Functional cardiac imaging by random access microscopy

Frontiers in Physiology

Volumn 5, Issue OCT, 2014, Pages

  Crocini, Claudia ^a   Coppini, Raffaele ^b   Ferrantini, Cecilia ^c   Pavone, Francesco S ^a,b,d   Sacconi, Leonardo ^a,d  

^a UNIVERSITY OF FLORENCE   (Italy)

^b UNIVERSITY OF FLORENCE   (Italy)

^c UNIVERSITY OF FLORENCE   (Italy)

^d ISTITUTO NAZIONALE DI OTTICA   (Italy)

Author keywords

Calcium imaging; Channelrhodopsin; Fluorescence; Microscopy; Optical stimulation; Voltage sensitive dye imaging

Indexed keywords

CALCIUM ION;

ARTICLE; BIOMICROSCOPY; CALCIUM SIGNALING; CALCIUM TRANSPORT; CARDIAC IMAGING; EXCITATION CONTRACTION COUPLING; FLUORESCENCE IMAGING; HEART; HEART MUSCLE CELL; HEART MUSCLE POTENTIAL; HEART RHYTHM; INTERCELLULAR SPACE; MEMBRANE DEPOLARIZATION; NONHUMAN; PHOTOCHEMISTRY; SIGNAL DETECTION; TRANSVERSE TUBULAR SYSTEM; VOLTAGE SENSITIVE DYE IMAGING;

EID: 84908455984     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2014.00403     Document Type: Article

References (40)

1. Andrasfalvy, B. K., Zemelman, B. V., Tang, J., and Vaziri, A. (2010). Two-photon single-cell optogenetic control of neuronal activity by sculpted light. Proc. Natl. Acad. Sci. U.S.A. 107, 11981-11986. doi: 10.1073/pnas.1006620107
2. Arrenberg, A. B., Stainier, D. Y., Baier, H., and Huisken, J. (2010). Optogenetic control of cardiac function. Science 330, 971-974. doi: 10.1126/science.1195929
3. Asghari, P., Schulson, M., Scriven, D. R., Martens, G., and Moore, E. D. (2009). Axial tubules of rat ventricular myocytes form multiple junctions with the sarcoplasmic reticulum. Biophys. J. 96, 4651-4660. doi: 10.1016/j.bpj.2009.02.058
4. Bers, D. M. (2002). Cardiac excitation-contraction coupling. Nature 415, 198-205. doi: 10.1038/415198a
5. Botcherby, E. J., Corbett, A., Burton, R. A., Smith, C. W., Bollensdorff, C., Booth, M. J., et al. (2013). Fast measurement of sarcomere length and cell orientation in Langendorff-perfused hearts using remote focusing microscopy. Circ. Res. 113, 863-870. doi: 10.1161/CIRCRESAHA.113.301704
6. Bruegmann, T., Malan, D., Hesse, M., Beiert, T., Fuegemann, C. J., Fleischmann, B. K., et al. (2010). Optogenetic control of heart muscle in vitro and in vivo. Nat. Methods 7, 897-900. doi: 10.1038/nmeth.1512
7. Bu, G., Adams, H., Berbari, E. J., and Rubart, M. (2009). Uniform action potential repolarization within the sarcolemma of in situ ventricular cardiomyocytes. Biophys. J. 96, 2532-2546. doi: 10.1016/j.bpj.2008.12.3896
8. Crocini, C., Coppini, R., Ferrantini, C., Yan, P., Loew, L. M., Tesi, C., et al. (2014). Defects in T-tubular electrical activity underlie local alterations of calcium release in heart failure. Proc. Natl. Acad. Sci. U.S.A. doi: 10.1073/pnas.1411557111. [Epub ahead of print].
9. (2+) release and the associated diastolic contraction during beta-adrenergic stimulation in rat ventricular cardiomyocytes. Basic Res. Cardiol. 106, 1009-1022. doi: 10.1007/s00395-011-0218-4
10. Ferrantini, C., Coppini, R., Sacconi, L., Tosi, B., Zhang, M. L., Wang, G. L., et al. (2014). Impact of detubulation on force and kinetics of cardiac muscle contraction. J. Gen. Physiol. 143, 783-797. doi: 10.1085/jgp.201311125
11. Gomez, A. M., Valdivia, H. H., Cheng, H., Lederer, M. R., Santana, L. F., Cannell, M. B., et al. (1997). Defective excitation-contraction coupling in experimental cardiac hypertrophy and heart failure. Science 276, 800-806.
12. Gourdie, R. G., Severs, N. J., Green, C. R., Rothery, S., Germroth, P., and Thompson, R. P. (1993). The spatial distribution and relative abundance of gap-junctional connexin40 and connexin43 correlate to functional properties of components of the cardiac atrioventricular conduction system. J. Cell. Sci. 105 (Pt 4), 985-991.
13. 2+ molecules. Nature 341, 65-68. doi: 10.1038/341065a0
14. Hobai, I. A., and O'rourke, B. (2001). Decreased sarcoplasmic reticulum calcium content is responsible for defective excitation-contraction coupling in canine heart failure. Circulation 103, 1577-1584. doi: 10.1161/01.CIR.103.11.1577
15. Howard, S. S., Straub, A., Horton, N., Kobat, D., and Xu, C. (2013). Frequency multiplexed multiphoton phosphorescence lifetime microscopy. Nat. Photonics 7, 33-37. doi: 10.1038/nphoton.2012.307
16. Ibrahim, M., Gorelik, J., Yacoub, M. H., and Terracciano, C. M. (2011). The structure and function of cardiac t-tubules in health and disease. Proc. Biol. Sci. 278, 2714-2723. doi: 10.1098/rspb.2011.0624
17. 2+ release through localized Ca2+ uncaging in smooth muscle. J. Gen. Physiol. 127, 225-235. doi: 10.1085/jgp.200509422
18. 2+ release. Biochem. J. 412, 171-178. doi: 10.1042/BJ20071287
19. Kleber, A. G. (2011). Gap junctions and conduction of cardiac excitation. Heart Rhythm 8, 1981-1984. doi: 10.1016/j.hrthm.2011.08.007
20. Liu, N., Colombi, B., Memmi, M., Zissimopoulos, S., Rizzi, N., Negri, S., et al. (2006). Arrhythmogenesis in catecholaminergic polymorphic ventricular tachycardia: insights from a RyR2 R4496C knock-in mouse model. Circ. Res. 99, 292-298. doi: 10.1161/01.RES.0000235869.50747.e1
21. Marks, A. R. (2013). Calcium cycling proteins and heart failure: mechanisms and therapeutics. J. Clin. Invest. 123, 46-52. doi: 10.1172/JCI62834
22. Matsumoto, N., Okazaki, S., Fukushi, Y., Takamoto, H., Inoue, T., and Terakawa, S. (2014). An adaptive approach for uniform scanning in multifocal multiphoton microscopy with a spatial light modulator. Opt. Express 22, 633-645. doi: 10.1364/OE.22.000633
23. 2+ from the sarcoplasmic reticulum in rat ventricular myocytes. J. Physiol. 559, 121-128. doi: 10.1113/jphysiol.2003.058917
24. Orchard, C. H., Bryant, S. M., and James, A. F. (2013). Do t-tubules play a role in arrhythmogenesis in cardiac ventricular myocytes? J. Physiol. 591, 4141-4147. doi: 10.1113/jphysiol.2013.254540
25. Oron, D., Papagiakoumou, E., Anselmi, F., and Emiliani, V. (2012). Two-photon optogenetics. Prog. Brain Res. 196, 119-143. doi: 10.1016/B978-0-444-59426-6.00007-0
26. Papagiakoumou, E., Anselmi, F., Begue, A., De Sars, V., Gluckstad, J., Isacoff, E. Y., et al. (2010). Scanless two-photon excitation of channelrhodopsin-2. Nat. Methods 7, 848-854. doi: 10.1038/nmeth.1505
27. Pogwizd, S. M., Schlotthauer, K., Li, L., Yuan, W., and Bers, D. M. (2001). Arrhythmogenesis and contractile dysfunction in heart failure: roles of sodium-calcium exchange, inward rectifier potassium current, and residual beta-adrenergic responsiveness. Circ. Res. 88, 1159-1167. doi: 10.1161/hh1101.091193
28. Revel, J. P., and Karnovsky, M. J. (1967). Hexagonal array of subunits in intercellular junctions of the mouse heart and liver. J. Cell Biol. 33, C7-C12.
29. Rickgauer, J. P., and Tank, D. W. (2009). Two-photon excitation of channelrhodopsin-2 at saturation. Proc. Natl. Acad. Sci. U.S.A. 106, 15025-15030. doi: 10.1073/pnas.0907084106
30. Rubart, M. (2004). Two-photon microscopy of cells and tissue. Circ. Res. 95, 1154-1166. doi: 10.1161/01.RES.0000150593.30324.42
31. Sacconi, L., Ferrantini, C., Lotti, J., Coppini, R., Yan, P., Loew, L. M., et al. (2012). Action potential propagation in transverse-axial tubular system is impaired in heart failure. Proc. Natl. Acad. Sci. U.S.A. 109, 5815-5819. doi: 10.1073/pnas.1120188109
32. Severs, N. J. (1994). Pathophysiology of gap junctions in heart disease. J. Cardiovasc. Electrophysiol. 5, 462-475.
33. Soeller, C., and Cannell, M. B. (1999). Examination of the transverse tubular system in living cardiac rat myocytes by 2-photon microscopy and digital image-processing techniques. Circ. Res. 84, 266-275.
34. 2+ waves at the border zone of the cryo-injured rat heart revealed by real-time confocal microscopy. J. Mol. Cell. Cardiol. 34, 1501-1512. doi: 10.1006/jmcc.2002.2096
35. Ter Keurs, H. E., and Boyden, P. A. (2007). Calcium and arrhythmogenesis. Physiol. Rev. 87, 457-506. doi: 10.1152/physrev.00011.2006
36. Tsujii, E., Tanaka, H., Oyamada, M., Fujita, K., Hamamoto, T., and Takamatsu, T. (2003). In situ visualization of the intracellular Ca2+ dynamics at the border of the acute myocardial infarct. Mol. Cell. Biochem. 248, 135-139. doi: 10.1023/A:1024188302849
37. Venetucci, L. A., Trafford, A. W., and Eisner, D. A. (2007a). Increasing ryanodine receptor open probability alone does not produce arrhythmogenic calcium waves: threshold sarcoplasmic reticulum calcium content is required. Circ. Res. 100, 105-111. doi: 10.1161/01.RES.0000252828.17939.00
38. Venetucci, L. A., Trafford, A. W., O'neill, S. C., and Eisner, D. A. (2007b). Na/Ca exchange: regulator of intracellular calcium and source of arrhythmias in the heart. Ann. N. Y. Acad. Sci. 1099, 315-325. doi: 10.1196/annals.1387.033
39. Yan, P., Acker, C. D., Zhou, W. L., Lee, P., Bollensdorff, C., Negrean, A., et al. (2012). Palette of fluorinated voltage-sensitive hemicyanine dyes. Proc. Natl. Acad. Sci. U.S.A. 109, 20443-20448. doi: 10.1073/pnas.1214850109
40. York, A. G., Parekh, S. H., Dalle Nogare, D., Fischer, R. S., Temprine, K., Mione, M., et al. (2012). Resolution doubling in live, multicellular organisms via multifocal structured illumination microscopy. Nat. Methods 9, 749-754. doi: 10.1038/nmeth.2025