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Computational 3D histological phenotyping of whole zebrafish by X-ray histotomography

Journal Article · · eLife
DOI:https://doi.org/10.7554/eLife.44898· OSTI ID:1558992
 [1];  [1];  [1];  [1];  [1];  [2];  [3];  [1];  [1];  [1];  [1];  [4];  [5];  [6];  [1];  [3];  [1]
  1. Penn State College of Medicine, Hershey, PA (United States)
  2. Duke Univ., Durham, NC (United States)
  3. The Univ. of Chicago, Chicago, IL (United States)
  4. Omnivision Technologies, Inc., Santa Clara, CA (United States)
  5. Brookhaven National Lab. (BNL), Upton, NY (United States)
  6. Argonne National Lab. (ANL), Lemont, IL (United States)

Organismal phenotypes frequently involve multiple organ systems. Histology is a powerful way to detect cellular and tissue phenotypes, but is largely descriptive and subjective. To determine how synchrotron-based X-ray micro-tomography (micro-CT) can yield 3-dimensional whole-organism images suitable for quantitative histological phenotyping, we scanned whole zebrafish, a small vertebrate model with diverse tissues, at ~1 micron voxel resolutions. Micro-CT optimized for cellular characterization (histotomography) allows brain nuclei to be computationally segmented and assigned to brain regions, and cell shapes and volumes to be computed for motor neurons and red blood cells. Striking individual phenotypic variation was apparent from color maps of computed densities of brain nuclei. Unlike histology, the histotomography also allows the study of 3-dimensional structures of millimeter scale that cross multiple tissue planes. We expect the computational and visual insights into 3D cell and tissue architecture provided by histotomography to be useful for reference atlases, hypothesis generation, comprehensive organismal screens, and diagnostics.

Research Organization:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Organization:
National Institutes of Health (NIH); USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
Grant/Contract Number:
AC02-06CH11357
OSTI ID:
1558992
Journal Information:
eLife, Journal Name: eLife Vol. 8; ISSN 2050-084X
Publisher:
eLife Sciences Publications, Ltd.Copyright Statement
Country of Publication:
United States
Language:
English

References (70)

Data from: Computational 3D histological phenotyping of whole zebrafish by X-ray histotomography dataset January 2019
Stages of embryonic development of the zebrafish journal July 1995
Technique: Imaging Earliest Tooth Development in 3D Using a Silver-Based Tissue Contrast Agent: Imaging Intact Embryonic Teeth in 3D journal December 2013
Submicron Imaging of Soft-Tissues Using Low-Dose Phase-Contrast X-Ray Synchrotron Microtomography With an Iodine Contrast Agent: Letter to the Editor journal July 2014
Histology-based screen for zebrafish mutants with abnormal cell differentiation journal October 2003
MicroCT for developmental biology: A versatile tool for high-contrast 3D imaging at histological resolutions journal March 2009
MicroCT for molecular imaging: Quantitative visualization of complete three-dimensional distributions of gene products in embryonic limbs journal September 2011
MicroCT for molecular imaging: Quantitative visualization of complete three-dimensional distributions of gene products in embryonic limbs journal November 2011
3D reconstruction of histological sections: Application to mammary gland tissue
  • Arganda-Carreras, Ignacio; Fernández-González, Rodrigo; Muñoz-Barrutia, Arrate
  • Microscopy Research and Technique, Vol. 73, Issue 11 https://doi.org/10.1002/jemt.20829
journal March 2010
Fine structural and cytochemical analysis of the staining of synaptic junctions with phosphotungstic acid journal March 1968
Acquisition, optimization and interpretation of X-ray computed tomographic imagery: applications to the geosciences journal May 2001
Comparative analysis of fixation and embedding techniques for optimized histological preparation of zebrafish journal June 2018
Whole-Brain Imaging with Single-Cell Resolution Using Chemical Cocktails and Computational Analysis journal April 2014
Saturated Reconstruction of a Volume of Neocortex journal July 2015
In Toto Imaging and Reconstruction of Post-Implantation Mouse Development at the Single-Cell Level journal October 2018
Whole-animal imaging, gene function, and the Zebrafish Phenome Project journal October 2011
Ex vivo characterization of articular cartilage and bone lesions in a rabbit ACL transection model of osteoarthritis using MRI and micro-CT journal December 2004
Three-dimensional network of Drosophila brain hemisphere journal November 2013
User-guided 3D active contour segmentation of anatomical structures: Significantly improved efficiency and reliability journal July 2006
Brain-wide Organization of Neuronal Activity and Convergent Sensorimotor Transformations in Larval Zebrafish journal November 2018
Three-dimensional microCT imaging of mouse development from early post-implantation to early postnatal stages journal November 2016
The Human Cell Atlas: from vision to reality journal October 2017
Synchrotron X-ray tomographic microscopy of fossil embryos journal August 2006
Structural and molecular interrogation of intact biological systems journal April 2013
The zebrafish reference genome sequence and its relationship to the human genome journal April 2013
X-ray phase-contrast in vivo microtomography probes new aspects of Xenopus gastrulation journal May 2013
High-throughput discovery of novel developmental phenotypes journal September 2016
Whole-brain serial-section electron microscopy in larval zebrafish journal May 2017
Simultaneous single-cell profiling of lineages and cell types in the vertebrate brain journal March 2018
Erratum: ViBE-Z: a framework for 3D virtual colocalization analysis in zebrafish larval brains journal September 2012
Scale: a chemical approach for fluorescence imaging and reconstruction of transparent mouse brain journal August 2011
Parasitoid biology preserved in mineralized fossils journal August 2018
Single-cell analysis of Schistosoma mansoni identifies a conserved genetic program controlling germline stem cell fate journal January 2021
Chunkflow: hybrid cloud processing of large 3D images by convolutional nets journal March 2021
Quantitative morphometric analysis of adult teleost fish by X-ray computed tomography journal November 2018
Three-dimensional virtual histology enabled through cytoplasm-specific X-ray stain for microscopic and nanoscopic computed tomography journal February 2018
Three-dimensional virtual histology of human cerebellum by X-ray phase-contrast tomography journal June 2018
Structure and Function of Skeletal Muscle in Zebrafish Early Larvae journal April 2008
X-ray energy optimisation in computed microtomography journal June 1989
In vivo small-animal imaging using micro-CT and digital subtraction angiography journal August 2008
A Life-Span Atlas for the Zebrafish journal May 2004
Whole-Body Imaging of a Hypercholesterolemic Female Zebrafish by Using Synchrotron X-Ray Micro-CT journal February 2015
Contrast-Enhanced X-Ray Micro-Computed Tomography as a Versatile Method for Anatomical Studies of Adult Zebrafish journal August 2016
Coherent X-Ray Optics book January 2006
In vivo myosin step-size from zebrafish skeletal muscle journal May 2016
A large-scale zebrafish gene knockout resource for the genome-wide study of gene function journal February 2013
Ilastik: Interactive learning and segmentation toolkit
  • Sommer, Christoph; Straehle, Christoph; Kothe, Ullrich
  • 2011 8th IEEE International Symposium on Biomedical Imaging (ISBI 2011), 2011 IEEE International Symposium on Biomedical Imaging: From Nano to Macro https://doi.org/10.1109/isbi.2011.5872394
conference March 2011
Essentials of Anatomic Pathology journal November 2006
Imaging applications of synchrotron X-ray phase-contrast microtomography in biological morphology and biomaterials science. I. General aspects of the technique and its advantages in the analysis of millimetre-sized arthropod structure journal July 2007
Optimizing synchrotron microCT for high-throughput phenotyping of zebrafish conference August 2010
Ultrastructural Mapping of the Zebrafish Gastrointestinal System as a Basis for Experimental Drug Studies journal January 2016
MicroCT for comparative morphology: simple staining methods allow high-contrast 3D imaging of diverse non-mineralized animal tissues journal January 2009
Observations on Histological Methods Involving the use of Phosphotungstic and Phosphomolybdic Acids, with Particular Reference to Staining with Phosphotungstic Acid/Haematoxylin journal September 1962
Stripe and ring artifact removal with combined wavelet—Fourier filtering journal January 2009
Plant Tissues in 3D via X-Ray Tomography: Simple Contrasting Methods Allow High Resolution Imaging journal September 2013
Ribbon scanning confocal for high-speed high-resolution volume imaging of brain journal July 2017
Quantifying Mesoscale Neuroanatomy Using X-Ray Microtomography journal September 2017
The Knockout Mouse Project
  • Libraries, The University of North Carolina at Chapel Hill University
  • The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/4j1y-b823
text January 2004
The Human Cell Atlas. text January 2017
Three-dimensional virtual histology of human cerebellum by X-ray phase-contrast tomography text January 2018
Rigid Embedding of Fixed and Stained, Whole, Millimeter-Scale Specimens for Section-free 3D Histology by Micro-Computed Tomography journal January 2018
Basics of cytology journal January 2011
Quantifying mesoscale neuroanatomy using X-ray microtomography preprint January 2016
Data from: Computational 3D histological phenotyping of whole zebrafish by X-ray histotomography dataset January 2019
Data from: Computational 3D histological phenotyping of whole zebrafish by X-ray histotomography dataset January 2019
The Human Cell Atlas text January 2017
Stripe and ring artifact removal with combined wavelet--Fourier filtering text January 2009
Parasitoid biology preserved in mineralized fossils text January 2018
Quantitative morphometric analysis of adult teleost fish by X-ray computed tomography text January 2018
The Human Cell Atlas journal December 2017

Cited By (6)

Data from: Computational 3D histological phenotyping of whole zebrafish by X-ray histotomography dataset January 2019
Data from: Computational 3D histological phenotyping of whole zebrafish by X-ray histotomography dataset January 2019
Zebrafish: An Emerging Model for Orthopedic Research journal December 2019
Micro-computed tomography as a platform for exploring Drosophila development journal November 2019
Data from: Computational 3D histological phenotyping of whole zebrafish by X-ray histotomography dataset January 2019
Taking a closer look at whole organisms journal June 2019


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