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BioMed Research International
Volume 2017, Article ID 5064683, 9 pages
https://doi.org/10.1155/2017/5064683
Research Article

Evaluation of Connexin 43 Redistribution and Endocytosis in Astrocytes Subjected to Ischemia/Reperfusion or Oxygen-Glucose Deprivation and Reoxygenation

1Department of Neurology, Affiliated Hospital of Taishan Medical University, Tai’an 271000, China
2Department of Neurosurgery, Affiliated Hospital of Taishan Medical University, Tai’an 271000, China
3Department of Neurology, The First Hospital of Jilin University, Changchun 130021, China

Correspondence should be addressed to Fang Deng; moc.qq@735148904 and Jiachun Feng; moc.621@knarfcjgnef

Received 9 December 2016; Revised 23 February 2017; Accepted 8 March 2017; Published 23 March 2017

Academic Editor: Esmaiel Jabbari

Copyright © 2017 Hongyan Xie et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. D. J. Rossi, J. D. Brady, and C. Mohr, “Astrocyte metabolism and signaling during brain ischemia,” Nature Neuroscience, vol. 10, no. 11, pp. 1377–1386, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. S. Olk, G. Zoidl, and R. Dermietzel, “Connexins, cell motility, and the cytoskeleton,” Cell Motility and the Cytoskeleton, vol. 66, no. 11, pp. 1000–1016, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. R. Dermietzel, E. L. Hertzberg, J. A. Kassier, and D. C. Spray, “Gap junctions between cultured astrocytes: immunocytochemical, molecular, and electrophysiological analysis,” Journal of Neuroscience, vol. 11, no. 5, pp. 1421–1432, 1991. View at Google Scholar · View at Scopus
  4. C. Giaume, C. Fromaget, A. El Aoumari, J. Cordier, J. Glowinski, and D. Grost, “Gap junctions in cultured astrocytes: single-channel currents and characterization of channel-forming protein,” Neuron, vol. 6, no. 1, pp. 133–143, 1991. View at Publisher · View at Google Scholar · View at Scopus
  5. L. Matsuuchi and C. C. Naus, “Gap junction proteins on the move: connexins, the cytoskeleton and migration,” Biochimica et Biophysica Acta—Biomembranes, vol. 1828, no. 1, pp. 94–108, 2013. View at Publisher · View at Google Scholar · View at Scopus
  6. D. W. Laird, “Life cycle of connexins in health and disease,” Biochemical Journal, vol. 394, no. 3, pp. 527–543, 2006. View at Publisher · View at Google Scholar · View at Scopus
  7. J. L. Solan and P. D. Lampe, “Connexin43 phosphorylation: structural changes and biological effects,” Biochemical Journal, vol. 419, no. 2, pp. 261–272, 2009. View at Publisher · View at Google Scholar · View at Scopus
  8. X. Wang, A. Ma, W. Zhu et al., “The role of connexin 43 and hemichannels correlated with the astrocytic death following ischemia/reperfusion insult,” Cellular and Molecular Neurobiology, vol. 33, no. 3, pp. 401–410, 2013. View at Publisher · View at Google Scholar · View at Scopus
  9. M. M. Falk, S. M. Baker, A. M. Gumpert, D. Segretain, and R. W. Buckheit III, “Gap junction turnover is achieved by the internalization of small endocytic double-membrane vesicles,” Molecular Biology of the Cell, vol. 20, no. 14, pp. 3342–3352, 2009. View at Publisher · View at Google Scholar · View at Scopus
  10. Y. Guo, C. Martinez-Williams, and D. E. Rannels, “Gap junction-microtubule associations in rat alveolar epithelial cells,” American Journal of Physiology—Lung Cellular and Molecular Physiology, vol. 285, no. 6, pp. L1213–L1221, 2003. View at Publisher · View at Google Scholar · View at Scopus
  11. D. W. Laird, “The gap junction proteome and its relationship to disease,” Trends in Cell Biology, vol. 20, no. 2, pp. 92–101, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. M. Z. Hossain, J. Peeling, G. R. Sutherland, E. L. Hertzberg, and J. I. Nagy, “Ischemia-induced cellular redistribution of the astrocytic gap junctional protein connexin43 in rat brain,” Brain Research, vol. 652, no. 2, pp. 311–322, 1994. View at Publisher · View at Google Scholar · View at Scopus
  13. E. E. Tansey, K. F. Kwaku, P. E. Hammer et al., “Reduction and redistribution of gap and adherens junction proteins after ischemia and reperfusion,” Annals of Thoracic Surgery, vol. 82, no. 4, pp. 1472–1479, 2006. View at Publisher · View at Google Scholar · View at Scopus
  14. T. Shinotsuka, M. Yasui, and M. Nuriya, “Astrocytic gap junctional networks suppress cellular damage in an in vitro model of ischemia,” Biochemical and Biophysical Research Communications, vol. 444, no. 2, pp. 171–176, 2014. View at Publisher · View at Google Scholar · View at Scopus
  15. S. F. Okada, L. Zhang, S. M. Kreda et al., “Coupled nucleotide and mucin hypersecretion from goblet-cell metaplastic human airway epithelium,” American Journal of Respiratory Cell and Molecular Biology, vol. 45, no. 2, pp. 253–260, 2011. View at Publisher · View at Google Scholar · View at Scopus
  16. J. L. Perez Velazquez, L. Kokarovtseva, R. Sarbaziha, Z. Jeyapalan, and Y. Leshchenko, “Role of gap junctional coupling in astrocytic networks in the determination of global ischaemia-induced oxidative stress and hippocampal damage,” European Journal of Neuroscience, vol. 23, no. 1, pp. 1–10, 2006. View at Publisher · View at Google Scholar · View at Scopus
  17. K. Jiang and A. Akhmanova, “Microtubule tip-interacting proteins: a view from both ends,” Current Opinion in Cell Biology, vol. 23, no. 1, pp. 94–101, 2011. View at Publisher · View at Google Scholar · View at Scopus
  18. A. Akhmanova and M. O. Steinmetz, “Tracking the ends: a dynamic protein network controls the fate of microtubule tips,” Nature Reviews Molecular Cell Biology, vol. 9, no. 4, pp. 309–322, 2008. View at Publisher · View at Google Scholar · View at Scopus
  19. S. D. Conner and S. L. Schmid, “Regulated portals of entry into the cell,” Nature, vol. 422, no. 6927, pp. 37–44, 2003. View at Publisher · View at Google Scholar · View at Scopus
  20. G. J. Doherty and H. T. McMahon, “Mechanisms of endocytosis,” Annual Review of Biochemistry, vol. 78, pp. 857–902, 2009. View at Publisher · View at Google Scholar · View at Scopus
  21. T. Kirchhausen, E. Macia, and H. E. Pelish, “Use of dynasore, the small molecule inhibitor of dynamin, in the regulation of endocytosis,” Methods in Enzymology, vol. 438, pp. 77–93, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. M. W. Pfaffl, “A new mathematical model for relative quantification in real-time RT–PCR,” Nucleic Acids Research, vol. 29, no. 9, p. e45, 2001. View at Publisher · View at Google Scholar · View at Scopus
  23. M. C. Fiori, L. Reuss, L. G. Cuello, and G. A. Altenberg, “Functional analysis and regulation of purified connexin hemichannels,” Frontiers in Physiology, vol. 5, article 71, 2014. View at Publisher · View at Google Scholar · View at Scopus
  24. T. Nakase, Y. Yoshida, and K. Nagata, “Enhanced connexin 43 immunoreactivity in penumbral areas in the human brain following ischemia,” GLIA, vol. 54, no. 5, pp. 369–375, 2006. View at Publisher · View at Google Scholar · View at Scopus
  25. M. Xie, C. Yi, X. Luo et al., “Glial gap junctional communication involvement in hippocampal damage after middle cerebral artery occlusion,” Annals of Neurology, vol. 70, no. 1, pp. 121–132, 2011. View at Publisher · View at Google Scholar · View at Scopus
  26. T. Nakase, G. Söhl, M. Theis, K. Willecke, and C. C. G. Naus, “Increased apoptosis and inflammation after focal brain ischemia in mice lacking connexin43 in astrocytes,” American Journal of Pathology, vol. 164, no. 6, pp. 2067–2075, 2004. View at Publisher · View at Google Scholar · View at Scopus
  27. J. A. Orellana, D. E. Hernández, P. Ezan et al., “Hypoxia in high glucose followed by reoxygenation in normal glucose reduces the viability of cortical astrocytes through increased permeability of connexin 43 hemichannels,” GLIA, vol. 58, no. 3, pp. 329–343, 2010. View at Publisher · View at Google Scholar · View at Scopus
  28. J. A. Orellana, N. Froger, P. Ezan et al., “ATP and glutamate released via astroglial connexin 43 hemichannels mediate neuronal death through activation of pannexin 1 hemichannels,” Journal of Neurochemistry, vol. 118, no. 5, pp. 826–840, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. A. D. Martinez and J. C. Sáez, “Regulation of astrocyte gap junctions by hypoxia–reoxygenation,” Brain Research Reviews, vol. 32, no. 1, pp. 250–258, 2000. View at Publisher · View at Google Scholar
  30. X. Dang, B. W. Doble, and E. Kardami, “The carboxy-tail of connexin-43 localizes to the nucleus and inhibits cell growth,” Molecular and Cellular Biochemistry, vol. 242, no. 1-2, pp. 35–38, 2003. View at Publisher · View at Google Scholar · View at Scopus
  31. D. V. Krysko, L. Leybaert, P. Vandenabeele, and K. D'Herde, “Gap junctions and the propagation of cell survival and cell death signals,” Apoptosis, vol. 10, no. 3, pp. 459–469, 2005. View at Publisher · View at Google Scholar · View at Scopus
  32. J. A. Orellana, N. Palacios-Prado, and J. C. Sáez, “Chlorpromazine reduces the intercellular communication via gap junctions in mammalian cells,” Toxicology and Applied Pharmacology, vol. 213, no. 3, pp. 187–197, 2006. View at Publisher · View at Google Scholar · View at Scopus
  33. D. C. Spray, R. Hanstein, S. V. Lopez-Quintero, R. F. Stout, S. O. Suadicani, and M. M. Thi, “Gap junctions and Bystander effects: good samaritans and executioners,” Wiley Interdisciplinary Reviews: Membrane Transport and Signaling, vol. 2, no. 1, pp. 1–15, 2013. View at Publisher · View at Google Scholar · View at Scopus
  34. N. Rouach, M. Segal, A. Koulakoff, C. Giaume, and E. Avignone, “Carbenoxolone blockade of neuronal network activity in culture is not mediated by an action of gap junctions,” Journal of Physiology, vol. 553, no. 3, pp. 729–745, 2003. View at Publisher · View at Google Scholar · View at Scopus
  35. M. V. Frantseva, L. Kokarovtseva, and J. L. Perez Velazquez, “Ischemia-induced brain damage depends on specific gap-junctional coupling,” Journal of Cerebral Blood Flow and Metabolism, vol. 22, no. 4, pp. 453–462, 2002. View at Google Scholar · View at Scopus
  36. Y. Leshchenko, S. Likhodii, W. Yue, W. M. Burnham, and J. L. Perez Velazquez, “Carbenoxolone does not cross the blood brain barrier: an HPLC study,” BMC Neuroscience, vol. 7, article 3, 2006. View at Publisher · View at Google Scholar · View at Scopus
  37. V. Benfenati, M. Caprini, G. P. Nicchia et al., “Carbenoxolone inhibits volume-regulated anion conductance in cultured rat cortical astroglia,” Revista de la Asociación Espaola de Neuropsiquiatría, vol. 3, pp. 323–336, 2009. View at Google Scholar
  38. P. Bazzigaluppi, I. Weisspapir, B. Stefanovic, L. Leybaert, and P. L. Carlen, “Astrocytic gap junction blockade markedly increases extracellular potassium without causing seizures in the mouse neocortex,” Neurobiology of Disease, vol. 101, pp. 1–7, 2017. View at Publisher · View at Google Scholar
  39. J. C. Sáez, V. M. Berthoud, M. C. Brañes, A. D. Martínez, and E. C. Beyer, “Plasma membrane channels formed by connexins: their regulation and functions,” Physiological Reviews, vol. 83, no. 4, pp. 1359–1400, 2003. View at Publisher · View at Google Scholar · View at Scopus
  40. R. M. Shaw, A. J. Fay, M. A. Puthenveedu, M. von Zastrow, Y.-N. Jan, and L. Y. Jan, “Microtubule plus-end-tracking proteins target gap junctions directly from the cell interior to adherens junctions,” Cell, vol. 128, no. 3, pp. 547–560, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. B. N. G. Giepmans, I. Verlaan, T. Hengeveld et al., “Gap junction protein connexin-43 interacts directly with microtubules,” Current Biology, vol. 11, no. 17, pp. 1364–1368, 2001. View at Publisher · View at Google Scholar · View at Scopus
  42. S. Olk, A. Turchinovich, M. Grzendowski et al., “Proteomic analysis of astroglial connexin43 silencing uncovers a cytoskeletal platform involved in process formation and migration,” GLIA, vol. 58, no. 4, pp. 494–505, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. N. J. Severs, K. S. Shovel, A. M. Slade, T. Powell, V. W. Twist, and C. R. Green, “Fate of gap junctions in isolated adult mammalian cardiomyocytes,” Circulation Research, vol. 65, no. 1, pp. 22–42, 1989. View at Publisher · View at Google Scholar · View at Scopus
  44. K. Jordan, R. Chodock, A. R. Hand, and D. W. Laird, “The origin of annular junctions: a mechanism of gap junction internalization,” Journal of Cell Science, vol. 114, no. 4, pp. 763–773, 2001. View at Google Scholar · View at Scopus
  45. G. Gaietta, T. J. Deerinck, S. R. Adams et al., “Multicolor and electron microscopic imaging of connexin trafficking,” Science, vol. 296, no. 5567, pp. 503–507, 2002. View at Publisher · View at Google Scholar · View at Scopus
  46. G. G. Hesketh, M. H. Shah, V. L. Halperin et al., “Ultrastructure and regulation of lateralized connexin43 in the failing heart,” Circulation Research, vol. 106, no. 6, pp. 1153–1163, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. G. Scita and P. P. Di Fiore, “The endocytic matrix,” Nature, vol. 463, no. 7280, pp. 464–473, 2010. View at Publisher · View at Google Scholar · View at Scopus
  48. A. M. Gumpert, J. S. Varco, S. M. Baker, M. Piehl, and M. M. Falk, “Double-membrane gap junction internalization requires the clathrin-mediated endocytic machinery,” FEBS Letters, vol. 582, no. 19, pp. 2887–2892, 2008. View at Publisher · View at Google Scholar · View at Scopus
  49. S. Mayor and R. E. Pagano, “Pathways of clathrin-independent endocytosis,” Nature Reviews Molecular Cell Biology, vol. 8, no. 8, pp. 603–612, 2007. View at Publisher · View at Google Scholar · View at Scopus
  50. E. Leithe, S. Sirnes, T. Fykerud, A. Kjenseth, and E. Rivedal, “Endocytosis and post-endocytic sorting of connexins,” Biochimica et Biophysica Acta—Biomembranes, vol. 1818, no. 8, pp. 1870–1879, 2012. View at Publisher · View at Google Scholar · View at Scopus
  51. J. T. Fong, R. M. Kells, A. M. Gumpert, J. Y. Marzillier, M. W. Davidson, and M. M. Falk, “Internalized gap junctions are degraded by autophagy,” Autophagy, vol. 8, no. 5, pp. 794–811, 2012. View at Publisher · View at Google Scholar · View at Scopus
  52. J. Gilleron, D. Carette, C. Fiorini et al., “The large GTPase dynamin2: a new player in connexin 43 gap junction endocytosis, recycling and degradation,” International Journal of Biochemistry and Cell Biology, vol. 43, no. 8, pp. 1208–1217, 2011. View at Publisher · View at Google Scholar · View at Scopus
  53. D. W. Laird, “Connexin phosphorylation as a regulatory event linked to gap junction internalization and degradation,” Biochimica et Biophysica Acta—Biomembranes, vol. 1711, no. 2, pp. 172–182, 2005. View at Publisher · View at Google Scholar · View at Scopus
  54. V. M. Berthoud, P. J. Minogue, J. G. Laing, and E. C. Beyer, “Pathways for degradation of connexins and gap junctions,” Cardiovascular Research, vol. 62, no. 2, pp. 256–267, 2004. View at Publisher · View at Google Scholar · View at Scopus