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Hedgehog regulation of superficial slow muscle fibres in Xenopus and the evolution of tetrapod trunk myogenesis.
Development. 2004 Jul; 131(14):3249-62.D

Abstract

In tetrapod phylogeny, the dramatic modifications of the trunk have received less attention than the more obvious evolution of limbs. In somites, several waves of muscle precursors are induced by signals from nearby tissues. In both amniotes and fish, the earliest myogenesis requires secreted signals from the ventral midline carried by Hedgehog (Hh) proteins. To determine if this similarity represents evolutionary homology, we have examined myogenesis in Xenopus laevis, the major species from which insight into vertebrate mesoderm patterning has been derived. Xenopus embryos form two distinct kinds of muscle cells analogous to the superficial slow and medial fast muscle fibres of zebrafish. As in zebrafish, Hh signalling is required for XMyf5 expression and generation of a first wave of early superficial slow muscle fibres in tail somites. Thus, Hh-dependent adaxial myogenesis is the likely ancestral condition of teleosts, amphibia and amniotes. Our evidence suggests that midline-derived cells migrate to the lateral somite surface and generate superficial slow muscle. This cell re-orientation contributes to the apparent rotation of Xenopus somites. Xenopus myogenesis in the trunk differs from that in the tail. In the trunk, the first wave of superficial slow fibres is missing, suggesting that significant adaptation of the ancestral myogenic programme occurred during tetrapod trunk evolution. Although notochord is required for early medial XMyf5 expression, Hh signalling fails to drive these cells to slow myogenesis. Later, both trunk and tail somites develop a second wave of Hh-independent slow fibres. These fibres probably derive from an outer cell layer expressing the myogenic determination genes XMyf5, XMyoD and Pax3 in a pattern reminiscent of amniote dermomyotome. Thus, Xenopus somites have characteristics in common with both fish and amniotes that shed light on the evolution of somite differentiation. We propose a model for the evolutionary adaptation of myogenesis in the transition from fish to tetrapod trunk.

Authors+Show Affiliations

Randall Centre, New Hunt's House, Guy's Campus, King's College London, London SE1 1UL, UK.No affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info availableNo affiliation info available

Pub Type(s)

Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, P.H.S.

Language

eng

PubMed ID

15201218

Citation

Grimaldi, Annalisa, et al. "Hedgehog Regulation of Superficial Slow Muscle Fibres in Xenopus and the Evolution of Tetrapod Trunk Myogenesis." Development (Cambridge, England), vol. 131, no. 14, 2004, pp. 3249-62.
Grimaldi A, Tettamanti G, Martin BL, et al. Hedgehog regulation of superficial slow muscle fibres in Xenopus and the evolution of tetrapod trunk myogenesis. Development. 2004;131(14):3249-62.
Grimaldi, A., Tettamanti, G., Martin, B. L., Gaffield, W., Pownall, M. E., & Hughes, S. M. (2004). Hedgehog regulation of superficial slow muscle fibres in Xenopus and the evolution of tetrapod trunk myogenesis. Development (Cambridge, England), 131(14), 3249-62.
Grimaldi A, et al. Hedgehog Regulation of Superficial Slow Muscle Fibres in Xenopus and the Evolution of Tetrapod Trunk Myogenesis. Development. 2004;131(14):3249-62. PubMed PMID: 15201218.
* Article titles in AMA citation format should be in sentence-case
TY - JOUR T1 - Hedgehog regulation of superficial slow muscle fibres in Xenopus and the evolution of tetrapod trunk myogenesis. AU - Grimaldi,Annalisa, AU - Tettamanti,Gianluca, AU - Martin,Benjamin L, AU - Gaffield,William, AU - Pownall,Mary E, AU - Hughes,Simon M, Y1 - 2004/06/16/ PY - 2004/6/18/pubmed PY - 2004/8/31/medline PY - 2004/6/18/entrez SP - 3249 EP - 62 JF - Development (Cambridge, England) JO - Development VL - 131 IS - 14 N2 - In tetrapod phylogeny, the dramatic modifications of the trunk have received less attention than the more obvious evolution of limbs. In somites, several waves of muscle precursors are induced by signals from nearby tissues. In both amniotes and fish, the earliest myogenesis requires secreted signals from the ventral midline carried by Hedgehog (Hh) proteins. To determine if this similarity represents evolutionary homology, we have examined myogenesis in Xenopus laevis, the major species from which insight into vertebrate mesoderm patterning has been derived. Xenopus embryos form two distinct kinds of muscle cells analogous to the superficial slow and medial fast muscle fibres of zebrafish. As in zebrafish, Hh signalling is required for XMyf5 expression and generation of a first wave of early superficial slow muscle fibres in tail somites. Thus, Hh-dependent adaxial myogenesis is the likely ancestral condition of teleosts, amphibia and amniotes. Our evidence suggests that midline-derived cells migrate to the lateral somite surface and generate superficial slow muscle. This cell re-orientation contributes to the apparent rotation of Xenopus somites. Xenopus myogenesis in the trunk differs from that in the tail. In the trunk, the first wave of superficial slow fibres is missing, suggesting that significant adaptation of the ancestral myogenic programme occurred during tetrapod trunk evolution. Although notochord is required for early medial XMyf5 expression, Hh signalling fails to drive these cells to slow myogenesis. Later, both trunk and tail somites develop a second wave of Hh-independent slow fibres. These fibres probably derive from an outer cell layer expressing the myogenic determination genes XMyf5, XMyoD and Pax3 in a pattern reminiscent of amniote dermomyotome. Thus, Xenopus somites have characteristics in common with both fish and amniotes that shed light on the evolution of somite differentiation. We propose a model for the evolutionary adaptation of myogenesis in the transition from fish to tetrapod trunk. SN - 0950-1991 UR - https://www.unboundmedicine.com/medline/citation/15201218/Hedgehog_regulation_of_superficial_slow_muscle_fibres_in_Xenopus_and_the_evolution_of_tetrapod_trunk_myogenesis_ L2 - http://dev.biologists.org/cgi/pmidlookup?view=long&pmid=15201218 DB - PRIME DP - Unbound Medicine ER -