Connexin hemichannel composition determines the FGF-1-induced membrane permeability and free [Ca2+]i responses

Molecular Biology of the Cell

Volumn 19, Issue 8, 2008, Pages 3501-3513

  Schalper, Kurt A ^a   Palacios Prado, Nicolás ^a   Retamal, Mauricio A ^a   Shoji, Kenji F ^a   Martínez, Agustín D ^b   Sáez, Juan C ^a  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b UNIVERSIDAD DE VALPARAÍSO   (Chile)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; CONNEXIN 26; CONNEXIN 43; CONNEXIN 45; FIBROBLAST GROWTH FACTOR 1; MAGNESIUM ION; MITOGEN ACTIVATED PROTEIN KINASE P38; VANILLOID RECEPTOR 1;

ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CARBOXY TERMINAL SEQUENCE; CELL DENSITY; CELL MEMBRANE PERMEABILITY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME ACTIVATION; FEMALE; HELA CELL; HUMAN; HUMAN CELL; PHYSIOLOGY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION;

CALCIUM; CELL MEMBRANE; CONNEXIN 43; CONNEXINS; ELECTROPHYSIOLOGY; ENZYME ACTIVATION; FIBROBLAST GROWTH FACTOR 1; HELA CELLS; HUMANS; MICROSCOPY, FLUORESCENCE; MODELS, BIOLOGICAL; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PERMEABILITY; PROTEIN STRUCTURE, TERTIARY;

EID: 54249087709     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E07-12-1240     Document Type: Article

References (53)

1. Bao, L., Locovei, S., and Dahl, G. (2004a). Pannexin membrane channels are mechanosensitive conduits for ATP. FEBS Lett. 572, 65-68.
2. Bao, X., Reuss, L., Altenberg, G. A. (2004b). Regulation of purified and reconstituted connexin 43 hemichannels by protein kinase C-mediated phosphorylation of Serine 368. J. Biol. Chem. 279, 20058-20066.
3. Böttcher, R. T., and Niehrs, C. (2005). Fibroblast growth factor signaling during early vertebrate development. Endocr. Rev. 26, 63-77.
4. Bradshaw, S. L., Naus C. C., Zhu, D., Kidder, G. M., D'Ercole, A. J., and Han, V. K. (1993). Alterations in the synthesis of insulin-like growth factor binding proteins and insulin-like growth factors in rat C6 glioma cells transfected with a gap junction connexin43 cDNA. Regul. Pept. 48, 99-112.
5. Cario-Toumaniantz, C., Loirand, G., Ladoux, A., and Pacaud, P. (1998). P2X7 receptor activation-induced contraction and lysis in human saphenous vein smooth muscle. Circ. Res. 83, 196-203.
6. Contreras, J. E., Sánchez, H. A., Eugenín, E. A., Speidel, D., Theis, M., Willecke, K., Bukauskas, F. F., Bennett, M. V., and Sáez, J. C. (2002). Metabolic inhibition induces opening of unapposed connexin 43 gap junction hemichannels and reduces gap junctional communication in cortical astrocytes in culture. Proc. Natl. Acad. Sci. USA 99, 495-500.
7. Contreras, J. E., Sáez, J. C., Bukauskas, F. F., and Bennett, M. V. (2003). Gating and regulation of connexin 43 (Cx43) hemichannels. Proc. Natl. Acad. Sci. USA 100, 11388-11393.
8. Corvalán, L. A., Araya, R., Brañes, M. C., Sáez, P. J., Kalergis, A. M., Tobar, J. A., Theis, M., Willecke, K., and Sáez, J. C. (2007). Injury of skeletal muscle and specific cytokines induce the expression of gap junction channels in mouse dendritic cells. J. Cell Physiol. 211, 649-660.
9. Coumoul, X., and Deng, C. X. (2003). Roles of FGF receptors in mammalian development and congenital diseases. Birth Defects Res. C. Embryo. Today 69, 286-304.
10. Dailey, L., Ambrosetti, D., Mansukhani, A., and Basilico, C. (2005). Mechanisms underlying differential responses to FGF signaling. Cytokine Growth Factor Rev. 16, 233-247.
11. De Vuyst, E., Decrock, E., Cabooter, L., Dubyak, G. R., Naus, C. C., Evans, W. H., and Leybaert, L. (2006). Intracellular calcium changes trigger connexin 32 hemichannel opening. EMBO J. 25, 34-44.
12. De Vuyst, E., Decrock, E., De Bock, M., Yamasaki, H., Naus, C. C., Evans, W. H., and Leybaert, L. (2007). Connexin hemichannels and gap junction channels are differentially influenced by lipopolysaccharide and basic fibroblast growth factor. Mol. Biol. Cell 18, 34-46.
13. Elfgang, C., Eckert, R., Lichtenberg-Frate, H., Butterweck, A., Traub, O., Klein, R. A., Hulser, D. F., and Willecke, K. (1995). Specific permeability and selective formation of gap junction channels in connexin-transfected HeLa cells. J. Cell Biol. 129, 805-817.
14. Evans, W. H., De Vuyst, E., and Leybaert, L. (2006). The gap junction cellular internet: connexin hemichannels enter the signalling limelight. Biochem. J. 397, 1-14.
15. 2+ entry and embryonic rat neural stem cell proliferation. J. Neurosci. 25, 2687-2701.
16. Garré, J. M., Retamal, M. A., Schalper, K., Barbeito, L., Bennett, M. V., Cassina, P., Sáez, J. C., and Abdura, V. (2006). FGF-1 and ATP increase permeability of spinal cord astrocytes in culture via P2X receptors and connexin-based hemichannels. Society for Neuroscience 2006 Abstract Viewer Program/Poster 136.8/D26.
17. González, H. E., Eugenín, E. A., Garcés, G., Solis, N., Pizarro, M., Accatino, L., and Sáez, J. C. (2002). Regulation of hepatic connexins in cholestasis: possible involvement of Kupffer cells and inflammatory mediators. Am. J. Physiol. Gastrointest Liver Physiol. 282, G991-G1001.
18. 2+ elevation leading to p38 MAPK phosphorylation and subsequent cell death via apoptosis in human osteosarcoma cells. Toxicology 231, 21-29.
19. Huang, Y., Grinspan, J. B., Abrams, C. K., and Scherer, S. S. (2007). Pannexin1 is expressed by neurons and glia but does not form functional gap junctions. Glia. 55, 46-56.
20. Itoh, N., and Ornitz, D. M. (2004). Evolution of the Fgf and Fgfr gene families. Trends Genet. 20, 563-569.
21. 2+ release in sensory neurons. J. Biol. Chem. 279, 16377-16387.
22. Kim, D. Y., Kam, Y., Koo, S. K., and Joe, C. O. (1999). Gating connexin 43 channels reconstituted in lipid vesicles by mitogen-activated protein kinase phosphorylation. J. Biol. Chem. 274, 5581-5587.
23. Klint, P., and Claesson-Welsh, L. (1999). Signal transduction by fibroblast growth factor receptors. Front. Biosci. 4, D165-D177.
24. Koffler, L., Roshong, S., Kyu Park, I., Cesen-Cummings, K., Thompson, D. C., Dwyer-Nield, L. D., Rice, P., Mamay, C., Malkinson, A. M., and Ruch, R. J. (2000). Growth inhibition in G(1) and altered expression of cyclin D1 and p27(kip-1) after forced connexin expression in lung and liver carcinoma cells. J. Cell Biochem. 79, 347-354.
25. Laing, J. G., Koval, M., and Steinberg, T. H. (2005). Association with ZO-1 correlates with plasma membrane partitioning in truncated connexin45 mutants. J. Membr. Biol. 207, 45-53.
26. Le, A. C., and Musil, L. S. (2001). A novel role for FGF and extracellular signal-regulated kinase in gap junction-mediated intercellular communication in the lens. J. Cell Biol. 154, 197-216.
27. Lee, J. C. et al. (1994). A protein kinase involved in the regulation of inflammatory cytokine biosynthesis. Nature 372, 739-746.
28. Matveev, S. V., and Smart, E. J. (2002). Heterologous desensitization of EGF receptors and PDGF receptors by sequestration in caveolae. Am. J. Physiol. Cell Physiol. 282, 935-946.
29. Mergler, S., Dannowski, H., Bednarz, J., Engelmann, K., Hartmann, C., and Pleyer, U. (2003). Calcium influx induced by activation of receptor tyrosine kinases in SV40-transfected human corneal endothelial cells. Exp. Eye Res. 77, 485-495.
30. Meyers, J. R., MacDonald, R. B., Duggan, A., Lenzi, D., Standaert, D. G., Corwin, J. T., and Corey, D. P. (2003). Lighting up the senses: FM1-43 loading of sensory cells through nonselective ion channels. J. Neurosci. 23, 4054-4065.
31. Munaron, L. (2002). Calcium signalling and control of cell proliferation by tyrosine kinase receptors (review). Int. J. Mol. Med. 10, 671-686.
32. Nagy, J. I., Dudek, F. E., and Rash, J. E. (2004). Update on connexins and gap junctions in neurons and glia in the mammalian nervous system. Brain Res. Brain Res. Rev. 47, 191-215.
33. North, R. A. (2002). Molecular physiology of P2X receptors. Physiol. Rev. 82, 1013-1067.
34. Pelegrin, P., and Surprenant, A. (2006). Pannexin-1 mediates large pore formation and interleukin-1beta release by the ATP-gated P2X7 receptor. EMBO J. 25, 5071-5082.
35. Peracchia, C. (2004). Chemical gating of gap junction channels; roles of calcium, pH and calmodulin. Biochim. Biophys. Acta 1662, 61-80.
36. Qin, H., Shao, Q., Curtis, H., Galipeau, J., Belliveau, D. J., Wang, T., Alaoui-Jamali, M. A., and Laird, D. W. (2002). Retroviral delivery of connexin genes to human breast tumor cells inhibits in vivo tumor growth by a mechanism that is independent of significant gap junctional intercellular communication. J. Biol. Chem. 277, 29132-29138.
37. Reimers, D., Prieto, R., Gimenez-Gallego, G., Cuevas, P., and Barrio, L.C. (2000). Acidic fibroblast growth factor inhibits junctional communication of Schwann cells in culture. Neurol. Res. 22, 685-691.
38. Retamal, M. A., Cortes, C. J., Reuss, L., Bennett, M. V., and Saez, J. C. (2006). S-nitrosylation and permeation through connexin 43 hemichannels in astrocytes: induction by oxidant stress and reversal by reducing agents. Proc. Natl. Acad. Sci. USA 103, 4475-4480.
39. Retamal, M. A., Schalper, K. A., Shoji, K. F., Bennett, M. V., and Sáez, J. C. (2007a). Opening of connexin 43 hemichannels is increased by lowering intracellular redox potential. Proc. Natl. Acad. Sci. USA 104, 8322-8327.
40. Retamal, M. A., Schalper, K. A., Shoji, K. F., Orellana, J. A., Bennett, M. V., and Sáez, J. C. (2007b). Possible involvement of different connexin43 domains in plasma membrane permeabilization induced by ischemia-reperfusion. J. Membr. Biol. 218, 49-63.
41. Retamal, M. A., Froger, N., Palacios-Prado, N., Ezan, P., Sáez, P. J., Sáez, J. C., and Giaume, C. (2007c). Cx43 hemichannels and gap junction channels in astrocytes are oppositely regulated by pro-inflammatory cytokines released from activated microglia. J. Neurosci. 27, 13781-13792.
42. Sáez, J. C., Berthoud, V. M., Brañes, M. C., Martínez, A. D., and Beyer, E. C. (2003). Plasma membrane channels formed by connexins: their regulation and functions. Physiol. Rev. 83, 1359-1400.
43. 2+ elevation but not cyclic AMP in PACAP-induced p38 MAP kinase activation in PC12 cells. Regul. Pept. 109, 149-153.
44. Scotet, E., and Houssaint, E. (1995). The choice between alternative IIIb and IIIc exons of the FGFR-3 gene is not strictly tissue-specific. Biochim. Biophys. Acta 1264, 238-242.
45. Singh, D., and Lampe, P. D. (2003). Identification of connexin-43 interacting proteins. Cell Commun. Adhes. 10, 215-220.
46. Solan, J. L., and Lampe, P. D. (2005). Connexin phosphorylation as a regulatory event linked to gap junction channel assembly. Biochim. Biophys. Acta 1711, 154-163.
47. Squecco, R., Sassoli, C., Nuti, F., Martinesi, M., Chellini, F., Nosi, D., Zecchi-Orlandini, S., Francini, F., Formigli, L., and Meacci, E. (2006). Sphingosine 1-phosphate induces myoblast differentiation through Cx43 protein expression: a role for a gap junction-dependent and -independent function. Mol. Biol. Cell 17, 4896-4910.
48. Thompson, R. J., Zhou, N., and MacVicar, B. A. (2006). Ischemia opens neuronal gap junction hemichannels. Science 312, 924-927.
49. Tokuda, H., Kozawa, O., and Uematsu, T. (2000). Basic fibroblast growth factor stimulates vascular endothelial growth factor release in osteoblasts: divergent regulation by p42/p44 mitogen-activated protein kinase and p38 mitogen-activated protein kinase. J. Bone Miner Res. 15, 2371-2379.
50. VanSlyke, J. K., and Musil, L. S. (2005). Cytosolic stress reduces degradation of connexin43 internalized from the cell surface and enhances gap junction formation and function. Mol. Biol. Cell 16, 5247-5257.
51. Warn-Cramer, B. J., and Lau, A. F. (2004). Regulation of gap junctions by tyrosine protein kinases. Biochim. Biophys. Acta 1662, 81-95.
52. Zakrzewska, M., Krowarsch, D., Wiedlocha, A., Olsnes, S., and Otlewski, J. (2005). Highly stable mutants of human fibroblast growth factor-1 exhibit prolonged biological action. J. Mol. Biol. 352, 860-875.
53. Zhan, X., Hu, X., Friesel, R., and Maciag, T. (1993). Long term growth factor exposure and differential tyrosine phosphorylation are required for DNA synthesis in BALB/c 3T3 cells. J. Biol. Chem. 268, 9611-9620.