Trichoplax adhaerens reveals a network of nuclear receptors sensitive to 9- cis -retinoic acid at the base of metazoan evolution
Abstract
Trichoplax adhaerens, the only known species of Placozoa is likely to be closely related to an early metazoan that preceded branching of Cnidaria and Bilateria. This animal species is surprisingly well adapted to free life in the World Ocean inhabiting tidal costal zones of oceans and seas with warm to moderate temperatures and shallow waters. The genome of T. adhaerens (sp. Grell) includes four nuclear receptors, namely orthologue of RXR (NR2B), HNF4 (NR2A), COUP-TF (NR2F) and ERR (NR3B) that show a high degree of similarity with human orthologues. In the case of RXR, the sequence identity to human RXR alpha reaches 81% in the DNA binding domain and 70% in the ligand binding domain. We show that T. adhaerens RXR (TaRXR) binds 9-cis retinoic acid (9-cis-RA) with high affinity, as well as high specificity and that exposure of T. adhaerens to 9-cis-RA regulates the expression of the putative T. adhaerens orthologue of vertebrate L-malate-NADP+ oxidoreductase (EC 1.1.1.40) which in vertebrates is regulated by a heterodimer of RXR and thyroid hormone receptor. Treatment by 9-cis-RA alters the relative expression profile of T. adhaerens nuclear receptors, suggesting the existence of natural ligands. Keeping with this, algal food composition has a profound effectmore »
- Authors:
-
- Charles Univ., Prague (Czech Republic). First Faculty of Medicine. Biocev; Heidelberg Univ. (Germany). Dept. of Medicine V.
- Charles Univ., Prague (Czech Republic). First Faculty of Medicine. Biocev
- Charles Univ., Prague (Czech Republic). First Faculty of Medicine. Biocev; Charles Univ., Prague (Czech Republic). Third Faculty of Medicine. Dept. of Pathology
- Czech Academy of Sciences, Třeboň (Czech Republic). Inst. of Microbiology. Lab. of Photosynthesis
- Univ. of Veterinary Medicine, Hannover (Germany). Inst. for Animal Ecology and Cell Biology; Yale Univ., New Haven, CT (United States). Dept. of Ecology and Evolutionary Biology
- Publication Date:
- Research Org.:
- Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC)
- OSTI Identifier:
- 1628930
- Grant/Contract Number:
- AC02-05CH11231
- Resource Type:
- Accepted Manuscript
- Journal Name:
- PeerJ
- Additional Journal Information:
- Journal Volume: 5; Journal ID: ISSN 2167-8359
- Publisher:
- PeerJ Inc.
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; Trichoplax adhaerens; RXR; 9-cis retinoic acid; food; ERR; HNF4; COUP; nuclear receptor
Citation Formats
Novotný, Jan Philipp, Chughtai, Ahmed Ali, Kostrouchová, Markéta, Kostrouchová, Veronika, Kostrouch, David, Kaššák, Filip, Kaňa, Radek, Schierwater, Bernd, Kostrouchová, Marta, and Kostrouch, Zdenek. Trichoplax adhaerens reveals a network of nuclear receptors sensitive to 9- cis -retinoic acid at the base of metazoan evolution. United States: N. p., 2017.
Web. doi:10.7717/peerj.3789.
Novotný, Jan Philipp, Chughtai, Ahmed Ali, Kostrouchová, Markéta, Kostrouchová, Veronika, Kostrouch, David, Kaššák, Filip, Kaňa, Radek, Schierwater, Bernd, Kostrouchová, Marta, & Kostrouch, Zdenek. Trichoplax adhaerens reveals a network of nuclear receptors sensitive to 9- cis -retinoic acid at the base of metazoan evolution. United States. https://doi.org/10.7717/peerj.3789
Novotný, Jan Philipp, Chughtai, Ahmed Ali, Kostrouchová, Markéta, Kostrouchová, Veronika, Kostrouch, David, Kaššák, Filip, Kaňa, Radek, Schierwater, Bernd, Kostrouchová, Marta, and Kostrouch, Zdenek. Fri .
"Trichoplax adhaerens reveals a network of nuclear receptors sensitive to 9- cis -retinoic acid at the base of metazoan evolution". United States. https://doi.org/10.7717/peerj.3789. https://www.osti.gov/servlets/purl/1628930.
@article{osti_1628930,
title = {Trichoplax adhaerens reveals a network of nuclear receptors sensitive to 9- cis -retinoic acid at the base of metazoan evolution},
author = {Novotný, Jan Philipp and Chughtai, Ahmed Ali and Kostrouchová, Markéta and Kostrouchová, Veronika and Kostrouch, David and Kaššák, Filip and Kaňa, Radek and Schierwater, Bernd and Kostrouchová, Marta and Kostrouch, Zdenek},
abstractNote = {Trichoplax adhaerens, the only known species of Placozoa is likely to be closely related to an early metazoan that preceded branching of Cnidaria and Bilateria. This animal species is surprisingly well adapted to free life in the World Ocean inhabiting tidal costal zones of oceans and seas with warm to moderate temperatures and shallow waters. The genome of T. adhaerens (sp. Grell) includes four nuclear receptors, namely orthologue of RXR (NR2B), HNF4 (NR2A), COUP-TF (NR2F) and ERR (NR3B) that show a high degree of similarity with human orthologues. In the case of RXR, the sequence identity to human RXR alpha reaches 81% in the DNA binding domain and 70% in the ligand binding domain. We show that T. adhaerens RXR (TaRXR) binds 9-cis retinoic acid (9-cis-RA) with high affinity, as well as high specificity and that exposure of T. adhaerens to 9-cis-RA regulates the expression of the putative T. adhaerens orthologue of vertebrate L-malate-NADP+ oxidoreductase (EC 1.1.1.40) which in vertebrates is regulated by a heterodimer of RXR and thyroid hormone receptor. Treatment by 9-cis-RA alters the relative expression profile of T. adhaerens nuclear receptors, suggesting the existence of natural ligands. Keeping with this, algal food composition has a profound effect on T. adhaerens growth and appearance. We show that nanomolar concentrations of 9-cis-RA interfere with T. adhaerens growth response to specific algal food and causes growth arrest. Our results uncover an endocrine-like network of nuclear receptors sensitive to 9-cis-RA in T. adhaerens and support the existence of a ligand-sensitive network of nuclear receptors at the base of metazoan evolution.},
doi = {10.7717/peerj.3789},
journal = {PeerJ},
number = ,
volume = 5,
place = {United States},
year = {Fri Sep 29 00:00:00 EDT 2017},
month = {Fri Sep 29 00:00:00 EDT 2017}
}
Works referenced in this record:
The evolution of the nuclear receptor superfamily
journal, June 2004
- Escriva, Héctor; Bertrand, Stéphanie; Laudet, Vincent
- Essays in Biochemistry, Vol. 40
Retinoic acid receptors and retinoid X receptors: interactions with endogenous retinoic acids.
journal, January 1993
- Allenby, G.; Bocquel, M. T.; Saunders, M.
- Proceedings of the National Academy of Sciences, Vol. 90, Issue 1
New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0
journal, March 2010
- Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent
- Systematic Biology, Vol. 59, Issue 3
Protein evolution by molecular tinkering: diversification of the nuclear receptor superfamily from a ligand-dependent ancestor
text, January 2010
- Bridgham, J. T.; Eick, G. N.; Larroux, C.
- Public Library of Science (PLoS)
A nuclear receptor-like pathway regulating multidrug resistance in fungi
journal, April 2008
- Thakur, Jitendra K.; Arthanari, Haribabu; Yang, Fajun
- Nature, Vol. 452, Issue 7187
Evolution of Retinoic Acid Receptors and Retinoic Acid Signaling
book, January 2014
- Gutierrez-Mazariegos, Juliana; Schubert, Michael; Laudet, Vincent
- Subcellular Biochemistry
Origin and evolution of the ligand-binding ability of nuclear receptors
journal, March 2011
- Markov, Gabriel V.; Laudet, Vincent
- Molecular and Cellular Endocrinology, Vol. 334, Issue 1-2
Activation of Liver X Receptors and Retinoid X Receptors Induces Growth Arrest and Apoptosis in Insulin-Secreting Cells
journal, April 2007
- Wente, Wolf; Brenner, Martin B.; Zitzer, Heike
- Endocrinology, Vol. 148, Issue 4
The nuclear receptor superfamily
journal, February 2003
- Robinson-Rechavi, M.
- Journal of Cell Science, Vol. 116, Issue 4
Tissue-specific regulation of two functional malic enzyme mRNAs by triiodothyronine
journal, September 1985
- Dozin, Beatrice; Magnuson, Mark A.; Nikodem, Vera M.
- Biochemistry, Vol. 24, Issue 20
Database resources of the National Center for Biotechnology Information
journal, November 2018
- Sayers, Eric W.; Agarwala, Richa; Bolton, Evan E.
- Nucleic Acids Research, Vol. 47, Issue D1
Ligand binding was acquired during evolution of nuclear receptors
journal, June 1997
- Escriva, H.; Safi, R.; Hanni, C.
- Proceedings of the National Academy of Sciences, Vol. 94, Issue 13
Database resources of the National Center for Biotechnology Information
journal, December 2007
- Wheeler, D. L.; Barrett, T.; Benson, D. A.
- Nucleic Acids Research, Vol. 36, Issue Database
Multigene Phylogeny of Choanozoa and the Origin of Animals
journal, May 2008
- Shalchian-Tabrizi, Kamran; Minge, Marianne A.; Espelund, Mari
- PLoS ONE, Vol. 3, Issue 5
Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega
journal, January 2011
- Sievers, Fabian; Wilm, Andreas; Dineen, David
- Molecular Systems Biology, Vol. 7, Issue 1
Phytol metabolites are circulating dietary factors that activate the nuclear receptor RXR.
journal, August 1996
- Kitareewan, S.; Burka, L. T.; Tomer, K. B.
- Molecular Biology of the Cell, Vol. 7, Issue 8
Maternal control of the Drosophila dorsal-ventral body axis
journal, May 2014
- Stein, David S.; Stevens, Leslie M.
- Wiley Interdisciplinary Reviews: Developmental Biology, Vol. 3, Issue 5
Evolution and Diversification of the Nuclear Receptor Superfamilya
journal, May 1998
- Escriva, Hector; Langlois, Marie-Claire; Mendonca, Ricardo Luis
- Annals of the New York Academy of Sciences, Vol. 839, Issue 1 TRENDS IN COM
Ligand-protein interactions in nuclear receptors of hormones
journal, June 2000
- Egea, Pascal F.; Klaholz, Bruno P.; Moras, Dino
- FEBS Letters, Vol. 476, Issue 1-2
Activation of RXR–PPAR heterodimers by organotin environmental endocrine disruptors
journal, March 2009
- le Maire, Albane; Grimaldi, Marina; Roecklin, Dominique
- EMBO reports, Vol. 10, Issue 4
New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0
text, January 2010
- Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent
- Oxford University Press
Amphioxus Postembryonic Development Reveals the Homology of Chordate Metamorphosis
journal, June 2008
- Paris, Mathilde; Escriva, Hector; Schubert, Michael
- Current Biology, Vol. 18, Issue 11
Inactivation of the Nuclear Orphan Receptor COUP-TFII by Small Chemicals
journal, January 2017
- Le Guével, Rémy; Oger, Frédérik; Martinez-Jimenez, Celia P.
- ACS Chemical Biology, Vol. 12, Issue 3
Potentially biogenic carbon preserved in a 4.1 billion-year-old zircon
journal, October 2015
- Bell, Elizabeth A.; Boehnke, Patrick; Harrison, T. Mark
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 47
Nuclear receptor-like transcription factors in fungi
journal, February 2009
- Naar, A. M.; Thakur, J. K.
- Genes & Development, Vol. 23, Issue 4
Activation of a member of the steroid hormone receptor superfamily by peroxisome proliferators
journal, October 1990
- Issemann, Isabelle; Green, Stephen
- Nature, Vol. 347, Issue 6294
Never Ending Analysis of a Century Old Evolutionary Debate: “Unringing” the Urmetazoon Bell
journal, February 2016
- Schierwater, Bernd; Holland, Peter W. H.; Miller, David J.
- Frontiers in Ecology and Evolution, Vol. 4
Trichoplax, the simplest known animal, contains an estrogen-related receptor but no estrogen receptor: Implications for estrogen receptor evolution
journal, August 2008
- Baker, Michael
- Nature Precedings
Trichoplax, the simplest known animal, contains an estrogen-related receptor but no estrogen receptor: Implications for estrogen receptor evolution
journal, August 2008
- Baker, Michael
- Nature Precedings
Evolution of the nuclear receptor superfamily: early diversification from an ancestral orphan receptor
journal, December 1997
- Laudet, V.
- Journal of Molecular Endocrinology, Vol. 19, Issue 3
Evolution of the nuclear receptor superfamily: early diversification from an ancestral orphan receptor
journal, December 1997
- Laudet, V.
- Journal of Molecular Endocrinology, Vol. 19, Issue 3
The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans
journal, February 2008
- King, Nicole; Westbrook, M. Jody; Young, Susan L.
- Nature, Vol. 451, Issue 7180
Ligand binding and nuclear receptor evolution
journal, July 2000
- Escriva, Hector; Delaunay, Franck; Laudet, Vincent
- BioEssays, Vol. 22, Issue 8
Trichoplax, the simplest known animal, contains an estrogen-related receptor but no estrogen receptor: Implications for estrogen receptor evolution
journal, October 2008
- Baker, Michael E.
- Biochemical and Biophysical Research Communications, Vol. 375, Issue 4
Steroid/thyroid hormone receptor genes in Caenorhabditis elegans.
journal, January 1995
- Kostrouch, Z.; Kostrouchova, M.; Rall, J. E.
- Proceedings of the National Academy of Sciences, Vol. 92, Issue 1
An Endogenous Mammalian Retinoid X Receptor Ligand, At Last!
journal, May 2016
- de Lera, Ángel R.; Krezel, Wojciech; Rühl, Ralph
- ChemMedChem, Vol. 11, Issue 10
Identification of thyroid hormone receptors in rat liver nuclei by photoaffinity labeling with L-thyroxine and triiodo-L-thyronine
journal, September 1985
- Dozin, Beatrice; Cahnmann, Hans J.; Nikodem, Vera M.
- Biochemistry, Vol. 24, Issue 19
Non-Photochemical Quenching in Cryptophyte Alga Rhodomonas salina Is Located in Chlorophyll a/c Antennae
journal, January 2012
- Kaňa, Radek; Kotabová, Eva; Sobotka, Roman
- PLoS ONE, Vol. 7, Issue 1
The Trox-2 Hox/ParaHox gene of Trichoplax (Placozoa) marks an epithelial boundary
journal, April 2004
- Dellaporta, Stephen; Holland, Peter; Schierwater, Bernd
- Development Genes and Evolution, Vol. 214, Issue 4
SMART: recent updates, new developments and status in 2015
journal, October 2014
- Letunic, Ivica; Doerks, Tobias; Bork, Peer
- Nucleic Acids Research, Vol. 43, Issue D1
Alterations in retinoid X receptor-α expression contribute to cell-type dependent differences in thyroid hormone regulation of malic enzyme transcription
journal, June 2000
- Fang, Xuexun; Hillgartner, F. Bradley
- Molecular and Cellular Endocrinology, Vol. 164, Issue 1-2
Global Habitat Suitability and Ecological Niche Separation in the Phylum Placozoa
journal, November 2015
- Paknia, Omid; Schierwater, Bernd
- PLOS ONE, Vol. 10, Issue 11
Is 9-Cis-Retinoic Acid the Endogenous Ligand for the Retinoic Acid-X Receptor?
journal, December 2006
- Wolf, George
- Nutrition Reviews, Vol. 64, Issue 12
Retinoic acid X receptor in the diploblast, Tripedalia cystophora
journal, November 1998
- Kostrouch, Z.; Kostrouchova, M.; Love, W.
- Proceedings of the National Academy of Sciences, Vol. 95, Issue 23
Protein Evolution by Molecular Tinkering: Diversification of the Nuclear Receptor Superfamily from a Ligand-Dependent Ancestor
journal, October 2010
- Bridgham, Jamie T.; Eick, Geeta N.; Larroux, Claire
- PLoS Biology, Vol. 8, Issue 10
9-cis-Retinoic Acid Decreases the Level of Its Cognate Receptor, Retinoid X Receptor, through Acceleration of the Turnover
journal, July 1999
- Nomura, Yoshio; Nagaya, Takashi; Hayashi, Yoshitaka
- Biochemical and Biophysical Research Communications, Vol. 260, Issue 3
Thyroid hormone receptor orthologues from invertebrate species with emphasis on Schistosoma mansoni
journal, January 2007
- Wu, Wenjie; Niles, Edward G.; LoVerde, Philip T.
- BMC Evolutionary Biology, Vol. 7, Issue 1
Emerging developmental model systems
journal, July 2006
- Kiefer, Julie C.
- Developmental Dynamics, Vol. 235, Issue 10
Phycobilisome Mobility and Its Role in the Regulation of Light Harvesting in Red Algae
journal, June 2014
- Kaňa, Radek; Kotabová, Eva; Lukeš, Martin
- Plant Physiology, Vol. 165, Issue 4
The Trichoplax genome and the nature of placozoans
journal, August 2008
- Srivastava, Mansi; Begovic, Emina; Chapman, Jarrod
- Nature, Vol. 454, Issue 7207
The genome portal of the Department of Energy Joint Genome Institute: 2014 updates
journal, November 2013
- Nordberg, Henrik; Cantor, Michael; Dusheyko, Serge
- Nucleic Acids Research, Vol. 42, Issue D1
Activation of Liver X Receptors and Retinoid X Receptors Induces Growth Arrest and Apoptosis in Insulin-Secreting Cells
journal, April 2007
- Wente, Wolf; Brenner, Martin B.; Zitzer, Heike
- Endocrinology, Vol. 148, Issue 4
The retinoid X receptors and their ligands
journal, January 2012
- Dawson, Marcia I.; Xia, Zebin
- Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, Vol. 1821, Issue 1
MINIREVIEW: Interactions Among a Subfamily of Nuclear Hormone Receptors: The Regulatory Zipper Model
journal, September 1990
- Forman, Barry Marc; Samuels, Herbert H.
- Molecular Endocrinology, Vol. 4, Issue 9
Inactivation of the Nuclear Orphan Receptor COUP-TFII by Small Chemicals
journal, January 2017
- Le Guével, Rémy; Oger, Frédérik; Martinez-Jimenez, Celia P.
- ACS Chemical Biology, Vol. 12, Issue 3
Polyunsaturated Fatty Acids Including Docosahexaenoic and Arachidonic Acid Bind to the Retinoid X Receptor α Ligand-binding Domain
journal, April 2004
- Lengqvist, Johan; Mata de Urquiza, Alexander; Bergman, Ann-Charlotte
- Molecular & Cellular Proteomics, Vol. 3, Issue 7
COUP orphan receptors are negative regulators of retinoic acid response pathways
journal, October 1992
- Tran, P.; Zhang, X. K.; Salbert, G.
- Molecular and Cellular Biology, Vol. 12, Issue 10
A nuclear receptor-like pathway regulating multidrug resistance in fungi
journal, April 2008
- Thakur, Jitendra K.; Arthanari, Haribabu; Yang, Fajun
- Nature, Vol. 452, Issue 7187
Activation of a member of the steroid hormone receptor superfamily by peroxisome proliferators
journal, October 1990
- Issemann, Isabelle; Green, Stephen
- Nature, Vol. 347, Issue 6294
The nuclear receptor superfamily
journal, February 2003
- Robinson-Rechavi, M.
- Journal of Cell Science, Vol. 116, Issue 4
Evolution of Retinoic Acid Receptors and Retinoic Acid Signaling
book, January 2014
- Gutierrez-Mazariegos, Juliana; Schubert, Michael; Laudet, Vincent
- Subcellular Biochemistry
Origin and evolution of the ligand-binding ability of nuclear receptors
journal, March 2011
- Markov, Gabriel V.; Laudet, Vincent
- Molecular and Cellular Endocrinology, Vol. 334, Issue 1-2
Potentially biogenic carbon preserved in a 4.1 billion-year-old zircon
journal, October 2015
- Bell, Elizabeth A.; Boehnke, Patrick; Harrison, T. Mark
- Proceedings of the National Academy of Sciences, Vol. 112, Issue 47
Database resources of the National Center for Biotechnology Information
journal, October 2020
- Sayers, Eric W.; Beck, Jeffrey; Bolton, Evan E.
- Nucleic Acids Research, Vol. 49, Issue D1
Mechanisms and significance of nuclear receptor auto- and cross-regulation
journal, January 2011
- Bagamasbad, Pia; Denver, Robert J.
- General and Comparative Endocrinology, Vol. 170, Issue 1
Amphioxus Postembryonic Development Reveals the Homology of Chordate Metamorphosis
journal, June 2008
- Paris, Mathilde; Escriva, Hector; Schubert, Michael
- Current Biology, Vol. 18, Issue 11
Nuclear receptors from the ctenophore Mnemiopsis leidyi lack a zinc-finger DNA-binding domain: lineage-specific loss or ancestral condition in the emergence of the nuclear receptor superfamily?
journal, January 2011
- Reitzel, Adam M.; Pang, Kevin; Ryan, Joseph F.
- EvoDevo, Vol. 2, Issue 1
Phytol metabolites are circulating dietary factors that activate the nuclear receptor RXR.
journal, August 1996
- Kitareewan, S.; Burka, L. T.; Tomer, K. B.
- Molecular Biology of the Cell, Vol. 7, Issue 8
Spatial regulation of Drosophila Snake protease activity in the generation of dorsal-ventral polarity
journal, December 1995
- Smith, Cynthia L.; Giordano, Heidi; Schwartz, Mark
- Development, Vol. 121, Issue 12
The Diploblast-Bilateria sister hypothesis: parallel evolution of a nervous systems in animals
journal, September 2009
- Schierwater, Bernd; Kolokotronis, Sergios-Orestis; Eitel, Michael
- Communicative & Integrative Biology, Vol. 2, Issue 5
Steroid/thyroid hormone receptor genes in Caenorhabditis elegans.
journal, January 1995
- Kostrouch, Z.; Kostrouchova, M.; Rall, J. E.
- Proceedings of the National Academy of Sciences, Vol. 92, Issue 1
Phycobilisome Mobility and Its Role in the Regulation of Light Harvesting in Red Algae
journal, June 2014
- Kaňa, Radek; Kotabová, Eva; Lukeš, Martin
- Plant Physiology, Vol. 165, Issue 4
The structure of the nuclear hormone receptors
journal, May 1999
- Kumar, Raj; Thompson, E. Brad
- Steroids, Vol. 64, Issue 5
Multigene Phylogeny of Choanozoa and the Origin of Animals
journal, May 2008
- Shalchian-Tabrizi, Kamran; Minge, Marianne A.; Espelund, Mari
- PLoS ONE, Vol. 3, Issue 5
Docosahexaenoic Acid, a Ligand for the Retinoid X Receptor in Mouse Brain
journal, December 2000
- Urquiza, A. M. d.; Liu, S.; Sjoberg, M.
- Science, Vol. 290, Issue 5499
Retinoic acid receptors and retinoid X receptors: interactions with endogenous retinoic acids.
journal, January 1993
- Allenby, G.; Bocquel, M. T.; Saunders, M.
- Proceedings of the National Academy of Sciences, Vol. 90, Issue 1
Ligand binding was acquired during evolution of nuclear receptors
journal, June 1997
- Escriva, H.; Safi, R.; Hanni, C.
- Proceedings of the National Academy of Sciences, Vol. 94, Issue 13
A Fast Photoisomerization Method for the Preparation of Tritium-Labeled 9-cis-Retinoic Acid of High Specific Activity
journal, May 1995
- Cahnmann, H. J.
- Analytical Biochemistry, Vol. 227, Issue 1
Retinoic acid X receptor in the diploblast, Tripedalia cystophora
journal, November 1998
- Kostrouch, Z.; Kostrouchova, M.; Love, W.
- Proceedings of the National Academy of Sciences, Vol. 95, Issue 23
9-cis-13,14-Dihydroretinoic Acid Is an Endogenous Retinoid Acting as RXR Ligand in Mice
journal, June 2015
- Rühl, Ralph; Krzyżosiak, Agnieszka; Niewiadomska-Cimicka, Anna
- PLOS Genetics, Vol. 11, Issue 6
SMART, a simple modular architecture research tool: Identification of signaling domains
journal, May 1998
- Schultz, J.; Milpetz, F.; Bork, P.
- Proceedings of the National Academy of Sciences, Vol. 95, Issue 11
SMART, a simple modular architecture research tool: Identification of signaling domains
journal, May 1998
- Schultz, J.; Milpetz, F.; Bork, P.
- Proceedings of the National Academy of Sciences, Vol. 95, Issue 11
Database resources of the National Center for Biotechnology Information
journal, January 2006
- Wheeler, D. L.
- Nucleic Acids Research, Vol. 34, Issue 90001
Locust retinoid X receptors: 9-Cis-retinoic acid in embryos from a primitive insect
journal, July 2008
- Nowickyj, S. M.; Chithalen, J. V.; Cameron, D.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 28
Locust retinoid X receptors: 9-Cis-retinoic acid in embryos from a primitive insect
journal, July 2008
- Nowickyj, S. M.; Chithalen, J. V.; Cameron, D.
- Proceedings of the National Academy of Sciences, Vol. 105, Issue 28
The genome of the choanoflagellate Monosiga brevicollis and the origin of metazoans
journal, February 2008
- King, Nicole; Westbrook, M. Jody; Young, Susan L.
- Nature, Vol. 451, Issue 7180
The Trichoplax genome and the nature of placozoans
journal, August 2008
- Srivastava, Mansi; Begovic, Emina; Chapman, Jarrod
- Nature, Vol. 454, Issue 7207
Nuclear receptor-like transcription factors in fungi
journal, February 2009
- Naar, A. M.; Thakur, J. K.
- Genes & Development, Vol. 23, Issue 4
Nuclear receptors in nematode development: Natural experiments made by a phylum
journal, February 2015
- Kostrouchova, Marta; Kostrouch, Zdenek
- Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms, Vol. 1849, Issue 2
Thyroid hormone receptor orthologues from invertebrate species with emphasis on Schistosoma mansoni
journal, January 2007
- Wu, Wenjie; Niles, Edward G.; LoVerde, Philip T.
- BMC Evolutionary Biology, Vol. 7, Issue 1
Docosahexaenoic Acid, a Ligand for the Retinoid X Receptor in Mouse Brain
journal, December 2000
- Urquiza, A. M. d.; Liu, S.; Sjoberg, M.
- Science, Vol. 290, Issue 5499
Novel Cell Types, Neurosecretory Cells, and Body Plan of the Early-Diverging Metazoan Trichoplax adhaerens
journal, July 2014
- Smith, Carolyn L.; Varoqueaux, Frédérique; Kittelmann, Maike
- Current Biology, Vol. 24, Issue 14
The retinoid X receptors and their ligands
journal, January 2012
- Dawson, Marcia I.; Xia, Zebin
- Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, Vol. 1821, Issue 1
Global Habitat Suitability and Ecological Niche Separation in the Phylum Placozoa
journal, November 2015
- Paknia, Omid; Schierwater, Bernd
- PLOS ONE, Vol. 10, Issue 11
Mechanisms and significance of nuclear receptor auto- and cross-regulation
journal, January 2011
- Bagamasbad, Pia; Denver, Robert J.
- General and Comparative Endocrinology, Vol. 170, Issue 1
Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega
journal, January 2011
- Sievers, Fabian; Wilm, Andreas; Dineen, David
- Molecular Systems Biology, Vol. 7, Issue 1
Emerging developmental model systems
journal, July 2006
- Kiefer, Julie C.
- Developmental Dynamics, Vol. 235, Issue 10
A Fast Photoisomerization Method for the Preparation of Tritium-Labeled 9-cis-Retinoic Acid of High Specific Activity
journal, May 1995
- Cahnmann, H. J.
- Analytical Biochemistry, Vol. 227, Issue 1
New Algorithms and Methods to Estimate Maximum-Likelihood Phylogenies: Assessing the Performance of PhyML 3.0
text, January 2010
- Guindon, Stéphane; Dufayard, Jean-François; Lefort, Vincent
- ETH Zurich
Activation of RXR–PPAR heterodimers by organotin environmental endocrine disruptors
journal, March 2009
- le Maire, Albane; Grimaldi, Marina; Roecklin, Dominique
- EMBO reports, Vol. 10, Issue 4
Protein Evolution by Molecular Tinkering: Diversification of the Nuclear Receptor Superfamily from a Ligand-Dependent Ancestor
journal, October 2010
- Bridgham, Jamie T.; Eick, Geeta N.; Larroux, Claire
- PLoS Biology, Vol. 8, Issue 10
9-cis-Retinoic Acid Decreases the Level of Its Cognate Receptor, Retinoid X Receptor, through Acceleration of the Turnover
journal, July 1999
- Nomura, Yoshio; Nagaya, Takashi; Hayashi, Yoshitaka
- Biochemical and Biophysical Research Communications, Vol. 260, Issue 3
Never Ending Analysis of a Century Old Evolutionary Debate: “Unringing” the Urmetazoon Bell
journal, February 2016
- Schierwater, Bernd; Holland, Peter W. H.; Miller, David J.
- Frontiers in Ecology and Evolution, Vol. 4
Nuclear receptor complement of the cnidarian Nematostella vectensis: phylogenetic relationships and developmental expression patterns
journal, January 2009
- Reitzel, Adam M.; Tarrant, Ann M.
- BMC Evolutionary Biology, Vol. 9, Issue 1
COUP orphan receptors are negative regulators of retinoic acid response pathways.
journal, October 1992
- Tran, P.; Zhang, X. K.; Salbert, G.
- Molecular and Cellular Biology, Vol. 12, Issue 10
SMART: recent updates, new developments and status in 2015
journal, October 2014
- Letunic, Ivica; Doerks, Tobias; Bork, Peer
- Nucleic Acids Research, Vol. 43, Issue D1
Autoregulation and crossregulation of nuclear receptor genes
journal, September 1994
- Tata, Jamshed R.
- Trends in Endocrinology & Metabolism, Vol. 5, Issue 7
Identification of thyroid hormone receptors in rat liver nuclei by photoaffinity labeling with L-thyroxine and triiodo-L-thyronine
journal, September 1985
- Dozin, Beatrice; Cahnmann, Hans J.; Nikodem, Vera M.
- Biochemistry, Vol. 24, Issue 19
Nuclear receptors from the ctenophore Mnemiopsis leidyi lack a zinc-finger DNA-binding domain: lineage-specific loss or ancestral condition in the emergence of the nuclear receptor superfamily?
journal, January 2011
- Reitzel, Adam M.; Pang, Kevin; Ryan, Joseph F.
- EvoDevo, Vol. 2, Issue 1
Thyroid hormone regulation of malic enzyme synthesis. Dual tissue-specific control.
journal, August 1986
- Dozin, B.; Magnuson, M. A.; Nikodem, V. M.
- Journal of Biological Chemistry, Vol. 261, Issue 22
Overexpression of the alpha-thyroid hormone receptor in avian cell lines. Effects on expression of the malic enzyme gene are selective and cell-specific.
journal, June 1992
- Hillgartner, F. B.; Chen, W.; Goodridge, A. G.
- Journal of Biological Chemistry, Vol. 267, Issue 17
Identification of a thyroid hormone response element in the malic enzyme gene.
journal, May 1990
- Petty, K. J.; Desvergne, B.; Mitsuhashi, T.
- Journal of Biological Chemistry, Vol. 265, Issue 13
Thyroid Hormone Regulation of Transcription Factors Involved in Malic Enzyme Gene Expression
journal, July 1989
- Petty, K. J.; Morioka, H.; Mitsuhashi, T.
- Journal of Biological Chemistry, Vol. 264, Issue 19
Spatial regulation of Drosophila Snake protease activity in the generation of dorsal-ventral polarity
journal, December 1995
- Smith, Cynthia L.; Giordano, Heidi; Schwartz, Mark
- Development, Vol. 121, Issue 12
Works referencing / citing this record:
Bioeffects of Prunus spinosa L. fruit ethanol extract on reproduction and phenotypic plasticity of Trichoplax adhaerens Schulze, 1883 (Placozoa)
journal, April 2019
- Albertini, Maria Cristina; Fraternale, Daniele; Semprucci, Federica
- PeerJ, Vol. 7