Super-resolution imaging of EC coupling protein distribution in the heart

Journal of Molecular and Cellular Cardiology

Volumn 58, Issue 1, 2013, Pages 32-40

  Soeller, Christian ^a   Baddeley, David ^a  

^a UNIVERSITY OF AUCKLAND   (New Zealand)

Author keywords

Calcium; Excitation contraction coupling; Heart; Immuno cytochemistry; Ryanodine receptor; Super resolution microscopy

Indexed keywords

CALCIUM CHANNEL; CALCIUM ION; CAVEOLIN 3; JUNCTOPHILIN 1; JUNCTOPHILIN 2; MEMBRANE PROTEIN; RYANODINE RECEPTOR; RYANODINE RECEPTOR 2; UNCLASSIFIED DRUG;

CALCIUM SIGNALING; CALCIUM TRANSPORT; CARDIAC IMAGING; CELL JUNCTION; CELLULAR DISTRIBUTION; CONFOCAL MICROSCOPY; ELECTRON MICROSCOPY; EXCITATION CONTRACTION COUPLING; HEART CONTRACTION; HEART MUSCLE CELL; HUMAN; MICROSCOPY; MOLECULAR IMAGING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REVIEW; STIMULATED EMISSION DEPLETION MICROSCOPY; STOCHASTIC OPTICAL RECONSTRUCTION MICROSCOPY; STRUCTURE ACTIVITY RELATION; STRUCTURED ILLUMINATION MICROSCOPY; TISSUE DISTRIBUTION;

ANIMALS; CALCIUM CHANNELS, L-TYPE; CALCIUM SIGNALING; EXCITATION CONTRACTION COUPLING; HEART VENTRICLES; HUMANS; MYOCYTES, CARDIAC; RYANODINE RECEPTOR CALCIUM RELEASE CHANNEL; SARCOPLASMIC RETICULUM;

EID: 84876303904     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2012.11.004     Document Type: Review

References (83)

1. Bers D.M. Cardiac excitation-contraction coupling. Nature 2002, 415:198-205.
2. Franzini-Armstrong C., Protasi F. Ryanodine receptors of striated muscles: a complex channel capable of multiple interactions. Physiol Rev 1997, 77:699-729.
3. Cannell M.B., Soeller C. Numerical analysis of ryanodine receptor activation by L-type channel activity in the cardiac muscle diad. Biophys J 1997, 73:112-122.
4. Cannell M.B., Kong C.H.T. Local control in cardiac E-C coupling. J Mol Cell Cardiol May 14 2011, [Published Online First]. 10.1016/j.yjmcc.2011.04.014.
5. Porter K.R., Palade G.E. Studies on the endoplasmic reticulum. III. Its form and distribution in striated muscle cells. J Biophys Biochem Cytol 1957, 3:269-300.
6. Franzini-Armstrong C. Membrane particles and transmission at the triad. Fed Proc 1975, 34:1382-1389.
7. Inui M., Saito A., Fleischer S. Purification of the ryanodine receptor and identity with feet structures of junctional terminal cisternae of sarcoplasmic-reticulum from fast skeletal-muscle. J Biol Chem 1987, 262:1740-1747.
8. 2+-release channel/ryanodine receptor is localized in junctional and corbular sarcoplasmic reticulum in cardiac muscle. J Cell Biol 1993, 120:969-980.
9. Chen-Izu Y., McCulle S.L., Ward C.W., Soeller C., Allen B.M., Rabang C., et al. Three-dimensional distribution of ryanodine receptor clusters in cardiac myocytes. Biophys J 2006, 91:1-13.
10. Scriven D.R.L., Dan P., Moore E.D.W. Distribution of proteins implicated in excitation-contraction coupling in rat ventricular myocytes. Biophys J 2000, 79:2682-2691.
11. Forssmann W.G., Girardier L. A study of the t system in rat heart. J Cell Biol 1970, 44:1-19.
12. Soeller C., Cannell M.B. Examination of the transverse tubular system in living cardiac rat myocytes by 2-photon microscopy and digital image-processing techniques. Circ Res 1999, 84:266-275.
13. Jayasinghe I., Crossman D., Soeller C., Cannell M. Comparison of the organization of t-tubules, sarcoplasmic reticulum and ryanodine receptors in rat and human ventricular myocardium. Clin Exp Pharmacol Physiol 2012, 39:469-476.
14. Wei S., Guo A., Chen B., Kutschke W., Xie Y.-P., Zimmerman K., et al. T-tubule remodeling during transition from hypertrophy to heart failure. Circ Res 2010, 107:520-531.
15. van Oort R.J., Garbino A., Wang W., Dixit S.S., Landstrom A.P., Gaur N., et al. Disrupted junctional membrane complexes and hyperactive ryanodine receptors after acute junctophilin knockdown in mice. Circulation 2011, 123:979-988.
16. 2+ signalling apparatus in failing heart cells. Cardiovasc Res 2012, 95:430-438.
17. Crossman D.J., Ruygrok P.R., Soeller C., Cannell M.B. Changes in the organization of excitation-contraction coupling structures in failing human heart. PLoS One 2011, 6:e17901.
18. Cheng H., Lederer W.J., Cannell M.B. Calcium sparks: elementary events underlying excitation-contraction coupling in heart muscle. Science 1993, 262:740-744.
19. Cheng H., Lederer W.J. Calcium sparks. Physiol Rev 2008, 88:1491-1545.
20. Franzini-Armstrong C., Protasi F., Ramesh V. Shape, size, and distribution of Ca(2+) release units and couplons in skeletal and cardiac muscles. Biophys J 1999, 77:1528-1539.
21. Brette F., Orchard C.H. Resurgence of cardiac t-tubule research. Physiology (Bethesda) 2007, 22:167-173.
22. Langer G.A., Peskoff A. Calcium concentration and movement in the diadic cleft space of the cardiac ventricular cell. Biophys J 1996, 70:1169-1182.
23. Soeller C., Cannell M.B. Numerical simulation of local calcium movements during L-type calcium channel gating in the cardiac diad. Biophys J 1997, 73:97-111.
24. Fabiato A. Calcium-induced release of calcium from the cardiac sarcoplasmic reticulum. Am J Physiol 1983, 245:C1-C14.
25. Stern M.D., Song L.-S., Cheng H., Sham J.S., Yang H.T., Boheler K.R., et al. Local control models of cardiac excitation-contraction coupling. A possible role for allosteric interactions between ryanodine receptors. J Gen Physiol 1999, 113:469-489.
26. DeRemigio H., Smith G.D. The dynamics of stochastic attrition viewed as an absorption time on a terminating Markov chain. Cell Calcium 2005, 38:73-86.
27. Meng X., Xiao B., Cai S., Huang X., Li F., Bolstad J., et al. Three-dimensional localization of serine 2808, a phosphorylation site in cardiac ryanodine receptor. J Biol Chem 2007, 282:25929-25939.
28. Baddeley D., Jayasinghe I.D., Lam L., Rossberger S., Cannell M.B., Soeller C. Optical single-channel resolution imaging of the ryanodine receptor distribution in rat cardiac myocytes. Proc Natl Acad Sci U S A 2009, 106:22275-22280.
29. Soeller C., Crossman D., Gilbert R., Cannell M.B. Analysis of ryanodine receptor clusters in rat and human cardiac myocytes. Proc Natl Acad Sci U S A 2007, 104:14958-14963.
30. Guo T., Cornea R.L., Huke S., Camors E., Yang Y., Picht E., et al. Kinetics of FKBP12.6 binding to ryanodine receptors in permeabilized cardiac myocytes and effects on Ca sparks. Circ Res 2010, 106:1743-1752.
31. Wang R., Chen W., Cai S., Zhang J., Bolstad J., Wagenknecht T., et al. Localization of an NH2-terminal disease-causing mutation hot spot to the 'clamp' region in the three-dimensional structure of the cardiac ryanodine receptor. J Biol Chem 2007, 282:17785-17793.
32. 2+ exchanger and caveolin-3 in developing rabbit cardiomyocytes. Cell Calcium 2009, 45:369-383.
33. Abbe E. Beiträge zur Theorie des Mikroskops und der mikroskopischen Wahrnehmung. Archiv für mikroskopische Antomie 1873, 9:413-420.
34. Webb R.H. Confocal optical microscopy. Rep Prog Phys 1999, 59:427-471.
35. Axelrod D. Total internal reflection fluorescence microscopy in cell biology. Traffic 2001, 2:764-774.
36. Dyba M., Jakobs S., Hell S.W. Immunofluorescence stimulated emission depletion microscopy. Nat Biotechnol 2003, 21:1303-1304.
37. Betzig E., Patterson G.H., Sougrat R., Lindwasser O.W., Olenych S., Bonifacino J.S., et al. Imaging intracellular fluorescent proteins at nanometer resolution. Science 2006, 313:1642-1645.
38. Hess S.T., Girirajan T.P.K., Mason M.D. Ultra-high resolution imaging by fluorescence photoactivation localization microscopy. Biophys J 2006, 91:4258-4272.
39. Rust M.J., Bates M., Zhuang X. Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat Methods 2006, 3:793-795.
40. van de Linde S., Löschberger 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.
41. Gustafsson M.G. Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy. J Microsc 2000, 198:82-87.
42. Heintzmann R., Cremer C.G. Laterally modulated excitation microscopy: improvement of resolution by using a diffraction grating. Proc SPIE 1999, 3568:185-196.
43. Hell S.W. Far-field optical nanoscopy. Science 2007, 316:1153-1158.
44. Huang B., Bates M., Zhuang X. Super-resolution fluorescence microscopy. Annu Rev Biochem 2009, 78:993-1016.
45. Schermelleh L., Heintzmann R., Leonhardt H. A guide to super-resolution fluorescence microscopy. J Cell Biol 2010, 190:165-175.
46. Leung B.O., Chou K.C. Review of super-resolution fluorescence microscopy for Biology. Appl Spectrosc 2011, 65:967-980.
47. Baddeley D., Cannell M.B., Soeller C. Visualization of localization microscopy data. Microsc Microanal 2010, 16:64-72.
48. Shroff H., Galbraith C.G., Galbraith J.A., Betzig E. Live-cell photoactivated localization microscopy of nanoscale adhesion dynamics. Nat Methods 2008, 5:417-423.
49. Lai F.A., Dent M., Wickenden C., Xu L., Kumari G., Misra M., et al. Expression of a cardiac Ca(2+)-release channel isoform in mammalian brain. Biochem J 1992, 288:553.
50. Heilemann M., van de Linde S., Schüttpelz 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.
51. van de Linde S., Wolter S., Heilemann M., Sauer M. The effect of photoswitching kinetics and labeling densities on super-resolution fluorescence imaging. J Biotechnol 2010, 149:260-266.
52. Mitchison T.J. Polewards microtubule flux in the mitotic spindle: evidence from photoactivation of fluorescence. J Cell Biol 1989, 109:637-652.
53. Baddeley D., Jayasinghe I.D., Cremer C., Cannell M.B., Soeller C. Light-induced dark states of organic fluochromes enable 30nm resolution imaging in standard media. Biophys J 2009, 96:L22-L24.
54. Heilemann M., van de Linde S., Mukherjee A., Sauer M. Super-resolution imaging with small organic fluorophores. Angew Chem Int Ed Engl 2009, 48:6903-6908.
55. Dempsey G.T., Vaughan J.C., Chen K.H., Bates M., Zhuang X. Evaluation of fluorophores for optimal performance in localization-based super-resolution imaging. Nat Methods 2011, 8:1027-1036.
56. Huang B., Wang W., Bates M., Zhuang X. Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy. Science 2008, 319:810-813.
57. Baddeley D., Crossman D., Rossberger S., Cheyne J.E., Montgomery J.M., Jayasinghe I.D., et al. 4D super-resolution microscopy with conventional fluorophores and single wavelength excitation in optically thick cells and tissues. PLoS One 2011, 6:e20645.
58. Baddeley D., Cannell M.B., Soeller C. Three-dimensional sub-100 nm super-resolution imaging of biological samples using a phase ramp in the objective pupil. Nano Res 2011, 1-10.
59. Shtengel G., Galbraith J.A., Galbraith C.G., Lippincott-Schwartz J., Gillette J.M., Manley S., et al. Interferometric fluorescent super-resolution microscopy resolves 3D cellular ultrastructure. Proc Natl Acad Sci U S A 2009, 106:3125-3130.
60. Paolini C., Protasi F., Franzini-Armstrong C. The relative position of RyR feet and DHPR tetrads in skeletal muscle. J Mol Biol 2004, 342:145-153.
61. 2+ release channel on lipid membranes. J Struct Biol 2005, 149:219-224.
62. 2+ signaling in the heart. J Cell Sci 2009, 122:1005-1013.
63. Asghari P., Scriven D.R.L., Hoskins J., Fameli N., Breemen C., Moore E.D.W. The structure and functioning of the couplon in the mammalian cardiomyocyte. Protoplasma 2011, 249:31-38.
64. Loschberger A., van de Linde S., Dabauvalle M.C., Rieger B., Heilemann M., Krohne G., et al. Super-resolution imaging visualizes the eightfold symmetry of gp210 proteins around the nuclear pore complex and resolves the central channel with nanometer resolution. J Cell Sci 2012, 125:570-575.
65. Tokunaga M., Imamoto N., Sakata-Sogawa K. Highly inclined thin illumination enables clear single-molecule imaging in cells. Nat Methods 2008, 5:159-161.
66. Huang B., Jones S.A., Brandenburg B., Zhuang X. Whole-cell 3D STORM reveals interactions between cellular structures with nanometer-scale resolution. Nat Methods 2008, 5:1047-1052.
67. Asghari P., Schulson M., Scriven D.R.L., Martens G., Moore E.D.W. Axial tubules of rat ventricular myocytes form multiple junctions with the sarcoplasmic reticulum. Biophys J 2009, 96:4651-4660.
68. Cella Zanacchi F., Lavagnino Z., Perrone Donnorso M., Del Bue A., Furia L., Faretta M., et al. Live-cell 3D super-resolution imaging in thick biological samples. Nat Methods 2011, 8:1047-1049.
69. Györke S., Terentyev D. Modulation of ryanodine receptor by luminal calcium and accessory proteins in health and cardiac disease. Cardiovasc Res 2007, 77:245-255.
70. 2+ sparks and in situ operation of the ryanodine receptor array in cardiac cells. Proc Natl Acad Sci U S A 2004, 101:3979-3984.
71. Bossi M., Fölling J., Belov V., Boyarskiy V., Medda Egner, et al. Multicolor far-field fluorescence nanoscopy through isolated detection of distinct molecular species. Nano Lett July 22 2008, [Published Online First]. 10.1021/nl801471d.
72. Testa I., Wurm C.A., Medda R., Rothermel E., Middendorf von C., Fölling J., et al. Multicolor fluorescence nanoscopy in fixed and living cells by exciting conventional fluorophores with a single wavelength. Biophys J 2010, 99:2686-2694.
73. Razani B., Woodman S.E., Lisanti M.P. Caveolae: from cell biology to animal physiology. Pharmacol Rev 2002, 54:431-467.
74. Takeshima H., Komazaki S., Nishi M., Iino M., Kangawa K. Junctophilins: a novel family of junctional membrane complex proteins. Mol Cell 2000, 6:11-22.
75. Manders E., Verbeek F., Aten J. Measurement of co-localization of objects in dual-colour confocal images. J Microsc 1993, 169:375-382.
76. Jayasinghe I.D., Baddeley D., Kong C.H.T., Wehrens X.H.T., Cannell M.B., Soeller C. Nanoscale organization of junctophilin-2 and ryanodine receptors within peripheral couplings of rat ventricular cardiomyocytes. Biophys J 2012, 102:L19-L21.
77. Maurer C., Qi R., Raghavan V. A linear time algorithm for computing exact Euclidean distance transforms of binary images in arbitrary dimensions. IEEE Trans Pattern Anal Mach Intell 2003, 25:265-270.
78. Watanabe S., Punge A., Hollopeter G., Willig K.I., Hobson R.J., Davis M.W., et al. Protein localization in electron micrographs using fluorescence nanoscopy. Nat Methods 2011, 8:80-84.
79. Wagner E., Lauterbach M.A., Kohl T., Westphal V., Williams G.S.B., Steinbrecher J.H., et al. Stimulated emission depletion live-cell super-resolution imaging shows proliferative remodeling of T-tubule membrane structures after myocardial infarction. Circ Res 2012, 111:402-414.
80. Hake J., Edwards A.G., Yu Z., Kekenes-Huskey P.M., Michailova A.P., McCammon J.A., et al. Modelling cardiac calcium sparks in a three-dimensional reconstruction of a calcium release unit. J Physiol (Lond) 2012, 590:4403-4422.
81. Annibale P., Vanni S., Scarselli M., Rothlisberger U., Radenovic A. Quantitative photo activated localization microscopy: unraveling the effects of photoblinking. PLoS One 2011, 6:e22678.
82. Lando D., Endesfelder U., Berger H., Subramanian L., Dunne P.D., McColl J., et al. Quantitative single-molecule microscopy reveals that CENP-ACnp1 deposition occurs during G2 in fission yeast. Open Biol 2012, 2:120078.
83. Piston D.W. Understand how it works. Nature 2012, 484:440-441.