Structural determinants and proliferative consequences of connexin 37 hemichannel function in insulinoma cells

Journal of Biological Chemistry

Volumn 289, Issue 44, 2014, Pages 30379-30386

  Good, Miranda E ^a   Ek Vitorín, José F ^a   Burt, Janis M ^a  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CELL MEMBRANES; CELL PROLIFERATION; PROTEINS;

EXTRACELLULAR LOOPS; GAP JUNCTION CHANNELS; GROWTH SUPPRESSIONS; INTERCELLULAR SIGNALING; PERMEATION PROPERTIES; PORE-FORMING DOMAIN; PROTEIN-PROTEIN INTERACTIONS; STRUCTURAL DETERMINANTS;

CYTOLOGY;

ALANINE; CONNEXIN 37; CYSTEINE; GAP JUNCTION CHANNEL; GLUTAMINE; HEMICHANNEL; ISOLEUCINE; LEUCINE; MEMBRANE PROTEIN; UNCLASSIFIED DRUG; GAP JUNCTION PROTEIN;

ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL MEMBRANE; CELL PROLIFERATION; CHANNEL GATING; CONTROLLED STUDY; GENE MUTATION; INSULINOMA CELL LINE; MUTANT; NONHUMAN; PANCREAS ISLET BETA CELL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; RAT; WILD TYPE; ANIMAL; CELL LINE; GAP JUNCTION; INSULINOMA; MEMBRANE POTENTIAL; METABOLISM; MISSENSE MUTATION; PHYSIOLOGY; PROTEIN TRANSPORT; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ANIMALS; CELL LINE; CELL LINE, TUMOR; CELL PROLIFERATION; CONNEXINS; GAP JUNCTIONS; INSULINOMA; ION CHANNEL GATING; MEMBRANE POTENTIALS; MUTATION, MISSENSE; PROTEIN TRANSPORT; RATS; SIGNAL TRANSDUCTION;

EID: 84908610893     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.583054     Document Type: Article

References (34)

1. Söhl, G., and Willecke, K. (2004) Gap junctions and the connexin protein family. Cardiovasc. Res. 62, 228-232
2. Goodenough, D. A., and Paul, D. L. (2003) Beyond the gap: functions of unpaired connexon channels. Nat. Rev. Mol. Cell Biol. 4, 285-294
3. Harris, A. L. (2001) Emerging issues of connexin channels: biophysics fills the gap. Q. Rev. Biophys. 34, 325-472
4. Kardami, E., Dang, X., Iacobas, D. A., and Nickel, B. E., Jeyaraman, M., Sri-sakuldee, W., Makazan, J., Tanguy, S., and Spray, D. C. (2007) The role of connexins in controlling cell growth and gene expression. Prog. Biophys. Mol. Biol. 94, 245-264
5. Vinken, M., Decrock, E., Leybaert, L., Bultynck, G., Himpens, B., Van-haecke, T., and Rogiers, V. (2012) Non-channel functions of connexins in cell growth and cell death. Biochim. Biophys. Acta 1818, 2002-2008
6. Hervé, J. C., and Derangeon, M. (2013) Gap-junction-mediated cell-to-cell communication. Cell Tissue Res. 352, 21-31
7. Burt, J. M., and Nelson, T. K., Simon, A. M., and Fang, J. S. (2008) Connexin 37 profoundly slows cell cycle progression in rat insulinoma cells. Am. J. Physiol. Cell Physiol. 295, C1103-C1112
8. Fang, J. S., and Angelov, S. N., Simon, A. M., and Burt, J. M. (2011) Cx37 deletion enhances vascular growth and facilitates ischemic limb recovery. Am. J. Physiol. Heart Circ. Physiol. 301, H1872-H1881
9. Good, M. E., and Nelson, T. K., Simon, A. M., and Burt, J. M. (2011) A functional channel is necessary for growth suppression by Cx37. J. Cell Sci. 124, 2448-2456
10. Nelson, T. K., and Sorgen, P. L., and Burt, J. M. (2013) Carboxy terminus and pore-forming domain properties specific to Cx37 are necessary for Cx37-mediated suppression of insulinoma cell proliferation. Am. J. Physiol. Cell Physiol. 305, C1246-C1256
11. Good, M. E., Ek-Vitorín, J. F., and Burt, J. M. (2012) Extracellular loop cysteine mutant of Cx37 fails to suppress proliferation of rat insulinoma cells. J. Membr. Biol. 245, 369-380
12. Dahl, G., Levine, E., Rabadan-Diehl, C., and Werner, R. (1991) Cell/cell channel formation involves disulfide exchange. Eur. J. Biochem. 197, 141-144
13. Foote, C. I., Zhou, L., Zhu, X., and Nicholson, B. J. (1998) The pattern of disulfide linkages in the extracellular loop regions of connexin 32 suggests a model for the docking interface of gap junctions. J. Cell Biol. 140, 1187-1197
14. Bao, X., Chen, Y., Reuss, L., and Altenberg, G. A. (2004) Functional expression in Xenopus oocytes of gap-junctional hemichannels formed by a cysteine-less connexin 43. J. Biol. Chem. 279, 9689-9692
15. Tong, D., and Li, T. Y., Naus, K. E., Bai, D., and Kidder, G. M. (2007) In vivo analysis of undocked connexin43 gap junction hemichannels in ovarian granulosa cells. J. Cell Sci. 120, 4016-4024
16. Nakagawa, S., Maeda, S., and Tsukihara, T. (2010) Structural and functional studies of gap junction channels. Curr. Opin. Struct. Biol. 20, 423-430
17. Maeda, S., Nakagawa, S., Suga, M., and Yamashita, E. (2009) Structure of the connexin 26 gap junction channel at 3.5 Å resolution. Nature 458, 597-602
18. Gong, X. Q., Nakagawa, S., Tsukihara, T., and Bai, D. (2013) A mechanism of gap junction docking revealed by functional rescue of a human-disease-linked connexin mutant. J. Cell Sci. 126, 3113-3120
19. Simon, A. M., Chen, H., and Jackson, C. L. (2006) Cx37 and Cx43 localize to zona pellucida in mouse ovarian follicles. Cell Commun. Adhes. 13, 61-77
20. Ek-Vitorín, J. F., and Burt, J. M. (2005) Quantification of gap junction selectivity. Am. J. Physiol. Cell Physiol. 289, C1535-C1546
21. Bednarczyk, D., and Mash, E. A., Aavula, B. R., and Wright, S. H. (2000) NBD-TMA: a novel fluorescent substrate of the peritubular organic cation transporter of renal proximal tubules. Pflugers Arch. 440, 184-192
22. Musil, L. S., and Goodenough, D. A. (1991) Biochemical analysis of con-nexin43 intracellular transport, phosphorylation, and assembly into gap junctional plaques. J. Cell Biol. 115, 1357-1374
23. Larson, D. M., and Seul, K. H., Berthoud, V. M., Lau, A. F., and Sagar, G. D., and Beyer, E. C. (2000) Functional expression and biochemical characterization of an epitope-tagged connexin37. Mol. Cell Biol. Res. Commun. 3, 115-121
24. Derouette, J. P., Desplantez, T., Wong, C. W., Roth, I., and Kwak, B. R., and Weingart, R. (2009) Functional differences between human Cx37 polymorphic hemichannels. J. Mol. Cell Cardiol. 46, 499-507
25. Vinken, M., Decrock, E., De Vuyst, E., Ponsaerts, R., D'hondt, C, Bultynck, G., Ceelen, L., Vanhaecke, T., Leybaert, L., and Rogiers, V. (2011) Connex-ins: sensors and regulators of cell cycling. Biochim. Biophys. Acta 1815, 13-25
26. Ek-Vitorin, J. F., and Burt, J. M. (2013) Structural basis for the selective permeability of channels made of communicating junction proteins. Biochim. Biophys. Acta 1828, 51-68
27. Larson, D. M., and Wrobleski, M. J., Sagar, G. D. V., Westphale, E. M., and Beyer, E. C. (1997) Differential regulation of connexin43 and connexin37 in endothelial cells by cell density, growth, and TGF-β-1. Am. J. Physiol. 272, C405-C415
28. Morel, S., Burnier, L., Roatti, A., Chassot, A., Roth, I., Sutter, E., Galan, K., Pfenniger, A., Chanson, M., and Kwak, B. R. (2010) Unexpected role for the human Cx37 C1019T polymorphism in tumour cell proliferation. Carcinogenesis. 31, 1922-1931
29. Grosely, R., and Kopanic, J. L., Nabors, S., Kieken, F., Spagnol, G., Al-Mugotir, M., Zach, S., and Sorgen, P. L. (2013) Effects of phosphorylation on the structure and backbone dynamics of the intrinsically disordered con-nexin43 C-terminal domain. J. Biol. Chem. 288, 24857-24870
30. Koval, M., and Molina, S. A., and Burt, J. M. (2014) Mix and match: investigating heteromeric and heterotypic gap junction channels in model systems and native tissues. FEBS Lett. 588, 1193-1204
31. Buehler, L.K., Stauffer, K. A., and Gilula, N. B., and Kumar, N. M. (1995) Single channel behavior of recombinant β2 gap junction connexons reconstituted into planar lipid bilayers. Biophys. J. 68, 1767-1775
32. Das, S., and Smith, T. D., Sarma, J. D., Ritzenthaler, J. D., Maza, J., and Kaplan, B. E., Cunningham, L. A., Suaud, L., Hubbard, M. J., Rubenstein, R. C, and Koval, M. (2009) ERp29 restricts Connexin43 oligomerization in the endoplasmic reticulum. Mol. Biol. Cell 20, 2593-2604
33. Smith, T. D., Mohankumar, A., Minogue, P. J., Beyer, E. C, Berthoud, V. M., and Koval, M. (2012) Cytoplasmic amino acids within the membrane interface region influence connexin oligomerization. J. Membr. Biol. 245, 221-230
34. Weber, P. A., Chang, H. C, Spaeth, K. E., and Nitsche, J. M., and Nicholson, B.J. (2004) The permeability of gap junction channels to probes of different size is dependent on connexin composition and permeant-pore affinities. Biophys. J. 87, 958-973