Independent specialisation of myosin II paralogues in muscle vs. non-muscle functions during early animal evolution: a ctenophore perspective

BMC Evolutionary Biology

Research Article

Michaël Manuel¹  Muriel Jager¹  Hervé Le Guyader¹  Cyrielle Dayraud¹  Alexandre Alié²  Eric Quéinnec³  Patrick Chang⁴ 

[1] Université Pierre et Marie Curie - Paris 6, UMR 7138 CNRS MNHN IRD, Case 05, 4ème étage, Bâtiment A, 7 quai St Bernard, 75005, Paris, France;Université Pierre et Marie Curie - Paris 6, UMR 7138 CNRS MNHN IRD, Case 05, 4ème étage, Bâtiment A, 7 quai St Bernard, 75005, Paris, France;Department of Biophysics, Laboratory of Molecular Developmental Biology, Graduate School of Science, Kyoto-University, Kitashirakawa-Oiwake, Sakyo-ku, 606-8502, Kyoto, Japan;Université Pierre et Marie Curie - Paris 6, UMR 7138 CNRS MNHN IRD, Case 05, 4ème étage, Bâtiment A, 7 quai St Bernard, 75005, Paris, France;UPMC Université Paris 6, UMR 7138 Systématique, Adaptation, Evolution CNRS MNHN IRD, Bâtiment A, 4ème étage, Case 05, Université Pierre et Marie Curie, 7 quai St Bernard, 75005, Paris, France;Université Pierre et Marie Curie- Paris 6, UMR 7009 CNRS, Observatoire Océanologique, 06230, Villefranche-sur-Mer, France;

关键词: Nurse Cell;    Muscle Cell Type;    Apical Organ;    Median Ridge;    Phalloidin Staining;   

DOI  :  10.1186/1471-2148-12-107

 received in 2012-04-02, accepted in 2012-06-14,  发布年份 2012

来源: Springer

【 摘 要 】

BackgroundMyosin II (or Myosin Heavy Chain II, MHCII) is a family of molecular motors involved in the contractile activity of animal muscle cells but also in various other cellular processes in non-muscle cells. Previous phylogenetic analyses of bilaterian MHCII genes identified two main clades associated respectively with smooth/non-muscle cells (MHCIIa) and striated muscle cells (MHCIIb). Muscle cells are generally thought to have originated only once in ancient animal history, and decisive insights about their early evolution are expected to come from expression studies of Myosin II genes in the two non-bilaterian phyla that possess muscles, the Cnidaria and Ctenophora.ResultsWe have uncovered three MHCII paralogues in the ctenophore species Pleurobrachia pileus. Phylogenetic analyses indicate that the MHCIIa / MHCIIb duplication is more ancient than the divergence between extant metazoan lineages. The ctenophore MHCIIa gene (PpiMHCIIa) has an expression pattern akin to that of "stem cell markers" (Piwi, Vasa…) and is expressed in proliferating cells. We identified two MHCIIb genes that originated from a ctenophore-specific duplication. PpiMHCIIb1 represents the exclusively muscular form of myosin II in ctenophore, while PpiMHCIIb2 is expressed in non-muscle cells of various types. In parallel, our phalloidin staining and TEM observations highlight the structural complexity of ctenophore musculature and emphasize the experimental interest of the ctenophore tentacle root, in which myogenesis is spatially ordered and strikingly similar to striated muscle formation in vertebrates.ConclusionMHCIIa expression in putative stem cells/proliferating cells probably represents an ancestral trait, while specific involvement of some MHCIIa genes in smooth muscle fibres is a uniquely derived feature of the vertebrates. That one ctenophore MHCIIb paralogue (PpiMHCIIb2) has retained MHCIIa-like expression features furthermore suggests that muscular expression of the other paralogue, PpiMHCIIb1, was the result of neofunctionalisation within the ctenophore lineage, making independent origin of ctenophore muscle cells a likely option.

【 授权许可】

Unknown   
© Dayraud et al.; licensee BioMed Central Ltd. 2012. This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.