Literature DB >> 29490984

The heart tube forms and elongates through dynamic cell rearrangement coordinated with foregut extension.

Hinako Kidokoro1,2,3, Sayuri Yonei-Tamura2, Koji Tamura2, Gary C Schoenwolf1, Yukio Saijoh4.   

Abstract

In the initiation of cardiogenesis, the heart primordia transform from bilateral flat sheets of mesoderm into an elongated midline tube. Here, we discover that this rapid architectural change is driven by actomyosin-based oriented cell rearrangement and resulting dynamic tissue reshaping (convergent extension, CE). By labeling clusters of cells spanning the entire heart primordia, we show that the heart primordia converge toward the midline to form a narrow tube, while extending perpendicularly to rapidly lengthen it. Our data for the first time visualize the process of early heart tube formation from both the medial (second) and lateral (first) heart fields, revealing that both fields form the early heart tube by essentially the same mechanism. Additionally, the adjacent endoderm coordinately forms the foregut through previously unrecognized movements that parallel those of the heart mesoderm and elongates by CE. In conclusion, our data illustrate how initially two-dimensional flat primordia rapidly change their shapes and construct the three-dimensional morphology of emerging organs in coordination with neighboring morphogenesis.
© 2018. Published by The Company of Biologists Ltd.

Entities:  

Keywords:  Actomyosin; Cardiogenesis; Cell rearrangement; Convergent extension; Heart fields; Heart tube formation; Morphogenesis

Mesh:

Substances:

Year:  2018        PMID: 29490984      PMCID: PMC5963862          DOI: 10.1242/dev.152488

Source DB:  PubMed          Journal:  Development        ISSN: 0950-1991            Impact factor:   6.868


  39 in total

1.  Rapid triple-labeling method combining in situ hybridization and double immunocytochemistry.

Authors:  Carmen Lopez-Sanchez; Virginio Garcia-Martinez; Aaron Lawson; Susan C Chapman; Gary C Schoenwolf
Journal:  Dev Dyn       Date:  2004-06       Impact factor: 3.780

2.  Planar cell polarity links axes of spatial dynamics in neural-tube closure.

Authors:  Tamako Nishimura; Hisao Honda; Masatoshi Takeichi
Journal:  Cell       Date:  2012-05-25       Impact factor: 41.582

3.  Bidirectional fusion of the heart-forming fields in the developing chick embryo.

Authors:  R A Moreno-Rodriguez; E L Krug; L Reyes; L Villavicencio; C H Mjaatvedt; R R Markwald
Journal:  Dev Dyn       Date:  2006-01       Impact factor: 3.780

Review 4.  Heart field: from mesoderm to heart tube.

Authors:  Radwan Abu-Issa; Margaret L Kirby
Journal:  Annu Rev Cell Dev Biol       Date:  2007       Impact factor: 13.827

Review 5.  The anatomy of cardiac looping: a step towards the understanding of the morphogenesis of several forms of congenital cardiac malformations.

Authors:  Jörg Männer
Journal:  Clin Anat       Date:  2009-01       Impact factor: 2.414

6.  Improved method for chick whole-embryo culture using a filter paper carrier.

Authors:  S C Chapman; J Collignon; G C Schoenwolf; A Lumsden
Journal:  Dev Dyn       Date:  2001-03       Impact factor: 3.780

7.  Bending of the looping heart: differential growth revisited.

Authors:  Yunfei Shi; Jiang Yao; Gang Xu; Larry A Taber
Journal:  J Biomech Eng       Date:  2014-08       Impact factor: 2.097

8.  TBX1 regulates epithelial polarity and dynamic basal filopodia in the second heart field.

Authors:  Alexandre Francou; Edouard Saint-Michel; Karim Mesbah; Robert G Kelly
Journal:  Development       Date:  2014-11       Impact factor: 6.868

9.  The endoderm and myocardium join forces to drive early heart tube assembly.

Authors:  Anastasiia Aleksandrova; Andras Czirok; Edina Kosa; Oleksandr Galkin; Tracey J Cheuvront; Brenda J Rongish
Journal:  Dev Biol       Date:  2015-05-05       Impact factor: 3.582

10.  Requirement of DLG1 for cardiovascular development and tissue elongation during cochlear, enteric, and skeletal development: possible role in convergent extension.

Authors:  Akiko Iizuka-Kogo; Takao Senda; Tetsu Akiyama; Atsushi Shimomura; Ryuji Nomura; Yoshimi Hasegawa; Ken-Ichi Yamamura; Hiroshi Kogo; Nobuhiko Sawai; Toshiyuki Matsuzaki
Journal:  PLoS One       Date:  2015-04-10       Impact factor: 3.240

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  11 in total

Review 1.  Division orientation: disentangling shape and mechanical forces.

Authors:  Tara M Finegan; Dan T Bergstralh
Journal:  Cell Cycle       Date:  2019-05-21       Impact factor: 4.534

2.  The Chiral Looping of the Embryonic Heart Is Formed by the Combination of Three Axial Asymmetries.

Authors:  Hisao Honda; Takaya Abe; Toshihiko Fujimori
Journal:  Biophys J       Date:  2019-12-18       Impact factor: 4.033

3.  A method for investigating spatiotemporal growth patterns at cell and tissue levels during C-looping in the embryonic chick heart.

Authors:  Nazanin Ebrahimi; Mahyar Osanlouy; Chris P Bradley; M Fabiana Kubke; Dane A Gerneke; Peter J Hunter
Journal:  iScience       Date:  2022-06-14

4.  A combined human gastruloid model of cardiogenesis and neurogenesis.

Authors:  Zachary T Olmsted; Janet L Paluh
Journal:  iScience       Date:  2022-05-30

Review 5.  Engineering Heart Morphogenesis.

Authors:  Christian J Mandrycky; Nisa P Williams; Ivan Batalov; Danny El-Nachef; Bernadette S de Bakker; Jennifer Davis; Deok-Ho Kim; Cole A DeForest; Ying Zheng; Kelly R Stevens; Nathan J Sniadecki
Journal:  Trends Biotechnol       Date:  2020-03-05       Impact factor: 19.536

6.  Left-handed cardiac looping by cell chirality is mediated by position-specific convergent extensions.

Authors:  Hisao Honda
Journal:  Biophys J       Date:  2021-10-23       Impact factor: 4.033

Review 7.  The Chicken as a Model Organism to Study Heart Development.

Authors:  Johannes G Wittig; Andrea Münsterberg
Journal:  Cold Spring Harb Perspect Biol       Date:  2020-08-03       Impact factor: 9.708

Review 8.  Of form and function: Early cardiac morphogenesis across classical and emerging model systems.

Authors:  Bhavana Shewale; Nicole Dubois
Journal:  Semin Cell Dev Biol       Date:  2021-05-14       Impact factor: 7.499

Review 9.  From Stripes to a Beating Heart: Early Cardiac Development in Zebrafish.

Authors:  Cassie L Kemmler; Fréderike W Riemslagh; Hannah R Moran; Christian Mosimann
Journal:  J Cardiovasc Dev Dis       Date:  2021-02-10

10.  Capturing Cardiogenesis in Gastruloids.

Authors:  Giuliana Rossi; Nicolas Broguiere; Matthew Miyamoto; Andrea Boni; Romain Guiet; Mehmet Girgin; Robert G Kelly; Chulan Kwon; Matthias P Lutolf
Journal:  Cell Stem Cell       Date:  2020-11-10       Impact factor: 24.633

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