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Cell and Tissue Research

, Volume 360, Issue 1, pp 129–141 | Cite as

Light sheet-based fluorescence microscopy (LSFM) for the quantitative imaging of cells and tissues

  • Francesco PampaloniEmail author
  • Bo-Jui Chang
  • Ernst H. K. Stelzer
Review

Abstract

In light sheet-based fluorescence microscopy (LSFM), only the focal plane is illuminated by a laser light sheet. Hence, only the fluorophores within a thin volume of the specimen are excited. This reduces photo-bleaching and photo-toxic effects by several orders of magnitude compared with any other form of microscopy. Therefore, LSFM (aka single/selective-plane illumination microscopy [SPIM] or digitally scanned light sheet microscopy [DSLM]) is the technique of choice for the three-dimensional imaging of live or fixed and of small or large three-dimensional specimens. The parallel recording of millions of pixels with modern cameras provides an extremely fast acquisition speed. Recent developments address the penetration depth, the resolution and the recording speed of LSFM. The impact of LSFM on research areas such as three-dimensional cell cultures, neurosciences, plant biology and developmental biology is increasing at a rapid pace. The development of high-throughput LSFM is the next leap forward, allowing the application of LSFM in toxicology and drug discovery screening.

Keywords

Light sheet-based fluorescence microscopy (LSFM) Digitally scanned light sheet-based microscopy Single/selective-plane illumination microscopy Three-dimensional cell cultures Cellular spheroids High-throughput LSFM 

Notes

Acknowledgments

We thank Nariman Ansari for many discussions on 3D cell culture, Daniel von Wangenheim for the comments on LSFM applications in plant research and Christian Mattheyer for his contribution to optical clearing.

References

  1. Ahrens MB, Orger MB, Robson DN, Li JM, Keller PJ (2013) Whole-brain functional imaging at cellular resolution using light-sheet microscopy. Nat Methods 10:413–420. doi: 10.1038/nmeth.2434 PubMedGoogle Scholar
  2. Barman I, Tan KM, Singh GP (2010) Optical sectioning using single-plane-illumination Raman imaging. J Raman Spectrosc 41:1099–1101. doi: 10.1002/jrs.2785 Google Scholar
  3. Baumgart E, Kubitscheck U (2012) Scanned light sheet microscopy with confocal slit detection. Opt Express 20:21805–21814. doi: 10.1364/OE.20.021805 PubMedGoogle Scholar
  4. Breuninger T, Greger K, Stelzer EHK (2007) Lateral modulation boosts image quality in single plane illumination fluorescence microscopy. Opt Lett 32:1938. doi: 10.1364/OL.32.001938 PubMedGoogle Scholar
  5. Brito C, Simão D, Costa I, Malpique R, Pereira CI, Fernandes P, Alves PM (2012) 3D cultures of human neural progenitor cells: dopaminergic differentiation and genetic modification. [corrected]. Methods 56:452–460. doi: 10.1016/j.ymeth.2012.03.005 PubMedGoogle Scholar
  6. Bruns T, Schickinger S, Wittig R, Schneckenburger H (2012) Preparation strategy and illumination of three-dimensional cell cultures in light sheet-based fluorescence microscopy. J Biomed Opt 17:101518. doi: 10.1117/1.JBO.17.10.101518 PubMedGoogle Scholar
  7. Bruns T, Schickinger S, Schneckenburger H (2014) Single plane illumination module and micro-capillary approach for a wide-field microscope. J Vis Exp 90:e51993. doi: 10.3791/51993 PubMedGoogle Scholar
  8. Capoulade J, Wachsmuth M, Hufnagel L, Knop M (2011) Quantitative fluorescence imaging of protein diffusion and interaction in living cells. Nat Biotechnol 29:835–839. doi: 10.1038/nbt.1928 PubMedGoogle Scholar
  9. Cella Zanacchi F, Lavagnino Z, Perrone Donnorso M, Del Bue A, Furia L, Faretta M, Diaspro A (2011) Live-cell 3D super-resolution imaging in thick biological samples. Nat Methods 8:1047–1049. doi: 10.1038/nmeth.1744 PubMedGoogle Scholar
  10. Cella Zanacchi F, Lavagnino Z, Faretta M, Furia L, Diaspro A (2013) Light-sheet confined super-resolution using two-photon photoactivation. PLoS One 8:e67667. doi: 10.1371/journal.pone.0067667 PubMedCentralPubMedGoogle Scholar
  11. Chen B-C, Legant WR, Wang K, Shao L, Milkie DE, Davidson MW, Betzig E (2014) Lattice light-sheet microscopy: imaging molecules to embryos at high spatiotemporal resolution. Science 346:1257998. doi: 10.1126/science.1257998 PubMedCentralPubMedGoogle Scholar
  12. Costa A, Candeo A, Fieramonti L, Valentini G, Bassi A (2013) Calcium dynamics in root cells of Arabidopsis thaliana visualized with selective plane illumination microscopy. PLoS One 8:e75646. doi: 10.1371/journal.pone.0075646 PubMedCentralPubMedGoogle Scholar
  13. Dean KM, Fiolka R (2014) Uniform and scalable light-sheets generated by extended focusing. Opt Express 22:26141. doi: 10.1364/OE.22.026141 PubMedGoogle Scholar
  14. Desmaison A, Lorenzo C, Rouquette J, Ducommun B, Lobjois V (2013) A versatile sample holder for single plane illumination microscopy. J Microsc 251:128–132. doi: 10.1111/jmi.12051 PubMedGoogle Scholar
  15. Dobosz M, Ntziachristos V, Scheuer W, Strobel S (2014) Multispectral fluorescence ultramicroscopy: three-dimensional visualization and automatic quantification of tumor morphology, drug penetration, and antiangiogenic treatment response. Neoplasia 16:1–W7. doi: 10.1593/neo.131848 PubMedCentralPubMedGoogle Scholar
  16. Dodt H-U, Leischner U, Schierloh A, Jährling N, Mauch CP, Deininger K, Becker K (2007) Ultramicroscopy: three-dimensional visualization of neuronal networks in the whole mouse brain. Nat Methods 4:331–336. doi: 10.1038/nmeth1036 PubMedGoogle Scholar
  17. Ertürk A, Becker K, Jährling N, Mauch CP, Hojer CD, Egen JG, Dodt H-U (2012) Three-dimensional imaging of solvent-cleared organs using 3DISCO. Nat Protoc 7:1983–1995. doi: 10.1038/nprot.2012.119 PubMedGoogle Scholar
  18. Fahrbach FO, Rohrbach A (2010) A line scanned light-sheet microscope with phase shaped self-reconstructing beams. Opt Express 18:24229–24244. doi: 10.1364/OE.18.024229 PubMedGoogle Scholar
  19. 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 PubMedGoogle Scholar
  20. Fahrbach FO, Gurchenkov V, Alessandri K, Nassoy P, Rohrbach A (2013a) Light-sheet microscopy in thick media using scanned Bessel beams and two-photon fluorescence excitation. Opt Express 21:13824–13839. doi: 10.1364/OE.21.013824 PubMedGoogle Scholar
  21. Fahrbach FO, Gurchenkov V, Alessandri K, Nassoy P, Rohrbach A (2013b) Self-reconstructing sectioned Bessel beams offer submicron optical sectioning for large fields of view in light-sheet microscopy. Opt Express 21:11425–11440. doi: 10.1364/OE.21.011425 PubMedGoogle Scholar
  22. Friedrich J, Seidel C, Ebner R, Kunz-Schughart LA (2009) Spheroid-based drug screen: considerations and practical approach. Nat Protoc 4:309–324. doi: 10.1038/nprot.2008.226 PubMedGoogle Scholar
  23. Gao L, Shao L, Higgins CD, Poulton JS, Peifer M, Davidson MW, Betzig E (2012) Noninvasive imaging beyond the diffraction limit of 3D dynamics in thickly fluorescent specimens. Cell 151:1370–1385. doi: 10.1016/j.cell.2012.10.008 PubMedCentralPubMedGoogle Scholar
  24. Gao L, Shao L, Chen B-C, Betzig E (2014) 3D live fluorescence imaging of cellular dynamics using Bessel beam plane illumination microscopy. Nat Protoc 9:1083–1101. doi: 10.1038/nprot.2014.087 PubMedGoogle Scholar
  25. Gebhardt JCM, Suter DM, Roy R, Zhao ZW, Chapman AR, Basu S, Xie XS (2013) Single-molecule imaging of transcription factor binding to DNA in live mammalian cells. Nat Methods 10:421–426. doi: 10.1038/nmeth.2411 PubMedCentralPubMedGoogle Scholar
  26. Greger K, Neetz MJ, Reynaud EG, Stelzer EHK (2011) Three-dimensional fluorescence lifetime imaging with a single plane illumination microscope provides an improved signal to noise ratio. Opt Express 19:20743–20750. doi: 10.1364/OE.19.020743 PubMedGoogle Scholar
  27. Gualda EJ, Simão D, Pinto C, Alves PM, Brito C (2014) Imaging of human differentiated 3D neural aggregates using light sheet fluorescence microscopy. Front Cell Neurosci 8:221. doi: 10.3389/fncel.2014.00221 PubMedCentralPubMedGoogle Scholar
  28. Hammen GF, Turaga D, Holy TE, Meeks JP (2014) Functional organization of glomerular maps in the mouse accessory olfactory bulb. Nat Neurosci 17:953–961. doi: 10.1038/nn.3738 PubMedCentralPubMedGoogle Scholar
  29. Huisken J (2012) Slicing embryos gently with laser light sheets. Bioessays 34:406–411. doi: 10.1002/bies.201100120 PubMedGoogle Scholar
  30. Huisken J, Stainier DYR (2007) Even fluorescence excitation by multidirectional selective plane illumination microscopy (mSPIM). Opt Lett 32:2608. doi: 10.1364/OL.32.002608 PubMedGoogle Scholar
  31. Huisken J, Stainier DYR (2009) Selective plane illumination microscopy techniques in developmental biology. Development 136:1963–1975. doi: 10.1242/dev.022426 PubMedCentralPubMedGoogle Scholar
  32. Huisken J, Swoger J, Del Bene F, Wittbrodt J, Stelzer EHK (2004) Optical sectioning deep inside live embryos by selective plane illumination microscopy. Science 305:1007–1009. doi: 10.1126/science.1100035 PubMedGoogle Scholar
  33. Kasthuri N, Lichtman JW (2007) The rise of the “projectome”. Nat Methods 4:307–308. doi: 10.1038/nmeth0407-307 PubMedGoogle Scholar
  34. Keller PJ (2013) Imaging morphogenesis: technological advances and biological insights. Science 340:1234168. doi: 10.1126/science.1234168 PubMedGoogle Scholar
  35. Keller PJ, Dodt H-U (2012) Light sheet microscopy of living or cleared specimens. Curr Opin Neurobiol 22:138–143. doi: 10.1016/j.conb.2011.08.003 PubMedGoogle Scholar
  36. Keller PJ, Pampaloni F, Lattanzi G, Stelzer EHK (2008a) Three-dimensional microtubule behavior in Xenopus egg extracts reveals four dynamic states and state-dependent elastic properties. Biophys J 95:1474–1486. doi: 10.1529/biophysj.107.128223 PubMedCentralPubMedGoogle Scholar
  37. Keller PJ, Schmidt AD, Wittbrodt J, Stelzer EHK (2008b) Reconstruction of zebrafish early embryonic development by scanned light sheet microscopy. Science 322:1065–1069. doi: 10.1126/science.1162493 PubMedGoogle Scholar
  38. Krieger JW, Singh AP, Garbe CS, Wohland T, Langowski J (2014) Dual-color fluorescence cross-correlation spectroscopy on a single plane illumination microscope (SPIM-FCCS). Opt Express 22:2358–2375. doi: 10.1364/OE.22.002358 PubMedGoogle Scholar
  39. Krzic U, Gunther S, Saunders TE, Streichan SJ, Hufnagel L (2012) Multiview light-sheet microscope for rapid in toto imaging. Nat Methods 9:730–733. doi: 10.1038/nmeth.2064 PubMedGoogle Scholar
  40. Lancaster MA, Renner M, Martin C-A, Wenzel D, Bicknell LS, Hurles ME, Knoblich JA (2013) Cerebral organoids model human brain development and microcephaly. Nature 501:373–379. doi: 10.1038/nature12517 PubMedGoogle Scholar
  41. Lorenzo C, Frongia C, Jorand R, Fehrenbach J, Weiss P, Maandhui A, Lobjois V (2011) Live cell division dynamics monitoring in 3D large spheroid tumor models using light sheet microscopy. Cell Div 6:22. doi: 10.1186/1747-1028-6-22 PubMedCentralPubMedGoogle Scholar
  42. Lucas M, Kenobi K, von Wangenheim D, Voβ U, Swarup K, De Smet I, Bennett MJ (2013) Lateral root morphogenesis is dependent on the mechanical properties of the overlaying tissues. Proc Natl Acad Sci U S A 110:5229–5234. doi: 10.1073/pnas.1210807110 PubMedCentralPubMedGoogle Scholar
  43. Mahou P, Vermot J, Beaurepaire E, Supatto W (2014) Multicolor two-photon light-sheet microscopy. Nat Methods 11:600–601. doi: 10.1038/nmeth.2963 PubMedGoogle Scholar
  44. Maizel A, von Wangenheim D, Federici F, Haseloff J, Stelzer EHK (2011) High-resolution live imaging of plant growth in near physiological bright conditions using light sheet fluorescence microscopy. Plant J 68:377–385. doi: 10.1111/j.1365-313X.2011.04692.x PubMedGoogle Scholar
  45. Mappes T, Jahr N, Csaki A, Vogler N, Popp J, Fritzsche W (2012) The invention of immersion ultramicroscopy in 1912—the birth of nanotechnology? Angew Chem 51:11208–11212. doi: 10.1002/anie.201204688 Google Scholar
  46. McLachlan D Jr (1964) Extreme focal depth in microscopy. Appl Opt 3:1009. doi: 10.1364/AO.3.001009 Google Scholar
  47. Mickoleit M, Schmid B, Weber M, Fahrbach FO, Hombach S, Reischauer S, Huisken J (2014) High-resolution reconstruction of the beating zebrafish heart. Nat Methods 11:919-922. doi: 10.1038/nmeth.3037 PubMedGoogle Scholar
  48. Neil MAA, Juskaitis R, Wilson T (1997) Method of obtaining optical sectioning by using structured light in a conventional microscope. Opt Lett 22:1905. doi: 10.1364/OL.22.001905 PubMedGoogle Scholar
  49. Niedworok CJ, Schwarz I, Ledderose J, Giese G, Conzelmann K-K, Schwarz MK (2012) Charting monosynaptic connectivity maps by two-color light-sheet fluorescence microscopy. Cell Rep 2:1375–1386. doi: 10.1016/j.celrep.2012.10.008 PubMedGoogle Scholar
  50. Oh SW, Harris JA, Ng L, Winslow B, Cain N, Mihalas S, Zeng H (2014) A mesoscale connectome of the mouse brain. Nature 508:207–214. doi: 10.1038/nature13186 PubMedGoogle Scholar
  51. Olarte OE, Licea-Rodriguez J, Palero JA, Gualda EJ, Artigas D, Mayer J, Loza-Alvarez P (2012) Image formation by linear and nonlinear digital scanned light-sheet fluorescence microscopy with Gaussian and Bessel beam profiles. Biomed Opt Express 3:1492–1505. doi: 10.1364/BOE.3.001492 PubMedCentralPubMedGoogle Scholar
  52. Oshima Y, Sato H, Kajiura-Kobayashi H, Kimura T, Naruse K, Nonaka S (2012) Light sheet-excited spontaneous Raman imaging of a living fish by optical sectioning in a wide field Raman microscope. Opt Express 20:16195. doi: 10.1364/OE.20.016195 Google Scholar
  53. Osten P, Margrie TW (2013) Mapping brain circuitry with a light microscope. Nat Methods 10:515–523. doi: 10.1038/nmeth.2477 PubMedCentralPubMedGoogle Scholar
  54. Pampaloni F, Stelzer E (2010) Three-dimensional cell cultures in toxicology. Biotechnol Genet Eng Rev 26:117–38. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/21415878 PubMedGoogle Scholar
  55. Pampaloni F, Reynaud EG, Stelzer EHK (2007) The third dimension bridges the gap between cell culture and live tissue. Nat Rev Mol Cell Biol 8:839–845. doi: 10.1038/nrm2236 PubMedGoogle Scholar
  56. Pampaloni F, Stelzer EHK, Masotti A (2009) Three-dimensional tissue models for drug discovery and toxicology. Recent Patents Biotechnol 3:103–117. doi: 10.2174/187220809788700201 Google Scholar
  57. Pampaloni F, Ansari N, Stelzer EHK (2013) High-resolution deep imaging of live cellular spheroids with light-sheet-based fluorescence microscopy. Cell Tissue Res 352:161–177. doi: 10.1007/s00441-013-1589-7 PubMedGoogle Scholar
  58. Pampaloni F, Berge U, Marmaras A, Horvath P, Kroschewski R, Stelzer EHK (2014a) Tissue-culture light sheet fluorescence microscopy (TC-LSFM) allows long-term imaging of three-dimensional cell cultures under controlled conditions. Integr Biol (Camb) 6:988-998. doi: 10.1039/c4ib00121d Google Scholar
  59. Pampaloni F, Stelzer EHK, Mattheyer C (2014b) Kapillarzelle, anordnung und verfahren zur aufnahme, zur positionierung und zur untersuchung einer mikroskopischen probe. Retrieved from https://www.google.com/patents/WO2014033320A1?cl=de&dq=francesco+pampaloni&hl=en&sa=X&ei=_yIUVMjOHcHMyAPRq4GwDQ&ved=0CDsQ6AEwBA
  60. Pampaloni F, Richa R, Ansari N, Stelzer EHK (2015) Live spheroid formation recorded with light sheet-based fluorescence microscopy. Methods Mol Biol 1251:43-57. doi:  10.1007/978-1-4939-2080-8_3 PubMedGoogle Scholar
  61. Pantazis P, Supatto W (2014) Advances in whole-embryo imaging: a quantitative transition is underway. Nat Rev Mol Cell Biol 15:327–339. doi: 10.1038/nrm3786 PubMedGoogle Scholar
  62. Patra B, Peng Y-S, Peng C-C, Liao W-H, Chen Y-A, Lin K-H, Lee C-H (2014) Migration and vascular lumen formation of endothelial cells in cancer cell spheroids of various sizes. Biomicrofluidics 8:052109. doi: 10.1063/1.4895568 PubMedGoogle Scholar
  63. Pitrone PG, Schindelin J, Stuyvenberg L, Preibisch S, Weber M, Eliceiri KW, Tomancak P (2013) OpenSPIM: an open-access light-sheet microscopy platform. Nat Methods 10:598–599. doi: 10.1038/nmeth.2507 PubMedGoogle Scholar
  64. 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 8:417–423. doi: 10.1038/nmeth.1586 PubMedCentralPubMedGoogle Scholar
  65. Preibisch S, Saalfeld S, Schindelin J, Tomancak P (2010) Software for bead-based registration of selective plane illumination microscopy data. Nat Methods 7:418–419. doi: 10.1038/nmeth0610-418 PubMedGoogle Scholar
  66. Preibisch S, Amat F, Stamataki E, Sarov M, Singer RH, Myers E, Tomancak P (2014) Efficient Bayesian-based multiview deconvolution. Nat Methods 11:645–648. doi: 10.1038/nmeth.2929 PubMedCentralPubMedGoogle Scholar
  67. Ritter JG, Veith R, Veenendaal A, Siebrasse JP, Kubitscheck U (2010) Light sheet microscopy for single molecule tracking in living tissue. PLoS One 5:e11639. doi: 10.1371/journal.pone.0011639 PubMedCentralPubMedGoogle Scholar
  68. Rosquete MR, von Wangenheim D, Marhavý P, Barbez E, Stelzer EHK, Benková E, Kleine-Vehn J (2013) An auxin transport mechanism restricts positive orthogravitropism in lateral roots. Curr Biol 23:817–822. doi: 10.1016/j.cub.2013.03.064 PubMedGoogle Scholar
  69. Sankaran J, Shi X, Ho LY, Stelzer EHK, Wohland T (2010) ImFCS: a software for imaging FCS data analysis and visualization. Opt Express 18:25468–25481. doi: 10.1364/OE.18.025468 PubMedGoogle Scholar
  70. Schmid B, Shah G, Scherf N, Weber M, Thierbach K, Campos CP, Huisken J (2013) High-speed panoramic light-sheet microscopy reveals global endodermal cell dynamics. Nat Commun 4:2207. doi: 10.1038/ncomms3207 PubMedCentralPubMedGoogle Scholar
  71. Sena G, Frentz Z, Birnbaum KD, Leibler S (2011) Quantitation of cellular dynamics in growing Arabidopsis roots with light sheet microscopy. PLoS One 6:e21303. doi: 10.1371/journal.pone.0021303 PubMedCentralPubMedGoogle Scholar
  72. Siedentopf H, Zsigmondy R (1902) Über Sichtbarmachung und Größenbestimmung ultramikoskopischer Teilchen, mit besonderer Anwendung auf Goldrubingläser. Ann Phys 315:1–39. doi: 10.1002/andp.19023150102 Google Scholar
  73. Silvestri L, Bria A, Sacconi L, Iannello G, Pavone FS (2012) Confocal light sheet microscopy: micron-scale neuroanatomy of the entire mouse brain. Opt Express 20:20582–20598. doi: 10.1364/OE.20.020582 PubMedGoogle Scholar
  74. Silvestri L, Bria A, Costantini I, Sacconi L, Peng H, Iannello G, Pavone FS (2013) Micron-scale resolution optical tomography of entire mouse brains with confocal light sheet microscopy. J Vis Exp 80:e50696. doi: 10.3791/50696 Google Scholar
  75. Singh AP, Krieger JW, Buchholz J, Charbon E, Langowski J, Wohland T (2013) The performance of 2D array detectors for light sheet based fluorescence correlation spectroscopy. Opt Express 21:8652–8668. doi: 10.1364/OE.21.008652 PubMedGoogle Scholar
  76. Spence RD, Kurth F, Itoh N, Mongerson CRL, Wailes SH, Peng MS, MacKenzie-Graham AJ (2014) Bringing CLARITY to gray matter atrophy. Neuroimage 101:625-632. doi: 10.1016/j.neuroimage.2014.07.017 PubMedCentralPubMedGoogle Scholar
  77. Stelzer EHK, Lindek S (1994) Fundamental reduction of the observation volume in far-field light microscopy by detection orthogonal to the illumination axis: confocal theta microscopy. Opt Commun 111:536–547. doi: 10.1016/0030-4018(94)90533-9 Google Scholar
  78. Strobl F, Stelzer EHK (2014) Non-invasive long-term fluorescence live imaging of Tribolium castaneum embryos. Development 141:2331–2338. doi: 10.1242/dev.108795 PubMedGoogle Scholar
  79. Susaki EA, Tainaka K, Perrin D, Kishino F, Tawara T, Watanabe TM, Ueda HR (2014) Whole-brain imaging with single-cell resolution using chemical cocktails and computational analysis. Cell 157:726–739. doi: 10.1016/j.cell.2014.03.042 PubMedGoogle Scholar
  80. Swoger J, Pampaloni F, Stelzer EHK (2014a) Imaging cellular spheroids with a single (selective) plane illumination microscope. Cold Spring Harb Protoc 2014:106–113. doi: 10.1101/pdb.prot080176 PubMedGoogle Scholar
  81. Swoger J, Pampaloni F, Stelzer EHK (2014b) Light-sheet-based fluorescence microscopy for three-dimensional imaging of biological samples. Cold Spring Harb Protoc 2014:1–8. doi: 10.1101/pdb.top080168 PubMedGoogle Scholar
  82. Temerinac-Ott M, Ronneberger O, Ochs P, Driever W, Brox T, Burkhardt H (2012) Multiview deblurring for 3-D images from light-sheet-based fluorescence microscopy. IEEE Trans Image Process 21:1863–1873. doi: 10.1109/TIP.2011.2181528 PubMedGoogle Scholar
  83. Tomer R, Khairy K, Keller PJ (2011) Shedding light on the system: studying embryonic development with light sheet microscopy. Curr Opin Genet Dev 21:558–565. doi: 10.1016/j.gde.2011.07.003 PubMedGoogle Scholar
  84. Tomer R, Khairy K, Amat F, Keller PJ (2012) Quantitative high-speed imaging of entire developing embryos with simultaneous multiview light-sheet microscopy. Nat Methods 9:755–763. doi: 10.1038/nmeth.2062 PubMedGoogle Scholar
  85. Tomer R, Ye L, Hsueh B, Deisseroth K (2014) Advanced CLARITY for rapid and high-resolution imaging of intact tissues. Nat Protoc 9:1682–1697. doi: 10.1038/nprot.2014.123 PubMedCentralPubMedGoogle Scholar
  86. Truong TV, Supatto W, Koos DS, Choi JM, Fraser SE (2011) Deep and fast live imaging with two-photon scanned light-sheet microscopy. Nat Methods 8:757–760. doi: 10.1038/nmeth.1652 PubMedGoogle Scholar
  87. Turaga D, Holy TE (2012) Organization of vomeronasal sensory coding revealed by fast volumetric calcium imaging. J Neurosci 32:1612–1621. doi: 10.1523/JNEUROSCI. 5339-11.2012 PubMedCentralPubMedGoogle Scholar
  88. Vermeer JEM, von Wangenheim D, Barberon M, Lee Y, Stelzer EHK, Maizel A, Geldner N (2014) A spatial accommodation by neighboring cells is required for organ initiation in Arabidopsis. Science 343:178–183. doi: 10.1126/science.1245871 PubMedGoogle Scholar
  89. Verveer PJ, Swoger J, Pampaloni F, Greger K, Marcello M, Stelzer EHK (2007) High-resolution three-dimensional imaging of large specimens with light sheet-based microscopy. Nat Methods 4:311–313. doi: 10.1038/NMETH1017 PubMedGoogle Scholar
  90. Vettenburg T, Dalgarno HIC, Nylk J, Coll-Lladó C, Ferrier DEK, Čižmár T, Dholakia K (2014) Light-sheet microscopy using an Airy beam. Nat Methods 11:541–544. doi: 10.1038/nmeth.2922 PubMedGoogle Scholar
  91. Vladimirov N, Mu Y, Kawashima T, Bennett DV, Yang C-T, Looger LL, Ahrens MB (2014) Light-sheet functional imaging in fictively behaving zebrafish. Nat Methods 11:883-884. doi: 10.1038/nmeth.3040 PubMedGoogle Scholar
  92. Voie AH (2002) Imaging the intact guinea pig tympanic bulla by orthogonal-plane fluorescence optical sectioning microscopy. Hear Res 171:119–128. doi: 10.1016/S0378-5955(02)00493-8 PubMedGoogle Scholar
  93. Voie AH, Spelman FA (1995) Three-dimensional reconstruction of the cochlea from two-dimensional images of optical sections. Comput Med Imaging Graph 19:377–384. doi: 10.1016/0895-6111(95)00034-8 PubMedGoogle Scholar
  94. Voie AH, Burns DH, Spelman FA (1993) Orthogonal-plane fluorescence optical sectioning: three-dimensional imaging of macroscopic biological specimens. J Microsc 170:229–236. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/8371260 PubMedGoogle Scholar
  95. Weber M, Huisken J (2011) Light sheet microscopy for real-time developmental biology. Curr Opin Genet Dev 21:566–572. doi: 10.1016/j.gde.2011.09.009 PubMedGoogle Scholar
  96. Weber M, Huisken J (2012) Omnidirectional microscopy. Nat Methods 9:656–657. doi: 10.1038/nmeth.2022 PubMedGoogle Scholar
  97. Wohland T, Shi X, Sankaran J, Stelzer EHK (2010) Single plane illumination fluorescence correlation spectroscopy (SPIM-FCS) probes inhomogeneous three-dimensional environments. Opt Express 18:10627–10641. doi: 10.1364/OE.18.010627 PubMedGoogle Scholar
  98. Wu J, Li J, Chan RKY (2013) A light sheet based high throughput 3D-imaging flow cytometer for phytoplankton analysis. Opt Express 21:14474–14480. doi: 10.1364/OE.21.014474 PubMedGoogle Scholar
  99. Wu Y, Ghitani A, Christensen R, Santella A, Du Z, Rondeau G, Shroff H (2011) Inverted selective plane illumination microscopy (iSPIM) enables coupled cell identity lineaging and neurodevelopmental imaging in Caenorhabditis elegans. Proc Natl Acad Sci U S A 108:17708–17713. doi: 10.1073/pnas.1108494108 PubMedCentralPubMedGoogle Scholar
  100. Wu Y, Wawrzusin P, Senseney J, Fischer RS, Christensen R, Santella A, Shroff H (2013) Spatially isotropic four-dimensional imaging with dual-view plane illumination microscopy. Nat Biotechnol 31:1032–1038. doi: 10.1038/nbt.2713 PubMedCentralPubMedGoogle Scholar
  101. Yang B, Treweek JB, Kulkarni RP, Deverman BE, Chen C-K, Lubeck E, Gradinaru V (2014) Single-cell phenotyping within transparent intact tissue through whole-body clearing. Cell 158:945–958. doi: 10.1016/j.cell.2014.07.017 PubMedGoogle Scholar
  102. Zhang P, Phipps ME, Goodwin PM, Werner JH (2014) Confocal line scanning of a Bessel beam for fast 3D imaging. Opt Lett 39:3682–3685. doi: 10.1364/OL.39.003682 PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2015

Authors and Affiliations

  • Francesco Pampaloni
    • 1
    Email author
  • Bo-Jui Chang
    • 1
  • Ernst H. K. Stelzer
    • 1
  1. 1.Physical Biology Group (FB 15, IZN), Buchmann Institute for Molecular Life Sciences (BMLS, CEF-MC)Goethe Universität Frankfurt am Main (Campus Riedberg)Frankfurt am MainGermany

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