14-3-3epsilon controls multiple developmental processes in the mouse heart

Adriana C. Gittenberger-de Groot, Tamara Hoppenbrouwers, Lucile Miquerol, Yasuhiro Kosaka, Robert E. Poelmann, Lambertus J. Wisse, H. Joseph Yost, Monique R.M. Jongbloed, Marco C. Deruiter, Luca Brunelli

Research output: Contribution to journalArticle

3 Citations (Scopus)

Abstract

Background:: 14-3-3ε plays an important role in the maturation of the compact ventricular myocardium by modulating the cardiomyocyte cell cycle via p27 kip1 . However, additional cardiac defects are possible given the ubiquitous expression pattern of this protein. Results:: Germ line deletion of 14-3-3ε led to malalignment of both the outflow tract (OFT) and atrioventricular (AV) cushions, with resulting tricuspid stenosis and atresia, mitral valve abnormalities, and perimembranous ventricular septal defects (VSDs). We confirmed myocardial non-compaction and detected a spongy septum with muscular VSDs and blebbing of the epicardium. These defects were associated with abnormal patterning of p27 kip1 expression in the subendocardial and possibly the epicardial cell populations. In addition to abnormal pharyngeal arch artery patterning, we found deep endocardial recesses and paucity of intramyocardial coronary vasculature as a result of defective coronary plexus remodeling. Conclusions:: The malalignment of both endocardial cushions provides a new explanation for tricuspid and mitral valve defects, while myocardial non-compaction provides the basis for the abnormal coronary vasculature patterning. These abnormalities might arise from p27 kip1 dysregulation and a resulting defect in epithelial-to-mesenchymal transformation. These data suggest that 14-3-3ε, in addition to left ventricular non-compaction (LVNC), might be linked to different forms of congenital heart disease (CHD). Developmental Dynamics 245:1107–1123, 2016.

Original languageEnglish (US)
Pages (from-to)1107-1123
Number of pages17
JournalDevelopmental Dynamics
Volume245
Issue number11
DOIs
StatePublished - Nov 1 2016

Fingerprint

Ventricular Heart Septal Defects
Endocardial Cushions
Tricuspid Atresia
Branchial Region
Epithelial-Mesenchymal Transition
Tricuspid Valve
Mitral Valve Stenosis
Pericardium
Blister
Mitral Valve
Cardiac Myocytes
Germ Cells
Heart Diseases
Myocardium
Cell Cycle
Arteries
Population
Proteins

Keywords

  • 14-3-3
  • cardiac outflow tract
  • coronary artery hypoplasia
  • endocardial cushion
  • heart development
  • mouse
  • myocardial hypoplasia
  • ventricular septal defect

ASJC Scopus subject areas

  • Developmental Biology

Cite this

Gittenberger-de Groot, A. C., Hoppenbrouwers, T., Miquerol, L., Kosaka, Y., Poelmann, R. E., Wisse, L. J., ... Brunelli, L. (2016). 14-3-3epsilon controls multiple developmental processes in the mouse heart. Developmental Dynamics, 245(11), 1107-1123. https://doi.org/10.1002/dvdy.24440

14-3-3epsilon controls multiple developmental processes in the mouse heart. / Gittenberger-de Groot, Adriana C.; Hoppenbrouwers, Tamara; Miquerol, Lucile; Kosaka, Yasuhiro; Poelmann, Robert E.; Wisse, Lambertus J.; Yost, H. Joseph; Jongbloed, Monique R.M.; Deruiter, Marco C.; Brunelli, Luca.

In: Developmental Dynamics, Vol. 245, No. 11, 01.11.2016, p. 1107-1123.

Research output: Contribution to journalArticle

Gittenberger-de Groot, AC, Hoppenbrouwers, T, Miquerol, L, Kosaka, Y, Poelmann, RE, Wisse, LJ, Yost, HJ, Jongbloed, MRM, Deruiter, MC & Brunelli, L 2016, '14-3-3epsilon controls multiple developmental processes in the mouse heart', Developmental Dynamics, vol. 245, no. 11, pp. 1107-1123. https://doi.org/10.1002/dvdy.24440
Gittenberger-de Groot AC, Hoppenbrouwers T, Miquerol L, Kosaka Y, Poelmann RE, Wisse LJ et al. 14-3-3epsilon controls multiple developmental processes in the mouse heart. Developmental Dynamics. 2016 Nov 1;245(11):1107-1123. https://doi.org/10.1002/dvdy.24440
Gittenberger-de Groot, Adriana C. ; Hoppenbrouwers, Tamara ; Miquerol, Lucile ; Kosaka, Yasuhiro ; Poelmann, Robert E. ; Wisse, Lambertus J. ; Yost, H. Joseph ; Jongbloed, Monique R.M. ; Deruiter, Marco C. ; Brunelli, Luca. / 14-3-3epsilon controls multiple developmental processes in the mouse heart. In: Developmental Dynamics. 2016 ; Vol. 245, No. 11. pp. 1107-1123.
@article{985a70ef83304ef3805a04da0a70fc1d,
title = "14-3-3epsilon controls multiple developmental processes in the mouse heart",
abstract = "Background:: 14-3-3ε plays an important role in the maturation of the compact ventricular myocardium by modulating the cardiomyocyte cell cycle via p27 kip1 . However, additional cardiac defects are possible given the ubiquitous expression pattern of this protein. Results:: Germ line deletion of 14-3-3ε led to malalignment of both the outflow tract (OFT) and atrioventricular (AV) cushions, with resulting tricuspid stenosis and atresia, mitral valve abnormalities, and perimembranous ventricular septal defects (VSDs). We confirmed myocardial non-compaction and detected a spongy septum with muscular VSDs and blebbing of the epicardium. These defects were associated with abnormal patterning of p27 kip1 expression in the subendocardial and possibly the epicardial cell populations. In addition to abnormal pharyngeal arch artery patterning, we found deep endocardial recesses and paucity of intramyocardial coronary vasculature as a result of defective coronary plexus remodeling. Conclusions:: The malalignment of both endocardial cushions provides a new explanation for tricuspid and mitral valve defects, while myocardial non-compaction provides the basis for the abnormal coronary vasculature patterning. These abnormalities might arise from p27 kip1 dysregulation and a resulting defect in epithelial-to-mesenchymal transformation. These data suggest that 14-3-3ε, in addition to left ventricular non-compaction (LVNC), might be linked to different forms of congenital heart disease (CHD). Developmental Dynamics 245:1107–1123, 2016.",
keywords = "14-3-3, cardiac outflow tract, coronary artery hypoplasia, endocardial cushion, heart development, mouse, myocardial hypoplasia, ventricular septal defect",
author = "{Gittenberger-de Groot}, {Adriana C.} and Tamara Hoppenbrouwers and Lucile Miquerol and Yasuhiro Kosaka and Poelmann, {Robert E.} and Wisse, {Lambertus J.} and Yost, {H. Joseph} and Jongbloed, {Monique R.M.} and Deruiter, {Marco C.} and Luca Brunelli",
year = "2016",
month = "11",
day = "1",
doi = "10.1002/dvdy.24440",
language = "English (US)",
volume = "245",
pages = "1107--1123",
journal = "Developmental Dynamics",
issn = "1058-8388",
publisher = "Wiley-Liss Inc.",
number = "11",

}

TY - JOUR

T1 - 14-3-3epsilon controls multiple developmental processes in the mouse heart

AU - Gittenberger-de Groot, Adriana C.

AU - Hoppenbrouwers, Tamara

AU - Miquerol, Lucile

AU - Kosaka, Yasuhiro

AU - Poelmann, Robert E.

AU - Wisse, Lambertus J.

AU - Yost, H. Joseph

AU - Jongbloed, Monique R.M.

AU - Deruiter, Marco C.

AU - Brunelli, Luca

PY - 2016/11/1

Y1 - 2016/11/1

N2 - Background:: 14-3-3ε plays an important role in the maturation of the compact ventricular myocardium by modulating the cardiomyocyte cell cycle via p27 kip1 . However, additional cardiac defects are possible given the ubiquitous expression pattern of this protein. Results:: Germ line deletion of 14-3-3ε led to malalignment of both the outflow tract (OFT) and atrioventricular (AV) cushions, with resulting tricuspid stenosis and atresia, mitral valve abnormalities, and perimembranous ventricular septal defects (VSDs). We confirmed myocardial non-compaction and detected a spongy septum with muscular VSDs and blebbing of the epicardium. These defects were associated with abnormal patterning of p27 kip1 expression in the subendocardial and possibly the epicardial cell populations. In addition to abnormal pharyngeal arch artery patterning, we found deep endocardial recesses and paucity of intramyocardial coronary vasculature as a result of defective coronary plexus remodeling. Conclusions:: The malalignment of both endocardial cushions provides a new explanation for tricuspid and mitral valve defects, while myocardial non-compaction provides the basis for the abnormal coronary vasculature patterning. These abnormalities might arise from p27 kip1 dysregulation and a resulting defect in epithelial-to-mesenchymal transformation. These data suggest that 14-3-3ε, in addition to left ventricular non-compaction (LVNC), might be linked to different forms of congenital heart disease (CHD). Developmental Dynamics 245:1107–1123, 2016.

AB - Background:: 14-3-3ε plays an important role in the maturation of the compact ventricular myocardium by modulating the cardiomyocyte cell cycle via p27 kip1 . However, additional cardiac defects are possible given the ubiquitous expression pattern of this protein. Results:: Germ line deletion of 14-3-3ε led to malalignment of both the outflow tract (OFT) and atrioventricular (AV) cushions, with resulting tricuspid stenosis and atresia, mitral valve abnormalities, and perimembranous ventricular septal defects (VSDs). We confirmed myocardial non-compaction and detected a spongy septum with muscular VSDs and blebbing of the epicardium. These defects were associated with abnormal patterning of p27 kip1 expression in the subendocardial and possibly the epicardial cell populations. In addition to abnormal pharyngeal arch artery patterning, we found deep endocardial recesses and paucity of intramyocardial coronary vasculature as a result of defective coronary plexus remodeling. Conclusions:: The malalignment of both endocardial cushions provides a new explanation for tricuspid and mitral valve defects, while myocardial non-compaction provides the basis for the abnormal coronary vasculature patterning. These abnormalities might arise from p27 kip1 dysregulation and a resulting defect in epithelial-to-mesenchymal transformation. These data suggest that 14-3-3ε, in addition to left ventricular non-compaction (LVNC), might be linked to different forms of congenital heart disease (CHD). Developmental Dynamics 245:1107–1123, 2016.

KW - 14-3-3

KW - cardiac outflow tract

KW - coronary artery hypoplasia

KW - endocardial cushion

KW - heart development

KW - mouse

KW - myocardial hypoplasia

KW - ventricular septal defect

UR - http://www.scopus.com/inward/record.url?scp=84988377976&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84988377976&partnerID=8YFLogxK

U2 - 10.1002/dvdy.24440

DO - 10.1002/dvdy.24440

M3 - Article

C2 - 27580238

AN - SCOPUS:84988377976

VL - 245

SP - 1107

EP - 1123

JO - Developmental Dynamics

JF - Developmental Dynamics

SN - 1058-8388

IS - 11

ER -