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Nuclear hormone receptor signaling in amphioxus

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Abstract

The nuclear hormone receptors (NRs) form a superfamily of transcription factors unified by conserved protein structure and mode of function. While most members of this superfamily are activated by ligands, such as thyroid hormones, steroids, vitamin D or retinoic acid, other NRs are called orphan receptors because they have no known ligand. NR-dependent signaling is crucial for vertebrate development with the majority of receptors being expressed in the developing embryo. Due to massive gene duplications during vertebrate diversification, there are usually more NRs in vertebrates than in invertebrates. In this study, we examine the evolutionary diversification of the NR superfamily and of NR-dependent signaling in chordates (vertebrates, tunicates, and amphioxus). We take advantage of the unique features of the genome of the invertebrate amphioxus, which is characterized by a vertebrate-like gene content without having undergone massive duplications, to assess the NR signaling complement (NRs and NR coregulators) of the ancestral chordate. We find 33 NRs in amphioxus, which are more NRs than originally anticipated. This increase is mainly due to an amphioxus-specific duplication of genes encoding receptors of the NR1H group. In addition, there are three heterologous NRs in amphioxus that could not be placed within the framework of the NR superfamily. Apart from these exceptions, there is usually one amphioxus NR or NR signaling coregulator for each paralogous group of two, three, or four human receptors suggesting that the ancestral chordate had a set of 22 different NRs plus one copy of each NR coregulator.

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Acknowledgments

The authors would like to thank Michael E. Baker for critical reading of the manuscript. This work was supported by grants from the ANR and the CNRS to M.S., the MENRT to M.S. and V.L. and by CRESCENDO, a European Union Integrated Project of FP6, and by CASCADE, a Network of Excellence of FP6. S.B. is funded by an ARC postdoctoral fellowship.

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Authors and Affiliations

  1. CNRS UMR5242-INRA 1288-ENS-UCBL, Institut de Génomique Fonctionnelle de Lyon, IFR128 BioSciences Lyon-Gerland, Ecole Normale Supérieure de Lyon, 46 allée d’Italie, 69364, Lyon Cedex 07, France

    Michael Schubert, Frédéric Brunet, Mathilde Paris, Gérard Benoit & Vincent Laudet

  2. CNRS UMR7628, UPMC Univ Paris 06, Observatoire Océanographique, 66651, Banyuls-sur-Mer, France

    Stéphanie Bertrand

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  1. Michael Schubert
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  2. Frédéric Brunet
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  3. Mathilde Paris
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  4. Stéphanie Bertrand
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  5. Gérard Benoit
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  6. Vincent Laudet
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Correspondence to Vincent Laudet.

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Communicated by J.J. Gibson-Brown

Michael Schubert and Frédéric Brunet are equal first authors.

Electronic supplementary material

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Supplementary Table S1

Sequence IDs and alleles of nuclear hormone receptors (NRs) in the genome of Branchiostoma floridae. (DOC 97.0KB)

Supplementary Table S2

Sequence IDs and alleles of nuclear hormone receptor coregulators (NRCs) in the genome of Branchiostoma floridae.(DOC 41.0KB)

Fig. S1

Phylogeny of the nuclear hormone receptor (NR) superfamily. The maximum likelihood tree is based on NRs from humans (Homo sapiens), sea squirts (Ciona intestinalis), fruit flies (Drosophila melanogaster) and amphioxus (Branchiostoma floridae). Human (Homo sapiens) NRs are shown in black, sea squirt (Ciona intestinalis) NRs in green, fruit fly (Drosophila melanogaster) NRs in blue and amphioxus (Branchiostoma floridae) NRs in red. Bootstrap support values are given for each branch (PDF 64.1 KB)

Fig. S2

Phylogeny of the NCOA family. The tree is the result of a maximum likelihood analysis. Bootstrap support values are given for each branch. Sequences are indicated as sequence IDs plus species name. The single amphioxus (Branchiostoma floridae) NCOA homolog is highlighted in red. (PDF 56.0 KB)

Fig. S3

Phylogeny of the CBP and P300 family. The tree is the result of a maximum likelihood analysis. Bootstrap support values are given for each branch. Sequences are indicated as sequence IDs plus species name. The single amphioxus (Branchiostoma floridae) CBP/P300 homolog is highlighted in red (PDF 58.9 KB)

Fig. S4

Phylogeny of the PGC1 family. The tree is the result of a maximum likelihood analysis. Bootstrap support values are given for each branch. Sequences are indicated as sequence IDs plus species name. The single amphioxus (Branchiostoma floridae) PGC1 homolog is highlighted in red (PDF 57.8 KB)

Fig. S5

Phylogeny of the NCOR/SMRT family. The tree is the result of a maximum likelihood analysis. Bootstrap support values are given for each branch. Sequences are indicated as sequence IDs plus species name. The single amphioxus (Branchiostoma floridae) NCOR homolog is highlighted in red (PDF 55.7 KB)

Fig. S6

Phylogeny of the MED1/TRAP220 family. The tree is the result of a maximum likelihood analysis. Bootstrap support values are given for each branch. Sequences are indicated as sequence IDs plus species name. The single amphioxus (Branchiostoma floridae) TRAP220 homolog is highlighted in red (PDF 49.8 KB)

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Schubert, M., Brunet, F., Paris, M. et al. Nuclear hormone receptor signaling in amphioxus. Dev Genes Evol 218, 651–665 (2008). https://doi.org/10.1007/s00427-008-0251-y

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