scholarly journals Transcriptional activation of elephant shark mineralocorticoid receptor by corticosteroids, progesterone, and spironolactone

2019 ◽  
Vol 12 (584) ◽  
pp. eaar2668 ◽  
Author(s):  
Yoshinao Katsu ◽  
Satomi Kohno ◽  
Kaori Oka ◽  
Xiaozhi Lin ◽  
Sumika Otake ◽  
...  
Keyword(s):  
Transcription Factors ◽  
Transcriptional Activation ◽  
Mineralocorticoid Receptor ◽  
Common Ancestor ◽  
Cartilaginous Fish ◽  
Reproductive Physiology ◽  
Elephant Shark ◽  
Terrestrial Vertebrates ◽  
The Common ◽  
The Brain

The mineralocorticoid receptor (MR) is a nuclear receptor and part of a large and diverse family of transcription factors that also includes receptors for glucocorticoids, progesterone, androgens, and estrogens. The corticosteroid aldosterone is the physiological activator of the MR in humans and other terrestrial vertebrates; however, its activator is not known in cartilaginous fish, the oldest group of extant jawed vertebrates. Here, we analyzed the ability of corticosteroids and progesterone to activate the full-length MR from the elephant shark (Callorhinchus milii). On the basis of their measured activities, aldosterone, cortisol, 11-deoxycorticosterone, corticosterone, 11-deoxcortisol, progesterone, and 19-norprogesterone are potential physiological mineralocorticoids. However, aldosterone, the physiological mineralocorticoid in humans and other terrestrial vertebrates, is not found in cartilaginous or ray-finned fish. Although progesterone activates MRs in ray-finned fish, progesterone does not activate MRs in humans, amphibians, or alligator, suggesting that during the transition to terrestrial vertebrates, progesterone lost the ability to activate the MR. Both elephant shark MR and human MR are expressed in the brain, heart, ovary, testis, and other nonepithelial tissues, suggesting that MR expression in diverse tissues evolved in the common ancestor of jawed vertebrates. Our data suggest that 19-norprogesterone– and progesterone-activated MR may have unappreciated functions in reproductive physiology.

scholarly journals Transcriptional Activation of Elephant Shark Mineralocorticoid Receptor by Corticosteroids, Progesterone and Spironolactone

2018 ◽  
Author(s):  
Yoshinao Katsu ◽  
Satomi Kohno ◽  
Kaori Oka ◽  
Xiaozhi Lin ◽  
Sumika Otake ◽  
...  
Keyword(s):  
Transcriptional Activation ◽  
Mineralocorticoid Receptor ◽  
Common Ancestor ◽  
Cartilaginous Fish ◽  
Full Length ◽  
Elephant Shark ◽  
Terrestrial Vertebrates ◽  
Epithelial Tissues ◽  
The Common ◽  
The Brain

AbstractWe report the analysis of activation of full-length mineralocorticoid receptor (MR) from elephant shark, a cartilaginous fish belonging to the oldest group of jawed vertebrates by corticosteroids and progesterone. Based on their measured activities, aldosterone, cortisol, 11-deoxycorticosterone, corticosterone, 11-deoxcortisol, progesterone and 19-norprogesterone are potential physiological mineralocorticoids. However, aldosterone, the physiological mineralocorticoid in humans and other terrestrial vertebrates, is not found in cartilaginous or ray-finned fishes. Although progesterone activates ray-finned fish MRs, progesterone does not activate human, amphibian or alligator MRs, suggesting that during the transition to terrestrial vertebrates, progesterone lost the ability to activate the MR. Both elephant shark MR and human MR are expressed in the brain, heart, ovary, testis and other non-epithelial tissues, indicating that MR expression in diverse tissues evolved in the common ancestor of jawed vertebrates. Our data suggest that progesterone-activated MR may have unappreciated functions in elephant shark ovary and testis.

scholarly journals Transcriptional Activation of Elephant Shark Mineralocorticoid Receptor by Corticosteroids, Progesterone and Spironolactone

2019 ◽  
Author(s):  
Yoshinao Katsu ◽  
Satomi Kohno ◽  
Kaori Oka ◽  
Xiaozhi Lin ◽  
Sumika Otake ◽  
...  
Keyword(s):  
Sequence Analysis ◽  
Human Brain ◽  
Transcriptional Activation ◽  
Mineralocorticoid Receptor ◽  
Cartilaginous Fish ◽  
Full Length ◽  
Rna Sequence ◽  
Elephant Shark ◽  
Terrestrial Vertebrates ◽  
Cartilaginous Fishes

We report the analysis of activation by corticosteroids and progesterone of full-length mineralocorticoid receptor (MR) from elephant shark, a cartilaginous fish belonging to the oldest group of jawed vertebrates.  Based on their measured activities, aldosterone, cortisol, 11-deoxycorticosterone, corticosterone, 11-deoxcortisol, progesterone and 19-norprogesterone are potential physiological mineralocorticoids.  However, aldosterone, the physiological mineralocorticoid in humans and other terrestrial vertebrates, is not found in cartilaginous or ray-finned fishes.  Because progesterone is a precursor for corticosteroids that activate elephant shark MR, we propose that progesterone was an ancestral ligand for elephant shark MR.  Although progesterone activates ray-finned fish MRs, progesterone does not activate human, amphibian or alligator MRs, suggesting that during the transition to terrestrial vertebrates, progesterone lost the ability to activate the MR.  Comparison of RNA-sequence analysis of elephant shark MR with that of human MR suggests that MR expression in the human brain, heart, ovary, testis and other non-epithelial tissues evolved in cartilaginous fishes.  Together, these data suggest that progesterone-activated MR may have unappreciated functions in elephant shark ovary and testis.

scholarly journals Transcriptional Activation of Elephant Shark Mineralocorticoid Receptor by Corticosteroids, Progesterone and Spironolactone

2019 ◽  
Author(s):  
Yoshinao Katsu ◽  
Satomi Kohno ◽  
Kaori Oka ◽  
Xiaozhi Lin ◽  
Sumika Otake ◽  
...  
Keyword(s):  
Sequence Analysis ◽  
Human Brain ◽  
Transcriptional Activation ◽  
Mineralocorticoid Receptor ◽  
Cartilaginous Fish ◽  
Full Length ◽  
Rna Sequence ◽  
Elephant Shark ◽  
Terrestrial Vertebrates ◽  
Cartilaginous Fishes

We report the analysis of activation by corticosteroids and progesterone of full-length mineralocorticoid receptor (MR) from elephant shark, a cartilaginous fish belonging to the oldest group of jawed vertebrates. Based on their measured activities, aldosterone, cortisol, 11-deoxycorticosterone, corticosterone, 11-deoxcortisol, progesterone and 19-norprogesterone are potential physiological mineralocorticoids. However, aldosterone, the physiological mineralocorticoid in humans and other terrestrial vertebrates, is not found in cartilaginous or ray-finned fishes. Because progesterone is a precursor for corticosteroids that activate elephant shark MR, we propose that progesterone was an ancestral ligand for elephant shark MR. Although progesterone activates ray-finned fish MRs, progesterone does not activate human, amphibian or alligator MRs, suggesting that during the transition to terrestrial vertebrates, progesterone lost the ability to activate the MR. Comparison of RNA-sequence analysis of elephant shark MR with that of human MR suggests that MR expression in the human brain, heart, ovary, testis and other non-epithelial tissues evolved in cartilaginous fishes. Together, these data suggest that progesterone-activated MR may have unappreciated functions in elephant shark ovary and testis.

scholarly journals Progesterone: An Enigmatic Ligand for the Mineralocorticoid Receptor

2020 ◽  
Author(s):  
Michael Baker ◽  
Yoshinao Katsu
Keyword(s):  
Mineralocorticoid Receptor ◽  
Physiological Role ◽  
Reproductive Physiology ◽  
Elephant Shark ◽  
Terrestrial Vertebrates ◽  
High Affinity ◽  
Reproductive Tissues ◽  
Terrestrial Vertebrate ◽  
Functional Consequences ◽  
Cartilaginous Fishes

The progesterone receptor (PR) mediates progesterone regulation of female reproductive physiology, as well as gene transcription in non-reproductive tissues, such as brain, bone, lung and vasculature, in both women and men. An unusual property of progesterone is its high affinity for the mineralocorticoid receptor (MR), which regulates electrolyte transport in the kidney in humans and other terrestrial vertebrates. In humans, rats, alligators and frogs, progesterone antagonizes activation of the MR by aldosterone, the physiological mineralocorticoid in terrestrial vertebrates. In contrast, in elephant shark, ray-finned fishes and chickens, progesterone activates the MR. Interestingly, cartilaginous fishes and ray-finned fishes do not synthesize aldosterone, raising the question of which steroid(s) activate the MR in cartilaginous fishes and ray-finned fishes. The simpler synthesis of progesterone, compared to cortisol and other corticosteroids, makes progesterone a candidate physiological activator of the MR in elephant sharks and ray-finned fishes. Elephant shark and ray-finned fish MRs are expressed in diverse tissues, including heart, brain and lung, as well as, ovary and testis, two reproductive tissues that are targets for progesterone, which together suggests a multi-faceted physiological role for progesterone activation of the MR in elephant shark and ray-finned fish. The functional consequences of progesterone as an antagonist of some terrestrial vertebrate MRs and as an agonist of fish and chicken MRs are not fully understood. Indeed, little is known of physiological activities of progesterone via any vertebrate MR.

scholarly journals 30 YEARS OF THE MINERALOCORTICOID RECEPTOR: Evolution of the mineralocorticoid receptor: sequence, structure and function

2017 ◽  
Vol 234 (1) ◽  
pp. T1-T16 ◽  
Author(s):  
Michael E Baker ◽  
Yoshinao Katsu
Keyword(s):  
Transcriptional Activation ◽  
Mineralocorticoid Receptor ◽  
Strong Response ◽  
Terrestrial Vertebrates ◽  
Selective Ligand ◽  
And Function ◽  
Receptor Evolution ◽  
Corticoid Receptor ◽  
Jawless Fish ◽  
Combine Sequence

The mineralocorticoid receptor (MR) is descended from a corticoid receptor (CR), which has descendants in lamprey and hagfish, cyclostomes (jawless fish), a taxon that evolved at the base of the vertebrate line. A distinct MR and GR first appear in cartilaginous fishes (Chondrichthyes), such as sharks, skates, rays and chimeras. Skate MR has a strong response to corticosteroids that are mineralocorticoids and glucocorticoids in humans. The half-maximal responses (EC50s) for skate MR for the mineralocorticoids aldosterone and 11-deoxycorticosterone are 0.07 nM and 0.03 nM, respectively. EC50s for the glucocorticoids cortisol and corticosterone are 1 nM and 0.09 nM, respectively. The physiological mineralocorticoid in ray-finned fish, which do not synthesize aldosterone, is not fully understood because several 3-ketosteroids, including cortisol, 11-deoxycortisol, corticosterone, 11-deoxycorticosterone and progesterone are transcriptional activators of fish MR. Further divergence of the MR and GR in terrestrial vertebrates, which synthesize aldosterone, led to emergence of aldosterone as a selective ligand for the MR. Here, we combine sequence analysis of the CR and vertebrate MRs and GRs, analysis of crystal structures of human MR and GR and data on transcriptional activation by 3-ketosteroids of wild-type and mutant MRs and GRs to investigate the evolution of selectivity for 3-ketosteroids by the MR in terrestrial vertebrates and ray-finned fish, as well as the basis for binding of some glucocorticoids by human MR and other vertebrate MRs.

scholarly journals Aldosterone, Dexamethasone and Triamcinolone Activate African Lungfish Mineralocorticoid Receptor: Increased Activation After Removal of the Amino-Terminal Domain

2021 ◽  
Author(s):  
Yoshinao Katsu ◽  
Shin Oana ◽  
Xiaozhi Lin ◽  
Susumu Hyodo ◽  
Michael E. Baker
Keyword(s):  
Transcriptional Activation ◽  
Mineralocorticoid Receptor ◽  
Activation Function ◽  
Binding Domain ◽  
Full Length ◽  
Terrestrial Vertebrates ◽  
Amino Terminal ◽  
Terminal Domain ◽  
Cartilaginous Fishes ◽  
African Lungfish

A distinct mineralocorticoid receptor (MR) ortholog first appears in cartilaginous fishes, such as sharks, skates, rays and chimaeras. Although aldosterone, the main physiological mineralocorticoid in humans and other terrestrial vertebrates, is a transcriptional activator of skate MR and elephant shark MR, aldosterone is not synthesized by cartilaginous fishes. Aldosterone, first appears in lungfish, which are lobe-finned fish that are forerunners of terrestrial vertebrates. Aldosterone activation of the MR regulates internal homeostasis of water, sodium and potassium, which was critical in the conquest of land by vertebrates. We studied transcriptional activation of the slender African lungfish (Protopterus dolloi) MR by aldosterone, other corticosteroids and progesterone and find that aldosterone, 11-deoxycorticosterone, 11-deoxycortisol and progesterone have half-maximal responses (EC50s) below 1 nM and are potential physiological mineralocorticoids. In contrast, EC50s for corticosterone and cortisol were 23 nM and 66 nM, respectively. Unexpectedly, truncated lungfish MR, consisting of the DNA-binding domain, hinge domain and steroid-binding domain, had a stronger response to aldosterone, other corticosteroids and progesterone than did full-length lungfish MR, indicating that an allosteric action of the N-terminal domain represses steroid activation of lungfish MR. This contrasts to human MR in which the N-terminal domain contains an activation function. BLAST searches of GenBank did not retrieve a GR ortholog, leading us to test dexamethasone and triamcinolone for activation of lungfish MR. At 10 nM, both synthetic glucocorticoids are about 4-fold stronger than 10 nM aldosterone in activating full-length lungfish MR, leading us to propose that lungfish MR also functions as a GR.

scholarly journals Genomes of early-diverging streptophyte algae shed light on plant terrestrialization

Nature Plants ◽  
2019 ◽  
Vol 6 (2) ◽  
pp. 95-106 ◽  
Author(s):  
Sibo Wang ◽  
Linzhou Li ◽  
Haoyuan Li ◽  
Sunil Kumar Sahu ◽  
Hongli Wang ◽  
...  
Keyword(s):  
Transcription Factors ◽  
Common Ancestor ◽  
Cellulose Synthase ◽  
Dynamic Nature ◽  
Terrestrial Environment ◽  
Freshwater Habitat ◽  
Terrestrial Environments ◽  
The Common ◽  
Shed Light ◽  
Size And Structure

AbstractMounting evidence suggests that terrestrialization of plants started in streptophyte green algae, favoured by their dual existence in freshwater and subaerial/terrestrial environments. Here, we present the genomes of Mesostigma viride and Chlorokybus atmophyticus, two sister taxa in the earliest-diverging clade of streptophyte algae dwelling in freshwater and subaerial/terrestrial environments, respectively. We provide evidence that the common ancestor of M. viride and C. atmophyticus (and thus of streptophytes) had already developed traits associated with a subaerial/terrestrial environment, such as embryophyte-type photorespiration, canonical plant phytochrome, several phytohormones and transcription factors involved in responses to environmental stresses, and evolution of cellulose synthase and cellulose synthase-like genes characteristic of embryophytes. Both genomes differed markedly in genome size and structure, and in gene family composition, revealing their dynamic nature, presumably in response to adaptations to their contrasting environments. The ancestor of M. viride possibly lost several genomic traits associated with a subaerial/terrestrial environment following transition to a freshwater habitat.

scholarly journals Evolution of the Mineralocorticoid Receptor: Sequence, Structure and Function

2017 ◽  
Author(s):  
Michael E. Baker ◽  
Yoshinao Katsu
Keyword(s):  
Transcriptional Activation ◽  
Mineralocorticoid Receptor ◽  
Sequence Structure ◽  
Strong Response ◽  
Terrestrial Vertebrates ◽  
Cartilaginous Fishes ◽  
And Function ◽  
Corticoid Receptor ◽  
Jawless Fish ◽  
Combine Sequence

Abstract.The mineralocorticoid receptor (MR) is descended from a corticoid receptor (CR), which has descendants in lamprey and hagfish, cyclostomes (jawless fish), a taxon that evolved at the base of the vertebrate line. A distinct MR and GR first appear in cartilaginous fishes (Chondrichthyes), such as sharks, skates, rays and chimaeras. Skate MR has a strong response to corticosteroids that are mineralocorticoids and glucocorticoids in humans. The half-maximal responses (EC50s) for skate MR for the mineralocorticoids aldosterone and 11-deoxycorticosterone are 0.07 nM and 0.03 nM, respectively. EC50s for the glucocorticoids cortisol and corticosterone are 1 nM and 0.09 nM, respectively. The physiological mineralocorticoid in ray-finned fish, which do not synthesize aldosterone, is not fully understood because several 3-ketosteroids, including cortisol, 11-deoxycortisol, corticosterone, 11-deoxycorticosterone and progesterone are transcriptional activators of fish MR. Divergence of the MR and GR in terrestrial vertebrates, which synthesize aldosterone, led to increased selectivity of the MR for aldosterone, coupled with a diminished response to cortisol and corticosterone. Here, we combine sequence analysis of the CR and vertebrate MRs and GRs, analysis of crystal structures of human MR and GR and data on transcriptional activation by 3-ketosteroids of wild-type and mutant MRs and GRs to investigate the evolution of selectivity for 3-ketosteroids by the MR in terrestrial vertebrates and ray-finned fish, as well as the basis for binding of some glucocorticoids by human MR and other vertebrate MRs.

scholarly journals Evolutionary Transition From Water to Land in Vertebrates Illuminated by Basal Ray-Finned Fish Vomeronasal Type 2 Receptor (OlfC) Genes

2021 ◽  
Author(s):  
Zicong Zhang ◽  
Atsuhiro Sakuma ◽  
Shigehiro Kuraku ◽  
Masato Nikaido
Keyword(s):  
Amino Acids ◽  
Multigene Family ◽  
Teleost Fish ◽  
Common Ancestor ◽  
Cartilaginous Fish ◽  
Exhaustive Search ◽  
Evolutionary Transition ◽  
Spotted Gar ◽  
The Common

Abstract The vomeronasal type 2 receptor (V2R, also called OlfC) multigene family is found in a broad range of jawed vertebrates from cartilaginous fish to tetrapods. V2Rs encode receptors for food-related amino acids in teleost fish, whereas for peptide pheromones in mammals. In addition, V2Rs of teleost fish are phylogenetically distinct from those of tetrapods, implying a drastic change in the V2Rrepertoire during terrestrial adaptation. To understand the process of diversification of V2Rs in vertebrates from “fish-type” to “tetrapod-type”, we conducted an exhaustive search for V2Rs in cartilaginous fish (chimeras, sharks, and skates) and basal ray-finned fish (reedfish, sterlet, and spotted gar), and compared them with those of teleost, coelacanth, and tetrapods. Phylogenetic and synteny analyses on 1897V2Rs revealed that basal ray-finned fish possess unexpectedly higher number of V2Rs compared with cartilaginous fish, implying that V2Rgene repertoires expanded in the common ancestor of Osteichthyes. Furthermore, reedfish and sterlet possessed various V2Rs that belonged to both “fish-type” and “tetrapod-type”, suggesting that the common ancestor of Osteichthyes possess “tetrapod-type” V2Rs although they inhabited underwater environments. Thus, the unexpected diversity of V2Rs in basal ray-finned fish illuminates the process of how the osteichthyan ancestors adapt from water to land.

scholarly journals Aldosterone, Dexamethasone and Triamcinolone Activate African Lungfish Mineralocorticoid Receptor: Increased Activation After Removal of the Amino-Terminal Domain

2021 ◽  
Author(s):  
Yoshinao Katsu ◽  
Shin Oana ◽  
Xiaozhi Lin ◽  
Susumu Hyodo ◽  
Michael E. Baker
Keyword(s):  
Transcriptional Activation ◽  
Mineralocorticoid Receptor ◽  
Activation Function ◽  
Binding Domain ◽  
Full Length ◽  
Terrestrial Vertebrates ◽  
Amino Terminal ◽  
Terminal Domain ◽  
Cartilaginous Fishes ◽  
African Lungfish

Abstract A distinct mineralocorticoid receptor (MR) ortholog first appears in cartilaginous fishes, such as sharks, skates, rays and chimaeras. Although aldosterone, the main physiological mineralocorticoid in humans and other terrestrial vertebrates, is a transcriptional activator of skate MR and elephant shark MR, aldosterone is not synthesized by cartilaginous fishes. Aldosterone, first appears in lungfish, which are lobe-finned fish that are forerunners of terrestrial vertebrates. Aldosterone activation of the MR regulates internal homeostasis of water, sodium and potassium, which was critical in the conquest of land by vertebrates. We studied transcriptional activation of the slender African lungfish (Protopterus dolloi) MR by aldosterone, other corticosteroids and progesterone and find that aldosterone, 11-deoxycorticosterone, 11-deoxycortisol and progesterone have half-maximal responses (EC50s) below 1 nM and are potential physiological mineralocorticoids. In contrast, EC50s for corticosterone and cortisol were 23 nM and 66 nM, respectively. Unexpectedly, truncated lungfish MR, consisting of the DNA-binding domain, hinge domain and steroid-binding domain, had a stronger response to aldosterone, other corticosteroids and progesterone than did full-length lungfish MR, indicating that an allosteric action of the N-terminal domain represses steroid activation of lungfish MR. This contrasts to human MR in which the N-terminal domain contains an activation function. BLAST searches of GenBank did not retrieve a GR ortholog, leading us to test dexamethasone and triamcinolone for activation of lungfish MR. At 10 nM, both synthetic glucocorticoids are about 4-fold stronger than 10 nM aldosterone in activating full-length lungfish MR, leading us to propose that lungfish MR also functions as a GR.

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