Abstract
The fashion today is to disparage technology-led research but our view is that cell biologists, in particular, should be proud of their 'progress through technology'. The 'cell theory' itself, arguably the oldest cornerstone in the theoretical foundations of biology, emerged because Hooke, van Leeuwenhoek and others had, more than a century earlier, pioneered the enabling technology — the microscope. We develop this theme with reference to our own field of research: the locomotion of cultured tissue cells.
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References
Inwood, S. The man who knew too much: the strange and inventive life of Robert Hooke 1635–1703 (Macmillan, London, UK, 2002).
Hooke, R. Micrographia: or some physiological descriptions of minute bodies made by magnifying glasses with observations and inquiries thereupon. (Printed by Jo. Martyn and Ja. Allestry, printers to the Royal Society, London, UK, 1665).
Ford, B. J. First steps in experimental microscopy, Leeuwenhoek as practical scientist. The Microscope 43, 47–57 (1995).
Schliwa, M. The evolving complexity of cytoplasmic structure. Nature Rev. Mol. Cell Biol. 3, 291–295 (2002).
Remak, R. Neurologische Erläuterungen. Arch. Anat. Physiol. wiss Med. 1844, 463–472 (1844).
Frixione, E. Sigmund Freud's contribution to the history of the neuronal cytoskeleton. J. Histor. Neurosci. 12, 12–24 (2003).
Tauber, A. I. Metchnikoff and the phagocytosis theory. Nature Rev. Mol. Cell Biol. 4, 897–901 (2003).
Abercrombie, M. Ross Granville Harrison 1870–1959. Biographical Memoirs of Fellows of The Royal Society 7, 111–126 (1961).
Harrison, R. G. Observations on the living developing nerve fiber. Anat. Rec. 1, 116–118 (1907).
Canti, R. G. Cinematograph demonstration of living tissue cells growing in vitro. Arch. Exper. Zellforsch. 6, 86–97 (1928).
Dunn, G. A. Transmitted-light interference microscopy: a technique born before its time. Proc. RMS 33, 189–196 (1998).
Zernike, F. How I discovered phase contrast. Science 121, 345–349 (1955).
Allen, R. D., David, G. B. & Nomarski, G. The Zeiss–Nomarski differential interference equipment for transmitted-light microscopy. Z. Wiss. Mikrosk. 69, 193–221 (1969).
Allen, R. D. & Kamiya, N. (eds) Primitive motile systems in cell biology. (Academic Press, New York & London, 1964).
Curtis, A. S. G. The adhesion of cells to glass: a study by interference reflection microscopy. J. Cell Biol. 19, 199–215 (1964).
Abercrombie, M. & Dunn, G. A. Adhesions of fibroblasts to substratum during contact inhibition observed by interference reflection microscopy. Exp. Cell Res. 92, 57–62 (1975).
Izzard, C. S. & Lochner, L. R. Cell-to-substrate contacts in living fibroblasts: an interference reflexion study with an evaluation of the technique. J. Cell Sci. 21, 129–159 (1976).
Lazarides, E. & Weber, K. Actin antibody: the specific visualization of actin filaments in non-muscle cells. Proc. Natl Acad. Sci. USA 71, 2268–2272 (1974).
Ploem, J. S. A study of filters and light sources in immunofluorescence microscopy. Ann. NY Acad. Sci. 177, 414–429 (1971).
Taylor, D. L. & Wang, Y. Molecular cytochemistry: incorporation of fluorescently labeled actin into living cells. Proc. Natl Acad. Sci. USA 75, 857–861 (1978).
Allen, R. D., Allen, N. S. & Travis, J. L. Video-enhanced contrast, differential interference contrast (AVEC-DIC) microscopy: a new method capable of analyzing microtubule-related motility in the reticulopodial network of Allogromia laticollaris. Cell Motil. 1, 291–302 (1981).
Inoué, S. Video Microscopy (Plenum Press, New York, USA, 1986).
Minsky, M. Memoir on inventing the confocal scanning microscope. Scanning 10, 128–138 (1988).
Amos, W. B. & White, J. G. How the confocal laser scanning microscope entered biological research. Biol. Cell 95, 335–342 (2003).
Prasher, D. C., Eckenrode, V. K., Ward, W. W., Prendergast, F. G. & Cormier, M. J. Primary structure of the Aequorea victoria green-fluorescent protein. Gene 111, 229–233 (1992).
Pelham, R. J. Jr & Wang, Y. High resolution detection of mechanical forces exerted by locomoting fibroblasts on the substrate. Mol. Biol. Cell 10, 935–945 (1999).
Galbraith, C. G., Yamada, K. M. & Sheetz, M. P. The relationship between force and focal complex development. J. Cell Biol. 159, 695–705 (2002).
Zicha, D., Dunn, G. A. & Brown, A. F. A new direct-viewing chemotaxis chamber. J. Cell Sci. 99, 769–775 (1991).
Allen, W. E., Jones, G. E., Pollard, J. & Ridley, A. J. Rho, Rac and Cdc42 regulate actin organisation and cell adhesion in macrophages. J. Cell Sci. 110, 707–720 (1997).
Allen, W. E., Zicha, D., Ridley, A. J. & Jones, G. E. A role for Cdc42 in macrophage chemotaxis. J. Cell Biol. 141, 1147–1157 (1998).
Etienne-Manneville, S. & Hall, A. Rho GTPases in cell biology. Nature 420, 629–635 (2002).
Pollard, T. D., Blanchoin, L. & Mullins, R. D. Molecular mechanisms controlling actin filament dynamics in nonmuscle cells. Annu. Rev. Biophys. Biomol. Struct. 29, 545–576 (2000).
Axelrod, D., Koppel, D. E., Schlessinger, J., Elson, E. & Webb, W. W. Mobility measurement by analysis of fluorescence photobleaching recovery kinetics. Biophys. J. 16, 1055–1069 (1976).
Reits, E. A. & Neefjes, J. J. From fixed to FRAP: measuring protein mobility and activity in living cells. Nature Cell Biol. 3, 145–147 (2001).
Mitchison, T. J., Sawin, K. E., Theriot, J. A., Gee, K. & Mallavarapu, A. Caged fluorescent probes. Methods Enzymol. 291, 63–78 (1998).
Patterson, G. H. & Lippincott-Schwartz J. A photoactivatable GFP for selective photolabeling of proteins and cells. Science 297, 1873–1877 (2002).
Dunn, G. A., Dobbie, I. M., Monypenny J., Holt, M. R. & Zicha, D. Fluorescence localization after photobleaching (FLAP): a new method for studying protein dynamics in living cells. J. Microsc. 205, 109–112 (2002).
Zicha, D. et al. Rapid actin transport during cell protrusion. Science 300, 142–145 (2003).
Waterman-Storer, C. M. & Salmon, E. D. Actomyosin-based retrograde flow of microtubules in the lamella of migrating epithelial cells influences microtubule dynamic instability and turnover and is associated with microtubule breakage and treadmilling. J. Cell Biol. 139, 417–434 (1997).
Watanabe, N. & Mitchison, T. J. Single-molecule speckle analysis of actin filament turnover in lamellipodia. Science 295, 1083–1086 (2002).
Miki, M., O'Donoghue, S. I. & dos Remedios, C. G. Structure of actin observed by fluorescence resonance energy transfer spectroscopy. J. Muscle Res. Cell Motil. 13, 132–145 (1992).
Lanni, F., Waggoner, A. S. & Taylor, D. L. Structural organization of interphase 3T3 fibroblasts studied by total internal reflection fluorescence microscopy. J. Cell Biol. 100, 1091–1102 (1985).
Schwille, P., Haupts, U., Maiti, S. & Webb, W. W. Molecular dynamics in living cells observed by fluorescence correlation spectroscopy with one- and two-photon excitation. Biophys. J. 77, 2251–2265 (1999).
Zipfel, W. R., Williams, R. M. & Webb, W. W. Nonlinear magic: multiphoton microscopy in the biosciences. Nature Biotechnol. 21, 1369–1377 (2003).
Condeelis, J. & Segall J. E. Intravital imaging of cell movement in tumours. Nature Rev. Cancer 12, 921–930 (2003).
Dickinson, M. E., Murray, B. A., Haynes, S. M., Waters, C. W. & Longmuir K. J. Using electroporation and lipid-mediated transfection of GFP-expressing plasmids to label embryonic avian cells for vital confocal and two-photon microscopy. Differentiation 5, 172–180 (2002).
Bastiaens, P. I. & Pepperkok, R. Observing proteins in their natural habitat: the living cell. Trends Biochem. Sci. 25, 631–637 (2000).
Metchnikoff, E. Lectures on the Comparative Pathology of Inflammation. (Reprinted by Dover, New York, 1968). (Translated by F. A. Starling and E. H. Starling.)
Schwann, T. A. H. Mikroskopische Untersuchungen über die Übereinstimmung in der Struktur und dem Wachsthum der Thiere und Pflanzen (Sander, Berlin, Germany, 1839).
Coons, A. H. & Kaplan, M. H. Localization of antigens in tissue cells. Improvements in a method for the detection of antigen by means of fluorescent antibody. J. Exp. Med. 91, 1–13 (1950).
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Work in our laboratory is funded by the Medical Research Council and the Wellcome Trust.
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Dunn, G., Jones, G. Cell motility under the microscope: Vorsprung durch Technik. Nat Rev Mol Cell Biol 5, 667–672 (2004). https://doi.org/10.1038/nrm1439
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DOI: https://doi.org/10.1038/nrm1439
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