Probing cellular processes by long-term live imaging - historic problems and current solutions

Journal of Cell Science

Volumn 126, Issue 17, 2013, Pages 3805-3815

  Coutu, Daniel L ^a   Schroeder, Timm ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

Biosensors; Fluorescence; Hardware; Single cell imaging; Software; Time lapse microscopy

Indexed keywords

FLUORESCENT DYE;

ARTICLE; BIOLOGY; BIOSENSOR; CELL CULTURE; CELL SURVIVAL; CONFOCAL MICROSCOPY; CULTURE MEDIUM; CYTOLOGY; FLUORESCENCE; IMAGE ANALYSIS; IMAGE DISPLAY; INFORMATION PROCESSING; MAMMAL CELL; MICROENVIRONMENT; MULTIPHOTON MICROSCOPY; NUCLEAR MAGNETIC RESONANCE IMAGING; PHOTOTOXICITY; PRIORITY JOURNAL; PROTEIN ENGINEERING; SINGLE CELL ANALYSIS; TIME LAPSE IMAGING; TIME-LAPSE VIDEO MICROSCOPY;

BIOSENSORS; FLUORESCENCE; HARDWARE; SINGLE-CELL IMAGING; SOFTWARE; TIME-LAPSE MICROSCOPY;

ANIMALS; BIOSENSING TECHNIQUES; CELL CULTURE TECHNIQUES; CELLS, CULTURED; DIAGNOSTIC IMAGING; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MICROSCOPY, FLUORESCENCE; TIME-LAPSE IMAGING;

EID: 84883303584     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.118349     Document Type: Article

References (92)

1. Ai, H. W., Shaner, N. C., Cheng, Z., Tsien, R. Y. and Campbell, R. E. (2007). Exploration of new chromophore structures leads to the identification of improved blue fluorescent proteins. Biochemistry 46, 5904-5910.
2. Aoki, K., Komatsu, N., Hirata, E., Kamioka, Y. and Matsuda, M. (2012). Stable expression of FRET biosensors: a new light in cancer research. Cancer Sci. 103, 614- 619.
3. Asami, M., Pilz, G. A., Ninkovic, J., Godinho, L., Schroeder, T., Huttner, W.B. and Götz, M. (2011). The role of Pax6 in regulating the orientation and mode of cell division of progenitors in the mouse cerebral cortex. Development 138, 5067-5078.
4. Bancaud, A., Huet, S., Rabut, G. and Ellenberg, J. (2010). Fluorescence perturbation techniques to study mobility and molecular dynamics of proteins in live cells: FRAP, photoactivation, photoconversion, and FLIP. Cold Spring Harb. Protoc. 2010, pdb.top90.
5. Bertrand, J. Y., Chi, N. C., Santoso, B., Teng, S., Stainier, D. Y. R. and Traver, D. (2010). Haematopoietic stem cells derive directly from aortic endothelium during development. Nature 464, 108-111.
6. Bonarius, H. P., de Gooijer, C. D., Tramper, J. and Schmid, G. (1995). Determination of the respiration quotient in mammalian cell culture in bicarbonate buffered media. Biotechnol. Bioeng. 45, 524-535.
7. Breithaupt, H. (2002). Rhythm 'n' biology: what happens if cell biology and techno music meet? EMBO Rep. 3, 813-815.
8. Burtscher, I. and Lickert, H. (2009). Foxa2 regulates polarity and epithelialization in the endoderm germ layer of the mouse embryo. Development 136, 1029-1038.
9. Cardona, A. and Tomancak, P. (2012). Current challenges in open-source bioimage informatics. Nat. Methods 9, 661-665.
10. Carpenter, A. E., Kamentsky, L. and Eliceiri, K. W. (2012). A call for bioimaging software usability. Nat. Methods 9, 666-670.
11. Chalfie, M., Tu, Y., Euskirchen, G., Ward, W. W. and Prasher, D. C. (1994). Green fluorescent protein as a marker for gene expression. Science 263, 802-805.
12. Chevroton, L. and Vle's, M. F. (1909). La cinématique de la segmentation de l'oeuf et la chronophotographie du développement de l'Oursin. C. R. Seances Acad. Sci. 149, 806-809.
13. Comandon, J. (1909). Cinématographie, a' l'ultra-microscope, de microbes vivants et des particules mobiles. C. R. Seances Acad. Sci. 149, 938-941.
14. Costa, M. R., Wen, G., Lepier, A., Schroeder, T. and Götz, M. (2008). Par-complex proteins promote proliferative progenitor divisions in the developing mouse cerebral cortex. Development 135, 11-22.
15. Costa, M. R., Bucholz, O., Schroeder, T. and Götz, M. (2009). Late origin of gliarestricted progenitors in the developing mouse cerebral cortex. Cereb. Cortex 19 Suppl 1, i135-i143.
16. Costa, M. R., Ortega, F., Brill, M. S., Beckervordersandforth, R., Petrone, C., Schroeder, T., Götz, M. and Berninger, B. (2011). Continuous live imaging of adult neural stem cell division and lineage progression in vitro. Development 138, 1057- 1068.
17. Cubitt, A. B., Heim, R., Adams, S. R., Boyd, A. E., Gross, L. A. and Tsien, R. Y. (1995). Understanding, improving and using green fluorescent proteins. Trends Biochem. Sci. 20, 448-455.
18. de Chaumont, F., Dallongeville, S., Chenouard, N., Hervé, N., Pop, S., Provoost, T., Meas-Yedid, V., Pankajakshan, P., Lecomte, T., Le Montagner, Y. et al. (2012). Icy: an open bioimage informatics platform for extended reproducible research. Nat. Methods 9, 690-696.
19. Discher, D. E., Mooney, D. J. and Zandstra, P. W. (2009). Growth factors, matrices, and forces combine and control stem cells. Science 324, 1673-1677.
20. Dixit, R. and Cyr, R. (2003). Cell damage and reactive oxygen species production induced by fluorescence microscopy: effect on mitosis and guidelines for noninvasive fluorescence microscopy. Plant J. 36, 280-290.
21. Dunn, G. A. and Jones, G. E. (2004). Cell motility under the microscope: Vorsprung durch Technik. Nat. Rev. Mol. Cell Biol. 5, 667-672.
22. Dykstra, B., Ramunas, J., Kent, D., McCaffrey, L., Szumsky, E., Kelly, L., Farn, K., Blaylock, A., Eaves, C. and Jervis, E. (2006). High-resolution video monitoring of hematopoietic stem cells cultured in single-cell arrays identifies new features of selfrenewal. Proc. Natl. Acad. Sci. USA 103, 8185-8190.
23. Eagle, H. (1971). Buffer combinations for mammalian cell culture. Science 174, 500- 503.
24. Edelstein, A., Amodaj, N., Hoover, K., Vale, R. and Stuurman, N. (2010). Computer control of microscopes using mManager. Curr. Protoc. Mol. Biol. 92, 14.20.1- 14.20.17.
25. Eilken, H. M., Nishikawa, S.-I. and Schroeder, T. (2009). Continuous single-cell imaging of blood generation from haemogenic endothelium. Nature 457, 896-900.
26. Eilken, H., Rieger, M., Hoppe, P., Hermann, A., Smejkal, B., Drew, E., Thum, M., Ninkovic, J., Beckervordersandforth, R. and Schroeder, T. (2010). Continuous long-term detection of live cell surface markers by ''in culture'' antibody staining. Protoc. exch.. 2011, doi:10.1038.
27. Eliceiri, K. W., Berthold, M. R., Goldberg, I. G., Ibáñez, L., Manjunath, B. S., Martone, M. E., Murphy, R. F., Peng, H., Plant, A. L., Roysam, B. et al. (2012). Biological imaging software tools. Nat. Methods 9, 697-710.
28. Endele, M. and Schroeder, T. (2012). Molecular live cell bioimaging in stem cell research. Ann. N. Y. Acad. Sci. 1266, 18-27.
29. Fink, R. (2011). A single frame: imaging live cells twenty-five years ago. Genesis 49, 484-487.
30. Frigault, M. M., Lacoste, J., Swift, J. L. and Brown, C. M. (2009). Live-cell microscopy - tips and tools. J. Cell Sci. 122, 753-767.
31. Frischknecht, F., Gunzer, M. and Shorte, S. L. (2009). Retrospective: Birth of the cool - imaging and microbiology from Ibn al-Haytham to Jean Comandon. Biotechnol. J. 4, 787-790.
32. Gilbert, P. M., Havenstrite, K. L., Magnusson, K. E. G., Sacco, A., Leonardi, N. A., Kraft, P., Nguyen, N. K., Thrun, S., Lutolf, M. P. and Blau, H. M. (2010). Substrate elasticity regulates skeletal muscle stem cell self-renewal in culture. Science 329, 1078-1081.
33. Gobaa, S., Hoehnel, S., Roccio, M., Negro, A., Kobel, S. and Lutolf, M. P. (2011). Artificial niche microarrays for probing single stem cell fate in high throughput. Nat. Methods 8, 949-955.
34. Godley, B. F., Shamsi, F. A., Liang, F.-Q., Jarrett, S. G., Davies, S. and Boulton, M. (2005). Blue light induces mitochondrial DNA damage and free radical production in epithelial cells. J. Biol. Chem. 280, 21061-21066.
35. Grzelak, A., Rychlik, B. and Bartosz, G. (2001). Light-dependent generation of reactive oxygen species in cell culture media. Free Radic. Biol. Med. 30, 1418-1425.
36. Haugh, J. M. (2012). Live-cell fluorescence microscopy with molecular biosensors: what are we really measuring? Biophys. J. 102, 2003-2011.
37. Heim, R. and Tsien, R. Y. (1996). Engineering green fluorescent protein for improved brightness, longer wavelengths and fluorescence resonance energy transfer. Curr. Biol. 6, 178-182.
38. Henrickson, S. E., Mempel, T. R., Mazo, I. B., Liu, B., Artyomov, M. N., Zheng, H., Peixoto, A., Flynn, M. P., Senman, B., Junt, T. et al. (2008). T cell sensing of antigen dose governs interactive behavior with dendritic cells and sets a threshold for T cell activation. Nat. Immunol. 9, 282-291.
39. Herman, B. (2002). Fluorescence microscopy. Curr. Protoc. Immunol. 4, 21.2.1- 21.2.10.
40. Hiraoka, Y., Sedat, J. W. and Agard, D. A. (1987). The use of a charge-coupled device for quantitative optical microscopy of biological structures. Science 238, 36-41.
41. Huisken, J., Swoger, J., Del Bene, F., Wittbrodt, J. and Stelzer, E. H. K. (2004). Optical sectioning deep inside live embryos by selective plane illumination microscopy. Science 305, 1007-1009.
42. Huth, J., Buchholz, M., Kraus, J. M., Mølhave, K., Gradinaru, C., v Wichert, G., Gress, T. M., Neumann, H. and Kestler, H. A. (2011). TimeLapseAnalyzer: multitarget analysis for live-cell imaging and time-lapse microscopy. Comput. Methods Programs Biomed. 104, 227-234.
43. Inoué, S. and Spring, K. R. (1997). Video Microscopy, The Fundamentals, 2nd edn. New York, NY: Plenum Press.
44. Joubert, J. and Sharma, D. (2011). Light microscopy digital imaging. Curr. Protoc. Cytometry 58, 2.3.1-2.3.11.
45. Junt, T., Moseman, E. A., Iannacone, M., Massberg, S., Lang, P. A., Boes, M., Fink, K., Henrickson, S. E., Shayakhmetov, D. M., Di Paolo, N. C. et al. (2007). Subcapsular sinus macrophages in lymph nodes clear lymph-borne viruses and present them to antiviral B cells. Nature 450, 110-114.
46. Kanaan, A., Douglas, R. M., Alper, S. L., Boron, W. F. and Haddad, G. G. (2007). Effect of chronic elevated carbon dioxide on the expression of acid-base transporters in the neonatal and adult mouse. Am. J. Physiol. 293, R1294-R1302.
47. Kankaanpää , P., Paavolainen, L., Tiitta, S., Karjalainen, M., Päivärinne, J., Nieminen, J., Marjomäki, V., Heino, J. and White, D. J. (2012). BioImageXD: an open, general-purpose and high-throughput image-processing platform. Nat. Methods 9, 683-689.
48. Kissa, K. and Herbomel, P. (2010). Blood stem cells emerge from aortic endothelium by a novel type of cell transition. Nature 464, 112-115.
49. Klein, J., Leupold, S., Biegler, I., Biedendieck, R., Münch, R. and Jahn, D. (2012). TLM-Tracker: software for cell segmentation, tracking and lineage analysis in timelapse microscopy movies. Bioinformatics 28, 2276-2277.
50. Kokkaliaris, K. D., Loeffler, D. and Schroeder, T. (2012). Advances in tracking hematopoiesis at the single-cell level. Curr. Opin. Hematol. 19, 243-249.
51. Kremers, G.-J., Gilbert, S. G., Cranfill, P. J., Davidson, M. W. and Piston, D. W. (2011). Fluorescent proteins at a glance. J. Cell Sci. 124, 157-160.
52. Kuang, S., Kuroda, K., Le Grand, F. and Rudnicki, M. A. (2007). Asymmetric selfrenewal and commitment of satellite stem cells in muscle. Cell 129, 999-1010.
53. Kuehn, M. R., Bradley, A., Robertson, E. J. and Evans, M. J. (1987). A potential animal model for Lesch-Nyhan syndrome through introduction of HPRT mutations into mice. Nature 326, 295-298.
54. Landecker, H. (2006). Microcinematography and the History of Science and Film. Isis 97, 121-132.
55. Landecker, H. (2009). Seeing things: from microcinematography to live cell imaging. Nat. Methods 6, 707-709.
56. Lang, M., Rudolf, F. and Stelling, J. (2012). Use of YouScope to implement systematic microscopy protocols. Curr. Protoc. Mol. Biol. 98, 14.21.1-14.21.23.
57. Lecault, V., Vaninsberghe, M., Sekulovic, S., Knapp, D. J. H. F., Wohrer, S., Bowden, W., Viel, F., McLaughlin, T., Jarandehei, A., Miller, M. et al. (2011). High-throughput analysis of single hematopoietic stem cell proliferation in microfluidic cell culture arrays. Nat. Methods 8, 581-586.
58. Lichtman, J. W. and Conchello, J.-A. (2005). Fluorescence microscopy. Nat. Methods 2, 910-919.
59. Lin, C.-H., Lee, J. K. and LaBarge, M. A. (2012). Fabrication and use of microenvironment microarrays (MEArrays). J. Vis. Exp. 2012.
60. Lippincott-Schwartz, J. and Patterson, G. H. (2003). Development and use of fluorescent protein markers in living cells. Science 300, 87-91.
61. LoBiondo, J., Abramowitz, M. and Friedman, M. M. (2011). Microscope objectives. Curr. Protoc Cytom. 58, 2.2.1-2.2, 15.
62. Lutolf, M. P., Doyonnas, R., Havenstrite, K., Koleckar, K. and Blau, H. M. (2009a). Perturbation of single hematopoietic stem cell fates in artificial niches. Integr. Biol. (Camb) 1, 59-69.
63. Lutolf, M. P., Gilbert, P. M. and Blau, H. M. (2009b). Designing materials to direct stem-cell fate. Nature 462, 433-441.
64. Müller-Taubenberger, A. and Anderson, K. I. (2007). Recent advances using green and red fluorescent protein variants. Appl. Microbiol. Biotechnol. 77, 1-12.
65. Myers, G. (2012). Why bioimage informatics matters. Nat. Methods 9, 659-660.
66. Newman, R. H., Fosbrink, M. D. and Zhang, J. (2011). Genetically encodable fluorescent biosensors for tracking signaling dynamics in living cells. Chem. Rev. 111, 3614-3666.
67. Paddock, S. (2001). A brief history of time-lapse. Biotechniques 30, 283-286, 288- 289.
68. Pattison, D. I. and Davies, M. J. (2006). Actions of ultraviolet light on cellular structures. EXS 96, 131-157.
69. Piston, D. W. (1999). Imaging living cells and tissues by two-photon excitation microscopy. Trends Cell Biol. 9, 66-69.
70. Pizon, A. (1905). Une nouvelle application de la chronophotographie: la Biotachygraphie. In Comptes rendus des séances du sixie'me Congrés international de zoologie tenu a' Berne du 14 au 16 août 1904, pp. 404-409. Berne: W. Kundig & Fils.
71. Prasher, D. C., Eckenrode, V. K., Ward, W. W., Prendergast, F. G. and Cormier, M. J. (1992). Primary structure of the Aequorea victoria green-fluorescent protein. Gene 111, 229-233.
72. Ravin, R., Hoeppner, D. J., Munno, D. M., Carmel, L., Sullivan, J., Levitt, D. L., Miller, J. L., Athaide, C., Panchision, D. M. and McKay, R. D. G. (2008). Potency and fate specification in CNS stem cell populations in vitro. Cell Stem Cell 3, 670- 680.
73. Rieger, M. A., Hoppe, P. S., Smejkal, B. M., Eitelhuber, A. C. and Schroeder, T. (2009). Hematopoietic cytokines can instruct lineage choice. Science 325, 217-218.
74. Ries, J. (1909). Kinematographie der Befruchtung und Zellteilung. Archiv für Mikroskopishe Anatomie 74, 1-31.
75. Roux, P., Mü nter, S., Frischknecht, F., Herbomel, P. and Shorte, S. L. (2004). Focusing light on infection in four dimensions. Cell. Microbiol. 6, 333-343.
76. Salmon, W. C. and Waters, J. C. (2011). CCD cameras for fluorescence imaging of living cells. Cold Spring Harb. Protoc. 2011, pdb.top113.
77. Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B. et al. (2012). Fiji: an opensource platform for biological-image analysis. Nat. Methods 9, 676-682.
78. Schneider, C. A., Rasband, W. S. and Eliceiri, K. W. (2012). NIH Image to ImageJ: 25 years of image analysis. Nat. Methods 9, 671-675.
79. Schroeder, T. (2008). Imaging stem-cell-driven regeneration in mammals. Nature 453, 345-351.
80. Schroeder, T. (2011). Long-term single-cell imaging of mammalian stem cells. Nat. Methods 8 Suppl., S30-S35.
81. Shimomura, O., Johnson, F. H. and Saiga, Y. O. (1962). Extraction, purification and properties of aequorin, a bioluminescent protein from the luminous hydromedusan, Aequorea. J. Cell. Comp. Physiol. 59, 223-239.
82. Sluder, G., Nordberg, J. J., Miller, F. J. and Hinchcliffe, E. H. (2007). A sealed preparation for long-term observations of cultured cells. CSH Protoc. 2007, pdb.prot4660.
83. Stent, G. S. and Weisblat, D. A. (1985). Cell lineage in the development of invertebrate nervous systems. Annu. Rev. Neurosci. 8, 45-70.
84. Stephens, D. J. and Allan, V. J. (2003). Light microscopy techniques for live cell imaging. Science 300, 82-86.
85. Stern, C. D. and Fraser, S. E. (2001). Tracing the lineage of tracing cell lineages. Nat. Cell Biol. 3, E216-E218.
86. Sung, J. H., Zhang, H., Moseman, E. A., Alvarez, D., Iannacone, M., Henrickson, S. E., de la Torre, J. C., Groom, J. R., Luster, A. D. and Von Andrian, U. H. (2012). Chemokine guidance of central memory T cells is critical for antiviral recall responses in lymph nodes. Cell 150, 1249-1263.
87. Talbot, F. (1913). Practical Cinematography and its Applications. London: William Heinemann.
88. Tay, S., Hughey, J. J., Lee, T. K., Lipniacki, T., Quake, S. R. and Covert, M. W. (2010). Single-cell NF-kappaB dynamics reveal digital activation and analogue information processing. Nature 466, 267-271.
89. Taylor, R. J., Falconnet, D., Niemistö, A., Ramsey, S. A., Prinz, S., Shmulevich, I., Galitski, T. and Hansen, C. L. (2009). Dynamic analysis of MAPK signaling using a high-throughput microfluidic single-cell imaging platform. Proc. Natl. Acad. Sci. USA 106, 3758-3763.
90. Walter, T., Shattuck, D. W., Baldock, R., Bastin, M. E., Carpenter, A. E., Duce, S., Ellenberg, J., Fraser, A., Hamilton, N., Pieper, S. et al. (2010). Visualization of image data from cells to organisms. Nat. Methods 7 Suppl, S26-S41.
91. Whitman, C. O. (1878). The embryology of clepsine. Q. J. Microsc. Sci. s2-18, 215- 315.
92. Zhang, J., Campbell, R. E., Ting, A. Y. and Tsien, R. Y. (2002). Creating new fluorescent probes for cell biology. Nat. Rev. Mol. Cell Biol. 3, 906-918.