Cx43 associates with Nav1.5 in the cardiomyocyte perinexus

Journal of Membrane Biology

Volumn 245, Issue 7, 2012, Pages 411-422

  Rhett, J Matthew ^a   Ongstad, Emily L ^a   Jourdan, Jane ^a   Gourdie, Robert G ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Connexin43; Duolink; Gap junction; Hemichannel; Nav1.5; Perinexus; Sodium channel

Indexed keywords

CONNEXIN 43; PROTEIN ZO1; SODIUM CHANNEL NAV1.5; TRITON X 100;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; GAP JUNCTION; HEART MUSCLE CELL; HYPOTHESIS; IMAGE ANALYSIS; IMMUNOFLUORESCENCE TEST; NONHUMAN; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; QUANTITATIVE ANALYSIS; RAT; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; CELLS, CULTURED; CONNEXIN 43; IMMUNOHISTOCHEMISTRY; MYOCYTES, CARDIAC; NAV1.5 VOLTAGE-GATED SODIUM CHANNEL; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84866022277     PISSN: 00222631     EISSN: 14321424     Source Type: Journal    
DOI: 10.1007/s00232-012-9465-z     Document Type: Article

References (59)

1. Baker SM, Kim N, Gumpert AM, Segretain D, Falk MM (2008) Acute internalization of gap junctions in vascular endothelial cells in response to inflammatory mediator-induced G-protein coupled receptor activation. FEBS Lett 582:4039-4046
2. Beahm DL, Oshima A, Gaietta GM, Hand GM, Smock AE, Zucker SN, Toloue MM, Chandrasekhar A, Nicholson BJ, Sosinsky GE (2006) Mutation of a conserved threonine in the third transmembrane helix of alpha-and beta-connexins creates a dominant-negative closed gap junction channel. J Biol Chem 281:7994-8009 (Pubitemid 43847417)
3. 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)
4. Clausson CM, Allalou A, Weibrecht I, Mahmoudi S, Farnebo M, Landegren U, Wahlby C, Soderberg O (2011) Increasing the dynamic range of in situ PLA. Nat Methods 8:892-893
5. Cohen SA (1996) Immunocytochemical localization of rH1 sodium channel in adult rat heart atria and ventricle. Presence in terminal intercalated disks. Circulation 94:3083-3086 (Pubitemid 26427470)
6. Colussi C, Berni R, Rosati J, Straino S, Vitale S, Spallotta F, Baruffi S, Bocchi L, Delucchi F, Rossi S, Savi M, Rotili D, Quaini F, Macchi E, Stilli D, Musso E, Mai A, Gaetano C, Capogrossi MC (2010) The histone deacetylase inhibitor suberoylanilide hydroxamic acid reduces cardiac arrhythmias in dystrophic mice. Cardiovasc Res 87:73-82
7. Decrock E, De Vuyst E, Vinken M, Van Moorhem M, Vranckx K, Wang N, Van Laeken L, De Bock M, D'Herde K, Lai CP, Rogiers V, Evans WH, Naus CC, Leybaert L (2009) Connexin 43 hemichannels contribute to the propagation of apoptotic cell death in a rat C6 glioma cell model. Cell Death Differ 16:151-163
8. Delmar M, Liang FX (2012) Connexin43 and the regulation of intercalated disc function. Heart Rhythm 9:835-838
9. Desplantez T, Dupont E, Severs NJ, Weingart R (2007) Gap junction channels and cardiac impulse propagation. J Membr Biol 218:13-28 (Pubitemid 350132121)
10. Evans WH, Martin PE (2002) Gap junctions: structure and function (review). Mol Membr Biol 19:121-136 (Pubitemid 34753316)
11. Flores CE, Nannapaneni S, Davidson KG, Yasumura T, Bennett MV, Rash JE, Pereda AE (2012) Trafficking of gap junction channels at a vertebrate electrical synapse in vivo. Proc Natl Acad Sci USA 109:E573-E582
12. Fort AG, Murray JW, Dandachi N, Davidson MW, Dermietzel R, Wolkoff AW, Spray DC (2011) In vitro motility of liver connexin vesicles along microtubules utilizes kinesin motors. J Biol Chem 286:22875-22885
13. Gaietta G, Deerinck TJ, Adams SR, Bouwer J, Tour O, Laird DW, Sosinsky GE, Tsien RY, Ellisman MH (2002) Multicolor and electron microscopic imaging of connexin trafficking. Science 296:503-507 (Pubitemid 34408665)
14. Gutstein DE, Morley GE, Tamaddon H, Vaidya D, Schneider MD, Chen J, Chien KR, Stuhlmann H, Fishman GI (2001) Conduction slowing and sudden arrhythmic death in mice with cardiacrestricted inactivation of connexin43. Circ Res 88:333-339 (Pubitemid 32173758)
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. Hunter AW, Barker RJ, Zhu C, Gourdie RG (2005) Zonula occludens-1 alters connexin43 gap junction size and organization by influencing channel accretion. Mol Biol Cell 16:5686-5698 (Pubitemid 41752218)
17. Jansen JA, Noorman M, Musa H, Stein M, de Jong S, van der Nagel R, Hund TJ, Mohler PJ, Vos MA, van Veen TA, de Bakker JM, Delmar M, van Rijen HV (2012) Reduced heterogeneous expression of Cx43 results in decreased Nav1.5 Expression and reduced sodium current which accounts for arrhythmia vulnerability in conditional Cx43 knockout mice. Heart Rhythm 9:600-607
18. Jarvius J, Melin J, Goransson J, Stenberg J, Fredriksson S, Gonzalez-Rey C, Bertilsson S, Nilsson M (2006) Digital quantification using amplified single-molecule detection. Nat Methods 3:725-727 (Pubitemid 44275741)
19. Johnson R, Hammer M, Sheridan J, Revel JP (1974) Gap junction formation between reaggregated Novikoff hepatoma cells. Proc Natl Acad Sci USA 71:4536-4540
20. Johnson RG, Meyer RA, Li XR, Preus DM, Tan L, Grunenwald H, Paulson AF, Laird DW, Sheridan JD (2002) Gap junctions assemble in the presence of cytoskeletal inhibitors, but enhanced assembly requires microtubules. Exp Cell Res 275:67-80
21. Johnson RG, Reynhout JK, TenBroek EM, Quade BJ, Yasumura T, Davidson KG, Sheridan JD, Rash JE (2012) Gap junction assembly: roles for the formation plaque and regulation by the C-terminus of connexin43. Mol Biol Cell 23:71-86
22. Kamasawa N, Furman CS, Davidson KG, Sampson JA, Magnie AR, Gebhardt BR, Kamasawa M, Yasumura T, Zumbrunnen JR, Pickard GE, Nagy JI, Rash JE (2006) Abundance and ultrastructural diversity of neuronal gap junctions in the OFF and ON sublaminae of the inner plexiform layer of rat and mouse retina. Neuroscience 142:1093-1117 (Pubitemid 44636068)
23. Kleber AG, Rudy Y (2004) Basic mechanisms of cardiac impulse propagation and associated arrhythmias. Physiol Rev 84:431-488 (Pubitemid 38365490)
24. Koval M (2006) Pathways and control of connexin oligomerization. Trends Cell Biol 16:159-166 (Pubitemid 43358004)
25. Kucera JP, Rohr S, Rudy Y (2002) Localization of sodium channels in intercalated disks modulates cardiac conduction. Circ Res 91:1176-1182 (Pubitemid 36076367)
26. Lal R, John SA, Laird DW, Arnsdorf MF (1995) Heart gap junction preparations reveal hemiplaques by atomic force microscopy. Am J Physiol 268:C968-C977
27. Lampe PD, Cooper CD, King TJ, Burt JM (2006) Analysis of connexin43 phosphorylated at S325, S328 and S330 in normoxic and ischemic heart. J Cell Sci 119:3435-3442 (Pubitemid 44405227)
28. Lauf U, Giepmans BN, Lopez P, Braconnot S, Chen SC, Falk MM (2002) Dynamic trafficking and delivery of connexons to the plasma membrane and accretion to gap junctions in living cells. Proc Natl Acad Sci USA 99:10446-10451
29. Li H, Liu TF, Lazrak A, Peracchia C, Goldberg GS, Lampe PD, Johnson RG (1996) Properties and regulation of gap junctional hemichannels in the plasma membranes of cultured cells. J Cell Biol 134:1019-1030 (Pubitemid 26278225)
30. Lin X, Liu N, Lu J, Zhang J, Anumonwo JM, Isom LL, Fishman GI, Delmar M (2011) Subcellular heterogeneity of sodium current properties in adult cardiac ventricular myocytes. Heart Rhythm 8:1923-1930
31. Liu TF, Johnson RG (1999) Effects of TPA on dye transfer and dye leakage in fibroblasts transfected with a connexin 43 mutation at ser368. Methods Find Exp Clin Pharmacol 21:387-390 (Pubitemid 29334280)
32. Maier SK, Westenbroek RE, Schenkman KA, Feigl EO, Scheuer T, Catterall WA (2002) An unexpected role for brain-type sodium channels in coupling of cell surface depolarization to contraction in the heart. Proc Natl Acad Sci USA 99:4073-4078 (Pubitemid 34252231)
33. Malhotra JD, Thyagarajan V, Chen C, Isom LL (2004) Tyrosinephosphorylated and nonphosphorylated sodium channel beta1 subunits are differentially localized in cardiac myocytes. J Biol Chem 279:40748-40754 (Pubitemid 39287670)
34. Mori Y, Fishman GI, Peskin CS (2008) Ephaptic conduction in a cardiac strand model with 3D electrodiffusion. Proc Natl Acad Sci USA 105:6463-6468 (Pubitemid 351758368)
35. Musil LS, Goodenough DA (1991) Biochemical analysis of connexin43 intracellular transport, phosphorylation, and assembly into gap junctional plaques. J Cell Biol 115:1357-1374 (Pubitemid 21909980)
36. Musil LS, Goodenough DA (1993) Multisubunit assembly of an integral plasma membrane channel protein, gap junction connexin43, occurs after exit from the ER. Cell 74:1065-1077 (Pubitemid 23289463)
37. Noorman M, van Rijen HV, van Veen TA, de Bakker JM, Stein M (2008) Differences in distribution of fibrosis in the ventricles underlie dominant arrhythmia vulnerability of the right ventricle in senescent mice. Neth Heart J 16:356-358
38. Noorman M, van der Heyden MA, van Veen TA, Cox MG, Hauer RN, de Bakker JM, van Rijen HV (2009) Cardiac cell-cell junctions in health and disease: electrical versus mechanical coupling. J Mol Cell Cardiol 47:23-31
39. Palatinus JA, O'Quinn MP, Barker RJ, Harris BS, Jourdan J, Gourdie RG (2011) ZO-1 determines adherens and gap junction localization at intercalated disks. Am J Physiol Heart Circ Physiol 300:H583-H594
40. Palatinus JA, Rhett JM, Gourdie RG (2012) The connexin43 carboxyl terminus and cardiac gap junction organization. Biochim Biophys Acta 1818:1831-1843
41. Petitprez S, Zmoos AF, Ogrodnik J, Balse E, Raad N, El-Haou S, Albesa M, Bittihn P, Luther S, Lehnart SE, Hatem SN, Coulombe A, Abriel H (2011) SAP97 and dystrophin macromolecular complexes determine two pools of cardiac sodium channels Nav1.5 in cardiomyocytes. Circ Res 108:294-304
42. Quist AP, Rhee SK, Lin H, Lal R (2000) Physiological role of gapjunctional hemichannels. Extracellular calcium-dependent isosmotic volume regulation. J Cell Biol 148:1063-1074
43. Rhett JM, Gourdie RG (2012) The perinexus: a new feature of Cx43 gap junction organization. Heart Rhythm 9:619-623
44. Rhett JM, Jourdan J, Gourdie RG (2011) Connexin 43 connexon to gap junction transition is regulated by zonula occludens-1. Mol Biol Cell 22:1516-1528
45. Rodriguez-Sinovas A, Boengler K, Cabestrero A, Gres P, Morente M, Ruiz-Meana M, Konietzka I, Miro E, Totzeck A, Heusch G, Schulz R, Garcia-Dorado D (2006) Translocation of connexin 43 to the inner mitochondrial membrane of cardiomyocytes through the heat shock protein 90-dependent TOM pathway and its importance for cardioprotection. Circ Res 99:93-101 (Pubitemid 44297060)
46. Saez JC, Contreras JE, Bukauskas FF, Retamal MA, Bennett MV (2003) Gap junction hemichannels in astrocytes of the CNS. Acta Physiol Scand 179:9-22 (Pubitemid 37083058)
47. Severs NJ, Bruce AF, Dupont E, Rothery S (2008) Remodelling of gap junctions and connexin expression in diseased myocardium. Cardiovasc Res 80:9-19
48. 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)
49. Shintani-Ishida K, Uemura K, Yoshida K (2007) Hemichannels in cardiomyocytes open transiently during ischemia and contribute to reperfusion injury following brief ischemia. Am J Physiol Heart Circ Physiol 293:H1714-H1720 (Pubitemid 47367219)
50. Smyth JW, Vogan JM, Buch PJ, Zhang SS, Fong TS, Hong TT, Shaw RM (2012) Actin cytoskeleton rest stops regulate anterograde traffic of connexin 43 vesicles to the plasma membrane. Circ Res 110:978-989
51. Solan JL, Lampe PD (2007) Key connexin 43 phosphorylation events regulate the gap junction life cycle. J Membr Biol 217:35-41 (Pubitemid 350160003)
52. Solan JL, Marquez-Rosado L, Sorgen PL, Thornton PJ, Gafken PR, Lampe PD (2007) Phosphorylation at S365 is a gatekeeper event that changes the structure of Cx43 and prevents down-regulation by PKC. J Cell Biol 179:1301-1309 (Pubitemid 350277746)
53. Stein M, van Veen TA, Remme CA, Boulaksil M, Noorman M, van Stuijvenberg L, van der Nagel R, Bezzina CR, Hauer RN, de Bakker JM, van Rijen HV (2009) Combined reduction of intercellular coupling and membrane excitability differentially affects transverse and longitudinal cardiac conduction. Cardiovasc Res 83:52-60
54. Tence M, Ezan P, Amigou E, Giaume C (2012) Increased interaction of connexin43 with zonula occludens-1 during inhibition of gap junctions by G protein-coupled receptor agonists. Cell Signal 24:86-98
55. Thompson RJ, Zhou N, MacVicar BA (2006) Ischemia opens neuronal gap junction hemichannels. Science 312:924-927 (Pubitemid 43727327)
56. van Zeijl L, Ponsioen B, Giepmans BN, Ariaens A, Postma FR, Varnai P, Balla T, Divecha N, Jalink K, Moolenaar WH (2007) Regulation of connexin43 gap junctional communication by phosphatidylinositol 4, 5-bisphosphate. J Cell Biol 177:881-891 (Pubitemid 46873093)
57. Veeraraghavan R, Salama ME, Poelzing S (2012) Interstitial volume modulates the conduction velocity-gap junction relationship. Am J Physiol Heart Circ Physiol 302:H278-H286
58. Yuan D, Wang Q, Wu D, Yu M, Zhang S, Li L, Tao L, Harris AL (2012) Monocyte-endothelial adhesion is modulated by Cx43-stimulated ATP release from monocytes. Biochem Biophys Res Commun 420:536-541
59. Zhu C, Barker RJ, Hunter AW, Zhang Y, Jourdan J, Gourdie RG (2005) Quantitative analysis of ZO-1 colocalization with Cx43 gap junction plaques in cultures of rat neonatal cardiomyocytes. Microsc Microanal 11:244-248 (Pubitemid 40870193)