Degradation of gap junction connexins is regulated by the interaction with Cx43-interacting protein of 75 kDa (CIP75)

Biochemical Journal

Volumn 466, Issue 3, 2015, Pages 571-585

  Kopanic, Jennifer L ^a   Schlingmann, Barbara ^b   Koval, Michael ^b   Lau, Alan F ^c,d,e   Sorgen, Paul L ^a   Su, Vivian F ^c,d  

^a UNIVERSITY OF NEBRASKA MEDICAL CENTER   (United States)

^b Allergy Asthma and Immunology Clinic of Georgetown   (United States)

^c UNIVERSITY OF HAWAII CANCER CENTER   (United States)

^d UNIVERSITY OF HAWAII   (United States)

^e UNIVERSITY OF HAWAII   (United States)

Author keywords

CIP75; Connexin; ERAD; Proteasome; Protein degradation

Indexed keywords

BORTEZOMIB; CONNEXIN 32; CONNEXIN 40; CONNEXIN 43; CONNEXIN 45; CX43 INTERACTING PROTEIN OF 75; PROTEASOME; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; PROTEIN BINDING;

ARTICLE; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CELL INTERACTION; CELL MIGRATION; CELLULAR DISTRIBUTION; ENDOPLASMIC RETICULUM ASSOCIATED DEGRADATION; ENZYME REGULATION; FEMALE; GAP JUNCTION; HELA CELL LINE; HUMAN; HUMAN CELL; NUCLEAR MAGNETIC RESONANCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; TRANSIENT TRANSFECTION; UBIQUITINATION; ANIMAL; CHEMISTRY; CHICKEN; METABOLISM; PHYSIOLOGY; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE;

ANIMALS; CHICKENS; CONNEXIN 43; GAP JUNCTIONS; HELA CELLS; HUMANS; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY;

EID: 84934888770     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20141042     Document Type: Article

References (53)

1. Goodenough, D.A., Goliger, J.A. and Paul, D.L. (1996) Connexins, connexons, and intercellular communication. Annu. Rev. Biochem. 65, 475-502 CrossRef PubMed
2. Nelis, E., Haites, N. and Van Broeckhoven, C. (1999) Mutations in the peripheral myelin genes and associated genes in inherited peripheral neuropathies. Hum. Mutat. 13, 11-28 CrossRef PubMed
3. Laird, D.W. (2014) Syndromic and non-syndromic disease-linked Cx43 mutations. FEBS Lett. 588, 1339-1348 CrossRef PubMed
4. Berger, A.C., Kelly, J.J., Lajoie, P., Shao, Q. and Laird, D.W. (2014) Mutations in Cx30 that are linked to skin disease and non-syndromic hearing loss exhibit several distinct cellular pathologies. J. Cell Sci. 127, 1751-1764 CrossRef PubMed
5. Gerido, D.A. and White, T.W. (2004) Connexin disorders of the ear, skin, and lens. Biochim. Biophys. Acta 1662, 159-170 CrossRef PubMed
6. Severs, N.J., Bruce, A.F., Dupont, E. and Rothery, S. (2008) Remodelling of gap junctions and connexin expression in diseased myocardium. Cardiovasc. Res. 80, 9-19 CrossRef PubMed
7. Nielsen, M.S., Nygaard Axelsen, L., Sorgen, P.L., Verma, V., Delmar, M. and Holstein-Rathlou, N.H. (2012) Gap junctions. Compr. Physiol. 2, 1981-2035 PubMed
8. van Veen, A.A., van Rijen, H.V. and Opthof, T. (2001) Cardiac gap junction channels: modulation of expression and channel properties. Cardiovasc. Res. 51, 217-229 CrossRef PubMed
9. Laird, D.W. (2006) Life cycle of connexins in health and disease. Biochem. J. 394, 527-543 CrossRef PubMed
10. Bouvier, D., Kieken, F., Kellezi, A. and Sorgen, P.L. (2008) Structural changes in the carboxyl terminus of the gap junction protein connexin 40 caused by the interaction with c-Src and zonula occludens-1. Cell Commun. Adhes. 15, 107-118 CrossRef PubMed
11. Bouvier, D., Kieken, F. and Sorgen, P.L. (2007) (1)H, (13)C, and (15)N backbone resonance assignments of the carboxyl terminal domain of Connexin40. Biomol. NMR Assign. 1, 155-157 CrossRef PubMed
12. Kopanic, J.L., Al-Mugotir, M.H., Kieken, F., Zach, S., Trease, A.J. and Sorgen, P.L. (2014) Characterization of the connexin45 carboxyl-terminal domain structure and interactions with molecular partners. Biophys. J. 106, 2184-2195 CrossRef PubMed
13. Kopanic, J.L. and Sorgen, P.L. (2013) Chemical shift assignments of the connexin45 carboxyl terminal domain: monomer and dimer conformations. Biomol. NMR Assign. 7, 293-297 CrossRef PubMed
14. Sorgen, P.L., Duffy, H.S., Sahoo, P., Coombs, W., Delmar, M. and Spray, D.C. (2004) Structural changes in the carboxyl terminus of the gap junction protein connexin43 indicates signaling between binding domains for c-Src and zonula occludens-1. J. Biol. Chem. 279, 54695-54701 CrossRef PubMed
15. Cumberworth, A., Lamour, G., Babu, M.M. and Gsponer, J. (2013) Promiscuity as a functional trait: intrinsically disordered regions as central players of interactomes. Biochem. J. 454, 361-369 CrossRef PubMed
16. Dunker, A.K., Brown, C.J., Lawson, J.D., Iakoucheva, L.M. and Obradovic, Z. (2002) Intrinsic disorder and protein function. Biochemistry 41, 6573-6582 CrossRef PubMed
17. Gao, J. and Xu, D. (2012) Correlation between posttranslational modification and intrinsic disorder in protein. Pac. Symp. Biocomput. 94-103
18. Herve, 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 CrossRef PubMed
19. Beardslee, M.A., Laing, J.G., Beyer, E.C. and Saffitz, J.E. (1998) Rapid turnover of connexin43 in the adult rat heart. Circ. Res. 83, 629-635 CrossRef PubMed
20. Darrow, B.J., Laing, J.G., Lampe, P.D., Saffitz, J.E. and Beyer, E.C. (1995) Expression of multiple connexins in cultured neonatal rat ventricular myocytes. Circ. Res. 76, 381-387 CrossRef PubMed
21. Fallon, R.F. and Goodenough, D.A. (1981) Five-hour half-life of mouse liver gap-junction protein. J. Cell. Biol. 90, 521-526 CrossRef PubMed
22. Laird, D.W., Puranam, K.L. and Revel, J.P. (1991) Turnover and phosphorylation dynamics of connexin43 gap junction protein in cultured cardiac myocytes. Biochem. J. 273, 67-72 PubMed
23. Musil, L.S., Le, A.C., VanSlyke, J.K. and Roberts, L.M. (2000) Regulation of connexin degradation as a mechanism to increase gap junction assembly and function. J. Biol. Chem. 275, 25207-25215 CrossRef PubMed
24. Su, V. and Lau, A.F. (2014) Connexins: mechanisms regulating protein levels and intercellular communication. FEBS Lett. 588, 1212-1220 CrossRef PubMed
25. Thevenin, A.F., Kowal, T.J., Fong, J.T., Kells, R.M., Fisher, C.G. and Falk, M.M. (2013) Proteins and mechanisms regulating gap-junction assembly, internalization, and degradation. Physiology 28, 93-116 CrossRef PubMed
26. Kieken, F., Spagnol, G., Su, V., Lau, A.F. and Sorgen, P.L. (2010) NMR structure note: UBA domain of CIP75. J. Biomol. NMR 46, 245-250 CrossRef PubMed
27. Li, X., Su, V., Kurata, W.E., Jin, C. and Lau, A.F. (2008) A novel connexin43-interacting protein, CIP75, which belongs to the UbL-UBA protein family, regulates the turnover of connexin43. J. Biol. Chem. 283, 5748-5759 CrossRef PubMed
28. Su, V. and Lau, A.F. (2009) Ubiquitin-like and ubiquitin-associated domain proteins: significance in proteasomal degradation. Cell. Mol. Life Sci. 66, 2819-2833 CrossRef PubMed
29. Su, V., Hoang, C., Geerts, D. and Lau, A.F. (2014) CIP75 (connexin43-interacting protein of 75 kDa) mediates the endoplasmic reticulum dislocation of connexin43. Biochem. J. 458, 57-67 CrossRef PubMed
30. Su, V., Nakagawa, R., Koval, M. and Lau, A.F. (2010) Ubiquitin-independent proteasomal degradation of endoplasmic reticulum-localized connexin43 mediated by CIP75. J Biol. Chem. 285, 40979-40990 CrossRef PubMed
31. Kelly, S.M., VanSlyke, J.K. and Musil, L.S. (2007) Regulation of ubiquitin-proteasome system mediated degradation by cytosolic stress. Mol. Biol. Cell. 18, 4279-4291 CrossRef PubMed
32. Minogue, P.J., Beyer, E.C. and Berthoud, V.M. (2013) A connexin50 mutant, CX50fs, that causes cataracts is unstable, but is rescued by a proteasomal inhibitor. J. Biol. Chem. 288, 20427-20434 CrossRef PubMed
33. Stauch, K., Kieken, F. and Sorgen, P. (2012) Characterization of the structure and intermolecular interactions between the connexin 32 carboxyl-terminal domain and the protein partners synapse-associated protein 97 and calmodulin. J. Biol. Chem. 287, 27771-27788 CrossRef PubMed
34. Nelson, T.K., 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, C1246-1256 CrossRef PubMed
35. Sorgen, P.L., Duffy, H.S., Cahill, S.M., Coombs, W., Spray, D.C., Delmar, M. and Girvin, M.E. (2002) Sequence-specific resonance assignment of the carboxyl terminal domain of Connexin43. J. Biomol. NMR 23, 245-246 CrossRef PubMed
36. Delaglio, F., Grzesiek, S., Vuister, G.W., Zhu, G., Pfeifer, J. and Bax, A. (1995) NMRPipe: a multidimensional spectral processing system based on UNIX pipes. J. Biomol. NMR 6, 277-293 CrossRef PubMed
37. Johnson, B.A. and Blevins, R.A. (1994) NMR view: a computer program for the visualization and analysis of NMR data. J. Biomol. NMR 4, 603-614 CrossRef PubMed
38. Bouvier, D., Spagnol, G., Chenavas, S., Kieken, F., Vitrac, H., Brownell, S., Kellezi, A., Forge, V. and Sorgen, P.L. (2009) Characterization of the structure and intermolecular interactions between the connexin40 and connexin43 carboxyl-terminal and cytoplasmic loop domains. J. Biol. Chem. 284, 34257-34271 CrossRef PubMed
39. Elenes, S., Martinez, A.D., Delmar, M., Beyer, E.C. and Moreno, A.P. (2001) Heterotypic docking of Cx43 and Cx45 connexons blocks fast voltage gating of Cx43. Biophys. J. 81, 1406-1418 CrossRef PubMed
40. 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 CrossRef PubMed
41. Das Sarma, J., Wang, F. and Koval, M. (2002) Targeted gap junction protein constructs reveal connexin-specific differences in oligomerization. J. Biol. Chem. 277, 20911-20918 CrossRef PubMed
42. Maza, J., Das Sarma, J. and Koval, M. (2005) Defining a minimal motif required to prevent connexin oligomerization in the endoplasmic reticulum. J. Biol. Chem. 280, 21115-21121 CrossRef PubMed
43. Su, V., Knutson, A., Lau, K., Kurata, W., Berestecky, J. and Lau, A.F. (2009) Generation and characterization of mouse monoclonal antibodies against CIP75, an UbL-UBA domain-containing protein. Hybridoma (Larchmt) 28, 79-84 CrossRef PubMed
44. Su, V. and Lau, A.F. (2012) Ubiquitination, intracellular trafficking, and degradation of connexins. Arch. Biochem. Biophys. 524, 16-22 CrossRef PubMed
45. VanSlyke, J.K. and Musil, L.S. (2002) Dislocation and degradation from the ER are regulated by cytosolic stress. J. Cell Biol. 157, 381-394 CrossRef PubMed
46. Kato, T., Iwasaki, Y.K. and Nattel, S. (2012) Connexins and atrial fibrillation: filling in the gaps. Circulation 125, 203-206 CrossRef PubMed
47. Das, S., Smith, T.D., Sarma, J.D., Ritzenthaler, J.D., Maza, J., 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 CrossRef PubMed
48. 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 CrossRef PubMed
49. Dunn, C.A., Su, V., Lau, A.F. and Lampe, P.D. (2012) Activation of Akt, not connexin 43 protein ubiquitination, regulates gap junction stability. J. Biol. Chem. 287, 2600-2607 CrossRef PubMed
50. Qin, H., Shao, Q., Igdoura, S.A., Alaoui-Jamali, M.A. and Laird, D.W. (2003) Lysosomal and proteasomal degradation play distinct roles in the life cycle of Cx43 in gap junctional intercellular communication-deficient and -competent breast tumor cells. J. Biol. Chem. 278, 30005-30014 CrossRef PubMed
51. Gemel, J., Simon, A.R., Patel, D., Xu, Q., Matiukas, A., Veenstra, R.D. and Beyer, E.C. (2014) Degradation of a connexin40 mutant linked to atrial fibrillation is accelerated. J. Mol. Cell. Cardiol. 74, 330-339 CrossRef PubMed
52. Herve, J.C. and Dhein, S. (2010) Peptides targeting gap junctional structures. Curr. Pharm. Des. 16, 3056-3070 CrossRef PubMed
53. Herve, J.C. and Dhein, S. (2006) Pharmacology of cardiovascular gap junctions. Adv. Cardiol. 42, 107-131 CrossRef PubMed