Super-resolution fluorescencemicroscopy of the cardiac connexome reveals plakophilin-2 inside the connexin43 plaque

Cardiovascular Research

Volumn 100, Issue 2, 2013, Pages 231-240

  Agullo Pascual, Esperanza ^a   Reid, Dylan A ^a   Keegan, Sarah ^a   Sidhu, Manavjeet ^a   Fenyö, David ^a   Rothenberg, Eli ^a   Delmar, Mario ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Ankyrin G; Connexin43; Plakophilin 2

Indexed keywords

ANKYRIN; CONNEXIN 43; PLAKOPHILIN; PLAKOPHILIN 2; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; ANK3 PROTEIN, MOUSE; PKP2 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL COMMUNICATION; CELL JUNCTION; CELL STRUCTURE; COMPARATIVE STUDY; CONNEXOME; CONTROLLED STUDY; DESMOSOME; DIFFRACTION; FLUORESCENCE MICROSCOPY; FREEZE FRACTURE; GAP JUNCTION; HEART MUSCLE CELL; HEART VENTRICLE; ILLUMINATION; IMAGE RECONSTRUCTION; IMMUNOFLUORESCENCE MICROSCOPY; MOLECULAR IMAGING; NONHUMAN; PRIORITY JOURNAL; RAT; WESTERN BLOTTING; ANIMAL; ANKYRIN-G; CHEMISTRY; CONNEXIN43; METHODOLOGY; MONTE CARLO METHOD; MOUSE; PLAKOPHILIN-2; ULTRASTRUCTURE;

ANKYRIN-G; CONNEXIN43; PLAKOPHILIN-2;

ANIMALS; ANKYRINS; CONNEXIN 43; DESMOSOMES; GAP JUNCTIONS; MICE; MICROSCOPY, FLUORESCENCE; MONTE CARLO METHOD; MYOCYTES, CARDIAC; PLAKOPHILINS; RATS;

EID: 84885391271     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvt191     Document Type: Article

References (32)

1. Born MW, E. Principles of Optics: Electromagnetic Theory of Propagation, Interference and Diffraction of Light. Cambridge: Cambridge University Press, 1997.
2. Heilemann M, van de Linde S, Schuttpelz M, Kasper R, Seefeldt B, Mukherjee A et al. Subdiffraction-resolution fluorescence imaging with conventional fluorescent probes. Angew Chem Int Ed Engl 2008;47:6172-6176.
3. Baddeley D, Jayasinghe ID, Lam L, Rossberger S, Cannell MB, Soeller C. Optical singlechannel resolution imaging of the ryanodine receptor distribution in rat cardiac myocytes. Proc Natl Acad Sci U S A 2009;106:22275-22280.
4. Soeller C, Baddeley D. Super-resolution imaging of EC coupling protein distribution in the heart. J Mol Cell Cardiol 2013;58:32-40.
5. Wong J, Baddeley D, Bushong EA, Yu Z, Ellisman MH, Hoshijima M et al. Nanoscale distribution of ryanodine receptors and caveolin-3 in mouse ventricular myocytes: dilation of T-tubules near junctions. Biophys J 2013;104:L22-L24.
6. Oxford EM, Musa H, Maass K, Coombs W, Taffet SM, Delmar M. Connexin43 remodeling caused by inhibition of plakophilin-2 expression in cardiac cells. Circ Res 2007;101: 703-711.
7. Asimaki A, Tandri H, Huang H, Halushka MK, Gautam S, Basso C et al. A new diagnostic test for arrhythmogenic right ventricular cardiomyopathy. N Engl J Med 2009;360: 1075-1084.
8. Li J, Patel VV, Kostetskii I, Xiong Y, Chu AF, Jacobson JT et al. Cardiac-specific loss of N-cadherin leads to alteration in connexins with conduction slowing and arrhythmogenesis. Circ Res 2005;97:474-481.
9. Sato PY, Musa H, Coombs W, Guerrero-Serna G, Patino GA, Taffet SM et al. Loss of plakophilin-2 expression leads to decreased sodium current and slower conduction velocity in cultured cardiac myocytes. Circ Res 2009;105:523-526.
10. Agullo-Pascual E, Delmar M. The noncanonical functions of Cx43 in the heart. J Membr Biol 2012;245:477-482.
11. Kaplan SR, Gard JJ, Protonotarios N, Tsatsopoulou A, Spiliopoulou C, Anastasakis A et al. Remodeling of myocyte gap junctions in arrhythmogenic right ventricular cardiomyopathy due to a deletion in plakoglobin (Naxos disease). Heart Rhythm 2004;1:3-11.
12. Kizhatil K, Davis JQ, Davis L, Hoffman J, Hogan BL, Bennett V. Ankyrin-G is a molecular partner of E-cadherin in epithelial cells and early embryos. J Biol Chem 2007;282: 26552-26561.
13. Lowe JS, Palygin O, Bhasin N, Hund TJ, Boyden PA, Shibata E et al. Voltage-gated Nav channel targeting in the heart requires an ankyrin-G dependent cellular pathway. J Cell Biol 2008;180:173-186.
14. Zhou D, Lambert S, Malen PL, Carpenter S, Boland LM, Bennett V. Ankyring is required for clustering of voltage-gated Nachannels at axon initial segments and for normal action potential firing. J Cell Biol 1998;143:1295-1304.
15. Sato PY, Coombs W, Lin X, Nekrasova O, Green KJ, Isom LL et al. Interactions between ankyrin-G, Plakophilin-2, and Connexin43 at the cardiac intercalated disc. Circ Res 2011; 109:193-201.
16. Rhett JM, Jourdan J, Gourdie RG. Connexin 43 connexon to gap junction transition is regulated by zonula occludens-1. Mol Biol Cell 2011;22:1516-1528.
17. Henriques R, Lelek M, Fornasiero EF, Valtorta F, Zimmer C, Mhlanga MM. Quick PALM: 3D real-time photoactivation nanoscopy image processing in Image J. Nat Methods 2010; 7:339-340.
18. Malkusch S, Muranyi W, Muller B, Krausslich HG, Heilemann M. Single-molecule coordinate-based analysis of the morphology of HIV-1 assembly sites with nearmolecular spatial resolution. Histochem Cell Biol 2013;139:173-179.
19. Yamaguchi S, Reid DA, Rothenberg E, Darwin AJ. Changes in Psp protein binding partners, localization and behaviour upon activation of the Yersinia enterocolitica phage shock protein response. Mol Microbiol 2013;87:656-671.
20. Hong M, Bao L, Kefaloyianni E, Agullo-Pascual E, Chkourko H, Foster M et al. Heterogeneity of ATP-sensitive K+ channels in cardiac myocytes: enrichment at the intercalated disk. J Biol Chem 2012;287:41258-41267.
21. Chkourko HS, Guerrero-Serna G, Lin X, Darwish N, Pohlmann JR, Cook KE et al. Remodeling of mechanical junctions and of microtubule-associated proteins accompany cardiac connexin43 lateralization. Heart Rhythm 2012;9:1133-1140 e1136.
22. Simonson PD, Rothenberg E, Selvin PR. Single-molecule-based super-resolution images in the presence of multiple fluorophores. Nano Lett 2011;11:5090-5096.
23. Dani A, Huang B, Bergan J, Dulac C, Zhuang X. Superresolution imaging of chemical synapses in the brain. Neuron 2010;68:843-856.
24. Palatinus JA, Rhett JM, Gourdie RG. The connexin43 carboxyl terminus and cardiac gap junction organization. Biochim Biophys Acta 2012;1818:1831-1843.
25. van de Linde S, Loschberger A, Klein T, Heidbreder M, Wolter S, Heilemann M et al. Direct stochastic optical reconstruction microscopy with standard fluorescent probes. Nat Protoc 2011;6:991-1009.
26. Kordeli E, Lambert S, Bennett V, Ankyrin G. A new ankyrin gene with neural-specific isoforms localized at the axonal initial segment and node of Ranvier. J Biol Chem 1995;270: 2352-2359.
27. Thaxton C, Pillai AM, Pribisko AL, Dupree JL, Bhat MA. Nodes of Ranvier act as barriers to restrict invasion of flanking paranodal domains in myelinated axons. Neuron 2011;69: 244-257.
28. Jansen JA, Noorman M, Musa H, Stein M, de Jong S, van der Nagel R et al. Reduced heterogeneous expression of Cx43 results in decreased Nav1.5 expression and reduced sodium current that accounts for arrhythmia vulnerability in conditional Cx43 knockout mice. Heart Rhythm 2012;9:600-607.
29. Desplantez T, McCain ML, Beauchamp P, Rigoli G, Rothen-Rutishauser B, Parker KK et al. Connexin43 ablation in foetal atrial myocytes decreases electrical coupling, partner connexins, and sodium current. Cardiovasc Res 2012;94:58-65.
30. Lubkemeier I, Requardt RP, Lin X, Sasse P, Andrie R, Schrickel JW et al. Deletion of the last five C-terminal amino acid residues of connexin43 leads to lethal ventricular arrhythmias in mice without affecting coupling via gap junction channels. Basic Res Cardiol 2013; 108:348.
31. Rhett JM, Ongstad EL, Jourdan J, Gourdie RG. Cx43 associates with Na(v)1.5 in the cardiomyocyte perinexus. J Membr Biol 2012;245:411-422.
32. Delmar M, McKenna WJ. The cardiac desmosome and arrhythmogenic cardiomyopathies: from gene to disease. Circ Res 2010;107:700-714.