Versatile whole-organ/body staining and imaging based on electrolyte-gel properties of biological tissues.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
27 04 2020
27 04 2020
Historique:
received:
05
09
2019
accepted:
31
03
2020
entrez:
29
4
2020
pubmed:
29
4
2020
medline:
11
8
2020
Statut:
epublish
Résumé
Whole-organ/body three-dimensional (3D) staining and imaging have been enduring challenges in histology. By dissecting the complex physicochemical environment of the staining system, we developed a highly optimized 3D staining imaging pipeline based on CUBIC. Based on our precise characterization of biological tissues as an electrolyte gel, we experimentally evaluated broad 3D staining conditions by using an artificial tissue-mimicking material. The combination of optimized conditions allows a bottom-up design of a superior 3D staining protocol that can uniformly label whole adult mouse brains, an adult marmoset brain hemisphere, an ~1 cm
Identifiants
pubmed: 32341345
doi: 10.1038/s41467-020-15906-5
pii: 10.1038/s41467-020-15906-5
pmc: PMC7184626
doi:
Substances chimiques
Electrolytes
0
Fluorescent Dyes
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1982Références
Spalteholz, W. Über das Durchsichtigmachen von menschlichen und tierischen Präparaten (S. Hirzel, Leipzig, 1914).
Susaki, E. A. & Ueda, H. R. Whole-body and whole-organ clearing and imaging techniques with single-cell resolution: toward organism-level systems biology in mammals. Cell Chem. Biol. 23, 137–157 (2016).
pubmed: 26933741
Ueda, H. R. et al. Tissue clearing and its applications in neuroscience. Nat. Rev. Neurosci. 21, 61–79 (2020).
pubmed: 31896771
Treweek, J. B. & Gradinaru, V. Extracting structural and functional features of widely distributed biological circuits with single cell resolution via tissue clearing and delivery vectors. Curr. Opin. Biotechnol. 40, 193–207 (2016).
pubmed: 27393829
pmcid: 4975678
Bishop, C. A. & O’Shea, M. Neuropeptide proctolin (H-Arg-Try-Leu-Pro-Thr-OH): immunocytochemical mapping of neurons in the central nervous system of the cockroach. J. Comp. Neurol. 207, 223–238 (1982).
pubmed: 6125531
Beltz, B. S. & Kravitz, E. A. Mapping of serotonin-like immunoreactivity in the lobster nervous system. J. Neurosci. 3, 585–602 (1983).
pubmed: 6338162
pmcid: 6564544
Dent, J. A., Polson, A. G. & Klymkowsky, M. W. A whole-mount immunocytochemical analysis of the expression of the intermediate filament protein vimentin in Xenopus. Development 105, 61–74 (1989).
pubmed: 2806118
Renier, N. et al. iDISCO: a simple, rapid method to immunolabel large tissue samples for volume imaging. Cell 159, 896–910 (2014).
pubmed: 25417164
Belle, M. et al. Tridimensional visualization and analysis of early human development. Cell 169, 161–173 e112 (2017).
pubmed: 28340341
Gleave, J. A., Lerch, J. P., Henkelman, R. M. & Nieman, B. J. A method for 3D immunostaining and optical imaging of the mouse brain demonstrated in neural progenitor cells. PLoS ONE 8, e72039 (2013).
pubmed: 23936537
pmcid: 3735582
Sillitoe, R. V. & Hawkes, R. Whole-mount immunohistochemistry: a high-throughput screen for patterning defects in the mouse cerebellum. J. Histochem. Cytochem. 50, 235–244 (2002).
pubmed: 11799142
Chung, K. et al. Structural and molecular interrogation of intact biological systems. Nature 497, 332–337 (2013).
pubmed: 23575631
pmcid: 4092167
Susaki, E. A. et al. Whole-brain imaging with single-cell resolution using chemical cocktails and computational analysis. Cell 157, 726–739 (2014).
pubmed: 24746791
Tainaka, K. et al. Whole-body imaging with single-cell resolution by tissue decolorization. Cell 159, 911–924 (2014).
pubmed: 25417165
Hama, H. et al. ScaleS: an optical clearing palette for biological imaging. Nat. Neurosci. 18, 1518–1529 (2015).
pubmed: 26368944
Yang, B. et al. Single-cell phenotyping within transparent intact tissue through whole-body clearing. Cell 158, 945–958 (2014).
pubmed: 25088144
pmcid: 4153367
Renier, N. et al. Mapping of brain activity by automated volume analysis of immediate early genes. Cell 165, 1789–1802 (2016).
pubmed: 27238021
pmcid: 4912438
Cai, R. et al. Panoptic imaging of transparent mice reveals whole-body neuronal projections and skull-meninges connections. Nat. Neurosci. 22, 317–327 (2018).
pubmed: 30598527
pmcid: 6494982
Kubota, S. I. et al. Whole-body profiling of cancer metastasis with single-cell resolution. Cell Rep. 20, 236–250 (2017).
pubmed: 28683317
Nojima, S. et al. CUBIC pathology: three-dimensional imaging for pathological diagnosis. Sci. Rep. 7, 9269 (2017).
pubmed: 28839164
pmcid: 5571108
Lai, H. M. et al. Next generation histology methods for three-dimensional imaging of fresh and archival human brain tissues. Nat. Commun. 9, 1066 (2018).
pubmed: 29540691
pmcid: 5852003
Tanaka, N. et al. Whole-tissue biopsy phenotyping of three-dimensional tumours reveals patterns of cancer heterogeneity. Nat. Biomed. Eng. 1, 796 (2017).
pubmed: 31015588
Hildebrand, S. et al. Scalable labeling for cytoarchitectonic characterization of large optically cleared human neocortex samples. Sci. Rep. 9, 10880 (2019).
pubmed: 31350519
pmcid: 6659684
Zhao, S. et al. Cellular and molecular probing of intact human organs. Cell 180, 796–812 e719 (2020).
pubmed: 32059778
Murray, E. et al. Simple, scalable proteomic imaging for high-dimensional profiling of intact systems. Cell 163, 1500–1514 (2015).
pubmed: 26638076
pmcid: 5275966
Kim, S. Y. et al. Stochastic electrotransport selectively enhances the transport of highly electromobile molecules. Proc. Natl Acad. Sci. USA 112, E6274–6283 (2015).
pubmed: 26578787
Lee, E. et al. ACT-PRESTO: rapid and consistent tissue clearing and labeling method for 3-dimensional (3D) imaging. Sci. Rep. 6, 18631 (2016).
pubmed: 26750588
pmcid: 4707495
Liebmann, T. et al. Three-dimensional study of Alzheimer’s disease hallmarks using the idisco clearing method. Cell Rep. 16, 1138–1152 (2016).
pubmed: 27425620
pmcid: 5040352
Tanaka, T. Gels. Sci. Am. 244, 124–136, 138 (1981).
Amiya, T. & Tanaka, T. Phase transitions in crosslinked gels of natural polymers. Macromolecules 20, 1162–1164 (1987).
Morell, P. & Quarles, R.H. in Basic Neurochemistry: Molecular, Cellular and Medical Aspects 6th edn, (eds Siegel, GJ, Albers, RW, et al.) (Lippincott-Raven, Philadelphia, 1999).
Beaucage, G. Small-angle scattering from polymeric mass fractals of arbitrary mass-fractal dimension. J. Appl. Cryst. 29, 134–146 (1996).
Carboni, E. et al. Imaging of neuronal tissues by x-ray diffraction and x-ray fluorescence microscopy: evaluation of contrast and biomarkers for neurodegenerative diseases. Biomed. Opt. Express 8, 4331–4347 (2017).
pubmed: 29082068
pmcid: 5654783
Mikula, S., Binding, J. & Denk, W. Staining and embedding the whole mouse brain for electron microscopy. Nat. Methods 9, 1198–1201 (2012).
pubmed: 23085613
Shibayama, M. I. F., Inamoto, S. & Nomura, S. pH and salt concentration dependence of the microstructure of poly(N-isopropylacrylamide-co-acrylic acid) gels. J. Chem. Phys. 105, 4358–4366 (1996).
Murakami, T. C. et al. A three-dimensional single-cell-resolution whole-brain atlas using CUBIC-X expansion microscopy and tissue clearing. Nat. Neurosci. 21, 625–637 (2018).
pubmed: 29507408
Schaefer, D. W. Polymers, fractals, and ceramic materials. Science 243, 1023–1027 (1989).
pubmed: 17734805
Annaka, M. T. T. Multiple phases of polymer gels. Nature 355, 430–432 (1992).
Cussler, E.L. Diffusion: Mass Transfer in Fluid Systems (Cambridge University Press, 2009).
Tainaka, K. et al. Chemical landscape for tissue clearing based on hydrophilic reagents. Cell Rep. 24, 2196–2210 (2018).
pubmed: 30134179
Saito, T. et al. Single App knock-in mouse models of Alzheimer’s disease. Nat. Neurosci. 17, 661–663 (2014).
pubmed: 24728269
Feng, G. P. et al. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 28, 41–51 (2000).
pubmed: 11086982
Menegas, W. et al. Dopamine neurons projecting to the posterior striatum form an anatomically distinct subclass. Elife 4, e10032 (2015).
pubmed: 26322384
pmcid: 4598831
Ye, L. et al. Wiring and molecular features of prefrontal ensembles representing distinct experiences. Cell 165, 1776–1788 (2016).
pubmed: 27238022
pmcid: 5708551
Taniguchi, H. et al. A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex. Neuron 71, 995–1013 (2011).
pubmed: 21943598
pmcid: 3779648
Osakada, F. & Callaway, E. M. Design and generation of recombinant rabies virus vectors. Nat. Protoc. 8, 1583–1601 (2013).
pubmed: 23887178
pmcid: 4028848
Tatsuki, F. et al. Involvement of Ca(2+)-dependent hyperpolarization in sleep duration in mammals. Neuron 90, 70–85 (2016).
pubmed: 26996081
Xiong, B. et al. Precise cerebral vascular atlas in stereotaxic coordinates of whole mouse brain. Front. Neuroanat. 11, 128 (2017).
pubmed: 29311856
pmcid: 5742197
Delaney, C. L., Brenner, M. & Messing, A. Conditional ablation of cerebellar astrocytes in postnatal transgenic mice. J. Neurosci. 16, 6908–6918 (1996).
pubmed: 8824329
pmcid: 6579279
Chen, F., Tillberg, P. W. & Boyden, E. S. Expansion microscopy. Science 347, 543–548 (2015).
pubmed: 25592419
pmcid: 4312537
Richardson, D. S. & Lichtman, J. W. Clarifying Tissue Clearing. Cell 162, 246–257 (2015).
pubmed: 26186186
pmcid: 4537058
Cazemier, J. L., Clasca, F. & Tiesinga, P. H. Connectomic analysis of brain networks: novel techniques and future directions. Front. Neuroanat. 10, 110 (2016).
pubmed: 27881953
pmcid: 5101213
Park, Y.G. et al. Protection of tissue physicochemical properties using polyfunctional crosslinkers. Nat. Biotechnol. 37, 73–83 (2018).
Miyamichi, K. et al. Dissecting local circuits: parvalbumin interneurons underlie broad feedback control of olfactory bulb output. Neuron 80, 1232–1245 (2013).
pubmed: 24239125
pmcid: 3932159
Suzuki, H. et al. Protective effects of recombinant osteopontin on early brain injury after subarachnoid hemorrhage in rats. Crit. Care Med. 38, 612–618 (2010).
pubmed: 19851092
pmcid: 2808465
Yatsushige, H. et al. Role of c-Jun N-terminal kinase in early brain injury after subarachnoid hemorrhage. J. Neurosci. Res. 85, 1436–1448 (2007).
pubmed: 17410600
Tanaka, T. Collapse of gels and the critical endpoint. Phys. Rev. Lett. 40, 820 (1978).
Voogd, J., Feirabend, M.K.P. Classic methods in neuroanatomy. In Methods in Neurobiology (ed. Lahue, R.) (Springer, US, 1981).
Gao, L. Extend the field of view of selective plan illumination microscopy by tiling the excitation light sheet. Opt. Express 23, 6102–6111 (2015).
pubmed: 25836834
Meijering, E. H., Niessen, W. J. & Viergever, M. A. Quantitative evaluation of convolution-based methods for medical image interpolation. Med. Image Anal. 5, 111–126 (2001).
pubmed: 11516706
Avants, B. B., Epstein, C. L., Grossman, M. & Gee, J. C. Symmetric diffeomorphic image registration with cross-correlation: evaluating automated labeling of elderly and neurodegenerative brain. Med. Image Anal. 12, 26–41 (2008).
pubmed: 17659998
Ollion, J. et al. TANGO: a generic tool for high-throughput 3D image analysis for studying nuclear organization. Bioinformatics 29, 1840–1841 (2013).
pubmed: 23681123
pmcid: 3702251
Yushkevich, P. A. et al. User-guided 3D active contour segmentation of anatomical structures: Significantly improved efficiency and reliability. Neuroimage 31, 1116–1128 (2006).
pubmed: 16545965