Live cell-lineage tracing and machine learning reveal patterns of organ regeneration

Despite the intrinsically stochastic nature of damage, sensory organs recapitulate normal architecture during repair to maintain function. Here we present a quantitative approach that combines live cell-lineage tracing and multifactorial classification by machine learning to reveal how cell identity...

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Main Authors: Oriol Viader-Llargués, Valerio Lupperger, Laura Pola-Morell, Carsten Marr, Hernán López-Schier
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2018-03-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/30823
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author Oriol Viader-Llargués
Valerio Lupperger
Laura Pola-Morell
Carsten Marr
Hernán López-Schier
author_facet Oriol Viader-Llargués
Valerio Lupperger
Laura Pola-Morell
Carsten Marr
Hernán López-Schier
author_sort Oriol Viader-Llargués
collection DOAJ
description Despite the intrinsically stochastic nature of damage, sensory organs recapitulate normal architecture during repair to maintain function. Here we present a quantitative approach that combines live cell-lineage tracing and multifactorial classification by machine learning to reveal how cell identity and localization are coordinated during organ regeneration. We use the superficial neuromasts in larval zebrafish, which contain three cell classes organized in radial symmetry and a single planar-polarity axis. Visualization of cell-fate transitions at high temporal resolution shows that neuromasts regenerate isotropically to recover geometric order, proportions and polarity with exceptional accuracy. We identify mediolateral position within the growing tissue as the best predictor of cell-fate acquisition. We propose a self-regulatory mechanism that guides the regenerative process to identical outcome with minimal extrinsic information. The integrated approach that we have developed is simple and broadly applicable, and should help define predictive signatures of cellular behavior during the construction of complex tissues.
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spelling doaj.art-7b8f26c13b5d4f44b8b89e32366ab7ae2022-12-22T03:52:10ZengeLife Sciences Publications LtdeLife2050-084X2018-03-01710.7554/eLife.30823Live cell-lineage tracing and machine learning reveal patterns of organ regenerationOriol Viader-Llargués0Valerio Lupperger1Laura Pola-Morell2Carsten Marr3Hernán López-Schier4https://orcid.org/0000-0001-7925-7439Unit Sensory Biology & Organogenesis, Helmholtz Zentrum München, Neuherberg, Germany; Laboratory of Sensory Cell Biology, Centre for Genomic Regulation, Barcelona, SpainInstitute of Computational Biology, Helmholtz Zentrum München, Neuherberg, GermanyUnit Sensory Biology & Organogenesis, Helmholtz Zentrum München, Neuherberg, Germany; Laboratory of Sensory Cell Biology, Centre for Genomic Regulation, Barcelona, SpainInstitute of Computational Biology, Helmholtz Zentrum München, Neuherberg, GermanyUnit Sensory Biology & Organogenesis, Helmholtz Zentrum München, Neuherberg, Germany; Laboratory of Sensory Cell Biology, Centre for Genomic Regulation, Barcelona, SpainDespite the intrinsically stochastic nature of damage, sensory organs recapitulate normal architecture during repair to maintain function. Here we present a quantitative approach that combines live cell-lineage tracing and multifactorial classification by machine learning to reveal how cell identity and localization are coordinated during organ regeneration. We use the superficial neuromasts in larval zebrafish, which contain three cell classes organized in radial symmetry and a single planar-polarity axis. Visualization of cell-fate transitions at high temporal resolution shows that neuromasts regenerate isotropically to recover geometric order, proportions and polarity with exceptional accuracy. We identify mediolateral position within the growing tissue as the best predictor of cell-fate acquisition. We propose a self-regulatory mechanism that guides the regenerative process to identical outcome with minimal extrinsic information. The integrated approach that we have developed is simple and broadly applicable, and should help define predictive signatures of cellular behavior during the construction of complex tissues.https://elifesciences.org/articles/30823regenerationsensory organneuromastmachine learninglive imagingclonal analysis
spellingShingle Oriol Viader-Llargués
Valerio Lupperger
Laura Pola-Morell
Carsten Marr
Hernán López-Schier
Live cell-lineage tracing and machine learning reveal patterns of organ regeneration
eLife
regeneration
sensory organ
neuromast
machine learning
live imaging
clonal analysis
title Live cell-lineage tracing and machine learning reveal patterns of organ regeneration
title_full Live cell-lineage tracing and machine learning reveal patterns of organ regeneration
title_fullStr Live cell-lineage tracing and machine learning reveal patterns of organ regeneration
title_full_unstemmed Live cell-lineage tracing and machine learning reveal patterns of organ regeneration
title_short Live cell-lineage tracing and machine learning reveal patterns of organ regeneration
title_sort live cell lineage tracing and machine learning reveal patterns of organ regeneration
topic regeneration
sensory organ
neuromast
machine learning
live imaging
clonal analysis
url https://elifesciences.org/articles/30823
work_keys_str_mv AT oriolviaderllargues livecelllineagetracingandmachinelearningrevealpatternsoforganregeneration
AT valeriolupperger livecelllineagetracingandmachinelearningrevealpatternsoforganregeneration
AT laurapolamorell livecelllineagetracingandmachinelearningrevealpatternsoforganregeneration
AT carstenmarr livecelllineagetracingandmachinelearningrevealpatternsoforganregeneration
AT hernanlopezschier livecelllineagetracingandmachinelearningrevealpatternsoforganregeneration