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Hepatocyte Growth Factor Is Crucial For Development Of The Carapace In Turtles

Y. Kawashima-Ohya, Y. Narita, H. Nagashima, R. Usuda, S. Kuratani
Published 2011 · Biology, Medicine

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Turtles are characterized by their shell, composed of a dorsal carapace and a ventral plastron. The carapace first appears as the turtle‐specific carapacial ridge (CR) on the lateral aspect of the embryonic flank. Accompanying the acquisition of the shell, unlike in other amniotes, hypaxial muscles in turtle embryos appear as thin threads of fibrous tissue. To understand carapacial evolution from the perspective of muscle development, we compared the development of the muscle plate, the anlage of hypaxial muscles, between the Chinese soft‐shelled turtle, Pelodiscus sinensis, and chicken embryos. We found that the ventrolateral lip (VLL) of the thoracic dermomyotome of P. sinensis delaminates early and produces sparse muscle plate in the lateral body wall. Expression patterns of the regulatory genes for myotome differentiation, such as Myf5, myogenin, Pax3, and Pax7 have been conserved among amniotes, including turtles. However, in P. sinensis embryos, the gene hepatocyte growth factor (HGF), encoding a regulatory factor for delamination of the dermomyotomal VLL, was uniquely expressed in sclerotome and the lateral body wall at the interlimb level. Implantation of COS‐7 cells expressing a HGF antagonist into the turtle embryo inhibited CR formation. We conclude that the de novo expression of HGF in the turtle mesoderm would have played an innovative role resulting in the acquisition of the turtle‐specific body plan.
This paper references
Identification and expression of the lamprey Pax6 gene: evolutionary origin of the segmented brain of vertebrates.
Y. Murakami (2001)
10.1038/376768A0
Essential role for the c-met receptor in the migration of myogenic precursor cells into the limb bud
F. Bladt (1995)
10.1038/NEWS.2008.1260
How The Turtle Gets Its Shell
N. Gilbert (2008)
10.1038/35040549
Evolutionary origins of vertebrate appendicular muscle
C. Neyt (2000)
10.1007/BF00304424
Early stages of chick somite development
B. Christ (2004)
10.1038/13843
Early specification of limb muscle precursor cells by the homeobox gene Lbx1h
K. Schäfer (1999)
10.1007/978-0-387-09606-3_1
Formation and differentiation of avian somite derivatives.
B. Christ (2008)
The role of SF/HGF and c-Met in the development of skeletal muscle.
S. Dietrich (1999)
10.1016/S0092-8674(03)00268-X
A Somitic Compartment of Tendon Progenitors
A. E. Brent (2003)
Early myotome specification regulates PDGFA expression and axial skeleton development.
M. Tallquist (2000)
Die Morphologie der Tetrapodenrippen. Zool. Jahrb. Abt. Anat. Ont. Tiere
S W Emelianov (1936)
The development and evolution of the turtle body plan
A. C. Burke (1991)
10.1002/j.1460-2075.1992.tb05236.x
Co‐operativity of functional domains in the muscle‐specific transcription factor Myf‐5.
B. Winter (1992)
10.1006/DBIO.1998.9053
Distinct regulatory elements govern Fgf4 gene expression in the mouse blastocyst, myotomes, and developing limb.
D. Fraidenraich (1998)
Turtles
A. C. Burke (2009)
10.1006/DBIO.1996.0329
Regulation and function of SF/HGF during migration of limb muscle precursor cells in chicken.
S. Heymann (1996)
10.2108/zsj.18.705
Normal Embryonic Stages of the Chinese Softshelled Turtle Pelodiscus sinensis (Trionychidae)
Masayoshi Tokita (2001)
10.1002/AJA.1002020108
Expression of the hepatocyte growth factor gene during chick limb development
F. Myokai (1995)
10.1006/DBIO.1996.0260
Scatter factor/hepatocyte growth factor (SF/HGF) induces emigration of myogenic cells at interlimb level in vivo.
B. Brand-Saberi (1996)
10.1016/S0012-1606(02)00051-9
Ventral axial organs regulate expression of myotomal Fgf-8 that influences rib development.
R. Huang (2003)
10.1002/JEZ.1103
Development of an evolutionarily novel structure: fibroblast growth factor expression in the carapacial ridge of turtle embryos.
G. A. Loredo (2001)
10.1016/S0092-8674(00)81372-0
Uncoupling of Grb2 from the Met Receptor In Vivo Reveals Complex Roles in Muscle Development
F. Maina (1996)
Summary Six 1 and Six 4 homeoproteins are required for Pax 3 and Mrf expression during myogenesis in the mouse embryo
Raphaelle Grifone
Isolation of a novel human gene, APCDD1, as a direct target of the beta-Catenin/T-cell factor 4 complex with probable involvement in colorectal carcinogenesis.
M. Takahashi (2002)
10.1016/0092-8674(79)90043-6
Characterization of Op3, a lysis-defective mutant of bacteriophage f2
P. Model (1979)
10.1006/DBIO.1999.9215
Rib truncations and fusions in the Sp2H mouse reveal a role for Pax3 in specification of the ventro-lateral and posterior parts of the somite.
D. Henderson (1999)
10.1002/dvdy.21177
Evolutionary perspectives from development of mesodermal components in the lamprey
R. Kusakabe (2007)
10.1002/JEZ.B.21059
How the turtle forms its shell: a paracrine hypothesis of carapace formation.
J. Cebra-Thomas (2005)
Alterations in somite patterning of Myf-5-deficient mice: a possible role for FGF-4 and FGF-6.
S. Grass (1996)
Disruption of the mouse MRF4 gene identifies multiple waves of myogenesis in the myotome.
A. Patapoutian (1995)
10.1242/dev.01773
Six1 and Six4 homeoproteins are required for Pax3 and Mrf expression during myogenesis in the mouse embryo
Raphaelle Grifone (2005)
10.1016/S0092-8674(00)81073-9
Know Your Neighbors: Three Phenotypes in Null Mutants of the Myogenic bHLH Gene MRF4
E. Olson (1996)
Dermomyotomal origin of the ribs as revealed by extirpation and transplantation experiments in chick and quail embryos.
N. Kato (1998)
10.1016/S0959-437X(02)00339-8
Developmental regulation of somite derivatives: muscle, cartilage and tendon.
A. E. Brent (2002)
10.1006/DBIO.2000.9839
Activation of fgf4 gene expression in the myotomes is regulated by myogenic bHLH factors and by sonic hedgehog.
D. Fraidenraich (2000)
10.1038/nature08875
APCDD1 is a novel Wnt inhibitor mutated in hereditary hypotrichosis simplex
Yutaka Shimomura (2010)
The role of Lbx1 in migration of muscle precursor cells.
H. Brohmann (2000)
10.1016/S0012-1606(02)00117-3
Contribution of somitic cells to the avian ribs.
D. J. R. Evans (2003)
10.1002/AJA.1001950404
A series of normal stages in the development of the chick embryo
V. Hamburger (1951)
10.1093/ICB/31.4.616
The Development and Evolution of the Turtle Body Plan: Inferring Intrinsic Aspects of the Evolutionary Process from Experimental Embryology
A. Burke (1991)
10.1006/DBIO.1997.8670
Different MRF4 knockout alleles differentially disrupt Myf-5 expression: cis-regulatory interactions at the MRF4/Myf-5 locus.
J. K. Yoon (1997)
10.1016/j.ydbio.2008.08.034
Dynamic regulation of retinoic acid-binding proteins in developing, adult and neoplastic skin reveals roles for beta-catenin and Notch signalling.
C. Collins (2008)
10.1007/s00429-004-0417-y
Formation and differentiation of the avian dermomyotome
M. Scaal (2004)
10.1172/JCI36460
Astrocyte elevated gene-1 regulates hepatocellular carcinoma development and progression.
Byoung Kwon Yoo (2009)
10.1016/j.gde.2009.08.001
Distinct and dynamic myogenic populations in the vertebrate embryo.
M. Buckingham (2009)
10.1016/J.DEVCEL.2004.05.006
A two-step mechanism for myotome formation in chick.
J. Gros (2004)
10.1016/S0014-5793(97)01475-0
HGF/NK4 is a specific antagonist for pleiotrophic actions of hepatocyte growth factor
K. Date (1997)
10.1111/j.1525-142X.2006.00115.x
Unique features of Myf‐5 in turtles: nucleotide deletion, alternative splicing, and unusual expression pattern
Y. Ohya (2006)
Pax-3 is necessary for migration but not differentiation of limb muscle precursors in the mouse.
G. Daston (1996)
10.1002/j.1460-2075.1995.tb07101.x
Inactivation of Myf‐6 and Myf‐5 genes in mice leads to alterations in skeletal muscle development.
T. Braun (1995)
HGF in turtle shell evolution 267 Kawashima-Ohya et al
10.1126/science.1173826
Evolution of the Turtle Body Plan by the Folding and Creation of New Muscle Connections
H. Nagashima (2009)
10.1002/dvdy.20235
Turtle–chicken chimera: An experimental approach to understanding evolutionary innovation in the turtle
H. Nagashima (2005)
Die Morphologie der Tetrapodenrippen
S. W. Emelianov (1936)
MyoD expression marks the onset of skeletal myogenesis in Myf-5 mutant mice.
T. Braun (1994)
10.1016/S0092-8674(00)80189-0
Redefining the Genetic Hierarchies Controlling Skeletal Myogenesis: Pax-3 and Myf-5 Act Upstream of MyoD
S. Tajbakhsh (1997)
Expression of the met receptor tyrosine kinase in muscle progenitor cells in somites and limbs is absent in Splotch mice.
X. Yang (1996)
10.1016/j.devcel.2010.02.011
Evidence for a myotomal Hox/Myf cascade governing nonautonomous control of rib specification within global vertebral domains.
Tânia Vinagre (2010)
10.1242/dev.002618
On the carapacial ridge in turtle embryos: its developmental origin, function and the chelonian body plan
H. Nagashima (2007)
10.1002/JEZ.B.21027
Hox code in embryos of Chinese soft-shelled turtle Pelodiscus sinensis correlates with the evolutionary innovation in the turtle.
Y. Ohya (2005)
10.1046/j.1525-142x.2001.003002047.x
Morphogenesis of the turtle shell: the development of a novel structure in tetrapod evolution
S. Gilbert (2001)
10.1002/(SICI)1097-0185(19990701)255:3<353::AID-AR11>3.0.CO;2-H
Abnormal skeletogenesis occurs coincident with increased apoptosis in the Splotch (Sp2H) mutant: Putative roles for Pax3 and PDGFRα in rib patterning
E. D. Dickman (1999)
10.1111/j.1525-142X.2005.05002.x
Comprehensive survey of carapacial ridge‐specific genes in turtle implies co‐option of some regulatory genes in carapace evolution
Shigehiro Kuraku (2005)
10.1126/SCIENCE.1094291
Convergence of Wnt, ß-Catenin, and Cadherin Pathways
W. Nelson (2004)
10.1002/jmor.1051990310
Development of the turtle carapace: Implications for the evolution of a novel bauplan
A. Burke (1989)
10.1038/sj.onc.1210056
Diversity of LEF/TCF action in development and disease
L. Arce (2006)
10.1006/DBIO.1998.9041
A crucial role for Pax3 in the development of the hypaxial musculature and the long-range migration of muscle precursors.
P. Tremblay (1998)
Sclerotomal origin of the ribs.
R. Huang (2000)
10.1007/s00429-004-0408-z
Formation and differentiation of the avian sclerotome
B. Christ (2004)
10.1101/GAD.9.11.1388
Inactivation of the myogenic bHLH gene MRF4 results in up-regulation of myogenin and rib anomalies.
W. Zhang (1995)
10.1038/364501A0
Muscle deficiency and neonatal death in mice with a targeted mutation in the myogenin gene
P. Hasty (1993)
10.1038/sj.onc.1209859
A positive feedback loop between hepatocyte growth factor receptor and β-catenin sustains colorectal cancer cell invasive growth
A. Rasola (2007)
10.1111/j.1525-142X.2010.00451.x
Evolutionary developmental perspective for the origin of turtles: the folding theory for the shell based on the developmental nature of the carapacial ridge
S. Kuratani (2011)
10.1002/dvdy.20832
Establishment of the epaxial–hypaxial boundary in the avian myotome
M. Ahmed (2006)
10.1093/NAR/28.9.1994
The human LEF-1 gene contains a promoter preferentially active in lymphocytes and encodes multiple isoforms derived from alternative splicing.
K. Hovanes (2000)
10.1242/dev.01605
Genetic analysis of interactions between the somitic muscle, cartilage and tendon cell lineages during mouse development
A. E. Brent (2005)
The PDGF alpha receptor is required for neural crest cell development and for normal patterning of the somites.
Philippe Soriano (1997)
10.1016/0092-8674(92)90507-9
Targeted inactivation of the muscle regulatory gene Myf-5 results in abnormal rib development and perinatal death
T. Braun (1992)
Turtles . . . again. Evol. Dev
A C Burke (2009)
10.1128/MCB.21.17.5857-5868.2001
Oncogenic Mutants of RON and MET Receptor Tyrosine Kinases Cause Activation of the β-Catenin Pathway
A. Danilkovitch-Miagkova (2001)
10.1007/s00427-003-0347-3
Msx genes are expressed in the carapacial ridge of turtle shell: a study of the European pond turtle, Emys orbicularis
C. Vincent (2003)
10.1038/nature07533
An ancestral turtle from the Late Triassic of southwestern China
C. Li (2008)
10.1002/dvdy.20587
Evolution and developmental patterning of the vertebrate skeletal muscles: Perspectives from the lamprey
R. Kusakabe (2005)
Hepatocyte Growth Factor Induces Wnt-independent Nuclear Translocation of β-Catenin after Met-β-Catenin Dissociation in Hepatocytes
S. P. Monga (2002)



This paper is referenced by
10.1007/s12565-011-0121-y
Body plan of turtles: an anatomical, developmental and evolutionary perspective
H. Nagashima (2011)
10.1242/dev.109041
The origin and loss of periodic patterning in the turtle shell
J. Moustakas-Verho (2014)
10.1371/journal.pone.0066357
The Embryonic Transcriptome of the Red-Eared Slider Turtle (Trachemys scripta)
Nicholas J. Kaplinsky (2013)
10.1007/978-94-007-4309-0_4
Origin of the Turtle Body Plan: The Folding Theory to Illustrate Turtle-Specific Developmental Repatterning
H. Nagashima (2013)
10.1016/j.bone.2012.05.002
Variation in osteocytes morphology vs bone type in turtle shell and their exceptional preservation from the Jurassic to the present.
E. Cadena (2012)
10.1111/j.1525-142X.2012.00560.x
Fixed cervical count and the origin of the mammalian diaphragm
E. Buchholtz (2012)
10.1038/ng.2615
The draft genomes of soft–shell turtle and green sea turtle yield insights into the development and evolution of the turtle–specific body plan
Zhuo Wang (2013)
10.1387/ijdb.140296jp
Comparative analysis of pleurodiran and cryptodiran turtle embryos depicts the molecular ground pattern of the turtle carapacial ridge.
Juan Pascual-Anaya (2014)
10.1002/jez.b.22600
Emerging from the rib: resolving the turtle controversies.
R. Rice (2015)
10.1111/joa.12189
Comparative study of the shell development of hard‐ and soft‐shelled turtles
H. Nagashima (2014)
10.1016/j.gde.2017.03.016
Patterning of the turtle shell.
J. Moustakas-Verho (2017)
10.1111/ede.12351
Transcriptomic similarities and differences between the limb bud AER and unique carapacial ridge of turtle embryos
G. A. Cordero (2020)
10.3389/fmars.2017.00400
Hatchlings of the Marine Turtle Lepidochelys olivacea Display Signs of Prenatal Stress at Emergence after Being Incubated in Man-Made Nests: A Preliminary Report
Ma. A. Herrera-Vargas (2017)
10.1002/jez.b.22579
The evolutionary origin of the turtle shell and its dependence on the axial arrest of the embryonic rib cage.
Tatsuya Hirasawa (2015)
10.1007/978-4-431-54634-4_23
The Turtle Evolution: A Conundrum in Vertebrate Evo-Devo
Naoki Irie (2014)
10.1007/978-4-431-54634-4
New Principles in Developmental Processes
H. Kondoh (2014)
10.1371/journal.pone.0050197
Evolutionary and Biological Implications of Dental Mesial Drift in Rodents: The Case of the Ctenodactylidae (Rodentia, Mammalia)
Helder Gomes Rodrigues (2012)
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