Emergence, development and diversification of the TGF-β signalling pathway within the animal kingdom

Huminiecki, Łukasz; Goldovsky, Leon; Freilich, Shiri; Moustakas, Aristidis; Ouzounis, Christos A.; Heldin, Carl‐Henrik

doi:10.1186/1471-2148-9-28

Cited by 151 publications

(131 citation statements)

References 69 publications

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“…Members of the TGFβ superfamily of signal transduction pathways are conserved from early multicellular animals, such as trichoplax, to humans (32). Thus, our findings regarding the interplay of BMP receptor trafficking and signaling outputs have important implications for related receptors throughout metazoan phylogenies.…”

Section: Discussionmentioning

confidence: 83%

BMP signaling requires retromer-dependent recycling of the type I receptor

Gleason

Akintobi²,

Grant³

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

105

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The transforming growth factor β (TGFβ) superfamily of signaling pathways, including the bone morphogenetic protein (BMP) subfamily of ligands and receptors, controls a myriad of developmental processes across metazoan biology. Transport of the receptors from the plasma membrane to endosomes has been proposed to promote TGFβ signal transduction and shape BMP-signaling gradients throughout development. However, how postendocytic trafficking of BMP receptors contributes to the regulation of signal transduction has remained enigmatic. Here we report that the intracellular domain of Caenorhabditis elegans BMP type I receptor SMA-6 (small-6) binds to the retromer complex, and in retromer mutants, SMA-6 is degraded because of its missorting to lysosomes. Surprisingly, we find that the type II BMP receptor, DAF-4 (dauer formation-defective-4), is retromer-independent and recycles via a distinct pathway mediated by ARF-6 (ADP-ribosylation factor-6). Importantly, we find that loss of retromer blocks BMP signaling in multiple tissues. Taken together, our results indicate a mechanism that separates the type I and type II receptors during receptor recycling, potentially terminating signaling while preserving both receptors for further rounds of activation.endocytosis | receptor trafficking | C. elegans

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Section: Discussionmentioning

confidence: 83%

BMP signaling requires retromer-dependent recycling of the type I receptor

Gleason

Akintobi²,

Grant³

et al. 2014

Proc. Natl. Acad. Sci. U.S.A.

105

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“…Now known to be unique to Metazoa [24 -26], a full complement of TGF-b signalling components (TGF-b and BMP ligands, their receptors, and numerous SMAD cofactors) has been found in cnidarians [27 -29], placozoans [15], sponges [30] and, most recently, the ctenophores Mnemiopsis leidyi [31] and Pleurobrachia bachei (table 1). Non-metazoan unikonts lack not only the ligands, receptors and SMAD cofactors [17,[24][25][26], but also most of the inhibitors. This pathway is a clear example of a metazoan innovation [25], and the presence of all elements together in ctenophores suggests that this system was actively transducing extracellular signals into transcriptional responses in the ancestral metazoan.…”

Section: Pathways That Unite Metazoans (A) Transforming Growth Factormentioning

confidence: 99%

Phylogenetic evidence for the modular evolution of metazoan signalling pathways

Babonis¹,

Martindale²

2017

Phil. Trans. R. Soc. B

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One contribution of 17 to a theme issue 'Evo-devo in the genomics era, and the origins of morphological diversity'. Communication among cells was paramount to the evolutionary increase in cell type diversity and, ultimately, the origin of large body size. Across the diversity of Metazoa, there are only few conserved cell signalling pathways known to orchestrate the complex cell and tissue interactions regulating development; thus, modification to these few pathways has been responsible for generating diversity during the evolution of animals. Here, we summarize evidence for the origin and putative function of the intracellular, membrane-bound and secreted components of seven metazoan cell signalling pathways with a special focus on early branching metazoans (ctenophores, poriferans, placozoans and cnidarians) and basal unikonts (amoebozoans, fungi, filastereans and choanoflagellates). We highlight the modular incorporation of intra-and extracellular components in each signalling pathway and suggest that increases in the complexity of the extracellular matrix may have further promoted the modulation of cell signalling during metazoan evolution. Most importantly, this updated view of metazoan signalling pathways highlights the need for explicit study of canonical signalling pathway components in taxa that do not operate a complete signalling pathway. Studies like these are critical for developing a deeper understanding of the evolution of cell signalling.This article is part of the themed issue 'Evo-devo in the genomics era, and the origins of morphological diversity'.

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“…In ascidians the ancestral bilaterian TGF receptor repertoire is expanded to three type II receptors: this is the first example of a bilaterian TGF-b receptor duplication, mapping to chordates which is propagated through vertebrates (Huminiecki et al, 2009). …”

Section: Introductionmentioning

confidence: 99%

“…In ascidians, at least two R-SMADs (one TGF-b and one BMP), one Co-SMAD and one I-SMAD have been described (Huminiecki et al, 2009).…”

Section: Introductionmentioning

confidence: 99%