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Muscle contraction controls skeletal morphogenesis through regulation of chondrocyte convergent extension.

Abstract Convergent extension driven by mediolateral intercalation of chondrocytes is a key process that contributes to skeletal growth and morphogenesis. While progress has been made in deciphering the molecular mechanism that underlies this process, the involvement of mechanical load exerted by muscle contraction in its regulation has not been studied. Using the zebrafish as a model system, we found abnormal pharyngeal cartilage morphology in both chemically and genetically paralyzed embryos, demonstrating the importance of muscle contraction for zebrafish skeletal development. The shortening of skeletal elements was accompanied by prominent changes in cell morphology and organization. While in control the cells were elongated, chondrocytes in paralyzed zebrafish were smaller and exhibited a more rounded shape, confirmed by a reduction in their length-to-width ratio. The typical columnar organization of cells was affected too, as chondrocytes in various skeletal elements exhibited abnormal stacking patterns, indicating aberrant intercalation. Finally, we demonstrate impaired chondrocyte intercalation in growth plates of muscle-less Sp(d) mouse embryos, implying the evolutionary conservation of muscle force regulation of this essential morphogenetic process.Our findings provide a new perspective on the regulatory interaction between muscle contraction and skeletal morphogenesis by uncovering the role of muscle-induced mechanical loads in regulating chondrocyte intercalation in two different vertebrate models.
PMID
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Authors

Mayor MeshTerms
Keywords
Journal Title developmental biology
Publication Year Start




PMID- 22884393
OWN - NLM
STAT- MEDLINE
DCOM- 20121108
LR  - 20131121
IS  - 1095-564X (Electronic)
IS  - 0012-1606 (Linking)
VI  - 370
IP  - 1
DP  - 2012 Oct 1
TI  - Muscle contraction controls skeletal morphogenesis through regulation of
      chondrocyte convergent extension.
PG  - 154-63
LID - 10.1016/j.ydbio.2012.07.026 [doi]
AB  - Convergent extension driven by mediolateral intercalation of chondrocytes is a
      key process that contributes to skeletal growth and morphogenesis. While progress
      has been made in deciphering the molecular mechanism that underlies this process,
      the involvement of mechanical load exerted by muscle contraction in its
      regulation has not been studied. Using the zebrafish as a model system, we found 
      abnormal pharyngeal cartilage morphology in both chemically and genetically
      paralyzed embryos, demonstrating the importance of muscle contraction for
      zebrafish skeletal development. The shortening of skeletal elements was
      accompanied by prominent changes in cell morphology and organization. While in
      control the cells were elongated, chondrocytes in paralyzed zebrafish were
      smaller and exhibited a more rounded shape, confirmed by a reduction in their
      length-to-width ratio. The typical columnar organization of cells was affected
      too, as chondrocytes in various skeletal elements exhibited abnormal stacking
      patterns, indicating aberrant intercalation. Finally, we demonstrate impaired
      chondrocyte intercalation in growth plates of muscle-less Sp(d) mouse embryos,
      implying the evolutionary conservation of muscle force regulation of this
      essential morphogenetic process.Our findings provide a new perspective on the
      regulatory interaction between muscle contraction and skeletal morphogenesis by
      uncovering the role of muscle-induced mechanical loads in regulating chondrocyte 
      intercalation in two different vertebrate models.
CI  - Copyright (c) 2012 Elsevier Inc. All rights reserved.
FAU - Shwartz, Yulia
AU  - Shwartz Y
AD  - Department of Molecular Genetics, Weizmann Institute of Science, PO Box 26,
      Rehovot 76100, Israel.
FAU - Farkas, Zsuzsanna
AU  - Farkas Z
FAU - Stern, Tomer
AU  - Stern T
FAU - Aszodi, Attila
AU  - Aszodi A
FAU - Zelzer, Elazar
AU  - Zelzer E
LA  - eng
PT  - Journal Article
PT  - Research Support, Non-U.S. Gov't
DEP - 20120802
PL  - United States
TA  - Dev Biol
JT  - Developmental biology
JID - 0372762
RN  - 17466-45-4 (Phalloidine)
RN  - P4448TJR7J (Alcian Blue)
SB  - IM
MH  - Alcian Blue
MH  - Animals
MH  - Biomechanical Phenomena
MH  - Bone and Bones/*embryology
MH  - Cartilage/anatomy & histology/*embryology
MH  - Cell Movement/physiology
MH  - Cell Shape
MH  - Chondrocytes/cytology/*physiology
MH  - Growth Plate/*embryology
MH  - Immunohistochemistry
MH  - In Situ Hybridization
MH  - Mice
MH  - Models, Statistical
MH  - Muscle Contraction/*physiology
MH  - Neural Crest/physiology
MH  - Osteogenesis/*physiology
MH  - Phalloidine
MH  - Zebrafish
EDAT- 2012/08/14 06:00
MHDA- 2012/11/09 06:00
CRDT- 2012/08/14 06:00
PHST- 2012/05/09 00:00 [received]
PHST- 2012/07/23 00:00 [revised]
PHST- 2012/07/25 00:00 [accepted]
PHST- 2012/08/14 06:00 [entrez]
PHST- 2012/08/14 06:00 [pubmed]
PHST- 2012/11/09 06:00 [medline]
AID - S0012-1606(12)00410-1 [pii]
AID - 10.1016/j.ydbio.2012.07.026 [doi]
PST - ppublish
SO  - Dev Biol. 2012 Oct 1;370(1):154-63. doi: 10.1016/j.ydbio.2012.07.026. Epub 2012
      Aug 2.