Imaging and quantitation techniques for tracking cargo along endosome-to-Golgi transport pathways

Cells

Volumn 2, Issue 1, 2013, Pages 105-123

  Chia, Pei Zhi Cheryl ^a   Gleeson, Paul A ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Endosomes; Flow cytometry; Fluorescent proteins; Golgi apparatus; Optical imaging; Super resolution microscopy

Indexed keywords

FLUORESCENT DYE; GREEN FLUORESCENT PROTEIN;

CELL TRACKING; CELL TRANSPORT; ELECTRON MICROSCOPY; ENDOSOME; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; FLUORESCENCE IMAGING; GOLGI COMPLEX; HIGH THROUGHPUT SCREENING; HUMAN; INTERNALIZATION; INTRACELLULAR MEMBRANE; LYSOSOME; MICROSCOPY; NONHUMAN; PROTEIN LOCALIZATION; REVIEW;

EID: 84930893126     PISSN: None     EISSN: 20734409     Source Type: Journal    
DOI: 10.3390/cells2010105     Document Type: Review

References (92)

1. Gruenberg, J.; Griffiths, G.; Howell, K.E. Characterization of the early endosome and putative endocytic carrier vesicles in vivo and with an assay of vesicle fusion in vitro. J. Cell Biol. 1989, 108, 1301-1316.
2. Bonifacino, J.S.; Rojas, R. Retrograde transport from endosomes to the trans-Golgi network. Nat. Rev. Mol. Cell Biol. 2006, 7, 568-579.
3. Johannes, L.; Popoff, V. Tracing the retrograde route in protein trafficking. Cell 2008, 135, 1175-1187.
4. Ghosh, P.; Dahms, N.M.; Kornfeld, S. Mannose 6-phosphate receptors: New twists in the tale. Nat. Rev. Mol. Cell Biol. 2003, 4, 202-212.
5. Ghosh, R.N.; Mallet, W.G.; Soe, T.T.; McGraw, T.E.; Maxfield, F.R. An endocytosed TGN38 chimeric protein is delivered to the TGN after trafficking through the endocytic recycling compartment in CHO cells. J. Cell Biol. 1998, 142, 923-936.
6. Sandvig, K.; van Deurs, B. Delivery into cells: Lessons learned from plant and bacterial toxins. Gene Ther. 2005, 12, 865-872.
7. Shewan, A.M.; van Dam, E.M.; Martin, S.; Luen, T.B.; Hong, W.; Bryant, N.J.; James, D.E. GLUT4 recycles via a trans-Golgi network (TGN) subdomain enriched in Syntaxins 6 and 16 but not TGN38: Involvement of an acidic targeting motif. Mol. Biol Cell 2003, 14, 973-986.
8. Plaut, R.D.; Carbonetti, N.H. Retrograde transport of pertussis toxin in the mammalian cell. Cell Microbiol. 2008, 10, 1130-1139.
9. Utskarpen, A.; Slagsvold, H.H.; Iversen, T.G.; Walchli, S.; Sandvig, K. Transport of ricin from endosomes to the Golgi apparatus is regulated by Rab6A and Rab6A'. Traffic 2006, 7, 663-672.
10. Abbe, E. Beitrage zur Theorie des Mikroskops und der mikroskopischen Wahrmehmung. Arch. Mikrosk. Anat. 1873, 9, 413-420.
11. Huang, B.; Babcock, H.; Zhuang, X. Breaking the diffraction barrier: super-resolution imaging of cells. Cell 2010, 143, 1047-1058.
12. Lippincott-Schwartz, J.; Patterson, G.H. Photoactivatable fluorescent proteins for diffraction-limited and super-resolution imaging. Trends Cell Biol. 2009, 19, 555-565.
13. Schermelleh, L.; Heintzmann, R.; Leonhardt, H. A guide to super-resolution fluorescence microscopy. J. Cell. Biol. 2010, 190, 165-175.
14. Toomre, D.; Bewersdorf, J. A new wave of cellular imaging. Annu. Rev. Cell Dev. Biol. 2010, 26, 285-314.
15. Gustafsson, M.G. Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy. J. Microsc. 2000, 198, 82-87.
16. Gustafsson, M.G. Nonlinear structured-illumination microscopy: Wide-field fluorescence imaging with theoretically unlimited resolution. Proc. Natl. Acad. Sci. USA 2005, 102, 13081-13086.
17. Schermelleh, L.; Carlton, P.M.;. Haase, S.; Shao, L.; Winoto, L.; Kner, P.; Burke, B.; Cardoso, M.C.; Agard, D.A.; Gustafsson, M.G.; et al. Subdiffraction multicolor imaging of the nuclear periphery with 3D structured illumination microscopy. Science 2008, 320, 1332-1336.
18. Ach, T.; Best, G.; Rossberger, S.; Heintzmann, R.; Cremer, C.; Dithmar, S. Autofluorescence imaging of human RPE cell granules using structured illumination microscopy. Br. J. Ophthalmol. 2012, 96, 1141-1144.
19. Hanssen, E.; Carlton, P.; Deed, S.; Klonis, N.; Sedat, J.; DeRisi, J.; Tilley, L. Whole cell imaging reveals novel modular features of the exomembrane system of the malaria parasite, Plasmodium falciparum. Int J. Parasitol. 2010, 40, 123-134.
20. Meyer, L.; Wildanger, D.; Medda, R.; Punge, A.; Rizzoli, S.O.; Donnert, G.; Hell, S.W. Dual-color STED microscopy at 30-nm focal-plane resolution. Small 2008, 4, 1095-1100.
21. Moneron, G.; Medda, R.; Hein, B.; Giske, A.; Westphal, V.; Hell, S.W. Fast STED microscopy with continuous wave fiber lasers. Opt. Express 2010, 18, 1302-1309.
22. Schroder, J.; Benink, H.; Dyba, M.; Los, G.V. In vivo labeling method using a genetic construct for nanoscale resolution microscopy. Biophys. J. 2009, 96, L01-L03.
23. Rittweger, E.; Han, K.Y.; Irvine, S.E.; Eggeling, C.; Hell, S.W. STED microscopy reveals crystal colour centres with nanometric resolution. Nature Photonics 2009, 3, 144-147.
24. Harke, B.; Ullal, C.K.; Keller, J.; Hell, S.W. Three-dimensional nanoscopy of colloidal crystals. Nano Lett. 2008, 8, 1309-1313.
25. Hein, B.; Willig, K.I.; Hell, S.W. Stimulated emission depletion (STED) nanoscopy of a fluorescent protein-labeled organelle inside a living cell. Proc. Natl. Acad. Sci USA 2008, 105, 14271-14276.
26. Donnert, G.; Keller, J.; Wurm, C.A.; Rizzoli, S.O.; Westphal, V.; Schonle, A.; Jahn, R.; Jakobs, S.; Eggeling, C.; Hell, S.W. Two-color far-field fluorescence nanoscopy. Biophys. J. 2007, 92, L67-L69.
27. Buckers, J.; Wildanger, D.; Vicidomini, G.; Kastrup, L.; Hell, S.W. Simultaneous multi-lifetime multi-color STED imaging for colocalization analyses. Opt. Express 2011, 19, 3130-3143.
28. Schmidt, R.; Wurm, C.A.; Jakobs, S.; Engelhardt, J.; Egner, A.; Hell, S.W. Spherical nanosized focal spot unravels the interior of cells. Nat. Methods 2008, 5, 539-544.
29. Betzig, E.; Patterson, G.H.; Sougrat, R.; Lindwasser, O.W.; Olenych, S.; Bonifacino, J.S.; Davidson, M.W.; Lippincott-Schwartz, J.; Hess, H.F. Imaging intracellular fluorescent proteins at nanometer resolution. Science 2006, 313, 1642-1645.
30. Hess, S.T.; Girirajan, T.P.; Mason, M.D. Ultra-high resolution imaging by fluorescence photoactivation localization microscopy. Biophys. J. 2006, 91, 4258-4272.
31. Rust, M.J.; Bates, M.; Zhuang, X. Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (STORM). Nat. Methods 2006, 3, 793-795.
32. Shtengel, G.; Galbraith, J.A.; Galbraith, C.G.; Lippincott-Schwartz, J.; Gillette, J.M.; Manley, S.; Sougrat, R.; Waterman, C.M.; Kanchanawong, P.; Davidson, M.W.; et al. Interferometric fluorescent super-resolution microscopy resolves 3D cellular ultrastructure. Proc. Natl. Acad. Sci. USA 2009, 106, 3125-3130.
33. Williamson, D.J.; Owen, D.M.; Rossy, J.; Magenau, A.; Wehrmann, M.; Gooding, J.J.; Gaus, K. Pre-existing clusters of the adaptor Lat do not participate in early T cell signaling events. Nat. Immunol. 2011, 12, 655-662.
34. Egner, A.; Geisler, C.; von Middendorff, C.; Bock, H.; Wenzel, D.; Medda, R.; Andresen, M.; Stiel, A.C.; Jakobs, S.; Eggeling, C.; et al. Fluorescence nanoscopy in whole cells by asynchronous localization of photoswitching emitters. Biophys. J. 2007, 93, 3285-3290.
35. Bates, M.; Huang, B.; Dempsey, G.T.; Zhuang, X. Multicolor super-resolution imaging with photo-switchable fluorescent probes. Science 2007, 317, 1749-1753.
36. Heilemann, M.; van de Linde, S.; Schuttpelz, M.; Kasper, R.; Seefeldt, B.; Mukherjee, A.; Tinnefeld, P.; Sauer, M. Subdiffraction-resolution fluorescence imaging with conventional fluorescent probes. Angew. Chem. Int. Edit. 2008, 47, 6172-6176.
37. Huang, B.; Wang, W.; Bates, M.; Zhuang, X. Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy. Science 2008, 319, 810-813.
38. Simmons, S.R.; Pawley, J.B.; Albrecht, R.M. Optimizing parameters for correlative immunogold localization by video-enhanced light microscopy, high-voltage transmission electron microscopy, and field emission scanning electron microscopy. J. Histochem. Cytochem. 1990, 38, 1781-1785.
39. Van Weering, J.R.; Brown, E.; Sharp, T.H.; Mantell, J.; Cullen, P.J.; Verkade, P. Intracellular membrane traffic at high resolution. Methods Cell Biol. 2010, 96, 619-648.
40. Polishchuk, R.S.; Polishchuk, E.V.; Marra, P.; Alberti, S.; Buccione, R.; Luini, A.; Mironov, A.A. Correlative light-electron microscopy reveals the tubular-saccular ultrastructure of carriers operating between Golgi apparatus and plasma membrane. J. Cell Biol. 2000, 148, 45-58.
41. Polishchuk, R.S.; San Pietro, E.; Di Pentima, A.; Tete, S.; Bonifacino, J.S. Ultrastructure of long-range transport carriers moving from the trans Golgi network to peripheral endosomes. Traffic 2006, 7, 1092-1103.
42. Van Rijnsoever, C.; Oorschot, V.; Klumperman, J. Correlative light-electron microscopy (CLEM) combining live-cell imaging and immunolabeling of ultrathin cryosections. Nat. Methods 2008, 5, 973-980.
43. Van Weering, J.R.; Brown, E.; Sharp, T.H.; Mantell, J.; Cullen, P.J.; Verkade, P. Intracellular membrane traffic at high resolution. Methods Cell Biol. 2010, 96, 619-648.
44. Heim, R.; Cubitt, A.B.; Tsien, R.Y. Improved green fluorescence. Nature 1995, 373, 663-664.
45. Cormack, B.P.; Valdivia, R.H.; Falkow, S. FACS-optimized mutants of the green fluorescent protein (GFP). Gene 1996, 173, 33-38.
46. Heim, R.; Tsien, R.Y. Engineering green fluorescent protein for improved brightness, longer wavelengths and fluorescence resonance energy transfer. Curr. Biol. 1996, 6, 178-182.
47. 2+based on green fluorescent proteins and calmodulin. Nature 1997, 388, 882-887.
48. Matz, M.V.; Fradkov, A.F.; Labas, Y.A.; Savitsky, A.P.; Zaraisky, A.G.; Markelov, M.L.; Lukyanov, S.A. Fluorescent proteins from nonbioluminescent Anthozoa species. Nat. Biotechnol. 1999, 17, 969-973.
49. Baird, G.S.; Zacharias, D.A.; Tsien, R.Y. Biochemistry, mutagenesis, and oligomerization of DsRed, a red fluorescent protein from coral. Proc. Natl. Acad. Sci. USA 2000, 97, 11984-11989.
50. Terskikh, A.; Fradkov, A.; Ermakova, G.; Zaraisky, A.; Tan, P.; Kajava, A.V.; Zhao, X.; Lukyanov, S.; Matz, M.; Kim, S.; Weissman, I.; Siebert, P. "Fluorescent timer": Protein that changes color with time. Science 2000, 290, 1585-1588.
51. Bevis, B.J.; Glick, B.S. Rapidly maturing variants of the Discosoma red fluorescent protein (DsRed). Nat. Biotechnol. 2002, 20, 83-87.
52. Gross, L.A.; Baird, G.S.; Hoffman, R.C.; Baldridge, K.K.; Tsien, R.Y. The structure of the chromophore within DsRed, a red fluorescent protein from coral. Proc. Natl. Acad. Sci USA 2000, 97, 11990-11995.
53. Shaner, N.C.; Campbell, R.E.; Steinbach, P.A.; Giepmans, B.N.; Palmer, A.E.; Tsien, R.Y. Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat. Biotechnol. 2004, 22, 1567-1572.
54. Subach, F.V.; Subach, O.M.; Gundorov, I.S.; Morozova, K.S.; Piatkevich, K.D.; Cuervo, A.M.; Verkhusha, V.V. Monomeric fluorescent timers that change color from blue to red report on cellular trafficking. Nat. Chem. Biol. 2009, 5, 118-126.
55. Lippincott-Schwartz, J.; Altan-Bonnet, N.; Patterson, G.H. Photobleaching and photoactivation: Following protein dynamics in living cells. Nat. Cell. Biol. 2003, 5(Suppl.), S7-S14.
56. Lukyanov, K.A.; Chudakov, D.M.; Lukyanov, S.; Verkhusha, V.V. Innovation: Photoactivatable fluorescent proteins. Nat. Rev. Mol. Cell Biol. 2005, 6, 885-891.
57. Remington, S.J. Fluorescent proteins: Maturation, photochemistry and photophysics. Curr. Opin. Struct. Biol. 2006, 16, 714-721.
58. Patterson, G.H.; Lippincott-Schwartz, J. A photoactivatable GFP for selective photolabeling of proteins and cells. Science 2002, 297, 1873-1877.
59. McKinney, S.A.; Murphy, C.S.; Hazelwood, K.L.; Davidson, M.W.; Looger, L.L. A bright and photostable photoconvertible fluorescent protein. Nat. Methods 2009, 6, 131-133.
60. Bates, M.; Blosser, T.R.; Zhuang, X. Short-range spectroscopic ruler based on a single-molecule optical switch. Phys. Rev. Lett. 2005, doi:10.1103/PhysRevLett.94.108101.
61. Baddeley, D.; Jayasinghe, I.D.; Cremer, C.; Cannell, M.B.; Soeller, C. Light-induced dark states of organic fluochromes enable 30 nm resolution imaging in standard media. Biophys. J. 2009, 96, L22-L24.
62. Dempsey, G.T.; Bates, M.; Kowtoniuk, W.E.; Liu, D.R.; Tsien, R.Y.; Zhuang, X. Photoswitching mechanism of cyanine dyes. J. Am. Chem. Soc. 2009, 131, 18192-18193.
63. Ando, R.; Mizuno, H.; Miyawaki, A. Regulated fast nucleocytoplasmic shuttling observed by reversible protein highlighting. Science 2004, 306, 1370-1373.
64. Habuchi, S.; Ando, R.; Dedecker, P.; Verheijen, W.; Mizuno, H.; Miyawaki, A.; Hofkens, J. Reversible single-molecule photoswitching in the GFP-like fluorescent protein Dronpa. Proc. Natl. Acad. Sci. USA 2005, 102, 9511-9516.
65. Fuchs, J.; Bohme, S.; Oswald, F.; Hedde, P.N.; Krause, M.; Wiedenmann, J.; Nienhaus, G.U. A photoactivatable marker protein for pulse-chase imaging with super-resolution. Nat. Methods 2010, 7, 627-630.
66. Grabenbauer, M.; Geerts, W.J.; Fernadez-Rodriguez, J.; Hoenger, A.; Koster, A.J.; Nilsson, T. Correlative microscopy and electron tomography of GFP through photooxidation. Nat. Methods 2005, 2, 857-862.
67. Shu, X.; Lev-Ram, V.; Deerinck, T.J.; Qi, Y.; Ramko, E.B.; Davidson, M.W.; Jin, Y.; Ellisman, M.H.; Tsien, R.Y. A genetically encoded tag for correlated light and electron microscopy of intact cells, tissues, and organisms. PLoS Biol. 2011, 9, e1001041.
68. North, A.J. Seeing is believing? A beginners' guide to practical pitfalls in image acquisition. J. Cell Biol. 2006, 172, 9-18.
69. Bolte, S.; Cordelieres, F.P. A guided tour into subcellular colocalization analysis in light microscopy. J. Microsc. 2006, 224, 213-232.
70. Manders, E.M.; Stap, J.; Brakenhoff, G.J.; van Driel, R.; Aten, J.A. Dynamics of three-dimensional replication patterns during the S-phase, analysed by double labelling of DNA and confocal microscopy. J. Cell Sci. 1992, 103, 857-862.
71. Zinchuk, V.; Zinchuk, O.; Okada, T. Quantitative colocalization analysis of multicolor confocal immunofluorescence microscopy images: pushing pixels to explore biological phenomena. Acta Histochem. Cytochem. 2007, 40, 101-111.
72. Bolte, S.; Talbot, C.; Boutte, Y.; Catrice, O.; Read, N.D.; Satiat-Jeunemaitre, B. FM-dyes as experimental probes for dissecting vesicle trafficking in living plant cells. J. Microsc. 2004, 214, 159-173.
73. Roerdink, Jos B.T.M.; Meijster, A. The watershed transform: definitions, algorithms and parallelization strategies. Fund. Inform. 2000, 41, 187-226.
74. Lachmanovich, E.; Shvartsman, D.E.; Malka, Y.; Botvin, C.; Henis, Y.I.; Weiss, A.M. Co-localization analysis of complex formation among membrane proteins by computerized fluorescence microscopy: Application to immunofluorescence co-patching studies. J. Microsc. 2003, 212, 122-131.
75. Boutte, Y.; Crosnier, M.T.; Carraro, N.; Traas, J.; Satiat-Jeunemaitre, B. The plasma membrane recycling pathway and cell polarity in plants: studies on PIN proteins. J. Cell Sci. 2006, 119, 1255-1265.
76. Woodcroft, B.J.; Hammond, L.; Stow, J.L.; Hamilton, N.A. Automated organelle-based colocalization in whole-cell imaging. Cytometry A 2009, 75, 941-950.
77. Jaskolski, F.; Mulle, C.; Manzoni, O.J. An automated method to quantify and visualize colocalized fluorescent signals. J. Neurosci. Methods 2005, 146, 42-49.
78. Hoffman, R.A. Unit 1 23 Pulse width for particle sizing. Curr. Protoc. Cytom. 2009, doi: 10.1002/0471142956.cy0123s50.
79. Wersto, R.P.; Chrest, F.J.; Leary, J.F.; Morris, C.; Stetler-Stevenson, M.A.; Gabrielson, E. Doublet discrimination in DNA cell-cycle analysis. Cytometry 2001, 46, 296-306.
80. Ramdzan, Y.M.; Polling, S.; Chia, C.P.; Ng, I.H.; Ormsby, A.R.; Croft, N.P.; Purcell, A.W.; Bogoyevitch, M.A.; Ng, D.C.; Gleeson, P.A.; et al. Tracking protein aggregation and mislocalization in cells with flow cytometry. Nat. Methods 2012, 9, 467-470.
81. Nakao, H.; Takeda, T. Escherichia coli Shiga toxin. J. Nat. Toxins 2000, 9, 299-313.
82. Gruenberg, J. The endocytic pathway: A mosaic of domains. Nat. Rev. Mol. Cell Biol. 2001, 2, 721-730.
83. Lieu, Z.Z.; Gleeson, P.A. Endosome-to-Golgi transport pathways in physiological processes. Histol. Histopathol. 2011, 26, 395-408.
84. Mari, M.; Bujny, M.V.; Zeuschner, D.; Geerts, W.J.; Griffith, J.; Petersen, C.M.; Cullen, P.J.; Klumperman, J.; Geuze, H.J. SNX1 defines an early endosomal recycling exit for sortilin and mannose 6-phosphate receptors. Traffic 2008, 9, 380-393.
85. Kukulski, W.; Schorb, M.; Kaksonen, M.; Briggs, J.A. Plasma membrane reshaping during endocytosis is revealed by time-resolved electron tomography. Cell 2012, 150, 508-520.
86. Chan, W.C.; Nie, S. Quantum dot bioconjugates for ultrasensitive nonisotopic detection. Science 1998, 281, 2016-2018.
87. Fomenko, V.; Nesbitt, D.J. Solution control of radiative and nonradiative lifetimes: A novel contribution to quantum dot blinking suppression. Nano Lett. 2008, 8, 287-293.
88. Chien, C.Y.; Chang, Y.J.; Chen, K.H.; Lai, W.T.; George, T.; Scherer, A.; Li, P.W. Nanoscale, catalytically enhanced local oxidation of silicon-containing layers by 'burrowing' Ge quantum dots. Nanotechnology 2011, doi:10.1088/0957-4484/22/43/435602.
89. Shi, X.; Xie, Z.; Song, Y.; Tan, Y.; Yeung, E.S.; Gai, H. Superlocalization spectral imaging microscopy of a multicolor quantum dot complex. Anal. Chem. 2012, 84, 1504-1509.
90. Schieber, C.; Bestetti, A.; Lim, J.P.; Ryan, A.D.; Nguyen, T.L.; Eldridge, R.; White, A.R.; Gleeson, P.A.; Donnelly, P.S.; Williams, S.J.; Mulvaney, P. Conjugation of transferrin to azide-modified CdSe/ZnS core-shell quantum dots using cyclooctyne click chemistry. Angew. Chem. Int. Edit. 2012, 51, 10523-10527.
91. Duong, T.; Goud, B.; Schauer, K. Closed-form density-based framework for automatic detection of cellular morphology changes. Proc. Natl. Acad. Sci. USA 2012, 109, 8382-8387.
92. Schauer, K.; Duong, T.; Bleakley, K.; Bardin, S.; Bornens, M.; Goud, B. Probabilistic density maps to study global endomembrane organization. Nat. Methods 2010, 7, 560-566.