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Entropic effects in cell lineage tree packings.

ABSTRACT: Optimal packings [1, 2] of unconnected objects have been studied for centuries [3-6], but the packing principles of linked objects, such as topologically complex polymers [7, 8] or cell lineages [9, 10], are yet to be fully explored. Here, we identify and investigate a generic class of geometrically frustrated tree packing problems, arising during the initial stages of animal development when interconnected cells assemble within a convex enclosure [10]. Using a combination of 3D imaging, computational image analysis, and mathematical modelling, we study the tree packing problem in Drosophila egg chambers, where 16 germline cells are linked by cytoplasmic bridges to form a branched tree. Our imaging data reveal non-uniformly distributed tree packings, in agreement with predictions from energy-based computations. This departure from uniformity is entropic and affects cell organization during the first stages of the animal's development. Considering mathematical models of increasing complexity, we investigate spherically confined tree packing problems on convex polyhedrons [11] that generalize Platonic and Archimedean solids. Our experimental and theoretical results provide a basis for understanding the principles that govern positional ordering in linked multicellular structures, with implications for tissue organization and dynamics [12, 13].

SUBMITTER: Alsous JI

PROVIDER: S-EPMC6419958 | biostudies-literature | 2018 Oct

REPOSITORIES: biostudies-literature

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Entropic effects in cell lineage tree packings.

Alsous Jasmin Imran JI Villoutreix Paul P Stoop Norbert N Shvartsman Stanislav Y SY Dunkel Jӧrn J

Nature physics 20180716 10

Optimal packings [1, 2] of unconnected objects have been studied for centuries [3-6], but the packing principles of linked objects, such as topologically complex polymers [7, 8] or cell lineages [9, 10], are yet to be fully explored. Here, we identify and investigate a generic class of geometrically frustrated tree packing problems, arising during the initial stages of animal development when interconnected cells assemble within a convex enclosure [10]. Using a combination of 3D imaging, computa ...[more]

PMID: 30881478

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Project description:The somatic diversity of antigen-recognizing B-cell receptors (BCRs) arises from Variable (V), Diversity (D), and Joining (J) (VDJ) recombination and somatic hypermutation (SHM) during B-cell development and affinity maturation. The VDJ junction of the BCR heavy chain forms the highly variable complementarity determining region 3 (CDR3), which plays a critical role in antigen specificity and binding affinity. Tracking the selection and mutation of the CDR3 can be useful in characterizing humoral responses to infection and vaccination. Although tens to hundreds of thousands of unique BCR genes within an expressed B-cell repertoire can now be resolved with high-throughput sequencing, tracking SHMs is still challenging because existing annotation methods are often limited by poor annotation coverage, inconsistent SHM identification across the VDJ junction, or lack of B-cell lineage data. Here, we present B-cell repertoire inductive lineage and immunosequence annotator (BRILIA), an algorithm that leverages repertoire-wide sequencing data to globally improve the VDJ annotation coverage, lineage tree assembly, and SHM identification. On benchmark tests against simulated human and mouse BCR repertoires, BRILIA correctly annotated germline and clonally expanded sequences with 94 and 70% accuracy, respectively, and it has a 90% SHM-positive prediction rate in the CDR3 of heavily mutated sequences; these are substantial improvements over existing methods. We used BRILIA to process BCR sequences obtained from splenic germinal center B cells extracted from C57BL/6 mice. BRILIA returned robust B-cell lineage trees and yielded SHM patterns that are consistent across the VDJ junction and agree with known biological mechanisms of SHM. By contrast, existing BCR annotation tools, which do not account for repertoire-wide clonal relationships, systematically underestimated both the size of clonally related B-cell clusters and yielded inconsistent SHM frequencies. We demonstrate BRILIA's utility in B-cell repertoire studies related to VDJ gene usage, mechanisms for adenosine mutations, and SHM hot spot motifs. Furthermore, we show that the complete gene usage annotation and SHM identification across the entire CDR3 are essential for studying the B-cell affinity maturation process through immunosequencing methods.

Dataset Information

Entropic effects in cell lineage tree packings.

Publications

Entropic effects in cell lineage tree packings.

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