Unusual evolution of 11β‐ and 17β‐hydroxysteroid and retinol dehydrogenases

11β‐hydroxysteroid dehydrogenases regulate glucocorticoid concentrations and 17β‐hydroxysteroid dehydrogenases regulate estrogen and androgen concentrations in mammals. Phylogenetic analysis of the sequences from two 11β‐hydroxysteroid dehydrogenases and four mammalian 17β‐hydroxysteroid dehydrogenases indicates unusual evolution in these enzymes. Type 1 11β‐ and 17β‐hydroxysteroid dehydrogenases are on the same branch; Type 2 enzymes cluster on another branch with β‐hydroxybutyrate dehydrogenase, 11‐cis retinol dehydrogenase and retinol dehydrogenase; Type 3 17β‐hydroxysteroid dehydrogenase is on a third branch; while the pig dehydrogenase clusters with a yeast multifunctional enzyme on a fourth branch. Pig 17β‐hydroxysteroid dehydrogenase appears to have evolved independently from the other three 17β‐hydroxysteroid dehydrogenase dehydrogenases; in which case, the evolution of 17β‐hydroxysteroid dehydrogenase activity is an example of functional convergence. The phylogeny also suggests that independent evolution of specificity toward C11 substituents on glucocorticoids and C17 substituents on androgens and estrogens has occurred in Types 1 and 2 11β‐ and 17β‐hydroxysteroid dehydrogenases.

[1]  R F Doolittle,et al.  Progressive alignment and phylogenetic tree construction of protein sequences. , 1990, Methods in enzymology.

[2]  W. Fitch,et al.  Construction of phylogenetic trees. , 1967, Science.

[3]  Z. Krozowski,et al.  11β-Hydroxysteroid dehydrogenase and the short-chain alcohol dehydrogenase (SCAD) superfamily , 1992, Molecular and Cellular Endocrinology.

[4]  C. Edwards,et al.  Localisation of 11 beta-hydroxysteroid dehydrogenase--tissue specific protector of the mineralocorticoid receptor. , 1988, Lancet.

[5]  M. Baker,et al.  Expansion of the mammalian 3β‐hydroxysteroid dehydrogenase/plant dihydroflavonol reductase superfamily to include a bacterial cholesterol dehydrogenase, a bacterial UDP‐galactose‐4‐epimerase, and open reading frames in vaccinia virus and fish lymphocystis disease virus , 1992, FEBS letters.

[6]  T. Mune,et al.  NAD(+)-dependent isoform of 11 beta-hydroxysteroid dehydrogenase. Cloning and characterization of cDNA from sheep kidney. , 1994, The Journal of biological chemistry.

[7]  J. L. Napoli,et al.  Cloning of a cDNA for Liver Microsomal Retinol Dehydrogenase , 1995, The Journal of Biological Chemistry.

[8]  M. Poutanen,et al.  Differential estrogen substrate specificities for transiently expressed human placental 17 beta-hydroxysteroid dehydrogenase and an endogenous enzyme expressed in cultured COS-m6 cells. , 1993, Endocrinology.

[9]  J. W. Valentine.  Late Precambrian bilaterians: grades and clades. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[10]  J. Aitchison,et al.  cDNA cloning and primary structure determination of the peroxisomal trifunctional enzyme hydratase-dehydrogenase-epimerase from the yeast Candida tropicalis pK233. , 1988, Gene.

[11]  P. White,et al.  The human gene for 11 beta-hydroxysteroid dehydrogenase. Structure, tissue distribution, and chromosomal localization. , 1991, The Journal of biological chemistry.

[12]  J. Funder,et al.  Mineralocorticoid action: target tissue specificity is enzyme, not receptor, mediated. , 1988, Science.

[13]  A. Náray-Fejes-Tóth,et al.  llβ-Hydroxysteroid Dehydrogenase Activity in the Renal Target Cells of Aldosterone* , 1991 .

[14]  R. Vihko,et al.  Genomic organization and DNA sequences of human 17β‐hydroxysteroid dehydrogenase genes and flanking regions , 1992 .

[15]  B. Rossier,et al.  Corticosterone induces 11 beta-HSD and mineralocorticoid specificity in an amphibian urinary bladder cell line. , 1993, The American journal of physiology.

[16]  J. Nap,et al.  Developmental Biology of a Plant-Prokaryote Symbiosis: The Legume Root Nodule , 1990, Science.

[17]  H. Erdjument-Bromage,et al.  Molecular cloning and characterization of (R)-3-hydroxybutyrate dehydrogenase from human heart. , 1992, The Journal of biological chemistry.

[18]  W. W. Zhang,et al.  Primary structure of rat liver D-beta-hydroxybutyrate dehydrogenase from cDNA and protein analyses: a short-chain alcohol dehydrogenase. , 1992, Biochemistry.

[19]  J. Hiltunen,et al.  Peroxisomal multifunctional beta-oxidation protein of Saccharomyces cerevisiae. Molecular analysis of the fox2 gene and gene product. , 1992, The Journal of biological chemistry.

[20]  M. Baker.  SEQUENCES OF INTEREST: Human Placental 17β-Hydroxysteroid Dehydrogenase is Homologous to NodG Protein of Rhizobium meliloti , 1989 .

[21]  F. Leenders,et al.  Molecular cloning and amino acid sequence of the porcine 17β‐estradiol dehydrogenase , 1994 .

[22]  Robert F. Fisher,et al.  Rhizobium–plant signal exchange , 1992, Nature.

[23]  R F Doolittle,et al.  Convergent evolution: the need to be explicit. , 1994, Trends in biochemical sciences.

[24]  C. Monder.  Corticosteroids, receptors, and the organ‐specific functions of 11β‐hydroxysteroid dehydrogenase , 1991, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[25]  R. Doolittle.  Similar amino acid sequences: chance or common ancestry? , 1981, Science.

[26]  J. Adamski,et al.  Purification and properties of oestradiol 17 beta-dehydrogenase extracted from cytoplasmic vesicles of porcine endometrial cells. , 1992, The Biochemical journal.

[27]  K. O. Elliston,et al.  Expression cloning and characterization of human 17 beta-hydroxysteroid dehydrogenase type 2, a microsomal enzyme possessing 20 alpha-hydroxysteroid dehydrogenase activity. , 1993, The Journal of biological chemistry.

[28]  A. Náray-Fejes-Tóth,et al.  Expression cloning of the aldosterone target cell-specific 11 beta-hydroxysteroid dehydrogenase from rabbit collecting duct cells. , 1995, Endocrinology.

[29]  F. Leenders,et al.  The sequence of porcine 80 kDa 17β-estradiol dehydrogenase reveals similarities to the short chain alcohol dehydrogenase family, to actin binding motifs and to sterol carrier protein , 1994, Molecular and Cellular Endocrinology.

[30]  S. Gould,et al.  Exaptation—a Missing Term in the Science of Form , 1982, Paleobiology.

[31]  Michael E. Baker,et al.  Genealogy of regulation of human sex and adrenal function, prostaglandin action, snapdragon and petunia flower colors, antibiotics, and nitrogen fixation: functional diversity from two ancestral dehydrogenases , 1991, Steroids.

[32]  U. Hellman,et al.  The Retinal Pigment Epithelial-specific 11-cis Retinol Dehydrogenase Belongs to the Family of Short Chain Alcohol Dehydrogenases (*) , 1995, The Journal of Biological Chemistry.

[33]  C. Edwards,et al.  Rat liver 11 beta-hydroxysteroid dehydrogenase complementary deoxyribonucleic acid encodes oxoreductase activity in a mineralocorticoid-responsive toad bladder cell line. , 1993, Endocrinology.

[34]  J. Mason,et al.  Human kidney 11 beta-hydroxysteroid dehydrogenase is a high affinity nicotinamide adenine dinucleotide-dependent enzyme and differs from the cloned type I isoform. , 1994, The Journal of clinical endocrinology and metabolism.

[35]  J. Cronan,et al.  The gene encoding Escherichia coli acyl carrier protein lies within a cluster of fatty acid biosynthetic genes. , 1992, The Journal of biological chemistry.

[36]  M. Baker.  Protochlorophyllide reductase is homologous to human carbonyl reductase and pig 20 beta-hydroxysteroid dehydrogenase. , 1994, The Biochemical journal.

[37]  S. Miller,et al.  Unexpected presence of estrogens in culture medium supplements: subsequent metabolism by the yeast Sacchromyces cerevisiae. , 1986, Endocrinology.

[38]  M Krook,et al.  Characteristics of short-chain alcohol dehydrogenases and related enzymes. , 1991, European journal of biochemistry.

[39]  K. O. Elliston,et al.  Male pseudohermaphroditism caused by mutations of testicular 17β–hydroxysteroid dehydrogenase 3 , 1994, Nature Genetics.

[40]  M. Baker.  Endocrine Activity of Plant-Derived Compounds: An Evolutionary Perspective , 1995, Proceedings of the Society for Experimental Biology and Medicine. Society for Experimental Biology and Medicine.

[41]  M. Takahashi,et al.  Distribution of 17β-hydroxysteroid dehydrogenase gene expression and activity in rat and human tissues , 1992, The Journal of Steroid Biochemistry and Molecular Biology.

[42]  M. Baker.  A common ancestor for Candida tropicalis and dehydrogenases that synthesize antibiotics and steroids , 1990, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[43]  Z. Krozowski,et al.  Cloning and tissue distribution of the human 1 lβ-hydroxysteroid dehydrogenase type 2 enzyme , 1994, Molecular and Cellular Endocrinology.

[44]  D. Stevens,et al.  Estrogens inhibit mycelium-to-yeast transformation in the fungus Paracoccidioides brasiliensis: implications for resistance of females to paracoccidioidomycosis , 1984, Infection and immunity.

[45]  T. Miura,et al.  Hormonal induction of all stages of spermatogenesis in vitro in the male Japanese eel (Anguilla japonica). , 1991, Proceedings of the National Academy of Sciences of the United States of America.