Dynamic interaction networks in a hierarchically organized tissue

Abstract Intercellular (between cell) communication networks maintain homeostasis and coordinate regenerative and developmental cues in multicellular organisms. Despite the importance of intercellular networks in stem cell biology, their rules, structure and molecular components are poorly understoo...

Full description

Saved in:
Bibliographic Details
Main Authors: Daniel C Kirouac, Caryn Ito, Elizabeth Csaszar, Aline Roch, Mei Yu, Edward A Sykes, Gary D Bader, Peter W Zandstra
Format: Article
Language:English
Published: Springer Nature 2010-10-01
Series:Molecular Systems Biology
Subjects:
Online Access:https://doi.org/10.1038/msb.2010.71
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1849225763397566464
author Daniel C Kirouac
Caryn Ito
Elizabeth Csaszar
Aline Roch
Mei Yu
Edward A Sykes
Gary D Bader
Peter W Zandstra
author_facet Daniel C Kirouac
Caryn Ito
Elizabeth Csaszar
Aline Roch
Mei Yu
Edward A Sykes
Gary D Bader
Peter W Zandstra
author_sort Daniel C Kirouac
collection DOAJ
description Abstract Intercellular (between cell) communication networks maintain homeostasis and coordinate regenerative and developmental cues in multicellular organisms. Despite the importance of intercellular networks in stem cell biology, their rules, structure and molecular components are poorly understood. Herein, we describe the structure and dynamics of intercellular and intracellular networks in a stem cell derived, hierarchically organized tissue using experimental and theoretical analyses of cultured human umbilical cord blood progenitors. By integrating high‐throughput molecular profiling, database and literature mining, mechanistic modeling, and cell culture experiments, we show that secreted factor‐mediated intercellular communication networks regulate blood stem cell fate decisions. In particular, self‐renewal is modulated by a coupled positive–negative intercellular feedback circuit composed of megakaryocyte‐derived stimulatory growth factors (VEGF, PDGF, EGF, and serotonin) versus monocyte‐derived inhibitory factors (CCL3, CCL4, CXCL10, TGFB2, and TNFSF9). We reconstruct a stem cell intracellular network, and identify PI3K, Raf, Akt, and PLC as functionally distinct signal integration nodes, linking extracellular, and intracellular signaling. This represents the first systematic characterization of how stem cell fate decisions are regulated non‐autonomously through lineage‐specific interactions with differentiated progeny.
format Article
id doaj-art-58beec843042450bbc1c0ff43879ba37
institution Kabale University
issn 1744-4292
language English
publishDate 2010-10-01
publisher Springer Nature
record_format Article
series Molecular Systems Biology
spelling doaj-art-58beec843042450bbc1c0ff43879ba372025-08-24T12:00:37ZengSpringer NatureMolecular Systems Biology1744-42922010-10-016111610.1038/msb.2010.71Dynamic interaction networks in a hierarchically organized tissueDaniel C Kirouac0Caryn Ito1Elizabeth Csaszar2Aline Roch3Mei Yu4Edward A Sykes5Gary D Bader6Peter W Zandstra7Institute for Biomaterials and Biomedical Engineering, University of TorontoInstitute for Biomaterials and Biomedical Engineering, University of TorontoInstitute for Biomaterials and Biomedical Engineering, University of TorontoEcole Polytechnique Fédérale de LausanneInstitute for Biomaterials and Biomedical Engineering, University of TorontoInstitute for Biomaterials and Biomedical Engineering, University of TorontoTerrence Donnelly Centre for Cellular and Biomolecular Research, University of TorontoInstitute for Biomaterials and Biomedical Engineering, University of TorontoAbstract Intercellular (between cell) communication networks maintain homeostasis and coordinate regenerative and developmental cues in multicellular organisms. Despite the importance of intercellular networks in stem cell biology, their rules, structure and molecular components are poorly understood. Herein, we describe the structure and dynamics of intercellular and intracellular networks in a stem cell derived, hierarchically organized tissue using experimental and theoretical analyses of cultured human umbilical cord blood progenitors. By integrating high‐throughput molecular profiling, database and literature mining, mechanistic modeling, and cell culture experiments, we show that secreted factor‐mediated intercellular communication networks regulate blood stem cell fate decisions. In particular, self‐renewal is modulated by a coupled positive–negative intercellular feedback circuit composed of megakaryocyte‐derived stimulatory growth factors (VEGF, PDGF, EGF, and serotonin) versus monocyte‐derived inhibitory factors (CCL3, CCL4, CXCL10, TGFB2, and TNFSF9). We reconstruct a stem cell intracellular network, and identify PI3K, Raf, Akt, and PLC as functionally distinct signal integration nodes, linking extracellular, and intracellular signaling. This represents the first systematic characterization of how stem cell fate decisions are regulated non‐autonomously through lineage‐specific interactions with differentiated progeny.https://doi.org/10.1038/msb.2010.71cellular networkshematopoiesisintercellular signalingself‐renewalstem cells
spellingShingle Daniel C Kirouac
Caryn Ito
Elizabeth Csaszar
Aline Roch
Mei Yu
Edward A Sykes
Gary D Bader
Peter W Zandstra
Dynamic interaction networks in a hierarchically organized tissue
Molecular Systems Biology
cellular networks
hematopoiesis
intercellular signaling
self‐renewal
stem cells
title Dynamic interaction networks in a hierarchically organized tissue
title_full Dynamic interaction networks in a hierarchically organized tissue
title_fullStr Dynamic interaction networks in a hierarchically organized tissue
title_full_unstemmed Dynamic interaction networks in a hierarchically organized tissue
title_short Dynamic interaction networks in a hierarchically organized tissue
title_sort dynamic interaction networks in a hierarchically organized tissue
topic cellular networks
hematopoiesis
intercellular signaling
self‐renewal
stem cells
url https://doi.org/10.1038/msb.2010.71
work_keys_str_mv AT danielckirouac dynamicinteractionnetworksinahierarchicallyorganizedtissue
AT carynito dynamicinteractionnetworksinahierarchicallyorganizedtissue
AT elizabethcsaszar dynamicinteractionnetworksinahierarchicallyorganizedtissue
AT alineroch dynamicinteractionnetworksinahierarchicallyorganizedtissue
AT meiyu dynamicinteractionnetworksinahierarchicallyorganizedtissue
AT edwardasykes dynamicinteractionnetworksinahierarchicallyorganizedtissue
AT garydbader dynamicinteractionnetworksinahierarchicallyorganizedtissue
AT peterwzandstra dynamicinteractionnetworksinahierarchicallyorganizedtissue