3-Keto-Steroid transactivation of mineralocorticoid receptors from Amur sturgeon (Acipenser schrenckii) and tropical gar (Atractosteus tropicus)

We investigated the response to a panel of steroids of the mineralocorticoid receptor (MR) in Amur sturgeon and tropical gar, two basal ray-finned fish, whose ancestors evolved before zebrafish and other teleosts. Half-maximal responses (EC50s) for transcriptional activation of sturgeon MR by 11-deoxycorticosterone, corticosterone, 11-deoxycortisol, cortisol and aldosterone, and progesterone were between 13 pM and 150 pM. Gar MR EC50s were between 8 pM and 55 pM. Such low EC50s support regulation of MR activity by these steroids in sturgeon and gar. Companion studies with human MR and zebrafish MR found higher EC50s compared to EC50s for sturgeon and gar MR, with EC50s for zebrafish MR closer to gar and sturgeon MR than was human MR. Zebrafish MR EC50s were between 75 pM and 740 pM; for human MR, EC50s were between 65 pM and 2 nM. Unexpectedly, progesterone was an agonist for all ray-finned fish MRs, in contrast to its antagonist activity for human MR. Sturgeon, gar and zebrafish MRs contain a serine corresponding to serine-810 in human MR, hypothesized as critical for progesterone antagonism. Progesterone is an agonist forSer810Leu MR. Our data suggests an alternative mechanism for progesterone as an MR agonist in these three ray-finned fishes.

[1]  M. Baker,et al.  Allosteric role of the amino-terminal A/B domain on corticosteroid transactivation of gar and human glucocorticoid receptors , 2015, The Journal of Steroid Biochemistry and Molecular Biology.

[2]  M. Baker,et al.  Origin of the response to adrenal and sex steroids: Roles of promiscuity and co-evolution of enzymes and steroid receptors , 2015, The Journal of Steroid Biochemistry and Molecular Biology.

[3]  M. Taves,et al.  Steroid profiling reveals widespread local regulation of glucocorticoid levels during mouse development. , 2015, Endocrinology.

[4]  N. Faresse.  Post-translational modifications of the mineralocorticoid receptor: How to dress the receptor according to the circumstances? , 2014, The Journal of Steroid Biochemistry and Molecular Biology.

[5]  G. Jirikowski,et al.  Adrenal steroids in the brain: Role of the intrinsic expression of corticosteroid-binding globulin (CBG) in the stress response , 2014, Steroids.

[6]  M. Baker,et al.  Evolution of hormone selectivity in glucocorticoid and mineralocorticoid receptors , 2013, The Journal of Steroid Biochemistry and Molecular Biology.

[7]  J. Seckl,et al.  11β-hydroxysteroid dehydrogenases: intracellular gate-keepers of tissue glucocorticoid action. , 2013, Physiological reviews.

[8]  M. Lombès,et al.  The mineralocorticoid signaling pathway throughout development: expression, regulation and pathophysiological implications. , 2013, Biochimie.

[9]  L. Guillette,et al.  Molecular cloning and characterization of the corticoid receptors from the American alligator , 2013, Molecular and Cellular Endocrinology.

[10]  P. Griffin,et al.  Binding of the N-terminal Region of Coactivator TIF2 to the Intrinsically Disordered AF1 Domain of the Glucocorticoid Receptor Is Accompanied by Conformational Reorganizations* , 2012, The Journal of Biological Chemistry.

[11]  C. Gomez-Sanchez,et al.  The Ubiquitous Mineralocorticoid Receptor: Clinical Implications , 2012, Current Hypertension Reports.

[12]  F. Wurm,et al.  Poly(ethyleneimine)-mediated large-scale transient gene expression: influence of molecular weight, polydispersity and N-propionyl groups. , 2012, Macromolecular bioscience.

[13]  M. Young,et al.  Mechanisms of ligand specificity of the mineralocorticoid receptor. , 2012, The Journal of endocrinology.

[14]  Chie Mori,et al.  Corticosteroids stimulate the amphibious behavior in mudskipper: Potential role of mineralocorticoid receptors in teleost fish , 2011, Physiology & Behavior.

[15]  M. Nei,et al.  MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. , 2011, Molecular biology and evolution.

[16]  C. Gomez-Sanchez,et al.  Extra-adrenal glucocorticoids and mineralocorticoids: evidence for local synthesis, regulation, and function. , 2011, American journal of physiology. Endocrinology and metabolism.

[17]  A. Bass,et al.  Evolution of ligand specificity in vertebrate corticosteroid receptors , 2011, BMC Evolutionary Biology.

[18]  Eric A. Ortlund,et al.  Protein Evolution by Molecular Tinkering: Diversification of the Nuclear Receptor Superfamily from a Ligand-Dependent Ancestor , 2010, PLoS biology.

[19]  S. McCormick,et al.  11-Deoxycortisol is a corticosteroid hormone in the lamprey , 2010, Proceedings of the National Academy of Sciences.

[20]  T. Iguchi,et al.  Estrogen-dependent transactivation of amphioxus steroid hormone receptor via both estrogen and androgen response elements. , 2010, Endocrinology.

[21]  P. Fuller,et al.  Structural and functional characterization of the interdomain interaction in the mineralocorticoid receptor. , 2009, Molecular endocrinology.

[22]  Gabriel V. Markov,et al.  Independent elaboration of steroid hormone signaling pathways in metazoans , 2009, Proceedings of the National Academy of Sciences of the United States of America.

[23]  A. Odermatt,et al.  Mineralocorticoid receptors: Emerging complexity and functional diversity , 2009, Steroids.

[24]  L. Guillette,et al.  Molecular cloning, characterization, and evolutionary analysis of estrogen receptors from phylogenetically ancient fish. , 2008, Endocrinology.

[25]  S. Carroll,et al.  Evolution of hormone signaling in elasmobranchs by exploitation of promiscuous receptors. , 2008, Molecular biology and evolution.

[26]  G. Flik,et al.  Corticosteroid receptors involved in stress regulation in common carp, Cyprinus carpio. , 2008, The Journal of endocrinology.

[27]  N. Bury,et al.  Evolution of the corticosteroid receptor signalling pathway in fish. , 2007, General and comparative endocrinology.

[28]  Fumiko Ohta,et al.  The medaka draft genome and insights into vertebrate genome evolution , 2007, Nature.

[29]  Donald P. McDonnell,et al.  International Union of Pharmacology. LXV. The Pharmacology and Classification of the Nuclear Receptor Superfamily: Glucocorticoid, Mineralocorticoid, Progesterone, and Androgen Receptors , 2006, Pharmacological Reviews.

[30]  P. Prunet,et al.  Multiple corticosteroid receptors in fish: from old ideas to new concepts. , 2006, General and comparative endocrinology.

[31]  P. Webb.  Faculty Opinions recommendation of Evolution of hormone-receptor complexity by molecular exploitation. , 2006 .

[32]  M. Lombès,et al.  The mineralocorticoid receptor: a journey exploring its diversity and specificity of action. , 2005, Molecular endocrinology.

[33]  H. Xu,et al.  Structural and biochemical mechanisms for the specificity of hormone binding and coactivator assembly by mineralocorticoid receptor. , 2005, Molecular cell.

[34]  X. Hu,et al.  The ligand-dependent interaction of mineralocorticoid receptor with coactivator and corepressor peptides suggests multiple activation mechanisms. , 2005, Molecular endocrinology.

[35]  D. B. Hales,et al.  Overview of steroidogenic enzymes in the pathway from cholesterol to active steroid hormones. , 2004, Endocrine reviews.

[36]  Charles E. Chapple,et al.  Genome duplication in the teleost fish Tetraodon nigroviridis reveals the early vertebrate proto-karyotype , 2004, Nature.

[37]  D. Pearce,et al.  Mechanisms of mineralocorticoid action: determinants of receptor specificity and actions of regulated gene products , 2004, Trends in Endocrinology & Metabolism.

[38]  Robert C. Edgar,et al.  MUSCLE: multiple sequence alignment with high accuracy and high throughput. , 2004, Nucleic acids research.

[39]  M. Baker,et al.  Evolution of glucocorticoid and mineralocorticoid responses: go fish. , 2003, Endocrinology.

[40]  Anna K. Greenwood,et al.  Multiple corticosteroid receptors in a teleost fish: distinct sequences, expression patterns, and transcriptional activities. , 2003, Endocrinology.

[41]  M. Kusakabe,et al.  11beta-hydroxysteroid dehydrogenase complementary deoxyribonucleic acid in rainbow trout: cloning, sites of expression, and seasonal changes in gonads. , 2003, Endocrinology.

[42]  D. Russell,et al.  Clinical importance of the cytochromes P450 , 2002, The Lancet.

[43]  C. Breuner,et al.  Plasma binding proteins as mediators of corticosteroid action in vertebrates. , 2002, The Journal of endocrinology.

[44]  T. Willson,et al.  Crystal Structure of the Glucocorticoid Receptor Ligand Binding Domain Reveals a Novel Mode of Receptor Dimerization and Coactivator Recognition , 2002, Cell.

[45]  J. W. Thornton.  Evolution of vertebrate steroid receptors from an ancestral estrogen receptor by ligand exploitation and serial genome expansions , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[46]  P. Sigler,et al.  Activating mineralocorticoid receptor mutation in hypertension exacerbated by pregnancy. , 2000, Science.

[47]  J. Funder,et al.  Exclusion of corticosterone from epithelial mineralocorticoid receptors is insufficient for selectivity of aldosterone action: in vivo binding studies. , 1996, Endocrinology.

[48]  J. Joss,et al.  The steroidogenic response to angiotensin II in the Australian lungfish, Neoceratodus forsteri , 1994, Journal of Comparative Physiology B.

[49]  F. Holsboer,et al.  Pharmacological and functional characterization of human mineralocorticoid and glucocorticoid receptor ligands. , 1993, European journal of pharmacology.

[50]  N. Saitou,et al.  The neighbor-joining method: a new method for reconstructing phylogenetic trees. , 1987, Molecular biology and evolution.

[51]  J. Felsenstein.  CONFIDENCE LIMITS ON PHYLOGENIES: AN APPROACH USING THE BOOTSTRAP , 1985, Evolution; international journal of organic evolution.

[52]  M. Baker,et al.  Epithelial sodium transport and its control by aldosterone: the story of our internal environment revisited. , 2015, Physiological reviews.

[53]  G. Flouriot,et al.  11-deoxycorticosterone is a potent agonist of the rainbow trout (Oncorhynchus mykiss) mineralocorticoid receptor. , 2005, Endocrinology.

[54]  K. Gilmour.  Mineralocorticoid receptors and hormones: fishing for answers. , 2005, Endocrinology.

[55]  N. Saito.  The neighbor-joining method : A new method for reconstructing phylogenetic trees , 1987 .