Cx50 requires an intact PDZ-binding motif and ZO-1 for the formation of functional intercellular channels

Molecular Biology of the Cell

Volumn 22, Issue 23, 2011, Pages 4503-4512

  Chai, Zhifang ^a   Goodenough, Daniel A ^a   Paul, David L ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAP JUNCTION PROTEIN; PROTEIN ZO1; SMALL INTERFERING RNA;

ARTICLE; CELL COMMUNICATION; CONTROLLED STUDY; GAP JUNCTION; HUMAN; HUMAN CELL; INTERCELLULAR SPACE; PDZ DOMAIN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN MOTIF;

AMINO ACID MOTIFS; ANIMALS; BINDING SITES; CELL COMMUNICATION; CONNEXINS; EYE PROTEINS; GAP JUNCTIONS; GENE KNOCKOUT TECHNIQUES; HELA CELLS; HUMANS; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUTATION; PHOSPHOPROTEINS; PROTEIN STRUCTURE, TERTIARY; RNA, SMALL INTERFERING;

EID: 82655189989     PISSN: 10591524     EISSN: 19394586     Source Type: Journal    
DOI: 10.1091/mbc.E11-05-0438     Document Type: Article

References (60)

1. Beyer EC, Paul DL, Goodenough DA (1987). Connexin43: a protein from rat heart homologous to a gap junction protein from liver. J Cell Biol 105, 2621-2629. (Pubitemid 18017692)
2. Brizzard BL, Chubet RG, Vizard DL (1994). Immunoaffinity purification of FLAG epitope-tagged bacterial alkaline phosphatase using a novel monoclonal antibody and peptide elution. Biotechniques 16, 730-735. (Pubitemid 2067227)
3. Derosa AM, Mui R, Srinivas M, White TW (2006). Functional characterization of a naturally occurring cx50 truncation. Invest Ophthalmol Vis Sci 47, 4474-4481. (Pubitemid 46579375)
4. Ebihara L, Xu X, Oberti C, Beyer EC, Berthoud VM (1999). Co-expression of lens fiber connexins modifies hemi-gap-junctional channel behavior. Biophys J 76, 198-206. (Pubitemid 29202449)
5. Eckert R (2002). pH gating of lens fibre connexins. Pflugers Arch 443, 843-851.
6. Elfgang C, Eckert R, Lichtenberg-Fraté H, Butterweck A, Traub O, Klein RA, Hülser DF, Willecke K (1995). Specific permeability and selective formation of gap junction channels in connexin-transfected HeLa cells. J Cell Biol 129, 805-817.
7. Flores CE, Li X, Bennett MV, Nagy JI, Pereda AE (2008). Interaction between connexin35 and zonula occludens-1 and its potential role in the regulation of electrical synapses. Proc Natl Acad Sci USA 105, 12545-12550.
8. Frenzel EM, Johnson RG (1996). Gap junction formation between cultured embryonic lens cells is inhibited by antibody to N-cadherin. Dev Biol 179, 1-16. (Pubitemid 26363243)
9. Giepmans BN, Moolenaar WH (1998). The gap junction protein connexin43 interacts with the second PDZ domain of the zona occludens-1 protein. Curr Biol 8, 931-934. (Pubitemid 28371760)
10. Goodenough DA, Paul DL (2009). Gap junctions. Cold Spring Harbor Perspect Biol 1:a002576.
11. Guerrier A, Fonlupt P, Morand I, Rabilloud R, Audebet C, Krutovskikh V, Gros D, Rousset B, Munari-Silem Y (1995). 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 108, 2609-2617.
12. Helbig I, Sammler E, Eliava M, Bolshakov AP, Rozov A, Bruzzone R, Monyer H, Hormuzdi SG (2010). In vivo evidence for the involvement of the carboxy terminal domain in assembling connexin 36 at the electrical synapse. Mol Cell Neurosci.
13. Hopperstad MG, Srinivas M, Spray DC (2000). Properties of gap junction channels formed by Cx46 alone and in combination with Cx50. Biophys J 79, 1954-1966.
14. Hunter AW, Barker RJ, Zhu C, Gourdie RG (2005). ZO-1 alters connexin43 gap junction size and organization by influencing channel accretion. Mol Biol Cell 16, 5686-5698. (Pubitemid 41752218)
15. Hunter AW, Gourdie RG (2008). The second PDZ domain of zonula occludens-1 is dispensable for targeting to connexin 43 gap junctions. Cell Commun Adhes 15, 55-63.
16. Itoh M, Nagafuchi A, Yonemura S, Kitani-Yasuda T, Tsukita S, Tsukita SH (1993). The 220-kD protein colocalizing with cadherins in non-epithelial cells is identical to ZO-1, a tight junction-associated protein in epithelial cells: cDNA cloning and immunoelectron microscopy. J Cell Biol 121, 491-502. (Pubitemid 23131262)
17. Jiang JX, Goodenough DA (1996). Heteromeric connexons in lens gap junction channels. Proc Natl Acad Sci USA 93, 1287-1291. (Pubitemid 26052881)
18. Kausalya PJ, Reichert M, Hunziker W (2001). Connexin45 directly binds to ZO-1 and localizes to the tight junction region in epithelial MDCK cells. FEBS Lett 505, 92-96. (Pubitemid 32831036)
19. Keane RW, Mehta PP, Rose B, Honig LS, Loewenstein WR, Rutishauser U (1988). Neural differentiation, NCAM-mediated adhesion, and gap junctional communication in neuroectoderm. A study in vitro. J Cell Biol 106, 1307-1319.
20. Koval M (2006). Pathways and control of connexin oligomerization. Trends Cell Biol 16, 159-166.
21. Laing JG, Manley-Markowski RN, Koval M, Civitelli R, Steinberg TH (2001). Connexin45 interacts with zonula occludens-1 and connexin43 in osteoblastic cells. J Biol Chem 276, 23051-23055.
22. Langlois S, Cowan KN, Shao Q, Cowan BJ, Laird DW (2008). Caveolin-1 and -2 interact with connexin43 and regulate gap junctional intercellular communication in keratinocytes. Mol Biol Cell 19, 912-928. (Pubitemid 351481808)
23. Lee HJ, Zheng JJ (2010). PDZ domains and their binding partners: structure, specificity, and modification. Cell Commun Signal 8, 8.
24. Li X, Ionescu AV, Lynn BD, Lu S, Kamasawa N, Morita M, Davidson KG, Yasumura T, Rash JE, Nagy JI (2004a). Connexin47, connexin29 and connexin32 co-expression in oligodendrocytes and cx47 association with zonula occludens-1 (ZO-1) in mouse brain. Neuroscience 126, 611-630. (Pubitemid 38759255)
25. Li X, Lu S, Nagy JI (2009). Direct association of connexin36 with zonula occludens-2 and zonula occludens-3. Neurochem Int 54, 393-402.
26. Li X, Olson C, Lu S, Kamasawa N, Yasumura T, Rash JE, Nagy JI (2004b). Neuronal connexin36 association with zonula occludens-1 protein (ZO-1) in mouse brain and interaction with the first PDZ domain of ZO-1. Eur J Neurosci 19, 2132-2146. (Pubitemid 38582202)
27. Lin JS, Eckert R, Kistler J, Donaldson P (1998). Spatial differences in gap junction gating in the lens are a consequence of connexin cleavage. Eur J Cell Biol 76, 246-250. (Pubitemid 28431572)
28. Lin JS, Fitzgerald S, Dong YM, Knight C, Donaldson P, Kistler J (1997). Processing of the gap junction protein connexin50 in the ocular lens is accomplished by calpain. Eur J Cell Biol 73, 141-149. (Pubitemid 27267911)
29. Liu L, Li Y, Lin J, Liang Q, Sheng X, Wu J, Huang R, Liu S, Li Y (2010). Connexin43 interacts with caveolin-3 in the heart. Mol Biol Rep 37, 1685-1691.
30. Maass K et al. (2004). Defective epidermal barrier in neonatal mice lacking the c-terminal region of connexin43. Mol Biol Cell 15, 4597-4608. (Pubitemid 39299107)
31. Magnotti LM, Goodenough DA, Paul DL (2011). Functional heterotypic interactions between astrocyte and oligodendrocyte connexins. Glia 59, 26-34.
32. Manthey D, Banach K, Desplantez T, Lee CG, Kozak CA, Traub O, Weingart R, Willecke K (2001). Intracellular domains of mouse connexin26 and -30 affect diffusional and electrical properties of gap junction channels. J Membr Biol 181, 137-148. (Pubitemid 32466639)
33. Martin PE, Blundell G, Ahmad S, Errington RJ, Evans WH (2001). Multiple pathways in the trafficking and assembly of connexin 26, 32 and 43 into gap junction intercellular communication channels. J Cell Sci 114, 3845-3855. (Pubitemid 33094699)
34. Meyer RA, Laird DW, Revel JP, Johnson RG (1992). Inhibition of gap junction and adherens junction assembly by connexin and A-CAM antibodies. J Cell Biol 119, 179-189.
35. Morley GE, Taffet SM, Delmar M (1996). Intramolecular interactions mediate pH regulation of connexin43 channels. Biophys J 70, 1294-1302. (Pubitemid 26073042)
36. Musil LS, Cunningham BA, Edelman GM, Goodenough DA (1990). Differential phosphorylation of the gap junction protein connexin43 in junctional communication-competent and deficient cell lines. J Cell Biol 111, 2077-2088.
37. Nielsen PA, Baruch A, Shestopalov VI, Giepmans BN, Dunia I, Benedetti EL, Kumar NM (2003). Lens connexins α3 (Cx46) and α8 (Cx50) interact with zonula occludens protein-1 (ZO-1). Mol Biol Cell 14, 2470-2481. (Pubitemid 36724335)
38. Nielsen PA, Beahm DL, Giepmans BN, Baruch A, Hall JE, Kumar NM (2002). Molecular cloning, functional expression, and tissue distribution of a novel human gap junction forming protein, connexin-31.9. J Biol Chem 277, 38272-38283. (Pubitemid 35154682)
39. Puller C, de Sevilla Muller LP, Janssen-Bienhold U, Haverkamp S (2009). ZO-1 and the spatial organization of gap junctions and glutamate receptors in the outer plexiform layer of the mammalian retina. J Neurosci 29, 6266-6275.
40. Orthmann-Murphy JL, Freidin M, Fischer E, Scherer SS, Abrams CK (2007). Two distinct heterotypic channels mediate gap junction coupling between astrocyte and oligodendrocyte connexins. J Neurosci 27, 13949-13957. (Pubitemid 351377852)
41. Paul DL, Ebihara L, Takemoto LJ, Swenson KI, Goodenough DA (1991). Connexin46, a novel lens gap junction protein, induces voltage-gated currents in nonjunctional plasma membrane of Xenopus oocytes. J Cell Biol 115, 1077-1089. (Pubitemid 21909955)
42. Qu C, Gardner P, Schrijver I (2009). The role of the cytoskeleton in the formation of gap junctions by connexin 30. Exp Cell Res 315, 1683-1692.
43. Rong P, Wang X, Niesman I, Wu Y, Benedetti LE, Dunia I, Levy E, Gong X (2002). Disruption of Gja8 (alpha8 connexin) in mice leads to microphthalmia associated with retardation of lens growth and lens fiber maturation. Development 129, 167-174. (Pubitemid 34863785)
44. Schubert AL, Schubert W, Spray DC, Lisanti MP (2002). Connexin family members target to lipid raft domains and interact with caveolin-1. Biochemistry 41, 5754-5764. (Pubitemid 34462696)
45. Segretain D, Falk MM (2004). Regulation of connexin biosynthesis, assembly, gap junction formation, and removal. Biochim Biophys Acta 1662, 3-21. (Pubitemid 38366510)
46. Shaw RM, Fay AJ, Puthenveedu MA, von Zastrow M, Jan YN, Jan LY (2007). Microtubule plus-end-tracking proteins target gap junctions directly from the cell interior to adherens junctions. Cell 128, 547-560. (Pubitemid 46198893)
47. Singh D, Solan JL, Taffet SM, Javier R, Lampe PD (2005). Connexin43 interacts with zona occludens-1 and -2 proteins in a cell cycle stage specific manner. J Biol Chem 280, 30416-30421. (Pubitemid 41216225)
48. Songyang Z, Fanning AS, Fu C, Xu J, Marfatia SM, Chishti AH, Crompton A, Chan AC, Anderson JM, Cantley LC (1997). Recognition of unique carboxyl-terminal motifs by distinct PDZ domains. Science 275, 73-77. (Pubitemid 27020310)
49. Stergiopoulos K, Alvarado JL, Mastroianni M, Ek-Vitorin JF, Taffet SM, Delmar M (1999). Hetero-domain interactions as a mechanism for the regulation of connexin channels. Circ Res 84, 1144-1155. (Pubitemid 29244776)
50. Stevenson BR, Siliciano JD, Mooseker MS, Goodenough DA (1986). Identification of ZO-1: a high molecular weight polypeptide associated with the tight junction (zonula occludens) in a variety of epithelia. J Cell Biol 103, 755-766. (Pubitemid 17177325)
51. Thomas T, Jordan K, Laird DW (2001). Role of cytoskeletal elements in the recruitment of Cx43-GFP and Cx26- YFP into gap junctions. Cell Adhes Commun 8, 231-236. (Pubitemid 34982292)
52. Toyofuku T, Yabuki M, Otsu K, Kuzuya T, Hori M, Tada M (1998). Direct association of the gap junction protein connexin-43 with ZO-1 in cardiac myocytes. J Biol Chem 273, 12725-12731. (Pubitemid 28246824)
53. VanSlyke JK, Naus CC, Musil LS (2009). Conformational maturation and post-ER multisubunit assembly of gap junction proteins. Mol Biol Cell 20, 2451-2463.
54. Wei CJ, Francis R, Xu X, Lo CW (2005). Connexin43 associated with an N-cadherin-containing multiprotein complex is required for gap junction formation in NIH3T3 cells. J Biol Chem 280, 19925-19936. (Pubitemid 41379521)
55. White TW (2002). Unique and redundant connexin contributions to lens development. Science 295, 319-320.
56. White TW, Bruzzone R, Goodenough DA, Paul DL (1992). Mouse Cx50, a functional member of the connexin family of gap junction proteins, is the lens fiber protein MP70. Mol Biol Cell 3, 711-720. (Pubitemid 23084555)
57. White TW, Bruzzone R, Wolfram S, Paul DL, Goodenough DA (1994). Selective interactions among the multiple connexin proteins expressed in the vertebrate lens: the second extracellular domain is a determinant of compatibility between connexins. J Cell Biol 125, 879-892. (Pubitemid 24151182)
58. White TW, Goodenough DA, Paul DL (1998). Targeted ablation of connexin50 in mice results in microphthalmia and zonular pulverulent cataracts. J Cell Biol 143, 815-825. (Pubitemid 28512573)
59. Xu X, Berthoud VM, Beyer EC, Ebihara L (2002). Functional role of the carboxyl terminal domain of human connexin 50 in gap junctional channels. J Membr Biol 186, 101-112. (Pubitemid 34252646)
60. Zhang JT, Chen MG, Foote CI, Nicholson BJ (1996). Membrane integration of in vitro-translated gap junctional proteins - co- and post-translational mechanisms. Mol Biol Cell 7, 471-482. (Pubitemid 26089660)