Assessing Myf5 and Lbx1 contribution to carapace development by reproducing their turtle-specific signatures in mouse embryos.
body plan
carapace morphogenesis
mouse genetics
somite patterning
vertebrate evolution
Journal
Developmental dynamics : an official publication of the American Association of Anatomists
ISSN: 1097-0177
Titre abrégé: Dev Dyn
Pays: United States
ID NLM: 9201927
Informations de publication
Date de publication:
10 2022
10 2022
Historique:
revised:
16
05
2022
received:
18
01
2022
accepted:
19
05
2022
pubmed:
27
5
2022
medline:
6
10
2022
entrez:
26
5
2022
Statut:
ppublish
Résumé
The turtle carapace is an evolutionary novelty resulting from changes in the processes that build ribs and their associated muscles in most tetrapod species. Turtle embryos have several unique features that might play a role in this process, including the carapacial ridge, a Myf5 gene with shorter coding region that generates an alternative splice variant lacking exon 2, and unusual expression patterns of Lbx1 and HGF. We investigated these turtle-specific expression differences using genetic approaches in mouse embryos. At mid-gestation, mouse embryos producing Myf5 transcripts lacking exon 2 replicated some early properties of turtle somites, but still developed into viable and fertile mice. Extending Lbx1 expression into the hypaxial dermomyotomal lip of trunk somites to mimic the turtle Lbx1 expression pattern, produced fusions in the distal part of the ribs. Turtle-like Myf5 activity might generate a plastic state in developing trunk somites under which they can either enter carapace morphogenetic routes, possibly triggered by signals from the carapacial ridge, or still engage in the development of a standard tetrapod ribcage in the absence of those signals. In addition, trunk Lbx1 expression might play a later role in the formation of the lateral border of the carapace.
Sections du résumé
BACKGROUND
The turtle carapace is an evolutionary novelty resulting from changes in the processes that build ribs and their associated muscles in most tetrapod species. Turtle embryos have several unique features that might play a role in this process, including the carapacial ridge, a Myf5 gene with shorter coding region that generates an alternative splice variant lacking exon 2, and unusual expression patterns of Lbx1 and HGF.
RESULTS
We investigated these turtle-specific expression differences using genetic approaches in mouse embryos. At mid-gestation, mouse embryos producing Myf5 transcripts lacking exon 2 replicated some early properties of turtle somites, but still developed into viable and fertile mice. Extending Lbx1 expression into the hypaxial dermomyotomal lip of trunk somites to mimic the turtle Lbx1 expression pattern, produced fusions in the distal part of the ribs.
CONCLUSIONS
Turtle-like Myf5 activity might generate a plastic state in developing trunk somites under which they can either enter carapace morphogenetic routes, possibly triggered by signals from the carapacial ridge, or still engage in the development of a standard tetrapod ribcage in the absence of those signals. In addition, trunk Lbx1 expression might play a later role in the formation of the lateral border of the carapace.
Substances chimiques
Myf5 protein, mouse
0
Myogenic Regulatory Factor 5
0
Plastics
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1698-1710Informations de copyright
© 2022 American Association for Anatomy.
Références
Gilbert SF, Loredo GA, Brukman A, Burke AC. Morphogenesis of the turtle shell: the development of a novel structure in tetrapod evolution. Evol Dev. 2001;3:47-58. doi:10.1046/j.1525-142X.2001.003002047.x
Hirasawa T, Pascual-Anaya J, Kamezaki N, Taniguchi M, Mine K, Kuratani S. The evolutionary origin of the turtle shell and its dependence on the axial arrest of the embryonic rib cage. JEX-B Mol Dev Evol. 2015;324:194-207. doi:10.1002/jez.b.22579
Brent AE, Braun T, Tabin CJ. Genetic analysis of interactions between the somitic muscle, cartilage and tendon cell lineages during mouse development. Development. 2005;132:515-528. doi:10.1242/dev.01605
Grass S, Arnold HH, Braun T. Alterations in somite patterning of Myf-5-deficient mice: a possible role for FGF-4 and FGF-6. Development. 1996;122:141-150. doi:10.1242/dev.122.1.141
Olson EN, Arnold HH, Rigby PWJ, Wold BJ. Know your neighbors: three phenotypes in null mutants of the myogenic bHLH gene MRF4. Cell. 1996;85:1-4. doi:10.1016/S0092-8674(00)81073-9
Vinagre T, Moncaut N, Carapuço M, Nóvoa A, Bom J, Mallo M. Evidence for a Myotomal Hox/Myf Cascade governing nonautonomous control of rib specification within global vertebral domains. Dev Cell. 2010;18:655-661. doi:10.1016/j.devcel.2010.02.011
Patapoutian A, Yoon JK, Miner JH, Wang S, Stark K, Wold B. Disruption of the mouse MRF4 gene identifies multiple waves of myogenesis in the myotome. Development. 1995;121:3347-3358. http://www.ncbi.nlm.nih.gov/pubmed/7588068
Tallquist MD, Weismann KE, Hellstrom M, Soriano P. Early myotome specification regulates PDGFA expression and axial skeleton development. Development. 2000;127:5059-5070. doi:10.1242/dev.127.23.5059
Huang R, Zhi Q, Schmidt C, Wilting J, Brand-Saberi B, Christ B. Sclerotomal Origin of the Ribs. Development. 2000;127:527-532. doi:10.1242/dev.127.3.527
Wood WM, Otis C, Etemad S, Goldhamer DJ. Development and patterning of rib primordia are dependent on associated musculature. Dev Biol. 2020;468:133-145. doi:10.1016/j.ydbio.2020.07.015
Burke AC, Nowicki JL. A new view of patterning domains in the vertebrate mesoderm. Dev Cell. 2003;4:159-165. doi:10.1016/S1534-5807(03)00033-9
Nagashima H, Kuraku S, Uchida K, Ohya YK, Narita Y, Kuratani S. On the carapacial ridge in turtle embryos: its developmental origin, function and the chelonian body plan. Development. 2007;134:2219-2226. doi:10.1242/dev.002618
Moustakas JE. Development of the carapacial ridge: implications for the evolution of genetic networks in turtle shell development. Evol Dev. 2008;10:29-36. doi:10.1111/j.1525-142X.2007.00210.x
Burke AC. Development of the turtle carapace: implications for the evolution of a novel bauplan. J Morphol. 1989;199:363-378. doi:10.1002/jmor.1051990310
Kawashima-Ohya Y, Narita Y, Nagashima H, Usuda R, Kuratani S. Hepatocyte growth factor is crucial for development of the carapace in turtles. Evol Dev. 2011;13:260-268. doi:10.1111/j.1525-142X.2011.00474.x
Burke AC. The development and evolution of the turtle body plan: inferring intrinsic aspects of the evolutionary process from Experimental embryology. Am Zool. 1991;31:616-627.
Cebra-Thomas J, Tan F, Sistla S, et al. How the turtle forms its shell: a paracrine hypothesis of carapace formation. JEZ-B, Mol Dev Evol. 2005;304:558-569. doi:10.1002/jez.b.21059
Nagashima H, Sugahara F, Takechi M, et al. Evolution of the turtle body plan by the folding and creation of new muscle connections. Science. 2009;325:193-196. doi:10.1126/science.1173826
Lyson TR, Schachner ER, Botha-Brink J, et al. Origin of the unique ventilatory apparatus of turtles. Nat Commun. 2014;5:5211. doi:10.1038/ncomms6211
Hirasawa T, Nagashima H, Kuratani S. The endoskeletal origin of the turtle carapace. Nat Commun. 2013;4:2107. doi:10.1038/ncomms3107
Brohmann H, Jagla K, Birchmeier C. The role of Lbx1 in migration of muscle precursor cells. Development. 2000;127:437-445.
Dietrich S, Abou-Rebyeh F, Brohmann H, et al. The role of SF/HGF and c-met in the development of skeletal muscle. Development. 1999;126:1621-1629. doi:10.1242/dev.126.8.1621
Heymann S, Koudrova M, Arnold HH, Köster M, Braun T. Regulation and function of SF/HGF during migration of limb muscle precursor cells in chicken. Dev Biol. 1996;180:566-578. doi:10.1006/dbio.1996.0329
Gross MK, Moran-Rivard L, Velasquez T, Nakatsu MN, Jagla K, Goulding M. Lbx1 is required for muscle precursor migration along a lateral pathway into the limb. Development. 2000;127:413, 10603357-424.
Birchmeier C, Brohmann H. Genes that control the development of migrating muscle precursor cells. Curr Opin Cell Biol. 2000;12:725-730. doi:10.1016/S0955-0674(00)00159-9
Mennerich D, Schäfer K, Braun T. Pax-3 is necessary but not sufficient for lbx1 expression in myogenic precursor cells of the limb. Mech Dev. 1998;73:147-158. doi:10.1016/S0925-4773(98)00046-X
Ohya YK, Usuda R, Kuraku S, Nagashima H, Kuratani S. Unique features of Myf-5 in turtles: nucleotide deletion, alternative splicing, and unusual expression pattern. Evol Dev. 2006;8:415-423. doi:10.1111/j.1525-142X.2006.00115.x
Floß T, Arnold HH, Braun T. Myf-5m1/Myf-6m1compound heterozygous mouse mutants down-regulate Myf-5 expression and exert rib defects: evidence for long-range cis effects on Myf-5 transcription. Dev Biol. 1996;174:140-147. doi:10.1006/dbio.1996.0058
Winter B, Braun T, Arnold HH. Co-operativity of functional domains in the muscle-specific transcription factor Myf-5. EMBO J. 1992;11:1843-1855. doi:10.1002/j.1460-2075.1992.tb05236.x
Summerbell D, Halai C, Rigby PWJ. Expression of the myogenic regulatory factor Mrf4 precedes or is contemporaneous with that of Myf5 in the somitic bud. Mech Dev. 2002;117:331-335. doi:10.1016/S0925-4773(02)00208-3
Mallo M. The axial musculoskeletal system. In: Baldock R, Bard J, Davidson DR, Morriss-Kay G, eds. Kaufman's Atlas of Mouse Development Supplement. New York: Academic Press; 2016:165-175. doi:10.1016/b978-0-12-800043-4.00013-0
Brown CB, Engleka KA, Wenning J, Min ML, Epstein JA. Identification of a hypaxial somite enhancer element regulating Pax3 expression in migrating myoblasts and characterization of hypaxial muscle Cre transgenic mice. Genesis. 2005;41:202-209. doi:10.1002/gene.20116
Lepper C, Conway SJ, Fan CM. Adult satellite cells and embryonic muscle progenitors have distinct genetic requirements. Nature. 2009;460:627-631. doi:10.1038/nature08209
Gros J, Scaal M, Marcelle C. A two-step mechanism for myotome formation in chick. Dev Cell. 2004;6:875-882. doi:10.1016/j.devcel.2004.05.006
Schäfer K, Braun T. Early specification of limb muscle precursor cells by the homeobox gene Lbx1h. Nat Genet. 1999;23:213-216. doi:10.1038/13843
Braun T, Rudnicki MA, Arnold HH, Jaenisch R. Targeted inactivation of the muscle regulatory gene Myf-5 results in abnormal rib development and perinatal death. Cell. 1992;71:369-382. doi:10.1016/0092-8674(92)90507-9
Yee SP, Rigby PWJ. The regulation of myogenin gene expression during the embryonic development of the mouse. Genes Dev. 1993;7:1277-1289. doi:10.1101/gad.7.7a.1277
Pownall ME, Gustafsson MK, Emerson CP. Myogenic regulatory factors and the specification of muscle progenitors in vertebrate embryos. Annu Rev Cell Dev Biol. 2002;18:747-783. doi:10.1146/annurev.cellbio.18.012502.105758
Crottini A, Madsen O, Poux C, Strauß A, Vieites DR, Vences M. Vertebrate time-tree elucidates the biogeographic pattern of a major biotic change around the K-T boundary in Madagascar. Proc Natl Acad Sci U S A. 2012;109:5358-5363. doi:10.1073/pnas.1112487109
Hogan B, Beddington R, Constantini F, Lacy E. Manipulating the Mouse Embryo: A Laboratory Manual. 2nd ed. Cold Spring Harbor, NY: Cold Spring Harbour Laboratory Press; 1994.
Aires R, de Lemos L, Nóvoa A, et al. Tail bud progenitor activity relies on a network comprising Gdf11, Lin28, and Hox13 genes. Dev Cell. 2019;48:383-395. doi:10.1016/j.devcel.2018.12.004
Mallo M, Brändlin I. Segmental identity can change independently in the hindbrain and rhombencephalic neural crest. Dev Dyn. 1997;210:146-156. doi:10.1002/(SICI)1097-0177(199710)210:2<146::AID-AJA7>3.0.CO;2-G