A Subpopulation of Smooth Muscle Cells, Derived from Melanocyte-Competent Precursors, Prevents Patent Ductus Arteriosus

Ichiro Yajima, Sophie Colombo, Isabel Puig, Delphine Champeval, Mayuko Kumasaka, Elodie Belloir, Jacky Bonaventure, Manuel Mark, Hiroaki Yamamoto, Mark M. Taketo, Philippe Choquet, Heather C. Etchevers, Friedrich Beermann, Véronique Delmas, Laurent Monassier, Lionel Larue

Research output: Contribution to journalArticle

9 Citations (Scopus)

Abstract

Background: Patent ductus arteriosus is a life-threatening condition frequent in premature newborns but also present in some term infants. Current mouse models of this malformation generally lead to perinatal death, not reproducing the full phenotypic spectrum in humans, in whom genetic inheritance appears complex. The ductus arteriosus (DA), a temporary fetal vessel that bypasses the lungs by shunting the aortic arch to the pulmonary artery, is constituted by smooth muscle cells of distinct origins (SMC1 and SMC2) and many fewer melanocytes. To understand novel mechanisms preventing DA closure at birth, we evaluated the importance of cell fate specification in SMC that form the DA during embryonic development. Upon specific Tyr::Cre-driven activation of Wnt/β-catenin signaling at the time of cell fate specification, melanocytes replaced the SMC2 population of the DA, suggesting that SMC2 and melanocytes have a common precursor. The number of SMC1 in the DA remained similar to that in controls, but insufficient to allow full DA closure at birth. Thus, there was no cellular compensation by SMC1 for the loss of SMC2. Mice in which only melanocytes were genetically ablated after specification from their potential common precursor with SMC2, demonstrated that differentiated melanocytes themselves do not affect DA closure. Loss of the SMC2 population, independent of the presence of melanocytes, is therefore a cause of patent ductus arteriosus and premature death in the first months of life. Our results indicate that patent ductus arteriosus can result from the insufficient differentiation, proliferation, or contractility of a specific smooth muscle subpopulation that shares a common neural crest precursor with cardiovascular melanocytes.

Original languageEnglish
Article numbere53183
JournalPLoS ONE
Volume8
Issue number1
DOIs
Publication statusPublished - 2013 Jan 31
Externally publishedYes

Fingerprint

ductus arteriosus
patent ductus arteriosus
melanocytes
smooth muscle
myocytes
Muscle
Cells
Specifications
Catenins
Arches
Chemical activation
death
neural crest
pulmonary artery
inheritance (genetics)
neonates
embryogenesis
animal models
lungs
cells

ASJC Scopus subject areas

  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

Cite this

A Subpopulation of Smooth Muscle Cells, Derived from Melanocyte-Competent Precursors, Prevents Patent Ductus Arteriosus. / Yajima, Ichiro; Colombo, Sophie; Puig, Isabel; Champeval, Delphine; Kumasaka, Mayuko; Belloir, Elodie; Bonaventure, Jacky; Mark, Manuel; Yamamoto, Hiroaki; Taketo, Mark M.; Choquet, Philippe; Etchevers, Heather C.; Beermann, Friedrich; Delmas, Véronique; Monassier, Laurent; Larue, Lionel.

In: PLoS ONE, Vol. 8, No. 1, e53183, 31.01.2013.

Research output: Contribution to journalArticle

Yajima, I, Colombo, S, Puig, I, Champeval, D, Kumasaka, M, Belloir, E, Bonaventure, J, Mark, M, Yamamoto, H, Taketo, MM, Choquet, P, Etchevers, HC, Beermann, F, Delmas, V, Monassier, L & Larue, L 2013, 'A Subpopulation of Smooth Muscle Cells, Derived from Melanocyte-Competent Precursors, Prevents Patent Ductus Arteriosus', PLoS ONE, vol. 8, no. 1, e53183. https://doi.org/10.1371/journal.pone.0053183
Yajima, Ichiro ; Colombo, Sophie ; Puig, Isabel ; Champeval, Delphine ; Kumasaka, Mayuko ; Belloir, Elodie ; Bonaventure, Jacky ; Mark, Manuel ; Yamamoto, Hiroaki ; Taketo, Mark M. ; Choquet, Philippe ; Etchevers, Heather C. ; Beermann, Friedrich ; Delmas, Véronique ; Monassier, Laurent ; Larue, Lionel. / A Subpopulation of Smooth Muscle Cells, Derived from Melanocyte-Competent Precursors, Prevents Patent Ductus Arteriosus. In: PLoS ONE. 2013 ; Vol. 8, No. 1.
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