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Applications of phototransformable fluorescent proteins for tracking the dynamics of cellular components

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Abstract

In the past few decades, fluorescent proteins have revolutionized the field of cell biology. Phototransformable fluorescent proteins are capable of changing their excitation and emission spectra after being exposed to specific wavelength(s) of light. The majority of phototransformable fluorescent proteins have originated from marine organisms. Genetic engineering of these proteins has made available many choices for different colors, modes of conversion, and other biophysical properties. Their phototransformative property has allowed the highlighting and tracking of subpopulations of cells, organelles, and proteins in living systems. Furthermore, phototransformable fluorescent proteins have offered new methods for superresolution fluorescence microscopy and optogenetics manipulation of proteins. One of the major advantages of phototransformable fluorescent proteins is their applicability for visualizing newly synthesized proteins that are en route to their final destinations. In this paper, we will discuss the biological applications of phototransformable fluorescent proteins with special emphasis on the application of tracking membrane proteins in vertebrate photoreceptor cells.

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References

  1. R. Ando, H. Hama, M. Yamamoto-Hino, H. Mizuno and A. Miyawaki, An optical marker based on the UV-induced green-to-red photoconversion of a fluorescent protein, Proc. Natl. Acad. Sci. U. S. A., 2002, 99, 12651–12656.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. G. H. Patterson and J. Lippincott-Schwartz, A photoactivatable GFP for selective photolabeling of proteins and cells, Science, 2002, 297, 1873–1877.

    Article  CAS  PubMed  Google Scholar 

  3. K. Nienhaus, G. U. Nienhaus, J. Wiedenmann and H. Nar, Structural basis for photo-induced protein cleavage and green-to-red conversion of fluorescent protein EosFP, Proc. Natl. Acad. Sci. U. S. A., 2005, 102, 9156–9159.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. V. Adam, K. Nienhaus, D. Bourgeois and G. U. Nienhaus, Structural basis of enhanced photoconversion yield in green fluorescent protein-like protein Dendra2, Biochemistry, 2009, 48, 4905–4915.

    Article  CAS  PubMed  Google Scholar 

  5. O. M. Subach, G. H. Patterson, L. M. Ting, Y. Wang, J. S. Condeelis and V. V. Verkhusha, A photoswitchable orange-to-far-red fluorescent protein, PSmOrange, Nat. Methods, 2011, 8, 771–777.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. F. V. Subach, V. N. Malashkevich, W. D. Zencheck, H. Xiao, G. S. Filonov, S. C. Almo and V. V. Verkhusha, Photoactivation mechanism of PAmCherry based on crystal structures of the protein in the dark and fluorescent states, Proc. Natl. Acad. Sci. U. S. A., 2009, 106, 21097–21102.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. J. J. van Thor, T. Gensch, K. J. Hellingwerf and L. N. Johnson, Phototransformation of green fluorescent protein with UV and visible light leads to decarboxylation of glutamate 222, Nat. Struct. Biol., 2002, 9, 37–41.

    Article  PubMed  CAS  Google Scholar 

  8. R. Ando, H. Mizuno and A. Miyawaki, Regulated fast nucleocytoplasmic shuttling observed by reversible protein highlighting, Science, 2004, 306, 1370–1373.

    Article  CAS  PubMed  Google Scholar 

  9. M. Andresen, A. C. Stiel, S. Trowitzsch, G. Weber, C. Eggeling, M. C. Wahl, S. W. Hell and S. Jakobs, Structural basis for reversible photoswitching in Dronpa, Proc. Natl. Acad. Sci. U. S. A., 2007, 104, 13005–13009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. V. Adam, B. Moeyaert, C. C. David, H. Mizuno, M. Lelimousin, P. Dedecker, R. Ando, A. Miyawaki, J. Michiels, Y. Engelborghs and J. Hofkens, Rational design of photoconvertible and biphotochromic fluorescent proteins for advanced microscopy applications, Chem. Biol., 2011, 18, 1241–1251.

    Article  CAS  PubMed  Google Scholar 

  11. J. Fuchs, S. Bohme, F. Oswald, P. N. Hedde, M. Krause, J. Wiedenmann and G. U. Nienhaus, A photoactivatable marker protein for pulse-chase imaging with superresolution, Nat. Methods, 2010, 7, 627–630.

    Article  CAS  PubMed  Google Scholar 

  12. V. Adam, Phototransformable fluorescent proteins: which one for which application?, Histochem. Cell Biol., 2014, 142, 19–41.

    Article  CAS  PubMed  Google Scholar 

  13. V. Adam, R. Berardozzi, M. Byrdin and D. Bourgeois, Phototransformable fluorescent proteins: Future challenges, Curr. Opin. Chem. Biol., 2014, 20, 92–102.

    Article  CAS  PubMed  Google Scholar 

  14. C. Duan, V. Adam, M. Byrdin and D. Bourgeois, Structural basis of photoswitching in fluorescent proteins, Methods Mol. Biol., 2014, 1148, 177–202.

    Article  CAS  PubMed  Google Scholar 

  15. R. W. Young, The renewal of photoreceptor cell outer segments, J. Cell Biol., 1967, 33, 61–72.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. D. S. Williams, Photoreceptor cell biology and inherited retinal degenerations, World Scientific, 2004.

    Book  Google Scholar 

  17. K. Hatta, H. Tsujii and T. Omura, Cell tracking using a photoconvertible fluorescent protein, Nat. Protoc., 2006, 1, 960–967.

    Article  CAS  PubMed  Google Scholar 

  18. T. Sato, M. Takahoko and H. Okamoto, HuC:Kaede, a useful tool to label neural morphologies in networks in vivo, Genesis, 2006, 44, 136–142.

    Article  CAS  PubMed  Google Scholar 

  19. T. Mutoh, T. Miyata, S. Kashiwagi, A. Miyawaki and M. Ogawa, Dynamic behavior of individual cells in developing organotypic brain slices revealed by the photoconvertable protein Kaede, Exp. Neurol., 2006, 200, 430–437.

    Article  CAS  PubMed  Google Scholar 

  20. P. M. Kulesa, J. M. Teddy, D. A. Stark, S. E. Smith and R. McLennan, Neural crest invasion is a spatially-ordered progression into the head with higher cell proliferation at the migratory front as revealed by the photoactivatable protein, KikGR, Dev. Biol., 2008, 316, 275–287.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. D. A. Stark and P. M. Kulesa, An in vivo comparison of photoactivatable fluorescent proteins in an avian embryo model, Dev. Dyn., 2007, 236, 1583–1594.

    Article  CAS  PubMed  Google Scholar 

  22. S. Nowotschin and A. K. Hadjantonakis, Use of KikGR a photoconvertible green-to-red fluorescent protein for cell labeling and lineage analysis in ES cells and mouse embryos, BMC Dev. Biol., 2009, 9, 49.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  23. S. A. Wacker, F. Oswald, J. Wiedenmann and W. Knochel, A green to red photoconvertible protein as an analyzing tool for early vertebrate development, Dev. Dyn., 2007, 236, 473–480.

    Article  CAS  PubMed  Google Scholar 

  24. K. Geurtzen, F. Knopf, D. Wehner, L. F. Huitema, S. Schulte-Merker and G. Weidinger, Mature osteoblasts dedifferentiate in response to traumatic bone injury in the zebrafish fin and skull, Development, 2014, 141, 2225–2234.

    Article  CAS  PubMed  Google Scholar 

  25. W. P. Dempsey, S. E. Fraser and P. Pantazis, PhOTO zebrafish: a transgenic resource for in vivo lineage tracing during development and regeneration, PLoS One, 2012, 7, e32888.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. K. Kishi, T. A. Onuma and H. Nishida, Long-distance cell migration during larval development in the appendicularian, Oikopleura dioica, Dev. Biol., 2014, 395, 299–306.

    Article  CAS  PubMed  Google Scholar 

  27. M. J. Murray and R. Saint, Photoactivatable GFP resolves Drosophila mesoderm migration behaviour, Development, 2007, 134, 3975–3983.

    Article  CAS  PubMed  Google Scholar 

  28. S. J. Caron, D. Prober, M. Choy and A. F. Schier, In vivo birthdating by BAPTISM reveals that trigeminal sensory neuron diversity depends on early neurogenesis, Development, 2008, 135, 3259–3269.

    Article  CAS  PubMed  Google Scholar 

  29. M. Tomura, N. Yoshida, J. Tanaka, S. Karasawa, Y. Miwa, A. Miyawaki and O. Kanagawa, Monitoring cellular movement in vivo with photoconvertible fluorescence protein “Kaede” transgenic mice, Proc. Natl. Acad. Sci. U. S. A., 2008, 105, 10871–10876.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. M. Tomura, T. Honda, H. Tanizaki, A. Otsuka, G. Egawa, Y. Tokura, H. Waldmann, S. Hori, J. G. Cyster, T. Watanabe, Y. Miyachi, O. Kanagawa and K. Kabashima, Activated regulatory T cells are the major T cell type emigrating from the skin during a cutaneous immune response in mice, J. Clin. Invest., 2010, 120, 883–893.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Y. Imanishi, K. H. Lodowski and Y. Koutalos, Two-photon microscopy: shedding light on the chemistry of vision, Biochemistry, 2007, 46, 9674–9684.

    Article  CAS  PubMed  Google Scholar 

  32. T. Chtanova, H. R. Hampton, L. A. Waterhouse, K. Wood, M. Tomura, Y. Miwa, C. R. Mackay, R. Brink and T. G. Phan, Real-time interactive two-photon photoconversion of recirculating lymphocytes for discontinuous cell tracking in live adult mice, J. Biophotonics, 2014, 7, 425–433.

    Article  CAS  PubMed  Google Scholar 

  33. A. J. Muller, S. Aeschlimann, R. Olekhnovitch, M. Dacher, G. F. Spath and P. Bousso, Photoconvertible pathogen labeling reveals nitric oxide control of Leishmania major infection in vivo via dampening of parasite metabolism, Cell Host Microbe, 2013, 14, 460–467.

    Article  CAS  PubMed  Google Scholar 

  34. A. Lovy, A. J. Molina, F. M. Cerqueira, K. Trudeau and O. S. Shirihai, A faster, high resolution, mtPA-GFP-based mitochondrial fusion assay acquiring kinetic data of multiple cells in parallel using confocal microscopy, Journal of Visualized Exp., 2012, e3991.

    Google Scholar 

  35. M. Karbowski, D. Arnoult, H. Chen, D. C. Chan, C. L. Smith and R. J. Youle, Quantitation of mitochondrial dynamics by photolabeling of individual organelles shows that mitochondrial fusion is blocked during the Bax activation phase of apoptosis, J. Cell Biol., 2004, 164, 493–499.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. M. Karbowski, M. M. Cleland and B. A. Roelofs, Photoactivatable green fluorescent protein-based visualization and quantification of mitochondrial fusion and mitochondrial network complexity in living cells, Methods Enzymol., 2014, 547, 57–73.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. S. B. Berman, Y. B. Chen, B. Qi, J. M. McCaffery, E. B. Rucker 3rd, S. Goebbels, K. A. Nave, B. A. Arnold, E. A. Jonas, F. J. Pineda and J. M. Hardwick, Bcl-x L increases mitochondrial fission, fusion, and biomass in neurons, J. Cell Biol., 2009, 184, 707–719.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. R. Anand, T. Wai, M. J. Baker, N. Kladt, A. C. Schauss, E. Rugarli and T. Langer, The i-AAA protease YME1L and OMA1 cleave OPA1 to balance mitochondrial fusion and fission, J. Cell Biol., 2014, 204, 919–929.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Y. J. Lee, S. Y. Jeong, M. Karbowski, C. L. Smith and R. J. Youle, Roles of the mammalian mitochondrial fission and fusion mediators Fis1, Drp1, and Opa1 in apoptosis, Mol. Biol. Cell, 2004, 15, 5001–5011.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. X. Huang, L. Sun, S. Ji, T. Zhao, W. Zhang, J. Xu, J. Zhang, Y. Wang, X. Wang, C. Franzini-Armstrong, M. Zheng and H. Cheng, Kissing and nanotunneling mediate intermitochondrial communication in the heart, Proc. Natl. Acad. Sci. U. S. A., 2013, 110, 2846–2851.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. F. Legros, A. Lombes, P. Frachon and M. Rojo, Mitochondrial fusion in human cells is efficient, requires the inner membrane potential, and is mediated by mitofusins, Mol. Biol. Cell, 2002, 13, 4343–4354.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. N. Ishihara, A. Jofuku, Y. Eura and K. Mihara, Regulation of mitochondrial morphology by membrane potential, and DRP1-dependent division and FZO1-dependent fusion reaction in mammalian cells, Biochem. Biophys. Res. Commun., 2003, 301, 891–898.

    Article  CAS  PubMed  Google Scholar 

  43. H. Chen, S. A. Detmer, A. J. Ewald, E. E. Griffin, S. E. Fraser and D. C. Chan, Mitofusins Mfn1 and Mfn2 coordinately regulate mitochondrial fusion and are essential for embryonic development, J. Cell Biol., 2003, 160, 189–200.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Y. Mattenberger, D. I. James and J. C. Martinou, Fusion of mitochondria in mammalian cells is dependent on the mitochondrial inner membrane potential and independent of microtubules or actin, FEBS Lett., 2003, 538, 53–59.

    Article  CAS  PubMed  Google Scholar 

  45. A. H. Pham, J. M. McCaffery and D. C. Chan, Mouse lines with photo-activatable mitochondria to study mitochondrial dynamics, Genesis, 2012, 50, 833–843.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. S. A. McKinney, C. S. Murphy, K. L. Hazelwood, M. W. Davidson and L. L. Looger, A bright and photostable photoconvertible fluorescent protein, Nat. Methods, 2009, 6, 131–133.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. S. Richert, S. Kleinecke, J. Gunther, F. Schaumburg, J. Edgar, G. U. Nienhaus, K. A. Nave and C. M. Kassmann, In vivo labeling of peroxisomes by photoconvertible mEos2 in myelinating glia of mice, Biochimie, 2014, 98, 127–134.

    Article  CAS  PubMed  Google Scholar 

  48. R. H. Kohler, J. Cao, W. R. Zipfel, W. W. Webb and M. R. Hanson, Exchange of protein molecules through connections between higher plant plastids, Science, 1997, 276, 2039–2042.

    Article  CAS  PubMed  Google Scholar 

  49. E. Y. Kwok and M. R. Hanson, GFP-labelled Rubisco and aspartate aminotransferase are present in plastid stromules and traffic between plastids, J. Exp. Bot., 2004, 55, 595–604.

    Article  CAS  PubMed  Google Scholar 

  50. M. H. Schattat, S. Griffiths, N. Mathur, K. Barton, M. R. Wozny, N. Dunn, J. S. Greenwood and J. Mathur, Differential coloring reveals that plastids do not form networks for exchanging macromolecules, Plant Cell, 2012, 24, 1465–1477.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. M. H. Schattat, K. A. Barton and J. Mathur, The myth of interconnected plastids and related phenomena, Protoplasma, 2015, 252, 359–371.

    Article  CAS  PubMed  Google Scholar 

  52. J. H. Tam, C. Seah and S. H. Pasternak, The Amyloid Precursor Protein is rapidly transported from the Golgi apparatus to the lysosome and where it is processed into beta-amyloid, Mol. Brain, 2014, 7, 54.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  53. S. C. Brown, S. Bolte, M. Gaudin, C. Pereira, J. Marion, M. N. Soler and B. Satiat-Jeunemaitre, Exploring plant endomembrane dynamics using the photoconvertible protein Kaede, Plant J., 2010, 63, 696–711.

    Article  CAS  PubMed  Google Scholar 

  54. M. Bourge, C. Fort, M. N. Soler, B. Satiat-Jeunemaitre and S. C. Brown, A pulse-chase strategy combining click-EdU and photoconvertible fluorescent reporter: tracking Golgi protein dynamics during the cell cycle, New Phytol., 2015, 205, 938–950.

    Article  CAS  PubMed  Google Scholar 

  55. J. Januschke, S. Llamazares, J. Reina and C. Gonzalez, Drosophila neuroblasts retain the daughter centrosome, Nat. Commun., 2011, 2, 243.

    Article  PubMed  CAS  Google Scholar 

  56. J. H. Imai, X. Wang and S. H. Shi, Kaede-centrin1 labeling of mother and daughter centrosomes in mammalian neocortical neural progenitors, in Curr. Protoc. Stem. Cell Biol, 2010, ch. 5, Unit 5A 5.

  57. X. Wang, J. W. Tsai, J. H. Imai, W. N. Lian, R. B. Vallee and S. H. Shi, Asymmetric centrosome inheritance maintains neural progenitors in the neocortex, Nature, 2009, 461, 947–955.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. S. Mukhopadhyay, R. Rohatgi, G-protein-coupled receptors, Hedgehog signaling and primary cilia, Semin. Cell Dev. Biol., 2014, 33, 63–72.

    Article  CAS  PubMed  Google Scholar 

  59. J. Kim, E. Y. Hsia, J. Kim, N. Sever, P. A. Beachy and X. Zheng, Simultaneous measurement of smoothened entry into and exit from the primary cilium, PLoS One, 2014, 9, e104070.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  60. R. M. Wachter, J. L. Watkins and H. Kim, Mechanistic diversity of red fluorescence acquisition by GFP-like proteins, Biochemistry, 2010, 49, 7417–7427.

    Article  CAS  PubMed  Google Scholar 

  61. J. Wiedenmann, S. Ivanchenko, F. Oswald, F. Schmitt, C. Rocker, A. Salih, K. D. Spindler and G. U. Nienhaus, EosFP, a fluorescent marker protein with UV-inducible green-to-red fluorescence conversion, Proc. Natl. Acad. Sci. U. S. A., 2004, 101, 15905–15910.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. J. Mathur, R. Radhamony, A. M. Sinclair, A. Donoso, N. Dunn, E. Roach, D. Radford, P. S. Mohaghegh, D. C. Logan, K. Kokolic and N. Mathur, mEosFP-based green-to-red photoconvertible subcellular probes for plants, Plant Physiol., 2010, 154, 1573–1587.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. N. G. Gurskaya, V. V. Verkhusha, A. S. Shcheglov, D. B. Staroverov, T. V. Chepurnykh, A. F. Fradkov, S. Lukyanov and K. A. Lukyanov, Engineering of a monomeric green-to-red photoactivatable fluorescent protein induced by blue light, Nat. Biotechnol., 2006, 24, 461–465.

    Article  CAS  PubMed  Google Scholar 

  64. S. Habuchi, H. Tsutsui, A. B. Kochaniak, A. Miyawaki and A. M. van Oijen, mKikGR, a monomeric photoswitchable fluorescent protein, PLoS One, 2008, 3, e3944.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  65. H. Tsutsui, S. Karasawa, H. Shimizu, N. Nukina and A. Miyawaki, Semi-rational engineering of a coral fluorescent protein into an efficient highlighter, EMBO Rep., 2005, 6, 233–238.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. D. A. Zacharias, J. D. Violin, A. C. Newton and R. Y. Tsien, Partitioning of lipid-modified monomeric GFPs into membrane microdomains of live cells, Science, 2002, 296, 913–916.

    Article  CAS  PubMed  Google Scholar 

  67. M. Zhang, H. Chang, Y. Zhang, J. Yu, L. Wu, W. Ji, J. Chen, B. Liu, J. Lu, Y. Liu, J. Zhang, P. Xu and T. Xu, Rational design of true monomeric and bright photoactivatable fluorescent proteins, Nat. Methods, 2012, 9, 727–729.

    Article  CAS  PubMed  Google Scholar 

  68. H. Hoi, N. C. Shaner, M. W. Davidson, C. W. Cairo, J. Wang and R. E. Campbell, A monomeric photoconvertible fluorescent protein for imaging of dynamic protein localization, J. Mol. Biol., 2010, 401, 776–791.

    Article  CAS  PubMed  Google Scholar 

  69. D. M. Chudakov, S. Lukyanov and K. A. Lukyanov, Using photoactivatable fluorescent protein Dendra2 to track protein movement, BioTechniques, 2007, 42, 553, 555, 557 passim.

    Article  CAS  PubMed  Google Scholar 

  70. D. M. Chudakov, S. Lukyanov and K. A. Lukyanov, Tracking intracellular protein movements using photoswitchable fluorescent proteins PS-CFP2 and Dendra2, Nat. Protoc., 2007, 2, 2024–2032.

    Article  CAS  PubMed  Google Scholar 

  71. K. Nienhaus, G. U. Nienhaus, Fluorescent proteins for live-cell imaging with super-resolution, Chem. Soc. Rev., 2014, 43, 1088–1106.

    Article  CAS  PubMed  Google Scholar 

  72. N. C. Shaner, M. Z. Lin, M. R. McKeown, P. A. Steinbach, K. L. Hazelwood, M. W. Davidson and R. Y. Tsien, Improving the photostability of bright monomeric orange and red fluorescent proteins, Nat. Methods, 2008, 5, 545–551.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. S. Kuruppu, N. Tochon-Danguy and A. I. Smith, Applicability of green fluorescence protein in the study of endothelin converting enzyme-1c trafficking, Protein Sci., 2013, 22, 306–313.

    Article  CAS  PubMed  Google Scholar 

  74. I. I. Shemiakina, G. V. Ermakova, P. J. Cranfill, M. A. Baird, R. A. Evans, E. A. Souslova, D. B. Staroverov, A. Y. Gorokhovatsky, E. V. Putintseva, T. V. Gorodnicheva, T. V. Chepurnykh, L. Strukova, S. Lukyanov, A. G. Zaraisky, M. W. Davidson, D. M. Chudakov and D. Shcherbo, A monomeric red fluorescent protein with low cytotoxicity, Nat. Commun., 2012, 3, 1204.

    Article  CAS  PubMed  Google Scholar 

  75. V. Magidson and A. Khodjakov, Circumventing photodamage in live-cell microscopy, Methods Cell Biol., 2013, 114, 545–560.

    Article  PubMed  Google Scholar 

  76. N. C. Shaner, P. A. Steinbach and R. Y. Tsien, A guide to choosing fluorescent proteins, Nat. Methods, 2005, 2, 905–909.

    Article  CAS  PubMed  Google Scholar 

  77. S. Brogi, A. Tafi, L. Desaubry, C. G. Nebigil, Discovery of GPCR ligands for probing signal transduction pathways, Front. Pharmacol., 2014, 5, 255.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  78. A. Schmidt, B. Wiesner, K. Weisshart, K. Schulz, J. Furkert, B. Lamprecht, W. Rosenthal and R. Schulein, Use of Kaede fusions to visualize recycling of G protein-coupled receptors, Traffic, 2009, 10, 2–15.

    Article  CAS  PubMed  Google Scholar 

  79. A. Varadi, E. K. Ainscow, V. J. Allan and G. A. Rutter, Involvement of conventional kinesin in glucose-stimulated secretory granule movements and exocytosis in clonal pancreatic beta-cells, J. Cell Sci., 2002, 115, 4177–4189.

    Article  CAS  PubMed  Google Scholar 

  80. M. Ohara-Imaizumi, Y. Nakamichi, T. Tanaka, H. Ishida and S. Nagamatsu, Imaging exocytosis of single insulin secretory granules with evanescent wave microscopy: distinct behavior of granule motion in biphasic insulin release, J. Biol. Chem., 2002, 277, 3805–3808.

    Article  CAS  PubMed  Google Scholar 

  81. M. Hao, X. Li, M. A. Rizzo, J. V. Rocheleau, B. M. Dawant and D. W. Piston, Regulation of two insulin granule populations within the reserve pool by distinct calcium sources, J. Cell Sci., 2005, 118, 5873–5884.

    Article  CAS  PubMed  Google Scholar 

  82. S. Baltrusch and S. Lenzen, Monitoring of glucose-regulated single insulin secretory granule movement by selective photoactivation, Diabetologia, 2008, 51, 989–996.

    Article  CAS  PubMed  Google Scholar 

  83. A. Miyawaki, Proteins on the move: insights gained from fluorescent protein technologies, Nat. Rev. Mol. Cell Biol., 2011, 12, 656–668.

    Article  CAS  PubMed  Google Scholar 

  84. G. Kaur, M. W. Costa, C. M. Nefzger, J. Silva, J. C. Fierro-Gonzalez, J. M. Polo, T. D. Bell and N. Plachta, Probing transcription factor diffusion dynamics in the living mammalian embryo with photoactivatable fluorescence correlation spectroscopy, Nat. Commun., 2013, 4, 1637.

    Article  PubMed  CAS  Google Scholar 

  85. N. Plachta, T. Bollenbach, S. Pease, S. E. Fraser and P. Pantazis, Oct4 kinetics predict cell lineage patterning in the early mammalian embryo, Nat. Cell Biol., 2011, 13, 117–123.

    Article  CAS  PubMed  Google Scholar 

  86. N. Honkura, M. Matsuzaki, J. Noguchi, G. C. Ellis-Davies and H. Kasai, The subspine organization of actin fibers regulates the structure and plasticity of dendritic spines, Neuron, 2008, 57, 719–729.

    Article  CAS  PubMed  Google Scholar 

  87. P. D. Calvert, W. E. Schiesser and E. N. Pugh Jr., Diffusion of a soluble protein, photoactivatable GFP, through a sensory cilium, J. Gen. Physiol., 2010, 135, 173–196.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. M. Najafi, N. A. Maza and P. D. Calvert, Steric volume exclusion sets soluble protein concentrations in photoreceptor sensory cilia, Proc. Natl. Acad. Sci. U. S. A., 2012, 109, 203–208.

    Article  CAS  PubMed  Google Scholar 

  89. Y. T. Kao, X. Zhu and W. Min, Protein-flexibility mediated coupling between photoswitching kinetics and surrounding viscosity of a photochromic fluorescent protein, Proc. Natl. Acad. Sci. U. S. A., 2012, 109, 3220–3225.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. M. Najafi, M. Haeri, B. E. Knox, W. E. Schiesser and P. D. Calvert, Impact of signaling microcompartment geometry on GPCR dynamics in live retinal photoreceptors, J. Gen. Physiol., 2012, 140, 249–266.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. A. Yildiz, J. N. Forkey, S. A. McKinney, T. Ha, Y. E. Goldman and P. R. Selvin, Myosin V walks hand-over-hand: single fluorophore imaging with 1.5-nm localization, Science, 2003, 300, 2061–2065.

    Article  CAS  Google Scholar 

  92. A. D. Douglass and R. D. Vale, Single-molecule microscopy reveals plasma membrane microdomains created by protein-protein networks that exclude or trap signaling molecules in T cells, Cell, 2005, 121, 937–950.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Y. Teramura, J. Ichinose, H. Takagi, K. Nishida, T. Yanagida and Y. Sako, Single-molecule analysis of epidermal growth factor binding on the surface of living cells, EMBO J., 2006, 25, 4215–4222.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  94. A. Kusumi, Y. Sako and M. Yamamoto, Confined lateral diffusion of membrane receptors as studied by single particle tracking (nanovid microscopy). Effects of calcium-induced differentiation in cultured epithelial cells, Biophys. J., 1993, 65, 2021–2040.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. S. Manley, J. M. Gillette, G. H. Patterson, H. Shroff, H. F. Hess, E. Betzig and J. Lippincott-Schwartz, High-density mapping of single-molecule trajectories with photoactivated localization microscopy, Nat. Methods, 2008, 5, 155–157.

    Article  CAS  PubMed  Google Scholar 

  96. F. V. Subach, G. H. Patterson, M. Renz, J. Lippincott-Schwartz and V. V. Verkhusha, Bright monomeric photoactivatable red fluorescent protein for two-color super-resolution sptPALM of live cells, J. Am. Chem. Soc., 2010, 132, 6481–6491.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. R. M. Clegg, Fluorescence resonance energy transfer, Curr. Opin. Biotechnol., 1995, 6, 103–110.

    Article  CAS  Google Scholar 

  98. H. Wolf, B. G. Barisas, K. J. Dietz and T. Seidel, Kaede for detection of protein oligomerization, Mol. Plant, 2013, 6, 1453–1462.

    Article  CAS  PubMed  Google Scholar 

  99. O. M. Subach, D. Entenberg, J. S. Condeelis and V. V. Verkhusha, A FRET-facilitated photoswitching using an orange fluorescent protein with the fast photoconversion kinetics, J. Am. Chem. Soc., 2012, 134, 14789–14799.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  100. X. X. Zhou, H. K. Chung, A. J. Lam and M. Z. Lin, Optical control of protein activity by fluorescent protein domains, Science, 2012, 338, 810–814.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. A. B. Arrenberg, F. Del Bene and H. Baier, Optical control of zebrafish behavior with halorhodopsin, Proc. Natl. Acad. Sci. U. S. A., 2009, 106, 17968–17973.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. G. S. Baird, D. A. Zacharias and R. Y. Tsien, Circular permutation and receptor insertion within green fluorescent proteins, Proc. Natl. Acad. Sci. U. S. A., 1999, 96, 11241–11246.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. J. Nakai, M. Ohkura and K. Imoto, A high signal-to-noise Ca(2+) probe composed of a single green fluorescent protein, Nat. Biotechnol., 2001, 19, 137–141.

    Article  CAS  PubMed  Google Scholar 

  104. H. Hoi, T. Matsuda, T. Nagai and R. E. Campbell, Highlightable Ca2+ indicators for live cell imaging, J. Am. Chem. Soc., 2013, 135, 46–49.

    Article  CAS  PubMed  Google Scholar 

  105. B. F. Fosque, Y. Sun, H. Dana, C. T. Yang, T. Ohyama, M. R. Tadross, R. Patel, M. Zlatic, D. S. Kim, M. B. Ahrens, V. Jayaraman, L. L. Looger and E. R. Schreiter, Neural circuits. Labeling of active neural circuits in vivo with designed calcium integrators, Science, 2015, 347, 755–760.

    Article  CAS  PubMed  Google Scholar 

  106. A. T. Vessoni, A. R. Muotri and O. K. Okamoto, Autophagy in stem cell maintenance and differentiation, Stem Cells Dev., 2012, 21, 513–520.

    Article  CAS  PubMed  Google Scholar 

  107. K. Jing and K. Lim, Why is autophagy important in human diseases?, Exp. Mol. Med., 2012, 44, 69–72.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. D. W. Hailey and J. Lippincott-Schwartz, Using photoactivatable proteins to monitor autophagosome lifetime, Methods Enzymol., 2009, 452, 25–45.

    Article  CAS  PubMed  Google Scholar 

  109. L. Esteban-Martinez and P. Boya, Autophagic flux determination in vivo and ex vivo, Methods, 2015, 75C, 79–86.

    Article  CAS  Google Scholar 

  110. D. W. Hailey, A. S. Rambold, P. Satpute-Krishnan, K. Mitra, R. Sougrat, P. K. Kim and J. Lippincott-Schwartz, Mitochondria supply membranes for autophagosome biogenesis during starvation, Cell, 2010, 141, 656–667.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. M. Tasaki, S. Asatsuma and K. Matsuoka, Monitoring protein turnover during phosphate starvation-dependent autophagic degradation using a photoconvertible fluorescent protein aggregate in tobacco BY-2 cells, Front. Plant Sci., 2014, 5, 172.

    Article  PubMed  PubMed Central  Google Scholar 

  112. J. Zhang, Teaching the basics of autophagy and mitophagy to redox biologists-Mechanisms and experimental approaches, Redox Biol., 2015, 4, 242–259.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. H. Koga, M. Martinez-Vicente, F. Macian, V. V. Verkhusha and A. M. Cuervo, A photoconvertible fluorescent reporter to track chaperone-mediated autophagy, Nat. Commun., 2011, 2, 386.

    Article  PubMed  CAS  Google Scholar 

  114. M. Kon, R. Kiffin, H. Koga, J. Chapochnick, F. Macian, L. Varticovski and A. M. Cuervo, Chaperone-mediated autophagy is required for tumor growth, Sci. Transl. Med., 2011, 3, 109ra117.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  115. L. Zhang, N. G. Gurskaya, E. M. Merzlyak, D. B. Staroverov, N. N. Mudrik, O. N. Samarkina, L. M. Vinokurov, S. Lukyanov and K. A. Lukyanov, Method for real-time monitoring of protein degradation at the single cell level, BioTechniques, 2007, 42, 446, 448, 450.

    Article  CAS  PubMed  Google Scholar 

  116. K. H. Lodowski, R. Lee, P. Ropelewski, I. Nemet, G. Tian and Y. Imanishi, Signals governing the trafficking and mistrafficking of a ciliary GPCR, rhodopsin, J. Neurosci., 2013, 33, 13621–13638.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  117. K. H. Lodowski and Y. Imanishi, Monitoring of rhodopsin trafficking and mistrafficking in live photoreceptors, Methods Mol. Biol., 2015, 1271, 293–307.

    Article  CAS  PubMed  Google Scholar 

  118. A. Poetsch, L. L. Molday and R. S. Molday, The cGMP-gated channel and related glutamic acid-rich proteins interact with peripherin-2 at the rim region of rod photoreceptor disc membranes, J. Biol. Chem., 2001, 276, 48009–48016.

    Article  CAS  PubMed  Google Scholar 

  119. G. Tian, P. Ropelewski, I. Nemet, R. Lee, K. H. Lodowski and Y. Imanishi, An unconventional secretory pathway mediates the cilia targeting of peripherin/rds, J. Neurosci., 2014, 34, 992–1006.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  120. L. M. Ritter, N. Khattree, B. Tam, O. L. Moritz, F. Schmitz and A. F. Goldberg, In situ visualization of protein interactions in sensory neurons: glutamic acid-rich proteins (GARPs) play differential roles for photoreceptor outer segment scaffolding, J. Neurosci., 2011, 31, 11231–11243.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. T. K. Kerppola, Bimolecular fluorescence complementation (BiFC) analysis as a probe of protein interactions in living cells, Annu. Rev. Biophys., 2008, 37, 465–487.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. S. Karan, H. Zhang, S. Li, J. M. Frederick and W. Baehr, A model for transport of membrane-associated phototransduction polypeptides in rod and cone photoreceptor inner segments, Vision Res., 2008, 48, 442–452.

    Article  CAS  PubMed  Google Scholar 

  123. J. Wang and D. Deretic, Molecular complexes that direct rhodopsin transport to primary cilia, Prog. Retinal Eye Res., 2014, 38, 1–19.

    Article  CAS  Google Scholar 

  124. I. Nemet, P. Ropelewski and Y. Imanishi, Rhodopsin trafficking and mistrafficking: signals, molecular components, and mechanisms, Prog. Mol. Biol. Transl. Sci., 2015, 132, 39–71.

    Article  PubMed  Google Scholar 

  125. K. Miyaguchi and P. H. Hashimoto, Evidence for the transport of opsin in the connecting cilium and basal rod outer segment in rat retina: rapid-freeze, deep-etch and horseradish peroxidase labelling studies, J. Neurocytol., 1992, 21, 449–457.

    Article  CAS  PubMed  Google Scholar 

  126. S. Obata and J. Usukura, Morphogenesis of the photoreceptor outer segment during postnatal development in the mouse (BALB/c) retina, Cell Tissue Res., 1992, 269, 39–48.

    Article  CAS  PubMed  Google Scholar 

  127. J. Z. Chuang, Y. Zhao and C. H. Sung, SARA-regulated vesicular targeting underlies formation of the light-sensing organelle in mammalian rods, Cell, 2007, 130, 535–547.

    Article  CAS  PubMed  Google Scholar 

  128. R. H. Steinberg, S. K. Fisher and D. H. Anderson, Disc morphogenesis in vertebrate photoreceptors, J. Comp. Neurol., 1980, 190, 501–508.

    Article  CAS  PubMed  Google Scholar 

  129. I. Nemet, G. Tian and Y. Imanishi, Organization of cGMP sensing structures on the rod photoreceptor outer segment plasma membrane, Channels (Austin), 2014, 8, 528–535.

    Article  Google Scholar 

  130. R. S. Molday, D. Hicks and L. Molday, Peripherin. A rim-specific membrane protein of rod outer segment discs, Invest. Ophthalmol. Visual Sci., 1987, 28, 50–61.

    CAS  Google Scholar 

  131. N. J. Cook, L. L. Molday, D. Reid, U. B. Kaupp and R. S. Molday, The cGMP-gated channel of bovine rod photoreceptors is localized exclusively in the plasma membrane, J. Biol. Chem., 1989, 264, 6996–6999.

    Article  CAS  PubMed  Google Scholar 

  132. D. S. Williams, K. A. Linberg, D. K. Vaughan, R. N. Fariss and S. K. Fisher, Disruption of microfilament organization and deregulation of disk membrane morphogenesis by cytochalasin D in rod and cone photoreceptors, J. Comp. Neurol., 1988, 272, 161–176.

    Article  CAS  PubMed  Google Scholar 

  133. I. Nemet, G. Tian and Y. Imanishi, Submembrane assembly and renewal of rod photoreceptor cGMP-gated channel: insight into the actin-dependent process of outer segment morphogenesis, J. Neurosci., 2014, 34, 8164–8174.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  134. M. A. Maw, D. Corbeil, J. Koch, A. Hellwig, J. C. Wilson-Wheeler, R. J. Bridges, G. Kumaramanickavel, S. John, D. Nancarrow, K. Roper, A. Weigmann, W. B. Huttner and M. J. Denton, A frameshift mutation in prominin (mouse)-like 1 causes human retinal degeneration, Hum. Mol. Genet., 2000, 9, 27–34.

    Article  CAS  PubMed  Google Scholar 

  135. A. Rattner, P. M. Smallwood, J. Williams, C. Cooke, A. Savchenko, A. Lyubarsky, E. N. Pugh and J. Nathans, A photoreceptor-specific cadherin is essential for the structural integrity of the outer segment and for photoreceptor survival, Neuron, 2001, 32, 775–786.

    Article  CAS  PubMed  Google Scholar 

  136. Z. Yang, Y. Chen, C. Lillo, J. Chien, Z. Yu, M. Michaelides, M. Klein, K. A. Howes, Y. Li, Y. Kaminoh, H. Chen, C. Zhao, Y. T. Al-Sheikh, G. Karan, D. Corbeil, P. Escher, S. Kamaya, C. Li, S. Johnson, J. M. Frederick, Y. Zhao, C. Wang, D. J. Cameron, W. B. Huttner, D. F. Schorderet, F. L. Munier, A. T. Moore, D. G. Birch, W. Baehr, D. M. Hunt, D. S. Williams and K. Zhang, Mutant prominin 1 found in patients with macular degeneration disrupts photoreceptor disk morphogenesis in mice, J. Clin. Invest., 2008, 118, 2908–2916.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  137. Z. Han, D. W. Anderson and D. S. Papermaster, Prominin-1 localizes to the open rims of outer segment lamellae in Xenopus laevis rod and cone photoreceptors, Invest. Ophthalmol. Visual Sci., 2012, 53, 361–373.

    Article  CAS  Google Scholar 

  138. A. Rattner, J. Chen and J. Nathans, Proteolytic shedding of the extracellular domain of photoreceptor cadherin. Implications for outer segment assembly, J. Biol. Chem., 2004, 279, 42202–42210.

    Article  CAS  PubMed  Google Scholar 

  139. M. S. Kinney and S. K. Fisher, The photoreceptors and pigment epithelium of the larval Xenopus retina: morphogenesis and outer segment renewal, Proc. R. Soc. London, B, 1978, 201, 149–167.

    Article  CAS  Google Scholar 

  140. M. Hofmann, C. Eggeling, S. Jakobs and S. W. Hell, Breaking the diffraction barrier in fluorescence microscopy at low light intensities by using reversibly photoswitchable proteins, Proc. Natl. Acad. Sci. U. S. A., 2005, 102, 17565–17569.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. T. Grotjohann, I. Testa, M. Leutenegger, H. Bock, N. T. Urban, F. Lavoie-Cardinal, K. I. Willig, C. Eggeling, S. Jakobs and S. W. Hell, Diffraction-unlimited all-optical imaging and writing with a photochromic GFP, Nature, 2011, 478, 204–208.

    Article  CAS  PubMed  Google Scholar 

  142. P. Dedecker, G. C. Mo, T. Dertinger and J. Zhang, Widely accessible method for superresolution fluorescence imaging of living systems, Proc. Natl. Acad. Sci. U. S. A., 2012, 109, 10909–10914.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  143. T. Dertinger, R. Colyer, G. Iyer, S. Weiss and J. Enderlein, Fast, background-free, 3D super-resolution optical fluctuation imaging (SOFI), Proc. Natl. Acad. Sci. U. S. A., 2009, 106, 22287–22292.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  144. B. Moeyaert, N. Nguyen Bich, E. De Zitter, S. Rocha, K. Clays, H. Mizuno, L. van Meervelt, J. Hofkens and P. Dedecker, Green-to-red photoconvertible Dronpa mutant for multimodal super-resolution fluorescence microscopy, ACS Nano, 2014, 8, 1664–1673.

    Article  CAS  PubMed  Google Scholar 

  145. C. H. Sung, C. Makino, D. Baylor and J. Nathans, A rhodopsin gene mutation responsible for autosomal dominant retinitis pigmentosa results in a protein that is defective in localization to the photoreceptor outer segment, J. Neurosci., 1994, 14, 5818–5833.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. V. S. Lopes, D. Jimeno, K. Khanobdee, X. Song, B. Chen, S. Nusinowitz and D. S. Williams, Dysfunction of heterotrimeric kinesin-2 in rod photoreceptor cells and the role of opsin mislocalization in rapid cell death, Mol. Biol. Cell, 2010, 21, 4076–4088.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  147. J. Mazelova, L. Astuto-Gribble, H. Inoue, B. M. Tam, E. Schonteich, R. Prekeris, O. L. Moritz, P. A. Randazzo and D. Deretic, Ciliary targeting motif VxPx directs assembly of a trafficking module through Arf4, EMBO J., 2009, 28, 183–192.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. C. M. Louie, G. Caridi, V. S. Lopes, F. Brancati, A. Kispert, M. A. Lancaster, A. M. Schlossman, E. A. Otto, M. Leitges, H. J. Grone, I. Lopez, H. V. Gudiseva, J. F. O’Toole, E. Vallespin, R. Ayyagari, C. Ayuso, F. P. Cremers, A. I. den Hollander, R. K. Koenekoop, B. Dallapiccola, G. M. Ghiggeri, F. Hildebrandt, E. M. Valente, D. S. Williams and J. G. Gleeson, AHI1 is required for photoreceptor outer segment development and is a modifier for retinal degeneration in nephronophthisis, Nat. Genet., 2010, 42, 175–180.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. T. Li, W. K. Snyder, J. E. Olsson and T. P. Dryja, Transgenic mice carrying the dominant rhodopsin mutation P347S: evidence for defective vectorial transport of rhodopsin to the outer segments, Proc. Natl. Acad. Sci. U. S. A., 1996, 93, 14176–14181.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. G. J. Pazour, S. A. Baker, J. A. Deane, D. G. Cole, B. L. Dickert, J. L. Rosenbaum, G. B. Witman and J. C. Besharse, The intraflagellar transport protein, IFT88, is essential for vertebrate photoreceptor assembly and maintenance, J. Cell Biol., 2002, 157, 103–113.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  151. D. Shcherbo, E. M. Merzlyak, T. V. Chepurnykh, A. F. Fradkov, G. V. Ermakova, E. A. Solovieva, K. A. Lukyanov, E. A. Bogdanova, A. G. Zaraisky, S. Lukyanov and D. M. Chudakov, Bright far-red fluorescent protein for whole-body imaging, Nat. Methods, 2007, 4, 741–746.

    Article  CAS  PubMed  Google Scholar 

  152. P. K. Kim, D. W. Hailey, R. T. Mullen and J. Lippincott-Schwartz, Ubiquitin signals autophagic degradation of cytosolic proteins and peroxisomes, Proc. Natl. Acad. Sci. U. S. A., 2008, 105, 20567–20574.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Y. Kabeya, N. Mizushima, T. Ueno, A. Yamamoto, T. Kirisako, T. Noda, E. Kominami, Y. Ohsumi and T. Yoshimori, LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing, EMBO J., 2000, 19, 5720–5728.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  154. D. O. Wang, S. M. Kim, Y. Zhao, H. Hwang, S. K. Miura, W. S. Sossin, K. C. Martin, Synapse- and stimulus-specific local translation during long-term neuronal plasticity, Science, 2009, 324, 1536–1540.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  155. G. Tian, K. H. Lodowski, R. Lee and Y. Imanishi, Retrograde intraciliary trafficking of opsin during the maintenance of cone-shaped photoreceptor outer segments of Xenopus laevis, J. Comp. Neurol., 2014, 522, 3577–3589.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Correspondence to Yoshikazu Imanishi.

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Parts of the data in this paper were presented during the 16th International Congress on Photobiology held in Cordoba, Argentina, on September 8–12, 2014.

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Nemet, I., Ropelewski, P. & Imanishi, Y. Applications of phototransformable fluorescent proteins for tracking the dynamics of cellular components. Photochem Photobiol Sci 14, 1787–1806 (2015). https://doi.org/10.1039/c5pp00174a

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