Connexin47, connexin29 and connexin32 co-expression in oligodendrocytes and Cx47 association with zonula occludens-1 (ZO-1) in mouse brain

Neuroscience

Volumn 126, Issue 3, 2004, Pages 611-630

  Li, X ^a   Ionescu, A V ^a   Lynn, B D ^a   Lu, S ^a,c   Kamasawa, N ^b   Morita, M ^b   Davidson, K G V ^b   Yasumura, T ^b   Rash, J E ^b   Nagy, J I ^a  

^a UNIVERSITY OF MANITOBA   (Canada)

^b Department of Environmental and Radiological Health Sciences   (United States)

^c WEIFANG MEDICAL UNIVERSITY   (China)

Author keywords

2 ,3 cyclic nucleotide 3 phosphodiesterase; A A junctions; A O junctions; astrocyte to astrocyte gap junctions; astrocytes to oligodendrocytes gap junctions; CNPase; connexin32; connexin43; connexin47; Cx; gap junctions; glia; PDZ domains

Indexed keywords

CONNEXIN 29; CONNEXIN 32; CONNEXIN 47; GAP JUNCTION PROTEIN; PROTEIN; UNCLASSIFIED DRUG; ZONULA OCCLUDENS 1;

ANIMAL TISSUE; ARTICLE; ASTROCYTE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; GAP JUNCTION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; TISSUE DISTRIBUTION;

ANIMALS; ASTROCYTES; BLOTTING, WESTERN; BRAIN; CELL COMMUNICATION; CONNEXINS; FLUORESCENT ANTIBODY TECHNIQUE; FREEZE FRACTURING; GAP JUNCTIONS; HELA CELLS; HUMANS; MALE; MEMBRANE PROTEINS; MICE; MICROSCOPY, CONFOCAL; OLIGODENDROGLIA; PHOSPHOPROTEINS; RATS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPINAL CORD; TIGHT JUNCTIONS;

EID: 2942627583     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2004.03.063     Document Type: Article

References (73)

1. Aaku-Saraste E., Helwig A., Huttner W.B. Loss of occludin and functional tight junctions, but not ZO-1, during neural tube closure Remodeling of the neuroepithelium prior to neurogenesis. Dev Biol. 180:1996;664-679
2. Altevogt B.M., Kleopa K.A., Postma F.R., Scherer S.S., Paul D.L. Connexin29 is uniquely distributed within myelinating glial cells of the central and peripheral nervous systems. J Neurosci. 22:2002;6458-6570
3. Bahr M., Andres F., Timmerman V., Nelis M.E., Van Broeckhoven C., Dichgans J. Central visual, acoustic and motor pathway involvement in Charcot-Marie-Tooth family with an asn205ser mutation in the connexin32 gene. J Neurol Neurosurg Psychiatry. 66:1999;202-206
4. Bronstein J.M., Popper P., Micevych P.E., Farber D.B. Isolation and characterization of a novel oligodendrocyte-specific protein. Neurology. 47:1996;772-778
5. Bronstein J.M., Micevych P.E., Chen K. Oligodendrocyte-specific protein (OSP) is a major component of CNS myelin. J Neurosci Res. 50:1997;713-720
6. Condorelli D.F., Trovato-Salinaro A., Mudo G., Mirone M.B., Belluardo N. Cellular expression of connexins in the rat brain Neuronal localization, effects of kainate-induced seizures and expression in apoptotic cells. Eur J Neurosci. 18:2003;1807-1827
7. Dermietzel R., Schunke D., Leibstein A. The oligodendrocytic junctional complex. Cell Tissue Res. 193:1978;61-72
8. Dermietzel R., Krause D. Molecular anatomy of the blood-brain barrier as defined by immunocytochemistry. Int Rev Cytol. 127:1991;57-109
9. Filippov M.A., Hormuzdi S.G., Fuchs E.C., Moyer H. A reporter allele for investigating connexin26 gene expression in the mouse brain. Eur J Neurosci. 18:2003;3183-3192
10. Fujimoto K. Freeze-fracture replica electron microscopy combined with SDS digestion for cytochemical labeling of integral membrane proteins Application to the immunogold labeling of intercellular junctional complexes. J Cell Sci. 108:1995;3443-3449
11. Giepmans B.N., Moolenaar W.H. The gap junction protein connexin43 interacts with the second PDZ domain of the zonula occludens-1 protein. Curr Biol. 8:1998;931-934
12. Gonzalez-Mariscal L., Betanzos A., Nava P., Jaramillo B.E. Tight junction proteins. Prog Biophys Mol Biol. 81:2003;1-44
13. Goodenough D.A., Goliger J.A., Paul D.L. Connexins, connexons, and intercellular communication. Annu Rev Biochem. 65:1996;475-502
14. Gow A., Southwood C.M., Li J.S., Pariali M., Riordan G.P., Brodie S.E., Danias J., Bronstein J.M., Kachar B., Lazzarini R.A. CNS myelin and sertoli cell tight junction strands are absent in Osp/claudin-11 null mice. Cell. 99:1999;649-659
15. 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
16. Howarth A.G., Hughes M.R., Stevenson B.R. Detection of the tight junction-associated protein ZO-1 in astrocytes and other non-epithelial cell types. Am J Physiol. 262:1992;C461-C469
17. Inagaki M., Irie K., Deguchi-Tawarada M., Ikeda W., Ohtsuka T., Takeuchi M., Takai Y. Nectin-dependent localization of ZO-1 at puncta adhaerentia junctions between the mossy fiber terminals and the dendrites of the pyramidal cells in the CA3 area of adult mouse hippocampus. J Comp Neurol. 460:2003;514-524
18. Itoh M., Yonemura S., Nagafuchi A., Tsukita S., Tsukita S. A 220-kD undercoat-constitutive protein Its specific localization at cadherin-based cell-cell adhesion sites. J Cell Biol. 115:1991;1449-1462
19. Itoh M., Nagafuchi A., Yonemura S., Kitani-Yasuda T., Tsukita S., Tsukita S. The 220-kD protein colocalizing with cadherins in nonepithelial cells is identical to ZO-1, a tight junction-associated protein in epithelial cells cDNA cloning and immunoelectron microscopy. J Cell Biol. 121:1993;491-502
20. Kausalya P.J., Reichert M., Hunziker W. Conneixn45 directly binds to ZO-1 and localizes to the tight junction region in epithelial MDCK cells. FEBS Lett. 505:2001;92-96
21. Kumar N.M., Gilula N.B. The gap junction communication channel. Cell. 84:1996;381-388
22. Laing J.G., Manley-Markowski R.N., Koval M., Civitelli R., Steinberg T.H. Connexin45 interacts with zonula occludens-1 and connexin43 in osteoblastic cells. J Biol Chem. 276:2001;23051-23055
23. Li J., Hertzberg E.L., Nagy J.I. Connexin32 in oligodendrocytes and association with myelinated fibers in mouse and rat brain. J Comp Neurol. 379:1997;571-591
24. Li W.E.I., Ochalski P.A.Y., Hertzberg E.L., Nagy J.I. Immunorecognition, ultrastructure and phosphorylation status of astrocytic gap junctions and connexin43 in rat brain after cerebral focal ischemia. Eur J Neurosci. 10:1998;2444-2463
25. Li X., Lynn B.D., Olson C., Meier C., Davidson K.G., Yasumura T., Rash J.E., Nagy J.I. Connexin29 expression, immunocytochemistry and freeze-fracture replica immunogold labelling (FRIL) in sciatic nerve. Eur J Neurosci. 16:2002;795-806
26. Li X., Olson C., Lu S., Kamasawa N., Yasamura T., Rash J.E., Nagy J.I. Neuronal connexin36 association with zonula occludens-1 protein (Z0-1) in mouse brain and interaction with the first PDZ domain of ZO-1. Eur J Neurosci. 19:2004;2132-2146
27. Lynn B.D., Li X., Cattini P.A., Turley E.A., Nagy J.I. Identification of sequence, protein isoforms, and distribution of the hyaluronan-binding protein RHAMM in adult and developing rat brain. J Comp Neurol. 439:2001;315-330
28. Lynn B.D., Rempel J.L., Nagy J.I. Enrichment of neuronal and glial connexins in the postsynaptic density subcellular fraction of rat brain. Brain Res. 898:2001;1-8
29. Massa P.T., Mugnaini E. Cell junctions and intramembrane particles of astrocytes and oligodendrocytes A freeze-fracture study. Neuroscience. 7:1982;523-538
30. Meier C.R., Dermietzel R., Davidson K.G.V., Yasamura T., Rash J.E. Connexin32-containing gap junctions in Schwann cells at the internodal zone of myelin compaction and in Schmidt-Lanterman incisures. J Neurosci. 24:2004;3186-3198
31. Menichella D.M., Goodenough D.A., Sirkowski E., Scherer S.S., Paul D.L. Connexins are critical for normal myelination in the CNS. J Neurosci. 23:2003;5963-5973
32. Miragall F., Krause D., de Vries U., Dermietzel R. Expression of the tight junction protein ZO-1 in the olfactory system Presence of ZO-1 on olfactory sensory neurons and glial cells. J Comp Neurol. 341:1994;433-448
33. Mitic L.L., Anderson J.M. Molecular architecture of tight junctions. Annu Rev Physiol. 60:1998;121-142
34. Morita K., Sasaki H., Fujimoto K., Furuse M., Tsukita S. Claudin-11/OSP-based tight junctions of myelin sheaths in brain and Sertoli cells in testis. J Cell Biol. 145:1999;579-588
35. Mugnaini E. 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. Fedoroff S., Vernadakis A. Astrocytes, Vol. I. 1986;329-371 New York Academic Press, New York
36. Musil L.S., Goodenough D.A. Biochemical analysis of connexin43 intracellular transport, phosphorylation, and assembly into gap junctional plaques. J Cell Biol. 115:1991;1357-1374
37. Nagy J.I., Patel D., Ochalski P.A., 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
38. Nagy J.I., Rash J.E. Connexins and gap junctions of astrocytes and oligodendrocytes in the CNS. Brain Res Rev. 32:2000;29-44
39. Nagy J.I., Li X., Rempel J., Stelmack G., Patel D., Staines W.A., Yasumura T., Rash J.E. 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
40. Nagy J.I., Ionescu A.V., Lynn B.D., Rash J.E. Connexin29 and connexin32 at oligodendrocyte and astrocyte gap junctions and in myelin of the mouse central nervous system. J Comp Neurol. 464:2003;356-370
41. Nagy J.I., Ionescu A.V., Lynn B.D., Rash J.E. Coupling of astrocyte connexins Cx26, Cx30, Cx43 to oligodendrocyte Cx29, Cx32, Cx47 Implications from normal and connexin32 knockout mice. Glia. 44:2003;205-218
42. Nagy JI, Dudek FE, Rash JE (2004) Update on connexins and gap junctions in neurons and glia in the nervous system. Brain Res Rev, in press.
43. Nielsen P.A., Beahm D.L., Giepmans B.N., Baruch A., Hall J.E., Kumar N.M. Molecular cloning, functional expression, and tissue distribution of a novel human gap junction-forming protein, connexin-31.9 Interaction with zona occludens protein-1. J Biol Chem. 277:2002;38272-38283
44. Nielsen P.A., Baruch A., Shestopalov V.I., Giepmans B.N., Benedetti E.I., Kumar N.M. Lens connexins Cx46 and Cx50 interact with zonula occludens protein-1 (ZO-1). Mol Biol Cell. 14:2003;2470-2481
45. Odermatt B., Wellershaus K., Wallraff A., Seifert G., Degen J., Euwens C., Fuss B., Bussow H., Schilling K., Steinhauser C., Willecke K. Connexin 47 (Cx47)-deficient mice with enhanced green fluorescent protein reporter gene reveal predominant oligodendrocytic expression of Cx47 and display vacuolized myelin in the CNS. J Neurosci. 23:2003;4549-4559
46. Pastor A., Kremer M., Möller T., Kettenmann H., Dermietzel R. Dye-coupling between spinal cord oligodendrocytes is restricted to gray matter Indication for functional autocellular territories in white matter oligodendrocytes. Glia. 24:1998;108-120
47. Pereda A., O'Brien J., Nagy J.I., Bukauskas F., Davidson K.G.V., Yasumura T., Rash J.E. Connexin35 mediates electrical transmission at mixed synapses on Mauthner cells. J Neurosci. 23:2003;7489-7503
48. Petrov T., Howarth A.G., Krukoff T.L., Stevenson B.R. Distribution of the tight junction-associated protein ZO-1 in circumventricular organs of the CNS. Mol Brain Res. 21:1994;235-246
49. 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 system, with evidence for a "panglial syncytium" that is not coupled to neurons. J Comp Neurol. 388:1997;265-292
50. Rash J.E., Yasumura T. Direct immunogold labeling of connexins and aquaporin4 in freeze-fracture replicas of liver, brain and spinal cord: factors limiting quantitative analysis. Cell Tissue Res. 296:1999;307-321
51. Rash J.E., Yasumura T., Dudek F.E. Ultrastructure, histological distribution, and freeze-fracture immunocytochemistry of gap junctions in rat brain and spinal cord. Cell Biol Internat. 22:1998;731-749
52. Rash J.E., Staines W.A., Yasumura T., Patel D., Furman C.S., Stelmack G.L., Nagy J.I. Immunogold evidence that neuronal gap junctions in adult rat brain and spinal cord contain connexin-36 but not connexin-32 or connexin-43. Proc Natl Acad Sci USA. 97:2000;7573-7578
53. Rash J.E., Yasumura T., Dudek F.E., Nagy J.I. Cell-specific expression of connexins and evidence of restricted gap junctional coupling between glial cells and between neurons. J Neurosci. 15:2001;1983-2000
54. Rash JE, Pereda A, Kamasawa N, Furman CS, Yasumura T, Davidson KGV, Dudek FE, Olson C, Li X, Nagy JI (2004) High-resolution proteomic mapping in the vertebrate central nervous system: close proximity of connexin35 to NMDA glutamate receptor clusters and co-localization of connexin36 with immunoreactivity for zonula occludens protein-1 (ZO-1). J Neurocytol, in press.
55. Saitou M., Ando-Akatsuka Y., Itoh M., Furuse M., Inazawa J., Fujimoto K., Tsukita S. Mammalian occludin in epithelial cells Its expression and subcellular distribution. Eur J Cell Biol. 73:1997;222-231
56. Scadding J.W. Development of ongoing activity, mechanosensitivity, and adrenaline sensitivity in severed peripheral nerve axons. Exp Neurol. 73:1981;345-364
57. Scherer S.S., Deschenes S.M., Xu Y.T., Grinspan J.B., Fischbeck K.H., Paul D.L. Connexin32 is a myelin-related protein in the PNS and CNS. J Neurosci. 15:1995;8281-8294
58. Shinowara N.L., Beutel W.B., Revel J.P. Comparative analysis of junctions in the myelin sheath of central and peripheral axons of fish, amphibians and mammals A freeze-fracture study using complementary replicas. J Neurocytol. 9:1980;15-38
59. Smith G.M., Shine H.D. Immunofluorescent labeling of tight junctions in the rat brain and spinal cord. Int J Dev Neurosci. 10:1992;387-392
60. Spray D.C., Dermietzel R. X-linked dominant Charcot-Marie-Tooth disease and other potential gap junction diseases of the nervous system. Trends Neurosci. 18:1995;256-262
61. Stevenson B.R., Siliciano J.D., Mooseker M.S., Goodenough D.A. Identification of ZO-1 A high molecular weight polypeptide associated with the tight junction (zonula occludens) in a variety of epithelia. J Cell Biol. 103:1986;755-766
62. Teubner B., Odermatt B., Guldenagel M., Sohl G., Degen J., Bukauskas F., Kronengold J., Verselis V.K., Jung Y.T., Kozak C.A., Schilling K., Willecke K. Functional expression of the new gap junction gene connexin47 transcribed in mouse brain and spinal cord neurons. J Neurosci. 21:2001;1117-1126
63. Thomas M.A., Huang S., Cokoja A., Riccio O., Staub O., Suter S., Chanson M. Interaction of connexins with protein partners in the control of channel turnover and gating. Biol Cell. 94:2002;445-456
64. Tiwari-Woodruff S.K., Buznikov A.G., Vu T.Q., Micevych P.E., Chen K., Kornblum H.I., Bronstein J.M. OSP/claudin-11 forms a complex with a novel member of the tetraspanin super family and beta1 integrin and regulates proliferation and migration of oligodendrocytes. J Cell Biol. 153:2001;295-305
65. 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;12725-12731
66. Verity A.N., Campagnoni A.T. Regional expression of myelin protein genes in the developing mouse brain In situ hybridization studies. J Neurosci Res. 21:1988;238-248
67. Vorbrodt A.W., Dobrogowska D.H. Molecular anatomy of intercellular junctions in brain endothelial and epithelial barriers Electron microscopist's view. Brain Res Rev. 42:2003;221-242
68. White T.W., Bruzzone R. Multiple connexin proteins in single intercellular channels Connexin compatibility and functional consequences. J Bioenerg Biomemb. 28:1996;339-350
69. Willecke K., Eiberger J., Degen J., Eckardt D., Romualdi A., Guldenagel M., Deutsch U., Sohl G. Structural and functional diversity of connexin genes in the mouse and human genome. Biol Chem. 383:2002;725-737
70. Wolburg H., Lippoldt A. Tight junctions of the blood-brain barrier Development, composition and regulation. Vascul Pharmacol. 38:2002;323-337
71. 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
72. 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
73. Zhurinsky J., Shtutman M., Ben-Ze'ev A. Differential mechanisms of LEF/TCF family-dependent transcriptional activation by beta-catenin and plakoglobin. Mol Cell Biol. 20:2000;4238-4252