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

Abstract

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.

Authors:
ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1]; ORCiD logo [1];  [2];  [3];  [1];  [1]; ORCiD logo [1]; ORCiD logo [1];  [4];  [5];  [6];  [1]; ORCiD logo [3]; ORCiD logo [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)
Publication Date:
Research Org.:
Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
National Institutes of Health (NIH); USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1558992
Grant/Contract Number:  
AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
eLife
Additional Journal Information:
Journal Volume: 8; Journal ID: ISSN 2050-084X
Publisher:
eLife Sciences Publications, Ltd.
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Ding, Yifu, Vanselow, Daniel J., Yakovlev, Maksim A., Katz, Spencer R., Lin, Alex Y., Clark, Darin P., Vargas, Phillip, Xin, Xuying, Copper, Jean E., Canfield, Victor A., Ang, Khai C., Wang, Yuxin, Xiao, Xianghui, De Carlo, Francesco, van Rossum, Damian B., La Riviere, Patrick, and Cheng, Keith C. Computational 3D histological phenotyping of whole zebrafish by X-ray histotomography. United States: N. p., 2019. Web. doi:10.7554/eLife.44898.
Ding, Yifu, Vanselow, Daniel J., Yakovlev, Maksim A., Katz, Spencer R., Lin, Alex Y., Clark, Darin P., Vargas, Phillip, Xin, Xuying, Copper, Jean E., Canfield, Victor A., Ang, Khai C., Wang, Yuxin, Xiao, Xianghui, De Carlo, Francesco, van Rossum, Damian B., La Riviere, Patrick, & Cheng, Keith C. Computational 3D histological phenotyping of whole zebrafish by X-ray histotomography. United States. doi:10.7554/eLife.44898.
Ding, Yifu, Vanselow, Daniel J., Yakovlev, Maksim A., Katz, Spencer R., Lin, Alex Y., Clark, Darin P., Vargas, Phillip, Xin, Xuying, Copper, Jean E., Canfield, Victor A., Ang, Khai C., Wang, Yuxin, Xiao, Xianghui, De Carlo, Francesco, van Rossum, Damian B., La Riviere, Patrick, and Cheng, Keith C. Tue . "Computational 3D histological phenotyping of whole zebrafish by X-ray histotomography". United States. doi:10.7554/eLife.44898. https://www.osti.gov/servlets/purl/1558992.
@article{osti_1558992,
title = {Computational 3D histological phenotyping of whole zebrafish by X-ray histotomography},
author = {Ding, Yifu and Vanselow, Daniel J. and Yakovlev, Maksim A. and Katz, Spencer R. and Lin, Alex Y. and Clark, Darin P. and Vargas, Phillip and Xin, Xuying and Copper, Jean E. and Canfield, Victor A. and Ang, Khai C. and Wang, Yuxin and Xiao, Xianghui and De Carlo, Francesco and van Rossum, Damian B. and La Riviere, Patrick and Cheng, Keith C.},
abstractNote = {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.},
doi = {10.7554/eLife.44898},
journal = {eLife},
number = ,
volume = 8,
place = {United States},
year = {2019},
month = {5}
}

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    Works referencing / citing this record:

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    journal, July 1995

    • Kimmel, Charles B.; Ballard, William W.; Kimmel, Seth R.
    • Developmental Dynamics, Vol. 203, Issue 3
    • DOI: 10.1002/aja.1002030302

    Technique: Imaging Earliest Tooth Development in 3D Using a Silver-Based Tissue Contrast Agent: Imaging Intact Embryonic Teeth in 3D
    journal, December 2013

    • Raj, Muhammad T.; Prusinkiewicz, Martin; Cooper, David M. L.
    • The Anatomical Record, Vol. 297, Issue 2
    • DOI: 10.1002/ar.22845

    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

    • Khonsari, R. H.; Healy, C.; Ohazama, A.
    • The Anatomical Record, Vol. 297, Issue 10
    • DOI: 10.1002/ar.22997

    Histology-based screen for zebrafish mutants with abnormal cell differentiation
    journal, October 2003

    • Mohideen, Manzoor-Ali P. K.; Beckwith, Lee G.; Tsao-Wu, Gladys S.
    • Developmental Dynamics, Vol. 228, Issue 3
    • DOI: 10.1002/dvdy.10407

    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

    • Metscher, Brian D.; Müller, Gerd B.
    • Developmental Dynamics, Vol. 240, Issue 10
    • DOI: 10.1002/dvdy.22733

    3D reconstruction of histological sections: Application to mammary gland tissue
    journal, March 2010

    • Arganda-Carreras, Ignacio; Fernández-González, Rodrigo; Muñoz-Barrutia, Arrate
    • Microscopy Research and Technique, Vol. 73, Issue 11
    • DOI: 10.1002/jemt.20829

    Comparative analysis of fixation and embedding techniques for optimized histological preparation of zebrafish
    journal, June 2018

    • Copper, Jean E.; Budgeon, Lynn R.; Foutz, Christina A.
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    • Nature, Vol. 497, Issue 7449
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    Simultaneous single-cell profiling of lineages and cell types in the vertebrate brain
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    • DOI: 10.1038/nbt.4103

    Erratum: ViBE-Z: a framework for 3D virtual colocalization analysis in zebrafish larval brains
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    Parasitoid biology preserved in mineralized fossils
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    • van de Kamp, Thomas; Schwermann, Achim H.; dos Santos Rolo, Tomy
    • Nature Communications, Vol. 9, Issue 1
    • DOI: 10.1038/s41467-018-05654-y

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    journal, November 2018


    Three-dimensional virtual histology enabled through cytoplasm-specific X-ray stain for microscopic and nanoscopic computed tomography
    journal, February 2018

    • Busse, Madleen; Müller, Mark; Kimm, Melanie A.
    • Proceedings of the National Academy of Sciences, Vol. 115, Issue 10
    • DOI: 10.1073/pnas.1720862115

    Three-dimensional virtual histology of human cerebellum by X-ray phase-contrast tomography
    journal, June 2018

    • Töpperwien, Mareike; van der Meer, Franziska; Stadelmann, Christine
    • Proceedings of the National Academy of Sciences, Vol. 115, Issue 27
    • DOI: 10.1073/pnas.1801678115

    Structure and Function of Skeletal Muscle in Zebrafish Early Larvae
    journal, April 2008

    • Dou, Ying; Andersson-Lendahl, Monika; Arner, Anders
    • The Journal of General Physiology, Vol. 131, Issue 5
    • DOI: 10.1085/jgp.200809982

    X-ray energy optimisation in computed microtomography
    journal, June 1989


    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
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    • Babaei, Fatemeh; Hong, Tony Liu Chi; Yeung, Kelvin
    • Zebrafish, Vol. 13, Issue 4
    • DOI: 10.1089/zeb.2016.1245

    In vivo myosin step-size from zebrafish skeletal muscle
    journal, May 2016

    • Burghardt, Thomas P.; Ajtai, Katalin; Sun, Xiaojing
    • Open Biology, Vol. 6, Issue 5
    • DOI: 10.1098/rsob.160075

    A large-scale zebrafish gene knockout resource for the genome-wide study of gene function
    journal, February 2013


    Ultrastructural Mapping of the Zebrafish Gastrointestinal System as a Basis for Experimental Drug Studies
    journal, January 2016

    • Cheng, Delfine; Shami, Gerald J.; Morsch, Marco
    • BioMed Research International, Vol. 2016
    • DOI: 10.1155/2016/8758460

    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


    Rigid Embedding of Fixed and Stained, Whole, Millimeter-Scale Specimens for Section-free 3D Histology by Micro-Computed Tomography
    journal, January 2018

    • Lin, Alex Y.; Ding, Yifu; Vanselow, Daniel J.
    • Journal of Visualized Experiments, Issue 140
    • DOI: 10.3791/58293

    Basics of cytology
    journal, January 2011