Fluorescent Methods to Study Biological Membranes pp 367-388 | Cite as
Unveiling Biophysical and Biological Properties of a Hypothetical Membrane Receptor by Exploiting Recent Imaging Advances
Abstract
Fluorescence microscopy is indispensable in the study of biological systems at various length scales. This rapidly evolving field continues to offer researchers cutting-edge techniques that enhance spatial and temporal resolution, especially with the invention of superresolution methodologies. In this chapter, we focus on techniques that have aided in the understanding of various cell biological phenomena. Each technique has certain boundaries of spatial and temporal resolution, and fluorophore density in a particular biological sample may limit the applicability of some techniques. We discuss strengths and weaknesses of many such techniques by considering their use in understanding the biological function of a hypothetical membrane receptor. We conclude that a combination of techniques is required to fully understand any cell biological process.
Keywords
Fluorescence Light microscopy Molecular Interactions Spectroscopy Superresolution microscopyNotes
Acknowledgments
We would like to thank Steve Vogel for valuable discussions and Travis Crites for critical reading of the manuscript.
References
- 1.Conchello JA, Lichtman JW (2005) Optical sectioning microscopy. Nat Methods 2(12):920–931. doi: 10.1038/nmeth815 CrossRefGoogle Scholar
- 2.Sanderson MJ, Parker I (2003) Video-rate confocal microscopy. Methods Enzymol 360:447–481. doi: 10.1016/S0076-6879(03)60123-0 CrossRefGoogle Scholar
- 3.Botcherby EJ, Booth MJ, Juskaitis R, Wilson T (2009) Real-time slit scanning microscopy in the meridional plane. Opt Lett 34(10):1504–1506. doi: 10.1364/OL.34.001504 CrossRefGoogle Scholar
- 4.Toomre D, Pawley JB (2006) Disk-scanning confocal microscopy, vol chapter 10. In: Handbook of biological confocal microscopy. Springer, US. doi: 10.1007/978-0-387-45524-2_10
- 5.Wilson T (2010) Spinning-disk microscopy systems. Cold Spring Harb Protoc 2010 (11):pdb top88. doi: 10.1101/pdb.top88
- 6.Ichihara A, Tanaami T, Isozaki K, Sugiyama Y, Kosugi Y, Mikuriya K, Abe M, Uemura I (1996) High-speed confocal fluorescence microscopy using a nipkow scanner with microlenses - for 3-d imaging of fluorescent molecule in real-time. Bioimages 4:57–62Google Scholar
- 7.Stehbens S, Pemble H, Murrow L, Wittmann T (2012) Imaging intracellular protein dynamics by spinning disk confocal microscopy. Methods Enzymol 504:293–313. doi: 10.1016/B978-0-12-391857-4.00015-X CrossRefGoogle Scholar
- 8.Nakano A (2002) Spinning-disk confocal microscopy – a cutting-edge tool for imaging of membrane traffic. Cell Struct Funct 27(5):349–355. doi: 10.1247/csf.27.349 CrossRefGoogle Scholar
- 9.Wang E, Babbey CM, Dunn KW (2005) Performance comparison between the high-speed yokogawa spinning disc confocal system and single-point scanning confocal systems. J Microsc 218(Pt 2):148–159. doi: 10.1111/j.1365-2818.2005.01473.x CrossRefGoogle Scholar
- 10.Fischer RS, Wu Y, Kanchanawong P, Shroff H, Waterman CM (2011) Microscopy in 3d: a biologist's toolbox. Trends Cell Biol 21(12):682–691. doi: 10.1016/j.tcb.2011.09.008 CrossRefGoogle Scholar
- 11.Carrizosa E, Gomez TS, Labno CM, Klos Dehring DA, Liu X, Freedman BD, Billadeau DD, Burkhardt JK (2009) Hematopoietic lineage cell-specific protein 1 is recruited to the immunological synapse by il-2-inducible t cell kinase and regulates phospholipase cgamma1 microcluster dynamics during t cell spreading. J Immunol 183(11):7352–7361. doi: 10.4049/jimmunol.0900973 CrossRefGoogle Scholar
- 12.Mattheyses AL, Simon SM, Rappoport JZ (2010) Imaging with total internal reflection fluorescence microscopy for the cell biologist. J Cell Sci 123(Pt 21):3621–3628. doi: 10.1242/jcs.056218 CrossRefGoogle Scholar
- 13.Axelrod D (2008) Chapter 7: Total internal reflection fluorescence microscopy. Methods Cell Biol 89:169–221. doi: 10.1016/S0091-679X(08)00607-9 CrossRefGoogle Scholar
- 14.Ezratty EJ, Bertaux C, Marcantonio EE, Gundersen GG (2009) Clathrin mediates integrin endocytosis for focal adhesion disassembly in migrating cells. J Cell Biol 187(5):733–747. doi: 10.1083/jcb.200904054 CrossRefGoogle Scholar
- 15.Puthenveedu MA, von Zastrow M (2006) Cargo regulates clathrin-coated pit dynamics. Cell 127(1):113–124. doi: 10.1016/j.cell.2006.08.035 CrossRefGoogle Scholar
- 16.Merrifield CJ, Feldman ME, Wan L, Almers W (2002) Imaging actin and dynamin recruitment during invagination of single clathrin-coated pits. Nat Cell Biol 4(9):691–698. doi: 10.1038/ncb837 CrossRefGoogle Scholar
- 17.Rappoport JZ, Simon SM, Benmerah A (2004) Understanding living clathrin-coated pits. Traffic 5(5):327–337. doi: 10.1111/j.1600-0854.2004.00187.x CrossRefGoogle Scholar
- 18.Leonard D, Hayakawa A, Lawe D, Lambright D, Bellve KD, Standley C, Lifshitz LM, Fogarty KE, Corvera S (2008) Sorting of egf and transferrin at the plasma membrane and by cargo-specific signaling to eea1-enriched endosomes. J Cell Sci 121(Pt 20):3445–3458. doi: 10.1242/jcs.031484 CrossRefGoogle Scholar
- 19.Tokunaga M, Imamoto N, Sakata-Sogawa K (2008) Highly inclined thin illumination enables clear single-molecule imaging in cells. Nat Methods 5(2):159–161. doi: 10.1038/nmeth1171 CrossRefGoogle Scholar
- 20.Campi G, Varma R, Dustin ML (2005) Actin and agonist mhc-peptide complex-dependent t cell receptor microclusters as scaffolds for signaling. J Exp Med 202(8):1031–1036. doi: 10.1084/jem.20051182 CrossRefGoogle Scholar
- 21.Carrasco YR, Fleire SJ, Cameron T, Dustin ML, Batista FD (2004) Lfa-1/icam-1 interaction lowers the threshold of b cell activation by facilitating b cell adhesion and synapse formation. Immunity 20(5):589–599. doi: 10.1016/S1074-7613(04)00105-0 CrossRefGoogle Scholar
- 22.Reck-Peterson SL, Yildiz A, Carter AP, Gennerich A, Zhang N, Vale RD (2006) Single-molecule analysis of dynein processivity and stepping behavior. Cell 126(2):335–348. doi: 10.1016/j.cell.2006.05.046 CrossRefGoogle Scholar
- 23.Murase K, Fujiwara T, Umemura Y, Suzuki K, Iino R, Yamashita H, Saito M, Murakoshi H, Ritchie K, Kusumi A (2004) Ultrafine membrane compartments for molecular diffusion as revealed by single molecule techniques. Biophys J 86(6):4075–4093. doi: 10.1529/biophysj.103.035717 CrossRefGoogle Scholar
- 24.Umemura YM, Vrljic M, Nishimura SY, Fujiwara TK, Suzuki KG, Kusumi A (2008) Both mhc class II and its gpi-anchored form undergo hop diffusion as observed by single-molecule tracking. Biophys J 95(1):435–450. doi: 10.1529/biophysj.107.123018 CrossRefGoogle Scholar
- 25.Reck-Peterson SL, Derr ND, Stuurman N (2010) Imaging single molecules using total internal reflection fluorescence microscopy (tirfm). Cold Spring Harb Protoc 2010 (3):pdb top73. doi: 10.1101/pdb.top73
- 26.Douglass AD, Vale RD (2005) Single-molecule microscopy reveals plasma membrane microdomains created by protein-protein networks that exclude or trap signaling molecules in t cells. Cell 121(6):937–950. doi: 10.1016/j.cell.2005.04.009 CrossRefGoogle Scholar
- 27.Dustin ML, Depoil D (2011) New insights into the t cell synapse from single molecule techniques. Nat Rev Immunol 11(10):672–684. doi: 10.1038/nri3066 CrossRefGoogle Scholar
- 28.Maiti S, Haupts U, Webb WW (1997) Fluorescence correlation spectroscopy: diagnostics for sparse molecules. Proc Natl Acad Sci USA 94(22):11753–11757. doi: 10.1073/pnas.94.22.11753 CrossRefGoogle Scholar
- 29.Chiantia S, Ries J, Schwille P (2009) Fluorescence correlation spectroscopy in membrane structure elucidation. Biochim Biophys Acta 1788(1):225–233. doi: 10.1016/j.bbamem.2008.08.013 CrossRefGoogle Scholar
- 30.Garcia-Saez AJ, Schwille P (2007) Single molecule techniques for the study of membrane proteins. Appl Microbiol Biotechnol 76(2):257–266. doi: 10.1007/s00253-007-1007-8 CrossRefGoogle Scholar
- 31.Sengupta P, Balaji J, Maiti S (2002) Measuring diffusion in cell membranes by fluorescence correlation spectroscopy. Methods 27(4):374–387. doi: 10.1016/S1046-2023(02)00096-8 CrossRefGoogle Scholar
- 32.Bacia K, Schwille P (2007) Practical guidelines for dual-color fluorescence cross-correlation spectroscopy. Nat Protoc 2(11):2842–2856. doi: 10.1038/nprot.2007.410 CrossRefGoogle Scholar
- 33.Rarbach M, Kettling U, Koltermann A, Eigen M (2001) Dual-color fluorescence cross-correlation spectroscopy for monitoring the kinetics of enzyme-catalyzed reactions. Methods 24(2):104–116. doi: 10.1006/meth.2001.1172 CrossRefGoogle Scholar
- 34.Kolin DL, Ronis D, Wiseman PW (2006) K-space image correlation spectroscopy: a method for accurate transport measurements independent of fluorophore photophysics. Biophys J 91(8):3061–3075. doi: 10.1529/biophysj.106.082768 CrossRefGoogle Scholar
- 35.Gustafsson MG (2000) Surpassing the lateral resolution limit by a factor of two using structured illumination microscopy. J Microsc 198(Pt 2):82–87. doi: 10.1046/j.1365-2818.2000.00710.x CrossRefGoogle Scholar
- 36.Gustafsson MG, Shao L, Carlton PM, Wang CJ, Golubovskaya IN, Cande WZ, Agard DA, Sedat JW (2008) Three-dimensional resolution doubling in wide-field fluorescence microscopy by structured illumination. Biophys J 94(12):4957–4970. doi: 10.1529/biophysj.107.120345 CrossRefGoogle Scholar
- 37.Elia N, Sougrat R, Spurlin TA, Hurley JH, Lippincott-Schwartz J (2011) Dynamics of endosomal sorting complex required for transport (escrt) machinery during cytokinesis and its role in abscission. Proc Natl Acad Sci USA 108(12):4846–4851. doi: 10.1073/pnas.1102714108 CrossRefGoogle Scholar
- 38.Guizetti J, Schermelleh L, Mantler J, Maar S, Poser I, Leonhardt H, Muller-Reichert T, Gerlich DW (2011) Cortical constriction during abscission involves helices of escrt-III-dependent filaments. Science 331(6024):1616–1620. doi: 10.1126/science.1201847 CrossRefGoogle Scholar
- 39.Mattila PK, Lappalainen P (2008) Filopodia: molecular architecture and cellular functions. Nat Rev Mol Cell Biol 9(6):446–454. doi: 10.1038/nrm2406 CrossRefGoogle Scholar
- 40.Toomre D, Bewersdorf J (2010) A new wave of cellular imaging. Annu Rev Cell Dev Biol 26:285–314. doi: 10.1146/annurev-cellbio-100109-104048 CrossRefGoogle Scholar
- 41.Hell SW, Wichmann J (1994) Breaking the diffraction resolution limit by stimulated emission: stimulated-emission-depletion fluorescence microscopy. Opt Lett 19(11):780–782. doi: 10.1364/OL.19.000780 CrossRefGoogle Scholar
- 42.Klar TA, Jakobs S, Dyba M, Egner A, Hell SW (2000) Fluorescence microscopy with diffraction resolution barrier broken by stimulated emission. Proc Natl Acad Sci USA 97(15):8206–8210. doi: 10.1073/pnas.97.15.8206 CrossRefGoogle Scholar
- 43.Hell SW (2009) Microscopy and its focal switch. Nat Methods 6(1):24–32. doi: 10.1038/nmeth.1291 CrossRefGoogle Scholar
- 44.Eggeling C, Ringemann C, Medda R, Schwarzmann G, Sandhoff K, Polyakova S, Belov VN, Hein B, von Middendorff C, Schonle A, Hell SW (2009) Direct observation of the nanoscale dynamics of membrane lipids in a living cell. Nature 457(7233):1159–1162. doi: 10.1038/nature07596 CrossRefGoogle Scholar
- 45.Sieber JJ, Willig KI, Kutzner C, Gerding-Reimers C, Harke B, Donnert G, Rammner B, Eggeling C, Hell SW, Grubmuller H, Lang T (2007) Anatomy and dynamics of a supramolecular membrane protein cluster. Science 317(5841):1072–1076. doi: 10.1126/science.1141727 CrossRefGoogle Scholar
- 46.Neumann D, Buckers J, Kastrup L, Hell SW, Jakobs S (2010) Two-color sted microscopy reveals different degrees of colocalization between hexokinase-i and the three human vdac isoforms. PMC Biophys 3(1):4. doi: 10.1186/1757-5036-3-4 CrossRefGoogle Scholar
- 47.Berning S, Willig KI, Steffens H, Dibaj P, Hell SW (2012) Nanoscopy in a living mouse brain. Science 335(6068):551. doi: 10.1126/science.1215369 CrossRefGoogle Scholar
- 48.Tonnesen J, Nadrigny F, Willig KI, Wedlich-Soldner R, Nagerl UV (2011) Two-color sted microscopy of living synapses using a single laser-beam pair. Biophys J 101(10):2545–2552. doi: 10.1016/j.bpj.2011.10.011 CrossRefGoogle Scholar
- 49.Urban NT, Willig KI, Hell SW, Nagerl UV (2011) Sted nanoscopy of actin dynamics in synapses deep inside living brain slices. Biophys J 101(5):1277–1284. doi: 10.1016/j.bpj.2011.07.027 CrossRefGoogle Scholar
- 50.Westphal V, Rizzoli SO, Lauterbach MA, Kamin D, Jahn R, Hell SW (2008) Video-rate far-field optical nanoscopy dissects synaptic vesicle movement. Science 320(5873):246–249. doi: 10.1126/science.1154228 CrossRefGoogle Scholar
- 51.Lee CJ, Boller KJ (2012) The noise-limited-resolution for stimulated emission depletion microscopy of diffusing particles. Opt Express 20(12):12793–12798. doi: 10.1364/OE.20.012793 CrossRefGoogle Scholar
- 52.Bates M, Huang B, Zhuang X (2008) Super-resolution microscopy by nanoscale localization of photo-switchable fluorescent probes. Curr Opin Chem Biol 12(5):505–514. doi: 10.1016/j.cbpa.2008.08.008 CrossRefGoogle Scholar
- 53.Betzig E, Patterson GH, Sougrat R, Lindwasser OW, Olenych S, Bonifacino JS, Davidson MW, Lippincott-Schwartz J, Hess HF (2006) Imaging intracellular fluorescent proteins at nanometer resolution. Science 313(5793):1642–1645. doi: 10.1126/science.1127344 CrossRefGoogle Scholar
- 54.Aitken CE, Marshall RA, Puglisi JD (2008) An oxygen scavenging system for improvement of dye stability in single-molecule fluorescence experiments. Biophys J 94(5):1826–1835. doi: 10.1529/biophysj.107.117689 CrossRefGoogle Scholar
- 55.Bates M, Blosser TR, Zhuang X (2005) Short-range spectroscopic ruler based on a single-molecule optical switch. Phys Rev Lett 94(10):108101CrossRefGoogle Scholar
- 56.Rust MJ, Bates M, Zhuang X (2006) Sub-diffraction-limit imaging by stochastic optical reconstruction microscopy (storm). Nat Methods 3(10):793–795. doi: 10.1038/nmeth929 CrossRefGoogle Scholar
- 57.Wiedenmann J, Gayda S, Adam V, Oswald F, Nienhaus K, Bourgeois D, Nienhaus GU (2011) From eosfp to mirisfp: structure-based development of advanced photoactivatable marker proteins of the gfp-family. J Biophotonics 4(6):377–390. doi: 10.1002/jbio.201000122 CrossRefGoogle Scholar
- 58.Lippincott-Schwartz J, Patterson GH (2009) Photoactivatable fluorescent proteins for diffraction-limited and super-resolution imaging. Trends Cell Biol 19(11):555–565. doi: 10.1016/j.tcb.2009.09.003 CrossRefGoogle Scholar
- 59.Brakemann T, Stiel AC, Weber G, Andresen M, Testa I, Grotjohann T, Leutenegger M, Plessmann U, Urlaub H, Eggeling C, Wahl MC, Hell SW, Jakobs S (2011) A reversibly photoswitchable gfp-like protein with fluorescence excitation decoupled from switching. Nat Biotechnol 29(10):942–947. doi: 10.1038/nbt.1952 CrossRefGoogle Scholar
- 60.Gould TJ, Verkhusha VV, Hess ST (2009) Imaging biological structures with fluorescence photoactivation localization microscopy. Nat Protoc 4(3):291–308. doi: 10.1038/nprot.2008.246 CrossRefGoogle Scholar
- 61.Shroff H, Galbraith CG, Galbraith JA, Betzig E (2008) Live-cell photoactivated localization microscopy of nanoscale adhesion dynamics. Nat Methods 5(5):417–423. doi: 10.1038/nmeth.1202 CrossRefGoogle Scholar
- 62.Wu M, Huang B, Graham M, Raimondi A, Heuser JE, Zhuang X, De Camilli P (2010) Coupling between clathrin-dependent endocytic budding and f-bar-dependent tubulation in a cell-free system. Nat Cell Biol 12(9):902–908. doi: 10.1038/ncb2094 CrossRefGoogle Scholar
- 63.Lillemeier BF, Mortelmaier MA, Forstner MB, Huppa JB, Groves JT, Davis MM (2010) Tcr and lat are expressed on separate protein islands on t cell membranes and concatenate during activation. Nat Immunol 11(1):90–96. doi: 10.1038/ni.1832 CrossRefGoogle Scholar
- 64.Williamson DJ, Owen DM, Rossy J, Magenau A, Wehrmann M, Gooding JJ, Gaus K (2011) Pre-existing clusters of the adaptor lat do not participate in early t cell signaling events. Nat Immunol 12(7):655–662. doi: 10.1038/ni.2049 CrossRefGoogle Scholar
- 65.Sherman E, Barr V, Manley S, Patterson G, Balagopalan L, Akpan I, Regan CK, Merrill RK, Sommers CL, Lippincott-Schwartz J, Samelson LE (2011) Functional nanoscale organization of signaling molecules downstream of the t cell antigen receptor. Immunity 35(5):705–720. doi: 10.1016/j.immuni.2011.10.004 CrossRefGoogle Scholar
- 66.Dani A, Huang B, Bergan J, Dulac C, Zhuang X (2010) Superresolution imaging of chemical synapses in the brain. Neuron 68(5):843–856. doi: 10.1016/j.neuron.2010.11.021 CrossRefGoogle Scholar
- 67.Juette MF, Gould TJ, Lessard MD, Mlodzianoski MJ, Nagpure BS, Bennett BT, Hess ST, Bewersdorf J (2008) Three-dimensional sub-100 nm resolution fluorescence microscopy of thick samples. Nat Methods 5(6):527–529. doi: 10.1038/nmeth.1211 CrossRefGoogle Scholar
- 68.Huang B, Wang W, Bates M, Zhuang X (2008) Three-dimensional super-resolution imaging by stochastic optical reconstruction microscopy. Science 319(5864):810–813. doi: 10.1126/science.1153529 CrossRefGoogle Scholar
- 69.Jares-Erijman EA, Jovin TM (2006) Imaging molecular interactions in living cells by fret microscopy. Curr Opin Chem Biol 10(5):409–416. doi: 10.1016/j.cbpa.2006.08.021 CrossRefGoogle Scholar
- 70.Ghosh S, Saha S, Goswami D, Bilgrami S, Mayor S (2012) Dynamic imaging of homo-fret in live cells by fluorescence anisotropy microscopy. Methods Enzymol 505:291–327. doi: 10.1016/B978-0-12-388448-0.00024-3 CrossRefGoogle Scholar
- 71.Vogel SS, Thaler C, Blank PS, Koushik S (2009) Time resolved fluorescence anisotropy vol chapter 10. In: Flim microscopy in biology and medicine. CRC Press Taylor & Francis Group, LondonGoogle Scholar
- 72.Sharma P, Varma R, Sarasij RC, Ira GK, Krishnamoorthy G, Rao M, Mayor S (2004) Nanoscale organization of multiple gpi-anchored proteins in living cell membranes. Cell 116(4):577–589. doi: 10.1016/S0092-8674(04)00167-9 CrossRefGoogle Scholar
- 73.Sun Y, Hays NM, Periasamy A, Davidson MW, Day RN (2012) Monitoring protein interactions in living cells with fluorescence lifetime imaging microscopy. Methods Enzymol 504:371–391. doi: 10.1016/B978-0-12-391857-4.00019-7 CrossRefGoogle Scholar
- 74.Rosso L, Fernicola VC (2006) Time- and frequency- domain analyses of fluorescnece lifetime for temperature sensing. Rev Scientific Instrumentation 77:034901. doi: 10.1063/1.2176085 CrossRefGoogle Scholar
- 75.Stockl MT, Herrmann A (2010) Detection of lipid domains in model and cell membranes by fluorescence lifetime imaging microscopy. Biochim Biophys Acta 1798(7):1444–1456. doi: 10.1016/j.bbamem.2009.12.015 CrossRefGoogle Scholar
- 76.Duncan RR, Bergmann A, Cousin MA, Apps DK, Shipston MJ (2004) Multi-dimensional time-correlated single photon counting (tcspc) fluorescence lifetime imaging microscopy (flim) to detect fret in cells. J Microsc 215(Pt 1):1–12. doi: 10.1111/j.0022-2720.2004.01343.x CrossRefGoogle Scholar
- 77.Wallrabe H, Periasamy A (2005) Imaging protein molecules using fret and flim microscopy. Curr Opin Biotechnol 16(1):19–27. doi: 10.1016/j.copbio.2004.12.002 CrossRefGoogle Scholar
- 78.Nguyen TA, Sarkar P, Veetil JV, Koushik SV, Vogel SS (2012) Fluorescence polarization and fluctuation analysis monitors subunit proximity, stoichiometry, and protein complex hydrodynamics. PLoS One 7(5):e38209. doi: 10.1371/journal.pone.0038209 CrossRefGoogle Scholar
- 79.Koushik SV, Vogel SS (2008) Energy migration alters the fluorescence lifetime of cerulean: implications for fluorescence lifetime imaging forster resonance energy transfer measurements. J Biomedical Optics 13(3):031204. doi: 10.1117/1.2940367 CrossRefGoogle Scholar
- 80.Luchowski R, Matveeva EG, Gryczynski I, Terpetschnig EA, Patsenker L, Laczko G, Borejdo J, Gryczynski Z (2008) Single molecule studies of multiple-fluorophore labeled antibodies. Effect of homo-fret on the number of photons available before photobleaching. Curr Pharmaceutical Biotechnol 9(5):411–420CrossRefGoogle Scholar
- 81.Storez H, Scott MG, Issafras H, Burtey A, Benmerah A, Muntaner O, Piolot T, Tramier M, Coppey-Moisan M, Bouvier M, Labbe-Jullie C, Marullo S (2005) Homo- and hetero-oligomerization of beta-arrestins in living cells. J Biol Chem 280(48):40210–40215. doi: 10.1074/jbc.M508001200 CrossRefGoogle Scholar
- 82.Abankwa D, Gorfe AA, Inder K, Hancock JF (2010) Ras membrane orientation and nanodomain localization generate isoform diversity. Proc Natl Acad Sci USA 107(3):1130–1135. doi: 10.1073/pnas.0903907107 CrossRefGoogle Scholar
- 83.Treanor B, Lanigan PM, Kumar S, Dunsby C, Munro I, Auksorius E, Culley FJ, Purbhoo MA, Phillips D, Neil MA, Burshtyn DN, French PM, Davis DM (2006) Microclusters of inhibitory killer immunoglobulin-like receptor signaling at natural killer cell immunological synapses. J Cell Biol 174(1):153–161. doi: 10.1083/jcb.200601108 CrossRefGoogle Scholar
- 84.Keller PJ, Stelzer EH (2010) Digital scanned laser light sheet fluorescence microscopy. Cold Spring Harb Protoc (5):pdb top78. doi: 10.1101/pdb.top78
- 85.Tomer R, Khairy K, Keller PJ (2011) Shedding light on the system: studying embryonic development with light sheet microscopy. Curr Opin Genet Dev 21(5):558–565. doi: 10.1016/j.gde.2011.07.003 CrossRefGoogle Scholar
- 86.Planchon TA, Gao L, Milkie DE, Davidson MW, Galbraith JA, Galbraith CG, Betzig E (2011) Rapid three-dimensional isotropic imaging of living cells using Bessel beam plane illumination. Nat Methods 8(5):417–423. doi: 10.1038/nmeth.1586 CrossRefGoogle Scholar
- 87.Fahrbach FO, Rohrbach A (2012) Propagation stability of self-reconstructing bessel beams enables contrast-enhanced imaging in thick media. Nat Commun 3:632. doi: 10.1038/ncomms1646 CrossRefGoogle Scholar
- 88.Holekamp TF, Turaga D, Holy TE (2008) Fast three-dimensional fluorescence imaging of activity in neural populations by objective-coupled planar illumination microscopy. Neuron 57(5):661–672. doi: 10.1016/j.neuron.2008.01.011 CrossRefGoogle Scholar
- 89.Shtengel G, Galbraith JA, Galbraith CG, Lippincott-Schwartz J, Gillette JM, Manley S, Sougrat R, Waterman CM, Kanchanawong P, Davidson MW, Fetter RD, Hess HF (2009) Interferometric fluorescent super-resolution microscopy resolves 3d cellular ultrastructure. Proc Natl Acad Sci USA 106(9):3125–3130. doi: 10.1073/pnas.0813131106 CrossRefGoogle Scholar
- 90.Kanchanawong P, Shtengel G, Pasapera AM, Ramko EB, Davidson MW, Hess HF, Waterman CM (2010) Nanoscale architecture of integrin-based cell adhesions. Nature 468(7323):580–584. doi: 10.1038/nature09621 CrossRefGoogle Scholar