Statistical analysis of 3D images detects regular spatial distributions of centromeres and chromocenters in animal and plant nuclei

Autor: Véronique Duranthon, Valérie Gaudin, Pierre-Gaël Adenot, Zichuan Liu, Eve Devinoy, Philippe Andrey, Leila Tirichine, Cathy Hue-Beauvais, Yves Maurin, Nicole Houba-Hérin, Pascale Debey, Kiên Kiêu, Eric Biot, Clémence Kress, Gaetan Lehmann, Nathalie Beaujean
Přispěvatelé: Neurobiologie de l'Olfaction et Modélisation en Imagerie (NOeMI), Institut National de la Recherche Agronomique (INRA), Institut Fédératif de Recherche 144 (NeuroSud Paris) (IFR 144), Université Pierre et Marie Curie - Paris 6 (UPMC), Unité de recherche Mathématiques et Informatique Appliquées (MIA), Unité de recherche génomique et physiologie de la lactation (GPL), Biologie du développement et reproduction (BDR), Centre National de la Recherche Scientifique (CNRS)-École nationale vétérinaire d'Alfort (ENVA)-Institut National de la Recherche Agronomique (INRA), Institut Jean-Pierre Bourgin (IJPB), Institut National de la Recherche Agronomique (INRA)-AgroParisTech, École nationale vétérinaire - Alfort (ENVA)-Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS), Neurobiologie de l'Olfaction et de la Prise Alimentaire (NOPA), Génomique et Physiologie de la Lactation (GPL), Biologie du Développement et Reproduction (BDR)
Jazyk: angličtina
Rok vydání: 2010
Předmět:
[SDV]Life Sciences [q-bio]
Arabidopsis
blastocyste
0302 clinical medicine
Heterochromatin
chromosome
lcsh:QH301-705.5
Spatial organization
Genomic organization
Genetics
0303 health sciences
Microscopy
Confocal
Ecology
Nuclear Proteins
eucaryote
medicine.anatomical_structure
Computational Theory and Mathematics
Modeling and Simulation
Female
Interphase
Cell Biology/Nuclear Structure and Function
Rabbits
Monte Carlo Method
Research Article
noyau cellulaire
Centromere
Biology
03 medical and health sciences
Cellular and Molecular Neuroscience
Imaging
Three-Dimensional
Mammary Glands
Animal
medicine
Animals
Molecular Biology
Spatial analysis
Ecology
Evolution
Behavior and Systematics
030304 developmental biology
Cell Nucleus
Models
Statistical
gène
statistique
Embryo
Mammalian
Cell nucleus
lcsh:Biology (General)
Evolutionary biology
embryon
Mathematics/Statistics
cellule
Nucleus
030217 neurology & neurosurgery
Zdroj: PLoS Computational Biology
PLoS Computational Biology, Public Library of Science, 2010, 6 (7), pp.e10000853 1-15. ⟨10.1371/journal.pcbi.1000853⟩
PLoS Computational Biology, 2010, 6 (7), pp.e10000853 1-15. ⟨10.1371/journal.pcbi.1000853⟩
PLoS Computational Biology, Vol 6, Iss 7, p e1000853 (2010)
Plos Computational Biology 7 (6), e10000853 1-15. (2010)
ISSN: 1553-734X
1553-7358
DOI: 10.1371/journal.pcbi.1000853⟩
Popis: In eukaryotes, the interphase nucleus is organized in morphologically and/or functionally distinct nuclear “compartments”. Numerous studies highlight functional relationships between the spatial organization of the nucleus and gene regulation. This raises the question of whether nuclear organization principles exist and, if so, whether they are identical in the animal and plant kingdoms. We addressed this issue through the investigation of the three-dimensional distribution of the centromeres and chromocenters. We investigated five very diverse populations of interphase nuclei at different differentiation stages in their physiological environment, belonging to rabbit embryos at the 8-cell and blastocyst stages, differentiated rabbit mammary epithelial cells during lactation, and differentiated cells of Arabidopsis thaliana plantlets. We developed new tools based on the processing of confocal images and a new statistical approach based on G- and F- distance functions used in spatial statistics. Our original computational scheme takes into account both size and shape variability by comparing, for each nucleus, the observed distribution against a reference distribution estimated by Monte-Carlo sampling over the same nucleus. This implicit normalization allowed similar data processing and extraction of rules in the five differentiated nuclei populations of the three studied biological systems, despite differences in chromosome number, genome organization and heterochromatin content. We showed that centromeres/chromocenters form significantly more regularly spaced patterns than expected under a completely random situation, suggesting that repulsive constraints or spatial inhomogeneities underlay the spatial organization of heterochromatic compartments. The proposed technique should be useful for identifying further spatial features in a wide range of cell types.
Author Summary Several reports suggest functional relationships within the spatial organization of the nucleus, gene regulation and cell differentiation. However, it still remains difficult to extract common rules, mostly because i) most data have been gathered on limited sets of nuclear elements and in nuclei outside their normal physiological environment, and ii) few three-dimensional (3D) quantitative measures have been performed. Thus, we questioned whether common nuclear organization principles exist in the animal and plant kingdoms. For that purpose, we investigated the 3D distribution of centromeres/chromocenters in five populations of animal and plant nuclei: rabbit embryos at 8-cell and blastocyst stages, rabbit mammary gland epithelial cells and Arabidopsis thaliana plantlets. We set up adapted procedures to segment confocal images and developed a new analytical methodology based on distances between positions within the nucleus and centromeres/chromocenters. We showed that in all systems, despite large differences in chromosome number (44 in rabbit; 10 in A. thaliana) and genome size (rabbit estimated size 2.77 Gbp; A. thaliana 125 Mbp), centromeres/chromocenters form significantly more regularly spaced patterns than expected under a completely random situation. This suggests that, whatever their specific features, conserved rules govern the spatial distribution of genomes in nuclei of differentiated cells.
Databáze: OpenAIRE
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