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

Volumn 97, Issue 1, 2000, Pages 113-123

  Li, W E I ^a   Nagy, J I ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

Author keywords

Astrocytes; Connexin 43; Gap junctions; Nerve stimulation; Neuron astrocyte interaction; Phosphorylation

Indexed keywords

BUPIVACAINE; CAPSAICIN; CONNEXIN 43; EPITOPE; LOCAL ANESTHETIC AGENT; MONOCLONAL ANTIBODY; POLYCLONAL ANTIBODY; TETRODOTOXIN;

AFFERENT NERVE GROUP 1; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; ASTROCYTE; CELL COMMUNICATION; CELL INTERACTION; CONTROLLED STUDY; DEPHOSPHORYLATION; ELECTRON MICROSCOPY; GAP JUNCTION; GLIA CELL; IMMUNOHISTOCHEMISTRY; LUMBAR SPINAL CORD; MALE; MICROSCOPY; NERVE CELL; NERVE FIBER C; NERVE STIMULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT; REGULATORY MECHANISM; SCIATIC NERVE; SPINAL CORD DORSAL HORN; WESTERN BLOTTING;

ANIMALS; ASTROCYTES; BLOTTING, WESTERN; CONNEXIN 43; ELECTRIC STIMULATION; GAP JUNCTIONS; IMMUNOHISTOCHEMISTRY; MALE; MICROSCOPY, ELECTRON; NERVE FIBERS; NOCICEPTORS; POSTERIOR HORN CELLS; RATS; RATS, SPRAGUE-DAWLEY; SCIATIC NERVE; SPINAL CORD;

EID: 0034076871     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(00)00032-4     Document Type: Article

References (71)

1. Beyer E.C., Paul D.L., Goodenough D.A. Connexin43: a protein from rat heart homologous to a gap junction protein from liver. J. Cell Biol. 105:1987;2621-2629.
2. Blenk K.H., Janig W., Michaelis M., Vogel C. Prolonged injury discharge in unmyelinated nerve fibres following transection of the sural nerve in rats. Neurosci. Lett. 215:1996;185-188.
3. Bruzzone B., White T.W., Paul D.L. Connections with connexins: the molecular basis of direct intercellular signalling. Eur. J. Biochem. 238:1996;1-27.
4. Campos de Carvalho A.C., Roy C., Hertzberg E.L., Tanowitz H.B., Kessler J.A., Weiss L.M., Wittner M., Dermietzel R., Gao Y., Spray D.C. Gap junction disappearance in astrocytes and leptomeningeal cells as a consequence of protozoan infection. Brain Res. 790:1998;304-314.
5. Chisamore B., Solc M., Dow K. Excitatory amino acid regulation of astrocyte proteoglycans. Devl Brain Res. 97:1996;22-28.
6. Cotrina M.L., Kang J., Lin J.H.C., Bueno E., Hansen T.W., He L., Liu Y., Nedergaard M. Astrocytic gap junctions remain open during ischemic conditions. J. Neurosci. 18:1998;2520-2537.
7. Crow D.S., Beyer E.C., Paul D.L., Kobe S.S., Lau A.F. Phosphorylation of connexin43 gap junction protein in uninfected and Rous sarcoma virus-transformed mammalian fibroblasts. Molec. cell. Biol. 10:1990;1754-1763.
8. Cruciani V., Mikalsen S.O. Stimulated phosphorylation of intracellular connexin43. Expl Cell Res. 251:1999;285-298.
9. Enkvist M.O., McCarthy K.D. Activation of protein kinase C blocks astroglial gap junction communication and inhibits the spread of calcium waves. J. Neurochem. 59:1992;519-526.
10. Giaume C., McCarthy K.D. Control of gap-junctional communication in astrocytic networks. Trends Neurosci. 19:1996;319-325.
11. Giaume C., Tabernero A., Medina J.M. Metabolic trafficking through astrocytic gap junctions. Glia. 21:1997;114-123.
12. Giepmans B.N., Moolenaar W.H. The gap junction protein connexin43 interacts with the second PDZ domain of the zona occludens-1 protein. Curr. Biol. 8:1998;931-934.
13. Godwin A.J., Green L.M., Walsh M.P., McDonald J.R., Walsh D.A., Fletcher W.H. In situ regulation of cell-cell communication by the cAMP-dependent protein kinase and protein kinase C. Molec. cell. Biochem. 127/128:1993;293-307.
14. Goldberg G.S., Lau A.F. Dynamics of connexin43 phosphorylation in pp60v-src-transformed cells. Biochem. J. 295:1993;735-742.
15. Goodenough D.A., Goliger J.A., Paul D.L. Connexins, connexons, and intercellular communication. A. Rev. Biochem. 65:1996;475-502.
16. Hofer A., Saez J.C., Chang C.C., Trosko J.E., Spray D.C., Dermietzel R. C-erbB2/neu transfection induces gap junctional communication incompetence in glial cells. J. Neurosci. 16:1996;4311-4321.
17. Hosli E., Hosli L. Receptors for neurotransmitters on astrocytes in the mammalian central nervous system. Prog. Neurobiol. 40:1993;477-506.
18. Hossain M.Z., Murphy L.J., Nagy J.I. Phosphorylated forms of connexin43 predominate in rat brain: demonstration by rapid inactivation of brain metabolism. J. Neurochem. 62:1994;2394-2403.
19. Hossain M.Z., Peeling J., Sutherland G.R., Hertzberg E.L., Nagy J.I. Ischemia-induced cellular redistribution of the astrocytic gap junctional protein connexin43 in rat brain. Brain Res. 652:1994;311-322.
20. Kasuya Y., Abe Y., Hama H., Sakurai T., Asada S., Masaki T., Goto K. Endothelin-1 activates mitogen-activated protein kinases through two independent signalling pathways in rat astrocytes. Biochem. biophys. Res. Commun. 204:1994;1325-1333.
21. Kenins P. Responses of single nerve fibres to capsaicin applied to the skin. Neurosci. Lett. 29:1982;83-88.
22. Kimelberg H.K. Receptors on astrocytes - what possible functions? Neurochem. Int. 26:1995;27-40.
23. Konietzko U., Muller C.M. Astrocytic dye coupling in rat hippocampus: topography, developmental onset, and modulation by protein kinase C. Hippocampus. 4:1994;297-306.
24. Kriz N., Sykova E., Ujec E., Vyklicky L. Changes of extracellular potassium concentration induced by neuronal activity in the spinal cord of the cat. J. Physiol. 238:1974;1-15.
25. Kumar N.M., Gilula N.B. The gap junction communication channel. Cell. 84:1996;381-388.
26. Laird D.W., Puranam K.L., Revel J.-P. Turnover and phosphorylation dynamics of connexin43 gap junction protein in cultured cardiac myocytes. Biochem. J. 273:1991;67-72.
27. Laird J.M.A., Bennett G.J. An electrophysiological study of dorsal horn neurons in the spinal cord of rats with an experimental peripheral neuropathy. J. Neurophysiol. 69:1993;2072-2085.
28. Lau A.F., Kurata W.E., Kanemitsu M.Y., Loo L.W.M., Warn-Cramer B.J., Eckhart W., Lampe P.D. Regulation of connexin43 function by activated tyrosine protein kinases. J. Bioenerg. Biomembr. 28:1996;359-368.
29. Lazarini F., Strosberg A.D., Couraud P.O., Cazaubon S.M. Coupling of ETB endothelin receptor to mitogen-activated protein kinase stimulation and DNA synthesis in primary cultures of rat astrocytes. J. Neurochem. 66:1996;459-465.
30. Li W.E.I., Ochalski P.A.Y., Hertzberg E.L., Nagy J.I. Immunorecognition, ultrastructure and phorphorylation status of astrocytic gap junctions and connexin43 in rat brain after cerebral focal ischaemia. Eur. J. Neurosci. 10:1998;2444-2463.
31. Lynn B., Ye W., Cotsell B. The actions of capsaicin applied topically to the skin of the rat on C-fibre afferents, antidromic vasodilatation and substance P levels. Br. J. Pharmac. 107:1992;400-406.
32. Marrero H., Orkand R.K. Nerve impulses increase glial intercellular permeability. Glia. 16:1996;285-289.
33. Martinez A.D., Saez J.C. Arachidonic acid-induced dye uncoupling in rat cortical astrocytes is mediated by arachidonic acid byproducts. Brain Res. 816:1999;411-423.
34. Mikalsen S.-O., Husoy T., Vikhamar G., Sanner T. Induction of phosphotyrosine in the gap junction protein, connexin43. Fedn Eur. Biochem. Socs Lett. 401:1997;271-275.
35. Moreno A.P., Saez J.C., Fishman G.I., Spray D.C. Human connexin43 gap junction channels: regulation of unitary conductances by phosphorylation. Circulation Res. 74:1994;1050-1057.
36. Mugnaini E. (1986) Cell junctions of astrocytes, ependyma, and related cells in the mammalian central nervous system with emphasis on the hypothesis of a generalized functional syncytium of supporting cells. In: Astrocytes, (eds Fedoroff S. and Vernadakis A.), Vol. 1. Academic, New York.
37. Musil L.S., Cunningham B.A., Edelman G.M., Goodenough D.A. Differential phosphorylation of the gap junction protein connexin43 in junctional communication-competent and -deficient cell lines. J. Cell Biol. 111:1990;2077-2088.
38. Mussini J., Biral D., Marin O., Furlan S., Salvatori S. Myotonic dystrophy protein kinase expressed in rat cardiac muscle is associated with sarcoplasmic reticulum and gap junctions. J. Histochem. Cytochem. 47:1999;383-392.
39. Nagy J. I. and Dermietzel R. (2000) Gap junctions and connexins in the mammalian central nervous system. In Advances in Molecular and Cell Biology (ed. Hertzberg E. L.), Vol. 18. JAI, New York (in press).
40. Nagy J.I., Li W.E.I., Roy C., Doble B.W., Gilchrist J.S., Kardami E., Hertzberg E.L. Selective monoclonal antibody recognition and cellular localization of an unphosphorylated form of connexin43. Expl Cell Res. 236:1997;127-136.
41. Nagy J.I., Patel D., Ochalski P.A.Y., Li J., Hertzberg E.L. Evidence for the co-localization of another connexin with connexin-43 at astrocytic gap junctions in rat brain. Neuroscience. 78:1997;533-548.
42. Nagy J.I., Patel D., Ochalski P.A.Y., Stelmack G.L. Connexin30 in rodent, cat and human brain: selective expression in gray matter astrocytes, co-localization with connexin43 at gap junctions and late developmental appearance. Neuroscience. 88:1999;447-468.
43. Nagy J.I., Rash J.E. Connexins and gap junctions of astrocytes and oligodendrocytes in the CNS. Brain Res. Rev. 2000;. (in press).
44. Nagy J.I., Yamamoto T., Sawchuk M.A., Nance D.M., Hertzberg E.L. Quantitative immunohistochemical and biochemical correlates of connexin43 localization in rat brain. Glia. 5:1992;1-9.
45. Newman E.A. Regulation of potassium levels by glial cells in the retina. Trends Neurosci. 8:1985;156-159.
46. Ochalski P.A.Y., Frankenstein U.N., Hertzberg E.L., Nagy J.I. Connexin-43 in rat spinal cord: localization in astrocytes and identification of heterotypic astro-oligodendrocytic gap junctions. Neuroscience. 76:1997;931-945.
47. Ochalski P.A.Y., Sawchuk M.A., Hertzberg E.L., Nagy J.I. Astrocytic gap junction removal, connexin43 redistribution, and epitope masking at excitatory amino acid lesion sites in rat brain. Glia. 14:1995;279-294.
48. Oelze I., Kartenbeck J., Crusius K., Alonso A. Human papillomavirus type 16 E5 protein affects cell-cell communication in an epithelial cell line. J. Virol. 69:1995;4489-4494.
49. Orkand R.K., Nicholls J.G., Kuffler S.W. Effect of nerve impulses on the membrane potential of glial cells in the central nervous system of amphibia. J. Neurophysiol. 29:1966;788-806.
50. Rash J.E., Duffy H.S., Dudek F.E., Bilhartz B.L., Whalen L.R., Yasumura T. Grid-mapped freeze-fracture analysis of gap junctions in gray and white matter of adult rat central nervous sytem, with evidence for a "panglial syncytium" that is not coupled to neurons. J. comp. Neurol. 388:1997;265-292.
51. Rohlmann A., Laskawi R., Hofer A., Dobo E., Dermietzel R., Wolff J.R. Facial nerve lesions lead to increased immunostaining of the astrocytic gap junction protein (connexin 43) in the corresponding facial nucleus of rats. Neurosci. Lett. 154:1993;206-208.
52. Rohlmann A., Laskawi R., Hofer A., Dermietzel R., Wolff J.R. Astrocytes as rapid sensors of peripheral axotomy in the facial nucleus of rats. NeuroReport. 5:1994;409-412.
53. + concentration in astrocytes. Glia. 20:1997;299-307.
54. Saez J. C., Berthoud V. M., Moreno A. P. and Spray D. C. (1993) Gap junctions: multiplicity of controls in differentiated and undifferentiated cells and possible functional implications. In: (eds Shenolikar S. and Nairn A. C.), Vol. 27. Advances in Second Messenger and Phosphoprotein Research, Raven, New York.
55. Saez J.C., Nairn A.C., Czernik A.J., Fishman G.I., Spray D.C., Hertzberg E.L. Phosphorylation of connexin43 and the regulation of neonatal rat cardiac myocyte gap junctions. J. molec. cell. Cardiol. 29:1997;2131-2145.
56. Sawchuk M.A., Hossain M.Z., Hertzberg E.L., Nagy J.I. In situ transblot and immunocytochemical comparisons of astrocytic connexin43 responses to NMDA and kainic acid in rat brain. Brain Res. 683:1995;153-157.
57. Szolcsanyi J. Selective responsiveness of polymodal nociceptors of the rabbit ear to capsaicin, bradykinin and ultraviolet radiation. J. Physiol. 388:1987;9-23.
58. Tabernero A., Giaume C., Medino J.M. Endothelin-1 regulates glucose utilization in cultured rat astrocytes by controlling intercellular communication through gap junctions. Glia. 16:1996;187-195.
59. Theriault E., Frankenstein U.N., Hertzberg E.L., Nagy J.I. Connexin43 and astrocytic gap junctions in the rat spinal cord after acute compression injury. J. comp. Neurol. 382:1997;199-214.
60. Toyofuku T., Yabuki M., Otsu K., Kuzuya T., Hori M., Tada M. Direct association of the gap junction protein connexin-43 with ZO-1 in cardiac myocytes. J. biol. Chem. 273:1998;12,725-12,731.
61. Tsacopoulos M., Magistretti P.J. Metabolic coupling between glia and neurons. J. Neurosci. 16:1996;877-885.
62. Unger V.M., Kumar N.M., Gilula N.B., Yeager M. Electron cryo-crystallography of a recombinant cardiac gap junction channel. Novartis Foundation Symp. 219:1999;22-37.
63. Vukelic J.I., Yamamoto T., Hertzberg E.L., Nagy J.I. Depletion of connexin43-immunoreactivity in astrocytes after kainic acid-induced lesions in rat brain. Neurosci. Lett. 130:1991;120-124.
64. Vyklicky L., Sykova E., Kriz N., Ujec E. Post-stimulation changes of extracellular potassium concentration in the spinal cord of the rat. Brain Res. 45:1972;608-611.
65. Wall P.D., Waxman S., Basbaum A. Ongoing activity in peripheral nerve: injury discharge. Expl. Neurol. 45:1974;576-589.
66. Walz W. Role of glial cells in the regulation of the brain ion microenvironment. Prog. Neurobiol. 33:1989;309-333.
67. Wolburg H., Rohlmann A. Structure-function relationships in gap junctions. Int. Rev. Cytol. 157:1995;315-373.
68. Woolf C.J., Fitzgerald M. The properties of neurones recorded in the superficial dorsal horwn of the rat spinal cord. J. comp. Neurol. 221:1983;313-328.
69. Woolf C.J., King A.E. Physiology and morphology of multireceptive neurons with C-afferent fiber inputs in the deep dorsal horn of the rat lumbar spinal cord. J. Neurophysiol. 58:1987;460-479.
70. Yamamoto T., Ochalski A., Hertzberg E.L., Nagy J.I. LM and EM immunolocalization of the gap junctional protein connexin 43 in rat brain. Brain Res. 508:1990;313-319.
71. Yamamoto T., Ochalski A., Hertzberg E.L., Nagy J.I. On the organization of astrocytic gap junctions in rat brain as suggested by LM and EM immunohistochemistry of connexin43 expression. J. comp. Neurol. 302:1990;853-883.