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Title: Soft X-Ray Tomography Reveals Gradual Chromatin Compaction and Reorganization during Neurogenesis In Vivo

The realization that nuclear distribution of DNA, RNA, and proteins differs between cell types and developmental stages suggests that nuclear organization serves regulatory functions. Understanding the logic of nuclear architecture and how it contributes to differentiation and cell fate commitment remains challenging. Here, we use soft X-ray tomography (SXT) to image chromatin organization, distribution, and biophysical properties during neurogenesis in vivo. Our analyses reveal that chromatin with similar biophysical properties forms an elaborate connected network throughout the entire nucleus. Although this interconnectivity is present in every developmental stage, differentiation proceeds with concomitant increase in chromatin compaction and re-distribution of condensed chromatin toward the nuclear core. HP1β, but not nucleosome spacing or phasing, regulates chromatin rearrangements because it governs both the compaction of chromatin and its interactions with the nuclear envelope. Our experiments introduce SXT as a powerful imaging technology for nuclear architecture.
Authors:
 [1] ;  [2] ;  [3] ;  [4] ;  [5] ;  [5] ;  [6] ;  [4] ;  [7] ;  [8]
  1. Univ. of California, San Francisco, CA (United States). Dept. of Anatomy; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Physical Biosciences Division; Univ. of California, San Francisco, CA (United States). National Center for X-Ray Tomography; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  2. Univ. of California, San Francisco, CA (United States). Program in Biomedical Sciences
  3. Foundation for Research and Technology-Hellas (FORTH), Ioannina (Greece). Inst. of Molecular Biology and Biotechnology, Division of Biomedical Research
  4. Broad Inst. of MIT and Harvard, Cambridge, MA (United States); Massachusetts Inst. of Technology (MIT), Cambridge, MA (United States). Computer Science and Artificial Intelligence Lab.
  5. Univ. of California, San Francisco, CA (United States). Program in Neurosciences
  6. Univ. of Jyvaeskylae, Jyvaeskylae (Finland). Dept. of Physics
  7. Univ. of California, San Francisco, CA (United States). Dept. of Anatomy; Univ. of California, San Francisco, CA (United States). Program in Biomedical Sciences; Univ. of California, San Francisco, CA (United States). Program in Neurosciences; Columbia Univ., New York, NY (United States). Zuckerman Mind, Brain, and Behavior Inst., Dept. of Biochemistry and Molecular Biophysics
  8. Univ. of California, San Francisco, CA (United States). Dept. of Anatomy; Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Physical Biosciences Division; Univ. of California, San Francisco, CA (United States). National Center for X-Ray Tomography
Publication Date:
Grant/Contract Number:
AC02-05CH11231; R01DA030320; U01DA040582
Type:
Published Article
Journal Name:
Cell Reports
Additional Journal Information:
Journal Volume: 17; Journal Issue: 8; Journal ID: ISSN 2211-1247
Publisher:
Elsevier
Research Org:
Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 60 APPLIED LIFE SCIENCES; 46 INSTRUMENTATION RELATED TO NUCLEAR SCIENCE AND TECHNOLOGY; chromatin; nucleus; soft X-ray tomography; olfactory sensory neurons; nuclear organization; differentiation; neurogenesis
OSTI Identifier:
1399023
Alternate Identifier(s):
OSTI ID: 1377588

Le Gros, Mark A., Clowney, E. Josephine, Magklara, Angeliki, Yen, Angela, Markenscoff-Papadimitriou, Eirene, Colquitt, Bradley, Myllys, Markko, Kellis, Manolis, Lomvardas, Stavros, and Larabell, Carolyn A.. Soft X-Ray Tomography Reveals Gradual Chromatin Compaction and Reorganization during Neurogenesis In Vivo. United States: N. p., Web. doi:10.1016/j.celrep.2016.10.060.
Le Gros, Mark A., Clowney, E. Josephine, Magklara, Angeliki, Yen, Angela, Markenscoff-Papadimitriou, Eirene, Colquitt, Bradley, Myllys, Markko, Kellis, Manolis, Lomvardas, Stavros, & Larabell, Carolyn A.. Soft X-Ray Tomography Reveals Gradual Chromatin Compaction and Reorganization during Neurogenesis In Vivo. United States. doi:10.1016/j.celrep.2016.10.060.
Le Gros, Mark A., Clowney, E. Josephine, Magklara, Angeliki, Yen, Angela, Markenscoff-Papadimitriou, Eirene, Colquitt, Bradley, Myllys, Markko, Kellis, Manolis, Lomvardas, Stavros, and Larabell, Carolyn A.. 2016. "Soft X-Ray Tomography Reveals Gradual Chromatin Compaction and Reorganization during Neurogenesis In Vivo". United States. doi:10.1016/j.celrep.2016.10.060.
@article{osti_1399023,
title = {Soft X-Ray Tomography Reveals Gradual Chromatin Compaction and Reorganization during Neurogenesis In Vivo},
author = {Le Gros, Mark A. and Clowney, E. Josephine and Magklara, Angeliki and Yen, Angela and Markenscoff-Papadimitriou, Eirene and Colquitt, Bradley and Myllys, Markko and Kellis, Manolis and Lomvardas, Stavros and Larabell, Carolyn A.},
abstractNote = {The realization that nuclear distribution of DNA, RNA, and proteins differs between cell types and developmental stages suggests that nuclear organization serves regulatory functions. Understanding the logic of nuclear architecture and how it contributes to differentiation and cell fate commitment remains challenging. Here, we use soft X-ray tomography (SXT) to image chromatin organization, distribution, and biophysical properties during neurogenesis in vivo. Our analyses reveal that chromatin with similar biophysical properties forms an elaborate connected network throughout the entire nucleus. Although this interconnectivity is present in every developmental stage, differentiation proceeds with concomitant increase in chromatin compaction and re-distribution of condensed chromatin toward the nuclear core. HP1β, but not nucleosome spacing or phasing, regulates chromatin rearrangements because it governs both the compaction of chromatin and its interactions with the nuclear envelope. Our experiments introduce SXT as a powerful imaging technology for nuclear architecture.},
doi = {10.1016/j.celrep.2016.10.060},
journal = {Cell Reports},
number = 8,
volume = 17,
place = {United States},
year = {2016},
month = {11}
}