Transit amplifying cells coordinate mouse incisor mesenchymal stem cell activation

Jemma Victoria Walker; Heng Zhuang; Donald Singer; Charlotte Sara Illsley; Wai Ling Kok; Kishor K. Sivaraj; Yan Gao; Chloe Bolton; Yuying Liu; Mengyuan Zhao; Portia Rebecca Clare Grayson; Shuang Wang; Jana Karbanová; Tim Lee; Stefano Ardu; Qingguo Lai; Jihui Liu; Moustapha Kassem; Shuo Chen; Kai Yang; Yuxing Bai; Christopher Tredwin; Alexander C. Zambon; Denis Corbeil; Ralf Adams; Basem M. Abdallah; Bing Hu

doi:10.1038/s41467-019-11611-0

Transit amplifying cells coordinate mouse incisor mesenchymal stem cell activation

Jemma Victoria Walker
, Heng Zhuang
, Donald Singer
, Charlotte Sara Illsley
, Wai Ling Kok
, Kishor K. Sivaraj
, Yan Gao
, Chloe Bolton
, Yuying Liu
, Mengyuan Zhao
, Portia Rebecca Clare Grayson
, Shuang Wang
, Jana Karbanová
, Tim Lee
, Stefano Ardu
, Qingguo Lai
, Jihui Liu
, Moustapha Kassem
, Shuo Chen
, Kai Yang

Yuxing Bai, Christopher Tredwin, Alexander C. Zambon, Denis Corbeil, Ralf Adams, Basem M. Abdallah, Bing Hu^*

^*Corresponding author for this work

University of Plymouth
Peking University
Taikang Bybo Dental Group Beijing
University of Münster
Capital Medical University
Shenyang Stomatological Hospital
Beijing Stomatological Hospital
National University of Singapore
Technical University of Denmark
Scripps Colleges
University of Geneva
Shandong University
The University of Texas Health Science Center at San Antonio
University of Copenhagen
King Faisal University

Research output: Contribution to journal › Journal article › Research › peer-review

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Abstract

Stem cells (SCs) receive inductive cues from the surrounding microenvironment and cells. Limited molecular evidence has connected tissue-specific mesenchymal stem cells (MSCs) with mesenchymal transit amplifying cells (MTACs). Using mouse incisor as the model, we discover a population of MSCs neibouring to the MTACs and epithelial SCs. With Notch signaling as the key regulator, we disclose molecular proof and lineage tracing evidence showing the distinct MSCs contribute to incisor MTACs and the other mesenchymal cell lineages. MTACs can feedback and regulate the homeostasis and activation of CL-MSCs through Delta-like 1 homolog (Dlk1), which balances MSCs-MTACs number and the lineage differentiation. Dlk1’s function on SCs priming and self-renewal depends on its biological forms and its gene expression is under dynamic epigenetic control. Our findings can be validated in clinical samples and applied to accelerate tooth wound healing, providing an intriguing insight of how to direct SCs towards tissue regeneration.

Original language	English
Article number	3596
Journal	Nature Communications
Volume	10
Issue number	1
Number of pages	18
ISSN	2041-1723
DOIs	https://doi.org/10.1038/s41467-019-11611-0
Publication status	Published - 9. Aug 2019

Funding

We would like to thank G.P. Dotto for initial support of the project; M.C. Reymond for assisting SEM; N. Ditzel for technical assistance of animal breeding, and A. Miyawaki for mAG-hGeminin (1/110)-pCSII-EF-MCS and mCherry-hCdt1(30/120)-pCSII-EF-MCS vectors. This work was supported by the National Natural Science Foundation of China to H.Z. (30801289 and 81371138), National Institutes of Health to S.C. (RO1DE019802), the Deutsche Forschungsgemeinschaft (SFB 655 B3) to D.C., the European Union Marie Skłodowska-Curie Actions (618930, OralStem FP7-PEOPLE-2013-CIG), the European Regional Development Fund and the Biotechnology and Biological Sciences Research Council of the UK (BB/L02392X/1) to B.H.

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Transit amplifying cells coordinate mouse incisor mesenchymal stem cell activationFinal published version, 13 MBLicence: CC BY

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Walker, J. V., Zhuang, H., Singer, D., Illsley, C. S., Kok, W. L., Sivaraj, K. K., Gao, Y., Bolton, C., Liu, Y., Zhao, M., Grayson, P. R. C., Wang, S., Karbanová, J., Lee, T., Ardu, S., Lai, Q., Liu, J., Kassem, M., Chen, S., ... Hu, B. (2019). Transit amplifying cells coordinate mouse incisor mesenchymal stem cell activation. Nature Communications, 10(1), Article 3596. https://doi.org/10.1038/s41467-019-11611-0

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title = "Transit amplifying cells coordinate mouse incisor mesenchymal stem cell activation",

abstract = "Stem cells (SCs) receive inductive cues from the surrounding microenvironment and cells. Limited molecular evidence has connected tissue-specific mesenchymal stem cells (MSCs) with mesenchymal transit amplifying cells (MTACs). Using mouse incisor as the model, we discover a population of MSCs neibouring to the MTACs and epithelial SCs. With Notch signaling as the key regulator, we disclose molecular proof and lineage tracing evidence showing the distinct MSCs contribute to incisor MTACs and the other mesenchymal cell lineages. MTACs can feedback and regulate the homeostasis and activation of CL-MSCs through Delta-like 1 homolog (Dlk1), which balances MSCs-MTACs number and the lineage differentiation. Dlk1{\textquoteright}s function on SCs priming and self-renewal depends on its biological forms and its gene expression is under dynamic epigenetic control. Our findings can be validated in clinical samples and applied to accelerate tooth wound healing, providing an intriguing insight of how to direct SCs towards tissue regeneration.",

author = "Walker, \{Jemma Victoria\} and Heng Zhuang and Donald Singer and Illsley, \{Charlotte Sara\} and Kok, \{Wai Ling\} and Sivaraj, \{Kishor K.\} and Yan Gao and Chloe Bolton and Yuying Liu and Mengyuan Zhao and Grayson, \{Portia Rebecca Clare\} and Shuang Wang and Jana Karbanov{\'a} and Tim Lee and Stefano Ardu and Qingguo Lai and Jihui Liu and Moustapha Kassem and Shuo Chen and Kai Yang and Yuxing Bai and Christopher Tredwin and Zambon, \{Alexander C.\} and Denis Corbeil and Ralf Adams and Abdallah, \{Basem M.\} and Bing Hu",

year = "2019",

month = aug,

day = "9",

doi = "10.1038/s41467-019-11611-0",

language = "English",

volume = "10",

journal = "Nature Communications",

issn = "2041-1723",

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Walker, JV, Zhuang, H, Singer, D, Illsley, CS, Kok, WL, Sivaraj, KK, Gao, Y, Bolton, C, Liu, Y, Zhao, M, Grayson, PRC, Wang, S, Karbanová, J, Lee, T, Ardu, S, Lai, Q, Liu, J, Kassem, M, Chen, S, Yang, K, Bai, Y, Tredwin, C, Zambon, AC, Corbeil, D, Adams, R, Abdallah, BM & Hu, B 2019, 'Transit amplifying cells coordinate mouse incisor mesenchymal stem cell activation', Nature Communications, vol. 10, no. 1, 3596. https://doi.org/10.1038/s41467-019-11611-0

TY - JOUR

T1 - Transit amplifying cells coordinate mouse incisor mesenchymal stem cell activation

AU - Walker, Jemma Victoria

AU - Zhuang, Heng

AU - Singer, Donald

AU - Illsley, Charlotte Sara

AU - Kok, Wai Ling

AU - Sivaraj, Kishor K.

AU - Gao, Yan

AU - Bolton, Chloe

AU - Liu, Yuying

AU - Zhao, Mengyuan

AU - Grayson, Portia Rebecca Clare

AU - Wang, Shuang

AU - Karbanová, Jana

AU - Lee, Tim

AU - Ardu, Stefano

AU - Lai, Qingguo

AU - Liu, Jihui

AU - Kassem, Moustapha

AU - Chen, Shuo

AU - Yang, Kai

AU - Bai, Yuxing

AU - Tredwin, Christopher

AU - Zambon, Alexander C.

AU - Corbeil, Denis

AU - Adams, Ralf

AU - Abdallah, Basem M.

AU - Hu, Bing

PY - 2019/8/9

Y1 - 2019/8/9

N2 - Stem cells (SCs) receive inductive cues from the surrounding microenvironment and cells. Limited molecular evidence has connected tissue-specific mesenchymal stem cells (MSCs) with mesenchymal transit amplifying cells (MTACs). Using mouse incisor as the model, we discover a population of MSCs neibouring to the MTACs and epithelial SCs. With Notch signaling as the key regulator, we disclose molecular proof and lineage tracing evidence showing the distinct MSCs contribute to incisor MTACs and the other mesenchymal cell lineages. MTACs can feedback and regulate the homeostasis and activation of CL-MSCs through Delta-like 1 homolog (Dlk1), which balances MSCs-MTACs number and the lineage differentiation. Dlk1’s function on SCs priming and self-renewal depends on its biological forms and its gene expression is under dynamic epigenetic control. Our findings can be validated in clinical samples and applied to accelerate tooth wound healing, providing an intriguing insight of how to direct SCs towards tissue regeneration.

AB - Stem cells (SCs) receive inductive cues from the surrounding microenvironment and cells. Limited molecular evidence has connected tissue-specific mesenchymal stem cells (MSCs) with mesenchymal transit amplifying cells (MTACs). Using mouse incisor as the model, we discover a population of MSCs neibouring to the MTACs and epithelial SCs. With Notch signaling as the key regulator, we disclose molecular proof and lineage tracing evidence showing the distinct MSCs contribute to incisor MTACs and the other mesenchymal cell lineages. MTACs can feedback and regulate the homeostasis and activation of CL-MSCs through Delta-like 1 homolog (Dlk1), which balances MSCs-MTACs number and the lineage differentiation. Dlk1’s function on SCs priming and self-renewal depends on its biological forms and its gene expression is under dynamic epigenetic control. Our findings can be validated in clinical samples and applied to accelerate tooth wound healing, providing an intriguing insight of how to direct SCs towards tissue regeneration.

U2 - 10.1038/s41467-019-11611-0

DO - 10.1038/s41467-019-11611-0

M3 - Journal article

C2 - 31399601

AN - SCOPUS:85070367007

SN - 2041-1723

VL - 10

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 3596

ER -

Transit amplifying cells coordinate mouse incisor mesenchymal stem cell activation

Abstract

Funding

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