cAMP and cGMP contribute to sensory neuron hyperexcitability and hyperalgesia in rats with dorsal root ganglia compression

Journal of Neurophysiology

Volumn 95, Issue 1, 2006, Pages 479-492

  Song, Xue Jun ^a   Wang, Zheng Bei ^a   Gan, Qiang ^a   Walters, Edgar T ^b  

^a Parker College of Chiropractic   (United States)

^b UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1H 1,2,4 OXADIAZOLO[4,3 A]QUINOXALIN 1 ONE; 8 BROMO CYCLIC AMP; 9 (TETRAHYDRO 2 FURYL)ADENINE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC GMP; CYCLIC GMP DEPENDENT PROTEIN KINASE; STEEL;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BEHAVIOR; CONTROLLED STUDY; DEPOLARIZATION; DRUG EFFECT; ELECTROPHYSIOLOGY; FOOT; HEATING; HYPERALGESIA; IN VIVO STUDY; INTRACELLULAR SPACE; LATENT PERIOD; MALE; NERVE COMPRESSION; NERVE EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; RAT; SENSORY NERVE CELL; SPINAL GANGLION; STIMULUS RESPONSE; ACTION POTENTIAL; ANIMAL; INJURY; METABOLISM; PATHOPHYSIOLOGY; RADICULOPATHY; SPRAGUE DAWLEY RAT;

ACTION POTENTIALS; ANIMALS; CYCLIC AMP; CYCLIC GMP; GANGLIA, SPINAL; HYPERALGESIA; MALE; NEURONS, AFFERENT; RADICULOPATHY; RATS; RATS, SPRAGUE-DAWLEY;

EID: 33644801168     PISSN: 00223077     EISSN: None     Source Type: Journal    
DOI: 10.1152/jn.00503.2005     Document Type: Article

References (100)

1. Abdulla FA and Smith PA. Axotomy- and autotomy-induced changes in the excitability of dorsal root ganglion neurons. J Neurophysiol 85: 630-643, 2001a.
2. + currents of rat dorsal root ganglion neurons. J Neurophysiol 85: 644-658, 2001b.
3. Aley KO and Levine JD. Role of protein kinase A in the maintenance of inflammatory pain. J Neurosci 19: 2181-2186, 1999.
4. Aley KO and Levine JD. Different peripheral mechanisms mediate enhanced nociception in metabolic/toxic and traumatic painful peripheral neuropathies in the rat. Neuroscience 111: 389-397, 2002.
5. Aley KO, McCarter G, and Levine JD. Nitric oxide signaling in pain and nociceptor sensitization in the rat. J Neurosci 18: 7008-7014, 1998.
6. Amir R, Kocsis JD, and Devor M. Multiple interacting sites of ectopic spike electrogenesis in primary sensory neurons. J Neurosci 25: 2576-2585, 2005.
7. Amir R, Michaelis M, and Devor M. Burst discharge in primary sensory neurons: triggered by subthreshold oscillations, maintained by depolarizing afterpotentials. J Neurosci 22: 1187-1198, 2002.
8. Anderson P, Storm J, and Wheal HV. The thresholds of action potentials evoked by synapses on the dendrites of pyramidal cells in the rat hippocampus in vitro. J Physiol 383: 509-526, 1987.
9. Baccei ML and Kocsis JD. Voltage-gated calcium currents in axotomized adult rat cutaneous afferent neurons. J Neurophysiol 83: 2227-2238, 2000.
10. Bauer MB, Murphy S, and Gebhart GF. Stimulation of cyclic GMP production via a nitrosyl factor in sensory neuronal cultures by algesic or inflammatory agents. J Neurochem 65: 363-372, 1995.
11. Bennett GJ and Xie YK. A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 33: 87-107, 1988.
12. Bolyard LA, Van Looy JW, and Vasko MR. Sensitization of rat sensory neurons by chronic exposure to forskolin or 'inflammatory cocktail' does not downregulate and requires continuous exposure. Pain 88: 277-285, 2000.
13. Burchiel KJ. Spontaneous generation in normal and denervated dorsal root ganglia: sensitivity to alpha-adrenergic stimulation and hypoxia. Exp Neurol 85: 257-272, 1984.
14. Cardenas LM, Cardenas CG, and Scroggs RS. 5HT increases excitability of nociceptor-like rat dorsal root ganglion neurons via cAMP-coupled TTX-resistant Na(+) channels. J Neurophysiol 86: 241-248, 2001.
15. Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, and Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389: 816-824, 1997.
16. Clatworthy AL and Walters ET. Rapid amplification and facilitation of mechanosensory discharge in Aplysia by noxious stimulation. J Neurophysiol 70: 1181-1194, 1993.
17. Costigan M, Befort K, Karchewski L, Griffin RS, D'Urso D, Allchorne A, Sitarski J, Mannion JW, Pratt RE, and Woolf CJ. Replicate high-density rat genome oligonucleotide microarrays reveal hundreds of regulated genes in the dorsal root ganglion after peripheral nerve injury. BMC Neurosci 3: 16, 2002.
18. Cui M and Nicol GD. Cyclic AMP mediates the prostaglandin E2-induced potentiation of bradykinin excitation in rat sensory neurons. Neurosci 66: 459-466, 1995.
19. Devor M. The pathophysiology of damaged peripheral nerves. In: Text Book of Pain, 3rd ed., edited by Wall PD and Melzack R. London: Churchill Livingstone, 1994, p. 79-100.
20. Devor M. Unexplained peculiarities of the dorsal root ganglion. Pain Suppl 6: S27-S35, 1999.
21. Duarte ID, dos Santos IR, Lorenzetti BB, and Ferreira SH. Analgesia by direct antagonism of nociceptor sensitization involves the arginine-nitric oxide-cGMP pathway. Eur J Pharmacol 217: 225-227, 1992.
22. England S, Beyan S, and Docherty RJ. PGE2 modulates the tetrodotoxin-resistant sodium current in neonatal rat dorsal root ganglion neurones via the cyclic AMP-protein kinase A cascade. J Physiol 495: 429-440, 1996.
23. Evans AR, Vasko MR, and Nicol GD. The cAMP transduction cascade mediates the PGE2-induced inhibition of potassium currents in rat sensory neurones. J Physiol 516: 163-178, 1999.
24. Everill B and Kocsis JD. Reduction in potassium current in identified cutaneous afferent dorsal root ganglion neurons after axotomy. J Neurophysiol 82: 700-708, 1999.
25. 2+ dependent process. Prostaglandins 18: 179-190, 1979.
26. 2+ influx in visceral afferent neurons. Brain Res 345: 345-349, 1985.
27. Gallego R, Ivorra I, and Morales A. Effects of central or peripheral axotomy on membrane properties of sensory neurones in the petrosal ganglion of the cat. J Physiol 391: 39-56, 1987.
28. Gasull X, Liao X, Dulin MF, Phelps C, and Walters ET. Evidence that long-term hyperexcitability of the sensory neuron soma induced by nerve injury in Aplysia is adaptive. J Neurophysiol In press.
29. + current in nociceptors. Proc Natl Acad Sci USA 93: 1108-1112, 1996.
30. Gurtu S and Smith PA. Electrophysiological characteristics of hamster dorsal root ganglion cells and their response to axotomy. J Neurophysiol 59: 408-423, 1988.
31. Hargreaves K, Dubner R, Brown F, Flores C, and Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32: 77-88, 1988.
32. Hess DT, Patterson SI, Smith DS, and Skene JH. Neuronal growth cone collapse and inhibition of protein fatty acylation by nitric oxide. Nature 366: 562-565, 1993.
33. Hingtgen CM, Waite KJ, and Vasko MR. Prostaglandins facilitate peptide release from rat sensory neurons by activating the adenosine 3′,5′-cyclic monophosphate transduction cascade. J Neurosci 15: 5411-5419, 1995.
34. Honda A, Adams SR, Sawyer CL, Lev-Ram V, Tsien RY, and Dostmann WR. Spatiotemporal dynamics of guanosine 3′,5′-cyclic monophosphate revealed by a genetically encoded, fluorescent indicator. Proc Natl Acad Sci USA 98: 2437-2442, 2001.
35. Hu SJ, Song XJ, Greenquist KW, Zhang JM, and LaMotte RH. Protein kinase A modulates spontaneous activity in chronically compressed dorsal root ganglion neurons in the rat. Pain 94: 39-46, 2001.
36. Hu SJ and Xing J. An experimental model for chronic compression of dorsal root ganglion produced by intervertebral foramen stenosis in the rat. Pain 77: 15-23, 1998.
37. Ingram SL and Williams JT. Opioid inhibition of Ih via adenylyl cyclase. Neuron 13: 179-186, 1994.
38. Ingram SL and Williams JT. Modulation of the hyperpolarization-activated current (Ih) by cyclic nucleotides in guinea-pig primary afferent neurons. J Physiol 492: 97-106, 1996.
39. Ishikawa K, Tanaka M, Black JA, and Waxman SG. Changes in expression of voltage-gated potassium channels in dorsal root ganglion neurons following axotomy. Muscle Nerve 22: 502-507, 1999.
40. Ji RR and Woolf CJ. Neuronal plasticity and signal transduction in nociceptive neurons: implications for the initiation and maintenance of pathological pain. Neurobiol Dis 8: 1-10, 2001.
41. Jiang H, Shabb JB, and Corbin JD. Cross-activation: overriding cAMP/cGMP selectivities of protein kinases in tissues. Biochem Cell Biol 70: 1283-1289, 1992.
42. Kajander KC and Bennett GL. Onset of a painful neuropathy in rat: a partial and differential deafferentation and spontaneous discharge in Aβ and Aδ primary afferent neurons. J Neurophysiol 68: 734-744, 1992.
43. Kandel ER. The molecular biology of memory storage: a dialogue between genes and synapses. Science 294: 1030-1038, 2001.
44. Kim SH and Chung JM. An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 50: 355-363, 1992.
45. Kim CH, Oh Y, Chung JM, and Chung K. Changes in three subtypes of tetrodotoxin sensitive sodium channel expression in the axotomized dorsal root ganglion in the rat. Neurosci Lett 323: 125-128, 2002.
46. Kress M, Rodl J, and Reeh PW. Stable analogues of cyclic AMP but not cyclic GMP sensitize unmyelinated primary afferents in rat skin to heat stimulation but not to inflammatory mediators, in vitro. Neuroscience 74: 609-617, 1996.
47. Lewin MR and Walters ET. Cyclic GMP pathway is critical for inducing long-term sensitization of nociceptive sensory neurons. Nat Neurosci 2: 18-23, 1999.
48. Liao X, Gunstream JD, Lewin MR, Ambron RT, and Walters ET. Activation of protein kinase A contributes to the expression but not the induction of long-term hyperexcitability caused by axotomy of Aplysia sensory neurons. J Neurosci 19: 1247-1256, 1999.
49. Liu CN, Wall PD, Ben-Dor E, Michaelis M, Amir R, and Devor M. Tactile allodynia in the absence of C-fiber activation: altered firing properties of DRG neurons following spinal nerve injury. Pain 85: 503-521, 2000.
50. A currents by capsaicin in rat trigeminal ganglion neurons. J Neurophysiol 89: 1387-1401, 2003.
51. Liu L, Yang T, Bruno MJ, Andersen OS, and Simon SA. Voltage-gated ion channels in nociceptors: modulation by cGMP. J Neurophysiol 92: 2323-2332, 2004.
52. Lopshire JC and Nicol GD. Activation and recovery of the PGE2-mediated sensitization of the capsaicin response in rat sensory neurons. J Neurophysiol 78: 3154-3164, 1997.
53. Lopshire JC and Nicol GD. The cAMP transduction cascade mediates the prostaglandin E2 enhancement of the capsaicin-elicited current in rat sensory neurons: whole-cell and single-channel studies. J Neurosci 18: 6081-6092, 1998.
54. Ma C and LaMotte RH. Enhanced excitability of dissociated primary sensory neurons after chronic compression of the dorsal root ganglion in the rat. Pain 113: 106-1012, 2005.
55. Ma C, Shu Y, Zheng Z, Chen Y, Yao H, Greenquist KW, White FA, and LaMotte RH. Similar electrophysiological changes in axotomized and neighboring intact dorsal root ganglion neurons. J Neurophysiol 89: 1588-1602, 2003.
56. Ma QP and Woolf CJ. Basal and touch-evoked fos-like immunoreactivity during experimental inflammation in the rat. Pain 67: 307-316, 1996.
57. Malmberg AB, Chen C, Tonegawa S, and Basbaum AI. Preserved acute pain and reduced neuropathic pain in mice lacking PKCgamma. Science 278: 239-240, 1997.
58. Mannion AF, Muntener M, Taimela S, and Dvorak J. A randomized clinical trial of three active therapies for chronic low back pain. Spine 24: 2435-2448, 1999.
59. Meller ST and Gebhart GF. Nitric oxide (NO) and nociceptive processing in the spinal cord. Pain 52: 127-136, 1993.
60. Miletic G, Pankratz MT, and Miletic V. Increases in the phosphorylation of cyclic AMP response element binding protein (CREB) and decreases in the content of calcineurin accompany thermal hyperalgesia following chronic constriction injury in rats. Pain 99: 493-500, 2002.
61. Morris R, Southam E, Braid DJ, and Garthwaite J. Nitric oxide may act as a messenger between dorsal root ganglion neurones and their satellite cells. Neurosci Lett 137: 29-32, 1992.
62. Muller U. Prolonged activation of cAMP-dependent protein kinase during conditioning induces long-term memory in honeybees. Neuron 27: 159-168, 2000.
63. Neumann S, Doubell TP, Leslie T, and Woolf CJ. Inflammatory pain hyperalgesia mediated by phenotypic switch in myelinated primary sensory neurons. Nature 384: 360-364, 1996.
64. Niedbala B, Sanchez A, and Feria M. Nitric oxide mediates neuropathic pain behavior in peripherally denervated rats. Neurosci Lett 188: 57-60, 1995.
65. Pollock J, Crawford JH, Wootton JF, Corrie JE, and Scott RH. A comparison between the distinct inward currents activated in rat cultured dorsal root ganglion neurones by intracellular flash photolysis of two forms of caged cyclic guanosine monophosphate. Neurosci Lett 338: 143-146, 2003.
66. Qian YF, Chao DS, Santillano DR, Cornwell TL, Nairn AC, Greengard P, Lincoln TM, and Bredt DS. cGMP-dependent protein kinase in dorsal root ganglion: relationship with nitric oxide synthase and nociceptive neurons. J Neurosci 16: 3130-3138, 1996.
67. Rathee PK, Distler C, Obreja O, Neuhuber W, Wang GK, Wang SY, Nau C, and Kress M. PKA/AKAP/VR-1 module: a common link of Gs-mediated signaling to thermal hyperalgesia. J Neurosci 22: 4740-4745, 2002.
68. + currents in cutaneous afferent dorsal root ganglion neurones following axotomy. Neurbiol Dis 2: 3-12, 1995.
69. + channel pathway. Proc Natl Acad Sci USA 101: 3680-3685, 2004.
70. Salter M, Strijbos PJ, Neale S, Duffy C, Follenfant RL, and Garthwaite J. The nitric oxide-cyclic GMP pathway is required for nociceptive signalling at specific loci within the somatosensory pathway. Neuroscience 73: 649-655, 1996.
71. Schmidt H, Werner M, Heppenstall PA, Henning M, More MI, Kuhbandner S, Lewin GR, Hofmann F, Feil R, and Rathjen FG. cGMP-mediated signaling via cGKIalpha is required for the guidance and connectivity of sensory axons. J Cell Biol 159: 489-498, 2002.
72. Schmidtko A, Ruth P, Geisslinger G, and Tegeder I. Inhibition of cyclic guanosine 5′-monophosphate-dependent protein kinase I (PKG-I) in lumbar spinal cord reduces formalin-induced hyperalgesia and PKG upregulation. Nitric Oxide 8: 89-94, 2003.
73. Seltzer Z, Dubner R, and Shir Y. A novel behavioral model of neuropathic pain disorders produced in rats by partial sciatic nerve injury. Pain 43: 205-218, 1990.
74. Shi TJ, Holmberg K, Xu ZQ, Steinbusch H, de Vente J, and Hökfelt T. Effect of peripheral nerve injury on cGMP and nitric oxide synthase levels in rat dorsal root ganglia: time course and coexistence. Pain 78: 171-180, 1998.
75. Smith JA, Davis CL, and Burgess GM. Prostaglandin E2-induced sensitization of bradykinin-evoked responses in rat dorsal root ganglion neurons is mediated by cAMP-dependent protein kinase A. Eur J Neurosci 12: 3250-3258, 2000.
76. Song H, Ming G, He Z, Lehmann M, McKerracher L, Tessier-Lavigne M, and Poo M. Conversion of neuronal growth cone responses from repulsion to attraction by cyclic nucleotides. Science 281: 1515-1518, 1998.
77. Song XJ, Hu SJ, Greenquist KW, Zhang JM, and LaMotte RH. Mechanical and thermal hyperalgesia and ectopic neuronal discharge after chronic compression of dorsal root ganglia. J Neurophysiol 82: 3347-3358, 1999.
78. Song XJ, Vizcarra C, Xu DS, Rupert RL, and Wong ZN. Hyperalgesia and neural excitability following injuries to central and peripheral branches of axons and somata of dorsal root ganglion neurons. J Neurophysiol 89: 2185-2193, 2003a.
79. Song XJ, Xu DS, Vizcarra C, and Rupert RL. Onset and recovery of hyperalgesia and hyperexcitability of sensory neurons following intervertebral foramen volume reduction and restoration. J Manipulative Physiol Ther 26: 426-436, 2003b.
80. Song XJ, Zhang JM, Hu SJ, and LaMotte RH. Somata of nerve-injured sensory neurons exhibit enhanced responses to inflammatory mediators. Pain 104: 701-709, 2003c.
81. Southall MD and Vasko MR. Prostaglandin receptor subtypes, EP3C and EP4, mediate the prostaglandin E2-induced cAMP production and sensitization of sensory neurons. J Biol Chem 276: 16083-16091, 2001.
82. Stebbing MJ, Eschenfelder S, Habler HJ, Acosta MC, Janig W, and McLachlan EM. Changes in the action potential in sensory neurones after peripheral axotomy in vivo. Neuroreport 10: 201-206, 1999.
83. Study RE and Kral MG. Spontaneous action potential activity in isolated dorsal root ganglion neurons from rats with a painful neuropathy. Pain 65: 235-242, 1996.
84. Sung YJ, Walters ET, and Ambron RT. A neuronal isoform of protein kinase G couples mitogen-activated protein kinase nuclear import to axotomy-induced long-term hyperexcitability in Aplysia sensory neurons. J Neurosci 24: 7583-7595, 2004.
85. Taiwo YO, Bjerknes LK, Goetzl EJ, and Levine JD. Mediation of primary afferent peripheral hyperalgesia by the cAMP second messenger system. Neuroscience 32: 577-580, 1989.
86. Tegeder I, Del Turco D, Schmidtko A, Sausbier M, Feil R, Hofmann F, Deller T, Ruth P, and Geisslinger G. Reduced inflammatory hyperalgesia with preservation of acute thermal nociception in mice lacking cGMP-dependent protein kinase I. Proc Natl Acad Sci USA 101: 3253-3257, 2004.
87. Thippeswamy T and Morris R. Evidence that nitric oxide-induced synthesis of cGMP occurs in a paracrine but not an autocrine fashion and that the site of its release can be regulated: studies in dorsal root ganglia in vivo and in vitro. Nitric Oxide 5: 105-115, 2001.
88. Valder CR, Liu JJ, Song YH, and Luo ZD. Coupling gene chip analyses and rat genetic variances in identifying potential target genes that may contribute to neuropathic allodynia development. J Neurochem 87: 560-573, 2003.
89. Vivancos GG, Parada CA, and Ferreira SH. Opposite nociceptive effects of the arginine/NO/cGMP pathway stimulation in dermal and subcutaneous tissues. Br J Pharmacol 138: 1351-1357, 2003.
90. Wall PD and Devor M. Sensory afferent impulse originates from dorsal root ganglia as well as from the periphery in normal and nerve injury rats. Pain 17: 321-339, 1983.
91. Wall PD and Gutnick M. Ongoing activity in peripheral nerves: the physiology and pharmacology of impulses originating from a neuroma. Exp Neurol 43: 580-593, 1974.
92. Waxman SG. The molecular pathophysiology of pain: abnormal expression of sodium channel genes and its contributions to hyperexcitability of primary sensory neurons. Pain 6: 133-140, 1999.
93. Waxman SG, Cummins TR, Dib-Hajj SD, and Black JA. Voltage-gated sodium channels and the molecular pathogenesis of pain: a review. J Rehabil Res Dev 37: 517-528, 2000.
94. Waxman SG, Cummins TR, Dib-Hajj S, Fjell J, and Black JA. Sodium channels, excitability of primary sensory neurons, and the molecular basis of pain. Muscle Nerve 22: 1177-1187, 1999.
95. Waxman SG, Kocsis JD, and Black JA. Type III sodium channel mRNA is expressed in embryonic but not adult spinal sensory neurons, and is reexpressed following axotomy. J Neurophysiol 72: 466-470, 1994.
96. Xiao HS, Huang QH, Zhang FX, Bao L, Lu YJ, Guo C, Yang L, Huang WJ, Fu G, Xu SH, Cheng XP, Yan Q, Zhu ZD, Zhang X, Chen Z, and Han ZG. Identification of gene expression profile of dorsal root ganglion in the rat peripheral axotomy model of neuropathic pain. Proc Natl Acad Sci USA 99: 8360-8365, 2002.
97. Yao H, Donnelly DF, Ma C, and LaMotte RH. Upregulation of the hyperpolarization-activated cation current after chronic compression of the dorsal root ganglion. J Neurosci 23: 2069-2074, 2003.
98. Zhang JM, Donnelly DF, Song XJ, and LaMotte RH. Axotomy increases the excitability of dorsal root ganglion cells with unmyelinated axons. J Neurophysiol 78: 2790-2794, 1997.
99. Zhang JM, Song XJ, and LaMotte RH. Enhanced excitability of sensory neurons in rats with cutaneous hyperalgesia produced by chronic compression of the dorsal root ganglion. J Neurophysiol 82: 3359-3366, 1999.
100. Zimmermann M. Pathobiology of neuropathic pain. Eur J Pharmacol 429: 23-37, 2001.