Retrograde viral vector-mediated inhibition of pontospinal noradrenergic neurons causes hyperalgesia in rats

Journal of Neuroscience

Volumn 29, Issue 41, 2009, Pages 12855-12864

  Howorth, Patrick W ^a   Thornton, Simon R ^a   O'Brien, Victoria ^a   Smith, Wynne D ^a   Nikiforova, Natalia ^b   Teschemacher, Anja G ^a   Pickering, Anthony E ^a,c  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY HOSPITALS BRISTOL NHS FOUNDATION TRUST   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; AVV PRS EGFP VECTOR; AVV PRS HKIR 2.1 VECTOR; BARIUM; CATECHOLAMINE; CFA; FORMALDEHYDE; FREUND ADJUVANT; INWARDLY RECTIFYING POTASSIUM CHANNEL; INWARDLY RECTIFYING POTASSIUM CHANNEL SUBUNIT KIR2.1; PROTEIN C FOS; UNCLASSIFIED DRUG; VIRUS VECTOR; DOPAMINE BETA MONOOXYGENASE; ENHANCED GREEN FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN; NORADRENALIN;

ADENOVIRUS; ALLODYNIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR; BRAIN SLICE; CELL CULTURE; CELL STRAIN; COLD ALLODYNIA; CONTROLLED STUDY; GENE DELIVERY SYSTEM; GENE EXPRESSION; GROWTH INHIBITION; HYPERALGESIA; HYPERPOLARIZATION; IN VIVO STUDY; INJECTION; LUMBAR SPINE; MALE; MEMBRANE POTENTIAL; NERVE EXCITABILITY; NERVE INJURY; NEUROPATHIC PAIN; NOCICEPTION; NONHUMAN; NORADRENERGIC NERVE; PONTOSPINAL NORADRENERGIC NEURON; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; SPINAL CORD DORSAL HORN; TACTILE ALLODYNIA; ANIMAL; CELL COUNT; CELL MEMBRANE POTENTIAL; DISEASE MODEL; GENE VECTOR; GENETIC TRANSFECTION; GENETICS; IN VITRO STUDY; LAMINECTOMY; METABOLISM; METHODOLOGY; MOTOR ACTIVITY; NERVE CELL; NEWBORN; PAIN ASSESSMENT; PAIN THRESHOLD; PATCH CLAMP; PATHOLOGY; PATHOPHYSIOLOGY; PERIPHERAL NEUROPATHY; PHYSIOLOGY; PONS; PROMOTER REGION; WISTAR RAT;

ADENOVIRIDAE; ANIMALS; ANIMALS, NEWBORN; CATECHOLAMINES; CELL COUNT; DISEASE MODELS, ANIMAL; DOPAMINE BETA-HYDROXYLASE; GENETIC VECTORS; GREEN FLUORESCENT PROTEINS; HYPERALGESIA; LAMINECTOMY; MALE; MEMBRANE POTENTIALS; MOTOR ACTIVITY; NEURONS; NOREPINEPHRINE; PAIN MEASUREMENT; PAIN THRESHOLD; PATCH-CLAMP TECHNIQUES; PC12 CELLS; PERIPHERAL NERVOUS SYSTEM DISEASES; PONS; POTASSIUM CHANNELS, INWARDLY RECTIFYING; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS C-FOS; RATS; RATS, WISTAR; TRANSFECTION;

EID: 70350455045     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.1699-09.2009     Document Type: Article

References (88)

1. Akli S, Caillaud C, Vigne E, Stratford-Perricaudet LD, Poenaru L, Perricaudet M, Kahn A, Peschanski MR (1993) Transfer of a foreign gene into the brain using adenovirus vectors. Nat Genet 3:224-228. (Pubitemid 23096557)
2. Amendola M, Venneri MA, Biffi A, Vigna E, Naldini L (2005) Coordinate dual-gene transgenesis by lentiviral vectors carrying synthetic bidirectional promoters. Nat Biotechnol 23:108-116. (Pubitemid 41724633)
3. Bewig B, Schmidt WE (2000) Accelerated titering of adenoviruses. Biotechniques 28:870-873.
4. Bodnar RJ, Mann PE, Stone EA (1985) Potentiation of cold-water swim analgesia by acute, but not chronic desipramine administration. Pharmacol Biochem Behav 23:749-752.
5. Bohn LM, Xu F, Gainetdinov RR, Caron MG (2000) Potentiated opioid analgesia in norepinephrine transporter knock-out mice. J Neurosci 20:9040-9045. (Pubitemid 32042905)
6. Burnett A, Gebhart GF (1991) Characterization of descending modulation of nociception from the A5 cell group. Brain Res 546:271-281.
7. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL (1994) Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods 53:55-63.
8. Clark FM, Proudfit HK (1991a) 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.
9. Clark FM, Proudfit HK (1991b) The projection of locus coeruleus neurons to the spinal cord in the rat determined by anterograde tracing combined with immunocytochemistry. Brain Res 538:231-245.
10. Crawley JN, Roth RH, Maas JW (1979) Locus coeruleus stimulation increases noradrenergic metabolite levels in rat spinal cord. Brain Res 166:180-184.
11. Decosterd I, Woolf CJ (2000) Spared nerve injury: an animal model of persistent peripheral neuropathic pain. Pain 87:149-158. (Pubitemid 30621447)
12. Dixon WJ (1980) Efficient analysis of experimental observations. Annu Rev Pharmacol Toxicol 20:441-462.
13. Dodt HU, Zieglgänsberger W (1990) Visualizing unstained neurons in living brain slices by infrared DIC- videomicroscopy. Brain Res 537:333-336.
14. Duale H, Kasparov S, Paton JF, Teschemacher AG (2005) Differences in transductional tropism of adenoviral and lentiviral vectors in the rat brainstem. Exp Physiol 90:71-78.
15. Duale H, Waki H, Howorth P, Kasparov S, Teschemacher AG, Paton JF (2007) Restraining influence of A2 neurons in chronic control of arterial pressure in spontaneously hypertensive rats. Cardiovasc Res 76:184-193. (Pubitemid 47371117)
16. 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. (Pubitemid 8234766)
17. Eaton MJ, Blits B, Ruitenberg MJ, Verhaagen J, Oudega M (2002) Amelioration of chronic neuropathic pain after partial nerve injury by adeno-associated viral (AAV) vector-mediated over-expression of BDNF in the rat spinal cord. Gene Ther 9:1387-1395. (Pubitemid 35244164)
18. Eisenach JC, DuPen S, Dubois M, Miguel R, Allin D (1995) Epidural clonidine analgesia for intractable cancer pain. The Epidural Clonidine Study Group. Pain 61:391-399.
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. (Pubitemid 16067433)
20. Fields H (2004) State-dependent opioid control of pain. Nat Rev Neurosci 5:565-575.
21. Fritschy JM, Grzanna R (1990) Demonstration of two separate descending noradrenergic pathways to the rat spinal cord: evidence for an intragriseal trajectory of locus coeruleus axons in the superficial layers of the dorsal horn. J Comp Neurol 291:553-582.
22. Glorioso JC, Fink DJ (2004) Herpes vector-mediated gene transfer in treatment of diseases of the nervous system. Annu Rev Microbiol 58:253-271.
23. Graham FL, Prevec L (1995) Methods for construction of adenovirus vectors. Mol Biotechnol 3:207-220.
24. Green GM, Lyons L, Dickenson AH (1998) Alpha2-adrenoceptor antagonists enhance responses of dorsal horn neurones to formalin induced inflammation. Eur J Pharmacol 347:201-204. (Pubitemid 28234457)
25. Guyenet PG (1980) The coeruleospinal noradrenergic neurons: anatomical and electrophysiological studies in the rat. Brain Res 189:121-133.
26. Hammond DL, Yaksh TL (1984) Antagonism of stimulation-produced antinociception by intrathecal administration of methysergide or phentolamine. Brain Res 298:329-337.
27. Han MH, Bolaños CA, Green TA, Olson VG, Neve RL, Liu RJ, Aghajanian GK, Nestler EJ (2006) Role of cAMP response element-binding protein in the rat locus ceruleus: regulation of neuronal activity and opiate withdrawal behaviors. J Neurosci 26:4624-4629.
28. Hargreaves K, Dubner R, Brown F, Flores C, Joris J (1988) A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32:77-88. (Pubitemid 18149685)
29. Hayashida K, Clayton BA, Johnson JE, Eisenach JC (2008) Brain derived nerve growth factor induces spinal noradrenergic fiber sprouting and enhances clonidine analgesia following nerve injury in rats. Pain 136:348-355. (Pubitemid 351680250)
30. Hentall ID, Mesigil R, Pinzon A, Noga BR (2003) Temporal and spatial profiles of pontine-evoked monoamine release in the rat's spinal cord. J Neurophysiol 89:2943-2951. (Pubitemid 36682647)
31. Hnasko TS, Perez FA, Scouras AD, Stoll EA, Gale SD, Luquet S, Phillips PE, Kremer EJ, Palmiter RD (2006) Cre recombinase-mediated restoration of nigrostriatal dopamine in dopamine-deficient mice reverses hypophagia and bradykinesia. Proc Natl Acad Sci U S A 103:8858-8863. (Pubitemid 43878108)
32. Holden JE, Schwartz EJ, Proudfit HK (1999) Microinjection of morphine in the A7 catecholamine cell group produces opposing effects on nociception that are mediated by alpha1- and alpha2-adrenoceptors. Neuroscience 91:979-990.
33. Howe MW, Feig SL, Osting SM, Haberly LB (2008) Cellular and subcellular localization of Kir2.1 subunits in neurons and glia in piriform cortex with implications for K+ spatial buffering. J Comp Neurol 506:877-893.
34. Howorth PW, Teschemacher AG, Pickering AE (2009) Retrograde adenoviral vector targeting of nociresponsive pontospinal noradrenergic neurons in the rat in vivo. J Comp Neurol 512:141-157.
35. Hwang DY, Carlezon WA Jr, Isacson O, Kim KS (2001) A high-efficiency synthetic promoter that drives transgene expression selectively in noradrenergic neurons. Hum Gene Ther 12:1731-1740. (Pubitemid 32911639)
36. Iadarola MJ, Brady LS, Draisci G, Dubner R (1988) Enhancement of dynorphin gene expression in spinal cord following experimental inflammation: stimulus specificity, behavioral parameters and opioid receptor binding. Pain 35:313-326. (Pubitemid 19010487)
37. 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. (Pubitemid 34106630)
38. Jasmin L, Boudah A, Ohara PT (2003) Long-term effects of decreased noradrenergic central nervous system innervation on pain behavior and opioid antinociception. J Comp Neurol 460:38-55. (Pubitemid 36438276)
39. Johns DC, Marx R, Mains RE, O'Rourke B, Marbán E (1999) Inducible genetic suppression of neuronal excitability. J Neurosci 19:1691-1697. (Pubitemid 29094187)
40. Jones SL (1991) Descending noradrenergic influences on pain. Prog Brain Res 88:381-394.
41. Jones SL, Gebhart GF (1986a) Characterization of coeruleospinal inhibition of the nociceptive tail-flick reflex in the rat: mediation by spinal alpha 2-adrenoceptors. Brain Res 364:315-330. (Pubitemid 16104666)
42. Jones SL, Gebhart GF (1986b) Quantitative characterization of ceruleospinal inhibition of nociceptive transmission in the rat. J Neurophysiol 56:1397-1410.
43. + channel mRNAs are differentially expressed in the adult rat brain. J Neurosci 16:3559-3570.
44. Kubo Y, Baldwin TJ, Jan YN, Jan LY (1993) Primary structure and functional expression of a mouse inward rectifier potassium channel. Nature 362:127-133. (Pubitemid 23085250)
45. 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. (Pubitemid 34603315)
46. Liu RJ, Wang R, Nie H, Zhang RX, Qiao JT, Dafny N (1997a) Effects of intrathecal monoamine antagonists on the nociceptive c-Fos expression in a lesioned rat spinal cord. Int J Neurosci 91:169-180. (Pubitemid 27490961)
47. Liu Y, Himes BT, Moul J, Huang W, Chow SY, Tessler A, Fischer I (1997b) Application of recombinant adenovirus for in vivo gene delivery to spinal cord. Brain Res 768:19-29. (Pubitemid 27433472)
48. Lonergan T, Teschemacher AG, Hwang DY, Kim KS, Pickering AE, Kasparov S (2005) Targeting brain stem centers of cardiovascular control using adenoviral vectors: impact of promoters on transgene expression. Physiol Genomics 20:165-172. (Pubitemid 40388515)
49. 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.
50. Ma W, Eisenach JC (2003) Chronic constriction injury of sciatic nerve induces the up-regulation of descending inhibitory noradrenergic innervation to the lumbar dorsal horn of mice. Brain Res 970:110-118. (Pubitemid 36423186)
51. Mansikka H, Lähdesmäki J, Scheinin M, Pertovaara A (2004) Alpha(2A) adrenoceptors contribute to feedback inhibition of capsaicin-induced hyperalgesia. Anesthesiology 101:185-190. (Pubitemid 38833281)
52. Martin WJ, Gupta NK, Loo CM, Rohde DS, Basbaum AI (1999) Differential effects of neurotoxic destruction of descending noradrenergic pathways on acute and persistent nociceptive processing. Pain 80:57-65.
53. Mata M, Hao S, Fink DJ (2008) Applications of gene therapy to the treatment of chronic pain. Curr Gene Ther 8:42-48.
54. Melzack R, Wall PD, Ty TC (1982) Acute pain in an emergency clinic: latency of onset and descriptor patterns related to different injuries. Pain 14:33-43.
55. Millan MJ (1997) The role of descending noradrenergic and serotoninergic pathways in the modulation of nociception: focus on receptor multiplicity. In: The pharmacology of pain (Dickenson A, Besson JM, eds), pp 385-446. Berlin: Springer.
56. Millan MJ (2002) Descending control of pain. Prog Neurobiol 66:355-474.
57. Miller JF, Proudfit HK (1990) Antagonism of stimulation-produced antinociception from ventrolateral pontine sites by intrathecal administration of alpha-adrenergic antagonists and naloxone. Brain Res 530:20-34.
58. Mizuno H, Hirano T, Tagawa Y (2007) Evidence for activity-dependent cortical wiring: formation of interhemispheric connections in neonatal mouse visual cortex requires projection neuron activity. J Neurosci 27:6760-6770. (Pubitemid 46983436)
59. North RA, Yoshimura M (1984) The actions of noradrenaline on neurones of the rat substantia gelatinosa in vitro. J Physiol 349:43-55.
60. Omote K, Kawamata T, Kawamata M, Namiki A (1998) Formalin-induced nociception activates a monoaminergic descending inhibitory system. Brain Res 814:194-198. (Pubitemid 29023426)
61. Paxinos G, Watson C (2005) The rat brain in stereotaxic coordinates, Ed 5. Amsterdam: Elsevier Academic.
62. Pertovaara A (2006) Noradrenergic pain modulation. Prog Neurobiol 80:53-83.
63. Rahman W, D'Mello R, Dickenson AH (2008) Peripheral nerve injuryinduced changes in spinal alpha(2)-adrenoceptor-mediated modulation of mechanically evoked dorsal horn neuronal responses. J Pain 9:350-359.
64. Reddy SV, Maderdrut JL, Yaksh TL (1980) Spinal cord pharmacology of adrenergic agonist-mediated antinociception. J Pharmacol Exp Ther 213:525-533. (Pubitemid 10085156)
65. Reynolds DV (1969) Surgery in the rat during electrical analgesia induced by focal brain stimulation. Science 164:444-445.
66. Ridoux V, Robert JJ, Zhang X, Perricaudet M, Mallet J, Le Gal La Salle G (1994) Adenoviral vectors as functional retrograde neuronal tracers. Brain Res 648:171-175. (Pubitemid 24171588)
67. Sagen J, Proudfit HK (1984) Effect of intrathecally administered noradrenergic antagonists on nociception in the rat. Brain Res 310:295-301. (Pubitemid 14033107)
68. Salbaum JM, Cirelli C, Walcott E, Krushel LA, Edelman GM, Tononi G (2004) Chlorotoxin-mediated disinhibition of noradrenergic locus coeruleus neurons using a conditional transgenic approach. Brain Res 1016:20-32. (Pubitemid 38834270)
69. Sluka KA, Westlund KN (1992) Spinal projections of the locus coeruleus and the nucleus subcoeruleus in the Harlan and the Sasco Sprague- Dawley rat. Brain Res 579:67-73.
70. Sonohata M, Furue H, Katafuchi T, Yasaka T, Doi A, Kumamoto E, Yoshimura M (2004) Actions of noradrenaline on substantia gelatinosa neurones in the rat spinal cord revealed by in vivo patch recording. J Physiol 555:515-526. (Pubitemid 38380008)
71. 2 agonists and is necessary for spinal adrenergic- opioid synergy. J Neurosci 17:7157-7165.
72. Stoppini L, Buchs PA, Muller D (1991) A simple method for organotypic cultures of nervous tissue. J Neurosci Methods 37:173-182.
73. Sugimoto M, Kuraishi Y, Satoh M, Takagi H (1986) Involvement of medullary opioid-peptidergic and spinal noradrenergic systems in the regulation of formalin-induced persistent pain. Neuropharmacology 25:481-485. (Pubitemid 16036362)
74. Teschemacher AG, Paton JF, Kasparov S (2005) Imaging living central neurones using viral gene transfer. Adv Drug Deliv Rev 57:79-93.
75. Tsuruoka M, Willis WD Jr (1996) Bilateral lesions in the area of the nucleus locus coeruleus affect the development of hyperalgesia during carrageenaninduced inflammation. Brain Res 726:233-236. (Pubitemid 26292251)
76. Viisanen H, Pertovaara A (2007) Influence of peripheral nerve injury on response properties of locus coeruleus neurons and coeruleospinal antinociception in the rat. Neuroscience 146:1785-1794. (Pubitemid 46783215)
77. Wang S, Teschemacher AG, Paton JF, Kasparov S (2006) Mechanism of nitric oxide action on inhibitory GABAergic signaling within the nucleus tractus solitarii. FASEB J 20:1537-1539.
78. Wei F, Dubner R, Ren K (1999) Nucleus reticularis gigantocellularis and nucleus raphe magnus in the brain stem exert opposite effects on behavioral hyperalgesia and spinal Fos protein expression after peripheral inflammation. Pain 80:127-141.
79. Wei H, Pertovaara A (2006) Spinal and pontine alpha2-adrenoceptors have opposite effects on pain-related behavior in the neuropathic rat. Eur J Pharmacol 551:41-49. (Pubitemid 44648060)
80. 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.
81. Westlund KN, Bowker RM, Ziegler MG, Coulter JD (1983) Noradrenergic projections to the spinal cord of the rat. Brain Res 263:15-31. (Pubitemid 13160133)
82. Williams JT, Marshall KC (1987) Membrane properties and adrenergic responses in locus coeruleus neurons of young rats. J Neurosci 7:3687-3694.
83. Williams JT, North RA, Shefner SA, Nishi S, Egan TM (1984) Membrane properties of rat locus coeruleus neurones. Neuroscience 13:137-156. (Pubitemid 14033088)
84. Wilson SP, Yeomans DC, Bender MA, Lu Y, Goins WF, Glorioso JC (1999) Antihyperalgesic effects of infection with a preproenkephalin-encoding herpes virus. Proc Natl Acad Sci U S A 96:3211-3216. (Pubitemid 29148870)
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. (Pubitemid 29076719)
86. Xu Y, Gu Y, Xu GY, Wu P, Li GW, Huang LY (2003) Adeno-associated viral transfer of opioid receptor gene to primary sensory neurons: a strategy to increase opioid antinociception. Proc Natl Acad Sci U S A 100: 6204-6209. (Pubitemid 36576954)
87. Yeomans DC, Clark FM, Paice JA, Proudfit HK (1992) Antinociception induced by electrical stimulation of spinally projecting noradrenergic neurons in the A7 catecholamine cell group of the rat. Pain 48:449-461.
88. Yu CR, Power J, Barnea G, O'Donnell S, Brown HE, Osborne J, Axel R, Gogos JA (2004) Spontaneous neural activity is required for the establishment and maintenance of the olfactory sensory map. Neuron 42:553-566. (Pubitemid 38639876)