14-3-3θ facilitates plasma membrane delivery and function of mechanosensitive connexin 43 hemichannels

Journal of Cell Science

Volumn 127, Issue 1, 2014, Pages 137-146

  Batra, Nidhi ^a   Riquelme, Manuel A ^a   Burra, Sirisha ^a   Jiang, Jean X ^a  

^a UNIVERSITY OF TEXAS HEALTH SCIENCE CENTER AT SAN ANTONIO   (United States)

Author keywords

14 3 3; Connexion; Hemichannel

Indexed keywords

14 3 3 THETA PROTEIN; ALPHA5 INTEGRIN; BREFELDIN A; CONNEXIN 43; PROTEIN 14 3 3; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL STRESS; CELL SURFACE; CONTROLLED STUDY; GOLGI COMPLEX; INTRACELLULAR SIGNALING; MOLECULAR INTERACTION; MOUSE; NONHUMAN; OSSIFICATION; OSTEOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION;

14-3-3; CONNEXION; HEMICHANNEL;

14-3-3 PROTEINS; ANIMALS; BREFELDIN A; CELL MEMBRANE; CONNEXIN 43; FEMUR; GENE EXPRESSION REGULATION; GOLGI APPARATUS; INTEGRIN ALPHA5; MECHANOTRANSDUCTION, CELLULAR; MICE; OSTEOCYTES; PRIMARY CELL CULTURE; PROTEIN SYNTHESIS INHIBITORS; PROTEIN TRANSPORT;

EID: 84891403754     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.133553     Document Type: Article

References (36)

1. Batra, N., Burra, S., Siller-Jackson, A. J., Gu, S., Xia, X., Weber, G. F., DeSimone, D., Bonewald, L. F., Lafer, E. M., Sprague, E. et al. (2012a). Mechanical stress-activated integrin α5b1 induces opening of connexin 43 hemichannels. Proc. Natl. Acad. Sci. USA 109, 3359-3364.
2. Batra, N., Kar, R. and Jiang, J. X. (2012b). Gap junctions and hemichannels in signal transmission, function and development of bone. Biochim. Biophys. Acta 1818, 1909-1918.
3. Chanson, M., Kotsias, B. A., Peracchia, C. and O'Grady, S. M. (2007). Interactions of connexins with other membrane channels and transporters. Prog. Biophys. Mol. Biol. 94, 233-244.
4. Cherian, P. P., Siller-Jackson, A. J., Gu, S., Wang, X., Bonewald, L. F., Sprague, E. and Jiang, J. X. (2005). Mechanical strain opens connexin 43 hemichannels in osteocytes: a novel mechanism for the release of prostaglandin. Mol. Biol. Cell 16, 3100-3106.
5. Civitelli, R. (2008). Cell-cell communication in the osteoblast/osteocyte lineage. Arch. Biochem. Biophys. 473, 188-192.
6. Deakin, N. O., Bass, M. D., Warwood, S., Schoelermann, J., Mostafavi-Pour, Z., Knight, D., Ballestrem, C. and Humphries, M. J. (2009). An integrinalpha4-14-3-3zeta-paxillin ternary complex mediates localised Cdc42 activity and accelerates cell migration. J. Cell Sci. 122, 1654-1664.
7. el-Fouly, M. H., Trosko, J. E. and Chang, C. C. (1987). Scrape-loading and dye transfer. A rapid and simple technique to study gap junctional intercellular communication. Exp. Cell Res. 168, 422-430.
8. Fritton, S. P. and Weinbaum, S. (2009). Fluid and solute transport in bone: flowinduced mechanotransduction. Annu. Rev. Fluid Mech. 41, 347-374.
9. Gardino, A. K., Smerdon, S. J. and Yaffe, M. B. (2006). Structural determinants of 14-3-3 binding specificities and regulation of subcellular localization of 14-3-3-ligand complexes: a comparison of the X-ray crystal structures of all human 14-3-3 isoforms. Semin. Cancer Biol. 16, 173-182.
10. Genetos, D. C., Kephart, C. J., Zhang, Y., Yellowley, C. E. and Donahue, H. J. (2007). Oscillating fluid flow activation of gap junction hemichannels induces ATP release from MLO-Y4 osteocytes. J. Cell. Physiol. 212, 207-214.
11. Goodenough, D. A. and Paul, D. L. (2003). Beyond the gap: functions of unpaired connexon channels. Nat. Rev. Mol. Cell Biol. 4, 285-295.
12. Han, D. C., Rodriguez, L. G. and Guan, J. L. (2001). Identification of a novel interaction between integrin beta1 and 14-3-3beta. Oncogene 20, 346-357.
13. Hervé, J. C., Bourmeyster, N., Sarrouilhe, D. and Duffy, H. S. (2007). Gap junctional complexes: from partners to functions. Prog. Biophys. Mol. Biol. 94, 29-65.
14. Hughes-Fulford, M. (2004). Signal transduction and mechanical stress. Sci. STKE 2004, RE12.
15. Jacobs, C. R., Temiyasathit, S. and Castillo, A. B. (2010). Osteocyte mechanobiology and pericellular mechanics. Annu. Rev. Biomed. Eng. 12, 369-400.
16. Kato, Y., Windle, J. J., Koop, B. A., Mundy, G. R. and Bonewald, L. F. (1997). Establishment of an osteocyte-like cell line, MLO-Y4. J. Bone Miner. Res. 12, 2014-2023.
17. Liu, D., Bienkowska, J., Petosa, C., Collier, R. J., Fu, H. and Liddington, R. (1995). Crystal structure of the zeta isoform of the 14-3-3 protein. Nature 376, 191-194.
18. Liu, J., He, X., Qi, Y., Tian, X., Monkley, S. J., Critchley, D. R., Corbett, S. A., Lowry, S. F., Graham, A. M. and Li, S. (2011). Talin1 regulates integrin turnover to promote embryonic epithelial morphogenesis. Mol. Cell. Biol. 31, 3366-3377.
19. Mrowiec, T. and Schwappach, B. (2006). 14-3-3 proteins in membrane protein transport. Biol. Chem. 387, 1227-1236.
20. Musil, L. S. and Goodenough, D. A. (1993). Multisubunit assembly of an integral plasma membrane channel protein, gap junction connexin43, occurs after exit from the ER. Cell 74, 1065-1077.
21. Muslin, A. J., Tanner, J. W., Allen, P. M. and Shaw, A. S. (1996). Interaction of 14-3-3 with signaling proteins is mediated by the recognition of phosphoserine. Cell 84, 889-897.
22. Nufer, O. and Hauri, H. P. (2003). ER export: call 14-3-3. Curr. Biol. 13, R391-R393.
23. Nurmi, S. M., Gahmberg, C. G. and Fagerholm, S. C. (2006). 14-3-3 proteins bind both filamin and alphaLbeta2 integrin in activated T cells. Ann. N. Y. Acad. Sci. 1090, 318-325.
24. O'Kelly, I., Butler, M. H., Zilberberg, N. and Goldstein, S. A. (2002). Forward transport. 14-3-3 binding overcomes retention in endoplasmic reticulum by dibasic signals. Cell 111, 577-588.
25. Okamoto, Y. and Shikano, S. (2011). Phosphorylation-dependent C-terminal binding of 14-3-3 proteins promotes cell surface expression of HIV co-receptor GPR15. J. Biol. Chem. 286, 7171-7181.
26. Orr, A. W., Helmke, B. P., Blackman, B. R. and Schwartz, M. A. (2006). Mechanisms of mechanotransduction. Dev. Cell 10, 11-20.
27. Park, D. J., Freitas, T. A., Wallick, C. J., Guyette, C. V. and Warn-Cramer, B. J. (2006). Molecular dynamics and in vitro analysis of Connexin43: A new 14-3-3 mode-1 interacting protein. Protein Sci. 15, 2344-2355.
28. Preisinger, C., Short, B., De Corte, V., Bruyneel, E., Haas, A., Kopajtich, R., Gettemans, J. and Barr, F. A. (2004). YSK1 is activated by the Golgi matrix protein GM130 and plays a role in cell migration through its substrate 14-3-3zeta. J. Cell Biol. 164, 1009-1020.
29. Shikano, S., Coblitz, B., Sun, H. and Li, M. (2005). Genetic isolation of transport signals directing cell surface expression. Nat. Cell Biol. 7, 985-992.
30. Shikano, S., Coblitz, B., Wu, M. and Li, M. (2006). 14-3-3 proteins: regulation of endoplasmic reticulum localization and surface expression of membrane proteins. Trends Cell Biol. 16, 370-375.
31. Siller-Jackson, A. J., Burra, S., Gu, S., Xia, X., Bonewald, L. F., Sprague, E. and Jiang, J. X. (2008). Adaptation of connexin 43-hemichannel prostaglandin release to mechanical loading. J. Biol. Chem. 283, 26374-26382.
32. Silver, F. H. and Siperko, L. M. (2003). Mechanosensing and mechanochemical transduction: how is mechanical energy sensed and converted into chemical energy in an extracellular matrix? Crit. Rev. Biomed. Eng. 31, 255-331.
33. Xiao, B., Smerdon, S. J., Jones, D. H., Dodson, G. G., Soneji, Y., Aitken, A. and Gamblin, S. J. (1995). Structure of a 14-3-3 protein and implications for coordination of multiple signalling pathways. Nature 376, 188-191.
34. Yaffe, M. B. (2002). How do 14-3-3 proteins work?-Gatekeeper phosphorylation and the molecular anvil hypothesis. FEBS Lett. 513, 53-57.
35. Yaffe, M. B., Rittinger, K., Volinia, S., Caron, P. R., Aitken, A., Leffers, H., Gamblin, S. J., Smerdon, S. J. and Cantley, L. C. (1997). The structural basis for 14-3-3:phosphopeptide binding specificity. Cell 91, 961-971.
36. Yuan, H., Michelsen, K. and Schwappach, B. (2003). 14-3-3 dimers probe the assembly status of multimeric membrane proteins. Curr. Biol. 13, 638-646.