Evidence that the human cell cycle is a series of uncoupled, memoryless phases

Abstract The cell cycle is canonically described as a series of four consecutive phases: G1, S, G2, and M. In single cells, the duration of each phase varies, but the quantitative laws that govern phase durations are not well understood. Using time‐lapse microscopy, we found that each phase duration...

Full description

Saved in:
Bibliographic Details
Main Authors: Hui Xiao Chao, Randy I Fakhreddin, Hristo K Shimerov, Katarzyna M Kedziora, Rashmi J Kumar, Joanna Perez, Juanita C Limas, Gavin D Grant, Jeanette Gowen Cook, Gaorav P Gupta, Jeremy E Purvis
Format: Article
Language:English
Published: Springer Nature 2019-03-01
Series:Molecular Systems Biology
Subjects:
Online Access:https://doi.org/10.15252/msb.20188604
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849389062773800960
author Hui Xiao Chao
Randy I Fakhreddin
Hristo K Shimerov
Katarzyna M Kedziora
Rashmi J Kumar
Joanna Perez
Juanita C Limas
Gavin D Grant
Jeanette Gowen Cook
Gaorav P Gupta
Jeremy E Purvis
author_facet Hui Xiao Chao
Randy I Fakhreddin
Hristo K Shimerov
Katarzyna M Kedziora
Rashmi J Kumar
Joanna Perez
Juanita C Limas
Gavin D Grant
Jeanette Gowen Cook
Gaorav P Gupta
Jeremy E Purvis
author_sort Hui Xiao Chao
collection DOAJ
description Abstract The cell cycle is canonically described as a series of four consecutive phases: G1, S, G2, and M. In single cells, the duration of each phase varies, but the quantitative laws that govern phase durations are not well understood. Using time‐lapse microscopy, we found that each phase duration follows an Erlang distribution and is statistically independent from other phases. We challenged this observation by perturbing phase durations through oncogene activation, inhibition of DNA synthesis, reduced temperature, and DNA damage. Despite large changes in durations in cell populations, phase durations remained uncoupled in individual cells. These results suggested that the independence of phase durations may arise from a large number of molecular factors that each exerts a minor influence on the rate of cell cycle progression. We tested this model by experimentally forcing phase coupling through inhibition of cyclin‐dependent kinase 2 (CDK2) or overexpression of cyclin D. Our work provides an explanation for the historical observation that phase durations are both inherited and independent and suggests how cell cycle progression may be altered in disease states.
format Article
id doaj-art-81290e9fcfee4492b0f34caf81dfef6d
institution Kabale University
issn 1744-4292
language English
publishDate 2019-03-01
publisher Springer Nature
record_format Article
series Molecular Systems Biology
spelling doaj-art-81290e9fcfee4492b0f34caf81dfef6d2025-08-20T03:42:04ZengSpringer NatureMolecular Systems Biology1744-42922019-03-0115311910.15252/msb.20188604Evidence that the human cell cycle is a series of uncoupled, memoryless phasesHui Xiao Chao0Randy I Fakhreddin1Hristo K Shimerov2Katarzyna M Kedziora3Rashmi J Kumar4Joanna Perez5Juanita C Limas6Gavin D Grant7Jeanette Gowen Cook8Gaorav P Gupta9Jeremy E Purvis10Department of Genetics, University of North Carolina at Chapel HillDepartment of Genetics, University of North Carolina at Chapel HillDepartment of Genetics, University of North Carolina at Chapel HillDepartment of Genetics, University of North Carolina at Chapel HillDepartment of Genetics, University of North Carolina at Chapel HillDepartment of Biochemistry and Biophysics, University of North Carolina at Chapel HillDepartment of Pharmacology, University of North Carolina at Chapel HillDepartment of Biochemistry and Biophysics, University of North Carolina at Chapel HillDepartment of Biochemistry and Biophysics, University of North Carolina at Chapel HillLineberger Comprehensive Cancer Center, University of North Carolina at Chapel HillDepartment of Genetics, University of North Carolina at Chapel HillAbstract The cell cycle is canonically described as a series of four consecutive phases: G1, S, G2, and M. In single cells, the duration of each phase varies, but the quantitative laws that govern phase durations are not well understood. Using time‐lapse microscopy, we found that each phase duration follows an Erlang distribution and is statistically independent from other phases. We challenged this observation by perturbing phase durations through oncogene activation, inhibition of DNA synthesis, reduced temperature, and DNA damage. Despite large changes in durations in cell populations, phase durations remained uncoupled in individual cells. These results suggested that the independence of phase durations may arise from a large number of molecular factors that each exerts a minor influence on the rate of cell cycle progression. We tested this model by experimentally forcing phase coupling through inhibition of cyclin‐dependent kinase 2 (CDK2) or overexpression of cyclin D. Our work provides an explanation for the historical observation that phase durations are both inherited and independent and suggests how cell cycle progression may be altered in disease states.https://doi.org/10.15252/msb.20188604cell cyclecell‐to‐cell variabilitycomputational systems biologyErlang modelsingle‐cell dynamics
spellingShingle Hui Xiao Chao
Randy I Fakhreddin
Hristo K Shimerov
Katarzyna M Kedziora
Rashmi J Kumar
Joanna Perez
Juanita C Limas
Gavin D Grant
Jeanette Gowen Cook
Gaorav P Gupta
Jeremy E Purvis
Evidence that the human cell cycle is a series of uncoupled, memoryless phases
Molecular Systems Biology
cell cycle
cell‐to‐cell variability
computational systems biology
Erlang model
single‐cell dynamics
title Evidence that the human cell cycle is a series of uncoupled, memoryless phases
title_full Evidence that the human cell cycle is a series of uncoupled, memoryless phases
title_fullStr Evidence that the human cell cycle is a series of uncoupled, memoryless phases
title_full_unstemmed Evidence that the human cell cycle is a series of uncoupled, memoryless phases
title_short Evidence that the human cell cycle is a series of uncoupled, memoryless phases
title_sort evidence that the human cell cycle is a series of uncoupled memoryless phases
topic cell cycle
cell‐to‐cell variability
computational systems biology
Erlang model
single‐cell dynamics
url https://doi.org/10.15252/msb.20188604
work_keys_str_mv AT huixiaochao evidencethatthehumancellcycleisaseriesofuncoupledmemorylessphases
AT randyifakhreddin evidencethatthehumancellcycleisaseriesofuncoupledmemorylessphases
AT hristokshimerov evidencethatthehumancellcycleisaseriesofuncoupledmemorylessphases
AT katarzynamkedziora evidencethatthehumancellcycleisaseriesofuncoupledmemorylessphases
AT rashmijkumar evidencethatthehumancellcycleisaseriesofuncoupledmemorylessphases
AT joannaperez evidencethatthehumancellcycleisaseriesofuncoupledmemorylessphases
AT juanitaclimas evidencethatthehumancellcycleisaseriesofuncoupledmemorylessphases
AT gavindgrant evidencethatthehumancellcycleisaseriesofuncoupledmemorylessphases
AT jeanettegowencook evidencethatthehumancellcycleisaseriesofuncoupledmemorylessphases
AT gaoravpgupta evidencethatthehumancellcycleisaseriesofuncoupledmemorylessphases
AT jeremyepurvis evidencethatthehumancellcycleisaseriesofuncoupledmemorylessphases