Reconstruction of Contemporary Human Stem Cell Dynamics with Oscillatory Molecular Clocks

Author:

Gabbutt CalumORCID,Schenck Ryan OORCID,Weisenberger DanORCID,Kimberley ChristopherORCID,Berner AlisonORCID,Househam JacobORCID,Lakatos EszterORCID,Robertson-Tessi MarkORCID,Martin IsabelORCID,Patel RoshaniORCID,Clark SueORCID,Latchford AndrewORCID,Barnes ChristopherORCID,Leedham Simon JORCID,Anderson Alexander RAORCID,Graham Trevor AORCID,Shibata DarrylORCID

Abstract

AbstractMolecular clocks record cellular ancestry. However, currently used clocks ‘tick too slowly’ to measure the short-timescale dynamics of cellular renewal in adult tissues. Here we develop ‘rapidly oscillating DNA methylation clocks’ where ongoing (de)methylation causes the clock to ‘tick-tock’ back-and-forth between methylated and unmethylated states like a pendulum. We identify oscillators using standard methylation arrays and develop a mathematical modelling framework to quantitatively measure human adult stem cell dynamics from these data. Small intestinal crypts were inferred to contain slightly more stem cells than colon (6.5 ± 1.0 vs 5.8 ± 1.7 stem cells/crypt) with slower stem cell replacement in small intestine (0.79 ± 0.5 vs 1.1 ± 0.8 replacements/stem cell/year). Germline APC mutation increased the number of replacements per crypt (13.0 ± 2.4 replacements/crypt/year vs 6.9 ± 4.6 for healthy colon). In blood, we measure rapid expansion of acute leukaemia and slower growth of chronic disease. Rapidly oscillating molecular clocks are a new methodology to quantitatively measure human somatic cell dynamics.

Publisher

Cold Spring Harbor Laboratory

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