Self-organization of genome expression from embryo to terminal cell fate: Single-cell statistical mechanics of biological regulation

Alessandro Giuliani, Masa Tsuchiya, Kenichi Yoshikawa

Research output: Contribution to journalArticle

Abstract

A statistical mechanical mean-field approach to the temporal development of biological regulation provides a phenomenological, but basic description of the dynamical behavior of genome expression in terms of autonomous self-organization with a critical transition (Self-Organized Criticality: SOC). This approach reveals the basis of self-regulation/organization of genome expression, where the extreme complexity of living matter precludes any strict mechanistic approach. The self-organization in SOC involves two critical behaviors: scaling-divergent behavior (genome avalanche) and sandpile-type critical behavior. Genome avalanche patterns-competition between order (scaling) and disorder (divergence) reflect the opposite sequence of events characterizing the self-organization process in embryo development and helper T17 terminal cell differentiation, respectively. On the other hand, the temporal development of sandpile-type criticality (the degree of SOC control) in mouse embryo suggests the existence of an SOC control landscape with a critical transition state (i.e., the erasure of zygote-state criticality). This indicates that a phase transition of the mouse genome before and after reprogramming (immediately after the late 2-cell state) occurs through a dynamical change in a control parameter. This result provides a quantitative open-thermodynamic appreciation of the still largely qualitative notion of the epigenetic landscape. Our results suggest: (i) the existence of coherent waves of condensation/de-condensation in chromatin, which are transmitted across regions of different gene-expression levels along the genome; and (ii) essentially the same critical dynamics we observed for cell-differentiation processes exist in overall RNA expression during embryo development, which is particularly relevant because it gives further proof of SOC control of overall expression as a universal feature.

Original languageEnglish
Article number13
JournalEntropy
Volume20
Issue number1
DOIs
Publication statusPublished - Jan 1 2018

Fingerprint

genome
embryos
statistical mechanics
cells
avalanches
mice
zygotes
condensation
scaling
chromatin
gene expression
divergence
disorders
thermodynamics

Keywords

  • Autonomous self-organized criticality
  • Critical transition state
  • Early embryo development
  • Genome avalanche
  • Reprogramming
  • Self-organization
  • Single-cell differentiation
  • Single-cell genome dynamics
  • Statistical thermodynamics

ASJC Scopus subject areas

  • Physics and Astronomy(all)

Cite this

Self-organization of genome expression from embryo to terminal cell fate : Single-cell statistical mechanics of biological regulation. / Giuliani, Alessandro; Tsuchiya, Masa; Yoshikawa, Kenichi.

In: Entropy, Vol. 20, No. 1, 13, 01.01.2018.

Research output: Contribution to journalArticle

@article{c3cf07c479ed45afa0fdb58bb267de0c,
title = "Self-organization of genome expression from embryo to terminal cell fate: Single-cell statistical mechanics of biological regulation",
abstract = "A statistical mechanical mean-field approach to the temporal development of biological regulation provides a phenomenological, but basic description of the dynamical behavior of genome expression in terms of autonomous self-organization with a critical transition (Self-Organized Criticality: SOC). This approach reveals the basis of self-regulation/organization of genome expression, where the extreme complexity of living matter precludes any strict mechanistic approach. The self-organization in SOC involves two critical behaviors: scaling-divergent behavior (genome avalanche) and sandpile-type critical behavior. Genome avalanche patterns-competition between order (scaling) and disorder (divergence) reflect the opposite sequence of events characterizing the self-organization process in embryo development and helper T17 terminal cell differentiation, respectively. On the other hand, the temporal development of sandpile-type criticality (the degree of SOC control) in mouse embryo suggests the existence of an SOC control landscape with a critical transition state (i.e., the erasure of zygote-state criticality). This indicates that a phase transition of the mouse genome before and after reprogramming (immediately after the late 2-cell state) occurs through a dynamical change in a control parameter. This result provides a quantitative open-thermodynamic appreciation of the still largely qualitative notion of the epigenetic landscape. Our results suggest: (i) the existence of coherent waves of condensation/de-condensation in chromatin, which are transmitted across regions of different gene-expression levels along the genome; and (ii) essentially the same critical dynamics we observed for cell-differentiation processes exist in overall RNA expression during embryo development, which is particularly relevant because it gives further proof of SOC control of overall expression as a universal feature.",
keywords = "Autonomous self-organized criticality, Critical transition state, Early embryo development, Genome avalanche, Reprogramming, Self-organization, Single-cell differentiation, Single-cell genome dynamics, Statistical thermodynamics",
author = "Alessandro Giuliani and Masa Tsuchiya and Kenichi Yoshikawa",
year = "2018",
month = "1",
day = "1",
doi = "10.3390/e20010013",
language = "English",
volume = "20",
journal = "Entropy",
issn = "1099-4300",
publisher = "Multidisciplinary Digital Publishing Institute (MDPI)",
number = "1",

}

TY - JOUR

T1 - Self-organization of genome expression from embryo to terminal cell fate

T2 - Single-cell statistical mechanics of biological regulation

AU - Giuliani, Alessandro

AU - Tsuchiya, Masa

AU - Yoshikawa, Kenichi

PY - 2018/1/1

Y1 - 2018/1/1

N2 - A statistical mechanical mean-field approach to the temporal development of biological regulation provides a phenomenological, but basic description of the dynamical behavior of genome expression in terms of autonomous self-organization with a critical transition (Self-Organized Criticality: SOC). This approach reveals the basis of self-regulation/organization of genome expression, where the extreme complexity of living matter precludes any strict mechanistic approach. The self-organization in SOC involves two critical behaviors: scaling-divergent behavior (genome avalanche) and sandpile-type critical behavior. Genome avalanche patterns-competition between order (scaling) and disorder (divergence) reflect the opposite sequence of events characterizing the self-organization process in embryo development and helper T17 terminal cell differentiation, respectively. On the other hand, the temporal development of sandpile-type criticality (the degree of SOC control) in mouse embryo suggests the existence of an SOC control landscape with a critical transition state (i.e., the erasure of zygote-state criticality). This indicates that a phase transition of the mouse genome before and after reprogramming (immediately after the late 2-cell state) occurs through a dynamical change in a control parameter. This result provides a quantitative open-thermodynamic appreciation of the still largely qualitative notion of the epigenetic landscape. Our results suggest: (i) the existence of coherent waves of condensation/de-condensation in chromatin, which are transmitted across regions of different gene-expression levels along the genome; and (ii) essentially the same critical dynamics we observed for cell-differentiation processes exist in overall RNA expression during embryo development, which is particularly relevant because it gives further proof of SOC control of overall expression as a universal feature.

AB - A statistical mechanical mean-field approach to the temporal development of biological regulation provides a phenomenological, but basic description of the dynamical behavior of genome expression in terms of autonomous self-organization with a critical transition (Self-Organized Criticality: SOC). This approach reveals the basis of self-regulation/organization of genome expression, where the extreme complexity of living matter precludes any strict mechanistic approach. The self-organization in SOC involves two critical behaviors: scaling-divergent behavior (genome avalanche) and sandpile-type critical behavior. Genome avalanche patterns-competition between order (scaling) and disorder (divergence) reflect the opposite sequence of events characterizing the self-organization process in embryo development and helper T17 terminal cell differentiation, respectively. On the other hand, the temporal development of sandpile-type criticality (the degree of SOC control) in mouse embryo suggests the existence of an SOC control landscape with a critical transition state (i.e., the erasure of zygote-state criticality). This indicates that a phase transition of the mouse genome before and after reprogramming (immediately after the late 2-cell state) occurs through a dynamical change in a control parameter. This result provides a quantitative open-thermodynamic appreciation of the still largely qualitative notion of the epigenetic landscape. Our results suggest: (i) the existence of coherent waves of condensation/de-condensation in chromatin, which are transmitted across regions of different gene-expression levels along the genome; and (ii) essentially the same critical dynamics we observed for cell-differentiation processes exist in overall RNA expression during embryo development, which is particularly relevant because it gives further proof of SOC control of overall expression as a universal feature.

KW - Autonomous self-organized criticality

KW - Critical transition state

KW - Early embryo development

KW - Genome avalanche

KW - Reprogramming

KW - Self-organization

KW - Single-cell differentiation

KW - Single-cell genome dynamics

KW - Statistical thermodynamics

UR - http://www.scopus.com/inward/record.url?scp=85040609483&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85040609483&partnerID=8YFLogxK

U2 - 10.3390/e20010013

DO - 10.3390/e20010013

M3 - Article

AN - SCOPUS:85040609483

VL - 20

JO - Entropy

JF - Entropy

SN - 1099-4300

IS - 1

M1 - 13

ER -