Biogenesis and degradation of gap junctions

Connexins: A Guide

Volumn , Issue , 2009, Pages 225-240

  Musil, Linda S ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

Author keywords

Assembly; Cx26; Cx32; Cx43; Cx46; Degradation; Endoplasmic reticulum; ER associated degradation; Golgi; Heat shock; Hemichannel; Lysosome; Proteasome; Trans Golgi network; Ubiquitin

Indexed keywords

EID: 77951243502     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1007/978-1-59745-489-6_9     Document Type: Chapter

References (63)

1. Valiunas V, Bukauskas FF, Weingart R. Conductances and selective permeability of connexin43 gap junction channels examined in neonatal rat heart cells. Circ Res. 1997;80:708-19.
2. Castro C, Gomez-Hernandez JM, Silander K, Barrio LC. Altered formation of hemichannels and gap junction channels caused by C-terminal connexin-32 mutations. J Neurosci. 1999;19:3752-60.
3. Zhang JT, Chen M, Foote CI, Nicholson BJ. Membrane integration of in vitro-translated gap junctional proteins: co- and posttranslational mechanisms. Mol Biol Cell. 1996;7:471-82.
4. Falk MM, Buehler LK, Kumar NM, Gilula NB. Cell-free synthesis and assembly of connexins into functional gap junction membrane channels. EMBO J. 1997;16:2703-16.
5. Falk MM, Kumar NM, Gilula NB. Membrane insertion of gap junction connexins: polytopic channel-forming membrane proteins. J Cell Biol. 1994;127:343-55.
6. Van Slyke JK, Musil LS. Dislocation and degradation from the ER are regulated by cytosolic stress. J Cell Biol. 2002;157:381-94.
7. Meusser B, Hirsch C, Jarosch E, Sommer T. ERAD: the long road to destruction. Nat Cell Biol. 2005;7:766-72.
8. Glickman MH, Ciechanover A. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev. 2002;82:373-428.
9. Jarosch E, Lenk U, Sommer T. Endoplasmic reticulum-associated protein degradation. Int Rev Cytol. 2003;223:39-81.
10. Groll M, Huber R. Inhibitors of the eukaryotic 20S proteasome core particle: a structural approach. Biochim Biophys Acta. 2004;1695:33-44.
11. Van Slyke JK, Deschenes SM, Musil LS. Intracellular transport, assembly, and degradation of wildtype and disease-linked mutant gap junction proteins. Mol Biol Cell. 2000;11:1933-46.
12. Kelly SM, Vanslyke JK, Musil LS. Regulation of ubiquitin-proteasome system-mediated degradation by cytosolic stress. Mol Biol Cell. 2007;18:4279-91.
13. Goldberg GS, Lampe PD, Nicholson BJ. Selective transfer of endogenous metabolites through gap junctions composed of different connexins. Nat Cell Biol. 1999;1:457-9.
14. Nakamura TY, Yamamoto I, Kanno Y, Shiba Y, Goshima K. Metabolic coupling of glutathione between mouse and quail cardiac myocytes and its protective role against oxidative stress. Circ Res. 1994;74:806-16.
15. Laing JG, Tadros PN, Green K, Saffitz JE, Beyer EC. Proteolysis of connexin43-containing gap junctions in normal and heat-stressed cardiac myocytes. Cardiovasc Res. 1998;38:711-8.
16. Hamada N, Kodama S, Suzuki K, Watanabe M. Gap junctional intercellular communication and cellular response to heat stress. Carcinogenesis. 2003;24:1723-8.
17. Mitra S, Annamalai L, Chakraborty S, Johnson K, Song X, Batra S, Mehta, P. Androgenregulated formation and degradation of gap junctions in androgen-responsive human prostate cancer cells. Mol Biol Cell. 2006;17:5400-16.
18. Kang SW, Rane NS, Kim SJ, Garrison JL, Taunton J, Hegde RS. Substrate-specific translocational attenuation during ER stress defines a pre-emptive quality control pathway. Cell. 2006;127:999-1013.
19. Musil LS, Goodenough DA. Multisubunit assembly of an integral plasmamembrane channel protein, gap junction connexin43, occurs after exit from the ER. Cell. 1993;74:1065-77.
20. Koval M, Harley JE, Hick E, Steinberg TH. Connexin46 is retained as monomers in a trans-Golgi compartment of osteoblastic cells. J Cell Biol. 1997;137:847-57.
21. Sarma JD, Wang F, Koval M. Targeted gap junction protein constructs reveal connexinspecific differences in oligomerization. J Biol Chem. 2002;277:20911-8.
22. Maza J, Das Sarma J, Koval M. Defining a minimal motif required to prevent connexin oligomerization in the endoplasmic reticulum. J Biol Chem. 2005;280:21115-21.
23. Van Slyke JK, Musil LS. Exogenous overexpression of connexins induces premature assembly of connexons in the ER J. Cell Commun Adhes. 2005;12:86.
24. Omori Y, Mesnil M, Yamasaki H. Connexin 32 mutations from X-linked Charcot-Marie-Tooth disease patients: functional defects and dominant-negative effects. Mol Biol Cell. 1996;7:907-16.
25. Kumar NM, Gilula NB. Molecular biology and genetics of gap junction channels. Semin Cell Biol. 1992;3:3-16.
26. Koch AW, Farooq A, Shan W, Zeng L, Colman DR, Zhou MM. Structure of the neural (N-) cadherin prodomain reveals a cadherin extracellular domain-like fold without adhesive characteristics. Structure. 2004;12:793-805.
27. Lagree V, Brunschwig K, Lopez P, Gilula NB, Richard G, Falk MM. Specific amino-acid residues in the N-terminus and M3 implicated in channel function and oligomerization compatibility of connexin43. J Cell Sci. 2003;116:3189-201.
28. Thomas T, Jordan K, Simek J, Shao Q, Jedeszko C, Walton P, Laird DW. Mechanisms of Cx43 and Cx26 transport to the plasma membrane and gap junction regeneration. J Cell Sci. 2005;118:4451-62.
29. George CH, Kendall JM, Evans WH. Intracellular trafficking pathways in the assembly of connexins into gap junctions. J Biol Chem. 1999;274:8678-85.
30. Lauf U, Lopez P, Falk MM. Expression of fluorescently tagged connexins: a novel approach to rescue function of oligomeric DsRed-tagged proteins. FEBS Lett. 2001;498:11-5.
31. Sá ez JC, Retamal MA, Basilio D, Bukauskas FF, Bennett MVL. Connexin-based gap junction hemichannels: gating mechanisms. Biochim Biophys Acta. 2005;1711:215-24.
32. Ebihara L. New roles for connexons. News Physiol Sci. 2003;18:100-3.
33. Goodenough DA, Paul DL. Beyond the gap: functions of unpaired connexon channels. Nat Rev Mol Cell Biol. 2003;4:285-94.
34. Harris AL. Emerging issues of connexin channels: biophysics fills the gap. Qtly Rev Biophys. 2001;34:325-472.
35. Lauf U, Giepmans BN, Lopez P, Braconnot S, Chen SC, Falk MM. Dynamic trafficking and delivery of connexons to the plasma membrane and accretion to gap junctions in living cells. Proc Natl Acad Sci USA. 2002;99:10446-51.
36. Gaietta G, Deerinck DT, Adams SR, Bouwer J, Tour O, Laird DW, Sosinsky GE, Tsien RY, Ellisman MH. Multicolor and electron microscopic imaging of connexin trafficking. Science. 2002;296:503-7.
37. Shaw RM, Fay AJ, Puthenveedu MA, von Zastrow M, Jan YN, Jan LY. Microtubule plus-end-tracking proteins target gap junctions directly from the cell interior to adherens junctions. Cell. 2007;128:547-60.
38. Guerrier A, Fonlupt P, Morand I, Rabilloud R, Audebet C, Krutovskikh V, Gros D, Rousset B, Munari-Silem Y. Gap junctions and cell polarity: connexin32 and connexin43 expressed in polarized thyroid epithelial cells assemble into separate gap junctions, which are located in distinct regions of the lateral plasma membrane domain. J Cell Sci. 1995;108:2609-17.
39. Wang Y, Rose B. An inhibition of gap-junctional communication by cadherins. J Cell Sci. 1997;110:301-9.
40. Johnson RG, Meyer RA, Lampe PD. Gap junction formation: a self-assembly model involving membrane domains of lipid and protein. In: Sperelakis N, Cole WC, editors. Cell interactions and gap junctions. Boca Raton, FL: CRC Press; 1989. pp. 159-79.
41. Traub O, Look J, Dermietzel R, Brummer F, Hülser D, Willecke K. Comparative characterization of the 21-kD and 26-kD gap junction proteins in murine liver and cultured hepatocytes. J Cell Biol. 1989;108:1039-51.
42. Musil LS, Le AC, Van Slyke JK, Roberts LM. Regulation of connexin degradation as a mechanismto increase gap junctionassembly andfunction. JBiolChem. 2000;275:25207-15.
43. Beardslee MA, Laing JG, Beyer EC, Saffitz JE. Rapid turnover of connexin43 in the adult rat heart. Circ Res. 1998;83:629-35.
44. Musil LS, Goodenough DA. Biochemical analysis of connexin43 intracellular transport, phosphorylation, and assembly into gap junctional plaques. J Cell Biol. 1991;115:1357-74.
45. Van Slyke JK, Musil LS. Cytosolic stress reduces degradation of connexin43 internalized from the cell surface and enhances gap junction formation and function. Mol Biol Cell. 2005;16:5247-57.
46. Fallon RF, Goodenough DA. Five-hour half-life of mouse liver gap-junction protein. J Cell Biol. 1981;90:521-6.
47. Fishman GI, Gao Y, Hertzberg EL, Spray DC. Reversible intercellular coupling by regulated expression of a gap junction channel gene. Cell Adhes Commun. 1995;3:353-65.
48. Jordan K, Chodock R, Hand AR, Laird DW. The origin of annular junctions: a mechanism of gap junction internalization. J Cell Sci. 2001;114:763-73.
49. McNeil PL, Steinhardt RA. Plasma membrane disruption: repair, prevention, adaptation. Annu Rev Cell Dev Biol. 2003;19:697-731.
50. Fujimoto K, Nagafuchi A, Tsukita S, Kuraoka A, Ohokuma A, Shibata Y. Dynamics of connexins, E-cadherin and a-catenin on cell membranes during gap junction formation. J Cell Sci. 1997;110:311-22.
51. Larsen WJ, Tung HN. Origin and fate of cytoplasmic gap junction vesicles in rabbit granulosa cells. Tissue Cell. 1978;10:585-598.
52. Qin H, Shao Q, Igdoura SA, Alaoui-Jamali MA, Laird DW. Lysosomal and proteasomal degradation play distinct roles in the life cycle of Cx43 in gap junctional intercellular communicationdeficient and -competent breast tumor cells. J Biol Chem. 2003;278:30005-14.
53. Laing JG, Tadros PN, Westphale EM, Beyer EC. Degradation of connexin43 gap junctions involves both the proteasome and the lysosome. Exp Cell Res. 1997;236:482-92.
54. Tsukamoto T, Nigam SK. Cell-cell dissociation upon epithelial cell scattering requires a step mediated by the proteasome. J Biol Chem. 1999;274:24579-84.
55. Longva KE, Blystad FD, Stang E, Larsen AM, Johannessen LE, Madshus IH. Ubiquitination and proteasomal activity is required for transport of the EGF receptor to inner membranes of multivesicular bodies. J Cell Biol. 2002;156:843-54.
56. Younger JM, Ren HY, Chen L, Fan CY, Fields A, Patterson C, Cyr DM. A foldable CFTRδF508 biogenic intermediate accumulates upon inhibition of the Hsc70-CHIP E3 ubiquitin ligase. J Cell Biol. 2004;167:1075-85.
57. Johnson R, Hammer M, Sheridan J, Revel JP. Gap junction formation between reaggregated Novikoff hepatoma cells. Proc Natl Acad Sci USA. 1974;71:4536-40.
58. Solan JL, Lampe PD. Connexin phosphorylation as a regulatory event linked to gap junction channel assembly. Biochim Biophys Acta. 2005;1711:154-63.
59. Hunter AW, Barker RJ, Zhu C, Gourdie RG. Zonula occludens-1 alters connexin43 gap junction size and organization by influencing channel accretion. Mol Biol Cell. 2005;16:5686-98.
60. Ahmad S, Tang W, Chang Q, Qu Y, Hibshman J, Li Y, Söhl G, Willecke K, Chen P, Lin X. Restoration of connexin26 protein level in the cochlea completely rescues hearing in a mouse model of human connexin30-linked deafness. Proc Natl Acad Sci USA. 2007;104:1337-41.
61. Mesnil M, Crespin S, Avanzo JL, Zaidan-Dagli ML. Defective gap junctional intercellular communication in the carcinogenic process. Biochim Biophys Acta. 2005;1719:125-45.
62. Mesnil M. Connexins and cancer. Biol Cell. 2002;94:493-500.
63. Mesnil M, Yamasaki H. Bystander effect in herpes simplex virus-thymidine kinase/ganciclovir cancer gene therapy: role of gap-junctional intercellular communication. Cancer Res. 2000;60:3989-99.