C, Giaconi S, Gazzetti P, Ferdeghini M. 1988. Relationship between pain sensitivity, cardiovascular reactivity to cold pressor test and indexes of activity of the adrenergic and opioid system. Clin Exp Hypertens 10:383-390.
67. Rupniak NM, Hill RG. 1999. Neurokinin antagonists. In: Sawynok J, Cowan A, editors. Novel aspects of pain management. Opioids and beyond. New York: Wiley-Liss. p 135-155.
68. Rupniak NM, Carlson EJ, Webb JK, Harrison T, Porsolt RD, Roux S, de Felipe C, Hunt SP, Oates B, Wheeldon A. 2001. Comparison of the phenotype of NK1R-/- mice with pharmacological blockade of the substance P (NK1) receptor in assays for antidepressant and anxiolytic drugs. Behav Pharmacol 12:497-508.
69. Sagen J, Proudfit HK. 1984. Effect of intrathecally administered noradrenergic antagonists on nociception in the rat. Brain Res 310:295-301.
70. Sawynok J, Reid A. 1987. Effect of 6-hydroxydopamine-induced lesions to ascending and descending noradrenergic pathways on morphine analgesia. Brain Res 419:156-165.
71. Sawynok J, Reid A. 1996. Interactions of descending serotonergic systems with other neurotransmitters in the modulation of nociception. Behav Brain Res 73:63-68.
72. Stone LS, Broberger C, Vulchanova L, Wilcox GL, Hokfelt T, Riedl MS, Elde R. 1998. Differential distribution of alpha2A and alpha2C adrenergic receptor immunoreactivity in the rat spinal cord. J Neurosci 18:5928-5937.
73. Szot P, Weinshenker D, White SS, Robbins CA, Rust NC, Schwartzkroin PA, Palmiter RD. 1999. Norepinephrine-deficient mice have increased susceptibility to seizure-inducing stimuli. J Neurosci 19:10985-10992.
74. Takagi H, Harima A. 1996. Analgesic effect of L-threo-3,4-dihydroxyphenylserine (L-DOPS) in patients with chronic pain. Eur Neuropsychopharmacol 6:43-47.
75. Takagi H, Shiomi H, Kuraishi Y, Fukui K, Ueda H. 1979. Pain and the bulbospinal noradrenergic system: pain-induced increase in normetanephrine content in the spinal cord and its modification by morphine. Eur J Pharmacol 54:99-107.
76. Tavares I, Lima D, Coimbra A. 1997. The pontine A5 noradrenergic cells which project to the spinal cord dorsal horn are reciprocally connected with the caudal ventrolateral medulla in the rat. Eur J Neurosci 9:2452-2461.
77. Tillet Y, Batailler M, Krieger-Poullet M, Thibault J. 1990. Presence of dopamine-immunoreactive cell bodies in the catecholaminergic group A15 of the sheep brain. Histochemistry 93:327-333.
78. Umeda E, Satoh T, Nagashima H, Potter PE, Tarkovacs G, Vizi ES. 1997. alpha 2A subtype of presynaptic alpha 2-adrenoceptors modulates the release of [3H]-noradrenaline from rat spinal cord. Brain Res Bull 42:129-132.
79. Velazquez RA, McCarson KE, Cai Y, Kovacs KJ, Shi Q, Evensjo M, Larson AA. 2002. Upregulation of neurokinin-1 receptor expression in rat spinal cord by an N-terminal metabolite of substance P. Eur J Neurosci 16:229-241.
80. Wang SJ, Cheng LL, Gean PW. 1999. Cross-modulation of synaptic plasticity by beta-adrenergic and 5-HT1A receptors in the rat basolateral amygdala. J Neurosci 19:570-577.
81. Weinshenker D, Szot P, Miller NS, Rust NC, Hohmann JG, Pyati U, White SS, Palmiter RD. 2001. Genetic comparison of seizure control by norepinephrine and neuropeptide Y. J Neurosci 21:7764-7769.
82. West WL, Yeomans DC, Proudfit HK. 1993. The function of noradrenergic neurons in mediating antinociception induced by electrical stimulation of the locus coeruleus in two different sources of Sprague-Dawley rats. Brain Res 626:127-135.
83. Wiedenmayer CP, Barr GA. 2000. Mu opioid receptors in the ventrolateral periaqueductal gray mediate stress-induced analgesia but not immobility in rat pups. Behav Neurosci 114:125-136.
84. Wiley RG, Kline IR. 2000. Neuronal lesioning with axonally transported toxins. J Neurosci Methods 103:73-82.
85. Xu M, Kontinen VK, Kalso E. 1999. Endogenous noradrenergic tone controls symptoms of allodynia in the spinal nerve ligation model of neuropathic pain. Eur J Pharmacol 366:41-45.
86. Yaksh TL, Pogrel JW, Lee YW, Chaplan SR. 1995. Reversal of nerve ligation-induced allodynia by spinal alpha-2 adrenoceptor agonists. J Pharmacol Exp Ther 272:207-214.
87. Yamamoto T, Nozaki-Taguchi N. 1996. Clonidine, but not morphine, delays the development ofthermal hyperesthesia induced by sciatic nerve constriction injury in the rat. Anesthesiology 85:835-845.
88. Yamamoto T, Sakashita Y. 1999. The role of the spinal opioid receptor likel receptor, the NK-1 receptor, and cyclooxygenase-2 in maintaining postoperative pain in the rat. Anesth Analg 89:1203-1208.
89. Yashpal K, Pitcher GM, Henry JL. 1995. Noxious peripheral stimulation produces antinociception mediated via substance P and opioid mechanisms in the rat tail-flick test. Brain Res 674:97-103.
90. Zhang C, Davies MF, Guo TZ, Maze M. 1999. The analgesic action of nitrous oxide is dependent on the release of norepinephrine in the dorsal horn of the spinal cord. Anesthesiology 91:1401-1407.
91. Zhong FX, Ji XQ, Tsou K. 1985. Intrathecal DSP4 selectively depletes spinal noradrenaline and attenuates morphine analgesia. Eur J Pharmacol 116:327-330.