Differential connexin expression, gap junction intercellular coupling, and hemichannel formation in NT2/D1 human neural progenitors and terminally differentiated hNT neurons

Journal of Neuroscience Research

Volumn 72, Issue 3, 2003, Pages 393-404

  Boucher, Sherri ^a   Bennett, Steffany A L ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Connexin; Differentiation; Gap junction; Hemichannel; Progenitor

Indexed keywords

18ALPHA GLYCYRRHETINIC ACID; 4,4' DIISOTHIOCYANATOSTILBENE 2,2' DISULFONIC ACID; CHLORIDE CHANNEL; CONNEXIN 26; CONNEXIN 32; CONNEXIN 36; CONNEXIN 37; CONNEXIN 43; FLUFENAMIC ACID; GAP JUNCTION PROTEIN;

ARTICLE; CELL DIFFERENTIATION; CELL TRANSPLANTATION; CHANNEL GATING; GAP JUNCTION; HUMAN; HUMAN CELL; MEMBRANE CHANNEL; NERVE CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; STEM CELL; TERATOCARCINOMA;

ANTINEOPLASTIC AGENTS; BASE SEQUENCE; BLOTTING, WESTERN; CELL COMMUNICATION; CELL DIFFERENTIATION; CONNEXINS; GAP JUNCTIONS; GENE EXPRESSION; HUMANS; IMMUNOHISTOCHEMISTRY; MOLECULAR SEQUENCE DATA; NEURONS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEQUENCE HOMOLOGY; STEM CELLS; TERATOCARCINOMA; TRETINOIN; TUMOR CELLS, CULTURED;

EID: 0037405358     PISSN: 03604012     EISSN: None     Source Type: Journal    
DOI: 10.1002/jnr.10575     Document Type: Article

References (54)

1. Altevogt BM, Kleopas A, Postma FR, Scherer SS, Paul DL. 2002. Connexin29 is uniquely distributed within myelinating glial cells of the central and peripheral nervous system. J Neurosci 22:6458-6470.
2. Andrews PW, Damjanov I, Simon D, Banting GS, Carlin C, Dracopoli NC, Fogh J. 1984. Pluripotent embryonal carcinoma clones derived from the human teratocarcinoma cell line Tera-2. Lab Invest 50:147-162.
3. Baker KA, Hong M, Sadi D, Mendez I. 2000. Intrastriatal and intranigral grafting of hNT neurons in the 6-OHDA rat model of Parkinson's disease. Exp Neurol 162:350-360.
4. Baldassarre G, Boccia A, Bruni P, Sandomenico C, Barone MV, Pepe S, Angrisano T, Belletti B, Motti ML, Fusco A, Viglietto G. 2000. Retinoic acid induces neuronal differentiation of embryonal carcinoma cells by reducing proteasome-dependent proteolysis of the cyclin-dependent inhibitor p27. Cell Growth Differ 11:517-526.
5. Bani-Yaghoub M, Bechberger JF, Naus CCG. 1997. Reduction of connexin43 expression and dye-coupling during neuronal differentiation of human NTera2/Clone D1 Cells. J Neurosci Res 49:19-31.
6. Bani-Yaghoub M, Underhill TM, Naus CC. 1999a. Gap junction blockage interferes with neuronal and astroglial differentiation of mouse P19 embryonal carcinoma cells. Dev Genet 24:69-81.
7. Bani-Yaghoub M, Felker JM, Naus CC. 1999b. Human NT2/D1 cells differentiate into functional astrocytes. Neuroreport 10:3843-3846.
8. Bani-Yaghoub M, Bechberger JF, Underhill TM, Naus CCG. 1999c. The effects of gap junction blockage on neuronal differentiation of human NTera2/Clone D1 cell. Exp Neurol 156:16-32.
9. Bennett SAL, Chen J, Pappas BA, Roberts DCS, Tenniswood M. 1998. Alterations in platelet activating factor receptor expression associated with neuronal apoptosis in an in vivo model of excitotoxicity. Cell Death Differ 5:867-875.
10. Bennett SAL, Pappas BA, Stevens WD, Davidson CM, Fortin T, Chen J. 2000. Cleavage of amyloid precursor protein elicited by chronic cerebral hypoperfusion. Neurobiol Aging 21:207-214.
11. Bittman KS, LoTurco JJ. 1999. Differential regulation of connexin 26 and 43 in murine neocortical precursors. Cereb Cortex 9:188-195.
12. Bittman K, Owens DF, Kriegstein AR, LoTurco JJ. 1997. Cell coupling and uncoupling in the ventricular zone of the developing neocortex. J Neurosci 17:7037-7044.
13. Bruzzone R, White TW, Paul DL. 1996. Connections with connexins: the molecular basis of direct intercellular signaling. Eur J Biochem 238:1-27.
14. Castro C, Gomez-Hernandez JM, Silander K, Barrio LC. 1999. Altered formation of hemichannels and gap junction channels caused by C-terminal connexin-32 mutations. J Neurosci 19:3752-3760.
15. Crain B, Cotman C, Taylor D, Lynch G. 1973. A quantitative electron microscopic study of synaptogenesis in the dentate gyrus of the rat. Brain Res 63:195-204.
16. Dermietzel R, Spray DC. 1993. Gap junctions in the brain: where, what type, how many and why? Trends Neurosci 16:186-192.
17. Duffy HS, John GR, Lee SC, Brosnan CF, Spray DC. 2000. Reciprocal regulation of the junctional proteins claudin-1 and connexin43 by interleukin-1beta in primary human fetal astrocytes. J Neurosci 20: RC114.
18. Duval N, Gomes D, Calaora V, Calabrese A, Mead P, Bruzzone R. 2002. Cell coupling and Cx43 expression in embryonic mouse neural progenitor cells. J Cell Sci 115:3241-3251.
19. Ferrari A, Ehler E, Nitsch PM, Gotz J. 2000. Immature human NT2 cells grafted into mouse brain differentiate into neuronal and glial cell types. FEBS Lett 486:121-125.
20. Fulton BP. 1995. Gap junctions in the developing nervous system. Perspect Dev Neurobiol 12:327-334.
21. Gage FH. 2000. Mammalian neural stem cells. Science 267:1433-1438.
22. Garbuzova-Davis S, Willing AE, Milliken M, Saporta S, Zigova T, Cahill DW, Sanberg PR. 2002. Positive effect of transplantation of hNT neurons (NTera 2/D1 cell-line) in a model of familial amyotrophic lateral sclerosis. Exp Neurol 174:169-180.
23. Guthrie SC, Gilula NB. 1989. Gap junctional communication and development. Trends Neurosci 12:12-16.
24. Harris AL. 2001. Emerging issues of connexin channels: biophysics fills the gap. Q Rev Biophys 34:325-472.
25. Hurlbert MS, Gianani RI, Hutt C, Freed CR, Kaddis FG. 1999. Neural transplantation of hNT neurons for Huntington's disease. Cell Transplant 8:143-151.
26. Kammermans M, Fahrenfort I, Schultz K, Janssen-Bienhold U, Sjoerdsma T, Weiler R. 2001. Hemichannel-mediated inhibition in the outer retina. Science 292:1178-1180.
27. Larson DM, Seul KH, Berthoud VM, Lau AF, Sagar GD, Beyer EC. 2000. Functional expression and biochemical characterization of an epitopetagged connexin37. Mol Cell Biol Res Commun 3:115-121.
28. Lo Turco JJ, Kriegstein AR. 1991. Clusters of coupled neutralists in embryonic neocortex. Science 252:563-566.
29. Meltzer CC, Kondziolka D, Villemagne VL, Wechsler L, Goldstein S, Thurlbom KR, Gebel J, Elder EM, DeCesare S, Jacobs S. 2001. Serial [18F] fluorodeoxyglucose positron emission topography after human neuronal implantation for stroke. Neurosurgery 49:586-591.
30. Mercier F, Hatton GL. 2001. Connexin 26 and basic fibroblast growth factor are expressed primarily in the suppial and subependymal layers in adult brain parenchyma: roles in stem cell proliferation and morphological plasticity? J Comp Neurol 431:88-104.
31. Nadarajah B, Jones AM, Evans WH, Parnavelas JG. 1997. Differential expression of connexins during neocortical development and neuronal circuit formation. J Neurosci 17:3096-3111.
32. Nagy JI, Li X, Rempel J, Stelmack G, Patel D, Staines WA, Yasumaura T, Rash JE. 2001. Connexin26 in adult rodent central nervous system: demonstration at astrocytic gap junctions and colocalization with connexin30 and connexin43. J Comp Neurol 441:302-323.
33. Nelson PT, Kondziolka D, Wechsler L, Goldstein S, Gebel J, Decesare S, Elder EM, Zhang PJ, Jacobs A, McGrogan M, Lee VM, Trojanowski JO. 2002. Clonal human (hNT) neuron grafts for stroke therapy: neuropathology in a patient 27 months after implantation. Am J Pathol 160:1201-1206.
34. Peinado A. 2001. Immature neocortical neurons exist as extensive syncitial networks linked by dendrodendritic electrical connections. J Neurophysiol 85:620-629.
35. Peinado A, Yester R, Katz LC. 1993a. Extensive dye coupling between rat neocortical neurons during the period of circuit formation. Neuron 10:103-114.
36. Peinado A, Yuste R, Katz LC. 1993b. Gap junctional communication and the development of local circuits in neocortex. Cereb Cortex 3:488-498.
37. Pleasure SJ, Page C, Lee VM-Y. 1992. Pure, post mitotic, polarized human neurons derived from NTera 2 cells provide a system for expressing exogenous proteins in terminally differentiated neurons. J Neurosci 12: 1802-1815.
38. Plotkin LI, Manolagas SC, Bellido T. 2002. Transduction of cell survival signals by connexin-43 hemichannels. J Biol Chem 277:8648-8657.
39. Rash JE, Staines WA, Yasumura T, Patel D, Furman CS, Stelmack GL, Nagy JL. 2000. 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 97:7573-7578.
40. Rash JE, Yasumura T, Davidson KG, Furman CS, Dudek FE, Nagy JL. 2001. Identification of cells expressing Cx43, Cx30, Cx26, Cx32 and Cx36 in gap junctions of rat brain and spinal cord. Cell Adhes Commun 8:315-320.
41. Rozental R, Morales M, Mehler MF, Urban M, Kremer M, Dermeitzel R, Kessler JA, Spray DC. 1998. Changes in the properties of gap junctions during neuronal differentiation of hippocampal progenitor cells. J Neurosci 18:1753-1762.
42. Rozental R, Srinivas M, Gokhan S, Urban M, Dermietzel R, Kessler JA, Spray DC, Mehler MF. 2000. Temporal expression of neuronal connexins during hippocampal ontogeny. Brain Res Brain Res Rev 32:57-71.
43. Sandhu JK, Sikorska M, Walker PR. 2002. Characterization of astrocytes derived from human NTera-2/D1 embryonal carcinoma cells. J Neurosci Res 68:604-612.
44. Saporta S, Willing AE, Zigova T, Daadi MM, Sanberg PR. 2001. Comparison of calcium-binding proteins expressed in cultured hNT neurons and hNT neurons transplanted into the rat striatum. Exp Neurol 167:252-259.
45. Sodja C, Fang H, Dasgupta T, Ribecco M, Walker PR, Sikorska M. 2002. Identification of functional dopamine receptors in human teratocarcinoma NT2 cells. Brain Res Mol Brain Res 99:83-91.
46. Srinivas M, Rozental R, Kojima T, Dermietzel R, Mehler M, Condorelli DF, Kessler JA, Spray DC. 1999. Functional properties of channels formed by the neuronal gap junction protein connexin36. J Neurosci 19:9848-9855.
47. Stout CE, Costantin JL, Naus CC, Charles AC. 2002. Intercellular calcium signaling in astrocytes via ATP release through connexin hemichannels. J Biol Chem 22:10482-10488.
48. Temple S. 2001. The development of neural stem cells. Nature 414:112-117.
49. Teubner B, Degen J, Sohl G, Guldenagel M, Bukauskas FF, Trexler EB, Verselis VK, De Zeeuw CI, Lee CG, Kozak CA, Petrasch-Parwez E, Dermietzel R, Willecke K. 2000. Functional expression of the murine connexin 36 gene coding for a neuron-specific gap junctional protein. J Membrane Biol 176:249-262.
50. Teubner B, Odermatt B, Guldenagel M, Sohl G, Degen J, Bukauskas F, Kronengold J, Verselis VK, Jung YT, Kozak CA, Schilling K, Willecke K. 2001. Functional expression of the new gap junction gene connexin47 transcribed in mouse brain and spinal cord neurons. J Neurosci 21:1117-11126.
51. Traub O, Hertlein B, Kasper M, Eckert R, Krisciukaitis A, Hulser D, Willecke K. 1998. Characterization of the gap junction protein connexin37 in murine endothelium, respiratory epithelium, and after transfection in human HeLa cells. Eur J Cell Biol 77:313-322.
52. Valiunas V. 2002. Biophysical properties of connexin-45 gap junction hemichannels studies in vertebrate cells. J Gen Physiol 119:147-164.
53. Willecke K, Eiberger J, Degen J, Eckardt D, Romualdi A, Guldenagel M, Deutsch U, Sohl G. 2001. Structural and functional diversity of connexin genes in the mouse and human genome. Biol Chem 383:725-737.
54. Willing AE, Garbuzova-Davis S, Saporta S, Milliken M, Cahill DW, Sanberg PR. 2001. hNT neurons delay onset of motor deficits in a model of amyotrophic lateral sclerosis. Brain Res Bull 56:525-530.