Spinal gap junctions: Potential involvement in pain facilitation

Journal of Pain

Volumn 5, Issue 7, 2004, Pages 392-405

  Spataro, Leah E ^a   Sloane, Evan M ^a   Milligan, Erin D ^a   Wieseler Frank, Julie ^a   Schoeniger, Diana ^a   Jekich, Brian M ^a   Barrientos, Ruth M ^a   Maier, Steven F ^a   Watkins, Linda R ^a,b  

^a UNIVERSITY OF COLORADO   (United States)

^b Dept Psychol Camp Box 345 U ^*  (United States)

Author keywords

astrocytes; Carbenoxolone; mechanical allodynia; spinal cord; thermal hyperalgesia

Indexed keywords

CARBENOXOLONE; GLYCYRRHIZIC ACID; INTERLEUKIN 1; INTERLEUKIN 6;

ALLODYNIA; ANALGESIC ACTIVITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; CYTOKINE RELEASE; DISEASE MODEL; DRUG EFFECT; DRUG MECHANISM; EXCITATION; GAP JUNCTION; GLIA CELL; HYPERALGESIA; INFLAMMATION; LOW DRUG DOSE; MALE; NERVE COMPRESSION; NERVE INJURY; NEUROPATHIC PAIN; NONHUMAN; PAIN; RAT; SCIATIC INFLAMMATORY NEUROPATHY; SCIATIC NEUROPATHY; SPINAL CORD; THERMAL STIMULATION;

ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; ANTI-ULCER AGENTS; CARBENOXOLONE; CHRONIC DISEASE; GAP JUNCTIONS; GLYCYRRHIZIC ACID; HIV ENVELOPE PROTEIN GP120; HYPERALGESIA; INJECTIONS, SPINAL; INTERLEUKIN-1; MALE; NERVE COMPRESSION SYNDROMES; PAIN; POSTERIOR HORN CELLS; RATS; RATS, SPRAGUE-DAWLEY; SCIATIC NEUROPATHY; SPECIFIC PATHOGEN-FREE ORGANISMS;

EID: 6944237013     PISSN: 15265900     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jpain.2004.06.006     Document Type: Article

References (64)

1. H. Aldskogius, E.N. Kozlova Central neuron-glial and glial-glial interactions following axons injury Prog Neurobiol 55 1998 1 26
2. A. Araque, V. Parpura, R.P. Sanzgiri, P.G. Haydon Tripartite synapses: Glia, the unacknowledged partner Trends Neurosci 22 1999 208 215
3. G. Baranauskas, A. Nistri Sensitization of pain pathways in the spinal cord: Cellular mechanisms Prog Neurobiol 54 1998 349 365
4. G.J. Bennett, Y.K. Xie A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man Pain 33 1988 87 8107
5. F. Blomstrand, N.D. Aberg, P.S. Eriksson, E. Hansson, L. Ronnback Extent of intercellular calcium wave propagation is related to gap junction permeability and level of connexin-43 expression in astrocytes in primary cultures from four brain regions Neuroscience 92 1999 255 265
6. E.A. Bushong, M.E. Martone, Y.Z. Jones, M.H. Ellisman Protoplasmic astrocytes in CA1 stratum radiatum occupy separate anatomical domains J Neurosci 22 2002 183 192
7. G. Carmignoto Reciprocal communication systems between astrocytes and neurones Prog Neurobiol 62 2000 561 581
8. M. Chacur, E.D. Milligan, L.S. Gazda, C. Armstrong, H. Wang, K.J. Tracey, S.F. Maier, L.R. Watkins A new model of sciatic inflammatory neuritis (SIN): Induction of unilateral and bilateral mechanical allodynia following acute unilateral peri-sciatic immune activation in rats Pain 94 2001 231 244
9. Q. Chang, M. Gonzalez, M.J. Pinter, R.J. Balice-Gordon Gap junctional coupling and patterns of connexin expression among neonatal rat lumbar spinal motor neurons J Neurosci 19 1999 10813 10828
10. S.R. Chaplan, F.W. Bach, J.W. Pogrel, J.M. Chung, T.L. Yaksh Quantitative assessment of tactile allodynia in the rat paw J Neurosci Meth 53 1994 55 63
11. J.S. Davidson, I.M. Baumgarten Glycyrrhetinic acid derivatives: A novel class of inhibitors of gap-junctional intercellular communication - structure-activity relationships J Pharmacol Exp Ther 246 1988 1104 1107
12. J.S. Davidson, I.M. Baumgarten, E.H. Harley Reversible inhibition of intercellular junctional communication by glycyrrhetinic acid Biochem Biophys Res Commun 134 1986 29 36
13. J.A. DeLeo, R.W. Colburn Proinflammatory cytokines and glial cells: Their role in neuropathic pain L. Watkins Cytokines and Pain 1999 Birkhauser Basel, Switzerland 159 182
14. J.A. DeLeo, F.Y. Tanga, V.L. Tawfik Neuroimmune activation and neuroinflammation in chronic pain and opioid tolerance/hyperalgesia Neuroscientist 10 2004 40 52
15. R. Dermietzel Diversification of gap junction proteins (connexins) in the central nervous sytem and the concept of functional compartments Cell Biol Int 22 1998 719 730
16. W.L. Duax, D. Ghosh, V. Pletnev Steroid dehydrogenase structures, mechanism of action, and disease Vitam Horm 58 2000 121 148
17. Eugenin EA, Eckardt D, Theis M, Willecke K, Bennett MV, Saez JC: Microglia at brain stab wounds express connexin 43 and in vitro form functional gap junctions after treatment with interferon-gamma and tumor necrosis factor-alpha. Proc Natl Acad Sci 98:4190-4195, 2001
18. M.V. Frantseva, L. Kokarovtseva, C.G. Naus, P.L. Carlen, D. MacFabe, J.L. Perez Velazquez Specific gap junctions enhance the neuronal vulnerability to brain traumatic injury J Neurosci 22 2002 644 653
19. K.-Y. Fu, A.R. Light, G.K. Matsushima, W. Maixner Microglial reactions after subcutaneous formalin injection into the rat hind paw Brain Res 825 1999 59 67
20. C.J. Garrison, P.M. Dougherty, S.M. Carlton GFAP expression in lumbar spinal cord of naive and neuropathic rats treated with MK-801 Exp Neurol 129 1994 237 243
21. G.S. Goldberg, A.P. Moreno, J.F. Bechberger, S.S. Hearn, R.R. Shivers, D.J. MacPhee, Y.C. Zhang, C.C. Naus Evidence that disruption of connexon particle arrangements in gap junction plaques is associated with inhibition of gap junctional communication by a glycyrrhetinic acid derivative Exp Cell Res 222 1996 48 53
22. F. Hajos, M. Kalman Distribution of glial fibrillary acidic protein (GFAP)-immunoreactive astrocytes in the rat brain II. Mesencephalon, rhombencephalon and spinal cord Exp Brain Res 78 1989 164 173
23. M.K. Hansen, K.T. Nguyen, L.E. Goehler, R.P. Gaykema, M. Fleshner, S.F. Maier, L.R. Watkins Effects of vagotomy on lipopolysaccharide-induced brain interleukin-1beta protein in rats Auton Neurosci 85 2000 119 126
24. K. Hargreaves, R. Dubner, F. Brown, C. Flores, J. Joris A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia Pain 32 1998 77 88
25. L.O.J. Harvey Efficient estimation of sensory thresholds Behav Res Methods Instrum Comput 18 1986 623 632
26. P.G. Haydon GLIA: Listening and talking to the synapse Nat Rev Neurosci 2 2001 185 193
27. P.H. Jellinck, C. Monder, B.S. McEwen, R.R. Sakai Differential inhibition of 11 beta-hydroxysteroid dehydrogenase by carbenoxolone in rat brain regions and peripheral tissues J Steroid Biochem Mol Biol 46 1993 209 213
28. Laughlin TM, Bethea JR, Yezierski RP, Wilcox GL: Cytokine involvement in dynorphin-induced allodynia. Pain 84:159-167, 2000
29. W.E. Li, J.I. Nagy Activation of fibres in rat sciatic nerve alters phosphorylation state of connexin-43 at astrocytic gap junctions in spinal cord: Evidence for junction regulation by neuronal-glial interactions Neuroscience 97 2000 113 123
30. S.T. Meller, C. Dyskstra, D. Grzybycki, S. Murphy, G.F. Gebhart The possible role of glia in nociceptive processing and hyperalgesia in the spinal cord of the rat Neuropharmacology 33 1994 1471 1478
31. Millan MJ: Descending control of pain. Prog Neurobiol 66:355-474, 2002
32. E.D. Milligan, J.L. Hinde, K.K. Mehmert, S.F. Maier, L.R. Watkins A method for increasing the viability of the external portion of the lumbar catheters placed in the spinal subarachnoid space of rats J Neurosci Methods 90 1999 81 86
33. E.D. Milligan, S.F. Maier, L.R. Watkins Sciatic inflammatory neuropathy: A new model for studying neuropathic pain of inflammatory origin D. Luo Pain Research Methods and Protocols: Methods of Molecular Medicine 2002 Humana Press New York, NY 67 89
34. E.D. Milligan, K.K. Mehmert, J.L. Hinde, L.O.J. Harvey, D. Martin, K.J. Tracey, S.F. Maier, L.R. Watkins Thermal hyperalgesia and mechanical allodynia produced by intrathecal administration of the human immunodeficiency virus-1 (HIV-1) envelope glycoprotein, gp120 Brain Res 861 2000 105 116
35. E.D. Milligan, K.A. O'Connor, K.T. Nguyen, C.B. Armstrong, C. Twining, R. Gaykema, A. Holguin, D. Martin, S.F. Maier, L.R. Watkins Intrathecal HIV-1 envelope glycoprotein gp120 enhanced pain states mediated by spinal cord proinflammatory cytokines J Neurosci 21 2001 2808 2819
36. E.D. Milligan, C. Twining, M. Chacur, J. Biedenkapp, K. O'Connor, S. Poole, K.J. Tracey, D. Martin, S.F. Maier, L.R. Watkins Spinal glia and proinflammatory cytokines mediate mirror-image neuropathic pain J Neurosci 23 2003 1026 1040
37. M.P. Moisan, J.R. Seckl, C.R. Edwards 11 Beta-hydroxysteroid dehydrogenase bioactivity and messenger RNA expression in rat forebrain: Localization in hypothalamus, hippocampus, and cortex Endocrinology 127 1990 1450 1455
38. J.I. Nagy, X. Li, J. Rempel, G. Stelmack, D. Patel, W.A. Staines, T. Yasumura, J.E. Rash Connexin26 in adult rodent central nervous system: Demonstration at astrocytic gap junctions and colocalization with connexin30 and connexin43 J Comp Neurol 441 2001 302 323
39. C.C. Naus, M. Bani-Yaghoub Gap junctional communication in the developing central nervous system Cell Biol Int 22 1998 751 763
40. E.A. Newman Propagation of intercellular calcium waves in retinal astrocytes and Muller cells J Neurosci 21 2001 2215 2223
41. K.A. O'Connor, A. Holguin, M.K. Hansen, S.F. Maier, L.R. Watkins A method for measuring multiple cytokines from small samples Brain Behav Immun 18 2004 274 280
42. P.A. Ochalski, U.N. Frankenstein, E.L. Hertzberg, J.I. Nagy Connexin-43 in rat spinal cord: localization in astrocytes and identification of heterotypic astro-oligodendrocytic gap junctions Neuroscience 76 1997 931 945
43. M.A. Ozog, R. Siushansian, C.C. Naus Blocked gap junctional coupling increases glutamate-induced neurotoxicity in neuron-astrocyte co-cultures J Neuropathol Exp Neurol 61 2002 132 141
44. V. Parpura, T.A. Basarsky, F. Liu, K. Jeftinija, S. Jeftinija, P.G. Haydon Glutamate-mediated astrocyte-neuron signalling Nature 369 1994 744 747
45. L. Pasti, A. Volterra, T. Pozzan, G. Carmignoto Intracellular calcium oscillations in astrocytes: A highly plastic, bidirectional form of communication between neurons and astrocytes in situ J Neurosci 17 1997 7817 7830
46. P.E. Paulson, T.J. Morrow, K.L. Casey Bilateral behavioral and regional cerebral blood flow changes during painful peripheral mononeuropathy in the rat Pain 84 2000 233 245
47. J.E. Rash, T. Yasumura, K.G. Davidson, C.S. Furman, F.E. Dudek, J.I. Nagy Identification of cells expressing Cx43, Cx30, Cx26, Cx32 and Cx36 in gap junctions of rat brain and spinal cord Cell Commun Adhes 8 2001 315 320
48. J.E. Rash, T. Yasumura, F.E. Dudek, J.I. Nagy Cell-specific expression of connexins and evidence of restricted gap junctional coupling between glial cells and between neurons J Neurosci 21 2001 1983 2000
49. A. Rohlmann, R. Laskawi, A. Hofer, R. Dermietzel, J.R. Wolff Astrocytes as rapid sensors of peripheral axotomy in the facial nucleus of rats Neuroreport 5 1994 409 412
50. N. Rouach, M. Segal, A. Koulakoff, C. Giaume, E. Avignone Carbenoxolone blockade of neuronal network activity in culture is not mediated by an action on gap junctions J Physiol 553 2003 729 745
51. R. Rozental, M. Srinivas, D.C. Spray How to close a gap junction channel R. Bruzzone C. Giaume Methods in Molecular Biology: Connexin Methods and Protocols, vol 154 2001 Humana Press Totwa, NJ 447 476
52. Schoeniger D: Spinal interleukin-6 as a potential mediator of HIV-1 gp120 induced exaggerated pain states. Boulder, CO, Department of Psychology and the Center for Neuroscience, University of Colorado, 2004, pp 1-76
53. J.S. Schweitzer, H. Wang, Z.Q. Xiong, J.L. Stringer pH Sensitivity of non-synaptic field bursts in the dentate gyrus J Neurophysiol 84 2000 927 933
54. P.M. Stewart, C.B. Whorwood, B.R. Walker Steroid hormones and hypertension: The cortisol-cortisone shuttle Steroids 58 1993 614 620
55. S.M. Sweitzer, D. Martin, J.A. DeLeo Intrathecal interleukin-1 receptor antagonist in combination with soluble tumor necrosis factor receptor exhibits an anti-allodynic action in a rat model of neuropathic pain Neuroscience 103 2001 529 539
56. M.C. Tresch, O. Kiehn Motor coordination without action potentials in the mammalian spinal cord Nat Neurosci 3 2000 593 599
57. B. Treutwein, H. Strasburger Fitting the psychometric function Percept Psychophys 61 1999 87 8106
58. A.D. VanHaarst, L.A. Welberg, W. Sutanto, M.S. Oitzl, E.R. DLoet 11 Beta-hydroxysteroid dehydrogenase activity in the hippocampus: Implications for in vivo corticosterone receptor binding and cell nuclear retention J Neuroendocrinol 8 1996 595 600
59. A. Verkhratsky, R.K. Orkand, H. Kettenmann Glial calcium: Homeostasis and signaling function Physiol Rev 78 1998 99 9141
60. S. Vesce, P. Bezzi, A. Volterra The active role of astrocytes in synaptic transmission Cell Mol Life Sci 56 1999 991 991000
61. W. Volknandt Vesicular release mechanisms in astrocytic signalling Neurochem Int 41 2002 301 306
62. L.R. Watkins, E.D. Milligan, S.F. Maier Glial activation: A driving force for pathological pain Trends Neurosci 24 2001 450 455
63. Watkins LR, Milligan ED, Maier SF: Immune and glial involvement in physiological and pathological exaggerated pain states, in Dostrovsky JO, Carr DB, Koltzenburg M (eds): Advances in Pain Research and Therapy. Seattle, WA, IASP Press, 2003, in press
64. M. Zimmermann Ethical guidelines for investigators of experimental pain in conscious animals Pain 16 1983 109 110